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Environmental Pollution 178 (2013) 483e492

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Environmental Pollution

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Review

The physical impacts of microplastics on marine organisms: A review

Stephanie L. Wright a,*, Richard C. Thompson b, Tamara S. Gallowaya

aBiosciences, College of Life and Environmental Sciences, Geoffrey Pope Building, University of Exeter, Stocker Road, Exeter, Devon EX4 4QD, United Kingdomb School of Marine Science and Engineering, University of Plymouth, Drake Circus, Plymouth, Devon PL4 8AA, United Kingdom

a r t i c l e i n f o

Article history:Received 13 October 2012Received in revised form7 February 2013Accepted 13 February 2013

Keywords:MicroplasticsPlastic debrisMarine litterMarine invertebratesFood web

* Corresponding author.E-mail address: sw393@exeter.ac.uk (S.L. Wright).

0269-7491/$ e see front matter � 2013 Elsevier Ltd.http://dx.doi.org/10.1016/j.envpol.2013.02.031

a b s t r a c t

Plastic debris at the micro-, and potentially also the nano-scale, are widespread in the environment.Microplastics have accumulated in oceans and sediments worldwide in recent years, with maximumconcentrations reaching 100 000 particles m3. Due to their small size, microplastics may be ingested bylow trophic fauna, with uncertain consequences for the health of the organism. This review focuses onmarine invertebrates and their susceptibility to the physical impacts of microplastic uptake. Some of themain points discussed are (1) an evaluation of the factors contributing to the bioavailability of micro-plastics including size and density; (2) an assessment of the relative susceptibility of different feedingguilds; (3) an overview of the factors most likely to influence the physical impacts of microplastics suchas accumulation and translocation; and (4) the trophic transfer of microplastics. These findings areimportant in guiding future marine litter research and management strategies.

� 2013 Elsevier Ltd. All rights reserved.

1. Introduction

In contemporary society, plastic has achieved a pivotal status,with extensive commercial, industrial, medicinal and municipalapplications. Demand is considerable; annual plastic production hasincreased dramatically from 1.5 million tonnes in the 1950s toapproximately 280 million tonnes in 2011 (PlasticsEurope, 2012).Through accidental release and indiscriminate discards, plasticwaste has accumulated in the environment at an uncontrollablerate, where it is subjected to wind and river-driven transport, ulti-mately reaching the coast. Due to its lightweight, durable nature,plastic has become a prevalent, widespread element of marine litter(Moore, 2008; Thompson et al., 2009); the most commonly pro-duced and therefore encountered polymers being polypropylene(PP), polyethylene (PE) and polyvinylchloride (PVC) composing 24%,21% and 19% of global plastic production in 2007, respectively(Andrady, 2011). Recently, inconspicuous microscopic plastic parti-cles, referred to here as ‘microplastics’, have been identified as aubiquitous component of marine debris. Defined as less than 5 mmin size by the National Oceanic and Atmospheric Administration(NOAA), microplastics can be of primary (purposefully manufac-tured to be of microscopic size) or secondary (derived from thefragmentation of macroplastic items) origin. They have been accu-mulating in oceansworldwide over the last four decades (Carpenter

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et al., 1972), from low background levels to localized ‘hotspots’ (seeTable 1). Present onbeaches, in surfacewaters, throughout thewatercolumn and within the benthos (Lattin et al., 2004; Moore et al.,2001; Thompson et al., 2004), microplastics have pervaded eventhe most remote marine environments (e.g. Ivar do Sul et al., 2009).

Gyres are particular hotspots for microplastic accumulation.Recently a maximum concentration and mass of 32.76 particles m3

and 250mgm3 respectively have been recorded in the North PacificSubtropical Gyre (Goldstein et al., 2012). Industrial coastal areashave also been identified as microplastic hotspots; concentrationsof approximately 100 000 plastic particles m3 of seawater havebeen reported in a Swedish harbour area adjacent to a PE produc-tion plant (Noren and Naustvoll, 2010). Sediment from denselypopulated coastal areas can be heavily contaminated with micro-plastics. Browne et al. (2011) found microplastics on eighteenshores across six continents, with a tendency towards fibrousshapes. Maximum concentrations of 124 fibres l�1 were reportedand a significant relationship between microplastic abundance andhuman population-density was found (Browne et al., 2011). Thus asthe human population continues to increase, the prevalence ofmicroplastics will also most probably increase. Previous studieshave found a predominance of fibrous microplastics (see Claessenset al., 2011; Thompson et al., 2004). Despite a variety of forms fromirregular fragments to spherules, it seems likely that fibrousmicroplastics are most abundant in the marine environment.

A temporal increase in the abundance of marine microplasticshas been indicated. Recently, combined data from peer-reviewedliterature, publicly available data and new data sets revealed

Table 1The spatial distribution and abundance of microplastics, as summarised from a selection of reports. Values are reported to the nearest integer.

Location Maximum observedconcentration

Reference

Coastal waters, Sweden 102 000 particles m3 Noren and Naustvoll, 2010Coastal Waters, California 3 particles m3 Doyle et al., 2011Coastal waters, New England 3 particles m3 Carpenter et al., 1972Open ocean, North West Atlantic 67 000 particles km2 Colton et al., 1974Northwest Mediterranean Sea 1 particle m2 Collignon et al., 2012Beach, Malta >1000 particles m2 Turner and Holmes, 2011Beach, UK 8 particles kg�1 Thompson et al., 2004Estuarine sediment, UK 31 particles kg�1 Thompson et al., 2004Subtidal sediment, UK 86 particles kg�1 Thompson et al., 2004Subtidal sediment, Florida 214 particles l�1 Graham and Thompson, 2009Subtidal sediment, Maine 105 particles l�1 Graham and Thompson, 2009Harbour sediment, Sweden 50 particles l�1 Norén, 2008Industrial harbour sediment, Sweden 3320 particles l�1 Norén, 2008Industrial coast sediment, Sweden 340 l�1 Norén, 2008Ship-breaking yard sediment, India 89 mg kg�1* Reddy et al., 2006Harbour sediment, Belgium 7 mg kg�1 Claessens et al., 2011Continental shelf sediment, Belgium 1 mg kg�1 Claessens et al., 2011Beach, Belgium 1 mg kg�1 Claessens et al., 2011Beach, Portugal 6 particles m2 Martins and Sobral, 2011Beach, East Frisian Islands, Germany 621 particles 10 g�1 Liebezeit and Dubaish, 2012

* Including glass wool.

S.L. Wright et al. / Environmental Pollution 178 (2013) 483e492484

changes in the abundance and mass of microplastics in the NorthPacific Subtropical Gyre. Abundance and mass increased by twoorders of magnitude from a median of 0e0.116 particles m3 and 0e0.086 mg m3, respectively from 1972e87 to 1999e2010. This isbelieved to have been driven by a localised increase in microplasticabundance (Goldstein et al., 2012). Additionally, North Atlantic andNorth Sea surface samples collected by a Continuous PlanktonRecorder (CPR, Sir Alister Hardy Foundation for Ocean Science),coincided with a growth in global plastic production (Thompsonet al., 2004). Archived plastic samples from the west NorthAtlantic Ocean over the past 24 years have revealed a decrease inmean particle size from 10.66 mm in the 1990s to 5.05 mm in the2000s. Sixty nine per cent of fragments were 2e6 mm (Morét-Ferguson et al., 2010), highlighting a prevalence of small plasticparticles. Given the continual fragmentation of plastic items, par-ticle concentrations are likely to increase with decreasing size.

The entanglement in and ingestion of macroplastic items iswidely recognised in vertebrates. Over 250 marine species arebelieved to be impacted byplastic ingestion (Laist,1997). The demiseof higher organisms, typically vertebrates, is highly emotive andultimatelymore conspicuous to observers. As a result, such instancesare often subject to extensive scientific research andmedia coverage.Information regarding the biological impacts of microplastics onmarine organisms, however, has received less attention and is onlyjust emerging. A technical report considering the impacts of marinedebris on biodiversity revealed that over 80% of reported incidentsbetween organisms and marine debris was associated with plasticwhilst 11% of all reported encounters are with microplastics (GEF,2012). Since microplastics occupy the same size fraction as sedi-ments and some planktonic organisms, they are potentiallybioavailable to a wide range of organisms. Microplastics can beingested by low trophic suspension, filter and deposit feeders,detritivores and planktivores (Browne et al., 2008; Graham andThompson, 2009; Murray and Cowie, 2011; Thompson et al.,2004). Therefore, they may accumulate within organisms, result-ing in physical harm, such as by internal abrasions and blockages. Inaddition to the potential physical impacts of ingested microplastics,toxicity could also arise from leaching constituent contaminantssuch as monomers and plastic additives, capable of causing carci-nogenesis and endocrine disruption (see Oehlmann et al., 2009;Talsness et al., 2009). Furthermore, microplastics are liable toconcentrate hydrophobic persistent organic pollutants (POPs),

which have a greater affinity for the hydrophobic surface of plasticcompared to seawater.Due to their large surfacearea tovolume ratio,microplastics can becomeheavily contaminatede up to sixorders ofmagnitude greater than ambient seawater ewith waterborne POPs(Hirai et al., 2011;Mato et al., 2001). This presents a possible route ofexposure to marine organisms, whereby bioaccumulation and bio-magnification could occur through the food chain. The transfer ofPOPs tomarine organisms viamicroplastic vectors is not consideredin detail in this review (for examples see Teuten et al., 2009); how-ever the pathways and uptake of microplastic particles are clearly ofrelevance to chemical transfer, as well as physical harm.

Given the growing evidence outlined above, this review e

focussing on marine invertebrates e aims to: (1) summarise thefactors contributing to the bioavailability of microplastics; (2)outline the susceptibility of different feeding guilds to microplasticingestion; (3) determine the factors likely to influence the physicalimpacts of microplastics; and (4) discuss microplastic transferthrough the food chain.

2. Factors affecting the bioavailability of microplastics

2.1. Size

A key factor contributing to the bioavailability of microplastics istheir small size, making them available to lower trophic organisms.Many of these organisms exert limited selectivity between particlesand capture anything of appropriate size (Moore, 2008). Alterna-tively, higher trophic planktivores could passively ingest micro-plastics during normal feeding behaviour or mistake particles fornatural prey. Work by Fossi et al. (2012) investigated the impacts ofmicroplastics on the Mediterranean fin whale Balaenoptera phys-alus, one of the largest filter feeders in the world. B. physalus canengulf approximately 70 000 L of water at one time, potentiallyrisking microplastic ingestion both directly and indirectly from thewater and plankton, respectively. Using phthalate contamination asa proxy for microplastic ingestion, the authors concluded thatB. physalus could be consuming microplastics (Fossi et al., 2012).

2.2. Density

The density of the plastic particles will determine bioavail-ability in the water column; hence the type of plastic ingested

S.L. Wright et al. / Environmental Pollution 178 (2013) 483e492 485

may vary between organisms. Planktivores, filter feeders andsuspension feeders inhabiting the upper water column are likelyto encounter positively buoyant, low-density plastics, such as PE(specific gravity 0.91e0.94), on the sea surface (see Fig. 1). Thebuoyancy of plastic is influenced by biofouling, for example, PEfood bags (20 � 28 cm) displayed a well-developed biofilmwithin one week, which continued to increase throughout athree week exposure period. By the third week, the PE food bagshad started to sink below the sea surface, indicating neutralbuoyancy (Lobelle and Cunliffe, 2011). The rate of biofoulingdepends on parameters such as surface energy and hardness ofthe polymer, as well as water conditions (Muthukumar et al.,2011). De-fouling in the water column by foraging organismsis a potential pathway for microplastic particles to return to theseaeair interface (Andrady, 2011). This cyclic pattern may makemicroplastics available to organisms occupying different depthsof the water column at different times (see Fig. 1). Alternatively,fouled microplastics could continue to sink, as would high-density plastics such as PVC (specific gravity 1.38). Such parti-cles will become available to benthic suspension and depositfeeders and detritivores as they sink, eventually reaching thebenthos (see Fig. 1).

2.3. Abundance

An increase in the abundance of microplastics in the marineenvironment will also affect its bioavailability, as the chance anorganism will encounter a microplastic particle is enhanced.Therefore the progressive fragmentation of macroplastic items islikely to increase the amount of particles available for ingestion to awider range of organisms (Browne et al., 2007, 2008; Thompsonet al., 2009).

Fra

UV

mic

Sedimentation of

high density

polymers

Sinking due to

biofouling

f

Secondary

microplastics

Trophic

transfer

Colonisation by rafting

communities

Fig. 1. Potential pathways for the transport of m

2.4. Colour

The colour of microplastics may potentially contribute to thelikelihood of ingestion, due to prey item resemblance. Shaw andDay (1994) reported that plastic particles sampled from the NorthPacific exhibited size variation related to colour; white plasticparticles consistently decreased in abundance with decreasing sizeclass. Some commercially important fish and their larvae are visualpredators, preying on small zooplankton, and may feed on micro-plastics which most resemble their prey i.e. white, tan and yellowplastic (Shaw and Day, 1994). To further support the influence ofcolour on bioavailability, fish from the Niantic Bay area, New En-gland had ingested only opaque, white polystyrene spherules.These were present in equal proportion with clear polystyrenespherules, indicating selectivity (Carpenter et al., 1972). Micro-plastic ingestion due to food resemblance may also be applicable topelagic invertebrates, which are visual raptorial predators (Greene,1985).

3. Biological interactions

Microplastic bioavailability could be enhanced by biologicalfactors. The ingestion of polystyrene (PS) beads (100 nm) bysuspension-feeding bivalve molluscs significantly increased whenthey were incorporated into manually-generated aggregates,formed by rolling natural seawater in the laboratory. The seasonalflocculation of natural particulates into sinking aggregates is animportant pathway for energy transfer between pelagic andbenthic habitats (Ward and Kach, 2009). Consequently, the poten-tial for microplastics to become incorporated into marine aggre-gates may present a further mode of entry into the food chain. Onceingested, microplastics could sequentially be egested within fecal

gmentation due to

, mechanical and

robial degradation

Bioturbation

Sedimentation

via marine snow

De-

ouling

Primary

microplastics

Effects

due to

ingestion

Ingestion by

zooplankton and

fish

Resuspension in

faeces and

pseudofaeces

icroplastics and its biological interactions.

S.L. Wright et al. / Environmental Pollution 178 (2013) 483e492486

matter. Suspension feeders and detritivores may ingest suchegested microplastics (see Fig. 1). Sediment-dwelling organisms,such as the lugworm Arenicola marina, are capable of bioturbation(cycling the upper layers of sediment). Microplastic particles whichhave settled on the benthos could be drawn into the sediment,where they would be available to infauna (see Fig. 1).

3.1. The susceptibility of marine organisms to microplastic ingestion

The potential for microplastics to cause harm in marine organ-isms is initially likely to be governed by the susceptibility of speciesto ingest and/or interact with them. Selectivity is evident in particleingestion of natural substances in a range of species and it istherefore likely that such selectivity will extend to microplastics.Various laboratory studies have reported the ingestion of micro-plastics by invertebrates from a range of feeding guilds.

3.1.1. Detritivores and deposit feedersSince microplastics occur in sedimentary habitats, deposit- and

detritus- feeding organisms are susceptible to exposure. Thompsonet al. (2004) reported microplastic (20e2000 mm) ingestion in theomnivorous amphipod Orchestia gammarellus and the deposit-feeding polychaete A. marina. Amphipods may directly mistakemicroplastics as a natural food source and could therefore beregarded as primary consumers of microplastics (Murray andCowie, 2011). The marine polychaete A. marina is capable of size-based selectivity, whereby smaller particles stick to the mucus-lined proboscis papillae and are retained, whilst larger particlesare rejected (Zebe and Schiedek, 1996). Plastic particles within thissize range are therefore likely to be retained and ingested (seeTable 2). Morét-Ferguson et al. (2010) report a shift in the abun-dance of plastic debris to smaller size categories in the westernNorth Atlantic Ocean. If this finding is extrapolated to other regions,then it is likely more particles are gradually becoming available tothese organisms.

Microplastic ingestion has also been documented in thebenthic holothurians (sea cucumbers) Thyonella gemmate, Hol-othuria floridana, H. grisea and Cucumaria frondosa. Generallyscavengers, they feed on debris in the benthic zone of the oceanand adopt a non-selective feeding strategy whereby large volumesof sediment are ingested; the associated organic debris and mi-croorganisms of which is retained. Graham and Thompson (2009)found individuals belonging to four species of two orders ingestedsignificantly more plastic (0.25 mme15 mm) than expected e

between 2- and 20- fold more PVC fragments and between 2- and138- fold more nylon line fragments (up to 517 fibres per indi-vidual) e based on plastic to sand grain ratios from each sedimenttreatment. This suggests individuals were selectively ingestingplastic particles, which may be attributed to the feeding

Table 2Marine organisms susceptible to microplastic ingestion and their encounter pathways.

Species Encounter pathway

Marine algae e.g. Scenedesmus Adsorbs nanoplastics, espGrazing microzooplankton e.g. the

marine ciliate Strombidium sulcatumSize-based selectivity indi

Benthic deposit feeders e.g. the polychaeteArenicola marina and the holothurianHolothuria floridana

The sea bed is a sink for hadopted by A. marina indiselectively ingests plastic

Benthic scavengers e.g. the crustaceanNephrops norvegicus

Fibrous microplastics havehas shown plastic microfifood it scavenges or sedim

Mesozooplankton e.g. echinoderm larvae,calanoid copepods, chaetognaths

Low density microplasticsindustrial harbours; size-b

Benthic suspension feeders e.g. the bivalveMytilus edulis

Susceptible to sinking mic

techniques adopted by each order. Species’ exhibited either activeforaging in the upper millimetres of the sediment (aspidochir-otids), frequently encountering plastic particles, or less activeforaging involving brushing tentacles over the surface of thesediment (dendrochirotids), thus, only exposed and/or protrudingparticles were obtained. Both tentacle types could contact theplastic particles with limited shovelling and sand ingestion due tothe large surface area of the plastic. Benthic holothurians dis-played both random (the animals had to forage to encounterplastic particles) and selective (once encountered, plastic wasseparated from the sediment) feeding methods. This contradictstheir indiscriminate feeding strategy; something which couldpotentially occur in all non-selective feeders when presented withmicroplastics. Size affected ingestion, as <0.5 mm PVC shavingswere ingested 37 more times than the predicted quantitycompared to <17 times more for other size categories. Moreover,ingestion was limited when individuals encountered PVC pellets(4.0 mm diameter), possibly due to a restriction imposed bymouth size or difficulty in grasping them with their tentacles.Whether there was an impact on the physiological condition ofthe organisms following plastic ingestion remains unknown.

The authors also analysed sediment samples from sites wherethe animals were collected, which were found to be contaminatedwith microplastics (105e214 plastic particles l�1), predominantlyin fibrous forms. This corresponds with recent studies, which havefound a prevalence of microplastic fibres in coastal sediments(Browne et al., 2011; Claessens et al., 2011). Since Graham andThompson (2009) found benthic holothurians mostly ingestedplastic fibres, it is likely that microplastic ingestion is occurring inthe natural environment (see Table 2).

The non-selective benthic scavenger and predatory crustaceanNephrops norvegicus has also been shown to ingest small plasticfragments. Gut content analysis found that 83 per cent of animalscollected from the Clyde Sea contained plastic, the majority ofwhich took the form of tangled nylon-strand balls. This coincideswith the dominance of plastic fibres contaminating sediments aspreviously mentioned. Additionally, laboratory-based feeding ex-periments using ‘seeded’ fish revealed 100 per cent of individualsingested and retained 5 mm nylon rope fragments (Murray andCowie, 2011). These findings highlight the passive nature of plas-tic ingestion inN. norvegicus; whilst consuming sediment, or via thefood it scavenges, suggesting a trophic link (Murray and Cowie,2011; see Table 2).

3.1.2. Planktivores, filter-feeders and suspension-feedersDue to the similarity between the specific gravity of plastic

microspheres and algae, plastic microspheres have the potential tobe prey analogues for planktivores and may be handled andingested in a similar manner (Brillant and MacDonald, 2000). The

ecially when positively charged.cates potential to ingest microplastics of appropriate size.

igh-density microplastics; size-based, deposit- feeding strategiescate potential to ingest microplastics of appropriate size; H. Floridanaparticles, showing a preference for fibrous shapes.been found to accumulate in marine sediments; gut content analysis

bers are being ingested in the environment; ingestion is passive viaent.present on the sea surface with greatest abundances in gyres andased selectivity indicates potential to ingest microplastics of appropriate size.roplastics; have been found to ingest microplastics despite low qualitative value.

S.L. Wright et al. / Environmental Pollution 178 (2013) 483e492 487

common use of plastic microspheres in laboratory-based feedingexperiments emphasises the likelihood for microplastic ingestion.

Marine ciliates are capable of engulfing microplastics. Usingplastic microspheres in laboratory experiments, Christaki et al.(1998) investigated ciliate ingestion as a function of particle sizeand surface characteristics. They found size played a key role, asclearance rates for plastic microspheres (0.75 mm) were indistin-guishable from those for fluorescently labelled cells, indicating anabsence of chemosensory-mediated selection. Thus, if ciliatesencounter plastic particles of appropriate size in the marine envi-ronment, they present a potential pathway for plastic transferwithin the food chain (see Table 2).

In a laboratory study investigating particle capture and sus-pension feeding methods, sea urchin, sea star, sand dollar, brittlestar and sea cucumber larvae captured and ingested 10e20 mm PSdivinylbenzene (dvb) microspheres. In echinoderm larvae, filterfeeding is largely governed by the presence of a ciliated band whichencircles the mouth. Particles are extracted from suspension by ashort reversal in the direction of the cilia beat across the band. Ciliathen transfer the accumulated particles to the mouth for ingestion(Hart, 1991). Particle capture and ingestion seems to be based onsize selectivity, thus, if echinoderm larvae encounter microplasticsof an appropriate size in the environment, they are likely to becaptured and ingested (see Table 2). Whether the microsphereswere subsequently egested or accumulated in the gut was notdetermined.

As well as echinoderm larvae, laboratory work on the larvae ofthe marine polychaete worm Galeolaria caespitose showed inges-tion of 3 mm and 10 mm neutral-density polymer microspheres. Thelarvae ingested substantially more of the smaller 3 mm micro-spheres, emphasising the importance of size in microplasticingestion (Bolton and Havenhand, 1998). Furthermore, this high-lights the idea that the continuous fragmentation of plastic intosmaller particles will increase its availability.

Wilson (1973) found the filter-feeding calanoid copepod Acartiatonsa ingested microplastics during food size selection experi-ments. Particle capture is achieved by creating currents which passthrough a ‘basket’ formed fromvarious appendages, or by sweepingnet-like appendages through the water column (Wilson, 1973).A. tonsa selectively ingested plastic beads ranging from 13.9 to59 mm. Selectivity was based on the size frequency distribution ofavailable particles, choosing the largest abundant beads inconjunction with a passive filtering process. Wilson (1973)hypothesised that selectivity was attained through either discrim-inating between which particles were grasped or particles whichwere detected on feeding appendages yet disregarded. This reaf-firms the capacity for zooplankton to ingest microplastics.

Marine zooplankton, particularly members of the herbivorousconstituent, have proven to ingest microplastics in laboratorystudies. The prevalence of low-density microplastics on the seasurface suggests euphotic zooplankton, including commerciallyimportant larvae, are susceptible to microplastic ingestion.

Benthic suspension feeders may additionally be susceptible tosinking microplastic particles; numerous bivalve mollusc speciesingest microplastics (see Table 2). The suspension-feeding commonmussel Mytilus edulis has been shown to capture and ingestmicroplastic particles ranging from2 to 16 mm in size (Browne et al.,2008; Ward and Kach, 2009; Ward and Targett, 1989; Ward et al.,2003). In suspension-feeding bivalves, particle capture, retentionand sorting occur prior to ingestion. In order to capture particles acurrent is created by the lateral cilia on the ctenidial filaments,which flows into the inhalant siphon. Particles encounter thefrontal surfaces of filaments located on the ctenidium and becometrapped in a fine mucus layer; cirral-trapping is fundamental toparticle retention (Ward and Shumway, 2004). Most bivalves

capture and retain 3e4 mm particles with 100 per cent efficiencyand are capable of withholding particles as small as 1 mm diameterwith a reduced efficiency of approximately 50 per cent (Gosling,2003). Since microplastics >1.6 mm in size occur in coastal envi-ronments (Ng and Obbard, 2006), it is plausible that microplasticsof optimum size for bivalve capture and retention exist and areconsequently ingested.

As bivalves exert limited control on the types of particlescaptured, they can capture particles of low-nutritive value. How-ever, bivalves have the capacity to sort particles prior to ingestion,discriminating between similar-sized particles based on quality;unfavourable particles are subsequently rejected as pseudofaeces(Gosling, 2003; Ward and Shumway, 2004). Pre-ingestive sortingspecifically concerning microplastics has so far not been described.

Histological sampling and fluorescence microscopy haverevealed the presence of 2 mm and 4e16 mm microspheres in thegut cavity and digestive tubules of M. edulis (Browne et al., 2008).This suggests thatM. edulis exerts selectivity based on size, shape ordensity irrespective of particle quality as denoted by surfacechemistry during pre-ingestive particle sorting. Due to theirinherent feeding strategy, the apparent inability to sort and rejectmicroplastics prior to ingestion may be applicable to allsuspension-feeding bivalve molluscs.

The above studies used concentrations ranging from 1000 to20 000 particles ml�1 (Bolton and Havenhand, 1998; Ward andKach, 2009; Ward and Targett, 1989; Wilson, 1973). One of thehighest microplastics concentration reported from the marineenvironment is 0.102 particles ml�1 in Swedish coastal watersadjacent to a PE production plant (Norén, 2008). Clearly, laboratoryconcentrations exceed reported environmental levels by severalorders of magnitude, however the results do provide evidence thatif encountered, microplastics may be captured and ingested bymarine invertebrates.

Microplastics may not only enter the food chain via ingestion, asthey have demonstrated a capacity to adsorb to organisms. At thebase of the food web, the freshwater and freshwater/marine algalcells Chlorella and Scenedesmus respectively adsorbed chargednanoplastics (20 nm). A preference for positively charged particleswas reported, probably due to the electrostatic attraction betweenthe beads and cellulose constituent of the living cells. Nanoplasticsorption was further dependent on algal morphology and motility,with the flagellate Scenedesmus displaying a greater binding affinityto particles (Bhattacharya et al., 2010; see Table 2).

4. Factors influencing the physical impacts of microplastics

There is a wealth of literature regarding macroplastic ingestionin vertebrates (e.g. Denuncio et al., 2011; Laist, 1997; Lazar andGracan, 2011; van Franeker et al., 2011; Yamashita et al., 2011),reporting global impacts including: internal and/or external abra-sions and ulcers; and blockages of the digestive tract, which canresult in satiation, starvation and physical deterioration. In turn thiscan lead to reduced reproductive fitness, drowning, diminishedpredator avoidance, impairment of feeding ability, the potentialtransfer of damaging toxicants from seawater and ultimately death(Gregory, 2009). Such detrimental effects are also likely to apply tosmaller organisms including invertebrates, which ingest micro-plastics. For example, potentially fatal injuries such as blockagesthroughout the digestive system or abrasions from sharp objects.Other feasible impacts have been suggested by the Marine StrategyFramework Directive Task Group 10 (Galgani et al., 2010) andinclude: blockage of enzyme production; diminished feedingstimulus; nutrient dilution; reduced growth rates; lowered steroidhormone levels; delayed ovulation and reproductive failure; andabsorption of toxins. There is potential for microplastics to clog and

S.L. Wright et al. / Environmental Pollution 178 (2013) 483e492488

block the feeding appendages of marine invertebrates or even tobecome embedded in tissues (Derraik, 2002): plastic fragments andPP and/or monofilament line have been found in the tissues of twofilter feeding salps - Thetys vagina e collected from neuston sam-ples in the NPCG (Moore et al., 2001). Some of the factors likely toinfluence the physical and chemical impact of microplastics andtheir transfer through the food chain are discussed below.

4.1. Accumulation

The capacity formicroplastics to accumulatewithin an organismis likely to affect the associated physical impact of microplasticingestion. So far, there is limited literature regarding the accumu-lation of microplastics in marine invertebrates. A plankton tow insouth New England coastal waters collected a 20 mm long chae-tognath, Sagitta elegans, which had a 0.6 mm diameter spherule inits intestine (Carpenter et al., 1972). It was not confirmed whetherthis was plastic, however the spherule was described as beingidentical to PS spherules also collected in the tow. Nevertheless thishighlights the ability for similar particles to accumulate in marineinvertebrates.

In laboratory studies microplastics have been shown to accu-mulate in the digestive cavity and tubules of bivalve molluscs(Brillant andMacDonald, 2000; Browne et al., 2008).Within 30minof ingestion, 20 mm PS microspherules were observed in the pri-mary ducts and tubules of the sea scallop Placopecten magellanicus’digestive gland where they persisted for up to 48 h. The micro-spherules were absent from the epithelial cells of the gut, implyingthey were not phagocytised. Despite being taken up by the diges-tive tubules, the microspherules were of a similar size to theepithelial cells and therefore may have been too large to permitphagocytosis (Brillant and MacDonald, 2000). In M. edulis, mid guthistological sections revealed 2 mm fluorescently-labelled and 4e16 mm non-labelled PS microspheres accumulating in the digestivecavity and tubules following a 12 h exposure (Browne et al., 2008).

Accumulation of microplastic particles in marine invertebratescould potentially cause blockages throughout the digestive system,suppressing feeding due to satiation. Alternatively, predation ofmicroplastic-contaminated marine invertebrates may present apathway for plastic transfer along the food chain.

Besides internal accumulation, the external adsorption ofmicroplastics may also cause harm. Bhattacharya et al. (2010) foundthe binding of plastic beads (20 nm) to the algal species Chlorellaand Scenedesmus inhibited photosynthesis, potentially due to thephysical blockage of light and air. Moreover, it increased reactiveoxygen species production, indicating a state of oxidative stress(Bhattacharya et al., 2010). Despite using extremely high concen-trations e 1.4e40 mg ml�1 e relative to environmental levels, thisstudy highlights the potential for microscopic plastic particles toadhere to algal cells, possibly impacting on photosynthesis. As algaeplay a key role in aquatic food webs, the productivity and resilienceof ecosystems could be compromised if high concentrations occurdue to the adverse effects of plastic particles.

4.2. Translocation

Andrady (2011) states that due to a lack of enzymatic pathwaysavailable to break down plastics in filter-feeding organisms,microplastics are unlikely to be digested or absorbed and cantherefore be considered bio-inert. However, they may pass throughcell membranes and become incorporated into body tissuesfollowing ingestion. Fluorescence and confocal microscopyrevealed 3 mm and 9.6 mm fluorescent PS microspheres in thehaemolymph and haemocytes of the suspension feeder M. edulis,three days after short (three hour) pulse exposures to 15 000

particles 350 ml-1 (Browne et al., 2008). This implied the micro-spheres had translocated across the gut epithelial lining into thecircularity system; however, the precise mechanism(s) for uptakeacross the epithelial lining remains unknown, as does the precisetranslocation time (Browne et al., 2008). In rats and humans,enterocytes are responsible for the transportation of particlesacross the epithelium by phagocytosis into the circularity fluid.

The smaller microspheres (3 mm) typically had the greatestabundance (>60 per cent) in both haemolymph and haemocytes. Asimilar pattern has been shown in rats whereby 14 nm latex par-ticles were in contact with colonic enterocytes within 2 min ofintroduction compared to 30 min for 415 nm particles (Hussainet al., 2001). This implies the rapid translocation of smaller parti-cles is applicable to both invertebrates and vertebrates. If phago-cytosis is the primarymechanism for translocation of microplastics,it is conceivable that a greater abundance of small-sized particlesare phagocytised due to the limited capacity of the phagosomewithin each cell (Browne et al., 2008). As plastic continues tofragment, the potential for it to accumulate within the circulatoryfluid and phagocytic cells of an organism is likely to increase, as thesmaller the microplastics, the greater the abundance available fortranslocation.

Despite the presence of microplastic particles in M. edulis’ hae-molymph and haemocytes, no toxicological effects were observed(Browne et al., 2008). Conversely, indications of granulocytomaformation (inflammation), an increase in haemocytes and a sig-nificant decrease in lysosome stability were observed in M. edulisafter 48 h, following plastic particle (1e80 mm) uptake into thevacuoles of the digestive gland (GESAMP, 2010). Consequently, theenergy allocated to immune function in such scenarios maycompromise normal physiological processes. Over time, this couldhave a detrimental effect on the health of the organism, at both theindividual and population level.

Once translocated from the gut to the circulatory system,microplastics can be retained for several weeks. PS microspherespersisted in M. edulis haemolymph and haemocytes for as long as48 days (Browne et al., 2008). Such tenacity could be applicableacross species and thusmicroplastics may be transported to varioustissues and organs via the haemolymph, potentially accumulatingand causing harm. In turn, this could facilitate the transfer ofmicroplastics to higher trophic organisms.

Presently, more research is required to determine the upper andlower size limits for translocation to occur in organisms. Addi-tionally, the behaviour and fate of micro-particles of differentpolymer types and shapes also needs to be established. In thenatural environment, organisms may be exposed to microplasticsthroughout their lifetime as opposed to short experimental dura-tions. Thus the continual ingestion and accumulation of such par-ticles may incur chronic effects. Moreover, many different polymersoccur in the environment, whichmay elicit a different response to asingle polymer.

4.3. Shape

The potential adverse effects associated with the presence ofmicroplastics are likely to vary with particle shape. Carbon nano-tubules have exhibited lung damage; Warheit et al. (2004) foundthe lung tissue of rats exposed to single-wall carbon nanotubulesdisplayed inflammation and cell injury. In mesoporous silicananoparticles (MSNs), shape can influence the efficiency and abilityof drug delivery irrespective of chemical composition, surfacecharge and diameter; rod-shaped MSNs showed increased cellularuptake and therefore a greater effect on apoptosis, migration anddisruption of cytoskeleton organisation. Long rod-shaped nano-particles severely reduced cell viability and apoptosis compared to

S.L. Wright et al. / Environmental Pollution 178 (2013) 483e492 489

sphere and short rod-shaped nanoparticles. An explanation forsuch shape-related toxicity is that the long rod-shaped MSNs areeasily up-taken by cells due to the greater contact area and po-tential for interaction (Huang et al., 2010). Given that marinemicroplastics occur in a variety of shapes from fibres to irregularfragments to spheres and rods, there is potential for the physicaladverse effects of polymers to alter depending on form. Along theBelgian coast, plastic fibres formed the majority (59%) of micro-plastic debris sampled (Claessens et al., 2011), with average con-centrations of 81.0 � 37.2, 65.6 � 15.3 and 66.3 � 28.6 fibres kg�1

for beach, harbour and sea sampling stations respectively. Con-centrations of plastic fibres (<1 mm) ranging from 2 (Australia) to31 (Portugal) fibres 250 ml�1 contaminated 18 shores across sixcontinents, with concentration positively correlating with popula-tion density (Browne et al., 2011). Thus, benthic and sediment-dwelling organisms inhabiting such areas are vulnerable to theshape-related toxicity of plastic fibres, if ingested.

4.4. Egestion

There is very little information available regarding the capacityfor marine organisms to egest microplastics. Through fecal castanalysis, Thompson et al. (2004) found some microplastic particleswere defecated by the lugworm A. marina. To assess the ingestion ofmicroplastic fragments and pellets in benthic holothurians, faecaldebris was collected from individuals held in the laboratory. Thequantity of defecated microplastic particles was then enumerated(Graham and Thompson, 2009). Through egestion, it is possiblethat an organismwill prevent any detrimental effects caused by theingestion of plastic particles.

The estuarine copepod Eurytemora affinis demonstrated anability to regurgitate latex beads (mean diameter 15 mm). Labora-tory feeding trials were conducted with 3e90 beads ml�1 concen-trations; beads were ingested at mean rates of up to 59 000particles per copepod per hour. The capability for plastic micro-spherule ingestion was demonstrated, as was the potential foraccumulation inside the gut cavity of E. affinis. However, followingthe initial microspherule ingestion, the particles were subsequentlyregurgitated between 1 and 3 h later. This was indicated by adecrease then sequential increase of latex microspherules in thefeeding suspension coinciding with an absence of latex micro-spherules in the fecal pellets of E. affinis. Alternatively, bacterial-coated latex microspherules (15 mm) were retained and succes-sively egested in fecal pellets (Powell and Berry, 1990), highlightingan ability to reject un-nutritious particles.

Egestion rates are likely to affect the capacity for potentiallyadhered contaminants to desorb in addition to the likelihood oftransfer to the food chain. Predation could still occur within thetimeframe. The diurnal vertical migration of zooplankton couldfurther transport microplastics to predators occupying variousdepths of the water column.

4.5. Population-level effects

Aside from physical and chemical impacts, microplastics alsohave a potential role in providing a new hard-substrate habitat forrafting communities, which was previously limited to items such asfloating wood, pumice, and sea shells. In 2001, Moore et al. foundmonofilament line 10 cm below the sea surface to be colonisedwithdiatoms and other microalgae. Recently, microplastics have beenidentified as an important oviposition resource for the pelagic in-sect Halobates sericeus, indicated by a positive correlation betweenH. sericeus eggs on microplastics and microplastic abundance. Thepelagic invertebrate community represents a crucial link betweenprimary producers and nektonic species. Thus, changes in the

population structure of H. sericeus may lead to ecosystem wideconsequences (Goldstein et al., 2012).

The increasing abundance of microplastics may be capable ofmodifying community-wide assemblages. Additionally, micro-plastics present a mechanism for long distance transport of raftingspecies, enhancing biogeographic connectivity. The most commonrafting species are from the phyla Cnidaria, Crustacea and Ecto-procta (Thiel and Gutow, 2005). These species may be consideredthe most vulnerable to population-level microplastic-associatedchanges.

4.6. Transfer to the food chain

At present, there are few studies on the bioaccumulation ofplastics and their associated POPs across marine trophic levels.Given that lower trophic organisms, specifically invertebrates, caningest and accumulate microplastic particles, it is likely thatmicroplastics will be introduced to the food web. Laboratorymicroplastic ingestion studies have mostly focussed on in-vertebrates, however, in situ work has discovered microplasticingestion in several vertebrate species.

Lusher et al. (2012) found microplastics in 36.5% of fishbelonging to 10 species sampled from the English Channel, irre-spective of habitat (pelagic vs. demersal). An average of 1.9 � 0.1particles were recovered from those which contained plastic, themain polymers being polyamide and polyester, which are mate-rials commonly used in the fishing industry (Lusher et al., 2012).Whilst the biological consequences remain unclear, such findingsare comparable to those from the North Pacific Central Gyre re-ported by Boerger et al. (2010); small plastic fragments werefound in approximately one third of all fish caught. Individualsfrom the most common species caught (Myctophum auro-lanternatum, Myctophidae) contained an average of six plasticpieces and the most frequently ingested size class across all spe-cies was 1e2.79 mm. The majority of fish caught in this studybelonged to the Myctophidae, a low-trophic, mesopelagic familywhich adopts diurnal feeding behaviour, preying upon planktonnear the surface at night. As the most commonly ingested plasticcolours (white, clear and blue out of 12 reported colours) weresimilar to that of plankton species inhabiting the North PacificCentral Gyre, the Myctophidae may mistake small plastic frag-ments for their natural food source (Boerger et al., 2010). Alter-natively, the myctophids could consume plankton which haspreviously ingested microplastics or ingest plastic passively. Sincethe most commonly occurring plastic colours in tow samplesmatched those ingested, it is likely the Myctophidae are notshowing selectivity but ingesting particles in a more passivemanner. The toxicological effects of plastic ingestion in mycto-phids remains to be determined, however if they are unable toegest small plastic fragments, the plastic may accumulate andcompromise normal feeding activity. Additionally, the Myctophi-dae are preyed upon by tuna, squid, odontoceti whales, seabirdsand fur seals (Boerger et al., 2010). Thus there are several routes ofentry to various compartments of the marine food web.

Higher trophic level organisms have been found to ingestmicroplastics transported by prey items. Microplastic particlesapproximately 1 mm in diameter were recorded in the scat of furseals and Hooker’s sea lions (Goldsworthy et al., 1997; McMahonet al., 1999). The presence of plastic coincided with otoliths of themyctophid fish Electrona subaspera, suggesting a trophic link.Eriksson and Burton (2003) further investigated the transfer ofplastic particles in Antarctic fur seals. Scats of Arctocephalus tropi-calis and A. gazellawere collected fromMacquarie Island, Australia,during the periods 1990e1991 and 1996e1997. Out of 145 sealscats, 164 small plastic particles (generally ranging from 2 to 5 mm)

Table 3Areas for future research.

� The destination of ingested microplastics within marine invertebrates inaddition to potential adverse effects remains unknown, emphasising a needfor laboratory studies focussing on the physical impacts of microplastics

� Given the occurrence of different shapes and plastic types in the marineenvironment, research into the impacts of these factors on marine organismsshould be conducted

� The bioavailability of constituent contaminants is undetermined. This high-lights a requirement for further laboratory studies to establish the effects ofageing on the concentration of microplastic additives, their bioavailabilityand the associated toxicological impacts

� The role of microplastics as a vector for environmental POPs is uncertain.Laboratory studies investigating the bioavailability and associated toxico-logical impacts of microplastic-associated POPs are required

� There are presently no conclusive reports on the transfer of microplastics tohigher trophic levels and whether they act as a vector for contaminants.Studies are needed to understand the capacity for microplastics and theirassociated contaminants to be transported along marine food webs via tro-phic interactions as well as an estimation of population and ecosystem levelimpacts.

S.L. Wright et al. / Environmental Pollution 178 (2013) 483e492490

were recovered. However, the sieves used to separate the plasticfrom the scat had a mesh size >0.5 mm, suggesting that any plasticparticles <0.5 mmwere not retained. Thus the quantities obtainedare likely to be an underestimation. Interestingly, during 1990e1991, one plastic particle per scat was recorded, whilst during1996e1997 up to four particles per scat (1%) were documented;possibly a result of the increasing abundance of plastic debris in themarine environment. PE (93%) was the primary polymer groupidentified from the samples, followed by PP (4%), which closelymatched polymer types identified in beach flotsam from the samelocation. Nearly all fragments were irregular in form and approxi-mately one third had one sharp edge, indicating there is potentialfor internal abrasion. Eriksson and Burton (2003) believed therewas little possibility that the seal species’ were directly ingestingplastic particles; a plastic-concentrating vector, such as fish, is amore likely explanation.

Several fish species caught in New England coastal waterscontained plastic microspherules identical to those collected dur-ing plankton tows in the same area (0.1e2 mm); winter flounder(Pseudopleuronectes americanus) and grubby (Myoxocephalusaenaeus) larvae, approximately 5 mm in length, contained 0.5 mmdiameter plastic microspherules (Carpenter et al., 1972). Byextrapolating this data and that from Goldsworthy et al. (1997),Eriksson and Burton (2003) estimated that minimum concentra-tion factors of plastic particles to seals ranges from 22 to 160 times.The narrow range of particle parameters (size and shape) observed,suggests that selectivity is being practiced. E. subaspera, a majorcomponent of the fur seal diet, is likely to consume copepods 1e9 mm in size near the surface waters. This size range has a 95 percent overlap with the plastic particles found in scats, indicating thetransfer of microplastics across trophic levels is plausible.

Microplastics have the potential to be ingested by baleenwhale species through indirect consumption via planktonic prey.Mono-(2-ethylhexyl) phthalate (MEHP) contamination of theblubber of the Mediterranean fin whale B. physalus has recentlybeen suggested as an indication that microplastic ingestion oc-curs, either from the water column or via a planktonic vector.Fifty six percent of neustonic and planktonic samples from theMediterranean Sea contained microplastics e up to 9.67 particlesm3. This coincided with high levels of phthalates in the watercolumn, specifically di-2-ethylhexyl phthalate (DEHP) and MEHP,comparative to the levels found in the blubber samples. The useof phthalates and plastics additives such as antimicrobials, dyesor stabilisers as tracers for microplastic ingestion and bio-accumulation is certainly a promising avenue for future research(Fossi et al., 2012).

At present, there is limited information regarding the impacts ofmicroplastics on food webs and no associated laboratory experi-ments have been conducted. Therefore, it remains undeterminedwhether plastic of any size can be transferred to higher trophiclevels. There are well documented examples of trophic transfer formany POPswithinmarine foodwebs, for example dioxins, PCBs andpolybrominated diphenylethers, many of which have been re-ported to associate with oceanic plastics (Ogata et al., 2009) andsome of which can biomagnify (Hu et al., 2005). Generally, theextent of trophic transfer is dependent on characteristics includingthe octanolewater partition coefficient (Kow) and metabolictransformation rate of the compound under consideration (Wanet al., 2005). The effect of co-ingestion of microplastics on thetrophodynamic behaviour of POPs and plastics additives remainsan important topic for further study. Other important factors toconsider for the transfer of microplastics and their associated POPsare organism-dependent gut retention times, as well as the fractionof consumed microplastics that are capable of moving across thegut epithelium and into other tissues or organs.

5. Conclusions

Low density microplastic debris is accumulating in ocean gyresand pelagic invertebrates inhabiting these regions may be sus-ceptible to microplastic ingestion. In addition, the benthos is likelyto be a sink for high density microplastics. Some organisms mayhave the capacity to egest microplastics, possibly leading to theirincorporation into marine aggregates. Benthic suspension- anddeposit- feeders are therefore likely to ingest sinking and sedi-mentary microplastics. Fibres are the most commonly encoun-tered form of microplastics in the marine environment. Benthicholothurians were found to selectively ingest microplastics,showing a preference for fibrous shapes. Additionally, benthicscavengers are susceptible to fibrous microplastic exposure, as gutcontent analysis revealed nylon fibres in N. norvegicus. This im-plies their habitat is a sink for fibres. Since shape may play a role inthe toxicity of ingested microplastics e long, rod-shaped nano-particles are considered more toxic than spherules e these or-ganisms can be considered sensitive to the potential physicaltoxicity of microplastics.

The presence of microplastics in myctophid fish and Hooker’ssea lion and fur seal scats suggest microplastic transfer throughpelagic food chains: microplasticsezooplanktonemyctophid fish-Hooker’s sea lions/fur seals. Such lower trophic organisms there-fore represent a vector formicroplastic transfer and their associatedcontaminants.

Microplastics may not only affect species at the organism-level;they also have the capacity to modify population structure. Specieswhich were once restricted by a lack of hard substrate, such as themarine insect H. Sericeus, are now able to proliferate. This may beapplicable to a wide range of organisms with potential impacts onecosystem dynamics.

The accumulation of microplastic debris has presented a newmarine habitat where biological interactions are taking place. Thishabitat and its environmental impacts are still emerging areas ofresearch. It is hoped that future work on this growing issue (seeTable 3) will contribute to the development of better methods forcontrolling marine litter.

References

Andrady, A.L., 2011. Microplastics in the marine environment. Marine PollutionBulletin 62 (8), 1596e1605.

Bhattacharya, P., Lin, S., Turner, J.P., Ke, P.C., 2010. Physical adsorption of chargedplastic nanoparticles affects algal photosynthesis. The Journal of PhysicalChemistry C 114, 16556e16561.

S.L. Wright et al. / Environmental Pollution 178 (2013) 483e492 491

Boerger, C.M., Lattin, G.L., Moore, S.L., Moore, C.J., 2010. Plastic ingestion byplanktivorous fishes in the North Pacific Central Gyre. Marine Pollution Bulletin60, 2275e2278.

Bolton, T.F., Havenhand, J.N., 1998. Physiological versus viscosity-induced effects ofan acute reduction in water temperature on microsphere ingestion by trocho-phore larvae of the serpulid polychaete Galeolaria caespitosa. Journal ofPlankton Research 20 (11), 2153e2164.

Brillant, M.G.S., MacDonald, B.A., 2000. Postingestive selection in the sea scallop,Placopecten magellanicus (Gmelin): the role of particle size and density. Journalof Experimental Marine Biology and Ecology 253 (2), 211e227.

Browne, M.A., Galloway, T.S., Thompson, R.C., 2007. Microplasticdan emergingcontaminant of potential concern? Integrated Environmental Assessment andManagement 3 (4), 559e561.

Browne, M.A., Dissanayake, A., Galloway, T.S., Lowe, D.M., Thompson, R.C., 2008.Ingested microscopic plastic translocates to the circulatory system of themussel, Mytilus edulis (L.). Environmental Science and Technology 42 (13),5026e5031.

Browne, M.A., Crump, P., Nivens, S.J., Teuten, E., Tonkin, A., Galloway, T.,Thompson, R., 2011. Accumulation of microplastics on shorelines worldwide:sources and sinks. Environmental Science and Technology 45 (21), 9175e9179.

Carpenter, E.J., Anderson, S.J., Harvey, G.R., Miklas, H.P., Peck, B.B., 1972. Polystyrenespherules in coastal waters. Science 178 (4062), 749e750.

Christaki, U., Dolan, J.R., Pelegri, S., Rassoulzadegan, F., 1998. Consumption ofpicoplankton-size particles by marine ciliates: effects of physiological state ofthe ciliate and particle quality. Limnology and Oceanography 43, 458e464.

Claessens, M., De Meester, S., Van Landuyt, L., De Clerck, K., Janssen, C.R., 2011.Occurrence and distribution of microplastics in marine sediments along theBelgian coast. Marine Pollution Bulletin 62 (10), 2199e2204.

Collignon, A., Hecq, J.H., Galgani, F., Voisin, P., Collard, F., Goffart, A., 2012. Neustonicmicroplastic and zooplankton in the North Western Mediterranean Sea. MarinePollution Bulletin 64 (4), 861e864.

Colton, J.B., Knapp, F.D., Burns, B.R., 1974. Plastic particles in surface waters of theNorthwestern Atlantic. Science 185 (4150), 491e497.

Denuncio, P., Bastida, R., Dassis, M., Giardino, G., Gerpe, M., Rodriguez, D., 2011.Plastic ingestion in Franciscana dolphins, Pontoporia blainvillei (Gervais andd’Orbigny, 1844), from Argentina. Marine Pollution Bulletin 62 (8), 1836e1841.

Derraik, J.G.B., 2002. The pollution of the marine environment by plastic debris: areview. Marine Pollution Bulletin 44 (9), 842e852.

Doyle, M.J., Watson, W., Bowlin, N.M., Sheavly, S.B., 2011. Plastic particles in coastalpelagic ecosystems of the Northeast Pacific ocean. Marine EnvironmentalResearch 71, 41e52.

Eriksson, C., Burton, H., 2003. Origins and biological accumulation of small plasticparticles in fur seals from Macquarie Island. AMBIO: A Journal of the HumanEnvironment 32 (6), 380e384.

Fossi, M.C., Panti, C., Gurranti, C., Coppola, D., Giannetti, M., Marsili, L., Minutoli, R.,2012. Are baleen whales exposed to the threat of microplastics? A case study ofthe Mediterranean fin whale (Balaenoptera physalus). Marine Pollution Bulletin64 (11), 2374e2379.

Galgani, F., Fleet, D., Van Franeker, J., Katsanevakis, S., Maes, T., Mouat, J.,Oosterbaan, L., Poitou, I., Hanke, G., Thompson, R., Amato, E., Birkun, A.,Janssen, C., 2010. In: Zampoukas, N. (Ed.), Marine Strategy Framework Directive,Task Group 10 Report, Marine Litter. EUR 24340 EN e 2010.

GEF, 2012. Secretariat of the Convention on Biological Diversity and Scientific andTechnical Advisory Panel GEF, Impacts of Marine Debris on Biodiversity: Cur-rent Status and Potential Solutuions, vol. 67. p. 9. Montreal.

GESAMP (2010, IMO/FAO/UNESCO-IOC/UNIDO/WMO/IAEA/UN/UNEP Joint Group ofExperts on the Scientific Aspects of Marine Environmental Protection). Bowmer,T., Kershaw, P.J., (Eds.), 2010. Proceedings of the GESAMP International Work-shop on Plastic Particles as a Vector in Transporting Persistent, Bio-accumulating and Toxic Substances in the Oceans. GESAMP Rep. Stud. No. 82,68 pp.

Goldstein, M.C., Rosenberg, M., Cheng, L., 2012. Increased oceanic microplasticdebris enhances oviposition in an endemic pelagic insect. Biology Letters 8 (5),817e820.

Goldsworthy, S.D., Hindell, M.A., Crowley, H.M., 1997. Diet and diving behaviour ofsympatric fur seals Arctocephalus gazella and A. tropicalis at Macquarie Island.In: Hindell, M., Kemper, C. (Eds.), Marine Mammal Research in the SouthernHemisphere. Status, Ecology and Medicine, vol. 1. Surrey Beatty & Sons, NewSouth Wales, Australia, pp. 151e163.

Gosling, E., 2003. Bivalve Molluscs: Biology, Ecology and Culture, first ed. Wiley-Blackwell.

Graham, E.R., Thompson, J.T., 2009. Deposit- and suspension-feeding sea cucumbers(Echinodermata) ingest plastic fragments. Journal of Experimental MarineBiology and Ecology 368 (1), 22e29.

Greene, C.H., 1985. Planktivore functional groups and patterns of prey selection inpelagic communities. Journal of Plankton Research 7 (1), 35e40.

Gregory, M.R., 2009. Environmental implications of plastic debris in marine settingse entanglement, ingestion, smothering, hangers-on, hitch-hiking and alieninvasions. Philosophical Transactions of the Royal Society of London B: Bio-logical Sciences 364 (1526), 2013e2025.

Hart, M.W., 1991. Particle capture and the method of suspension feeding by echi-noderm larvae. Biology Bulletin 180 (1), 12e27.

Hirai, H., Takada, H., Ogata, Y., Yamashita, R., Mizukawa, K., Saha, M., Kwan, C.,Moore, C., Gray, H., Laursen, D., Zettler, E.R., Farrington, J.W., Reddy, C.M.,Peacock, E.E., Ward, M.W., 2011. Organic micropollutants in marine plastics

debris from the open ocean and remote and urban beaches. Marine PollutionBulletin 62 (8), 1683e1692.

Hu, J., Jin, F., Wan, Y., Yang, M., An, L., An, W., Tao, S., 2005. Trophodynamicbehaviour of 4-nonylphenol and nonylphenol polyethoxylate in a marine foodweb from Bohai Bay, North China: comparison to DDTs. Environmental Scienceand Technology 39 (13), 4801e4807.

Huang, X., Teng, X., Chen, D., Tang, F., He, J., 2010. The effect of the shape of mes-oporous silica nanoparticles on cellular uptake and cell function. Biomaterials31 (3), 438e448.

Hussain, N., Jaitley, V., Florence, A.T., 2001. Recent advances in the understanding ofuptake of microparticulates across the gastrointestinal lymphatics. AdvancedDrug Delivery Reviews 50 (1e2), 107e142.

Ivar do Sul, J.A., Spengler, A., Costa, M.F., 2009. Here, there and everywhere. Smallplastic fragments and pellets on beaches of Fernando de Noronha (EquatorialWestern Atlantic). Marine Pollution Bulletin 58 (8), 1236e1238.

Laist, D.W., 1997. Impacts of marine debris: entanglement of marine life in marinedebris including a comprehensive list of species with entanglement andingestion records. In: Coe, J.M., Rogers, D.B. (Eds.), Marine Debrisesources,Impacts and Solutions. Springer-Verlag New York Inc., New York, pp. 99e139.

Lattin, G.L., Moore, C.J., Zellers, A.F., Moore, S.L., Weisberg, S.B., 2004. A comparisonof neustonic plastic and zooplankton at different depths near the southernCalifornia shore. Marine Pollution Bulletin 49 (4), 291e294.

Lazar, B., Gracan, R., 2011. Ingestion of marine debris by loggerhead sea turtles,Caretta caretta, in the Adriatic sea. Marine Pollution Bulletin 62 (1), 43e47.

Liebezeit, G., Dubaish, F., 2012. Microplastics in beaches of the Frisian IslandsSpiekeroog and Kachelotplate. Bulletin of Environmental Contamination andToxicology 89 (1), 213e217.

Lobelle, D., Cunliffe, M., 2011. Early microbial biofilm formation on marine plasticdebris. Marine Pollution Bulletin 62 (1), 197e200.

Lusher, A.L., McHugh, M., Thompson, R.C., 2012. Occurrence of microplastics in thegastrointestinal tract of pelagic and demersal fish from the English Channel.Marine Pollution Bulletin 67 (1e2), 94e99.

Martins, J., Sobral, P., 2011. Plastic marine debris on the Portuguese coastline: amatter of size? Marine Pollution Bulletin 62 (12), 2649e2653.

Mato, Y., Isobe, T., Takada, H., Kanehiro, H., Ohtake, C., Kaminuma, T., 2001. Plasticresin pellets as a transport medium for toxic chemicals in the marine envi-ronment. Environmental Science and Technology 35 (2), 318e324.

McMahon, C.R., Hooley, D., Robinson, S., 1999. The diet of itinerant male Hooker’ssea lions, Phocarctos hookeri, at sub-Antarctic Macquarie Island. WildlifeResearch 26 (6), 839e846.

Moore, C.J., 2008. Synthetic polymers in the marine environment: a rapidlyincreasing, long-term threat. Environmental Research 108 (2), 131e139.

Moore, C.J., Moore, S.L., Leecaster, M.K., Weisberg, S.B., 2001. A comparison of plasticand plankton in the North Pacific Central Gyre. Marine Pollution Bulletin 42(12), 1297e1300.

Morét-Ferguson, S., Law, K.L., Proskurowski, G., Murphy, E.K., Peacock, E.E.,Reddy, C.M., 2010. The size, mass, and composition of plastic debris in thewestern North Atlantic Ocean. Marine Pollution Bulletin 60 (10), 1873e1878.

Murray, F., Cowie, P.R., 2011. Plastic contamination in the decapod crustaceanNephrops norvegicus (Linnaeus, 1758). Marine Pollution Bulletin 62 (6),1207e1217.

Muthukumar, T., Aravinthan, A., Lakshmi, K., Venkatesan, R., Vedaprakash, L.,Doble, M., 2011. Fouling and stability of polymers and composites in marineenvironment. International Biodeterioration and Biodegradation 65 (2),276e284.

Ng, K.L., Obbard, J.P., 2006. Prevalence of microplastics in Singapore’s coastal marineenvironment. Marine Pollution Bulletin 52 (7), 761e767.

Norén, F., 2008. Small Plastic Particles in Coastal Swedish Waters. N-Researchreport, commissioned by KIMO Sweden.

Noren, F., Naustvoll, F., 2010. Survey of Microscopic Anthropogenic Particles inSkagerrak. Commissioned by KLIMA- OG FORURENSNINGSDIREKTORATET,Norway.

Oehlmann, J.R., Schulte-Oehlmann, U., Kloas, W., Jagnytsch, O., Lutz, I., Kusk, K.O.,Wollenberger, L., Santos, E.M., Paull, G.C., Van Look, K.J.W., Tyler, C.R., 2009.A critical analysis of the biological impacts of plasticizers on wildlife. Philo-sophical Transactions of the Royal Society of London B: Biological Science 364(1526), 2047e2062.

Ogata, Y., Takada, H., Mizukawa, K., Hirai, H., Iwasa, S., et al., 2009. InternationalPellet Watch: global monitoring of persistent organic pollutants (POPs) incoastal waters. 1. Initial phase data on PCBs, DDTs, and HCHs. Marine PollutionBulletin 58, 1437e1446.

PlasticsEurope, 2012. Plastics e the Facts 2012: an Analysis of European PlasticsProduction, Demand and Waste Data for 2011 (10.10.2012). http://www.plasticseurope.org/Document/plastics-the-facts-2012.aspx?Page¼DOCUMENT&FolID¼2.

Powell, M.D., Berry, A.J., 1990. Ingestion and regurgitation of living and inert ma-terials by the estuarine copepod Eurytemora affinis (Poppe) and the influence ofsalinity. Estuarine, Coastal and Shelf Science 31 (6), 763e773.

Reddy, M., Adimurthy, S., Ramachandraiah, G., 2006. Description of the smallplastics fragments in marine sediments along the Alang-Sosiya ship-breakingyard, India. Estuarine, Coastal and Shelf Science 68 (3e4), 656e660.

Shaw, D.G., Day, R.H., 1994. Colour- and form- dependent loss of plastic micro-debris from the North Pacific Ocean. Marine Pollution Bulletin 28 (1), 39e43.

Talsness, C.E., Andrade, A.J.M., Kuriyama, S.N., Taylor, J.A., vom Saal, F.S., 2009.Components of plastic: experimental studies in animals and relevance for

S.L. Wright et al. / Environmental Pollution 178 (2013) 483e492492

human health. Philosophical Transactions of the Royal Society of London B:Biological Science 364 (1526), 2079e2096.

Teuten, E.L., Saquing, J.M., Knappe, D.R.U., Barlaz, M.A., Jonsson, S., Bjorn, A.,Rowland, S.J., Thompson, R.C., Galloway, T.S., Yamashita, R., Ochi, D.,Watanuki, Y., Moore, C., Viet, P.H., Tana, T.S., Prudente, M., Boonyatumanond, R.,Zakaria, M.P., Akkhavong, K., Ogata, Y., Hirai, H., Iwasa, S., Mizukawa, K.,Hagino, Y., Imamura, A., Saha, M., Takada, H., 2009. Transport and release ofchemicals from plastics to the environment and to wildlife. PhilosophicalTransactions of the Royal Society of London B: Biological Science 364 (1526),2027e2045.

Thiel, M., Gutow, L., 2005. The ecology of rafting in the marine environment.II. Therafting organisms and community. Oceanography and Marine Biology: anAnnual Review 43, 279e418.

Thompson, R.C., Moore, C.J., vom Saal, F.S., Swan, S.H., 2009. Plastics, the environ-ment and human health: current consensus and future trends. PhilosophicalTransactions of the Royal Society of London B: Biological Science 364 (1526),2153e2166.

Thompson, R.C., Olsen, Y., Mitchell, R.P., Davis, A., Rowland, S.J., John, A.W.G.,McGonigle, D., Russell, A.E., 2004. Lost at sea: where is all the plastic? Science304 (5672), 838.

Turner, A., Holmes, L., 2011. Occurrence, distribution and characteristics of beachedplastic production pellets on the island of Malta (central Mediterranean). Ma-rine Pollution Bulletin 62 (2), 377e381.

van Franeker, J.A., Blaize, C., Danielsen, J., Fairclough, K., Gollan, J., Guse, N.,Hansen, P.L., Heubeck, M., Jensen, J.K., Le Guillou, G., Olsen, B., Olsen, K.O.,Pedersen, J., Stienen, E.W., Turner, D.M., 2011. Monitoring plastic ingestion by

the northern fulmar Fulmarus glacialis in the North Sea. Environmental Pollu-tion 159 (10), 2609e2615.

Wan, Y., Hu, J., Yang, M., an, L., an, W., Jin, X., H, T., Itoh, M., 2005. Characterization oftrophic transfer for polychlorinated dibenzo p dioxins, dibenzofurans, non andmono ortho polychlorinated biphenyls in the marine food web of Bohai Bay,North China. Environmental Science and Technology 39 (8), 2417e2425.

Ward, J.E., Targett, N.M., 1989. Influence of marine microalgal metabolites on thefeeding behavior of the blue mussel Mytilus edulis. Marine Biology 101, 313e321.

Ward, J.E., Shumway, S.E., 2004. Separating the grain from the chaff: particle se-lection in suspension- and deposit-feeding bivalves. Journal of ExperimentalMarine Biology and Ecology 300 (1e2), 83e130.

Ward, J.E., Kach, D.J., 2009. Marine aggregates facilitate ingestion of nanoparticles bysuspension-feeding bivalves. Marine Environmental Research 68 (3), 137e142.

Ward, J.E., Levinton, J.S., Shumway, S.E., 2003. Influence of diet on pre-ingestiveparticle processing in bivalves: I: transport velocities on the ctenidium. Jour-nal of Experimental Marine Biology and Ecology 293 (2), 129e149.

Warheit, D.B., Laurence, B.R., Reed, K.L., Roach, D.H., Reynolds, G.A.M., Webb, T.R.,2004. Comparative pulmonary toxicity assessment of single-wall carbonnanotubes in rats. Toxicological Sciences 77 (1), 117e125.

Wilson, D.S., 1973. Food size selection among copepods. Ecology 54 (4), 909e914.Yamashita, R., Takada, H., Fukuwaka, M., Watanuki, Y., 2011. Physical and chemical

effects of ingested plastic debris on short-tailed shearwaters, Puffinus tenuir-ostris, in the North Pacific ocean. Marine Pollution Bulletin 62 (12), 2845e2849.

Zebe, E., Schiedek, D., 1996. The lugworm Arenicola marina: a model of physiologicaladaptation to life in the intertidal sediments. Helgoland Marine Research 50 (1),37e68.