REVIEW ARTICLE

PUBLISHED: 20 APRIL 2017 | VOLUME: 1 | ARTICLE NUMBER: 0116

Interactions of microplastic debris throughout the

marine ecosystem
Tamara S. Galloway*, Matthew Cole and Ceri Lewis
Marine microscopic plastic (microplastic) debris is a modern societal issue, illustrating the challenge of balancing the con­
venience of plastic in daily life with the prospect of causing ecological harm by careless disposal. Here we develop the con­
cept of microplastic as a complex, dynamic mixture of polymers and additives, to which organic material and contaminants
can success­ively bind to form an ‘ecocorona’, increasing the density and surface charge of particles and changing their bio­
availability and toxicity. Chronic exposure to microplastic is rarely lethal, but can adversely affect individual animals, reducing
feeding and depleting energy stores, with knock-on effects for fecundity and growth. We explore the extent to which ecological
processes could be impacted, including altered behaviours, bioturbation and impacts on carbon flux to the deep ocean. We
discuss how microplastic compares with other anthropogenic pollutants in terms of ecological risk, and consider the role of
science and society in tackling this global issue in the future.

R
esearch reporting the presence of plastic debris in the oceans target tissues and altering metabolic and reproductive endpoints15,16.
has been in the literature since the 1970s1, when mass pro- The current consensus drawn from laboratory experiments, quantita-
duction methods first started to increase the scale and scope tive assessments and modelling studies is that the net contribution of
of plastic use. Fast-forward to the present day and plastics have plastics to bioaccumulation of hydrophobic contaminants by marine
become a ubiquitous feature of modern life and a dominant mate- animals is likely to be small in comparison with uptake of contami-
rial in the consumer marketplace, with global production figures nants directly from water 15. Instead, it is the selective nature of the
currently in excess of 300 million tonnes per year 2. Around 50% of compounds transferred and the ways in which they are presented to
plastic items are used just once before being discarded, resulting in tissues and cell receptors that pose a novel risk13.
a growing burden of plastic waste, enough, it has been suggested, There have been calls for microplastic to be reclassified as hazard-
to leave an identifiable imprint in the geochemical fossil record3. ous17, but regulation to restrict the mass flow of plastic debris into the
An estimated 4.8–12.7 million tonnes of plastic was discharged into oceans has been hampered by a lack of knowledge of how impacts
the oceans in 20104, and models have conservatively estimated over on individual organisms might lead to ecological harm. This is con-
5 trillion pieces of plastic are floating in the world’s oceans5. Tiny firmed by a recent systematic review of 245 studies in which bio-
plastic fragments, fibres and granules, termed microplastic (one logical impacts of marine debris were reported, identifying that the
micrometre to five millimetres in diameter) are the predominant majority of studies were at the sub-organismal or individual level,
form of ocean plastic debris6. Microplastic includes items manufac- with few, if any, able to demonstrate ecological harm at higher levels
tured to be small, such as exfoliating microbeads added to cosmet- of biological organization18. What, then, are some of the main areas
ics, synthetic particles used in air blasting and antifouling of boats, for ecological concern? How do we extrapolate from the effects on
and microspheres used in clinical medicine for drug delivery (ref. 7 individuals to the ecological processes most likely to be impacted?
and references therein). Secondary microplastic forms via fragmen- How does microplastic compare with other anthropogenic stressors
tation of plastic debris in the environment through photooxidation, threatening ocean life?
mechanical action and biodegradation8,9. The timescale and scope of
fragmentation is uncertain; in the cold, oxygen-limiting conditions The dynamic nature of microplastic
found in marine waters and sediments it could take over 300 years A key issue in understanding the ways in which microplastic
for a 1 mm particle to reach a diameter of 100 nm (ref. 10). interacts with the surrounding environment is its dynamic nature
Microplastic is a concern because its small size is within the opti- (Fig. 1). The size, shape, charge and other properties of micro­plastic
mal prey range for many animals within the marine food web11. are constantly changing, altering its biological fate and bioavail-
Microplastic is ingested by filter, suspension and detritus feeders liv- ability. The vast majority of microplastic in the oceans is believed
ing in the water column and bottom sediments, and has been found to originate from weathering of larger items8, through mechanical
in the guts of invertebrates, fish, turtles and other larger animals, action and degradation, driven largely by UV-radiation-induced
including species intended for human consumption or those play- photooxidation, releasing low-molecular-weight polymer frag-
ing critical ecological roles12. Modern plastics are typically a complex ments such as monomers and oligomers, and forming fragments of
cocktail of polymers, residual monomers and chemical additives. increasingly smaller size9. A mismatch in the expected size distri-
Absorbed organic matter 13, bacteria14 and chemical contaminants15 bution of microplastic in ocean surface field surveys highlights the
add to their complexity. The transfer of these substances to animal plausibility that millimetre-scale debris may be fragmenting to form
tissues increases their potential to cause harm, since many plastic nanoplastic19. Although measuring plastic of this minute size in the
additives and persistent waterborne chemicals are endocrine disrup- oceans presents technical challenges that have not yet been met,
tors, capable of activating hormone signal transduction pathways in recently a solar reactor was used to illustrate that nanoplastic could

College of Life and Environmental Sciences: Biosciences, University of Exeter, Exeter EX4 4QD, UK. *e-mail: t.s.galloway@exeter.ac.uk

NATURE ECOLOGY & EVOLUTION 1, 0116 (2017) | DOI: 10.1038/s41559-017-0116 | www.nature.com/natecolevol 1

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REVIEW ARTICLE NATURE ECOLOGY & EVOLUTION

Plastic input Particle surfaces, the absorbsome and the ecocorona

UV
The surface properties of microplastic play an important part in
determining its ecological impacts. Plastics characteristically have
smooth, hydrophobic surfaces that have no net charge, but this
changes rapidly in seawater (Fig. 2). Substances from the water col-
umn or sediment are rapidly accumulated, including organic mat-
ter, nutrients, hazardous hydrophobic contaminants and bacteria,
Degradation
the latter attracted by the nutritious content of organic material.
Degradation A better understanding of the factors that can influence absorp-
tion onto the surface of microplastic can be gleaned from the litera-
ture relating to the protein corona that forms on nanoparticles from
biological fluids such as serum and cytoplasm. According to this
Nanoplastic Microplastic Macroplastic paradigm, the surface of nanomaterials in biological fluids rapidly
<0.1 μm 0.1 μm–5 mm >5 mm

Varying density
becomes coated with proteins and biomolecules, which strongly
Aggregation
influence the interaction of nanoparticles with cells and tissues,
and ultimately their persistence, bioavailability, toxicity 26,27 and eco­
toxicity 28. The protein corona concept recognizes a tightly adhered
‘hard corona’ which remains strongly bound to the particle as it
moves between compartments, and a ‘soft corona’ made up of more
loosely bound proteins in dynamic exchange with surrounding
molecules29. Importantly, of the many thousands of proteins present
in serum, only a limited number of around 125 proteins selectively
bind to particle surfaces, and these are not always the most abun-
Ecocorona Faeces Marine snow dant ones. This so-called absorbome forms in layers, with some
proteins recognizing the nanoparticle surface directly, and others
Plastic export? associating with the already coated particle through protein-protein
interactions30. Why this happens is unknown, but may relate to
the propensity for certain extracellular proteins (for example, lipo­
Figure 1 | Schematic illustration of the dynamic changes experienced proteins) to form nanoscale biomolecule clusters. Hence, the nano-
by microplastic in the water column. Plastic entering marine ecosystems particles act like scaffolds and in turn may alter the conformation
from terrestrial and maritime sources is vulnerable to photooxidation of the absorbed proteins, changing their epitope recognition and/or
by ultraviolet (UV), mechanical and biological degradation resulting modifying interactions with cellular receptors13. The corona can
in fragmentation to smaller sizes. Adherence of macromolecules and also contain other biomolecules such as carbohydrates, which tend
microorganisms to the surface of micro- and nanoplastic result in the to be multivalent and the net effect is to engage the nanoparticle sur-
formation of an ecocorona. Interactions with biota and marine aggregates face with multiple, varied receptors on the cell surface, enhancing or
repackage microplastic into faeces and marine snows. These biological sometimes inhibiting their internalization into cells31.
processes increase the relative size, chemical signature and density of the A parallel concept for understanding the behaviour and ecologi-
plastic particles. The density of a plastic particle will affect its position cal impacts of micro- and nanoplastics is that of the ecocorona13.
within the water column, potentially resulting in export to the seafloor. Natural waters contain natural organic macromolecules (NOM)
that typically host high amounts of humic and fulvic acids, excreted
form from the fragmentation of weathered polyethylene and poly- waste products and exuded lipids and polysaccharides, proteins
propylene microplastic collected from marine waters20. The nano- and macromolecules, all forming a complex polymeric mixture
plastic consisted of smaller (<50 nm) spherical particles and larger, that varies seasonally and spatially. The way in which NOM inter-
uneven fractal fragments, likely to exhibit differences in diffusion acts with particle surfaces in the aquatic environment mirrors the
properties and porosity. formation of the protein corona in biological fluids. Components
The presence of nanoplastic is important from an ecological con- of NOM can be absorbed by particles in layers, varying in thick-
text because its microscopic size allows it to pass across biological ness from flat monolayers to multilayers, consistent with the notion
barriers and to enter cells, whilst high surface area to volume ratios of the hard and soft protein corona32. This means that microplastic
enhance its reactivity 21. In addition, the atoms located at the sur- could retain a record of its environmental progress into different
face of a nanoplastic have fewer particles around them, compared compartments, in much the same way as nanoparticles do in serum
with micrometre-scale particles, and this leads to a lower binding and when moving into different cellular locations. For example, it
energy per atom with decreasing particle size. Nanoparticles hence has been shown33 that microplastic ingested by planktonic copepods
have a tendency to aggregate with other particles, natural colloids were egested within faecal pellets along with high concentrations
and suspended solids22; for example, 30 nm nanopolystyrene rapidly of organic matter. Under these circumstances, the microplastic may
formed millimetre-sized aggregates in seawater with high attach- retain an ecocorona composed of macromolecules absorbed from
ment efficiencies23. Since aggregates will have a higher density than biological fluids that will subsequently exchange and interact with
dispersed particles, their settling rate through the water column will organic materials, minerals and other components of marine snows
be increased. Settling of micro- and nanoplastic through the water in their new environment. This could explain why microplastic
column varies depending on the type of polymer, surface chemis- behaves differently to other inert materials such as clay when it is
try and the extent of biofouling by microbial biofilms and rafting ingested, often being retained for longer in the gut 34.
organisms24. Microplastic will settle until it reaches the often vari- The idea of absorbed layers also supports the notion of micro-
able density of surrounding seawater, allowing it to remain adrift and plastic contributing towards a Trojan horse effect for pollutants,
potentially to move long distances through the action of ocean cur- in which particles contribute towards the flux of contaminants
rents19. The timescale for these processes remains unknown; although acquired from the surrounding environment and released into the
plastics can disperse rapidly across the ocean surface, particles may gut fluids, tissues or cells of the ingesting organism35. Contaminants
take many weeks or years to reach the ocean floor 25. bound onto microplastic in layers could be more bioavailable to

2 NATURE ECOLOGY & EVOLUTION 1, 0116 (2017) | DOI: 10.1038/s41559-017-0116 | www.nature.com/natecolevol

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NATURE ECOLOGY & EVOLUTION REVIEW ARTICLE
Infochemicals
a
Perhaps of most interest in considering the ecological interactions
of microplastic is the concept of selective binding of secretory mol-
ecules. The protein corona formed in biological fluids contains a sig-
nificant proportion of proteins involved in transport and signalling,
including immunoglobulins and albumins30. Natural organic mat-
ter likewise contains many molecules that are deliberately excreted
or exuded to perform specific biological functions for marine ani-
mals. Chemical sensing is a ubiquitous means of communication
and allows for many inter- and intra-species interactions, including
symbiosis, mate detection and predator–prey cues. A core selection
of chemical cues drives complex foraging cascades across multiple
trophic levels, from behavioural attractions in locating foraging
zooplankton to global scale impacts on climate39. These ‘infochemi-
cals’ include dimethylsulfide (DMS), a sulfur-containing compound
produced by phytoplankton, which induces foraging activity in a
wide range of animals. Experimental studies using polypropylene
100 μm
and polyethylene, both abundant in marine debris, showed that
both could acquire an active DMS signature after less than a month
of exposure in the ocean. Responsiveness to DMS can occur at con-
b centrations as low as 10–12 M and a positive relationship was found
between DMS responsiveness and plastic ingestion using data from
over 13,000 seabirds40. These results provide compelling evidence to
explain the high rates of ingestion of plastic debris by seabirds and
also support the notion of an ecocorona showing selective binding
of an important marine infochemical.
In another study of predator–prey cues, Daphnia magna, small
crustaceans central to aquatic food webs, were exposed to nano­
polystyrene preconditioned in water from neonate cultures. The
toxicity of the nanopolystyrene was enhanced and the particles were
retained for longer in the animals’ guts. Daphnia show profound
changes in feeding, reproduction and other traits in response to
predator ‘kairomones’ (interspecies pheromones) and inspection of
the particle surface confirmed the presence of a protein layer that
was exchanging and rearranging over time41.
These results support the notion that a secreted protein eco­
100 μm
corona can form on microplastic and can mediate its ingestion in
both microfauna and macrofauna. Thus the ecocorona concept
could help to explain the high rates of ingestion of microplastic
Figure 2 | Scanning electron microscopy images of microplastics. reported in so many animals across multiple trophic levels34, by
a, Polyethylene microbead purified from a facewash. b, Polyethylene enhancing the attractiveness of microplastic as a food item.
fragment collected from beach litter. Images: A. Watts.
Microbial communities and marine snows
organisms if absorbed via an ecocorona layer rather than directly to The ecorona could additionally modulate the absorption of bacte-
the surface of the plastic35. This concept supports a study of the bio- ria. Analysis of weathered microplastic debris collected from the sea
availability of silver to zebrafish (Danio rerio), which was reduced surface revealed a diverse microbial community of colonizing bacte-
when fish were presented with microplastic to which silver was ria, including heterotrophs, autotrophs, predators and symbionts14.
already absorbed, compared with co-exposure to plastic and silver Opportunistic bacteria form biofilms on any available surface, gain-
at the same time36. ing access to nutritious matter, protection and enhanced dispersal.
Ecocorona components could also influence the movement and Microplastic biofilms appear distinct compared with those on other
behaviour of microplastic. Humic substances are weak acids and marine substrata and are shaped by spatial and seasonal factors42.
are negatively charged under environmental pH conditions. Their Vibrio are ubiquitous marine bacteria frequently reported in plastic-
propensity to bind to particles in marine waters is borne out by the associated biofilms43 and some species, such as Vibrio crassostrea are
finding that virtually all weathered microplastic isolated from sea- associated with pathogenic infections in oysters. Colonization of
water has a negative charge37. Once absorbed to particles, the charge microplastics by V.  crassostrea is enhanced when the micro­plastic
and flexibility of humic substances will tend to stabilize and dis- was already coated by a layer of marine aggregates containing a
perse particles into the water column, which could enhance their multispecies natural assemblage, that is, they are secondary 44 rather
bioavailability for filter-feeding and suspension-feeding organisms. than primary colonizers showing chemotactic attraction to the
Exopolymeric substances are exuded by unicellular and multi­cellular particle surface. The layering of primary and secondary colonizing
organisms including bacteria and phytoplankton and consist largely bacteria provides further support for the concept of a layered eco-
of long-chained polysaccharides that can form rigid, fibrillar chains. corona documenting the movement of particles through different
Exopolymeric substances can link to form gels, mucilage and slime environmental compartments over time.
aggregates, which play an essential role in nutrient cycling 38. When The tendency for microplastic to become incorporated into
absorbed to microplastics such substances are likely to encourage excreted and egested organic materials33 and marine aggregates is an
aggregation, increasing the density, sinking rate and bioavailability important observation45. The sinking of organic and inorganic aggre-
of microplastic to detritus feeders on the ocean floor. gated matter (marine snow) from the surface is crucial for removal of

NATURE ECOLOGY & EVOLUTION 1, 0116 (2017) | DOI: 10.1038/s41559-017-0116 | www.nature.com/natecolevol 3

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REVIEW ARTICLE NATURE ECOLOGY & EVOLUTION

Microplastic Microplastic ingestion rarely causes mortality, with few signifi­

Ingestion cant impacts on survival rate. As a result, LC50 values (the con-
Uptake across membranes centration required to cause lethality in 50% of the population)
Release of co-contaminants
are rarely reported. Notable exceptions include: 100% mortality
of common goby following 96  h exposure to polyethylene with
thology Morta
200 μg l–1 pyrene52; 0% survival of Asian green mussels exposed to
topa nd Ingestio lity
His olic dema nr
ta b eserv es Ind ividual g ates 2,160 mg l–1 polyvinylchloride (PVC) for 91 days53; and 50% sur-
Me rgetic r row
O
ty ne th F vival of Daphnia magna neonates after 14 days exposure to 100,000
sis ili e E Lar ffsp ecu
to stab ons va rin
e resp ld g particles ml–1 of polyethylene54. In all such cases, concentrations far

nd viab men
ag ra p

ev
Ph mb po

ity ilit t
oc n

exceeded environmental relevance.

age Me A

Organs Individual
ic

elo
yt

An emerging paradigm is that chronic exposure to micro­plastic

p
y
Cells Population is associated with reduced ingestion of natural prey, resulting in

Eco mmuni
Gene ex ctivity
Oxidative ression

Co
shortfalls in energy and reduced growth and fecundity 55. Reduced

syst
Beh function
dam

of E
relecol food consumption following ingestion of microplastic is associated

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a

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ed nse
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Enzyme

o v
og ance
res pe

with reductions in: metabolic rate, byssus production and survival

ty shifts
ica
Subcellular Ecosystem
p
S

in Asian green mussels53; fecundity and survival in copepods56;

Biological Level of biological growth, development and survival in Daphnia54; nutritional state
endpoints organization and growth in langoustine57; and energetic reserves in shore crabs
and lugworms58,59. However, impacts on feeding are not always
Figure 3 | Simplified scheme illustrating potential impacts of exposure to evident, with a number of suspension-feeding (for example, oys-
microplastic across successive levels of biological organization. ter larvae, urchin larvae, European flat oysters, Pacific oysters)60–63
and detritivorous (for example, isopods, amphipods)64,65 inverte-
inorganic photosynthetically fixed carbon and the cycling of essen- brates showing no indication of impaired ingestion when exposed
tial nutrients to the deep ocean, and marine snows contain diverse to microplastics.
microbial communities that degrade organic matter during the sink- Reproductive output is a particularly sensitive endpoint, with
ing process. Hence they secrete a wide range of hydrolytic enzymes energetic depletion resulting from microplastic exposure affecting
for degrading proteins, lipids and other macromolecules associated fecundity and fertility. In adult Pacific oysters (Crassostrea gigas),
with these complex particles. The attached microbial communities at an eight-week exposure to polystyrene microbeads across a repro-
depth appear to be ‘inherited’ from the microbial communities found ductive cycle resulted in reduced sperm motility, oocyte numbers
at the ocean surface, that is, they are carried there with the sinking (fecundity) and size (energetic investment per oocyte). Following
particles46. This is intriguing, since sinking microplastic could host fertilization, larval yield and growth were also significantly reduced
a different portfolio of microorganisms to those found on marine without any further microplastic exposure as a carryover from the
snow particles. Microbial communities are highly concentrated in adult exposures63. Similar effects have been observed with the cope-
marine snows, reaching concentrations 10,000 times higher than in pods Tigriopus japonicus 66 and Calanus helgolandicus 56, and rotifer
surrounding waters and this enhances the release of quorum sen- Brachionus koreanus 50, with reduced fecundity, egg size, hatching
sors by marine snow communities47. Quorum sensors are signalling success and survival of progeny. These findings suggest that the phys-
molecules released by bacteria in response to cell density that con- ical presence of microplastic particles where there should otherwise
trol many metabolic processes including the hydrolysis of complex be food, and the longer gut passage times of these non-­nutritious
organic materials. It is an interesting speculation that such quorum- particles is associated with adverse biological impacts.
sensing regulators could, in doing so, favour the formation of com-
munities capable of degrading hydrocarbon polymers, allowing in From individuals to ecological processes
time for degradation and mineralization of the plastics themselves. A general paradigm of ecotoxicology is that the impact of a pollut-
Characterizing the relationship between microplastic, marine ant cascades through levels of biological organization such that bio­
aggregates, the microbial communities associated with them and chemical changes at subcellular levels precede changes to cells and
the extent to which both microplastic and microbial communities tissues, which in turn affect physiological functions and individual
change as they sink to the ocean floor is likely to be a fruitful and fitness (that is, populations) and ultimately ecosystems49 (Fig.  3).
important future research priority. Directly linking sub-organism-level impacts to the ecosystem level
is hugely challenging for any environmental pollutant, yet it is the
Biological effects to individuals ecosystem-level impact of a contaminant that is of ultimate con-
Microplastic poses a risk to organisms across the full spectrum cern. An individual’s behaviour forms an important link between
of biological organization from cellular to population level effects physiological and ecological processes and is a sensitive measure of
(summarized in Fig.  3)48. Understanding the potential impacts of response to environmental stress or pollutants67. Hence behavioural
microplastic across all biological levels is key for the development changes can serve as early warning signs for ecosystem level effects68.
of effective risk assessments, for example using the adverse out- Understanding how the presence of microplastic changes complex
comes pathway (AOP) approach, common in chemical regulation49. behaviours such as predator–prey interactions, burrowing and
Most studies have focused on individual level effects of microplastic orientation are essential to understanding its ecological impact 67.
ingestion in adult organisms, often combined with effects of micro-
plastics at the cellular and sub-cellular level. For example, negative Behaviour
impacts of polystyrene microbead ingestion by rotifers on adult A handful of studies have considered altered behaviour, such as
growth rate, fecundity and lifespan has been observed50. They then motility, hiding responses and predator–prey interactions, result-
used in vitro tests to relate these effects to activation of antioxidant- ing from microplastic exposure. The predatory performance of
related enzymes and mitogen-activated protein kinases (MAPK) juvenile gobies (Pomatoschistus microps) in catching prey (Artemia
signalling pathways associated with inflammation and apoptosis. spp.) was reduced by 65% and feeding efficiency by 50% in labo-
Sub-cellular oxidative stress responses to polystyrene microbead ratory bioassays when fish were simultaneously exposed to poly-
(2–6 μm) ingestion have also been reported51 in mussels exposed to ethylene microspheres of a similar size and abundance to prey 69.
2,000 particles per ml seawater. Artemia are highly mobile, raising the possibility that the stationary

4 NATURE ECOLOGY & EVOLUTION 1, 0116 (2017) | DOI: 10.1038/s41559-017-0116 | www.nature.com/natecolevol

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NATURE ECOLOGY & EVOLUTION REVIEW ARTICLE
microplastic reduced the discrimination of the fish for their prey.
Beachhoppers show characteristic behaviours including distinctive
jumping, a highly energy-dependent process, and shelter relocation
post disturbance, driven largely by hygrokinetic (favouring move- Filtering
ment towards humid conditions) and intraspecific interactions70.
Exposure of the Australian beachhopper Platorchestia smithi to
beach sediments containing 3.8% by weight polyethylene micro- Particle capture
spheres led to reduced jumping, whilst the time taken to return Egestion
to shelters post disturbance was not changed71. Beachhoppers that
ingested microplastic were significantly heavier, with an increase
in gut retention times. Similarly, in the freshwater crustacean Burial?
D. magna, ingestion of 1-μm polyethylene particles from the water
column caused immobilization in a dose- and time-dependent
manner 72. Weight gain may contribute directly to reduced motility,
but motility may also be affected indirectly as a result of reduced
Incorporation
energy uptake from the diet. Reduced energy reserves34,56, for exam- into burrow walls?
ple, could influence a wide range of behaviours, including those
associated with risk versus benefit decisions in feeding behaviour.
Studies in social vertebrates (for example, birds and fish) show how
individuals will accept a greater risk of predation to obtain food with
increasing hunger or energy deficit 73–75. The internal state of animals
can significantly determine their choice between alternative behav-
ioural tactics76, providing an interesting hypothetical mechanism by Figure 4 | Mechanisms by which benthic organisms could influence the
which microplastic ingestion may influence complex behaviour and partitioning of microplastics between the water column and sediments.
species interactions. The filter-feeding action of benthic mussels and sea squirts can draw down
microplastic from the water column towards the benthos, increasing its
Bioturbation bioavailability to sediment-dwelling organisms. Bioturbating species such
The reworking of sediments by plants and animals contributes as brittlestars and deposit-feeding polychaetes may then incorporate
towards ecosystem functioning by modifying benthic seascapes, microplastic into sediments to varying depths through burrowing behaviour.
increasing nutrient flux across the benthic boundary layer and
altering habitat structure for other benthic organisms. Hence it can the biogeochemistry and the timing of food presence in pelagic
link individual physiology with ecosystem function. Throughout food webs79. Microplastic ingestion reduced the energetic intake of
coastal and shelf seas benthic environments, the burrowing activi- the copepod Calanus helgolandicus by 40% in laboratory exposures,
ties of meiofaunal and macrofaunal invertebrates such as polychaete even when the abundance of microplastic was an order of magnitude
worms, brittlestars and amphipods, whose biomass in continen- less than that of prey 56.
tal shelf sediments can be up to 200 g dry weight per m2 (ref.  77), If similar reductions in consumption are observed across entire
influences the physical and chemical properties of the sediment zooplankton communities as a result of microplastic ingestion this
where they live. When the large deposit feeding polychaete worm could have knock-on effects for pelagic ecosystems. However, whilst
Arenicola marina was chronically exposed for a month to sediment zooplankton ingestion of microplastic has been reported for natu-
containing 5% by weight PVC, there was a significant reduction in rally caught animals80, we know little of the extent of microplastic
feeding activity and the gut passage time of sediments was 1.5 times consumption within communities in their natural settings, let alone
longer 34. Extrapolation of this data to the Wadden Sea predicted this how it might influence the dynamics of mixed species assemblages.
level of contamination would lead to 130  m3 less sediment being Zooplankton not only influence planktonic assemblages via their feed-
turned over annually for that population alone. A subsequent study ing behaviour and prey selection but contribute to carbon transport
suggested that exposure of A. marina to polyethylene and PVC in to deeper waters through excretion of ingested organic matter 81–83.
sediments would reduce the surface area available for sediment– In laboratory exposure studies copepods egested micropolystyrene-
water exchange, and hence the release of inorganic nutrients, by laden faecal pellets of reduced density and integrity and which had
10–16% (ref. 78). a 2.25-fold reduction in sinking rate33. Extrapolating these results to
The feeding behaviour of A. marina, and other bioturbators such the average depth of the ocean would hypothetically result in fae-
as brittlestars, could alter the distributions of microplastics at the cal pellets taking on average 53 days longer to sink to the benthos.
water/sediment interface, enhancing mixing of particles deeper into Polyethylene and polypropylene micro­plastics, which are very com-
the sediments (Fig.  4) making them bioavailable for other meio­ mon in surface waters of oceanic regions, may have an even more
fauna. Benthic filter feeders such as mussels and sea squirts process pronounced effect on faecal pellet sinking speed, because they are
large volumes of seawater per hour through their siphons. Expelled less dense than the polystyrene used in these experiments. Given the
waste water and pseudofaeces could draw down microplastics importance of zooplankton faecal material in driving carbon export
from the water column to the benthic boundary layer, leading to from surface waters, such reductions in density and sinking rates
incorporation into sediments by burrowing species. Hence, micro- could potentially contribute to global scale alterations in carbon flux
plastics may impact feeding rates of key species, whilst the same if zooplankton across the oceans are indeed consuming microplastic
feeding activities may impact the fate of microplastics within the particles in sufficient quantities25.
marine environment.
Conclusions and future directions
Zooplankton feeding and carbon export What emerges from this account are the varied ways in which the
Altered feeding behaviour in zooplankton in the presence of micro- influx of microplastic into the oceans could plausibly be impact-
plastics may contribute towards larger scale effects due to their ing ecological processes. Microplastic represents a novel matrix,
important role within pelagic ecosystems. For example, prey selec- providing an alternative surface for pollutants, bacteria and other
tion by zooplankton can have a disproportionate impact on both types of organic matter to absorb, interact, and be transported. Its

NATURE ECOLOGY & EVOLUTION 1, 0116 (2017) | DOI: 10.1038/s41559-017-0116 | www.nature.com/natecolevol 5

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REVIEW ARTICLE NATURE ECOLOGY & EVOLUTION

450 150
Table 1 | Comparison of microplastic against the criteria proposed for
classification of pollutants as persistent organic pollutants under the 400

Plastic debris per annum (tonnes ×106)

Stockholm Convention and against the criteria for recognition as a

Oil spilled per annum (tonnes ×103)

350
planetary boundary threat.
300 100
Classifications and criteria Criterion met?
Persistent organic pollution* 250
Environmentally persistent Yes
200
Transported over large distances Yes
Bioaccumulate through the food web Yes 150 50

Cause adverse health effects Yes 100

Planetary boundary threat†
50
Disruptive effect on vital Earth system processes of which Uncertain
we are ignorant 0 0
1970s 1980 1990s 2000s 2010s 2020s
Disruptive effect is not discovered until the associated Uncertain
impacts manifest at a global scale
Figure 5 | Graph showing global statistics for the amount of crude oil
Impacts are poorly reversible as the pollutant cannot be Yes
spilled at sea compared with the increase in terrestrial plastics export
readily reduced in the environment
into the oceans, as a function of time. The blue line shows global spillages
*Data from refs 91,92. †Data from refs 86,93. of crude oil compiled by the International Tanker Owners Pollution
Federation87. The orange line shows estimated amount of plastic debris
discharged to the oceans, extrapolated from refs 4,90.
bioavailability to marine animals appears to be rarely lethal, but
chronic exposures can evidently alter feeding, energy assimilation,
growth and reproductive output. Extrapolating these impacts to criteria of planetary boundary threats could therefore be one way of
the ecosystem level challenges our current abilities to measure and encourage global action towards remediation and control (Table 1).
model relevant processes on a global scale, but we can deduce that
potential impacts include behavioural changes to predator–prey Is microplastic a marker of the Anthropocene?
relationships, bioturbation, and perturbations to carbon cycling. Microplastic could also be viewed as a new anthropogenic material,
How do we respond to these observations and what can we do to alongside the products of mining, waste disposal and urbanization,
mitigate them? How does microplastic compare with other anthro- identified as geological materials displaced by human activity with
pogenic stressors and can we use existing tools for monitoring the potential for long term persistence3. According to this view, the
and remediation? massive increase in the production and release of plastics is mir-
rored by several other substances, including aluminium, concrete
Is microplastic a persistent pollutant? and synthetic fibres for which hundreds of thousands of tonnes are
A wide range of policy documents and procedures are in place manufactured each year, sufficient to leave an imprint of population
to assess and restrict the release of chemical pollutants, includ- growth and industrialization in the fossil record. By defining these
ing international treaties, for example, the Montreal Convention, products as markers of a new geological epoch, the Anthropocene,
Stockholm Convention, Minamata Convention, and diverse the authors argue that this places the impetus on human society to
national legal instruments. In general, chemicals are assessed and acknowledge the consequences of its own actions.
controlled according to their persistence, bioaccumulation potential The opportunity for change and remediation is not outside the
and toxicity and controlled accordingly 84. It could be argued that realms of possibility. Figure 5 shows how global action has been suc-
since these measures have been so successful in controlling other cessful in reducing the amount of spilled oil reaching the oceans each
persistent pollution threats, such as organochlorine pesticides and year as a result of concerted global action to improve tanker safety 87.
polychlorinated biphenyls, they should also be sufficient to curtail Statistical data for global emissions of hazardous waste is hard to
microplastic pollution. An immediate problem is presented by the come by, but systematic data gathered by the US Environmental
observation that a microplastic is not an individual entity, but con- Protection Agency on chemical waste emissions by US industries
sists of a complex mixture of polymers, additive chemicals, absorbed revealed impressive reductions, from some 278 million tonnes
organics and living substances. The assessment of each substance of hazardous waste generated by chemical plants in 1991, to just
individually is unlikely to reflect the net sum of their action or to 35 million tonnes in 200988. This latter improvement was brought
adequately assess their bioavailability to organisms85. Despite this about through an industry-led move towards green chemistry,
limitation, comparison of microplastic against the criterion for clas- which aimed to redesign chemical processes to make them cleaner,
sification as a persistent organic pollutant under the Stockholm safer and more energy efficient. Polymers make up around 24% of
Convention shows the concept of including them to be worthy of the output of chemical industries worldwide89, raising the possibil-
discussion (Table 1). ity that concerted action to improve current chemical management
and disposal practices for polymers is a real possibility that could
Is microplastic a planetary boundary threat? lead to a similar positive reduction in waste.
Another way of viewing microplastic could be as a planetary Meeting the challenges posed by microplastic requires us, as a
boundary threat. Chemical pollution has been identified as one of society, to actively engage and consider our role in patterns of con-
the anthropogenic impacts of such magnitude that it threatens to sumption and careless disposal. Industry can play its role by reas-
exceed global resilience, alongside stressors such as climate change, sessing the integrated management of chemical production. Finally,
biodiversity and ocean acidification86. By identifying these science- we have a golden opportunity as scientists to find innovative ways
based planetary threats, we can theoretically encourage boundaries of rising to the multidisciplinary global challenge posed by the vast
to be set at a global scale to allow humanity to flourish without caus- tide of marine microplastic debris which threatens to engulf our
ing unacceptable global change. Assessing microplastic against the oceans, before it causes irreversible harm.

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NATURE ECOLOGY & EVOLUTION REVIEW ARTICLE
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