Microbial hitchhikers on marine plastic debris: Human exposure risks at bathing waters and beach environments

https://doi.org/10.1016/j.marenvres.2016.04.006Get rights and content

Highlights

  • Marine plastic debris could be a reservoir of pathogens harmful to human health.

  • The longevity of plastics can aid in the spread of diseases across long distances.

  • Plastic-associated microbes can be detrimental to bathing and beach environments.

  • Links between plastic debris, pathogens and public health are yet unexplored.

Abstract

Marine plastic debris is well characterized in terms of its ability to negatively impact terrestrial and marine environments, endanger coastal wildlife, and interfere with navigation, tourism and commercial fisheries. However, the impacts of potentially harmful microorganisms and pathogens colonising plastic litter are not well understood. The hard surface of plastics provides an ideal environment for opportunistic microbial colonisers to form biofilms and might offer a protective niche capable of supporting a diversity of different microorganisms, known as the “Plastisphere”. This biotope could act as an important vector for the persistence and spread of pathogens, faecal indicator organisms (FIOs) and harmful algal bloom species (HABs) across beach and bathing environments. This review will focus on the existent knowledge and research gaps, and identify the possible consequences of plastic-associated microbes on human health, the spread of infectious diseases and bathing water quality.

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.

References (128)

  • L.S. Fendall et al.

    Contributing to marine pollution by washing your face: microplastics in facial cleansers

    Mar. Pollut. Bull.

    (2009)
  • L. Hall-Stoodley et al.

    Biofilm formation and dispersal and the transmission of human pathogens

    Trends Microbiol.

    (2005)
  • I.M. Head et al.

    Bioremediation of petroleum hydro- carbon contaminants in marine habitats

    Curr. Opin. Biotech.

    (1999)
  • C.D. Heaney et al.

    Water quality, weather and environmental factors associated with fecal indicator organism density in beach sand at two recreational marine beaches

    Sci. Total Environ.

    (2014)
  • T.J. Hoellein et al.

    Abundance and environmental drivers of anthropogenic litter on 5 Lake Michigan beaches: a study facilitated by citizen science data collection

    J. Gt. Lakes. Res.

    (2015)
  • H.K. Imhof et al.

    Contamination of beach sediments of a subalpine lake with microplastic particles

    Curr. Biol.

    (2013)
  • J.A. Ivar do Sul et al.

    The present and future of microplastic pollution in the marine environment. Environ

    Poll

    (2014)
  • P.L. Jokiel

    Long-distance dispersal by rafting: reemergence of an old hypothesis

    Endeavour

    (1990)
  • S. Kako et al.

    A decadal prediction of the quantity of plastic marine debris littered on beaches of the East Asian marginal seas

    Mar. Pollut. Bull.

    (2014)
  • D. Kay et al.

    Faecal indicator organism concentrations in sewage and treated effluents

    Water Res.

    (2008)
  • G.L. Lattin et al.

    A comparison of neustonic plastic and zooplankton at different depths near the southern California shore

    Mar. Pollut. Bull.

    (2004)
  • M.J. Lehtola et al.

    Microbiology, chemistry, and biofilm development in a pilot drinking water distribution system with copper and plastic pipes

    Water Res.

    (2004)
  • B. Lévesque et al.

    Study of the bacterial content of ring-billed gull droppings in relation to recreational water quality

    Water Res.

    (2000)
  • J. Li et al.

    Microplastics in commercial bivalves from China

    Environ. Pollut.

    (2015)
  • D. Lobelle et al.

    Early microbial biofilm formation on marine plastic debris

    Mar. Pollut. Bull.

    (2011)
  • C.R. Mansilha et al.

    Bathing waters: new directive, new standards, new quality approach

    Mar. Pollut. Bull.

    (2009)
  • K.J. McDermid et al.

    Quantitative analysis of small-plastic debris on beaches in the Hawaiian archipelago

    Mar. Pollut. Bull.

    (2004)
  • T.E. Minchinton

    Rafting on wrack as a mode of dispersal for plants in coastal marshes

    Aquat. Bot.

    (2006)
  • C.J. Moore et al.

    A comparison of plastic and plankton in the North Pacific central Gyre

    Mar. Pollut. Bull.

    (2001)
  • C.J. Moore

    Synthetic polymers in the marine environment: a rapidly increasing, long-term threat

    Environ. Res.

    (2008)
  • A. Nauendorf et al.

    Microbial colonization and degradation of polyethylene and biodegradable plastic bags in temperate fine-grained organic-rich marine sediments

    Mar. Pollut. Bull.

    (2016)
  • K.L. Ng et al.

    Prevalence of microplastics in Singapore's coastal marine environment

    Mar. Pollut. Bull.

    (2006)
  • W.G. Pichel et al.

    Marine debris collects within the North Pacific subtropical convergence zone

    Mar. Pollut. Bull.

    (2007)
  • R.S. Quilliam et al.

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

    Mar. Pollut. Bull.

    (2014)
  • R.S. Quilliam et al.

    Resolving conflicts in public health protection and ecosystem service provision at designated bathing waters

    J. Environ. Manag.

    (2015)
  • L.A. Amaral-Zettler et al.

    The biogeography of the Plastisphere: implications for policy

    Front. Ecol. Environ.

    (2015)
  • D.K.A. Barnes

    Human rubbish assists alien invasions of seas

    Sci. World J.

    (2002)
  • D.K.A. Barnes

    Invasions by marine life on plastic debris

    Nature

    (2002)
  • D.K.A. Barnes et al.

    Rafting by five phyla on man-made flotsam in the Southern Ocean

    Mar. Ecol. Prog. Ser.

    (2003)
  • D.K.A. Barnes et al.

    Drifting plastic and its consequences for sessile organism dispersal in the Atlantic Ocean

    Mar. Biol.

    (2005)
  • D.K.A. Barnes et al.

    Accumulation and fragmentation of plastic debris in global environments

    Philos. Trans. R. Soc. Lond. B

    (2009)
  • M. Bravo et al.

    Rafting on abiotic substrata: properties of floating items and their influence on community succession

    Mar. Ecol. Prog. Ser.

    (2011)
  • J.-F. Briand et al.

    Pioneer marine biofilms on artificial surfaces including antifouling coatings immersed in two contrasting French Mediterranean coast sites

    Biofouling

    (2012)
  • M.A. Browne et al.

    Ingested microscopic plastic translocates to the circulatory system of the mussel, Mytilus edulis (L.)

    Environ. Sci. Technol.

    (2008)
  • M.A. Browne et al.

    Spatial patterns of plastic debris along estuarine shorelines

    Environ. Sci. Technol.

    (2010)
  • M.A. Browne et al.

    Accumulation of microplastic on shorelines worldwide: sources and sinks

    Environ. Sci. Technol.

    (2011)
  • M.A. Browne et al.

    Spatial and temporal patterns of stranded intertidal marine debris: is there a picture of global change?

    Environ. Sci. Technol.

    (2015)
  • S.E. Bryan et al.

    Rapid, long-distance dispersal by pumice rafting

    PloS One

    (2012)
  • E.J. Carpenter et al.

    Plastics on the Sargasso sea surface

    Science

    (1972)
  • E.J. Carpenter et al.

    Polystyrene spherules in coastal waters

    Science

    (1972)
  • Cited by (243)

    • Understanding the role of microplastics in oral cancer

      2024, Pathology Research and Practice
    View all citing articles on Scopus
    View full text