First Symposium on Steller’s and White-tailed Sea Eagles in East Asia pp. 91-106, 2000
UETA, M. & MCGRADY, M.J. (eds) Wild Bird Society of Japan, Tokyo Japan

Contamination by chlorinated hydrocarbons and lead in Steller’s Sea Eagle
and White-tailed Sea Eagle from Hokkaido, Japan
Hisato IWATA1*, Mafumi WATANABE2, Eun-Young KIM1, Rie GOTOH2,
Genta YASUNAGA2, Shinsuke TANABE2, Yasushi MASUDA3 & Shoichi FUJITA1
1. Department of Environmental Veterinary Sciences, Graduate School of Veterinary Medicine, Hokkaido
University, N18 W9 North Ward, Sapporo, Japan.
2. Department of Environment Conservation, Ehime University, Tarumi 3-5-7, Matsuyama, Japan.
3. Shiretoko Museum, Honmachi 49, Shari, Hokkaido, Japan.

Abstract. Chronic exposure to man-made chemicals, particularly chlorinated hydrocarbons, in raptors
has been associated with reproductive impairment and population declines. In addition, incidents of
sub-lethal and lethal lead poisoning in raptors through ingestion of spent gunshot have been reported.
However, little information is available on the contaminant levels of Steller’s Sea Eagle (SSE:
Haliaeetus pelagicus) and White-tailed Sea Eagle (WSE: H. albicilla) from Hokkaido, Japan. The
objective of this study was to determine the levels of toxic contaminants including polychlorinatedbiphenyls (PCBs), organochlorine pesticides, and lead in sea eagles wintering in Hokkaido, and toevaluate the ecotoxicological risk based on their concentrations. SSEs and WSEs which were founddead or debilitated and subsequently died in Hokkaido from 1986 to 1998 were analysed.
All eagles contained detectable amounts of PCBs, DDTs, hexachlorocyclohexane isomers, chlordane
related compounds, and hexachlorobenzene. The highest concentrations of PCBs and DDTs in breast
muscles were 18,000 and 17,000 ng/g (wet weight), respectively. Furthermore, non-ortho and monoortho substituted coplanar PCB congeners were also detected, leading to 60-540 pg/g of 2,3,7,8tetrachlorodibenzo-p-dioxin toxic equivalents derived from WHO toxic equivalence factors in thebreast muscles. Our previous survey of contaminants in the Far East showed that atmosphericconcentrations of PCBs and DDTs in Khabarovsk and Magadan were much higher than those in
Hokkaido and North Pacific, suggesting the potential that some east Siberian cities might be a source ofcontamination found in eagles. Residue levels of PCBs and DDTs in breast muscles of SSEs werecomparable to those of raptors collected after the 1980s from North America. Risk assessments
based on the residue levels of coplanar PCB congeners and p,p’-DDE detected in these eagles indicatedtheir potential of hepatic cytochrome P450 1A induction and eggshell thinning.
High lead concentrations of over 10,000 ng/g (dry weight) were detected in the livers of some SSEs and
WSEs. Three of six dead or moribund SSEs (50%) and three of three WSEs (100%) with livers
analyzed for lead died from lead poisoning. Five of the six lead poisoned eagles had lead bullet
fragments in their gizzards. The hair of deer was found along with a lead fragment in the intestine of* Present address: Center for Marine Environmental Studies, Ehime University, 3-5-7 Tarumi, Matsuyama,
Japan. e-mail: iwatahisa@aol.com

92
a SSE. In Hokkaido, whole and partial carcasses of deer shot by hunters are left in the field. These arepotential sources of lead fragments that are ingested by scavenging raptors during and after thehunting season. Therefore, secondary poisoning by the lead fragment embedded in the tissue of deer is
implicated as the main cause of death. Mercury and cadmium concentrations in the tissue of these
species were low, implying that the toxicities of these elements were negligible.

INTRODUCTION
Chlorinated hydrocarbons (CHCs) are ubiquitous contaminants detected in various
environmental compartments on a global scale (Iwata et al. 1993), and are notably
bioaccumulated in higher trophic organisms through the food web (Muir et al. 1988, Tanabe1988). Contamination of marine organisms by CHCs, such as polychlorinated biphenyl (PCB)
and DDT, continues to be an issue of growing concern. Concerns are based on the implicationthat CHCs can cause a variety of adverse effects including teratogenicity, reproductive failure,and endocrine disruption in higher trophic animals such as raptors and fish-eating waterbirds(Giesy et al. 1994).
Lead poisoning of waterfowl through the ingestion of spent lead shot has also beenreported in various areas of the world (Anderson 1975, Guitart et al. 1994). In addition, it is
known that raptors have been exposed to high levels of lead through secondary ingestion oflead shot embedded in the tissue of waterfowl and other prey. The widespread mortality of
raptors by secondary lead poisoning, especially Bald Eagle Haliaeetus leucocephalus andsome hawks that feed on dead or wounded waterfowl, has been documented in the UnitedStates, Canada and Europe (Reichel et al. 1984, Elliott et al. 1992, Pain & Amiard-Triquet1993). In these countries, concern over lead poisoning led, in the 1980’s, to the progressive
prohibition of the use of lead shot to harvest waterfowl. In Japan, no such restriction has been
introduced.
Steller’s Sea Eagle (SSE: H. pelagicus) and White-tailed Sea Eagle (WSE: H. albicilla)
are classified as “vulnerable” and “endangered”, respectively in the Red Data Book of theEnvironment Agency of Japan. SSE breeds on large rivers and the coast in northeast SiberiaKamchatka and winters to northern Japan, Kamchatka and south of Korea (Nakagawa et al.
1987). WSE in the Far East is distributed in Kamchatka, Okhotsk, Sakhalin and Hokkaido andwinters to Japan and Korea (Knystautas 1993). Hokkaido is a critical habitat area for both
species.
Little information is available on the contaminant levels of CHCs and lead in these sea
eagles. The objective of this study was to determine the levels of CHCs and toxic metals
including lead, mercury and cadmium in SSE and WSE migrating to Hokkaido, Japan, and toevaluate the ecotoxicological risk based on their concentrations. This paper summarizes datapreviously reported in several papers by our group (Iwata et al. 1997, Kim et al. 1999,
Yasunaga et al. 2000) and includes some additional data.

93
Table 1. Details of Steller's Sea Eagles (SSEs) and White-tailed
Sea Eagles (WSEs) analyzed.
Sample No.
1
2
3
4
5
6
7

Species
SSE
SSE
SSE
SSE
SSE
SSE
SSE

Collection date
Apr. 1995
Feb. 1994
Dec. 1986
Feb. 1997
Jan. 1998
Feb. 1998
Mar. 1998

Body weight (kg)
4.3
4.2
6.0
3.7
4.6
4.2
3.8

sex
♀

8
9
10

WSE
WSE
WSE

Jan. 1997
Dec. 1997
Feb. 1998

4.7
3.7
3.8

♀
♀
♀

♂

♀
♀
♀
？
♂

MATERIALS AND METHODS
SamplesSeven SSEs and three WSEs were collected in eastern Hokkaido, within the main area
where deer hunting was permitted from 1986 to 1998 (Table 1). Two SSEs (sample nos. 1 and
3) and one WSE (no. 8) were found dead. One SSE (no. 2), with an external injury on the left
wing, was captured, but died on the same day. The other eagles were found in a debilitatedcondition, captured, but subsequently died. From the intestine or gizzard of two SSEs (nos. 4
and 7) and all WSEs (nos. 8-10), lead bullet fragments were found. Deer hair along with ametallic fragment was also found in the intestine of a SSE (no. 4). In the case of carcass no.8
(WSE), one fragment was collected from the gizzard, two fragments were embedded in bone,
one in fat around the abdominal membrane, and seven in muscle. The injuries around thefragments embedded in body tissues had healed, indicating this bird had survived being shot.
The birds in whose alimentary canal lead fragments were found showed clinical signs of leadpoisoning including hypertrophy of the gall bladder and green feces.
Carcasses were weighed, a clinical diagnosis was made, and liver, kidney and breast
muscle were removed and stored at -20°C until analysis.
Chemical analysis
The analysis of CHCs, including hexachlorobenzene (HCB), hexachlorocyclohexane(HCH: α and β isomers), chlordane compounds (CHLs: cis-chlordane, trans-chlordane, cisnonachlor, trans-nonachlor, and oxychlordane), and DDTs (p,p’-DDE, p,p’-DDD, and p,p’DDT) was performed following the procedure described by Tanabe et al. (1984). Briefly, theanalytical method involved Soxhlet extraction of homogenized fat samples (5 g) with a mixtureof diethyl-ether and hexane (3 : 1, 400 ml), followed by elution through a florisil packed
glass column with 150 ml of 20% hexane-washed water in acetonitorile, for the removal of fat.
The eluent was collected in a separation funnel containing 100 ml hexane and 600 ml hexanewashed water. Subsequently, the concentrated hexane layer was cleaned and fractionated94
with a 12 g florisil packed glass column. The first fraction eluted with hexane contained
HCB, PCBs, p,p’-DDE and trans-nonachlor, while the second fraction, eluted with 20%
dichloromethane in hexane, was comprised of other organochlorine pesticides. Each fraction
was concentrated and the extracts were subjected to a further clean-up with a 5% mixture of
fuming H2SO4 in concentrated H2SO4.
The extraction and separation of individual PCB congeners including non-ortho PCBs
(3,3’,4,4’-TeCB, 3,3’,4,4’,5-PeCB and 3,3’,4,4’,5,5’-HxCB) and mono-ortho PCBs
(2,3,3’,4,4’-PeCB, 2,3’,4,4’,5-PeCB and 2,3,3’,4,4’,5-HxCB) followed the KOH-digestion
method by Wakimoto et al. (1971), and the activated carbon column method by Tanabe et al.
(1987), respectively.
The quantification of organochlorine pesticides were made on a gas chromatogragh(Hewlett-Packard 5890) equipped with a 63Ni electron capture detector and moving needletype injection port. Analysis of the PCB congeners was made using the gas chromatogragh
coupled with mass spectrometry (Hewlett-Packard 5972). A DB-1 capillary column (30 m x
0.25 mm i.d., film thickness of 0.25 micro meter, J&W Scientific, CA, USA) was employed forthe separation of individual compounds.
An equivalent mixture of Kanechlor preparations (KC-300, KC-400, KC-500 and KC600) with known PCB composition and content was used as a standard. Concentrations ofindividually resolved peaks of PCB isomers and congeners were summed to obtain total PCB
concentration. Organochlorine pesticides and coplanar PCB congeners were quantified fromindividually resolved peak areas with the corresponding peak areas of authentic standards.
Concentrations of CHCs were given on wet weight basis.
For metal analyses, the method has been reported in detail elsewhere (Kim et al. 1999;
Yasunaga et al. 1999). Three subsamples of each tissue were analyzed to avoid local tissue
contamination by lead-shot damage. Subsamples were dried to a constant weight in an oven at
80°C for 12hrs. Analyses for lead and cadmium were performed by inductively coupledplasma-mass spectrometer (ICP-MS; Perkin Elmer ELAN 5000), after microwave digestion
with nitric acid in a PTFE (Teflon) vessel (Okamoto 1994). A mixed multi-element standard
solution was prepared from 10 micro g/g stock solution. NIST SRM 1577b bovine liver wasused for the determination of recoveries of these two elements. Recoveries of lead andcadmium were in the range of 97-116% and 95-105% of the certified values, respectively.
Total mercury levels were determined by cold vapor technique using Sansou Automatic
Mercury Analyzer Model MERCURY-3000 spectra-photometer and Shimadzu AA-680 after
microwave digestion with nitric acid (Akagi & Nishimura 1991). Analytical quality assurance
was conducted using a standard reference material, NIES No. 1 (Okamoto et al. 1978).
Recovery of mercury was 98% of the certified value. Concentrations of all the elements
were given on dry weight basis.

95

RESULTS AND DISCUSSION
CHC levels and source allocation
Table 2 shows levels of CHCs in SSE and WSE. All eagles were contaminated bydetectable amounts of CHCs. No differences in CHC accumulation were observed between
SSE and WSE. Among the CHCs analyzed, the concentrations of PCBs and DDT wererelatively higher than those of other compounds. The highest concentrations of PCBs reached
18 and 41 micro g/g (wet weight) in breast muscle and liver, respectively. The highest total
DDT concentrations were 17 micro g/g in the breast muscle and 15 micro g/g in the liver.
These concentrations were higher than those in most other bird species in Japan such as
Common Cormorants Phalacrocorax carbo, Black-crowned Night Heron Nycticorax
nycticorax, and Mountain Hawk-eagle Spizaetus nipalensis reported by Hoshi et al. (1998).
One reason for the elevated residue levels found in these eagles may be the relatively higher
trophic level to which they belong. Sea eagles mainly feed on fish, including Walleye Pollock
and salmon, and occasionally stranded marine mammals. Some components of the sea eagle’s
diet are likely to contribute to the high contaminant levels observed.
Furthermore, three non-ortho (3,3’,4,4’-TeCB, 3,3’,4,4’,5-PeCB, 3,3’,4,4’,5,5’-HxCB)
and three mono-ortho (2,3,3’,4,4’-PeCB, 2,3’,4,4’,5-PeCB, 2,3,3’,4,4’,5-HxCB) substituted
coplanar PCB congeners were also detected in significant amounts (Table 2). Concentrationsof mono-ortho coplanar PCBs were greater than non-ortho congeners in all the samples
analyzed. For the non-ortho PCBs, the levels of 3,3’,4,4’-TeCB and 3,3’,4,4’,5-PeCB varied
widely among samples, while 3,3’,4,4’,5,5’-HxCB was consistently lowest. As for the monoortho PCBs, in most samples the pattern was 2,3’,4,4’,5-PeCB > 2,3,3’,4,4’-PeCB >2,3,3’,4,4’,5-HxCB. The 2,3,7,8-tetrachlorodibenzo-p-dioxin toxic equivalents (TEQs)
calculated with WHO toxic equivalence factors (Ahlborg et al., 1994) ranged from 60-540 pg
TEQ/g (wet weight) in the breast muscle and 36-2100 pgTEQ/g in the liver. In the coplanar
PCB congeners, 3,3’,4,4’,5-PeCB made a greater contribution to total TEQs, and followed by
2,3’,4,4’,5-PeCB.
A survey of CHC contamination in the Far East including the area used by these eagles
for breeding and wintering showed that atmospheric CHC levels in Khabarovsk and Magadan
were much higher than those in Hokkaido and the North Pacific Ocean (Iwata et al. 1995). In
air samples from Khabarovsk where elevated PCB levels were recorded, congeners with fouror five chlorines were detected at higher levels. This profile was very similar to that of the PCB
product, Sovol, that was manufactured in the former Soviet Union. In contrast, air samples
from Chaun exhibited the lowest concentration of PCBs, and contained chlorinated congeners
with two or three chlorines that are known to be preferentially transported by air to remoteareas. These results suggest a potential for Khabarovsk and Magadan to be CHC
contamination sources for eagles that breed in these areas, and others that migrate through but
feed during passage. Recent studies of migration routes of SSE and WSE by satellite tracking
confirms this risk of exposures. SSE tracked from wintering grounds in Hokkaido migrate toTable 2. Concentrations of CHCs (ng/g on wet weight basis) and metals (micro g/g on dry weight basis) in tissues of SSEs and WSEs.
1
SSE
BM
L
K
8.7
4.5

2
SSE
BM
0.91

3
SSE
BM
L
6.7
6.5

K

4
SSE
L
K
3.5

5
SSE
L
3.7

K

6
SSE
BM
L
0.94

K

7
SSE
BM
L
4.3

K

8
WSE
L
K
5.8

9
WSE
L
4.4

10
WSE
BM
L
5.2

HCB

31

17

85

50

44

110

23

18

29

9.6

9.7

11

HCHs
α-HCH
β-HCH

0.52
73

< 0.2
36

2.5
450

1.8
310

1.6
250

1.6
400

0.47
44

1.2
79

0.55
64

0.21
43

0.70
72

0.37
25

DDTs
p,p' -DDE
p,p' -DDD
p,p' -DDT

2200
92
13

580
31
2.5

17000
190
34

3100 2800
310 230
23
9.7

15000
300
23

390
65
2.9

850
84
15

1800
72
12

2500
26
1.7

590
38
3.7

1200
53
<1.5

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

110
29
5.3
27
190

39
10
< 0.9
8.8
56

790
44
7.2
160
2000

100
72
13
47
310

55
49
6.6
34
230

380
79
7.3
180
1600

18
16
<0.5
15
65

61
20
<0.5
22
130

87
29
<0.5
49
430

26
7.7
0.92
19
82

17
16
<0.5
20
82

28
17
<0.5
22
90

0.14
0.23
0.06

1.0
2.3
0.55

3.7
1.7
0.24

3.1
1.5
0.23

5.0
11
3.8

0.34
0.23
0.072

0.37
0.31
0.091

0.71
1.1
0.37

0.98
1.1
0.39

0.54
0.42
0.093

0.68
0.61
0.20

25
86
14
0.042
820

420
1700
180
0.54
18000

140 160
380 4703760
0.24 0.254300 5000

1500
4700
710
2.1
41000

24
70
4.7
0.036
820

44
140
18
0.060
2400

51
150
20
0.14
1900

130
500
110
0.23
6000

0.40
150
15
0.066
1600

49
170
20
0.095
1800

0.11 0.11
0.06 0.21 1.1
0.15 1.3 < 0.001 1.0 1.3
5.0
13
2.7
16 12

4.0
0.033
1.8

79 58
0.67 6.5
2.6 5.4

77
0.26
2.0

9.3
0.015
1.4

PCBs
non-ortho coplanar PCBs
3,3',4,4'-TeCB
0.40
3,3',4,4',5-PeCB
0.63
3,3',4,4',5,5'-HxCB
0.19
mono-ortho coplanar PCBs
2,3,3',4,4'-PeCB
51
2,3',4,4',5-PeCB
210
2,3,3',4,4',5-HxCB
26
TEQ (WHO)
0.10
Total PCBs
2100
Metals
Pb
Cd
Hg

4.0
< 0.050.68

75 102
1.3 5.1
2.8 5.5

BM: breast muscle, L: liver, K: kidney

0.04
0.07
0.16 < 0.05
4.6
0.83

0.06 0.06
0.18 1.0
4.2 7.6

139 670.61 7.9
7.0 15232 103
0.61 3.6
4.9 8.4

96

Sample Nos.
Species
Tissuelipid content (%)

K

174 141
0.26 2.3
3.7 19

97
northern Sakhalin and then to nearby continental seaboards (Amur-Shantarskiye Islands) in
spring (Ueta et al. 2000). Also juvenile SSE fledged in Magadan wintered in Hokkaido(McGrady et al. 2000), and WSE satellite tracked in spring migrate from Hokkaido to Sakhalin,then along the coast of the Ohotsk Sea, and spend the summer in northern Kamchatka (Ueta etal. 1998).
Table 3 compares levels of CHCs in SSE and WSE with those in eagles from otherlocations. The concentrations in breast muscle and liver of SSE and WSE appear to becomparable to those of Bald Eagle from Lake Superior and British Columbia, and residue
levels in breast muscles of SSE and WSE from Hokkaido were equal to or less than those inEuropean WSE collected from the Baltic Sea and north western Poland.
Toxicological implications by CHCs
Avian egg shell thinning is thought to be influenced mainly by exposure to p,p’-DDT
metabolites, p,p’-DDE. Although we could not measure thickness of SSE and WSE egg
shell, degree of egg shell thinning was assessed from p,p’-DDE concentrations in breast
muscle using the negative relationships between egg p,p’-DDE levels and shell thickness
observed in three raptors, Cooper’s Hawk Accipiter striatus, Sharp-shinned Hawk A. cooperii,
and Goshawk A. gentilis, by Elliott et al. (1994). On the assumptions that p,p’-DDE level inbreast muscle reflects the residue level in egg and there is no differences in the regression
slopes of eggshell thickness on p,p’-DDE exposure between the three hawk species and the sea
eagles, reductions in shell thickness of 2.8-20% were anticipated. In addition, p,p’-DDE
concentrations in breast muscle from eagle no.2 and liver from eagle no.4 were greater than the
no-observable-adverse-effect concentrations (3.5 micro g/g) for Bald Eagle proposed by
Wiemeyer et al. (1984) and Bowerman et al. (1995).
Coplanar PCB congeners are structural analogues with polychlorinated dibenzo-pdioxins, which are known to produce a broad spectrum of biological and toxicologicalresponses including hepatic cytochrome P450 1A (CYP 1A) induction in animals. The
responses to both compounds are mediated through an aryl hydrocarbon receptor. Consistent
structure-activity relationships have been found for such responses among dioxin and coplanar
PCB congeners. Therefore, the toxic potencies of each congener have been evaluated as
toxic equivalence factor given to the individual compounds, which have been used to calculate
TEQ in environmental samples containing a complex mixture of congeners. In the breast
muscles of two SSE (nos. 2 and 3) and the livers of two SSE (nos. 3 and 4) and one WSE (no.
8) were 1.1-10 times greater than a lowest-observable-effect level (210 pg TEQ/g) for CYP1A
induction in bald eagle chick liver (Elliott et al. 1996b). TEQ values suggests possible hepatic
CYP1A induction in some eagles in this study, if assumptions are correct that there are nodifferences in TEQs between adult and chick, and no differences in responses to CYP1A
induction among the eagle species.
In a review of the effects of TEQs on birds by Giesy et al. (1994), the lowest-observable-

Table 3. Comparison of CHC concentartions (ng/g on wet weight basis) in the tissues of eagles.
Japan

Japan

Hokkaido

Hokkaido

USA

PolandFinlandFinlandFinland

Japan

Japan

CanadaUSA

CanadaFinlandFinlandFinland

Baltic Sea

Baltic Sea

Baltic Sea

Hokkaido

Hokkaido

BC

Columbia R.

BC

Baltic Sea

Lapland

Baltic Sea

Species

SSE

WSE

BE

Tissue

BM

BM

BM

WSE

WSE

WSE

WSE

SSE

WSE

BE

BE

BE

WSE

WSE

WSE

BM

BM

BM

BM

L

L

L

Egg

Egg

Egg

Egg

HCB

18-85

11

20-40

Egg

29-21057-1350

38-596

17-1109.6-9.7

6-89<10-500

40-220311

70

51-166α-HCH

0.52-2.5

0.37

β-HCH

64-450

25

<5.1

<3

<0.2-1.6

0.21-0.70<3<336-400

43-72

1-308

p,p' -DDE

850-17000

1200

10000-67000

470-32100

p,p' -DDD

72-31053

530-1800

58-18803518-27500

390-15000

590-2500

56-26800

8800

910

5210-9000

48-72131-300

26-38

312

53

p,p' -DDT

12-34

<1.5

<10

<3

60-175

2.5-23

1.7

<3

<3

310-1200

43-1440

18-380

17-26

169

24

79-310<3-12610-79

7.7-16

138

11

11-24

8-407

<0.9-7.3

0.92

6

<3

8.8-180

19-20
331

19

108-416

L. Superior North Western

HCHs

66-330DDTs
120-6600

4000-20000

6900-36000

300-2600

CHLs
oxychlordane

61-79028

cis -chlordane

20-72

17

trans -chlordane<0.5-13<0.5

cis -nonachlor22-16022trans -nonachlor130-2000

90

3,3',4,4'-TeCB

0.37-3.7

0.68

2.9-140

3,3',4,4',5-PeCB

0.31-2.3

0.61

1.2-160

3,3',4,4',5,5'-HxCB

0.091-0.55

0.20

0.15-38200

76-150070
430-990

4-303

71-38023-1610390-3500

63-313

19-1130

255-1285

56-1600

82

1.7-2.2

9.8-710.49-3.8

0.14-5.0

0.54-0.98

0.248-2.3

2.0-12

21

9.8

0.82-1.1

4.9-44

0.97-51

3.3-32

0.23-11

0.42-1.1

0.349-9.96

3.3-1320.6

0.95

5.2-8.9

1.4-9.3<0.2-200.77-6.4

0.06-3.8

0.093-0.39

0.056-2.64

0.55-2.1

6<0.2

1.1-2.2

PCBs
non-ortho coplanar PCBs

mono-ortho coplanar PCBs
2,3,3',4,4'-PeCB

44-42049

510-2140

110-1210

24-1500

0.40-1303-12892,3',4,4',5-PeCB

140-1700

170

1530-5660

388-3990

70-4700

150-500

37-4539

2,3,3',4,4',5-HxCB

18-18020337-2140

68-1030

4.7-710

15-110Total PCBs

1900-18000

1800

820-41000

1600-6000

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This study

This study

This study

This study

270-14000

4600-480000

14000-60000

3020-245000

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Falandysz

Koistinen

Tarhanen

Koistinen

1991

et al . 1994

et al. 1995#

et al. 1989

et al . 1997

# Recalculated from the concentrations on fat weight basis. BC: British Columbia, BE: Bald Eagle, BM: breast muscle, L: liver126-230
387-775
124-184265-15100

4800-26700

11000-170000

48500

5900

Elliott

Anthony

Elliott

Tarhanen

Tarhanen

Koistinen

et al. 1996a

et al . 1993

et al. 1996b#

et al. 1989

et al. 1989

et al. 199798

NationLocation

99
adverse-effect concentration values were about 10 pgTEQ/g in avian eggs and tissues.
Koistinen et al. (1997) proposed a value of 7 pgTEQ/g in WSE egg as the lowest-observableadverse-effect concentration. All the TEQs calculated in the tissues of SSEs and WSEs in thisstudy exceeded the lowest-observable-adverse-effect concentration.
It should be noted that the TEQ values we report do not include the contributions of
dioxins and furans. Thus, it is likely that our TEQ values are underestimates. In Baltic WSE
muscle and eggs, PCB congeners accounted for 56 to 74 % of total TEQs (Koistinen et al.
1997).
Another indirect indication of CYP1A induction may be inferred from examination of3,3’,4,4’-TeCB/3,3’,4,4’,5-PeCB ratios, which varied greatly between eagles with coplanar
PCB exposure. In the two eagles with more than 500 pgTEQ/g (nos. 2 and 4), the ratios weremuch lower. The ratios for nos. 2 and 4 eagles were 0.43 and 0.45, respectively, while the ratio
for other eagles with lower TEQs was 1.21 ± 0.56 (mean ± SD). The declining ratios may
indicate that hepatic CYP1A is induced in the eagles exposed to the elevated coplanar PCBs,
and consequently more metabolizable 3,3’,4,4’-TeCB was preferentially degraded by the
enzyme. These indirect indications in some eagles may also imply the possibility of other arylhydrocarbon receptor mediated responses such as immunological and reproductive effects,
which have been reported to correlate with hepatic CYP1A induction (Safe 1990, FernandezSalguerro et al. 1995).
Pb, Cd and Hg levels and their toxicological implications
The concentrations of lead, cadmium and mercury in the liver, muscle and kidney ofSSEs and WSEs are shown in Table 2. Lead concentrations in all tissues of four SSEs (nos. 2,
3, 5 and 6) were less than 0.5 micro g/g dry weight. However, high lead concentrations (over50 micro g/g dry weight) were found in the liver and kidney of the other SSEs (nos. 1, 4 and 7)
and all WSEs (nos. 8, 9 and 10).
Lead concentrations in the tissues of birds that do not have any contact with sources oflead contamination (e.g. lead mining and lead shot) are generally very low. Hepatic leadconcentrations found in raptors which were not diagnosed as having died of lead poisoning
have been reported to be less than 2 micro g/g dry weight (Pain et al. 1995). Some authors
have suggested that concentrations of 8-10 micro g/g wet weight indicate acute exposure andsufficient residues to cause mortality (Pattee et al. 1981, Craig et al. 1990). In the present
study, 10 micro g/g Pb wet weight (approximately 35 micro g/g dry weight based on a watercontent of liver and kidney tissues of ca. 65%) was used to indicate acute exposure. Hepaticand renal lead concentrations of three SSEs and three WSEs exceeded this level. Comparisonof our data to the concentrations in lead-poisoned raptors previously reported (Table 4),suggested that eagles analyzed in this study were suffering from lead poisoning. Thisconclusion was also supported by presence of lead fragments in the intestine or gizzard andclinical signs of lead poisoning, such as hypertrophy of the gall bladder and green feces.

100

Table 4. Comparison of hepatic Hg and Pb concentrations (micro g/g on dry weight basis) in acute poisoned raptor species with those in Steller's Sea Eagles
and White-tailed Sea Eagles.
No. Hg concentration*
Steller's Sea Eagle
White-tailed Sea Eagle

63

Hg-poisoned species
White-tailed Sea Eagle
White-tailed Sea Eagle
White-tailed Sea Eagle

3

ReferenceNo.

Pb concentration*

Reference

2.8-16
2.0-3.7

This study
This study

Steller's sea eagle
White-tailed sea eagle

630.06-232
77-174This study
This study

16.1-94.9
169

Henriksson et al. (1966)
Koeman et al. (1972)

Pb-poisoned species
Bald Eagle
Bald Eagle

362

17.5-21480.5, 52.5

105, 38.5, 116

Falandysz (1984)
Falandysz (1986)
Falandysz et al. (1988)

Bald Eagle

4

59.5

Franson (1996)
Jacobson et al. (1977)
Redig et al. (1980)
Pattee et al. (1981)

California Condor
Andean Condor
KingVulture

3
1
2

21, 80.5, 123
133
221, 24.5

Wiemeyer et al. (1988)
Locke et al. (1969)
Decker et al. (1979)* Dry weight based on a water content of liver and kidney tissue of ca. 65%.

101
In autumn, the most important food resource for SSE and WSE is spawning salmon (Uetaet al. 1999). In winter, eagles feed in limited areas where active fisheries are, mainly upon fishthat have fallen from nets (WGWS 1996) and upon the carcasses of beached marine mammals(Nakagawa 1998). Since the mid 1990s, the distribution of wintering eagles has shifted into
mountain areas, and this has been linked to changes in the availability of winter prey. It isthought that due to a recent decline in fish abundance in areas where eagles traditionallycongregated and fed, wintering eagles have shifted their diet toward the abundant deercarcasses resulting from human hunting activity in mountain areas (WGWS 1996, Nakagawa
1998). In Hokkaido, deer hunting is used in an attempt to control the size of the deer
population. Whole and partial carcasses of deer shot by hunters are left in the field. Leadfragments embedded in the tissue of deer are ingested by scavenging raptors during and after
the hunting season.
In the present study, the hair of deer was found along with a lead fragment in theintestine of a SSE suffering from lead poisoning (no. 4). This suggests that lead from the deercarcasses is a main cause of death of eagles in which lead fragments were found. On the other
hand, the origin of lead in the SSE which exhibited high lead concentration in the tissues, but
had no deer hair in the digestive tract (no.1) was unclear.
In Japan, lead poisoning in large waterfowl such as swans has been known since 1980.
Honda et al. (1990) reported that lead poisoning occurred in 7 cases of Whooper Swan Cygnus
cygnus and Bewick’s Swan C. columbianus collected in Hokkaido and northeastern Japan
during 1984-1987. Lead poisoning in 120 individual Whooper Swans and White-fronted
Geese Anser albifrons migrating to Hokkaido was also reported in 1989 and 1990 (Ochiai et al.
1992, Murase et al. 1992). Ochiai et al. (1993) reported the occurrence of lead shot instomach contents of 56 ducks of 9 species collected from three areas of Hokkaido in 1991. The
percentages of ducks from these areas with lead were 19-27%. These results suggest that alarge number of waterfowl in Japan may be exposed to lead shot by ingestion, although thesample size is not large enough for statistical analysis. The occurrence and frequency oflead poisoning and secondary poisoning in other birds are unclear.
In Japan, the total amount of lead used for hunting game birds and deer amount to about
75 tons every year (Pain 1992). No regulation of lead bullet use has been introduced by theJapanese government (On Jan. 21, 2000, Environment Agency of Japan announced ban of leadbullet use in Hokkaido from the next hunting season), and it is feared that if lead bullets are not
restricted, lead poisoning could be a significant cause of eagle mortality in the future. During
1997 to 1999, a total of 55 dead or debilitated SSEs and WSEs in Hokkaido were examined forlead poisoning. Fourty six eagles were found to have died from lead poisoning (Kurosawa
2000). While the loss of habitat, and persecution of eagles have been recognized as primarysources of mortality, lead poisoning in the wintering areas could be another important cause of
mortality and may contribute to population decrease.
Mercury concentrations ranged from 5.5-15 in kidney and 2.8-16 micro g/g dry weight in102
liver (Table 2). Ranges of cadmium concentrations in the kidney and liver of SSEs were 1.07.9 and 0.15-1.3 micro g/g dry weight, respectively. Only trace levels of these elements weredetected in muscle. Cadmium and mercury concentrations in WSEs were similar to those in
SSEs.
Published values of mercury concentrations in raptors found dead and considered tohave been exposed directly to toxic levels of mercury are summarized in Table 4. Although it
would be difficult to suggest critical residue levels of mercury that are applicable to all raptors,
concentrations in the liver and kidney in excess of 30 mercury mg/kg wet weight(approximately 105 mg/kg dry weight) would appear to be lethal to a range of species of
raptors (Thompson 1996). Mercury concentrations in the liver and kidney of SSEs and WSEs
in the present study were less than 16 micro g/g dry weight, and unlikely to be a direct cause ofdeath or debilitation, even though slight differences in sensitivity to mercury may exist
between species.
Garcia-Fernandez et al. (1995) reported that concentrations of cadmium in the kidney ofdiurnal raptors ranged from 0.35-6.14 micro g/g dry weight (based on a water content ofliver and kidney tissues of ca. 65%). The range of cadmium concentration in the kidney ofSSEs and WSEs the present study was 1.0-7.9 and 2.3-6.5 micro g/g dry weight, respectively.
This range of cadmium concentrations was similar to those in other healthy raptors.
The distribution patterns of mercury and cadmium concentrations in tissues agreed withthose found in many other bird species (Osborn et al. 1979, Honda et al. 1986, Kim et al.
1996). Cadmium concentrations in birds are typically highest in the kidney, lower in the liver,and at trace levels in muscle. For healthy, adult birds in wild populations, the concentration of
cadmium in the liver is usually between one half and one tenth of the concentration in thekidney of the same bird (Honda et al. 1990, Osborn et al. 1979, Kim et al. 1996).
Scheuhammer (1987) suggested that comparing liver and kidney concentrations of cadmium
may indicate acute exposure to cadmium. Under acute exposure, birds in such a situation
would be expected to have hepatic cadmium concentrations as high as or higher than those in
the kidney. In the present study, the ratios of cadmium concentration of liver to kidney in botheagles ranged from 0.08 to 0.25, implying that the cadmium exposures for these birds were nottoxic.

CONCLUSIONS
CHC analysis showed coplanar PCBs and p,p’-DDE to have accumulated in the tissues ofSSEs and WSEs wintering in Japan. The CHC residue levels in some eagles appeared to begreater than the no- or lowest-observable-adverse-effect concentrations that are responsible for
CYP1A induction and egg shell thinning. From a long term view, the current concentrations ofthese CHCs may cause chronic adverse effects in the Far East populations of SSEs and WSEs.
However, acute poisoning through the ingestion of lead fragments is likely to have a negative
effect on the eagle populations in the short term. Further epidemiological studies of the

103
contaminant exposure and toxicological effects including sampling of eagle eggs and juveniles
in their breeding areas would be necessary to evaluate more accurately the threat topopulations.

ACKNOWLEDGMENTS
The authors would like to thank Drs. M. Ueta (Wild Bird Society of Japan), H. Takanaga (National
Institute for Environmental Studies, Japan), M. McGrady (Boise State University, USA) and C.J. Henny(National Biological Survey, USA) for their useful comments on this manuscript. This study was
supported by Grants-in Aid for the Scientific Research from the Ministry of Education, Science andCulture of Japan to Hisato Iwata (Grants Nos. 09306021 and 09876084).

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