SC/F14/J23

Pattern of mercury accumulation in the Antarctic
minke whale and its prey based on JARPAII data
GENTA YASUNAGA, TAKEHARU BANDO AND YOSHIHIRO FUJISE
Institute of Cetacean Research, 4-5 Toyomi-cho, Chuo-ku, Tokyo 104-0055, Japan.

Contact e-mail:yasunaga@cetacean.jp
ABSTRACTTo examine the features of accumulation and yearly changes of total Hg in Antarctic Ocean
Areas IV and V, total Hg levels in samples from Antarctic krill (Euphausia superba), andAntarctic minke whales (Balaenoptera bonaerensis), were measured. Total Hg levels in
Antarctic krill from Areas IV and V were in the range 0.006-0.026 and 0.003-0.052 ppm dry wt.,
respectively. There were no significant differences between Areas. No yearly changes of total Hglevels in Antarctic krill were observed in samples from both Areas in the period from 2005 to
2011. Hg levels in liver of Antarctic minke whales from Areas IV and V were in the range
0.003-0.13 and <0.001-0.25 ppm wet wt., respectively. Hepatic Hg levels of minke whales of all
age groups in Area IV decreased significantly with research years and that of 15-26 year olds in
Area V increased significantly.
KEYWORDS: ANTARCTIC MINKE WHALE; TRACE ELEMENT; BIOACCUMULATION,
AGE TREND, FOOD AVAILABILITYINTRODUCTION
In 1994, the International Whaling Commission (IWC) decided to establish a regular agenda item forresearch on the effects of environmental change on cetaceans in the Scientific Committee (SC) (IWC,1995). At the IWC/SC meeting in 1994, the Committee addressed: (1) global warming; (2) ozone
depletion; (3) pollution; (4) direct and indirect fisheries; (5) noise; and (6) other human activities (e.g.
tourism, coastal development) (IWC, 1995). However, because of the difficulty to examine all topics
simultaneously, it agreed to initially focus on two specialized items; the relationships between chemical
pollutants and cetaceans, and the potential ecological effects of climate change and ozone depletion on
cetaceans (IWC, 1999). The SC decided to hold two workshops (IWC, 1999). The JARPA was designed
to cover these items by collecting related samples and data from the beginning of the program, in order to
respond to a growing concern over environmental changes. Some results on the effects of environmental
changes on cetaceans in JARPA surveys were reported in the JARPA review meeting in 1997
(Government of Japan, 1995; Fujise et al., 1997).
Fujise et al. (1997), Watanabe et al. (1998) and Honda et al. (2006) reported that 'yearly changes of ageaccumulation patterns of hepatic Hg in Antarctic minke whales (Balaenoptera bonaerensis) suggest
possible environment changes such as changes of food availability.’ This hypothesis was also supportedby the studies on biological parameters (Zenitani et al., 1997), body fatness and blubber thickness (Osumi
et al., 1997; Konishi et al., 2008) of Antarctic minke whales. At the 2006 JARPA review meeting,
Yasunaga et al. (2006) reported that Hg intake in young minke whales (1-15 years) significantly
decreased with sampling years, while that of individuals over 16 years old was stable. These results canbe interpreted as changes of the feeding environment of Antarctic minke whales in the later years of the
JARPA.
The objective of the pollution studies in the JARPAII is to continuously monitor levels and behavior of
Hg in minke whales and their food item, Antarctic krill (Euphausia superba). However, most of thesamples for this study since 2005/2006 were lost after the 2011 earthquake and tsunami (see IWC, 2012).
Therefore, the limited number of samples from 2007/2008 and 2010/2011 that were not lost in thedisaster were compared with the previous JARPA data from 1988/1989 and 2004/2005, so that the recent
trend of Hg levels in minke whales could be examined.

1

MATERIALS AND METHODS
Materials
Antarctic krill samples were obtained from stomach contents of a total of 30 Antarctic minke whales
sampled from Areas IV (70-130E) in 2005/2006, 2007/2008 and 2009/2010, and V (130E-170W) in
2006/2007, 2008/2009 and 2010/2011 in JARPAII (Table 1, Fig. 1). All samples were stored in 10%
formalin solution until analysis. Hg was measured from liver samples of 31 (11 males and 20 females)minke whales taken from Areas IV in 2007/2008 and those of 51 males taken from Area V in 2010/2011.
Because of the absence of sex difference of hepatic Hg in minke whales (Fujise et al., 1997; Yasunaga etal., 2006), liver sample of males and females were combined in 2007/2008 (Table 1). All cryopreserved
samples were stored in polyethylene bags at -20°C until analysis.
Laboratory analysis
In the laboratory the whole body of the krill were rinsed with milli-Q water, weighted, dried for 12 hr. at
80°C and reweighted. The samples homogenized using an agate mortar were measured twice. The liver
samples were stripped externally to avoid contamination and were collected from three places. The
samples were measured three times. For Hg analysis, the samples (ca. 100 mg) were set on a ceramic boat
and were subjected to cold-vapor atomic absorption spectrometry with heat-vaporization, gold
amalgamation method (Nippon Instruments Co., MA-3000). Accuracy and precision of the methods wereconfirmed using standard materials, DORM-3 (NRCC: muscle of dogfish).
Statistical analysis
Differences of Hg concentration in Antarctic krill among the samples from both areas were assessed by
Kruscal-Wallis test, and those between Area IV and V were assessed by Mann-Whitney U test (Zar,
1999). Difference of Hg concentrations in the livers of minke whales between Areas IV and V was also
assessed by Mann-Whitney U test (Zar, 1999). Temporal trends of hepatic Hg levels in minke whales
were assessed by simple linear regression analysis (Zar, 1999). In the regression analysis, hepatic Hglevels in minke whales were logarithmically converted, because the distribution of persistent toxic metals,
such as Hg, levels in biota are skewed to higher order. A p value of less than 0.05 was used as thecriterion of statistical significance. These statistical analyses were executed by PASW Statics 17.0 for
Windows (SPSS Co. Ltd.).

RESULTS
Antarctic krill
Hg levels in Antarctic krill form Areas IV and V were in the range 0.006-0.026 and 0.003-0.052 ppm dry
wt., respectively (Table 2). Plots of Hg levels in krill during 2005/2006 and 2009/2010 in Area IV, during
2006/2007 and 2010/2011 in Area V against their sampling years are shown in Fig. 2. No significant
differences were observed in Hg concentrations in krill among the research years in both areas.
Antarctic minke whale
Table 3 shows Hg levels in liver of minke whales form Area IV in 2007/2008 and Area V in 2010/2011,
and those of JARPA data in 1988/89 and 2004/2005 (Yasunaga et al., 2006). Total Hg levels in liver ofminke whales from Areas IV in 2007/2008 and V in 2010/2011 were in the range 0.003-0.13 and <0.0010.25 ppm wet wt., respectively. Plots of hepatic Hg levels in minke whales of 3 age groups (1-15, 16-25
and over 26 years old) in Area IV during a period from 1989/1990 to 2007/2008 and in Area V in the
period from 1988/1989 to 2010/2011 are shown in Fig. 3a and 3b.
Hepatic Hg levels in Area V in 2010/2011 were significantly higher than those in Area IV in 2007/2008
in all age groups with Mann-Whitney U test (p<0.05). Significant linear regression equation wereobserved in in all year groups in Area IV (p<0.05, inclination: -) and 16-25 years old in Area V (p<0.05,
inclination: +).

DISCUSSION
Hg levels in Antarctic krill
It is known that the minke whale is a useful species for examining Hg levels given its high position on thefood chain and long life span (Honda et al., 1987; Yasunaga et al., 2009). Furthermore, Antarctic minke
whales in the Antarctic Ocean mainly feed on the Antarctic krill (Ichii and Kato, 1991; Ichii et al., 1998).
It is important that temporal Hg levels of Antarctic krill in the research area are revealed forunderstanding the accumulation of Hg in minke whales. Yasunaga et al. (2009) reported that temporal2

trends of Hg concentrations in Antarctic krill were not observed during years from 1989 to 1999 using
cryopreserved samples. We analyzed 30 formalin-stored krill samples during the period from 2005/2006
to 2010/2011 in both areas because cryopreserved samples for this monitoring study were lost after the2011 earthquake and tsunami (see IWC, 2012). Formalin-stored samples are not necessary appropriate for
Hg monitoring in biota, because mercury in the human organs immersed in 10% formalin solution isreleased out of the organs (Miyama and Suzuki, 1971). Accordingly, Hg levels in the formalin solution
stored in 05/06-AM507, 07/08-AM307 and 09/10-AM464 were measured, and were 0.003, 0.001 and
0.002 ppm, respectively. This result suggests that the influence of the release of Hg is likely small forassessing spatial trends within a short period. Consequently, the results of no temporal and no regional
trend of Hg in Antarctic krill in the period from 2005/2006 to 2010/2011 in both areas would beappropriate.
Spatial and temporal trend of hepatic Hg
No spatial significant difference of hepatic Hg levels between Area IV in 2007/08 and Area V in 2010/11
was observed. The results indicated that hepatic Hg levels of all age groups in Area IV (Fig. 3a) weresignificantly decreased with research years and that of 15-26 years old in Area V (Fig. 3b) weresignificantly increased.
Assuming a constant level of Hg in a food item, Hg levels in minke whales indicate food intake over along period (Honda et al., 1987; Fujise et al., 1997). Honda et al. (1987) found no significant linear
correlation between Hg in minke whales and ages, suggesting the possibility of the increased food intake
after the 1980’s. Fujise et al. (1997) reported hepatic Hg levels in younger minke whales were lower inthe 1994/95 than those in 1980’s, suggesting possibility that the increased food intake has begun todecrease in 1990’s. Whether or not the increasing in hepatic Hg for age group 15-26 years old in Area V
is related to a increased food intake is unknown at present.

ACKNOWLEDGMENTS
We thank L.A. Pastene of the Institute of Cetacean Research and K. Honda of Ehime University for
helpful suggestions and criticism on the manuscript.

REFERENCES
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mercury accumulations of southern minke whales in past fifteen years. Paper SC/M97/20 presented to
the IWC Intercessional Working Group to Review Data and Results from Special Permit Research onminke whales in the Antarctic, May 1997 (unpublished). 16pp.
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Honda, K., Yamamoto, Y., Kato, H. and Tatsukawa, R. 1987. Heavy metal accumulations and their recentchanges in southern minke whales Balaenoptera acutorostrata. Arch. Environ. Contam. Toxicol.
16:209- 16.
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Antarctic minke whale, Balaenoptera bonaerensis, as tracer of historical change of Antarctic marine
ecosystem during 1980-1999. Bull. Environ. Contam. Toxicol. 76:140-7.
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45:53-103.
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3International Whaling Commission. 2012. Report of the Scientific Committee. Annex P1. Effect of the
March 11th earthquake and tsunami on JARPAII/JARPNII data and samples. J. Cetacean Res. Manage.
(Suppl.) 13:308-9.
Konishi, K., Tamura, T., Zenitani, R., Bando, T., Kato, H. and Walløe, L. 2008. Decline in energy storage
in the Antarctic minke whale (Balaenoptera Bonaerensis) in the Southern Ocean. Polar Biol. 31:150920.
Miyama, T. and Suzuki, T. 1971. Release of mercury from organs and breakage of carbon-mercury bondin tissues due to formalin fixation. Sangyo Igaku 13(6):56-7.
Ohsumi, S., Fujise, Y., Ishikawa, H., Hakamada, T, Zenitani, R. and Matsuoka, K. 1997. The fattyness of
the Antarctic minke whale and its yearly change. Paper SC/M97/18 presented to the IWC Intersessional
Working Group to Review Data and Results from Special Permit Research on Minke whales in the
Antarctic, May 1997 (unpublished). 21pp.
Watanabe, I., Yamamoto, Y., Honda, K., Fujise, Y., Kato, H., Tanabe, S. and Tatsukawa, R. 1998.
Comparison of mercury accumulation in Antarctic minke whale collected in 1980-82 and 1984-86.
Nippon Suisan Gakkaishi, 64:105-9. (in Japanese)
Yasunaga, G., Fujise, Y., Zenitani, R., Honda, K. and Kato, H. 2006. Yearly trend of trace element
accumulation in liver of Antarctic minke whale, Balaenoptera bonaerensis. Paper SC/D06/J28
presented to the IWC Sponsored Meeting to Review Data and Results from the Japanese Whale
Research Program under Special Permit in the Antarctic (JARPA) (JARPA Review Meeting), December
2006 (unpblished). 23pp.
Yasunaga, G. and Fujise, Y. 2009. Temporal trends and factors affecting mercury levels in common
minke, Bryde's and sei whales and their prey species in the western North Pacific. Paper SC/J09/JR23
presented to the IWC Sponsored Meeting to Review Data and Results from the Japanese Whale
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Review Meeting), Tokyo, January 2009 (unpublished). 13pp.
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Zenitani, R., Fujise, Y. and Kato. H. 1997. Biological parameters of Southern minke whales based onmaterials collected by the JARPA survey under special permit in 1987/88 to 1995/96. Paper SC/M97/12
presented to the IWC Intercessional Working Group to Review Data and Results from Special Permit
Research on Minke whales in the Antarctic, May 1997 (unpublished). 19pp.

4

Table 1. Samples of Antarctic minke whales and Antarctic krill taken from the stomach contents
examined in the present study.
Species(Scientific name )Antarctic krill(Euphausia superba )Antarctic minke whale(Balaenoptera bonaerensis )

Year

Area

n sex

2005/2006
2006/2007
2007/2008
2008/20092009/20102010/2011

Area IV
Area V
Area IV
Area V
Area IV
Area V

2007/2008

Area IV

2010/2011

Area V55555511 males20 females
51 malesBody length (m)Ave. (min.-max.)

7.95 (5.53-9.58)
8.15 (6.79-9.07)
8.46 (5.31-9.67)

Table 2. Total Hg concentrations (μg/g dry wt.) of Antarctic krill taken from stomach of Antarctic minke
whales in JARPAII surveys.
research year

2005/2006

2007/20082009/2010

total

average±SD0.019 ± 0.004

0.011 ± 0.004

0.013 ± 0.008

0.014 ± 0.006

Area-IVrange(

0.012 - 0.022) (0.006 - 0.016) (0.007 - 0.026) (0.006 - 0.026

n

5

5

5

5

research year

2006/2007

2008/20092010/2011

total

average±SD0.036 ± 0.017

0.016 ± 0.012

0.017 ± 0.007

0.024 ± 0.015)

Area-Vrange
n(0.017 - 0.052) (0.003 - 0.031

5

5

) (

0.011 - 0.028
5) (0.003 - 0.052)

5

Table 3. Total mercury concentrations in liver of Antarctic minke whales taken from Areas IV and V in
JARPA and JARPAII surveys.
Age Class
89/90 Ave±SD
range (
n
91/92 Ave±SD
range (
n
93/94 Ave±SD
range (
n
95/96 Ave±SD
range (
n
97/98 Ave±SD
range (
n
99/00 Ave±SD
range (
n
01/02 Ave±SD
range (
n
03/04 Ave±SD
range (
n1-15 years old
0.078 ± 0.036
0.027 - 0.166
41
0.078 ± 0.037
0.036 - 0.1515
0.038 ± 0.019
0.012 - 0.080
16
0.048 ± 0.028
0.012 - 0.1530
0.041 ± 0.027
0.004 - 0.098
13
0.040 ± 0.024
0.007 - 0.076
10
0.033 ± 0.018
0.008 - 0.064
10
0.033 ± 0.028
0.004 - 0.096
10Area IV
16-25 years old
Ovre 26 years old
0.078 ± 0.034
0.088 ± 0.041) ( 0.033 - 0.14 ) ( 0.021 - 0.16 )32
27
0.070 ± 0.032
0.071 ± 0.029) ( 0.037 - 0.14 ) ( 0.045 - 0.13 )1011
0.069 ± 0.046
0.065 ± 0.057) ( 0.024 - 0.16 ) ( 0.014 - 0.20 )8120.061 ± 0.017
0.060 ± 0.024) ( 0.039 - 0.086 ) ( 0.035 - 0.15 )13
27
0.086 ± 0.030
0.089 ± 0.056) ( 0.049 - 0.13 ) ( 0.038 - 0.16 )66
0.067 ± 0.015
0.070 ± 0.041) ( 0.044 - 0.084 ) ( 0.029 - 0.13 )550.054 ± 0.023
0.075 ± 0.017) ( 0.031 - 0.086 ) ( 0.056 - 0.092 )550.060 ± 0.023
0.050 ± 0.034) ( 0.034 - 0.087 ) ( 0.019 - 0.11 )5
5

07/08 Ave±SD 0.037 ± 0.032
0.044 ± 0.027
0.038 ± 0.026
range ( <0.001 - 0.13 ) ( 0.018 - 0.082 ) ( 0.003 - 0.066 )
23
n
4
4

Area VAge Class1-15 years old
16-25 years old
Ovre 26 years old
88/89 Ave±SD0.061 ± 0.031
0.079 ± 0.033
0.095 ± 0.072
range ( 0.006 - 0.14 ) ( 0.030 - 0.13 ) ( 0.023 - 0.23 )
36
12
7
n
90/91 Ave±SD0.067 ± 0.023
0.074 ± 0.030
0.088 ± 0.031
range ( 0.038 - 0.11 ) ( 0.036 - 0.12 ) ( 0.056 - 0.16 )
14
10
12
n
92/93 Ave±SD0.082 ± 0.034
0.064 ± 0.037
0.084 ± 0.044
range ( 0.041 - 0.15 ) ( 0.029 - 0.14 ) ( 0.027 - 0.18 )
11
9
16
n
94/95 Ave±SD0.067 ± 0.036
0.086 ± 0.041
0.12 ± 0.049
range ( 0.015 - 0.15 ) ( 0.046 - 0.18 ) ( 0.052 - 0.24 )
18
16
15
n
96/97 Ave±SD0.069 ± 0.074
0.068 ± 0.032
0.095 ± 0.042
range ( 0.007 - 0.27 ) ( 0.028 - 0.12 ) ( 0.047 - 0.20 )
11
5
12
n
98/99 Ave±SD0.050 ± 0.028
0.10 ± 0.049
0.13 ± 0.11
range ( 0.008 - 0.11 ) ( 0.054 - 0.19 ) ( 0.039 - 0.43 )
27
11
14
n
00/01 Ave±SD0.051 ± 0.020
0.067 ± 0.030
0.13 ± 0.074
range ( 0.027 - 0.090 ) ( 0.044 - 0.12 ) ( 0.054 - 0.24 )105
5
n
02/03 Ave±SD0.044 ± 0.029
0.13 ± 0.066
0.13 ± 0.084
range ( 0.006 - 0.095 ) ( 0.063 - 0.24 ) ( 0.060 - 0.27 )1055
n04/05 Ave±SD0.048 ± 0.025
0.078 ± 0.037
0.075 ± 0.020
range ( 0.019 - 0.086 ) ( 0.047 - 0.14 ) ( 0.058 - 0.11 )105
5n
10/11 Ave±SD 0.066 ± 0.040
0.11 ± 0.048
0.089 ± 0.042
range ( <0.001 - 0.15 ) ( 0.036 - 0.21 ) ( 0.022 - 0.15 )
27
15
9
n

5

Area IV

Area V

Total Hg concentrations in Antarctic krill (μg/g dry wt.)

Figure 1. Sampling area of Antarctic minke whales in JARPAII surveys.

0.060
0.050

Area IV

0.040
0.030
0.020
0.010
0.000
2004

2005
2006 2007/2008
2007
2008 2009/2010
2009
2010
2005/2006

2011

0.060
0.050

Area V

0.040
0.030
0.020
0.010
0.000
2004

2005

2006
2007 2008/2009
2008
2009 2010/2011
2010
2011
2006/2007
Research years

Figure 2. Total mercury concentrations (μg/g dry wt.) in Antarctic krill
taken from sotmach content of Antarctic minke whales in JARPAII surveys.

60.300Area IV
1-15 years old

Total mercury concentrations (ppm wet.) in liver

0.200

0.100

0.000

‘89/90‘91/92‘93/94‘95/96‘97/98‘99/00‘01/02‘03/04
1988
1990
1992
1994
1996
1998
2000
2002
2004

0.300

‘07/08
2006
2008

Area IV
16-25 years old

0.200

0.100

0.000

‘89/90‘91/92‘93/94‘95/96‘97/98‘99/00‘01/02‘03/04
1988
1990
1992
1994
1996
1998
2000
2002
2004

‘07/08
2006
2008

0.300

Area IVOver 26 years old

0.200

0.100

0.000

‘89/90‘91/92‘93/94‘95/96‘97/98‘99/00‘01/02‘03/04
1988
1993
1998
2003

‘07/082008

Research year

Figure 3a. Total mercury concentrations (ppm wet wt.) in liver of Antarctic minke whales in Area IV in
the JARPA and JARPAII surveys.
●: Hg concentrations in individuals, ―――: simple linear regression line―◇―: Average of Hg concentrations in whales in each research year.
0.300

Area V
1-15 years old

Total mercury concentrations (ppm wet.) in liver

0.200

0.100

0.000

‘88/89 ‘90/91 ‘92/93‘00/02 2002
‘02/03‘04/05
1987
1992 ‘94/95‘96/97‘98/99
1997

0.300

‘10/11

2007

Area V
16-25 years old

0.200

0.100

0.000

‘88/89 ‘90/91 ‘92/93‘00/02 2002
‘02/03‘04/05
1987
1992 ‘94/95‘96/97‘98/99
1997‘10/11

2007

0.500
0.400

Area VOver 26 years old

0.300
0.200
0.100
0.000

‘88/89 ‘90/91 ‘92/93‘00/02 2002
‘02/03‘04/05
1987
1992 ‘94/95‘96/97‘98/99
1997‘10/11

2007

Research year

Figure 3b. Total mercury concentrations (ppm wet wt.) in liver of Antarctic minke whales in Area V in the
JARPA and JARPAII surveys.
●: Hg concentrations in individuals, ―――: simple linear regression line―◇―: Average of Hg concentrations in whales in each research year.

7