Sources of Low Level Human Fecal Markers in Recreational Waters of Two Santa Barbara, CA Beaches: Roles of WWTP Outfalls and Swimmers
Graphical abstract
Introduction
Fecal contamination of coastal zones, particularly recreational waters, is of great concern to public health. Human pathogens in contaminated coastal waters cause severe illness worldwide, with annually more than 120 million gastrointestinal and 50 million severe respiratory illnesses estimated to be associated with swimming or bathing in polluted coastal waters (Shuval, 2003). To monitor fecal contamination in coastal waters, fecal indicator bacteria (FIB) including total coliform (TC), fecal coliform or Escherichia coli (EC), and enterococci (ENT) are used as indicators due to their abundances in feces (Harwood et al., 2014). California law mandates (by Assembly Bill 411, or AB411) weekly FIB testing from April to October in surf zone waters of recreational beaches that exceed 150 million user-days annually by tourists and residents who swim, wade, surf, and dive (https://www.waterboards.ca.gov/water_issues/programs/beaches/beach_water_quality/). Swimming advisories, beach closures, stormwater green infrastructure, and sanitary infrastructure investigations with abatement actions are management practices that are implemented where FIB concentrations exceed water quality criteria.
However, FIB may originate from animal feces that are of low risk to human health due to host specificity of pathogens, particularly enteric viruses (Sinclair et al., 2009). FIB can also persist in the environment (Field and Samadpour, 2007; Harwood et al., 2014). Epidemiological studies conclude that FIB are unreliable sole measures of public health risk (Arnold et al., 2013; Colford et al., 2007). To determine public health relevant fecal sources, microbial source tracking (MST) prioritizes quantifying genetic markers encoding 16S rRNA of host-coevolved or -associated microorganisms such as the HF183 human fecal DNA marker (Boehm et al., 2013 and 2015; Field and Samadpour, 2007; Harwood et al., 2014; Mayer et al., 2018).
In urban settings, potential human fecal sources include leaking sanitary sewers and sewage overflows (Sikich et al., 2018). Coastal watersheds may have fecal contaminated creeks draining through coastal lagoons, or other transitional waters, to beach waters (Riedel et al., 2015). Runoff-generating rain events can mobilize human or animal fecal surface deposits in watersheds, with storm drainage conveying fecal materials to coastal waters (U.S. Environmental Protection Agency, 2004). Watershed sediments, urban creek outlets or scour ponds, groundwater, and beach sands (Russell et al., 2013) can be reservoirs of fecal materials that are released gradually to surf zone waters (Ishii et al., 2007). Harbors with boats, and moored boats in ocean anchorage areas, could be fecal sources to surf zone waters. WWTP treated effluent ocean outfalls can discharge fecal markers (Boehm et al., 2002). Onshore, beach campers are possible human fecal contamination sources (Noble et al., 2000). Yet, such multiple sources are rarely investigated comprehensively.
Previously, drainages, creeks, and rivers were shown to discharge fecal contamination into California recreational beaches (Cao et al., 2017; Ervin et al., 2014; Goodwin et al., 2016; Riedel et al., 2015; Sikich et al., 2018). Enhanced Watershed Management Programs which are costly to local and State water government agencies (California Water Boards Los Angeles Region 4, 2018; Ervin et al., 2014; Goodwin et al., 2016; San Diego Regional Water Quality Control Board, 2017; Sikich et al., 2018) have been implemented for abating such fecal contamination. However, sources of low but chronic human fecal markers in coastal California recreational beach surf zone waters during the summer AB411 periods remain unresolved (Cao et al., 2017; Jennings et al., 2018; McQuaig et al., 2012; Riedel et al., 2015; Russell et al., 2013; Santoro and Boehm, 2007). Systematic evaluation of all possible human fecal sources is needed (Griffith et al., 2013).
Here, two popular recreational beaches with historically-elevated surf zone FIB concentrations, Leadbetter Beach and East Beach, in Santa Barbara, CA, were investigated in a 3-year study to determine fecal sources. Besides FIB and human, dog, and gull fecal markers, pathogens including human adenovirus and Salmonella bacteria were also determined in this study to evaluate the potential risk to human health. For the first time in coastal urban California during dry weather, all hypothesized human fecal sources and transmission routes were rigorously tested, including watersheds, urban creek outlets and scour ponds, groundwater transport, supratidal and intertidal beach sands, storm drains, sanitary sewers, septic systems, harbor facilities with boats, moored boats in anchorage areas, recycled water, the treated WWTP effluent discharged from two nearby ocean outfalls, as well as beach campers and swimmers. After excluding almost all potential human fecal sources and transmission routes, the results demonstrated that consistent human marker HF183 detections in surf zones at low concentration levels correlated with swimmer counts, with the potential additional influence of WWTP effluent. Surf zone recreation has been recognized as a source of FIB to the surf zone (Elmir et al., 2007; (Elmir et al., 2009) ), but this is the first time that counts of swimmers were found to be significantly correlated to human-associated fecal markers in a field study of recreational beaches. The results inform expectations of human fecal contamination and markers in recreational beaches for future water quality criteria that may regard human fecal markers, with potential benefit to regulators, managers, and researchers.
Section snippets
Beaches, overall study structure, and sample analyses
Two urban Santa Barbara, California recreational beaches were studied: Leadbetter Beach (LB) at Honda Creek and East Beach (EB) at Sycamore Creek. Arroyo Hondo (AH) was the rural reference beach (Fig. S1). LB and EB were selected due to historically elevated surf zone FIB concentrations, with LB and EB exceeding the U.S. Environmental Protection Agency Beach Action Advisory (BAV) in 2013 by 18% and 5% respectively (NRDC, 2014). This study was structured as an MST program (Griffith et al., 2013)
Reference beach fecal contamination and host-associated marker specificity
Human- and dog-associated markers, and pathogens (Salmonella spp. and human adenovirus) were not detected in AH (reference beach) surf zone, lower watershed water, or beach sand samples (Table S1), discounting regional contamination. AH surf zone waters, and some sand samples harbored Gull2TaqMan markers (including at ROQ levels), but FIB concentrations were low.
Fresh gull and other seabird feces from the Santa Barbara area (Table S1) did not contain human markers, DogBact markers, or human
Discussion
Considering the frequencies of dogs and gulls or other seabirds at beaches, it is not surprising that such hosts are often identified as major FIB sources in surf zones (Converse et al., 2012; Goodwin et al., 2016; Wright et al., 2009), as shown in this study. However, animal feces typically pose fewer risks to public health due to the host specificity of many pathogens. Here, similarly to prior studies of recreational beaches (Cao et al., 2017; Jennings et al., 2018; McQuaig et al., 2012;
Conclusions
Low levels of chronic HF183 in recreational beach surf zone waters have long been observed, pointing to ongoing public health risks. In a comprehensive three-year summertime assessment of two urban California beaches, surf zone FIB contamination was mainly attributed to gull and dog wastes. After excluding almost all other human fecal sources, HF183 in surf zones was attributable to swimmers, particularly in the afternoon, but two WWTP outfalls in the vicinity could not be ruled out as sources.
Declaration of Competing Interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Acknowledgements
This study was supported by the State of California Clean Beach Initiative, using funds from Proposition 84, and from funds provided by Mr. Henry (Sam) Wheeler. We acknowledge the assistance of Tania Gomez Ayala, Marina Feraud, Mitchell Maier, Patrick Roehrdanz, Ying Wang, Dr. Monika Mortimer, Christoph Pierre, Christian Orsini, and Eric Hessell at UCSB as well as Geosyntec Consultants’ researchers including Stacy Isaac, Adam Questad, and Maia Colyar. We also thank Hillary Hauser of Heal the
References (49)
- et al.
Performance of forty-one microbial source tracking methods: a twenty-seven lab evaluation study
Water Res
(2013) - et al.
Quantitative evaluation of enterococci and Bacteroidales released by adults and toddlers in marine water
Water Res
(2009) - et al.
Quantitative evaluation of bacteria released by bathers in a marine water
Water Res
(2007) - et al.
Characterization of fecal concentrations in human and other animal sources by physical, culture-based, and quantitative real-time PCR methods
Water Res
(2013) - et al.
Fecal source tracking, the indicator paradigm, and managing water quality
Water Res
(2007) - et al.
Survival and persistence of host-associated Bacteroidales cells and DNA in comparison with Escherichia coli and Enterococcus in freshwater sediments as quantified by PMA-qPCR and qPCR
Water Res
(2015) - et al.
A hydrologic and geomorphic model of estuary breaching and closure
Geomorphology
(2013) - et al.
Long-term monitoring of molecular markers can distinguish different seasonal patterns of fecal indicating bacteria sources
Water Res
(2015) - et al.
Quantification of pathogens and markers of fecal contamination during storm events along popular surfing beaches in San Diego, California
Water Res
(2018) - et al.
Microbial load from animal feces at a recreational beach
Mar. Pollut. Bull.
(2009)
Swimmer illness associated with marine water exposure and water quality indicators: impact of widely used assumptions
Epidemiology
Cross-shelf transport at Huntington Beach. Implications for the fate of sewage discharged through an offshore ocean outfall
Environ. Sci. Technol.
Human-associated fecal quantitative polymerase chain reaction measurements and simulated risk of gastrointestinal illness in recreational waters contaminated with raw sewage
Environ. Sci. Technol. Lett.
Estimating the probability of illness due to swimming in recreational water with a mixture of human- and gull-associated microbial source tracking markers
Environ. Sci. Process Impacts
California Water Boards Los Angeles Region 4
Watershed Management Programs
Regional assessment of human fecal contamination in southern California coastal drainages
Int. J. Environ. Res. Public Health
Critical evaluation of the factors affecting Escherichia coli environmental decay for outfall plume models
Rev. Ambient. Água.
Water quality indicators and the risk of illness at beaches with nonpoint sources of fecal contamination
Epidemiology
Dramatic improvements in beach water quality following gull removal
Environ. Sci. Technol.
Microbial source tracking in a coastal California watershed reveals canines as controllable sources of fecal contamination
Environ. Sci. Technol.
Rainfall-induced runoff from exposed streambed sediments: an important source of water pollution
J. Environ. Qual.
Dilution models for effluent discharges
(Visual Plumes
Assessment of enteric pathogen shedding by bathers during recreational activity and its impact on water quality
Quantitative Microbiology
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2024, Science of the Total EnvironmentAssessing multiple fecal sources to surf zone waters of two recreational beaches by bacterial community analysis
2022, Water ResearchCitation Excerpt :In the prior study upon which this research builds, all hypothesized fecal sources were rigorously tested for two popular urban recreational beaches (Leadbetter Beach and East Beach at Sycamore Creek in Santa Barbara, CA), with bather shedding clearly identified as a source of HF183 fecal markers in surf zones, yet while not ruling out treated WWTP effluent as another source (Li et al., 2021). Additionally, the possible contamination of recycled water, which is used for irrigation of plants including those proximate to the beaches, was unresolved in surf zone waters (Li et al., 2021). To understand the possible contributions of treated WWTP effluent and recycled water to chronically low HF183-impacted surf zones, and to further confirm the impacts of bather shedding, bacterial community analysis based on 16S rRNA gene sequencing was utilized in this study.
Molecular microbiological approaches reduce ambiguity about the sources of faecal pollution and identify microbial hazards within an urbanised coastal environment
2022, Water ResearchCitation Excerpt :Indeed, at site SW5.1 levels of the Lachno3 marker were 1.1 × 105 copies/100 ml prior to the rainfall event and the Lachno3 and HF183 markers reached 1.98 × 107 copies/100 ml and 2.45 × 106 copies/100 ml respectively after 3.8 mm of rain. While these levels are an order of magnitude lower observed in raw sewage (Sauer et al., 2011; Li et al., 2021a), they are high relative to concentrations observed in other coastal environments (Liang et al., 2021; Rothenheber and Jones, 2018). It is not uncommon for dry weather sewage leaks to occur within stormwater drains (Sercu et al., 2009), and, notably, Drain 5 is adjacent to a sewage pumping station behind Rose Bay beach, which may contribute to high background levels of both sewage markers at Neilson park and is potentially worthy of further examination.