Microbial hitchhikers on marine plastic debris: Human exposure risks at bathing waters and beach environments
Introduction
Marine plastic debris is an environmental pollutant of growing concern, with its detrimental effects on aquatic and coastal wildlife already well documented (Hammer et al., 2012, Gregory, 2009, Derraik, 2002). The durable, light weight and inexpensive nature of plastic has made it a ubiquitous choice for many industrial and consumer products (Osborn and Stojkovic, 2014). More than 200 M tonnes of plastic are produced annually worldwide (Ivar do Sul and Costa, 2014), facilitating its entry and accumulation in coastal waters and beach environments. Approximately 4.8–12.7 M tonnes of plastic waste entered the ocean from 192 coastal countries in 2010 alone (Jambeck et al., 2015), with global changes in rainfall, wind speed, and more frequent flood and storm events predicted to further increase the amount of stranded and drifting plastics in the coastal zone (Young et al., 2011, Gulev and Grigorieva, 2004, Meier and Wahr, 2002, Goldenberg et al., 2001).
Marine plastic debris includes large, macro particles such as carrier bags, bottles and fishing gear (Eriksen et al., 2014), and now more frequently microplastics and nanoplastics (Driedger et al., 2015, Andrady, 2011). Microplastics, defined generally as plastic particles less than 5 mm in diameter (NOAA et al., 2009), include “primary” microplastics present in cosmetic care products, clothes fibres, and the industrial discharge of virgin plastic production pellets (Eerkes-Medrano et al., 2015, Wagner et al., 2014, Browne et al., 2011, Cole et al., 2011, Fendall and Sewell, 2009), along with “secondary” microplastics that frequently enter waterways through the breakdown of macro particles by a combination of physical, biological and chemical processes (Ryan et al., 2009, Thompson et al., 2004). The majority of plastic debris entering the oceans are a result of the direct and improper disposal of terrestrial waste and the discard of plastics at sea (Hammer et al., 2012, Barnes et al., 2009). In addition, rivers, tides, wind, heavy rainfall, and storm and sewage discharge facilitate the dispersal of both macro and microplastics within marine and freshwater environments (Wagner et al., 2014, Reisser et al., 2013), with an estimated 5.25 trillion plastic particles weighing approximately 269,000 tonnes currently floating in the sea (Eriksen et al., 2014). However, this number is likely to be much higher, with a recent study by Van Sebille et al. (2015) estimating microplastic abundance (defined here as those plastic particles <200 mm in diameter) to range from 15 to 51 trillion particles, and weighing between 93 and 236 thousand metric tonnes.
The impacts of marine plastic debris go beyond simply posing a threat to marine wildlife (Fig. 1). Marine plastics can lead to economic losses by interfering with the shipping and fishing industries, and posing a significant threat to recreational tourism (Pichel et al., 2007, Sheavly and Register, 2007). Beaches polluted with medical and sanitary waste constitute a public health risk, devalue the experience of beachgoers, and can often require costly beach-cleaning efforts (Moore, 2008). With quantities of beach-cast plastic expected to rise due to more severe weather events, coastal areas dependent on tourism are likely to face a number of socio-economic challenges (Mcllgorm et al., 2011).
Plastic debris can provide a novel mechanism for the spread of invasive and alien species, in addition to that facilitated by natural substances like rafts of vegetation, wood, or pumice (Bryan et al., 2012, Minchinton, 2006, Jokiel, 1990). A diverse range of organisms has already been found colonising macro-plastics, and in some cases has led to the introduction of non-native species into new habitats (Gregory, 2009, Barnes, 2002a, Barnes, 2002b). Until very recently, however, little attention has been paid to the concept of plastic providing a novel means of spatial and temporal transport for microorganisms across marine and coastal environments (Amaral-Zettler et al., 2015, Caruso, 2015). The physical properties of plastic can provide a unique habitat capable of supporting diverse microbial communities (Zettler et al., 2013, Harrison et al., 2011), with the buoyant and persistent nature of plastic possibly contributing to the survival and long-distance transport of those microbial hitchhikers that associate with its surface. The biofilms that colonise this so-called plastisphere could also be a reservoir for pathogenic microbes, faecal indicator organisms (FIOs) and harmful algal bloom (HAB) species. Plastic debris could therefore be acting as a potential vector for the wide-scale dissemination of these organisms (Oberbeckmann et al., 2015, Zettler et al., 2013, Masó et al., 2003).
A few recent studies have shown evidence for the formation of biofilms by bacteria and FIOs (such as Escherichia coli) on plastic water distribution pipes (Yu et al., 2010, Lehtola et al., 2004), and the persistence of potentially harmful pathogens (such as certain strains of Vibrio spp.) on plastic debris (McCormick et al., 2014, Zettler et al., 2013), although this is speculative at best. However, the ability of microorganisms to persist on beach-stranded plastic debris and increase dissemination of potentially pathogenic microbes in coastal zones needs urgent addressing to allow regulators and beach managers to make more informed decisions about public safety at bathing environments. Beaches and coastal environments form some of the most ecologically and socio-economically important habitats worldwide (Harley et al., 2006), and ecosystem services in these areas are already facing significant pressure from anthropogenic activities (Quilliam et al., 2015, Schlacher et al., 2007a, Schlacher et al., 2006). In Europe, the quality of bathing water and safety of beaches is governed by the EU Bathing Water Directive (BWD; 2006/7/EC). The BWD sets standards for microbial water quality via the use of FIOs for the assessment of faecal pollution. The BWD also requires the production of a Bathing Water Profile (BWP) for all designated EU bathing waters (Mansilha et al., 2009), which contains details on the nature of possible pollution sources that could have negative impacts on a bather's health (Schernewski et al., 2012). Designations such as the Blue Flag award are also influenced by water quality classifications reported under the BWD.
Epidemiological studies have reported the relationship between bathing water quality and the occurrence of adverse human health effects such as gastrointestinal (GI) symptoms, respiratory diseases, and eye, nose and throat infections (Wade et al., 2006, Zmirou et al., 2003, Prüss, 1998). Whilst most of these studies have focused on waters impacted by municipal-wastewater effluent, the impacts of other diffuse sources of pollution remain relatively unexplored (Soller et al., 2010). With the potential of plastic providing a possible site for pathogen and FIO attachment, and the subsequent dissemination of these organisms in the marine environment, a better understanding of these processes is required in order to ensure beach safety. Assessing beach and bathing environments for stranded plastic debris and analysing it for associated FIOs and pathogens could provide a better insight into the quality of European bathing waters through the production of a more detailed BWP, as well as enabling plastic debris to qualify as a potential indicator and carrier of FIOs and pathogens that could present a risk to human health. This could further help prevent economic losses associated with beach closures, and enable beaches to maintain their Blue Flag status (Schernewski et al., 2012, Wyer et al., 2010).
Against a backdrop of changing climate, the persistent multi-pollutant effects of plastic debris in coastal environments increases the urgency to understand the risks of human exposure to plastic pollution and inform more sustainable beach management options. The aim of this review is to explore the potential of marine plastics to serve as a mechanism for the persistence and transmission of FIOs and potentially pathogenic or harmful microorganisms, and the pathways of human exposure risk in coastal environments.
Section snippets
The Plastisphere: an anthropogenic ecological habitat
Biofilms are formed by the microbial secretion of extracellular polymeric substances (EPS), which include proteins, glycoproteins, and glycolipids (Flemming et al., 2007) that act as a type of architectural scaffolding, forming a matrix around microbes and enabling their attachment to a variety of different biotic and abiotic surfaces (O'Toole et al., 2000). This helps provide a protective environment that enables microorganisms to grow in hostile habitats and facilitates easy dispersal (
Plastic dispersal: dissemination of pathogenic and harmful microbes
The introduction of invasive species into new habitats through colonisation of natural substances, such as wood, dead plants and pumice (Bryan et al., 2012, Minchinton, 2006, Van Duzer, 2004), and the ability of intertidal species to travel great distances offshore on floating rafts of seaweed (Ingólfsson, 2000) are well described. An increase in anthropogenic waste, in particular plastic litter, provides another mechanism for facilitating the dispersal of non-native species in marine
Implications for bathing water quality: human health and beach management
FIOs such as E. coli and intestinal enterococci are widely used to monitor the quality of bathing waters and beach environments. These microorganisms mainly inhabit the mammalian gut, but can be delivered to the wider aquatic environment from numerous diffuse and point sources including sewage discharge, agricultural storm run-off, and sewer overflows (Oliver et al., 2005, Oliver et al., 2015, Kay et al., 2008). The rate of FIO delivery to receiving waters will vary according to land-use and
Conclusion
The negative impacts of marine plastic debris are widespread, but not yet fully understood. Marine and freshwater plastic debris is constantly being modified by the chemical and physical environment; therefore, biofilm communities colonising plastics need to be dynamic with an ability to adapt to their changing environment. The potential for complex interactions between plastic waste and microorganisms of human health significance are currently poorly understood, yet a number of emerging
Acknowledgements
The authors would like to acknowledge the Marine Alliance for Science and Technology for Scotland (MASTS) and The University of Stirling for providing the funding to conduct this research. We also thank the reviewers of this manuscript for their positive input and ideas that helped structure this paper.
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