Abstract
Microplastics are an emerging marine pollutant. It is important to understand their distribution in the marine environment and their implications on marine habitats and marine biota. Microplastics have been found in almost every marine habitat around the world, with plastic composition and environmental conditions significantly affecting their distribution. Marine biota interact with microplastics including birds, fish, turtles, mammals and invertebrates. The biological repercussions depend on to the size of microplastics encountered, with smaller sizes having greater effects on organisms at the cellular level. In the micrometre range plastics are readily ingested and egested, whereas nanometre-sized plastics can pass through cell membranes. Despite concerns raised by ingestion, the effects of microplastic ingestion in natural populations and the implications for food webs are not understood. Without knowledge of retention and egestion rates of field populations, it is difficult to deduce ecological consequences. There is evidence to suggest that microplastics enter food chains and there is trophic transfer between predators and prey. What is clear is that further research on a variety of marine organisms is required to understand the environmental implications of microplastics in more detail and to establish effects in natural populations.
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1 Introduction
With the increasing reliance on plastics as an everyday item, and rapid increase in their production and subsequent disposal, the environmental implications of plastics are a growing concern. The benefits of plastics, including their durability and resistance to degradation, inversely result in negative environmental impacts. As user-plastics are primarily “single use” items they are generally disposed of within one year of production, and whilst some plastic waste is recycled, the majority ends up in land-fill. Concerns arise when plastics enter the marine environment through indiscriminate disposal and it has been estimated that up to 10 % of plastic debris produced will enter the sea (Thompson 2006). Interactions between litter and the marine environment are complex. The impacts of larger plastic debris are discussed by Kühn et al. (2015) and consequences include aesthetic, social and economic issues (Newman et al. 2015), and numerous environmental impacts on marine biota (Derraik 2002; Barnes et al. 2009). However, with an ever increasing reliance on plastic products, and as plastic production, use and disposal continue, microplastics are of increasing concern (Sutherland et al. 2010). Microplastics enter the sea from a variety of sources (Browne 2015) and distributed by oceans currents; these ubiquitous contaminants are widespread (Cózar et al. 2014). The amount of microplastics in the sea will continue to rise, leading to gradual but significant accumulation in coastal and marine environments (Andrady and Neal 2009).
Increasing evidence of microplastics in the sea has led to a need to understand its environmental impacts as a form of marine pollution. A recent review of marine debris research found only 10 % of publications to focus on microplastics, the majority of which were from the last decade (CBD 2012). Even though plastic is the primary constituent of marine debris, microplastics are considered under-researched due to difficulties in assessing their distribution and abundance (Doyle et al. 2011). It has only been in recent years that international, national and regional efforts were made to quantify microplastics in the sea. The Marine Strategy Framework Directive (MSFD, 2008/56/EC) has highlighted concerns for environmental implications of marine litter and one of the key attributes of the MSFD is to determine the ecological harm caused by microplastics and their associated chemicals (Zarfl et al. 2011).
Microplastics were first described as microscopic particles in the region of 20 µm diameter (Thompson et al. 2004). For the purpose of this study, microplastic refers to items <5 mm in size using the criteria developed by US National Oceanic and Atmospheric Administration (NOAA) (Arthur et al. 2009). The small size of microplastics makes them available for interaction with marine biota in different trophic levels. By inhabiting different marine habitats, a range of organisms are vulnerable to exposure (Wright et al. 2013a). At the millimetre and micrometre scale, sorption of microplastics is dominated by bulk portioning, with effects including blockages when fibres or fragments form aggregates. Whereas at smaller size ranges, specifically the nanometre scale, there is a potential for microplastics to cause harm to organisms (Galloway 2015; Koelmans et al. 2015). Additionally, the consequences of exposure to chemicals associated with plastics are being investigated (Rochman 2015). A widely cited hypothesis explores how the large surface area to volume ratio of microplastics leaves them prone to adsorbing waterborne organic pollutants and the potential for toxic plasticisers to leach from polymer matrices into organisms tissues (Teuten et al. 2007). It was further hypothesized that if subsequently ingested, microplastics may act as a route for toxin introduction to the food chain (Teuten et al. 2009). Whether microplastics act as vectors depends on the gradient between microplastics and biota lipids (Koelmans 2015).
It is important to understand the transport and distribution of microplastics before understanding their fate, including the physical and chemical effects they could have on marine organisms. The objectives of this chapter are to assess the environmental impact of microplastic in the sea by: (1) summarising the distribution of marine microplastics, including the use of models to understand the distribution; (2) determine the interaction of microplastics with marine organisms.
2 The Global Distribution of Microplastics in the Sea
From strandlines on beaches to the deep seafloor and throughout the water column, microplastic research is dominated by studies monitoring microplastic distribution and abundance in the marine environment (Ivar du Sol and Costa 2014). A recent estimate suggested there could be between 7000 and 35,000 tons of plastic floating in the open ocean (Cózar et al. 2014). Another study estimated that more than five trillion pieces of plastic and >250,000 t are currently floating in the oceans (Eriksen et al. 2014). Once in the sea microplastics are transported around the globe by ocean currents where they persist and accumulate. Microplastics are suspended in the water column (e.g. Lattin et al. 2004), surface waters (e.g. Cózar et al. 2014), coastal waters (e.g. Ng and Obbard 2006), estuaries (e.g. Browne et al. 2010), rivers (Sadri and Thompson 2014), beaches (e.g. Browne et al. 2011) and deep-sea sediments (Van Cauwenberghe et al. 2013b; Woodall et al. 2014; Fischer et al. 2015). Suspended in the water column, microplastics can become trapped by ocean currents and accumulate in central ocean regions (e.g. Law et al. 2010). Ocean gyres and convergent zones are noteworthy areas of debris accumulation, as the rotational pattern of currents cause high concentrations of plastics to be captured and moved towards the centre of the region (Karl 1999). As gyres are present in all of the world’s oceans, microplastic accumulation can occur at a global scale and has been documented during the past four decades. Distribution is further influenced by wind mixing, affecting the vertical movement of plastics (Kukulka et al. 2012). Physical characteristics of plastic polymers, including their density, can influence their distribution in the water column and benthic habitats (Murray and Cowie 2011). Buoyant plastics float at the surface, whereas more dense microplastics or those fouled by biota sink to the sea floor. It has recently been estimated that 50 % of the plastics from municipal waste have a higher density than seawater such that it will readily sink to the seafloor (Engler 2012). It is currently not economically feasible nor is it desirable to remove microplastics from the ocean.
A number of concerns have been raised regarding the assessment of microplastic distribution. There are multiple pathways for the introduction of microplastics into the marine environment which do not have accurate timescales for the rate of degradation (Ryan et al. 2009). Quantification is complicated by the size of the oceans in relation to the size of plastics being assessed (Cole et al. 2011), which are further confounded by ocean currents and seasonal patterns introducing spatial and temporal variability (Doyle et al. 2011). As a result, there are various techniques applied to the sampling of microplastics in the marine environment (Löder and Gerdts 2015). Results of studies have been reported in different dimensions, e.g. the number of microplastics in a known water volume (particles m−3) or area measurements (particles km−2). This discrepancy presents a problem when comparing between studies, as it is not possible to compare results directly. For the purpose of this review, which aims to carry out a critical assessment of the global knowledge of microplastic distribution, a conversion was made to enable comparisons between the different dimensions of measurement. It is reasonable to assume that surface samples are collected in the top 0.20 m of water and therefore by making a simple calculation to add a third dimension (firstly converting particle km−2 to m−2, then multiplying by 0.20 m to convert to a volume measurement, m−3) we are able to compare different sampling methods in a variety of geographical locations. However, because of current directions in relation to boats, and approximate vessel speeds, it is difficult to calculate the amount of water passing through a net. As nets can ride out of the water, the exact volume of water passing through is unknown: the calculations have to be considered, at best, estimations.
It is important to understand the distribution of microplastics in the sea to grasp their potential impacts. This section will present a number of studies documenting microplastics in geographical regions including the Pacific, Atlantic, European Seas and the Mediterranean Sea, Indian Ocean and polar regions. It will introduce modelling strategies that have been utilised to understand microplastic distribution and accumulation around the globe.
2.1 Microplastics in the Pacific Ocean
Numerous studies on microplastics have been undertaken in the Pacific Ocean, the world’s largest water basin (Table 10.1). One area which has received considerable attention is the North Pacific Central Gyre (NPCG) located off the west coast of California, USA. The gyre contains possibly the most well publicised area of plastic accumulation, known as the “Great Pacific Garbage Patch” (Kaiser 2010). Microplastic concentrations in the NPCG have increased by two orders of magnitude in the last four decades (Goldstein et al. 2012). In comparison, microplastic abundance in the North Pacific subtropical gyre (NPSG) is widespread and spatially variable, but values are two orders of magnitude lower than in the NPCG (Goldstein et al. 2013). Microplastic studies in the south Pacific are limited to the subtropical gyre where an increasing trend of microplastics was found towards the centre of the gyre (5.38 particles m−3 Footnote 1 Eriksen et al. 2013). In a similar way to macroplastic debris, oceanographic features strongly affect the distribution of microplastics in open oceans and areas of upwelling create oceanographic convergence zones for marine debris.
Coastal ecosystems of the Pacific appear to be impacted by microplastics in areas of nutrient upwelling (Doyle et al. 2011) and influenced by local weather systems (Moore et al. 2002; Lattin et al. 2004). Microplastic load increased further inshore, reflecting the inputs from terrestrial runoff and particles re-suspended from sediments following storms (Lattin et al. 2004). Microplastics are in turn transported by ocean currents from populated coastal areas (Reisser et al. 2013). This is also reflected in offshore subsurface waters which had 4–27 times less plastics than coastal sites in the northeast Pacific (Desforges et al. 2014).
Pre-production plastic resin pellets and fragments wash up on coastlines worldwide and have been recovered from several Pacific beaches (Table 10.2). Plastic pellets, typically 3–5 mm in size, are made predominantly from the polymers polyethylene and polypropylene (Endo et al. 2005; Ogata et al. 2009). The average abundance of plastic fragments on beaches in the southeast Pacific was greater in isolated areas (Easter Island: >800 items m−2) than on beaches from continental Chile (30 items m−2) (Hidalgo-Ruz and Thiel 2013). This trend has been seen in the Hawaiian archipelago, where the remotest beaches on Midway Atoll and Moloka’I contained the highest quantity of plastic particles (McDermid and McMullen 2004; Corcoran et al. 2009; Cooper and Corcoran 2010).
2.2 Microplastics in the Atlantic Ocean
Research on microplastic distribution in the Atlantic is less extensive than in the Pacific (Table 10.3), but includes a number of long-term studies. A time-series conducted in the north Atlantic and Caribbean Sea identified microplastics in 62 % of the trawls conducted with densities reaching 580,000 particles km−2 (Law et al. 2010). Distinct patterns emerged with the highest concentration (83 % of plastics) in subtropical latitudes, 22°N and 88°N, of the north Atlantic gyre marking the presence of a large-scale convergence zone (Law et al. 2010; Morét-Ferguson et al. 2010) similar to the south Pacific (Eriksen et al. 2013). Converging surface currents driven by winds are assumed to be the driving force of this accumulation. To assess long-term trends in abundance, a time-series data set of continuous plankton recorder (CPR) samples from north Atlantic shipping routes were re-examined and microplastics were identified from the 1960s with a significant increase over time (Thompson et al. 2004). Regular sampling schemes have begun to monitor the spatial and temporal trends of microplastics in the northeast Atlantic and found microplastics to be widespread and abundant (Lusher et al. 2014).
Microplastics accumulate in the coastal pelagic zones of the Atlantic (Table 10.3). Water samples from the Portuguese coast identified microplastics in 61 % of the samples with higher concentrations found in Costa Vicentina and Lisbon (0.036 and 0.033 particles m−3, respectively) than in the Algarve and Aveiro (0.014 and 0.002 particles m−3, respectively). These results are probably related to the proximity to urban areas and river runoff (Frias et al. 2014), which is similar to the trend seen in the Pacific. Following a MARMAP cruise in the south Atlantic, microplastic beads were present in 14.6–34.2 % of tows conducted (van Dolah et al. 1980). Pelagic subsurface plankton samples from a geographically isolated archipelago, Saint Peter and Saint Paul, were not free of microplastic fragments. Modelling studies suggested that oceanographic mechanisms promote the topographic trapping of zooplankton and therefore microplastics might be retained by small-scale circulation patterns (Ivar do Sul et al. 2013). Additionally, research in the Firth of Clyde (U.K.) indicated that intense environmental sampling regimes are necessary to encompass the small-scale and temporal variation in coastal microplastic abundance (Welden, pers. comm.).
Microplastic granules and pellets have been identified on Atlantic beaches since the 1980s (Table 10.4). It was hypothesised that pre-production pellets are transported by trans-oceanic currents before being washed ashore in areas such as the mid-Atlantic Archipelago, Fernando de Noronha (Ivar do Sul et al. 2009). Fragments make up a considerable proportion of marine debris on saltmarsh beaches in North Carolina (Viehman et al. 2011), the Canary Islands (Baztan et al. 2014) and beaches and intertidal plains in Brazil (Costa et al. 2010, 2011). Whereas, fibres were primarily identified in sediment samples from an intertidal ecosystem in Nova Scotia, Canada (Mathalon and Hill 2014).
2.3 Microplastics in European Seas and the Mediterranean Sea
Marine litter including microplastic is a serious concern in the Mediterranean, with plastics accounting for 70–80 % of litter identified (Fossi et al. 2014). This enclosed water basin is not free of microplastic contamination (Table 10.5). Levels of microplastics in surface waters of the northwest Mediterranean were similar to those reported for the NPCG, (0.27 particles m−3 Footnote 2 Collignon et al. 2012), and areas far away from point sources of pollution have high microplastic abundance (0.15 particles m−3; de Lucia et al. 2014). Interestingly, fewer particles were recorded from surface waters from coastal Corsica (0.012 particles m−3 Footnote 3 ;Collignon et al. 2014). Microplastic distribution is strongly influenced by wind stress, which may redistribute particles in the upper layers of the water column and preclude sampling by surface tows (Collignon et al. 2012). Oceanographic influences may affect the distribution of microplastics in the Mediterranean. Further research will help to clarify if the new hypothesis by de Lucia et al. (2014) holds, which suggests that upwelling dilutes the amount of plastic in the surface waters.
Microplastics, including beads and pellets, have been widely reported for sedimentary habitats and beaches in European Seas and the Mediterranean Sea (Table 10.6). Microplastics have been extracted from sediments from Norderney, in the North Sea (Dekiff et al. 2014; Fries et al. 2013) and samples taken at the East Frisian Islands, where tidal flats were more contaminated than sandy beaches (Liebezeit and Dubaish 2012). Areas of low hydrodynamics appear to have high microplastic abundance, such as the Venice lagoon (Vianello et al. 2013). Reduced water movement could also be attributed to the difference between concentrations of microplastics in Belgium: higher concentrations of microplastics were identified in sediments from Belgium harbors (Claessens et al. 2011) than in beach samples (Van Cauwenberghe et al. 2013a). Lastly, microplastics were recorded in deep offshore sediments (Van Cauwenberghe et al. 2013b; Fischer et al. 2015), which shows that microplastics sink to the deep seafloor. In fact, the deep seafloor may be considered a major sink for microplastic debris (Woodall et al. 2014) and explain the current mismatch between estimated global inputs of plastic debris to the oceans (Jambeck et al. 2015) and field data (Cózar et al. 2014; Eriksen et al. 2014), which refer largely to floating litter.
2.4 Microplastics in the Indian Ocean and Marginal Seas
To date there are few large-scale reports on microplastics from the Indian Ocean. Reddy et al. (2006) reported microplastic fragments from a ship-breaking yard in the Arabian Sea, and microplastics accounted for 20 % of the plastics recorded on sandy beaches in Mumbai (Jayasiri et al. 2013). Pellets were also recorded on Malaysian beaches (Ismail et al. 2009). Most of the studies shown in Table 10.7 are part of the “International Pellet Watch” (Takada 2006; Ogata et al. 2009). Shoreline surveys conducted in surface waters and sediments on Singapore’s coasts identified microplastics >2 µm (Ng and Obbard 2006). This highlights an area that requires further investigation to obtain a wider picture of microplastic distribution around the globe.
2.5 Microplastics in Polar Regions
Prior to 2014, there had been no direct studies of microplastics in either the Arctic or Antarctica; the plastic flux into the Arctic Ocean has been calculated to range between 62,000 and 105,000 tons per year, with variation due to spatial heterogeneity, temporal variability and different sampling methods (Zarfl and Matthies 2010). With the estimated value four to six orders of magnitude below the atmospheric transport and ocean current fluxes, the study concluded that plastic transport levels to the Arctic are negligible and that plastics are not a likely vector for organic pollutants to the Arctic. However, Obbard et al. (2014) published results from ice cores collected from remote locations in the Arctic Ocean. The levels of microplastics observed (range: 38–234 particles m−3) were two orders of magnitude greater than previously reported in the Pacific gyre (Goldstein et al. 2012). Macroplastics have been identified floating in surface waters of Antarctica. However, trawls for microplastics did not catch any particles (Barnes et al. 2010). Dietary studies of birds from the Canadian Arctic have reported ingested plastics (Mallory et al. 2006; Provencher et al. 2009, 2010), and macroplastics were observed on the deep Arctic seafloor (Bergmann and Klages 2012). This indirect evidence suggests that microplastics have already entered polar regions. A modelling study even suggests the presence or formation of a sixth garbage patch in the Barents Sea (van Sebille et al. 2012).
2.6 Modelling the Distribution of Microplastics
Studies have highlighted the interaction of oceanographic and environmental variables on the distribution of microplastics (e.g. Eriksen et al. 2013). As polymer densities affect the distribution of plastics in the water column, it is important to understand how microplastics are transported at the surface and at depths. Knowledge of point-source pollution, including riverine input and sewage drainage into marine and coastal environments, can be useful in understanding the extent to which certain ecosystems are affected. Furthermore, knowledge of plastic accumulation on beaches will benefit the study of microplastics. For example, a study of plastic litter washed onto beaches developed a particle tracking model, which indicated that, if levels of plastic outflow remain constant over the coming decade, plastic litter quantity on beaches would continue to increase, and in some cases (3 % of all east Asian beaches) could see a 250-fold increase in plastic litter (Kako et al. 2014). If not removed, these larger items of plastic litter will break down into microplastics over time.
The fate of plastics in the marine environment is affected by poorly understood geophysical processes, including ocean mixing of the sea-surface boundary layer, re-suspension from sediments, and sinking rates plastics denser than seawater. Modelling approaches are required to further understand, and accurately estimate the global distribution, residence time, convergence zones, and ecological consequences of microplastics (Ballent et al. 2013). Models predicting the breakdown, fragmentation, and subsequent mixing and re-suspension of microplastics in sediments and seawater could provide an estimation of microplastic accumulation over short and long time scales; as well as an estimation of the dispersal patterns of microplastics in the marine environment. Generalized linear models have indicated that oceanographic mechanisms may promote topographic trapping of zooplankton and microplastics, which may be retained by small-scale circulation patterns in the Equatorial Atlantic, suggesting there is an outward gradient of microplastics moving offshore (Ivar do Sul et al. 2013). The recovery of plastic from surface seawater is dependent on wind speeds: stronger winds resulted in the capture of fewer plastics because wind-induced mixing of the surface layer vertically distributes plastics (Kulkula et al. 2012). Furthermore, by integrating the effect of vertical wind mixing on the concentrations of plastics in Australian waters, researchers estimated depth-integrated plastic concentrations, with high concentrations expected at low wind speeds. Thus, with the inverse relationship between wind force and plastic concentration, net tow concentrations of microplastics increased by a factor of 2.8 (Reisser et al. 2013).
Ballent et al. (2013) used the MOHID modelling system to predict the dispersal of non-buoyant pellets in Portugal using their density, settling velocity and re-suspension characteristics. Researchers simulated the transport of microplastic pellets over time using oceanographic processes, scales and systems. Model predictions suggest that the bottom topography restricts pellet movement at the head of the Nazaré Canyon with a potential area of accumulation of plastics pellets on the seafloor, implying long-term exposure of benthic ecosystems to microplastics. Tidal forces, as well as large-scale oceanographic circulation patterns are likely to transport microplastics up and down the Nazaré Canyon, which may be greatly increased during mass transport of waters linked to storms (Ballent et al. 2013) or deep-water cascading events (Durrieu de Madron et al. 2013).
With residence times from decades to centuries predicted for microplastics in the benthic environment (Ballent et al. 2013), future studies should assess the degradation of microplastics on the seafloor to be able to estimate residence times in those potential sink environments. Coupled with observations of microplastics in surface waters, the total oceanic plastic concentrations might be underestimated because of limited but growing knowledge of the geophysical and oceanographic processes in the surface waters. Furthermore, as microplastics degrade towards a nanometre scale, transport properties may be affected, and as a result, long-term transport models will need to be corrected. Modelling should be adapted to bring in ecological consequences of microplastics in benthic environments and the water column. Research should focus on critical areas such as biodiversity hotspots and socio-economic hotspots that could affect vulnerable marine biota and coastal communities.
2.7 Summary
Microplastics have been documented in almost every habitat of the open oceans and enclosed seas, including beaches, surface waters, water column and the deep seafloor. Although most water bodies have been investigated, there is a lack of published work from polar regions and the Indian Ocean. Further research is required to accurately estimate the amount of different types of microplastics in benthic environments around the globe. Distribution of microplastics depends on environmental conditions including ocean currents, horizontal and vertical mixing, wind mixing and biofilm formation, as well as the properties of individual plastic polymers. A number of modelling approaches have been considered in the recent literature, which highlighted the effect of wind on the distribution of microplastics in the ocean. Oceanographic modelling of floating debris has shown accumulation in ocean gyres, and the distribution of microplastics within the water column appears to be dependent on the composition, density and shape of plastic polymers affecting their buoyancy. Further modelling studies may help to identify and predict regions with ecological communities and fisheries more vulnerable to the potential consequences of plastic contamination. The distribution of microplastic plays a significant role in terms of which organisms and habitats are affected. Widespread accumulation and distribution of microplastics raises concerns regarding the interaction and potential effects on marine organisms.
3 Interactions of Microplastics with Marine Organisms
Recently, Wright et al. (2013a) discussed the biological factors, which could enhance microplastic bioavailability to marine organisms: the varying density of microplastics allows them to occupy different areas of the water column and benthic sediments. As microplastics interact with plankton and sediment particles, both suspension and deposit feeders may be at risk of accidentally or selectively ingesting marine debris. However, the relative impacts are likely to vary across the size spectrum of microplastic in relation to the organisms affected, which is dependent on the size of the microplastic particles encountered. Microplastics in the upper end of the size spectrum (1–5 mm) may compromise feeding and digestion. For example, Codina-García et al. (2013) isolated such pellets and fragments from the stomachs of seabirds. Particles <20 µm are actively ingested by small invertebrates (e.g. Thompson et al. 2004) but they are also egested (e.g. Lee et al. 2013). Studies have shown that nanoparticles can translocate (e.g. Wegner et al. 2012) and model simulations have indicated that nano-sized polystyrene (PS) particles may permeate into the lipid membranes of organisms, altering the membrane structure, membrane protein activity, and therefore cellular function (Rossi et al. 2013). The following section deals with incidences of ingestion, trophic transfer and provision of new habitat by the presence of microplastics in the marine environment. Although the sections contain examples, comprehensive lists of microplastics ingestion are included in the corresponding tables.
3.1 Ingestion
Ingestion is the most likely interaction between marine organisms and microplastics. Microplastics’ small size gives them the potential to be ingested by a wide range of biota in benthic and pelagic ecosystems. In some cases, organisms feeding mechanisms do not allow for discrimination between prey and anthropogenic items (Moore et al. 2001). Secondly, organisms might feed directly on microplastics, mistaking them for prey or selectively feed on microplastics in place of food (Moore 2008). If there is a predominance of microplastic particles associated with planktonic prey items, organisms could be unable to differentiate or prevent ingestion. A number of studies have reported microplastics from the stomachs and intestines of marine organisms, including fish and invertebrates. Watts et al. (2014) showed that shore crabs (Carcinus maenas) will not only ingest microplastics along with food (evidence in the foregut) but also draw plastics into the gill cavity because of their ventilation mechanism: this highlights that it is important to consider all sorts of routes of exposure to microplastics. If organisms ingest microplastics they could have adverse effects on individuals by disrupting feeding and digestion (GESAMP 2010). Laboratory (Table 10.8) and field (Table 10.9) studies highlighted that microplastics are mistaken for food by a wide variety of animals including birds, fish, turtles, mammals and invertebrates. Despite concerns raised regarding microplastic ingestion, few studies specifically examined the occurrence of microplastic in natural, in situ, populations as it is methodologically challenging to assess microplastic ingestion in the field (Browne et al. 2008).
3.1.1 Planktonic Invertebrates
Microplastics can enter the very base of the marine food web via absorption. Such was observed when charged nano-polystyrene beads were absorbed into the cellulose of a marine alga (Scenedesmus spp.), which inhibited photosynthesis and caused oxidative stress (Bhattacharya et al. 2010). Microplastics can also affect the function and health of marine zooplankton (Cole et al. 2013; Lee et al. 2013). Decreased feeding was observed following ingestion of polystyrene beads by zooplankton (Cole et al. 2013). Furthermore, adult females and nauplius larvae of the copepod (Tigriopus japonicus) survived acute exposure, but increased mortality rates were observed following a two-generation chronic toxicity test (12.5 µg mL−1) (Lee et al. 2013). Although a third of gooseneck barnacle (Lepas spp.) stomachs examined contained microplastics, no adverse effect was reported for these filter feeders (Goldstein and Goodwin 2013). Interestingly, the stomachs of mass stranded Humboldt squids (Dosidicus gigas) contained plastic pellets (Braid et al. 2012). This large predatory cephalopod usually feeds at depth between 200 and 700 m. The route of uptake is unclear; the squid may have fed directly on sunken pellets, or on organisms with pellets in their digestive system.
3.1.2 Benthic Invertebrates
A number of benthic invertebrates have been studied under laboratory conditions to investigate the consequences of microplastic ingestion (Table 10.8). Laboratory feeding and retention trials have focused on direct exposure of invertebrates to microplastic particles (as summarised by Cole et al. 2011; Wright et al. 2013a). Exposure studies demonstrated that benthic invertebrates including lugworms (Arenicola marina), amphipods (Orchestia gammarellus) and blue mussels (Mytilus edulis) feed directly on microplastics (Thompson et al. 2004; Wegner et al. 2012), and deposit-feeding sea cucumbers even selectively ingested microplastic particles (Graham and Thompson 2009).
Although microplastic uptake was recorded for a number of species, organisms appear to reject microplastics before digestion and excrete microplastics after digestion. Pseudofaeces production is a form of rejection before digestion but requires additional energetic cost. Furthermore, prolonged pseudofaeces production could lead to starvation (Wegner et al. 2012). On the other hand, polychaete worms, sea cucumbers and sea urchins are able to excrete unwanted materials through their intestinal tract without suffering obvious harm (Thompson et al. 2004; Graham and Thompson 2009; Kaposi et al. 2014). Adverse effects of microplastic ingestion were reported for lugworms: weight loss was positively correlated with concentration of spiked sediments (40–1300 µm polystyrene) (Besseling et al. 2013). Similarly, Wright et al. (2013b) recorded significantly reduced feeding activity and significantly decreased energy reserves in lugworm exposed to 5 % un-plasticised polyvinyl chloride (U-PVC). Supressed feeding reduced energy assimilation, compromising fitness. At the chronic exposure level, either fewer particles were ingested overall or a lack of protein coating on the U-PVC may have weakened particle adhesion to the worm's feeding apparatus.
Several studies have raised concern for microplastic retention and transference between organisms’ tissues. For example, microplastics were retained in the digestive tract of mussels, and transferred to the haemolymph system after three days (Browne et al. 2008). However, negative effects on individuals were not detected. Von Moos et al. (2012) tracked particles of high density polyethylene (HDPE) into the lysosomal system of mussels after three hours of exposure; particles were taken up by the gills and transferred to the digestive tract and lysosomal system, again triggering an inflammatory immune response. It should be noted, however, that while these studies succeeded in determining the pathways of microplastics in organisms the exposure concentrations used to achieve this goal exceeded those expected in the field, such that the results have to be treated with care.
Studies of microplastic ingestion by benthic invertebrates in the field are less common than laboratory studies. Murray and Cowie (2011) identified fibres of monofilament plastics that could be sourced to fibres of trawls and fragments of plastic bags in the intestines of the commercially valuable Norway lobster (Nephrops norvegicus). These results indicated that normal digestive processes do not eliminate some of the filaments as they cannot pass through the gastric mill system. Norway lobsters have various feeding modes, including scavenging and predation, and are not adapted to cut flexible filamentous materials (Murray and Cowie 2011). The identification of microplastics in organisms that are caught for commercial purposes and subsequently consumed whole (including guts) highlights the potential human health implications. For example, field-caught brown shrimps (Crangon crangon) (Pott 2014) and farmed and store-brought bivalves (De Witte et al. 2014; Van Cauwenberghe and Janssen 2014) had microplastics in their digestive system.
Invertebrates could be used as indicator species for environmental contamination. Species such as Nephrops are able to integrate seasonal variation in microplastic abundance, providing an accurate measure of environmental contamination (Welden, pers. comm.). Additional studies are required to understand the flux of microplastic within benthic sediments and the interaction between different species of benthic infauna feeding in/or manipulating the sediment, such as bivalves and worms. Benthic infauna could ingest and/or excrete microplastics, the individuals or their faecal pellets may in turn be ingested by secondary consumers, thus affecting higher trophic levels.
3.1.3 Fish
Some of the earliest studies noting ingestion of microplastics by wild-caught fish include coastal species from the USA (Carpenter et al. 1972) and the U.K. (Kartar et al. 1973, 1976). More recent studies from the NPCG reported microplastic (fibres, fragments and films) ingestion by mesopelagic fish (Boerger et al. 2010; Davison and Asch 2011; Choy and Drazen 2013). Estuarine environments and their inhabitants are also prone to plastic contamination, which is hardly surprising given the riverine input (e.g. Morritt et al. 2014). Estuarine fish affected include catfish, Ariidae, (23 % of individuals examined) and estuarine drums, Scianenidae, (7.9 % of individuals examined), which spend their entire life cycle in estuaries (Possatto et al. 2011; Dantas et al. 2012). Similarly, 13.4 % of bottom-feeding fish (Gerreidae) from a tropical estuary in northeast Brazil contained microplastics in their stomachs (Ramos et al. 2012). The authors suggested that ingestion occurred during suction feeding on biofilms.
Lusher et al. (2013) reported microplastic polymers from 10 fish species from the English Channel. Of the 504 fish examined, 37 % had ingested a variety of microplastics, the most common being polyamide and the semi-synthetic material rayon. Similarly, Boerger et al. (2010) recorded microplastics in 35 % planktivorous fish examined from the NPCG (94 % of which were plastic fragments). Fish from the northern North Sea ingested microplastics at significantly lower levels (1.2 %) compared to those from the southern North Sea (5.4 %) (Foekema et al. 2013). All the studies cited suggest direct ingestion as the prime route of exposure, either targeted as food or mistaken for prey items. No adverse effects of ingestion were reported. Consequently, studies are required to follow the route of microplastic ingestion in fish, to assess if microplastics are egested in faecal pellets as seen in invertebrates. Dos Santos and Jobling (1992) showed that microplastic beads (2 mm) were excreted quickly following ingestion, whereas larger beads (5 mm) were held for prolonged periods of time. This implies that larger items of plastic might pose a greater risk following ingestion whereas smaller microplastics are likely to be excreted along with natural faeces.
3.1.4 Sea Birds
Numerous studies have dealt with the ingestion of marine debris by sea birds (see Kühn et al. 2015). Microplastics and small plastic items have been isolated from birds targeted deliberately for dietary studies, dead cadavers, regurgitated samples and faeces (Table 10.10). Nearly 50 species of Procellariiformes (fulmars, petrels, shearwaters, albatrosses), known to feed opportunistically at the sea surface had microplastics in their stomachs. Ingested microplastics appeared to comprise primarily of pellets and user-fragments (Ryan 1987; Robards et al. 1995) although there was a decrease in the proportion of pellets ingested by birds from the south Atlantic between the 1980s and 2006 (Ryan 2008). This trend is also true for short-tailed shearwater (Puffinus tenuirostris) from the North Sea (Vlietstra and Parga 2002). In this case however, the mass of industrial plastics (pellets) have decreased by half and the mass of plastic fragments has tripled (van Franeker et al. 2011). It is possible that the shift in the type of plastic consumed may be explained by fragmentation of larger user-plastics into smaller microplastics, the accumulation of user-plastic over time and a decreased disposal of industrial plastics (Thompson et al. 2004), or simply by a stronger awareness of the presence of microplastics.
Seabirds appear to be able to remove microplastics from their digestive tracts as regurgitation has been observed in the boluses of glaucous-winged gulls (Larus glaucescens) (Lindborg et al. 2012). However, this suggests that parents expose their offspring to plastics during feeding. Juveniles of northern fulmars (Fulmarus glacialis) had more plastic in their intestines than adults (Kühn and van Franeker 2012), with higher quantities in areas of higher fishing and shipping traffic (van Franeker et al. 2011). Still, as the majority of birds examined did not die as a direct result of microplastic uptake, it can be concluded that microplastic ingestion does not affect seabirds as severely as macroplastic ingestion. To date, there have been no studies demonstrating nanometre-sized microplastics in sea birds. This could be because it is extremely difficult to control laboratory conditions in terms of contamination.
3.1.5 Marine Mammals
Only one study on microplastic ingestion by marine mammals has been published to date. Bravo Rebolledo et al. (2013) recorded microplastics in stomachs (11 %, n = 100) and intestines (1 %, n = 107) of harbour seals (Phoca vitulina). Direct microplastic ingestion by other species of marine mammals has not been observed. However, larger plastics items were identified in the stomachs of numerous cetaceans (46 % of all species; Baulch and Perry 2014, see also Kühn et al. 2015). The frequency of microplastic uptake by marine mammals is hitherto unknown, but could occur through filter feeding, inhalation at the water-air interface, or via trophic transfer from prey items. As baleen whales (Mysticetes) strain water between baleen plates, to trap planktonic organisms and small fish (Nemoto 1970), they may incidentally trap microplastics. Thus, their feeding mode may render baleen whales more susceptible to direct microplastic ingestion than toothed (Odotocetes) or beaked whales (Ziphiids) which are active predators of squid and fish (Pauly et al. 1998). It is also likely that marine mammals are exposed to microplastic via trophic transfer from prey species. For example, microplastics were recorded from the scats of fur seals (Arctocephalus spp.) believed to originate from lantern fish (Electrona subaspera) (Eriksson and Burton 2003).
Cetaceans were suggested as sentinels for microplastic pollution (Fossi et al. 2012a; Galgani et al. 2014). However, it is notoriously difficult to extract and subsequently assess microplastics from cetacean stomachs, the often large size and decomposition rate of stomachs make sampling almost impossible. Furthermore, strandings are infrequent and unpredictable. Although adaption of sampling methods for smaller organisms such as fish and birds have the potential to be implemented, further work is necessary. The assessment of phthalate concentrations in the blubber of stranded fin whales (Balaenoptera physalus) (Fossi et al. 2012b, 2014) could serve as an indicator for the uptake of microplastics, but this raises other concerns as it is not possible to distinguish the origin of the phthalates. Exposure routes could be via micro- or macroplastics or simply from direct uptake of chemicals from the surrounding seawater into the blubber. Further work is essential to assess if microplastics significantly affect marine mammals.
3.1.6 Sea Turtles
Although all species of marine turtle ingest macroplastics (Derraik 2002; Schuyler et al. 2014; Kühn et al. 2015), only one study reported plastic pellets in the stomachs of the herbivorous green turtles (Chelonia mydas) (Tourinho et al. 2010). It is highly likely that other species of sea turtle also ingest microplastics incidentally or directly, depending on their feeding habits (Schuyler et al. 2014). Neonatal and oceanic post-hatchlings are generalist feeders (Bjorndal 1997), targeting plankton from surface waters and microplastic uptake may occur. Trophic transfer from prey items could be a pathway to larger individuals; loggerhead (Caretta caretta) and Kemp’s Ridley (Lepidochelys kempii) turtles are carnivores, feeding on crustaceans and bivalves (Bjorndal 1997), which ingest microplastics (e.g. Browne et al. 2008). Flatbacks (Natator depressa) are also carnivores but feed on soft bodied invertebrates (Bjorndal 1997), including sea cucumbers, which again, ingest microplastics (Graham and Thompson 2009). Leatherbacks (Dermochelys coriacea) feed on gelatinous organisms (Bjorndal 1997) and are thus more likely to ingest macroplastics because of their size and similarity to prey items. If microplastics are ingested they could affect sea turtle growth and development if they are not egested. Additional work is required to understand whether turtles actively ingest microplastics, and if so, the extent of the harm caused.
3.2 Trophic Transfer
Absorption and ingestion of microplastics by organisms from the primary trophic level, e.g. phytoplankton and zooplankton, could be a pathway into the food chain (Bhattacharya et al. 2010). Many species of zooplankton undergo a diurnal migration. Migrating zooplankton could be considered a vector of microplastic contamination to greater depths of the water column and its inhabitants, either through predation or the production of faecal pellets sinking to the seafloor (Wright et al. 2013a). Only a few studies deal with the potential for microplastics to be transferred between trophic levels following ingestion. Field observation highlighted the presence of microplastics in the scat of fur seals (Arctocephalus spp.) and Eriksson and Burton (2003) suggested that microplastics had initially been ingested by the fur seals’ prey, the plankton feeding Mycophiids. In feeding experiments, Farrell and Nelson (2013) identified microplastic in the gut and haemolymph of the shore crab (Carcinus maenas), which had previously been ingested by blue mussels (Mytilus edulis). There was large variability in the number of microspheres in tissues samples, and the results have to be treated with caution as the number of individuals was low and the exposure levels used exceeded those from the field. Similarly, Nephrops-fed fish, which had been seeded with microplastic strands of polypropylene rope were found to ingest but not to excrete the strands (Murray and Cowie 2011), again implying potential trophic transfer. As mentioned above, microplastics were also detected in cod, whiting, haddock, bivalves and brown shrimp, which are consumed by humans and raises concerns about trophic transfer to humans and human exposure (see Galloway 2015). Further studies are required to increase our understanding of trophic transfer.
3.3 Microplastic Effect on Habitats
Surfaces of buoyant microplastics provide habitats for rafting organisms. For example, pelagic insects (Halobates micans and H. sericeus) utilize microplastic pellets for oviposition (Goldstein et al. 2012; Majer et al. 2012). Indeed, Goldstein et al. (2012) attributed an overall increase in H. sericeus and egg densities in the NPCG to high concentrations of microplastics. Likewise, plastics serve as a floating habitat for bacterial colonisation (Lobelle and Cunliffe 2011). Microorganisms including Bacillus bacteria (mean: 1664 ± 247 individuals mm−2) and pennate diatoms (mean: 1097 ± 154 individuals mm−2) were identified on plastic items from the North Pacific gyre (Carson et al. 2013). These studies suggest that microplastics affect the distribution and dispersal of marine organisms and may represent vectors to alien invasion. Plastics colonised by pathogenic viruses or bacteria may spread the potential for disease, but there is currently no evidence to support this hypothesis.
Microplastic buried in sediments could have fundamental impacts on marine biota as they increase the permeability of sediment and decrease thermal diffusivity (Carson et al. 2011). This may affect temperature-dependent processes. For example, altered temperatures during incubation can bias the sex ratios of sea turtle eggs. At 30 °C, equal numbers of males and female embryos develop, whereas at temperatures <28 °C all embryos become male (Yntema and Mrosovsky 1982). With microplastics in sediments it will take longer to reach maximum temperatures because of its increased permeability. Therefore, eggs may require a longer incubation period, with more male hatchlings because of the insulating effect. Microplastic concentrations as low as 1.5 can decrease maximum temperatures by 0.75 °C (Carson et al. 2011), which has important implications for sexual bias in sea turtles including loggerhead turtles (Caretta caretta) and hawksbill turtles (Eretmochelys imbricata) (Yntema and Mrosovsky 1982; Mrosovsky et al. 1992). Changes in the sediment temperatures could also affect infaunal organisms as it may affect enzymatic and other physiological processes, feeding and growth rates, locomotory speeds, reproduction and ultimately population dynamics. However, this remains speculative until further researched.
3.4 Summary
Microplastic ingestion has been documented for a range of marine vertebrates and invertebrates (Fig. 10.1). Interactions were recorded primarily during controlled laboratory studies, but results from field sampling of wild populations also indicate microplastic ingestion. In the case of some invertebrates, adverse physiological and biological effects were reported. The biological repercussions depend on to the size of microplastics with smaller sizes having greater effects on organisms at the cellular level. In the micrometre range, plastics are readily ingested and egested whereas nanometre-sized plastics can pass through cell membranes. Acute exposure experiments demonstrated significant biological effects including weight loss, reduced feeding activity, increased phagocytic activity and transference to the lysosomal (storage) system. Larger microplastics (2–5 mm) may take longer to pass from the stomachs of organisms and could be retained in the digestive system, potentially increasing the exposure time to adsorbed toxins (see Rochman 2015).
Microplastic interactions in the marine environment including environmental links (solid arrows) and biological links (broken arrows), which highlights potential trophic transfer (Photos of microplastics: A. Lusher)
It is important to determine the ecological effects of microplastic ingestion. Studies are required to assess the contamination of more species of fish, marine mammals and sea turtles, as well as consequences of microplastic uptake and retention. Further research is necessary to determine the limits of microplastic translocation between tissues, and assess the differences between multiple polymer types and shapes. It is likely that additional species of invertebrate ingest microplastics in wild populations, as fibres and fragments found in the field are actively selected in experiments. Although some organisms appear to be able to differentiate between microplastics and prey, and microplastic excretion has been recorded. Without knowledge of retention and egestion rates of field populations, it is difficult to deduce ecological consequences. There is some evidence to suggest that microplastics enter the food chain and transfer of microplastics between trophic levels implies bioaccumulation and biomagnification. Despite concerns raised by ingestion in the marine environment, the effects of microplastic ingestion in natural populations and the implications for food webs are not understood. Such knowledge is crucial in order to be able to develop and implement effective management strategies (Thompson et al. 2009). Additional studies are required to understand the flux of microplastic from benthic sediments to the infauna. Lastly, microplastics provide open ocean habitats for colonisation by invertebrates, bacteria and viruses. As a result, these organisms can be transported over large distances by ocean currents and/or through the water column (Kiessling et al. 2015).
4 Conclusion
Microplastics have been found in almost every marine habitat around the world, and plastic density along with ocean currents appears to have a significant effect on their distribution. Modelling studies suggest that floating debris accumulates in ocean gyres but this is dependent on the composition and shape of individual polymers. The widespread distribution and accumulation of microplastics raises concerns regarding the interaction and potential effects of microplastics on marine organisms. As microplastics interact with plankton and sediments, both suspension and deposit feeders may accidentally or selectively ingest microplastics. Despite concerns regarding ingestion, only a limited number of studies examined microplastic ingestion in the field. Knowledge of the retention rates of microplastics would enable estimations of the impacts of microplastic uptake. If rejection occurs before digestion, microplastics might pose less of a threat to organisms than initially assumed. However, there could be energetic costs associated with the production of pseudofaeces. Laboratory studies can be used to determine the end point of microplastic ingestion, and would benefit from using multiple types of microplastics to simulate field conditions. Unfortunately, it is difficult to establish a direct link between microplastics and adverse effects on marine biota experimentally. Furthermore, due to the difficult nature of field studies, it will be harder to understand effects on natural populations.
As microplastic research is still in its infancy, there are many more unanswered questions, the answers to which are required to build on current knowledge to develop a clearer picture of the impact of microplastics in the sea.
Notes
- 1.
Calculated from km−2.
- 2.
Calculated from 1.334 particles m−2.
- 3.
Calculated from 0.062 particles m−2.
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Acknowledgments
The author would like to thank Emily Lorch, Julia Hemprich, Chelsea Rochman, Rick Officer and Ian O’Connor for their useful comments on an earlier draft. Bart Koelmans and an anonymous reviewer improved an earlier version of the manuscript. Marta Bolgan for the illustrations in Fig. 10.1. The author was awarded an Irish Research Council postgraduate scholarship [Project ID: GOIPG/2013/284] and a Galway-Mayo Institute of Technology 40th Anniversary studentship to conduct her Ph.D. research.
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Lusher, A. (2015). Microplastics in the Marine Environment: Distribution, Interactions and Effects. In: Bergmann, M., Gutow, L., Klages, M. (eds) Marine Anthropogenic Litter. Springer, Cham. https://doi.org/10.1007/978-3-319-16510-3_10
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