Marine Pollution Bulletin 95 (2015) 248–252

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Marine Pollution Bulletin

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

Microplastic in a macro filter feeder: Humpback whale Megaptera

novaeangliae
E. Besseling a,b,⇑, E.M. Foekema b, J.A. Van Franeker b, M.F. Leopold b, S. Kühn b, E.L. Bravo Rebolledo b,
E. Heße b, L. Mielke b, J. IJzer c, P. Kamminga d, A.A. Koelmans a,b
a
Aquatic Ecology and Water Quality Management Group, Wageningen University, P.O. Box 47, 6700 AA Wageningen, The Netherlands
b
IMARES – Institute for Marine Resources & Ecosystem Studies, Wageningen UR, P.O. Box 68, 1970 AB IJmuiden, The Netherlands
c
Faculty of Veterinary Medicine, Department of Pathobiology, Utrecht University, P.O. Box 80158, 3508 TD Utrecht, The Netherlands
d
Naturalis Biodiversity Center, P.O. Box 9517, 2300 RA Leiden, The Netherlands

a r t i c l e i n f o a b s t r a c t

Article history: Marine filter feeders are exposed to microplastic because of their selection of small particles as food
Available online 24 April 2015 source. Baleen whales feed by filtering small particles from large water volumes. Macroplastic was found
in baleen whales before. This study is the first to show the presence of microplastic in intestines of a
Keywords: baleen whale (Megaptera novaeangliae). Contents of its gastrointestinal tract were sieved, dissolved in
Microplastic 10% potassium hydroxide and washed. From the remaining dried material, potential synthetic polymer
Filter feeders particles were selected based on density and appearance, and analysed by Fourier transform infrared
Humpback whale
(FTIR) spectroscopy. Several polymer types (polyethylene, polypropylene, polyvinylchloride,
Ingestion
polyethylene terephthalate, nylon) were found, in varying particle shapes: sheets, fragments and threads
with a size of 1 mm to 17 cm. This diversity in polymer types and particle shapes, can be interpreted as a
representation of the varying characteristics of marine plastic and the unselective way of ingestion by
M. novaeangliae.
Ó 2015 Elsevier Ltd. All rights reserved.

1. Introduction Cauwenberghe and Janssen, 2014) and in planktivorous fish

(Boerger et al., 2010; Foekema et al., 2013). By filtering a size range
Microplastic (i.e. particles with a synthetic origin <5 mm, from plankton up to small fish (Deméré, 2014; Nemoto, 1970),
Barnes et al., 2009) is present in the marine environment due to baleen whales can potentially ingest microplastic directly from
direct disposal and degradation of larger plastic items (Barnes the water column as well as via prey species. Exposure of baleen
et al., 2009) and was first emphasised in the 1970’s (Carpenter whales to microplastic has therefore been hypothesised recently
et al., 1972). Because of its small size and wide spread occurrence, (Fossi et al., 2012; Fossi et al., 2014). Phthalates in the blubber tis-
microplastic is now thought to be available to species throughout sue as indirect indication of microplastic in a fin whale have been
the marine food web (Cole et al., 2011). Only a few studies about suggested by Fossi et al. (2012), although this does not differenti-
possible negative effects of microplastic on organisms have been ate between phthalate uptake from food items (zooplankton, small
published (Lee et al., 2013; Besseling et al., 2013; Browne et al., fish) and microplastic. Baleen whales are suggested to be useful as
2013; Wright et al., 2013; Rochman et al., 2014). So far reported a monitoring species in the implementation of Descriptor 10
possible negative effects of microplastic are on survival, feeding, (Marine litter) of the Marine Strategy Framework Directive
oxidative status and uptake of persistent organic pollutants (MSFD, Fossi et al., 2012; Fossi et al., 2014; Galgani et al., 2014),
(Besseling et al., 2014). even though direct measurement of microplastic in baleen whales
Due to their feeding behaviour, filter feeders are thought to col- has not yet been reported.
lect microplastic particles from the water column. Microplastic has Mesoplastic (i.e. items with a synthetic origin of 5–20 mm) is
indeed been encountered in bivalves (De Witte et al., 2014; Van often included in the macroplastic size category (i.e. items with a
synthetic origin >20 mm, Barnes et al., 2009). This includes plastic
lids, bags and fishing lines and has been found in 31 marine mam-
⇑ Corresponding author at: Aquatic Ecology and Water Quality Management
Group, Wageningen University, P.O. Box 47, 6700 AA Wageningen, The Netherlands.
mal species, including baleen whales (Simmonds, 2012). Records of
Tel.: +31 317487124. macroplastic in Cetacean species are increasing. While being
E-mail address: [email protected] (E. Besseling). reported in at least 26 Cetacean species before (Denuncio et al.,

http://dx.doi.org/10.1016/j.marpolbul.2015.04.007
0025-326X/Ó 2015 Elsevier Ltd. All rights reserved.
 E. Besseling et al. / Marine Pollution Bulletin 95 (2015) 248–252 249

2011), macroplastic is reported in 48 (56% of) Cetacean species by marking gauge (for subsequent volume calculation) and subjected
2014 (Baulch and Perry) and in 61.5% in the review by Kühn et al., to Fourier transform infrared (FTIR) analyses. FTIR spectra of the
(2015). Examples are 28% of examined Franciscana dolphins samples were gained with a Varian Scimitar 1000 FT-IR spectrom-
(Pontoporia blainvillei) having plastic in their stomach, including eter equipped with a DTSG-detector. Sample and reference spectra
microplastic (Denuncio et al., 2011), micro- and mesoplastic in were obtained using a measurement resolution of 4 cm1, follow-
True’s beaked whales (Mesoplodon mirus, Lusher et al., 2015), sev- ing Gonzalez-Contreras et al. (2010).
ere incidences of large macroplastic quantities causing starvation
and death in a beaked whale and several sperm whales 2.3. Data analysis
(Mesoplodon densirostris, Physeter microcephalus, Secchi and
Zarzur, 1999; De Stephanis et al., 2013) and marine debris in two FTIR spectra of the particles were compared with reference
baleen whale species, Minke and Sei whale (Balaenoptera acutoros- polymer spectra (Thompson et al., 2004; Ng and Obbard, 2006)
trata, B. borealis, Baulch and Perry, 2014). Raised hypotheses based of the seven most produced polymers polyethylene (PE),
on these incidences are that (1) chances of micro- and macroplastic polypropylene (PP), polyvinylchloride (PVC), polyethylene tereph-
ingestion are higher for relatively passive feeders, as compared to thalate (PET), polystyrene (PS) and nylon (PA) (Andrady, 2011).
active predators (Di Beneditto and Awabdi, 2014), (2) even small Additionally, comparisons with reference spectra of natural rubber
amounts of macroplastic can cause obstruction of the digestive and cellulose were made. Statistical analyses were performed with
tract (Simmonds, 2012; De Stephanis et al., 2013), and (3) linear regression in ‘RStudio’ statistical software (Version 0.98.976,
microplastic might be of special concern as it may clog the filtering R Development Core Team). Particles where the quality index i.e.
apparatus of organisms (Simmonds, 2012). Theoretically, all of the correlation coefficient (R2) of the comparison with reference
these hypotheses apply to baleen whales. spectra was >0.7 were classified as synthetic polymers.
The non-selective feeding mode of many baleen whale species
by ingesting material surrounding the intended prey in the water 3. Results
with a size large enough to be retained by their baleens (Johnson
and Wolman, 1984), might result in exposure to microplastic. 3.1. Post-mortem examination
The ratio between microplastic and zooplankton (Collignon et al.,
2012) indicates a possible daily intake of 3.7 thousand microplastic According to the well-developed musculature and blubber
particles in fin whales in the Mediterranean (Fossi et al., 2014). thickness, the humpback whale was in good nutritional condition.
Negative effects of microplastic uptake on organisms in the marine Severe post-mortal decomposition of all internal organs prevented
environment might occur, though the information about effects is detailed macroscopic and microscopic evaluation. About a fifth to
still limited. Meanwhile, microplastic is already present in the mar- tenth of the total length of the gastrointestinal tract was sampled
ine environment (Cole et al., 2011). This is why we studied the for content analysis. There were few contents in the gastrointesti-
occurrence of microplastic in a stranded baleen whale, a humpback nal tract. Continued digestion of the contents of the gastrointesti-
whale. Our study describes the first reported case of microplastic nal tract during the four days of stranding, might have resulted
ingested by a humpback whale, and discusses it within the context in fluid contents that were partly deflated from the gastrointestinal
of microplastic uptake related to ecological traits. tract during sampling. The primary cause of the stranding could
not be identified. However, prolonged stranding in itself caused
2. Materials and methods deterioration and death of the animal.

2.1. Animal 3.2. Plastic

At December 12th 2012, a 10.34 m long, ca. 16 thousand kg A total of 45 particles of possible synthetic origin was found in
juvenile female humpback whale (Megaptera novaeangliae) the gastrointestinal tract samples. Of these, 77.7% was large
stranded on a sandbank between harbour city Den Helder and enough (>1 mm2) to be analysed by FTIR. Of these particles,
the island Texel in The Netherlands, and was publically called
‘Johanna’. Four days later, it died.

2.2. Sampling

Two days post-mortem, necropsy was performed on the

severely autolytic carcass. Wood shreds were used around the
humpback carcass for absorption of body fluids. Multiple tissue
samples were preserved, including part of the gastrointestinal tract
for content analysis. Gastrointestinal tract samples were stored at
18 °C till further processing. After thawing, samples were
sequentially sieved over two sieves with a mesh size of 1 mm
and 0.5 mm. Subsequently, the residues were dissolved in 10%
potassium hydroxide (KOH) solution. The remainder was washed
according to previous methods in a washing machine in double
washing bags, the inner bag having a mesh size of 300 lm and
1 mm
the outer bag 120 lm (Bravo Rebolledo et al., 2013). After washing,
the samples were dried for three hours at 70 °C. From the remain-
ing material, possible synthetic polymer particles were selected
Fig. 1. Polypropylene (PP) particle found in the gastrointestinal tract samples of the
based on density (floating/sinking in saturated NaCl dispersion) studied humpback whale, R2 = 0.82. Additional photos of other particles found in
and appearance (Zeiss Stereo Discovery V8 microscope) according the gastrointestinal tract of the studied humpback whale are given in the
to previous procedures (Van Franeker et al., 2011), measured by supporting information of this article.
250 E. Besseling et al. / Marine Pollution Bulletin 95 (2015) 248–252

Table 1
Particle shape, number and size of particles and percentage of the total plastic volume found in the studied humpback whale, per polymer type with average R2 values and ranges,
together with the percentage of the total global production of these polymer types, PE (polyethylene), PA (nylon), PP (polypropylene), PVC (polyvinylchloride) and PET
(polyethylene terephthalate) (Andrady, 2011).

Polymer type Average R2 Particle shape Number of particles Size (mm) % Volume % Global production
PE 0.90 (0.88–0.98) Sheet 9 3.3–12  0.3–8.2  0.04–0.2 55.01 38
PA 0.80 (0.70–0.96) Thread, fragment 4 2.3–170  0.1–1.5  0.1–0.4 37.64 <3
PP 0.82 Sheet 1 3.6  2.4  0.1 5.61 24
PVC 0.82 Sheet 1 5.8  3.3  0.01 0.97 19
PET 0.82 Fragment 1 1.1  0.8  0.2 0.77 7

45.7% had a synthetic origin (Fig. 1), 25.7% had a natural origin and humpback whale we studied. The daily filtered water volume of
for 28.6% no matching spectra were obtained. The identified poly- humpback whales has to our knowledge not been reported yet.
mer types were PE, PP, PVC, PET and PA (Table 1). For size cate- For baleen whale species with similar feeding type (Deméré,
gories, we follow the classification of Barnes et al. (2009). Of the 2014; Nemoto, 1970), we here assume that daily filtered water vol-
synthetic particles, 12.5% had a maximum dimension of 2.5– ume is constant per unit surface of the baleen plate rows. We use
17 cm (macroplastic). These were threads, with a diameter of the formula:
0.1–0.23 mm. 50% had a size of 5.8–12.0 mm by 0.3–8.2 mm  
BPRy
(mesoplastic). Those were all sheets. The remaining 37.5% con- V W;y ¼ V W;x ð1Þ
BPRx
sisted of sheets and fragments with a size of 1.1–4.7 mm by 0.4–
2.4 mm (microplastic). The found plastic particles all made up less with VW (m3) the average daily filtered water volume and BPR (m2)
than 3.5 mm3 per particle. As particles might fall apart during pas- the average surface of the baleen plate rows for species y and spe-
sage of the gastrointestinal tract, sampling or processing, we dis- cies x. Fossi et al. (2014) report a daily filtered water volume of
cuss particle volumes instead of particle numbers. A total plastic 5.9 thousand m3 for fin whales. With the BPR of 4 m2 of fin whales
volume of 13.7 mm3 was encountered, of which most was PE and and 2.6 m2 of humpback whales (Nemoto, 1970), we calculate a
PA (Table 1), which might represent the worldwide most produced daily filtered water volume of 3.8 thousand m3 for humpback
polymer (PE) as well as polymers used in the marine environment whales. The gut passage time (GPT) of baleen whales is to our
in fishing gear (Andrady, 2011). knowledge unknown. We here make the assumption that the GPT
There were few remainders of fish found in the gastrointestinal can be assumed to be constant per unit length of the gastrointesti-
tract samples, being small fish bones, vertebra and otoliths of her- nal tract, across Cetacean species. We use the formula:
ring and sprat. Wood shreds were found in the gastrointestinal   
tract samples, most likely originating from the necropsy site.
BGy BLy
GPTy ¼ GPTx ð2Þ
Twenty-five gram of comparable wood shreds was investigated BGx BLx
by microscope. No plastic particles were found among these wood with GPT (h) the average gut passage time, BG the body to gastroin-
shreds. testinal tract length ratio and BL the body length for species y and
The high variation in particle appearance and polymer type of species x. A GPTx of 4.2 h has been reported for (Cetacean species)
the plastic found in the gastrointestinal tract samples is an indica- Amazon river dolphins (Inia geoffrensi) with a BLx of 2.22 m
tion that the particles originate from the marine environment. (Kastelein et al., 1999). By lacking the BGx for the Amazon river dol-
Studying synthetic fibres in the gastrointestinal tract samples phin species we use BGx of another river dolphin (Gangetic dolphin,
was omitted, because of the high risk of fibres being caused by Platanista gangetica) of 7.3 (Slijper, 1979). We use a BGy of 5.5 for
methodological contamination during sampling and analyses, i.e. humpback whales (Slijper, 1979) and BLy of the studied humpback
clothes, washing bags (Foekema et al., 2013; Fries et al., 2013). whale of 10.34 m, and calculate the GPT of the studied humpback
As fragments, threads and sheets are less than fibres prone to con- whale to be 14.6 h. For inert particles, the particle content of the
taminate samples during the used methods and additionally water volume ingested within the GPT, can be seen as the steady
because of the eroded condition of the found particles, we render state concentration of plastic in a filter feeding organism. We use
it likely that they were ingested by the humpback whale at sea. the formula:
Humpback whales have an intestine length of about 5.5 times
their body length (Slijper, 1979), such that the sampled humpback NP
C SS ¼
ð3Þ
whale was estimated to have an intestine length of about 57 m. As V W GPT
24
a fifth to a tenth of this length was sampled, it is likely that five to
with CSS (plastics/m3) the steady state concentration of plastic in the
ten times as much plastic was present on a whole organism basis if
humpback whale, NP (n), VW (m3) and GPT (h) respectively the
we neglect gastrointestinal tract section type, than encountered in
number of particles, daily filtered water volume and gut passage
the subsample. That would result in an estimate of up to 160 small
time of the studied humpback whale. With this formula we calcu-
plastic particles or a volume of up to 137 mm3 of plastic in the
late the filtered water volume of the humpback whale within the
whole humpback whale.

gut passage time V W GPT24
to be 2.3 thousand m3 of water and CSS
3
to be 0.07 plastics/m . We hypothesis that CSS is directly related
4. Discussion to the concentration of plastic in the foraging area of a filter feeding
organism. We use the formula:
By combining information on daily filtered water volume, gut
C SS  C fa ð4Þ
passage time and plastic particle numbers in an organism, it is pos-
sible to calculate a plastic concentration in an organisms’ foraging with Cfa the concentration of plastic in the foraging area of the
area from biological traits. The estimated concentration then can humpback whale. The average microplastic particle concentration
be compared with data on measured concentrations. Here we per- in the Northeast Atlantic is 0.1 microplastics/m3 excluding syn-
formed such a calculation by using plastic numbers of the thetic fibres (Lusher et al., 2014). This measured concentration in
 E. Besseling et al. / Marine Pollution Bulletin 95 (2015) 248–252 251

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