Science of the Total Environment 650 (2019) 1521–1528

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Science of the Total Environment

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

First assessment of persistent organic pollutant contamination in blubber

of Chilean blue whales from Isla de Chiloé, southern Chile
J. Muñoz-Arnanz a,⁎, A.D. Chirife b, B. Galletti Vernazzani c, E. Cabrera c, M. Sironi d, J. Millán b,
C.R.M. Attard e,f, B. Jiménez a
a
Department of Instrumental Analysis and Environmental Chemistry, Institute of Organic Chemistry, (IQOG-CSIC), Juan de la Cierva 3, Madrid, Spain
b
Facultad de Ciencias de la Vida, Universidad Andres Bello, República 252, Santiago, Chile
c
Centro de Conservación Cetacea (CCC), Casilla 19178 Correo Alonso de Cordoba, Santiago, Chile
d
Instituto de Conservación de Ballenas, O'Higgins 4380, 1429 Buenos Aires, Argentina
e
Molecular Ecology Lab, College of Science and Engineering, Flinders University, GPO Box 2100, Adelaide, South Australia 5001, Australia
f
Cetacean Ecology, Behaviour and Evolution Lab, College of Science and Engineering, Flinders University, GPO Box 2100, Adelaide, South Australia 5001, Australia

H I G H L I G H T S G R A P H I C A L A B S T R A C T

• First data on POPs from Southern

Hemisphere blue whales
• PCBs, most abundant among study POPs
• High contributions of lower substituted
PCB and PBDE congeners
• Marked contribution of BDE-28, never
reported in any cetacean species

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

Article history: Persistent organic pollutants (POPs) were assessed for the first time in blue whales from the South Pacific Ocean.
Received 6 July 2018 Concentrations of polychlorinated biphenyls (PCBs), polybrominated diphenyl ethers (PBDEs), hexachloroben-
Received in revised form 4 September 2018 zene (HCB) and dichlorodiphenyltrichloroethane and its main metabolites (DDTs), were determined in 40 blub-
Accepted 5 September 2018
ber samples from 36 free-ranging individuals and one stranded, dead animal along the coast of southern Chile
Available online 06 September 2018
between 2011 and 2013. PCBs were the most abundant pollutants (2.97–975 ng/g l.w.), followed by DDTs
Editor: D. Barcelo (3.50–537 ng/g l.w.), HCB (nd–77.5 ng/g l.w.) and PBDEs (nd–33.4 ng/g l.w). There was evidence of differences
between sexes, with lower loads in females potentially due to pollutants passing to calves. POP concentrations
Keywords: were higher in specimens sampled in 2013; yet, between-year differences were only statistically significant for
Baleen whales HCB and PBDEs. Lower chlorinated (penta N tetra N tri) and brominated (tetra N tri) congeners were the most
POPs prevalent among PCBs and PBDEs, respectively, mostly in agreement with findings previously reported in blue
Southern Hemisphere and other baleen whales. The present study provides evidence of lower levels of contamination by POPs in east-
PCBs ern South Pacific blue whales in comparison to those reported for the Northern Hemisphere.
PBDEs
© 2018 Published by Elsevier B.V.
DDTs

1. Introduction

It has been long recognized that persistent organic pollutants (POPs)

are threats to public health and ecosystems (Jones and de Voogt, 1999).
⁎ Corresponding author. This lead to the enactment of the Stockholm Convention in 2001 under
E-mail address: [email protected] (J. Muñoz-Arnanz). the United Nations Environment Programme, which seeks to ban and/or

https://doi.org/10.1016/j.scitotenv.2018.09.070
0048-9697/© 2018 Published by Elsevier B.V.
1522 J. Muñoz-Arnanz et al. / Science of the Total Environment 650 (2019) 1521–1528

minimize POP production and use internationally (UNEP, 2001). Aside Particularly, among mysticetes, very little is known concerning POP
from their toxicity, these pollutants are bioaccumulative, resistant to contamination in blue whales (Balaenoptera musculus) despite being
degradation (metabolic or otherwise) and capable of long-range trans- the largest and one of the most emblematic extant inhabitants of the
portation. In consequence, a large number of studies has proven a gen- ocean. The blue whale is a cosmopolitan species whose worldwide cur-
eralized distribution of these chemicals in marine wildlife from all rent numbers are diminished, primarily as consequence of the massive
oceans and depths (Alonso et al., 2014; Burreau et al., 2006; Corsolini hunt carried out during the whaling era. Hence, today it is classified as
et al., 2002; Crain et al., 2009; Fisk et al., 2001; Lukyanova et al., 2014; endangered in the Red List of Threatened Species of the International
Tanabe, 2002; Tanabe et al., 1994; Tolosa et al., 1997). The impact of Union for Conservation of Nature and Natural Resources (IUCN, 2008).
POPs in marine mammal populations is, however, difficult to assess Despite their low trophic level as strict feeders on krill, blue whales
due to the logistics of collecting samples from highly mobile, ocean- may face an important health threat derived from accumulation of
dwelling animals and confounding factors from other cumulative POPs based upon 1) their long lifespan of up to ninety years (Sears and
anthropogenic impacts (Crain et al., 2009; Reijnders et al., 2009). Yet, Perrin, 2009), and 2) the sheer magnitude of bioconcentration processes
studies to date have suggested a link between high levels of POPs such as a result of massive amounts of ingested prey. To date only four studies
as polychlorinated biphenyls (PCBs), polybrominated diphenyl ethers have reported POP concentrations in blue whales, all of them from the
(PBDEs) or organochlorine pesticides (e.g. hexachlorobenzene (HCB) Northern Hemisphere: Gulf of St. Lawrence, Canada (Gauthier et al.,
or dichlorodiphenyltrichloroethane (DDT)), and adverse health effects 1997; Metcalfe et al., 2004), Gulf of California, Mexico (Fossi et al.,
on marine mammals. Specifically, a potential deleterious influence on 2014) and Santa Barbara, USA (Trumble et al., 2013), finding relatively
their immune and endocrine systems, reproduction and offspring survi- high concentrations for some pollutants such as DDTs and PCBs.
vorship rates, and ultimately on population growth has been docu- Three subspecies of blue whales are currently recognized in the
mented (Bossart, 2011; Desforges et al., 2016; Hall et al., 2006; Hunt Southern Hemisphere: the pygmy blue whale (Balaenoptera musculus
et al., 2013; Yordy et al., 2010). For instance, PCBs are thought to have brevicauda) in the sub-Antarctic zone; the Antarctic blue whale (B. m.
caused higher susceptibility and played an important role in the intermedia), which summers in the Antarctic Zone (Rice, 1998), and
development of the epizootic infection by a morbillivirus involved in a an unnamed subspecies, the Chilean blue whale off Chile that is inter-
massive striped dolphin (Stenella coeruleoalba) die-off in the mediate in size between the other two. This unnamed subspecies has
Mediterranean Sea (Aguilar and Borrell, 1994; Aguilar and Raga, 1993; been accepted by the Taxonomy Committee of the Society for Marine
Kannan et al., 1993). Mammalogy (SMM, 2018), considering morphometric (Branch et al.,
Among cetaceans, that is, mysticetes (baleen whales) and 2007a), acoustic (McDonald et al., 2006) and genetic (LeDuc et al.,
odontocetes (dolphins, porpoises and toothed whales), the highest 2007; Torres-Florez et al., 2014) evidences.
POP concentrations have been described in odontocetes as consequence Isla Grande de Chiloé, in southern Chile, is known as an important
of being apex predators in marine food webs. A paradigmatic example is austral summer and autumn feeding ground for this population with
that of the Orca (Orcinus orca), for which levels reported in different among the highest sighting rates in the Southern Hemisphere (Branch
studies make the species the most contaminated with PCBs on Earth et al., 2007b; Galletti Vernazzani et al., 2012). Capture-recapture open
(Jepson and Law, 2016). Concern about these heightened PCB concen- population models estimated that ~570–760 whales are feeding season-
trations is ongoing as a possible cause for current declines in marine ally in this region with high inter-annual return rates. This suggests the
apex predators globally (Jepson and Law, 2016; Stuart-Smith and number of whales using this feeding ground is relatively small and show
Jepson, 2017). Concurrently, monitoring of POPs in cetaceans continues a high degree of site-fidelity to Isla de Chiloé (Galletti Vernazzani et al.,
to increase, with most studies reporting on samples from stranded spec- 2017).
imens rather than free-ranging animals due to the undeniable complex- The main objective of this work was to gauge for the first time -to the
ity and associated cost with sampling free-ranging cetaceans (García- best of our knowledge- the degree of contamination by PCBs, HCB, DDTs
Alvarez et al., 2014). In many cases the blubber, which represents the and PBDEs in Chilean blue whales. This sought to inform about the
largest fat compartment in cetacean species, is analyzed. This tissue ac- health status of this recovering subspecies, pave the way for future stud-
counts for 70–95% of the whole body burden of lipophilic pollutants ies of blue whales in the Southern Hemisphere, and showcase the po-
such as most POPs (Reijnders et al., 2009; Yordy et al., 2010). Moreover, tential for baleen whales to act as sentinel organisms of ocean
bubbler biopsies can be obtained in a non-lethal and minimally invasive contamination.
way from free-ranging animals by means of biopsy darts or poles
(Bilgmann et al., 2007; Krützen et al., 2002), which becomes a strategy 2. Material and methods
of the utmost importance for hazard assessment in endangered species
of marine mammals (Fossi et al., 2014; Hunt et al., 2013; Marsili et al., 2.1. Sampling
2000).
To date, most of the available data about POPs in cetaceans originate Forty-one integument blubber samples of blue whales were ob-
from environmental surveys or monitoring activities focused on both tained in March 2011 (n = 13), 2012 (n = 3) and 2013 (n = 25).
the Northern Hemisphere (mostly from North Atlantic and European Forty samples were biopsies collected from free-ranging specimens
waters), and different species of toothed whales. On the other hand, sampled in Chilean waters (41.8300–42.3364S, 73.7679–74.4747W,
there is a paucity of studies on POPs in the Southern Hemisphere and Fig. 1). One sample was obtained from a dead animal stranded on the
in baleen whales in general. It is commonly assumed that mysticetes coast of southern Chile (41.5584S, 73.7679W). Marine surveys were
face a lower chemical risk in comparison to odontocetes derived from conducted within 12 km from the coastline, on board the 7 m Alfaguara
their lower trophic level; and thereby, from a reduced biomagnification research vessel. The primary/main survey area was off northwestern
of POPs, among other pollutants (Bengtson Nash et al., 2013). Nonethe- Isla de Chiloé (Fig. 1) and data collected during marine surveys included
less, baleen whales often experience prolonged fasting periods owing to photo-identification, biopsy samples, group composition, behavior,
reproduction, breeding and migration, when they rely on their lipid weather and sea conditions, associated fauna and sea surface tempera-
storage as capital breeders. It is during these periods when an important tures (SST). The position of a whale or group of whales was determined
mobilization of their lipid resources takes place along with their previ- using GPS.
ously sequestered lipophilic pollutants. In consequence, these phases Biopsy samples were collected at a distance of approximately 20 m
of heightened fat mobilization represent times of increased chemical using biopsy darts (5 mm diameter and 4 cm long) attached to alumi-
risk for these species, including their offspring (Bengtson Nash et al., num and carbon fiber arrows (Easton Superlite A/C/C), fired with a
2013; Desforges et al., 2016; Polischuk et al., 2002). crossbow. Biopsies were obtained from the flank of the whales anterior
 J. Muñoz-Arnanz et al. / Science of the Total Environment 650 (2019) 1521–1528 1523

Isla
Grande
de Chiloé

Fig. 1. Map of the sampling area.

to the dorsal fin. After collecting the floating dart, each sample was care- Arnanz et al. (2016) with some modifications. Briefly, lyophilized blub-
fully extracted from the tip with clean forceps. Skin was removed from ber samples were homogenized with 5 g of anhydrous Na2SO4, spiked
the sample and stored separately in 20% dimethyl sulfoxide saturated with a suite of 13C12-PCBs (2500 pg), 13C12-BDE-138 (3750 pg), 13C12-
with NaCl or 95% ethanol for sex determination, whereas blubber was HCB (5000 pg) and D8-DDTs (5000 pg of o,p′-, p,p′-DDT, and p,p′-
wrapped in acetone rinsed aluminum foil and placed in sterile DDE). Soxhlet extraction was carried out for 24 h using pre-cleaned cel-
Eppendorf tubes, then stored in a cooler with ice packs and subse- lulose thimbles and a mixture of n-hexane:dichloromethane (9:1 v/v).
quently at −20 °C in the laboratory. Ulterior photo ID and genetic anal- Lipid content of each sample was determined gravimetrically. Purifica-
ysis proved that four specimens were double-sampled: three of them tion of extracts was achieved by low pressure chromatography on neu-
twice in 2013 and the fourth in 2011 and again in 2013. tral and acidic silica gel multilayer. Final extracts were evaporated using
a TurboVap® system until ~1 mL, transferred to vials and reduced to in-
2.2. Sex determination cipient dryness under a gentle nitrogen steam. Samples were
reconstituted in a solution of 25 μL of 13C12-PCB-111,170,178, 13C12-
DNA was extracted from the skin tissue following a modified salting- BDE-139 and 13C10-p,p′-DDT in nonane as internal standards for instru-
out protocol (Sunnucks and Hales, 1996). The sex of each specimen was mental analysis. Information about all materials and standards used is
determined by PCR amplification of a fragment of the genes ZFX/ZFY provided in Table S1.
and SRY using primers designed by Aasen and Medrano (1990) and
Fain and LeMay (1995), respectively, and following the method of 2.3.2. Instrumental determination
Gilson et al. (1998). The sex of four animals could not be determined Twenty ortho and mono-ortho PCB congeners (# 28, 52, 95, 101, 105,
due to insufficient quality or quantity of the DNA. 114, 118, 123, 132, 138, 149, 153, 156, 157, 167, 170, 180, 183, 189, 194),
six DDTs (p,p′- and o,p′-DDT, -DDE and -DDD), and HCB were analyzed
2.3. Analysis of POPs by gas chromatography low resolution mass spectrometry (GC-LRMS)
using a 7890N gas chromatograph coupled with a 5975C quadrupole
2.3.1. Sample treatment mass spectrometer (Agilent, Palo Alto, CA, USA) operated in selected
Blubber samples (~200 mg on average) were lyophilized and then ion monitoring mode (SIM) and electronic impact (EI) as ionization
extracted and purified following the procedure detailed in Muñoz- mode. Quantification of the target analytes was based on the isotopic
1524 J. Muñoz-Arnanz et al. / Science of the Total Environment 650 (2019) 1521–1528

dilution technique. Fifteen brominated BDE congeners, from tri- to Table 1

deca-substituted (# 17, 28, 47, 66, 85, 99, 100, 153, 154, 183, 184, 191, Average, median, range, detection frequencies (% N LOQ) of total PCBs, DDTs, HCB and
PBDEs detailed by males (n = 18), females (n = 16), unknown sex (n = 4) and total spec-
196, 197, 209), were analyzed by GC-LRMS using a 6890N gas chro- imens (n = 38).
matograph coupled with a 5975 quadrupole mass spectrometer
(Agilent, Palo Alto, CA, USA) operated in SIM with negative chemical Sex Average Median Range NLOQ
(ng/g l. (ng/g l. (ng/g l. (%)
ionization (NCI). Quantification of PBDEs was based on the internal
w.) w.) w.)
standard (13C12-BDE-139) technique. Full details on each chromato-
PCBs (20 congeners) Male 136 118 8.66–470 100
graphic and MS method can be found in Muñoz-Arnanz et al. (2016)
Female 167 78.5 2.97–975 100
and the Supplementary material. Unknown 136 81 28.7–352 100
Total 149 95.3 2.97–975 100
2.4. QA/QC HCB Male 20.4 15.2 7.84–77.5 100
Female 10.8 11.0 ND–17.0 88
Unknown 27.3 18.8 8.79–63.1 100
Metal and glassware material was thoroughly cleaned (3×) with Total 17.4 12.7 ND–77.5 95
three solvents of decreasing polarity: acetone, dichloromethane and DDTs (6 isomers) Male 49.6 34.6 11.0–196 100
n-hexane. A procedural blank was analyzed within each batch of five Female 16.7 11.9 3.50–54.3 100
samples covering each analytical step. Care was taken to minimize ex- Unknown 170 58.3 28.0–537 100
Total 48.4 26.7 3.50–537 100
posure to UV light throughout the entire analytical procedure. Quantifi-
PBDEs (15 Male 9.48 6.05 1.32–33.4 100
cation was carried out according to the following criteria: (a) ratio congeners) Female 4.00 3.63 ND–14.2 81
between the two monitored ions within ±15% of the theoretical Unknown 12.9 11.7 1.06–26.1 75
value, and (b) limits of quantification (LOQs) corresponding to S/N of Total 7.69 4.95 ND–33.4 90
10. Quantifications based on the isotopic dilution technique were inher-
ently recovery corrected and when quantifiable levels of a given analyte
were found in a procedural blank, these were subtracted from the corre-
sponding batch of samples. Calibration curves (ten points from 1 to the measured contamination in a comparative way with closely re-
1000 pg/μL for PCBs, DDTs and HCB and seven points from 1 to lated species. The very few data available for blue whales on the
250 pg/μL for PBDEs) were daily checked. Satisfactory analyses (n = same POPs are shown in Table 2. Any comparison between data ob-
3) of the certified standard reference material SRM 1945 (“Organics in tained in this study with those reported in the literature must be
Whale Blubber”, NIST) were achieved. Further information pertaining exerted with caution given the important differences in the number
QA/QC including surrogate recoveries, reference material values and of sampled specimens, sampling techniques (biopsies vs. stranded an-
limits of detection of the target compounds is provided in Tables S2 imals), years and geographical areas. However, blue whales from
and S3. Chilean waters showed markedly lower levels –of at least one order
of magnitude- for all study pollutants compared to other studies. The
2.5. Data analysis greatest difference was in the case of DDTs, for which concentrations
found in Chilean specimens were up to two orders of magnitude
All concentrations are given in ng/g on lipid weight (l.w.) basis. lower than those reported in blue whales from Canada and Mexico
Samples with concentrations below quantification limits were (Table 2). In consequence, the present study provides further evidence
assigned a value of zero and regarded as not detected (ND). Statistical for a lower degree of contamination by POPs in the eastern South
analyses were carried out with SigmaPlot for Windows version 12.0 Pacific compared to the Canadian North Atlantic in the 90s and to the
(Systat Software Inc., CA, USA). Since data were not normally distrib- Gulf of California in recent years. This scenario is also in agreement
uted (Shapiro–Wilk test, p b 0.001), they were log10-transformed in with the reduced degree of contamination found by numerous studies
order to meet normality. Differences in pollutant loads between in marine mammals from South Pacific waters relative to those from
years and sexes were studied by means of t-tests. Pearson's Northern Hemisphere regions (Aguilar et al., 2002; Alonso et al.,
correlations were used to explore relationships among the four groups 2014; Bengtson Nash et al., 2013; Connell et al., 1999; O'Shea and
of pollutants. The minimum significance level was set at α = 0.05. Brownell, 1994).
Both samples from the four specimens sampled twice were analyzed. Interestingly, lower concentrations were described for PCBs and
In the case of the three specimens sampled two times in March 2013, PBDEs in the earplug cerumen from a single specimen sampled in
average concentration values were obtained and used in statistical California waters, while higher values were found for DDTs (Table 2).
analyses. In the case of the specimen sampled in 2011 and 2013, The authors described how the total POP burden in blubber equaled
concentration values from each year were kept and regarded as about 90% of the total accumulative burden in the earplug of that partic-
different specimens. ular specimen (Trumble et al., 2013). Nonetheless, the value of this
comparison is limited and subjected to the fact of being only one animal
3. Results and discussion and having no knowledge about the differential transfer and accumula-
tion of each specific pollutant in blubber vs. cerumen. Additionally, data
3.1. Pollutant concentrations are provided in ng/g cerumen basis instead of ng/g lipid weight basis.
When comparing with data from other baleen whale species from
All target POPs were detected in the analyzed blubber samples. The other Southern Hemisphere geographical areas caution is, again, man-
average, median and range of concentration values are summarized in datory. However, blubber data from both southern right whales
Table 1. It is noteworthy highlighting the broad range of values found, (SRWs, Eubalaena australis) sampled in Argentinian waters (Torres
especially for PCBs and DDTs, which is likely to be attributed to et al., 2015) and humpback whales (HWs, Megaptera novaeangliae)
differences in age, sex and reproductive status of the sampled speci- from Australian waters (Bengtson Nash et al., 2013) seem to be loosely
mens. The relative abundance of the study contaminants followed comparable in magnitude for the target compounds (Table 2). Based on
the order PCBs N DDTs N HCB N PBDEs. This pattern is similar to what the similar length of their food chains, as bioindicator organisms, the
has been described in liver of penguins (Spheniscus magellanicus) variability for each species in the relative abundance of one or another
from south-central Chile (Baldassin et al., 2016); yet, the lack of type of pollutants (PCBs N DDTs in SRWs and HCB N DDTs N PCBs in
studies on POPs in blue whales, or most species of cetaceans from HWs) is likely a direct reflection of the contamination patterns in their
the South Pacific Ocean for that matter, makes it challenging to analyze different feeding grounds.
 J. Muñoz-Arnanz et al. / Science of the Total Environment 650 (2019) 1521–1528 1525

Table 2
Average reported concentrations in the literature for PCBs, DDTs, HCB and PBDEs in blubber samples and earplug cerumen from blue, humpback and southern right whales.

Samples Species PCBs HCB DDTs PBDEs Sampling area & year Type of blubber Reference
(ng/g l.w.) (ng/g l.w.) (ng/g l.w.) (ng/g l.w.) sample

Males (n = 18) Balaenoptera 136 20.4 49.6 9.48 Southern Chile Biopsy This study
Females (n = 16) musculus 167 10.8 16.7 4.00 2011–2013 (1 stranding)
Unknown (n = 4) 136 27.3 170 12.9
Unknown sex (n = 3) Balaenoptera 2220 125 3130 – Gulf of St. Lawrence (Canada) Stranding Gauthier et al. (1997)
musculus 1992
Males (n = 38) Balaenoptera 2020 226 3420 – Gulf of St. Lawrence (Canada) Biopsy Metcalfe et al. (2004)
Females (n = 27) musculus 1220 90.0 1350 – 1992–1997
Males (n = 3) Balaenoptera 4910 – 3930 32.9 Gulf of California (Mexico) Biopsy Fossi et al. (2014)
Females (n = 3) musculus 2550 – 902 19.7 2010
Male (n = 1)a Balaenoptera 5.9–30 – 120–830 0.19–5.9 Santa Barbara (USA) Stranding Trumble et al. (2013)
musculus 2007 (earplug cerumen)
Males (n = unknown) Megaptera 18.0 91 51.0 – Moreton Bay Marine Park Biopsy Bengtson Nash et al.
novaeangliae Australia (2013)
2008–2011
Males (n = 15)b Eubalaena australis Península Valdés Stranding Torres et al. (2015)
Females (n = 18) 7.5 – 5.75 – Argentina
Unknown (n = 2) 2003–2011
a
Concentration given as a range of ng/g d.w. (cerumen basis) along ~25 cm earplug cerumen.
b
Average concentration for the whole collection of samples in ng/g w.w.

Among the scarce known data on PBDEs in blubber from Pacific congeners, notably penta-chlorinated PCB-95 and -101. Important
baleen whales to date are those reported in stranded juvenile HWs contributions (5–10%) were also found for congeners 153 N 52 N 28
in Hawaiian islands, for which a median level of 7.05 ng/g l.w. and N 149 N 138–132. This is somewhat similar to that described by
range 2.08–39.2 ng/g l.w. were found (Bachman et al., 2014). Interest-
ingly, these values are remarkably similar to those from southern 3.5
Chile blue whales, and contrast with the rest of target pollutants, A
found in these same HWs at greater levels. Notably, HCB median 3.0
concentrations (115 ng/g l.w.) and range (167–336 ng/g l.w.) were * * *
log(concentration [ng/g l.w.])

one order of magnitude higher in HWs, which mostly reflects the 2.5 p=0.004 p<0.001 p=0.002
heightened degree of contamination in their North Pacific feeding
2.0
grounds. Nevertheless, it is plausible that differences in species,
m m
specimen's age and sampling techniques could play an important f
1.5
role confounding direct comparisons among all contaminant families, m
f
as it might be the case of PBDEs. 1.0 m
f
Statistically significant sex differences were found (t-test, p b 0.05)
among contaminant concentrations for all groups of pollutants save 0.5 f
for PCBs (Fig. 2A), with males exhibiting the highest burdens. Lower
loads in females were expected owing to the pollutant transfer taking 0.0
place from mothers to calves during pregnancy and lactation periods
(Aguilar et al., 1999; Tanabe et al., 1994). It is worth noting, however,
how PCB concentrations -the most prevalent group among the study PCBs HCB DDTs PBDEs
pollutants- were not significantly higher in males, and for which there
is no clear explanation. When contrasting 2011 against 2013 –the only 3.5
two years with a large enough sample size for a valid comparison- a B
common pattern of greater concentration in 2013 was found for all 3.0
groups of pollutants (Fig. 2B). Nonetheless, these differences were
log (concentration [ng/g l.w.])

only statistically significant in the case of HCB and PBDEs. Relationships 2.5
* *
among the four groups of pollutants were explored by means of p=0.002 p<0.001
2.0
Pearson's correlations (Table 3), finding positive and statistically signif- 2013
icant (p b 0.05) correlations among HCB, DDTs and PBDEs. On the con- 2011 2013
1.5 2011
trary, PCBs were only weakly and positively correlated with DDTs (p 2013
= 0.020) and marginally with PBDEs (p = 0.052). Contamination of
1.0 2011 2013
the marine media by POPs reflects inputs from both local sources and
long-range transportation mechanisms. Thus, the different behavior 0.5
found for PCBs in relation to sex and sampling years in comparison to 2011
the rest of target pollutants, together with its lower degree of correla- 0.0
tion to all of them, might highlight the existence of specific sources
and/or differential transport mechanisms for PCBs involved in the
Chilean blue whales' body burdens. PCBs HCB DDTs PBDEs

3.2. Pollutant profiles Fig. 2. Box-and-whisker plots of PCB, HCB, DDT and PBDE concentrations by A) sex [males
(m) and females (f)], and B) year (2011 and 2013). Boxes are depicted as first and third
quartiles with the drawn median and whiskers corresponding to 5 and 95% percentiles.
In terms of abundance profiles, the average PCB content (Fig. 3) Statistically significant differences between groups (t-test) are indicated with an asterisk
was mostly dominated (~15%) by lower-medium chlorinated and p-value.
1526 J. Muñoz-Arnanz et al. / Science of the Total Environment 650 (2019) 1521–1528

Table 3 respectively. The heighten decrease of DDT levels in the area along
Pearson correlation results among target contaminants. Correlation coefficients and p with the prevalence of p,p′-DDE among DDTs suggests a likely reduction
values are shown.
in the use and input of this pesticide in the environment accordingly to
Log (HCB) Log (DDTs) Log (PBDEs) its worldwide ban that Chile implemented in 1984 (Henriquez et al.,
Log (PCBs) 0.282 0.376 0.318 2006).
p = 0.086 p = 0.020 p = 0.052 The average PBDE congener profile was noticeably dominated
Log (HCB) 0.649 0.692 by lower brominated congeners, namely, BDE-47 (~42%) followed
p b 0.001 p b 0.001
by BDE-28 (~26%) and important contributions (N10%) from BDE-99
Log (DDTs) 0.489
p = 0.002 and -85 (Fig. 4). In general, these results are congruent with the blue
whale's low trophic level, given that these congeners have been found
prevalent in zooplankton from an Arctic food web (de Wit et al., 2006)
and in Antarctic krill (Chiuchiolo et al., 2004; Corsolini et al., 2006).
Gauthier et al. (1997) in Canadian blue whales, at least in the predomi- The predominance of lower brominated congeners such as BDE-47
nance of PCB-101 (with PCB-95 not analyzed) over hexa- (153,138) and and -99 is in agreement too with what has been reported in Pacific
hepta-chlorinated (180) congeners. Furthermore, penta-chlorinated HWs (Bachman et al., 2014). Conversely, such a marked contribution
PCBs (followed by tri- and tetra-) were found dominant as well by of BDE-28 has never been reported –to the best of our knowledge- in
Torres et al. (2015) in Argentinian SRWs and by Bengtson Nash et al. any cetacean species. It could be the result of biodegradation from
(2013) in Australian HWs. This is interesting since PCBs such as 153, higher brominated congeners or a singular lack of this congener's
118 and 180 are examples of the most recalcitrant PCB congeners and, metabolization and/or elimination in blue whales, which warrants fur-
therefore, generally found as the most abundant owing to their high re- ther research on this issue.
sistance to biodegradation (Borja et al., 2005). However, it is consistent
with surface oceans being enriched in lower chlorinated PCB congeners
(Jurado et al., 2004), and also consistent with the shortness of the baleen 4. Conclusions
whales' food chains. This last fact could account for the absence of clear
biomagnification of higher chlorinated congeners. While the PCB con- By means of a non-lethal and minimally invasive approach such as
tent of krill in the study area was not assessed, the profile with the blubber biopsies, this study has assessed for the first time -to the au-
highest contribution from penta- and tetra-chlorinated congeners is thors' knowledge- the POP burden of blue whales in the Chilean
also in good agreement with that reported in mussels (Perumytilus coast and elsewhere in the Southern Hemisphere. Given the few
purpuratus) from southern Chile (Mendoza et al., 2006). These are existing works reporting chemical contamination on blue whales,
regarded as indicators of pollutants' bioavailability in the water media this study has contributed to mitigate the lack of scientific data on en-
due to their filter feeding behavior and their low level of metabolic ac- vironmental pollution by POPs in both this species and the South Pa-
tivities (Tanabe et al., 2008). cific Ocean as geographical area. Important differences in sampling
For DDTs the relative contribution to the average total content techniques, number and age of specimens, and sampling years were
followed the pattern: p,p′-DDE (~72%) ≫ p,p′-DDD (~15%) N p,p′-DDT acknowledged among previous investigations and this study. None-
(~7%) N o,p′-DDT (5.5%) N o,p′-DDD (0.5%) N o,p′-DDE (not detected). theless, comparisons of PCB, DDT, HCB and PBDE levels against pub-
The relatively high abundance of p,p′-DDD is in line with what has lished data on blubber from Northern Hemisphere blue whales
been previously observed in blue whales (Gauthier et al., 1997; clearly suggested a lower degree of contamination by these pollutants
Metcalfe et al., 2004) and other baleen species (Bachman et al., 2014; in the southern Chilean environment. Comparison to other South
Bengtson Nash et al., 2013). In consonance, the average value and Hemisphere phylogenetically close species -baleen- showed variabil-
range for the ratio Rp,p′ (=[p,p′-DDE + p,p′-DDD]/[p,p′-DDT]) was ity in terms of the relative abundance of each pollutant, which in
28.2 and 3.26–375 ng/g l.w., respectively. Values N1 for this ratio are turn, reflected on the type and degree of contamination in geographi-
commonly regarded as indication of legacy inputs of this pesticide cally different feeding grounds. Thus, it seems that despite their legacy
(Muñoz-Arnanz and Jiménez, 2011). In terms of DDT levels in cetaceans nature, PCBs are still lingering in the coast of southern Chile, being
from the study area, it exists only one study reporting concentrations on prevalent among the rest of investigated POPs. The bioaccumulation
blubber from Bryde's whales (Balaenoptera edeni) and fin whales patterns of different pollutant congeners were in agreement with ex-
(Balaenoptera physalus) in Chilean waters (Pantoja et al., 1984), back pectations based on the short food chain in blue whales: there were
in 1983. Both species are phylogenetically close to the blue whale, and high contributions of lower chlorinated PCB congeners and lower bro-
the average DDT levels (∑DDTs) established in that study were minated PBDE congeners. This altogether suggests that blue whales
589 ng/g (fresh weight, n = 2) and 54.4 ng/g (fresh weight, n = 2), and other baleen whales could be valid and useful sentinel organisms
of ocean contamination.

18
congener contribution (%)

16 50
congener contribuon (%)

14
12 40
10
30
8
6 20
4
2 10
0
0
28
52
95
101
105
114
118
123
132
138
149
153
156
157
167
170
180
183
189
194

17 28 47 66 85 99 100 153 154 183 184 191 196 197 209

PCB congener PBDE congener

Fig. 3. Relative contribution of each PCB congener to the total PCB content. Error bars Fig. 4. Relative contribution of each PBDE congener to the total PBDE content. Error bars
represent the standard error. represent the standard error.
 J. Muñoz-Arnanz et al. / Science of the Total Environment 650 (2019) 1521–1528 1527

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