Cetacean Population Studies
V01日

Publication Committee
for the Cetacean Population Studies

2020

ヽ

2

Cetacean Population Studies

Volume 2, June 2020

Publication Committee
for the Cetacean Population Studies
Tokyo, Japan

Contents
Foreword …………………………………………………………………………………………

1

Memory of Dr. Seiji Ohsumi 12 July 1930 – 2 November 2019 ………………………………

2

Full paper
GOTO, M., KITAKADO, T., and PASTENE, L. A.
A preliminary study of epigenetic estimation of age of the Antarctic minke whale
Balaenoptera bonaerensis ………………………………………………………………………

5

MATSUOKA, K., and HAKAMADA, T.
Density distribution of several major whale species in the Indo-Pacific region of Antarctic
using JARPA and JARPAII sighting data obtained through 1987/88 – 2008/09 seasons ……… 15
YASUNAGA, G., and FUJISE Y.
Concentration of persistent organic pollutants (POPs) in three species of baleen whalesin the western North Pacific …………………………………………………………………… 39
Archival Index ………………………………………………………………………………… 55
Subject Index …………………………………………………………………………………… 56
Author Index …………………………………………………………………………………… 57
Guide for Authors ……………………………………………………………………………… 58

目次

初めに ……………………………………………………………………………………………

1

大隅清治先生追悼の辞 …………………………………………………………………………

2

研究論文
後藤睦夫、北門利英、パステネ L. A.
クロミンククジラを対象とした予備的なエピジェネティック年齢査定 …………………

5

松岡耕二、袴田高志
JARPA 1987/88～ JARPAII 2008/09期のデータを用いた
南極海（インド洋－太平洋区）における主要大型鯨類の地理的分布密度 ……………… 15
安永玄太、藤瀬良弘
北西太平洋のヒゲクジラ類 3 種の有機汚染物質（POPs）汚染の現状 …………………… 39
著者及びタイトル索引 ………………………………………………………………………… 55
件名索引 ………………………………………………………………………………………… 56
著者索引 ………………………………………………………………………………………… 57
執筆要領 ………………………………………………………………………………………… 58

Foreword
Remarkable evolution in cetacean studies in recent decades owes much to major journals that have madesignificant contribution to the development of modern cetology: Discovery Reports, published by the
National Institute of Oceanography in the United Kingdom, and Norwegian Whaling Gazette in Norway,
as well as The Scientific Reports of the Whales Research Institute in Japan.
The Scientific Reports of the Whales Research Institute was first published in 1948, a year after the
Whales Research Institute was established. Aiming to share valuable research findings and scientificknowledge worldwide, the publication was formatted in English since its beginning, quite an ambitious
attempt in Japan still recovering from the devastation of World War II.
Since its first publication, a total of 246 scientists contributed 419 scientific papers to The Scientific
Reports of the Whales Research Institute. It is widely acknowledged and appreciated that these scientificpapers were the foundation for the development of cetacean studies worldwide, and in today’s terms, it
was a research journal that had a significant impact factor, or high number of citations. Regrettably, however, The Scientific Reports of the Whales Research Institute was discontinued in 1988 with the 39th
volume after the institute was reorganized into the Institute of Cetacean Research.
In the 30 years since then, various types of journals on cetacean studies have been published globally,each offering different perspectives on scientific research outcomes. As for Japan, no research journal
matching The Scientific Reports of the Whales Research Institute in its quality has been published. It is
probably because many domestic cetologists have sought to publish their papers in international research
journals based outside Japan.
As the global environment surrounding the issue of whaling became increasingly complex, we haveobserved a shift in publishing policies among these journals, rejecting papers whose findings are basedon specific research methods such as lethal sampling. Because of this, no small numbers of papers submitted by biological scientists using samples collected through lethal surveys, even just for some parts, havebeen denied proper reviews. While we agree that animal ethics should be given high priority when writinga research paper, if a paper, the research method of which is allowed under domestic and internationalrules, is rejected, it is a decision made beyond scientific judgment.
Our new journal for cetacean population studies intends to follow the scientific policy of The Scientific
Reports of the Whales Research Institute, that is, to contribute to global development of cetacean studies.
As long as submitted papers conform to scientifically-accepted animal ethics, we do not make distinctions
based on research methods. At the same time, to maintain the journal’s neutrality in the complex global
environment surrounding whaling issues, the journal will be published from a newly organized committee,
rather than as a bulletin type scientific report from a specific research institute. The title of the new journal will be Cetacean Population Studies to be abbreviated CPOPS, and we aim to keep our door wide-open
for researchers worldwide, contribute to the scientific development of resource studies for marine mammals especially focusing on cetaceans, and nurture many aspiring scientists.

December 31, 2018

Cetacean Population Studies (CPOPS)
Vol. 2, 2020, 2-3

Seiji Ohsumi, Ph. D.
Chairman
Publication Committee for the Cetacean Population Studies

1

Memory of Dr. Seiji Ohsumi 12 July 1930 – 2 November 2019
We very much regret to inform you that Dr. Seiji Ohsumi, aged 89, Chairman of Governing Councilof Cetacean Population Studies (CPOPS) unfortunately died at 7:55 PM on November 2, 2019 due toan acute myocardial infarction.
Dr. Ohsumi had been one of the leading members of the IWC/SC for very long time through the 1960’s
to the 2010’s, serving as head of the Japanese delegation to the IWC/SC during many years in 1990s.

Dr. Seiji Ohsumi was born on July 12, 1930 in Gunma Prefecture, the center of Japan. He had been atemporary member of the Whales Research Institute while he was a graduate student of the Faculty ofAgriculture at the University of Tokyo. Subsequently he became a permanent scientist in 1958. In his
early days at the WRI he was mainly engaged in field science at numerous places where whaling
occurred as well as laboratory analyses under the supervision of the late Professor Masaharu Nishiwaki(senior scientist at WRI) and the late Dr. Hideo Omura (Director general of WRI). In this way hegained biological knowledge about both large and small cetaceans. His first paper in English was
published in the Scientific Report of WRI in 1954 [9: 165 – 177] under his original name of Seiji
Kimura and was titled “On the sexual maturity of the sei whale of the Bonin waters”.
His Ph.D. thesis submitted to the University of Tokyo, examined age determination with a focus on
fin whales and titled “A study on age determination of the fin whale”, in which he found and confirmed
annual deposition rate of growth layer in fin whale earplugs, which was one of most important issues
in stock management of fin whales.
Dr. Seiji Ohsumi moved to a government fisheries laboratory in May 1966 and was assigned head ofcetacean population studies at the Far Seas Fisheries Research Laboratory (currently, National
Research Institute of Far Seas Fisheries) in August 1967. He served as director general at FSFRL from
October 1988 to March 1991.

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After retirement as a government scientist, he was nominated as a trustee on the board directors of theInstitute of Cetacean Research, Tokyo in April 1991. Subsequently, he was nominated as the director
general of the ICR in December 1995. He continued to serve in the position of director general until
December 2003.
Subsequently Dr. Ohsumi was nominated as a senior scientific adviser in January 2004, and as anhonorary scientific adviser in October 2015. He remained in that position until November 2019 andcontinued to travel from his home in Shinjuku to the ICR almost daily until November 1, 2019. Seiji
always said that “I continue to go to the office each day because this is my eternal mission.”
During the period through the 1950s to the 2010s, he made tremendous scientific works and publishednumerous scientific articles on cetaceans over 500 papers including both English and Japanese articles.
One of his academically important papers was on the school structure of sperm whales titled “Someinvestigations on the school structure of sperm whale (Scientific Report of WRI, 23: 1 – 25.)”. During
his academic years he received numerous numbers of awards including the Royal Norwegian Orderof Merit, Special Award of the Mammal Society of Japan, etc.
His public memorial service was held at 13:00 on December 23, 2019 at the Mariners Court HotelTokyo (Harumi, Tokyo), jointly hosted by the Institute of Cetacean Research and Seiji Ohsumi’s family. The co-mourners were Dr. Yoshihiro Fujise (Director general of ICR), Drs. Masako Osumi (wife,
Professor Emeritus of Japan Women’s University) and Noriko Osumi (daughter, Professor of theMedical school, Tohoku University).
The next volume, CPOPS Vol. 3, will be designated as “Memorial Volume for Dr. Seiji Ohsumi”, wewould request widely to submit paper contributions from various areas and peoples.
June 1, 2020
Hidehiro Kato
Chairman Alternate, Publication Committee for the Cetacean Population Studies

Cetacean Population Studies (CPOPS)
Vol. 2, 2020, 2-3

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EPIGENETIC ESTIMATION OF AGE OF THE ANTARCTIC MINKE WHALE

Full paper

A PRELIMINARY STUDY OF EPIGENETIC
ESTIMATION OF AGE OF THE ANTARCTICMINKE WHALE BALAENOPTERA BONAERENSIS
Mutsuo GOTO1*, Toshihide KITAKADO2 and Luis A. PASTENE1
Institute of Cetacean Research, 4 – 5 Toyomi-cho, Chuo-ku, Tokyo 104 – 0055, Japan*(Corresponding author: goto@cetacean.jp)
2
Tokyo University of Marine Science and Technology, 4 – 5 – 7 Konan, Minato-ku, Tokyo 108 – 8477, Japan
1

Abstract
Age is one of the most important life history parameters for assessment and management ofmarine living resources. Counting of the growth layers deposited in the earplugs is the mostaccepted technique for determining chronological age of baleen whales. However unreadable
growth layers form in the earplugs of some individual whales. In such cases, alternative methods of age estimation are required. The objective of the present study was to examine the utility of the DNA methylation technique as a proxy to estimate chronological age in the Antarctic
minke whale. For this purpose, skin tissues of a total of 100 Antarctic minke whales sampled
in the Pacific region of the Antarctic by JARPAII surveys were used. Earplug-based age datafrom the same whales were used for calibration purposes. Seven CpG sites in three genes(TET2, CDKN2A and GRIA2) were selected for the analysis. In a previous study, these sites
showed significant correspondence between methylation levels and age in humpback whales.
Methylation levels of the seven CpG sites were scored successfully. Four CpG sites showedsignificant regressions with age, which contrasted with the case of the humpback whale where
all seven sites showed significant regressions with age. The assay predicted age from skinsamples with a standard deviation of 8.865 years. This low precision makes the age estimatedby the CpG methylation technique unsuitable for use in population dynamics models such as
the statistical catch-at-age (SCAA). Furthermore CpGs methylation levels fluctuated among
body positions of the whale, particularly between dorsal (exposure to sunlight) and ventral
sides. The precision of the CpG methylation technique for age estimation could be improvedby increasing the number of CpG sites showing a good correlation with age, and this work is
ongoing. In addition, other factors including variation of CpG methylation levels between different tissues should be examined to further evaluate the utility of the DNA methylation techniques as a proxy of age estimation in baleen whales.
Key words: Antarctic minke whale, age estimation, epigenetics, DNA methylation, proxy of
earplugs.

Introduction

Age is one of the most important life history parameters for assessment and management of marine
living resources. In baleen whales, age has been determined using a variety of methods such as
examination of baleen plates (Nishiwaki, 1951; Zenitani and Kato, 2010), earplugs (Lockyer, 1984)
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GOTO, KITAKADO AND PASTENE

and tympanic bulla (Christensen, 1995). Counting of the growth layers deposited in the earplugs is themost accepted technique for determining chronological age of baleen whales (Lockyer, 1984). Earplugbased age determination has the advantage that it is time- and cost-efficient, and the technique can beused on available historical samples.
The Antarctic minke whale (Balaenoptera bonaerensis) is one of the smallest balaenopterid species,
which is widely distributed in the Southern Hemisphere. This species is considered the most abundantbaleen whale species, with a total abundance estimated at 515,000 (IWC, 2012). During the assessmentof this species, the International Whaling Commission Scientific Committee (IWC SC) successfully
applied statistical catch-at-age (SCAA) analyses. A summary history of the application of SCAA tothis species was presented by Punt (2014), and an assessment of Antarctic minke whales using SCAA
was reported by Punt et al. (2014). Among the most important outputs from the SCAA analyses was
the information on the age-specific natural mortality and the historical trends of the stocks. The key
input data for the SCAA analyses consisted of catches, abundance estimates, length frequency data
and age-at-length data. Age data was obtained from reading earplugs of Antarctic minke whales caught
during past commercial whaling operations and by scientific surveys by the Japanese Whale Research
Program under Special Permit in the Antarctic (JARPA/JARPAII).
While earplug’s growth layers reading is considered the most acceptable technique for age determination in whales, unreadable growth layers form in the earplugs of some individual baleen whales(Maeda et al., 2013; George et al., 1999). In the case of the Antarctic minke whale, determining theage by reading earplugs of immature whales is particularly difficult. In such cases, alternative methodsof age determination are required.
Indices of chronological age of whales have been developed using molecular approaches. These
include length of telomeres (Olsen et al., 2012; 2014), and epigenetic technique based on DNA methylation (Polanowski et al., 2014). Another technique is based on enantiomers of aspartic acid in eyelens, the aspartic acid racemization (AAR) technique, which was successfully applied to Antarctic
minke whales (Yasunaga et al., 2017).
The present study focuses on the estimation of age in Antarctic minke whale based on the epigenetic approach. The best studied class of epigenetic change in vertebrates is the methyl group presenceor absence at the C5 position of Cytosine residues that are adjacent to Guanidine residues (‘CpG
sites’). CpG methylation levels play an important role in the control of gene expression, where higher
methylation levels (‘hypermethylation’) generally reduce gene transcription rate. Methylation changes
at specific CpGs have been linked to age in mice (Maegawa et al., 2010) and humans (Christensen etal., 2009; Gronniger et al., 2010; Bocklandt et al., 2011; Koch and Wagner, 2011; Hannum et al.,2013). It should be noted that the CpG methylation technique does not provide the chronological ageof the individuals but rather a physiological age that can be used as a proxy for chronological age.
The CpG methylation approach was recently applied to known age (from photo-identification studies) humpback whales (Polanowski et al., 2014). These authors assayed 37 cytosines for methylationlevel in humpback whale skin of which seven had significant age-related profiles. They selected thethree most age-information cytosine markers for a humpback whale epigenetic age assay. The assay
had a coefficient of estimation (R2) of 0.787, and predicted age from skin samples with a standard
deviation of 2.991 years.
The objective of the present study was to examine the utility of the CpG methylation technique asa proxy to determine chronological age in the Antarctic minke whale, by using the same three informative cytosine markers of the humpback whale (Polanowski et al., 2014). The ages of the Antarctic
minke whales examined for this epigenetic study were available from earplug’s readings, and thesedata were used for calibration purposes.
Apart from the investigation of informative CpG sites, several other factors should be considered tofurther investigate the utility of the CpG methylation technique for determining age of whales for
population-level analyses (see summary in IWC, 2017). For example, it was suggested there is a need

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EPIGENETIC ESTIMATION OF AGE OF THE ANTARCTIC MINKE WHALE

to better understand the ‘stressors’ (e.g. sunlight) that may affect the calibration of the methylation
approach. A secondary objective of the present study was therefore to investigate changes of the CpG
methylation levels with regard the body positions where the skin samples were obtained, i.e. parts withmore or less exposure to sunlight.

Materials and methods

Whale sampling
Antarctic minke whales used in the present study were caught in the austral summer seasons 2010/11
and 2011/12 in the Pacific sector of the Antarctic comprised of the area between 130°E – 145°W by
surveys of the Second Phase of the Japanese Whale Research Program under Special Permit in the
Antarctic (JARPAII). For the CpG methylation study a total of 100 whales were selected from the total
number of whales caught in the two austral summer seasons. The selection was based on the qualityof their age information from earplugs, information used for calibration purposes. The age determination based on earplugs was conducted by a researcher from the Institute of Cetacean Research (ICR)
following Lockyer (1984). Each individual age was determined by counting growth layers appearing
on the bisected surface of the earplug using a stereoscope microscope, assuming an annual depositionof growth layers (i.e. one pair of dark and pale laminae accumulated per year). For the 100 whales
selected, age information from the earplugs was considered as ‘Excellent’ (very clear Growth LayerGroups (GLGs), and low likelihood of aging reading error) or ‘Good’ (most of the GLGs are clear,and moderate likelihood of aging reading error). Table 1 shows the number of individuals used in thisstudy by sampling season, sex and age classes.
Tissue sampling and DNA extraction
Skin tissue samples were obtained from each of the 100 whales, from the left lateral part of theirbody (sampling position ‘6’ in Fig. 1). Tissue samples were stored in 95% ethanol until DNA extraction. Genomic DNA was extracted from 0.05 g of skin tissues using Gentra Puregene kits (QIAGEN).
Table 1. Sample used in the epigenetic study of Antarctic minke whale, by
austral summer season, sex and age classes. Age data shown in this tablewere obtained by earplug readings, and were used for calibration purposes.
Age

SeasonSex

2010/2011

F

10

16

9

3

M

7

8

8

2

F

1

8

11

6

2011/2012

M
Total

–10

11 – 20 21–30 31–40

41–
3

Total
41
25

1

27

1

3

1

1

1

7

19

35

29

12

5

100

Fig. 1. Whale body positions compared for methylation levels of CpG sites. Additional three positions (8 – 10, not shown) corresponded to injured parts by cookie cutter shark.
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GOTO, KITAKADO AND PASTENE

Extracted DNA was stored in TE buffer (10 mM Tris-HCl, 1 mM EDTA, pH 8.0). The IWC guidelines
for DNA data quality (IWC, 2009) were followed as much as possible (see Kanda et al., 2014).
Identification of age-related CpG sites in the Antarctic minke whale
The procedure for identification of age-related CpG sites and measurement of methylation levels in
Antarctic minke whales followed Polanowski et al. (2014), and their explanation of procedures isrepeated below. The following three genes (seven CpG sites) were selected because they showed significant correspondence between CpG methylation levels and age in humpback whales: TET2
(CpG+16, CpG + 21 and CpG + 31 sites); CDKN2A (CpG + 297, CpG + 303 and CpG + 309 sites), and
GRIA2 (CpG + 202 site).
Three candidate regulatory region sequences of Antarctic minke whale (Kishida et al., 2015) weretaken from GenBank and BLAT searches of the humpback whale genome. Where candidate genes had
a clearly orthologous regulatory region in the humpback whale genome, primers for amplification of
Antarctic minke whale sequences were designed by eye based on homologous humpback whale
sequences (Table 2).
Measurement of cytosine methylation levels
Methylation levels in the CpG sites were measured with Qiagen PyroMark assays. The pyrosequencing assays were designed using PYROMARK Assay Design Software (Version 2.0.1, Qiagen). Antarctic minke whale DNA was converted using the Epitect Bisulphite Conversion Kit (Qiagen). The
assay regions were PCR amplified using a biotin-labelled, HPLC-purified primer and standard
sequencing grade primer (Table 2). Amplification reactions consisted of 12.5 μl PYROMARK mastermix, 2.5 μl Coral Load, 1 μl each of 5 μM forward and 5 μM reverse primers, 2 μl of bisulphite
converted template DNA and 6 μl of water. Thermocycling conditions were 15 min at 95°C followedby 45 cycles of 30 s at 95°C, 30 s at 56°C and 30 s at 72°C and a final extension step of 10 min at
72°C. Pyrosequencing was performed on a PYROMARK 24 Pyrosequencing System (Qiagen). The
PYROMARK Q24 software gave percentage methylation values for each CpG site.
Comparison between methylation level of CpG sites and age determined by earplug readings
The methylation levels for each of the seven CpG sites were compared to the ages determined byearplug readings, for n = 100 individuals. Linear regression was used to investigate how much of thevariation in CpG site methylation was explained by age differences. The accuracy and precision of the
Antarctic minke whale epigenetic age assays were assessed with a Leave One Out Cross Validation(LOOCV) (Picard and Cook, 1984) analysis for the seven methylation sites combined.
Table 2. Primers used for amplification of Antarctic minke whale
sequences in the identification of age-related CpG sites by the
PyroMark assay.
Sequence Name

8

Sequence (5’ to 3’)

Gria2_F-Bio

Biotin-GGGTGAGTGTGTGAGTGTA

Gria2_R

AAACCCTATCTCCCAAATCCTAC

Gria2_SQACTAAATACAACTTCCAAC

TET2_F

GTGGTTAAAGTAAATAGAAGGT

TET2_R-Bio

Biotin-CAAAAACACTCCCCAATTTCTET2_SQGGTTAAAGTAAATAGAAGGTG

Cdkn2a_F

AGAGATTTTTGGTAAAGGGGAGAT

Cdkn2a_R-Bio

Biotin-CCCCATATACCTTTCAATCCTCC

Cdkn2a_SQ

TTGGGGAGTTTTTAGAT
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Table 3. Data of Antarctic minke whales examined for variation of
methylation levels among body positions (see Fig. 1).
Whale No.

Sex

Body length (m) Body position (Figure 1)

1

Male

5.61

1 – 7; 8 – 10

2

Female6.56

1 – 7; 8 – 10

3

Male

8.66

1 – 7; 8 – 10

4

Male

8.03

1 – 7; 8 – 10

5

Female9.56

1 – 7; 8 – 10

6

Female9.30

1–7; 8

Table 4. Information of additional sampling positions(8 – 10) that corresponded to parts of the body injured
or with Cookie cutter shark marks. D: dorsal side; L:lateral side; and V: ventral side.
Whale No. Injured parts Cookie cutter shark marks
1

8 (D)

9 (L), 10 (V)2–

8 (D), 9 (V), 10 (L)

3

9 (D)

8 (V), 10 (D)4–

8 (V), 9 (L), 10 (L)5–

8 (L), 9 (L), 10 (L)

6

8 (L)

–

Variation of the methylation levels of CpG sites with body position
Six Antarctic minke whales sampled during the 2016/2017 New Scientific Whale Research Programin the Antarctic Ocean (NEWREP-A) survey in the sector comprised of the area between 45° – 150°E
were used for this experiment. Skin samples were collected from four positions of the dorsal side
(positions 1– 4), two positions of the lateral side (positions 5 – 6), and one position of the ventral side
(position 7) (Fig. 1, Table 3). Also, in the case of five whales (all except whale No. 6 in Table 3),
additional sampling was carried out at three positions (8 – 10) that corresponded to parts of the body
injured or with Cookie cutter shark (Isistius brasiliensis) marks (Table 4). Cookie cutter sharks live inthe depths of all the oceans near the equator. Their top teeth are small, pointy and sharp to grasp holdof the whale or other prey’s skin. Turning in a circle, this shark carves a round chunk of flesh out with
its larger razor-sharp, serrated or saw-like bottom teeth. In a flash, the cookie cutter scoops out themeal. Its preys are left with an almost perfectly round mark that looks like someone used a roundcookie cutter on its body (Compagno, 1984). In the case of whale No. 6, only one additional position
was investigated (position 8; Table 3). In total, 58 skin samples were collected for this experiment.
Tissue preservation, DNA extraction and DNA-M procedures were the same as explained earlier.
Methylation levels of the seven CpG sites in each of the six whales were compared among the seven
body positions shown in Fig. 1.

Results

Identification of age-related epigenetic markers in Antarctic minke whale
The PCR amplifications using a biotin-labelled primer set for the three genes were checked for quality by the agarose gel. The three genes for all individuals were amplified successfully. After pyrosequencing assay, the quality checks by PYROMARK Q24 software were evaluated as high (passed) for
the three genes of all individuals and methylation levels for each CpG site were assessed.
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Comparison between cytosine methylation level and age determined by earplug readings
The regressions of age and methylation levels in each of the seven CpG sites are shown in Fig. 2.
The highest R2 was observed in site TET2_CpG + 31 (0.1874) and the lowest in site CDKN2A_
CpG+297 (< 0.0001). Four CpG sites had a significant regression relationship with age (TET2_
CpG + 16, P = 0.014; TET2_CpG + 21, P = 0.009; TET2_CpG + 31, P = 6.88e-06; and CDKN2A_
CpG + 309, P = 0.005). The other three sites (GRIA2_CpG + 202, CDKN2A_CpG + 297 and
CDKN2A_CpG + 303) had a non-significant regression relationship with age (P > 0.05).
The precision of the Antarctic minke whale epigenetic age assay as assessed by the LOOCV isshown in Fig. 3. The overall precision was estimated as the standard deviation of the mean difference
between known and estimated ages, which was 8.865 years.
Variation of the methylation levels of CpG sites with body position
Fig. 4 shows the variation of the methylation levels of CpG sites at different positions in the whale
body of six individual Antarctic minke whales. This analysis was made for the three genes and sevenCpG sites (excepting some few for which amplification failed). Methylation level of the seven CpG
sites fluctuated with body positions regardless of the body length of the whales. In particular, the three
TET2’s CpG sites showed that the difference between the maximum and the minimum values of methylation levels was 50% or more among body positions. The ratio of maximum and the minimum
methylation level of the TET2’s sites were 2.1 – 3.2 fold in the whale No. 2; 1.3 – 1.7 fold in the whale
No. 5; and 1.6 – 2.4 fold in the whale No. 6 (Table 3; Fig. 4). The average methylation level per indiTET2

TET2

TET2

Fig. 2. Regressions of CpG methylation level and age determined by earplug readings atseven sites selected for Antarctic minke whale. CpG methylation level was measured
at each site by a PyroMark assay in n = 100 whales.

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Fig. 3. The precision of the Antarctic
minke whale epigenetic age assay by a
Leave One Out Cross Validation(LOOCV) analysis for seven CpG methylation sites combined. 95% confidence
limits for age prediction are shown.

Fig. 4. Comparison of CpG methylation levels at multiple body positions in six individual Antarctic minke
whales: ( ) GRIA2_CpG+202, ( ) TET2_CpG+16,( ) TET2_CpG + 21, ( ) TET2_CpG + 31, ( )CDKN2A_CpG+297, ( ) CDKN2A_CpG+303 and( ) CDKN2A_CpG+309. See Figure 1 for explanation of body positions.
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GOTO, KITAKADO AND PASTENE

vidual, per TET2’s site was 12.5% in the four dorsal positions, 11.5% in the two lateral positions and7.5% in the ventral position. The three TET2’s sites in three individuals (whales No. 2, 5 and 6)
showed the lowest methylation level in body position seven (ventral side), compared with the otherpositions (Table 3; Fig. 4).
Regarding additional sampling positions (8 – 10) that corresponded to parts of the body with Cookie
cutter shark marks, the average methylation level per individual, per TET2’s site in the whales No. 2
and 5 was 10.2%. This value was lower than the average methylation level in the four dorsal positions
or in the two lateral positions, and higher than in the single ventral position.

Discussion

This study provided a good opportunity to compare the utility of the same CpG sites to determining
age in two baleen whale species. The present study took advantages of a substantial number of Antarctic minke whales for which age had been determined independently by earplug readings. Suchinformation was of great utility for calibration purposes.
As noted earlier chronological age is important for assessment purposes related to the Antarctic
minke whale such as that conducted using SCAA (Punt et al., 2014). Such models require precise
information on the age of individual whales. In this regard the precision of the age estimates by the
CpG methylation approach was low in both humpback (standard deviation of 2.991 years, Polanowski
et al., 2014) and Antarctic minke (standard deviation of 8.865 years) whales. It should be noted that
the LOOCV estimates of standard deviation in both species are not comparable as the analysis in
humpback whales was based on three sites while the Antarctic minke whale analysis was based onseven sites. In any case, the low precision in both cases makes the age estimated by the CpG methylation approach unsuitable for use in population dynamics models such as the SCAA. Kitakado(2016) showed that the precision of methylation-based recruitment in the Antarctic minke whale ismuch worse than that for earplug-based readings, with the methylation-based results hardly better thanthose without any age information at all.
On the other hand the CpG methylation technique does not provide the chronological age of theindividuals but rather a physiological age that can be used as a proxy for chronological age. Thus
physiological and metabolic differences between species, means that the technique will need to becalibrated for each species (IWC, 2016). This study made a contribution in this regard as the performance of the same genetic markers was compared between two different species of baleen whales. In
fact, some differences were observed between the two species in the pattern of methylation levels withrespect to the age. For example in the case of the humpback whale all seven loci showed significant
regression with age while in the case of the Antarctic minke whale only four of those loci showed asignificant regression relationship. Tanabe et al. (2020) concluded that age-related CpGs can differ
even between closely related species, and that it is necessary to find species-specific age-related CpGs
for estimating the age of animals using this technique.
This present study found that CpG methylation levels vary substantially among different parts of the
body from which skin samples were obtained. In particular differences were observed between dorsal(body parts exposed to sunlight) and ventral (body parts not exposed to sunlight). Gronniger et al.
(2010) showed that aging and sun exposure are associated with comparably small, but significant
changes in the DNA methylation patterns of human epidermis and dermis samples. There is a need tobetter understand the ‘stressors’ (e.g. sunlight) that may affect the calibration of the methylation
approach and further studies should be conducted in the future. On the other hand, the effects on
methylation levels of acquired external injures including Cookie cutter shark marks might be minimal
for the Antarctic minke whales.
The screening of a substantial number of CpG sites based on Human BeadChip microarray has

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EPIGENETIC ESTIMATION OF AGE OF THE ANTARCTIC MINKE WHALE

already started for the Antarctic minke whale, and results will be presented in the near future. Precisionof the CpG methylation technique for age estimation could be improved by increasing the number of
CpG sites showing a good correlation with age.
Apart from increasing the number of CpG sites to increase the precision of the age estimates, otheraspects should be considered to further evaluate the utility of the CpG methylation approach as a proxyof chronological age in baleen whales. For example, correlation between chronological age and methylation profile varies a great deal among different tissues (Horvath, 2013). In addition to skin, biopsy
samples typically include connective tissue and the lipid filled fat cells and these tissues should also
be investigated (Arner et al., 2015). These studies should continue in the future using a large numberof CpG sites and whales.

Acknowledgements

We thank the researchers and crew members that participated in JARPAII and NEWREP-A surveys
for the collection of the genetic samples used in this study. We express our gratitude to T. Bando(Institute of Cetacean Research) for providing age information of Antarctic minke whales used in thisstudy. We also thank M. Taguchi (Institute of Cetacean Research) for her useful suggestions on thisstudy, and H. Oikawa (Institute of Cetacean Research) for his laboratory assistance. Finally, we are
deeply grateful for the fair and constructive reviews of anonymous reviewers.

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Gronniger, E., Weber, B., Heil, O., Peters, N., Stab, F., Wenck, H., Korn, B., Winnefeld, M. and Lyko, F. 2010. Aging andchronic sun exposure cause distinct epigenetic changes in human skin. PLoS Genetics 6, e1000971.
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Deconde, R., Chen, M., Rajapakse, I., Friend, S., Ideker, T. and Zhang, K. 2013. Genome-wide methylation profiles
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International Whaling Commission. 2016. Report of the Expert Panel to Review the Proposal by Japan for NEWREP-A.
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Kanda, N., Goto, M., Oikawa, H. and Pastene, L. A. 2014. Update of note on sampling and laboratory procedure protocolsof the genetic work at the Institute of Cetacean Research (SC/F14/J27rev). Paper SC/65b/DNA1 presented to the IWC
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smell and taste in whales. Zoological Letters 1: 9.
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Lockyer, C. 1984. Age determination by means of the earplug in baleen whales. Rep. int. Whal. Commn. 34: 692 – 696.
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using the method of gelatinized extraction of earplug. NAMMCO Sci. Publ. doi: 10.7557/3.260.
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Mol. Ecol. Resour. 14(5): 976–987.
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J. Cetacean Res. Manage. 14: 81–92.
Punt, A. E., Hakamada, T., Bando, T. and Kitakado, T. 2014. Assessment of Antarctic minke whales using statistical catchat-age analysis. J. Cetacean Res. Manage. 14: 93 – 116.
Tanabe, A., Shimizu, R., Osawa, Y., Suzuki, M., Ito, S., Goto, M., Pastene, L. A., Fujise, Y. and Sahara, H. 2020. Ageestimation by DNA methylation in Antarctic minke whale. Fish. Sci. 86(1): 35 – 41.
Yasunaga, G., Pastene, L. A., Bando, T., Hakamada, T. and Fujise, Y. 2017. Age estimation of Antarctic minke whales
Balaenoptera bonaerensis based on aspartic acid racemization technique Fish. Sci. 83: 947 – 954
Zenitani, R. and Kato, H. 2010. The growth of baleen plates in Antarctic minke whales, with special reference to the
V-Shape notch appearing at the outer edge of the plates. Nippon Suisan Gakkaishi 76: 870 – 876 (in Japanese withEnglish abstract).

Received: October 16, 2019
Accepted: March 10, 2020

© ICR
Photo 1. Antarctic minke whale

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DENSITY DISTRIBUTION OF ANTARCTIC WHALES

Full paper

DENSITY DISTRIBUTION OF SEVERAL MAJOR
WHALE SPECIES IN THE INDO-PACIFIC REGIONOF ANTARCTIC USING JARPA AND JARPAIISIGHTING DATA OBTAINED THROUGH
1987/88 –2008/09 SEASONS
Koji MATSUOKA* and Takashi HAKAMADA
Institute of Cetacean Research, 4 – 5 Toyomi-cho, Chuo-ku, Tokyo 104 – 0055, Japan(*Corresponding author: matsuoka@cetacean.jp)

Abstract
This paper examined the geographical distribution of several whale species in the IndoPacific region of the Antarctic during the austral summer. The analyses were based on sighting
data collected systematically by JARPA and JARPAII surveys in the longitudinal sector of
35°E – 145°W, south of 60°S, between 1987/88 and 2008/09. The searching effort comprised a
total of 353,134 n.miles. The Antarctic minke whale was the species most frequently sighted,
followed by killer, humpback, unidentified beaked, fin, sperm, southern bottlenose, blue, southern right and sei whales. Density index of whales (DIW: no. of individuals sighted/100 n.miles)
was calculated using all primary effort and sightings data and its geographical distribution plotted on maps with Lat. 1 degree × Long. 1 degree squares for each species. These maps are moredetailed compared to those of the previous maps which used 5° × 5°squares in the 1960s. The
geographical distribution was described for each whale species together with some features of
their distribution. For example, sei, dwarf minke, humpback and southern bottlenose whales
were not sighted in the Ross Sea, distribution areas of southern right whales were limited to thesector 80°E and 135°E, and high-density areas of humpback whales were observed between
80°E and 110°E. The large scale and long-term sighting data set has made a substantial contribution to understanding the geographical distribution patterns and habitat use of whales in the
Antarctic ecosystem.
Key words: Antarctic, distribution, baleen whales, toothed whales.

Introduction

One of the main sources of large scale and long-term sighting data for assessing the population
status of whale species in the Antarctic is the JARPA (Japanese Whale Research Program under Special
Permit in the Antarctic), the first phase of which was conducted between 1987/88 and 2004/05, with
its second phase, JARPAII (sighting component), conducted between 2005/06 and 2008/09. One of
the features of JARPA and JARPAII is that, unlike the IWC/IDCR (International Whaling Commission/
International Decade for Cetacean Research)-SOWER (Southern Ocean Whale and Ecosystem
Research) programmes conducted from 1978/79 to 2009/10 (Matsuoka et al., 2003a), surveys havebeen repeated in the same area and in the same months every second season over a long period. CurCetacean Population Studies (CPOPS)
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MATSUOKA AND HAKAMADA

rent distribution maps are more detailed for each Area compared to those of the IDCR/SOWER maps
which had covered the area only three times for each set of circumpolar data on whales. Therefore,
the JARPA and JARPAII surveys facilitate description of the extent of detailed local distribution ofwhales.
The sighting data collected during the JARPA and JARPAII have been used for studying the distribution patterns and estimated abundance of several large whale species (Kishino et al., 1991;
Kasamatsu et al., 2000; Matsuoka et al., 2003b, 2011; Branch et al., 2004; Murase et al., 2002, 2014).
The objective of this study was to investigate the geographical distribution patterns of large whale
species in the Indo-Pacific region of the Antarctic during the austral summer feeding season. The study
was based on sighting data collected systematically by the JARPA and JARPAII surveys.

Materials and Methods

Research area
The research area comprised the Indo-Pacific region of the Antarctic every year, specifically the IWC
Management Areas IIIE (35° – 70°E), IV (70° – 130°E), V (130°E – 170°W) and VIW (170° – 145°W),
south of 60°S (Fig. 1). Each individual survey was conducted from December to March during australsummer (Fig. 2).
These Areas were divided into two sectors (western sector and eastern sector). Each sector was also
divided into two strata (northern and southern strata), along the 60°S latitude line to the line of 45 n.miles
from the ice-edge (northern stratum), and ice-edge to 45 n.miles from the ice-edge line (southern stratum),except for the Prydz Bay and the Ross Sea regions. The Prydz Bay is defined as south of 66°S, and theRoss Sea is defined as south of 69°S. There are no stratifications for Areas IIIE and VIW in JARPA. In
JARPAII, there are stratifications for Areas IIIE and VIW which are the same as in Area IV (Fig. 3).

Fig. 1. The main research area of the JARPA and JARPAII surveys between 35°E and 145°W, south of 60°S withsearching efforts (red lines) in the period 1987/88–2008/09, including the transit sighting surveys between low
latitude and Antarctic regions with the IWC Antarctic Areas for the management of baleen whales (except
Bryde’s whale).

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DENSITY DISTRIBUTION OF ANTARCTIC WHALES

Sighting data
The collection procedures and analyses of sighting data that have been used in JARPA are very
similar to those used in IWC/IDCR-SOWER cruises. Activities aboard the ship are classified into two
principal groups: On-effort and Off-effort. On-effort activities are times when full search effort is being
executed and conditions (such as weather and sea conditions) are within acceptable parameters to
conduct research. Off-effort activities are all activities that are not On-effort. All sightings recorded
while the ship is On-effort are classified as Primary sightings. All other sightings are Secondary sightings.
Primary search effort is only conducted in acceptable weather conditions. These conditions aredefined as visibility better than 2.0 n.miles, with wind speed less than 20 knots and Beaufort sea stateless than 6. These conditions are used as guidelines; in some circumstances, less severe conditions
may still be inappropriate for search effort. The sighting procedure in JARPAII (2005/06 – 2008/09)
did not differ substantially from JARPA (Hakamada et al., 2006; Nishiwaki et al., 2014).
The research vessels (ship length averages about 70 meters) were equipped with a top barrel (almost
20 meters from the sea level), from which three men conducted sighting observations. On the upper
bridge (almost 11.5 meter from the sea level), a captain, a gunner, a helmsman and a researcher also
conducted sightings. The sighting activity was carried out from 30 minutes after sunrise to 30 minutes
before sunset. The survey ship speed averages about 11.5 knots.
When a sighting is made, the topman (or upper bridge observer) gives an estimate of the distanceand angle to the sighting and the ship turns immediately, regardless of the angle to the sighting. The
whales were approached and the species, number of animals and number of calves (if present) determined. In order to save valuable research time, closure to the sighting position of whales that can bepositively identified as long-diving species (such as sperm whales or beaked whales) may be abandoned if it is considered that the animals have dived.
In addition, using the round-trip transit sighting surveys were also conducted every season between
low latitude and Antarctic regions, although the searching effort was low compared to that south of
60°S (Fig. 1).

Fig. 2. Start and end dates of JARPA and JARPA II surveys (1989/90–
2008/09) in the research area.
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MATSUOKA AND HAKAMADA

III-E
1

1 9 8 9 /9 0

1 9 9 1 /9 2

1 9 9 3 /9 4

IV-NW IV-NE
5
2

IV-NW IV-NE
5
1

IV-NW IV-NE
5
2

IV-SW
3

IV-SW
3

IV-SW
3

IV-SE
1

IV-SE
2

1 9 9 5 /9 6

IV-SE
1

IV-NW IV-NE
3
5

III-E
1

IV-SW
2

IV-PB
4

IV-PB
4

IV-PB
4

IV-PB
4

1 9 9 7 /9 8

1 9 9 9 /0 0

2 0 0 1 /0 2

2 0 0 3 /0 4

IV-NW IV-NE
2
4

IV-NW IV-NE
2
3

IV-NW IV-NE
2
3

IV-SW
5

IV-SE
3

III-E
1

IV-SW
5

IV-PB
6

IV-SE
4

IV-PB
6

2 0 0 5 /0 6
III-NE IV-NW IV-NE V-NW
34
62
III-SE IV-SW IV-SE V-SW
3
4
6
2

V-NE
1
V-SE
1

III-E
1

IV-SW
5

IV-SE
4

IV-NW IV-NE
2
3

III-E
1

IV-SW
5

IV-PB
6

IV-PB
6

2 0 0 7 /0 8
III-NE IV-NW IV-NE V-NW
1
2
3
4
III-SE IV-SW IV-SE V-SW
12
3
4

unsurveyed

IV-PB
5

IV-SE
6

IV-SE
4

V-NE
V-SE

unsurveyed

IV-PB
unsurveyed

1 9 9 0 /9 1

1 9 9 2 /9 3

1 9 9 4 /9 5

1 9 9 6 /9 7

V-NW
2

V-NE
4

V-NW
3

V-NE
1

V-NW
2

V-NE
3

V-NW
4

V-NE
2

V-SW
1

V-SE
3

V-SW
2

V-SE
4

V-SW
1

V-SE
4

V-SW
3

V-SE
5

1 9 9 8 /9 9
V-NW
2

V-NE
1

V-SW
3

V-SE
4

2 0 0 0 /0 1
VI-W
5

V-NW
4

V-NE
2

V-SW
5

V-SE
3

2 0 0 6 /0 7

2 0 0 2 /0 3
VI-W
1

V-NW
4

V-NE
2

V-SW
5

V-SE
3

VI-W
1

2 0 0 4 /0 5
VI-W
1

V-NW
4

V-NE
2

V-SW
5

V-SE
3

VI-W
1

2 0 0 8 /0 9

V-NW
4

V-NE
2

VI-NW
1

V-SW
4

V-SE
3

VI-SW
1

V-NW
1

V-NE
4

VI-NW
2

V-SW
1

V-SE
3

VI-SW
2

Fig. 3. Survey order by strata for the period from 1989/90 to 2008/09 seasons. Key: III= Area III, IV= Area IV,
V = Area V, VI = Area VI, E = East, W = West, NW= North-West, NE= North-East, SW= South-West, SE= SouthEast, PB = Prydz Bay. A common number in a season indicates that two strata were surveyed in the same
period. V-NE, V-SE and IV-PB strata could not be surveyed at all in 2007/08 season (Hakamada and Matsuoka,
2014a).

Density index of whales and mean school size
The Density Index of Whales (DIW), i.e. the number of individual whales sighted per 100 n.miles,
was calculated for each Lat.1° × Long.1° grid square. The mean school size (Mss) in this study is thearithmetic mean (i.e. number of animals divided by number of schools).

18

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DENSITY DISTRIBUTION OF ANTARCTIC WHALESResults and Discussion

Searching efforts
A total of 353,134 n.miles were surveyed in Areas IIIE, IV, V and VIW, south of 60°S, between
1989/90 and 2008/09. Fig. 4 shows the distribution of the primary searching effort (n.miles). All gridsquares were searched and the research area south of 60°S was completely covered.
Distribution of whales
Tables 1a and 1b show a summary of the primary sightings of baleen and toothed whales, respec-

Fig. 4. Distribution of the primary searching effort by Lat.1° × Long.1° squares in JARPA and JARPAII
surveys in the period 1987/88 – 2008/09 seasons.
Table 1a. Summary of baleen whale species sighted in the Indo-Pacific region of the Antarctic.
No.

SeasonResearch Effort
area(n.miles)Blue whale

Fin whalesch. ind. calfsch.

Sei whale

Ant. minke whale

Dwarf minke
whale

Humpback whale

S. right whaleind.

calf sch. ind. calf

sch.

ind.

calf sch. ind. calf

sch.

ind.

calf sch. ind. calf

1

1987/88IV

8,860.6

0

0

0

3

3

0

1

1

0

237

719

0

1

2

0

35

76

0

1

1

0

2

1988/89

V

10,806.7

2

3

0

7

16

0

0

0

0

353

768

0

5

5

0

1

2

0

0

0

0

3

1989/90IV

16,423.2

5

9

0

5

20

0

0

0

0

758

1,968

0

3

3

0

121

210

11

2

2

0

4

1990/91

V

14,660.0

4

6

0

33

67

0

0

0

0

740

1,713

0

6

6

0

58

90

0

0

0

0

5

1991/92

IV

17,844.1

3

3

0

8

34

0

2

2

0

597

2,030

0

0

0

0

177

321

7

26

30

0

6

1992/93

V

13,924.9

7

9

0

15

27

1

2

4

0

1,024

3,228

0

7

7

0

28

56

5

3

4

0

7

1993/94

IV

17,957.3

5

9

0

9

26

0

0

0

0

688

1,619

0

4

4

0

133

220

1

11

14

0

8

1994/95

V

14,047.7

13

20

1

73

241

1

2

5

0

823

2,453

0

6

6

0

131

228

9

0

0

0

9

1995/96

IIIE, IV

21,466.7

9

16

0

60

214

1

0

0

0

887

2,008

0

2

2

0

325

562

10

8

8

0

10

1996/97

V, VIW

17,783.2

7

9

0

37

82

1

1

1

0

853

2,610

0

9

9

0

114

200

3

0

0

0

11

1997/98

IIIE, IV

21,594.4

16

25

0

18

57

0

0

0

0

672

1,373

0

2

2

0

577

1,122

2

34

37

0

12

1998/99

V, VIW

8,066.5

4

7

1

45

222

1

0

0

0

826

2,665

0

3

3

0

106

203

7

0

0

0

13

1999/2000

IIIE, IV

16,341.5

25

53

2

66

356

3

0

0

0

1,507

6,581

0

0

0

0

661

1,269

5

3

3

0

14

2000/01

V, VIW

20,421.3

10

18

0

114

374

0

7

13

0

1,907

4,949

0

27

27

0

191

341

3

2

2

0

15

2001/02

IIIE, IV

19,767.4

17

26

1

143

983

2

1

2

0

1,867

4,374

0

0

0

0

1,219

2,387

5

15

22

1

16

2002/03

V, VIW

18,126.2

5

10

0

52

216

0

8

14

0

2,420

6,531

0

6

6

0

145

228

4

0

0

0

17

2003/04

IIIE, IV

19,287.4

32

61

0

109

446

0

0

0

0

1,092

3,250

0

2

2

0

1,690

3,134

5

1

2

1

18

2004/05

V, VIW

18,486.7

12

16

0

49

118

1

1

1

0

1,663

4,278

0

0

0

0

197

336

2

2

2

0

19

2005/06

IIIE, IV

16,372.7

24

38

2

188

748

1

2

3

0

1,657

4,375

0

0

0

0

1,702

3,200

22

53

73

4

20

2006/07

V, VIW

11,968.8

7

12

1

37

253

0

0

0

0

969

2,169

0

1

1

0

160

283

13

0

0

0

21

2007/08

IIIE, IV

14,575.3

43

84

1

48

134

4

2

2

0

823

1,702

0

0

0

0

1,314

2,536

7

72

96

0

22

2008/09

V, VIW

14,351.4

14

28

1

109

440

2

5

7

0

1,870

4,668

0

0

0

0

339

587

8

0

0

0

-

Total

-

353,134

264 46210

1,228 5,077

18

34

55

0

24,233 66,031

0

84

85

0

9,424 17,591 129 233 296

6

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MATSUOKA AND HAKAMADA

Table 1b. Summary of toothed whale species sighted in the Indo-Pacific region of the Antarctic.
Research Effort
area(n.miles)S. bottlenose
whale

Sperm whale

Unid. beaked
whalesKiller whale

No.

Season

sch.

ind.

calf

sch.

ind.

calf

sch.

ind.

calf

sch.

ind.

calf

1

1987/88IV

8,860.6

6

6

0

3

5

0

87

218

0

20

194

0

2

1988/89

V

10,806.7

81

91

0

2

4

0

65

143

0

31

189

0

3

1989/90IV

16,423.2

204

215

0

23

46

0

281

514

0

69

859

0

4

1990/91

V

14,660.0

175

188

0

13

26

0

241

421

1

32

870

2

5

1991/92

IV

17,844.1

225

233

0

29

51

0

181

304

1

53

805

0

6

1992/93

V

13,924.9

105

108

0

10

19

0

202

361

0

82

1,130

0

7

1993/94

IV

17,957.3

321

336

0

145

243

0

205

337

0

56

399

1

8

1994/95

V

14,047.7

133

135

0

74

146

1

168

263

0

35

281

1

9

1995/96

IIIE, IV

21,466.7

341

352

0

137

273

1

161

284

0

109

1,282

1

10

1996/97

V, VIW

17,783.2

121

128

0

75

128

0

78

144

1

50

539

4

11

1997/98

IIIE, IV

21,594.4

295

302

0

222

409

0

197

338

0

82

931

9

12

1998/99

V, VIW

8,066.5

49

50

0

23

53

0

35

54

0

35

409

5

13

1999/2000

IIIE, IV

16,341.5

195

204

0

138

251

0

110

188

0

109

2,011

7

14

2000/01

V, VIW

20,421.3

100

106

0

72

121

0

173

272

0

72

1,471

2

15

2001/02

IIIE, IV

19,767.4

269

272

0

126

226

0

134

205

0

79

939

0

16

2002/03

V, VIW

18,126.2

128

129

0

97

168

0

113

154

0

63

953

0

17

2003/04

IIIE, IV

19,287.4

222

223

0

154

274

0

208

338

0

120

1,348

0

18

2004/05

V, VIW

18,486.7

105

108

0

44

78

0

89

159

0

78

1,472

3

19

2005/06

IIIE, IV

16,372.7

181

182

0

88

179

0

135

244

0

100

1,563

3

20

2006/07

V, VIW

11,968.8

63

63

0

51

80

0

66

88

0

44

394

0

21

2007/08

IIIE, IV

14,575.3

280

280

0

79

157

1

102

155

0

62

790

0

22

2008/09

V, VIW

14,351.4

75

76

0

32

61

0

77

140

0

38

788

14

-

Total

-

353,134

3,674 3,787

0

1,637 2,998

3

3,108 5,324

3

1,419 19,617

52

Table 2. Summary of sighting information for the whole research area in the period 1987/88-2008/09, for whale
species and month. Sch: number of primary sightings of schools; Ind: number of primary sightings of individuals; Calf: number of calves; Mss: mean school size (Ind./Sch.); DIS: Density Index (schools/100 n.miles);
DIW: Density Index (individuals/100 n.miles).
All Areas (IIIE, IV, V and VIW;
south of 60S, 35E-145W)

Species
Sch.

Ind.

Order
of

Dec.

Jan.

Feb.

Mar.

Calf

Mss

DIS

DIW

DIW

DIW

DIW

DIW

DIW

Blue whale

286

495

11

1.73

0.081

0.140

8

0.281

0.092

0.101

0.102

Fin whale

1,268

5,209

20

4.11

0.359

1.475

5

1.323

0.794

1.760

3.059

Sei whale

36

59

0

1.64

0.010

0.017

11

0.002

0.004

0.020

0.044

0

2.71

7.223 19.561

1

10.173 14.301 33.331 19.436

Antarctic minke whale
Dwarf minke whale

25,507 69,076

0

1.01

0.024

0.024

10

0.008

0.031

0.039

0.008

Humpback whale

10,036 18,770 137

1.87

2.842

5.315

3

3.425

4.842

7.337

6.708

Southern right whale

235

298

6

1.27

0.067

0.084

9

0.001

0.014

0.156

0.292

Sperm whale

3,810

3,926

0

1.03

1.079

1.112

6

1.500

1.272

0.992

0.292

Southern bottlenose whale

1,666

3,045

3

1.83

0.472

0.862

7

0.932

0.974

0.787

0.570

Unid. beaked whale

3,175

5,457

3

1.72

0.899

1.545

4

1.864

1.594

1.123

1.209

Killer whale

1,472

20,56959

13.97 0.417

5.825

2

1.935

5.692

9.303

6.624

20

84

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tively for each individual survey. Table 2 shows the summary of sighting data for each species suchas the number of calves and the observed mean school size. Total DIW for each species were the total
numbers of sighted individuals divided by the total effort and multiplied by 100. Monthly DIW wereobtained similarly. Figs. 5a – 5d show the maps of the DIW for Antarctic blue (Balaenoptera musculusintermedia), fin (B. physalus) and sei (B. borealis), Antarctic minke (B. bonaerensis), dwarf minke (B.
a. subsp.), humpback (Megaptera novaeangliae), southern right (Eubalaena australis), sperm (Physeter macrocephalus), southern bottlenose (Hyperoodon planifrons), unidentified beaked (Ziphiidae) andkiller (Orcinus orca) whales, for each Lat.1° × Long.1° grid square. Figs. 6a and 6b show the longitudinal band of DIW for each species. Figs. 7a and 7b show the latitudinal band of DIW for eachspecies. Fig. 8 shows a plot with time trends of DIW for each species. Fig. 9 shows the monthly change
in DIW for most of the species.
A description of the geographical distribution of each whale species is presented and discussed
below.
Blue whale
Blue whale ranked 8th for DIW among the ten species sighted in the research area (Table 2). Blue
whales were widely distributed in the research area, not only in the northern stratum, but also in thesouthern stratum. High density values were recorded for this species in Area IIIE, particularly between
45°E and 65°E (Fig. 5a). Blue whales were rarely found in Prydz Bay, but were sighted in the Ross
Sea between 70°S and 77°S. A total of 286 schools (495 individuals), including eleven calves, weresighted south of 60°S (Table 2). Observed mean school size was 1.73 individuals. Sighting rate of amother and calf pair was 3.85% (11 out of 286 schools) which is the highest number compared to otherbaleen whale species in the Antarctic. A high-density area was observed between 35°E and 65°E (Fig.
6a). The DIW of this species was 0.140 for the whole survey period and the indices were almost
stable from December to March (Table 2; Fig. 9). Previous studies have noted that blue whales are
more common close to the ice edge than in more northerly waters (e.g. Kasamatsu et al., 2000). Thisappears to be true for 110°E eastward, although there are blue whale sightings at or around 60°S in
the region 45°E – 110°E (Figs. 6a and 7a). Similar distribution pattern was observed by Branch (2007).
Two subspecies of blue whales exist in the Southern Hemisphere: the Antarctic (or true) blue whale(Balaenoptera musculus intermedia) and the pygmy blue whale (B. m. brevicauda) (Mackintosh, 1966;
Ichihara, 1966; Rice, 1998). Complete reviews of the spatial and seasonal distributions, as well as
densities and movements of blue whales has been provided by Kato et al. (1995), Branch (2007) and
Branch et al. (2007), respectively. These studies indicated that there is little evidence that pygmy blue
whales migrate to high latitudes of the Antarctic, with less than 1% of the records south of 52°S beingof this subspecies. There have been a couple of genetic studies reporting some population structure in
Antarctic blue whales (Sremba et al., 2012, Attard et al., 2016), but there is limited evidence for multiple separate populations in these papers.
The latest abundance estimate of this species (south of 60°S, 35°E – 145°W) was 1,223 whales(CV = 0.345) in the 2007/08 and 2008/09 seasons, and the abundance trend was 8.2% (95% CI: 3.9%,
12.5%) between 1995/96 and 2008/09 combined for Areas IIIE, IV, V and VIW, based on JARPA and
JARPAII data (Matsuoka and Hakamada, 2014). In this study, no formal analysis has been conducted
but it is probable that the trend of DIW is increasing (Fig. 8). There is a need for continued monitoringof the abundance and abundance trends of this species, especially because it provides an excellent
opportunity to improve our understanding of the dynamics of baleen whale populations recoveringfrom low levels.
Fin whale
Fin whales ranked 5th for DIW among the ten species sighted in the research area. A total of 1,268
schools (5,209 individuals), including 20 calves, were sighted (Table 2). Observed mean school size
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MATSUOKA AND HAKAMADA

was 4.11 individuals. This species was more frequently encountered in Areas V and VIW than in Areas
IIIE and IV in both northern and southern strata. High density areas were observed in Areas IIIE andIV, particularly between 55°E and 80°E, and in Area V between 163°E and 170°W (Figs. 5a and 6a).
Fin whales tended to be distributed more northerly than blue whales (Fig. 7a). The DIW of this species
was 1.475 for the whole period and the indices increased from December to March (Fig. 9).
In the summer feeding grounds in the Antarctic, fin whales occur year-round, but a higher density
is found from November to May (Kasamatsu et al., 1996; Mackintosh, 1966). These whales can befound as far south as 65 – 70°S, but most of the population seems to occur north of 60°S (Miyashita
et al., 1995). Catches occurred throughout the Antarctic, but most whales (~73%) were taken in IWC
Management Areas II and III (Kasamatsu et al., 1996). Sighting data of this study suggest that the fin
whale’s spatial distribution varies across ocean basins. In this study, no formal analysis has been conducted but it is probable that there is an increasing trend of DIW (Fig. 8). Historically more blue
whales were caught than fin whales in the earlier years of pelagic whaling, and thus fin whales arelikely less depleted than blue whales now, given their much higher sighting rates. There have been acouple of genetic studies on population structure for fin whales in the management Areas III, IV, V
and VI (e.g. Goto and Taguchi, 2019), but these studies did not find any genetic structure in the
research area.
Sei whale
The sei whale was rarely sighted in the research area. A total of 36 schools (59 individuals) weresighted south of 60°S (Table 2), with no calves observed. Observed mean school size was 1.64 individuals. Sei whales occurred more frequently in Areas V and VIW than in Areas IIIE and IV in thenorthern strata (Fig. 5a). High density areas were observed in Area VW, particularly between 150°E
and 160°E (Fig. 6a). Sei whales were tended to distribute more northerly between 40°S and 45°S
compared to fin and blue whales (Fig. 7a). The DIW of this species was 0.017 for the whole research
period.
In summer, sei whales do not venture into higher latitude waters near the Antarctic continent as muchas some other baleen whales. Most of the population occurs between 40°S and 60°S, usually north of
the Antarctic Convergence (Miyashita et al., 1995). Juveniles are found further north than matureindividuals. Occurrence in low latitude wintering grounds has been recorded from March to December,but abundance peaks from June/July to August/September (Horwood, 1987). In late spring and summer, abundance peaks in November between 30°S and 50°S. As the seasons progress, relatively morewhales are observed south of 40°S and abundance between 50°S and 60°S increases consistently until
March (Horwood, 1987). The results in the present study are consistent with those of previous studies.
Antarctic minke whale
The Antarctic minke whale was the most frequently sighted species throughout the surveys. A totalof 25,507 schools (69,076 individuals) were sighted south of 60°S (Table 2). No calves were observed.
Observed mean school size was 2.71 individuals. High density areas were observed along the ice-edge,
especially between 140°E and 160°E, in the Ross Sea and the Prydz Bay (Fig. 5b). Antarctic minke
whales were widely and evenly distributed in the area south of 60°S (Figs. 6a and 7a). The DIW ofthis species for the whole research period was the highest of all recorded species (19.561). The indicesincreased from December to February and decreased in March (Fig. 9).
In the austral summer, the majority of Antarctic minke whales congregate in the Southern Ocean,with the greatest densities being close to and within the pack ice, and lower densities with increasing
distance from the ice (Kasamatsu et al., 2000; Hakamada and Matsuoka, 2014a; Herr et al., 2019),
including some north of 60°S. Antarctic minke whales are noticeably well adapted to living within theice (Ainley et al., 2007), but the exact proportion of these whales found within the pack ice, and inpolynyas, is currently a source of debate. It is possible that a large proportion of the population exists

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Fig. 5a. DIW of blue, fin and sei whales in the Indo-Pacific region of the Antarctic, based on one degreesquares (whole research period).
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MATSUOKA AND HAKAMADA

within the pack ice, out of reach of ship-based sighting surveys (Murase et al., 2005; 2014; Shimada
and Kato, 2007; Williams et al., 2014).
There have been a couple of genetic studies reporting some population structure in Antarctic minke
whales which indicated at least two stocks in the research areas: P-stock originating from breeding
grounds in the western South Pacific and I-stock originating in the Indian Ocean. The study also suggested that the two stocks overlap geographically in a wide area of the Antarctic located at 130°E–165°E,
which changes by year and sex depending on the krill availability (Pastene and Goto, 2016).
Dwarf minke whale
Distribution of dwarf minke whale was limited within the research area. There were two separate
areas of distribution between 120°E and 147°E, and between 165°E and 170°W in the northern stratum(mainly between 48°S and 63°S), south of Australia and New Zealand (Figs. 5b, 6a and 7a). The dwarf
minke whale has a white band on the flipper that distinguishes it from the Antarctic minke whale, but
it was only recently identified as separate from Antarctic minke whales (Best, 1985; Rice, 1998;
Pastene et al., 2010). Based on previous information, only a small percentage of minke whales in the
Antarctic (south of 60°S) are dwarf minke whales. For example, in the IDCR/SOWER surveys from
1993/94–1997/98, only 0.2% of the identified sightings were dwarf minke whales (2 out of 906)
(Branch and Butterworth, 2001). Based on this, no formal analysis has been conducted but it is probable that less than 0.2% of the minke whales south of 60°S are dwarf minke whales. In this study, only
0.129 % (85 out of 66,031) of the identified sightings were dwarf minke whales south of 60°S. Katoet al. (in press) further examined this aspect by a more extended data set.
Humpback whale
The humpback whale held the 3rd rank among the ten species sighted in the research area. A totalof 10,036 schools (18,770 individuals), including 137 calves, were sighted (Table 2). Observed meanschool size was 1.87 individuals. Humpbacks were widely distributed in the research area in both
northern and southern strata. They were rarely found within Prydz Bay and no sightings occurred southof 73°S in the Ross Sea. This is a very curious difference in their distribution compared to blue whales
and Antarctic minke whales. The current distribution map of this species suggests that humpback
whales are encountered more frequently in the sector 80°E – 110°E from the ice-edge to 60°S becauseof its high productivity (Figs. 5b and 6a). A high density area was observed in the north between 58°S
and 65°S (Fig. 7a). In the 80°E – 110°E sector, large scale distribution changes and a “Shift in baleen
whale dominance” from Antarctic minke to humpback whales was observed between 85°E and 110°E(Matsuoka et al., 2011; Matsuoka and Hakamada, 2014; Murase et al., 2014; Hakamada and Matsuoka,
2014b). The DIW of this species was 5.315 for the whole survey period. Indices increased from
December to February and decreased in March (Fig. 9).
There have been a couple of genetic studies reporting some population structure of humpback
whales in the Antarctic (Pastene et al., 2019), which suggested the core distribution areas for each ofthe ‘D: western Australia stock’ and ‘E1: eastern Australia stock’ and possible mixing areas around
130°E.
IDCR/SOWER circumpolar cruises encountered humpback whales more frequently in the sectors
20°E–40°E, 80°E – 100°E and 150°E – 180° (Branch, 2011). It has been suggested that such changes
are related to changing oceanographic and krill environment conditions such as the effect of regime
shift in global sea-surface temperatures in relation to El Nino-southern oscillation events (Watanabe
et al., 2014; Naganobu et al., 2014). This suggestion should be further investigated in the future.
Southern right whale
A total of 235 schools (298 individuals), including six calves, were sighted (Table 2). Distribution
area of this species was limited at certain longitudes of the sector 80°E – 135°E, south of Western

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Fig. 5b. DIW of Antarctic minke, dwarf minke and humpback whales in the Indo-Pacific region of the
Antarctic, based on one degree squares (whole research period).
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MATSUOKA AND HAKAMADA

Australia (Figs. 5c and 6a). Sighting rate of mother and calf pairs was 2.54% (6 out of 235 schools)
which is highest number compared to other baleen whale species in the Antarctic. Southern rightwhales tended to be distributed more northerly between 40°S and 45°S and more southerly between
62°S and 65°S (Fig. 7a).
The DIW of this species was 0.084 for the whole survey period. Indices increased from December
to March (Fig. 9). In summer, southern right whales migrate south, but generally not as far south asother baleen whale species. Southern right whales appear to occur near the subtropical convergence insummer (January to March) at around 40°S – 50°S (Ohsumi and Kasamatsu, 1985), but there arerecords of these animals much further south, for example, around 60°S – 65°S, south of Australia(Bannister et al., 1999; 2008). The population estimate for the coastal area of Western Australia was
2,400 in 2006 (Bannister, 2008). A current estimate in Area IV south of 60°S is 1,557 individuals (95%CI, 871–2,783), based on JARPAII data for the 2007/08 season (Matsuoka and Hakamada, 2014). This
indicates that southern right whales migrate and make the Antarctic region an important feeding
ground in the Austral summer.
Sperm whale
The sperm whale held the 6th rank among the ten species sighted in the research area. A total of
3,810 schools (3,926 individuals) were sighted. No calves were observed (Table 2). Of these sightings,
most were single large males (96.5%) and, consequently, the observed mean school size was 1.03.
Sperm whales were widely distributed in the research area with high density values being recorded
between 35°E and 100°E and between 170°E and 170°W, in the mouth of the Ross Sea (Figs. 5c and6b). These whales tended to be concentrated on the Antarctic continental slope, on the southern
Kerguelen Plateau, and around the mouth of the Ross Sea, where the depth was usually between 1,000
and 4,000 m. This species was rarely found within Prydz Bay or in the Ross Sea (Fig. 5c). Latitudinally,
sperm whales tended to be distributed between 40°S and 45°S and between 61°S and 73°S (Fig. 7b).
There were no sightings south of 74°S in the Ross Sea. In this study, no formal analysis has been
conducted but it is probable that the trend of DIW was stable (Fig. 8). The DIW of this species was
1.081 for the whole research period. The indices decreased from December to March (Fig. 9).
Southern bottlenose whales
The southern bottlenose whale was ranked 7th among the ten species sighted in the research area.
A total of 1,666 schools (3,045 individuals), including three calves, were sighted (Table 2). These
whales were widely distributed in the research area but were rarely sighted within Prydz Bay and in
the Ross Sea. High density values of this whale were observed between 35°E and 70°E (Figs. 5c and6b). Southern bottlenose whales were latitudinally distributed between 47°S and 70°S (Fig. 7b).
Observed mean school size was 1.83 individuals. The DIW of this species was 0.862 for the wholesurvey period. Indices decreased from December to March (Fig. 9).
Unidentified beaked whales
Unidentified beaked whales held the 4th rank among the ten species sighted in the research area. A
total of 3,175 schools (5,457 individuals), including three calves, were sighted (Table 2). The sightings
were recorded as unidentified species but confirmed as beaked whales. These ‘unidentified beaked
whales’ possibly included the southern bottlenose whale (Hyperoodon planifrons), Arnoux’s beaked
whale (Berardius arnuxii), strap-toothed whale (Mesoplodon layardii), Grey’s beaked whale (M. grayi)and Cuvier’s beaked whale (Ziphius cavirostris). The distribution pattern of the unidentified beaked
whales was consistent with that of southern bottlenose whales (Fig. 5d).
Killer whale
Killer whales held the 2nd rank among the ten species sighted in the research area. A total of 1,472

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Fig. 5c. DIW of southern right, sperm and southern bottlenose whales in the Indo-Pacific region of the
Antarctic, based on Lat.1° × Long.1° squares (whole research period).
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MATSUOKA AND HAKAMADA

Unid. beaked whale

Fig. 5d. DIW of unidentified beaked and killer whales in the Indo-Pacific region of the Antarctic, basedon Lat.1° × Long.1° squares (whole research period).

schools (20,569 individuals), including 59 calves, were sighted (Table 2). Observed mean school size
was 13.97 individuals. The DIW of this species was 5.825 for the whole study period (Table 2). These
whales were widely distributed in the research area longitudinally and latitudinally (Figs. 6b and 7b),and were more frequently sighted in the southern stratum. High density areas were observed near the
ice-edge or within Prydz Bay and in the Ross Sea where the pack-ice had melted on the continental
shelf slope in February (Figs. 5d, 6b, 7b and 9). Killer whale abundance in the Antarctic was estimatedby Branch and Butterworth (2001), and appears to be far higher than in any other ocean in the world.
In this study, no formal analysis has been conducted but it is probable that the trend of DIW wasstable (Fig. 8). The large school size of killer whales considered to be fish eaters were often sighted
in the Prydz Bay and the Ross Sea. Further analyses will be required to definitively identify the killer
whale type (fish eater or marine mammal eater etc.) as part of ongoing Antarctic ecosystem research.

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DENSITY DISTRIBUTION OF ANTARCTIC WHALESBlue whale

Fin whale

Sei whale

Antarctic minke whale

Dwarf minke whale

Humpback whale

Southern right whale

Fig. 6a. The longitudinal band of DIW for blue, fin, sei, Antarctic minke, dwarf minke, humpback and southern
right whales in the Indo-Pacific region of the Antarctic, based on Lat.1° × Long.1° squares (whole research
period).
Sperm whale

Southern bottlenose whale

Unidentified beaked whale

Killer whale

Fig. 6b. The longitudinal band of DIW for sperm, southern bottlenose, unidentified beaked and killer whales in
the Indo-Pacific region of the Antarctic, based on Lat.1° × Long.1° squares (whole research period).
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MATSUOKA AND HAKAMADABlue whale

Fin whale

Sei whale

Antarctic minke whale

Dwarf minke whale

Humpback whale

Southern right whale

Fig. 7a. The latitudinal band of DIW for blue, fin, sei, Antarctic minke, dwarf minke, humpback and southern
right whales in the Indo-Pacific region of the Antarctic, based on Lat.1° × Long.1° squares (whole research
period).

Sperm whale

Southern bottlenose whale

Unidentified beaked whale

Killer whale

Fig. 7b. The latitudinal band of DIW for sperm, southern bottlenose, unidentified beaked and killer whales in the
Indo-Pacific region of the Antarctic, based on Lat.1° × Long.1° squares (whole research period).

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DENSITY DISTRIBUTION OF ANTARCTIC WHALESBlue whale

Fin whale
4.00

0.05

0.40

3.50

0.04

0.35

0.03

2.50

0.20

2.00

DIW

0.25

DIW

DIW

0.04

3.00

0.30

1.50

0.15

0.05

0.50

0.00

0.00

1987

1991

1995

1999

2003

2007

0.01
1987

1991

1995

30.00

14.00

0.07

12.00

0.02

5.00

0.01

0.00

0.00
2003

2007

1987

1991

1995

1999

2003

0.00

2007

1.80

1.40

1.60

DIW

DIW

0.00

0.00

1991

1995

1999

2003

2007

2003

2007

1.00
0.80
0.60

0.40
0.20

2007

1.20

0.80

0.05

1999

1.40

0.60

0.10

1995

S. bottlenose whale

1.60

1.00

0.15

1991

Season

1.20

1987

1987

Sperm whale

0.20

2003

2.00

S. right whale

0.25

2007

6.00

Season

0.30

2003

4.00

Season

0.35

1999

8.00

0.04

10.00

1995

10.00

0.03

1999

1991

Humpback whale

0.08

DIW

DIW

15.00

1995

1987

Season

0.05

20.00

DIW

0.00

2007

0.06

25.00

DIW

2003

Dwarf minke whale

Ant. minke whale

0.40
0.20
1987

1991

1995

1999

2003

2007

SeasonSeasonUnid. beaked whales

0.00

1987

1991

1995

1999

SeasonKiller whale

3.50

10.00
9.00

3.00

8.00

2.50

7.00
6.00

DIW

2.00
1.50

5.00
4.00
3.00

1.00

2.00

0.50
0.00

1999

Season

35.00

1991

0.02

0.01

Season

1987

0.03

0.02

1.00

0.10

DIW

Sei whale

0.45

1.00
1987

1991

1995

1999

2003

2007

Season

0.00

1987

1991

1995

1999

2003

2007

SeasonFig. 8. Plot with time trends in DIW for each species and unidentified beaked whales in the Indo-Pacific regionof the Antarctic (south of 60°S) during 1987/88 to 2008/09 seasons.

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MATSUOKA AND HAKAMADA

Fig. 9. Yearly trend in DIW for baleen (top) and toothed (bottom) whales inthe the Indo-Pacific region of the Antarctic (south of 60°S) during 1987/88
to 2008/09 seasons.

Conclusions

Importance of monitoring whale populations
Most large whales were heavily exploited during the past century and most of the stocks in theSouthern Hemisphere were substantially depleted. In the Antarctic Ocean, catches of southern right,
humpback, blue, fin and sei whales were prohibited in 1932, 1963, 1964, 1976 and 1978, respectively.
Eighty years have passed since the southern right whale has been protected, and more than 50 years
have passed since the humpback whale and blue whale have been protected. In the coastal waters ofSouth America, South Africa and along the east and west coasts of Australia, significant recovery ofsouthern right whales and humpback whales in these breeding areas has been recently reported. On
the other hand, the information on the present status of pelagic species, such as blue, fin and sei whales
was limited. The IWC/IDCR-SOWER cruises have covered the same area every year for 6 years
however this is insufficient for monitoring the ecosystem. On the other hand, JARPA and JARPAII
have been monitoring baleen whale species populations by large-scale and long-term line transect
surveys for over 30 years in Areas IV and V. However, the survey years is still not enough to detect

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precise yearly trends for whale populations. For this reason, the JASS-A (Japanese Abundance andStock structure Surveys in the Antarctic) was started from the 2019/2020 season as a successor to theJapanese Antarctic survey programs such as JARPAII and NEWREP-A (New Scientific Whale
Research Program in the Antarctic Ocean), in order to continue to provide additional information about
the recovery of whale stocks (Government of Japan, 2019).
Relationship between distribution and oceanographic conditions
There was a common pattern for several whale species to concentrate mainly in the sector
80°E–110°E, south of 60°S. This area is characterised by a large meander (rise to 61°S and slowmoving down to 63°S) of the southern boundary of the Antarctic Circumpolar Current (ACC), which
seems to be caused by large-scale upwelling with nutritious bottom waters, resulting from the bottom
shape of the southern Kerguelen Plateau (Watanabe et al., 2014; Naganobu et al., 2014). The BROKE
Australian Antarctic survey previously indicated the possibility of large-scale upwelling between 80°E
and 100°E (Bindoff et. al., 2000). In the JARPA 1999/2000 cruise, a high density of Euphausiids wasreported between 100°E and 120°E (Murase et al., 2002). Humpback, southern right, large male spermand southern bottlenose whales used this longitudinal section between 80°E and 100°E as their key
feeding area from December to March. It is necessary to further investigate the relationship between
whale distribution and oceanographic condition shifts such as the effect of regime shift in global seasurface temperatures in relation to El Nino-southern oscillation events (Matsuoka et al., 2003;
Watanabe et al., 2014; Naganobu et al., 2006; 2014).

Acknowledgements

We are grateful to all successive cruise leaders, researchers, captain and crew members for their hard
works under difficult conditions in the JARPA and JARPAII surveys from which the data used in thepresent study were collected. We also would like to express our gratitude to Drs. Seiji Ohsumi(deceased), Hiroshi Hatanaka, Hidehiro Kato, Yoshihiro Fujise and Luis Pastene of the Institute of
Cetacean Research, Dr. Tomio Miyashita, the National Research Institute of Far Seas Fisheries(Shimizu), Dr. Hiroto Murase, Tokyo University of Marine Science and Technology, for their usefulcomments on earlier versions of this paper. We also thank to Mr. Nishiwaki Shigetoshi, secretary andother members of the Institute of Cetacean Research (ICR) for their contribution for the database. All
photographs are provided by ICR. The manuscript benefited from helpful comments from threeanonymous reviewers. Finally, we are deeply grateful for the fair and constructive reviews of anonymous reviewers.

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Received: October 17, 2019
Accepted: March 31, 2020
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MATSUOKA AND HAKAMADA© ICR
Photo 1. Two surfacing Antarctic blue whales during biopsy experiment in the Antarctic.

© ICR
Photo 2. Five fin whales surfacing in the Antarctic.

© ICR
Photo 3. Surfacing sei whale.

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DENSITY DISTRIBUTION OF ANTARCTIC WHALES© ICRPhoto 4. Seven Antarctic minke whales surfacing near pack-ice.

© ICR
Photo 5. Surfaced humpback whale in the Antarctic.

© ICR
Photo 6. Surfacing southern right whale during biopsy experiment in the Antarctic.
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MATSUOKA AND HAKAMADA© ICR
Photo 7. Surfacing sperm whales near pack-ice in the Antarctic.

© ICR
Photo 8. Surfacing southern bottlenose whales in the Antarctic.

© ICR
Photo 9. Killer whales in the Antarctic.

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LEGACY POPS LEVELS IN NORTH PACIFIC BALEEN WHALES

Full paper

CONCENTRATION OF PERSISTENT ORGANICPOLLUTANTS (POPs) IN THREE SPECIES OF BALEENWHALES IN THE WESTERN NORTH PACIFIC
Genta YASUNAGA* and Yoshihiro FUJISE
Institute of Cetacean Research, Toyomi Shinko Building 5F, 4 – 5 Toyomi-cho, Chuo-ku,
Tokyo 104–0055, Japan *(Corresponding author: yasunaga@cetacean.jp)

Abstract
Concentrations of PCB congeners and DDT, HCH, HCB and CHL isomers in the blubber offive mature males of each of common minke, sei and Bryde’s whales taken by the Japanese
Whale Research Program under Special Permit in the western North Pacific-Phase II (JARPNII)
in 2011 were determined. For comparison, concentrations of these compounds in the blubberof five mature male Antarctic minke whales taken by the Japanese Whale Research Program
under Special Permit in the Antarctic-Phase II (JARPAII) in 2010/11 in the Pacific sector of the
Antarctic were also determined. Concentrations of PCBs were highest among organochlorines
in the whales from the western North Pacific, and were much higher than PCBs concentrationsin the Antarctic minke whales. Concentrations of HCB, DDTs and CHLs in Antarctic minke
whales were higher or of the same order as North Pacific sei and Bryde’s whales but much lower
than those in North Pacific common minke whales. Differences are explained by the different
trophic levels of the species and or the source of the pollutants. The accumulation of detectable
112 PCB congeners in the whale blubber samples was investigated by principal component
analysis (PCA). Two significant factors, in which 72.5% (PC1) and 8.5% (PC2) of the total
variance in the data were found. These were attributed to possible trophic level and pollution
sources. The main component isomers from pesticide products originating in DDTs and HCHs
were comparatively lower, although high levels of trans-chlordane contained in an insecticide
were not detected in the whales from the western North Pacific. These results suggest that in
the western North Pacific, a great deal of time has passed since the release of DDTs, HCHs andCHLs into the environment.
Key words:

common minke whale, sei whale, Bryde’s whale, North Pacific, organic pollutants, POPs.

Introduction

Persistent organic pollutants (POPs) are organic compounds that are resistant to environmental degradation through chemical and biological processes, therefore they have the potential to be transported
over long distances. The manufacture, use and import/export of the specified compounds have beenstrictly restricted since the adoption of the Stockholm Convention on POPs by the United Nations
Environment Programme in 2001 (Hagen and Walls, 2005). Among them, polychlorinated biphenyls(PCBs), dichloro-diphenyl-trichloroethanes (DDTs), hexachlorocyclohexanes (HCHs), hexachlorobenzene (HCB) and chlordanes (CHLs) are commonly called ‘legacy POPs’ (French et al., 2006), which
had been produced and used in large quantities worldwide since the middle of last century. However,Cetacean Population Studies (CPOPS)
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YASUNAGA AND FUJISE

the legacy POPs remain a major environmental challenge for human health and wildlife risk.
In order to understand the fate of these compounds in the environment, it is necessary to directly
monitor POPs levels in sea water and the atmosphere in the ocean areas which play a role as a final
sink for POPs (Tanabe et al., 1994). However, such monitoring generally produces unrealistic measures because of their extremely low concentrations and instability in the environment (Tanabe andSubramanian, 2006). Consequently, as a possible integrator of POPs, marine organisms such as mussels (Goldberg, 1986), squids (Yamada et al., 1997) and skipjack tuna (Ueno et al., 2003) have been
investigated as bioindicators to monitor the fate and behavior of pollutants in the marine environment.
Baleen whales have also been suggested as a suitable bioindicator for monitoring POPs levels in offshore waters, because they are mobile and long-lived animals, characteristics that mean that POPs canbe monitored in wide sea areas and integrated in some way over time.
In the western North Pacific, yearly change of legacy POPs concentrations in marine mammals havebeen reported previously. Tanabe et al. (1994) reported temporal variation of legacy POPs in female
northern fur seals (Callorhinus ursinus) from 1971 to 1988. The PCB and DDT concentrations showeda maximum around 1976 and then decreased until 1988. HCH concentrations decreased moderately inthe research period. Aono et al. (1997) compared legacy POPs in blubber of common minke whales(Balaenoptera acutorostrata) from the western North Pacific in 1987 with those in 1994. Their results
showed that the concentrations of DDTs, HCHs and HCB in 1987 were comparable or higher thanthose in 1994, whereas concentrations of PCBs and CHLs in 1987 were considerably higher than thosein 1994. On the other hand, Yasunaga, Hakamada and Fujise (2016) reported that yearly changes of
PCB concentrations were not observed in common minke whales from the offshore area in the period
2002–2013. These results imply that PCB concentrations in baleen whales from the western North
Pacific decreased until the end of the decade of the 1990’s and then stabilized since the 2000’s. Marine
mammals are good bioindicators of POPs in the marine environment, although there are limitations
due to confounding factors such as sex, age, metabolism, and feeding (Tanabe and Subramanian, 2006).
The aim of the present study was to investigate the levels of concentration of legacy POPs in three
species of baleen whales in the western North Pacific, common minke, sei (B. borealis) and Bryde’s(B. edeni) whales. Samples from the Antarctic minke whale (B. bonaerensis) were used for comparison. Potentially the outputs from this study can provide a better understanding of the current fate andbehavior of legacy POPs in the marine environment.

Materials and Methods

SamplesCommon minke, sei and Bryde’s whales used in this study were sampled during the 2012 survey of
the Japanese Whale Research Program under Special Permit in the western North Pacific-Phase II(JARPNII). Common minke whales were sampled in sub-area 7, sei whales in sub-area 9 and Bryde’s
whales in sub-areas 8 and 9, excluding the EEZ of foreign countries, which were established by the
Scientific Committee of the International Whaling Commission (IWC) for management purposes(IWC, 1994) (Table 1, Fig. 1). For the analyses, only mature males were used in this study. The rational for this was as follows: (1) lipophilic POPs levels in whale body increase with age especially at
young stage; (2) female whales were not used since accumulation depends on several reproductive
processes such as parturition and lactation (Tanabe and Subramanian, 2006). Males of common minke,
sei and Bryde’s whales were defined as sexually mature by testis weight (larger side) of more than
290 g, 1,090 g and 560 g, respectively (Bando et al., unpublished data). Maturity of one common
minke whale could not be identified by testis weight, however its body length (8.16 m) was much
longer than the maximum body length of the males older than 14 years (mean 7.54 m; n = 57, Zenitani,
Kato and Fujise, 2000). For the purpose of POPs analysis, blubber tissues were obtained from the40

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LEGACY POPS LEVELS IN NORTH PACIFIC BALEEN WHALES

Table 1. Biological data of mature males of common minke, sei and Bryde’s whales
sampled in the western North Pacific, and Antarctic minke whales sampled in the
Antarctic Ocean (see Fig.1 for definition of sub-areas).
Species

Sampling dateCommon minke whale

Sei whale

Bryde’s whale

Fig. 1

Antarctic minke whale

Area

Body length (m)May 22 2012

sub-area 7

7.33

May 22 2012

sub-area 7

7.55

May 25 2012

sub-area 7

7.40

May 25 2012

sub-area 7

7.70

June 1 2012

sub-area 7

8.16

June 18 2012

sub-area 9

13.55

June 25 2012

sub-area 9

13.74

July 2 2012

sub-area 9

13.48

July 16 2012

sub-area 9

14.03

July 19 2012

sub-area 9

13.48

July 22 2012

sub-area 9

12.22

July 24 2012

sub-area 9

12.69

July 25 2012

sub-area 9

13.06

July 26 2012

sub-area 8

13.32

July 27 2012

sub-area 8

13.38

January 5 2011

Antarctic Area V*

8.67

January 16 2011

Antarctic Area V

8.78

January 16 2011

Antarctic Area V

8.35

January 31 2011

Antarctic Area V

8.77

February 2 2011

Antarctic Area V

8.31*: Area V in the Antarctic is comprised between 130°E and 170°W

50˚N

45˚

40˚

Sub-area 7

Sub-area 8

Sub-area 9

35˚
140˚

150˚

160˚

170˚E

Fig. 1. Subareas surveyed by the JARPNII research excluding the EEZ offoreign countries. Sub-areas definitions are based on IWC (1994).
Cetacean Population Studies (CPOPS)
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41

YASUNAGA AND FUJISE

central lateral part of each whale by researchers on board the research base ship. The blubber samples
were stored at – 20°C until chemical analyses. Chemical analyses were also conducted on samples
from five mature male Antarctic minke whales sampled during the 2010/2011 survey of the Japanese
Whale Research Program under Special Permit in the Antarctic-Phase II (JARPAII) in the Pacific sector of the Antarctic (Area V, 130°E-170°W), which were used for comparative purposes (Table 1).
Laboratory analysis
Chemical analyses of the PCBs, DDTs, HCHs, HCB and CHLs were carried at the Miura Instituteof Environmental Science using the standard method described by the Environmental Agency of Japan(Japan Environmental Agency, 1998), with some modifications.
Approximately 10 g of blubber were placed into a glass test tube, surrogate standard was added, andthen homogenized with 20 mL of acetone and 40 mL of n-hexane. Then, the solution was filtered. This
extraction procedure was repeated twice. All the solvent layers were combined and washed with 100
mL of 2% sodium chloride solution. The extracts were filtered through 20 g of anhydrous Na2SO4 andfinally concentrated to 10 mL. Two milliliters of each of the extracts were purified using multilayer
silica gel column chromatography composed of two components – 4 g of silica gel impregnated withsulfuric acid (44% mass fraction: 44% H2SO4-Si) and 3 g of silica gel impregnated with silver nitrate(10% mass fraction: 10% AgNO3-Si). All the analytes were eluted with 200 mL of 5% dichloromethane/nhexane. After that, the clean-up of the extract was performed by gel permeation chromatography(column: Shodex CLNpak PAE-2000AC) in order to remove remaining hydrocarbons. The mobile
phase used acetone with a flow rate of 3.5 mL/min. The eluted solutions were then concentrated.
POPs were determined by a GC-MS (JEOL Ltd., JMS-700; JMS-SX102A). Concentrations of POPs
were expressed on a lipid weight basis (ng/g lipid wt.). The quality control of the data was provided
throughout the analyses by use of the certified reference material ‘Organics in cod liver oil’ (NIST
1588a). The results were 1,626.4 ng/g fresh wt. for ∑PCBs, 596 ng/g for p,p’-DDE, 236 ng/g for p,p’DDD, 417 ng/g for p,p’-DDT, 161.2 ng/g for cis-chlordane, 217.4 ng/g for trans-nonachlor, 67.0 ng/g
for cis-nonachlor, 133 ng/g for HCB, and 78.7 ng/g for α-HCH, while the certified values by NIST
were 1,789.1 ng/g for fresh wt. ∑PCBs, 651 ± 11 ng/g/ for p,p’-DDE, 254 ± 11 ng/g for p,p’-DDD,
524 ± 12 ng/g for p,p’-DDT, 167.0 ± 5.0 ng/g for cis-chlordane, 214.6 ± 7.9 ng/g for trans-nonachlor,
94.8 ± 2.8 ng/g for cis-nonachlor, 157.8 ± 5.0 ng/g for HCB, and 85.3 ± 3.4 ng/g for α-HCH. Here,∑PCBs includes PCB congener numbers 28, 31, 44, 49, 52, 66, 87, 95, 101, 105, 110, 118, 128, 132,
138, 149, 151, 153, 156, 159, 163, 164, 170, 180, 182, 183, 187, 190, 194 and 201 (IUPAC numbering). The detection limit was calculated in accordance with the standard method described by theEnvironmental Agency of Japan (Japan Environmental Agency, 1998), which were 0.3 ng/g lipid wt.
(H6CBs), 0.2 ng/g lipid wt. (α-HCH, β-HCH, oxychlordane, trans-chlordane, trans-nonachlor, cisnonachlor, p,p’-DDE, p,p’-DDD, T4CBs, P5CBs and O8CBs), 0.1 ng/g lipid wt. (γ-HCH, cis-chlordane, p,p’-DDT and H7CBs), 0.08 ng/g lipid wt. (HCB, T3CBs and N9CBs), and 0.04 ng/g lipid wt.
(M1CBs, D2CBs and D10CBs).
Statistical analysis
The concentrations of POPs among species were first analyzed by the Kruskal-Wallis test. Pairwise
comparisons between species were then performed by the Steel-Dwass post hoc test for multiple comparisons. All differences with p < 0.05 were considered statistically significant. Principal component
analysis (PCA) was used to assess the difference of composition of detectable PCB congeners in blubber among species caused by habitats, feeding habits and other biological factors. Principal components were derived from standardized data via the correlation matrix. PCA of all 112 PCB congeners
were computed on the correlation matrix of the untransformed ng/g lipid wt. data and the projectionsof the factor scores of each sample along the first 2 principal component axes (PC1 and PC2) werecomputed. These statistical analyses were executed by SPSS ver.11 for Windows (SPSS Co. Ltd.).

42

Cetacean Population Studies (CPOPS)
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LEGACY POPS LEVELS IN NORTH PACIFIC BALEEN WHALESResults and Discussion

Concentration of POPs
Table 2 shows the concentrations of POPs in blubber of common minke, sei, Bryde’s and Antarctic
minke whales. POPs were detected in all the blubber samples. Relative concentrations of POPs in the
blubber of the whale species were significantly higher in the following orders, PCBs: common minke >sei; Bryde’s > Antarctic minke whales; HCHs: common minke > sei > Bryde’s > Antarctic minke
whales; HCB: common minke; Antarctic minke > sei; Bryde’s whales; CHLs and DDTs: common
minke; sei; Bryde’s > Antarctic minke whales (p < 0.05).
The POPs concentrations in the sample from the North Pacific whales were clearly higher than thosein Antarctic minke whales except for HCB. Concentrations of most POPs such as PCBs levels inenvironmental samples were highest in northern hemisphere temperate locations (ca. 30-70°N) whereanthropogenic usage and atmospheric emissions have been concentrated, whereas relatively volatile
chemicals such as HCB levels in environmental samples are related with absolute latitude in bothhemispheres due to cold condensation (Iwata et al., 1993; Meijer et al., 2003). The levels of PCBs
were highest among POPs in the baleen whales from the northern Pacific, whereas they were comparatively lower than HCB, DDTs and CHLs in Antarctic minke whales. PCBs are still being released
into the environment, whereas production and usage were banned in the 1970s in developed countriesof the middle latitude of the northern hemisphere (Weber and Goerke, 2003). Furthermore, PCBs withhigher lipophilicity are less transportable than the other OCs in the marine environment. Our finding
indicates that PCBs may still be of importance for health effects on aquatic organisms in the western
North Pacific, even though PCB levels have been decreasing in marine mammals here (Tanabe et al.,
1994; Aono et al., 1997; Yasunaga, Hakamada and Fujise, 2016).
In the western North Pacific in particular, PCBs, HCHs and HCB levels in common minke whales
were higher than those in sei and Bryde’s whales. This result is explained by the different feeding
habits of those species. Common minke whales feed mainly on fishes such as Pacific saury and sardine
while that sei and Bryde’s whales feed mainly on zooplankton and smaller fishes (Konishi et al., 2009).
There were no differences in CHLs and DDTs levels among the three species. The effect of diet isparticularly significant because the concentration of many persistent pollutants increases through thefood web, and therefore tissue concentrations in marine mammals depend on concentrations of thePOPs in the food organisms at the various trophic levels. The extent of biomagnification of eachchemical is also influenced by other factors such as chemical and physical properties and metabolism(Aguilar, Borrell and Pastor, 1999).
Composition of PCB congeners
Table 3 shows concentrations of PCB congeners in blubber samples of common minke, sei, Bryde’s
and Antarctic minke whales, and Fig. 2 shows their profiles. The most prevalent congeners in all whale
Table 2. Concentrations of POPs (ng/g lipid wt.) in the blubber of common minke, sei, Bryde’s whales from thewestern North Pacific, and Antarctic minke whales from the Antarctic.
SpeciesnFat (%)

Common minke
whale

5

29.3
3,100
2,000
670
250
1,300
(20.6 - 49.1) (1,400 - 8,000) (800 - 5,800) (410 - 1,500) (160 - 360) (620 - 3,100)

Sei whale5

73.0(65.6 - 77.4)

130(67 - 210)

71
(32 - 130)91
(30 - 150)

21
(15 - 28)59
(31 - 90)

Bryde’s whale5

51.9(17.5 - 79.5)

140(85 - 200)82
(36 - 130)13(7.0 - 19)

17(14 - 22)68
(38 - 88)

Antarctic minke
whale

5

61.2
(44.0 - 75.0)

33(19 - 57)

69
(35 - 110)0.52
(0.22 - 0.89)

140(90 - 250)

34
(18 - 59)

Cetacean Population Studies (CPOPS)
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PCBs

DDTs

HCHs

HCB

CHLs

43

YASUNAGA AND FUJISE

Table 3. Average concentrations of PCB congeners (ng/g lipid wt.) in blubber samples of common minke, sei,
Bryde’s whales from the western North Pacific, and Antarctic minke whales from the Antarctic.
PCB isomers
Nos. of Cl IUPAC No.

Common minke whaleng/g%

Sei whaleng/g%

Bryde’s whaleng/g%Antarctic minke whale
ng/g
%

D2CBs

#10,#4#8,#5#11#12,#13
#15
sum

0.41
1.2
N.D
N.D
0.37
2.0

0.01
0.04
0.00
0.00
0.01
0.06

0.37
0.70
N.D
N.D
0.24
1.3

0.29
0.55
0.00
0.00
0.19
1.0

0.48
1.1
N.D
0.30
0.29
2.2

0.34
0.81
0.00
0.21
0.21
1.6

0.063
0.054
0.053
N.D
0.030
0.20

0.19
0.17
0.16
0.00
0.09
0.61

T3CBs

#19
#18
#17
#24,#27#32,#16#26#25#31,#28#33,#20
#22
#37
sum

N.D
3.6
0.49
0.29
0.87
0.50
0.53
5.6
3.5
0.51
N.D
16

0.00
0.12
0.02
0.01
0.03
0.02
0.02
0.18
0.11
0.02
0.00
0.51

0.11
1.2
0.37
0.15
0.59
0.22
0.15
2.4
0.83
0.43
0.22
6.7

0.09
0.97
0.29
0.12
0.46
0.17
0.12
1.9
0.65
0.34
0.17
5.3

N.D
1.2
0.47
N.D
0.76
0.26
0.23
3.3
1.1
0.62
N.D
7.9

0.00
0.89
0.33
0.00
0.54
0.18
0.16
2.3
0.78
0.44
0.00
5.7

N.D
0.14
0.036
0.031
0.065
0.026
N.D
0.23
0.11
0.045
N.D
0.69

0.00
0.44
0.11
0.09
0.20
0.08
0.00
0.70
0.33
0.14
0.00
2.1

T4CBs

#53
#51
#45
#69,#46#52,#73#43,#49#47,#48,#75#44#59,#42#41#64,#68#40,#57#74#70,#76#80#66#56,#60
sum

2.1
0.82
0.73
N.D
100
14
14
5.0
2.0
2.6
0.65
1.1
63
3.0
N.D
8.0
1.9
220

0.07
0.03
0.02
0.00
3.3
0.45
0.44
0.16
0.07
0.08
0.02
0.03
2.0
0.10
0.00
0.26
0.06
7.2

0.34
N.D
0.34
N.D
8.6
2.4
1.9
2.0
0.45
N.D
0.32
0.26
3.2
0.51
N.D
2.5
0.55
23

0.27
0.00
0.27
0.00
6.8
1.9
1.5
1.6
0.35
0.00
0.25
0.20
2.5
0.40
0.00
2.0
0.43
18

0.30
N.D
N.D
N.D
5.4
1.6
1.3
1.2
0.52
0.46
0.35
N.D
2.7
0.50
N.D
1.4
0.57
16

0.21
0.00
0.00
0.00
3.8
1.2
0.94
0.84
0.37
0.33
0.25
0.00
1.9
0.35
0.00
0.99
0.40
12

0.068
N.D
N.D
0.074
2.0
0.43
0.36
0.27
0.11
0.16
0.37
0.073
0.67
0.093
0.11
0.26
0.058
5.1

0.21
0.00
0.00
0.22
6.2
1.3
1.1
0.82
0.35
0.50
1.1
0.22
2.0
0.28
0.33
0.78
0.18
16

P5CBs

#96
#103
#100
#94
#93
#95
#121,#92#89#84#90,#101#99#119#97,#86#125,#87#117,#115,#85
#110
#82
#124
#123,#106
#118
#114
#122
#105,#127
sum

1.4
1.5
1.4
1.2
2.7
59
14
6.9
2.8
110
190
3.2
6.0
11
N.D
18
2.5
2.0
9.8
220
N.D
0.83
7.7
670

0.05
0.05
0.05
0.04
0.09
1.9
0.47
0.22
0.09
3.4
6.2
0.10
0.19
0.35
0.00
0.58
0.08
0.07
0.31
7.1
0.00
0.03
0.25
22

N.D
N.D
N.D
N.D
N.D
6.6
0.78
1.5
0.85
10
6.0
N.D
1.6
2.0
N.D
1.1
0.44
N.D
0.46
7.6
0.34
N.D
1.6
41

0.00
0.00
0.00
0.00
0.00
5.2
0.61
1.2
0.67
7.8
4.7
0.00
1.2
1.6
0.00
0.82
0.35
0.00
0.36
6.0
0.26
0.00
1.3
32

N.D
N.D
N.D
N.D
N.D
4.4
0.60
N.D
N.D
N.D
6.2
N.D
1.2
1.5
N.D
2.2
0.39
N.D
0.56
9.1
0.40
N.D
1.7
28

0.00
0.00
0.00
0.00
0.00
3.1
0.43
0.00
0.00
0.00
4.4
0.00
0.83
1.1
0.00
1.6
0.28
0.00
0.40
6.5
0.28
0.00
1.2
20

N.D
N.D
N.D
N.D
0.088
1.8
0.13
0.36
0.13
3.1
1.2
N.D
0.26
0.46
0.96
0.22
0.090
N.D
0.15
1.6
N.D
N.D
0.095
11

0.00
0.00
0.00
0.00
0.27
5.5
0.39
1.1
0.38
9.4
3.7
0.00
0.80
1.4
2.9
0.68
0.27
0.00
0.47
4.8
0.00
0.00
0.29
32

44

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LEGACY POPS LEVELS IN NORTH PACIFIC BALEEN WHALES
H6CBs

#155
#150
#148
#136
#154
#151
#135,#144#147#149#139,#140#134#143,#142,#133#146#153,#132,#168
#141
#130
#137
#138,#163,#160
#129
#166
#159
#128
#167
#156
#157
sum

6.7
1.7
2.8
28
7.6
25
35
4.4
240
3.7
2.1
11
81
640
2.5
22
19
450
1.5
4.3
1.2
11
18
25
7.5
1,700

0.22
0.05
0.09
0.91
0.24
0.81
1.1
0.14
7.8
0.12
0.07
0.34
2.6
21
0.08
0.71
0.60
14
0.05
0.14
0.04
0.35
0.59
0.79
0.24
53

N.D
N.D
N.D
1.3
N.D
2.7
1.5
0.44
8.0
N.D
N.D
0.40
2.3
15
0.45
0.54
0.62
11
N.D
N.D
N.D
1.0
0.55
0.67
N.D
47

0.00
0.00
0.00
1.0
0.00
2.1
1.2
0.34
6.3
0.00
0.00
0.31
1.8
12
0.36
0.42
0.49
8.3
0.00
0.00
0.00
0.82
0.43
0.53
0.00
36

0.58
N.D
N.D
1.3
N.D
3.0
1.6
0.47
9.5
N.D
N.D
0.40
3.3
22
0.81
0.70
0.79
16
N.D
N.D
N.D
0.97
0.69
1.0
N.D
62

0.41
0.00
0.00
0.92
0.00
2.1
1.2
0.33
6.7
0.00
0.00
0.28
2.4
15
0.58
0.50
0.56
11
0.00
0.00
0.00
0.69
0.49
0.74
0.00
44

N.D
N.D
N.D
0.55
N.D
0.89
0.53
0.11
2.5
N.D
N.D
0.13
0.77
3.4
0.19
0.13
0.17
2.5
N.D
N.D
N.D
0.12
0.18
0.18
N.D
12

0.00
0.00
0.00
1.7
0.00
2.7
1.6
0.32
7.7
0.00
0.00
0.39
2.4
10
0.57
0.38
0.51
7.7
0.00
0.00
0.00
0.37
0.53
0.55
0.00
38

H7CBs

#188
#184
#179
#176
#186
#178
#175
#187,#182
#183
#185
#174
#177
#171
#172,#192#180#191#170,#190
#189
sum

4.7
3.7
28
7.1
13
17
3.4
120
43
2.0
37
28
11
10
140
1.3
48
3.3
520

0.15
0.12
0.89
0.23
0.42
0.55
0.11
3.9
1.4
0.06
1.2
0.90
0.37
0.33
4.4
0.04
1.5
0.11
21

N.D
0.23
0.85
0.31
N.D
0.54
N.D
3.0
0.93
N.D
0.85
0.70
0.23
0.25
2.7
N.D
0.97
N.D
16

0.00
0.18
0.67
0.24
0.00
0.42
0.00
2.3
0.73
0.00
0.67
0.55
0.18
0.20
2.1
0.00
0.76
0.00
14

N.D
0.25
1.0
0.34
N.D
0.93
0.17
4.7
1.5
N.D
1.4
1.2
0.46
0.59
5.3
N.D
1.7
0.18
24

0.00
0.18
0.72
0.24
0.00
0.66
0.12
3.4
1.1
0.00
1.0
0.84
0.33
0.42
3.7
0.00
1.2
0.13
19

N.D
N.D
0.35
0.088
N.D
0.17
0.055
0.93
0.19
0.052
0.39
0.20
0.053
0.097
1.0
N.D
0.27
N.D
8.6

0.00
0.00
1.1
0.27
0.00
0.53
0.17
2.8
0.57
0.16
1.2
0.62
0.16
0.30
3.1
0.00
0.82
0.00
16

O8CBs

#202
#201
#197
#200
#198
#199
#203,#196
#195
#194
#205
sum

6.4
3.9
3.4
1.8
1.1
13
14
3.1
9.3
1.2
57

0.20
0.13
0.11
0.06
0.03
0.42
0.44
0.10
0.30
0.04
1.8

N.D
N.D
N.D
N.D
N.D
0.26
0.30
N.D
0.21
N.D
0.77

0.00
0.00
0.00
0.00
0.00
0.20
0.23
0.00
0.16
0.00
0.60

0.26
N.D
N.D
N.D
N.D
0.60
0.49
N.D
0.30
N.D
1.6

0.18
0.00
0.00
0.00
0.00
0.42
0.35
0.00
0.21
0.00
1.2

0.084
0.070
N.D
N.D
N.D
0.15
0.087
N.D
0.078
N.D
0.47

0.26
0.21
0.00
0.00
0.00
0.46
0.27
0.00
0.24
0.00
1.4

N9CBs

#208
#207
#206
sum

2.0
2.1
2.5
6.6

0.07
0.07
0.08
0.21

N.D
N.D
N.D
ND

0.00
0.00
0.00
0.00

0.19
0.23
N.D
0.42

0.13
0.17
0.00
0.30

0.044
0.030
0.038
0.11

0.13
0.09
0.11
0.34

D10CBs

#209

3.7

0.12

0.13

0.10

0.38

0.27

0.037

0.11

3,100

100

130

100

140

100

33

100

Total-PCBs

Cetacean Population Studies (CPOPS)
Vol. 2, 2020, 39-53

45

25
Common minke whale
Sei whale

20

Bryde's whale
15

Antarctic minke whale

10

5

0

#10,#4#8,#5#11#12,#13
#15
#19
#18
#17
#24,#27#32,#16#26#25#31,#28#33,#20
#22
#37
#53
#51
#45
#69,#46#52,#73#43,#49#47,#48,#75#44#59,#42#41#64,#68#40,#57#74#70,#76#80#66#56,#60
#96
#103
#100
#94
#93
#95
#121,#92#89#84#90,#101#99#119#97,#86#125,#87#117,#115,#85
#110
#82
#124
#123,#106
#118
#114
#122
#105,#127
#155
#150
#148
#136
#154
#151
#135,#144#147#149#139,#140#134#143,#142,#133#146#153,#132,#168
#141
#130
#137
#138,#163,#160
#129
#166
#159
#128
#167
#156
#157
#188
#184
#179
#176
#186
#178
#175
#187,#182
#183
#185
#174
#177
#171
#172,#192#180#191#170,#190
#189
#202
#201
#197
#200
#198
#199
#203,#196
#195
#194
#205
#208
#207
#206
#209

The percentage of the PCB isomers in total PCBs (%)

YASUNAGA AND FUJISE

N9CBs

D2CBs

T3CBs

T4CBs

P5CBs

H6CBs

H7CBs

O8CBs

D10CBsFig. 2. The percentage profiles of the PCB isomers in total PCBs (%) in blubber of common minke, sei, Bryde’s
from the western North Pacific, and Antarctic minke whales from the Antarctic.

species were hexachlorobiphenyl CB-153, 132 and 168. In order to clarify features of accumulationof PCB congeners, PCA was conducted using the detectable 112 PCB congeners in common minke,sei, Bryde’s and Antarctic minke whales. The results showed that the two principal components (PCs)represented 72.5% (PC1) and 8.5% (PC2) of the variance (Table 4, Fig. 3a, 3b). Focusing on PCB
congener with high correlation coefficients of PC1 and low correlation coefficients of PC2, PC1 waspositively correlated with mainly higher-chlorinated PCB congeners (hexa- to deca-chlorinated) andpart of tetra-chlorinated congeners (Fig. 3a). PC2 was positively correlated with part of di- and trichlorinated PCB congeners, although it was negatively correlated with CB-11, tetra- and penta- chlorinated congeners (Fig. 3a).
With the exception of one common minke whale having higher PC1 and lower PC2, the coefficientsof PC2 of three whale species in the western North Pacific were clearly higher than those of Antarctic
minke whales (Fig 3b), which can be interpreted as geographical difference of their habitats. Then,
PC2 might be associated with higher levels of di- (CB-4, 5, 8 and 10) and tri- (CB-16, 25 and 32)
chlorinated PCB congeners in the three baleen whales in the western North Pacific whales and higher
levels of di- (CB-11), tetra- (CB-46, 69 and 80) and penta- (CB-85, 115 and 117) chlorinated congeners
in Antarctic minke whales. Although there was insufficient information given for some isomers, CB-11
was unintentionally produced in certain processes of the diarylide pigment production (Hu andHornbuckle, 2010), whereas CB-4, 5 and 8 are slightly contained in technical PCB, Kanechlors having
made in Japan before the 1960’s (Takasuga, Inoue and Ohi, 1995; Jarman, et al., 1998). Furthermore,
Vorkamp (2016) established that CB-11 was the most predominant PCB congener in the atmosphere
1.000

CB-32,16

(a)

CB-25

CB-4,10.800

CB-5,8

D2CBs
T3CBs
T4CBs
P5CBs

.600

H6CDs

3.0

H7CDs
O8CDs

.400

(b)

2.0

CB-41

PC2

.200

-0.4

-0.2

.000

CB-40,57
0

0.2

0.4

CB-11
CB-80

0.8

1

1.2

1.0

Sei whale
Bryde's whale

0.0

Antarc�c minke
whale

-1.0

CB-51

-.200

CB-46,69

0.6

CB-70,76
CB-52,73
CB-74

D10CDsPC2 (8.5%)

N9CDs

Common minke
whale

-2.0

-1.0

0.0

1.0

2.0

3.0

4.0

PC1 (72.5%)

-.400

-.600

CB-85,115,117
-.800

PC1

Fig. 3. Distribution of PCB congeners (a) and whale species (b) plotted against the PC1 and PC2 in two-dimensional principal component analysis for the detectable 112 PCB congeners in blubber of common minke, sei,
Bryde’s whales from the western North Pacific, and Antarctic minke whales from the Antarctic.

46

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LEGACY POPS LEVELS IN NORTH PACIFIC BALEEN WHALES

Table 4. Factor loadings of a selection of individual
PCB isomer concentrations in blubber samples ofcommon minke, sei, Bryde’s from the western
North Pacific and Antarctic minke whales from theAntarctic to the two principal components (PCs) 1
and 2.
PCB isomers
Nos. of Cl IUPAC No.

PC1

PC2

D2CBs

#10,#4#8,#5#11#12,#13
#15

0.206
0.318
–0.250–0.101–0.2370.776
0.740–0.609
0.052
0.607

T3CBs

#19
#17
#24,#27#32,#16#26#25#31,#28#33,#20#22#37–0.119–0.2470.051–0.044
0.704
0.041
0.806
0.952
0.206
–0.0990.078
0.399–0.013
0.860
0.551
0.880
0.522
0.197
0.467
0.085

T4CBs

#53
#51
#45
#69,#46#52,#73#43,#49#47,#48,#75#44#59,#42#41#64,#68#40,#57#74#70,#76#80#66#56,#60

0.924
0.923
0.706
–0.179
0.988
0.949
0.950
0.909
0.924
0.927
–0.239
0.920
0.997
0.970
–0.293
0.950
0.948

0.249
–0.1530.122–0.487
0.097
0.236
0.229
0.261
0.272
0.157
0.061
0.105
0.028
0.156
–0.701
0.203
0.218

#96
#103
#100
#94
#93
#95
#121,#92#89#84#90,#101#99#119#97,#86#125,#87#117,#115,#85
#110
#82
#124
#123,#106
#118
#114

0.874
0.951
0.918
0.874
0.980
0.971
0.996
0.917
0.783
0.95
0.995
0.368
0.889
0.945
–0.287
0.929
0.886
0.887
0.990
0.995
–0.115–0.3380.064–0.126–0.338
0.062
0.171
0.028
0.276
0.489
0.219
–0.025
0.618
0.323
0.243
–0.6930.249
0.124–0.333–0.121–0.015
0.131

P5CBs

Cetacean Population Studies (CPOPS)
Vol. 2, 2020, 39-53#122#105,#127

0.115
0.916

0.003
0.328

H6CBs

#155
#150
#148
#136
#154
#151
#135,#144#147#149#139,#140#134#143,#142,#133#146#153,#132,#168
#141
#130
#137
#138,#163,#160
#129
#166
#159
#128
#167
#156
#157

0.933
0.931
0.874
0.990
0.996
0.974
0.993
0.981
0.993
0.874
0.874
0.988
0.990
0.990
0.912
0.982
0.984
0.991
0.928
0.950
0.788
0.961
0.983
0.991
0.985

0.182
–0.183–0.338–0.082–0.0620.173–0.0830.097–0.074–0.338–0.338–0.127–0.105–0.0200.248–0.155–0.149–0.010–0.172–0.2450.053
0.191–0.156–0.106–0.147

H7CBs

#188
#184
#179
#176
#186
#178
#175
#187,#182
#183
#185
#174
#177
#171
#172,#192#180#191#170,#190
#189

0.228
0.915
0.984
0.980
0.228
0.949
0.937
0.986
0.984
0.992
0.980
0.986
0.982
0.979
0.981
0.115
0.977
0.939

0.392
–0.033–0.116–0.1590.392–0.199–0.235–0.040–0.110–0.041–0.112–0.090–0.141–0.146–0.0190.003–0.037–0.218

O8CBs

#202
#201
#197
#200
#198
#199
#203,#196
#195
#194
#205

0.989
0.990
0.874
0.913
0.887
0.979
0.979
0.955
0.972
0.911

–0.116–0.122–0.338–0.306–0.332–0.097–0.090–0.196–0.113–0.299

N9CBs

#208
#207
#206

0.979
0.983
0.977

–0.074–0.007–0.061

D10CBs

#209

0.978

0.038

72.5

8.5

% total variance

47

YASUNAGA AND FUJISEof the Antarctic region, because only this congener is ubiquitously present globally, although otherlower chlorinated congeners are easily degraded in the atmosphere. Therefore, composition of lower
chlorinated congeners in the whale body would be especially influenced by environmental factors suchas the distance from anthropogenic sources and latitude.
With the exception of one common minke whale having higher PC1 and lower PC2, coefficients of
PC1 were in the order of common minke > Bryde’s = sei > Antarctic minke whales, which is consistent with trophic levels based on their feeding ecology reported in previous studies (Konishi et al.,2009; Tamura and Konishi, 2009). In the western North Pacific baleen whales, the second mostprevalent congeners in common minke, sei and Bryde’s whales were hexachlorobiphenyl CB-138, 163
and 160. This was negatively correlated with lower-chlorinated PCB congeners (di- to penta-chlorinated) which are rapidly metabolized and eliminated in the marine environment although they havehigher mobility and therefore more available to aquatic organisms (de Boer et al., 2001). This suggeststhat PC1 can explain the persistence of PCB congeners through the food chain in the marine environment.
In previous studies, hexa-chlorinated CB-153 was the most prevalent congener, followed by CB-138
in small cetaceans such as Dall’s porpoise, striped dolphin and finless porpoise from the western North
Pacific (Minh et al., 2000), whereas CB-153 was also the most prevalent congener, followed by
CB-128 in common minke whales from the Northeast Atlantic (Kleivane and Skaare, 1998). The difference in the secondary dominant congeners is mainly because CB-128 is partly contained in Aroclors
which had been used as PCB products in Europe, whereas it is contained in lesser amounts in Kanechlors which had been used in Japan (Kannan, Maruya and Tanabe, 1997). This suggests that levelsof CB-128 in baleen whales would reflect their habitat.

Table 5. Average concentrations (ng/g lipid wt.) and percentages (%) of DDT isomers in the blubber samples of common minke, sei, Bryde’s whales from the western North Pacific and Antarctic
minke whales.
SpeciesnCommon minke

5

whale
Sei whale

5p,p’-DDE

p,p’-DDD

p,p’-DDT

Total-DDTs

average

1,600

330

99

2,000

%

( 78.5 )( 16.1 )( 4.9 )

44

18

7.9

( 62.5 )( 24.7 )( 11.1 )

61

13

7.8

( 74.5 )( 15.8 )( 9.5 )

48

6.4

16

( 70.1 )( 9.3 )

( 22.5 )40%

80%

average%

Bryde’s whale

5

average%

Antarctic minke
whale

5

average%0%

Common minke whale

Sei whale

20%

60%

71
82
69

100%

p,p’-DDE
p,p'-DDE
p,p'-DDD
p,p’-DDD
p,p'-DDT
p,p’-DDT

Bryde's whale

Antarc�c minke whale

Fig. 4. Compositions of DDTs in the blubber of common minke,sei, Bryde’s whales from the western North Pacific, and Antarctic minke whales.

48

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LEGACY POPS LEVELS IN NORTH PACIFIC BALEEN WHALES

Composition of DDT, HCH and CHL isomers
The averages of percentage of p,p’-DDT in the whale species in this study were in the order ofAntarctic minke whale (20.0%) > Bryde’s whale (8.7%) ≈ common minke whale (7.4%) > sei whale(3.3%) (Table 5; Fig. 4). The p,p’-DDE/total DDT ratio is widely used as an indicator of the time
elapsed since releasing technical DDT into the environment (Borrell and Aguilar, 1987), because technical DDTs which have been used to control malaria are composed of almost all p,p’-DDT (De Jager
et al., 2006), and p,p’-DDT released in the environment is changed to p,p’-DDE in the animal bodyand the environment (Okonkwo et al., 2008). Our results are consistent with previous reports thatp,p’-DDE/total DDT ratios in male Antarctic minke whales had decreased for 1984/1985 (ca. 40%)
and 1992/1993 (ca. 25%) (Aono et al., 1997), and that of mature male common minke whales sampled
in sub-area 7 for 1996 and 1998 was 8.9% (calculated by mean of p,p’-DDT 184 ng/g lipid wt. andtotal DDT 2,060 ng/g lipid wt.) (Fujise et al., 2000). This suggests that a technical DDT might havebeen slightly used in the southern hemisphere.
In the ratios of the three baleen whale species in the western North Pacific, that of sei whale washigher than those of the other whales. Notably, that of sei whale was higher than that of Bryde’s whalein spite of the same levels of DDTs (Table 2) and trophic position. The production and usage of DDTs
had been discontinued in the early 1970’s in most developed countries, whereas they have been continued until now for malaria and leishmaniasis control in the tropical developing countries (De Jager
et al., 2006). Moreover, van den Berg, Manuweera and Konradsen (2017) estimated DDT usage globally declined by 30 percent from 2001 to 2014, mainly because of the reduction in India which holds
84% of the total global stockpile. Our result suggests that the lower p,p’-DDT ratio of sei whales
compared to common minke and Bryde’s whales in the northern hemisphere might be the distance of
their habitat to the major technical DDT sources. This is also consistent with the fact that the ratios ofTable 6. Average concentrations (ng/g lipid wt.) and percentages (%) of HCH isomers in blubbersamples of common minke, sei, Bryde’s whales from the western North Pacific and Antarctic
minke whales.
SpeciesnCommon minke

5

whale
Sei whale
Bryde’s whale
Antarctic minke
whale

5
5
5

α-HCH

β-HCH

γ-HCH

Total-HCHs

21

650

7.9

670

%

( 3.2 )

( 96.7 )( 1.2 )

average

3.3

85

1.1

%

( 3.6 )

( 93.2 )( 1.2 )

average

0.59

12

0.28

%

( 4.7 )

( 98.4 )( 2.2 )

average

0.12

0.10

0.37

%

( 22.9 )( 19.7 )( 69.8 )average0%
Common minke whale

Sei whale

20%

40%

60%

80%

91
13
0.52

100%

α-HCH
β-HCH
γ-HCH

Bryde's whale

Antarc�c minke whale

Fig. 5. Compositions of HCHs in the blubber of common
minke, sei, Bryde’s from the western North Pacific, andAntarctic minke whales.
Cetacean Population Studies (CPOPS)
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49

YASUNAGA AND FUJISE

common minke whale in this study was lower than that of common minke whale collected in 2006
from the Korean coast (ca. 35-40%) (Moon et al., 2010).
The averages of percentage of β-HCH accounted for over 90% of total HCHs in common minke,
sei and Bryde’s whales from the western North Pacific, whereas the percentage of γ-HCH was thedominant isomer of HCHs in Antarctic minke whales (Table 6; Fig. 5). An odorless γ-HCH purified
from technical HCH has been produced and used worldwide since the 1950’s, although the technical
HCH (α-HCH: 53-70%, β-HCH: 3-14%, γ-HCH: 10-18% and others) having a persistent bad smell
and taste had been produced as a pesticide in Europe and other countries in the late 1940’s and 50’s
(Vijgen et al., 2011). After then, the mass-production base of γ-HCH moved to China, Russia andIndia, now leaving only a small number of producing countries (India and Romania) (Vijgen et al.,2011). It is noted that γ-HCH is produced from 8 times the amount of technical HCH to it and that theresidue was not properly treated in the producing countries. Therefore, HCH emissions have been
almost all only γ-HCH in the southern hemisphere, suggesting that this may be reflected in the HCHlevels in Antarctic minke whales.
In the three whale species in the western North Pacific, β -HCH is much higher than γ-HCH, whereas
β-HCH is a minor component in a technical HCH. Because γ-HCH is rapidly metabolized, the β-HCH
is consistently found in higher concentrations in mammals (Willett, Ulrich and Hites, 1988).
The percentages of CHL isomers in common minke, sei and Bryde’s whales from the western North
Pacific were in the order of trans-nanochlor > cis-nonachlor, whereas those in Antarctic minke whales
were in the order of trans-nanochlor > oxychlordane (Table 7; Fig. 6). Technical CHLs were used for
insecticide in Japan until 1986, of which 60-70% consisted of cis- and trans-chlordane (Loganathan
et al., 1993). Trans-chlordane was not detected in all four whale species in this study, whereas cischlordane was detected at relatively low levels. Ueno et al. (2003) reported that their trans-chlordane /Table 7. Average concentrations (ng/g lipid wt.) and percentages (%) of CHL isomers in blubber samples ofcommon minke, sei, Bryde’s whales from the western North Pacific and Antarctic minke whales.
SpeciesnCommon minke

5

whale

transcistranscisoxychlordane chlordane
chlordane nonachlor nonachlor Total-CHLs
average
%

150

N.D.

33

950

210

( 11.1 )( 0.0 )

( 2.5 )

( 71.1 )( 15.7 )

7.6

N.D.

3.3

36

12

Sei whale5

average( 12.9 )( 0.0 )

( 5.6 )

( 61.4 )( 20.1 )Bryde’s whale

5

average

4.2

N.D.

9.8

39

14

%

( 6.2 )

( 0.0 )

( 14.5 )( 57.8 )( 21.0 )

11

N.D.

1.3

16

4.8

( 33.2 )( 0.0 )

( 3.9 )

( 48.9 )( 14.2 )%Antarctic minke
whale

5

average%0%

Common minke whale

Sei whale

Bryde's whale

20%

40%

60%

80%

1,300
59
68
34

100%

oxychlordane
oxychlordane
trans-chlordane
trans-chlordane
cis-chlordane
cis-chlordane
trans-nonachlortrans-nonachlor
cis-nonachlor
cis-nonachlor

Antarc�c minke whale

Fig. 6. Compositions of CHLs in the blubber of common minke, sei, Bryde’s
from the western North Pacific, and Antarctic minke whales.

50

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LEGACY POPS LEVELS IN NORTH PACIFIC BALEEN WHALES

trans-nanochlor ratios are in the range of 2.9-3.4, and decreasing ratio in the environment means thattime has passed after technical CHLs release. This implies that the four baleen whale species from thewestern North Pacific and Antarctic would not have been recently exposed to new technical CHLs.

Conclusion

To examine the accumulation features and current status of POPs in the western North Pacific, thepresent study determined the concentrations of these compounds in the blubber of common minke, sei
and Bryde’s whales. The study found that there have been no recent anthropogenic inputs of legacy
POPs in the western North Pacific, however, the POPs compositions in the whales might reflect theirusage and fate. Understanding the historical usage and fate of these compounds may help predict their
future behavior in the marine environment.

Acknowledgments

We would like to thank the captains, crews and scientists involved in the JARPN II and JARPA II
surveys. These research programs were conducted with permission from the Fisheries Agency of theGovernment of Japan. Finally, we are deeply grateful for the fair and constructive reviews of anonymous reviewers.

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Jarman, W. M., Hilkert, A., Bacon, C. E., Collister, J. W., Ballschmiter, K and Risebrough, R. W. 1998. Compound-specificCetacean Population Studies (CPOPS)
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Yasunaga, G. Hakamada, T. and Fujise, Y. 2016. Update of the analyses on temporal trend of PCB levels in common
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Received: October 28, 2019
Accepted: March 5, 2020

52

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LEGACY POPS LEVELS IN NORTH PACIFIC BALEEN WHALES© ICRPhoto 1. Common minke whale© ICR
Photo 2. Sei whale© ICR
Photo 3. Bryde’s whale
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ARCHIVAL INDEXCETACEAN POPULATION STUDIES, TOKYO, JAPAN
Volume 2, June 2020
Goto, M., Kitakado, T., and Pastene, L. A. A preliminary study of epigenetic estimation of age of the
Antarctic minke whale Balaenoptera bonaerensis 5 – 14.
Matsuoka, K., and Hakamada, T. Density distribution of several major whale species in the Indo-Pacificregion of Antarctic using JARPA and JARPAII sighting data obtained through 1987/88 – 2008/09
seasons 15 – 38.
Yasunaga, G., and Fujise Y. Concentration of persistent organic pollutants (POPs) in three species ofbaleen whales in the western North Pacific

39 – 53.

Volume 1, December 2018
Kishiro, T. Satellite tracking of coastal Bryde’s whales Balaenoptera edeni along the southwest coast ofJapan 3– 13.
Nakamura, G., Ryeng, K. A., Kadowaki, I., Hayashi, R., Nagatsuka, S., Hirose, A., Fujise, Y., and Haug,
T. Comparison of shapes of the white flipper patch between two sub-species of common minke whales(Balaenoptera acutorostrata) 15 – 24.
Hirose, A., Kishida, T., and Nakamura, G. Nasal mucosa resembling an olfactory system in the common
minke whale (Balaenoptera acutorostrata) 25 – 28.

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SUBJECT INDEXage estimation 2: 5 – 14
Antarctic 2: 15 – 38
Antarctic minke whale 2: 5 – 14, 2: 15 – 38
Balaenoptera acutorostrata 1: 15 – 24
baleen whale 1: 25 – 28
baleen whales 2: 15 – 38
blue whale 2: 15 – 38
Bryde’s whales 2: 39 – 53
coastal Bryde’s Whale 1: 3 – 13
common minke whale 1: 15 – 24, 2: 39 – 53
distribution 2: 15 – 38
DNA methylation 2: 5 – 14
epigenetics 2: 5 – 14
fin whale 2: 15 – 38
flipper 1: 15– 24
histology 1: 25 – 28
humpback whale 2: 15 – 38
killer whale 2: 15 – 38
movement 1: 3 – 13
nasal cavity 1: 25 – 28
North Pacific 2: 39 – 53
olfaction 1: 25 – 28
olfactory epithelium 1: 25 – 28
organic pollutants 2: 39 – 53
POPs 2: 39– 53
proxy of earplugs 2: 5 – 14
satellite tracking 1: 3 – 13
sei whale 2: 39 – 53
subspecies 1: 15 – 24
southern bottlenose whale 2: 15 – 38
southern right whale 2: 15 – 38
sperm whale 2: 15 – 38
taxonomy 1: 15 – 24
toothed whales 2: 15 – 38
white patch morphology 1: 15 – 24

Cetacean Population Studies (CPOPS)
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AUTHOR INDEX

F
Fujise, Y.

1: 15 – 24, 2: 39 – 53

G
Goto, M.

2: 5 – 14

H
Hakamada, T. 2: 15 – 38
Haug, T. 1: 15 – 24
Hayashi, R. 1: 15 – 24
Hirose, A. 1: 15 – 24, 1: 25 – 28

K
Kadowaki, I. 1: 15 – 24
Kishida, T. 1: 25 – 28
Kishiro, T. 1: 3 – 13
Kitakado, T. 2: 5 – 14

M
Matsuoka, K.

2: 15 – 38

N
Nagatsuka, S. 1: 15 – 24
Nakamura, G. 1: 15 – 24, 1: 25 – 28

P
Pastene, L. A.

2: 5 – 14R
Ryeng, K. A.

1: 15 – 24

Y
Yasunaga, G.

2: 39 – 53

Cetacean Population Studies (CPOPS)
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Guide for Authors
CETACEAN POPULATION STUDIES (CPOPS) is an English peer reviewed on-line journal which
publishes scientific articles on cetaceans and other marine mammals in the form of (1) Original study Full paper, (2) Original study - Short note, (3) Review of studies, (4) Photo gallery with explanatory noteas well as (5) Others, subject to authorization by the editor in chief in advance of formal submission.
CPOPS welcomes contributions from accredited scientists in any country. Copyright for articles publishedin CPOPS is transferred to CPOPS when the article is accepted for publication. Articles published in
CPOPS may not be reproduced, in whole or in part, without written permission from CPOPS. CPOPS
does not charge any submission or publication fee.
Full paper and Short note
A Full paper is a self-contained piece of work composed of systematic analyses which are scientificallyorganized using a significant number of samples or a significant quality of information. For clarificationof structure, the paper should be subdivided into meaningful sections such as introduction, materials
and methods, results and discussion, etc. The paper should include an appropriate abstract (less than
300 words) and keywords (less than 6 words), and a list of references cited in the text.
A Short note should be composed of important information or analyses which are also scientificallyorganized, but it is not necessary that the information is based on a sufficient number of samples orobservations. The short note contents do not need to be subdivided by sections as in the case of a full
paper. It should include an appropriate abstract (less than 100 words) and key words. The short noteshould not exceed 6 printed pages in length and include some thoughtfully selected tables and figures.
Please visit CPOPS home page (https://cpops.jp) for further details.
Submission of Manuscripts
Manuscripts should be original work not previously published. Manuscripts must (in principle) be
prepared in Microsoft WORD or PDF files and submitted electronically through the CPOPS manuscript
submission system (will be available in due course) or to the E-mail address below.
E-mail: cpopspaper@gmail.com
The information obtained through paper submission will not be used for purposes other than those of
publication without the consent of the author himself/herself.
Manuscripts are peer-reviewed typically by three anonymous referees nominated by the editorial board.
Contributors, if they wish, can suggest specific names of up to two experts with sufficient knowledge
and experience to review the paper. The editor in chief will attempt to include one reviewer from thenominated experts.
When contributors are requested to revise their manuscripts, they can resubmit, within 30 days, therevised manuscript incorporating comments and suggestions by referees, together with an attached note
describing how the revision has been carried out. The final decision on acceptance or rejection for
publication is that of the editor in chief in consultation with other members of the editorial board.
The “Instructions to Contributors” may be revised from time to time according to development of
CPOPS and discussions in the editorial board.
You can find the Organization of Manuscripts, General Instructions and the Cover page template formanuscript submission in the following link.
https://cpops.jp/paper_submission/index.html
Cetacean Population Studies (CPOPS)
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