Seaweeds and plastic debris can influence the survival of faecal indicator organisms in beach environments
Introduction
Escherichia coli and enterococci are faecal indicator organisms (FIOs) commonly used by environmental regulators around the world to provide a measure of microbial pollution in bathing waters (Mansilha et al., 2009). Although FIOs are not pathogenic, compared with quantifying individual waterborne pathogens, their enumeration is relatively straightforward (Quilliam et al., 2011). The primary habitat of E. coli and enterococci is the mammalian gut; however, it is becoming clear that FIOs can persist in the environment for significant periods of time (Ferguson and Signoretto, 2011, Byappanahalli et al., 2012, Hernandez et al., 2014).
The environmental pathways for contamination of bathing waters by FIOs can include both diffuse and point-source inputs, e.g. pasture grazed by livestock and sewage discharges. Diffuse source inputs are driven largely by high rainfall, and the subsequent generation of run-off within agricultural catchments is known to contribute to rapid incidental losses of FIOs from land to water via a number of hydrological pathways (Oliver et al., 2005). High flow conditions in streams and rivers may also remobilise stores of FIOs from streambed sediments, to the further detriment of downstream microbial water quality (Muirhead et al., 2004, Yakirevich et al., 2013). While diffuse source contributions of FIOs to bathing waters tend to dominate during wet weather, the risk of point-source microbial inputs via spills from combined sewer overflows (CSOs) can also increase if sewerage infrastructure struggles to cope with potentially high volumes of urban run-off during intense rainfall and flood conditions (Kay et al., 2008).
Maintaining and improving the microbial quality of EU bathing waters is regulated by the Bathing Water Directive (76/160/EEC) and the revised Bathing Water Directive (rBWD; 2006/7/EC). From 2015, the number of designated bathing waters falling below the legally enforceable ‘sufficient’ standard is likely to rise with the first reporting of classifications linked to the rBWD (Chawla et al., 2005, Oliver et al., 2014). The rBWD introduces more stringent standards for microbial water quality and also promotes pro-active management of the beach environment through the production of a bathing water profile (BWP) for all designated bathing waters. The BWP is intended to provide a qualitative appraisal of potential pollutant sources linked to physical, geographical and hydrological characteristics of the beach environment. Compliance with the (r)BWD also drives designations such as the Blue Flag award, the loss of which has the potential to impact on tourism and local coastal economies (Wyer et al., 2010). The rBWD thus provides significant impetus for EU regulators to identify and manage potential environmental reservoirs of FIOs, in addition to agricultural and sewage related inputs, which could contribute to decreased water quality at bathing beaches.
The survival of FIOs in beach sand is well documented and certain species of freshwater macroalgae washed up on bathing beaches have been shown to harbour FIOs, including human pathogenic bacteria (Ishii et al., 2006, Skalbeck et al., 2010). The nuisance filamentous green alga Cladophora growing in eutrophic regions of the Great Lakes in the US is often associated with significant levels of Shigella, Salmonella, Campylobacter, and E. coli O157, with evidence for enhanced survival of Salmonella and Shigella in association with Cladophora in freshwater microcosms (Ishii et al., 2006, Byappanahalli et al., 2009). There is also some evidence that marine beach-cast wrack can play a role in enhancing the persistence of FIOs (Imamura et al., 2011). The seaweed surface is an ideal environment for the formation of biofilm, which provides a nutrient-rich habitat for bacterial communities and a niche for protection from harmful UV light and predation (Egan et al., 2013). Living seaweeds can harbour relatively high concentrations of pathogenic species of bacteria, such as Vibrio, e.g. Vibrio vulnificus and Vibrio parahaemolyticus (Mahmud et al., 2007, Mahmud et al., 2008). However, there remains a significant lack of understanding about the role of living and senescing seaweeds in facilitating the persistence of FIOs in the marine environment, and the effect this has on bathing water quality for the microbial compliance parameters currently used by EU regulators (Anderson et al., 1997, Hannah and Cowey, 2009).
In catchments containing areas of intensive agriculture, increased inputs of FIOs to bathing waters could be coupled with excessive growth of seaweeds due to concomitant eutrophic conditions. Understanding the role seaweeds play in facilitating the persistence of FIOs in bathing waters therefore, is crucial for informing environmental management decisions (and improving BWPs) designed to decrease the risk of exposure to potential human pathogens. Consequently, the aim of this study was to, (i) determine the spatial distribution of FIOs and Vibrio spp. colonising living seaweed fronds across the intertidal zone of a beach; and (ii) to quantify the survival dynamics of waterborne E. coli in microcosms containing senescing brown, red or green seaweeds, in the presence or absence of an autochthonous bacterial community.
Section snippets
Field site and transect sampling
Bracken Bay in Ayr, Scotland, consists of a 0.84 km stretch of sand and shingle beach with a bedrock foreshore. This site is adjacent to a popular tourist holiday park and is situated approximately 800 m south–west of a designated bathing water site (Heads of Ayr beach). The rural catchment draining into this part of the coast is just over 4 km2 with intensive dairy farming being the main agricultural activity. Average summer rainfall for the region is 392 mm compared to 331 mm across the rest of
Spatial distribution of bacteria colonising living seaweed and sand across the intertidal zone
The concentration of bacteria present in the sand beneath the seaweed at each point of both the vertical and horizontal transect was consistently greater than the number of cells recovered from the living seaweed fronds (Table 1). In general, the distribution of Vibrio spp., E. coli and enterococci was patchy across the two transects, and although there were ‘hotspots’ at the top of the beach near the strandline, these were not spatially consistent across the beach. The spatial distribution of
FIO colonisation of living seaweed fronds and plastic rubbish
Living seaweeds can by colonised by a wide range of bacteria, with some evidence that attachment by microbial communities can be host specific (Egan et al., 2013). There are several reports of FIOs being associated with living seaweed fronds, although these have come from warm coastal waters in areas with high pollution and nutrient input (Vairappan and Suzuki, 2000, Musa and Wei, 2008). Our survey of living F. spiralis fronds in the intertidal zone found little evidence of consistent
References (41)
- et al.
Enterococci in the New Zealand environment: implications for water quality monitoring
Water Sci. Technol.
(1997) - et al.
Seasonal stability of Cladophora-associated Salmonella in Lake Michigan watersheds
Water Res.
(2009) - et al.
Threats to sandy beach ecosystems: a review
Estuar. Coast. Shelf Sci.
(2009) The pollution of the marine environment by plastic debris: a review
Mar. Pollut. Bull.
(2002)- et al.
The response of macrofauna communities and shorebirds to macrophyte wrack subsidies on exposed sandy beaches of southern California
Estuar. Coast. Shelf Sci.
(2003) Mechanical grooming and beach award status are associated with low strandline biodiversity in Scotland
Estuar. Coast. Shelf Sci.
(2012)- et al.
Effects of full-scale beach renovation on fecal indicator levels in shoreline sand and water
Water Res.
(2014) - et al.
Faecal indicator organism concentrations in sewage and treated effluents
Water Res.
(2008) - et al.
Microbial water pollution: a screening tool for initial catchment-scale assessment and source apportionment
Sci. Total Environ.
(2010) - et al.
Seaweeds as a reservoir for diverse Vibrio parahaemolyticus populations in Japan
Int. J. Food Microbiol.
(2007)
Bathing waters: new directive, new standards, new quality approach
Mar. Pollut. Bull.
Faecal bacteria yields in artificial flood events: quantifying in-stream stores
Water Res.
Opportunities and limitations of molecular methods for quantifying microbial compliance parameters in EU bathing waters
Environ. Int.
Unearthing human pathogens at the agricultural–environment interface: A review of current methods for the detection of Escherichia coli O157 in freshwater ecosystems
Agric. Ecosyst. Environ.
Monitoring marine recreational water quality using multiple microbial indicators in an urban tropical environment
Water Res.
Fecal indicator organism density in beach sands: impact of sediment grain size, uniformity, and hydrologic factors on surface water loading
J. Great Lakes Res.
Evaluating short-term changes in recreational water quality during a hydrograph event using a combination of microbial tracers, environmental microbiology, microbial source tracking and hydrological techniques: a casestudy in Soutwest Wales, UK
Water Res.
Modeling transport of Escherichia coli in a creek during and after artificial high-flow events: three year study and analysis
Water Res.
Enterococci in the environment
Microbiol. Mol. Biol. Rev.
An assessment of the impact of the proposed EU bathing water directive on Irish coastal bathing area compliance
Water Sci. Technol.
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