Seaweeds and plastic debris can influence the survival of faecal indicator organisms in beach environments

Highlights

• The revised Bathing Water Directive sets higher standards for microbial water quality.

• Seaweeds could provide a protected environment for faecally-derived bacteria.

• Senescing brown seaweeds can enhance waterborne E. coli survival.

• FIO survival on bathing beaches could be facilitated by beach-cast brown seaweeds.

Abstract

The revised Bathing Water Directive (rBWD) introduces more stringent standards for microbial water quality and promotes more pro-active management of the beach environment through the production of a bathing water profile (BWP). The aim of this study was to determine whether living seaweeds in the littoral zone are colonised by faecal indicator organisms (FIOs), and to quantify the survival dynamics of waterborne Escherichia coli in microcosms containing senescing seaweeds. Living seaweed (Fucus spiralis) was not associated with FIO colonisation, although could be providing a protected environment in the underlying sand. Senescing seaweeds enhanced waterborne E. coli survival compared to plastic debris, with the brown seaweed Laminaria saccharina facilitating greater E. coli persistence than either Chondrus crispus or Ulva lactuca. This has important implications for FIO survival on bathing beaches as the majority of beach-cast biomass is composed of brown seaweeds, which could support significant levels of FIOs.

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.