7
Published: January 26, 2011 r2011 American Chemical Society 1466 dx.doi.org/10.1021/es1032025 | Environ. Sci. Technol. 2011, 45, 14661472 ARTICLE pubs.acs.org/est A Thermodynamic Approach for Assessing the Environmental Exposure of Chemicals Absorbed to Microplastic Todd Gouin,* ,Nicola Roche, Rainer Lohmann, and GeoHodges Safety and Environmental Assurance Centre, Unilever, Colworth Science Park, Sharnbrook, Bedfordshire, U.K., MK44 1LQ Graduate School of Oceanography, University of Rhode Island, South Ferry Road, Narragansett, Rhode Island, 02882 United States b S Supporting Information ABSTRACT: The environmental distribution and fate of micro- plastic in the marine environment represents a potential cause of concern. One aspect is the inuence that microplastic may have on enhancing the transport and bioavailability of persistent, bioaccu- mulative, and toxic substances (PBT). In this study we assess these potential risks using a thermodynamic approach, aiming to prioritize the physicochemical properties of chemicals that are most likely absorbed by microplastic and therefore ingested by biota. Using a multimedia modeling approach, we dene a chemical space aimed at improving our understanding of how chemicals partition in the marine environment with varying volume ratios of air/water/organic carbon/polyethylene, where polyethylene represents a main group of microplastic. Results suggest that chemicals with log K OW > 5 have the potential to partition >1% to polyethylene. Food-web model results suggest that reductions in body burden concentrations for nonpolar organic chemicals are likely to occur for chemicals with log K OW between 5.5 and 6.5. Thus the relative importance of microplastic as a vector of PBT substances to biological organisms is likely of limited importance, relative to other exposure pathways. Nevertheless, a number of data-gaps are identied, largely associated with improving our understanding of the physical fate of microplastic in the environment. INTRODUCTION Societal demand for plastic material continues to increase, with global plastic manufacture and consumption estimated to be 308 million tonnes annually. 1 It is notable that approximately 50% of all plastic used is for single-use disposable applications. 2 In Europe, a combination of plastic recovery programs, including mechanical recycling, feedstock recycling, and energy recovery (i. e., combustion of waste for energy generation) have resulted in a recovery rate of only 39% of plastic waste generated in 2003. 2 Relatively poor plastic recovery rates, combined with inappropri- ate disposal of plastic products, is thus a signicant factor inuencing the potential for plastic debris to enter the environment. 3,4 Unfortunately, there is a paucity of data quanti- tatively assessing the release rates of plastic to the terrestrial and aquatic environments. Nevertheless, based on a number of semiquantitative and/or qualitative assessments, the observation of plastic debris and its temporal and spatial accumulation, particu- larly in the marine environment, imply cause for concern. 3-11 Whereas a number of studies report the eects of macro- plastic (>5 mm) on the marine environment (see for instance refs 3 and 12), concerns regarding the potential eects of microplastic (<5 mm) have only recently emerged. 3,13-17 Emis- sions of microplastic to the global marine environment include both primary sources (as derived from hand and facial cleansers, cosmetic preparations, airblast cleaning media, and production waste from plastic processing plants) and secondary sources (derived from fragmentation of macro-plastic as a result of photodegradation and abrasion due to wave action). 3,4,18,19 Based on observations that the amount of macro-plastic accu- mulating in the marine environment is rapidly increasing, 3 it is reasonable to expect that secondary sources of microplastic will dominate its environmental occurrence. 4 Nevertheless, several studies note that while primary sources of microplastic represent a relatively insignicant contribution to the microplastic litter present in the marine environment, the lack of understanding regarding its environmental fate and behavior in the global oceans warrants caution with respect to its use, while a quantitative under- standing regarding the potential risks is evaluated. 18-20 For in- stance, a number of hazards have been identied relating to the potential impact that microplastic derived from primary sources may have on the oceanic environment. Foremost among these is the potential for microplastic to act as a vector for persistent, bioaccumulative, and toxic substances (PBT). 21 Consequently, given the lack of understanding regarding the environmental fate and ecotoxicological eects of microplastic, either derived from Received: September 20, 2010 Accepted: January 11, 2011 Revised: January 10, 2011

A Thermodynamic Approach for Assessing the Environmental ...web.uri.edu/lohmannlab/files/Gouin-et-al-Microplastic-EST11.pdf · A Thermodynamic Approach for Assessing the Environmental

  • Upload
    lykhanh

  • View
    214

  • Download
    0

Embed Size (px)

Citation preview

Published: January 26, 2011

r 2011 American Chemical Society 1466 dx.doi.org/10.1021/es1032025 | Environ. Sci. Technol. 2011, 45, 1466–1472

ARTICLE

pubs.acs.org/est

A Thermodynamic Approach for Assessing the EnvironmentalExposure of Chemicals Absorbed to MicroplasticTodd Gouin,*,† Nicola Roche,† Rainer Lohmann,‡ and Geoff Hodges†

†Safety and Environmental Assurance Centre, Unilever, Colworth Science Park, Sharnbrook, Bedfordshire, U.K., MK44 1LQ‡Graduate School of Oceanography, University of Rhode Island, South Ferry Road, Narragansett, Rhode Island, 02882 United States

bS Supporting Information

ABSTRACT: The environmental distribution and fate of micro-plastic in the marine environment represents a potential cause ofconcern. One aspect is the influence thatmicroplastic may have onenhancing the transport and bioavailability of persistent, bioaccu-mulative, and toxic substances (PBT). In this study we assess thesepotential risks using a thermodynamic approach, aiming toprioritize the physicochemical properties of chemicals that aremost likely absorbed by microplastic and therefore ingested bybiota. Using a multimedia modeling approach, we define achemical space aimed at improving our understanding of howchemicals partition in the marine environment with varyingvolume ratios of air/water/organic carbon/polyethylene, wherepolyethylene represents amain group ofmicroplastic. Results suggest that chemicals with logKOW>5have the potential to partition >1%to polyethylene. Food-webmodel results suggest that reductions in body burden concentrations for nonpolar organic chemicals are likelyto occur for chemicals with log KOW between 5.5 and 6.5. Thus the relative importance of microplastic as a vector of PBT substances tobiological organisms is likely of limited importance, relative to other exposure pathways. Nevertheless, a number of data-gaps areidentified, largely associated with improving our understanding of the physical fate of microplastic in the environment.

’ INTRODUCTION

Societal demand for plastic material continues to increase,with global plastic manufacture and consumption estimated to be308 million tonnes annually.1 It is notable that approximately50% of all plastic used is for single-use disposable applications.2

In Europe, a combination of plastic recovery programs, includingmechanical recycling, feedstock recycling, and energy recovery (i.e., combustion of waste for energy generation) have resulted in arecovery rate of only 39% of plastic waste generated in 2003.2

Relatively poor plastic recovery rates, combined with inappropri-ate disposal of plastic products, is thus a significant factorinfluencing the potential for plastic debris to enter theenvironment.3,4 Unfortunately, there is a paucity of data quanti-tatively assessing the release rates of plastic to the terrestrial andaquatic environments. Nevertheless, based on a number ofsemiquantitative and/or qualitative assessments, the observationof plastic debris and its temporal and spatial accumulation, particu-larly in the marine environment, imply cause for concern.3-11

Whereas a number of studies report the effects of macro-plastic (>5 mm) on the marine environment (see for instancerefs 3 and 12), concerns regarding the potential effects ofmicroplastic (<5 mm) have only recently emerged.3,13-17 Emis-sions of microplastic to the global marine environment includeboth primary sources (as derived from hand and facial cleansers,cosmetic preparations, airblast cleaning media, and production

waste from plastic processing plants) and secondary sources(derived from fragmentation of macro-plastic as a result ofphotodegradation and abrasion due to wave action).3,4,18,19

Based on observations that the amount of macro-plastic accu-mulating in the marine environment is rapidly increasing,3 it isreasonable to expect that secondary sources of microplastic willdominate its environmental occurrence.4 Nevertheless, severalstudies note that while primary sources of microplastic representa relatively insignificant contribution to the microplastic litterpresent in the marine environment, the lack of understandingregarding its environmental fate and behavior in the global oceanswarrants caution with respect to its use, while a quantitative under-standing regarding the potential risks is evaluated.18-20 For in-stance, a number of hazards have been identified relating to thepotential impact that microplastic derived from primary sourcesmay have on the oceanic environment. Foremost among these isthe potential for microplastic to act as a vector for persistent,bioaccumulative, and toxic substances (PBT).21 Consequently,given the lack of understanding regarding the environmental fateand ecotoxicological effects of microplastic, either derived from

Received: September 20, 2010Accepted: January 11, 2011Revised: January 10, 2011

1467 dx.doi.org/10.1021/es1032025 |Environ. Sci. Technol. 2011, 45, 1466–1472

Environmental Science & Technology ARTICLE

primary or secondary sources, there is clearly a need to identifyappropriate scientific methods that might help quantify thepotential environmental risks associated with this material.

In this study we investigate the environmental risks associatedwith microplastic, with an emphasis on assessing the interactionof PBT substances with microplastic material in the environmentand its subsequent fate within a food-webmodel. This is achievedby first utilizing a thermodynamic approach that aims at assessingthe equilibrium distribution of chemicals with varying physi-cal-chemical properties within an illustrative model environ-ment. The model environment includes a sensitivity analysis thatconstrains the influence of varying volume ratios of air, water,sediment, and polyethylene microplastic on partitioning beha-vior. Second, the study aims at predicting how consumption ofmicroplastic by aquatic organisms, using a steady-state food-webmodel, might influence body-burden concentrations, with anemphasis on exploring which model parameters influence anincrease or a decrease in body-burden levels as compared to a dietthat does not include microplastic. Results from the largelythermodynamic approaches used in this study are then used torecommend how research might be directed to better addresspriority data gaps.

’METHODS

Equilibrium Partitioning. It is well understood that plasticpolymers, such as polyethylene, have the capacity to absorbhydrophobic organic chemicals (HOCs), which has resulted insuggestions for their use as passive samplers.22-25 Additionally,the mechanisms that influence sorption and desorption willdepend on both the sorbent and sorbate properties.17 Conse-quently, developing methods to assess the kinetics of sorption/desorption and equilibrium partitioning to plastic polymericmaterial that may be emitted to the environment is essentialfor improving our understanding of how HOCs of concern mayinteract with marine microplastic litter. It is suggested thatsignificant insight regarding these processes can be obtainedfrom observations related to the calibration of plastic polymericmaterial used for passive samplers, such as the use of performancereference compounds (PRC) to assist in understanding thekinetics of sorption/desorption and the time required for thepassive sampler to reach equilibrium.26,27 As a first screen foridentifying the relative importance of how organic contaminantsmay interact with primary sources of microplastic, we haveutilized a multimedia modeling approach, based on fugacity.28

The multimedia unit world environment has been selected torepresent a coastal marine system with dimensions consistentwith the marine environment of the Northwestern HawaiianIslands (360 000 km2), where it has been estimated that 50tonnes of plastic debris are accumulating annually.29 In thismodel system the water column depth is 10 m, the sedimentdepth is 10 cm, and the height of the atmosphere is 1 km.Additionally, an open ocean environment is also modeled, usinga similar area but assuming a water depth of 20 m and nosediment compartment. As an illustrative example, we haveassumed a minimum volume of plastic of 55 m3, based on theobservations of Dameron et al.29 This volume assumes that thedensity of plastic is approximately 0.9 g 3 cm

-3, consistent withthe density of low density polyethylene. If we further assume thatthis plastic material has the potential to accumulate, consistentwith observations of the accumulation of microplastic in thewaters between Iceland and the British Isles prior to the 1990s,10

we can investigate how changes in volume ratios between waterand plastic influence the partitioning of HOCs. For instance, arecent study reports that the maximum mass of plastic debris inthe North Atlantic Subtropical Gyre is approximately 1100tonnes,30 or about 1200 m3.To give context with respect to the amount of primary

microplastic emitted to the aquatic environment, based on theusage of polyethylene microplastic beads used in personal careproducts, we estimate that the per capita consumption of micro-plastic used in personal care products for the U.S. population isapproximately 2.4mg 3 person

-13 d

-1 (Supporting Information).The U.S. population is thus emitting 263 tonnes 3 yr

-1 polyethy-lene microplastic. This amount represents approximately 25% ofthe mass of plastic estimated to be present in the North AtlanticSubtropical Gyre.30 Given the wide dispersive use of microplasticused in personal care products across the U.S., it is thus believedthat the volumes of plastic used in the illustrative multimediamodel of 55 and 1200 m3 are representative of both ambient andworst-case scenarios, respectively.Chemical Space Diagrams. We propose that a key compo-

nent of understanding how chemicals might interact in themodelenvironment described above is to discharge a suite of hypothe-tical HOCs with varying partitioning properties to an environ-ment in which thermodynamic equilibrium between media isassumed, and there are no advective losses. This is essentially aLevel I model, as described by Mackay.28 Using a graphicalapproach, analogous to Gouin et al.,31 we can estimate the massof organic carbon (MOC) to which HOCs will absorb based ontheir relationship with the organic carbon to water partitioncoefficient (KOC), which has units of L 3 kg

-1, as

MOC ¼FVsedj ð1Þwhere j is the fraction of organic carbon in the sediment (0.04),and F is the sediment density (2400 kg 3m

-3).At equilibrium the total mass of chemical (M) will be

distributed as

M ¼VWCW þVACA þVPECPE þMOCCOC

¼CWðVW þKAWVA þKPE - WVPE þMOCKOCÞ ð2Þwhere V is volume (m3), C is concentration (g 3m

-3), KAW is theair-water partition coefficient, KPE-W is the polyethylene-waterpartition coefficient, and the subscripts A,W, PE, andOC refer toair, water, polyethylene, and organic carbon, respectively.31 Themass fractions of the chemical in a particular medium (F) canthus be described as

Fi ¼ViKiW=ðKWWVW þKAWVA þKPE - WVPE þMOCKOCÞ ð3Þwhere i represents A, W, or PE, and KWW is 1.0.31 The fraction inorganic carbon is described as

FOC ¼MOCKOC=ðKWWVW þKAWVA þKPE - WVPE þMOCKOCÞð4Þ

Consequently a plot of the mass fraction versus KOC or KPE-W

and KAW that considers the volume ratios of air, water, andorganic carbon or polyethylene can be created to illustrate howchemicals might partition in the hypothetical marine environ-ments described.Food Web Model. Visualization of the interactions between

PBT substances and various types of environmental media usingthe graphical approach described above is helpful as a screening

1468 dx.doi.org/10.1021/es1032025 |Environ. Sci. Technol. 2011, 45, 1466–1472

Environmental Science & Technology ARTICLE

tool to prioritize the properties of substances that have thegreatest potential for sorption to microplastic. Prioritizing theproperties of chemicals thus allows us to assess the fate andbehavior of chemicals absorbed to microplastic within an organ-ism and associated food-chain, with an emphasis on assessing themovement of chemicals from the plastic and across the walls ofthe gastrointestinal (GI) tract of an organism. To mimic howchemical substances that absorb to microplastic behave in a food-web, we have utilized the bioaccumulation food-web modeldescribed by Arnot and Gobas,32 which is freely available fromthe Trent University Centre for Environmental Modeling andChemistry (CEMC) (http://www.trentu.ca/academic/aminss/envmodel) as the CEMC SFU AGRO model. It is notable thatonly the steady-state food-web component of the model has beenutilized, i.e., the water quality model component has not beenused, except to define a steady-state water concentration. Thefood-web includes several trophic levels, ranging from phyto-plankton, zooplankton, benthos, forage fish, and a piscivorousfish. In the interest of brevity, discussion of model results willfocus on the top predator organism (i.e., the piscivorous fish).The feeding matrix and input parameters for each of theorganisms are given in the Supporting Information.The food web model has been modified to include a poly-

ethylene microplastic component of an organisms’ diet. Themicroplastic is modeled as an additional organism, which is asphere with a diameter of 250 μm (8.2� 10-6 cm3) and assumesthat the polyethylene is equivalent to a 100% nonlipid organicmatter (NLOM) fraction.The uptake of chemicals in the model is based on a partition-

ing process between biota and water (KBW):

KBW ¼vLBKOW þKOWvNBβþ vWB ð5Þwhere vLB, vNB, and vWB represent the lipid, NLOM, and waterfractions of an organism, and β represents the sorption capacityof NLOM relative to octanol. Arnot and Gobas 32 suggest a valuefor β of 0.035 for biological organisms, which implies that thesorption affinity of NLOM is 3.5% of octanol. In the case ofplastics, we have assumed that the sorption capacity of theNLOM is 100% that of octanol. This is a conservative estimatebased on results reported in a number of recent studies thatdemonstrate a linear relationship between KOW and KPE-W forHOCs.22,33 We note that for PBTs with polar functional groups,KPE-W will be well below KOW,

22 we thus overestimate theimportance of microplastic as a vector for biological uptake forthese substances.Dietary assimilation efficiencies of lipid and NLOM are

described in the model for zooplankton and aquatic invertebratesas being 72% and 75%, respectively.32 Whereas fish assimilationsof lipid andNLOM are defined as 92% and 55%, respectively.32 Itis notable that dietary assimilation efficiency describes theefficiency of the organism to digest lipid and NLOM. Thisparameter thus influences the uptake of chemical across thegastrointestinal tract by defining the fraction of chemical sorbedto lipid or NLOM that will be available for uptake. Uptake intothe organism is described as a partitioning process, whereby apartition coefficient between the gastrointestinal tract and organ-ism (KGW) is defined as

KGW ¼ðvLGKOW þKOWvNGβþ vWGÞ=KBW ð6Þwhere vLB, vNB, and vWB represent the lipid, NLOM, and waterfractions of the gut contents of an organism, respectively.32 Thus,

the results of the food-webmodel describe the uptake of chemicalacross the GI tract as a steady-state process, which therefore doesnot consider the kinetics of desorption of chemicals from theplastic. Kinetic factors that likely influence this process will berelated to the gut retention time of the organism and theextraction efficiency of the gastrointestinal fluids for polyethyleneplastic. A more sophisticated dynamic model would thus berequired to directly assess desorption of chemicals from theplastic and uptake across the GI tract, with respect to time.Consequently, the model used in this study is limited to assessingthe relative importance of exposure to chemicals from the naturaldiet versus digestion of plastic debris, and to identify potentialdata-gaps in our understanding using a steady-state food-webmodel.To directly assess the influence of adding microplastic to the

Arnot and Gobas32 bioaccumulation food-web model, we havemodeled a suite of hypothetical organic chemicals with varyingpartition coefficients of one log unit of between 1 and 8 for logKOW, and-4 and 2 for log KAW. All chemicals are assumed to beperfectly persistent. The microplastic is assumed to be buoyant,and therefore resides in the water column, where it absorbschemicals, based on their log KOW, and is then consumed byorganisms at a rate of 10% of an organisms’ diet. Differences inthe chemical concentration for each of the organisms in the food-web with and without plastic are then derived as an estimate ofthe relative influence that inclusion of microplastic in an organ-isms’ diet may have on the bioaccumulation potential of anHOC.

Figure 1. Plot of the mass fraction versus log KAW and log KOC, andillustrating the distribution of 26 chemicals for which measured log KOC

data are available (stars). Also illustrated are regions representing FA(blue), FW (green), and FOC (brown), where chemicals will partition>99%. The lines represent 33% partitioning to air (blue), water (green),and organic carbon (brown). The dimensions of themodel environmentused in calculating the distributions are representative of the coastalenvironment, which includes 55 m3 of polyethylene and 6.91 � 108 m3

of organic carbon (Supporting Information).

1469 dx.doi.org/10.1021/es1032025 |Environ. Sci. Technol. 2011, 45, 1466–1472

Environmental Science & Technology ARTICLE

’RESULTS AND DISCUSSION

Equilibrium Partitioning and Chemical Space Diagrams.The volume ratio of air/water/organic carbon/polyethylene forthe marine coastal environment is 6.6� 1012:6.55� 1010:1.26�107:1. Figure 1 is a plot of the mass fraction versus log KAW andlogKOC, which graphically illustrates the equilibrium partitioningspace of a number of environmentally relevant chemicals forwhich measured KOC

34 data are available, within the marinecoastal environment defined in this study (Supporting In-formation). Only those substances with log KOC > 5.5 are likelyto partition significantly (>99%) to organic carbon. Based on thevolume ratios between organic carbon and polyethylene in thissystem, in which the organic carbon present in the system is1.26� 107 times greater than the polyethylene, it is reasonable toexpect that the majority of partitioning in this system will be tothe organic carbon fraction. Indeed, the results shown in Figure 1

do not include polyethylene because partitioning to polyethylenein this system is <0.1%, even for substances with log KPE-W > 7.Figure 2a illustrates the equilibrium partitioning of 32 chemi-

cals, for which measured KPE-W values are available,22,33 in anopen-ocean environment with an air/water/polyethylene ratio of3 � 1011:6.0 � 109:1 (i.e., volume of polyethylene = 1200 m3).Results shown in Figure 2a suggest that, based on the relativelysmall volume of polyethylene in the environment, organicchemicals of environmental relevance partition between the airand water, with significant cycling between these two compart-ments. If we assume, however, that the amount of plastic in thissystem will continue to accumulate as a result of continuousdischarge, then it is possible that the volume of plastic willincrease to a level where a significant fraction of chemical maypartition into it. Figure 2b illustrates the equilibrium partitioningin an open-ocean environment where the volume of plastic hasincreased by 3 orders of magnitude (i.e., 106 m3). In this systemwe begin to observe that substances with log KPE-W > 5 will nowhave the potential to partition >1% to polyethylene. Thus in asystem where there are large quantities of plastic, and limitednatural organic matter, significant partitioning of bioaccumula-tive HOCs into polyethylene plastic will occur. It is notable thatthis observation assumes that the presence of organic matter inthe water, such as phytoplankton, is negligible. Where popula-tions of phytoplankton are elevated, however, increased parti-tioning to the phytoplankton will likely occur, consistent withobservations of Dachs et al.,35 and thus the relative partitioning ofHOCs to polyethylene will decrease accordingly.The results in Figures 1 and 2 effectively illustrate the output of

a sensitivity analysis, which highlights the relative importance ofthe volume ratios between air, water, naturally occurring organiccarbon, and polyethylene plastic with respect to how the par-titioning behavior of chemicals will change with varying volumeratios. The results clearly imply that increasing quantities of plasticwillresult in competition for the sorption of hydrophobic substances to

Figure 2. Plot of the mass fraction versus log KAW and log KPE-W, and illustrating the distribution of 32 chemicals for which measured log KPE-W areavailable (squares). Also illustrated are regions representing FA (blue), FW (green), and FPE-W (brown), where chemicals will partition >99%. The linesrepresent 33% partitioning to air (blue), water (green), and polyethylene (brown). Part (a) represents an open ocean environment with 1200 m3 ofpolyethylene and (b) represents an open ocean environment with 106 m3 of polyethylene.

Figure 3. CEMC SFU Agro food-model results for reductions to bodyburden mass for a piscivorous fish consuming 10% microplastic. Theencircled areas represent the relative positions of polychlorinatedbiphenyls (PCBs) and polycyclic aromatic hydrocarbons (PAHs).

1470 dx.doi.org/10.1021/es1032025 |Environ. Sci. Technol. 2011, 45, 1466–1472

Environmental Science & Technology ARTICLE

naturally occurring organic carbon.Thus quantifying the amounts ofplastic in the environment is needed to improve our understandingof the relative importance of this process. It is notable that sincethis is an equilibrium partitioning approach, the size of the plasticdoes not influence the results illustrated. Thus the results relateto both macro- and microplastic material. The time to equilib-rium, however, will differ depending on the size of the material,with microplastic reaching equilibrium sooner thanmacroplastic.It has been suggested that substances absorbed into plastic

as a result of their partitioning behavior may be transported inthe environment from source regions and may cause a negativeimpact on remote environments. Zarfl et al.36 have assessed therelative importance of this transport mechanism to the ArcticOcean. Their results, however, suggest that this transport process, ascompared with the transport of pollutants via atmospheric andoceanic currents, is orders of magnitude smaller.36 Thus, themovement of plastic is not likely to be a significant vector fortransporting HOCs from source to remote regions.Nevertheless, Zarfl et al.36 imply that it may be possible that

highly hydrophobic organic chemicals (for instance log KOW>6.5), which typically partition strongly to sediment, and thereforehave limited transport potential, may have enhanced mobility ifabsorbed to buoyant microplastic material. Thus, concern re-garding the relative importance of microplastic as a vector forPBT substances remains, particularly given the suggestion that anorganism that consumes microplastic material, to which HOChave absorbed, can result in enhanced uptake by the organism.16

Results illustrated in Figures 1 and 2 thus suggest that thepotential for enhanced biological uptake, as a result of consumingmicroplastic, will likely be limited to chemicals with logKOC/LogKPE-W > 6.5, since these are the substances that have higherpotential for partitioning to polyethylene plastic, and thus willhave the greatest potential to cause a detrimental effect. It isnotable, however, that gastrointestinal absorption efficiency ofHOCs decreases beginning at about log KOW > 5.5.32,37 Thusassessing an organisms’ potential to extract highly HOCs ofenvironmental concern, absorbed to microplastic, will be com-plicated by a number of competing processes, which are exploredin greater detail below.SimulatingBiologicalUptakeandBioaccumulation. Figure 3

illustrates the chemical space related to reductions in body

burden concentrations associated with a piscivorous fish thatincludes a 10% microplastic component of its diet. The bioaccu-mulation of chemicals is shown to decline, with chemicals havinglog KOW of between about 6.5 and 7.5 showing >20% reductionin body burden concentrations as a consequence of including10% microplastic in the diet. Reductions in body burden con-centrations are also observed to increase as the amount ofmicroplastic in the diet increases.The observation of reductions in body burden concentrations

is due to the high sorption affinity assumed for polyethylene,which results in a fugacity gradient within the GI gut that doesnot favor transfer to the organism. For instance, organic matterthat is degraded in the GI gut results in contaminant concentra-tions increase per mass of organic carbon, thus there is anincrease in fugacity that favors transfer to the organism, ifpolyethylene is absent. If polyethylene is present in the GI gut,however, which is assumed to be nondegradable, then thefugacity increase will be less due to the sorption affinity of theplastic. Consequently, a reduced body burden concentration canbe realized. This hypothesis is consistent with other studies thathave demonstrated limited absorption efficiency related to theconsumption of nondigestable material.38 Moser and McLach-lan,38 for instance, observed that consumption of nondigestablefats, such as olestra, could be an efficient process for reducingchemical body burdens. Thus, the role of microplastic as a vectorfor enhanced biological exposure of PBT substances appears tobe of limited importance.Nevertheless, we further assess the potential for an increase in

body burden concentrations by performing a sensitivity analysison various input parameters defined in the food-web model.Figure 4 illustrates the results with respect to changing the dietaryassimilation efficiency of NLOMand the percent lipid in prey fishconsumed by the piscivorous fish.Figure 4 illustrates that decreases in body burden mass are less

pronounced in piscivorous fish that consumes microplastic alongwith prey with relatively low lipid content (1%) and which has anincreasing potential to digest NLOM. This observation appearsto be consistent with the hypothesis described earlier, in whichthe fugacity of a chemical within the GI gut of the organism canvary depending on the relative fractions of lipid and NLOMpresent in the system. Variability in the potential for the organism

Figure 4. Sensitivity analysis of dietary assimilation efficiency of NLOM and lipid content of forage fish defined in the CEMC SFU Agro food-model,with respect to changes in body burden concentrations of perfectly persistent hypothetical chemicals with varying partitioning properties.

1471 dx.doi.org/10.1021/es1032025 |Environ. Sci. Technol. 2011, 45, 1466–1472

Environmental Science & Technology ARTICLE

to digest NLOM relative to lipid will thus further influence thefugacity of the chemical in the GI gut, and consequently thetransfer of chemical to the organism. Consequently, the design ofan experiment aimed at assessing the role of ingested micro-plastic as a vector for exposure to PBT substances needs to con-sider not only the kinetics related to the digestion efficiency of theplastic (such as gut residence time and gut extraction efficiency),but also the influence of the natural diet.It is of interest to note that increasing the dietary assimilation

efficiency to 95% results in negligible differences in body burdenmass between an organism that consumes plastic and one thatdoes not (Figure 4). This is due to the increased capacity of theorganism to not only digest plastic polymeric material, but alsothe increased capacity to digest NLOMassociated with its naturaldiet. Clearly, caution is warranted with respect to this discussion,since the environmental relevance of an organism that is highlyefficient at digesting NLOM and which consumes a diet low inlipid content is likely limited.Addressing Limitations and Identifying Research Needs.

The theoretical approaches used in this study largely assumethermodynamic equilibrium. Consequently, there is a need to betterunderstand and assess the influence of kinetics with respect tosorption/desorption processes. For instance, what is the influ-ence of rubbery to glass transition of the plastic on the Fickiandiffusion of a chemical through the polymericmaterial? There aresome studies that have demonstrated that chemical diffusionthrough polyethylene decreases with increased crystallinity,39,40

however, further research regarding the relevance of this processas it pertains to sorption/desorption of environmentally relevantchemicals of concern is needed. Additionally, there is a need forimproving our understanding of how microbial biofouling influ-ences sorption/desorption processes. From observations basedon the use of PRC in passive samplers, for instance, it has beendemonstrated that biofouling can significantly influence uptakerates,41 thus improving our understanding of how this processinfluences both the fate of the plastics and chemicals sorbed tothe plastic and could enhance our ability to better assess therelative risk.Apart from the capacity for plastic debris to sorb chemicals of

concern, there is also a need to improve our understanding of thefate of the physical presence of the microplastic material inbiological organisms. Specifically, what are the gut retentiontimes and what fraction of microplastic consumed by an organ-ism moves across the epithelial tissue into the organism? Whatinfluence does the size and shape of the microplastic have withrespect to a toxicological response? Thus, while it appears thatthe role of microplastic as a vector for PBT substances may berelatively small when compared to other exposure pathways, itdoes appear that there are a number of data-gaps that need to beaddressed, particularly those quantifying the sources and sinks ofmicroplastic and an improved understanding of what the effectsof the physical presence of the material are on the environment.

’ASSOCIATED CONTENT

bS Supporting Information. Descriptions and calculationsof model dimensions and the volume of polyethylene used inpersonal care products, and tables summarizing input parametersused in the CEMC SFU Agro food-web model component. Thisinformation is available free of charge via the Internet at http://pubs.acs.org.

’AUTHOR INFORMATION

Corresponding Author*Tel.: þ44 1234264770; fax: þ44 1234 264744; e-mail: [email protected].

’ACKNOWLEDGMENT

Tom Hutchinson and Thomas Maes of CEFAS, StuartMarshall and Roger van Egmond of Unilever, and two anon-ymous reviewers are acknowledged for helpful discussions andcomments. Research was funded internally by Unilever throughits Science & Technology program.

’REFERENCES

(1) Andrady, A. L.; Neal, M. A. Applications and societal benefits ofplastics. Philos. Trans. R. Soc., B 2009, 364 (1526), 1977–1984.

(2) Hopewell, J.; Dvorak, R.; Kosior, E. Plastics recycling: challengesand opportunities. Philos. Trans. R. Soc., B 2009, 364 (1526), 2115–2126.

(3) Moore, C. J. Synthetic polymers in the marine environment: Arapidly increasing, long-term threat. Environ. Res. 2008, 108 (2), 131–139.

(4) Barnes, D. K. A.; Galgani, F.; Thompson, R. C.; Barlaz, M.Accumulation and fragmentation of plastic debris in global environ-ments. Philos. Trans. R. Soc., B 2009, 364 (1526), 1985–1998.

(5) Browne, M. A.; Galloway, T. S.; Thompson, R. C. SpatialPatterns of Plastic Debris along Estuarine Shorelines. Environ. Sci.Technol. 2010, 44 (9), 3404–3409.

(6) Corcoran, P. L.; Biesinger, M. C.; Grifi, M. Plastics and beaches:A degrading relationship. Mar. Pollut. Bull. 2009, 58 (1), 80–84.

(7) Goldberg, E. D. Plasticizing the seafloor: An overview. Environ.Technol. 1997, 18 (2), 195–201.

(8) Moore, S. L.; Gregorio, D.; Carreon, M.; Weisberg, S. B.;Leecaster, M. K. Composition and distribution of beach debris inOrange County, California. Mar. Pollut. Bull. 2001, 42 (3), 241–245.

(9) Provencher, J. F.; Gaston, A. J.; Mallory, M. L. Evidence forincreased ingestion of plastics by northern fulmars (Fulmarus glacialis) inthe Canadian Arctic. Mar. Pollut. Bull. 2009, 58 (7), 1092–1095.

(10) Thompson, R. C.; Olsen, Y.;Mitchell, R. P.; Davis, A.; Rowland,S. J.; John, A. W. G.; McGonigle, D.; Russell, A. E. Lost at Sea: Where IsAll the Plastic?. Science 2004, 304 (5672), 838.

(11) Watters, D. L.; Yoklavich, M. M.; Love, M. S.; Schroeder, D. M.Assessing marine debris in deep seafloor habitats off California. Mar.Pollut. Bull. 2010, 60 (1), 131–138.

(12) Gregory, M. R. Environmental implications of plastic debris inmarine settings-entanglement, ingestion, smothering, hangers-on, hitch-hiking and alien invasions. Philos. Trans. R. Soc., B 2009, 364 (1526),2013–2025.

(13) Browne, M. A.; Dissanayake, A.; Galloway, T. S.; Lowe, D. M.;Thompson, R. C. Ingested microscopic plastic translocates to thecirculatory system of the mussel,Mytilus edulis (L.). Environ. Sci. Technol.2008, 42 (13), 5026–5031.

(14) Graham, E. R.; Thompson, J. T. Deposit- and suspension-feeding sea cucumbers (Echinodermata) ingest plastic fragments. J. Exp.Mar. Biol. Ecol. 2009, 368 (1), 22–29.

(15) Mato, Y.; Isobe, T.; Takada, H.; Kanehiro, H.; Ohtake, C.;Kaminuma, T. Plastic resin pellets as a transport medium for toxicchemicals in the marine environment. Environ. Sci. Technol. 2001, 35 (2),318–324.

(16) Teuten, E. L.; Rowland, S. J.; Galloway, T. S.; Thompson, R. C.Potential for plastics to transport hydrophobic contaminants. Environ.Sci. Technol. 2007, 41 (22), 7759–7764.

(17) Teuten, E. L.; Saquing, J. M.; Knappe, D. R. U.; Barlaz, M. A.;Jonsson, S.; Bjorn, A.; Rowland, S. J.; Thompson, R. C.; Galloway, T. S.;Yamashita, R.; Ochi, D.; Watanuki, Y.; Moore, C.; Pham, H. V.; Tana,T. S.; Prudente, M.; Boonyatumanond, R.; Zakaria, M. P.; Akkhavong,K.; Ogata, Y.; Hirai, H.; Iwasa, S.; Mizukawa, K.; Hagino, Y.; Imamura,

1472 dx.doi.org/10.1021/es1032025 |Environ. Sci. Technol. 2011, 45, 1466–1472

Environmental Science & Technology ARTICLE

A.; Saha,M.; Takada, H. Transport and release of chemicals from plasticsto the environment and to wildlife. Philos. Trans. R. Soc., B 2009, 364(1526), 2027–2045.(18) Zitko, V.; Hanlon, M. Another Source of Pollution by Plastics -

Skin Cleaners with Plastic Scrubbers. Mar. Pollut. Bull. 1991, 22 (1),41–42.(19) Gregory, M. R. Plastic 'scrubbers' in hand cleansers: A further

(and minor) source for marine pollution identified. Mar. Pollut. Bull.1996, 32 (12), 867–871.(20) Fendall, L. S.; Sewell,M. A. Contributing tomarine pollution by

washing your face: Microplastics in facial cleansers. Mar. Pollut. Bull.2009, 58 (8), 1225–1228.(21) Betts, K. Why small plastic particles may pose a big problem in

the oceans. Environ. Sci. Technol. 2008, 42 (24), 8995.(22) Hale, S. E.; Martin, T. J.; Goss, K. U.; Arp, H. P. H.; Werner, D.

Partitioning of organochlorine pesticides from water to polyethylenepassive samplers. Environ. Pollut. 2010, 158 (7), 2511–2517.(23) Muller, J. F.; Manomanii, K.; Mortimer, M. R.; McLachlan,

M. S. Partitioning of polycyclic aromatic hydrocarbons in the poly-ethylene/water system. Fresenius' J. Anal. Chem. 2001, 371 (6), 816–822.(24) Adams, R. G.; Lohmann, R.; Fernandez, L. A.; Macfarlane, J. K.;

Gschwend, P. M. Polyethylene devices: Passive samplers for measuringdissolved hydrophobic organic compounds in aquatic environments.Environ. Sci. Technol. 2007, 41 (4), 1317–1323.(25) Lohmann, R.; Muir, D. Global Aquatic Passive Sampling

(AQUA-GAPS): Using Passive Samplers to Monitor POPs in theWaters of the World. Environ. Sci. Technol. 2010, 44 (3), 860–864.(26) Mayer, P.; Tolls, J.; Hermens, L.; Mackay, D. Equilibrium

sampling devices. Environ. Sci. Technol. 2003, 37 (9), 184A–191A.(27) Huckins, J. N.; Petty, J. D.; Lebo, J. A.; Almeida, F. V.; Booij, K.;

Alvarez, D. A.; Clark, R. C.; Mogensen, B. B. Development of thepermeability/performance reference compound approach for in situcalibration of semipermeable membrane devices. Environ. Sci. Technol.2002, 36 (1), 85–91.(28) Mackay, D. Multimedia Environmental Models: The Fugacity

Approach, 2nd ed.; CRC Press LLC: Boca Raton, FL, 2001.(29) Dameron, O. J.; Parke, M.; Albins, M. A.; Brainard, R. Marine

debris accumulation in the Northwestern Hawaiian Islands: Anexamination of rates and processes. Mar. Pollut. Bull. 2007, 54 (4),423–433.(30) Law, K. L.; Moret-Ferguson, S.; Maximenko, N. A.; Proskur-

owski, G.; Peacock, E. E.; Hafner, J.; Reddy, C. M. Plastic Accumulationin the North Atlantic Subtropical Gyre. Science 2010, 329 (5996), 1185–1188.(31) Gouin, T.; Mackay, D.; Webster, E.; Wania, F. Screening

chemicals for persistence in the environment. Environ. Sci. Technol.2000, 34 (5), 881–884.(32) Arnot, J. A.; Gobas, F. A. P. C. A food web bioaccumulation

model for organic chemicals in aquatic ecosystems. Environ. Toxicol.Chem. 2004, 23 (10), 2343–2355.(33) Smedes, F.; Geertsma, R. W.; van der Zande, T.; Booij, K.

Polymer-Water Partition Coefficients of Hydrophobic Compounds forPassive Sampling: Application of Cosolvent Models for Validation.Environ. Sci. Technol. 2009, 43 (18), 7047–7054.(34) Schuurmann, G.; Ebert, R. U.; Kuhne, R. Prediction of the

sorption of organic compounds into soil organic matter from molecularstructure. Environ. Sci. Technol. 2006, 40 (22), 7005–7011.(35) Dachs, J.; Lohmann, R.; Ockenden, W. A.; Mejanelle, L.;

Eisenreich, S. J.; Jones, K. C. Oceanic biogeochemical controls on globaldynamics of persistent organic pollutants. Environ. Sci. Technol. 2002, 36(20), 4229–4237.(36) Zarfl, C.; Klasmeier, J.; Matthies, M. A conceptual model

describing the fate of sulfadiazine and its metabolites observed inmanure-amended soils. Chemosphere 2009, 77 (6), 720–726.(37) Kelly, B. C.; Ikonomou, M. G.; Blair, J. D.; Morin, A. E.; Gobas,

F. A. P. C. Food web-specific biomagnification of persistent organicpollutants. Science 2007, 317 (5835), 236–239.

(38) Moser, G. A.; McLachlan, M. S. A non-absorbable dietary fatsubstitute enhances elimination of persistent lipophilic contaminants inhumans. Chemosphere 1999, 39 (9), 1513–1521.

(39) Lutzow, N.; Tihminlioglu, A.; Danner, R. P.; Duda, J. L.; DeHaan, A.;Warnier, G.; Zielinski, J. M. Diffusion of toluene and n-heptanein polyethylenes of different crystallinity. Polymer 1999, 40 (10), 2797–2803.

(40) Vittoria, V. Influence of the Crystallinity on the Transport-Properties of Polyethylene. J. Mater. Sci. 1995, 30 (15), 3954–3958.

(41) Harman, C.; Boyum, O.; Thomas, K. V.; Grung, M. Small ButDifferent Effect of Fouling on the Uptake Rates of SemipermeableMembrane Devices and Polar Organic Chemical Integrative Samplers.Environ. Toxicol. Chem. 2009, 28 (11), 2324–2332.