Content uploaded by Roberta Minutoli
Author content
All content in this area was uploaded by Roberta Minutoli on Dec 14, 2017
Content may be subject to copyright.
Are baleen whales exposed to the threat of microplastics? A case study
of the Mediterranean fin whale (Balaenoptera physalus)
Maria Cristina Fossi
a,
⇑
, Cristina Panti
b
, Cristiana Guerranti
a
, Daniele Coppola
a
, Matteo Giannetti
a,b
,
Letizia Marsili
a
, Roberta Minutoli
c
a
Department of Environmental Sciences, University of Siena, Via P.A. Mattioli 4, 53100 Siena, Italy
b
Department of Evolutionary Biology, University of Siena, Via A. Moro 2, 53100 Siena, Italy
c
Department of Animal Biology and Marine Ecology, University of Messina, Viale F. Stagno D’Alcontres, 31, 98166 Messina, Italy
article info
Keywords:
Microplastic particles
Mediterranean Sea
Neuston
Surface plankton
Phthalates
Fin whale
abstract
Baleen whales are potentially exposed to micro-litter ingestion as a result of their filter-feeding activity.
However, the impacts of microplastics on baleen whales are largely unknown. In this case study of the
Mediterranean fin whale (Balaenoptera physalus), we explore the toxicological effects of microplastics
on mysticetes. The study included the following three steps: (1) the collection/count of microplastics
in the Pelagos Sanctuary (Mediterranean Sea), (2) the detection of phthalates in surface neustonic/plank-
tonic samples, and (3) the detection of phthalates in stranded fin whales. A total of 56% of the surface
neustonic/planktonic samples contained microplastic particles. The highest abundance of microplastics
(9.63 items/m
3
) was found in the Portofino MPA (Ligurian Sea). High concentrations of phthalates (DEHP
and MEHP) were detected in the neustonic/planktonic samples. The concentrations of MEHP found in the
blubber of stranded fin whales suggested that phthalates could serve as a tracer of the intake of micro-
plastics. The results of this study represent the first warning of this emerging threat to baleen whales.
Ó2012 Elsevier Ltd. All rights reserved.
1. Introduction
The emerging issue of microplastics (plastic fragments smaller
than 5 mm) in the marine environment has recently received
increasing attention (Hidalgo-Ruz et al., 2012). This ubiquitous, per-
sistent form of micro-debris requires centuries to degrade com-
pletely. Microplastics are primarily the result of the degradation of
plastics released into the environment since the beginning of the
plastic age. Micro-debris floating in the Mediterranean Sea has
reached maximum levels of 892,000 particles/km
2
. Recently, Colli-
gnon et al. (2012) determined neustonic microplastic and zooplank-
ton abundance in the northwestern Mediterranean Sea and showed
that the estimated mean abundance of microplastics was of the
same order of magnitude as that found for the North Pacific Gyre
(0.334 particles/m
2
,Moore et al., 2001), underscoring the high level
of this emerging threat in the Mediterranean environment.
Microplastics accumulate at the sea surface, especially within
the neustonic habitat (Ryan et al., 2009). This habit harbors a spe-
cifically adapted zooplankton fauna. There is increasing concern
that a wide range of marine organisms are affected by plastic
wastes in the sea. However, the mechanical, physical and toxico-
logical impacts of these wastes are largely unknown. More than
180 species, including planktophagous species, have been shown
to absorb plastic debris. Macrodebris ingestion and entanglement
are well documented in sea birds, mammals and turtles and more
recently in fishes (planktivorous and benthophagous) and inverte-
brates (Robards et al., 1995; Derraik, 2002; Thompson et al., 2004;
Ryan et al., 2009; Boerger et al., 2010; Collignon et al., 2012; Pos-
satto et al., 2011; Dantas et al., 2012; Murray and Cowie, 2011).
No information has previously been reported on the impacts of
microplastics on baleen whales, such as fin whales (Balaenoptera
physalus). The filter-feeding activities of these whales represent a
potential source of exposure to micro-litter ingestion. The fin
whale, the only resident mysticete in the Mediterranean Sea, forms
aggregations during the summer on the feeding grounds of the Pel-
agos Sanctuary Marine Protected Area (MPA) (Notarbartolo di Sci-
ara et al., 2003). These whales feed primarily on planktonic
euphausiid species. With each mouthful, the whales can trap
approximately 70,000 l of water, and their feeding activities in-
clude surface feeding. They could therefore face risks caused by
the ingestion and degradation of microplastics. Micro-debris can
be a significant source of lipophilic chemicals (primarily persistent
organic pollutants – POPs) and a source of pollutants such as poly-
ethylene, polypropylene and, particularly, phthalates. These chem-
ical pollutants can potentially affect organisms (Teuten et al.,
2007), are potential endocrine disruptors and can affect population
viability. With their long lifespan, whales could be chronically
0025-326X/$ - see front matter Ó2012 Elsevier Ltd. All rights reserved.
http://dx.doi.org/10.1016/j.marpolbul.2012.08.013
⇑
Corresponding author. Tel.: +39 0577 232913; fax: +39 0577 232930.
E-mail addresses: fossi@unisi.it (M.C. Fossi), panti4@unisi.it (C. Panti), guerran-
ticri@unisi.it (C. Guerranti), coppola32@unisi.it (D. Coppola), giannetti12@unisi.it
(M. Giannetti), letizia.marsili@unisi.it (L. Marsili), rminutoli@unime.it (R. Minutoli).
Marine Pollution Bulletin xxx (2012) xxx–xxx
Contents lists available at SciVerse ScienceDirect
Marine Pollution Bulletin
journal homepage: www.elsevier.com/locate/marpolbul
Please cite this article in press as: Fossi, M.C., et al. Are baleen whales exposed to the threat of microplastics? A case study of the Mediterranean fin whale
(Balaenoptera physalus). Mar. Pollut. Bull. (2012), http://dx.doi.org/10.1016/j.marpolbul.2012.08.013
exposed to these persistent contaminants derived from the inges-
tion and degradation of microplastics.
One toxicological feature of the marine environment that can
affect filter-feeding organisms is the influence that microplastics
may produce by enhancing the transport and bioavailability of per-
sistent, bioaccumulative and toxic substances. In fact, chemicals
for which the logarithm of the octanol/water partitioning coeffi-
cient (K(OW)) > 5 can potentially be partitioned >1% to polyethyl-
ene, a major component of microplastics. Moreover,
contaminants such as phthalates and polycyclic aromatic hydro-
carbons (PAHs) are among the principal constituents of plastics.
The dialkyl or alkyl/aryl esters of 1,2-benzenedicarboxylic acid,
commonly known as phthalates, are high-production-volume syn-
thetic chemicals; moreover, they are not covalently bound to plas-
tic and migrate from the products to the environment, thus
becoming ubiquitous contaminants (Latini et al., 2009). Public
and scientific concern about the potential human and wildlife
health risks associated with exposure to phthalates has increased
in recent years. The primary focus has moved away from the hep-
atotoxic effects to the endocrine-disrupting potency of these
chemicals (Latini, 2005), which have been shown to be reproduc-
tive toxicants in animals (Borch et al., 2006). Di-(2-ethylhexyl)
phthalate (DEHP) is the most abundant phthalate in the environ-
ment. In both invertebrates and vertebrates, DEHP is rapidly
metabolized in the form of its primary metabolite, MEHP (mono-
(2-ethylhexyl) phthalate) (Barron et al., 1989), which can be used
as a marker of exposure to DEHP.
This case study examines the Mediterranean fin whale, one of
the largest filter feeders in the world. This study is the first inves-
tigation of the potential impact of microplastics in a baleen whale
and suggests the use of phthalates as a tracer of the intake of
microplastics through the ingestion of micro-debris and plankton.
2. Methodology
The study included the following three steps: (1) the collection,
counting and sorting of microplastics and planktonic organisms in
surface neustonic/planktonic and water column samples from the
Pelagos Sanctuary MPA (NW Mediterranean Sea); (2) the measure-
ment of phthalate concentrations in surface neustonic/planktonic
and water column samples; and (3) the measurement of phthalate
concentrations in stranded fin whale specimens collected on the
coasts of Italy.
2.1. Step I: collection and sorting of microplastics in surface neustonic/
planktonic and water column samples in the Pelagos Sanctuary
Surface neustonic/planktonic and water column samples were
collected in the Ligurian Sea and Sardinian Sea (Fig. 1a) in summer
2011 (June–July) during the day with a WP2 standard net (57 cm
mouth diameter, 200
l
m mesh size) equipped with a flowmeter
for the measurement of the filtered volumes. For each surface sam-
ple (n= 23; MPM3–MPM26), the net was towed horizontally just
below the water surface at a speed of approximately 1 knot for
15 min. For each water column sample (MPP3, MPP10 and
MPP22, corresponding to the same geographical coordinates as
MPM3, MPM10 and MPM22) (Fig. 1a), the same net was vertically
towed from a depth of 50 m to the surface at a speed of 1 m/s. In
both cases, the net was washed on board, and each 2-l sample
was split into two separate aliquots of 1 l each with a Folsom split-
ter. One 1-l aliquot was filtered on a 200
l
m mesh sieve and imme-
diately frozen in liquid nitrogen for the subsequent analysis of
phthalates. The second aliquot was preserved in 4% formalde-
hyde-seawater buffered solution for subsequent quali-quantitative
analyses. A total of 26 frozen and preserved samples were used for
this study. For the analysis of plankton and plastic particles, the
samples were observed under a Leica Wild M10 stereomicroscope.
The organisms were counted and taxonomically classified (Table 1,
Supplementary data). The plastic particles were counted and mea-
sured, and those smaller than 5 mm were classified as microplas-
tics. All the data were normalized to the total volume filtered
and expressed as individuals and items/m
3
. To compare the data
with data expressed as items/m
2
in the literature, the present data
can be converted by multiplying the values (items/m
3
) by 0.5 m,
the thickness of the water stratum sampled with the WP2 net as
described above.
2.2. Step II: detection of phthalates in surface neustonic/planktonic and
water column samples
DEHP and MEHP were analyzed in the surface neustonic/plank-
tonic and water column samples (0.5–0.7 g) from the two sampling
sub-areas (Ligurian Sea and Sardinian Sea) following a method de-
scribed by Takatori et al. (2004), with a few modifications de-
scribed in Guerranti et al. (2012). Each sample was thawed and
weighed, and acetone was added. The sample obtained in this
way was sonicated. The organic part, containing DEHP and MEHP,
was separated from the remaining water, and the supernatant was
isolated. The supernatant phase was then recovered and combined
with that resulting from the first extraction and was then evapo-
rated in a centrifugal evaporator. The extract was then resus-
pended with 0.5 ml of acetonitrile and passed through a nylon
filter with pores of 2
l
m. Subsequently, the sample was placed in
an autosampler vial and injected into an LC-ESI-MS system. The
instrumental analysis was performed with a Finnigan LTQ Thermo
LC/MSn 110 with an ESI interface. A total of 5
l
l of the extracted
sample was injected via the autosampler into the HPLC system. A
reverse-phase HPLC column (Wakosil 3C18, 2.0 100 mm, 3
l
m;
Wako Pure Chemical Industries Ltd.) was used. The mobile phases
consisted of 100% acetonitrile (A) and 0.05% aqueous acetic acid
(B). Elution was performed using an isocratic mode (A/B: 15/85,
v/v) at 0.25 ml/min. ESI-MS was operated in the negative or posi-
tive ion mode depending on the analytes (MEHP was detected in
the negative mode, whereas DEHP was detected in the positive
mode). The heated capillary and voltage were maintained at
500 °C and ±4.0 kV, respectively. The ions used for identification
were (parent ion/daughter ion) 277/134 and 391/149 for MEHP
and DEHP, respectively. For the quantitative analysis, a four-point
calibration curve prepared by the progressive dilution of a solution
of the two analytes of interest was used. Blanks were analyzed
with each set of five samples as a check for possible laboratory con-
tamination and interference. The data quality assurance and qual-
ity control protocols also included matrix spikes and continuing
calibration verification. The limits of detection (LODs) and limits
of quantification (LOQs) for the compounds analyzed were the val-
ues of the compound in the +3 SD and +10 SD blanks, respectively.
The LOD and LOQ were 1 and 2 ng/g, respectively, for MEHP and 5
and 10 ng/g, respectively, for DEHP.
The levels of analytes below the limits of detection (<LOD) were
specified as values equal to the value of the LOD. If the analyte was
present at levels between the LOD and the LOQ, the LOQ value was
used. The values are expressed as fresh weight (f.w.).
2.3. Step III: measurement of phthalate concentrations in stranded fin
whale specimens collected along the coasts of Italy
Blubber samples were collected close to the dorsal fin in five
stranded fin whales (sub-adults and adults) during the period July
2007–June 2011 at five different sites on the Italian coast. The sam-
ples were stored at 20 °C prior to analysis. The details of the loca-
tion and gender of the stranded whales are shown in Fig. 1b. DEHP
2M.C. Fossi et al. / Marine Pollution Bulletin xxx (2012) xxx–xxx
Please cite this article in press as: Fossi, M.C., et al. Are baleen whales exposed to the threat of microplastics? A case study of the Mediterranean fin whale
(Balaenoptera physalus). Mar. Pollut. Bull. (2012), http://dx.doi.org/10.1016/j.marpolbul.2012.08.013
Sardinian Sea
SARDINIA
MPM21
MPM25
MPM26
MPM24
MPM18
MPM17
MPM19
MPM20
MPM23
San Rossore PI (Male)
MEPH 53.98 ng/g
Orbetello GR (Male)
MEPH 51.84 ng/g
Castelsardo SS (nd)
MEPH 1.00 ng/ g
Amalfi SA (Female)
MEPH 99.93 ng/g
Palinuro SA (nd)
MEPH 83.12 ng/g
Phthalates concentration in superficial neustonic/planktonic samples
AREA
DEHP (ng/g) MEHP (ng/g)
n mean s.d. n mean s.d.
Ligurian Sea 14 18.38 44.39 14 61.93 124.26
Sardinian Sea 9 23.42 32.46 9 40.30 41.55
Microplastics
(Items/m3)
0-0.1
0.11-1
1.01-5
5.01-10
MEHP concentration in stranded fin whales (n=5)
SPECIES TISSUE Mean MEHP (ng/g)
Balaenoptera physalus Blubber 57.97
MPM4
MPM14 MPM15
MPM16
MPM3
MPM6
MPM5
MPM8
MPM7
MPM9
MPM10
MPM12
MPM13
MPM11
Ligurian Sea
LIGURIA
ab
100 Km
10 Km
10 Km
Fig. 1. (a) Microplastic particles in superficial neustonic/planktonic samples (items/m
3
) collected in the Pelagos Sanctuary (Ligurian Sea and Sardinian Sea) and mean DEPH
and MEPH concentrations (ng/g). Geographical coordinates of sampling sites are reported in Table 2 of Supplementary data. (b) DEHP concentrations (ng/g) in blubber
samples of five stranded fin whales collected along the Italian coasts during the period July 2007–June 2011 in five different locations.
Table 1
Microplastic particles in superficial neustonic/planktonic samples (items/m
3
) collected in the Pelagos Sanctuary, zooplankton abundance (ind/m
3
), DEPH and MEPH
concentrations (ng/g f.w.), mean values ± S.D. (see Fig. 1 for sampling sites).
Sample Items/m
3
Zooplankton abundance (ind/m
3
) DEHP (ng/g) MEHP (ng/g)
Ligurian Sea
MPM3 0.00 403.96 5.00 1.00
MPM4 0.10 167.78 5.00 55.20
MPM5 0.10 23.45 10.00 1.00
MPM6 0.00 43.67 172.41 3,12
MPM7 0.00 36.77 5.00 5.75
MPM8 0.05 204.71 5.00 454.07
MPM9 0.00 4275.51 5.00 1.00
MPM10 0.00 193.15 5.00 2.00
MPM11 1.35 377.49 5.00 37.64
MPM12 0.50 496.35 5.00 4.87
MPM13 0.33 6147.00 10.00 1.00
MPM14 9.67 4253.33 10.00 188.94
MPM15 0.04 179.51 10.00 25.68
MPM16 0.95 4645.71 5.00 85.78
Mean 0.94 ± 2.55 1532.03 18.38 ± 44.39 61.93 ± 124.26
Sardinian Sea
MPM17 0.00 82.74 76,02 19.83
MPM18 0.83 27.07 10.00 1.00
MPM19 0.11 744.54 10.00 11.30
MPM20 0.00 668.66 5.00 107.11
MPM21 0.03 90.19 10.00 35.56
MPM23 0.24 102.73 5.00 1.00
MPM24 0.00 523.27 84.81 109.93
MPM25 0.00 15000.00 5.00 30.64
MPM26 0.00 3919.72 5.00 46.34
Mean 0.13 ± 0.27 2350.99 23.42 ± 32.46 40.30 ± 41.55
Total Mean 0.62 ± 2.00 1852.49 20.36 ± 39.42 53.47 ± 99.34
M.C. Fossi et al. / Marine Pollution Bulletin xxx (2012) xxx–xxx 3
Please cite this article in press as: Fossi, M.C., et al. Are baleen whales exposed to the threat of microplastics? A case study of the Mediterranean fin whale
(Balaenoptera physalus). Mar. Pollut. Bull. (2012), http://dx.doi.org/10.1016/j.marpolbul.2012.08.013
and MEHP were extracted from blubber (1 g), and phthalate con-
centrations were measured with the method described above.
3. Results
Of the 23 surface neustonic/planktonic samples, 13 contained
plastic particles (Table 1,Fig. 1a). The highest microplastic abun-
dance (9.67 items/m
3
, equivalent to 4.83 items/m
2
) was found in
a sample collected near the Portofino MPA (Ligurian Sea). Large
amounts of plastic particles were detected in the surface neuston-
ic/planktonic samples collected in the Pelagos Sanctuary areas
investigated (mean value 0.62 items/m
3
). The amounts of plastic
particles were approximately seven times higher in the samples
from the Ligurian Sea (mean value 0.94 items/m
3
) than in the sam-
ples from the Sardinian Sea (mean value 0.13 items/m
3
)(Table 1).
Plastic particles were not found in the three water column samples
(Table 2). The planktonic species were taxonomically determined,
and the results are shown in Table 1 of Supplementary data.
High concentrations of the phthalates MEHP and DEHP were de-
tected for the first time in the surface neustonic/planktonic sam-
ples collected in the Pelagos Sanctuary areas. The values of MEHP
were approximately 1.5 times higher in the samples from the Lig-
urian Sea than in the samples from the Sardinian Sea. Lower con-
centrations of MEHP were detected in the 3 water column
samples than in the surface samples (Table 2).
The presence of harmful chemicals in Mediterranean fin whales,
associated with the potential intake of plastic derivatives by water
filtering and plankton ingestion, was demonstrated for the first
time by the results of this study, which documented the presence
of relevant concentrations of MEHP in the blubber of four out of
five stranded fin whales (Fig. 1b). MEHP is a marker for exposure
to DEHP, whereas DEHP was never detected in the samples. It is
not surprising that DEHP was not detected in these samples, as it
is well known that the DEHP is rapidly metabolized to MEHP, its
primary metabolite (Latini et al., 2004). The preliminary data ob-
tained by the current study suggest that phthalates can serve as
a tracer of the intake of microplastics by fin whales resulting from
the ingestion of micro-litter and plankton.
4. Discussion
The present study, following the recent publication by Collignon
et al. (2012), provides an initial insight into microplastic pollution
in the Mediterranean Sea by reporting the concentrations and spa-
tial distribution of microplastics in the area of Pelagos Sanctuary.
We emphasize that the mean abundance of microplastics esti-
mated in this study is of the same order of magnitude as that found
for the North Pacific Gyre (Collignon et al., 2012), suggesting the
high level of this emerging threat in the only pelagic MPA of the
Mediterranean Sea.
The Pelagos Sanctuary for Mediterranean Marine Mammals is a
marine protected area of approximately 90,000 km
2
in the north-
western Mediterranean Sea. A remarkable cetacean fauna consist-
ing of 8 species, including the baleen whale B. physalus, coexists in
the Sanctuary with very high levels of human pressure. Plastic
from coastal tourism, recreational and commercial fishing, marine
vessels and marine industries can directly enter the marine envi-
ronment and pose a risk to biota both as macroplastics and, follow-
ing long-term degradation, as microplastics. Within the Pelagos
Sanctuary, the Portofino MPA showed the highest values of micro-
plastic items/m
3
. This area was also confirmed as a ‘‘hot spot’’ for
microplastics by Collignon et al. (2012). These results serve to fo-
cus particular attention on the conservation status of an area with
a high level of exploitation by tourists and on the balance between
conservation measures and management.
Previously, very few studies have addressed the impact of
microplastics on filter-feeding organisms or other planktivorous
animals. No previous studies have assessed the potential impact
of microplastics on large filter-feeding organisms, such as baleen
whales.
At the lowest level of the food web, the great abundance of
microplastics in the photic zone could both interfere with and be
a severe threat to plankton viability. Microplastic debris has been
found in the gastrointestinal tracts of several planktivorous fishes
(Myctophidae,Stomiidae and Scomberesocidae) in the North Pacific
Gyre (Boerger et al., 2010). In the Mediterranean Sea, during the
survey recently carried out by Collignon et al. (2012), plastic mi-
cro-debris was found in the stomachs of myctophids (Myctophum
punctatum). Moreover, several studies report the ingestion of plas-
tic debris of different sizes, colors and shapes by both epibentho-
phagous and hyperbenthophagous fish species (Ariidae,Scianidae)
inhabiting a demersal estuarine environment in the tropical Wes-
tern South Atlantic (Costa et al., 2011; Possatto et al., 2011; Dantas
et al., 2012). The occurrence of interactions between several spe-
cies of marine mammals and marine debris (Williams et al.,
2011) and of plastic ingestion in Franciscana dolphins were also re-
cently reported (Denuncio et al., 2011). However, the physiological
and toxicological effects of plastic ingestion by filter-feeding
organisms are poorly investigated and understood, as are the
implications of plastic ingestion occurring through the food chain.
Marine plastics have been found to adsorb and transport chem-
icals, including high concentrations of organochlorines such as
polychlorinated biphenyls (PCBs), dichlorodiphenyl trichloroeth-
ane (DDT) and PAHs (Teuten et al., 2007). After the ingestion of
plastics by an organism, the presence of digestive surfactants is
known to increase the bioavailability of these compounds sorbed
to plastics (Voparil and Mayer, 2000) by markedly increasing the
desorption rate of plastics compared with that found in sea water
(Teuten et al., 2007). Due to the large surface-area-to-volume ratio
of microplastics, marine organisms may be particularly at risk of
exposure to leached additives after microplastics are ingested.
Such additives may interfere with biologically important pro-
cesses, potentially resulting in endocrine disruption (Barnes
et al., 2009; Lithner et al., 2009, 2011). In this context, it is known
that commonly used additives, such as brominated flame retar-
dants, phthalates and the constituent monomer bisphenol A, can
act as endocrine-disrupting chemicals because they can mimic,
compete with or disrupt the synthesis of endogenous hormones
(Talsness et al., 2009). In particular, phthalates have been associ-
ated with a range of molecular, cellular and organ effects in aquatic
invertebrates and fish (Oehlmann et al., 2009). Bisphenol A is both
Table 2
Microplastic particles in water column samples (items/m
3
) collected in the Pelagos Sanctuary, zooplankton abundance (ind/m
3
), DEPH and MEPH concentrations (ng/g f.w.), mean
values ± S.D (see Fig. 1 for sampling sites).
Sample Items/m
3
Zooplankton abundance (ind/m
3
) DEHP (ng/g) MEHP (ng/g)
MPP3 0.00 49.71 5.00 1.00
MPP10 0.00 1266.05 5.00 4.32
MPP22 0.00 864.88 5.00 1.00
Mean 0.00 726.88 5.00 ± 0.00 2.11 ± 1.92
4M.C. Fossi et al. / Marine Pollution Bulletin xxx (2012) xxx–xxx
Please cite this article in press as: Fossi, M.C., et al. Are baleen whales exposed to the threat of microplastics? A case study of the Mediterranean fin whale
(Balaenoptera physalus). Mar. Pollut. Bull. (2012), http://dx.doi.org/10.1016/j.marpolbul.2012.08.013
an estrogen agonist and an androgen antagonist, and it can differ-
entially affect reproduction and development, depending on its
concentration and the species affected. Nevertheless, Oehlmann
et al. (2009) note that there has been relatively little research into
the chronic effects of long-term exposure to these additives in
aquatic organisms.
The present data represent the first evidence of the potential
impact of the most abundant plastic derivatives (phthalates) in a
baleen whale, the second-largest filter feeder in the world: the
Mediterranean fin whale. The fin whale is a cosmopolitan cetacean.
It is found in the largest water masses of the world, from the equa-
tor to the polar regions. Despite its cosmopolitan distribution, it is
classified as Endangered on the IUCN Red List. In general, rorqual
feeding has been described as the largest biomechanical event that
has ever existed on Earth (Croll and Tershy, 2002). Fin whales cap-
ture food by initially swimming rapidly toward a school of prey
and then decelerating while opening the mouth to gulp vast quan-
tities of water and schooling prey. Fin and blue whales foraging on
krill off the coast concentrate their foraging effort on dense aggre-
gations of krill (150–300 m) in the water column during the day
and feed near the surface at night (Croll et al., 2005).
It is well known that the fin whale in the Mediterranean Sea
feeds preferentially on the planktonic euphausiid Meganyctiphanes
norvegica. Nevertheless, depending on the area and the season, the
whale feeds on a wide spectrum of marine organisms, including
copepods, other euphausiid species (e.g., Thysanoessa inermis,
Calanus finmarchicus,Euphausia krohni) and small schooling fish
(Orsi Relini and Giordano, 1992; Relini et al., 1992; Notarbartolo
di Sciara et al., 2003). With each mouthful, a fin whale can trap
approximately 70,000 l of water. For this reason, a whale could risk
ingesting a great amount of microplastic debris, both directly from
the water and indirectly from the plankton (during both surface
feeding and deeper feeding activity). After microplastics are in-
gested, a fin whale may be exposed directly to leached additives,
such as polybrominated diphenyl ethers, phthalates and bisphen-
olA and their potential toxicological effects.
Preliminary data on MEHP in 5 samples of Euphausia krohni col-
lected in the Sicilian Channel reported high concentrations of this
contaminant ranging from 8.35 to 51.14 ng/g. These results sug-
gested that plastic derivatives also occur in planktonic species
inhabiting the water column (unpublished data, Guerranti per-
sonal communication).
In view of the presence of microplastics in the Mediterranean
environment, the detection of plastic additives in the blubber of
fin whales and the long lifespan of the species, fin whales appear
to be chronically exposed to persistent and emerging contaminants
as a result of microplastic ingestion. In this context, the prelimin-
ary observations presented in this paper suggest that phthalates
can serve as a tracer for the intake of microplastics in micro-litter
and in plankton by fin whales. These observations represent a
warning that the endangered Mediterranean population of this ba-
leen whale is exposed to endocrine disruptors such as MEHP. The
results of this study are consistent with the evidence previously re-
ported by Fossi et al. (2010) of an early warning signal of endocrine
interference furnished by the up-regulation of the estrogen recep-
tor alpha gene detected in skin biopsies of male Mediterranean fin
whales compared with fin whales from the Sea of Cortez (Mexico).
This ‘‘undesirable biological effect’’ (in agreement with the descrip-
tion of the concept of biomarkers in Descriptor 8 of the Marine
Strategy Framework Directive) can suggest that the Mediterranean
population is exposed to a mixture of persistent and emerging
contaminants, such as endocrine disruptors, that may impair the
population viability of this already endangered species.
In this context, surveys covering much of the western Mediter-
ranean basin have estimated the fin whale population to be 3.583
individuals (Forcada et al., 1996), 901 of which inhabit the
Corsican-Ligurian-Provencal basin (Forcada et al., 1995). However,
according to more recent data on the Pelagos Sanctuary, the
estimated population has decreased markedly (approximately by
a factor of six) in the past 20 years (Panigada et al., 2011) raising
particular concerns about the status of this species.
In conclusion, the present data represent the first evidence of
the potential impact of plastic additives (phthalates) in baleen
whales. These results underscore the importance of future research
on the detection of the toxicological impact of micro-plastics in fil-
ter-feeding species such as mysticete cetaceans, the basking shark
and the devil ray. The results also underscore the potential use of
these species in the implementation of Descriptor 10 (marine lit-
ter) in the EU Marine Strategy Framework Directive as indicators
of the presence and impact of micro-litter in the pelagic
environment.
Acknowledgments
This project was supported by the Italian Ministry of Environ-
ment, Territory and Sea (prot n.39752/III-17). We thank Dr. Silvia
Maltese, Dr. Matteo Baini, Dr. Tommaso Campani, Dr. Ilaria Caliani
and Dr. Davide Bedocchi for their help during sampling activities.
We thank the Mediterranean Marine Mammals Tissue Bank,
Department of Experimental Veterinary Science (University of Pad-
ua, IT) for their collaboration in the sampling of stranded fin
whales.
Appendix A. Supplementary data
Supplementary data associated with this article can be found, in
the online version, at http://dx.doi.org/10.1016/j.marpolbul.2012.
08.013.
References
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. B
364 (1526), 1985–1998.
Barron, M.G., Schultz, I.R., Hayton, W.L., 1989. Presystemic branchial metabolism
limits di-2-ethylhexyl phthalate accumulation in fish. Toxicol. Appl. Pharmacol.
98, 49–57.
Boerger, C., Lattin, G., Moore, S.L., Moore, C.J., 2010. Plastic ingestion by
planktivorous fishes in the North Pacific Central Gyre. Mar. Pollut. Bull. 60
(12), 2275–2278.
Borch, J., Axelstad, M., Vinggaard, A.M., Dalgaard, M., 2006. Diisobutyl phthalate has
comparable anti-androgenic effects to di-n-butyl phthalate in fetal rat testis.
Toxicol. Lett. 163, 183–190.
Collignon, A., Hecq, J.H., Galgani, F., Voisin, P., Collard, F., Goffart, A., 2012. Neustonic
microplastic and zooplankton in the North Western Mediterranean Sea. Mar.
Pollut. Bull. 64, 861–864.
Costa, M.F., Silva-Cavalcanti, J.S., Barbosa, C.C., Portugal, J.L., Barleta, M., 2011.
Plastics buried in the inter-tidal plain of a tropical estaurine eco system. J. Coast.
Res. (SI 64), 339–343.
Croll, D.A., Tershy, B.R., 2002. Filter feeding. In: Perrin, W.F., Wursig, B., Thewissen,
J.G.M. (Eds.), Encyclopedia of Marine Mammals. Academic Press, San Diego, pp.
428–432.
Croll, D.A., Marinovic, B., Benson, S., Chavez, F.P., Black, N., Ternullo, R., Tershy, B.R.,
2005. From wind to whales: trophic links in a coastal upwelling system. Mar.
Ecol. Prog. Ser. 289, 117–130.
Dantas, D.V., Barleta, M., Ferreira da Costa, M., 2012. The seasonal and spatial
patterns of ingestion of polyfilamnt nylon fragments by estuarine drums
(Scianidae). Environ. Sci. Pollut. Res. 19, 600–606.
Denuncio, P., Bastida, R., Dassis, M., Giardino, G., Gerpe, M., Rodriguez, D., 2011.
Plastic ingestion in Franciscana dolphins, Pontoporia blainvillei (Gervais adn
d’Orbigny, 1844), from Argentina. Mar. Pollut. Bull. 62, 1836–1841.
Derraik, J.G.B., 2002. The pollution of the marine environment by plastic debris: a
review. Mar. Pollut. Bull. 44, 842–852.
Forcada, J., Notarbartolo di Sciara, G., Fabbri, F., 1995. Abundance of fin whales and
striped dolphins summering in the Corso Ligurian basin. Mammalia 59, 127–
140.
Forcada, J., Agiolar, A., Hammond, P., Pastor, X., Aguilar, R., 1996. Distribution
abundance of fin whales (Balaenoptera physalus) in the western Mediterranean
Sea during the summer. J. Zool. 238, 23–24.
Fossi, M.C., Urban, J., Casini, S., Maltese, S., Spinsanti, G., Panti, C., Porcelloni, S.,
Panigada, S., Lauriano, G., Niño-Torres, C., Rojas-Bracho, L., Jimenez, B., Muñoz-
M.C. Fossi et al. / Marine Pollution Bulletin xxx (2012) xxx–xxx 5
Please cite this article in press as: Fossi, M.C., et al. Are baleen whales exposed to the threat of microplastics? A case study of the Mediterranean fin whale
(Balaenoptera physalus). Mar. Pollut. Bull. (2012), http://dx.doi.org/10.1016/j.marpolbul.2012.08.013
Arnanz, Marsili, L., . A multi-trial diagnostic tool in fin whale (Balaenoptera
physalus) skin biopsies of the Pelagos Sanctuary (Mediterranean Sea) and the
Gulf of California (Mexico). Mar. Environ. Res. 69 (1), S17–S20.
Guerranti, C., Sbordoni, I., Fanello, E.L., Borghini, F., Corsi, I., Focardi, S.E., 2012.
Levels of phthalates in human milk samples from central Italy. Microchem. J.,
http://dx.doi.org/10.1016/j.microc.2012.06.014, in press.
Hidalgo-Ruz, V., Gutow, L., Thompson, R.C., Thiel, M., 2012. Microplastics in the
marine environment: a review of the methods used for identification and
quantification. Environ. Sci. Technol. 46 (6), 3060–3075.
Latini, G., 2005. Monitoring phthalate exposure in humans. Clin. Chim. Acta 361 (1),
20–29.
Latini, G., De Felice, C., Verrotti, A., 2004. Plasticizers, infant nutrition and
reproductive health. Reprod. Toxicol. 19, 27–33.
Latini, G., Wittassek, M., Del Vecchio, A., Presta, G., De Felice, C., Angerer, J., 2009.
Lactational exposure to phthalates in Southern Italy. Environ. Int. 35, 236–239.
Lithner, D., Damberg, J., Dave, G., Larsson, A., 2009. Leachates from plastic consumer
products – screening for toxicity with Daphniamagna. Chemosphere 74, 1195–
1200.
Lithner, D., Larsson, Å., Dave, G., 2011. Environmental and health hazard ranking
and assessment of plastic polymers based on chemical composition. Sci. Total
Environ. 409, 3309–3324.
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.
Murray, F., Cowie, F.R., 2011. Plastic contamination in the decapod crustacean
Nephrops norvegicus (Linnaeus, 1758). Mar. Pollut. Bull. 62 (6), 1207–1217.
Notarbartolo di Sciara, G., Zanardelli, M., Jahoda, M., Panigada, S., Airoldi, S., 2003.
The fin whale Balaenoptera physalus (L. 1758) in the Mediterranean Sea.
Mammal Rev. 33 (2), 105–150.
Oehlmann, J.R., Schulte-Oehlmann, U., Kloas, W., Jagnytsch, O., Lutz, I., Kusk, K.O.,
Wollenberger, L., Santos, E.M., Paull, G.C., Van Look, K.J.W., Tyler, C.R., 2009. A
critical analysis of the biological impacts of plasticizers on wildlife. Philos.
Trans. R. Soc. B 364, 2047–2062.
Orsi Relini, L., Giordano, A., 1992. Summer feeding of the fin whale, Balaenoptera
physalus, in the Liguro-Provençal Basin. Eur. Res. Cetaceans 6, 138–141.
Panigada, S., Lauriano, G., Burt, L., Pierantonio, N., Donovan, G., 2011. Monitoring
winter and summer abundance of cetaceans in the Pelagos Sanctuary
(northwestern Mediterranean Sea) through aerial surveys. PLoS One 6 (7),
e22878. http://dx.doi.org/10.1371/journal.pone.0022878.
Possatto, F.E., Barleta, M., Costa, M.F., Ivar do Sul, J.A., Dantas, D.V., 2011. Plastic
debris ingestion by marine catfish: an unexpected fisheries impact. Mar. Pollut.
Bull. 62, 1098–1102.
Relini, G., Orsi Relini, L., Cima, C., Fasciana, C., Fiorentino, F., Palandri, G., Relini, M.,
Tartaglia, M.P., Torchia, G., Zamboni, A., 1992. Macroplancton, Meganyctiphanes
norvegica, and fin whales, Balaenoptera physalus, along some transects in the
Ligurian Sea. Eur. Res. Cetaceans 6, 134–137.
Robards, M.D., Piatt, J.F., Wohl, K.D., 1995. Increasing frequency of plastic particles
ingested by seabirds in the subarctic North Pacific. Mar. Pollut. Bull. 30, 151–
157.
Takatori, S., Kitagawa, Y., Kitagawa, M., Nakazawa, H., Hori, S., 2004. Determination
of di(2-etylhexyl)phthalate and mono(2-etylhexyl)phthalates in human serum
using liquid chromatography–tandem mass spectrometry. J. Chromatogr. B 804,
397–401.
Ryan, P.G., Moore, C.J., Van Franeker, J.A., Moloney, C.L., 2009. Monitoring the
abundance of plastic debris in the marine environment. Philos. Trans. R. Soc. B
364, 1999–2012.
Talsness, C.E., Andrade, A.J.M., Kuriyama, S.N., Taylor, J.A., vom Saal, F.S., 2009.
Components of plastic: experimental studies in animals and relevance for
human health. Philos. Trans. R. Soc. B 364, 2079–2096.
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.
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.
Voparil, I.M., Mayer, L.M., 2000. Dissolution of sedimentary polycyclic aromatic
hydrocarbons into the lugworm’s (Arenicola marina) digestive fluids. Environ.
Sci. Technol. 34, 1221–1228.
Williams, R., Ashe, E., O’Hara, P.D., 2011. Marine mammals and debris in coastal
waters of British Columbia, Canada. Mar. Pollut. Bull. 62, 1303–1316.
6M.C. Fossi et al. / Marine Pollution Bulletin xxx (2012) xxx–xxx
Please cite this article in press as: Fossi, M.C., et al. Are baleen whales exposed to the threat of microplastics? A case study of the Mediterranean fin whale
(Balaenoptera physalus). Mar. Pollut. Bull. (2012), http://dx.doi.org/10.1016/j.marpolbul.2012.08.013
