Article

pubs.acs.org/est

Plastic in North Sea Fish

Edwin M. Foekema,*,† Corine De Gruijter,†,§ Mekuria T. Mergia,†,‡ Jan Andries van Franeker,∥
AlberTinka J. Murk,‡ and Albert A. Koelmans†,§
†
IMARES Wageningen UR, Department Experimental Ecology, P.O. Box 57, 1780 AB Den Helder, The Netherlands
‡
Wageningen University, Division of Toxicology, Tuinlaan 5, 6703 HE Wageningen, The Netherlands
§
Wageningen University, Aquatic Ecology and Water Quality Management Group, Department of Environmental Sciences, P.O. Box
47, 6700 AA Wageningen, The Netherlands
∥
IMARES Wageningen UR, Department Ecosystems, P.O. Box 167, 1790 AD Den Burg (Texel), The Netherlands
*
S Supporting Information

ABSTRACT: To quantify the occurrence of ingested plastic in fish species caught

at different geographical positions in the North Sea, and to test whether the fish
condition is affected by ingestion of plastics, 1203 individual fish of seven common
North Sea species were investigated: herring, gray gurnard, whiting, horse mackerel,
haddock, atlantic mackerel, and cod. Plastic particles were found in 2.6% of the
examined fish and in five of the seven species. No plastics were found in gray
gurnard and mackerel. In most cases, only one particle was found per fish, ranging
in size from 0.04 to 4.8 mm. Only particles larger than 0.2 mm, being the diameter
of the sieve used, were considered for the data analyses, resulting in a median
particle size of 0.8 mm. The frequency of fish with plastic was significantly higher
(5.4%) in the southern North Sea, than in the northern North Sea above 55°N
(1.2%). The highest frequency (>33%) was found in cod from the English
Channel. In addition, small fibers were initially detected in most of the samples, but
their abundance sharply decreased when working under special clean air conditions. Therefore, these fibers were considered to be
artifacts related to air born contamination and were excluded from the analyses. No relationship was found between the
condition factor (size−weight relationship) of the fish and the presence of ingested plastic particles.

■ INTRODUCTION
The amount of marine litter is ever increasing, and consists up
to 60 to 80% out of plastics.1 Accumulation of plastic is
therefore recognized as one of today’s major marine water
quality problems,2 and it is assumed that the amount disposed
will increase due to land-based sources as well as to maritime
activities.3 As most plastic debris is buoyant,1,4 it can be
transported by currents and winds, resulting in a widespread
occurrence across the oceans.5,6 The distribution is very patchy,
as it is affected by local wind and current conditions, coastal
geography, and by the way plastic enters the system.3
Plastics are very persistent 5 but are known to degrade into
smaller pieces.7,8 Degradation in water is particularly slow due
to reduced UV exposure and lower temperatures in the water
compared to land.3,9 Therefore, especially low density plastic
types that float can be broken down by UV−B radiation and
become brittle, and break down into microplastics (defined as
<5 mm1,10 and probably even smaller (nano) particles.11,12
Small fragments (<10 mm) are the most common size fractions
in the ocean gyres.13,14 The actual lifetime of plastic fragments
in the marine environment is unknown; estimates range from
years to centuries, dependent on the polymer’s physical and
chemical properties.1,15 Over the past 40 years, microplastics in
the North Pacific increased by 2 orders of magnitude.16
Large objects of plastic can pose a threat to marine organisms
by entanglement, whereas smaller items are available for
ingestion by many marine organisms including fish. The
occurrence of plastic debris in fish was noticed as early as 1972
by Carpenter et al.17 More recently, plastic particles were
encountered in different species.18−21 It is suggested that fish
ingest mainly those plastic fragments that have similar color and
shape as their food particles17,18 as is also the case with sea
turtles for which plastic bags resemble jelly fish.1 Because of the
wide variety of colors, sizes, and shapes of plastic fragments,
they will probably mimic a wide range of natural food sources.1
Several studies described the presence of ingested plastics in
fish (refs 17−21, and 22−24 but only one25 studied plastic in
North Sea fish. The North Sea is among the seas most
intensively used for fishing and shipping, so plastic waste is to
be expected. Monitoring studies with Northern Fulmars
revealed ingested plastics in 95% of these birds following a
clear spatial pattern. Northern Fulmars in the Channel area had
the highest plastic burden, and this gradually decreased in
northward direction.26 For fish, a relationship between the
Received: February 28, 2013
Revised: June 16, 2013
Accepted: June 18, 2013
Published: June 18, 2013

© 2013 American Chemical Society 8818 dx.doi.org/10.1021/es400931b | Environ. Sci. Technol. 2013, 47, 8818−8824
Environmental Science & Technology Article

Table 1. Sampling Dates and Positions, Sample Size, Average Weight and Length, And the Numbers and Percentage of
Individual Herring with Ingested Plastic
catch-date position sample size avg W (g) stdev W(g) avg L(cm) stdev L (cm) ind with plastic % ind with plastics
herring
15-feb-11 51.2N1.46E 42 132 24 27 1.6 1 2
15-feb-11 51.44N1.53E 18 142 35 28 2.0 0 <6
31-jan-11 52.23N2.50E 12 12 4 13 1.3 0 0
31-jan-11 52.23N3.16E 44 17 5 14 1.1 3 7
10-aug-10 56.16N0.33E 25 140 35 25 1.8 0 <4
13-jul-10 56.54N1.53E 25 151 36 25 1.9 0 <4
17-jul-10 58.54N3.46E 25 146 36 25 1.9 0 <4
16-jul-10 59.07N3.44E 25 147 35 25 1.9 1 4
31-jul-10 59.11N0.22E 25 260 69 30 1.9 1 4
11-aug-10 59.19N3.22E 25 136 35 25 1.8 0 <4
12-aug-10 59.36N3.51E 25 215 37 28 1.6 0 <4
29-jul-10 59.42N3.41E 25 272 57 30 1.8 0 <4
13-aug-10 59.44N3.53E 25 212 36 28 1.6 0 <4
14-jul-10 60.10N1.53E 25 151 38 25 1.9 0 <4
4-aug-10 60.11N2.14E 25 277 59 30 1.8 0 <4
19-jul-10 60.14N2.12E 25 261 58 30 2.0 1 4
15-jul-10 60.16N2.22E 25 256 51 30 1.8 0 <4
3-aug-10 60.23N1.54E 25 272 64 30 2.0 0 <4
30-jul-10 60.23N2.06E 25 288 60 30 1.7 0 <4
19-jul-10 60.26N2.12E 25 264 66 30 2.1 0 <4
2-aug-10 60.33N0.27E 25 255 57 30 1.9 0 <4
2-aug-10 60.37N0.31E 25 257 63 30 1.9 1 4
all herring 566 198 95 27 5.2 11 2

Table 2. Sampling Dates and Positions, Sample Size (n), Average Weight and Length, And the Numbers and Percentage of
Individual Fish with Ingested Plastic Per Species for Grey Gurnard, Mackerel, Cod, Whiting, Haddock and Horse Mackerel
catch-date position sample size avg W (g) stdev W(g) avg L(cm) stdev L (cm) ind. with plastic % ind. with plastics
gray gurnard
9-sep-10 55.21N00.65E 62 55 27 17 3.5 0 <2
9-sep-10 55.23N00.52E 26 64 42 18 3.9 0 <4
9-sep-10 55.37N00.45E 83 100 50 21 4.2 0 <1
all gray gurnard 171 0 <1
whiting
16-feb-11 50.32N0.34E 48 368 254 33.8 30.7 4 8
14-okt-10 52.45N3.40E 57 134 78 3.6 2.7 2 4
all whiting 105 306 121 32.1 3.5 6 6
horse mackerel
29-sep-10 49.30N3.00W 100 79 16 20.9 1.2 1 1
haddock
2-feb-11 56.16N1.26E 48 183 43 27.8 2.0 3 6
7-feb-11 57.13N1.33W 49 202 75 28.3 3.1 3 6
all haddock 97 192 75 28.1 3.1 6 6
mackerel
1-sep-10 57.14N1.18E 84 226 79 29 3.8 0 <1
cod
17-feb-11 50.56N1.34E 12 3529 2629 64 22.5 1 8
21-feb-11 51.29N3.8E 7 5112 1375 77 8.9 1 14
17-feb-11 51.40N2.37E 28 4280 3512 69 23.7 2 7
17-feb-11 51.8N2.9E 7 1795 1447 52 16.8 1 14
31-jan-11 52.23N2.50E 2 5436 1392 76 10.6 1 50
31-jan-11 52.23N3.16E 11 4 36
2-feb-11 55.49N0.35E 13 472 342 37 7.3 0 <8
all cod 80 3312 3019 61 23.0 10 13

geographical position on the amount of ingested plastics has
never been studied.
It has been suggested that ingestion of plastics can adversely
impact the condition of animals27 by reducing food uptake due
8819
to false feelings of satiation or by causing internal injury or
blockage of the intestinal tract. In addition, it has been
suggested that plastics could enhance the transfer of persistent
organic pollutants to the animals.4,28 As far as we know, the
dx.doi.org/10.1021/es400931b | Environ. Sci. Technol. 2013, 47, 8818−8824
Environmental Science & Technology Article

effects of ingested marine plastics on the condition of fish have
never been investigated.
The aims of this study were to quantify the occurrence,
number, and size of plastic particles in fish caught at different
geographical positions in the North Sea, and to test the
hypothesis that ingested plastic adversely affects the condition
of the fish. In total 1203 individual fish were sampled covering
seven species: cod (Gadus morhua), whiting (Merlangius
merlangus), haddock (Melanogrammus aeglef inus), herring
(Clupea harengus), horse mackerel (Trachurus trachurus), gray
gurnad (Eutrigla gurnardus), and atlantic mackerel (Scomber
scombrus). Size and weight of the fish were recorded for
calculation of the condition index. Plastic was isolated from the
fishes’ digestive tract and size and appearance was determined.
The polymer type of a selection of particles was characterized
by infrared spectrometry.
IR-spectrum 400−4000 cm−1) by TÜ V-Rheinland Nederland
BV.
Five particles smaller than the sieve diameter (0.2 mm) were
discovered, with a minimum size of 0.04 mm, but these were
not included in the analyses. Apart from these particles, very
thin and often less than 1 mm long colored textile fibers were
detected in almost every sample. As it was speculated that these
fibers could be airborne contamination from clothing, further
sample processing was performed in a clean air flow cabinet
after which the occurrence of these fibers strongly declined.
This indicates that utmost precautions are needed to prevent
air borne sample contamination during the whole process of
sample collection and laboratory analysis.19 These textile fibers
were at least partly considered artifacts and therefore further
excluded from data analysis.
Data Analysis. The frequencies of fish with ingested

■ METHODS
Sampling and Processing. The fish used for this study
plastics in the samples were not normally distributed per area.
In order to test the statistical significance of differences between
the Northern and the Southern North Sea the nonparametric
were sampled using a Grand Ouverture Verticale (GOV) trawl Mann−Whitney test was applied using the software package
with a minimum (cod-end) mesh size of 10 mm during daylight GraphPad PRISM V5.04.
hours at two periods. Between July and October 2010, 18 Condition index (K) was calculated from fish weight (W; g),
samples of herring, three samples of gray gurnard, one sample and body length (L; cm) using Fulton’s Condition Factor
of whiting, and one sample of mackerel were collected from the formula:
northern part of the North Sea, between 55° and 60°N. In W
January and February 2011, four samples of herring, seven K = 100 ×
L3
samples of cod, two samples of haddock, and a single sample of
whiting were collected from the southern part of the North Sea, The nonparametric Mann−Whitney test was also applied to
between 49° and 56°N. At least 80 individuals from each test the significance of the differences in body weight, length,
species were collected for investigation of the intestines for and condition factor between fish with and without ingested
plastics, the sampled numbers of individuals per location ranged plastics. Differences were considered significant at p < 0.05.
between 2 (cod) and 100 (horse mackerel). Sampling locations
and numbers of the collected species are presented in Tables 1
(herring) and 2 (other species).
■ RESULTS AND DISCUSSION
Occurrence of Plastics in North Sea Fish. Plastic
During the 2010 surveys, the sampled fish was stored directly particles were detected in five of the seven sampled species
at −20 °C. After thawing in the laboratory, length and weight (Tables 1 and 2). No plastics were found in gray gurnard and
was determined, and all of the contents of the esophagus, mackerel. Assuming the samples as representative for the
stomach, and intestines was collected in a jar that was then sampled locations this indicates that less than 0.6% of the local
filled with a 10% KOH solution (analytical reagent grade, gray gurnards and less than 1.2% of the mackerel contain
Fisher Chemical). The amount of KOH added was at least 3 ingested plastic. The highest frequency was observed in cod
times the volume of the biological material. The jars were (13% of the examined individuals), and the lowest in herring
stored at room temperature for 2 to 3 weeks until dissolution of (2%) and horse mackerel (1%). For whiting and haddock,
the organic material was observed to be complete. Jars were not plastic was found in 6% of the individuals.
stirred in order to prevent damage to plastic particles caused by Of the 1203 individual fish that were investigated, 33 (2.6%)
hard stomach constituents (e.g., shells). Previous tests contained plastic (Table 3). The highest frequency of fish with
confirmed the resistance of plastic particles against 10% KOH plastics was sampled in the southern North Sea, especially
(Mergia, unpublished data). During the 2011 surveys, length around 50°N and 52°N. No samples were collected around 53
and weight of the fish were measured on board ship and the
complete digestive tract (esophagus, stomach and intestines) Table 3. Percentage of Fish with Ingested Plastic As Sampled
was removed, put in a jar and stored at −20 °C. In the in the Southern and Northern, And the Whole North Sea,
laboratory, after thawing, 10% KOH solution was added and Presented Per Species and for All Species Together
the jars were stored for 2−3 weeks similar to the 2010 samples.
Once the organic material was degraded, the jars content was area 49−55°N 56−60°N 49−60°N
sieved (0.2 mm) to collect the nondigestible residue, which was
n % plastic n % plastic n % plastic
searched using a stereomicroscope. Plastic particles were
counted per individual fish, and color and shape was described. herring 116 1.7 450 0.4 566 1.4
Particle size was measured at their largest cross-section. In gray gurnard 0 171 0.0 171 <1
2010, this was done roughly using 1 mm as smallest unit, while whiting 105 5.7 0 105 5.7
in 2011 more accurate measurements were made applying an horse mackerel 100 1.0 0 100 1.0
ocular micrometer. To get an impression of the polymer haddock 0 97 6.2 97 6.2
composition of the particles, a selection of six particles mackerel 0 84 0.0 84 <1
representing the major visually distinguishable classes was cod 67 14.9 13 0.0 80 13
analyzed using Fourier transform infrared spectroscopy (FTIR; all species 388 5.4 815 1.2 1203 2.6

8820 dx.doi.org/10.1021/es400931b | Environ. Sci. Technol. 2013, 47, 8818−8824

Environmental Science & Technology
Figure 1. Numbers of fish sampled per species in bars, and the percentage of the fish (all species) that contained ingested plastics grouped per degree
N latitude (49 = 49°−50°N).
and 54°N, but from 55°N and further to the north the
frequency of fish with ingested plastics in our samples
decreased (Figure 1). The data show a peak in the frequency
of fish containing plastics in the English Channel. Since the
species composition of the samples varied per area, the
influence of species or area on the frequency of fish containing
plastics is not clear. For instance, the fact that no plastics were
found in mackerel and gray gurnard that were only sampled in
the northern North Sea, does not imply that these species are
also free of plastics in the southern North Sea.
If all species are included we found ingested plastic in 5.4% of
the fish from the southern North Sea, against 1.2% in the
northern North Sea (Table 3) a difference that was significant
(p=<0.001; Figure 2). Herring was the only species for which a
Figure 2. Percentage of fish containing ingested plastics in the samples
from the southern (49−54 N) and the northern North Sea (55−60
N). For all sampled species (herring, gray gurnard, whiting, horse
mackerel, haddock, mackerel, and cod) together, and for only herring.
Presented are median (horizontal line), 25−75 percentiles (box) and
range (bars) of the particles encountered. Statistical significance
differences are indicated by *** for p < 0.001.
broad set of adequate samples was available for the whole range
of North Sea locations: within this single species the frequency
of individuals with plastics was on average lower in the
northern North Sea without being statistically significant. Cod
was also sampled in both the southern (50−53°N, 6 samples,
67 individuals) and the northern North Sea (55°N, 1 sample,
13 individuals). In all six southern samples plastics were found
in 7 to 50% of the sampled fish (Table 2); none of 13
individuals from the single northern location was found to
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contain plastics. In spite of its small number, the cod samples
support the idea that frequency of plastic ingestion is lower in
the northern North Sea. Except for one cod sample, the
northern North Sea samples were all collected in 2010, whereas
the samples from the southern North Sea were collected in
2011. We assumed that no strong annual differences occurred.
The aforementioned methodological differences between 2010
and 2011 sample processing may have affected the detection of
the most inconspicuous, especially fiber-like plastics. However,
for reasons mentioned earlier, such fibers were not included in
our analyses. Therefore, we conclude that the higher frequency
of fish with ingested plastics in the southern North Sea
represents the higher local plastic pollution level. This
observation is in line with findings from the monitoring of
stomach contents of Fulmars.26
The percentage of individual fish containing plastics in our
study ranges per species between 0 and 13% for all North Sea
locations combined, and between 1.2% for all species combined
in the north to 5.4% for those in the south. Such levels compare
roughly to the 9.2% ingestion rate for mesopelagic fishes in the
plastic soup of the North Pacific Gyre reported by Davison and
Asch.19 Their sample sizes were too low to report ingestion
rates for separate species, but they noted a difference of 11.6%
for vertically migrating species to 4.8% for those that do not
regularly migrate to the more polluted surface. Boerger et al. 18
reported 35% frequency of ingestion in mesopelagic fish from
the gyre, but in their samples cod-end feeding could not be
excluded and may thus overestimate actual frequency of
ingestion.19 All our fish samples were obtained from nets
with minimum mesh sizes of 10 mm, which excludes the risk of
cod-end feeding of particles of sizes relevant in our study. A
recent study investigated the presence of ingested plastics in
fish from the English Channel at the southern border of the
area that was sampled for the present study (Latitude 50°16
N).25 In that study plastics were encountered in 36.5% of the
fish, which is five times higher than the frequency we
determined in the Southern North Sea. However, Lusher and
co-workers 25 reported that 68% of all encountered particles
consisted of fibers, while the smallest fibers were excluded in
our study for the reasons stated. It is not clear to what extent
the contribution of such fibers was underestimated in our
samples, or was overestimated as a result of air-borne
contamination in the samples of Lusher and colleagues. We
recommend that future research on ingested plastics in fish, as
well as in other organisms, is performed with special
precautions to avoid air-borne contamination with small fibers.
The handling of the biological sample (in our case the fish)
dx.doi.org/10.1021/es400931b | Environ. Sci. Technol. 2013, 47, 8818−8824
Environmental Science & Technology
should then preferably commence with rinsing the outside of
the specimen, while further processing, including dissection
should be done in a clean-air cabinet using dust-free clothing/
cloves.
Number and Size of the Particles. Of the 33 fish with
plastics, only 6 individuals contained more than 1 particle. The
maximum numbers of particles discovered in one fish was 4
(Table S1 in Supporting Information, SI). All plastic particles
that were encountered were less than 5 mm in size. This is in
line with studies performed in the North Pacific Ocean that
reported microplastics in a size class of 1−3 mm in the fish,18,19
and with recent work on fish from the English Channel where
1−2 mm was the most common size class of ingested
particles.25 The median size of the particles we found was 0.8
mm. In our North Sea samples, there were no significant
differences between particle size classes in the different fish
species (Figure 3).
Figure 3. Particle size distribution of microplastic detected in North
Sea fish. Presented are median (horizontal line), 25−75 percentiles
(box), and range (bars) of the particles encountered.
There was no clear relation between particle size and size of
the fish. Particles smaller than 1 mm were found in all size
classes of fish that ranged from 10 cm (herring) to almost 1 m
(cod) (Figure 4). Particles above 1.5 mm were only found in
Figure 4. Size of the ingested plastic particles plotted against body
weight of the fish per species.
fish above 20 cm in length, especially whiting and cod.
Differences between species might be expected due to
differences in diet, feeding behavior, and size. As planktivorous
species, herring 29 and horse mackerel 30 collect their food
primarily by filtering seawater. The fact that only particles
smaller than 1.5 mm were found in the intestine of these
species could indicate that these were filtered from the water
column and ingested with food items. The gadoid species,
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cod,31 haddock 32 and whiting,33 are primarily piscivorous and
contained also particles that were larger than what was found in
the planktivorous species. However, since the planktivorous fish
were also smaller than the piscivorous fish, it was not possible
to discriminate the influence of length from feeding behavior.
However, it is unlikely that the piscivorous fish actively ingested
the particles considering them as food items. The cod in which
plastic particles were discovered ranged in body length between
50 and 90 cm but contained only particles of less than 3 mm.
This is only a fraction of the size of a normal food items for
these fishes 33 and suggests that plastics of such sizes in their
body may reflect ingestion by coincidence or secondary
ingestion of plastics incorporated in their prey.
The observation that more than 80% of the fish with plastic
contained only a single particle, suggests that microplastics do
not accumulate inside the digestive tract of these fish for very
long periods.
Types of Plastics. The six plastic particles that were
analyzed with FTIR all were encountered in fish from the
southern North Sea. Two particles consisted of polyethylene
(PE), two particles of polypropylene (PP), and the two other
particles were polyethyleentereftalaat (PET) and styrene-
acrylate (SA), respectively. These results are indicative only,
because the sample size was too small to draw conclusions
about the relative contribution of the individual polymer types
in the ingested particles. Lusher et al. 25 also found those
polymer types in fish from the English Channel but identified
the bulk of their particles as the semi synthetic cellulosic
material rayon (58%), and polyamide (35%). The high
proportion of such polymers in their results must be linked
to the high proportion (68%) of textile fibers in their samples.
Relation with Fish Size and Condition. For most of the
species investigated, the condition factor was comparable for
the fish with and without ingested plastics (Table S2 of the SI).
Only in the case of haddock was the condition factor
significantly lower for the fish in which plastics were
encountered (p = 0.01). We argue that this observation is
insufficient to confirm the hypothesis that plastic affects the
condition index of fish. First, although the difference for
haddock was significant, the difference in the magnitude of the
condition index was marginal (0.85 ± 0.06 vs 0.78 ± 0.05).
Second, the difference was found for only one out of 5 species.
Furthermore, the very small size of the plastic particles found
and the limited occurrence suggest that the plastic does not
accumulate in the intestinal tract. The presence of plastics at
the moment of sampling than only indicates that this individual
fish has recently ingested plastic but does not mean it is
structurally more exposed than others. Also, the particles were
too small to expect they can cause feelings of satiation,
intestinal blockage, or play a relevant role as a carrier of
pollutants. In conclusion, it appears unlikely that the amounts
of plastics that we encountered will affect the condition of the
fish.
This may be influenced by particle size relative to fish size.
Impact of the type of plastic particles that we encountered may
be relevant to early life stages of fish, where a particle size of 1
mm is in theory large enough to cause effects like mentioned
above. Early literature, reviewed by Hoss 34 indicates that
sometimes high ingestion rates have been observed in wild
larval fish, but also mentions laboratory experiments that
suggest that larval and juvenile fish either rejected plastic
particles or passed them through the gut without obvious
dx.doi.org/10.1021/es400931b | Environ. Sci. Technol. 2013, 47, 8818−8824
Environmental Science & Technology
damage. Our study cannot shed light on this and further
investigations are recommended.
■
ASSOCIATED CONTENT
* Supporting Information
S (16) Goldstein, M. C.; Rosenberg, M.; Cheng, L. N. Increased
Tables showing additional information. This material is
available free of charge via the Internet at http://pubs.acs.org.
■
AUTHOR INFORMATION
Corresponding Author
*Phone: +31 317 487122; e-mail: edwin.foekema@wur.nl.
Notes
The authors declare no competing financial interest.
■
ACKNOWLEDGMENTS
The authors thank Ingeborg de Boois and the crew of the
research vessel Tridens for assisting in the fish sampling, Andre
Meijboom for his help with identification of plastics, and Ellen
Besseling for her comments on an earlier version of the
manuscript.
■
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