Chemosphere 269 (2021) 129401

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Anthropogenic and natural organohalogen compounds in melon-

headed whales (Peponocephala electra) stranded along the Japanese
coastal waters: Temporal trend analysis using archived samples in the
environmental specimen bank (es-BANK)
Tatsuya Kunisue a, *, Akitoshi Goto a, Tomoya Sunouchi a, Kana Egashira a, Mari Ochiai a,
Tomohiko Isobe b, Yuko Tajima c, Tadasu K. Yamada c, Shinsuke Tanabe a
a
Center for Marine Environmental Studies (CMES), Ehime University, 2-5 Bunkyo-cho, Matsuyama, 790-8577, Japan
b
Center for Environmental Health Sciences, National Institute for Environmental Studies, 16-2 Onogawa, Tsukuba, 305-8506, Japan
c
Department of Zoology, National Museum of Nature and Science, 4-1-1 Amakubo, Tsukuba, 305-0005, Japan

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

Organohalogen levels and temporal

trends were elucidated in melon-
headed whales.

Relatively high concentrations of
DDTs, PCBs, HBCDDs and Q1 were
detected.

CHL, PBDE, HBCDD, MeO-PBDE and
Q1 levels increased significantly since
1982.

The analyses from 2001 to 2015
showed PCB and PBDE congener-
specific temporal trends.

Melon-headed whales might be still
exposed to considerable organo-
halogen levels.

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

Article history: The present study determined recent accumulation levels of polychlorinated biphenyls (PCBs), dichlor-
Received 5 November 2020 odiphenyltrichloroethane and its metabolites (DDTs), hexachlorocyclohexane isomers (HCHs), chlordane
Received in revised form compounds (CHLs), hexachlorobenzene (HCB), polybrominated diphenyl ethers (PBDEs), hex-
17 December 2020
abromocyclododecanes (HBCDDs), polychlorinated diphenyl ethers (PCDEs), methoxylated-PBDEs (MeO-
Accepted 19 December 2020
PBDEs) and 2,3,30 ,4,40 ,5,50 -heptachloro-10 -methyl-1,20 -bipyrrole (Q1) in the blubber of melon-headed
Available online 22 December 2020
whales (Peponocephala electra) stranded along the Japanese coastal waters in 2015 and examined tem-
Handling Editor: Myrto Petreas poral trends of these organohalogen compound (OHC) levels by analyzing blubber samples of this species
archived in the environmental specimen bank which were collected in 1982, 2001, 2002, 2006, 2010 and
Keywords: 2011. The median concentrations in melon-headed whales stranded recently were in the order of
Organohalogen compounds DDTs z PCBs > HBCDDs > Q1 > CHLs > MeO-PBDEs > PBDEs > HCB > HCHs > PCDEs, indicating that
POPs considerable amounts of HBCDDs, in addition to DDTs and PCBs, have been transported to tropical and
Temporal trend subtropical waters of the open ocean and pelagic whale species might be exposed to relatively high levels
Melon-headed whale
of these OHCs. Temporal trend analyses of OHC levels in the blubber of melon-headed whales revealed
Open ocean
significant decrease for anthropogenic OCs such as DDTs, PCBs, HCB, HCHs and PCDEs, and significant

* Corresponding author. Center for Marine Environmental Studies (CMES), Ehime

University, Bunkyo-cho 2-5, Matsuyama, Ehime, 790-8577, Japan.
E-mail address: kunisue.tatsuya.ew@ehime-u.ac.jp (T. Kunisue).

https://doi.org/10.1016/j.chemosphere.2020.129401
0045-6535/© 2020 Elsevier Ltd. All rights reserved.
T. Kunisue, A. Goto, T. Sunouchi et al.
increase for CHLs, PBDEs, HBCDDs, MeO-PBDEs and Q1 since 1982. Besides, the analyses from 2001 to
2015 showed no decreasing trends (unchanged) for some PCB congeners, p,p’-DDE, cis- and trans-non-
achlors, Q1, BDE-47, -100 and 154, and significantly increasing trends for a-HBCDD and 6MeO-BDE47,
suggesting their chronic exposure for this pelagic whale species.
1. Introduction
It is common knowledge that organochlorine compounds (OCs)
such as polychlorinated biphenyls (PCBs), dichlorodiphenyltri-
chloroethane and its metabolites (DDTs), hexachlorocyclohexane
isomers (HCHs), chlordane compounds (CHLs) and hexa-
chlorobenzene (HCB) have a highly bioaccumulative nature and can
cause adverse effects on wildlife (Jones and de Voogt, 1999; Tanabe
2002); thus these OCs are strictly regulated for their abolition
(prohibition of production and use) according to the Stockholm
Convention on persistent organic pollutants (POPs). Brominated
flame retardants (BFRs) such as polybrominated diphenyl ethers
(PBDEs) and hexabromocyclododecanes (HBCDDs), which have
been registered as POPs during 2009e2017, also show similar
physicochemical properties and toxic effects as OCs (de Wit, 2002;
Darnerud, 2003). Despite the international regulation, the above
POPs have still been detected in a wide range of animals, especially
in high trophic level species at elevated levels (Tanabe and Ramu,
2012). Although environmental and human exposure levels of
POPs tend to decrease (Fång et al., 2015; Koshiba et al., 2019; Venier
et al., 2016), limited data on temporal trends of POP levels in the
open ocean, except polar regions (Rige
t et al., 2019), are available
because of the difficulty in continual sample collection. Considering
that POPs used inland are gradually transported to the open ocean
over time (Wania and Mackay, 1993), temporal trend analysis on
POPs contamination in oceanic regions is of essential importance in
understanding the effect of the Stockholm Convention on POPs.
Whale species, which are the top predators of the marine food
web, are considered to be susceptible to the effects of POPs expo-
sure, because of the higher accumulation levels and lower meta-
bolic capacity of these contaminants (Colborn and Smolen 1996;
Tanabe et al., 1994; Tanabe 2002). In fact, a previous study on
harbor porpoises (Phocoena phocoena) from the North and Baltic
Seas and Icelandic and Norwegian waters reported that thymic
atrophy and splenic depletion were significantly correlated to
increased PCB and PBDE levels (Beineke et al., 2005). Our study
group also revealed the association between parasitic infection and
elevated PCB levels in finless porpoises (Neophocaena phocae-
noides) from Seto Inland Sea and Omura Bay, Japan (Isobe et al.,
2011). A meta-analysis study using European data on PCB concen-
trations in cetaceans has recently reported the possibility that the
elevated PCB levels accumulated in several cetacean species are still
likely to cause population declines and suppress population re-
covery (Jepson et al., 2016). Despite considerable research on POPs
accumulated in cetaceans, fewer studies have been conducted for
POPs-like compounds. For instance, polychlorinated diphenyl
ethers (PCDEs) with similar physicochemical and toxicological
properties as PCBs and PBDEs, which have been mainly originated
from by-products of technical chlorophenols, have been detected in
river sediment and biota samples mainly from Finland (Domingo
2006). However, quantitative analysis of PCDEs is unavailable for
cetaceans so far. To our knowledge, only qualitative analysis of
PCDEs has been conducted by nontargeted comprehensive
screening for Atlantic common dolphin (Delphinus delphis) and
common bottlenose dolphin (Tursiops truncatus) (Hoh et al., 2012;
2
Chemosphere 269 (2021) 129401
© 2020 Elsevier Ltd. All rights reserved.
Shaul et al., 2015). Although recent studies also reported that
relatively high concentrations of natural organohalogen com-
pounds such as methoxylated-PBDEs (MeO-PBDEs) and
2,3,30 ,4,40 ,5,50 -heptachloro-10 -methyl-1,20 -bipyrrole (Q1) with
similar physicochemical properties as POPs were detected in
cetacean blubber (Alonso et al., 2014; Fujii et al., 2018), their tem-
poral trends remain unclear. Especially, given the potential for long-
distance transportation of POPs, temporal data on POPs and their
related compounds in pelagic whale species have important im-
plications to comprehend the contamination status in the ocean
regions. However, there are very few studies that investigated
recent accumulation levels of not only POPs but also other orga-
nohalogen compounds (OHCs) in such species. Our study group
demonstrated extremely gradual or no downward trends of OC
levels from 1980s to the early 2000s in pelagic whale species (Isobe
et al., 2009; Tanabe and Ramu, 2012).
Melon-headed whales (Peponocephala electra) targeted in this
study are distributed worldwide in tropical and subtropical waters
of the open ocean and are top predators feeding mainly on squid
and also on a variety of fish (Jefferson et al., 2015). Since the 1980s,
mass strandings of melon-headed whales have occurred several
times on the Pacific coast of Japan. Although the cause of the
strandings remains unknown, the exposure of melon-headed
whales to anthropogenic contaminants may be a potential
contributing factor. Our research group have previously analyzed
OCs and PBDEs in the blubber of melon-headed whales stranded
along the Japanese coastal waters in 1982, 2001, 2002 and 2006,
and demonstrated that PCBs and DDTs were predominant con-
taminants and the concentrations of PBDEs and chlordane com-
pounds (CHLs) significantly increased from 1982 to 2001/02 and
2006 (Kajiwara et al., 2008). Thus, offshore whale species including
melon-headed whale might be chronically exposed to relatively
high levels of OHCs also in late years, but their recent contamina-
tion status remains unresolved.
The present study determined the recent accumulation features
of anthropogenic and natural OHCs in the blubber of melon-headed
whales stranded along the Japanese coastal waters in 2015. In
addition, we examined temporal trends of OHC levels by analyzing
archived blubber samples in the environmental specimen bank (es-
BANK) which were collected during 1982e2011.
2. Materials and methods
2.1. Samples
Blubber samples (n ¼ 19) were collected from mature males of
melon-headed whales stranded along coastal waters in Chiba
prefecture in 2006 (n ¼ 2), Kagoshima prefecture in 2010 (n ¼ 3),
and Ibaraki prefecture in 2011 (n ¼ 7) and 2015 (n ¼ 7), which were
stored at 25  C in the es-BANK of Center for Marine Environ-
mental Studies (CMES), Ehime University, Japan (Tanabe and Ramu,
2012). Another set of blubber samples (n ¼ 19), which were pre-
viously used for the analysis of OCs and PBDEs by Kajiwara et al.
(2008) and have been stored in es-BANK, were also reanalyzed in
this study. The quantification values for OCs and PBDEs were cross-
T. Kunisue, A. Goto, T. Sunouchi et al.
checked between the present and previous (Kajiwara et al., 2008)
studies (see the QA/QC section). Sampling locations and sample
information are shown in Fig. S1 and Table S1.
2.2. Chemical analysis
Extraction and cleanup procedures were followed by our pre-
vious studies (Isobe et al., 2011; Mukai et al., 2020) with slight
modifications. About 2 g of a blubber sample was ground with
anhydrous sodium sulfate and then extracted using a high speed
solvent extractor (SE-100, Mitsubishi Chemical Analytech, Japan)
with acetone/hexane mixture (1:1 v/v). The crude extract was
solvent-exchanged into hexane and concentrated to 10 mL using a
rotary evaporator. An aliquot of the extract was spiked with 13C-
labeled b-HCH (Cambridge Isotope Laboratories, USA), PCBs (CB-28,
-52, 95, 101, 105, 118, 138, 153, 156, 157, 167, 178,
180, 189, 194, 202, 206, 208, and 209: Wellington Lab-
oratories, Canada), PBDEs (BDE-28, -47, 99, 100, 153, 154,
183: Wellington Laboratories, Canada), and HBCDDs (a-, b-, g-
isomers, Wellington Laboratories, Canada), and then passed
through a gel permeation chromatography (GPC packed Bio-Bead
S-X3, BioRad Laboratories, USA) with a DCM/hexane mixture (1:1
v/v) as eluent. This GPC-treated extract was further cleaned up and
separated into two fractions using an activated silica-gel column
(Wakogel DX, Wako Pure Chemical Industries, Japan): the first
fraction was eluted with a DCM/hexane mixture (5:95 v/v, 150 mL)
and subsequently the second fraction was eluted with another
mixture of DCM/hexane (25:75 v/v, 100 mL). The first fraction
containing organochlorine pesticides (OCPs), PCBs, PBDEs, PCDEs,
MeO-PBDEs and Q1 was spiked with 13C-labeled penta-
chloroanisole (PCA, Cambridge Isotope Laboratories, USA), CB-170,
BDE-126, and BDE-205 (Wellington Laboratories, Canada), and
solvent-exchanged into 50 mL of isooctane under a gentle nitrogen
gas. The second fraction (i.e., HBCDDs fraction) was concentrated to
dryness and immediately filled up to 100 mL with a methanol so-
lution containing deuterium-labeled a-, b-, g-HBCDDs (Wellington
Laboratories, Canada).
Instrumental analysis for the targeted OHCs was conducted
based on the method reported by Mukai et al. (2020). OCP and
PCDE concentrations were determined using a gas chromatograph-
triple quadrupole mass spectrometer (GC-MS/MS, Agilent Tech-
nologies, USA). HCHs, HCB, CHLs and DDTs were analyzed by using
a HP5-MS column (length: 30 m, internal diameter: 0.25 mm, film
thickness: 0.25 mm, Agilent J&W, USA), and target PCDE congeners
(CDE-47, -99, 100, 153, and 154) by using a DB1-MS column
(30 m, 0.25 mm, 0.25 mm, Agilent J&W, USA). The triple qMS was
operated in electron ionization (EI) with multiple reaction moni-
toring (MRM) mode. PCBs, PBDEs, MeO-PBDEs and Q1 were
quantified using a GC-qMS (Agilent Technologies, USA) in EI-
selected ion monitoring (SIM) mode. DB1-MS (30 m, 0.25 mm,
0.25 mm, Agilent J&W, USA) for PCBs and Q1 and DB5-HT (15 m,
0.25 mm, 0.1 mm Agilent J&W, USA) for PBDEs and MeO-PBDEs
were used as analytical columns. PCDEs and Q1 were quantified
based on the relative response factors for 13C-labeled PCB conge-
ners because the corresponding 13C- or deuterium-labeled surro-
gates are commercially unavailable. HBCDD concentrations were
determined using an Acquity ultra high pressure liquid chromato-
graph coupled with Quattro micro API mass spectrometer (Waters/
Micromass, Tokyo, Japan). Three HBCDD diastereomers (a-, b-, g-
HBCDDs) were separated by an Extend-C18 column (length:
100 mm, internal diameter: 2.1 mm, particle size: 5 mm, Agilent
Technologies, USA) and measured by negative electro spray ioni-
zation (ESI) with MRM mode.
Lipid contents were determined by measuring the total non-
volatile solvent extractable material on sub-samples taken from
3
Chemosphere 269 (2021) 129401
the original extracts. Concentrations of OHCs were expressed on
lipid weight basis throughout the text.
2.3. QA/QC
A procedural blank was analyzed with every batch of 7 samples
to check for contamination during the cleanup process. No sub-
stantial interference peaks were observed on the SIM and MRM
chromatograms obtained from the GC-MS(/MS) and LC-MS/MS
analyses. Recoveries of 13C-labeled internal standards ranged
from 44 to 140%. Limit of detection (LOD) for target compounds
were calculated according to the standardized protocol (JIS K0312),
and the values were as follows: HCB (0.090 ng/g lw), HCHs
(0.070 ng/g lw), CHLs (0.10 ng/g lw), DDTs (0.12 ng/g lw), PCBs
(0.022 ng/g lw), PBDEs (0.020 ng/g lw), HBCDDs (0.14 ng/g lw),
PCDEs (0.030 ng/g lw), MeO-PBDEs (0.12 ng/g lw), and Q1
(0.078 ng/g lw). Values below LOD were treated as zero in this
study. The accuracy for quantification of POPs was validated by
analyzing the certified reference material (CRM: homogenized
blubber of finless porpoises) provided by National institute for
Environmental Studies (NIES), Japan. The quantification data were
in good agreement with certificated values.
Kajiwara et al. (2008) previously analyzed PCBs, DDTs, CHLs,
HCHs, HCB, and PBDEs in the blubber samples (n ¼ 19) of mature
male melon-headed whales stranded along the Japanese coastal
waters in 1982 (n ¼ 5, Miyazaki prefecture), 2001 (n ¼ 2, Ibaraki
prefecture; n ¼ 3, Kagashima prefecture), 2002 (n ¼ 4, Ibaraki
prefecture), and 2006 (n ¼ 5, Chiba prefecture), which have been
stored in es-BANK, and all the data have already reposited and are
accessible in ChemTHEATRE (Chemical in the THEATRE: Tractable
and Heuristic E-Archive for Traceability and Responsible-care
Engagement), which is able to archive the information on chemi-
cal concentrations in environmental and biological specimens with
their metadata such as sampling date and location, species, bio-
metrics and so on (ChemTHEATRE, 2020). However, the data of OCs
were quantified using GC-electron capture detector (ECD) with the
external standard method, while PBDEs were analyzed by a stable
isotope-dilution GC-MS method. Actually, when concentrations of
PCBs, DDTs, CHLs, HCHs, HCB, and PBDEs re-measured in this study
were compared with the previous data (Kajiwara et al., 2008;
ChemTHEATRE, 2020), large gaps were observed for OCs in several
blubber samples (Table S2). This could be due to the incomplete
separation of interference peaks and the recovery-unadjusted
concentrations (without stable isotope-labeled internal stan-
dards) obtained with the previous GC-ECD method. Thus the re-
sults in Table S2 clearly indicate that the use of data analyzed by a
same method (updated method with high accuracy and precision)
is indispensable for temporal trend analysis. In this study, the
concentration data of PCBs, DDTs, CHLs, HCHs, HCB and PBDEs
quantified by the updated isotope-dilution GC-MS and GC-MS/MS
methods, as described in the previous section, were used.
2.4. Statistical analysis
We statistically analyzed the temporal trends of OHC levels in
mature male specimens (n ¼ 38) with approximately the same
body lengths (234e270 cm: See Table S1), because it is well known
that POPs show age (body length)-dependent accumulation prop-
erty in males, in addition to their possible maternal-to-fetal/infant
transfer in females. In fact, no significant correlations were
observed between the body lengths and accumulation levels of
each OHC in the mature male specimens analyzed in this study.
Thus relationships between the stranded years and log10-trans-
formed OHC levels were examined by linear regression analysis, as
reported by Isobe et al. (2009).
T. Kunisue, A. Goto, T. Sunouchi et al. Chemosphere 269 (2021) 129401

3. Results and discussion
3.1. Recent contamination status
OHCs were detected in all the blubber samples analyzed in this
study (Table 1 and Tables S3eS8) and the median concentrations in
specimens collected recently (in 2015) were in the order of DDTs
(median [min-max]: 10000 [6900e14000] ng/g) z PCBs (10000
[5800e14000] ng/g) > HBCDDs (8800 [4500e10000] ng/g) > Q1
(3700 [2400e5000] ng/g) > CHLs (2800 [1900e3900] ng/g) > MeO-
PBDEs (1100 [810e1300] ng/g) > PBDEs (320 [180e370] ng/
g) > HCB (190 [160e220] ng/g) > HCHs (180 [130e220] ng/
g) > PCDEs (7.8 [4.8e11] ng/g). Interestingly, HBCDD and Q1 con-
centrations were higher than classical POPs of CHLs, HCHs and HCB
in melon-headed whales stranded in the recent year. This result
indicates that considerable amounts of HBCDDs and Q1, in addition
to DDTs and PCBs, have been transported to tropical and subtropical
waters of the open ocean atmospherically, by oceanic current, and/
or by migration of prey organisms such as cephalopodan and fish,
and pelagic whale species might be exposed to relatively high
levels of these OHCs. To our knowledge, the present study reported
PCDE concentrations in melon-headed whales for the first time.
However, the accumulation levels were notably lower than those of
other OHCs, suggesting the low contamination load of PCDEs in the
open ocean.
When the compositions of PCBs, DDTs, HCHs, CHLs, PCDEs,
PBDEs and MeO-PBDEs in the recently-stranded melon-headed
whales were examined, all the seven specimens showed similar
profiles of these OHCs (Fig. 1). Penta-to hepta-chlorinated conge-
ners accounted for 88e92% of total PCBs, with predominant con-
geners of CB101 and CB118 for pentaCBs, CB138 and CB153 for
hexaCBs, CB180 and CB187 for heptaCBs (Table S3). As for OCPs,
p,p’-DDE, trans-nonachlor and b-HCH accounted for 72e81% of
DDTs, 67e73% of CHLs and 88e93% of HCHs, respectively (Fig. 1 and
Table S4). Previous studies have also reported similar composition
patterns in cetaceans and suggested that these OC compounds are
hard for their bodies to metabolize and are retained in the blubber
because of the high lipophilicity (Ramu et al., 2005; Tanabe et al.,
1997). In regard to PCDEs, relatively higher proportions of hexa-
chlorinated congeners, CDE153 and CDE154, were found in
melon-headed whales, although their levels were lower as
described earlier (Table S5). A review paper reported that studies in
the US and Finland have mainly detected tri- and tetra-CDEs in
mussels and hexaCDEs in fish (Domingo 2006). These observations
imply that melon-headed whales are exposed to relatively high
levels of hexaCDEs via fish intake and/or hexaCDEs are stable in
their bodies.
While BDE47 was predominant as is the case in previous studies
of cetaceans from the US and Europe (Bachman et al., 2014; Baro
n
et al., 2015), relatively higher proportions of BDE154 equivalent to
BDE47 were observed in melon-headed whales (Fig. 1 and
Table S6). Such higher accumulation profiles of BDE154 have been
reported also in other pelagic whale species stranded along the
Japanese coastal waters (Isobe et al., 2009). Considering that
BDE154 is contained in technical penta- and octa-BDE products and
their production has been voluntarily banned by the early 2000s
(La Guardia et al., 2006), the above results indicate the stability of
BDE154 in whale bodies. Among HBCDD diastereomers, only a-
HBCDD was detected in melon-headed whales (Table S7; b-HBCDD
and g-HBCDD were below LOD in all the samples), supporting its
highly bioaccumulative property as reported previously (Covaci
et al., 2006; Isobe et al., 2007). In melon-headed whales, 6MeO-
BDE47 accounted for 76e87% of MeO-PBDEs (Fig. 1 and Table S8).
Similar profiles of MeO-PBDEs have been shown in killer whales
(Orcinus orca) stranded on the Pacific coast of Japan (Haraguchi
et al., 2009).
A previous study has reported POP concentrations in the
blubber of three male melon-headed whales (calf, juvenile and
adult) stranded along the Hawaiian coastal waters in 2010 and 2011
(Bachman et al., 2014) and hence we made a comparison with the
recent data (2010, 2011 and 2015) analyzed in this study (Table 2).
Concentrations of PCBs, DDTs and CHLs in melon-headed whales
stranded along the Japanese coastal waters were noticeably lower
than those in an adult specimen from Hawaii, while the levels were
comparable to or slightly higher than those in calf and juvenile
specimens from Hawaii. Concentrations of HCHs, HCB and PBDEs in
melon-headed whales analyzed in this study were also lower than
those of the Hawaiian adult specimen. Although it is difficult to
precisely discuss the differences in POP levels because of the
comparison to only one Hawaiian adult specimen with an
extremely low lipid content (8.9% in Table 2), the above results
imply that melon-headed whales stranded along the Japanese
coastal waters have been exposed to relatively low levels of OCs and
PBDEs compared with the population migrating off Hawaii. Inter-
estingly, however, HBCDD concentrations in melon-headed whales
analyzed in this study were one order of magnitude higher than
those in the adult specimen from Hawaii (Table 2). This result
clearly indicates that the melon-headed whale population
migrating in tropical and subtropical waters of the western North
Pacific Ocean might be still exposed to high levels of HBCDDs and

Table 1
Median and range concentrations (ng/g lipid wt.) of OHCs in the blubber of male melon-head whales stranded along the Japanese coastal waters.

Stranded PCBs DDTs CHLs HCHs HCB PBDEs HBCDDs PCDEs MeO-PBDEs Q1
year
median (range) median (range) median (range) median median median median (range) median median (range) median (range)
(range) (range) (range) (range)

1982 23000 (20000- 39000 (34000- 1700 (1500 340 (160 300 (270 26 (21e30) 88 (76e140) 22 (15e28) 630 (450e680) 2800 (1900
(n ¼ 5) 26000) 46000) e2600) e550) e410) e3200)
2001 15000 (11000- 16000 (13000- 3600 (3000 240 (220 270 (200 410 (190 3000 (2400 12 (9.4e13) 760 (290e850) 3100 (1900
(n ¼ 5) 20000) 19000) e3900) e290) e310) e410) e4700) e3600)
2002 14000 (13000- 17000 (16000- 4500 (3700 280 (270 250 (210 420 (320 4400 (2500 9.1 (8.7e10) 840 (590e860) 3500 (2900
(n ¼ 4) 16000) 19000) e4600) e350) e270) e500) e5500) e3800)
2006 8200 (4900 12000 (6600 3000 (1600 190 (140 190 (140 330 (190 5500 (2200 7.7 (4.3e12) 870 (560 2400 (1500
(n ¼ 7) e17000) e27000) e5700) e270) e300) e530) e8300) e1100) e4200)
2010 17000 (16000- 19000 (18000- 3400 (3200 150 (140 180 (170 390 (390 2500 (2300 12 (12e13) 770 (730e830) 3700 (3300
(n ¼ 3) 18000) 22000) e3900) e210) e270) e430) e3900) e4300)
2011 15000 (11000- 22000 (16000- 4800 (3800 210 (140 240 (170 420 (340 5900 (3400 11 (9.0e13) 1100 (1000 4000 (3200
(n ¼ 7) 16000) 26000) e5900) e330) e280) e540) e14000) e1700) e4500)
2015 10000 (5800 10000 (6900 2800 (1900 180 (130 190 (160 320 (180 8800 (4500 7.8 (4.8e11) 1100 (810 3700 (2400
(n ¼ 7) e14000) e14000) e3900) e220) e220) e370) e10000) e1300) e5000)

4
T. Kunisue, A. Goto, T. Sunouchi et al.
Fig. 1. OHC compositions in the blubber of melon-headed whales stranded in 2015.
be at high risk. In fact, our group previously demonstrated a notably
higher HBCDD level in a skipjack tuna (Katsuwonus pelamis) spec-
imen collected around 150 east longitude than that in one around
180 east longitude in the North Pacific Ocean (Ueno et al., 2006)
and this could be due to larger past market demand for HBCDD in
Asia, mainly Japan and China, than in the US (Watanabe and Sakai,
2003; UNEP, 2011). Moreover it is noteworthy that PCB concen-
trations in four melon-headed whales stranded in 2015, in addition
to all the specimens stranded in 2010 and 2011, exceeded 9000 ng/g
lipid which was estimated as the lowest PCB toxicity threshold for
onset of physiological impacts (Jepson et al., 2016).
5
Chemosphere 269 (2021) 129401
3.2. Temporal trends of OHC levels
Temporal trend analyses of OHCs revealed significant reduction
in concentrations of DDTs, PCBs, HCB, HCHs and PCDEs in the
blubber of melon-headed whales since 1982 (Fig. 2 and Tables S9,
S10 and S11), reflecting the ban on their production and use dur-
ing 1970s and technical regulation of unintentional formation.
Although concentrations of HCB and HCHs significantly decreased
even after 2001, PCB and DDT levels showed no such decreasing
trends (unchanged) from 2001 to 2015 (Tables S9 and S10). The
trend observed for DDTs was attributed to the stabilized accumu-
lation of p,p’-DDE (Table S4), possibly because melon-headed
whales are continuously exposed to and/or hardly metabolize this
T. Kunisue, A. Goto, T. Sunouchi et al. Chemosphere 269 (2021) 129401

Table 2
Comparison of OHC concentrations (ng/g lipid wt.) in melon-headed whales stranded along the Japanese coastal waters in 2010, 2011 and 2015 (this study) with those stranded
along the Hawaiian coastal waters in 2010 and 2011 (Bachman et al., 2014).

Stranded Stranded Sex Lipid (%) PCBs DDTs CHLs HCHs HCB PBDEs HBCDDs Ref
site Year (maturity)

Kagoshima 2010 Male 66 (62 17000 (16000- 19000 (18000- 3400 (3200 150 (140 180 (170 390 (390 2500 (2300 This study
(adult) e79) 18000) a 22000) c e3900) e e210) g e270) e430) h e3900) j
Ibaraki 2011 Male 53 (41 15000 (11000- 22000 (16000- 4800 (3800 210 (140 240 (170 420 (340 5900 (3400 This study
(adult) e73) 16000) a 26000) c e5900) e e330) g e280) e540) h e14000) j
Ibaraki 2015 Male 52 (48 10000 (5800 10000 (6900 2800 (1900 180 (130 190 (160 320 (180 8800 (4500 This study
(adult) e62) e14000) a e14000) c e3900) e e220) g e220) e370) h e10000) j
O’ahu 2010 Male 51 3440 b 7240 d 821 f 77.3 g 265 104 i 53.6 j Bachman et al.,
(juvenile) (2014)
b d f g i j
O’ahu 2011 Male (Calf) 56 5040 9560 1380 112 435 331 99.1 Bachman et al.,
(2014)
b d f g i j
Maui 2011 Male 8.9 50200 99100 9520 276 420 1040 224 Bachman et al.,
(adult) (2014)
a
Sum of 55 PCB congeners.
b
Sum of 80 PCB congeners.
c
p,p’-DDT þ p,p’-DDE þ p,p’-DDD.
d
o,p’- and p,p’-DDT þ o,p’- and p,p’-DDE þ o,p’- and p,p’-DDD.
e
trans-chlordane þ cis-chlordane þ trans-nonachlor þ cis-nonachlor þ oxychlordane.
f
trans-chlordane þ cis-chlordane þ trans-nonachlor þ cis-nonachlor þ oxychlordane þ heptachlor.
g
a-HCH þ b-HCH þ g-HCH.
h
Sum of 25 PBDE congeners.
i
Sum of 28 PBDE congeners.
j
a-HBCDD þ b-HBCDD þ g-HBCDD.

compound, as described earlier. In fact, p,p’-DDT and p,p’-DDD
levels significantly decreased also since 2001 (Table S10). Inter-
estingly, g-HCH concentrations remained unchanged from 2001 to
2015, unlike total HCHs, although the levels (Table S4) and pro-
portions (Fig. 1) were much lower than those of b-HCH that showed
a significantly decreasing trend since 2001 (Table S10). This result
implies that g-HCH used as lindane until the regulation in 2009 is
still transported to subtropical waters of the open ocean, mainly via
the atmosphere. A recent study estimated fugacity ratios has re-
ported that g-HCH was volatilizing from surface seawater to the
atmosphere at lower latitude (9.0  N) of the North Pacific Ocean,
suggesting the secondary source for higher latitudes (Li et al.,
2020). As for PCBs, congener-specific temporal trends from 2001
to 2015 were found: the details are discussed in the next section.
On the other hand, concentrations of organobromine com-
pounds (i.e., PBDEs, HBCDDs, MeO-PBDEs), CHLs and Q1 signifi-
cantly increased since 1982 (Fig. 2). In addition, significantly
increasing HBCDD and MeO-PBDE concentrations and no signifi-
cant variations in PBDE, CHL and Q1 concentrations were observed
from 2001 to 2015 (Tables S10 and S11). These results indicate the
continuous transportation to tropical and subtropical waters of the
open ocean and chronic exposure for pelagic whale species by these
OHCs. Because large amounts of CHLs had been used as termiticides
in Japan until 1986, the increase trend of CHL levels in melon-
headed whales observed since 1982 might be reflecting the delay
in the implementation of the restriction on its use for termite
control. As for PBDEs and HBCDDs, it is speculated that relatively
recent registration as POPs (during 2009e2017) and continuous
environmental release from in-use and discarded electric and
electronic equipment (Abbasi et al., 2019) contributed to the tem-
poral trends. Although the contributing factor for MeO-PBDEs and
Q1 is unclear, climate variations may be responsible for the
increased trends of these natural OHCs since 1982. A recent study
pointed out that production of natural OHCs will be affected by
climate change impacts on marine producers and biogeochemical
cycles (Bidleman et al., 2020). Considering that MeO-PBDEs and Q1
are biosynthesized by marine primary producers (Bidleman et al.,
2020), their burden in the marine environment and exposure
levels for marine organisms at higher trophic levels could be
6
increased by overgrowth and activation of the producers associated
with global warming.
3.3. Temporal trends of PCB congener levels
As described in the previous section, congener-specific temporal
trends were observed for PCB levels in the blubber of melon-
headed whales stranded from 2001 to 2015 (Fig. 3 and Table S9),
even congeners with the same number of chlorine substituted.
Regarding PCB congeners detected at 10 times higher levels than
LOD in all the samples, CB-28 (3Cl), 44, 49, 74
(4Cl), 99, 110, 114, 118 (5Cl), 128, 138, 149, 151,
153, 158 (6Cl), 170, 171, 177, 178, 180, 183, 187, 191
(7Cl), and 194, 202 (8Cl) represented unchanged concentra-
tions, while significantly decreased trends were observed for CB-52
(4Cl), 87, 95, 101, 105 (5Cl), 156, 157, 167 (6Cl), 189
(7Cl), 199, 201 (8Cl), 206, 208 (9Cl), and 209 (10Cl)
(Table S9). Given almost the same physicochemical properties
among PCB congeners with the same number of chlorine
substituted (Hawker and Connell, 1988), the above differences in
temporal trends may be attributed to PCB congener-specific intake
via prey and/or metabolic capacity in melon-headed whales. To our
knowledge, no recent data on detailed PCB congener profiles in fish
and cephalopod from the North Pacific Ocean are available; only
total PCBs or homologue data have been reported in tables of
published scientific papers (e.g., Uekusa et al., 2017). Uekusa et al.
(2017) have described that CB-138 and -153 were dominant con-
geners and seven congeners of CB-28, -52, 101, 118, 138,
153, 180 accounted for significant proportions of total PCBs in
three marine fish from off Tohoku, Japan, which indicates that ce-
taceans stranded along the Japanese coastal waters might be
preferentially exposed to these PCB congeners.
As shown in Fig. 3 and Table S9, however, significantly
decreasing trends of CB-52 and CB-101 levels were observed in
melon-headed whales. It is known that cetaceans including melon-
headed whale have low metabolic capacity for PCBs (Tanabe 2002)
and actually have a deficiency of PB-type enzymes (CYP2B families)
(White et al., 2000), which are considered to be involved primarily
in the metabolism of PCB congeners without chlorine atoms on the
T. Kunisue, A. Goto, T. Sunouchi et al.
Fig. 2. Temporal trends of OHC concentrations in melon-headed whales stranded during 1982e2015. The temporal trends were examined by linear regression on log10-transformed
concentrations. P-values < 0.05 indicate significant increase or decrease.
meta- and para-positions (PB-type PCB congeners) (Ishida et al.,
1991). Given that cetaceans have MC-type enzymes (CYP1A fam-
ilies), which are considered to be involved primarily in the meta-
bolism of PCB congeners without chlorine atoms on the ortho- and
meta-positions (MC-type PCB congeners) (Ishida et al., 1991), and
can metabolize CB77 at rates comparable to rodent species (White
et al., 2000), melon-headed whales may efficiently metabolize MC-
type PCB congeners such as CB-105 and CB-156 which showed
decreasing trends in this study. Although the reason for the
decreased trends of CB-52 and CB101 levels is unknown, melon-
7
Chemosphere 269 (2021) 129401
headed whales could possibly metabolize these PB-type conge-
ners by CYP families other than CYP2B, as suggested previously for
other whale species (White et al., 2000). To our knowledge, infor-
mation on PCB congener-specific temporal trends is unavailable in
cetaceans.
3.4. Temporal trends of PBDE congener levels
As for PBDE congeners detected in all the blubber samples of
melon-headed whales, concentrations of BDE99 and BDE153
T. Kunisue, A. Goto, T. Sunouchi et al.
Fig. 3. Temporal trends of major PCB and PBDE congener concentrations in melon-headed whales from 2001 to 2015. The temporal trends were examined by linear regression on
log10-transformed concentrations. P-values < 0.05 indicate significant increase or decrease.
showed significant decreasing trends since 2001 (Fig. 3 and
Table S11). Considering that these two PBDE congeners are con-
tained in technical penta- and octa-BDE products (La Guardia et al.,
2006), their use regulation could be partly contributed to the above
phenomenon. However, such decreasing trends were not observed
for BDE47, BDE100, and BDE154 (Fig. 3 and Table S11), even though
these PBDE congeners are also contained in the technical formu-
lations (La Guardia et al., 2006) and the physicochemical properties
between BDE99 and BDE100, and between BDE153 and BDE154 are
almost the same (ATSDR, 2017). Especially BDE154 was detected at
concentrations higher than other PBDE congeners and comparable
to BDE47 in recently-stranded specimens, implying exposure to
relatively high levels of BDE154 through their prey and/or higher
stability of this congener in the whale body. Previous studies re-
ported that BDE47 was predominant and relatively higher levels of
BDE100 and BDE154, compared to BDE99 and BDE153, were
detected in marine fish and cephalopod collected off Japan in the
North Pacific Ocean (Ashizuka et al., 2005; Kakimoto et al., 2012). In
addition, our study group demonstrated that BDE47 and BDE154
with similar levels were predominant PBDE congeners detected in a
8
Chemosphere 269 (2021) 129401
skipjack tuna specimen collected in tropical waters of the North
Pacific Ocean (around 180 east longitude) (Ueno et al., 2004). As
described earlier, such higher accumulation levels of BDE154,
which were comparable to BDE47 levels, have been observed also
in the blubber of striped dolphins stranded along the Japanese
coastal waters (Isobe et al., 2009). Interestingly, Isobe et al. (2009)
have also shown higher levels of BDE154 than BDE47 in the liver,
muscle and brain of striped dolphins. These observations indicate
that exposure to relatively high levels of BDE154 for pelagic whale
species inhabiting the western North Pacific Ocean are still ongoing.
4. Conclusions
The present study elucidated the recent contamination levels
and compound-specific temporal trends of OHCs in the blubber of
melon-headed whales stranded along the Japanese coastal waters.
In recently-stranded melon-headed whales, DDTs and PCBs were
detected as predominant POPs, and Q1 and HBCDD concentrations
were higher than the levels of classical POPs such as CHLs, HCHs
and HCB, indicating that considerable amounts of Q1 and HBCDDs,
T. Kunisue, A. Goto, T. Sunouchi et al.
in addition to DDTs and PCBs, have been transported to tropical and
subtropical waters of the open ocean and pelagic whale species
might be exposed to relatively high levels of these OHCs. Temporal
trend analyses of OHCs by using blubber samples of melon-headed
whales archived in the es-BANK revealed significant increase in
concentrations of organobromine compounds (i.e., PBDEs, HBCDDs,
MeO-PBDEs), CHLs and Q1 since 1982, and significant decrease in
OC levels except for CHLs (i.e., DDTs, PCBs, HCB, HCHs, PCDEs) since
1982. This could be due to the timing of ban on their use and
production and the current climate change. Besides, the analyses
from 2001 to 2015 showed no decreasing trends (unchanged) for
some PCB congeners, p,p’-DDE, cis- and trans-nonachlors, Q1, BDE-
47, -100 and 154, and significantly increasing trends for a-HBCDD
and 6MeO-BDE47, suggesting their chronic exposure and potential
risks. As for these OHCs, continuous monitoring survey and toxi-
cological studies on multiple exposure are needed for pelagic whale
species.
Credit author statement
Tatsuya Kunisue: Writing e original draft & editing, Methodol-
ogy, Validation, Conceptualization, Funding acquisition, Project
administration, Supervision. Akitoshi Goto: Methodology, Valida-
tion, Visualization. Tomoya Sunouchi: Formal analysis, Investiga-
tion. Kana Egashira: Formal analysis. Mari Ochiai: Investigation,
Resources. Tomohiko Isobe: Investigation, Resources. Yuko Tajima:
Investigation, Resources. Tadasu K Yamada: Investigation, Re-
sources. Shinsuke Tanabe: Conceptualization
Data accessibility
Individual data on concentrations of organohalogen compounds
in the blubber of melon-headed whales analyzed in this study.
Repository: ChemTHEATRE.
URL: https://chem-theatre.com/project/PRA000111.
Declaration of competing interest
The authors declare that they have no known competing
financial interests or personal relationships that could have
appeared to influence the work reported in this paper.
Acknowledgment
We thank Shiozaki A, Oshihoi T, Saito A, Motogi K, Kume I,
Yoshinouchi Y, and Tamura S from Ehime University, the staff from
Hokota and Kashima City Office and Ibaraki Prefectural Oarai
Aquarium (AQUA WORLD) and other related workers for sample
collection. This study was supported by Grants-in-Aid (KAKENHI)
for Scientific Research (A) (No. 19H01167 and 19H01150) from Japan
Society for the Promotion of Science (JSPS), the Environment
Research and Technology Development Fund (SII-3-2[1]:
JPMEERF18S20303) of the Environmental Restoration and Conser-
vation Agency of Japan (ERCA), and the Ministry of Education,
Culture, Sports, Science and Technology, Japan (MEXT) to a project
on Joint/Research Center - Leading Academia in Marine and Envi-
ronment Pollution Research (LaMer).
Appendix A. Supplementary data
Supplementary data to this article can be found online at
https://doi.org/10.1016/j.chemosphere.2020.129401.
9
Chemosphere 269 (2021) 129401
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