You are on page 1of 10

Environmental Pollution 178 (2013) 483e492

Contents lists available at SciVerse ScienceDirect

Environmental Pollution
journal homepage: www.elsevier.com/locate/envpol

Review

The physical impacts of microplastics on marine organisms: A review


Stephanie L. Wright a, *, Richard C. Thompson b, Tamara S. Galloway a
a
Biosciences, College of Life and Environmental Sciences, Geoffrey Pope Building, University of Exeter, Stocker Road, Exeter, Devon EX4 4QD, United Kingdom
b
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 a b s t r a c t

Article history: Plastic debris at the micro-, and potentially also the nano-scale, are widespread in the environment.
Received 13 October 2012 Microplastics have accumulated in oceans and sediments worldwide in recent years, with maximum
Received in revised form concentrations reaching 100 000 particles m3. Due to their small size, microplastics may be ingested by
7 February 2013
low trophic fauna, with uncertain consequences for the health of the organism. This review focuses on
Accepted 13 February 2013
marine invertebrates and their susceptibility to the physical impacts of microplastic uptake. Some of the
main points discussed are (1) an evaluation of the factors contributing to the bioavailability of micro-
Keywords:
plastics including size and density; (2) an assessment of the relative susceptibility of different feeding
Microplastics
Plastic debris
guilds; (3) an overview of the factors most likely to influence the physical impacts of microplastics such
Marine litter as accumulation and translocation; and (4) the trophic transfer of microplastics. These findings are
Marine invertebrates important in guiding future marine litter research and management strategies.
Food web Ó 2013 Elsevier Ltd. All rights reserved.

1. Introduction et al., 1972), from low background levels to localized ‘hotspots’ (see
Table 1). Present on beaches, in surface waters, throughout the water
In contemporary society, plastic has achieved a pivotal status, column and within the benthos (Lattin et al., 2004; Moore et al.,
with extensive commercial, industrial, medicinal and municipal 2001; Thompson et al., 2004), microplastics have pervaded even
applications. Demand is considerable; annual plastic production has the most remote marine environments (e.g. Ivar do Sul et al., 2009).
increased dramatically from 1.5 million tonnes in the 1950s to Gyres are particular hotspots for microplastic accumulation.
approximately 280 million tonnes in 2011 (PlasticsEurope, 2012). Recently a maximum concentration and mass of 32.76 particles m3
Through accidental release and indiscriminate discards, plastic and 250 mg m3 respectively have been recorded in the North Pacific
waste has accumulated in the environment at an uncontrollable Subtropical Gyre (Goldstein et al., 2012). Industrial coastal areas
rate, where it is subjected to wind and river-driven transport, ulti- have also been identified as microplastic hotspots; concentrations
mately reaching the coast. Due to its lightweight, durable nature, of approximately 100 000 plastic particles m3 of seawater have
plastic has become a prevalent, widespread element of marine litter been reported in a Swedish harbour area adjacent to a PE produc-
(Moore, 2008; Thompson et al., 2009); the most commonly pro- tion plant (Noren and Naustvoll, 2010). Sediment from densely
duced and therefore encountered polymers being polypropylene populated coastal areas can be heavily contaminated with micro-
(PP), polyethylene (PE) and polyvinylchloride (PVC) composing 24%, plastics. Browne et al. (2011) found microplastics on eighteen
21% and 19% of global plastic production in 2007, respectively shores across six continents, with a tendency towards fibrous
(Andrady, 2011). Recently, inconspicuous microscopic plastic parti- shapes. Maximum concentrations of 124 fibres l1 were reported
cles, referred to here as ‘microplastics’, have been identified as a and a significant relationship between microplastic abundance and
ubiquitous component of marine debris. Defined as less than 5 mm human population-density was found (Browne et al., 2011). Thus as
in size by the National Oceanic and Atmospheric Administration the human population continues to increase, the prevalence of
(NOAA), microplastics can be of primary (purposefully manufac- microplastics will also most probably increase. Previous studies
tured to be of microscopic size) or secondary (derived from the have found a predominance of fibrous microplastics (see Claessens
fragmentation of macroplastic items) origin. They have been accu- et al., 2011; Thompson et al., 2004). Despite a variety of forms from
mulating in oceans worldwide over the last four decades (Carpenter irregular fragments to spherules, it seems likely that fibrous
microplastics are most abundant in the marine environment.
A temporal increase in the abundance of marine microplastics
* Corresponding author. has been indicated. Recently, combined data from peer-reviewed
E-mail address: sw393@exeter.ac.uk (S.L. Wright). literature, publicly available data and new data sets revealed

0269-7491/$ e see front matter Ó 2013 Elsevier Ltd. All rights reserved.
http://dx.doi.org/10.1016/j.envpol.2013.02.031
484 S.L. Wright et al. / Environmental Pollution 178 (2013) 483e492

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

Location Maximum observed Reference


concentration
Coastal waters, Sweden 102 000 particles m3 Noren and Naustvoll, 2010
Coastal Waters, California 3 particles m3 Doyle et al., 2011
Coastal waters, New England 3 particles m3 Carpenter et al., 1972
Open ocean, North West Atlantic 67 000 particles km2 Colton et al., 1974
Northwest Mediterranean Sea 1 particle m2 Collignon et al., 2012
Beach, Malta >1000 particles m2 Turner and Holmes, 2011
Beach, UK 8 particles kg1 Thompson et al., 2004
Estuarine sediment, UK 31 particles kg1 Thompson et al., 2004
Subtidal sediment, UK 86 particles kg1 Thompson et al., 2004
Subtidal sediment, Florida 214 particles l1 Graham and Thompson, 2009
Subtidal sediment, Maine 105 particles l1 Graham and Thompson, 2009
Harbour sediment, Sweden 50 particles l1 Norén, 2008
Industrial harbour sediment, Sweden 3320 particles l1 Norén, 2008
Industrial coast sediment, Sweden 340 l1 Norén, 2008
Ship-breaking yard sediment, India 89 mg kg1* Reddy et al., 2006
Harbour sediment, Belgium 7 mg kg1 Claessens et al., 2011
Continental shelf sediment, Belgium 1 mg kg1 Claessens et al., 2011
Beach, Belgium 1 mg kg1 Claessens et al., 2011
Beach, Portugal 6 particles m2 Martins and Sobral, 2011
Beach, East Frisian Islands, Germany 621 particles 10 g1 Liebezeit and Dubaish, 2012

* Including glass wool.

changes in the abundance and mass of microplastics in the North which have a greater affinity for the hydrophobic surface of plastic
Pacific Subtropical Gyre. Abundance and mass increased by two compared to seawater. Due to their large surface area to volume ratio,
orders of magnitude from a median of 0e0.116 particles m3 and 0e microplastics can become heavily contaminated e up to six orders of
0.086 mg m3, respectively from 1972e87 to 1999e2010. This is magnitude greater than ambient seawater e with waterborne POPs
believed to have been driven by a localised increase in microplastic (Hirai et al., 2011; Mato et al., 2001). This presents a possible route of
abundance (Goldstein et al., 2012). Additionally, North Atlantic and exposure to marine organisms, whereby bioaccumulation and bio-
North Sea surface samples collected by a Continuous Plankton magnification could occur through the food chain. The transfer of
Recorder (CPR, Sir Alister Hardy Foundation for Ocean Science), POPs to marine organisms via microplastic vectors is not considered
coincided with a growth in global plastic production (Thompson in detail in this review (for examples see Teuten et al., 2009); how-
et al., 2004). Archived plastic samples from the west North ever the pathways and uptake of microplastic particles are clearly of
Atlantic Ocean over the past 24 years have revealed a decrease in relevance to chemical transfer, as well as physical harm.
mean particle size from 10.66 mm in the 1990s to 5.05 mm in the Given the growing evidence outlined above, this review e
2000s. Sixty nine per cent of fragments were 2e6 mm (Morét- focussing on marine invertebrates e aims to: (1) summarise the
Ferguson et al., 2010), highlighting a prevalence of small plastic factors contributing to the bioavailability of microplastics; (2)
particles. Given the continual fragmentation of plastic items, par- outline the susceptibility of different feeding guilds to microplastic
ticle concentrations are likely to increase with decreasing size. ingestion; (3) determine the factors likely to influence the physical
The entanglement in and ingestion of macroplastic items is impacts of microplastics; and (4) discuss microplastic transfer
widely recognised in vertebrates. Over 250 marine species are through the food chain.
believed to be impacted by plastic ingestion (Laist, 1997). The demise
of higher organisms, typically vertebrates, is highly emotive and 2. Factors affecting the bioavailability of microplastics
ultimately more conspicuous to observers. As a result, such instances
are often subject to extensive scientific research and media coverage. 2.1. Size
Information regarding the biological impacts of microplastics on
marine organisms, however, has received less attention and is only A key factor contributing to the bioavailability of microplastics is
just emerging. A technical report considering the impacts of marine their small size, making them available to lower trophic organisms.
debris on biodiversity revealed that over 80% of reported incidents Many of these organisms exert limited selectivity between particles
between organisms and marine debris was associated with plastic and capture anything of appropriate size (Moore, 2008). Alterna-
whilst 11% of all reported encounters are with microplastics (GEF, tively, higher trophic planktivores could passively ingest micro-
2012). Since microplastics occupy the same size fraction as sedi- plastics during normal feeding behaviour or mistake particles for
ments and some planktonic organisms, they are potentially natural prey. Work by Fossi et al. (2012) investigated the impacts of
bioavailable to a wide range of organisms. Microplastics can be microplastics on the Mediterranean fin whale Balaenoptera phys-
ingested by low trophic suspension, filter and deposit feeders, alus, one of the largest filter feeders in the world. B. physalus can
detritivores and planktivores (Browne et al., 2008; Graham and engulf approximately 70 000 L of water at one time, potentially
Thompson, 2009; Murray and Cowie, 2011; Thompson et al., risking microplastic ingestion both directly and indirectly from the
2004). Therefore, they may accumulate within organisms, result- water and plankton, respectively. Using phthalate contamination as
ing in physical harm, such as by internal abrasions and blockages. In a proxy for microplastic ingestion, the authors concluded that
addition to the potential physical impacts of ingested microplastics, B. physalus could be consuming microplastics (Fossi et al., 2012).
toxicity could also arise from leaching constituent contaminants
such as monomers and plastic additives, capable of causing carci- 2.2. Density
nogenesis and endocrine disruption (see Oehlmann et al., 2009;
Talsness et al., 2009). Furthermore, microplastics are liable to The density of the plastic particles will determine bioavail-
concentrate hydrophobic persistent organic pollutants (POPs), 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 and 2.4. Colour
suspension feeders inhabiting the upper water column are likely
to encounter positively buoyant, low-density plastics, such as PE The colour of microplastics may potentially contribute to the
(specific gravity 0.91e0.94), on the sea surface (see Fig. 1). The likelihood of ingestion, due to prey item resemblance. Shaw and
buoyancy of plastic is influenced by biofouling, for example, PE Day (1994) reported that plastic particles sampled from the North
food bags (20  28 cm) displayed a well-developed biofilm Pacific exhibited size variation related to colour; white plastic
within one week, which continued to increase throughout a particles consistently decreased in abundance with decreasing size
three week exposure period. By the third week, the PE food bags class. Some commercially important fish and their larvae are visual
had started to sink below the sea surface, indicating neutral predators, preying on small zooplankton, and may feed on micro-
buoyancy (Lobelle and Cunliffe, 2011). The rate of biofouling plastics which most resemble their prey i.e. white, tan and yellow
depends on parameters such as surface energy and hardness of plastic (Shaw and Day, 1994). To further support the influence of
the polymer, as well as water conditions (Muthukumar et al., colour on bioavailability, fish from the Niantic Bay area, New En-
2011). De-fouling in the water column by foraging organisms gland had ingested only opaque, white polystyrene spherules.
is a potential pathway for microplastic particles to return to the These were present in equal proportion with clear polystyrene
seaeair interface (Andrady, 2011). This cyclic pattern may make spherules, indicating selectivity (Carpenter et al., 1972). Micro-
microplastics available to organisms occupying different depths plastic ingestion due to food resemblance may also be applicable to
of the water column at different times (see Fig. 1). Alternatively, pelagic invertebrates, which are visual raptorial predators (Greene,
fouled microplastics could continue to sink, as would high- 1985).
density plastics such as PVC (specific gravity 1.38). Such parti-
cles will become available to benthic suspension and deposit 3. Biological interactions
feeders and detritivores as they sink, eventually reaching the
benthos (see Fig. 1). Microplastic bioavailability could be enhanced by biological
factors. The ingestion of polystyrene (PS) beads (100 nm) by
2.3. Abundance suspension-feeding bivalve molluscs significantly increased when
they were incorporated into manually-generated aggregates,
An increase in the abundance of microplastics in the marine formed by rolling natural seawater in the laboratory. The seasonal
environment will also affect its bioavailability, as the chance an flocculation of natural particulates into sinking aggregates is an
organism will encounter a microplastic particle is enhanced. important pathway for energy transfer between pelagic and
Therefore the progressive fragmentation of macroplastic items is benthic habitats (Ward and Kach, 2009). Consequently, the poten-
likely to increase the amount of particles available for ingestion to a tial for microplastics to become incorporated into marine aggre-
wider range of organisms (Browne et al., 2007, 2008; Thompson gates may present a further mode of entry into the food chain. Once
et al., 2009). ingested, microplastics could sequentially be egested within fecal

Fragmentation due to
UV, mechanical and
microbial degradation Primary
Secondary microplastics
microplastics

Ingestion by
zooplankton and Effects
Colonisation by rafting fish due to
communities ingestion
De-
fouling

Sinking due to
Sedimentation of biofouling
high density
Sedimentation
polymers
via marine snow
Resuspension in
faeces and
Trophic pseudofaeces
transfer

Bioturbation

Fig. 1. Potential pathways for the transport of microplastics and its biological interactions.
486 S.L. Wright et al. / Environmental Pollution 178 (2013) 483e492

matter. Suspension feeders and detritivores may ingest such techniques adopted by each order. Species’ exhibited either active
egested microplastics (see Fig. 1). Sediment-dwelling organisms, foraging in the upper millimetres of the sediment (aspidochir-
such as the lugworm Arenicola marina, are capable of bioturbation otids), frequently encountering plastic particles, or less active
(cycling the upper layers of sediment). Microplastic particles which foraging involving brushing tentacles over the surface of the
have settled on the benthos could be drawn into the sediment, sediment (dendrochirotids), thus, only exposed and/or protruding
where they would be available to infauna (see Fig. 1). particles were obtained. Both tentacle types could contact the
plastic particles with limited shovelling and sand ingestion due to
3.1. The susceptibility of marine organisms to microplastic ingestion the large surface area of the plastic. Benthic holothurians dis-
played both random (the animals had to forage to encounter
The potential for microplastics to cause harm in marine organ- plastic particles) and selective (once encountered, plastic was
isms is initially likely to be governed by the susceptibility of species separated from the sediment) feeding methods. This contradicts
to ingest and/or interact with them. Selectivity is evident in particle their indiscriminate feeding strategy; something which could
ingestion of natural substances in a range of species and it is potentially occur in all non-selective feeders when presented with
therefore likely that such selectivity will extend to microplastics. microplastics. Size affected ingestion, as <0.5 mm PVC shavings
Various laboratory studies have reported the ingestion of micro- were ingested 37 more times than the predicted quantity
plastics by invertebrates from a range of feeding guilds. compared to <17 times more for other size categories. Moreover,
ingestion was limited when individuals encountered PVC pellets
3.1.1. Detritivores and deposit feeders (4.0 mm diameter), possibly due to a restriction imposed by
Since microplastics occur in sedimentary habitats, deposit- and mouth size or difficulty in grasping them with their tentacles.
detritus- feeding organisms are susceptible to exposure. Thompson Whether there was an impact on the physiological condition of
et al. (2004) reported microplastic (20e2000 mm) ingestion in the the organisms following plastic ingestion remains unknown.
omnivorous amphipod Orchestia gammarellus and the deposit- The authors also analysed sediment samples from sites where
feeding polychaete A. marina. Amphipods may directly mistake the animals were collected, which were found to be contaminated
microplastics as a natural food source and could therefore be with microplastics (105e214 plastic particles l1), predominantly
regarded as primary consumers of microplastics (Murray and in fibrous forms. This corresponds with recent studies, which have
Cowie, 2011). The marine polychaete A. marina is capable of size- found a prevalence of microplastic fibres in coastal sediments
based selectivity, whereby smaller particles stick to the mucus- (Browne et al., 2011; Claessens et al., 2011). Since Graham and
lined proboscis papillae and are retained, whilst larger particles Thompson (2009) found benthic holothurians mostly ingested
are rejected (Zebe and Schiedek, 1996). Plastic particles within this plastic fibres, it is likely that microplastic ingestion is occurring in
size range are therefore likely to be retained and ingested (see the natural environment (see Table 2).
Table 2). Morét-Ferguson et al. (2010) report a shift in the abun- The non-selective benthic scavenger and predatory crustacean
dance of plastic debris to smaller size categories in the western Nephrops norvegicus has also been shown to ingest small plastic
North Atlantic Ocean. If this finding is extrapolated to other regions, fragments. Gut content analysis found that 83 per cent of animals
then it is likely more particles are gradually becoming available to collected from the Clyde Sea contained plastic, the majority of
these organisms. which took the form of tangled nylon-strand balls. This coincides
Microplastic ingestion has also been documented in the with the dominance of plastic fibres contaminating sediments as
benthic holothurians (sea cucumbers) Thyonella gemmate, Hol- previously mentioned. Additionally, laboratory-based feeding ex-
othuria floridana, H. grisea and Cucumaria frondosa. Generally periments using ‘seeded’ fish revealed 100 per cent of individuals
scavengers, they feed on debris in the benthic zone of the ocean ingested and retained 5 mm nylon rope fragments (Murray and
and adopt a non-selective feeding strategy whereby large volumes Cowie, 2011). These findings highlight the passive nature of plas-
of sediment are ingested; the associated organic debris and mi- tic ingestion in N. norvegicus; whilst consuming sediment, or via the
croorganisms of which is retained. Graham and Thompson (2009) food it scavenges, suggesting a trophic link (Murray and Cowie,
found individuals belonging to four species of two orders ingested 2011; see Table 2).
significantly more plastic (0.25 mme15 mm) than expected e
between 2- and 20- fold more PVC fragments and between 2- and 3.1.2. Planktivores, filter-feeders and suspension-feeders
138- fold more nylon line fragments (up to 517 fibres per indi- Due to the similarity between the specific gravity of plastic
vidual) e based on plastic to sand grain ratios from each sediment microspheres and algae, plastic microspheres have the potential to
treatment. This suggests individuals were selectively ingesting be prey analogues for planktivores and may be handled and
plastic particles, which may be attributed to the feeding ingested in a similar manner (Brillant and MacDonald, 2000). The

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

Species Encounter pathway


Marine algae e.g. Scenedesmus Adsorbs nanoplastics, especially when positively charged.
Grazing microzooplankton e.g. the Size-based selectivity indicates potential to ingest microplastics of appropriate size.
marine ciliate Strombidium sulcatum
Benthic deposit feeders e.g. the polychaete The sea bed is a sink for high-density microplastics; size-based, deposit- feeding strategies
Arenicola marina and the holothurian adopted by A. marina indicate potential to ingest microplastics of appropriate size; H. Floridana
Holothuria floridana selectively ingests plastic particles, showing a preference for fibrous shapes.
Benthic scavengers e.g. the crustacean Fibrous microplastics have been found to accumulate in marine sediments; gut content analysis
Nephrops norvegicus has shown plastic microfibers are being ingested in the environment; ingestion is passive via
food it scavenges or sediment.
Mesozooplankton e.g. echinoderm larvae, Low density microplastics present on the sea surface with greatest abundances in gyres and
calanoid copepods, chaetognaths industrial harbours; size-based selectivity indicates potential to ingest microplastics of appropriate size.
Benthic suspension feeders e.g. the bivalve Susceptible to sinking microplastics; have been found to ingest microplastics despite low qualitative value.
Mytilus edulis
S.L. Wright et al. / Environmental Pollution 178 (2013) 483e492 487

common use of plastic microspheres in laboratory-based feeding capture and retain 3e4 mm particles with 100 per cent efficiency
experiments emphasises the likelihood for microplastic ingestion. and are capable of withholding particles as small as 1 mm diameter
Marine ciliates are capable of engulfing microplastics. Using with a reduced efficiency of approximately 50 per cent (Gosling,
plastic microspheres in laboratory experiments, Christaki et al. 2003). Since microplastics >1.6 mm in size occur in coastal envi-
(1998) investigated ciliate ingestion as a function of particle size ronments (Ng and Obbard, 2006), it is plausible that microplastics
and surface characteristics. They found size played a key role, as of optimum size for bivalve capture and retention exist and are
clearance rates for plastic microspheres (0.75 mm) were indistin- consequently ingested.
guishable from those for fluorescently labelled cells, indicating an As bivalves exert limited control on the types of particles
absence of chemosensory-mediated selection. Thus, if ciliates captured, they can capture particles of low-nutritive value. How-
encounter plastic particles of appropriate size in the marine envi- ever, bivalves have the capacity to sort particles prior to ingestion,
ronment, they present a potential pathway for plastic transfer discriminating between similar-sized particles based on quality;
within the food chain (see Table 2). unfavourable particles are subsequently rejected as pseudofaeces
In a laboratory study investigating particle capture and sus- (Gosling, 2003; Ward and Shumway, 2004). Pre-ingestive sorting
pension feeding methods, sea urchin, sea star, sand dollar, brittle specifically concerning microplastics has so far not been described.
star and sea cucumber larvae captured and ingested 10e20 mm PS Histological sampling and fluorescence microscopy have
divinylbenzene (dvb) microspheres. In echinoderm larvae, filter revealed the presence of 2 mm and 4e16 mm microspheres in the
feeding is largely governed by the presence of a ciliated band which gut cavity and digestive tubules of M. edulis (Browne et al., 2008).
encircles the mouth. Particles are extracted from suspension by a This suggests that M. edulis exerts selectivity based on size, shape or
short reversal in the direction of the cilia beat across the band. Cilia density irrespective of particle quality as denoted by surface
then transfer the accumulated particles to the mouth for ingestion chemistry during pre-ingestive particle sorting. Due to their
(Hart, 1991). Particle capture and ingestion seems to be based on inherent feeding strategy, the apparent inability to sort and reject
size selectivity, thus, if echinoderm larvae encounter microplastics microplastics prior to ingestion may be applicable to all
of an appropriate size in the environment, they are likely to be suspension-feeding bivalve molluscs.
captured and ingested (see Table 2). Whether the microspheres The above studies used concentrations ranging from 1000 to
were subsequently egested or accumulated in the gut was not 20 000 particles ml1 (Bolton and Havenhand, 1998; Ward and
determined. Kach, 2009; Ward and Targett, 1989; Wilson, 1973). One of the
As well as echinoderm larvae, laboratory work on the larvae of highest microplastics concentration reported from the marine
the marine polychaete worm Galeolaria caespitose showed inges- environment is 0.102 particles ml1 in Swedish coastal waters
tion of 3 mm and 10 mm neutral-density polymer microspheres. The adjacent to a PE production plant (Norén, 2008). Clearly, laboratory
larvae ingested substantially more of the smaller 3 mm micro- concentrations exceed reported environmental levels by several
spheres, emphasising the importance of size in microplastic orders of magnitude, however the results do provide evidence that
ingestion (Bolton and Havenhand, 1998). Furthermore, this high- if encountered, microplastics may be captured and ingested by
lights the idea that the continuous fragmentation of plastic into marine invertebrates.
smaller particles will increase its availability. Microplastics may not only enter the food chain via ingestion, as
Wilson (1973) found the filter-feeding calanoid copepod Acartia they have demonstrated a capacity to adsorb to organisms. At the
tonsa ingested microplastics during food size selection experi- base of the food web, the freshwater and freshwater/marine algal
ments. Particle capture is achieved by creating currents which pass cells Chlorella and Scenedesmus respectively adsorbed charged
through a ‘basket’ formed from various appendages, or by sweeping nanoplastics (20 nm). A preference for positively charged particles
net-like appendages through the water column (Wilson, 1973). was reported, probably due to the electrostatic attraction between
A. tonsa selectively ingested plastic beads ranging from 13.9 to the beads and cellulose constituent of the living cells. Nanoplastic
59 mm. Selectivity was based on the size frequency distribution of sorption was further dependent on algal morphology and motility,
available particles, choosing the largest abundant beads in with the flagellate Scenedesmus displaying a greater binding affinity
conjunction with a passive filtering process. Wilson (1973) to particles (Bhattacharya et al., 2010; see Table 2).
hypothesised that selectivity was attained through either discrim-
inating between which particles were grasped or particles which 4. Factors influencing the physical impacts of microplastics
were detected on feeding appendages yet disregarded. This reaf-
firms the capacity for zooplankton to ingest microplastics. There is a wealth of literature regarding macroplastic ingestion
Marine zooplankton, particularly members of the herbivorous in vertebrates (e.g. Denuncio et al., 2011; Laist, 1997; Lazar and
constituent, have proven to ingest microplastics in laboratory Gracan, 2011; van Franeker et al., 2011; Yamashita et al., 2011),
studies. The prevalence of low-density microplastics on the sea reporting global impacts including: internal and/or external abra-
surface suggests euphotic zooplankton, including commercially sions and ulcers; and blockages of the digestive tract, which can
important larvae, are susceptible to microplastic ingestion. result in satiation, starvation and physical deterioration. In turn this
Benthic suspension feeders may additionally be susceptible to can lead to reduced reproductive fitness, drowning, diminished
sinking microplastic particles; numerous bivalve mollusc species predator avoidance, impairment of feeding ability, the potential
ingest microplastics (see Table 2). The suspension-feeding common transfer of damaging toxicants from seawater and ultimately death
mussel Mytilus edulis has been shown to capture and ingest (Gregory, 2009). Such detrimental effects are also likely to apply to
microplastic particles ranging from 2 to 16 mm in size (Browne et al., smaller organisms including invertebrates, which ingest micro-
2008; Ward and Kach, 2009; Ward and Targett, 1989; Ward et al., plastics. For example, potentially fatal injuries such as blockages
2003). In suspension-feeding bivalves, particle capture, retention throughout the digestive system or abrasions from sharp objects.
and sorting occur prior to ingestion. In order to capture particles a Other feasible impacts have been suggested by the Marine Strategy
current is created by the lateral cilia on the ctenidial filaments, Framework Directive Task Group 10 (Galgani et al., 2010) and
which flows into the inhalant siphon. Particles encounter the include: blockage of enzyme production; diminished feeding
frontal surfaces of filaments located on the ctenidium and become stimulus; nutrient dilution; reduced growth rates; lowered steroid
trapped in a fine mucus layer; cirral-trapping is fundamental to hormone levels; delayed ovulation and reproductive failure; and
particle retention (Ward and Shumway, 2004). Most bivalves absorption of toxins. There is potential for microplastics to clog and
488 S.L. Wright et al. / Environmental Pollution 178 (2013) 483e492

block the feeding appendages of marine invertebrates or even to particles 350 ml-1 (Browne et al., 2008). This implied the micro-
become embedded in tissues (Derraik, 2002): plastic fragments and spheres had translocated across the gut epithelial lining into the
PP and/or monofilament line have been found in the tissues of two circularity system; however, the precise mechanism(s) for uptake
filter feeding salps - Thetys vagina e collected from neuston sam- across the epithelial lining remains unknown, as does the precise
ples in the NPCG (Moore et al., 2001). Some of the factors likely to translocation time (Browne et al., 2008). In rats and humans,
influence the physical and chemical impact of microplastics and enterocytes are responsible for the transportation of particles
their transfer through the food chain are discussed below. across the epithelium by phagocytosis into the circularity fluid.
The smaller microspheres (3 mm) typically had the greatest
4.1. Accumulation abundance (>60 per cent) in both haemolymph and haemocytes. A
similar pattern has been shown in rats whereby 14 nm latex par-
The capacity for microplastics to accumulate within an organism ticles were in contact with colonic enterocytes within 2 min of
is likely to affect the associated physical impact of microplastic introduction compared to 30 min for 415 nm particles (Hussain
ingestion. So far, there is limited literature regarding the accumu- et al., 2001). This implies the rapid translocation of smaller parti-
lation of microplastics in marine invertebrates. A plankton tow in cles is applicable to both invertebrates and vertebrates. If phago-
south New England coastal waters collected a 20 mm long chae- cytosis is the primary mechanism for translocation of microplastics,
tognath, Sagitta elegans, which had a 0.6 mm diameter spherule in it is conceivable that a greater abundance of small-sized particles
its intestine (Carpenter et al., 1972). It was not confirmed whether are phagocytised due to the limited capacity of the phagosome
this was plastic, however the spherule was described as being within each cell (Browne et al., 2008). As plastic continues to
identical to PS spherules also collected in the tow. Nevertheless this fragment, the potential for it to accumulate within the circulatory
highlights the ability for similar particles to accumulate in marine fluid and phagocytic cells of an organism is likely to increase, as the
invertebrates. smaller the microplastics, the greater the abundance available for
In laboratory studies microplastics have been shown to accu- translocation.
mulate in the digestive cavity and tubules of bivalve molluscs Despite the presence of microplastic particles in M. edulis’ hae-
(Brillant and MacDonald, 2000; Browne et al., 2008). Within 30 min molymph and haemocytes, no toxicological effects were observed
of ingestion, 20 mm PS microspherules were observed in the pri- (Browne et al., 2008). Conversely, indications of granulocytoma
mary ducts and tubules of the sea scallop Placopecten magellanicus’ formation (inflammation), an increase in haemocytes and a sig-
digestive gland where they persisted for up to 48 h. The micro- nificant decrease in lysosome stability were observed in M. edulis
spherules were absent from the epithelial cells of the gut, implying after 48 h, following plastic particle (1e80 mm) uptake into the
they were not phagocytised. Despite being taken up by the diges- vacuoles of the digestive gland (GESAMP, 2010). Consequently, the
tive tubules, the microspherules were of a similar size to the energy allocated to immune function in such scenarios may
epithelial cells and therefore may have been too large to permit compromise normal physiological processes. Over time, this could
phagocytosis (Brillant and MacDonald, 2000). In M. edulis, mid gut have a detrimental effect on the health of the organism, at both the
histological sections revealed 2 mm fluorescently-labelled and 4e individual and population level.
16 mm non-labelled PS microspheres accumulating in the digestive Once translocated from the gut to the circulatory system,
cavity and tubules following a 12 h exposure (Browne et al., 2008). microplastics can be retained for several weeks. PS microspheres
Accumulation of microplastic particles in marine invertebrates persisted in M. edulis haemolymph and haemocytes for as long as
could potentially cause blockages throughout the digestive system, 48 days (Browne et al., 2008). Such tenacity could be applicable
suppressing feeding due to satiation. Alternatively, predation of across species and thus microplastics may be transported to various
microplastic-contaminated marine invertebrates may present a tissues and organs via the haemolymph, potentially accumulating
pathway for plastic transfer along the food chain. and causing harm. In turn, this could facilitate the transfer of
Besides internal accumulation, the external adsorption of microplastics to higher trophic organisms.
microplastics may also cause harm. Bhattacharya et al. (2010) found Presently, more research is required to determine the upper and
the binding of plastic beads (20 nm) to the algal species Chlorella lower size limits for translocation to occur in organisms. Addi-
and Scenedesmus inhibited photosynthesis, potentially due to the tionally, the behaviour and fate of micro-particles of different
physical blockage of light and air. Moreover, it increased reactive polymer types and shapes also needs to be established. In the
oxygen species production, indicating a state of oxidative stress natural environment, organisms may be exposed to microplastics
(Bhattacharya et al., 2010). Despite using extremely high concen- throughout their lifetime as opposed to short experimental dura-
trations e 1.4e40 mg ml1 e relative to environmental levels, this tions. Thus the continual ingestion and accumulation of such par-
study highlights the potential for microscopic plastic particles to ticles may incur chronic effects. Moreover, many different polymers
adhere to algal cells, possibly impacting on photosynthesis. As algae occur in the environment, which may elicit a different response to a
play a key role in aquatic food webs, the productivity and resilience single polymer.
of ecosystems could be compromised if high concentrations occur
due to the adverse effects of plastic particles. 4.3. Shape

4.2. Translocation The potential adverse effects associated with the presence of
microplastics are likely to vary with particle shape. Carbon nano-
Andrady (2011) states that due to a lack of enzymatic pathways tubules have exhibited lung damage; Warheit et al. (2004) found
available to break down plastics in filter-feeding organisms, the lung tissue of rats exposed to single-wall carbon nanotubules
microplastics are unlikely to be digested or absorbed and can displayed inflammation and cell injury. In mesoporous silica
therefore be considered bio-inert. However, they may pass through nanoparticles (MSNs), shape can influence the efficiency and ability
cell membranes and become incorporated into body tissues of drug delivery irrespective of chemical composition, surface
following ingestion. Fluorescence and confocal microscopy charge and diameter; rod-shaped MSNs showed increased cellular
revealed 3 mm and 9.6 mm fluorescent PS microspheres in the uptake and therefore a greater effect on apoptosis, migration and
haemolymph and haemocytes of the suspension feeder M. edulis, disruption of cytoskeleton organisation. Long rod-shaped nano-
three days after short (three hour) pulse exposures to 15 000 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 for population structure of H. sericeus may lead to ecosystem wide
such shape-related toxicity is that the long rod-shaped MSNs are consequences (Goldstein et al., 2012).
easily up-taken by cells due to the greater contact area and po- The increasing abundance of microplastics may be capable of
tential for interaction (Huang et al., 2010). Given that marine modifying community-wide assemblages. Additionally, micro-
microplastics occur in a variety of shapes from fibres to irregular plastics present a mechanism for long distance transport of rafting
fragments to spheres and rods, there is potential for the physical species, enhancing biogeographic connectivity. The most common
adverse effects of polymers to alter depending on form. Along the rafting species are from the phyla Cnidaria, Crustacea and Ecto-
Belgian coast, plastic fibres formed the majority (59%) of micro- procta (Thiel and Gutow, 2005). These species may be considered
plastic debris sampled (Claessens et al., 2011), with average con- the most vulnerable to population-level microplastic-associated
centrations of 81.0  37.2, 65.6  15.3 and 66.3  28.6 fibres kg1 changes.
for beach, harbour and sea sampling stations respectively. Con-
centrations of plastic fibres (<1 mm) ranging from 2 (Australia) to 4.6. Transfer to the food chain
31 (Portugal) fibres 250 ml1 contaminated 18 shores across six
continents, with concentration positively correlating with popula- At present, there are few studies on the bioaccumulation of
tion density (Browne et al., 2011). Thus, benthic and sediment- plastics and their associated POPs across marine trophic levels.
dwelling organisms inhabiting such areas are vulnerable to the Given that lower trophic organisms, specifically invertebrates, can
shape-related toxicity of plastic fibres, if ingested. ingest and accumulate microplastic particles, it is likely that
microplastics will be introduced to the food web. Laboratory
4.4. Egestion microplastic ingestion studies have mostly focussed on in-
vertebrates, however, in situ work has discovered microplastic
There is very little information available regarding the capacity ingestion in several vertebrate species.
for marine organisms to egest microplastics. Through fecal cast Lusher et al. (2012) found microplastics in 36.5% of fish
analysis, Thompson et al. (2004) found some microplastic particles belonging to 10 species sampled from the English Channel, irre-
were defecated by the lugworm A. marina. To assess the ingestion of spective of habitat (pelagic vs. demersal). An average of 1.9  0.1
microplastic fragments and pellets in benthic holothurians, faecal particles were recovered from those which contained plastic, the
debris was collected from individuals held in the laboratory. The main polymers being polyamide and polyester, which are mate-
quantity of defecated microplastic particles was then enumerated rials commonly used in the fishing industry (Lusher et al., 2012).
(Graham and Thompson, 2009). Through egestion, it is possible Whilst the biological consequences remain unclear, such findings
that an organism will prevent any detrimental effects caused by the are comparable to those from the North Pacific Central Gyre re-
ingestion of plastic particles. ported by Boerger et al. (2010); small plastic fragments were
The estuarine copepod Eurytemora affinis demonstrated an found in approximately one third of all fish caught. Individuals
ability to regurgitate latex beads (mean diameter 15 mm). Labora- from the most common species caught (Myctophum auro-
tory feeding trials were conducted with 3e90 beads ml1 concen- lanternatum, Myctophidae) contained an average of six plastic
trations; beads were ingested at mean rates of up to 59 000 pieces and the most frequently ingested size class across all spe-
particles per copepod per hour. The capability for plastic micro- cies was 1e2.79 mm. The majority of fish caught in this study
spherule ingestion was demonstrated, as was the potential for belonged to the Myctophidae, a low-trophic, mesopelagic family
accumulation inside the gut cavity of E. affinis. However, following which adopts diurnal feeding behaviour, preying upon plankton
the initial microspherule ingestion, the particles were subsequently near the surface at night. As the most commonly ingested plastic
regurgitated between 1 and 3 h later. This was indicated by a colours (white, clear and blue out of 12 reported colours) were
decrease then sequential increase of latex microspherules in the similar to that of plankton species inhabiting the North Pacific
feeding suspension coinciding with an absence of latex micro- Central Gyre, the Myctophidae may mistake small plastic frag-
spherules in the fecal pellets of E. affinis. Alternatively, bacterial- ments for their natural food source (Boerger et al., 2010). Alter-
coated latex microspherules (15 mm) were retained and succes- natively, the myctophids could consume plankton which has
sively egested in fecal pellets (Powell and Berry, 1990), highlighting previously ingested microplastics or ingest plastic passively. Since
an ability to reject un-nutritious particles. the most commonly occurring plastic colours in tow samples
Egestion rates are likely to affect the capacity for potentially matched those ingested, it is likely the Myctophidae are not
adhered contaminants to desorb in addition to the likelihood of showing selectivity but ingesting particles in a more passive
transfer to the food chain. Predation could still occur within the manner. The toxicological effects of plastic ingestion in mycto-
timeframe. The diurnal vertical migration of zooplankton could phids remains to be determined, however if they are unable to
further transport microplastics to predators occupying various egest small plastic fragments, the plastic may accumulate and
depths of the water column. compromise normal feeding activity. Additionally, the Myctophi-
dae are preyed upon by tuna, squid, odontoceti whales, seabirds
4.5. Population-level effects and fur seals (Boerger et al., 2010). Thus there are several routes of
entry to various compartments of the marine food web.
Aside from physical and chemical impacts, microplastics also Higher trophic level organisms have been found to ingest
have a potential role in providing a new hard-substrate habitat for microplastics transported by prey items. Microplastic particles
rafting communities, which was previously limited to items such as approximately 1 mm in diameter were recorded in the scat of fur
floating wood, pumice, and sea shells. In 2001, Moore et al. found seals and Hooker’s sea lions (Goldsworthy et al., 1997; McMahon
monofilament line 10 cm below the sea surface to be colonised with et al., 1999). The presence of plastic coincided with otoliths of the
diatoms and other microalgae. Recently, microplastics have been myctophid fish Electrona subaspera, suggesting a trophic link.
identified as an important oviposition resource for the pelagic in- Eriksson and Burton (2003) further investigated the transfer of
sect Halobates sericeus, indicated by a positive correlation between plastic particles in Antarctic fur seals. Scats of Arctocephalus tropi-
H. sericeus eggs on microplastics and microplastic abundance. The calis and A. gazella were collected from Macquarie Island, Australia,
pelagic invertebrate community represents a crucial link between during the periods 1990e1991 and 1996e1997. Out of 145 seal
primary producers and nektonic species. Thus, changes in the scats, 164 small plastic particles (generally ranging from 2 to 5 mm)
490 S.L. Wright et al. / Environmental Pollution 178 (2013) 483e492

were recovered. However, the sieves used to separate the plastic Table 3
from the scat had a mesh size >0.5 mm, suggesting that any plastic Areas for future research.

particles <0.5 mm were not retained. Thus the quantities obtained  The destination of ingested microplastics within marine invertebrates in
are likely to be an underestimation. Interestingly, during 1990e addition to potential adverse effects remains unknown, emphasising a need
1991, one plastic particle per scat was recorded, whilst during for laboratory studies focussing on the physical impacts of microplastics
 Given the occurrence of different shapes and plastic types in the marine
1996e1997 up to four particles per scat (1%) were documented; environment, research into the impacts of these factors on marine organisms
possibly a result of the increasing abundance of plastic debris in the should be conducted
marine environment. PE (93%) was the primary polymer group  The bioavailability of constituent contaminants is undetermined. This high-
identified from the samples, followed by PP (4%), which closely lights a requirement for further laboratory studies to establish the effects of
ageing on the concentration of microplastic additives, their bioavailability
matched polymer types identified in beach flotsam from the same
and the associated toxicological impacts
location. Nearly all fragments were irregular in form and approxi-  The role of microplastics as a vector for environmental POPs is uncertain.
mately one third had one sharp edge, indicating there is potential Laboratory studies investigating the bioavailability and associated toxico-
for internal abrasion. Eriksson and Burton (2003) believed there logical impacts of microplastic-associated POPs are required
was little possibility that the seal species’ were directly ingesting  There are presently no conclusive reports on the transfer of microplastics to
higher trophic levels and whether they act as a vector for contaminants.
plastic particles; a plastic-concentrating vector, such as fish, is a Studies are needed to understand the capacity for microplastics and their
more likely explanation. associated contaminants to be transported along marine food webs via tro-
Several fish species caught in New England coastal waters phic interactions as well as an estimation of population and ecosystem level
contained plastic microspherules identical to those collected dur- impacts.
ing plankton tows in the same area (0.1e2 mm); winter flounder
(Pseudopleuronectes americanus) and grubby (Myoxocephalus
aenaeus) larvae, approximately 5 mm in length, contained 0.5 mm 5. Conclusions
diameter plastic microspherules (Carpenter et al., 1972). By
extrapolating this data and that from Goldsworthy et al. (1997), Low density microplastic debris is accumulating in ocean gyres
Eriksson and Burton (2003) estimated that minimum concentra- and pelagic invertebrates inhabiting these regions may be sus-
tion factors of plastic particles to seals ranges from 22 to 160 times. ceptible to microplastic ingestion. In addition, the benthos is likely
The narrow range of particle parameters (size and shape) observed, to be a sink for high density microplastics. Some organisms may
suggests that selectivity is being practiced. E. subaspera, a major have the capacity to egest microplastics, possibly leading to their
component of the fur seal diet, is likely to consume copepods 1e incorporation into marine aggregates. Benthic suspension- and
9 mm in size near the surface waters. This size range has a 95 per deposit- feeders are therefore likely to ingest sinking and sedi-
cent overlap with the plastic particles found in scats, indicating the mentary microplastics. Fibres are the most commonly encoun-
transfer of microplastics across trophic levels is plausible. tered form of microplastics in the marine environment. Benthic
Microplastics have the potential to be ingested by baleen holothurians were found to selectively ingest microplastics,
whale species through indirect consumption via planktonic prey. showing a preference for fibrous shapes. Additionally, benthic
Mono-(2-ethylhexyl) phthalate (MEHP) contamination of the scavengers are susceptible to fibrous microplastic exposure, as gut
blubber of the Mediterranean fin whale B. physalus has recently content analysis revealed nylon fibres in N. norvegicus. This im-
been suggested as an indication that microplastic ingestion oc- plies their habitat is a sink for fibres. Since shape may play a role in
curs, either from the water column or via a planktonic vector. the toxicity of ingested microplastics e long, rod-shaped nano-
Fifty six percent of neustonic and planktonic samples from the particles are considered more toxic than spherules e these or-
Mediterranean Sea contained microplastics e up to 9.67 particles ganisms can be considered sensitive to the potential physical
m3. This coincided with high levels of phthalates in the water toxicity of microplastics.
column, specifically di-2-ethylhexyl phthalate (DEHP) and MEHP, The presence of microplastics in myctophid fish and Hooker’s
comparative to the levels found in the blubber samples. The use sea lion and fur seal scats suggest microplastic transfer through
of phthalates and plastics additives such as antimicrobials, dyes pelagic food chains: microplasticsezooplanktonemyctophid fish-
or stabilisers as tracers for microplastic ingestion and bio- Hooker’s sea lions/fur seals. Such lower trophic organisms there-
accumulation is certainly a promising avenue for future research fore represent a vector for microplastic transfer and their associated
(Fossi et al., 2012). contaminants.
At present, there is limited information regarding the impacts of Microplastics may not only affect species at the organism-level;
microplastics on food webs and no associated laboratory experi- they also have the capacity to modify population structure. Species
ments have been conducted. Therefore, it remains undetermined which were once restricted by a lack of hard substrate, such as the
whether plastic of any size can be transferred to higher trophic marine insect H. Sericeus, are now able to proliferate. This may be
levels. There are well documented examples of trophic transfer for applicable to a wide range of organisms with potential impacts on
many POPs within marine food webs, for example dioxins, PCBs and ecosystem dynamics.
polybrominated diphenylethers, many of which have been re- The accumulation of microplastic debris has presented a new
ported to associate with oceanic plastics (Ogata et al., 2009) and marine habitat where biological interactions are taking place. This
some of which can biomagnify (Hu et al., 2005). Generally, the habitat and its environmental impacts are still emerging areas of
extent of trophic transfer is dependent on characteristics including research. It is hoped that future work on this growing issue (see
the octanolewater partition coefficient (Kow) and metabolic Table 3) will contribute to the development of better methods for
transformation rate of the compound under consideration (Wan controlling marine litter.
et al., 2005). The effect of co-ingestion of microplastics on the
trophodynamic behaviour of POPs and plastics additives remains References
an important topic for further study. Other important factors to
consider for the transfer of microplastics and their associated POPs Andrady, A.L., 2011. Microplastics in the marine environment. Marine Pollution
are organism-dependent gut retention times, as well as the fraction Bulletin 62 (8), 1596e1605.
Bhattacharya, P., Lin, S., Turner, J.P., Ke, P.C., 2010. Physical adsorption of charged
of consumed microplastics that are capable of moving across the plastic nanoparticles affects algal photosynthesis. The Journal of Physical
gut epithelium and into other tissues or organs. Chemistry 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 by debris from the open ocean and remote and urban beaches. Marine Pollution
planktivorous fishes in the North Pacific Central Gyre. Marine Pollution Bulletin Bulletin 62 (8), 1683e1692.
60, 2275e2278. Hu, J., Jin, F., Wan, Y., Yang, M., An, L., An, W., Tao, S., 2005. Trophodynamic
Bolton, T.F., Havenhand, J.N., 1998. Physiological versus viscosity-induced effects of behaviour of 4-nonylphenol and nonylphenol polyethoxylate in a marine food
an acute reduction in water temperature on microsphere ingestion by trocho- web from Bohai Bay, North China: comparison to DDTs. Environmental Science
phore larvae of the serpulid polychaete Galeolaria caespitosa. Journal of and Technology 39 (13), 4801e4807.
Plankton Research 20 (11), 2153e2164. Huang, X., Teng, X., Chen, D., Tang, F., He, J., 2010. The effect of the shape of mes-
Brillant, M.G.S., MacDonald, B.A., 2000. Postingestive selection in the sea scallop, oporous silica nanoparticles on cellular uptake and cell function. Biomaterials
Placopecten magellanicus (Gmelin): the role of particle size and density. Journal 31 (3), 438e448.
of Experimental Marine Biology and Ecology 253 (2), 211e227. Hussain, N., Jaitley, V., Florence, A.T., 2001. Recent advances in the understanding of
Browne, M.A., Galloway, T.S., Thompson, R.C., 2007. Microplasticdan emerging uptake of microparticulates across the gastrointestinal lymphatics. Advanced
contaminant of potential concern? Integrated Environmental Assessment and Drug Delivery Reviews 50 (1e2), 107e142.
Management 3 (4), 559e561. Ivar do Sul, J.A., Spengler, A., Costa, M.F., 2009. Here, there and everywhere. Small
Browne, M.A., Dissanayake, A., Galloway, T.S., Lowe, D.M., Thompson, R.C., 2008. plastic fragments and pellets on beaches of Fernando de Noronha (Equatorial
Ingested microscopic plastic translocates to the circulatory system of the Western Atlantic). Marine Pollution Bulletin 58 (8), 1236e1238.
mussel, Mytilus edulis (L.). Environmental Science and Technology 42 (13), Laist, D.W., 1997. Impacts of marine debris: entanglement of marine life in marine
5026e5031. debris including a comprehensive list of species with entanglement and
Browne, M.A., Crump, P., Nivens, S.J., Teuten, E., Tonkin, A., Galloway, T., ingestion records. In: Coe, J.M., Rogers, D.B. (Eds.), Marine Debrisesources,
Thompson, R., 2011. Accumulation of microplastics on shorelines worldwide: Impacts and Solutions. Springer-Verlag New York Inc., New York, pp. 99e139.
sources and sinks. Environmental Science and Technology 45 (21), 9175e9179. Lattin, G.L., Moore, C.J., Zellers, A.F., Moore, S.L., Weisberg, S.B., 2004. A comparison
Carpenter, E.J., Anderson, S.J., Harvey, G.R., Miklas, H.P., Peck, B.B., 1972. Polystyrene of neustonic plastic and zooplankton at different depths near the southern
spherules in coastal waters. Science 178 (4062), 749e750. California shore. Marine Pollution Bulletin 49 (4), 291e294.
Christaki, U., Dolan, J.R., Pelegri, S., Rassoulzadegan, F., 1998. Consumption of Lazar, B., Gracan, R., 2011. Ingestion of marine debris by loggerhead sea turtles,
picoplankton-size particles by marine ciliates: effects of physiological state of Caretta caretta, in the Adriatic sea. Marine Pollution Bulletin 62 (1), 43e47.
the ciliate and particle quality. Limnology and Oceanography 43, 458e464. Liebezeit, G., Dubaish, F., 2012. Microplastics in beaches of the Frisian Islands
Claessens, M., De Meester, S., Van Landuyt, L., De Clerck, K., Janssen, C.R., 2011. Spiekeroog and Kachelotplate. Bulletin of Environmental Contamination and
Occurrence and distribution of microplastics in marine sediments along the Toxicology 89 (1), 213e217.
Belgian coast. Marine Pollution Bulletin 62 (10), 2199e2204. Lobelle, D., Cunliffe, M., 2011. Early microbial biofilm formation on marine plastic
Collignon, A., Hecq, J.H., Galgani, F., Voisin, P., Collard, F., Goffart, A., 2012. Neustonic debris. Marine Pollution Bulletin 62 (1), 197e200.
microplastic and zooplankton in the North Western Mediterranean Sea. Marine Lusher, A.L., McHugh, M., Thompson, R.C., 2012. Occurrence of microplastics in the
Pollution Bulletin 64 (4), 861e864. gastrointestinal tract of pelagic and demersal fish from the English Channel.
Colton, J.B., Knapp, F.D., Burns, B.R., 1974. Plastic particles in surface waters of the Marine Pollution Bulletin 67 (1e2), 94e99.
Northwestern Atlantic. Science 185 (4150), 491e497. Martins, J., Sobral, P., 2011. Plastic marine debris on the Portuguese coastline: a
Denuncio, P., Bastida, R., Dassis, M., Giardino, G., Gerpe, M., Rodriguez, D., 2011. matter of size? Marine Pollution Bulletin 62 (12), 2649e2653.
Plastic ingestion in Franciscana dolphins, Pontoporia blainvillei (Gervais and Mato, Y., Isobe, T., Takada, H., Kanehiro, H., Ohtake, C., Kaminuma, T., 2001. Plastic
d’Orbigny, 1844), from Argentina. Marine Pollution Bulletin 62 (8), 1836e1841. resin pellets as a transport medium for toxic chemicals in the marine envi-
Derraik, J.G.B., 2002. The pollution of the marine environment by plastic debris: a ronment. Environmental Science and Technology 35 (2), 318e324.
review. Marine Pollution Bulletin 44 (9), 842e852. McMahon, C.R., Hooley, D., Robinson, S., 1999. The diet of itinerant male Hooker’s
Doyle, M.J., Watson, W., Bowlin, N.M., Sheavly, S.B., 2011. Plastic particles in coastal sea lions, Phocarctos hookeri, at sub-Antarctic Macquarie Island. Wildlife
pelagic ecosystems of the Northeast Pacific ocean. Marine Environmental Research 26 (6), 839e846.
Research 71, 41e52. Moore, C.J., 2008. Synthetic polymers in the marine environment: a rapidly
Eriksson, C., Burton, H., 2003. Origins and biological accumulation of small plastic increasing, long-term threat. Environmental Research 108 (2), 131e139.
particles in fur seals from Macquarie Island. AMBIO: A Journal of the Human Moore, C.J., Moore, S.L., Leecaster, M.K., Weisberg, S.B., 2001. A comparison of plastic
Environment 32 (6), 380e384. and plankton in the North Pacific Central Gyre. Marine Pollution Bulletin 42
Fossi, M.C., Panti, C., Gurranti, C., Coppola, D., Giannetti, M., Marsili, L., Minutoli, R., (12), 1297e1300.
2012. Are baleen whales exposed to the threat of microplastics? A case study of Morét-Ferguson, S., Law, K.L., Proskurowski, G., Murphy, E.K., Peacock, E.E.,
the Mediterranean fin whale (Balaenoptera physalus). Marine Pollution Bulletin Reddy, C.M., 2010. The size, mass, and composition of plastic debris in the
64 (11), 2374e2379. western North Atlantic Ocean. Marine Pollution Bulletin 60 (10), 1873e1878.
Galgani, F., Fleet, D., Van Franeker, J., Katsanevakis, S., Maes, T., Mouat, J., Murray, F., Cowie, P.R., 2011. Plastic contamination in the decapod crustacean
Oosterbaan, L., Poitou, I., Hanke, G., Thompson, R., Amato, E., Birkun, A., Nephrops norvegicus (Linnaeus, 1758). Marine Pollution Bulletin 62 (6),
Janssen, C., 2010. In: Zampoukas, N. (Ed.), Marine Strategy Framework Directive, 1207e1217.
Task Group 10 Report, Marine Litter. EUR 24340 EN e 2010. Muthukumar, T., Aravinthan, A., Lakshmi, K., Venkatesan, R., Vedaprakash, L.,
GEF, 2012. Secretariat of the Convention on Biological Diversity and Scientific and Doble, M., 2011. Fouling and stability of polymers and composites in marine
Technical Advisory Panel GEF, Impacts of Marine Debris on Biodiversity: Cur- environment. International Biodeterioration and Biodegradation 65 (2),
rent Status and Potential Solutuions, vol. 67. p. 9. Montreal. 276e284.
GESAMP (2010, IMO/FAO/UNESCO-IOC/UNIDO/WMO/IAEA/UN/UNEP Joint Group of Ng, K.L., Obbard, J.P., 2006. Prevalence of microplastics in Singapore’s coastal marine
Experts on the Scientific Aspects of Marine Environmental Protection). Bowmer, environment. Marine Pollution Bulletin 52 (7), 761e767.
T., Kershaw, P.J., (Eds.), 2010. Proceedings of the GESAMP International Work- Norén, F., 2008. Small Plastic Particles in Coastal Swedish Waters. N-Research
shop on Plastic Particles as a Vector in Transporting Persistent, Bio- report, commissioned by KIMO Sweden.
accumulating and Toxic Substances in the Oceans. GESAMP Rep. Stud. No. 82, Noren, F., Naustvoll, F., 2010. Survey of Microscopic Anthropogenic Particles in
68 pp. Skagerrak. Commissioned by KLIMA- OG FORURENSNINGSDIREKTORATET,
Goldstein, M.C., Rosenberg, M., Cheng, L., 2012. Increased oceanic microplastic Norway.
debris enhances oviposition in an endemic pelagic insect. Biology Letters 8 (5), Oehlmann, J.R., Schulte-Oehlmann, U., Kloas, W., Jagnytsch, O., Lutz, I., Kusk, K.O.,
817e820. Wollenberger, L., Santos, E.M., Paull, G.C., Van Look, K.J.W., Tyler, C.R., 2009.
Goldsworthy, S.D., Hindell, M.A., Crowley, H.M., 1997. Diet and diving behaviour of A critical analysis of the biological impacts of plasticizers on wildlife. Philo-
sympatric fur seals Arctocephalus gazella and A. tropicalis at Macquarie Island. sophical Transactions of the Royal Society of London B: Biological Science 364
In: Hindell, M., Kemper, C. (Eds.), Marine Mammal Research in the Southern (1526), 2047e2062.
Hemisphere. Status, Ecology and Medicine, vol. 1. Surrey Beatty & Sons, New Ogata, Y., Takada, H., Mizukawa, K., Hirai, H., Iwasa, S., et al., 2009. International
South Wales, Australia, pp. 151e163. Pellet Watch: global monitoring of persistent organic pollutants (POPs) in
Gosling, E., 2003. Bivalve Molluscs: Biology, Ecology and Culture, first ed. Wiley- coastal waters. 1. Initial phase data on PCBs, DDTs, and HCHs. Marine Pollution
Blackwell. Bulletin 58, 1437e1446.
Graham, E.R., Thompson, J.T., 2009. Deposit- and suspension-feeding sea cucumbers PlasticsEurope, 2012. Plastics e the Facts 2012: an Analysis of European Plastics
(Echinodermata) ingest plastic fragments. Journal of Experimental Marine Production, Demand and Waste Data for 2011 (10.10.2012). http://www.
Biology and Ecology 368 (1), 22e29. plasticseurope.org/Document/plastics-the-facts-2012.aspx?
Greene, C.H., 1985. Planktivore functional groups and patterns of prey selection in Page¼DOCUMENT&FolID¼2.
pelagic communities. Journal of Plankton Research 7 (1), 35e40. Powell, M.D., Berry, A.J., 1990. Ingestion and regurgitation of living and inert ma-
Gregory, M.R., 2009. Environmental implications of plastic debris in marine settings terials by the estuarine copepod Eurytemora affinis (Poppe) and the influence of
e entanglement, ingestion, smothering, hangers-on, hitch-hiking and alien salinity. Estuarine, Coastal and Shelf Science 31 (6), 763e773.
invasions. Philosophical Transactions of the Royal Society of London B: Bio- Reddy, M., Adimurthy, S., Ramachandraiah, G., 2006. Description of the small
logical Sciences 364 (1526), 2013e2025. plastics fragments in marine sediments along the Alang-Sosiya ship-breaking
Hart, M.W., 1991. Particle capture and the method of suspension feeding by echi- yard, India. Estuarine, Coastal and Shelf Science 68 (3e4), 656e660.
noderm larvae. Biology Bulletin 180 (1), 12e27. Shaw, D.G., Day, R.H., 1994. Colour- and form- dependent loss of plastic micro-
Hirai, H., Takada, H., Ogata, Y., Yamashita, R., Mizukawa, K., Saha, M., Kwan, C., debris from the North Pacific Ocean. Marine Pollution Bulletin 28 (1), 39e43.
Moore, C., Gray, H., Laursen, D., Zettler, E.R., Farrington, J.W., Reddy, C.M., Talsness, C.E., Andrade, A.J.M., Kuriyama, S.N., Taylor, J.A., vom Saal, F.S., 2009.
Peacock, E.E., Ward, M.W., 2011. Organic micropollutants in marine plastics Components of plastic: experimental studies in animals and relevance for
492 S.L. Wright et al. / Environmental Pollution 178 (2013) 483e492

human health. Philosophical Transactions of the Royal Society of London B: the northern fulmar Fulmarus glacialis in the North Sea. Environmental Pollu-
Biological Science 364 (1526), 2079e2096. tion 159 (10), 2609e2615.
Teuten, E.L., Saquing, J.M., Knappe, D.R.U., Barlaz, M.A., Jonsson, S., Bjorn, A., Wan, Y., Hu, J., Yang, M., an, L., an, W., Jin, X., H, T., Itoh, M., 2005. Characterization of
Rowland, S.J., Thompson, R.C., Galloway, T.S., Yamashita, R., Ochi, D., trophic transfer for polychlorinated dibenzo p dioxins, dibenzofurans, non and
Watanuki, Y., Moore, C., Viet, P.H., Tana, T.S., Prudente, M., Boonyatumanond, R., mono ortho polychlorinated biphenyls in the marine food web of Bohai Bay,
Zakaria, M.P., Akkhavong, K., Ogata, Y., Hirai, H., Iwasa, S., Mizukawa, K., North China. Environmental Science and Technology 39 (8), 2417e2425.
Hagino, Y., Imamura, A., Saha, M., Takada, H., 2009. Transport and release of Ward, J.E., Targett, N.M., 1989. Influence of marine microalgal metabolites on the
chemicals from plastics to the environment and to wildlife. Philosophical feeding behavior of the blue mussel Mytilus edulis. Marine Biology 101, 313e321.
Transactions of the Royal Society of London B: Biological Science 364 (1526), Ward, J.E., Shumway, S.E., 2004. Separating the grain from the chaff: particle se-
2027e2045. lection in suspension- and deposit-feeding bivalves. Journal of Experimental
Thiel, M., Gutow, L., 2005. The ecology of rafting in the marine environment.II. The Marine Biology and Ecology 300 (1e2), 83e130.
rafting organisms and community. Oceanography and Marine Biology: an Ward, J.E., Kach, D.J., 2009. Marine aggregates facilitate ingestion of nanoparticles by
Annual Review 43, 279e418. suspension-feeding bivalves. Marine Environmental Research 68 (3), 137e142.
Thompson, R.C., Moore, C.J., vom Saal, F.S., Swan, S.H., 2009. Plastics, the environ- Ward, J.E., Levinton, J.S., Shumway, S.E., 2003. Influence of diet on pre-ingestive
ment and human health: current consensus and future trends. Philosophical particle processing in bivalves: I: transport velocities on the ctenidium. Jour-
Transactions of the Royal Society of London B: Biological Science 364 (1526), nal of Experimental Marine Biology and Ecology 293 (2), 129e149.
2153e2166. Warheit, D.B., Laurence, B.R., Reed, K.L., Roach, D.H., Reynolds, G.A.M., Webb, T.R.,
Thompson, R.C., Olsen, Y., Mitchell, R.P., Davis, A., Rowland, S.J., John, A.W.G., 2004. Comparative pulmonary toxicity assessment of single-wall carbon
McGonigle, D., Russell, A.E., 2004. Lost at sea: where is all the plastic? Science nanotubes in rats. Toxicological Sciences 77 (1), 117e125.
304 (5672), 838. Wilson, D.S., 1973. Food size selection among copepods. Ecology 54 (4), 909e914.
Turner, A., Holmes, L., 2011. Occurrence, distribution and characteristics of beached Yamashita, R., Takada, H., Fukuwaka, M., Watanuki, Y., 2011. Physical and chemical
plastic production pellets on the island of Malta (central Mediterranean). Ma- effects of ingested plastic debris on short-tailed shearwaters, Puffinus tenuir-
rine Pollution Bulletin 62 (2), 377e381. ostris, in the North Pacific ocean. Marine Pollution Bulletin 62 (12), 2845e2849.
van Franeker, J.A., Blaize, C., Danielsen, J., Fairclough, K., Gollan, J., Guse, N., Zebe, E., Schiedek, D., 1996. The lugworm Arenicola marina: a model of physiological
Hansen, P.L., Heubeck, M., Jensen, J.K., Le Guillou, G., Olsen, B., Olsen, K.O., adaptation to life in the intertidal sediments. Helgoland Marine Research 50 (1),
Pedersen, J., Stienen, E.W., Turner, D.M., 2011. Monitoring plastic ingestion by 37e68.

You might also like