Size and dynamics of microplastic in gastrointestinal tracts of Northern Fulmars (Fulmarus glacialis) and Sooty Shearwaters (Ardenna grisea)

MPB-08283; No of Pages 8 Marine Pollution Bulletin xxx (2017) xxx–xxx

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

Size and dynamics of microplastic in gastrointestinal tracts of Northern Fulmars (Fulmarus glacialis) and Sooty Shearwaters (Ardenna grisea) Alicia K. Terepocki a,b, Alex T. Brush a,b, Lydia U. Kleine a,b, Gary W. Shugart a,⁎, Peter Hodum b a b

Slater Museum of Natural History, University of Puget Sound, Tacoma, WA 98416, United States Biology, University of Puget Sound, Tacoma, WA 98416, United States

a r t i c l e

i n f o

Article history: Received 17 August 2016 Received in revised form 20 December 2016 Accepted 21 December 2016 Available online xxxx Keywords: Microplastic Dynamics Flux Fulmarus glacialis Ardenna grisea NE pacific

a b s t r a c t We found microplastic in 89.5% of 143 Northern Fulmars from 2008 to 2013 and 64% of 25 Sooty Shearwaters in 2011–2012 that were found dead or stranded on Oregon and Washington beaches. Average plastic loads were 19.5 pieces and 0.461 g for fulmars and 13.3 pieces and 0.335 g for shearwaters. Pre-manufactured plastic pellets accounted for 8.5% of fulmar and 33% of shearwater plastic pieces. In both species, plastic in proventriculi averaged 2–3 mm larger in greatest dimension than in ventriculi. Intestinal plastic in fulmars averaged 1 mm less in greatest dimension than ventricular plastic. There was no significant reduction in pieces or mass of plastic in 33 fulmars held for a median of seven days in a plastic-free environment. Three fulmars that survived to be released from rehabilitation regurgitated plastic, which provided an alternative outlet for elimination of plastic and requires reassessment of the dynamics of plastic in seabird gastrointestinal tracts. © 2017 Elsevier Ltd. All rights reserved.

1. Introduction Microplastic particles are ubiquitous marine pollutants that are ingested by many seabirds, especially Procellariiformes. Factors that variously correlate with plastic loads include age, decade, location, breeding status, feeding mode, body condition, and species (see reviews Day et al., 1985; Ryan, 1987a, 1987b; Spear et al., 1995; Robards et al., 1997; Moser and Lee, 1992; Avery-Gomm et al., 2012; Bond et al., 2014; Van Franeker and Law, 2015; Trevail et al., 2015, Wilcox et al., 2015). These reviews emphasize the biological significance of plastic loads outlined by Day et al. (1985, p. 347) while recognizing the critical importance of the dynamics of plastic in gastrointestinal (GI) tracts. GI dynamics encompasses the interaction of ingestion and elimination and the resulting load of plastics birds retain. Short retention times likely minimize assumed impacts while making loads useful bioindicators at local scales. In contrast, longer retention times increase assumed impacts while reducing utility as bioindicators at local scales. Despite 30 years of reports of plastic ingestion in seabirds, dynamics are not well known even for a species commonly used as an indicator species, the Northern Fulmar (Fulmarus glacialis) (see Wilcox et al., 2015 for recent review). Initial studies of dynamics dealt primarily with small (4 mm, 20 mg; Day et al., 1985) pre-manufactured plastic resin pellets (nurdles), which were thought to be retained until ground away in the muscular gizzard, or ventriculus. Retention times of 6– ⁎ Corresponding author. E-mail address: [email protected] (G.W. Shugart).

12 months were estimated using rates of wear (Day, 1980 cited in Day et al., 1985; Day et al., 1985; Ryan and Jackson, 1987). Retention was assumed to follow Ryan's (1988) Annual Cycle Hypothesis that proposed that high plastic concentration in non-breeding areas and low concentration in breeding areas were associated with annual cycles of accumulation and elimination, respectively. However, patterns were inconsistent (Spear et al., 1995; Trevail et al., 2015). Recent considerations have suggested a shorter retention time of a few months, and this estimate was shortened further to a loss of 75% of plastic loads per month using mg of plastic/bird found in Cape Petrels (Daption capense) (Van Franeker et al., 2011; Van Franeker and Law, 2015). However, a loss rate calculated based on mg of plastic/particle of plastic (e.g. Ryan and Jackson, 1987) using the same data source predicted that it would take over a year for plastic to disappear (Fig. 1; Tables 1 and 2, Appendix A). Surprisingly, the Cape Petrel estimate, based on small sample sizes, provided the primary baseline estimate for loss rate in a recent overview (Van Franeker and Law, 2015). Although GI dynamics are not well understood, studies have found shifts in composition over time of environmental plastic from nurdles to larger pieces of post-manufactured or user plastic (Van Franeker and Meijboom, 2002; Vlietstra and Parga, 2002; Ryan, 2008). This complicates the interpretation of dynamics because projections in early studies dealt primarily with nurdles and nurdle-sized plastic (Day et al., 1985; Ryan and Jackson, 1987; Van Franeker and Law, 2015 Online Supplement). The shift in composition of plastic load primarily to user plastic (Vlietstra and Parga, 2002; Van Franeker and Meijboom, 2002; Ryan, 2008; Avery-Gomm et al., 2012; Van Franeker and Law, 2015)

http://dx.doi.org/10.1016/j.marpolbul.2016.12.064 0025-326X/© 2017 Elsevier Ltd. All rights reserved.

Please cite this article as: Terepocki, A.K., et al., Size and dynamics of microplastic in gastrointestinal tracts of Northern Fulmars (Fulmarus glacialis) and Sooty Shearwaters (Arden..., Marine Pollution Bulletin (2017), http://dx.doi.org/10.1016/j.marpolbul.2016.12.064

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A.K. Terepocki et al. / Marine Pollution Bulletin xxx (2017) xxx–xxx

Percent of Birds with Plastic

A

B Pieces of Plastic/Bird

60% 50% 40% 30% 20% 10% 0%

0

20

40

60

1.8 1.6 1.4 1.2 1 0.8 0.6 0.4 0.2 0

80

0

20

40

Day

C

D

80

18

30

16

25

Mg/Piece of Plastic

Mg of Plastic/Bird

60

Day

20 15 10 5

14 12 10 8 6 4 2

0

0

0

20

40

60

80

0

Day

100

200

300

Day

Fig. 1. Data from Van Franeker and Bell (1988) referenced in Van Franeker and Law (2015, Online Supplement Table 2) used to suggest a rapid loss of plastic in reference to Northern Fulmar loss rates. Plotted are data from samples from 1 to 10 December 1986 (5 Dec used for projections) (N = 9 birds) and 20 January 1985 (N = 20 birds). Projections were based on linear regression of (A) incidence or percent of birds with plastic, (B) pieces of plastic/bird, (C) mg/bird, and (D) mg/piece of plastic. Van Franeker and Law (2015, Online Supplement Table 2) estimated of loss of 75% of plastic in a month in plastic-free Antarctic waters with projected total loss between 51 and 72 days. However, wear rates based on mg/piece (e.g., Ryan and Jackson, 1987) suggest a much longer period of 269 days; x-axis on D extended to show this point.

involved larger pieces that presumably would take longer to pass through the GI tract, or be simply too large to pass (Day et al., 1985; Moser and Lee, 1992; Ryan, 1990). This change in the characteristics of plastic found in procellariiform seabirds necessitates reassessment of the dynamics of plastic in GI tracts, uses of plastic load as bioindicators, and biological significance of ingested plastic. In this study, we quantified size and distribution of plastic in GI tracts and reassessed dynamics of plastic in two seabird species while providing additional background data on plastic loads for individuals of both species found dead or stranded on Oregon and Washington beaches.

2. Material and methods

Oregon (southern most point 45° 21′ 0.72″N, 123° 58′ 22.79″W) and Pacific and Grays Harbor counties, Washington (northern most point 47° 1′ 49.78″N, 123° 58′ 43.72″W) during 2008–2013. Birds were picked up while conducting searches for beached birds by Wildlife Center of the North Coast personnel and by Slater Museum of Natural History staff. Northern Fulmars are North Pacific breeders that occupy colonies from late April-early May and migrate south in mid-October along the East Pacific coast (Mallory, 2008; Avery-Gomm et al., 2012; Donnelly-Greenan et al., 2014). Sooty Shearwaters breed in the Southern Hemisphere from late November-early December and April-early May (Warham, 1990) and then rapidly migrate to the North Pacific, averaging 910 km/day with reduced localized movement on wintering grounds of 220 km/day (Ogi, 1990; Shaffer et al., 2006; Mallory et al., 2012).

2.1. Study area and focal species Northern Fulmar and Sooty Shearwater (Ardenna grisea) specimens were found on Pacific Ocean beaches of Tillamook and Clatsop counties,

Table 1 Incidence of plastic in Northern Fulmars from Oregon and Washington beaches. There was no difference for birds with and without plastic across time intervals (Chi-square4 = 7.2, p = 0.125). Time interval

Plastic

No plastic

% with plastic

2008–2009 2009–2010 2010–2011 2011–2012 2012–2013 Total

11 17 70 13 17 128

1 5 5 2 2 15

91.7 77.3 93.3 86.7 89.5 89.5

Table 2 Time intervals (July–April) for pieces and mass of plastic in Northern Fulmars from Oregon and Washington coasts. GLM followed by pair-wise comparisons (Tukey) with matching superscripts indicating significantly different pair-wise comparison based on 95% confidence intervals.

Total pieces

Total mg

Time interval

N

Mean

SE

Range

Median

2008–2009 2009–20102 2010–20111 2011–2012 2012–20131,2 2008–20091 2009–20101,2,3 2010–20112 2011–2012 2012–20133

12 22 75 15 19 12 22 75 15 19

15 16 18 9 41 325 369 412 159 1090

4 7 2 3 8 132 252 65 49 364

0–53 0–143 0–118 0–44 0–117 0–1651 0–5567 0–2608 0–570 0–6982

11 4 11 5 33 149 30 206 62 515

Please cite this article as: Terepocki, A.K., et al., Size and dynamics of microplastic in gastrointestinal tracts of Northern Fulmars (Fulmarus glacialis) and Sooty Shearwaters (Arden..., Marine Pollution Bulletin (2017), http://dx.doi.org/10.1016/j.marpolbul.2016.12.064

A.K. Terepocki et al. / Marine Pollution Bulletin xxx (2017) xxx–xxx

2.2. Data collection In routine year-round searches, fulmars were found dead or stranded on beaches from July through April. Therefore, fulmar occurrence data were categorized as five successive time intervals spanning July to April to allow comparison of plastic load over time. Sooty Shearwaters appeared from April through December. Dead birds were frozen for later dissection. Fulmars that were alive were tracked during rehabilitation with the expectation that the length of time in a plastic-free environment of the recovery facility could be related to a reduction in plastic. Upon death these were frozen for later dissection. For fulmars, 33 were admitted to the rehab facility. Median time to death was seven days. For shearwaters, 12 were alive initially but died shortly thereafter (median two days). Determination of age and sex, and quantification of plastic followed standardized protocols (Winker, 2000; Van Franeker, 2004). Following established guidelines (Van Franeker and Meijboom, 2002; Van Franeker, 2004) age was categorized as 12 months of age or less (hereafter juvenile), N12 months old, but not adult (assumed 1 to 5 years), or adult, based on Bursa of Fabricius and gonad condition (see Van Franeker, 2004). For most analyses, the latter two categories were pooled because there were too few individuals in different age categories for separate comparisons. The proventriculus and ventriculus of each bird were removed, opened, and contents were rinsed in a 1 mm mesh strainer. Samples were dried and items were sorted using Van Franeker and Meijboom's (2002) categories for plastic and other items (Appendix A). Plastic objects were identified based on size, shape, surface, or color. If there was uncertainty about the identities of small objects, they were examined using a Leica™ zoom binocular dissecting scope and size, shape, surface, or color were compared to known plastic objects. Plastic was weighed on a Metler™ analytical balance to the nearest 0.1 mg. The greatest dimension of plastic pieces was measured with digital calipers to the nearest 0.1 mm for samples from 2008 to 2011 for plastic in fulmars and all shearwaters. In fulmar specimens from 2012 to 2013, the intestine was also opened and contents were rinsed through a 1 mm strainer in search of plastic. Specimens and plastic samples were archived at the Slater Museum of Natural History, University of Puget Sound. Some fulmar samples (31/34) from 2008 to 2009 and 2009–2010 were pooled and summary values were used in Avery-Gomm et al. (2012) to assess regional differences. These samples were used in this paper to address different questions related to differences between time periods and for measurement of plastic particles. 2.3. Statistical analysis Data were analyzed using Minitab 17.3.1 (2016). General Linear Models (GLM) were used to examine variation in the total number of plastic pieces and total mass (mg) in fulmars relative to time period, sex, age, and mode of death. Data used for GLM were left-skewed with right-tailed outliers which required ln(Total_Pieces + 1) and ln(Total_mg + 0.001) transformation (Van Franeker and Meijboom, 2002). Residual plots were examined for normality. Nonparametric tests were used where distributions did not meet parametric criteria, and medians were included in summaries in addition to mean ± SE for comparison to other studies. The two-sample signed rank test referred to as Wilcoxon-Mann-Whitney or Mann-Whitney (Zar, 1999) test in Minitab reports the statistic of Wilcoxon W. Probabilities were two-tailed. 3. Results A total of 143 Northern Fulmars were found during five July–April intervals spanning 2008–2013 (Table 1). Seventy-five percent (107/ 143) were found from October to January with the earliest date of 10 July and latest date 2 April. The overall incidence of plastic was 89.5%

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(128/143), with totals of 66.013 g and 2781 pieces recorded. Mean values based on all birds were 19.5 ± 2.1 pieces of plastic and 0.461 ± 0.074 g per individual. Of the plastic categories in Van Franeker and Meijboom (2002), “industrial plastic pellets” or nurdles and the user category of “fragments of more or less hard plastic items” accounted for 97.5% of pieces. The user plastic categories of “expanded foam” consisting of clumps and single beads of expanded polystyrene (beadboard) accounted for 2.4% of items in nine birds, and the user category of “threadlike” accounted for 1% of pieces in 10 birds. Items from other categories accounted for b 1% of items (Appendix A). There was no difference in the percentage of birds containing plastic between time intervals (Table 1). To discover if factors such as time-period, sex, age, or mode of death (dead vs alive then died in rehab) contributed to differences, we transformed data and used GLM. For total pieces, only time interval was significant (F4,126 = 3.11, p = 0.018) in two pair-wise comparisons (Table 2). For total mass, time interval (Table 2, F4,126 = 3.30, p = 0.013) for three paired comparisons and age (Table 3, F1,126 = 4.37, p = 0.039) contributed significantly to the model. The interaction of age and time period was not significant. For models, r2adj was 13.2% for total pieces and 8.9% for total mass indicating a low predictability of the models using age, sex and mode of death as factors. Thirty-three fulmars died over periods of time ranging from less than one day (overnight) to 56 days (median = seven days) after admission to the rehabilitation center. Linear regression of pieces and mg of plastic found in birds after death showed declines reaching zero at 46 and 41 days, respectively. However regressions were not significant (Fig. 2). Three fulmars that survived, and therefore were not included in the sample, regurgitated 6.669/22, 9.471/38, and 10.591/ 74 g/pieces of plastic during the initial stages of recovery while held in freshwater isolation tanks. Plastic was user plastic in Van Franeker and Meijboom's (2002) category of “fragments of more or less hard plastic items” except for two plastic labels, two pieces of foam, and two nurdles (Appendix A). Presumably, regurgitations were from the proventriculus (see Furness, 1985a, 1985b; Ryan, 1990; Moser and Lee, 1992; Van Franeker et al., 2011; Hutton et al., 2008; Van Franeker and Law, 2015). Of the fulmars that contained plastic, 98% (126/128) had plastic in the ventriculus, 48% (61/128) in the proventriculus, and 46% (59/128) in both stomachs. Two of 61 with proventricular plastic had no plastic in the ventriculus. Of the 59 birds with plastic in both stomachs, in paired comparisons, the average mass of pieces (mg/pieces) in the proventriculus (65.6 ± 14.9 mg/piece, range 1.2–576 mg/piece) was significantly greater than in the ventriculus (25.3 ± 4.0 mg/piece, range 0.2– 226 mg/piece) (paired-t58 = 2.66, p = 0.01). Again using paired comparisons, there was no significant difference in plastic mass between the two stomachs (proventriculus 519 ± 137 mg, ventriculus 418 ± 44 mg; paired-t58 = 0.80, p = 0.427). Therefore, the smaller average mass of ventricular plastic pieces reflected a greater number of smaller pieces (paired-t58 = 3.71, p b 0.0009) in the ventriculus (23.41 ± 2.93 pieces) than the proventriculus (10.51 ± 2.32 pieces). We found that 31% (5/16) of fulmar intestines contained plastic. Four birds each had one piece of plastic in their intestines; with a fifth bird containing two pieces. For these six pieces of plastic, mean greatest dimension was 4.8 ± 0.3 mm (N = 6, range 3.5–5.4 mm) and mass was 7.0 ± 1.4 mg (N = 6, 4.5–13.7 mg). Table 3 Age comparisons for pieces and mass of plastic in Northern Fulmars from Oregon and Washington coasts. GLM followed by pair-wise comparisons (Tukey) with matching superscripts indicating significantly different pair-wise comparison based on 95% confidence intervals. Two birds lacking age data were excluded.

Total pieces juvenile Total pieces non-juvenile Total mg juvenile1 Total mg non-juvenile1

N

Mean

SE

Range

Median

105 36 105 36

23 10 549 199

3 2 97 61

0–143 0–53 0–6982 0–1651

11 6 213 50

Please cite this article as: Terepocki, A.K., et al., Size and dynamics of microplastic in gastrointestinal tracts of Northern Fulmars (Fulmarus glacialis) and Sooty Shearwaters (Arden..., Marine Pollution Bulletin (2017), http://dx.doi.org/10.1016/j.marpolbul.2016.12.064

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A.K. Terepocki et al. / Marine Pollution Bulletin xxx (2017) xxx–xxx 120

Pieces of Plastic

100 80 60 40 20 0 0

10

20

30

40

50

60

Days in a Plastic Free Environment Until Death 1,800 1,600 1,400

Mg of Plastic

1,200 1,000 800 600 400 200 0 0

10

20

30

40

50

60

Days in a Plastic Free Environment Until Death Fig. 2. Regression of total pieces and total mass of plastic as a function of days spent in a plastic-free environment in a rehabilitation facility by Northern Fulmars. Regressions were not significant for pieces (y = −0.443x + 21.019, r2adj = 0.019, F1,29 = 1.580, p = 0.218) or mass (y = −9.468x + 384.560, r2adj = 0.052, F1,29 = 2.660, p = 0.114).

Nurdles accounted for 8.5% (N = 239) of the total pieces and 7% (4.5 g) of total mass of fulmar plastic. Nurdles were found more frequently in ventriculi (43%, 55/128) than in proventriculi (10%, 13/128) (Chi-square1, p b 0.0001). Comparison of nurdles in 13 fulmars that had nurdles in both stomachs indicated there were no significant differences in average mass (paired-t12 = 1.59, p = 0.136; ventriculus 24.3 ± 1.7 mg, proventriculus 20.9 ± 1.4 mg) or number of pieces(paired-t12 = 1.73, p = 0.121; ventriculus 5.7 ± 1.9 mg, proventriculus 2.4 ± 0.5 mg). A total of 25 Sooty Shearwaters were collected; 22 from June– September 2011 or 2012, one from April 2011, and two from May 2012. The incidence of plastic at 64% (16/25) was significantly lower than in fulmars (Chi-square1 = 9.099, p = 0.003). Totals of 330 pieces and 8.376 g of plastic were recovered with means per bird of 13.3 ± 3.5 pieces and 335 ± 86.7 mg (Table 4). Van Franeker and Meijboom's (2002) categories of “industrial plastic pellets” or nurdles and the user category of “fragments of more or less hard plastic items” accounted for 99.5% of pieces (Appendix A). Within the shearwaters, there was a difference in the incidence of plastic related to age with 85% (11/13) of juveniles containing plastic but only 41.7% (5/12) of non-juveniles (Chi-square1 = 6.838, p = 0.009), including four breeding age adults and one subadult. Of the nine birds that had no plastic, there were five adults, two subadults, and two juveniles supporting a conclusion that non-juveniles had little Table 4 Plastic loads in Sooty Shearwaters from Oregon and Washington beaches from 2010 to 2012.

All shearwaters Total_pieces Total_mass mg Only shearwaters with plastic Total_pieces Total_mass mg

N

Mean

SE

Range

Median

25 25

13.3 335

3.55 86.7

0–75 0–1555

11 257

16 16

20.8 523

4.6 111

1–75 10–1555

16 417

plastic. Similar to fulmars, plastic was more frequently found in the ventriculus. Of the 16 shearwaters that contained plastic, all contained ventricular plastic, but only seven of 16 (44%) also had plastic in the proventriculus. The seven shearwaters with plastic in both stomachs were juveniles. Nurdles accounted for 34% (88/330) of pieces and 33% (2.277 g/8376 g) of mass of plastic in the 16 shearwaters that contained plastic. Twelve had nurdles in the ventriculus (79 nurdles) while only two also had nurdles in the proventriculus (9 nurdles). The distribution of plastic in stomachs was presumably affected by size and the amount of plastic. Movement was assumed to be oneway from proventriculus to ventriculus because of a sphincter that prevented the reverse movement (Furness, 1985a, 1985b; Van Franeker and Meijboom, 2002). The sphincter limited the size of particles that could enter the ventriculus and average greatest dimension provided an estimate of this size. We found that pieces in the proventriculus had larger mean greatest dimension than those in the ventriculus for both species (fulmars: proventriculus N = 231, 8.32 ± 0.35 mm, range 1.5–28.9 mm; ventriculus N = 1095, 5.65 ± 0.07 mm, range 0.9– 16.8 mm) (two-sample t1235, unequal variances, p b 0.00001); shearwaters: proventriculus, N = 60, 7.68 ± 0.63 mm, range 3.5–25.5 mm; ventriculus, N = 270, 5.38 ± 0.17 mm, range 0.9–22 mm) (two-sample t328, unequal variances, p = 0.0007). The distribution of plastic between the two stomachs could also be affected by the amount in the ventriculus, which if full, could have resulted in a backup in the proventriculus (Van Franeker and Meijboom, 2002). We tested this assumption with a comparison of mass and pieces of plastic in the ventriculus of fulmars and shearwaters versus those without plastic in the proventriculus. We found that those with proventricular plastic had significantly more plastic in their ventriculus than those with no plastic in the proventriculus (Fig. 3) (fulmars, mass W59,67 = 4637.5, p b 0.0001; pieces W59,67 = 4496.0, p = 0.0003; shearwaters, mass W9,7 = 86.0, p = 0.006; pieces, W9,7, = 81.5, p = 0.023). 4. Discussion 4.1. Plastic in Northern Fulmars and Sooty Shearwaters from Oregon and Washington Northern Fulmars contained 19.5 ± 2.1 pieces and 0.461 ± 0.074 g of plastic and an incidence of 89.5% over five successive survey periods (Table 1). This is higher than a previous Oregon-Washington estimate of 0.326 g, which used only a portion of the data from the first two time periods (Avery-Gomm et al., 2012). The pooled totals were at the higher end of loads for fulmars found in other studies (reviewed in Bond et al., 2014, Table 2; Donnelly-Greenan et al., 2014). The heaviest mean load of 2.12 g and 17 pieces was found in 38 fulmars from the Northwestern Atlantic from 1978 to 1985 (Moser and Lee, 1992). It is worth noting that Moser and Lee's sample included presumably healthy birds that were shot rather than birds found on beaches that typically are in poor condition (Avery-Gomm et al., 2012; Donnelly-Greenan et al., 2014). The second highest load of 1.09 g and 25.4 pieces was found in 176 fulmars found dead on Nova Scotian beaches from 2000 to 2011 (Bond et al., 2014). Our finding that 66% of Sooty Shearwater from this region of the Northeastern Pacific Ocean contained plastic was expected based on previous reported incidences of 0–75% or 0–100% including encounters of three single birds (reviewed in Bond et al., 2014, Table 3). Omitted in the review was a large bycatch sample with an 85% incidence of plastic in 543 birds from the North Central Pacific in 1990–1991 (Robards et al., 1997), and samples from the equatorial Pacific showing incidence from 0 to 100% depending on age and time of year (Spear et al., 1995). Accounting for differences in the incidence, the number of total pieces, or total mass, typically frames the discussion in many plastic ingestion studies (Avery-Gomm et al., 2012; Van Franeker and Law, 2015). For the two species we considered, differences in incidence of

Please cite this article as: Terepocki, A.K., et al., Size and dynamics of microplastic in gastrointestinal tracts of Northern Fulmars (Fulmarus glacialis) and Sooty Shearwaters (Arden..., Marine Pollution Bulletin (2017), http://dx.doi.org/10.1016/j.marpolbul.2016.12.064

A.K. Terepocki et al. / Marine Pollution Bulletin xxx (2017) xxx–xxx

B. Northern Fulmar

A. Northern Fulmar 1000

40

900

35

Pieces f Plastic

MG of Plastic

800 700 600 500 400 300

30 25 20 15 10

200

5

100 0

0 with pv plastic

without pv plastic

Total

with pv plastic

1000

40

900

35

Pieces of Plastic

800 700 600 500 400 300 200

without pv plastic

Total

D. Sooty Shearwater

C. Sooty Sheawater

MG of Plastic

5

30 25 20 15 10 5

100 0

0 with pv plastic

without pv plastic

Total

with pv plastic

without pv plastic

Total

Fig. 3. Plastic in the ventriculus of Northern Fulmars and Sooty Shearwaters from Oregon and Washington beaches summarized by those with or without plastic in the proventriculus (pv) in first two columns of each figure. Totals (proventriculus + ventriculus) are in third column in each figure for birds with plastic in their proventriculus. For birds without proventricular plastic, the totals are the same for birds “without pv plastic”. Consult Table 5 for sample size, SE and ranges.

plastic could be related to migration routes, as fulmars migrate from the north while Sooty Shearwaters are trans-equatorial migrants from the Southern Hemisphere. Variation in fulmars between years and lower incidence of plastic ingestion by shearwaters may have reflected different residence times in areas that contained the main concentration of plastic, recently mapped as 500 km west of the California, Oregon and Washington coasts and extending in a broad latitudinal band into the mid-Pacific (see Law et al., 2014). Alternatively, differences may be related to different foraging strategies, as Northern Fulmars forage primarily at the surface while Sooty Shearwaters use pursuit diving (Day et al., 1985; Ryan, 1988; Moser and Lee, 1992). Data from both species indicated that juveniles had more plastic than subadult or adults. Inexperience of juveniles or spatiotemporal differences in migration typically have been cited as causes for fulmars and several other procellariids (Day et al., 1985; Ryan, 1988, 1990; Ogi, 1990; Robards et al., 1997; Vlietstra and Parga, 2002; Carey, 2011). We found only one other sample of aged Sooty Shearwaters (Table 8 in Spear et al., 1995), and in contrast to our findings and the general trend, these juvenile Sooty Shearwaters contained no plastic. This might be because they were collected south of the region of plastic concentration in the north middle latitudes (Law et al., 2014). Post-breeding adults moving north from breeding areas had only a 33% incidence of plastic (Spear et al., 1995), which would be most similar in timing to the Sooty Shearwaters we encountered. In contrast, all pre-breeding adults contained plastic as they migrated back from wintering areas in the central to north Pacific region after wintering or passing through higher concentration of plastic (Spear et al., 1995; Robards et al., 1997).

4.2. Dynamics, distribution and size of plastic in Procellariiformes GI tracts Dynamics of movement of plastic and size of plastic particles are related because there are physical limits to the size of plastic that can pass through gastrointestinal tracts. Movement is assumed to be from thinwalled proventriculus to thick-walled ventriculus, then into intestines and out of birds. Plastic found in ventriculi are assumed to be too large to pass into the intestine (Ryan, 2008; Mallory, 2008; Kühn, 2012; Van Franeker and Law, 2015). Although regurgitation of plastic has been suggested (Day et al., 1985; Ryan, 1988), only a few reports for Procellariiformes have been published, including Laysan Albatross (Phoebastria immutabilis) and Flesh-footed Shearwater (Ardenna carneipes) at fledging (Hutton et al., 2008; Young et al., 2009). Our confirmation that adult fulmars regurgitated relatively large volumes of plastic suggests an alternative outlet for plastic in addition to the passage through the gastrointestinal tract. In the following, we examined the potential effects of regurgitation on the size and distribution of plastic throughout the gastrointestinal tract. We first consider the ventriculus where plastic was most frequently found. We found that the maximum dimension of a piece of hard plastic in the ventriculus averaged 17 mm for Northern Fulmars and 22 mm for Sooty Shearwaters. The greatest ventricular masses of plastic recorded for fulmars include 0.916 g (Furness, 1985a) and 1.265 g (this study), but larger loads are possible with an exceptionally high mean of 1.83 g based on 38 fulmars that contained plastic (Moser and Lee, 1992). Shearwaters' ventricular capacity appeared to be similar (G. Shugart, pers. obs.). Moser and Lee (1992) did not provide a maximum but a

Please cite this article as: Terepocki, A.K., et al., Size and dynamics of microplastic in gastrointestinal tracts of Northern Fulmars (Fulmarus glacialis) and Sooty Shearwaters (Arden..., Marine Pollution Bulletin (2017), http://dx.doi.org/10.1016/j.marpolbul.2016.12.064

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A.K. Terepocki et al. / Marine Pollution Bulletin xxx (2017) xxx–xxx

comparably computed mean from our study (i.e., using 126 fulmars with plastic in the ventriculus) was 0.28 ± 0.03 g or about six times less than Moser and Lee (1992). Noting that our mean was four times less than our maximum load, Moser and Lee's (1992) maximum would have been higher. There are no estimates of the maximum load that a fulmar ventriculus could hold. However, Furness (1985a, Table 2) indicated that the 0.916 g of plastic filled 59% of relaxed and 15% distended ventricular volume. Using ratios, we calculated the maximum load in grams for relaxed and distended ventriculi as 1.6 g and 6.1 g, respectively (see Appendix A). Usually estimates for fulmars have combined plastic from the two stomachs, but the total amount of plastic usually was b0.5 g (Bond et al., 2014; Avery-Gomm et al., 2012; Donnelly-Greenan et al., 2014) which was well below capacity of 1.6 g for relaxed ventriculi. Therefore, both stomachs combined in the studies cited above had less plastic than relaxed ventriculi could hold except for Moser and Lee (1992). The six pieces of plastic found in fulmar intestines in our study averaged 4.8 mm (greatest dimension) and 7.1 mg, which provided estimates of the size of plastic that could pass into the intestine. We found plastic in only 31% (5/16) of intestines as opposed to 96% of ventriculi. There are no data for rates of movement through procellariids intestines, but in Cedar Waxwings (Bombycilla cedrorum), 4 mm diameter plastic beads similar in size to nurdles, were used to assess passage of simulated seeds through the intestine (Levey and Duke, 1992). Rates of movement were 0.14 cm/s indicating rapid passage in a bird about 1–2% the body mass of fulmars or shearwaters. Consequently, it is conceivable that objects the size of nurdles could pass rapidly and escape detection, which might account for our finding that only 31% of intestines contained plastic (also see Van Franeker and Law, 2015, Online Supplement). Intestinal plastic in our study was larger than a previous estimate of “approximately 2 mm” (Bravo Rebolledo, 2011 cited in Van Franeker and Law, 2015 Online Supplement). The pieces we found in intestines were also larger than the smallest pieces we found in ventriculi (range 0.9–16.6 mm). It was unclear how smaller pieces were retained in the ventriculus rather than passing into the intestine and out of the birds. Perhaps passage of food through the GI tract influenced retention and elimination from the ventriculus whereas starvation halted movement (Ogi, 1990; Moser and Lee, 1992). Additional measurements are needed for fulmars, and for Sooty Shearwater intestines, which were not examined, and other procellariids. Relative to the ventriculus, proventricular plastic was larger in average greatest dimension in both fulmars and shearwaters. We identified a previously undocumented relationship between the presence of proventricular plastic and the mass and number of plastic pieces in the ventriculus; for both species, individuals that had plastic in the proventriculus, had 2–4 times greater mass and more pieces of plastic in the ventriculus than those that had no plastic in the proventriculus (see Table 5). However, as noted previously, the ventricular mass was only about one-third the relaxed volume for fulmars (Furness, 1985a), which we assumed was similar to shearwaters. Thus, although it was possible that plastic in the proventriculus resulted from backup in the ventriculus (Van Franeker and Meijboom, 2002), this seemed unlikely because total mass of plastic was less than a relaxed ventriculus holds (Furness, 1985a). Although the relationship between proventricular and ventricular plastic could have been a finding unique to our study, comparative data are lacking because of a tendency to pool contents from stomachs in summaries (reviewed in Bond et al., 2014). In contrast to the ventricular loads in our sample, which presumably were constrained by the mass, volume, and size of particles, the proventriculus was distensible and, thus, capable of holding could hold greater sizes, masses, and volume (Van Franeker and Meijboom, 2002; Van Franeker, 2004). Previous studies have noted that in contrast to the ventriculus, the proventriculus was usually empty of food, plastic, natural non-food items such as pumice or pebbles, and other anthropogenic material (Furness, 1985a, 1985b; Spear et al., 1995; Moser and Lee,

Table 5 Plastic in the ventriculus of Northern Fulmars and Sooty Shearwaters from Oregon and Washington beaches summarized by those with or without plastic in the proventriculus (pv). For birds without proventricular plastic, the totals are the same as birds “without pv plastic”.

Fulmar, mass (mg) in ventriculus with pv plastic without pv plastic Fulmar, pieces, in ventriculus with pv plastic without pv plastic Total (ventriculus + proventriculus) with pv plastic, mass (mg) with pv plastic, pieces Shearwater, mass (mg) in ventriculus with pv plastic without pv plastic Shearwater, pieces in ventriculus with pv plastic without pv plastic Total (ventriculus + proventriculus) with pv plastic, mass (mg) with pv plastic, pieces

N

Mean

SE

Range

Median

59 67

418 165

44.2 17.8

5.5–1265 2.9–653

334 116

59 67

23.4 11.6

2.9 1.6

1–104 1–88

17 8

59 59

931 33.9

159 4.0

10–6982 3–143

568 29

7 9

594 262

57.2 65.8

340–767 10–516

565 311

7 9

25.4 10.6

4.2 2.2

10–42 1–17

25 14

7 7

860 34

170 7.8

362–1555 11–75

626 26

1992; Vlietstra and Parga, 2002). For example, in our study, only 48% of fulmars had plastic in the proventriculus while 96% had plastic the ventriculus. Similarly, 28% of shearwaters had proventricular plastic while 66% had plastic in the ventriculus. A lower incidence proventriculus plastic also was typically found in healthy procellariids that were shot or obtained from fisheries bycatch (Furness, 1985a, 1985b; Spear et al., 1995; Moser and Lee, 1992; Vlietstra and Parga, 2002), therefore, it doesn't appear that material found only in the ventriculus was an artifact of beached or starved birds. We interpret the lower incidence of plastic in the proventriculus, but a greater average size of particles when present in both stomachs, as follows. A possible explanation for smaller size of plastic in the ventriculus was that ventricular plastic was subjected to grinding and fragmentation. Our analysis of stomach contents of individual fulmars held in a plastic-free environment showed no significant trends for changes in mass and pieces. However, time period was relatively short (median seven days) and the initial size, mass, and numbers of plastic pieces were unknown, which introduced unquantified variability into these correlations. Variability in size was controlled in our comparison of nurdle size in pair-wise comparison of fulmar stomachs. Assuming a standard starting size, there was no difference in average nurdle size between proventriculus and ventriculus in fulmars which indicates that there was no significant wear for time in the ventriculus. Regurgitation similar to what we documented, either adventitiously during the non-breeding period or during provisioning of young complicates estimations of the rate of plastic loss. The loss of relatively large user pieces (Fig. 3 in Mallory, 2008; Fig. 4, this paper) through regurgitation would result in a rapid loss of plastic mass as Van Franeker and Law (2015) suggested but a residual amount of plastic in the ventriculus might persist for a longer period (e.g., Trevail et al., 2015) as Day et al. (1985) originally suggested. Our finding that birds with plastic in the proventriculus had correspondingly more in ventriculus was a relationship not identified in previous studies and may simply be an oversight since most studies pool proventricular and ventricular samples and present data as total plastic. The birds with proventricular plastic with relatively large ventricular loads (Table 5) would be most likely to suffer blockage and debilitation or death as relatively large user pieces were ingested, regurgitated, or passed into the ventriculus. The birds in our sample that were in this category may have suffered this fate. Dissection of proventriculi in the future should be done with this possibility in mind. In contrast, birds without proventricular plastic had 0.16–0.26 g of plastic and relatively few pieces (Table 5), which may have negligible impacts (Herzke et

Please cite this article as: Terepocki, A.K., et al., Size and dynamics of microplastic in gastrointestinal tracts of Northern Fulmars (Fulmarus glacialis) and Sooty Shearwaters (Arden..., Marine Pollution Bulletin (2017), http://dx.doi.org/10.1016/j.marpolbul.2016.12.064

A.K. Terepocki et al. / Marine Pollution Bulletin xxx (2017) xxx–xxx

7

Fig. 4. Large pieces of debris, primarily in Van Franeker and Meijboom (2002) category of user “fragments of more or less hard plastic items”, regurgitated by a live Northern Fulmar to left of scale and plastic retrieved from the proventriculus of a dead fulmar (GWS 3931) to right of scale. Many plastic pieces were so large that it was unlikely they could have passed into the ventriculus. See Appendix A for frequency of occurrence of items. In addition to hard plastic, at the bottom right is a piece of wood, top right is plastic film, top left is compressed foam.

al., 2016). These birds may have cleared much of the plastic from their system, but it also was possible that they ingested fewer, smaller pieces of plastic. This last suggestion highlights the need for a greater understanding of the GI dynamics of intake, loss, and retention, in order to clarify the biological significance of the plastic ingestion. Assuming GI dynamics were similar across studies, the utility of plastic loads as bioindicators would not be compromised. However, if larger plastic pieces were routinely regurgitated, plastic that was retained in stomachs might not provide a complete sample of what was ingested. We recommend additional research focused on metrics and distribution of plastic in both stomachs (i.e. proventriculus and ventriculus) and intestines to provide additional understanding of the dynamics and the flux of plastic in assessing the biological significance in Procellariiformes. Acknowledgements We thank the staff and volunteers of the Wildlife Center of the North Coast, Astoria, Oregon for obtaining specimens for the study. Sharnelle Fee, former Director, was instrumental in obtaining specimens and recording data on intake and time of death that was crucial for the time in captivity data analysis. The center operates under required federal and state rehabilitation permits. We also thank Dr. Shep Thorp, VMD, who provided valuable insights and assistance in dissection, necropsy and extraction of plastic and reviews by Peter H. Wimberger and an anonymous reviewer. Financial support to A. K. Terepocki came from a University of Puget Sound Summer Research Grant. Work-study grants to L. U. Kleine and H. P. Floren, who quantified nurdle data, partially funded their contributions. This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.

Appendix A. Supplementary data Supplementary data to this article can be found online at http://dx. doi.org/10.1016/j.marpolbul.2016.12.064.

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Please cite this article as: Terepocki, A.K., et al., Size and dynamics of microplastic in gastrointestinal tracts of Northern Fulmars (Fulmarus glacialis) and Sooty Shearwaters (Arden..., Marine Pollution Bulletin (2017), http://dx.doi.org/10.1016/j.marpolbul.2016.12.064