J-STAGE Advance published date: November 9, 2021

GENETIC MATCHES OF SOUTHERN RIGHT WHALESGENETIC MATCHES OF SOUTHERN RIGHT WHALESIN THE INDIAN SECTOR OF THE ANTARCTIC:A CONTRIBUTION TOWARDS UNDERSTANDING
THEIR MOVEMENT AND SITE-FIDELITY
Luis A. PASTENE1, 2*, Mutsuo GOTO1, Mioko TAGUCHI1
and Koji MATSUOKA1
Institute of Cetacean Research, 4–5 Toyomi-cho, Chuo-ku, Tokyo 104–0055, Japan
Project Microbiomes as Bioindicators of the Aquatic Ecosystem Health in Chilean Patagonia,
Centro de Estudios del Cuaternario de Fuego-Patagonia y Antártica (CEQUA), Punta Arenas, Chile*Corresponding author: pastene@cetacean.jp
12

Abstract
Genetic analyses were conducted to investigate the individual identiﬁcation (and matching)of southern right whales (Eubalaena australis) from samples collected in the austral summer
in the Indian Ocean sector of the Antarctic (between 80°–135°E, south of 60°S). The study was
conducted to evaluate the utility of this approach for studies on site ﬁdelity and range. In total,
157 skin biopsy samples were collected from free-ranging whales during fourteen summer surveys. The DNA was extracted from each biopsy sample, genotyped at fourteen microsatellite
loci, sequenced for 381 nucleotides of the mtDNA control region, and the sex determined by
the presence of a Y-chromosome speciﬁc locus. Eight matches were detected (four males andfour females) using individual matching by multi-locus genotypes supported by mtDNA haplotype and sex determination. Where photographs were available, two matches were conﬁrmed
by photo-identiﬁcation. These eight re-samples show that at least some males and females
returned to the same feeding grounds across years. The average longitudinal dispersal ranges,
latitudinal dispersal ranges and average direct distances between marks and recaptures were:
13°06′ and 7°15′; 1°23′ and 0°47′; and 361 n.miles and 199 n.miles for males and females,
respectively. The time spans ranged from 3–13 years with an average of 6.7 and 7.8 years formales and females, respectively. Sampling and matching occurred in an area where visual surveys showed aggregations of southern right whales associated with high krill concentration.
The study conﬁrms the feasibility of the genetic approach, but more deﬁnitive inferences onsite ﬁdelity and movement ranges will require a large number of biopsy samples genotyped,
from both south and north of 60°S.
Key words:

southern right whales, Antarctic, genetic tagging, site ﬁdelity, movement, distribution.

Introduction
Baleen whales are important components of the Antarctic marine ecosystem as top predators. Substantial changes in their abundance and distribution, for example due to past whaling or more recently
climate change, aﬀects the entire ecosystem. For this reason, systematic monitoring of baleen whale
abundance, pattern of movement and distribution in Antarctic waters is important.
A substantial amount of biological and ecological information on large whales and their environment was obtained in the Indo-Paciﬁc sector of the Antarctic (35°E–145°W) by the ‘Japanese Whale
Cetacean Popul. Stud. (CPOPS), Full paper
Vol. 3, 2021, 129–138

129

PASTENE, GOTO, TAGUCHI AND MATSUOKA

Research Program under Special Permit in the Antarctic’ Phases I and II (JARPA, JARPAII) and thesubsequent ‘New Whale Research Program in the Antarctic’ (NEWREP-A). These were conductedannually under the auspices of the Government of Japan between the 1987/88 and 2018/19 australsummer seasons under Article VIII of the International Convention for the Regulation of Whaling(ICRW). Most of the demographic and ecological analyses conducted under these research programs
targeted the Antarctic minke whale (Balaenoptera bonaerensis) and other Balaenopterid species (seesummaries of results in Murase et al. (2020) and Fujise and Pastene (2021)). In the context of thispaper, southern right whale (Eubalaena australis) sightings were recorded and where possible, photo-identiﬁcation and genetic samples were collected.
A further important source of information from Antarctic waters is the sightings, photo-identiﬁcation and biopsy data collected at the circumpolar level by the International Whaling Commission-International Decade for Cetacean Research/Southern Ocean Whale and Ecosystem Research (hereafter
IWC-IDCR/SOWER) surveys conducted between the 1978/79 and 2009/10 austral summer seasons.
Photo-identiﬁcation data and biopsy samples of species including southern right whales were collected
opportunistically during the IDCR/SOWER.
This study focuses on the southern right whales. The species has a circumpolar distribution. They
spend the austral winter in inshore waters of South America, South Africa and Australasia; in springwhales move south to spend the austral summer feeding in waters around Antarctic before returning
north in the autumn (Reeves et al., 2002). They can reach a maximum body length of 17 m and the
body length at birth is 4–4.6 m. They are believed to live more than 70 years and calves are produced
every 3–5 years (Reeves et al., 2002). The primary breeding grounds are located at South Africa,
South West Australia, Argentina, and New Zealand Sub-Antarctic (IWC, 2001; 2013; Carroll etal., 2016). Research eﬀort to investigate stock structure, distribution and abundance trend has focused
mainly on the breeding grounds, and limited information exists on the distribution, site ﬁdelity andmovements in the feeding grounds, and on the connection between breeding grounds in low latitude
waters and higher latitude feeding grounds.
Migration patterns, movements and feeding ground destinations have been studied using direct
approaches including photo-identiﬁcation and more recently, telemetry as well as indirect approaches
such as visual surveys and historic whaling records. Telemetry has been used to investigate movement
patterns of South African right whales (Mate et al., 2011) and western South Atlantic right whales(Zerbini et al., 2016; 2018). The telemetry and photo-identiﬁcation (e.g., Best et al., 1993) studies in
the Argentina and South African breeding grounds show that southern right whales are found throughout large areas of the South Atlantic Ocean and visit several potential feeding areas each season.
The focus of the present paper is the Indian Ocean sector of the Antarctic, between 80°–135°E,
south of 60°S. Previous studies have shown that animals from that sector are associated with breeding
grounds in the Australasian region (e.g., IWC, 2001; 2013). For example, Bannister (2001) reviewed
the distribution and movement of ‘Australian’ southern right whales based on historical whaling data,
recent sighting surveys, 1960s Soviet catch data and photo-identiﬁcation data. The review conﬁrmed
the traditional view of seasonal movements to and from coastal breeding grounds in warm waters andfeeding grounds in colder waters. In terms of direct evidence, he presented two photo-identiﬁcation
matches, the ﬁrst made between whales identiﬁed of either Western Australia or South Australia in
winter/spring and waters around 40°–44°S; 116°–125°E where a sighting of 35 animals had been madein December–January 1995–96 (Bannister et al., 1997). The other evidence was a southern right whale
photographed at 64°26′S; 114°54′E in February 1996, which had been identiﬁed over a period of 18
years on the coast of Western Australia (Bannister et al., 1999). These data suggest that at least someof the summer feeding aggregation of southern right whales in the Antarctic Indian Ocean sector belong to the South West Australian population.
Most recently, Mackay et al. (2020) presented telemetry information of six animals tagged in Australasian wintering grounds. They suggested at least three probable foraging grounds: to the southwest

130

Cetacean Popul. Stud. (CPOPS), Full paper
Vol. 3, 2021, 129–138

GENETIC MATCHES OF SOUTHERN RIGHT WHALES

of Western Australia, the Subtropical Front and Antarctic waters—the Subtropical Front appearing to
be a feeding ground for animals from both New Zealand and Australian waters. They also suggested
that the observed variable population growth rates between wintering grounds in Australasia might
reﬂect ﬁdelity to diﬀerent quality feeding grounds. Thus, similar to results from the South African andArgentina breeding grounds, Australasian animals appear to visit multiple potential feeding areas eachseason.
A high concentration of sightings of southern right whales was observed in the Indian sector (80°–135°E) of the Antarctic Ocean during various austral summer season cruises of JARPA and JARPAII(Matsuoka and Hakamada, 2020) and the IWC-IDCR/SOWER cruises. Biopsy samples collected
opportunistically during the IDCR/SOWER and JARPA/JARPAII surveys in that sector were used in
the present study on genetic matching based on microsatellite DNA (msDNA). The main objective of
the individual identiﬁcation based on genetic matching was to evaluate the utility of this approach to
study site ﬁdelity and ranges in this species. The use of genetic markers (‘tags’) has long been shown
to represent a viable alternative/supplement to photographic methods of individual recognition—suchmarkers are permanent in all individuals (Palsbøll et al., 1997a).

Materials and methods
Samples
A total of 157 skin/blubber biopsy samples were obtained opportunistically from free-ranging
southern right whales along the sighting surveys of JARPA/JARPAII (n=108) and IWC-IDCR/SOWER (n=49) in the Antarctic Indian sector (80°–135°E), south of 60°S from the 1993/94 to 2015/16
austral summer seasons. A variety of collection systems was used including crossbows, air guns andmodiﬁed shot guns, all using modiﬁed collection darts that took a small sample of skin and blubber.
The geographical distribution of the southern right whales sampled is shown in Fig. 1.
DNA extraction
Genomic DNA was extracted from approximately 0.05g of the outer epidermal layer of the skin tissue using standard phenol/chloroform protocols (Sambrook et al., 1989) or using Gentra Puregene kits
(QIAGEN). Extracted DNA was stored in TE buﬀer (10mM Tris-HCl, 1mM EDTA, pH 8.0).

Fig. 1. Geographical distribution of southern right whales in the Indian Ocean sector of the Antarctic examined in this study. Red: females; Blue: males. SWA: South West Australia. Light blue shading shows the ice
conﬁguration.
Cetacean Popul. Stud. (CPOPS), Full paper
Vol. 3, 2021, 129–138

131

PASTENE, GOTO, TAGUCHI AND MATSUOKA

Laboratory procedure for msDNA
Genetic variation was examined at 14 msDNA loci: EV1, EV14, EV21, EV37, EV94 (Valsecchi
and Amos, 1996), GT23, GT211, GT310 (Bérubé et al., 2000), GAT A28 (Palsbøll et al., 1997b), DlrFCB17 (Buchanan et al., 1996), TR3G2, TR2G5, TR2F3 and TR3F2 (Frasier et al., 2006). Details of
the laboratory work for msDNA are provided in Pastene and Goto (2016).
Laboratory procedure for mtDNA
Mitochondrial DNA (mtDNA) control region sequences were used as one way to conﬁrm individual
identiﬁcation by nuclear markers. Samples sharing a same genotype should also share a same haplotype.
The ﬁrst 470 base pairs (bp) at the 5′ end of the mtDNA control region were ampliﬁed by polymerase chain reaction (PCR). Details of the laboratory work for mtDNA sequencing are provided in
Pastene and Goto (2016).
Laboratory procedure for sex determination
Sex determination is important both to examine potential sex-speciﬁc patterns of movement as wellas an additional way to conﬁrm individual msDNA matching. Samples sharing the same genotype
should be of the same sex. The SRY locus located on the Y chromosome was used for sex determination following the method of Abe et al. (2001) with a slight modiﬁcation (see Milmann et al., 2021).
Analytical procedure
MtDNA
Variable sites and unique sequences (haplotypes) were identiﬁed using the program MacClade(Maddison and Maddison, 1989).
MsDNA
The computer program MICRO-CHECKER (van Oosterhout et al., 2004) was used to check fornull alleles and reading/typing errors. The probability that two unrelated individuals have identicalgenotype (i.e., an identical genetic ‘tag’) is negatively correlated with the number of loci analysed andthe degree of variation at each locus (Palsbøll, 1999). For this reason, it is important the estimationsof the nuclear DNA diversity of southern right whales at each msDNA locus, as well the probability ofidentity (I). The latter is the probability that two unrelated individuals from the same panmictic population have an identical composite genotype (see Paetkau and Strobeck, 1994). The I was estimatedper locus and across loci. The number of alleles per locus, inbreeding coeﬃcient (FIS) and expected
heterozygosity (HE) per locus was calculated using FSTAT 2.9.3 (Goudet, 1995). Statistical tests forthe deviations from expected Hardy–Weinberg genotypic proportions were conducted using GENEPOP 4.0 (Rousset, 2008), both by each locus and for all loci combined. Individuals with identicalmulti-locus genotypes sampled during the same sighting (duplicates) were investigated, and one fromeach duplicate was removed for subsequent analyses.

Results
Final dataset
There were four cases of biopsies with identical multi-locus genotypes sampled during the samesighting (duplicates). There were two cases of mother-oﬀspring pairs, which were deduced from observations at the ﬁeld and from genetic data. After removing four duplicates, the sample sizes for the
msDNA analyses on individual identiﬁcation was 153 (76 males and 77 females).

132

Cetacean Popul. Stud. (CPOPS), Full paper
Vol. 3, 2021, 129–138

GENETIC MATCHES OF SOUTHERN RIGHT WHALES

Level of msDNA diversity and probability of identity
No evidence of null alleles and typing/reading errors was found. Table 1 shows the estimated msDNA diversity indices. The number of alleles per locus ranged from 2 to 14 (average 7.5), and the HE
ranged from 0.07 to 0.89 (average 0.65). The FIS in each locus ranged from −0.035 to 0.162 (average
0.007). There was no signiﬁcant deviation from the Hardy–Weinberg genotypic proportion. I for eachlocus ranged from 0.022 at DlrFCB17 to 0.861 at EV21, which was estimated to be 1.95×10−10 when
all loci were combined.
Genetic matching
As shown in Table 2, eight matches were detected (four males and four females). The multi-locus
genotype matches were supported by mtDNA (same haplotype), sex determination (same sex), and, inthe two cases where pictures were available, by photo-identiﬁcation matches (Fig. 2).
Site-ﬁdelity and movement range
Figs. 3A–B show the geographical distribution of the matches of female and male southern rightwhales, respectively. Table 2 summarises the matches and associated data. The elapsed time between
sample and re-sample ranged between 3 and 13 years (average 7.25 years). In the case of females, therange was 3–11 years (average 7.75 years) and, in the case of males 4–13 years (average 6.75 years).
The average longitudinal dispersal ranges were 13°06′ and 7°15′ in males and females, respectively.
The average latitudinal dispersal ranges were 1°23′ and 0°47′ in males and females, respectively (Table 2). The average direct distances between sample and re-sample positions were 361 n.miles and
199 n.miles for males and females, respectively (Table 2). A statistical test showed no signiﬁcant differences between females and males in the direct distances between samples and re-samples (W=14,
Mann-Whitney, p=0.114).

Table 1. Indices of microsatellite DNA diversity in southern right whales from the Indian sector of the Antarctic: A: number of alleles; HE: expected heterozygosity; HW: P-value for the test of Hardy-Weinberg equilibrium; FIS: inbreeding coeﬃcient; and I: probability of identity.
Microsatellite loci

A

HE

HW

FIS

I

EV1
GT310
GT23
EV94
EV14
GT211
EV37
GATA28EV21
DlrFCB17
TR2F3
TR3G2
TR2G5
TR3F2

14
6
8
5
10
10
11
10
3
13
2
8
2
3

0.87
0.62
0.81
0.41
0.76
0.82
0.82
0.77
0.07
0.89
0.49
0.77
0.50
0.48

0.25
0.05
0.96
0.78
0.14
0.08
0.95
0.28
0.10
0.54
0.62
0.52
0.14
0.68

0.010
0.057
0.024
−0.0210.006
0.077−0.0170.006
0.162−0.0190.044−0.035−0.123
0.055

0.025
0.205
0.059
0.401
0.076
0.055
0.046
0.090
0.861
0.022
0.379
0.093
0.376
0.361

0.65

0.21

0.007

1.95e-10

Overall

Cetacean Popul. Stud. (CPOPS), Full paper
Vol. 3, 2021, 129–138

133

PASTENE, GOTO, TAGUCHI AND MATSUOKA

Table 2. Cases of sample/re-sample in southern right whales from the Indian sector of the Antarctic determined by microsatellite DNA genotyping. All genotype matches were supported by the mtDNA analysis(same haplotypes) and by the results of sex determination (same sex). Cases 2 and 3 (the only ones for whichphotographs were available) were conﬁrmed by photo-identiﬁcation, SR: sample/resample; ID: label of thewhale; S: sex; BL: body length determined visually by researchers from the vessels (in meters); ET: elapsed
time (year) between samples and re-samples; DD: direct distance between the positions of samples andre-samples (in n. miles); LAR: latitudinal dispersal range between samples and re-samples; LOR: longitudinal
dispersal range between samples and re-samples.
SR

ID

S

BL Date (D/M/Y)

Position

ET

DD

LAR

LOR

1

Sample93IVR004
Re-sample 98SWR046

M
M

14.3
14.3

05/03/1994
31/01/1999

64°14′S
62°40′

113°04′E99°30′

5377

1°34′ 13°34′2Sample97IVR007
Re-sample 01IVR023

M
M

11.9
12.9

15/01/1998
15/02/2002

62°55′
64°36′

100°28′92°15′

4

241

1°41′

3

Sample99IVR012
Re-sample 07IVR56

F
F

16.4
15.3

10/02/2000
01/03/2008

64°35′
64°54′

114°31′126°17′8

303

0°19′ 11°46′

4Sample98SWR140
Re-sample 01IVR018

F
F

13.4
13.3

05/02/1999
14/02/2002

63°19′
64°30′

103°28′93°50′

3

265

1°11′

5

Sample01IVR024
Re-sample 14AJ4R036

M
M

13.2
13.7

15/02/2002
28/02/2015

64°36′
64°05′

92°15′
111°02′13490

0°31′ 18°47′

6Sample98SWR137
Re-sample 07IVR49

F
F

13.1
12.8

02/02/1999
22/02/2008

63°00′
64°03′

100°50′95°29′

9

157

1°03′

5°21′

7

Sample98SWR141
Re-sample 09SWR011

F
F

12.8
13.2

07/02/1999
29/01/2010

63°55′
64°31′

105°42′107°58′

11

69

0°36′

2°16′

8

Sample09SWR008
Re-sample 14AJ4R004

M
M

13.2
12.7

24/01/2010
22/02/2015

64°27′
62°40′

111°38′99°47′

5335

1°47′ 11°51′

8°13′

9°38′

Discussion
Previously Carrol et al. (2016) carried out successfully a genetic matching study in southern rightwhales of the New Zealand nursery ground. The study presented here is the ﬁrst of such kind in southern right whales of the Indian sector of the Antarctic. Results of the Hardy–Weinberg equilibrium test
suggest that whales in this sector belong to the single putative ‘South Western Australia’ population
earlier identiﬁed by the IWC Scientiﬁc Committee (IWC, 2001; 2013) based upon inter alia resultsof photo-identiﬁcation matches (Bannister et al., 1999; Bannister, 2001). Individual identiﬁcation by
genetic matching has the potential to contribute to studies on movement and site ﬁdelity in this population. Here, some relevant aspects of this approach and its utility for southern right whales are discussed.
Utility of genetic matching for individual identiﬁcation of southern right whales
The number (n=14) of msDNA loci used in the present study and the degree of polymorphism(see Table 1) proved to be appropriate for the purpose of individual identiﬁcation in southern rightwhales. There was a very low estimated probability of identity i.e., two unrelated individuals having
an identical composite genotype. The eight cases of genotyping matching were supported by the mtDNA analyses (same haplotype) and sex determination (same sex). In addition, for the two cases where
photographs were available, genotyping matching was supported by photo-identiﬁcation. The authors
conclude that the eight cases of genotyping matching corresponded to matching of the same individual whales and thus conﬁrms the utility of genetic matching to identify individuals (see also Carrol etal., 2016).

134

Cetacean Popul. Stud. (CPOPS), Full paper
Vol. 3, 2021, 129–138

GENETIC MATCHES OF SOUTHERN RIGHT WHALES

Fig. 2 A: A southern right whale sighted in the Indian sector of the Antarctic on 15 January 1998 (left) andre-sighted in the same sector on 15 February 2002 (right) (Matching No. 2 in Table 2). B: A southern rightwhale sighted in the Indian sector of the Antarctic on 10 February 2000 (left) and re-sighted in the same sector
on 1 March 2008 (right) (Matching No. 3 in Table 2).

Fig. 3. Maps showing sample/re-sample positions referred to in the text. A: females–note that match 2002–
2008 was also conﬁrmed by photographs. B: males–note that match 1998–2002 was also conﬁrmed by photographs. Light blue shading shows the ice conﬁguration.

Utility for studies on site ﬁdelity and movement ranges of southern right whales
The eight matches here show that at least some females and males visit the same feeding groundin the Indian sector of the Antarctic south of 60°S in summer. The total samples and the matches bothwere close to 1 : 1 males and females. Although the direct distances between sample and re-sample
Cetacean Popul. Stud. (CPOPS), Full paper
Vol. 3, 2021, 129–138

135

PASTENE, GOTO, TAGUCHI AND MATSUOKA

by sex were statistically non-signiﬁcant, this probably relates to the small sample size. Qualitatively(Table 2 and Fig. 3), the results are not in conﬂict with the ﬁndings of Carroll et al. (2011) that males
are more mobile than females.
As explained earlier, telemetry data from southern right whales tagged in breeding grounds inAustralasia (Mackay et al., 2020), South Africa (Mate et al., 2011) and Argentina (Zerbini et al.,2016; 2018) suggested that individuals may visit several feeding grounds within the same season e.g.,
in middle latitudes and high latitudes, and this aspect of southern right whale’s ecology should beconsidered when discussing site ﬁdelity. The abundance of southern right whales in the Indian sectorof the Antarctic was estimated as 910 in 1988/89 from sightings data (95% CI: 409–2,026) (Matsuoka
and Hakamada, in press) and the number of individuals identiﬁed in this study was 145 (153 minus
eight individuals re-sampled). This corresponds to about 16% (range between about 1–36% of the estimated total population). The low number of matches limits the applicability of inferences on relativesite ﬁdelity and the pattern of longitudinal dispersal to the total population. The comparison above
should be seen with caution. The 1988/89 estimate has wide conﬁdence intervals and the biopsy sampling is pretty wide and carried out after the abundance estimates.
Whilst the present study conﬁrms the feasibility of the approach, it is clear that more deﬁnitive inferences on site ﬁdelity and movement ranges will require a larger number of biopsy samples, fromboth south and north of 60°S (all the samples in this study were obtained south of this latitude).
Food availability in the area of genetic matching
Recognizing the limited number (and sampling distribution) of samples, the present results allow
the formulation of the following ecological inferences for further investigation. The Indian Ocean
sector of Antarctic waters south of 60°S represents one of the several possible feeding grounds for theSouth West Australia population (e.g., see Mackay et al., 2020). Our results show that at least somesouthern right whales of both sexes return to the same sector at some point in their lives, presumably
for feeding. Matches were found in a broad area that has shown consistent annual aggregations ofsouthern right whales (e.g., Matsuoka and Hakamada, 2020) and that were seen in areas of high krill
concentrations (e.g., Murase et al, 2002; Matsuoka et al., 2003; Nicol, 2006).
Qualitative analyses of food consumption of southern right whales in the Antarctic Indian sector
could be investigated by stable isotope analyses of the same biopsy samples used in the present study.
Information on prey species consumed by southern right whales will assist in conﬁrming the ecological inference aforementioned.
Finally, genotyping data in this study can be used for other purposes, for example to estimate abundance and other demographic parameters (e.g., survival rates) of this species within a mark-recapture
context (e.g., Wade et al., 2010).
Acknowledgements

We thank Japanese and international researchers that participated in the JARPA/JARPAII and IDCR/SOWER research
programs for their eﬀort in collecting biopsy samples and for obtaining the ancillary data used in this study. Our gratitude
to Naohisa Kanda for his work on msDNA genotyping. We also thank Shigetoshi Nishiwaki (ICR) for starting the biopsy
sampling of this species in the Antarctic, and for useful comments on southern right whale ecology. Our gratitude to Tatsuya
Isoda (ICR) for his assistance in ﬁgure drawing and Kenji Konishi (ICR) for statistical assistance. Finally, we thank the anonymous reviewers and Greg P. Donovan for their comments and suggestions that improved substantially previous versions of
this paper.

References
Abe, H., Goto, M., Pastene, L.A., Dewa, K. and Naito, E. 2001. Practical use of multiplex ﬂuorescent PCR for cetacean sex
identiﬁcation. Mar. Mammal Sci. 17: 657–664. doi: 10.1111/j.1748-7692.2001.tb01011.x.
Bannister, J. L. 2001. Status of southern right whales (Eubalaena australis) oﬀ Australia. J. Cetacean Res. Manage. (Special

136

Cetacean Popul. Stud. (CPOPS), Full paper
Vol. 3, 2021, 129–138

GENETIC MATCHES OF SOUTHERN RIGHT WHALES
issue) 2: 103–110.
Bannister, J. L., Burnell, S., Burton, C. and Kato, H. 1997. Right whales oﬀ southern Australia: direct evidence for a link between onshore breeding grounds and oﬀshore probable feeding grounds. Rep. int. Whal. Commn. 47: 441–444.
Bannister, J. L., Pastene, L. A. and Burnell, S. R. 1999. First record of movement of a southern right whale (Eubalaena
australis) between warm water breeding grounds and the Antarctic Ocean, South of 60°S. Mar. Mammal Sci. 15(4):1337–1342. doi: 10.1111/j.1748-7692.1999.tb00895.x.
Bérubé, M., Jørgensen, H., Mcewing, R. and Palsbøll, P. J. 2000. Polymorphic di-nucleotide microsatellite loci isolated from the humpback whale, Megaptera novaeangliae. Mol. Ecol. 9(12): 2181–2183. doi: 10.1046/j.1365294x.2000.105315.x.
Best, P. B., Payne, R., Rowntree, V., Palazzo, J. T. and Both, M. D. 1993. Long-range movements of South Atlantic rightwhales, Eubalaena australis. Mar. Mammal Sci. 9 (3): 227–234. doi: 10.1111/j.1748-7692.1993.tb00451.x.
Buchanan, F. C., Friesen, M. K., Littlejohn, R. P. and Clayton, J. A. 1996. Microsatellites from beluga whale Delphinapterus
leucas. Mol. Ecol. 5: 571–575. doi: 10.1046/j.1365-294X.1996.00109.x.
Carroll, E. L., Patenaude, N. J., Alexander, A. M., Steel, D., Harcourt, R., Childerhouse, S., Smith, S., Bannister, J. L., Constantine, R. and Baker, C. S. 2011. Population structure and individual movement of southern right whales around New
Zealand and Australia. Mar. Ecol. Prog. Ser. 432: 257–268. doi: 10.3354/meps09145.
Carroll, E. L., Fewster, R. M, Childerhouse, S. J., Patenaude, N. J., Boren, L. and Baker, C.S. 2016. First direct evidence fornatal wintering ground ﬁdelity and estimate of juvenile survival in the New Zealand southern right whale Eubalaena
australis. PLoS ONE 11 (1): e0146590. doi:10.1371/journal.pone.0146590.
Frasier, T. R, Rastogi, T., Brown, M. W., Hamilton, P. K., Kraus, S. D. and White, B. N. 2006. Characterization of tetranucleotide microsatellite loci and development and validation of multiplex reactions for the study of right whale species(genus Eubalaena). Mol. Ecol. Note 6: 1025–1029. doi: 10.1111/j.1471-8286.2006.01417.x.
Fujise, Y. and Pastene, L. A. 2021. Whales as indicators of historical and current changes in the marine ecosystem of the Indo-Paciﬁc sector of the Antarctic. pp. 85–103. In: Kanao, M., Godone, D. and Dematteis, N. (eds.): Glaciers and Polar
Environment. IntechOpen, London, UK. I-XI+188 pp. doi: 10.5772/intechopen.94323.
Goudet, J. 1995. FSTAT, version 1.2: a computer program to calculate F-statistics. J. Hered. 86: 485–486. doi: 10.1093/
oxfordjournals.jhered.a111627.
International Whaling Commission. 2001. Report of the workshop on the comprehensive assessment of right whales: aworldwide comparison. J. Cetacean Res. Manage. (Special issue) 2: 1–60.
International Whaling Commission. 2013. Report of the IWC workshop on the Assessment of Southern Right Whales. J.
Cetacean Res. Manage. (Suppl.) 14: 437–462.
Mackay, A. I., Bailleul, F., Carroll, E. L., Andrews-Goﬀ, V., Baker, C. S., Bannister, J., Boren, L., Carlyon, K., Donnelly, D.
M., Double, M., Goldsworthy, S. D., Harcourt, R., Holman, D., Lowther, A., Parra, G. J. and Childerhouse, S. J. 2020.
Satellite derived oﬀshore migratory movements of southern right whales (Eubalaena australis) from Australian and
New Zealand wintering grounds. PLoS ONE 15 (5): e0231577. doi: 10.1371/journal.pone.0231577.
Maddison, W. P. and Maddison, D. R. 1989. Interactive analysis of phylogeny and character evolution using the computer
program MacClade. Folia Primatol. (Basel) 53 (1–4): 190–202. doi: 10.1159/000156416.
Mate, B. R., Best, P. B., Lagerquist, B. A. and Winsor, M. H. 2011. Coastal, oﬀshore and migratory movements of South
African right whales revealed by satellite telemetry. Mar. Mammal Sci. 27 (3): 455–476. doi: 10.1111/j.17487692.2010.00412.x.
Matsuoka, K., Watanabe, T., Ichii, T., Shimada, H. and Nishiwaki, S. 2003. Large whale distributions (south of 60°S,
35°E–130°E) in relation to the southern boundary of the Antarctic Circumpolar Current (A CC). pp. 26–30. In: Huiske,
A. H. L., Gieskes, W. W. C., Rozema, J., Schrno, R. M. L., van der Vies, S. M. & Wolﬀ, W.J. (eds.) Antarctic Biology
in a Global Context. Backhuys Publishers, Leiden, The Netherlands. 338 pp.
Matsuoka, K. and Hakamada, T. 2020. 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. Cetacean Popul. Stud. 2:
15–35. doi: 10.34331/cpops.2.1_15.
Matsuoka, K. and Hakamada, T. in press. Estimates of abundance south of 60°S for southern right whales (Eubalaena australis) in the Antarctic Area IV (80°–130°E) based on 1998/99 SOWER survey data. J. Cetacean Res. Manage.
Milmann, L., Taguchi, M., Siciliano, S., Baumgarten, J. E., Oliveira, L. R., Valiati, V. H., Goto, M., Ott, P. H. and Pastene, L.
A. 2021. New genetic evidences for distinct populations of the common minke whale (Balaenoptera acutorostrata) in
the Southern Hemisphere. Polar Biol. 44: 1575–1589. doi: 10.1007/s00300-021-02897-2.
Murase, H., Matsuoka, K., Ichii, T. and Nishiwaki, S. 2002. Relationship between the distribution of euphausiids and baleen
whales in the Antarctic (35°E–145°W). Polar Biol. 25: 135–145. doi: 10.1007/s003000100321.
Murase, H., Palka, D., Punt, A. E., Pastene, L. A., Kitakado, T., Matsuoka, K., Hakamada, T., Okamura, H., Bando, T., Tamura, T., Konishi, K., Yasunaga, G., Isoda, T. and Kato, H. 2020. Review of the assessment of two stocks of Antarctic
minke whales (eastern Indian Ocean and western South Paciﬁc). J. Cetacean Res. Manage. 21: 95–122.
Nicol, S. 2006. Krill, currents, and sea ice: Euphausia superba and its changing environment. BioScience 56 (2):111–120.
doi: 10.1641/0006-3568(2006)056[0111:KCASIE]2.0.CO;2.
Paetkau, D. and Strobeck, C. 1994. Microsatellite analysis of genetic variation in black bear populations. Mol. Ecol. 3: 489–
495. doi: 10.1111/j.1365-294x.1994.tb00127.x.
Palsbøll, P. J. 1999. Genetic tagging: contemporary molecular ecology. Biol. J. Linn. Soc. 68: 3–22. doi: 10.1111/j.1095-

Cetacean Popul. Stud. (CPOPS), Full paper
Vol. 3, 2021, 129–138

137

PASTENE, GOTO, TAGUCHI AND MATSUOKA
8312.1999.tb01155.x.
Palsbøll, P. J., Allen, J., Bérubé, M., Clapham, P. J., Feddersen, T.P., Hammond, P. S., Hudson, R. R., Jorgensen, H., Katona,
S., Larsen, A. H., Larsen, F., Lien, J., Mattila, D. K., Sigurjonsson, J., Sear, R., Smith, T., Sponer, R., Stevick, P. andOien, N. 1997a. Genetic tagging of humpback whales. Nature 388: 767–769. doi: 10.1038/42005.
Palsbøll, P. J., Bérubé, M., Larsen, A. H., and Jørgensen, H. 1997b. Primers for the ampliﬁcation of tri-and tetramer microsatellite loci in baleen whales. Mol. Ecol. 6: 893–895. doi: 10.1046/j.1365-294X.1997.d01-214.x.
Pastene, L. A. and Goto, M. 2016. Genetic characterization and population genetic structure of the Antarctic minke whale
Balaenoptera bonaerensis in the Indo-Paciﬁc region of the Southern Ocean. Fish. Sci. 82: 873–886. doi: 10.1007/
s12562-016-1025-5.
Reeves, R. R., Stewart, B. S., Clapham, P. J. and Powell, J. A. 2002. Guide to Marine Mammals of the World. National Audubon Society. Chanticleer Press, Inc., New York. 527 pp.
Rousset, F. 2008. Genepop’007: a complete re-implementation of the genepop software for Windows and Linux. Mol. Ecol.
Resour. 8: 103–106. doi: 10.1111/j.1471-8286.2007.01931.x.
Sambrook, J., Fritsch, E. F., and Maniatis, T. 1989. Molecular cloning: A laboratory manual. 2nd ed. Cold Spring Harbor
Laboratory, Cold Spring Harbor Laboratory Press, New York, USA.
Valsecchi, E., and Amos, W. 1996. Microsatellite markers for the study of cetacean populations. Mol. Ecol. 5: 151–156. doi:
10.1111/j.1365-294X.1996.tb00301.x.
van Oosterhout, C., Hutchinson, W. F., Wills, D. P. and Shipley, P. 2004. MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Mol. Ecol. Notes 4: 535–538. doi: 10.1111/j.14718286.2004.00684.x.
Wade, P. R., Kennedy, A., LeDuc, R. G., Barlow, J., Carretta, J., Shelden, K., Perryman, W. L., Pitman, R., Robertson, K. M.,
Rone, B., Salinas, J. C., Zerbini, A. N., Brownell, Jr R. L. and Clapham, P. J. 2010. The world’s smallest whale population? Biol. Lett. 7 (1): 83–85. doi: 10.1098/rsbl.2010.0477.
Zerbini, A. N., Ajó, A. F., Andriolo, A., Clapham, P. J., Crespo, E., Gonzalez, R., Harris, G., Mendez, M., Rosenbaum, H.,
Sironi, M., Sucunza, F. and Uhart, M. 2018. Satellite tracking of southern right whales (Eubalaena australis) from
Golfo San Matías, Rio Negro Province, Argentina. Paper SC/67B/CMP/17 presented to the IWC Scientiﬁc Committee,
May 2018 (unpublished). 10 pp. [Available from the IWC Oﬃce].
Zerbini, A. N., Rosenbaum, H., Mendez, M., Sucunza, F., Andriolo, A., Harris, G., Clapham, P. J., Sironi, M., Uhart, M. andAjó, A. F. 2016. Tracking southern right whales through the southwest Atlantic: an update on movements, migratoryroutes and feeding destinations. Paper SC/66b/BRG26 presented to the IWC Scientiﬁc Committee, June 2016 (unpublished). 16 pp. [Available from the IWC Oﬃce].

Received: September 25, 2020
Accepted: August 5, 2021
Published online: November 9, 2021

138

Cetacean Popul. Stud. (CPOPS), Full paper
Vol. 3, 2021, 129–138