Widespread distribution of microplastics in subsurface ...

Marine Pollution Bulletin 79 (2014) 94–99

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Marine Pollution Bulletin journal homepage: www.elsevier.com/locate/marpolbul

Widespread distribution of microplastics in subsurface seawater in the NE Pacific Ocean Jean-Pierre W. Desforges a, Moira Galbraith b, Neil Dangerfield b, Peter S. Ross c,⇑ a

School of Earth and Ocean Sciences, University of Victoria, PO Box 1700, Victoria, BC, Canada Institute of Ocean Sciences, Fisheries and Oceans Canada, PO Box 6000, Sidney, BC, Canada c Vancouver Aquarium, PO Box 3232, Vancouver, BC V6E 3G2, Canada b

a r t i c l e Keywords: British Columbia Pacific Ocean Microplastic Tsunami debris Litter Plastic

i n f o

a b s t r a c t We document the abundance, composition and distribution of microplastics in sub-surface seawaters of the northeastern Pacific Ocean and coastal British Columbia. Samples were acid-digested and plastics were characterized using light microscopy by type (fibres or fragments) and size (1000 lm). Microplastics concentrations ranged from 8 to 9200 particles/m3; lowest concentrations were in offshore Pacific waters, and increased 6, 12 and 27-fold in west coast Vancouver Island, Strait of Georgia, and Queen Charlotte Sound, respectively. Fibres accounted for 75% of particles on average, although nearshore samples had more fibre content than offshore (p < 0.05). While elevated microplastic concentrations near urban areas are consistent with land-based sources, the high levels in Queen Charlotte Sound appeared to be the result of oceanographic conditions that trap and concentrate debris. This assessment of microplastics in the NE Pacific is of interest in light of the on-coming debris from the 2011 Tohoku Tsunami. Ó 2013 Elsevier Ltd. All rights reserved.

1. Introduction The marine environment is host to increasing quantities of waste debris from human activities in and around the ocean (Arthur and Baker, 2011). Any persistent or manufactured solid material discarded in the marine or coastal environment is termed marine debris, of which a large fraction (60–80%) consists of plastic (GESAMP, 2010; UNEP, 2005). An estimated 1.3 plastic items can be found for every m2 of shoreline worldwide, based on a review of 201 beach surveys on five continents (Bravo et al., 2009). This debris is increasingly recognized as a threat to marine biota. For instance, through ingestion or entanglement, more than 267 species worldwide are estimated to be impacted by marine debris, including the majority of sea turtle species and almost 50% of all seabird and marine mammal species (Derraik, 2002). Over the past decade, efforts to document microplastics in the marine environment have increased. Microplastics have been defined as plastic particles 1 lm) are also included but less often detected (Arthur et al., 2009). Several plastic classes exist, but the most commonly found micro-debris particles include polyethylene (PE), polypropylene (PP), and polystyrene (PS) (Andrady, 2011). Microplastics are now ubiquitous in the marine environment, having

⇑ Corresponding author. Tel.: +1 604 659 3400; fax: +1 604 659 3562. E-mail address: [email protected] (P.S. Ross). 0025-326X/$ - see front matter Ó 2013 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.marpolbul.2013.12.035

been found in seawater at the surface and at depth, and in oceans and coastlines from the equator to the poles (Barnes et al., 2009). Despite the growing number of publications on the topic, large gaps still remain in our understanding of the source, transport and fate of microplastics in the marine environment. Microplastics consist of either deliberately manufactured commercial micro-particles, including scrubbers, abrasives, and precursor pellets (primary sources), or as fragments and fibres derived from the deterioration of larger products (secondary sources) (Hidalgo-Ruz et al., 2012). Plastic debris can originate from marine-based sources (i.e. fishing, aquaculture, shipping, etc.) or land-based sources (i.e. wastewater effluent, run-off, rivers), but the majority is believed to derive from the latter (Andrady, 2011). Regardless of origin, plastics are manufactured to be durable and thus persist in the environment, particularly in water where degradation can occur over decades (Hidalgo-Ruz et al., 2012). The abundance and distribution of microplastics in the marine environment are believed to be governed by prevailing surface circulation and winds, plastic density, colour and shape, and proximity to urban centres (Andrady, 2011; Browne et al., 2011, 2010; Doyle et al., 2011). Although the harmful effects of large plastic debris on marine wildlife have been well documented (i.e. Derraik, 2002), little is known about the effects of microplastics. Potential threats to biota may include physical harm from ingestion, leaching of toxic additives, and desorption of persistent, bioaccumulative and toxic

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(PBT) chemicals (GESAMP, 2010). Small plastic fragments are available to organisms at the base of the food web as they may be in the same size-range as natural food items. Recent studies have shown that plankton and several classes of invertebrates and vertebrates can ingest and accumulate microplastics (see review by Wright et al., 2013). Furthermore, microplastics have been found to concentrate a wide-range of organic contaminants in the aquatic environment due to their hydrophobic nature. Contaminants that have been adsorbed include polychlorinated biphenyls (PCBs), polycyclic aromatic hydrocarbons (PAHs), dichlorodiphenyltrichloroethane (DDT), polybrominated diphenylethers (PBDEs), and bisphenol A (BPA) (Mato et al., 2001; Rios et al., 2007; Teuten et al., 2009). Few studies have examined the bioaccumulation of PBT chemicals from plastics, although some studies suggest that PCB concentrations rose in lugworms (Arenicola marina) and seabirds (Puffinus gravis, Calonectris leucomelas) exposed to contaminated plastic particles (Ryan et al., 1988; Teuten et al., 2009, 2007). The aim of this study was to investigate the abundance, composition and distribution of marine microplastics in the NE Pacific Ocean in areas in and near the coastal waters of British Columbia (BC), Canada. Microplastics were quantified according to size (62–5000 lm) and shape (fibres or fragments) in sub-surface seawater. This study is particularly timely given the present movement of marine debris across the Pacific as a result of the 2011 Tohoku earthquake and resulting tsunami.

Regional comparisons were accomplished by grouping sites into oceanographic regions: NE Pacific Ocean, west coast Vancouver Island (WCVI), Queen Charlotte Sound (QCS), and Strait of Georgia (SoG). Regional differences were evaluated by ANOVA followed by Tukey’s HSD where significant using SPSS software (SPSS 16, IBM Inc.). Maps and contour plots were created using Ocean Data View 4 (Schlitzer, R. 2013, http://odv.awi.de).

2. Materials and methods

3. Results

2.1. Sampling

3.1. Microplastic abundance

Sampling was conducted aboard two oceanographic research cruises: the CCGS John P. Tully cruise of the Line P time series program in August 2012, and the La Perouse Monitoring Program cruise of September 2012 conducted by the Institute of Ocean Sciences (Fisheries and Oceans Canada). The sampling regime was developed to create a low cost, long-term monitoring program that is integrated into existing oceanographic programs. As such, sampling was conducted during standard cruise operations at scheduled Line P and La Perouse stations. Line P cruises collect transect data from coastal BC to approximately 1200 km offshore in the NE Pacific Ocean, while La Perouse regularly samples stations off coastal Vancouver Island (Fig. 1). Seawater was collected at 4.5 m below the surface using the saltwater intake system of the vessel. A flow-meter measured the volume of water pumped from the saltwater intake at each site, and the readings were converted to cubic meters of water filtered. Water was typically pumped for 10–20 min at each station, but this varied as a function of other oceanographic sampling taking place aboard the vessel. Water was first passed through a coarse 5 mm filter to remove large debris and organisms before entering the intake system, then run through a series of copper sieves of diminishing pore size: 250 lm, 125 lm, and 62.5 lm. The material on each sieve was rinsed with seawater into labelled 20 ml glass vials and stored refrigerated with 5–10% HCl at 4 °C at the Institute of Ocean Sciences (Sidney, BC).

Microplastics were detected at 34 stations, but concentrations varied considerably and ranged from 8 to 9180 particles/m3 (Table 1, Fig. 1). The concentration of microplastics was 4–27 times greater at sites nearshore (SoG, WCVI, and QCS) than sites offshore in the NE Pacific Ocean (Fig. 1, Table 1). Locally, the inland waters of QCS and the SoG had higher microplastic levels than the WCVI (p = 0.015 and p = 0.007 respectively, Table 1). A localized area of low concentrations southwest of Vancouver Island was evident, where levels were far below the average for coastal regions (Fig. 1).

2.2. Plastic analysis In the laboratory, organic material in the water samples were acid digested at 80–90 °C for 3 h using concentrated HCl. Nile red dye (3 lg/ml) was added each sample prior to being filtered through an HA Millipore mixed cellulose ester filter paper (47 mm, 0.45 lm pore size; EMD Millipore Corporation, Billerica, MA) under vacuum filtration. Filter paper was placed on solvent

rinsed foil and covered until analysis (same day). Samples were examined visually using optical microscopy (Zeiss stereoscope, Discovery V8; Carl Zeiss Canada Ltd., Toronto, ON) by counting plastics in 8 of 16 squares of a 7.8  7.5 mm grid. Plastics were identified according morphological characteristics and physical response features (e.g. response to physical stress; microplastics were bendable or soft) described by Hidalgo-Ruz et al. (2012). Particle size was measured and plastics were counted and categorized into two broad categories: fibres/filaments and fragments (i.e. pellets, thin films, fragments). Plastic data obtained from the three sieves was combined in order to better categorize the particles by size. Size categories were based on length measurements of the longest dimension of each particle: 1000 lm (1000–5000 lm). Particle counts were converted to number of particles per cubic meter of seawater for each station. 2.3. Statistical analysis

3.2. Plastic size distribution The mean size of microplastic particles was 606 ± 221 lm. The smallest particle documented was 64.8 lm, and the largest was 5810 lm (Table 1). Particle sizes increased linearly from the coast to approximately 600 km offshore, resulting in greater particle sizes in the NE Pacific Ocean and WCVI regions compared to the inland waters of QCS (p < 0.001, Table 1). The 100–500 lm size fraction was the most abundant of all size classes at most sampling stations, and largely explained the high total plastic concentrations observed in QCS (Table 1). 3.3. Plastic composition The majority of identified particles were fibres/filaments and angular plastic fragments, with few cases of other types of plastics (thin films or round fragments). Very brittle, brightly coloured fibres were abundant in most samples, but were not quantified as the acid digestion readily eliminated these. The colours of particles varied widely, but blue, red, black and purple were the most common. Fibres/filaments accounted for approximately three quarters of the identified particles in the collective dataset (Fig. 2). The fibre/filament concentrations followed total plastic patterns, with lowest concentrations offshore (NE Pacific < all

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(a)

3

)

10000

(b)

8000 6000 4000 2000 0

1

3

5

7

9

11

13

15

17

19

21

23

25

27

29

31

33

Fig. 1. Total microplastic concentrations (particles/m3; detected particles >62 lm) in subsurface waters (4.5 m) of the NE Pacific Ocean in and around coastal British Columbia, Canada. (a) Sample locations are numbered (1–34), and the concentration gradient was estimated using DIVA gridding function of Ocean Data View 4. (b) Total microplastic concentrations at each sampling station are grouped into major oceanographic regions for this study: northeastern Pacific Ocean (NE Pacific), west coast Vancouver Island (WCVI), Queen Charlotte Sound (QCS), and Strait of Georgia (SoG).

Table 1 Microplastic abundance (mean ± SD) and size distribution in subsurface seawater samples collected at 34 stations in the NE Pacific Ocean in and around coastal British Columbia, Canada. Stations are grouped into major geographical regions in this study: northeastern Pacific Ocean (NE Pacific), west coast Vancouver Island (WCVI), Queen Charlotte Sound (QCS) and Strait of Georgia (SoG). Different superscript letters for regions denote significant differences in concentration or particle size (ANOVA, Tukey’s HSD; p < 0.05). All quantified microplastic particles are >62 lm. Concentration (particles/m3)

Particle size (lm)

Particle size distribution (as a% of total) 100–500 lm

500–1000 lm

>1000 lm

NE pacific WCVI QCS SoG

279 ± 178a 1710 ± 1110b 7630 ± 1410c 3210 ± 628c

684 ± 953a 558 ± 521a 398 ± 376b 513 ± 494a,b

8.04 ± 10.3 3.48 ± 5.00 8.78 ± 6.65 7.02 ± 6.93

52.4 ± 17.2 59.9 ± 17.6 67.2 ± 2.31 56.4 ± 13.1

20.7 ± 12.2 22.5 ± 12.9 18.6 ± 6.22 21.6 ± 6.39

18.8 ± 8.28 14.0 ± 9.04 5.43 ± 1.84 14.9 ± 11.7

Mean all sites Min Max

2080 ± 2190 8.51 9180

606 ± 221 64.8 5810

5.92 ± 7.39 0.00 30.8

57.7 ± 16.0 23.1 84.2

21.5 ± 11.0 0.00 48.0

14.9 ± 9.37 0.00 33.3

regions, p < 0.001) and highest concentrations in QCS (not shown). Plastic fragment concentrations were uniform throughout the study area, with the exception that SoG had higher concentrations than NE Pacific Ocean (p = 0.01). Besides a local outlying area southwest of Vancouver Island, samples of microplastics typically comprised over 70% fibres in coastal and inland waters (Fig. 2). The contribution of fibres to total plastics decreased with increasing distance from shore (Fig. 2), such that the percentage of fibres was greater in QCS and the SoG than in NE Pacific Ocean (p = 0.02 and 0.05 respectively).

333 lm were used in these studies, which may have resulted in the loss of small particles compared to our study. For instance, plastic particle concentrations in Swedish waters were up to 100,000 times greater when sampled with a 80 lm rather than a 450 lm mesh (Noren, 2007). Compared to studies using similar mesh size, concentrations reported here are similar to those reported in the coastal waters of Sweden, but considerably lower than those in the North Sea (Dubaish and Liebezeit, 2013; Noren, 2007). Our study examined microplastics in subsurface seawater samples (4.5 m) which may differ in composition from those found at the surface due to differences in polymer density. However, Lattin et al. (2004) reported similar microplastic weight and density profiles at surface and at 5 m depth along the coast of California, likely due to ocean surface mixing. Overall, these results highlight the important contribution of smaller size fractions to the total plastic load. A common minimum particle size and a standardized sampling regime are two study design elements that would enable better comparisons among studies in the future, according to the Joint Group of Experts on the Scientific Aspects of Marine Environmental Protection (GESAMP, 2010). Our findings suggest that future monitoring would benefit from the use of mesh sizes smaller than those currently used in standard neuston nets. Greater plastic abundance was detected in coastal stations compared to offshore waters, consistent with studies that report that land-based human activities are a major source of microplastics to the marine environment (Barnes et al., 2009; Browne et al., 2011, 2010; Collignon et al., 2012; Doyle et al., 2011; Dubaish and Liebezeit, 2013; Ribic et al., 2010). The increased plastic concentrations nearshore was in part explained by an increase in fibre content, suggesting that sources may be due to fishing, recreational boating, and/or wastewater effluent. Browne et al. (2011) showed that disposal of municipal wastewater contaminated with fibres from washing clothes was a major source of plastic fibres in the UK. Vancouver, Victoria and Seattle are major urban centres that release their wastewater effluent into the SoG, Juan de Fuca Strait, and Puget Sound, respectively, providing a putative source of microplastics to this coastal region on the British Columbia (Canada) – Washington State (USA) boundary. Harbours and vessels have also been identified as sources of fibrous plastic particles (Dubaish and Liebezeit, 2013; Hinojosa and Thiel, 2009; Ng and Obbard, 2006; Noren, 2007). As we did not identify the specific polymer types, we cannot further speculate on the sources of the fibres at this time.

Researchers have been able to use Fourier transform-infrared spectroscopy (FT-IR) to identify the polymer type of individual plastic particles. Although knowing polymer type does not unequivocally establish the origin of plastic particles, it does provide information to help narrow the possibilities. Other studies have also reported a preponderance of fibre particles in the marine environment and have identified these as predominantly polypropylene, polyester, polyethylene, polyamide (nylon), acrylic, and polyvinyl alcohol (Browne et al., 2011, 2010; Claessens et al., 2011; Ng and Obbard, 2006). These polymer types are often used in textiles, and indeed Browne et al. (2011) showed that polymer composition in sediment closely reflected that in sewage treatment effluent (i.e. clothes washing). Nylon, polypropylene, polyvinyl alcohol and polyethylene are also used to make ropes, nets, and fishing lines (Claessens et al., 2011). Microplastic fragments are typically composed of polypropylene, polyethylene, polystyrene, polyester, and polyvinyl chloride (Andrady, 2011; Browne et al., 2010; Claessens et al., 2011; Cole et al., 2011). These are commonly used in consumer products (e.g., plastic bags, bottles, caps, films, containers, etc.) and likely originate from the break-down of larger macro-debris. Alternatively, polyethylene, polypropylene and polystyrene granules are found in cosmetic products as scrubbers, while acrylic and polyester scrubbers are used in air-blasting to remove rust and paint from machinery and boat hulls (Cole et al., 2011). Local patterns of coastal microplastic abundance appeared to be shaped by oceanographic conditions. The SoG is a relatively large channel, subject to strong tidal influences and large volume fluxes as freshwater from the Fraser River is mixed with Pacific water (Freeland et al., 1984; Pawlowicz et al., 2007). The result is a relatively short residence time of surface waters and strong outward flows, which may explain the moderate concentrations of plastics in the industrialized SoG compared to other nearshore sites. On the western coast of Vancouver Island, the dominant surface currents in summer are northward (Freeland et al., 1984). The intermediate concentrations of plastics along the WCVI are likely the combined results of local inputs, convergence from offshore currents, and outflow from the SoG. Interestingly, an area of low plastic concentration to the southwest of Vancouver Island coincides with a major local upwelling (La Pérouse Bank) (Freeland et al., 1984). This suggests that upwelling may provide a source of deep water with relative low levels of microplastics. Depth profiles for microplastics are needed to confirm this hypothesis.

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The high microplastic abundance in QCS was unexpected, as this area is sparsely populated and is home to few industries. These high numbers may be explained by several factors. First, the oceanographic setting in QCS is dynamic, in which freshwater inputs from the Queen Charlotte Strait (south–east) are mixed with Pacific waters to the north–west, and surface eddies dominate the circulation (Crawford et al., 1985; Freeland et al., 1984). Floating materials within the sound follow a clockwise gyre and may remain for several weeks before being flushed out into the Pacific (Crawford et al., 1985). Thus plastic particles converging from offshore Pacific currents and the northward coastal current may enter Queen Charlotte Sound, where local circulation acts to retain them. Second, QCS has a high concentration of finfish aquaculture installations (http://www.al.gov.bc.ca/fisheries/). Aquaculture facilities have been identified as important local sources of plastics (Arthur and Baker, 2011; Hinojosa and Thiel, 2009). Lastly, several harbours and recreational fishing activities likely supply microplastics to the area. Whatever the dominant source of microplastics in QCS, this area appears to represent a vulnerable receiving environment. It is interesting to note that these results are consistent with apparently high levels of large marine debris detected in QCS relative to other coastal regions of British Columbia (Williams et al., 2011). A major source of marine debris, including plastics, to the north Pacific is the Tohoku earthquake and resulting tsunami of 11 March 2011, after which it was estimated that over a million tonnes of debris was washed into the Pacific (http://www. kantei.go.jp). The prevailing winds create an eastward current in the north Pacific Ocean which acts to transport floating marine debris toward North America (Howell et al., 2012). Tsunami debris models (NOAA; http://marinedebris.noaa.gov; International Pacific Research Centre; http://iprc.soest.hawaii.edu) predict that buoyant debris (influenced by wind, i.e. positive windage) would reach the North-American coastline during the winter of 2011–2012. Indeed, sightings of tsunami debris continue to be reported (http://marinedebris.noaa.gov/tsunamidebris/debris_sightings.html). The transportation of microplastics differs from that of large buoyant debris in that they are entirely submerged (zero windage) and thus not exposed to direct wind stress (Lebreton and Borrero, 2013). The transport of microplastics across the Pacific Ocean is therefore expected to take place less quickly than buoyant items. Lebreton and Borrero (2013) modelled the transport of zero windage marine debris from the Tohoku Tsunami and predicted that it would reach the International Dateline after six months, but the eastward progression of debris would slow thereafter to the speed of the north Pacific current (5 cm/s). Using an average particle speed of 5 cm/s once past the Dateline, we estimate that a microplastic debris front would be situated near the centre of the Pacific (160° W) at the time of our sampling (August/September 2012). Estimates from the IPRC tsunami model are similar but show the debris front slightly eastward by September 2012 (150oW) (http://iprc.soest.hawaii.edu). Nonetheless, these results suggest that microplastic concentrations in coastal BC reported here can be considered as ‘‘background’’ prior to the influx of tsunami debris. The IPRC model predicts the debris front to reach the west coast of British Columbia by the spring of 2013. Lebreton and Borrero (2013) estimate the debris will reach the North American coastline by June 2014. The ingestion of microplastics has been documented in several classes of marine organisms, including zooplankton (e.g. copepods, euphausiids, larval fish, salps, and medusae), benthic invertebrates (polychaetes, crustaceans, echinoderms, bryozoans, and bivalves), and vertebrates (fish, sea-birds, and marine mammals) (reviewed by Wright et al., 2013). Microplastics have been found to accumulate through translocation into haemolymph of blue mussels (Mytilus edulis), resulting in granulocytoma and lysosomal membrane destabilization (inflammatory responses) (Browne

et al., 2008; von Moos et al., 2012). Reduced algal ingestion rates in copepods (Centropages typicus) and weight loss and reduced feeding activity in lugworms have been linked to microplastic ingestion (Besseling et al., 2013; Cole et al., 2013). Results from invertebrates are consistent with findings of reduced feeding and physical condition in sea-birds (Ryan, 1988; Spear et al., 1995). Toxic contaminant accumulation has also been attributed with plastic ingestion in lugworms, sea-birds, and marine mammals (Besseling et al., 2013; Fossi et al., 2012; Koelmans et al., 2013; Tanaka et al., 2013). The extent to which microplastics are harmful to marine biota remains a field of study worthy of heightened scrutiny given our report of widespread contamination of the NE Pacific Ocean.

Acknowledgements Thanks to the crew of the CCGS John P. Tully and the sea-going scientific staff of the Institute of Ocean Sciences (Fisheries and Oceans Canada); especially Doug Yelland and Marie Robert, chief scientists for the La Pérouse Zooplankton Monitoring Program and Line P Monitoring Program respectively. The authors kindly acknowledge the helpful discussions with Olga Lukyanova, Joel Baker and participants of the workshop on ‘‘Trends in Marine Contaminants’’ held at the 2011 Annual Conference of the North Pacific Marine Science Organization (PICES).

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