Correction

NEWS FEATURECorrection for “News Feature: Microplastics present pollutionpuzzle,” by Alla Katsnelson, which appeared in issue 18, May 5,2015, of Proc Natl Acad Sci USA (112:5547–5549; 10.1073/pnas.1504135112).The editors note that on page 5549, right column, second full

paragraph, lines 3–5, “Linda Amaral Zettler at the Woods HoleOceanographic Institution” should instead appear as “LindaAmaral Zettler at the Marine Biological Laboratory.” The onlineversion has been corrected.

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News Feature: Microplastics presentpollution puzzleTiny particles of plastic are awash in the oceans—but how are theyaffecting marine life?

Alla KatsnelsonScience Writer

When Mark Browne set out to study theplastic waste that litters the oceans, he hadn’tplanned on doing laundry in the name ofscience. Browne, an ecologist at the Univer-sity of New South Wales, Australia, was aim-ing to chart the quantities and types of plasticfragments washing up on shores worldwide.Five years ago, he and his colleagues hadalready found a surprisingly large amountof nylon and polyester fibers, particularlynear heavily populated areas. When theysampled sewage effluent, as well as decades-old sewage dumps, Browne and his col-leagues found the same range of fibers, in

exactly the same proportions of polymersused by the clothing industry.So Browne set up three washing machines

and began running synthetic blankets, shirts,and sweaters through the spin cycle, testingthe water that drained out of the machines.“Our water footprint was probably huge,” hesays, “but the amounts [of fibers] we detectedwere alarming.” Garments such as fleeces shedup to 1,900 tiny fibers every time they werewashed (1). Too small to be filtered out of thesewage system, the fibers would eventuallyfind their way to open water, Browne says.Such fibers are the most abundant type

of microplastic: pieces of plastic less than

5 millimeters in size that are becoming in-creasingly common in the ocean. Over thepast decade, Browne and a growing numberof other researchers have begun investigatingprecisely where microplastic is found andhow it affects marine life. Various groupshave found the stuff inside the digestive tractsof more than 100 different species (2), fromzooplankton to whales, and discovered that itcan pass through the gills of crabs and fish.Worryingly, microplastic also soaks up pol-lutants that are present in the ocean anddelivers them into sea creatures’ tissues.However, researchers still know remark-

ably little about how toxic this plastic maybe for humans and other animals, or thedisruption it causes to ecosystems. “In termsof demonstrating harm, the jury’s still out, inmy opinion,” says Richard Thompson, a ma-rine biologist at the University of Plymouth,United Kingdom. “I think that’s the cuttingedge of the science at the moment.”

Sounding the AlarmAbout 300 million tons of plastic is manu-factured every year, and between 5 and 13million tons of it of it ends up in the ocean.Where it lingers is still an open question (3).One study, based on samples taken on 24expeditions over six years, estimated thatsome 269,000 tons of the plastic remainsafloat on the ocean’s surface (4). Much ofthat is in “macro” form: large hunks of trash,such as fishing nets, buoys, and packagingthat litters shorelines or swirls around theenormous circular current systems of thePacific, Atlantic, and Indian Oceans.Quantifying seaborne microplastic—syn-thetic fibers, microbeads that are used incosmetics and industrial cleansers, and scrapsbroken off of every other type of plastic in thewater—is even more complicated. The mostrecent estimate of 35,500 tons (4) is on a parwith previous studies (5, 6), but the numberis much lower than expected. The missingmicroplastic waste has perhaps sunk into thedepths of the ocean, washed ashore onto

Polyethylene beads such as these, extracted from a cosmetic product and shown in an electronmicrograph, tend to pass through sewage treatment plants and end up in natural waters.Image courtesy of Adil Bakir and Richard Thompson (Plymouth University, United Kingdom).

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beaches, or been swallowed into the guts ofmarine animals.Thompson’s laboratory recently showed

that vast quantities of microplastic fibers arepresent on the deep sea floor, about fourtimes the amount seen at the surface (7).“Even if we could wave a magic wand andstop all inputs of debris to the ocean, thenumbers of microplastic pieces are only go-ing to increase in the next few decades be-cause of the legacy contaminants that arealready there,” Thompson says. Given thatplastic manufacturing is predicted to risesteadily to 33 billion tons by 2050, that in-crease is likely to be sharp.Thompson was one of the first scientists to

sound the alarm over microplastic. Research-ers first reported finding small pieces of plasticin fish more than 40 years ago (8), but itwasn’t until 2004 that Thompson showed thepresence of truly microscopic pieces, whichhe called microplastic. As a graduate student,Thompson had noticed the small fragmentsthat everyone else stomped over at volunteerbeach clean-ups. When he set up his ownresearch group Thompson sent his students tocollect the tiniest pieces of plastic they couldfind. He used a forensic technique calledFourier transform infrared spectroscopy toconfirm that the microscopic grains from sandand seawater were indeed plastic, and com-pared water from the Atlantic Ocean withsamples taken decades earlier to prove thatmicroplastic had become much more abun-dant over the years (9).By that time, Hideshige Takada, a geo-

chemist at Tokyo University of Agriculture andTechnology in Japan, was already analyzing thechemical composition of plastic resin pelletsthat a colleague had noticed on beaches inTokyo Bay. These 3-millimeter-wide granulesare the raw materials for commercial plasticproducts, and they are ubiquitous on shores

worldwide. Takada’s laboratory discoveredthat they contained organic pollutants such asdioxins, polychlorinated biphenyls (PCBs), anddichlorodiphenyltrichloroethane, at one milliontimes their concentrations in sea water (10).These hydrophobic contaminants have a highaffinity for the water-free environment foundbetween the long carbon chains that make upplastics, so the pellets mop up the chemicals asthey sail across the ocean.More recently, Chelsea Rochman, a post-

doctoral fellow in the aquatic health programat the University of California, Davis, mea-sured the amounts of PCBs and polycy-clic aromatic hydrocarbons (also persistentpollutants) that were absorbed or adsorbedby the five most common types of mass-produced plastic. Rochman deployed plasticsamples at five locations in the San Diego Bayfor up to 12 months, and found that poly-ethylene and polypropylene—the most widelyproduced and consumed plastics—could ac-cumulate roughly 10 times more of the pol-lutants than other types of microplastic (11).These sponge-like properties make the

widespread distribution of microplastic es-pecially concerning, researchers say. The par-ticles have been found in pretty much everyocean habitat from the tropics to the Arctic,and there is strong evidence for their long-term bioaccumulation in organisms. Takadaand his colleagues studied sea birds calledshort-tailed shearwaters (Puffinus tenuir-ostris) that had ingested microplastic loadedwith flame-retardant chemicals called poly-brominated diphenyl ethers (PDBEs), anddetected the pollutant in the birds’ adiposetissue (12). Rochman has found that pelagicfish—those that live between the shore and thesea floor—are more contaminated withPBDEs if they live in areas of greater plasticdensity (13). This finding suggests thatthe plastic noticeably contributed to theanimals’ PBDE levels.It’s not just the chemicals hidden inside

microplastic that can bioaccumulate. In somecases, the particles themselves find their wayfrom the gut into internal cells and tissues.Browne and his colleagues published the firststudy to show this. He collected mussels(Mytilus edulis) from the seaside in Cornwall,United Kingdom, and placed them into tankscontaining fluorescently labeled polystyrenemicrospheres. The particles quickly accumu-lated in the bivalves’ guts and then migratedto the circulatory system, where they per-sisted for more than 48 days (14). “This wasa game-changer, because up until that pointeveryone thought that these particles wouldbe ingested and then go right out the otherside,” says Browne.

This bioaccumulation has also been seenin wild bivalves. Last year, Belgian researchersstudying seafood from German farms andFrench supermarkets found that an aver-age portion of mussels contained about 90microplastic particles, and an order of oysterswould contain about 50 particles (15). How-ever, Reinhardt Saborowski, an ecologist atthe Helmholtz Center for Polar and MarineResearch in Bremerhaven, Germany, pointsout that this does not necessarily mean thatthe creatures are harmed by their plasticpassengers. Organisms are likely to respondto microplastic in different ways, he says,depending on their size, whether they feedselectively or not, and how easily substancespass from the digestive tract to other parts ofthe body. For example, Saborowski’s teamfound that a tiny marine isopod called Idoteaemarginata has a gut anatomy that preventsparticles from accumulating, which limitssome of the adverse effects that microplasticingestion could have, including clogged di-gestive organs and reduced appetite (16).Indeed, only a handful of studies have

found evidence of physiological, chemical, orother negative responses to microplastic in-gestion. In one, Browne’s group focused onlugworms (Arenicola marina), which live insediments on the shores of the United Statesand Europe and are eaten by many birds andfish. Browne reared the lugworms in sand

Microplastic particles (yellow) can cross fromthe digestive system into the blood cells (green)of mussels. Image courtesy of Mark Browne(University of New South Wales, Australia).

A surface trawl in the middle of the SouthAtlantic Gyre picks up plankton, shells, andbits of plastic. Image courtesy of Stiv Wilson(The Story of Stuff Project).

5548 | www.pnas.org/cgi/doi/10.1073/pnas.1504135112 Katsnelson

containing 5% microplastic (from polyvinylchloride), a rough estimation of naturallevels (although determining natural lev-els with any consistency has been difficult,Browne notes). That contamination alonereduced the worms’ capacity to deal withoxidative stress (which commonly occurs forthese organisms when the tide is out ona warm day) and led to an increase of hy-drogen peroxide in their tissues. Some of themicroplastic was contaminated with twochemical pollutants—nonylphenol and phen-anthrene—that are commonly found in oceanwater, as well as additives such as the anti-microbial agent triclosan. The organisms didn’tfare well: nonylphenol reduced their ability tofend off pathogenic bacteria by 60%. Triclo-san raised their mortality by more than 55%;it also reduced their ability to feed and en-gineer sediments, which helps maintain thediversity of tidal flats (17).In a complementary study from Thomp-

son’s laboratory, lugworms raised in sedimentcontaining 5% polyvinyl chloride ate less,showed increased inflammation, and alsosuffered a 50% drop in energy reserves, asmeasured by levels of carbohydrates, proteins,and fats in their bodies (18). And ongoingwork from Rochman’s laboratory found thatwhen a fish called the Japanese medaka(Oryzias latipes) was fed environmentally rel-evant levels of polyethylene marine debris,it experienced liver stress and signs of en-docrine disruption (19).Browne’s mussel study also found that

smaller microplastic particles transferred fromthe gut and bioaccumulated in other tissuesmore quickly than larger particles. He andothers believe that nano-scale particles couldcause even more harm, but the idea is diffi-cult to test because researchers do not yethave the tools to routinely sample micro-plastic smaller than 50 micrometers across,says Kara Lavender Law, research professorof oceanography at the Sea Education As-sociation in Woods Hole, Massachusetts.

A Pressing Issue?These studies come with a major caveat: al-most all of them were done in the laboratoryand it is not clear how well they reflect pro-cesses occurring in the wild. Persistent organicpollutants and other chemicals are alreadypresent in the marine environment, and it ishard to say how much additional harm a gulpof microplastics might cause. Plastic is veryvisible, says Christopher Reddy, a chemicaloceanographer at the Woods Hole Oceano-graphic Institution in Woods Hole, Massa-chusetts, so it gets a lot of attention. But otherenvironmental issues—carbon dioxide emis-sions, for example, or coastal erosion—are

significantly more problematic. “These arebig, pressing issues that are going to changeeconomies and change societies,” Reddy says.And at a chemical level, an organism’s

intake of toxic substances from microplasticmay be dwarfed by the inputs from its foodand water, according to modeling studiesby Bart Koelmans, an aquatic ecologist andchemist at Wageningen University in TheNetherlands (20, 21). Koelmans’s model pre-dicts the fate of different pollutants ingestedin food, water, and plastic particles, based

“This is only the start ofthinking about the problemin a rigorous way,” saysKara Lavender Law.

on factors such as the pollutants’ solubilityand the organisms’ digestion. Small ani-mals like marine worms are especially un-likely to absorb significant amounts ofchemicals because they probably retainmicroplastic in their guts for relatively shortperiods of time, the model suggests. And ifthe animal already has high levels of con-taminants in its system, the chemicals, inprinciple, could even be absorbed in theopposite direction—from the body to themicroplastic—which might produce a cleans-ing effect, says Koelmans.Modeling studies such as these have their

own limitations, though. It is not clear thatmodeling is any more accurate than labora-tory experiments in determining how theconcentrated presence of these chemicals in

microplastic affects organisms in nature, saysRochman. And Koelmans’s model does notreflect the impact of stress or inflammationcaused by microplastic ingestion. “This isa chemical model, but of course there is alsobiology,” he says.Ultimately, researchers agree that there are

still too many unknowns to fully assess theenvironmental damage caused by microplastic.However, a host of new studies, many ofwhich are moving from the laboratory tothe field, should fill in these gaps. Rochmanis expanding her work on how chemicaltransfer varies by plastic type and how bio-accumulation moves up the food chain. Agroup led by Robert Hale at the VirginiaInstitute of Marine Science in GloucesterPoint is gearing up to take a closer look atleaching from different types of plastic un-der a wide range of conditions.Meanwhile, Takada hopes to expand his

group’s work on short-tailed shearwaters toother animals, such as turtles and seals.Linda Amaral Zettler at the Marine Bio-logical Laboratory is studying how plasticsbreak down in the ocean, and hopes todiscover what role microbes play in the pro-cess. And Browne’s team recently embarkedon a study that will look beyond physiologyand assess the impacts of microplastic pollu-tion in the food web.Despite the warning signs that researchers

have already found, it may be many yearsbefore the microplastic pollution puzzle issolved. “This is only the start of thinking aboutthe problem in a rigorous way,” says Law.

1 Browne MA, et al. (2011) Accumulation of microplastic onshorelines woldwide: Sources and sinks. Environ Sci Technol 45(21):9175–9179.2 Secretariat of the Convention on Biological Diversity and the Scientificand Technical Advisory Panel—GEF (2012). Impacts of Marine Debris onBiodiversity: Current Status and Potential Solutions (Secretariat of theConvention on Biological Diversity, Montreal), Technical Series No. 67.3 Jambeck JR, et al. (2015) Marine pollution. Plastic waste inputsfrom land into the ocean. Science 347(6223):768–771.4 Eriksen M, et al. (2014) Plastic pollution in the world’s oceans:More than 5 trillion plastic pieces weighing over 250,000 tons afloatat sea. PLoS ONE 9(12):e111913.5 Law KL, et al. (2014) Distribution of surface plastic debris in theeastern Pacific Ocean from an 11-year data set. Environ Sci Technol48(9):4732–4738.6 Cózar A, et al. (2014) Plastic debris in the open ocean. Proc NatlAcad Sci USA 111(28):10239–10244.7 Woodall LC, et al. (2014) The deep sea is a major sink formicroplastic debris. R Soc Open Sci 1:140317.8 Carpenter EJ, Smith KL, Jr (1972) Plastics on the Sargasso seasurface. Science 175(4027):1240–1241.9 Thompson RC, et al. (2004) Lost at sea: Where is all the plastic?Science 304(5672):838.10 Takada S (2013) International Pellet Watch studies of the magnitudeand spatial variation of chemical risks associated with environmentalplastics. From Accumulation: The Material Politics of Plastic, edsGabrys J, et al. (Routledge, New York).11 Rochman CM, Hoh E, Hentschel BT, Kaye S (2013) Long-termfield measurement of sorption of organic contaminants to five typesof plastic pellets: Implications for plastic marine debris. Environ SciTechnol 47(3):1646–1654.

12 Tanaka K, et al. (2013) Accumulation of plastic-derived chemicalsin tissues of seabirds ingesting marine plastics. Mar Pollut Bull69(1-2):219–222.13 Rochman CM, et al. (2014) Polybrominated diphenyl ethers(PBDEs) in fish tissue may be an indicator of plastic contamination inmarine habitats. Sci Total Environ 476-477:622–633.14 Browne MA, Dissanayake A, Galloway TS, Lowe DM,Thompson RC (2008) Ingested microscopic plastic translocates tothe circulatory system of the mussel, Mytilus edulis (L). Environ SciTechnol 42(13):5026–5031.15 Van Cauwenberghe L, Janssen CR (2014) Microplastics in bivalvescultured for human consumption. Environ Pollut 193:65–70.16 Hämer J, Gutow L, Köhler A, Saborowski R (2014) Fate ofmicroplastics in the marine isopod Idotea emarginata. Environ SciTechnol 48(22):13451–13458.17 Browne MA, Niven SJ, Galloway TS, Rowland SJ, Thompson RC(2013) Microplastic moves pollutants and additives to worms, reducingfunctions linked to health and biodiversity. Curr Biol 23(23):2388–2392.18 Wright SL, Rowe D, Thompson RC, Galloway TS (2013)Microplastic ingestion decreases energy reserves in marine worms.Curr Biol 23(23):R1031–R1033.19 Rochman CM, Kurobe T, Flores I, Teh SJ (2014) Early warning signsof endocrine disruption in adult fish from the ingestion of polyethylenewith and without sorbed chemical pollutants from the marineenvironment. Sci Total Environ 493:656–661.20 Koelmans AA, Besseling E, Wegner A, Foekema EM (2013) Plasticas a carrier of POPs to aquatic organisms: A model analysis. EnvironSci Technol 47(14):7812–7820.21 Gouin T, Roche N, Lohmann R, Hodges G (2011) A thermodynamicapproach for assessing the environmental exposure of chemicalsabsorbed to microplastic. Environ Sci Technol 45(4):1466–1472.

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