Floating macro-litter along the Mediterranean French

Marine Pollution Bulletin 118 (2017) 155–166

Contents lists available at ScienceDirect

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

Floating macro-litter along the Mediterranean French coast: Composition, density, distribution and overlap with cetacean range Nathalie Di-Méglio a,⁎, Ilaria Campana a,b,c a b c

EcoOcéan Institut, 18 Rue des Hospices, 34090 Montpellier, France Tuscia University, Dep. of Ecological and Biological Sciences, Ichthyogenic Experimental Marine Center (CISMAR), Borgo Le Saline, 01016 Tarquinia, VT, Italy Accademia del Leviatano, V.le dell'Astronomia 19, 00144 Rome, Italy

a r t i c l e

i n f o

Article history: Received 4 October 2016 Received in revised form 8 February 2017 Accepted 9 February 2017 Available online 24 February 2017 Keywords: Floating macro-litter Plastics Pollution Cetaceans Liguro-Provençal basin

a b s t r a c t This study investigated the composition, density and distribution of floating macro-litter along the LiguroProvençal basin with respect to cetaceans presence. Survey transects were performed in summer between 2006 and 2015 from sailing vessels with simultaneous cetaceans observations. During 5171 km travelled, 1993 floating items were recorded, widespread in the whole study area. Plastics was the predominant category, with bags/packaging always representing N 45% of total items. Overall mean density (14.98 items/km2) was stable with significant increase reported only in 2010–2011; monthly analysis showed lower litter densities in July– September, suggesting possible seasonal patterns. Kernel density estimation for plastics revealed ubiquitous distribution rather than high accumulation areas, mainly due to the circulation dynamics of this area. The presence range of cetaceans (259 sightings, 6 species) corresponded by ~50% with plastic distribution, indicating high potential of interaction, especially in the eastern part of the area, but effective risks for marine species might be underrepresented. © 2017 Elsevier Ltd. All rights reserved.

1. Introduction Marine ecosystem is affected by various pressures related to human activities, such as coastal urbanisation, commercial and recreational maritime traffic, resources exploitation by fishery or drilling operations (Coll et al., 2012; Halpern et al., 2008). Anthropogenic pollution is a byproduct of all these activities, representing an input of unnatural substances in the ecosystem. The Mediterranean Sea represents a particularly sensitive ecosystem for the coexistence of high impacts and biodiversity richness (e.g. Coll et al., 2012; Pérès, 1978); indeed, the strong anthropogenic pressure, represented by the surrounding industrialised countries and high shipping levels, can jeopardize the fragile ecological balance of this semi-enclosed basin. Marine litter is defined as any persistent manufactured or processed solid material discarded, disposed of or abandoned in the marine and coastal environment (Coe and Rogers, 1997; Galgani et al., 2013). The complex path of marine litter includes sources, dispersal, fragmentation, degradation and release of new chemical compounds, deposition: thus, besides aesthetic impacts, debris represents hazards for marine life as it can interact with all levels of the trophic chain spoiling the normal ecosystem functioning (Baulch and Perry, 2014; Coe and Rogers, 1997; Cole ⁎ Corresponding author. E-mail addresses: [email protected] (N. Di-Méglio), [email protected] (I. Campana).

http://dx.doi.org/10.1016/j.marpolbul.2017.02.026 0025-326X/© 2017 Elsevier Ltd. All rights reserved.

et al., 2011; Derraik, 2002; Gall and Thompson, 2015; Gregory, 2009; Laist, 1997; Simmonds, 2012). For example, floating litter can help the dispersion of small invertebrates over broad ranges, potentially favouring also the distribution of alien species (Aliani and Molcard, 2003; Barnes, 2002; Derraik, 2002; McKinney, 1998); the accumulation on the seabed can provoke hypoxia in the benthic communities (Derraik, 2002; Goldberg, 1994). Interactions between litter and marine organisms have been reported for 693 different species, mainly occurring through entanglement and ingestion (Gall and Thompson, 2015): physical wounds, reduction of mobility, limitation of feeding success, blockage of the intestinal tract are among the detrimental consequences (e.g. Derraik, 2002; Gregory, 2009; Laist, 1997; Mato et al., 2001). Among all debris, plastic is the most ubiquitous and long-lasting material (Barnes et al., 2009; Derraik, 2002; Moore, 2015): it represents up to 80% or sometimes more of the waste that accumulates on land, shorelines, ocean surface or seabed (Barnes et al., 2009). Its slow degradation after ingestion by a variety of species causes an increased exposure to chemicals, enhance the availability and accumulation of persistent pollutants in the food chain (Carpenter and Smith, 1972; Cole et al., 2011; Davison and Asch, 2011; Engler, 2012; Fossi et al., 2016, 2014; Mazzariol et al., 2011; Ryan et al., 1988; Simmonds, 2012), besides playing a role in transporting other toxic substances (Endo et al., 2005; Mato et al., 2001; Teuten et al., 2007; Thompson et al., 2004). Given the exponential increase in use of artificial polymers, therefore in waste production (PlasticsEurope, 2015), research has been

156

N. Di-Méglio, I. Campana / Marine Pollution Bulletin 118 (2017) 155–166

expanding regarding this topic, especially to better understand sources, patterns and potential effects on ecosystems and human health in the long-term. In Europe, marine litter is included in the descriptors of the Marine Strategy Framework Directive for the evaluation and monitoring of ecological status of marine waters (MSFD), requiring the characterisation of the trends in the amount of litter in the water column, including floating at the surface (EC, 2008; Galgani et al., 2013, 2010). Accordingly, high trophic level organisms are considered as indicators for monitoring the effects of litter in marine ecosystems (Fossi et al., 2012a; Galgani et al., 2014, 2010). Surveying marine litter at surface can provide reliable estimate of its abundance and distribution patterns before it meets its unpredictable fate. Monitoring programmes of floating litter have been developed over wide geographical areas, reporting higher abundances generally related to shipping routes (Carić and Mackelworth, 2014; Ryan, 2013), urbanised coastal regions (Hinojosa and Thiel, 2009; Matsumura and Nasu, 1997; Thiel et al., 2013, 2003) and oceanic currents systems (Law, 2010; Shiomoto and Kameda, 2005; Yamashita and Tanimura, 2007). The Mediterranean Sea has been indicated as one of the areas of highest concentrations of marine waste in the world (Barnes et al., 2009; Eriksen et al., 2014; Jambeck et al., 2015; van Sebille, 2014), comparable to the levels of the five large oceanic accumulation patches (Collignon et al., 2012; Cózar et al., 2015; Suaria et al., 2016). Many studies have been focusing on beach litter (Ariza et al., 2008; Golik and Gertner, 1992; Munari et al., 2016; Poeta et al., 2014), seafloor (Galgani et al., 1996, 1995; Galil et al., 1995; Pham et al., 2014; Stefatos et al., 1999; Tubau et al., 2015) and floating macro-litter (Aliani et al., 2003; Kornilios et al., 1998; McCoy, 1988; Morris, 1980; Suaria and Aliani, 2014). However, different techniques, sea compartments and periods of research prevent uniform assessments of pollution loads (Deudero and Alomar, 2015; Ryan, 2013; Suaria and Aliani, 2014). Besides, litter distribution is strongly influenced by the variable circulation patterns of the basin where high energy systems, like the Liguro-Provençal Current, play a determinant role in redistributing floating particles (Mansui et al., 2015; Millot, 1999). Interactions with plastic have been reported in the Mediterranean Sea for many cetacean species of both oceanic and coastal habitats (Cuvier's beaked whale (Ziphius cavirostris), fin whale (Balaenoptera physalus), sperm whale (Physeter macrocephalus), striped dolphin (Stenella coeruleoalba), bottlenose dolphin (Tursiops truncatus)) (e.g. De Stephanis et al., 2013; Deudero and Alomar, 2015; Fossi et al., 2014; Gomerčić et al., 2006; Levy et al., 2009; Mazzariol et al., 2011), mainly using data obtained from stranded animals, then representing only the small portion of detectable impacts (Baulch and Perry, 2014). For example in the Mediterranean Sea, the death of a sperm whale of 4.5 t, was attributed to 7.6 kg of plastic debris in its stomach, which was ruptured probably due to the large plastic load (De Stephanis et al., 2013) and one bottlenose dolphin died due to nylon filaments wrapped around his larynx (Levy et al., 2009). Given the widespread exposure of animals to this threat, focusing studies on regions of high biodiversity and richness takes on a significant meaning from a conservation point of view (Fossi et al., 2012a; Galgani et al., 2014), as well as reporting about the areas where overlap between pollution and wildlife occurs and is detected at an early stage (Coll et al., 2012; Fossi et al., 2016). For all these reasons, in this study we wanted to investigate the presence of floating macro-litter in the Liguro-provençal basin in relation with the presence of cetaceans. Indeed, the Liguroprovençal Sea is characterised by high offshore primary productivity, which attracts a variety of predators, including six species of cetaceans (Tursiops truncatus, Stenella coeruleoalba, Globicephala melas, Grampus griseus, Physeter macrocephalus, Balaenoptera physalus) (Laran et al., 2016; Notarbartolo di Sciara and Birkun, 2010). This area is important for the feeding and reproduction of cetaceans and especially during the summer period (from the end of spring to the autumn) when the six species of cetaceans are present in large quantities. We therefore wanted to know if the aggregation zones of floating macro-litter were

those where the majority of cetaceans were observed. For this we provided a robust assessment conducted between 2006 and 2015 by contemporary observation on litter and marine life, in particular cetacean species. Data were collected during various campaigns conducted by EcoOcéan Institut (Nouvel Horizon, IMPACT-CET), and supported by WWF-France (Cap cétacés) and the Nicolas Hulot Foundation (Objectif cétacés). Aims of this research were: 1) to characterise floating macrolitter by composition, abundance and density over the whole study period; 2) to verify monthly (2007–2008) and yearly variations in composition, abundance and density; 3) to investigate distribution patterns of plastics and cetacean species, in order to provide a preliminary indication of areas of co-occurrence and potential risk. 2. Material and methods 2.1. Study area Surveys were carried out in the Liguro-Provençal basin within different campaigns conducted along the Mediterranean French region of Provence-Alpes-Côte d'Azur and Principality of Monaco. Some surveys extended in open sea and towards the Corsican coast, but for more detailed analysis we selected only an area of about 100 km width were the majority of effort was performed (Fig. 1). The Ligurian Sea is characterised by narrow continental shelf and steep descending slope reaching up to 2000 m depth. As for the whole northern Mediterranean, water dynamics is influenced by the permanent cyclonic circulation of the Liguro-Provençal Current, with its minor branch entering the continental shelf of the Gulf of Lion. Marked atmospheric forcing due to dominant north-westerly winds can affect general circulation, inducing vertical mixing, local enrichment and production activity (Béranger et al., 2010; Millot, 1999). The study area is partially included in the Pelagos Sanctuary for the protection of marine mammals (Notarbartolo di Sciara et al., 2008), with which shares ecological importance and species richness. Seven cetacean species are considered regular in this basin: striped dolphin, fin whale, sperm whale, long-finned pilot whale, Risso's dolphin, bottlenose dolphin and Cuvier's beaked whale (Laran et al., 2016; UNEP, 2013). Nevertheless, this area suffers high levels of anthropic pressure: in particular, it is crossed by shipping routes depending on the major port movements of Marseille, Toulon and Nice, but also seasonally characterised by pleasure boats traffic (Campana et al., 2015; David et al., 2011). The coastline is in fact dotted with famous touristic destinations (cities, islands, parks) which become particularly busy in summer months. 2.2. Survey methodology Visual surveys of floating macro litter (N1 cm) were conducted from sailing vessels between 2006 and 2015, mainly during summer months (Fig. 1). Surveys were performed simultaneously with transects looking for cetaceans during 98 days at sea: marine litter surveys were interrupted when cetaceans were sighted and registered, then resumed as the observations were over. Sampling was carried out in standard conditions at a speed around 6 (± 0.5) knots with three observers standing at the bow of the boat, approximately 3 m above sea level. They continuously scanned 180° ahead of the vessel, sighting all floating macro-litter and reporting it to a fourth person who recorded the time, type, size and number of objects seen. In parallel, information on sea state, light conditions as well as wind force were taken down, and a GPS continuously recorded the boat's position. For this study we only considered marine litter from anthropogenic sources and it was classified in three main categories: “Plastics”, “Styrofoam” and “Other items”. The Plastics category included: Bags (packaging, films, wrappings, sheets, divided in small, medium and large fragments), Bottles, Cans and Other plastic. In order to reduce the bias due to bad visibility, in our analysis we only took into account the surveys conducted in sea state ≤2 Beaufort.


157

Fig. 1. Study area with total transects and detailed yearly surveys performed continuously in standard effort conditions (sea state ≤2 Beaufort, speed between 5.5 and 6.5 knots) mainly during summer months between 2006 and 2015. The selected area is displayed in gray.

Table 1 Survey effort covered during the whole 2006–2015 study period and general results of floating macro-litter observations. Lines indicated with (*) report the information within the selected area.

Year

Period

2006 July & Oct 2006* July & Oct 2007 May–Sept 2007* May–Sept 2008 May–Oct 2008* May–Oct 2008* July 2009* July 2010* July 2011* July 2012* July 2013* July 2014* July 2015* July Total *Total: selected area Total: July 2008–15

Effort (km)

Total items

Total plastic items

Mean abundance (N items/km)

SD

Mean density (N items/km2)

SD

% Effort without litter

338.02 128.94 1678.63 1308.68 1857.51 1708.72 355.47 192.94 153.48 256.47 152.33 255.87 136.83 149.49 5171.57 4443.73 1652.86

61 51 622 483 618 598 70 125 159 131 49 157 47 24 1993 1824 762

50 42 561 433 545 527 54 117 122 90 40 141 40 22 1728 1574 626

0.20 0.33 0.36 0.36 0.32 0.32 0.22 0.95 0.90 0.74 0.29 0.45 0.46 0.28 0,41 0,44 0,55

0.32 0.39 0.36 0.40 0.41 0.43 0.36 1.67 0.83 0.64 0.27 0.38 0.52 0.41 0.57 0.6 0.75

4.03 6.87 12.49 12.47 12.54 13.74 7.55 37.49 31.32 23.11 12.54 18.19 17.99 9.27 14.98 16.21 19.65

7.64 10.46 14.55 15.92 17.51 18.50 12.84 73.88 29.78 19.93 12.77 16.66 19.91 13.35 22.84 24.09 29.83

51.5% 20.2% 3.5% 4.5% 15.2% 15.4% 42.6% 2.4% 2.5% 9.0% 0.6% 9.7% 14.9% 31.4% 12.4% 9.1% 16.7%

158


2.3. Data analysis We firstly investigated all records in a GIS software (QGIS version 2.6, 2014) in order to correctly distinguish for each transect the “on effort” portions, their relative length, the number of litter and cetaceans observations. Because of differences in the sampling effort (Table 1), data were firstly investigated over the whole surveyed area pooling together all records of the entire study period. Then, all analyses were performed over the selected area by pooling together all data of the entire study period and using monthly data of 2007–2008. Composition of litter sampled was investigated for the whole study period and per year as percentage contribution of each category to the whole composition. The number of objects observed along each transect was reported as abundance A ¼ nLFLT , where nFL is the number of floating litter, LT, the transect length (in km). Abundance was calculated for total litter items and single categories. The concentration of debris through the surveyed area was also analysed as it provides an estimate of debris density and can be better compared with other values from literature. We applied the strip transect method (Thiel et al., 2003) which considers the number of items sighted, the length of the transects and the strip width at each nFL side of the boat, as follows: D ¼ LT W , where WT is the width of the tranT sect (twice the monitored strip at each side of the boat, in km). Considering that sighting reliability for floating litter is variable for the different items categories, we estimated an effective range of 50 m each side of the boat for most of the items (like Aliani et al., 2003; Dufault and Whitehead, 1994). However, for items with neutral buoyancy remaining at the sub-surface, such as plastic Bags or other small debris, we estimated a conservative threshold of visibility of 10 m each side of the boat (Hinojosa and Thiel, 2009; Thiel et al., 2013, 2003). This measure allowed more accuracy in calculating densities when sorting data by litter categories, preventing estimation errors. In this way, density was calculated considering a monitored strip of 10 m for plastic Bags and other similar items, of 50 m for all other floating objects: for each transect the total density was defined by the sum of the two values. The sampling was not homogeneously distributed as different areas were covered each year. To overcome these differences, all records were mapped over a grid of 1 km × 1 km, for a total of 4665 cells. Using the fTools plugins in QGIS, we associated within each cell the total km travelled on effort, the number and type of items observed and the number of cetacean observations, in order to calculate standardised abundance of floating litter and cetaceans. The distance from nearest coast was also extracted for each cell. To avoid biases due to poorly surveyed cells, we selected only those with N100 m travelled on effort (4453 cells). On this basis, kernel density estimation was performed to show spatial clustering of floating litter and cetacean sightings, identifying areas of higher probability of occurrence. Analysis was weighted on the abundance values and carried out using the Heatmap plugin in QGIS over a radius of 5 km, considered an adequate range for floating litter, and therefore applied also to cetaceans. The whole distribution estimates of floating litter and cetaceans were represented by the 90% density contours, used to compare ranges and to calculate the percentage of shared surface between them. Cetacean ranges were compared with the distribution of plastic, considered the most representative category, using the Intersect function that extracts the surface of the area of overlap between the two layers of polygons. Overlap was calculated for all cetacean species, as well as for striped dolphin and fin whale that were the most sighted ones, and reported as percentage of these ranges. Higher density contours (70%) were found too limiting for the purpose of this study. 2.4. Statistical analyses A preliminary analysis was conducted within the plastic Bags category to investigate patterns of occurrence of the different sized fragments: a significant positive correlation (Spearman's R p b 0.0001)

was found between the abundance of small, medium, large fragments throughout the whole study period, indicating that on a large scale, this kind of items tends to distribute in the same way regardless the size. Consequently, we pooled together all items within this category. Spearman's Correlation was also applied to investigate relationships between litter abundance and distance from the nearest coast. Difference in marine litter composition between 2007 and 2008 was evaluated using the similarity percentage analysis (SIMPER, Clarke, 1993) with the Bray-Curtis similarity measure, to evaluate the relative contribution of each particular marine litter category to similarity. To investigate differences in litter density between years, months and categories the non-parametric tests of Mann-Whitney (MW) and Kruskall-Wallis (KW) were used; comparisons among categories were made on abundance values. All statistical analyses were carried out using the package PAST v. 2.17 (Hammer et al., 2001).

3. Results 3.1. Composition, abundance and density of floating macro-litter Between 2006 and 2015 281 transect were sampled for floating litter, covering an overall survey effort of 5171.52 km. 1993 objects were sighted throughout the entire study area, even in offshore transects, while no litter was observed over 12.4% of total km surveyed (Fig. 2). Among floating litter sighted during the whole study period (Table 1 and Fig. 3), the majority were made of Plastics (86.7%), mostly represented by Bags (65.9%) and Bottles (8.2%). Other plastic (10%) included balls, balloons, bottle caps, boat fenders and floating mattress, while plastic Cans only represented 2.6% and were never recorded in 2012 and 2015. Styrofoam items made up 9.5% of the floating litter, often occurring as fishing boxes or fragments. Other items represented only 3.8% of all the floating litter encountered and were as diversified as shoes, cardboard, wood crates, glass bottles, spray cans, cigarette butts, bodysurf and chairs. Marine litter total abundance in the study area was 0.41 items/km (± 0.57) while the mean density resulted of 14.98 items/km2 (±22.84). During the same surveys, a total of 2194 cetaceans were recorded during 292 sightings all through the area. The most frequent species observed were striped dolphin (210 sightings) and fin whale (42), followed by sperm whale (9), long-finned pilot whale (4), Risso's dolphin (3), bottlenose dolphin (2). In other observations, cetacean species were not identified (20 of small delphinids and 2 of large whales). Within the selected area 246 transect were considered, for a total survey effort of 4443.73 km; litter was encountered in the 90% of total effort performed (Table 1). The composition of the 1824 objects sighted was very similar to that of the entire study area (Plastics 86.3%, Styrofoam 9.8%, Other items 3.9%). Total abundance of marine litter resulted of 0.44 items/km (± 0.6) and a mean density of 16.21 items/km2 (± 24.09) was obtained in the selected area, that was then considered to be representative of the whole study area. Yearly composition showed the preponderance of Bags, which was always the most represented category (N 45%), except for 2006 when Bottles reached 39% (Fig. 4). Considering the other categories, Styrofoam reached the biggest proportion in July 2008 (20%) and Cans in 2014 (4.3%). Mean annual densities were investigated, showing minimum value in 2006, mainly represented by October surveys, and maximum in 2009–2010–2011 (Table 1 and Fig. 4). Statistics confirmed total densities of 2010–2011 as significantly higher than those resulting for 2006–2007–2008–2015 (KW test, p b 0.05). The high value obtained for 2009 was due to an outlier transect sampled offshore Cannes, where we detected a total of 66 items over 11 km surveyed. Considering the entire dataset, total litter abundance resulted higher at shorter distance from the nearest coast (Spearman's R = − 0.063


159

Fig. 2. Floating macro-litter observations during the whole 2006–2015 study period. The selected area is displayed in gray.

p b 0.0001), but this was not recorded considering each month separately. Within the selected area, a total of 259 cetacean sightings was recorded, accounting for a total 1981 animals. The most frequent species were striped dolphin (188), fin whale (36), sperm whale (9), followed by long-finned pilot whale (4), Risso's dolphin (2), bottlenose dolphin (2). 3.2. Comparison between 2007 and 2008 Data of 2007 and 2008 were collected between May and October and allowed detailed comparison at a monthly level. For a more accurate investigation, we considered all transects performed within the selected area, for a total effort of 1308 km covered in 2007 and 1708 km in 2008 (see Table 1). From 2007 to 2008 difference in total composition (May–September) was driven by an increase of Bags (SIMPER on presence of categories N56%), being always the dominant category over the others (Fig. 5,

KW within year, p b 0.0001). Percentage of composition decreased for Bottles and Other plastic, while Styrofoam occurrence raised, the three categories determining a cumulative contribution to dissimilarity of 34%; the remaining ones contributed to a lesser extent (b 5%). All Plastics represented in both years N 80% of litter composition, at total and monthly level. Results from pairwise Mann–Whitney tests between the total mean densities highlighted the similar presence of marine litter in the two years (Table 2 and Fig. 5). In fact, no statistical differences were detected between the total mean densities obtained for the whole period (May–September) and for each month (MW 2007 vs 2008, p N 0.05). Significant decrease of densities from 2007 to 2008 were instead observed for the categories Bottles and Other plastic (MW, p b 0.05), but the others did not change. Looking at the density of litter throughout the year, we could recognise a general trend with higher occurrence at the beginning and end of summer than in central summer months (Table 2 and Fig. 5). Mean total density in fact, showed peaks in May 2008, June 2007 and October 2008, while a decrease between July and September was observed in both

Fig. 3. Percentage composition of floating macro-litter categories observed during the whole 2006–2015 study period.

160


Fig. 4. Floating macro-litter observed during the whole 2006–2015 study period in the selected area. Left: annual percentage composition. Right: boxplots of annual mean densities (number of items/km2); one outlier transect (2009) was excluded to improve the visualisation of the results.

years. Significant differences (KW, p b 0.05) resulted for 2007 between June and August–September, and between May and September; July was excluded from the statistical analysis because of the few samples available. In 2008 total density of October was higher than those of July–September. Densities obtained for July and October 2006 were also consistent with this pattern (respectively 0.71 and 8.41 items/km2, Fig. 5). Looking at monthly densities of each litter category, in 2007 Bags and Styrofoam were the ones presenting significant decrease between June and August–September (KW, p b 0.05). In 2008 statistical differences among months (KW, p b 0.05) were observed for Bags: October N July–September; Cans: May–June–July N September; Styrofoam: June N August–September. Bottles was the only category not revealing significant monthly variations (Table 2). 3.3. Distribution of floating macro-litter and cetaceans We investigated in detail the distribution of all objects in the selected area, pooling together data of the whole study period on a grid of 1 km2 resolution. As previously shown, floating litter was widespread all through the study area but some uneven distribution was revealed. In fact, kernel analysis identified major distribution in the eastern part of the study area, for a total coverage of 4535 km2 included in the 90% isopleths (Fig. 6). Similar clustering was obtained considering only plastic objects, resulting in a global area of 5102 km2; distribution estimates for total litter and plastic corresponded by 97%, confirming plastic as representative of the whole floating litter even spatially. Densities estimates within the 70% probability contours defined a very reduced coverage, indicating limited areas of high accumulation. The global area (included in the 90% isopleths) estimated for cetacean presence in the whole study period occupied 3341 km2, mostly distributed in the eastern part of the study area. The 53.3% of this range resulted overlapping with the distribution of plastic, sharing an

area of 1781 km2. Looking at cetacean species, striped dolphin was the most common over the study area, occurring in single/coupled individuals, as well as large pods up to 80–150 animals. Fin whale was also quite frequent in the observations, mostly of isolated individuals, but groups of 3–4 animals were also recorded in front of Marseille. Total range calculated for striped dolphin was 2295 km2 overlapping by 61.4% with plastic distribution; fin whale sightings locations described a smaller range of 678 km2 presenting a 45.6% of correspondence with plastic presence. Main areas of co-occurrence were identified in the eastern part of the study area, where plastic density defined larger patches (Fig. 7A–B). Other species showed a scattered occurrence and the low number of sightings did not allow to perform a correct density estimation; however, we reported 9 sightings of squid-eaters (sperm whale, long-finned pilot whale, Risso's dolphin,) and one sighting of bottlenose dolphin occurring within the 90% density contour of plastic, accounting for more than the half of total records for these species (Fig. 7C). 4. Discussion 4.1. Composition, abundance and density of floating macro-litter Thanks to a consecutive database collected over a long period, our study gave an estimation of the composition, abundance and distribution of floating macro-litter in this part of the Liguro-Provençal basin, allowing interesting insight of the potential exposure of cetacean species to pollution. Floating litter was almost ubiquitous in the sampled area, confirming previous studies conducted in the same basin (Aliani et al., 2003; Cózar et al., 2015; Suaria and Aliani, 2014). Our results identified plastic as the most abundant and widespread items found, confirming that it is a permanent part of marine environment (Moore, 2015): as already emerged from previous studies conducted both in Mediterranean

Fig. 5. Total composition (left) and monthly densities (number of items/km2, ±5%) (right) of floating macro-litter observed in 2006, 2007, 2008.

N. Di-Méglio, I. Campana / Marine Pollution Bulletin 118 (2017) 155–166 Table 2 Mean densities (number of items/km2) of the floating macro-litter observed in 2007 and 2008: values per month, single categories and total litter. Mean density (N items/km2)

Bags

Bottles

Cans

Other plastic

Styrofoam

Other items

Total litter

2007

May June July August September Mean density 2007

10.33 21.58 0.00 4.56 3.58 11.09

0.21 0.69 0.00 0.29 0.16 0.37

0.08 0.11 0.00 0.32 0.08 0.12

0.34 0.65 0.37 0.61 0.21 0.46

0.02 0.88 0.37 0.00 0.00 0.34

0.25 0.06 0.00 0.00 0.12 0.10

11.24 23.97 0.74 5.78 4.16 12.47

2008

21.85 14.51 6.53 14.01 7.17 22.51 12.84

0.30 0.19 0.11 0.18 0.22 0.39 0.22

0.05 0.19 0.07 0.00 0.00 0.00 0.04

0.20 0.42 0.27 0.28 0.14 0.30 0.24

0.28 1.21 0.47 0.18 0.12 0.26 0.35

0.14 0.03 0.11 0.00 0.02 0.00 0.05

22.83 16.55 7.55 14.65 7.68 23.45 13.74

May June July August September October Mean density 2008

Sea and in other geographic areas, it occurred in almost the same proportions, representing between 60% and 80% of the total marine litter (e.g. Cózar et al., 2015; Derraik, 2002; Dufault and Whitehead, 1994; Morris, 1980; Suaria and Aliani, 2014; Thiel et al., 2013, 2011, 2003). This is also consistent with the outcomes of Deudero and Alomar (2015) who showed that in the Mediterranean Sea the highest amounts of plastics are reported for the north-western part. This well-known predominance of plastic at sea surface has been explained with its buoyancy and long-lasting characteristics, that make it more conspicuous during observations; as well, the widespread use of plastic products, also due to their cheapness, make them the majority of waste, easily discarded even after short usage, but also unintentionally lost and transported from land by rivers or wind (Derraik, 2002; Galgani et al., 2013; Gregory, 2009; Laist, 1997; Moore, 2015). Europe is the second producer in the global plastic market, and most of its production is generally converted into consumer packaging (PlasticsEurope, 2015), thus it is not surprising that Bags was the most recurring category in our samplings. We also demonstrated how the distribution of plastic bags described spatial occurrence of the total litter, and it was not depending on the fragments' size. This suggests that, for monitoring purposes (Arcangeli et al., 2015), surveys can be focused on macro-plastic, providing representative information on the total litter occurrence. Another important category was Styrofoam, which represented about 10% of total floating litter composition, in line with values reported by other researchers (Sá et al., 2015; Shiomoto and Kameda, 2005; Suaria and Aliani, 2014; Thiel et al., 2013; Yamashita and Tanimura, 2007). Hinojosa and Thiel (2009) instead, observed higher proportions of this material in the fjords of Chile, where intense aquaculture

161

activities are developed. Even in our study, this category gave an interesting indication on a monthly basis, presenting maximum occurrence in June, according to local fishing activities. Differences in sampling areas and techniques make comparisons among studies very challenging (Ryan, 2013); within the EU MSFD however, the number of items is requested for suitable comparison on litter amounts (Galgani et al., 2013). Our results obtained through a robust sampling effort, provided a mean density of floating litter for the whole study period of approximately 15 items/km2: similar range was observed on a yearly scale, except for 2010 and 2011, suggesting a quite stable amount of marine litter in the area, given that surveys covered different sections each year. Comparable densities were reported by Suaria and Aliani (2014) in the Sardinian Sea and Corsica Channel, even if from single surveys. Aliani et al. (2003) obtained similar values in the Ligurian Sea only for transects sampled in 1997, and not for the 2000, when lower densities were probably influenced by meteorological events. Earlier values reported for the whole basin were very much variable, instead, as Morris (1980) found about 2000 items/km2, while much lower surface density was inferred later by McCoy (1988, b2.5 items/km2). The variability in marine litter distribution and the gaps deriving from limited surveys produced uneven results all over the world (e.g. Law, 2010; Lecke-Mitchell and Mullin, 1997; Matsumura and Nasu, 1997; Moore et al., 2001; Ryan, 2013; Sá et al., 2015; Shiomoto and Kameda, 2005; Thiel et al., 2013; Uneputty and Evans, 1997; Yamashita and Tanimura, 2007), with only few studies presenting the same range of densities than ours (North Sea, Thiel et al., 2011; Nova Scotia, Dufault and Whitehead, 1994; Southern Chile, Thiel et al., 2003; Bay of Bengala, Ryan, 2013). That confirms why a multi-year monitoring is appropriate to provide information about the average levels and trends of pollution (Galgani et al., 2013, 2000). Thompson et al. (2004) found significant increase in floating plastic abundance from the 1960 to the 1990, but no variations in the last decade of their study, despite the increase in plastic production; they suggested a sort of compensation as a consequence of response to international regulations. Even Law (2010) observed no significant trends over 22 years in the North Atlantic, finding larger interannual variability only in the areas of extremely high densities. Here, we reported similar presence of marine litter through a 10-years time span, therefore suggesting a balance between inputs of material at sea and dispersal mechanisms, i.e. local and large-scale processes. 4.2. Possible sources Despite the constant average, our study seemed to highlight a dynamical pattern of floating litter densities, with minimum values in the middle of summer compared to other months, which was verified

Fig. 6. Kernel density estimation performed on 1 km × 1 km grid cells on abundance values of floating litter (left) and floating plastic (right) observed in the whole study period in the selected area. Relative 90% density contours are shown.

162


Fig. 7. Overlap between floating plastic and cetacean species. Kernel density estimation performed on 1 km × 1 km grid cells on abundance values of floating plastic and striped dolphin (A), floating plastic and fin whale (B). For other species only sightings locations are shown (C).


for both investigated years. Similar patterns were reported by LeckeMitchell and Mullin (1997), while other studies observed no seasonal variations (Thiel et al., 2013, 2011), attributing to several factors the production, transport and concentration of the debris. At a local scale, touristic centers, weather conditions, riverine inputs and biological activity are important features defining marine litter occurrence (Deudero and Alomar, 2015). In our study area, main sources surely include land based activities and riverine output, which are recognised among the primary sources of marine litter (Jambeck et al., 2015; Sadri and Thompson, 2014), but also fishing and shipping movements related to the large French ports might be important producer of the waste found the sea (Carić and Mackelworth, 2014; Sá et al., 2015). However, floating litter was found regardless of distance from shore as no correlation was detected in any month, suggesting no exclusive relationship with local coasts but possible inputs even from distant sources, as also confirmed for example by the occurrence of objects of Italian origin along the French coast around Nice (Galgani et al., 1995). During central summer months (July–September), the pressure due to touristic activities ashore and at sea significantly rise all along the French coast. Beaches are considered as sinks for floating litter, with sand acting as a natural trap (Araújo and Costa, 2006; Poeta et al., 2014; Van Cauwenberghe et al., 2013), and furthermore their maintenance and cleaning for touristic utilisation may limit the quantities of waste possibly reaching the sea. Summer is also the period when many sensibilisation activities take place to involve local people and tourists in beach cleaning, which can help prevent improper behaviour of bathers. On the contrary, the combined effects of the end of management and the change of general atmospheric regime can enhance land and river contribution, even from distant areas, inducing the increase of floating litter observed in other months. Looking at litter composition, Bags and Styrofoam were driving the variations among months. Bags and Bottles can have different and continuous sources all through the year, preventing any speculation about their origin. Conversely, some inference may come for Styrofoam which showed higher occurrence in June. The origin of this material is usually related to fishing activities (Hinojosa and Thiel, 2009; Suaria and Aliani, 2014), suggesting an influence of sea-based activities on the higher occurrence of litter in these periods, even if no other fishing-related items were detected. From these results, we can suppose that within our study area, marine litter has some constant inputs from local coastal activities, but even far away sources contribute to the pollution in this basin (Cózar et al., 2015), given its complex circulation patterns. Surely, it could be useful to improve our knowledge on the fine relationships between floating litter and meteorological and marine conditions to better understand its pathway. 4.3. Distribution of floating macro-litter and cetaceans Besides the importance of local sources, distribution of floating material is influenced by large mesoscale processes, such as winds, currents and gyres, which can transport the material even considerably far from the source areas (Dufault and Whitehead, 1994; Jambeck et al., 2015; Law, 2010; Moore, 2015; Thiel et al., 2011). Our study area is located along the Liguro-Provençal current, which plays an important role in transporting and distributing material (natural and anthropogenic) over the northern Mediterranean Sea, similarly to what occur in other large-scale circulation systems (e.g. Kuroshiro Current, Shiomoto and Kameda, 2005; Yamashita and Tanimura, 2007; North Atlantic, Law, 2010). Several simulations models of surface transport estimated fast spreading time for particles in the Ligurian Sea (around 800 km in 3 months, Mansui et al., 2015) due to this intense current, representing then an important transit system (Aliani and Molcard, 2003; van Sebille, 2014). In addition, the variable climatic regime of the northern Mediterranean Sea hampers the formation of long-term accumulation zones, resulting in the general low concentrations of debris indicated for this region (Cózar et al., 2015; Mansui et al., 2015). At a small scale, however,

163

the combination with wind-induced circulation can determine local retention mechanisms, that we identified in the eastern part of our study area in confined high density patches. As well, in the western part of the study area, where more pollution was expected because of the intense shipping loads (e.g. Carić and Mackelworth, 2014; Coll et al., 2012; Sá et al., 2015), we observed low amounts of litter at surface, as also reported by Collignon et al. (2012) from neustonic surveys: in fact, the main circulation pattern in the Gulf of Lion helps the retention of debris in its northern portion (Millot, 1999). Strong wind stress can potentially change water movements in the short-term, contributing to the dispersal of debris offshore (Collignon et al., 2012; Galgani et al., 1996, 1995), but also to its faster dilution and submersion, reducing density at surface (Astudillo et al., 2009; Kukulka et al., 2012; Suaria et al., 2016; Thiel et al., 2011). On the other hand, important sink areas of waste have been found in submarine canyons at the border of the Gulf of Lion continental shelf (Galgani et al., 2000, 1996, 1995; Pham et al., 2014; Tubau et al., 2015), confirming the complex and still unclear relationships among different sea compartments and the evident smallscale variability. It would therefore be interesting to realize analyses at a finer scale to identify the role of the hydrodynamics and the winds in driving the distribution of the marine litter, in particular in our zone of study where many marine species are concentrated. Indeed, the Liguro-Provençal basin is recognised as an ecologically rich area, hosting a diversified marine life, including cetaceans (Notarbartolo di Sciara et al., 2008; UNEP, 2013), but conservation concerns for many species have been also described (Coll et al., 2012; Notarbartolo di Sciara and Birkun, 2010). For example, the presence of cetaceans can be associated with convergence zones, where physiographic and biotic factors influence preys abundance, but also where marine litter accumulates (Fossi et al., 2016; Simmonds, 2012). Our data were mainly collected during summer, when all cetacean species take advantage of the great productivity of the basin, related to various mechanisms that enhance the primary production (Notarbartolo di Sciara et al., 2008). Our study showed that foraging habitats of cetaceans in this area overlap by 50% with surface litter, representing a high possibility of encounters, especially in the eastern sector. This result was surely guided by the larger range of striped dolphin, but it is noteworthy that even less frequent species presented more than the half of sightings included in the area of plastic distribution. We also stress that our estimates for cetaceans occurrence are highly conservative because calibrated on floating litter analyses, so the evaluation of their ranges, together with the overlap with marine pollution, are probably underrepresented. In this basin, cetacean species are known to exploit differentiate portions, according to their behaviour and feeding habits (e.g. Laran and Gannier, 2008; Praca and Gannier, 2007; UNEP, 2013), but the general co-occurrence of plastics and cetaceans can represent a potential exposure to this threat for all species. By detecting macro-plastic at surface we only described the visible portion of marine litter, which is composed by 92% by micro-plastics (b5 mm) (Eriksen et al., 2014; Suaria et al., 2016) and its ubiquitous distribution reported, rather than defined accumulation areas, implicates the greater possibility of interaction with all cetaceans. The impacts of plastic on marine species is well-recognised, mainly attributed to ingestion and entanglement (Baulch and Perry, 2014; Bergmann et al., 2015; Gall and Thompson, 2015; Laist, 1997; Simmonds, 2012), and produce multiple risk scenarios, according to the variability within all plastic objects and the species physical and behavioural characteristics. For example, sperm whale and fin whale report high levels of plastic contents because of their size and feeding strategies (De Stephanis et al., 2013; Fossi et al., 2016, 2012b; Mazzariol et al., 2011); while sperm whale can be mislead by plastic objects during its predatory activity, fin whale can directly ingest plastic material along with the preys during filter feeding activities occurring at surface, along with the indirect consumption through polluted zooplankton. Also small dolphins species exhibit accidental ingestion events (Baulch and Perry, 2014; Simmonds, 2012), with increasing reports coming from the Mediterranean Sea (Deudero and Alomar, 2015). Most of the information however, derives from studies based on stranded

164


animals, that represent only a small portion of the impacts occurring unseen at sea (Baulch and Perry, 2014; Simmonds, 2012). It has been estimated that 70% of the plastic sinks to the seafloor (Engler, 2012) as a consequence of reduced buoyancy due to fragmentation, water movements (Kukulka et al., 2012) or colonisation by different organisms (Aliani and Molcard, 2003; Barnes, 2002), therefore interaction with marine species can occur at different stages of this path and be not directly detectable. On the contrary, our study illustrates areas of co-occurrence of cetaceans and plastics, basically bags and packaging, where early stage of reasonable risk can be recognised (Coll et al., 2012). Again, the potential impact is only partially represented, as we surveyed litter at surface with no information about smaller fractions and its presence in water column (Barnes et al., 2009; Eriksen et al., 2014). Consumption of artificial materials has a variety of possible consequences, but other impacts need to be considered, because particular items can produce for example, entanglement or physical injuries (Baulch and Perry, 2014; Bergmann et al., 2015; Coe and Rogers, 1997; Derraik, 2002; Gall and Thompson, 2015; Laist, 1997); among these materials, metal, glass objects or fishing gears represented a minor proportion of floating litter from our surveys, but they have been found on the seafloor in the same area (Galgani et al., 2000). For example, we frequently observed floating Styrofoam objects, likely deriving from fishery industry; it can be reasonable to think that other fishing-related items can be found in the water column, representing risk elements for entanglement or ingestion, especially by deep-divers cetaceans like the sperm whale or the Risso's dolphin. For all these reasons, extrapolating true severity of marine litter interactions in wild populations of cetaceans is challenging (Deudero and Alomar, 2015) and detailed information is still needed to reliably quantify the problem at a specific level. It is finally necessary to remember that these situations constitute evident concern for marine organisms other than cetaceans, such as birds, sea turtles, fishes (e.g. Bergmann et al., 2015; Camedda et al., 2014; Davison and Asch, 2011; Ryan et al., 1988): this underlines the importance of tackling the issue of marine litter with respect to the whole marine community, especially in areas of high biodiversity like the Ligurian Sea (Coll et al., 2012). 5. Conclusions Our study highlighted the surface pollution by marine litter in a high energy basin, where interaction with cetaceans is likely to occur. Even if a general low density was observed, it is essential to remark that we monitored only the tip of the iceberg. In the Mediterranean Sea higher litter densities are reported for the seafloor than those estimated for floating litter (Pham et al., 2014; Stefatos et al., 1999; Tubau et al., 2015); nevertheless, the link between pollution in different marine compartments is not directly correlated and poorly studied (Schulz et al., 2015; Uneputty and Evans, 1997; Van Cauwenberghe et al., 2013). The use of complementary techniques for simultaneous surveys should be promoted, together with the detailed analysis of the dynamics of the study area; this potential synergy is necessary to better understand the impacts of marine litter at different levels of the ecosystems and in particular in cetaceans. Indeed, the impacts of marine macro-litter on cetaceans are numerous and can be either direct by ingestion, strangulation or indirect by ingestion of microparticles after degradation of macro-litter in the environment (Bergmann et al., 2015). The mechanisms of cetacean ingestion of waste are not well known, but from what can be seen at sea, cetaceans are well able to differentiate waste from their prey when they see it. We observed pilot-whale and Risso's dolphin playing for hours with plastic bags without ingesting them. Therefore it appears that cetaceans could only ingest macro-litter when using their echolocation system to detect their preys during deep dives or at night. They can confuse macro-litter, especially plastics fragments, with their preys, like squids. Moreover, these animals may also inadvertently swallow plastic during secondary ingestion, which occurs when animals feed on preys which have previously ingested debris, or during the filter feeding activity for the fin whale. Furthermore, the

degradation of macro-litter in micro-litter induces many other impacts on marine fauna. It is particularly the case for plastic which breaks up in micro-plastic, releasing the toxic chemicals that have been added to enhance the performance of these materials (such as phthalates, nonylphenol, bisphenol A, brominated flame retardants) (Bergmann et al., 2015; Teuten et al., 2009). Moreover, plastics fix toxic persistent organic pollutants such as DDT (dichlorodiphenyltrichloroethane, a pesticide) and PCBs (polychlorobiphenyls) or heavy metals, which also contaminate animals when they ingest the micro-fragments (Bergmann et al., 2015). All these toxic chemicals have important effects on marine fauna and in particular they are recognised as endocrine disruptors affecting, among other things, reproduction, cancers and liver toxicity (Rochman et al., 2013, 2014). Macro-litter can thus impact cetaceans in multiple ways and the repercussions can be carried out at the level of an individual or a population. This is of particular concern for species such as the sperm whale, which is already considered to be “Endangered” in the Mediterranean Sea (IUCN, 2016). Actions to reduce the presence of macro-litter at sea must therefore continue because the Mediterranean Sea is probably one of the most polluted areas, both at the surface and on the bottom (Cózar et al., 2015; Galgani et al., 2000). Our study provided only a preliminary identification of areas where cetaceans could be threatened by marine pollution, but finer-resolution studies are needed to improve the evaluation of potential direct or indirect impacts on cetaceans and other marine species living in the LiguroProvençal basin. This kind of information assumes relevant importance in areas of recognised biodiversity and strong anthropogenic pressures, such as the Mediterranean Sea (Coll et al., 2012; Halpern et al., 2008; Pérès, 1978). Finally, our data revealed a sensitive situation within the protected area of the Pelagos Sanctuary, but the complex combination with climatic mechanisms hampers the direct bearing of marine litter sources, making more difficult to establish targeted conservation actions.

Acknowledgements We would like to thank Dr. Léa David for her useful advice as well as all the people who participated in the data collection during the cruises of EcoOcéan Institut. Some of the campaigns have been supported by WWF France (Cap cétacés) and Nicolas Hulot Fondation (Objectif cétacés). Nathalie Di-Méglio planned and performed all data collection from 2006 to 2015, supervised the analyses and the paper structure at all stages. Ilaria Campana conducted all the analyses and wrote the first draft of this paper. All authors have approved the final version of this article. References Aliani, S., Molcard, A., 2003. Hitch-hiking on floating marine debris: macrobenthic species in the Western Mediterranean Sea. Hydrobiologia 503, 59–67. Aliani, S., Griffa, A., Molcard, A., 2003. Floating debris in the Ligurian Sea, north-western Mediterranean. Mar. Pollut. Bull. 46:1142–1149. http://dx.doi.org/10.1016/S0025326X(03)00192-9. Araújo, M.C.B., Costa, M.F., 2006. Municipal services on tourist beaches: costs and benefits of solid waste collection. J. Coast. Res. 225:1070–1075. http://dx.doi.org/10.2112/030069.1. Arcangeli, A., Azzolin, M., Campana, I., Castelli, A., Luperini, C., Marini, L., Paraboschi, M., Pellegrino, G., Ruvolo, A., Tringali, M., Vetrugno, A., Crosti, R., 2015. Cetaceans at risk by plastic debris: a protocol for simultaneous monitoring of marine litter and marine mega-fauna. First results from the FLT Mediterranean monitoring network. Biol. Mar. Mediterr. 22 (1), 218–219. Ariza, E., Jiménez, J.A., Sardá, R., 2008. Seasonal evolution of beach waste and litter during the bathing season on the Catalan coast. Waste Manag. 28:2604–2613. http://dx.doi. org/10.1016/j.wasman.2007.11.012. Astudillo, J.C., Bravo, M., Dumont, C.P., Thiel, M., 2009. Detached aquaculture buoys in the SE Pacific: potential dispersal vehicles for associated organisms. Aquat. Biol. 5: 219–231. http://dx.doi.org/10.3354/ab00151. Barnes, D.K.A., 2002. Biodiversity: invasions by marine life on plastic debris. Nature 416: 808–809. http://dx.doi.org/10.1038/416808a. Barnes, D.K.A., Galgani, F., Thompson, R.C., Barlaz, M., 2009. Accumulation and fragmentation of plastic debris in global environments. Philos. Trans. R. Soc. Lond. Ser. B Biol. Sci. 364:1985–1998. http://dx.doi.org/10.1098/rstb.2008.0205.

N. Di-Méglio, I. Campana / Marine Pollution Bulletin 118 (2017) 155–166 Baulch, S., Perry, C., 2014. Evaluating the impacts of marine debris on cetaceans. Mar. Pollut. Bull. 80:210–221. http://dx.doi.org/10.1016/j.marpolbul.2013.12.050. Béranger, K., Drillet, Y., Houssais, M.N., Testor, P., Bourdallé-Badie, R., Alhammoud, B., Bozec, A., Mortier, L., Bouruet-Aubertot, P., Crépon, M., 2010. Impact of the spatial distribution of the atmospheric forcing on water mass formation in the Mediterranean Sea. J. Geophys. Res. Oceans 115 (C12). http://dx.doi.org/10. 1029/2009JC005648. Bergmann, M., Gutow, L., Klages, M., 2015. Marine Anthropogenic Litter. Springer International Publishing, Cham 456pp. 0.1007/978-3-319-16510-3_1. Camedda, A., Marra, S., Matiddi, M., Massaro, G., Coppa, S., Perilli, A., Ruiu, A., Briguglio, P., de Lucia, G.A., 2014. Interaction between loggerhead sea turtles (Caretta caretta) and marine litter in Sardinia (Western Mediterranean Sea). Mar. Environ. Res. 100:25–32. http://dx.doi.org/10.1016/j.marenvres.2013.12.004. Campana, I., Crosti, R., Angeletti, D., Carosso, L., David, L., Di-Méglio, N., Moulins, A., Rosso, M., Tepsich, P., Arcangeli, A., 2015. Cetacean response to summer maritime traffic in the Western Mediterranean Sea. Mar. Environ. Res. 109, 1–8. Carić, H., Mackelworth, P., 2014. Cruise tourism environmental impacts - the perspective from the Adriatic Sea. Ocean Coast. Manag. http://dx.doi.org/10.1016/j.ocecoaman. 2014.09.008. Carpenter, E.J., Smith, K.L.J., 1972. Plastics on the Sargasso Sea Surface. Science 175: 1240–1241. http://dx.doi.org/10.1126/science.175.4027.1240. Clarke, K.R., 1993. Non-parametric multivariate analyses of changes in community structure. Aust. J. Ecol. 18, 117–143. Coe, J.M., Rogers, D.B., 1997. Marine Debris: Sources, Impacts, and Solutions. Springer Science & Business Media, New York 432 pp. Cole, M., Lindeque, P., Halsband, C., Galloway, T.S., 2011. Microplastics as contaminants in the marine environment: a review. Mar. Pollut. Bull. http://dx.doi.org/10.1016/j. marpolbul.2011.09.025. Coll, M., Piroddi, C., Albouy, C., Ben Rais Lasram, F., Cheung, W.W.L., Christensen, V., Karpouzi, V.S., Guilhaumon, F., Mouillot, D., Paleczny, M., Palomares, M.L., Steenbeek, J., Trujillo, P., Watson, R., Pauly, D., 2012. The Mediterranean Sea under siege: spatial overlap between marine biodiversity, cumulative threats and marine reserves. Glob. Ecol. Biogeogr. 21:465–480. http://dx.doi.org/10.1111/j.1466-8238. 2011.00697.x. Collignon, A., Hecq, J.H., Glagani, F., Voisin, P., Collard, F., Goffart, A., 2012. Neustonic microplastic and zooplankton in the North Western Mediterranean Sea. Mar. Pollut. Bull. 64:861–864. http://dx.doi.org/10.1016/j.marpolbul.2012.01.011. Cózar, A., Sanz-Martín, M., Martí, E., González-Gordillo, J.I., Ubeda, B., Gálvez, J.Á., Irigoien, X., Duarte, C.M., 2015. Plastic accumulation in the Mediterranean Sea. PLoS One 10: 1–12. http://dx.doi.org/10.1371/journal.pone.0121762. David, L., Alleaume, S., Guinet, C., 2011. Evaluation of the potential of collision between fin whales and maritime traffic in the north-western Mediterranean Sea in summer, and mitigation solutions. J. Mar. Anim. Ecol. 4, 17–28. Davison, P., Asch, R.G., 2011. Plastic ingestion by mesopelagic fishes in the North Pacific Subtropical Gyre. Mar. Ecol. Prog. Ser. 432:173–180. http://dx.doi.org/10.3354/ meps09142. De Stephanis, R., Giménez, J., Carpinelli, E., Gutierrez-Exposito, C., Cañadas, A., 2013. As main meal for sperm whales: plastics debris. Mar. Pollut. Bull. 69:206–214. http:// dx.doi.org/10.1016/j.marpolbul.2013.01.033. Derraik, J.G., 2002. The pollution of the marine environment by plastic debris: a review. Mar. Pollut. Bull. 44:842–852. http://dx.doi.org/10.1016/S0025-326X(02)00220-5. Deudero, S., Alomar, C., 2015. Mediterranean marine biodiversity under threat: reviewing influence of marine litter on species. Mar. Pollut. Bull. 98:58–68. http://dx.doi.org/10. 1016/j.marpolbul.2015.07.012. Dufault, S., Whitehead, H., 1994. Floating marine pollution in ‘the Gully’ on the continental slope, Nova Scotia. Mar. Pollut. Bull. 28, 489–493. Endo, S., Takizawa, R., Okuda, K., Takada, H., Chiba, K., Kanehiro, H., Ogi, H., Yamashita, R., Date, T., 2005. Concentration of polychlorinated biphenyls (PCBs) in beached resin pellets: variability among individual particles and regional differences. Mar. Pollut. Bull. 50:1103–1114. http://dx.doi.org/10.1016/j.marpolbul.2005.04.030. Engler, R.E., 2012. The complex interaction between marine debris and toxic chemicals in the ocean. Environ. Sci. Technol. http://dx.doi.org/10.1021/es3027105. Eriksen, M., Lebreton, L.C.M., Carson, H.S., Thiel, M., Moore, C.J., Borerro, J.C., Galgani, F., Ryan, P.G., Reisser, J., 2014. Plastic pollution in the world's oceans: more than 5 trillion plastic pieces weighing over 250,000 tons afloat at sea. PLoS One 9:1–15. http://dx.doi.org/10.1371/journal.pone.0111913. European Commission, 2008. Directive 2008/56/EC of the European Parliament and of the Council of 17 June 2008 establishing a framework for community action in the field of marine environmental policy (Marine Strategy Framework Directive). Off. J. Eur. Union L164, 19–40. Fossi, M.C., Casini, S., Caliani, I., Panti, C., Marsili, L., Viarengo, A., Giangreco, R., Notarbartolo di Sciara, G., Serena, F., Ouerghi, A., Depledge, M.H., 2012a. The role of large marine vertebrates in the assessment of the quality of pelagic marine ecosystems. Mar. Environ. Res. 77:156–158. http://dx.doi.org/10.1016/j.marenvres.2012. 03.003. Fossi, M.C., Panti, C., Guerranti, C., Coppola, D., Giannetti, M., Marsili, L., Minutoli, R., 2012b. Are baleen whales exposed to the threat of microplastics? A case study of the Mediterranean fin whale (Balaenoptera physalus). Mar. Pollut. Bull. 64:2374–2379. http:// dx.doi.org/10.1016/j.marpolbul.2012.08.013. Fossi, M.C., Baini, M., Marsili, L., Coppola, D., Baini, M., Giannetti, M., Guerranti, C., Marsili, L., Panti, C., de Sabata, E., Clò, S., 2014. Large filter feeding marine organisms as indicators of microplastic in the pelagic environment: the case studies of the Mediterranean basking shark (Cetorhinus maximus) and fin whale (Balaenoptera physalus). Mar. Environ. Res. 100:17–24. http://dx.doi.org/10.1016/j.marenvres.2014.02.002. Fossi, M.C., Marsili, L., Baini, M., Giannetti, M., Coppola, D., Guerranti, C., Caliani, I., Minutoli, R., Lauriano, G., Finoia, M.G., Rubegni, F., Panigada, S., Bérubé, M., Urban

165

Ramirez, J., Panti, C., 2016. Fin whales and microplastics: the Mediterranean Sea and the Sea of Cortez scenarios. Environ. Pollut. 209:68–78. http://dx.doi.org/10. 1016/j.envpol.2015.11.022. Galgani, F., Jaunet, F., Campillo, A., Guenegen, X., His, E., 1995. Distribution and abundance of debris on the continental shelf of the north-western Mediterranean sea. Mar. Pollut. Bull. 30, 713–717. Galgani, F., Souplet, A., Cadiou, Y., 1996. Accumulation of debris on the deep sea floor off the French Mediterranean coast. Mar. Ecol. Prog. Ser. 142:225–234. http://dx.doi.org/ 10.3354/meps142225. Galgani, F., Leaute, J.P., Moguedet, P., Souplet, A., Verin, Y., Carpentier, A., Goraguer, H., Latrouite, D., Andral, B., Cadiou, Y., Mahe, J.C., Poulard, J.C., Nerisson, P., 2000. Litter on the sea floor along European coasts. Mar. Pollut. Bull. 40:516–527. http://dx.doi. org/10.1016/S0025-326X(99)00234-9. Galgani, F., Fleet, D., Franeker, J.V., Katsanevakis, S., Maes, T., Mouat, J., Oosterbaan, L., Poitou, I., Hanke, G., Thompson, R., Amato, E., Birkun, A., Janssen, C., 2010. Task Group 10 Report: Marine Litter, Marine Strategy Framework Directive. Galgani, F., Hanke, G., Werner, S., De Vrees, L., 2013. Marine litter within the European Marine Strategy Framework Directive. ICES J. Mar. Sci. http://dx.doi.org/10.1093/ icesjms/fst122. Galgani, F., Claro, F., Depledge, M., Fossi, C., 2014. Monitoring the impact of litter in large vertebrates in the Mediterranean Sea within the European Marine Strategy Framework Directive (MSFD): constraints, specificities and recommendations. Mar. Environ. Res. 100:3–9. http://dx.doi.org/10.1016/j.marenvres.2014.02.003. Galil, B.S., Golik, A., Turkay, M., 1995. Litter at the bottom of the sea - a sea-bed survey in the eastern Mediterranean. Mar. Pollut. Bull. 30:22–24. http://dx.doi.org/10.1016/ 0025-326X(94)00103-G. Gall, S.C., Thompson, R.C., 2015. The impact of debris on marine life. Mar. Pollut. Bull. 92: 170–179. http://dx.doi.org/10.1016/j.marpolbul.2014.12.041. Goldberg, E.D., 1994. Diamonds and plastics are forever? Mar. Pollut. Bull. 28, 466. Golik, A., Gertner, Y., 1992. Litter on the Israeli coastline. Mar. Environ. Res. 33:1–15. http://dx.doi.org/10.1016/0141-1136(92)90002-4. Gomerčić, H., Duras Gomerčić, M., Gomerčić, T., Lucić, H., Dalebout, M., Galov, A., Škrtić, D., Ćurković, S., Vuković, S., Huber, D., 2006. Biological aspects of Cuvier's beaked whale (Ziphius cavirostris) recorded in the Croatian part of the Adriatic Sea. Eur. J. Wildl. Res. 52:182–187. http://dx.doi.org/10.1007/s10344-006-0032-8. Gregory, M.R., 2009. Environmental implications of plastic debris in marine settings–entanglement, ingestion, smothering, hangers-on, hitch-hiking and alien invasions. Philos. Trans. R. Soc. Lond. Ser. B Biol. Sci. 364:2013–2025. http://dx.doi.org/10. 1098/rstb.2008.0265. Halpern, B.S., Walbridge, S., Selkoe, K.A., Kappel, K.V., Micheli, F., D'Agrosa, C., Bruno, J.F., Casey, K.S., Ebert, C., Fox, H.E., Fujita, R., Heinemann, D., Lenihan, H.S., Madin, E.M.P., Perry, M.T., Selig, E.R., Spalding, M., Steneck, R., Watson, R., 2008. A global map of human impact on marine ecosystems. Science 319:948–952. http://dx.doi.org/10. 1126/science.1149345. Hammer, Ø., Harper, D.A.T., Ryan, P.D., 2001. PAST: paleontological statistics software package for education and data analysis. Palaeontol. Electron. 4 (1):1–9. http://dx. doi.org/10.1016/j.bcp.2008.05.025. Hinojosa, I.A., Thiel, M., 2009. Floating marine debris in fjords, gulfs and channels of southern Chile. Mar. Pollut. Bull. 58:341–350. http://dx.doi.org/10.1016/j.marpolbul. 2008.10.020. IUCN, 2016. Red List of Threatened Species. Version 2016-3. http://www.iucnredlist.org (Downloaded on 30 January 2017). Jambeck, J.R., Geyer, R., Wilcox, C., Siegler, T.R., Perryman, M., Andrady, A., Narayan, R., Lavender, K., 2015. Plastic waste inputs from land into the ocean. Science 347: 768–770. http://dx.doi.org/10.1017/CBO9781107415386.010. Kornilios, S., Drakopoulos, P.G., Dounas, C., 1998. Pelagic tar, dissolved/dispersed petroleum hydrocarbons and plastic distribution in the Cretan Sea, Greece. Mar. Pollut. Bull. 36:989–993. http://dx.doi.org/10.1016/S0025-326X(98)00102-7. Kukulka, T., Proskurowski, G., Morét-Ferguson, S., Meyer, D.W., Law, K.L., 2012. The effect of wind mixing on the vertical distribution of buoyant plastic debris. Geophys. Res. Lett. 39:1–6. http://dx.doi.org/10.1029/2012GL051116. Laist, D., 1997. Impacts of marine debris: entanglement of marine life in marine debris including a comprehensive list of species with entanglement and ingestion records. In: Coe, J.M., Rogers, D.B. (Eds.), Marine Debris - Sources, Impacts and Solutions. Springer-Verlag, New York:pp. 99–139 http://dx.doi.org/10.1007/978-1-4613-8486-1_10. Laran, S., Gannier, A., 2008. Spatial and temporal prediction of fin whale distribution in the northwestern Mediterranean Sea. ICES J. Mar. Sci. 65:1260–1269. http://dx.doi. org/10.1093/icesjms/fsn086. Laran, S., Pettex, E., Authier, M., Blanck, A., David, L., Dorémus, G., Falchetto, H., Monestiez, P., Van Canneyt, O., Ridoux, V., 2016. Seasonal distribution and abundance of cetaceans within French waters - part I: the North-Western Mediterranean, including the Pelagos sanctuary. Deep-Sea Res. II Top. Stud. Oceanogr. http://dx.doi.org/10. 1016/j.dsr2.2016.12.011. Law, K.L., 2010. Plastic Accumulation in the North Atlantic Subtropical Gyre. Science 329: 1185–1188. http://dx.doi.org/10.1126/science.1192321. Lecke-Mitchell, K.M., Mullin, K., 1997. Floating marine debris in the US Gulf of Mexico. Mar. Pollut. Bull. 34:702–705. http://dx.doi.org/10.1016/S0025-326X(97)00027-1. Levy, A.M., Brenner, O., Scheinin, A., Morick, D., Ratner, E., Goffman, O., Kerem, D., 2009. Laryngeal snaring by ingested fishing net in a common bottlenose dolphin (Tursiops truncatus) off the Israeli shoreline. J. Wildl. Dis. 45, 834–838. Mansui, J., Molcard, A., Ourmières, Y., 2015. Modelling the transport and accumulation of floating marine debris in the Mediterranean basin. Mar. Pollut. Bull. 91:249–257. http://dx.doi.org/10.1016/j.marpolbul.2014.11.037. Mato, Y., Isobe, T., Takada, H., Kanehiro, H., Ohtake, C., Kaminuma, T., 2001. Plastic resin pellets as a transport medium for toxic chemicals in the marine environment. Environ. Sci. Technol. 35:318–324. http://dx.doi.org/10.1021/es0010498.

166


Matsumura, S., Nasu, K., 1997. Distribution of floating debris in the North Pacific Ocean: sighting surveys 1986–1991. In: Coe, J.M., Rogers, D.B. (Eds.), Marine Debris: Sources, Impacts, and Solution. Springer, New York, pp. 15–24. Mazzariol, S., Guardo, G. Di, Petrella, A., Marsili, L., Fossi, C.M., Leonzio, C., Zizzo, N., Vizzini, S., Gaspari, S., Pavan, G., Podestà, M., Garibaldi, F., Ferrante, M., Copat, C., Traversa, D., Marcer, F., Airoldi, S., Frantzis, A., de Beraldo Quirós, Y., Cozzi, B., Fernández, A., 2011. Sometimes sperm whales (Physeter macrocephalus) cannot find their way back to the high seas: a multidisciplinary study on a mass stranding. PLoS One 6. http://dx.doi. org/10.1371/journal.pone.0019417. McCoy, F.W., 1988. Floating megalitter in the eastern Mediterranean. Mar. Pollut. Bull. 19: 25–28. http://dx.doi.org/10.1016/0025-326X(88)90749-7. McKinney, R.L., 1998. On predicting biotic homogenization–species area patterns in marine biota. Glob. Ecol. Biogeogr. Lett. 7, 297–301. Millot, C., 1999. Circulation in the Western Mediterranean Sea. J. Mar. Syst. 20:423–442. http://dx.doi.org/10.1016/S0924-7963(98)00078-5. Moore, C.J., 2015. How much plastic is in the ocean? You tell me! Mar. Pollut. Bull. 92:1–3. http://dx.doi.org/10.1016/j.marpolbul.2014.11.042. Moore, C.J., Moore, S.L., Leecaster, M.K., Weisberg, S.B., 2001. A comparison of plastic and plankton in the North Pacific central gyre. Mar. Pollut. Bull. 42 (12), 1297–1300. Morris, R.J., 1980. Floating plastic debris in the Mediterranean. Mar. Pollut. Bull. 11:125. http://dx.doi.org/10.1016/0025-326X(80)90073-9. Munari, C., Corbau, C., Simeoni, U., Mistri, M., 2016. Marine litter on Mediterranean shores: analysis of composition, spatial distribution and sources in north-western Adriatic beaches. Waste Manag. 49:483–490. http://dx.doi.org/10.1016/j.wasman. 2015.12.010. Notarbartolo di Sciara, G., Birkun Jr., A., 2010. Conserving Whales, Dolphins and Porpoises in the Mediterranean and Black Sea: An ACCOBAMS Status Report. ACCOBAMS, Monaco. Notarbartolo di Sciara, G., Agardy, T., Hyrenbach, D., Scovazzi, T., Van Klaveren, P., 2008. The Pelagos Sanctuary for Mediterranean marine mammals. Aquat. Conserv. Mar. Freshwat. Ecosyst. http://dx.doi.org/10.1002/aqc.855. Pérès, J.M., 1978. Vulnérabilité des écosystèmes Méditerranéens à la pollution. Ocean Manage. 3, 2. Pham, C.K., Ramirez-Llodra, E., Alt, C.H.S., Amaro, T., Bergmann, M., Canals, M., Company, J.B., Davies, J., Duineveld, G., Galgani, F., Howell, K.L., Huvenne, V.A.I., Isidro, E., Jones, D.O.B., Lastras, G., Morato, T., Gomes-Pereira, J.N., Purser, A., Stewart, H., Tojeira, I., Tubau, X., Van Rooij, D., Tyler, P.A., 2014. Marine litter distribution and density in European seas, from the shelves to deep basins. PLoS One 9. http://dx.doi.org/10.1371/ journal.pone.0095839. PlasticsEurope, 2015. Plastics - The Facts 2014/2015: An Analysis of European Plastics Production, Demand and Waste Data. PlasticsEurope, pp. 1–34. Poeta, G., Battisti, C., Acosta, A.T.R., 2014. Marine litter in Mediterranean sandy littorals: spatial distribution patterns along central Italy coastal dunes. Mar. Pollut. Bull. 89: 168–173. http://dx.doi.org/10.1016/j.marpolbul.2014.10.011. Praca, E., Gannier, A., 2007. Ecological niche of three teuthophageous odontocetes in the northwestern Mediterranean Sea. Ocean Sci. Discuss. 4:785–815. http://dx.doi.org/ 10.5194/osd-4-785-2007. Quantum GIS Development Team, 2014. Quantum GIS Geographic Information System. Open Source Geospatial Foundation Project. http://qgis.osgeo.org. Rochman, C.M., Hoh, E., Kurobe, T., Teh, S.J., 2013. Ingested plastic transfers hazardous chemicals to fish and induces hepatic stress. Sci. Rep. 3, 3263. Rochman, C.M., Kurobe, T., Flores, I., Teh, S.J., 2014. Early warning signs of endocrine disruption in adult fish from the ingestion of polyethylene with and without sorbed chemical pollutants from the marine environment. Sci. Total Environ. 493, 656–661. Ryan, P.G., 2013. A simple technique for counting marine debris at sea reveals steep litter gradients between the Straits of Malacca and the Bay of Bengal. Mar. Pollut. Bull. 69: 128–136. http://dx.doi.org/10.1016/j.marpolbul.2013.01.016. Ryan, P.G., Connell, A.D., Gardner, B.D., 1988. Plastic ingestion and PCBs in seabirds: is there a relationship? Mar. Pollut. Bull. 19:174–176. http://dx.doi.org/10.1016/0025326X(88)90674-1. Sá, S., Bastos-Santos, J., Araújo, H., Ferreira, M., Duro, V., Alves, F., Panta-Ferreira, B., Nicolau, L., Eira, C., Vingada, J., 2015. Spatial distribution of floating marine debris in offshore continental Portuguese waters. Mar. Pollut. Bull. 1–10. http://dx.doi.org/10. 1016/j.marpolbul.2016.01.011.

Sadri, S.S., Thompson, R.C., 2014. On the quantity and composition of floating plastic debris entering and leaving the Tamar Estuary, Southwest England. Mar. Pollut. Bull. 81, 55–60. Schulz, M., Krone, R., Dederer, G., Wätjen, K., Matthies, M., 2015. Comparative analysis of time series of marine litter surveyed on beaches and the seafloor in the southeastern North Sea. Mar. Environ. Res. 106:61–67. http://dx.doi.org/10.1016/j.marenvres. 2015.03.005. Shiomoto, A., Kameda, T., 2005. Distribution of manufactured floating marine debris in near-shore areas around Japan. Mar. Pollut. Bull. 50:1430–1432. http://dx.doi.org/ 10.1016/j.marpolbul.2005.08.020. Simmonds, M.P., 2012. Cetaceans and marine debris: the great unknown. J. Mar. Biol. 2012:1–8. http://dx.doi.org/10.1155/2012/684279. Stefatos, A., Charalampakis, M., Papatheodorou, G., Ferentinos, G., 1999. Marine debris on the Sea floor of the Mediterranean Sea: examples from two enclosed gulfs in Western Greece. Mar. Pollut. Bull. 38, 389–393. Suaria, G., Aliani, S., 2014. Floating debris in the Mediterranean Sea. Mar. Pollut. Bull. 86: 494–504. http://dx.doi.org/10.1016/j.marpolbul.2014.06.025. Suaria, G., Avio, C.G., Mineo, A., Lattin, G.L., Magaldi, M.G., Belmonte, G., Moore, C.J., Regoli, F., Aliani, S., 2016. The Mediterranean Plastic Soup: synthetic polymers in Mediterranean surface waters. Sci. Rep. 6:37551. http://dx.doi.org/10.1038/srep37551. Teuten, E.L., Rowland, S.J., Galloway, T.S., Thompson, R.C., 2007. Potential for plastics to transport hydrophobic contaminants. Environ. Sci. Technol. 41:7759–7764. http:// dx.doi.org/10.1021/es071737s. Teuten, E.L., Saquing, J.M., Knappe, D.R., Barlaz, M.A., Jonsson, S., Björn, A., Rowland, S.J., Thompson, R.C., Galloway, T.S., Yamashita, R., OCHI, D., Watanuki, Y., Moore, C., Viet, P.H., Tana, T.S., Prudente, M., Boonyatumanond, R., Zakaria, M.P., Akkhavong, K., Ogata, Y., Hirai, H., Iwasa, S., Mizukawa, K., Hagino, Y., Imamura, A., Saha, M., Takada, H., 2009. Transport and release of chemicals from plastics to the environment and to wildlife. Philos. Trans. R. Soc. B 364, 2027–2045. Thiel, M., Hinojosa, I., Vásquez, N., Macaya, E., 2003. Floating marine debris in coastal waters of the SE-Pacific (Chile). Mar. Pollut. Bull. 46:224–231. http://dx.doi.org/10.1016/ S0025-326X(02)00365-X. Thiel, M., Hinojosa, I.A., Joschko, T., Gutow, L., 2011. Spatio-temporal distribution of floating objects in the German Bight (North Sea). J. Sea Res. 65:368–379. http://dx.doi.org/ 10.1016/j.seares.2011.03.002. Thiel, M., Hinojosa, I.A., Miranda, L., Pantoja, J.F., Rivadeneira, M.M., Vásquez, N., 2013. Anthropogenic marine debris in the coastal environment: a multi-year comparison between coastal waters and local shores. Mar. Pollut. Bull. 71:307–316. http://dx.doi. org/10.1016/j.marpolbul.2013.01.005. Thompson, R.C., Olsen, Y., Mitchell, R.P., Davis, A., Rowland, S.J., John, A.W.G., McGonigle, D., Russell, A.E., 2004. Lost at sea: where is all the plastic? Science 304:838. http://dx. doi.org/10.1126/science.1094559. Tubau, X., Canals, M., Lastras, G., Rayo, X., Rivera, J., Amblas, D., 2015. Marine litter on the floor of deep submarine canyons of the Northwestern Mediterranean Sea: the role of hydrodynamic processes. Prog. Oceanogr. 134:379–403. http://dx.doi.org/10.1016/j. pocean.2015.03.013. UNEP-MAP-RAC/SPA, 2013. In: David, L., Di-Méglio, N. (Eds.), Important Areas for the Conservation of Cetaceans in the Gulf of Lions Shelf and Slope Area: Synthesis of Existing Data on Cetaceans and Threats. RAC/SPA, Tunis 37 pp. Uneputty, P., Evans, S.M., 1997. The impact of plastic debris on the biota of tidal flats in Ambon Bay (Eastern Indonesia). Mar. Environ. Res. 44:233–242. http://dx.doi.org/ 10.1016/S0141-1136(97)00002-0. Van Cauwenberghe, L., Claessens, M., Vandegehuchte, M.B., Mees, J., Janssen, C.R., 2013. Assessment of marine debris on the Belgian Continental Shelf. Mar. Pollut. Bull. 73: 161–169. http://dx.doi.org/10.1016/j.marpolbul.2013.05.026. van Sebille, E., 2014. Adrift.org.au - a free, quick and easy tool to quantitatively study planktonic surface drift in the global ocean. J. Exp. Mar. Biol. Ecol. 461:317–322. http://dx.doi.org/10.1016/j.jembe.2014.09.002. Yamashita, R., Tanimura, A., 2007. Floating plastic in the Kuroshio current area, western North Pacific Ocean. Mar. Pollut. Bull. 54:464–488. http://dx.doi.org/10.1016/j. marpolbul.2006.11.016.