Amberstripe scad Decapterus muroadsi (Carangidae) fish ingest blue microplastics resembling their copepod prey along the coast of Rapa Nui (Easter Island) in the South Pacific subtropical gyre

STOTEN-21888; No of Pages 8 Science of the Total Environment xxx (2017) xxx–xxx

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Short Communication

Amberstripe scad Decapterus muroadsi (Carangidae) fish ingest blue microplastics resembling their copepod prey along the coast of Rapa Nui (Easter Island) in the South Pacific subtropical gyre Nicolas Christian Ory a,b,⁎, Paula Sobral c, Joana Lia Ferreira d, Martin Thiel a,b,e a

Facultad Ciencias del Mar, Universidad Católica del Norte, Larrondo 1281, Coquimbo, Chile Millennium Nucleus Ecology and Sustainable Management of Oceanic Island (ESMOI), Coquimbo, Chile c MARE-NOVA, Faculdade de Ciências e Tecnologia, Universidade NOVA de Lisboa, Campus da Caparica, 2829-516 Caparica, Portugal d LAQV-REQUIMTE, Departamento de Conservação e Restauro, Faculdade de Ciências e Tecnologia, Universidade NOVA de Lisboa, 2829-516 Caparica, Portugal e Centro de Estudios Avanzados en Zonas Áridas (CEAZA), Coquimbo, Chile b

H I G H L I G H T S

G R A P H I C A L

A B S T R A C T

• Most (80%) of Decapterus muroadsi fish from Rapa Nui had ingested microplastics. • Blue polyethylene polymers were preferentially ingested by the fish. • Fish seem to mistakenly ingest blue microplastics similar to their copepod prey. • Floating microplastics may enter food webs through visual planktivorous fishes.

a r t i c l e

i n f o

Article history: Received 6 December 2016 Received in revised form 25 January 2017 Accepted 26 January 2017 Available online xxxx Editor: Kevin V. Thomas Keywords: Microplastic contamination Rapa Nui (Easter Island) Planktivorous fish South Pacific subtropical gyre Copepod prey

a b s t r a c t An increasing number of studies have described the presence of microplastics (≤5 mm) in many different fish species, raising ecological concerns. The factors influencing the ingestion of microplastics by fish remain unclear despite their importance to a better understanding of the routes of microplastics through marine food webs. Here, we compare microplastics and planktonic organisms in surface waters and as food items of 20 Amberstripe scads (Decapterus muroadsi) captured along the coast of Rapa Nui (Easter Island) to assess the hypothesis that fish ingest microplastics resembling their natural prey. Sixteen (80%) of the scad had ingested one to five microplastics, mainly blue polyethylene fragments that were similar in colour and size to blue copepod species consumed by the same fish. These results suggest that planktivorous fish, as a consequence of their feeding behaviour as visual predators, are directly exposed to floating microplastics. This threat may be exacerbated in the clear oceanic waters of the subtropical gyres, where anthropogenic litter accumulates in great quantity. Our study highlights the menace of microplastic contamination on the integrity of fragile remote ecosystems and the urgent need for efficient plastic waste management. © 2017 Elsevier B.V. All rights reserved.

⁎ Corresponding author at: Facultad Ciencias del Mar, Universidad Católica del Norte, Larrondo 1281, Coquimbo, Chile. E-mail address: [email protected] (N.C. Ory).

http://dx.doi.org/10.1016/j.scitotenv.2017.01.175 0048-9697/© 2017 Elsevier B.V. All rights reserved.

Please cite this article as: Ory, N.C., et al., Amberstripe scad Decapterus muroadsi (Carangidae) fish ingest blue microplastics resembling their copepod prey along the coast of Rapa Nui (Easter Island)..., Sci Total Environ (2017), http://dx.doi.org/10.1016/j.scitotenv.2017.01.175

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1. Introduction Within recent decades, anthropogenic waste has become ubiquitous throughout the world's oceans; plastic items constitute the most important part of marine litter (Galgani et al., 2015). Although the hazards of large plastic debris on marine ecosystems have been documented for several decades (Derraik, 2002; Laist, 1987; Laist, 1997), the threat of inconspicuous millimetre-sized fragments on marine ecosystems is still poorly known (Barboza and Gimenez, 2015; Lusher, 2015). Plastics floating at the sea surface are transported over long distances by winds and currents and accumulate in the centre of the subtropical gyres (Eriksen et al., 2014). During their time at the sea surface, plastic objects gradually fragment into smaller pieces under the action of sunlight, temperature, wave action, and organisms (Barnes et al., 2009). As a result, most anthropogenic litter items in the centre of the gyres are small (≤5 mm), i.e. microplastics (Eriksen et al., 2014). Microplastics represent a threat to the integrity of marine ecosystems because they are ingested by various organisms (review by Lusher, 2015) to which they may cause deleterious physiological and behavioural effects (UNEP, 2016; Wright et al., 2013a). Microplastics have been reported in many fish species in most environments (e.g. Anastasopoulou et al., 2013; Boerger et al., 2010; Dantas et al., 2012; Rummel et al., 2016). However, the factors influencing microplastic ingestion are still poorly studied, despite the importance of identifying these factors to gain better comprehension of microplastic transfer through trophic webs (do Sul et al., 2014). Some studies have suggested that fish ingest microplastics that they may have confused with natural prey (Boerger et al., 2010; Ramos et al., 2012; Rummel et al., 2016), but the microplastics and natural prey in fish have not yet been directly compared to those in the environment. Predators often adjust their attack strategy to the escape abilities of their prey (Cooper et al., 1985; Lazzaro, 1987). Visual predatory fish employ slow approaches to forage on prey with limited escape abilities, but they attack at higher velocity (Vinyard, 1980) and from longer distances (Utne-Palm, 1999) when feeding on very motile prey, which therefore are not carefully assessed before capture. Fish foraging on evasive prey should therefore be susceptible to mistakenly targeting non-dietary items that resemble their natural prey. Although capable of great bursts of speed to escape from their predators (Jiang and Kiørboe, 2011; O'Brien, 1979), copepods spend most of their time resting or swimming slowly in the water column (Yen, 2013); they are millimetre-sized and can differ greatly in colour (Conway, 2012). Many of the microplastics floating in the water column are similar in size and colour to copepods, which are common prey for many planktivorous fish species (Carpenter and Niem, 1999; Chesney et al., 2005; Turner, 2004). Therefore, planktivorous fish may erroneously capture microplastics that resemble their evasive copepod prey. The aim of this study was to compare the size and colour of microplastics and copepod species found in surface waters and in the digestive tract of Amberstripe scad, Decapterus muroadsi (Carangidae), captured along the coast of Rapa Nui to assess whether fish ingest microplastics similar in colour and size to their natural prey. Decapterus muroadsi is common in the central South Pacific Ocean, often schooling near the sea surface, where it feeds commonly on copepods (Carpenter and Niem, 1999; Randall and Cea, 2011). This species is an important fishery resource for the population of Rapa Nui, where it is consumed locally or used as bait by fishermen to capture larger predatory fish (Randall and Cea, 2011).

2. Materials and methods 2.1. Sampling of surface waters and fish guts Twenty D. muroadsi (mean size = 14.0 ± SE0.2 cm) were opportunistically collected between 1400 and 1600 h by a local fisherman on

the 27th of March 2015 in shallow water (b 30 m deep) on the southwest coast of Rapa Nui (Fig. 1). Fish were attracted near the sea surface with bread as bait and readily captured with a hand fishing net (round aperture 80 cm in diameter with 1-cm mesh size). Fish were stored in a clean, plastic cooler box and brought to the field-laboratory on Rapa Nui within 2 h. There, all fish were measured to the nearest centimetre and the gastrointestinal tract, from oesophagus to anus, of each individual was removed and immediately preserved in separate jars filled with 95% ethanol to be further analysed. Before use, all tools (e.g. scissors, forceps, sieve) were cleaned and visually inspected under a dissecting microscope to ensure that no plastic particles remained on their surface. Six water samples were collected from 1 to 8 April 2015 using a 2-m-long epineuston net (rectangular opening: 80 cm wide × 40 cm high) with 300-μm mesh opening and a PVC collector (11 cm diameter × 29 cm length) as the cod end. The volume of water filtered through the mesh was estimated with a HydroBios flowmeter attached across the centre of the net opening. The average volume of seawater filtered during a 20-min trawl was 623.0 ± 7.9 m3 (n = 6). Coordinates were taken at the beginning and at the end of each towing period to determine the area sampled. The epineuston net was pulled from a small fishing boat at a speed of 1.5 to 2.0 knots for 20 min, collecting particles floating within the upper 20–30 cm from the surface. All trawls were conducted within a nautical mile of the south and west coasts of Rapa Nui (Fig. 1) under calm seas (0 to 2 Douglas sea scale). No storm or strong current changes, which could have affected the distribution of floating microplastics within the water column (Eriksen et al., 2013), occurred between collections of the fish guts and the last of our water samplings (furthermore, samples from the coastal zone of Rapa Nui confirm consistently high microplastic abundances in this area, regardless of study year and season – Eriksen et al., 2013; Kiessling et al., unpublished data). At the end of each trawl, the content of the cod-end collector was transferred to a 500-mL glass flask and fixed in 70% ethanol. In the laboratory on Rapa Nui, the water samples were filtered through a 100-μm mesh sieve and fixed in 95% ethanol until analysed in the laboratory at the Universidad Católica del Norte (Coquimbo, Chile).

2.2. Analysis of fish guts and water samples The gut of each fish was weighed to the nearest 0.1 g and cut at the pylorus to separate the stomach-oesophagus section (hereafter referred to as stomach) and the intestine, which were then analysed separately. The stomach and intestine were weighed separately and cut open longitudinally with a scalpel; their content was gently removed with the scalpel and placed in two separate Petri dishes. Organic material remaining on internal walls of the stomach and intestine was transferred into the corresponding petri dish with a wash bottle of ethanol. The gut contents and water samples were examined at 6.5 to 50 × under a Zeiss Stemi 2006-C dissecting microscope. Prey in fish guts and water samples were identified to the lowest taxonomic level and counted to assess their abundance within each sample (Table S1). Copepods were used as model species to examine how prey colour and size influence selection by D. muroadsi. Copepods were identified following descriptive keys from Boltovskoy (1999) and were separated by the lowest possible taxon into clean petri dishes filled with ethanol. For each copepod taxon, pictures of groups of b 200 individuals, carefully disposed to not overlap each other, were taken to measure the prosoma length (see Fig. 1 in Uye, 1982); all individuals were measured for taxa with ≤ 100 individuals per sample, whereas, a haphazard subsample (at least 10% of the total number of individuals, but a minimum number of 100 individuals) was measured for taxa with N 100 individuals per sample.

Please cite this article as: Ory, N.C., et al., Amberstripe scad Decapterus muroadsi (Carangidae) fish ingest blue microplastics resembling their copepod prey along the coast of Rapa Nui (Easter Island)..., Sci Total Environ (2017), http://dx.doi.org/10.1016/j.scitotenv.2017.01.175

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Fig. 1. Location map of Rapa Nui (Easter Island, red square) and inset showing the area (black square) where D. muroadsi were fished and the paths (red lines) along which surface water samples were collected. (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)

2.3. Description of microplastics

2.4. Polymer analysis

All microplastic items in water and fish gut samples were visually identified and separated from the rest of the sample to be counted and further analysed. The general aspect of plastic particles was described by their type (adapted from Hidalgo-Ruz et al., 2012; Table S2). Fibres (diameter ≤ 0.05 mm) were not recorded in this study because neither on Rapa Nui nor in Coquimbo a chamber with clean air flow was available, and contamination with airborne fibres could have been high (see Foekema et al., 2013; ICES/CIEM, 2015) during fish dissection and sieving of the water samples. Indeed, during sample sorting in Coquimbo, one to five fibres were found in each control petri dish placed beside the dissecting microscope during sample sorting, confirming the high probability of fibre contamination of the samples by airborne particles. The calculations of microplastic densities in guts are thus conservative estimates. The dominant colour (covering N 50% of the surface of the particle) of each microplastic was described using 12 of the colour types most commonly used in the literature (Table S2). The size, edge sharpness, and degradation (see Table S2 for the description of the categories of each features) of each microplastic was described as these features may reflect the potential of particles to cause harm to organisms. For example, very long fragments may not pass the pyloric canal and accumulate in the stomach, sharp-edged fragments may lacerate the digestive tract tissues, or degraded fragments may release additives more easily than newer particles (UNEP, 2016). A picture of each microplastic particle was taken using a Canon Powershot SX210 IS with a 35-mm adaptor fixed to the microscopic binocular. The maximum length and width of each microplastic were measured to the nearest 0.1 mm with the program Image J (imagej.nih.gov/ij/). After description, microplastics were stored in a 5-mL plastic Eppendorf tube filled with 95% ethanol.

Particles were analysed by infrared spectroscopy in attenuated total reflectance mode (FTIR-ATR) for particles ≥ 200 μm and in transmittance mode (μ-FTIR) for particles b200 μm. The spectra in reflectance mode (ATR) were acquired with an Agilent Handheld 4300 FTIR Spectrometer with DTGS detector, controlled temperature, and diamond ATR sample interface; the analyses were performed at the sample surface. Transmittance spectra were obtained with a Nicolet Nexus spectrophotometer equipped with a Continuum microscope and a MCT-A detector cooled by liquid nitrogen; the analyses were performed in micro-samples previously compressed with a Thermo diamond anvil cell. All spectra were obtained with a resolution of 4 cm− 1 and 32 FTIR-ATR or 128 μ-FTIR scans. Spectra were compared with a reference spectra library and accepted with a match N85%. The identification of the two samples tentatively assigned to an epoxy-polyester coating was based on best expert judgment by the presence of specific absorption bands. In total, 29 particles were chosen to be the most representative of all particles found in surface waters (13 particles analysed out of 206 particles in water) and fish guts (16 particles analysed out of 44 particles in fish). 2.5. Statistical analyses All statistics were run using the program SPSS version 21. Bootstrap estimates with 1000 resamplings (if not indicated otherwise) of the data were used to estimate the standard error of the mean and of the median (see Quinn, 2002). 2.5.1. Fish random feeding We separately tested the two null hypotheses that D. muroadsi fed randomly on (a) microplastics and (b) copepods of different colour

Please cite this article as: Ory, N.C., et al., Amberstripe scad Decapterus muroadsi (Carangidae) fish ingest blue microplastics resembling their copepod prey along the coast of Rapa Nui (Easter Island)..., Sci Total Environ (2017), http://dx.doi.org/10.1016/j.scitotenv.2017.01.175

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using log-likelihood, goodness-of-fit test (Manly et al., 2002). For both tests, a first log-likelihood statistic (X2L1) was calculated: n

I

X2L1 ¼ 2 ∑ ∑ uij loge j¼1 i¼1

"

#

u
ij  ; E uij

where i is the resource (i.e., colour) category for I microplastics (I = 4) or copepods (I = 3), j is the individual fish n that respectively ingested microplastics (n = 16) or copepods (n = 20), uij is the observed count of colour category i in fish j, and E(uij) = ui+ u+j / u++ is the expected number of item i in the gut of fish j, where ui+ is the sum of all items of colour category i used by all the fish, u+j is the sum of all the items in the gut of fish j, and u++ is the sum of all items counted in all fish individuals (see Manly et al., 2002). A second log-likelihood statistic (X2L2) was calculated with E(uij) = πi u+ j, where πi is the proportion of microplastics or copepods of colour category i in the environment obtained from our neuston trawls (number of samplings = 6). The difference D = X2L2 − X2L1 that exceeded the critical value of a chi-squared distribution with I − 1 degrees of freedom indicated overall fish selectivity for microplastics or copepods of different colour categories. The null hypothesis was rejected at a conservative level of error α = 0.001 to overcome limitations of low sample size used in this study. 2.5.2. Fish selectivity Fish selectivity for a certain type of microplastic or copepod was analysed using the index of relative electivity E∗i proposed by Vanderploeg and Scavia (1979):

Ei ¼

Wi−ð1=mÞ ; Wi þ ð1=mÞ

where Wi = fi / Σfj, fi is the proportion of the available prey type i in fish's diet and fj is the sum of fi for all prey types m. Values of E∗i near zero indicate random feeding, whereas values close to −1 and +1 indicate avoidance and preference, respectively. 3. Results 3.1. Plastic particles in water samples and fish guts A total of 220 plastic items were found in the six seawater samples, with an average number of 0.06 ± SE 0.008 particles per m− 3 (64,907.5 ± 18,296.5 particles km−2). Of all the plastic particles found in our samples, 14 (~ 7%) were N5.0 mm long, ranging from 5.2 to 58.8 mm (mean = 16.6 ± 3.6 mm). Most of these larger plastics were transparent (n = 6) or green (n = 6) threads. Most of the microplastics (i.e. ≤5 mm, n = 206) collected were orange, white, transparent, or blue fragments; the remaining microplastics were transparent or green threads, except for one film (Fig. 2 and Table 1). The overall median length of microplastics in surface waters was 2.3 ± 0.4 mm, 0.1– 5.0 mm long; four of these particles were 0.1–0.2 mm long, which is smaller than the epineuston net mesh size. A total of 48 plastic particles were found in the 20 D. muroadsi analysed, with an average of 2.5 ± 0.4 particles per fish. Sixteen (80%) of the 20 fish had ingested one to five particles (3.1 ± 0.4 particles per fish); no microplastic was found in the other four fish analysed. Of these microplastics, 80% were hard fragments, 12% soft fragments, 6% threads, 2% films. The median size of the plastic particles ingested by D. muroadsi was 1.3 ± 0.1 mm, ranging from 0.2 to 5.0 mm (Fig. 2). Four of these microplastics were smaller b0.3 mm (i.e. smaller than the net mesh size). A majority of microplastics ingested by the fish were blue (40%; Fig. 2 and Fig. 3a–f), transparent (26%), or white (26%); the others were black (4%), grey (2%), or green (2%).

3.2. Polymer analysis From the 29 analysed particles, 27 were microplastics, one was a protein, and one could not be matched to any polymer in the reference library; the latter two were discarded. We consider that visual sorting was effective because N90% of the particles were confirmed to be microplastics. Of these, the majority 81% (22) were polyethylene (PE), 15% (4) were plastic paint (2 alkyd resins and 2 epoxy-polyesters), and 4% (1) were polypropylene (PP). All blue particles and some of the white, black, and transparent fragments analysed were PE. Orange particles were alkyd resins or epoxy-polyesters, one white particle was an alkyd resin, and one black thread was made from PP. Infrared assignments for analysed microplastic samples are shown in Table S3 and selected representative spectra in Fig. S1. 3.3. Microplastics and natural prey selection by fish Decapterus muroadsi had a significantly different selectivity among microplastics of the four colours (orange, white, transparent, and blue) most commonly found in water samples (p b 0.0001; Table S4). The proportion of blue microplastics in D. muroadsi guts was higher than expected by their proportion in water samples (Fig. 4a); the relative electivity index confirmed a selectivity by fish for blue microplastics (Ei = 0.4; Fig. 4c). Fish selectivity for transparent particles was weak (Ei = 0.1; Fig. 4c), whereas white fragments, although often found in fish, were ingested in lower proportion than expected by their proportion in water samples (Ei = −0.4; Figs. 2 and 4a). Orange microplastics were avoided (Ei = −1.0; Fig. 4c) as none was ingested by fish despite a high proportion in the water (Fig. 4a). All plastic particles found in water samples and fish guts were broken fragments of larger pieces with some alteration of their surface. Most plastic particles were degraded (25%) or very degraded (56%), some were weathered (13%), and few showed incipient alterations (4%) of their surface. About half (49%) of the plastic fragments had sharp, torn, or pointy edges; the other fragments had rounded or smooth edges. Most (74%) microplastics were found in the intestine of the fish, whereas the remaining 26% were found in the stomach. The gut contents of D. muroadsi collected around Rapa Nui was dominated by unidentified fish eggs (~ 45% of total prey items; Table S1), copepods (~20%), and cirriped cyprid (~12%) and nauplius (~9%) larvae. Overall, fish fed selectively on copepods of different colours (p b 0.0001; Table S4). The relative electivity index calculated for the blue copepods Pontella sinica (Pontellidae; Fig. 3g) and Sapphirina sp. (Sapphirinidae; Fig. 3h) indicated that fish fed on these species more than expected by their proportion in the environment (Ei = 0.2; Fig. 4b,d and Table 1). Fish commonly consumed the transparent-blue copepod Corycaeus sp. (Figs. 3i and 4b, and Table 1), but no evidence of selectively was found for that species (Ei = −0.1; Fig. 4d). Non-blue copepods were not preferentially consumed by the fish (Ei = −0.3, Fig. 4b,d and Table 1). In addition, the mean size of the blue copepods P. sinica (2.0 mm; SD 0.9) and Sapphirina sp. (0.7 mm; SD 0.1) was overall similar to that of blue particles ingested by fish (Fig. 2). 4. Discussion 4.1. Microplastic abundance and polymer type The abundance of microplastics 0.3–5.0 mm recorded in our water samples (~ 60,000 particles km−2) was similar to that found by Eriksen et al. (2013; ~50,000 particles km−2) within the same area at Rapa Nui using similar sampling and analytic methods. The origin of the microplastics found in the environment is challenging to determine because their advanced degradation make their original shape unrecognizable. All of the blue and transparent microplastics analysed and most of the white ones, representative of all the particles found in our water

Please cite this article as: Ory, N.C., et al., Amberstripe scad Decapterus muroadsi (Carangidae) fish ingest blue microplastics resembling their copepod prey along the coast of Rapa Nui (Easter Island)..., Sci Total Environ (2017), http://dx.doi.org/10.1016/j.scitotenv.2017.01.175

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Fig. 2. Size-frequency distribution (% of the total number) of microplastics (bars) of the four colours most frequently found in the 6 superficial water samples (195 microplastics in total; 6 black, 3 grey, 2 red, 2 yellow, 1 purple and 1 green particles are not shown here) and in the 16 fish that had ingested at least one microplastic (45 microplastics; 2 black and 1 green particles are not shown here). Size distributions of three blue-pigmented copepod species (scatter plots) found in the water samples and in the 20 fish that ingested copepods are shown. (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)

and fish samples, are polyethylene (PE), a widely used polymer, which is likely to be present at the surface because it is less dense than water. These microplastics are of the same type and colour as typical

fishing gear (e.g. storage boxes, insulated containers) that are commonly used on large fishing vessels and often wash ashore as large fragments on Rapa Nui (Kiessling et al., 2017).

Table 1 Mean, median (bootstrapped standard-error (SE) from 1000 samples if not indicated otherwise) total number and proportion (% of total number) of microplastics and copepod prey of different colours in fish guts and in surface water samples along the coast of Rapa Nui (Easter Island). Sample

Colour

Mean (SE)

Median

Number of items

Proportion (% total)h

4.0 (0.9)a 5.8 (0.0)b 13.7 (1.8)c 8.3 (1.4)b 1.8 (0.6)d 16.3 (2.9)e 196.5 (56.4)f 1097.8 (516.1)b

4.0 (1.1)a 5.0 (1.9)b 12.0 (2.1)c 8.5 (2.1)b 1.3 (0.6)d 17.5 (3.1)e 154.0 (92.2)f 500.5 (598.8)b

24 35 82 50 6 98 1179 6587

11.6 17.0 39.8 24.3 2.9 1.2 15.0 83.8

1.3 (0.2)g 0.9 (0.3) 0.7 (0.2) 0.0 1.4 (0.0) 2.5 (0.7) 13.6 (3.6) 23.3 (5.9)

1.0 (0.2)g 0.0 (0.5) 1.0 (0.4) 0.0 1.4 2.0 (0.9) 7.5 (4.0) 14.0 (4.9)

20 11 13 0 2 40 217 372

45.5 25.0 29.5 0.0 2.0 2.3 21.8 75.9

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Items per 1000 m of water (number of samples = 6) Microplastics Blue Transparent White Orange Black Copepods Blue Transparent/blue Other Items per fish stomach (number of samples = 20) Microplastics Blue Transparent White Orange Black Copepods Blue Transparent/blue Other a b c d e f g h

Based on 944 samples. Based on 991 samples. Based on 978 samples. Based on 733 samples. Based on 998 samples. Based on 977 samples. Based on 997 samples. Percentage does not sum 100 because microplastics in proportion b2% of the total are not displayed here.

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Fig. 3. Examples of (a–f) blue microplastics in D. muroadsi digestive tracts, and (g) copepod prey Pontella sinica male, (h) Sapphirina sp. and (i) Corycaeus sp. in superficial water along the coast of Rapa Nui (Easter Island). Scale bars represent 0.5 mm. (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)

The soft orange and white microplastics analysed were epoxy-polyester and alkyd resins, which are present in paints like those used in ship hulls, and therefore may come from large fishing vessels operating in the South Pacific gyre as well as from small vessels used by local fishermen. High density polymers, such as polyvinylchloride, polyethylene terephthalate, and polyester, were not found in our water and fish samples, probably because these particles are negatively-buoyant in seawater and sink to deeper water layers and the sea bottom. 4.2. Similarities between microplastics and prey ingested by fish

Fig. 4. Description of the proportion of (a) microplastics and (b) copepod species of different colours ingested by fish (n = 16 fish with ≥1 microplastic blue, orange, white or transparent, and n = 20 fish with copepods) and in the surface water samples (n = 6). Vertical lines indicate median values; boxes and whiskers extend from the 25th to the 75th percentile and from the 10th to the 90th percentiles, respectively; circles indicate values outside this range. A total of 7864 and 629 copepods individuals were respectively counted in the water and stomach samples. Relative electivity index (Ei) indicating fish preference (Ei N 0), no preference (Ei = 0) or avoidance (Ei b 0) for (c) microplastics and (d) copepod species of different colours.

Amberstripe scad around Rapa Nui showed selectivity for blue PE microplastics that are similar in colour to blue-pigmented copepod species that they commonly prey upon, which suggests that fish mistakenly ingested microplastics resembling their natural prey. These bluepigmented copepods live near the sea surface (Herring, 1965; Herring, 1972) where positively-buoyant microplastics are also commonly found. Blue particles are also common in other planktivorous fish captured in the North Pacific gyre (Boerger et al., 2010; Davison and Asch, 2011) as well as in bottom-dwelling estuarine fish (Dantas et al., 2012; Possatto et al., 2011; Ramos et al., 2012). In those studies, the resemblance between blue microplastics ingested by the fish and their natural prey was suggested, but direct comparisons between microplastics and prey ingested by the fish were not made. White microplastics were not preferentially ingested by D. muroadsi despite the fact that white fish eggs were a common dietary item of the fish. Considering that most microplastics, including white ones, in our water samples were broken fragments with angular edges and irregular shapes, the risk that fish confuse them with fish eggs is probably low. The size of the blue microplastics found in D. muroadsi was within the size range of the blue-pigmented copepods consumed by the fish, further indicating that the fish might have mistakenly ingested microplastics similar to their natural prey. Overall, the size of the microplastics was similar to that found in Decapterus macrosoma in Indonesia (Rochman et al., 2015) and in other planktivorous fish species (reviewed by Lusher, 2015). Despite the presence of longer particles in the environment, the longest plastic debris found in D. muroadsi stomachs was 5 mm. Similarly, microplastics constituted the majority of debris ingested by other planktivorous fish of similar size in the

Please cite this article as: Ory, N.C., et al., Amberstripe scad Decapterus muroadsi (Carangidae) fish ingest blue microplastics resembling their copepod prey along the coast of Rapa Nui (Easter Island)..., Sci Total Environ (2017), http://dx.doi.org/10.1016/j.scitotenv.2017.01.175

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North Atlantic and the Baltic Sea (Neves et al., 2015; Rummel et al., 2016). Planktivorous fish may thus select fragments b5 mm because their common prey organisms are usually below that threshold. Our study revealed that 80% (16) of the Decapterus muroadsi individuals captured at Rapa Nui had ingested at least one microplastic item. This percentage is substantially higher than the 29% reported from the congener D. macrosoma (Rochman et al., 2015) in Indonesia and other planktivorous species worldwide. For example, microplastics occurred in 35% (Boerger et al., 2010) and b 10% of planktivorous fish in the North Pacific Subtropical Gyre (Davison and Asch, 2011; Gassel et al., 2013) and in the North Sea (Foekema et al., 2013), 40–52% of fish in the English channel (Lusher et al., 2013), and 11% of mesopelagic fish in the NE Atlantic (Lusher et al., 2015b). The relatively high proportion of D. muroadsi with ingested microplastics in our study may be due to the large ratio of microplastics to plankton in the highly oligotrophic waters of the subtropical gyres (Moore et al., 2001). Furthermore, visually foraging fish attack evasive prey from longer distances in clear compared to turbid waters (Aksnes and Utne, 1997). In the clear waters around Rapa Nui (Morel et al., 2010), D. muroadsi may thus be particularly susceptible to mistakenly targeting microplastics that they could not have assessed carefully. Indeed, microplastics floating at the sea surface may appear to a hunting fish as similar to copepods. Many copepods are similar in size, shape, and colour to some microplastics and spend most of their time moving slowly in the water column (Yen, 2013) or drifting with the currents like non-organic particles. Microplastics were also often found in estuarine fish (Ramos et al., 2012), indicating that benthic fish are also exposed to contamination in water with low visibility. However, it is still unclear whether benthic fish indirectly ingested microplastic when capturing their prey or whether visual cues induced a direct ingestion of the particles. 4.3. Potential hazards of ingested microplastics on fish Microplastics may induce deleterious effects to the organisms that ingested them (Cole et al., 2015; Lusher, 2015; Sussarellu et al., 2016). Specifically, the shape of a particle may reflect its potential to cause harm (Costa and Barletta, 2015; Wright et al., 2013b). In our study, most microplastics found in D. muroadsi stomachs were broken fragments with sharp edges that may potentially tear the digestive tract tissues. These plastics were also very degraded and therefore more susceptible than newer particles to the release of hazardous additives (Lusher, 2015) and to have accumulated at their surface pathogenic microorganisms (Foulon et al., 2016) or contaminants from the seawater (Avio et al., 2015; Bakir et al., 2014). The average number of microplastics we found in D. muroadsi (~2.5 particles per fish) was similar to that found in various other planktivorous pelagic fish in other regions of the world (see Table 10.9 in Lusher, 2015). Although this abundance may appear low, the fate of microplastics in fish digestive tract remains unclear (see Boerger et al., 2010). Our observations revealed that most microplastics found in D. muroadsi were located in the intestine of the fish, meaning that they would probably have been egested with faeces, but the time they had been in the digestive tract of the fish remains unknown. Experiments in the laboratory have revealed that some of the microplastics ingested by fish are defecated after a couple of hours, whereas others remain in the fish for several days (Hoss and Settle, 1990) or weeks (Ory et al., unpublished data), and therefore expose the organisms to the transfer of potential contaminants from the microplastics. Further studies are needed to determine the residence time of microplastics inside the guts of fish prey and predators to evaluate their exposure to potential contamination from the particles. Vertical transfer of microplastics from prey to predator has been shown experimentally in planktonic organisms (Setälä et al., 2014) and fish (Mattsson et al., 2015) and suggested for marine mammals from indirect observations (Eriksson and Burton, 2003; Fossi et al., 2014; Lusher et al., 2015a; Unger et al., 2016), seabirds (Hammer et

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al., 2016) and fish (Murray and Cowie, 2011). The high frequency of D. muroadsi that had ingested microplastics in our study implies that their predators are exposed to microplastic contamination through trophic transfer as species from the genus Decapterus are common prey for various commercially important predatory fish, such as tuna, lancetfish, swordfish or marlin (Abitia-Cardenas et al., 1999; Dambacher et al., 2010; Potier et al., 2007) and seabirds (Harrison et al., 1983). Due to their feeding behaviour, visual predators, such as planktivorous fish, may be particularly exposed to the presence of microplastic particles floating within the upper layers of the water column. This threat may be exacerbated in the clear waters of the South Pacific Gyre, where microplastics accumulate in great quantities (Eriksen et al., 2014). Our study suggests that fish mistakenly ingest microplastics resembling their natural prey and sets a standard for further studies to confirm this assumption through direct comparisons of the abundance of ingested and environmentally available microplastics and fish prey. The findings of our study also highlight the threat that anthropogenic litter may pose on the integrity of fragile remote oceanic ecosystems, such as those surrounding Rapa Nui, and the urgent need to manage plastic waste efficiently. Acknowledgements We thank Erika Meerhoff for allowing us access to her samples to take the pictures of copepods shown here, Katharina Herzog for the many hours she spent sorting plankton samples, Enrique Hey for capturing the fish, Evelyn Lostarnau for designing the pictures of Fig. 3, Diego F. Figueroa to have helped with the identification of the copepod species and Carla Martins for assistance with the microplastics photos. We are grateful to Lars Gutow, Boris Worm, Raymond Bauer and Erin Easton for their helpful comments on the manuscript. NCO was supported by a postdoctoral FONDECYT grant (No. 3150636) from the Chilean Ministry of Education. This study also received support from the Chilean Millennium Initiative (grant NC120030), and from the Fundação para a Ciência e Tecnologia (FCT - PT), through the strategic project UID/MAR/ 04292/2013 and the grant awarded to PS (SFRH/BSAB/113789/2015). Appendix A Supplementary data The supporting information includes additional detailed information about the infrared spectra of the particles found in water and fish (Fig. S1). Table S1 lists the prey found in fish. Table S2 lists the physical features described for each microplastic particles found in water samples and in fish guts. Table S3 lists infrared assignment for microplastic samples and Table S4 describes the statistical values of the analysis of fish preference for prey and microplastics colours. Supplementary data associated with this article can be found in the online version, at http:// dx.doi.org/10.1016/j.scitotenv.2017.01.175. References Abitia-Cardenas, L.A., Galvan-Magaña, F., Gutierrez-Sanchez, F.J., Rodriguez-Romero, J., Aguilar-Palomino, B., Moehl-Hitz, A., 1999. Diet of blue marlin Makaira mazara off the coast of Cabo San Lucas, Baja California Sur. Mexico. Fish. Res. 44, 95–100. Aksnes, D.L., Utne, A.C.W., 1997. A revised model of visual range in fish. Sarsia 82, 137–147. Anastasopoulou, A., Mytilineou, C., Smith, C.J., Papadopoulou, K.N., 2013. Plastic debris ingested by deep-water fish of the Ionian Sea (Eastern Mediterranean). Deep-Sea Res. I Oceanogr. Res. Pap. 74, 11–13. Avio, C.G., Gorbi, S., Milan, M., Benedetti, M., Fattorini, D., d'Errico, G., et al., 2015. Pollutants bioavailability and toxicological risk from microplastics to marine mussels. Environ. Pollut. 198, 211–222. Bakir, A., Rowland, S.J., Thompson, R.C., 2014. Enhanced desorption of persistent organic pollutants from microplastics under simulated physiological conditions. Environ. Pollut. 185, 16–23. Barboza, L.G.A., Gimenez, B.C.G., 2015. Microplastics in the marine environment: current trends and future perspectives. Mar. Pollut. Bull. 97, 5–12. Barnes, D.K., Galgani, F., Thompson, R.C., Barlaz, M., 2009. Accumulation and fragmentation of plastic debris in global environments. Philos. Trans. R. Soc. B Biol. Sci. 364, 1985–1998.

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Please cite this article as: Ory, N.C., et al., Amberstripe scad Decapterus muroadsi (Carangidae) fish ingest blue microplastics resembling their copepod prey along the coast of Rapa Nui (Easter Island)..., Sci Total Environ (2017), http://dx.doi.org/10.1016/j.scitotenv.2017.01.175