Marine Pollution Bulletin 136 (2018) 547–564

Contents lists available at ScienceDirect

Marine Pollution Bulletin

journal homepage: www.elsevier.com/locate/marpolbul

Double trouble in the South Pacific subtropical gyre: Increased plastic ingestion by fish in the oceanic accumulation zone T ⁎ Ana Markica, , Clarisse Niemandb, James H. Bridsonc, Nabila Mazouni-Gaertnerd, Jean-Claude Gaertnere, Marcus Eriksenf, Melissa Boweng a University of Auckland, Institute of Marine Science, Leigh 0985, New Zealand b University of Waikato, School of Science, Hamilton 3216, New Zealand c Scion, Manufacturing and Bioproducts, Rotorua 3010, New Zealand d Université de la Polynésie Française, UMR-241 Ecosystèmes Insulaires Océaniens, BP 6570, Tahiti, French Polynesia e Institut de Recherche pour le Development, BP 529, Papeete, Tahiti, French Polynesia f The 5 Gyres Institute, Los Angeles, CA 90016, USA g University of Auckland, School of Environment, Auckland 1010, New Zealand

ARTICLE INFO ABSTRACT

Keywords: Fish are an important food source for South Pacific (SP) island countries, yet there is little information on Easter Island contamination of commercial marine fish species by plastic. The aim of our study was to perform a broad-scale Marine plastic pollution assessment of plastic ingestion by fish common in the diet of SP inhabitants. We examined 932 specimens from Microplastics 34 commercial fish species across four SP locations, and some of the prey they ingested, for the presence of Rapa Nui marine plastics. Plastic was found in 33 species, with an average ingestion rate (IR) of 24.3 ± 1.4% and plastic Seafood contamination load of 2.4 ± 0.2 particles per fish. Rapa Nui fish exhibited the greatest IR (50.0%), significantly greater than in Trophic transfer other three locations. Rapa Nui is located within the SP subtropical gyre, where the concentration of marine plastics is high and food is limited. Plastic was also found in prey, which confirms the trophic transfer of mi- croplastics.

1. Introduction Plastic debris is ubiquitous in all marine compartments, including coasts, surface waters, water column and seafloor (Galgani et al., 2015), Once a promising material of the future, plastic has gradually grown where it occurs in various sizes, shapes, colours and specific gravities into a global environmental threat. Plastic is a versatile synthetic ma- (Andrady, 2003). Due to such diversity, plastic debris poses a risk to a terial used in all aspects of human existence, but since it is generally range of marine animals (Kühn et al., 2015). In the past decade, much non-biodegradable in natural environments, it tends to accumulate. of the research focus has shifted from macro debris to minute plastic Although the mass production of plastics started only after WWII particles, or microplastics, commonly defined as particles smaller than (Thompson et al., 2009), today there are no plastic-free natural en- 5mm(Auta et al., 2017; Avio et al., 2017a). Microplastics are particles vironments. Plastic has been found in deep ocean trenches (Fischer either purposefully manufactured as miniscule particles (primary mi- et al., 2015) as well as in desert animals (Walde et al., 2007; Ahmed, croplastics), such as plastic pellets and various abrasives (e.g. mi- 2011). While in the past some believed that ‘littering is an aesthetic crobeads) or are formed by mechanical degradation of larger plastic problem rather than an ecological one’ (p. 22, Bascom, 1974), others re- debris (secondary microplastics) (Avio et al., 2017a). Due to the small cognised plastic pollution as a potential environmental threat as early particle size, microplastics are highly bioavailable and readily ingested as the 1960s and 1970s (Carpenter et al., 1972; Rothstein, 1973). by various marine organisms commonly consumed as seafood, such as However, the attention of academia and media intensified only re- mussels (De Witte et al., 2014), clams (Davidson and Dudas, 2016), cently, and most likely due to concerns related to human health, since shrimps (Devriese et al., 2015), lobsters (Murray and Cowie, 2011), there is increasing evidence of plastic contamination of seafood squids (Rosas-Luis, 2016) and fish (Rochman et al., 2015). Plastic in- (Galloway, 2015; Rochman et al., 2015; Santillo et al., 2017; Wright gestion occurs directly (primary ingestion), or indirectly, by eating and Kelly, 2017). contaminated prey (secondary ingestion), and can be either intentional

⁎ Corresponding author at: 160 Goat Island Rd, Institute of Marine Science, Leigh 0985, New Zealand. E-mail address: [email protected] (A. Markic). https://doi.org/10.1016/j.marpolbul.2018.09.031 Received 26 June 2018; Received in revised form 15 September 2018; Accepted 17 September 2018 0025-326X/ © 2018 Elsevier Ltd. All rights reserved. A. Markic et al. Marine Pollution Bulletin 136 (2018) 547–564

(mistaken prey identity) or unintentional (accidental ingestion through Zealand are some of the major population centres in the South Pacific filter-feeding or grazing) (Ryan, 2016). There is evidence that ingested region, while Rapa Nui has a low population, but was chosen due to its plastic debris causes an array of detrimental consequences, including position within the South Pacific subtropical gyre. We aimed to collect the build-up of toxic compounds associated with plastic debris, either locally caught species from various habitats and trophic levels. Al- directly from ingested plastic (Rochman et al., 2013) or via trophic though there is always a degree of uncertainty to the origin of the fish, transfer from prey to predator (Batel et al., 2016). This justifiably we made sure all the specimens were fresh, caught by local fishermen creates concern among seafood consumers about their health and and not imported. No ethical permit was needed for sample collection wellbeing (Santillo et al., 2017). as the fish were not caught specifically for research, but were obtained Plastic ingestion by marine fish has been studied intensively re- from local markets or fishermen. The species were identified by fish- cently, with at least 39 studies published since 2017. Most studies were eries officers, fishermen and fellow scientists. Further identification was conducted in the North Atlantic region, while the South Pacific region confirmed using Fishbase (Froese and Pauly, 2016), FAO (2016) and has been poorly studied. In Pacific Island countries, seafood is an in- New Zealand Ministry of Fisheries identification keys (McMillan et al., valuable food source (Gillett, 2011) and the assessment of plastic con- 2011). The number of collected species varied across locations and tamination of fish in this vast ocean region is of crucial importance. At depended on the availability of the local fish. The sample size (i.e. the the time of the preparations for this study (2015), there was no in- number of specimens per species) on all locations was N ≥ 10. The formation available on the state of the South Pacific fish. Meanwhile, collection was as random as possible, with specimens of the same six studies on plastic ingestion by fish in this region have been pub- species being collected from various sources on various days. The entire lished. However, only one of those studies (Mizraji et al., 2017) used GI tracts were removed from the fish, from the oesophagus to the vent. the recommended analytical method (Dehaut et al., 2016; Karami et al., The samples where the stomachs were everted, or the regurgitation 2017a), which includes chemical digestion of organic portion of the gut occurred, were not collected. A detailed description of the methods is content for more effective detection and isolation of plastic debris. In provided in the Supplementary information (Table S1). Biometrics data the other five studies, the gut content was only visually inspected, by (standard, total and fork length (cm), and mass (g)) of individual fish naked-eye or under a microscope (Cannon et al., 2016; Ory et al., 2017, were taken where possible prior to evisceration (Table S2). 2018; Forrest and Hindell, 2018; Halstead et al., 2018). The aim of our study was to perform a broad-scale assessment of 2.2. Diet analysis and gut fullness plastic ingestion by commercial fish species, from different habitats and trophic levels, commonly present in the diet of South Pacific Islanders. A basic diet analysis was done to be able to place each species into a Additionally, we were interested in investigating the differences in distinct trophic group, based on their feeding strategy. When much of plastic ingestion by fish inhabiting the centre of convergence of the the stomach content was digested or unidentifiable, additional in- subtropical gyre (near Rapa Nui, or Easter Island) and other sampling formation was extracted from Fishbase (Froese and Pauly, 2016) and locations in the South Pacific. A subtropical gyre is an oceanic con- FAO (2016). It should be noted that some stomach content might not be vergence zone where plastic debris accumulates in great abundance representative of the fish usual diet as it can easily be confounded by (Eriksen et al., 2013), and where the organisms are exposed to much bait items (e.g. bread, fish heads). The guts with the items identified as higher concentrations of plastic debris than outside of the gyre. Fur- bait were not included in the analysis to avoid the potential con- thermore, the transfer of plastic debris along the food web has been tamination from bait. Additionally, gut fullness index (GF, from 1 to 5) demonstrated experimentally (Farrell and Nelson, 2013), but there is no was recorded for each digestive tract based on visual assessment, one previous evidence of trophic transfer in field subjects. We intended to being empty and five being completely full. We acknowledge that this investigate this route of plastic contamination in fish by also examining type of analysis is subjective, but since only one person examined all the the gastrointestinal tract of undigested prey items from the stomach of guts and assigned the GF index, the estimation was consistent predatory fish. Lastly, we aimed to develop a cheap analytical method throughout the entire examination. which could be easily replicated in developing countries. Thus, the questions we address in our field study are: 2.3. Method testing

1. Is there a significant difference in plastic ingestion between the fish We established an analytical protocol which was a combination of from the South Pacific subtropical gyre (accumulation zone) and the previously published methods (Avio et al., 2015; Rochman et al., 2015). other three locations? The protocol was tested on the gut content of two genera, Scaber spp. 2. Is there evidence of trophic transfer of plastics, or secondary in- (Scaridae, parrotfish) and Lethrinus spp. (Lethrinidae, emperor), on five gestion? specimens of each genus. Each sample was spiked with 15 polyethylene 3. Are there patterns in the occurrence of plastic ingestion among ex- microbeads of three different colours (five red, five blue and five amined species with respect to trophic levels, feeding preferences transparent) and sizes ranging from 100 to 500 μm (more details in and habitats? Table S1). These two genera were selected due to the difference in their 4. Is there a common size, type, colour, opacity and polymer type of gut content, which represent the two extreme types of the gut content

marine plastics ingested by South Pacific fish? with respect to their ability to dissolve in H2O2 and the subsequent detectability of plastics during the microscopic analysis. The gut con- 2. Methods tent of parrotfish dissolves almost entirely, while the gut content of emperor usually contains plenty of undissolvable residue, such as shells, 2.1. Sample collection bones, scales and sediment, which makes the microscopic analysis more difficult. Samples of gastrointestinal (GI) tracts of 34 marine fish species (Table 1) were collected from four study locations (Auckland, Samoa, 2.4. Sample processing Tahiti, Rapa Nui) in the South Pacific region between September 2015 and October 2016 (Fig. 1). The sampling locations were selected based The samples were processed randomly, rather than consecutively on their population size or their geographical position in the South per species or per location, to avoid potential systematic errors due to Pacific. Greater concentrations of plastic debris are usually associated tired eye or lack of concentration. The gut content was extracted from with human population centres (Andrady, 2017), or accumulation the stomachs and the intestines onto a clean metal or ceramic plate zones of subtropical gyres (Eriksen et al., 2013). Samoa, Tahiti and New using a metal spatula. The content was first examined by naked-eye for

548 A. Markic et al. Marine Pollution Bulletin 136 (2018) 547–564

Table 1 A list of species collected from four locations (AKL – Auckland, SA – Samoa, TH – Tahiti, RN – Rapa Nui, N – sample size (number of individuals), Av. TL – average total body length, Av. m – average wet body mass, SE – standard error).

Order Family Species Common name Location N Av. TL ( ± SE) (cm) Av. m ( ± SE) (g)

Beloniformes Exocoetidae Cheilopogon pitcairnensis Flying fish TH 21 26.8 ± 0.5 167.0 ± 6.5 Hemiramphidae Hyporhamphus ihi Garfish AKL 24 24.9 ± 0.6 32.7 ± 2.3 Mugiliformes Mugilidae Ellochelon vaigiensis Squaretail mullet TH 33 31.0 ± 1.0 334.3 ± 34.5 Mugil cephalus Grey mullet AKL 22 n/a n/a Perciformes Acanthuridae Acanthurus lineatus Lined surgeonfish SA 24 22.6 ± 0.4 163.6 ± 6.8 Ctenochaetus striatus Striated surgeonfish SA, TH 29, 27 21.1 ± 0.2 161.7 ± 6.2 Naso lituratus Orangespine unicornfish SA 28 24.4 ± 1.0 241.5 ± 18.6 Naso unicornis Bluespine unicornfish SA 30 26.6 ± 1.8 419.6 ± 89.1 Carangidae Caranx papuensis Brassy trevally TH 32 10.7 ± 0.2 16.6 ± 0.7 Decapterus macrosoma Shortfin scad TH 25 20.5 ± 0.2 68.0 ± 2.6 Decapterus muroadsi Amberstripe scad RN 25 23.0 ± 1.0 119.0 ± 22.0 Seriola lalandi Yellowtail kingfish AKL 15 n/a n/a Trachurus novaezelandiae Yellowtail jack mackerel AKL 31 28.4 ± 0.7 206.7 ± 16.0 Centrolophidae Schedophilus velaini Violet warehou RN 14 n/a n/a Cheilodactylidae Nemadactylus macropterus Tarakihi AKL 23 35.7 ± 0.7 n/a Coryphaenidae Coryphaena hippurus Mahi-mahi TH 10 138.6 ± 3.3 10,910.0 ± 883.0 Gempylidae Thyrsites atun Snake mackerel RN 28 n/a n/a Kyphosidae Girella tricuspidata Luderick, parore AKL 20 34.8 ± 0.8 686.1 ± 44.6 Kyphosus sandwicensis Pacific chub RN 39 n/a n/a Lethrinidae Gnathodentex aureolineatus Striped large-eye bream TH 29 25.0 ± 0.2 263.2 ± 6.3 Lethrinus amboinensis Ambon emperor SA 26 38.2 ± 1.3 655.8 ± 71.5 Lethrinus obsoletus Orange-striped emperor SA 30 26.9 ± 0.3 243.7 ± 10.0 Lutjanidae Lutjanus gibbus Red snapper SA 29 32.4 ± 1.2 500.9 ± 54.7 Priacanthidae Heteropriacanthus cruentatus Glasseye RN 10 36.7 ± 1.7 n/a Scaridae Scarus niger Dusky parrotfish SA 30 25.3 ± 0.6 336.8 ± 22.5 Scarus oviceps Dark capped parrotfish SA 45 25.2 ± 0.4 231.8 ± 12.9 Scarus psittacus Common parrotfish TH 30 21.1 ± 0.2 164.8 ± 5.0 Scombridae Katsuwonus pelamis Skipjack tuna SA 26 69.6 ± 1.7 6018.5 ± 457.3 Thunnus albacares Yellowfin tuna SA, TH, RN 26, 33, 10 74.2 ± 1.8 5228.7 ± 343.7 Siganidae Siganus punctatus Goldspotted rabbitfish SA 29 21.1 ± 0.5 170.7 ± 12.4 Sparidae Pagrus auratus Australasian snapper AKL 22 32.9 ± 0.4 n/a Sphyraenidae Sphyraena forsteri Bigeye barracuda SA 12 58.0 ± 1.9 869.2 ± 105.0 Scorpaeniformes Triglidae Chelidonichthys kumu Bluefin gurnard AKL 27 34.0 ± 0.6 n/a Tetraodontiformes Monacanthidae Meuschenia scaber Leatherjacket AKL 19 27.0 ± 0.5 269.1 ± 12.7 larger plastic particles. If the sample contained an entire prey item with or objects, visually resembling synthetic materials, were stored in 2 ml their GI tract intact, the individual was rinsed with H2O2, removed and glass vials for further chemical analysis. Size, type, colour and opacity used for the analysis on secondary ingestion. After the rough visual were determined on a subsample of retrieved plastic particles. The examination for plastics, the content was homogenised with tweezers longest dimension of each microplastic was measured under a micro- and needles to facilitate chemical digestion. Homogenised samples scope using a micrometer slide and microscope camera software (Am- were subjected to chemical digestion in filtered 15% H2O2 (supplier Scope). The analytical procedure was the same for both primary and Consolidated Chemicals NZ Ltd) in clean glass jars at a 1:3 ratio (one secondary ingestion analysis. unit of the gut content into three units of H2O2). The jars were covered loosely with aluminium foil and heated at 60 °C until all organic matter 2.5. Polymer identification was digested (typically < 24 h, with a maximum of 14 days in case of larger samples). Digested samples were vacuum filtered using a set of Fourier transform infrared (FTIR) spectroscopy was used for up to four stainless steel filters (63 μm, 260 μm, 530 μm and 1 mm mesh polymer identification. FTIR spectra were obtained for a randomly sizes) (Fig. 2), to facilitate microscopic analysis by size separation of chosen subset of microplastics (128 particles) across all species, loca- undigested remains. Each stainless-steel filter was visually examined tions and habitats. Before analysis, all samples were dried at 70 °C for under a dissecting microscope at 6 to 40× magnification. All particles 4 h. Larger microplastics (> 300 μm) were analysed using a Bruker

Fig. 1. Map of sampling locations.

549 A. Markic et al. Marine Pollution Bulletin 136 (2018) 547–564

Fig. 2. Vacuum filtration system with a set of stainless steel filters. The rubber rings are used for sealing, and the polyvinyl chloride (PVC) pipe rings are used for separating the filters. The wide top ring is used to apply pressure to the rings to seal the filters.

Tensor 27 Instrument with a diamond attenuated total reflectance The differences in proportions (i.e. ingestion rates) between mul- (ATR) cell acquiring 32 background and sample scans from 725 to tiple groups were examined using chi-square test with Monte Carlo − − 4000 cm 1 at 4 cm 1 resolution. Smaller microplastics (< 300 μm) method (5000 simulations). The test included the Marascuilo procedure were analysed using a Bruker Tensor 27 Instrument connected to a which compares all pairs of proportions and identifies which pair is

Bruker IRScope II equipped with a mercury cadmium telluride (MCT) responsible for the rejection of H0. Spearman correlation for propor- detector. Samples were placed in a diamond compression cell and tions was used to analyse the relationship between ingestion rates of analysed in transmission with 32 background and samples scans from each species and their trophic level. Pearson correlation was used to − − 725 to 4000 cm 1 at 4 cm 1 resolution. All spectra were baseline examine the relationship between the gut fullness index and plastic load corrected using Bruker OPUS 7.2 software. More details on polymer per specimens which contained plastic. The statistical software XLSTAT characterisation can be found in Table S1. was used for these analyses. Only primary ingestion data were used for all analyses.

2.6. Data analysis 3. Results

Plastic ingestion is most commonly expressed as plastic ingestion 3.1. Information on collected species rate (IR), which is a percentage of individual fish of the same species that contained plastic. Plastic ingestion can also be expressed as plastic We analysed a total of 932 gastrointestinal tracts of 34 marine fi load (PL), or the number of plastic pieces per individual sh. Here, species, belonging to 5 orders and 20 families. There were 203, 363, plastic load per species is an arithmetic mean of plastic load values of 240 and 126 specimens analysed from Auckland, Samoa, Tahiti and all individuals with plastic. With respect to the terminology, if the term Rapa Nui, respectively. Sample sizes ranged from 10 to 45, with an plastic ingestion is used, it refers to primary ingestion, and overall in- average of 27 specimens per species (Table 1). Most examined in- gestion includes primary and secondary ingestion. In tabular and gra- dividuals had total body length between 20 and 40 cm, weighing < 1 kg phic display of results, we used standard error to express the variability (Table 1, detailed in Table S2). The smallest individuals were the ju- of data. As a measure of central tendency, we used weighted averages veniles of Caranx papuensis (Carangidae, brassy trevally) and the largest for ingestion rates, and arithmetic mean for plastics load. To express the were adult Coryphaena hippurus (Coryphaenidae, mahi-mahi), both fi precision of ingestion rate values, we provided con dence intervals for species collected in Tahiti. Due to insufficient consistency in recording fi fi 95% con dence level. The con dence intervals were computed in the sex data, they were not included in the table. Life stage was esti- software package SAS using Wilson score method with continuity cor- mated based on body lengths and the presence of gonads. Most in- rection, based on the formula provided by Newcombe (1998) (Table dividuals were adult fish, except brassy trevally from a Tahiti lagoon S1). and Thunnus albacares (Scombridae, yellowfin tuna) from the offshore fi ff To examine whether there was a signi cant di erence between waters of Tahiti and Samoa, which were all juveniles (except one larger several groups of interest or relationship between variables of interest, yellowfin tuna specimen from Samoa). the following hypotheses were tested: ff H0. There is no di erence in plastic ingestion rates across the four 3.2. Method testing sampling locations. H . There is no difference in plastic ingestion rates across different The recovery of test microbeads (15 per sample) from the samples 0 fi habitats. with little inorganic residue (parrot sh) was 98.7%, while from the samples with more residue (emperor) it was 85.3% (Table S3). Some ff ff H0. There is no di erence in plastic ingestion rates between di erent coloured microbeads faded during chemical digestion. trophic guilds.

H0. There is no correlation between plastic ingestion rates for each fish 3.3. Plastic ingestion species and their trophic levels. Of the 34 species examined, overall plastic ingestion was recorded H . There is no correlation between gut fullness index and plastic load. 0 in 33 species (Table 2). Plastic debris was found in 226 out of 932

550 A. Markic et al. Marine Pollution Bulletin 136 (2018) 547–564

Table 2 Plastic ingestion rates and plastic load for examined species (N – sample size, PI – primary ingestion, SI – secondary ingestion, PIR – primary ingestion rate, IR – − overall ingestion rate (PI + SI), SE – standard error, CI – 95% confidence interval, PL – overall plastic load (PI + SI), pc ind 1 – pieces per individual fish which ingested plastic).

− Species N (#) Fish with PI (#) Fish with SI (#) PIR (%) IR (%) IR ± SE IR CI lower IR CI upper No. of plastics PL (pcs ind 1)PL±SE

Auckland G. tricuspidata 20 14 0 70.0 70.0 10.2 45.7 87.2 83 5.9 1.3 M. scaber 19 7 0 36.8 36.8 11.1 17.2 61.4 14 2.0 0.5 S. lalandi 15 3 1 20.0 26.7 11.4 8.9 55.2 4 1.0 0.0 M. cephalus 22 3 0 13.6 13.6 7.3 3.6 35.6 6 2.0 0.6 N. macropterus 23 2 0 8.7 8.7 5.9 1.5 29.5 7 3.5 0.5 P. auratus 22 1 0 4.5 4.5 4.4 0.2 24.9 1 1.0 0.0 C. kumu 27 1 0 3.7 3.7 3.6 0.2 20.9 2 2.0 0.0 T. novaezelandiae 31 1 0 3.2 3.2 3.2 0.2 18.5 1 1.0 0.0 H. ihi 24 0 0 0.0 0.0 0.0 0.2 23.1 0 0.0 0.0 Total for Auckland 203 32 1 15.8 16.3 2.6 11.6 22.2 118 3.6 0.7 Samoa T. albacares 25 6 2 24.0 32.0 9.3 10.2 45.5 14 1.8 0.5 L. gibbus 29 6 1 20.7 24.1 7.9 11.0 43.9 12 1.7 0.0 S. niger 30 7 0 23.3 23.3 7.7 10.6 42.7 8 1.1 0.5 K. pelamis 26 6 0 23.1 23.1 8.3 9.8 44.1 9 1.5 0.2 L. amboinensis 26 6 0 23.1 23.1 8.3 9.8 44.1 10 1.7 0.3 C. striatus 29 6 0 20.7 20.7 7.5 8.7 40.2 6 1.0 0.3 A. lineatus 24 4 0 16.7 16.7 7.6 5.5 38.2 6 1.5 0.5 N. unicornis 30 5 0 16.7 16.7 6.8 6.3 35.5 7 1.4 0.4 S. forsteri 12 2 0 16.7 16.7 10.8 2.9 49.1 3 1.5 0.5 N. lituratus 28 4 0 14.3 14.3 6.6 4.7 33.6 7 1.8 0.5 S. punctatus 29 4 0 13.8 13.8 6.4 4.5 32.6 7 1.8 0.5 L. obsoletus 30 4 0 13.3 13.3 6.2 4.4 31.6 5 1.3 0.3 S. oviceps 45 5 0 11.1 11.1 4.7 4.2 24.9 14 2.8 1.6 Total for Samoa 363 65 3 17.9 18.7 2.0 14.9 23.2 108 1.6 0.1 Tahiti E. vaigiensis 33 16 0 48.5 48.5 8.7 31.2 66.2 68 4.3 1.7 C. papuensis 32 14 0 43.8 43.8 8.8 26.8 62.1 33 2.4 0.6 D. macrosoma 25 7 0 28.0 28.0 9.0 12.9 49.6 8 1.1 0.2 C. striatus 27 7 0 25.9 25.9 8.4 11.9 46.6 11 1.6 0.4 T. albacares 33 5 2 15.2 21.2 7.1 9.6 39.4 10 1.4 0.0 C. hippurus 10 2 0 20.0 20.0 12.6 3.5 55.8 4 2.0 0.6 S. psittacus 30 5 0 16.7 16.7 6.8 6.3 35.5 5 1.0 0.6 C. pitcairnensis 21 2 0 9.5 9.5 6.4 1.7 31.8 2 1.0 0.0 G. aureolineatus 29 2 0 6.9 6.9 4.7 1.2 24.2 2 1.0 0.0 Total for Tahiti 240 60 2 25.0 25.8 2.8 20.5 31.9 143 2.3 0.5 Rapa Nui T. albacares 10 7 0 70.0 70.0 14.5 35.4 91.9 22 3.1 1.1 D. muroadsi 25 16 0 64.0 64.0 9.6 42.6 81.3 39 2.4 0.6 S. velaini 14 8 0 57.1 57.1 13.2 29.7 81.2 20 2.5 0.5 K. sandwicensis 39 20 0 51.3 51.3 8.0 35.0 67.3 80a 4.0 0.7 T. atun 28 8 1 28.6 32.1 8.8 16.6 52.4 17 1.9 0.0 H. cruentatus 10 3 0 30.0 30.0 14.5 8.1 64.6 3 1.0 1.0 Total for Rapa Nui 126 62 1 49.2 50.0 4.5 41.0 59.0 181 2.9 0.3 Total for all locations 932 219 7 23.5 24.3 1.4 21.6 27.2 550 2.4 0.2

Note: a The number of plastic particles extracted from K. sandwicensis was 184 in total, but 104 particles were found in only one specimen, so these were excluded from calculations. specimens. Thus, the average overall ingestion rate across all species 3.3.1. Primary and secondary ingestion and locations was 24.3%, with 95% confidence intervals ranging from Out of 226 specimen which contained ingested plastic, 219 had 21.6 and 27.2%. Altogether, 550 particles were found in 226 fish, a plastic debris in their own gut content, which is considered primary plastic load of 2.4 ± 0.2 particles per fish. ingestion. To investigate the occurrence of secondary ingestion (i.e. No plastic ingestion was found only in Hyporhamphus ihi plastic ingestion by prey), we selected well-preserved prey of ten (Hemiramphidae, garfish) from New Zealand. The minimum ingestion coastal and offshore predatory fish species and examined their GI tract rate was 3.2% found in another New Zealand species, Trachurus no- for the presence of plastic debris (Table S4). A total of 17 plastic pieces vaezelandiae (Carangidae, yellowtail jack mackerel). The maximum were retrieved from 176 prey items (squid, crab, salp and small fish) ingestion rate of 70% was also recorded in a New Zealand species, from 10 out of 57 examined individual fish, thus secondary ingestion Girella tricuspidata (Kyphosidae, parore), as well as in yellowfin tuna was found in 17.5% of examined individuals. Since the prey samples from Rapa Nui. The maximum load per single fish was exceptionally were often pooled, it is not possible to know whether these 17 plastic high, and to our knowledge, it is the greatest amount of plastic debris pieces were found in separate prey items, or some prey had ingested reported from an individual fish. As much as 104 pieces of marine more than one piece of plastic. Out of 57 individuals, 22 were examined plastics were found in one Kyphosus sandwicensis (Kyphosidae, Pacific only for secondary ingestion (excluded from Table 2), while 35 were chub) from Rapa Nui, which was about 30 cm long and weighed ap- examined for both primary and secondary ingestion (included in proximately 500 g. Table 2). Of these 35, only primary ingestion was found in 14 in- dividuals (40%), only secondary ingestion was found in 7 individuals

551 A. Markic et al. Marine Pollution Bulletin 136 (2018) 547–564

3.6. Plastic ingestion with respect to trophic levels and guilds

Spearman correlation test showed no significant relationship (p > 0.05; R = −0.1) between the ingestion rate of each species and their trophic level. Based on the diet analysis, each fish species was placed into one of the five trophic guild categories: pelagic predators (nektivores feeding on fish and squid), benthic predators (fish feeding on benthic vagile invertebrates and small fish), planktivores (fish eating zooplankton and phytoplankton, including large zooplankton such as jellyfish and salps), omnivores (fish feeding on plant and animal matter, including detritus), and grazers (benthic herbivores, corallivores, spongivores and feeders on other sessile organisms) (Table S5). A sig- nificant difference was found in ingestion rates between benthic pre- dators and omnivores (p < 0.05) (Fig. 5).

3.7. Gut fullness

Most digestive tracts which contained plastic debris were com- pletely full (GF = 5, 90 guts), and only four were empty (GF = 1). Fig. 3. Comparison of primary ingestion rates across all four locations. There was a significant positive relationship (p < 0.05, R = +0.98) The box plot includes the weighted average (X), median value (horizonal line between the GF index and the average plastic load per specimens which inside the ‘box’) and outliers (○). contained plastics (Fig. 6).

(20%), and no primary or secondary ingestion was found in the re- 3.8. Properties of recovered plastics maining 14 individuals (40%). For further statistical analyses, only the primary ingestion data were used. 3.8.1. Size Out of 550 plastic particles recovered from fish guts (excluding 104 pieces from Pacific chub from Rapa Nui), a random subsample of 351 3.4. Plastic ingestion across locations particles was used for size distribution analysis. The great majority (95%) of plastic particles were microplastics smaller than 5 mm (Fig. 7). We found a significant difference in plastic ingestion rates between The most abundant were particles between 100 and 500 μm, followed the four locations, with Rapa Nui driving the difference (p < 0.05) by 1 to 5 mm particles. (Fig. 3). Marascuilo procedure showed that the other three locations were not significantly different from each other. The lowest average 3.8.2. Type ingestion rate per location was recorded in Auckland (15.8%), while Plastic particles were grouped into three groups based on the type: almost half (49.2%) of all examined fish from Rapa Nui contained fragments (broken pieces of hard plastic), films (thin soft plastic, such marine plastics. With respect to the overall plastic load, there was no as plastic bags or paint chips) and fibres (long and thin fibrous type of distinct pattern among locations. However, if G. tricuspidata, which plastic). Fibres were counted only if airborne contamination was ruled exhibited particularly high plastic load (Table 2), was excluded from out. Plastic debris recovered from all locations comprised 49% of plastic calculations for overall plastic load for Auckland, the trend would be fragments, 33% of plastic fibres and 18% of plastic film (Fig. 8a). With more similar to the trend observed in plastic ingestion rates. respect to habitats, fragments were more commonly found in oceanic pelagic habitats, while fibres were more common in coastal benthic habitats (Fig. 8b, c). With respect to trophic guilds, fibres were more 3.5. Plastic ingestion with respect to habitats often ingested by grazers and omnivores, while fragments by benthic and pelagic predators (Fig. 8d). To look at the patterns in plastic ingestion rates across different habitats, we broadly divided habitats into their horizontal (neritic, 3.8.3. Colour neritic-oceanic and oceanic) and vertical (benthic and demersal, ben- Colour distribution was determined on a random subsample of 396 thopelagic, and pelagic) components. Benthic and demersal species live plastic particles. Predominant colours were black (22%), blue (18%), on or near the bottom and feed on organisms (plant or animal) or dead white (17%) and colourless (12%) (Fig. 9a). All other colours con- matter (detritus) available there. Benthopelagic species live and feed on tributed with < 10%. There was a difference in colour distribution with the bottom as well as throughout the water column. Pelagic species respect to locations, habitats and feeding (Fig. 9b, c, d). forage on organisms that live at the surface or throughout the water column (Froese and Pauly, 2016). Neritic species live in coastal areas, 3.8.4. Opacity while oceanic species inhabit open waters. There are some species, such Opacity of the particles (i.e. transparent or opaque) was determined as Seriola lalandi (Carangidae, yellowtail kingfish), which live in both on a subsample of 480 plastic particles. Most particles were opaque coastal and oceanic waters (Table S5). (67%). The proportion of opaque particles decreases from Auckland to Since we found that the species from Rapa Nui had significantly Rapa Nui (Fig. 10). higher ingestion rates, we excluded them from further analyses. Species from other locations were pooled into categories, regardless of the lo- 3.8.5. Polymer type cation, to assure there are enough specimens in each category for a A random subsample of 128 plastic debris items (52 fragments, 35 more robust analysis. The vertical habitat components were sig- film and 41 fibres) was subjected to polymer characterisation using nificantly different from each other (p < 0.05), with benthopelagic FTIR spectroscopy. Of these, the analysis was inconclusive for six par- fish exhibiting the highest ingestion rates (31.4%) (Fig. 4a). With re- ticles due to either poor quality spectra or insufficient match with the spect to horizontal distribution, the ingestion rates were not different spectral database. Of the subset analysed, only one particle (CaCO3, among each other (p > 0.05) (Fig. 4b). HQI = 88%) was incorrectly identified as microplastic. Most common

552 A. Markic et al. Marine Pollution Bulletin 136 (2018) 547–564

a) b) 30 Pelagic 25 20 Benthopelagic 15 10 Benthic/demersal 5 Ingeson rate (%) 0 5 10 15 20 25 30 35 40 0 Ingeson rates (%) Neric Neric-oceanic Oceanic

Fig. 4. Plastic ingestion rates across a) vertical and b) horizontal components of marine habitats. Error bars present standard error.

4. Discussion Pelagic predator 4.1. General findings on plastic ingestion Benthic predator We found marine plastic debris in 97% of examined fish species (33 Plankvore out of 34), and almost a quarter (24.3%) of individual fish (226 out of 932) from four locations across the South Pacific region. In a similar Omnivore study, where the fish were collected from two distant locations, Indonesia and California, US, the average ingestion rate across 21 Grazer species was 24.2% (31 out of 128 individuals) (Rochman et al., 2015). Research on plastic ingestion by fish in the Pacific region started 0 5 10 15 20 25 30 35 40 45 only several years ago, and there is still limited information available on the matter. In a recently published study, Forrest and Hindell (2018) Ingeson rate (%) also collected fish from several locations across the South Pacific. They examined 126 specimens of 24 fish species from Lord Howe Island Fig. 5. Ingestion rates with respect to feeding strategies. Error bars present standard error. (Australia), French Polynesia and Henderson Island (British Overseas Territory), and found plastic in 10 individuals (7.9%) of six species (25%). Cannon et al. (2016) examined 20 marine fish species collected 3.5 in southeast Australian waters and Southern Ocean. They recovered Average PL 100 3 plastic debris from 1 out of 327 specimens, which is < 0.3%. In another ) -1 No. of stomachs study from Australian waters, substantially greater ingestion rates 80 2.5 (43%) were obtained from three fish species collected from the Sydney Harbour (Halstead et al., 2018). Further in the eastern South Pacific, 2 60 Ory et al. (2017) assessed plastic ingestion by Decapterus muroadsi 1.5 (Carangidae, amberstripe scad) from Rapa Nui, and uncovered plastics 40 from 80% of the specimens (16 out of 20). Ory et al. (2018) also col- 1 lected seven fish species along the west coast of South America and Av. plasc load (pcs ind

20 Number of stomachs 0.5 documented low ingestion rates of 2.1% (6 out of 292 individuals) in five species (71%). Mizraji et al. (2017) examined five fish species from 0 0 Chile and all had 100% ingestion rates. Methods for detecting plastic 12345 used in the Pacific studies, with the exception of Mizraji et al. (2017), Gut fullness included either naked-eye examination or microscopic analysis of the Fig. 6. Average plastic load per specimens which contained plastics, and the gut content. While these methods used to be widely accepted in the number of stomachs with plastics, for each category of gut fullness index (1 – past, current trends in analytical methodology tend to gravitate towards empty, 5 – completely full). Error bars present the standard error of plastic load. the more robust methods which include either chemical (as in Mizraji et al., 2017) or enzymatic digestion (Karlsson et al., 2017) of the gut ff polymer types were: polyester (28%), polyethylene (26%), rayon content for more e ective detection of plastic. Although the opportu- (17%), polypropylene (9%), polyvinyl chloride (7%) and other poly- nistic nature of sampling and the infeasibility of conducting more mers (12%), such as polyamide (4%), polyurethane (3%), acrylic (3%), complex analytical procedure is fully acknowledged, we suggest that, fi fi rubber (2%) and styrene acrylonitrile copolymer (< 1%) (Fig. 11a). thus far, the magnitude of plastic ingestion by South Paci c sh has The composition of extracted plastic debris by polymer type varied generally been underestimated. across locations (Fig. 11b). Different polymers were also present in different types of microplastics and vice versa (Fig. 11c, d). More than 4.1.1. Trophic transfer of plastic debris half of the analysed plastic debris was negatively buoyant (62%). Most To our knowledge, secondary plastic ingestion has not previously fibres and film were negatively buoyant, while the fragments were been investigated in any of the studies on plastic ingestion by wild mainly positively buoyant (Fig. 12a). The distribution of polymers marine fish. We found evidence of trophic transfer of plastic debris from across the vertical component of the habitats, according to their prey to predator in 10 out of 57 examined individual fish. This shows buoyancy (positive or negative), did not show any pattern, and sinking that the indirect uptake of marine plastics by fish via prey, previously and floating plastics were present in all three categories (Fig. 12b). tested in laboratory conditions (e. g. Santana et al., 2017), indeed oc- curs in nature. Au et al. (2017) emphasise the need for more research into trophic transfer of microplastics.

553 A. Markic et al. Marine Pollution Bulletin 136 (2018) 547–564

3% 7% 4% 4% 17 % 34 % 37 % 40 % 40 % >5mm 19 % 1-5 mm 24 % 0.5-1 mm 29 % 21 % 0.1-0.5 mm 29 % <0.1mm 60 % 38 % 32 % 35 % 24 % 1% 2% All locaons Auckland Samoa Tahi Rapa Nui

Fig. 7. Size distribution of retrieved plastic particles, overall and across locations.

4.2. Plastic ingestion with respect to locations, habitats and feeding from the 5 Gyres data set, on the SeaWiFS chlorophyll a distribution map (Fig. 13). The greatest debris concentrations overlap with the 4.2.1. Locations lowest primary production. Hence, we suggest that these two factors, We found significant difference in ingestion rates among the four greater accumulation of plastic debris and decreased food availability sampling locations. Rapa Nui fish ingested plastic debris significantly for fish, act together to cause significantly greater ingestion rates in more often (49.2%, p < 0.05) than fish from other locations. High Rapa Nui. densities of plastic debris are generally associated either with highly populated coastal areas or oceanic convergence zones (Lebreton et al., 4.2.2. Habitats 2012). New Zealand has the greatest population of all sampling loca- Benthopelagic fish in our study ingested plastic significantly more tions (~4.8 million), while Rapa Nui has the lowest (~4900) (Table frequently than benthic and pelagic fish (Fig. 4a). It should, however, fi ‘ ’ S6). However, Rapa Nui is situated in the South Paci c garbage patch , be noted that there were only three species pooled into the benthope- an oceanic accumulation zone of the subtropical gyre where in situ lagic category (70 specimens) (Table S5), and one of the species (Ello- sampling of the surface waters along a transect across the eastern South chelon vaigiensis, Mugilidae, squaretail mullet) exhibited high ingestion fi Paci c shows increased concentrations of plastic particles (Eriksen rates (48.5%), increasing the group's average. Nevertheless, in several et al., 2013). The greatest concentration of plastic debris found in the other studies, benthopelagic species were also found to have greater South Pacific subtropical gyre was 396,342 pieces of plastic per square −2 ingestion rates than benthic species. Bessa et al. (2018) reported 73% kilometre, with an average abundance of 26,898 pieces km in the ingestion rates in benthopelagic species and only 18% in demersal. fi east South Paci c. Although only a small number of specimens was assessed, Avio et al. In addition to the abundance of plastic due to accumulation, the (2017b) found great occurrence of ingestion in all species, and also ocean circulation in the subtropical gyres also results in oligotrophic recorded higher rates in benthopelagic (100%) than benthic species water that limits food availability and may contribute to increased in- (83%). Perhaps the fact that benthopelagic species feed in a habitat gestion of plastic. The surface waters of subtropical gyres are con- wider than pelagic or benthic species makes them exposed to more ‘ ’ sidered ocean deserts (Sigman and Hain, 2012) because they contain sources of plastic contamination. In contrast, Neves et al. (2015) found little dissolved nutrients due to the convergence and downwelling of slightly lower ingestion rates in benthopelagic species (18%) than in surface water. Satellite estimates of near-surface concentrations of benthic and demersal (22%), and pelagic (19%). Although Jabeen et al. chlorophyll a (TChla), indicative of primary productivity and phyto- (2017) reported 100% ingestion rates for all 21 marine fish species, plankton abundance (Huot et al., 2007), show low concentrations in according to the plastic load they provided their demersal and benthic subtropical gyres (Sigman and Hain, 2012), particularly the South Pa- species generally exhibited greater plastic load than benthopelagic and fi ci c subtropical gyre (SPSG) which is considered hyper-oligotrophic pelagic species. Several other studies also investigated plastic ingestion (Ras et al., 2008). Ras et al. (2008) compare the results of their in situ across habitats (Miranda and de Carvalho-Souza, 2016; Güven et al., TChla sample collection across the SPSG and the predictions based on 2017; Baalkhuyur et al., 2018); however, the comparison with our re- fi remotely sensed surface TChla, and nd they were generally in agree- sults is not possible due to inconsistencies in categorisation. In several ment, with the lowest concentrations of TChla measured roughly be- other studies, benthopelagic species were not examined or the ben- tween 100° and 120° W, the longitudes containing Rapa Nui (109° W). thopelagic category was not used (Lusher et al., 2013; Philips and fi The low productivity of the SPSG surface waters is also con rmed by Bonner, 2015; Rummel et al., 2016; McGoran et al., 2017; Murphy very low sedimentation rates in the deep ocean below (D'Hondt et al., et al., 2017). 2009). Furthermore, we found no difference in plastic ingestion with re- As the secondary productivity by heterotrophs (i.e. zooplankton, spect to the horizontal aspect of the habitats (Fig. 4b). Coastal fish in- nekton and benthos) directly depends on the availability of the phy- gested plastic slightly more often (19.9%) than the fish which inhabit toplankton biomass (Sigman and Hain, 2012), food availability for oceanic waters (18.1%) or both coastal and oceanic waters (18.5%). fi heterotrophs, including sh, in the oligotrophic waters of subtropical Plastic ingestion with respect to the horizontal aspect of habitats was gyres is consequently limited as well. Moore et al. (2001) sampled the also investigated in a study from the Gulf of Mexico, where offshore fish fi surface waters of the North Paci c subtropical gyre to assess the ratio of were found to have greater ingestion rates (22%), than the fish from neustonic plastic and zooplankton. They found that the abundance of harbours (5.9%) or bays (13.5%) (Philips and Bonner, 2015). the zooplankton was greater than that of plastic debris, but the mass of the plastic debris was six times greater than the mass of the plankton. We superimposed the surface concentrations of plastic debris, obtained 4.2.3. Feeding We found no causality between trophic levels and plastic ingestion

554 A. Markic et al. Marine Pollution Bulletin 136 (2018) 547–564

16 % 26 % 33 % 45 % 45 % 20 % 23 % a) 18 % Fibre 8% Film 21 % Fragment 64 % 49 % 51 % 47 % 34 %

All locaons Auckland Samoa Tahi Rapa Nui

20 % 13 % 34 % 37 % 36 % 42 % 21 % 19 % 10 % 11 % 16 % b) 17 % c)

61 % 66 % 56 % 53 % 41 % 47 %

Benthic Benthopelagic Pelagic Neric Neric-oceanic Oceanic

16 % 23 % 18 % 37 % 47 % 10 % 16 % 22 % 9% d) 18 % 72 % 68 % 54 % 55 % 35 %

Grazer Omnivore Plankvore Benthic Pelagic predator predator

Fig. 8. Distribution of plastic debris by type, a) overall and across locations, b) across the vertical and c) horizontal habitat components, and d) across trophic guilds. of different species. The same findings were obtained in other studies as benthic predators. These fish prey mainly on hard-shelled benthic in- well (Güven et al., 2017; Forrest and Hindell, 2018). Nevertheless, we vertebrates, such as crustaceans, molluscs and sea urchins, and occa- found a significant difference among five trophic guilds (Fig. 5). The sional fish, whose shells, bones and scales are not dissolvable in H2O2. omnivorous fish exhibited the greatest ingestion rates (34.5%), while These undigested remains make the visual examination more difficult, the lowest ingestion rates were recorded in benthic predators (11.8%), resulting in decreased plastic debris recovery. Due to this, our methods which were also significantly lower (p < 0.05) than the ingestion rates require improvement of the examination of the guts of benthic pre- of omnivores. However, we note, yet again, that only two species were dators. pooled into the omnivore group, one of which was the same squaretail Once again, the comparison of our results with other studies which mullet species as in the benthopelagic group, increasing the group's examined the patterns in feeding strategies was difficult due to classi- average ingestion rate. On the contrary, finding little plastic debris in fication inconsistencies. None of the studies used the same trophic guild our benthic predators is most likely, at least partially, owing to the categories of as in our study. Nevertheless, Mizraji et al. (2017) also deficiency of the analytical methods for the type of the gut content found greater incidence of plastic ingestion in omnivorous fish, than in found in benthic predators. As the method testing showed, the recovery herbivores and carnivores. Conversely, Jabeen et al. (2017) found the of the test microbeads was 83.5% from the gut content of emperors, as least plastic debris in omnivores, as opposed to carnivores and plank- opposed to 98.7% recovery from the guts of the parrotfish (Table S3). tivores. Miranda and de Carvalho-Souza (2016) examined 11 species of The main difference between the gut content of these species is the various feeding type, and found plastic debris only in two carnivorous amount of the undissolved residue, which can be particularly high in species. Philips and Bonner (2015) found the greatest ingestion rates in

555 A. Markic et al. Marine Pollution Bulletin 136 (2018) 547–564

100% 90% Black 80% Grey Brown 70% Green 60% Blue 50% Purple a) Pink 40% Red 30% Orange Yellow 20% White 10% Colourless 0% All locaons Auckland Samoa Tahi Rapa Nui

100% 90% 80% 70% 60% b) 50% c) 40% 30% 20% 10% 0% Benthic Benthopelagic Pelagic Neric Neric-oceanic Oceanic

100% 90% 80% 70% 60% d) 50% 40% 30% 20% 10% 0% Grazer Omnivore Plankvore Benthic Pelagic predator predator

Fig. 9. Colour distribution of retrieved plastic particles, a) overall and across locations, b) across the vertical and c) horizontal habitat components, and d) across trophic guilds.

pelagic carnivores (17.5%), but they did not examine omnivorous fish 21 % 26 % or herbivorous fish, only benthic invertivore-carnivores, pelagic carni- 33 % 37 % 48 % vores and pelagic invertivores. Due to such variability in categories among these studies, including ours, little can be deduced from the results on the patterns of plastic ingestion across trophic guilds. Transparent There are two species of the same family Kyphosidae which ex- 79 % hibited high propensity to plastic ingestion. Parore in New Zealand and 67 % 74 % Opaque 63 % Pacific chub in Rapa Nui had remarkably high ingestion rates of 70% 52 % − and 51%, and plastic load of 5.9 and 5.3 pc ind 1, respectively (Fig. 14). Furthermore, one Pacific chub had ingested 104 pieces of plastic, which is, to our knowledge, a world record in plastic load in fi All locaons Auckland Samoa Tahi Rapa Nui sh. These two species were the only herbivorous grazers collected at the two locations. In contrast, herbivorous grazers collected in Samoa Fig. 10. Opacity of recovered plastic debris, overall and across locations. and Tahiti (i.e. Acanthuridae and Scaridae) had much lower ingestion rates. High propensity to plastic ingestion in parore and Pacific chub is potentially specific to the Kyphosidae family. However, since we did

556 A. Markic et al. Marine Pollution Bulletin 136 (2018) 547–564

a) 15 % 11 % 11 % 9 % 12 % 5 % 7 % 13 % Other 7 % 28 % PVC 19 % 16 % PP 50 % 62 % b) 9 % 22 % RAY 21 % PE 20 % 17 % PES 41 % 39 % 26 % 24 % 15 %

Auckland Samoa Tahi Rapa Nui

c) 10 % 27 % 35 % 38 % 29 %

Fibre 95 % Film 41 % 55 % Fragment 61 % 62 %

24 % 18 % 5 % PES PE RAY PP PVC

2 % 8 % 9 % 14 % 19 % 3 % 6 % PVC 51 % 28 % PP d) 54 % Ray 8 % PE 44 % 31 % PES 23 %

Fibres Film Fragment

Fig. 11. a) The overall composition of the recovered plastic debris based on the polymer type, PES – polyester, PE – polyethylene, RAY – rayon, PP – polypropylene, PVC – polyvinyl chloride, b) composition by material across locations, c) distribution of microplastics type across the most common five polymers, and d) the polymer distribution for each microplastics type. not collect any species of this family in other locations, any firm con- 4.3. Characteristics of recovered plastic debris clusion would be invalid. More research on plastic ingestion by this family would be useful, and if the results show the high incidence of 4.3.1. Size ingestion is family-specific, these species could be used for biomoni- The great majority (95%) of plastic debris extracted from our toring, and should not be pooled with other species in studies on plastic samples was smaller than 5 mm. In South Pacific studies, most plastic ingestion. items isolated from fish were also microplastics (Ory et al., 2017, 2018; Forrest and Hindell, 2018). Size distribution of plastic debris across habitats and trophic guilds did not exhibit any specific patterns. How- ever, the increased proportion of fibres in Auckland samples, and fragments in Samoan samples, could explain the size distribution in

557 A. Markic et al. Marine Pollution Bulletin 136 (2018) 547–564

a) 15 % b) 43 % Pelagic 54 % 46 % 57 %

Floats 85 % Benthopelagic 79 % 21 % Sinks 57 % 43 % Benthic 59 % 41 % Fibres Film Fragment

Fig. 12. Proportion of sinking and floating polymers per a) microplastic type category and b) vertical habitat.

Fig. 13. The 5 Gyres surface plastics concentrations across the South Pacific (coloured scale in log10 of the number of particles per km2)(Eriksen et al., 2013) superimposed on the 13-year mean chlorophyll a derived from SeaWiFS ocean colour observations (grey scale in log10 of the concentration in mg/m3). (Data source: NASA, 2014). these locations, as the fibres are usually larger, or in this case longer, prey identity, we suggest they were most likely acquired via trophic than fragments (Fig. 7). transfer or inadvertently through water. Two studies from the North Pacific subtropical gyre, or the so-called ‘Great Pacific garbage patch’, reported ingestion of large plastic objects (up to 10–15 cm) by predatory pelagic fish (Choy and Drazen, 2013; 4.3.2. Type Jantz et al., 2013), which clearly implies mistaken prey identity. In our Almost half of the recovered microplastics were fragments (48%), fi fi study, we did not find any large items in yellowfin tuna, mahi-mahi, followed by bre and (35%) and lm (17%). Location wise, Samoan fi fi yellowtail kingfish or barracuda (Sphyraena forsteri, Sphyraenidae). The sh contained more fragments than sh from other location, while New fi fi largest piece of plastic debris (2.5 cm) was recovered from the grazer Zealand sh contained more bres (Fig. 8a). Rochman et al. (2015) fi parore from New Zealand. Since it is highly unlikely that the micro- reported similar discrepancy between microplastics extracted from sh fi plastics were ingested by large predatory fish as a result of mistaken collected in Indonesia and California, with fragments and bres being predominant in each location, respectively. They suggested that the

Fig. 14. Plastic debris isolated from a) 14 individuals of New Zealand Girella tricuspidata and b) 20 individuals of Rapa Nui Kyphosus sandwicensis.

558 A. Markic et al. Marine Pollution Bulletin 136 (2018) 547–564 difference in microplastics might be a result of different solid waste chemical digestion (e.g. 10% KOH) or at a lower digestion temperature management practices in these countries, with reduced waste collection (< 60 °C). Nuelle et al. (2014) and Karami et al. (2017a) also observed and disposal in Indonesia compared to California, leading to increased changes in colour of some test plastics, such as PET. However, they used chances of solid waste entering the environment. With respect to the even stronger H2O2 solution (30–35%). Interestingly, the test mi- fibres, the authors further suggest that the numerous waste water crobeads in our method testing faded considerably more in parrotfish treatment plants in California present more concentrated sources of (26 out of 74 microbeads) than in emperor samples (3 out of 64) (Table fibres, since the water treatment does not fully eliminate fibres. Such S3), suggesting there are factors affecting the change in test plastics concentrated source points lack in Indonesia. This scenario could be other than the type of solution and temperature, such as pH and di- translated to Samoa and New Zealand. According to the World Bank's gestive enzymes. report on global solid waste management, the effectiveness of solid waste management correlates to GDP (Hoornweg and Bhada-Tata, 4.3.4. Opacity 2012). Even though the low-middle-income countries, such as Samoa, Since we have not observed any distinct patterns in opacity with generate less waste than a high-income country, such as New Zealand, respect to habitats or feeding type, we do not have an explanation for the high-income countries have much more effective collection and the decreasing trend of opacity of microplastics from the western to the disposal than the low-middle-income countries. eastern locations (Fig. 10). Microplastics extracted from most species An obvious pattern in distribution by type was found across habitats were mainly opaque. Only Pacific chub and violet warehou (Schedo- and trophic guilds. Benthic and demersal fish contained more fibres, philus velaini, Centrolophidae) seem to have a potential preference for while pelagic fish contained more fragments (Fig. 8b). Furthermore, transparent microplastics. The main prey item found in warehou was offshore fish contained more fragments and considerably less fibre than transparent salps. Therefore, mistaken prey identity could be the likely coastal fish (Fig. 8c). With respect to feeding, grazers and omnivores cause of plastic ingestion. Pacific chub is considered a herbivore feeding seem to ingest more fibres than the other three trophic guilds (Fig. 8d). on benthic algae (Froese and Pauly, 2016), and we do not have an Fibres have been commonly found as the prevalent type of plastic explanation for the prevalence of transparent microplastics in these debris in benthic sediments (Claessenes et al., 2011; Frias et al., 2016), samples. while the fragments dominate surface waters (Doyle et al., 2011; Eriksen et al., 2013; Yonkos et al., 2014), which was further confirmed 4.3.5. Polymer type in a recent study on microplastic contamination in both compartments Polymer characterisation showed that the visual identification by (Maes et al., 2017). Additionally, since wastewaters are a known source microscopy was highly successful. Apart from the six unidentifiable of microfibre contamination (Browne et al., 2011), it is reasonable to particles, only one white particle was confirmed as not being of syn- expect a greater occurrence of fibres in coastal than oceanic fish species. thetic origin (HQI = 88%, CaCO3). Polyethylene (PE) and polyester The ingestion of fibres from the seafloor by grazers and omnivores most (PES) were the most abundant polymer types accounting for more than likely occurs inadvertently, while the ingestion of particles could result half of the particles. These polymers represent two of the more common from both unaware ingestion and mistaken prey identity. thermoplastics commonly produced by volume, which along with polypropylene (PP) and polyvinyl chloride (PVC) represent > 75% of 4.3.3. Colour world production (PlasticsEurope, 2018). Each of these polymers finds We observed a pattern in the distribution of the blue coloured mi- numerous applications, including packaging, textiles, agricultural and croplastics, which are, with respect to trophic guilds, dominant in pe- construction. The application typically used for each polymer type will lagic predators and planktivores, and habitat wise, in fish from pelagic largely dictate the type and prevalence of microplastics in the marine oceanic habitats (Fig. 9). Blue is also a dominant colour of microplastics environment (Booth et al., 2017). The application of PES is diverse. One from Rapa Nui fish, most likely because out of the six species examined, of the most common thermoplastic PES is the polyethylene ter- two of them were pelagic predators and two were planktivores (Table ephthalate (PET) (Strong, 2006), which is used for products such as S5). Ory et al. (2017) found blue to be a predominant colour of mi- plastic bottles, film packaging and fibres. Rayon is a semi-synthetic croplastics in amberstripe scad from Rapa Nui, based on which they material mainly used in the production of fibres for textiles, while PVC suggested that the ingestion occurs due to mistaken prey identity, as the is mostly used in building and construction (Strong, 2006; blue plastic fragments resemble their common prey, the blue copepods. PlasticsEurope, 2018). As expected, PES occurred in the form of fibres, However, planktivorous fish do not rely solely on vision while fragments and film subequally, rayon was predominantly in the form of feeding. Planktivores feed in two distinct ways, as visual particulate fibres, while PVC was only observed as fragments and film (Fig. 11c, d). feeders and nonvisual filter-feeders (Greene, 1985; Lazzaro, 1987). Distinction of rayon from cellulose fibres based on FTIR spectra is Several experimental studies demonstrated that some planktivorous fish difficult, particularly in environmental samples (Dris et al., 2018), thus can alternate their feeding behaviour between the two types, depending we did not attempt to distinguish them. In some studies rayon fibres on the prey size and concentration (van der Lingen, 1994) and light were excluded due to this difficulty (e.g. Peeken et al., 2018). We fully intensity (Holanov and Tash, 1978). van der Lingen (1994) showed that acknowledge there is a level of uncertainty in differentiation of artificial larger particles at lower concentrations elicit particulate feeding and cellulosic fibres from natural, but we have not excluded them from our smaller particles in greater concentrations elicit filter-feeding. Fur- analysis because many of the fibres were still coloured after chemical thermore, Holanov and Tash (1978) found that particulate feeding is a digestion with H2O2 which discolours biogenic matter (Nuelle et al., visual light-dependent process and occurs only in light intensities of 2014). Out of the 20 rayon/cellulose fibres we analysed, 14 were still bright moonlight or greater, while filter-feeding occurs at all light in- coloured (red, blue, brown and black) (see Fig. S1 in Supplementary tensities and, as authors suggest, is more likely induced by chemor- material). For the remaining 6 fibres (clear and white) we cannot eception rather than vision. Savoca et al. (2017) investigated the role of guarantee that they are artificial. However, during the microscopic odour in plastic debris ingestion. They found that, in the presence of analysis, we followed the basic criteria for distinguishing natural from solution made from biofouled marine plastic, anchovies behaved in a synthetic matter provided by Hidalgo-Ruz et al. (2012). Thus, we in- similar way as when presented with food odour, as opposed to ancho- cluded only fibres which did not contain any cellular or organic vies exposed to clean plastic odour, highlighting the importance of structures and which were equally thick throughout the entire length. chemosensory mechanism behind plastic ingestion by fish. Dris et al. (2018) noted that natural and artificial fibres should not be With respect to the discolouration of some of the test microbeads, excluded, because they are also vectors for pollutants such as colour we note that the colour composition of ingested plastics would poten- additives. tially be slightly different with another type of solution used for The volumetric mass density (i.e. mass into volume) of a polymer

559 A. Markic et al. Marine Pollution Bulletin 136 (2018) 547–564 will dictate the buoyancy and thus the behaviour in the marine en- potentially cause the same complications in smaller organisms (Wright vironment (Andrady, 2003). For example, PE and PP are less dense than et al., 2013), such as small fish, fish larvae and juveniles. water and they float, while PES, rayon and PVC are denser than water Due to the dual nature of plastic debris as a contaminant, it can be and they sink. According to these properties, it is reasonable to expect considered a multiple stressor (Rochman, 2013). Besides presenting a pelagic fish to ingest floating plastic and benthic fish to ingest mainly physical threat to organisms, marine plastics also act as a vector for sinking plastic. However, paradoxically, both types of plastics are found various toxic compounds. Namely, plastics in the marine environment in both benthic and pelagic fish (Fig. 12b). The most likely explanation tend to accumulate environmental contaminants already present in the for the negatively buoyant particles to be present in pelagic waters is water, such as persistent organic pollutants (POPs), onto their surfaces that they stay suspended in the water column due to their small size (Rochman, 2015; Andrady, 2017). Plastics also contain additives, some and, as such, their inability to settle (i.e. sink) in turbid ocean en- of which are toxic, incorporated to improve their chemical and me- vironments (Murray, 1970). Conversely, more intriguing is the occur- chanical properties. Although Grigorakis et al., 2017 showed that mi- rence of floating plastic in benthic habitats. The phenomenon of the croplastics and microfibres do not accumulate in the fish digestive tract, sinking of floating marine plastic has mainly been attributed to the it has been experimentally demonstrated that, during constant recur- change in their buoyancy via biofouling (Holmström, 1975; Ye and ring exposure to marine plastics, the chemical compounds associated Andrady, 1991). Fazey and Ryan (2016) found that the smaller the with them get transferred from plastics into animal's tissue (Oliveira plastic particles, the faster the biofouling and the sinking rates. Cole et al., 2013; Rochman et al., 2013; Hamlin et al., 2015; Luís et al., et al. (2016) also suggested the potential transfer of positively buoyant 2015), where they cause a range of anomalies, such as liver toxicity and microplastics to the seafloor via plankton faecal pellets. Consequently, pathology (Rochman et al., 2013), endocrine disruption (Rochman marine organisms are exposed to a range of plastic polymers, regardless et al., 2014a), changes in predatory performance (Luís et al., 2015) and of their feeding grounds. mortality (Oliveira et al., 2013; Hamlin et al., 2015). Hence, ingestion of plastic as frequently as found in the examined species must have 4.4. Putting things into perspective certain adverse effects on their general wellbeing. Different pollutants adsorbed on plastic debris desorb in different 4.4.1. Gut retention time rates depending on the combination of the synthetic material, POPs and The full exposure of fish to plastics via ingestion needs to consider desorbing conditions (e.g. sea water, cold-blooded and warm-blooded gut retention time as well as the ingestion rate. The content of a di- animals), as described by Bakir et al. (2014) in their experimental gestive tract represents only a snapshot of an individual's life, so even study. The solution representing gut conditions of cold-blooded animals the lowest ingestion rates indicate that these fish eat plastics regularly. had temperature of 18 °C and that of warm-blooded animals 38 °C. These snapshots might represent time frames ranging from several Desorption rates were found the highest in warm-blooded animals, and hours to two days, depending on the diet of the fish, their body size and the lowest in 18 °C sea water. Some fish, such as tunas, billfish, sharks the surrounding temperature (Tytler and Calow, 1985). Gut turnover and moonfish, are in fact endotherms, or warm-blooded animals (Block, time is considerably shorter in herbivorous fish than in carnivorous fish, 2011; Wegner et al., 2015). Carey et al. (1984) described warming of with evacuation time of about 6 h (3−10 h) and 22 h (6–48 h), re- the viscera in Thunnus thynnus (Scombridae, bluefin tuna) during di- spectively (Tytler and Calow, 1985). This implies that herbivorous gestion up to 10–15 °C above the surrounding water, which suggests species with the same ingestion rates as carnivorous species, in fact, that desorption of POPs from digested plastics would be greater in tunas ingest plastics approximately 3.5 times more often during a 24-hour and other warm-blooded fish species. Nevertheless, since the cold- period. With the assumption that the gut retention time of microplastics blooded fish remain body temperature similar to the temperature of the is the same as the retention time of natural gut content, and that the surrounding water, if they reside in tropical waters (e.g. Samoa and exposure to microplastics is constant in time, Halstead et al. (2018) Tahiti around 27–29 °C, from seatemperature.org) their body and gut estimated annual ingestion of microplastic particles by Gerres sub- temperature would be considerably higher than 18 °C. Presumably, this fasciatus (Gerreidae, silverbiddy) and Mugil cephalus (Mugilidae, flat- implies that POPs desorption rates would also be greater, and that, in head grey mullet) from Sydney Harbour to be around 600 and 11,000 general, fish from the warm climate are probably more susceptible to per individual, respectively, with silverbiddy having much lower in- accumulation of POPs from plastic debris than the fish in the colder gestion rates (21%) and longer gut retention time (12–24 h) than mullet climate. Respectively, this further means that the New Zealand cold- (64% ingestion rates, 2–6 h gut retention time). These biological and blooded fish, even if exposed to the same levels of plastic pollution, physiological differences among species should be considered when should accumulate less POPs. estimating the severity of plastic ingestion and its potential impacts on Most studies dealing with the impacts of plastic ingestion on fish are fish. experimental, while field observational studies mainly provide the in- Furthermore, we found that the abundance of plastic particles in the formation on the level of plastic contamination per individual fish (i.e. digestive tract is positively correlated with the amount of digesta plastic load) or per species (i.e. ingestion rate). In several studies, the (Fig. 6). Alomar and Deudero (2017) also found greater amounts of body condition of the fish was recorded and correlated with plastic load microplastics in fuller stomachs. However, Anastasopoulou et al. (2013) of individuals (Foekema et al., 2013; Rummel et al., 2016; Cardozo and Wieczorek et al. (2018) found no relationship between the gut et al., 2018; Compa et al., 2018; Hipfner et al., 2018). However, the fullness and the amount of recovered plastics. results of these studies are inconclusive, as in some studies the re- lationship between the body condition and plastic load was found 4.4.2. Physical and chemical impacts of plastic ingestion on fish and (Cardozo et al., 2018), while in others was not (Foekema et al., 2013; population-level consequences Rummel et al., 2016). The results are most likely inconsistent because Plastic ingestion has physical and chemical effects on organisms Fulton's condition factor (K), a commonly used measure of body con- (Ryan, 2016). The physical impacts include blockage, rupture, abrasion dition, is calculated from body mass and body length, two variables and lesions, satiation and starvation. Larger plastic debris, if sharp, can which do not change quickly in a short period of time. Thus, since it was puncture the digestive tract and cause mortality, as in the case of a experimentally demonstrated that the ingested plastic debris does not Rhincodon typus (Rhincodontidae, whale shark) which ingested a plastic accumulate in the digestive system of fish (Grigorakis et al., 2017), the straw (Haetrakul et al., 2007). In other cases, ingestion of larger plastic Fulton's factor could not be indicative of changes caused by the last debris (e.g. Choy and Drazen, 2013; Jantz et al., 2013; Jawad et al., meal of an individual. Unless, plastic ingestion in some individuals of 2016) could cause blockage, false sense of satiation, and starvation. the same species occurs as a result of a certain personality trait (e.g. However, relative to the size of the organism, microplastics could also Toms et al., 2010; Budaev and Brown, 2011), which would make these

560 A. Markic et al. Marine Pollution Bulletin 136 (2018) 547–564 individuals more prone to plastic ingestion than others. In that case, the minimise contamination (i.e. filtration of ethanol and assuring the work Fulton's factor should only be used for species which feed on plastic space and equipment were always clean), there is always a chance of debris intentionally (i.e. mistaken prey identity), rather than indis- contamination. Although we found very few fibres on the laboratory criminate feeders such as filter-feeders or benthic grazers. However, if blanks, we excluded fibres when there was less than three of them in Fulton's factor is used to compare the body condition of distant popu- one sample, unless the fibre had remains of biofouling. lations of the same species, it could show variations if the populations We acknowledge that H2O2 is not an ideal solution for chemical are exposed to different concentrations of plastic debris over a longer digestion due to foaming, fading of plastics and degrading nylon period of time (e.g. Compa et al., 2018). In conclusion, the reports of (Karami et al., 2017a). However, we had no other option as we were not the impacts of plastics in field studies are missing the comparison with a allowed to use hazardous chemicals due to lab restrictions. Further- control group, i.e. individuals that lived in plastic-free conditions. Ad- more, since we found that our plastics-isolation step was not as effective ditionally, the fact that some examined individuals in the field studies for the GI tracts with plenty of undissolvable material as it was for tracts did not have plastics present in their digestive system at the time when with substantially less inorganic material, we suggest potentially they were caught, does not mean they have not ingested plastic recently adding a density-separation step if it proves that no loss of microplastics and repeatedly over time. occurs. Many of the particles analysed by FTIR spectroscopy were brittle as 4.4.3. Anthropocentric concerns observed during sample preparation. This is indicative of photo-oxi- Since the seafood is an important food source, the question of dative degradation which was confirmed in many of the particles by − human health safety has been one of the main concerns when it comes presence of a broad peroxide band at 3300 cm 1 and a carbonyl band at − to plastic pollution (Santillo et al., 2017; Wright and Kelly, 2017). Apart approximately 1700 cm 1 (Cai et al., 2018). However, in cases where from the transfer of toxins from marine plastics to fish tissue being oxidation levels were very high, these peaks may hinder successful confirmed experimentally (Rochman et al., 2013, 2014a), plastic-re- database screening. This could lead to lower hit quality matches or lated toxins have also been found in the field-collected fish (Gassel possibly incorrect matches, especially giving results for carbonyl con- et al., 2013; Rochman et al., 2014b). In the past, microplastic debris taining polymers such as polyesters or polyurethanes. Including spectra had been found only in the digestive tracts of fish, but more recently the of polymers with varying levels of photo-oxidative degradation in the translocation of microplastics from the gut to the liver has been docu- database would likely improve the accuracy of FTIR spectroscopy based mented, both experimentally (Avio et al., 2015; Lu et al., 2016) and in identification methods. the field samples (Collard et al., 2017). Karami et al. (2017b) and Abbasi et al. (2018) found microplastics in the muscle tissue as well, the 4.5.2. Recommendations for future work edible part of the fish. Additionally, Schirinzi et al., 2017 exposed All possible measures should be taken to avoid procedural con- cerebral and epithelial human cells in vitro to various nanomaterials tamination of the samples during collection and analysis, having as few and microplastics and observed cytotoxicity in both cell lines. To our steps as possible from evisceration to chemical digestion. Laboratory knowledge, no human subjects have yet been tested for potential im- blanks should be used throughout the laboratory work. Fibres should pacts of seafood contaminated by microplastics and plastic-related not be excluded by default. Instead, they should be excluded based on compounds on their health. When dealing with such a complex en- the laboratory blanks and if the contamination cannot be ruled out. vironmental issue, which involves an omnipresent pollutant, a multi- The isolation of plastics should be done by chemical (Karami et al., disciplinary approach is needed to fully understand its extent and the 2017a) or enzymatic digestion (Karlsson et al., 2017) of the organic consequences. In response to public concerns, more research is needed portion of the gut content. Karami et al. (2017a) tested several different into the effects of contaminated seafood on human health. Finally, the methods and found 10% KOH at 40 °C to be the most efficient in di- impacts of pollutants on marine organisms should be investigated, not gesting the gut content and the least destructive for plastics. Based on only at a level of an individual organism, but at a population-level as our plastic debris size-distribution, since we found over 99% of plastic well, particularly in sublethal concentrations (Hamilton et al., 2016), debris to be larger than 100 μm, we would suggest the minimum mesh and in combination with a range of other anthropogenic and natural size of the filters used for filtrating the chemically digested sample to be stressors present in the environment (Breitburg and Riedel, 2005), 100 μm. which could consequently have repercussions on seafood security (Jennings et al., 2016). 5. Conclusion

4.5. Limitations of current methods and recommendations It is reasonable to assume that the occurrence of plastic ingestion by fish in the South Pacific region would be lower than in the regions with 4.5.1. Limitations of our study generally higher human population. However, the findings of this study Sample collection can be challenging in the Pacific Islands. Our suggest otherwise. Plastic ingestion rates found in the fish from the initial plan was to collect 30 specimens and over per species (N ≥ 30). South Pacific compare to the global ingestion rates. Due to limited land However, in some locations, such as Tahiti and Rapa Nui, obtaining fish area of the Pacific Island countries, fish are an invaluable food source was difficult and the sampling was opportunistic, so it was not always for its inhabitants, perhaps more so than in other regions. Exceptionally possible to collect the targeted number of specimens. If we did focus on high ingestion rates were found in fish from the remote Rapa Nui, most obtaining the targeted N, we would not be able to collect as many probably due to its position within the subtropical gyre with high species as we did. Thus, since there was no prior information on plastic concentrations of plastic and low food availability. This raises a ques- ingestion by fish in these locations and our study was baseline in tion of seafood safety and security for the inhabitants of remote islands nature, we decided that the tradeoff in favour of the number of species in convergence zones. Our results urge the need for drastic changes, and examined would be more informative and valuable. Based on the first improvement and adjustment of: i) legislation on national and inter- findings, the more in-depth research and investigation of the potential national level (import, littering, river dumping), ii) waste management impacts on the species more prone to plastic ingestion, and the asso- practices (reduction, recycling, recovery) and iii) education system and ciated population-level consequences, could be the next step. awareness raising of the issue. The number of steps from sample collection to sample processing should be minimised to avoid potential contamination of the samples. Acknowledgements However, we did not have the opportunity to analyse our samples at the place of collection. Even though we took preventative measures to We would like to thank the Secretariat of the Pacific Regional

561 A. Markic et al. Marine Pollution Bulletin 136 (2018) 547–564

Programme, the University of South Pacific in Samoa, Samoan Ministry 2011. Accummulation of microplastic on shorelines worldwide: sources and sinks. of Agriculture and Fisheries and the University of French Polynesia, for Environ. Sci. Technol. 49, 9175–9179. fi Budaev, S., Brown, C., 2011. Personality traits and behaviour. In: Brown, C., Laland, K., the logistic support. We are also grateful for the help from the sh- Krause, J. (Eds.), Fish Cognition and Behavior. Blaskwell Publishing, UK, pp. ermen of Marina Paea in Tahiti, fishermen of Rapa Nui, environmental 135–165. organisation Mesa del Mar in Rapa Nui and Sanford staff in New Cai, L., Wang, J., Peng, J., Wu, Z., Tan, X., 2018. Observation of the degradation of three types of plastic pellets exposed to UV irradiation in three different environments. Sci. Zealand, without whom this study would not be possible. Finally, a big Total Environ. 628–629, 740–747. thank you to Richard Taylor, Alwyn Rees, Errol Murray, Peter Browne, Cannon, S.M.E., Lavers, J.L., Figueiredo, B., 2016. Plastic ingestion by fish in the Southern Boyd Taylor, Karisa Pearson, Jianyong Jin, Michel Nieuwoudt and Hemisphere: a baseline study and review of methods. Mar. Pollut. Bull. 107, – Albina Avzalova who contributed to this study with their knowledge, 286 291. Cardozo, A.L.P., Farias, E.G.G., Rodrigues-Filho, J.L., Moteiro, I.B., Scandolo, T.M., wisdom and patience. Finally, we greatly appreciate the Ocean Biology Dantas, D.V., 2018. Feeding ecology and ingestion of plastic fragments by Priacanthus Processing Group (OBPG) providing the ocean colour data free for arenatus: what's the fisheries contribution to the problem? Mar. Pollut. Bull. 130, – public use. 19 27. Carey, F.G., Kanwisher, J.W., Stevens, E.D., 1984. Bluefin tuna warm their viscera during digestion. J. Exp. Biol. 109, 1–20. Funding Carpenter, E.J., Anderson, S.J., Harvey, G.R., Miklas, H.P., Peck, B.B., 1972. Polystyrene spherules in coastal waters. Science 173, 749–750. fi Choy, C.A., Drazen, J.C., 2013. Plastic for dinner? Observations of frequent debris in- This work was supported by the Secretariat of the Paci c Regional gestion by pelagic predatory fishes from the central North Pacific. Mar. Ecol. Prog. Environment Programme [grant number n/a, 2014]. Ser. 485, 155–163. Claessenes, M., De Meester, S., Van Landuyt, L., De Clerk, K., Janssen, C.R., 2011. Occurrence and distribution of microplastics in marine sediments along the Belgian Appendix A. Supplementary data coast. Mar. Pollut. Bull. 62, 2199–2204. Cole, M., Lindeque, P.K., Fileman, E., Clark, J., Lewis, C., Halsband, C., Galloway, T.S., Supplementary data to this article can be found online at https:// 2016. Microplastics alter the properties and sinking rates of zooplankton faecal pellets. Environ. Sci. Technol. 50, 3239–3246. doi.org/10.1016/j.marpolbul.2018.09.031. Collard, F., Gilbert, B., Compère, P., Eppe, G., Das, K., Jauniaux, T., Parmentier, E., 2017. Microplastics in livers of European anchovies (Engraulis encrasicolus, L.). Environ. References Pollut. 229, 1000–1005. Compa, M., Ventero, A., Iglesias, M., Deudero, S., 2018. Ingestion of microplastics and natural fibres in Sardina pilchardus (Walbaum, 1972) and Engraulis encrasicolus Abbasi, S., Soltani, N., Keshavarzi, B., Moore, F., Turner, A., Hassanaghaei, M., 2018. (Linnaeus, 1758) along the Spanish Mediterranean coast. Mar. Pollut. Bull. 128, Microplastics in different tissues of fish and prawn from the Musa Estuary, Persian 89–96. Gulf. Chemosphere 205, 80–87. Davidson, K., Dudas, S.E., 2016. Microplastic ingestion by wild and cultured Manila clams Ahmed, A.F., 2011. Esophageal obstruction in young camel calves (Camelus dromedarius). (Venerupis philippinarum) from Baynes Sound, British Columbia. Arch. Environ. Res. J. Vet. Sci. 4 (1), 20–26. Contam. Toxicol. 71, 147–156. Alomar, C., Deudero, S., 2017. Evidence of microplastic ingestion in the shark Galeus De Witte, B., Devriese, L., Bekaert, K., Hoffman, S., Vandermeersch, G., Cooreman, K., melastomus Rafinesque, 1810 in the continental shelf off the western Mediterranean Robbens, J., 2014. Quality assessment of the blue mussel (Mytilus edulis): comparison Sea. Environ. Pollut. 223, 223–229. between commercial and wild types. Mar. Pollut. Bull. 85, 146–155. Anastasopoulou, A., Mytilineou, C., Smith, C.J., Papadopoulou, K.N., 2013. Plastic debris Dehaut, A., Cassone, A.-L., Frère, L., Hermabessiere, L., Himber, C., Rinnert, E., Rivière, ingested by deep-water fish of the Ionian Sea (Eastern Mediterranean). Deep-Sea Res. G., Lambert, C., Soudant, P., Huvet, A., Duflos, G., Paul-Pont, I., 2016. Microplastics I 74, 11–13. in seafood: benchmark protocol for their extraction and characterization. Environ. Andrady, A.L., 2003. Plastics and the Environment. John Wiley & Sons, New York, pp. Pollut. 215, 223–233. 1–762. Devriese, L.I., van der Meulen, M.D., Maes, T., Bekaert, K., Paul-Pont, I., Frère, L., Andrady, A.L., 2017. The plastic in microplastics: a review. Mar. Pollut. Bull. 119 (1), Robbens, J., Vethaak, A.D., 2015. Microplastic contamination in brown shrimp 12–22. (Crangon crangon, Linnaeus 1758) from coastal waters of the Southern North Sea and Au, S.Y., Lee, C.M., Weinstein, J.E., van den Hurk, P., Klaine, S.J., 2017. Trophic transfer Channel area. Mar. Pollut. Bull. 98, 179–187. of microplastics in aquatic ecosystems: identifying critical research needs. Integr. D'Hondt, S., Spivack, A.J., Pockalny, R., Ferdelman, T.G., Fischer, J.P., Kallmeyer, J., Environ. Assess. Manag. 13 (3), 505–509. Abrams, L.J., Smith, D.C., Graham, D., Hasiuk, F., Schrum, H., Stancin, A.M., 2009. Auta, H.S., Emenike, C.U., Fauziah, S.H., 2017. Distribution and importance of micro- Subseafloor sedimentary life in the South Pacific Gyre. PNAS 106 (28), 11651–11656. plastics in the marine environment: a review of the sources, fate, effects, and po- Doyle, M.J., Watson, W., Bowlin, N.M., Sheavly, S.B., 2011. Plastic particles in coastal tential solutions. Environ. Int. 102, 165–176. pelagic ecosystems of the Northeast Pacific ocean. Mar. Environ. Res. 71, 41–52. Avio, C.G., Gorbi, S., Regoli, F., 2015. Experimental development of a new protocol for Dris, R., Gasperi, J., Rocher, V., Tassin, B., 2018. Synthetic and non-synthetic fibers in a extraction and characterization of microplastics in fish tissues: first observations in river under the impact of Paris Megacity: sampling methodological aspects and flux commercial species from Adriatic Sea. Mar. Environ. Res. 111, 18–26. estimations. Sci. Total Environ. 618, 157–164. Avio, C.G., Gorbi, S., Regoli, F., 2017a. Plastics and microplastics in the oceans: from Eriksen, M., Maximenko, N., Thiel, M., Cummins, A., Lattin, G., Wilson, S., Hafner, J., emerging pollutants to emerged threat. Mar. Environ. Res. 128, 2–11. Zellers, A., Rifman, S., 2013. Plastic pollution in the South Pacific subtropical gyre. Avio, C.G., Cardelli, L.R., Gorbi, S., Pellegrini, D., 2017b. Microplastics pollution after the Mar. Pollut. Bull. 68, 71–76. removal of the Costa Concordia wreck: first evidences from a biomonitoring case FAO, 2016. Aquatic Species Fact Sheet. FAO Fisheries and Aquaculture Department, study. Environ. Pollut. 227, 207–214. Rome Available at. http://www.fao.org/fishery/species/search/en (accessed Baalkhuyur, F.M., Bin Dohaish, E.-J.A., Elhalwagy, M.E.A., Alikunhi, N.M., AlSuwailem, January–June 2016). A.M., Røstad, A., Coker, D.J., Berumen, M.L., Duarte, C.M., 2018. Microplastic in the Farrell, P., Nelson, K., 2013. Trophic level transfer of microplastic: Mytilus edulis (L.) to gastrointestinal tract of fishes along the Saudi Arabian Red Sea coast. Mar. Pollut. Carcinus maenas (L.). Environ. Pollut. 177, 1–3. Bull. 131, 407–415. Fazey, F.M.C., Ryan, P.G., 2016. Biofouling on buoyant marine plastics: an experimental Bakir, A., Rowland, S.J., Thompson, R.C., 2014. Enhanced desorption of persistent or- study into the effect of size on surface longevity. Environ. Pollut. 210, 354–360. ganic pollutants from microplastics under simulated physiological conditions. Fischer, V., Elsner, N.O., Brenke, N., Schwabe, E., Brandt, A., 2015. Plastic pollution of Environ. Pollut. 185, 16–23. the Kuril-Kamchatka area (NW Pacific). Deep-Sea Res. II 111, 399–405. Bascom, W., 1974. The disposal of waste in the ocean. Sci. Am. 231 (2), 16–25. Foekema, E.M., Gruijter, C.D., Mergia, M.T., van Franeker, J.A., Murk, A.J., Koelmans, Batel, A., Linti, F., Scherer, M., Erdinger, L., Braunbeck, T., 2016. Transfer of benzo[a] A.A., 2013. Plastic in North Sea fish. Environ. Sci. Technol. 47, 8818–8824. pyrene from microplastics to Aremia nauplii and further to zebrafish via a trophic Forrest, A.K., Hindell, M., 2018. Ingestion of plastic by fish destined for human con- food web experiment: CYP1A induction and visual tracking of persistent organic sumption in remote South Pacific Islands. Aust. J. Marit. Ocean Aff. 10 (2), 81–97. pollutants. Environ. Toxicol. Chem. 35 (7), 1656–1666. Frias, J.P.G.L., Gago, J., Otero, V., Sobral, P., 2016. Microplastics in coastal sediments Bessa, F., Barría, P., Neto, J.M., Frias, J.P.G.L., Otero, V., Sobral, P., Marques, J.C., 2018. from Southern Portuguese shelf waters. Mar. Environ. Res. 114, 24–30. Occurrence of microplastics in commercial fish from a natural estuarine environment. Froese, R., Pauly, D., 2016. FishBase. World Wide Web electronic publication. Available Mar. Pollut. Bull. 128, 575–584. at: www.fishbase.org (accessed January–June 2016). Block, B.A., 2011. Endothermy in tunas, billfishes, and sharks. In: Encyclopedia of Fish Galgani, F., Hanke, G., Maes, T., 2015. Global distribution, composition and abundance of Physiology: From Genome to Environment. vol. 3. pp. 1914–1920. marine litter. In: Bergmann, M., Gutow, L., Klages, M. (Eds.), Marine Anthropogenic Booth, A.M., Kubowicz, S., Beegle-Krause, C.J., Skancke, J., Landsem, T., Throne-Holst, Litter. Springer Open, Heidelberg, pp. 29–56. M., Jahren, S., 2017. Microplastic in Global and Norwegian Marine Environments: Galloway, T.S., 2015. Micro- and nano-plastics and human health. In: Bergmann, M., Distributions, Degradation Mechanisms and Transport. SINTEF, Norway, pp. 147. Gutow, L., Klages, M. (Eds.), Marine Anthropogenic Litter. Springer Open, Breitburg, D.L., Riedel, G.F., 2005. Multiple stressors in marine systems. In: Norse, E.A., Heidelberg, pp. 343–366. Crowder, L.B. (Eds.), Marine Conservation Biology: The Science of Maintaining the Gassel, M., Harwani, S., Park, J.-S., Jahn, A., 2013. Detection of nonylphenol and per- Sea's Biodiversity. Island Press, Washington, DC, pp. 167–182. sistent organic pollutants in fish from the North Pacific Central Gyre. Mar. Pollut. Browne, M.A., Crump, P., Niven, S.J., Teuten, E., Tonkin, A., Galloway, T., Thompson, R., Bull. 73, 231–242.

562 A. Markic et al. Marine Pollution Bulletin 136 (2018) 547–564

Gillett, R., 2011. Fisheries of the Pacific Islands: regional and national information. In: Pollut. Bull. 67, 94–99. RAP Publication 2011/03. FAO Regional Office for Asia and the Pacific, Bangkok, Maes, T., Van der Muelen, M.D., Devriese, L.I., Leslie, H.A., Huvet, A., Frère, L., Robbens, Thailand (279 pages). J., Vethaak, A.D., 2017. Microplastics baseline surveys at the water surface and in Greene, C.H., 1985. Planktivore functional groups and patterns of prey selection in pe- sediments of the North-East Atlantic. Front. Mar. Sci. 4, 1–13. lagic communities. J. Plankton Res. 7 (1), 35–40. McGoran, A.R., Clark, P.F., Morritt, D., 2017. Presence of microplastic in the digestive Grigorakis, S., Mason, S.A., Drouillard, K.G., 2017. Determination of the gut retention of tracts of European flounder, Platichthys flesus, and European smelt, Osmerus eperlanus, plastic microbeads and microfibres in goldfish (Carassius auratus). Chemosphere 169, from the River Thames. Environ. Pollut. 220, 744–751. 233–238. McMillan, P.J., Francis, M.P., James, G.D., Paul, L.J., Marriott, P.J., Mackay, E., Wood, Güven, O., Gökdaǧ, K., Jovanović, B., Kideyş, A.E., 2017. Microplastic litter composition B.A., Griggs, L.H., Sui, H., Wei, F., 2011. New Zealand Fishes. Volume 1: a field guide of the Turkish territorial waters of the Mediterranean Sea, and its occurrence in the to common species caught by bottom aand midwater fishing. In: New Zealand gastrointestinal tract of fish. Environ. Pollut. 223, 286–294. Aquatic Environment and Biodiversity Report No. 68. Ministry of Fisheries, NIWA, Haetrakul, T., Munanansup, S., Assawawongkasem, N., Chansue, N., 2007. A case report: Wellington, pp. 329. stomach foreign object in whaleshark (Rhincodon typus) stranded in Thailand. In: Miranda, D.d.A., de Carvalho-Souza, G.F., 2016. Are we eating plastic-ingesting fish? ‘Proceedings of the 4th International Symposium on SEASTAR2000 and Asian Bio- Mar. Pollut. Bull. 103, 109–114. logging Science (The 8th SEASTAR2000 Workshop)’,15–17 December 2007, Phuket, Mizraji, R., Ahrendt, C., Perez-Venegas, D., Vargas, J., Pulgar, J., Aldana, M., Ojeda, F.P., Thailand, pp. 83–85. Duarte, C., Galbán-Malagón, C., 2017. Is the feeding type related with the content of Halstead, J.E., Smith, J.A., Carter, E.A., Lay, P.A., Johnston, E.L., 2018. Assessment tools microplastics in intertidal fish gut? Mar. Pollut. Bull. 116, 498–500. for microplastics and natural fibres ingested by fish in an urbanised estuary. Environ. Moore, C.J., Moore, S.L., Leecaster, M.K., Weisberg, S.B., 2001. A comparison of plastic Pollut. 234, 552–561. and plankton in the North Pacific Central Gyre. Mar. Pollut. Bull. 42 (12), Hamilton, P.B., Cowx, I.G., Oleksiak, M.F., Griffiths, A.M., Grahn, M., Stevens, J.R., 1297–1300. Carvalho, G.R., Nicol, E., Tyler, C.R., 2016. Population-level consequences for wild Murphy, F., Russell, M., Ewins, C., Quinn, B., 2017. The uptake of macroplastics & mi- fish exposed to sublethal concentrations of chemicals – a critical review. Fish Fish. 17, croplastics by demersal & pelagic fish in the Northeast Atlantic around Scotland. Mar. 545–566. Pollut. Bull. 122, 353–359. Hamlin, H.J., Marciano, K., Downs, C.A., 2015. Migration of nonylphenol from food- Murray, S.P., 1970. Settling velocities and vertical diffusion of particles in turbulent grade plastic is toxic to the coral reef fish species Pseudochromis fridmani. water. J. Geophys. Res. 75 (9), 1647–1654. Chemosphere 139, 223–228. Murray, F., Cowie, P.R., 2011. Plastic contamination in the decapod crustacean Nephrops Hidalgo-Ruz, V., Gutow, L., Thompson, R.C., Thiel, M., 2012. Microplastics in the marine norvegicus (Linnaeus, 1758). Mar. Pollut. Bull. 62, 1207–1217. environment: a review of the methods used for identification and quantification. NASA, 2014. SeaWiFS Ocean Color Data, Chlorophyl a. Goddard Space Flight Ceter, Environ. Sci. Technol. 46, 3060–3075. Ocean Ecology Laboratory, Ocean Biology Processing Group, NASA OB.DAAC. Hipfner, J.M., Galbraith, M., Tucker, S., 2018. Two forage fishes as potential conduits for https://oceancolor.gsfc.nasa.gov/citations/, Accessed date: 25 May 2018. the vertical transfer of microfibres in Northeastern Pacific Ocean food webs. Environ. Neves, D., Sobral, P., Ferreira, J.L., Pereira, T., 2015. Ingestion of microplastics by Pollut. 239, 215–222. commercial fish off the Portuguese coast. Mar. Pollut. Bull. 101, 119–126. Holanov, S.H., Tash, J.C., 1978. Particulate and filter feeding in threadfin shad, Dorosoma Newcombe, R.G., 1998. Two-sided confidence intervals for the single proportion: com- petenense,atdifferent light intensities. J. Fish Biol. 13, 619–625. parison of seven methods. Stat. Med. 17, 857–872. Holmström, A., 1975. Plastic films on the bottom of the Skagerack. Nature 255, 622–623. Nuelle, M.-T., Dekiff, J.H., Remy, D., Fries, E., 2014. A new analytical approach for Hoornweg, D., Bhada-Tata, P., 2012. What a Waste. A Global Review of Solid Waste monitoring microplastics in marine sediments. Environ. Pollut. 184, 161–169. Management. World Bank. Urban Development and Local Government Unit, Oliveira, M., Ribeiro, A., Hylland, K., Guilhermino, L., 2013. Single and combined effects Washington, pp. 98. of microplastics and pyrene on juveniles (0+ group) of the common goby Sea temperature. available at. https://www.seatemperature.org/, Accessed date: 11 May Pomatoschistus microps (Teleostei, Gobiidae). Ecol. Indic. 34, 641–647. 2018. Ory, N.C., Sobral, P., Ferreira, J.L., Thiel, M., 2017. Amberstripe scad Decapterus muroadsi Huot, Y., Babin, M., Bruyant, F., Grob, C., Twardowski, M.S., Claustre, H., 2007. Does (Carangidae) fish ingest blue microplastics resembling their copepod prey along the chlorophyll a provide the best index of phytoplankton biomass for primary pro- coast of Rapa Nui (Easter Island) in the South Pacific subtropical gyre. Sci. Total ductivity studies? Biogeosci. Discuss. 4, 707–745. Environ. 586, 430–437. Jabeen, K., Su, L., Li, J., Yang, D., Tong, C., Mu, J., Shi, H., 2017. Microplastics and Ory, N., Chagnon, C., Felix, F., Fernández, C., Ferreira, J.L., Gallardo, C., Ordóñez, O.G., mesoplastics in fish from coastal and fresh waters of China. Environ. Pollut. 221, Henostroza, A., Laaz, E., Mizraji, R., Mojica, H., Haro, V.M., Medina, L.O., Preciado, 141–149. M., Sobral, P., Urbina, M.A., Thiel, M., 2018. Low prevalence of microplastic con- Jantz, L.A., Morishige, C.L., Bruland, G.L., Lepczyk, C.A., 2013. Ingestion of plastic tamination in planktivorous fish species from the southeast Pacific Ocean. Mar. marine debris by longnose lancetfish (Alepisaurus ferox) in the North Pacific Ocean. Pollut. Bull. 127, 211–216. Mar. Pollut. Bull. 69, 97–104. Peeken, I., Primpke, S., Beyer, B., Gütermann, J., Katlein, C., Krumpen, T., Bergmann, M., Jawad, L.A., Humborsad, O.-B., Fjelldal, P.G., 2016. Record of litter ingestion by cod Hehemann, L., Gerdts, G., 2018. Arctic sea ice is an important temporal sink and (Gadus morhua) collected from Masfjorden, Western Norway. Int. J. Mar. Sci. 6 means of transport for microplastic. Nat. Commun. 9, 1505. (41), 1–4. Philips, M.B., Bonner, T.H., 2015. Occurrence and amount of microplastic ingested by Jennings, S., Stentiford, G.D., Leocadio, A.M., Jeffery, K.R., Metcalfe, J.D., Katsiadaki, I., fishes in watersheds of the Gulf of Mexico. Mar. Pollut. Bull. 100, 264–269. Auchterlonie, N.A., Mangi, S.C., Pinnegar, J.K., Ellis, T., Peeler, E.J., Luisetti, T., PlasticsEurope, 2018. Plastics – The Facts 2017: An Analysis of European Plastics Baker-Austin, C., Brown, M., Catchpole, T.L., Clyne, F.J., Dye, S.R., Edmonds, N.J., Production, Demand and Waste Data. PlasticsEurope, Belgium. Hyder, K., Lee, J., Lees, D.N., Morgan, O.C., O'Brien, C.M., Oidtmann, B., Posen, P.E., Ras, J., Claustre, H., Uitz, J., 2008. Spatial variability of phytoplankton pigment dis- Santos, A.R., Taylor, N.G.H., Turner, A.D., Townhill, B.L., Verner-Jeffreys, D.W., tributions in the Subtropical South Pacific Ocean: comparison between in situ and 2016. Aquatic food security: insights into challenges and solutions from an analysis of predicted data. Biogeosciences 5, 353–369. interactions between fisheries, aquaculture, food safety, human health, fish and Rochman, C.M., 2013. Plastics and priority pollutants: a multiple stressor in aquatic human welfare, economy and environment. Fish Fish. 17, 893–938. habitats. Environ. Sci. Technol. 47, 2439–2440. Karami, A., Golieskardi, A., Choo, C.K., Romano, N., Ho, Y.B., Salamatinia, B., 2017a. A Rochman, C.M., 2015. The complex mixture, fate and toxicity of chemicals associated high-performance protocol for extraction of microplastics in fish. Sci. Total Environ. with plastic debris in the marine environment. In: Bergmann, M., Gutow, L., Klages, 578, 485–494. M. (Eds.), Marine Anthropogenic Litter. Springer Open, Heidelberg, pp. 117–140. Karami, A., Golieskardi, A., Ho, Y.B., Larat, V., Salamantina, B., 2017b. Microplastics in Rochman, C.M., Hoh, E., Kurobe, T., Teh, S.J., 2013. Ingested plastic transfers hazardous eviscerated flesh and excised organs of dried fi sh. Sci. Rep. 7, 5473. https://doi.org/ chemicals to fish and induces hepatic stress. Sci. Rep. 3 (3263), 1–7. 10.1038/s41598-017-05828-6. Rochman, C.M., Kurobe, T., Flores, I., Teh, S.J., 2014a. Early warning signs of endocrine Karlsson, T.M., Vethaak, A.D., Almroth, B.C., Ariese, F., van Velzen, M., Hassellöv, M., disruption in adult fish from the ingestion of polyethylene with and without sorbed Leslie, H., 2017. Screening for microplastics in sediment, water, marine invertebrates chemical pollutants from the marine environment. Sci. Total Environ. 493, 656–661. and fish: method development and microplastics accumulation. Mar. Pollut. Bull. Rochman, C.M., Lewison, R.L., Eriksen, M., Allen, H., Cook, A.-M., Teh, S.J., 2014b. 122, 403–408. Polybrominated diphenyl ethers (PBDEs) in fish tissue may be an indicator of plastic Kühn, S., Rebolledo, E.L.B., van Franeker, J.A., 2015. Deleterious effects of litter on contamination in marine habitats. Sci. Total Environ. 476–477, 622–633. marine life. In: Bergmann, M., Gutow, L., Klages, M. (Eds.), Marine Anthropogenic Rochman, C.M., Tahir, A., Williams, S.L., Baxa, D.V., Lam, R., Miller, J.T., Teh, F.-C., Litter. Springer Open, Heidelberg, pp. 75–116. Werorilangi, S., Teh, S.J., 2015. Anthropogenic debris in seafood: plastic debris and Lazzaro, X., 1987. A review of planktivorous fish: their evolution, feeding behaviours, fibres from textiles in fish and bivalves sold for human consumption. Sci. Rep. 5, selectivities, and impacts. Hydrobiologia 146, 97–167. 14340. https://doi.org/10.1038/srep14340. Lebreton, L.C.-M., Greer, S.D., Borrero, J.C., 2012. Numerical modelling of floating debris Rosas-Luis, R., 2016. Description of plastic remains found in the stomach contents of the in the worls's oceans. Mar. Pollut. Bull. 64, 653–661. jumbo squid Dosidicus gigas landed in Ecuador during 2014. Mar. Pollut. Bull. 113, Lu, Y., Zhang, Y., Deng, Y., Jiang, W., Zhao, Y., Geng, J., Ding, L., Ren, H., 2016. Uptake 302–305. and accumulation of polystyrene microplastics in zebrafish (Danio rerio) and toxic Rothstein, S., 1973. Plastic particle pollution of the surface of the Atlantic Ocean: evi- effects in liver. Environ. Sci. Technol. 50, 4054–4060. dence from a seabird. Condor 75, 344–366. Luís, L.G., Ferreira, P., Fonte, E., Oliveira, M., Guilhermino, L., 2015. Does the presence of Rummel, C.D., Löder, M.G.J., Fricke, N.F., Lang, T., Griebeler, E.-M., Janke, M., Gerdts, microplastics influence the acute toxicity of chromium(VI) to early juveniles of the G., 2016. Plastic ingestion by pelagic and demersal fish from the North Sea and Baltic common goby (Pomatoschistus microps)? A study with juveniles from two wild es- Sea. Mar. Pollut. Bull. 102, 134–141. tuarine populations. Aquat. Toxicol. 164, 163–174. Ryan, P.G., 2016. Ingestion of plastics by marine organisms. In: Takada, H., Lusher, A.L., McHugh, M., Thompson, R.C., 2013. Occurrence of microplastics in the Karapanagioti, H.K. (Eds.), Hazardous Chemicals Associated With Plastics in the gastrointestinal tract of pelagic and demersal fish from the English Channel. Mar. Marine Environment. Springer International Publishing, Switzerland, pp. 1–32.

563 A. Markic et al. Marine Pollution Bulletin 136 (2018) 547–564

Santana, M.F.M., Moreira, F.T., Turra, A., 2017. Trophic transference of microplastics House, Kent, pp. 349. under a low exposure scenario: insights on the likelihood of particle cascading along van der Lingen, C.D., 1994. Effect of particle size and concentration on the feeding be- marine food-webs. Mar. Pollut. Bull. 121, 154–159. haviour of adult pilchard Sardinops sagax. Mar. Ecol. Prog. Ser. 109, 1–13. Santillo, D., Miller, K., Johnston, P., 2017. Microplastics as contaminants in commercially Walde, A.D., Harless, M.L., Delaney, D.K., Pater, L.L., 2007. Anthropogenic threat to the important seafood species. Integr. Environ. Assess. Manag. 13 (3), 516–521. desert tortoise (Gopherus agassizii): litter in the Mojave Desert. West. North Am. Nat. Savoca, M.S., Tyson, C.W., McGill, M., Slager, C.J., 2017. Odours from marine plastic 67 (1), 147–149. debris induce food search behaviours in a forage fish. Proc. R. Soc. B 284, 20171000. Wegner, N.C., Snodgrass, O.E., Dewar, H., Hyde, J.R., 2015. Whole-body endothermy in a https://doi.org/10.1098/rspb.2017.1000. mesopelagic fish, the opah, Lampris guttatus. Science 348 (6236), 786–789. Schirinzi, G.F., Pérez-Pomeda, I., Sanchís, J., Rossini, C., Farré, M., Barceló, D., 2017. Wieczorek, A.M., Morrison, L., Croot, P.L., Allcock, A.L., MacLoughlin, E., Savard, O., Cytotoxic effects of commonly used nanomaterials and microplastics on cerebral and Brownlow, H., Doyle, T.K., 2018. Frequency of microplastics in mesopelagic fishes epithelial human cells. Environ. Res. 159, 579–587. from the Northwest Atlantic. Front. Mar. Sci. 5 (39), 1–9. Sigman, D.M., Hain, M.P., 2012. The biological productivity of the ocean. Nat. Educ. 3 Wright, S.L., Kelly, F.J., 2017. Plastic and human health: a micro issue? Environ. Sci. (6), 1–16. Technol. 51, 6634–6647. Strong, A.B., 2006. Plastics: Materials and Processing. Pearson Education, Inc., New Wright, S.L., Thompson, R.C., Galloway, T.S., 2013. The physical impacts of microplastics Yersey, US, pp. 917. on marine organisms: a review. Environ. Pollut. 178, 483–492. Thompson, R.C., Swan, S.H., Moore, C.J., vom Saal, F.S., 2009. Our plastic age. Philos. Ye, S., Andrady, A.L., 1991. Fouling of floating plastic debris under Biscayne Bay ex- Trans. R. Soc. B 364, 1973–1976. posure conditions. Mar. Pollut. Bull. 22 (12), 608–613. Toms, C.N., Echevarria, D.J., Jouandot, D.J., 2010. A methodological review of person- Yonkos, L.T., Friedel, E.A., Perez-Reyes, A.C., Ghosal, S., Arthur, C.D., 2014. Microplastics ality-related studies in fish: focus on the shy-bold axis of behaviour. Int. J. Comp. in four estuarine rivers in the Chesapeake Bay, U.S.A. Environ. Sci. Technol. 48, Psychol. 23, 1–25. 14195–14202. Tytler, P., Calow, P., 1985. Fish Energetics, New Perspectives. Croom Helm Ltd. Provident

564