Environmental Toxicology and Chemistry, Vol. 21, No. 2, pp. 413–423, 2002
q 2002 SETAC
Printed in the USA
0730-7268/02 $9.00 1 .00
TOXAPHENE AND OTHER PERSISTENT ORGANOCHLORINE PESTICIDES IN THREE
SPECIES OF ALBATROSSES FROM THE NORTH AND SOUTH PACIFIC OCEAN
DEREK C.G. MUIR,*†,‡ PAUL D. JONES,§ HEIDI KARLSSON,† KRYSTINA KOCZANSKY,‡ GARY A. STERN,‡
KURUNTHACHALAM KANNAN,§ JAMES P. LUDWIG,\ HAMISH REID,# CHRIS J.R. ROBERTSON,††
and JOHN P. GIESY§
†National Water Research Institute, Environment Canada, Burlington Ontario L7R 4A6, Canada
‡Freshwater Institute, Fisheries and Oceans Canada, Winnipeg, Manitoba R3T 2N6, Canada
§National Food Safety and Toxicology Center, Department of Zoology and Institute for Environmental Toxicology, Michigan State University,
East Lansing, Michigan 48824, USA
\The SERE Group, 1670 Garnet Road, Victoria, British Columbia V8P 3C8, Canada
#Institute for Environmental Science and Research, Wellington, New Zealand
††Department of Conservation, Wellington, New Zealand
( Received 1 May 2001; Accepted 6 August 2001)
Abstract—Toxaphene and other persistent organochlorine (OC) pesticides (chlordane-related compounds [SCHL], DDT-related
compounds [SDDT], hexachlorocyclohexanes [SHCH], tris(p-chloro-phenyl)methane, hexachlorobenzene, octachlorostyrene, dieldrin) were determined in fat of Laysan albatross (Diomedea immutabilis) and in fat and eggs of blackfooted albatross (Diomedea
nigripes) from the central north Pacific Ocean. The HCH isomers and chlordane- and DDT-related compounds were also determined
in eggs of northern royal albatross (Diomedea sanfordi) collected in New Zealand. Toxaphene was detected in fat samples at mean
6 standard deviation (SD) levels ranging from 243 6 61 ng/g wet weight in Laysan albatross to 1,020 6 237 ng/g wet weight in
blackfooted albatross. These levels were higher than SCHL and SHCH but lower than SDDT. In eggs of blackfooted albatross,
toxaphene was the major OC pesticide, averaging 513 ng/g wet weight in two pooled samples compared with 293 ng/g wet weight
for SDDT. Two toxaphene congeners, the octachloroborane B8-1413 (Parlar 26) and the nonachlorobornane B9-1679 (P50), comprised about 38% of total toxaphene in both albatross species. All OC compounds were present at significantly higher levels in
blackfooted than Laysan albatross fat with the exception of SHCH, dieldrin, and octachlorostyrene. Mean levels of SDDT and
SHCH in northern royal albatross eggs from New Zealand were 4 and 60 times lower, respectively, than in blackfooted albatross
eggs. The pattern of OC pesticide accumulation was consistent with differences in distribution of the three species in the Pacific
Ocean, with highest levels in blackfooted albatross, which feed off the west coast of North America, intermediate levels in Laysan
albatross, which frequent the western Pacific, and lowest levels in northern royal albatross, which are confined to the southern
oceans surrounding the Antarctic.
Keywords—Toxaphene
Chlordane
Pesticides
Albatross
Pacific Ocean
lutants and the forthcoming United Nations Environment Program global ban list [4,8].
One of the difficulties in characterizing concentrations and
sources of toxaphene and chlordane is that they are both extensively biotransformed by mammals and birds [9–13]. The
metabolism of toxaphene has been studied in chickens [14]
but its metabolism by other avian species has not been investigated [10]. Information on the concentrations of toxaphene
and chlordane in avian species generally, and seabirds in particular, is limited. Apart from a report on the characterization
of toxaphene congeners in penguins [15], the only previously
published results are for guillemots and osprey from the Baltic
Sea and the Barents Sea [16,17]. There have been numerous
measurements of the major components in technical chlordane
in seabirds, e.g., cis-trans-chlordane, cis-trans-nonachlor, and
the toxic metabolite oxychlordane [18,19], but measurements
of some of the minor, but highly bioaccumulative, components
and metabolites are more limited [20,21].
The populations of albatross species in the north Pacific are
presently on the increase following the cessation of hunting
in the early 1900s [22]. Nonbreeding Laysan albatross (Diomedea immutabilis) mainly frequent the western Pacific and
Asian coasts, while blackfooted albatross (Diomedea nigripes)
are more common along the northeastern Pacific and North
INTRODUCTION
The global distribution of chlorinated aromatic compounds
such as polychlorinated biphenyls (PCBs) and organochlorine
(OC) pesticides such as hexachlorocyclohexanes, hexachlorobenzene, and DDT-related compounds in the marine environment has been well documented [1–3]. Less is known about
the extent of global contamination by other OC pesticides such
as toxaphene and chlordane. Toxaphene and chlordane were
widely used in the 1970s following bans in the United States,
Canada, and Europe on the extensive use of DDT. In the United
States, regulatory bans on toxaphene and chlordane use in
agriculture were imposed in 1982 and 1983, respectively, due
to concerns about carcinogenicity and environmental persistence and bioaccumulation [4,5]. Use of toxaphene continued
especially in Mexico, Central America, and the former Soviet
Union until the early 1990s [6,7]. Chlordane use continued in
many countries, including the United States, for nonagricultural purposes (e.g., termite control) until the mid-1990s (http:
//irptc.unep.ch/pops/pops-gs/popsgs.html) [4]. Both compounds have been placed on the United Nations Economic
Commission for Europe list of banned persistent organic pol* To whom correspondence may be addressed
(derek.muir@cciw.ca).
413
414
Environ. Toxicol. Chem. 21, 2002
American coasts. The northern royal albatross (Diomedea sanfordi) is believed to circumnavigate the southern polar oceans
on a two-year cycle and is found south of about 458 latitude
[23]. Thus, albatrosses are useful indicators of different sources of marine pollution in the Pacific Ocean.
Relatively high concentrations of chlorinated aromatic
compounds, including PCBs and their hydroxylated and methyl sulfone metabolites [24], polychlorinated dibenzo-p-dioxins, and dibenzofurans (PCDD/Fs) and non-ortho-substituted
PCBs were found in fat samples from the north Pacific populations [25], while lower concentrations were measured in
the south Pacific species [23]. Ortho-substituted PCBs and
DDT-related compounds were also reported in plasma samples
from the north Pacific populations [26]. Here we report concentrations of OC pesticides related compounds, with special
emphasis on specific toxaphene and chlordane components, in
fat samples from Laysan albatross and fat and egg samples
from blackfooted albatross from the Midway Atoll Islands.
Concentrations of hexachlorocyclohexane (HCH)-, chlordane
(CHL)-, and DDT-related compounds in these north Pacific
populations are compared with levels in eggs of the northern
royal albatross from the south Pacific Ocean.
MATERIALS AND METHODS
Sample collection and handling
Laysan and blackfooted albatross adults were collected
from Sand and Eastern Island, Midway Atoll (288119N,
1778229W) in the central north Pacific during 1994 (February,
March, November) and 1995 (February, November). Of the
26 birds, 15 were collected under the authority of a scientific
permit and 11 were injured birds that had been dead only a
few minutes. The nutritional status of all birds at death was
normal; none were starving. Birds were examined externally,
necropsied, and fat and other tissue samples were frozen in
clean, solvent-rinsed glass jars for subsequent analysis. Samples were frozen at 2208C until analysis. Two egg pools (n
5 10) from blackfooted albatross were prepared from eggs
collected in November 1994 from Sand Island by opening the
eggs into clean jars. Pools were homogenized before subsampling and analysis. Eggs of northern royal albatross from the
south Pacific Ocean were collected in the southern summers
of 1995 through 1998 by Department of Conservation field
staff from the Taiaroa Head Colony in New Zealand. Only
abandoned or dead eggs were collected.
Analysis of toxaphene and other organochlorine pesticides
Fat and egg samples of Laysan and blackfooted albatross
were extracted and analyzed by procedures identical to those
used to determine toxaphene and other OC pesticides in marine
mammal fats [27]. Samples were partially thawed, and 2 g
were combined with anhydrous Na2SO4 (heated at 6008C for
16 h prior to use). The mixture was then extracted two times
with hexane in a small (50-ml) ball mill, with centrifuging and
decanting of the hexane between extractions. Surrogate recovery standards of CB 30 and octachloronaphthalene were
added prior to extraction. Extractable lipids were determined
gravimetrically on a 10% portion of the extract. A portion of
the extract equivalent to about 100 mg lipid was chromatographed on Florisil (8 g 1.2% deactivated with H2O) to separate
PCBs, chlorobenzenes, 4,49-DDE, and mirex (hexane elution)
from most toxaphene components, chlordane-related compounds, and 4,49-DDT (second elution with dichloromethane:
D.C.G. Muir et al.
hexane 15:85). A third elution contained heptachlor epoxide,
tris (p -chlorophenyl)methane (TCPMe), tris ( p -chloro-phenyl)methanol (TCPMeOH), and dieldrin. Florisil eluates were
analyzed by high-resolution gas chromatography (GC) with
electron-capture detection using a 60 m 3 0.25-mm DB-5
column (J&W Scientific, Folsom, CA, USA) with H2 carrier
gas.
The analytical procedures used for the analysis of northern
royal albatross egg samples were the same as those described
previously [25]. In brief, eggs were fortified with isotopically
labeled PCB congeners and OC pesticides and extracted four
times by blending with acetone:hexane (2:1). The extract was
dried with anhydrous Na2SO4, evaporated to near dryness, and
taken up in hexane. Lipid removal was performed by washing
the hexane with concentrated sulfuric acid. The extract was
chromatographed on Florisil to separate PCBs from most OC
pesticides. The OCs were determined by GC using high-resolution mass spectrometry (MS) at mass resolution of 8,000
using authentic standards for calibration.
Chlordane-related compounds were quantified with individual standards except for the Cl9 component MC6, which
was quantified using the response factor of trans-nonachlor
(t-nonachlor). Minor Cl6–8-containing components [13,28], C,
MC1, U82, U83, and MC5, were quantified using trans-chlordane. Total chlordane was the sum of all chlordane-related
compounds including heptachlor epoxide and oxychlordane.
Toxaphene was quantified by GC electron-capture detector
(ECD) using a single response factor based on 27 peaks in a
technical toxaphene standard. Two polychlorinated bornane
congeners (CHBs), P26 (or B8-1413; 2-exo,3-endo,5-exo,6endo ,8,8,10,10-octachlorobornane) and P50 (B9-1679; 2exo ,3- endo ,5- exo ,6- endo ,8,8,9,10,10-nonachlorobornane),
were quantified using an analytical standard obtained from
Promochem (Wesel, Germany).
Both TCPMe and TCPMeOH were quantified with authentic standards generously provided by R.J. Norstrom (Canadian
Wildlife Service, Hull, PQ, Canada). Extracts were also analyzed for hexachlorocyclohexanes (HCH), hexachlorobenzene
(HCB), octachlorostyrene, and six DDT-related compounds using authentic standards.
The CHBs were confirmed and quantified in two albatross
fat samples by high-resolution electron capture negative ion
mass spectrometry (GC-ECNIMS) using a mass resolution of
12,000. The GC-ECNIMS conditions have been described previously [29].
Quality assurance included participation in the International
Council for the Exploration of the Sea, Copenhagen, Denmark,
interlaboratory studies on PCB congeners in seal blubber [30]
and in an interlaboratory comparison of toxaphene in the National Institute of Standards and Technology (Gaithersburg,
MD, USA) cod liver [31]. Analyses of northern royal albatross
were conducted by a laboratory accredited by the New Zealand
Testing Laboratory Accreditation Council. The National Institute of Standards and Technology cod liver oil (SRM1588)
was analyzed every 10 samples. Recoveries of internal standards, PCB 30 and octachloronaphthalene, ranged from 88 to
99%. Detection limits (based on a minimum peak integration
area 1 3 SD of the lowest calibration standard) ranged from
about 0.02 to 0.1 ng/g for CHB congeners and other OC pesticides based on a typical sample weight of 2 g wet weight.
Statistical analyses were conducted using the SYSTAT statistical package (SPSS, Chicago, IL, USA). Preliminary statistical analyses showed no significant differences in mean
Toxaphene in albatrosses from the Pacific Ocean
concentrations in fat of any OCs between males and females
for the Laysan or blackfooted albatross (Student’s t test, p .
0.05) or in fat samples collected in November/December versus those collected in February/March. Therefore, comparisons
were limited to differences between species and levels of various OC compounds. Coefficients of skewness and kurtosis
for all major OCs detected in fat of each species were generally
,2, indicating no significant deviations from a normal distribution. Comparisons between the two species were made with
wet weight concentrations because lipid content of fat samples
was almost identical in both species, averaging 91 6 3%.
Statistical comparisons were made using the Student’s t test
assuming different variances.
RESULTS
Confirmation of toxaphene
Toxaphene was detected in both Laysan and blackfooted
albatross samples at higher concentrations than several other
OC pesticides (hexachlorocyclohexane-related compounds
[SHCH] and chlordane-related compounds [SCHL]) but less
than concentrations of DDT-related compounds (SDDT) (Table 1). Toxaphene was not determined in the northern royal
albatross samples. The profile of toxaphene congeners in albatross fat did not resemble technical toxaphene (Fig. 1). It
was dominated by two components, the octachloroborane B81413 and the nonachlorobornane B9-1679, which comprised
about 38% of total toxaphene in both blackfooted albatross
and Laysan albatross when quantified as individual congeners.
In Laysan albatross, two other octachlorobornane peaks (identified as B8-1412, 2-endo,3-exo,5-endo,6-exo,8,8 9,10-octachlorobornane, and B8-1414/1945 [P40/41, 2-endo,3-exo,5endo,6-exo,8c,9b,10a,10c (or 10b)-octachlorobornane and 2exo,3-endo,5-exo,8c,9b,9c,10a,10b-octachlorobornane] based
on retention times of authentic standards) were also present at
high concentrations although not quantified (Fig. 2). The B81412 and B8-1414/1945 were also present in blackfooted albatross but at a lesser proportion than B9-1679 (Figs. 1 and
2). There was good agreement (620%) between total toxaphene quantified by GC-ECD and GC-ECNIMS. The GC-ECD
was found to overestimate concentrations of B8-1413 and B91679 relative to results reported by GC-ECNIMS by 44 and
15%, respectively. In the case of B8-1413, this may have been
due to coelution of other OCs, which has been observed by
other authors [32]. Nevertheless, because of the predominance
of the two congeners in the GC-ECD chromatogram, it was
useful for quantitation in individual samples. Toxaphene concentrations in the National Institute of Standards and Technology 1588 cod liver oil averaged 4020 ng/g lipid weight,
within the range reported by others for this standard reference
material [33].
Comparison of OC levels between species
Concentrations of total toxaphene and congeners B8-1413
and B9-1679 were significantly greater in blackfooted than in
Laysan albatross (t test, p , 0.01) (Table 1). The average total
toxaphene concentration was 1,022 ng/g (wet wt) in blackfooted albatross and 243 ng/g (wet wt) in Laysan albatross.
Concentrations of toxaphene in both species were significantly
correlated (p , 0.05) with concentrations of other recalcitrant
OC pesticides (SCHL, SDDT, HCB, mirex) but not with
SHCH or dieldrin (Table 2). Toxaphene was also present in
eggs of blackfooted albatross, averaging 513 ng/g (wet wt) in
Environ. Toxicol. Chem. 21, 2002
415
two pools (Table 1). Toxaphene was the most prominent OC
pesticide in eggs, with levels 1.75 times greater than SDDT
and 13 times greater than SCHL.
Chlordane-related compounds were detected in all fat and
egg samples, with higher levels in blackfooted than in Laysan
albatross and very low ng/g levels in northern royal albatross
(Table 1). Blackfooted and Laysan albatross had similar proportions of the major chlordane-related components (Fig. 3).
Oxychlordane was the predominant compound, followed by
trans-nonachlor, heptachlor epoxide, and the nonachlor isomer
MC6 [13]. Octachlordanes U82 and U83, previously identified
in technical chlordane by Dearth and Hites [13] and Karlsson
et al. [28] and in seal and polar bear fat by Muir et al. [34],
were found in all samples. Minor chlordane components C,
MC1, MC6, and U1 (photoheptachlor), which have been reported in seals and polar bears [34,35], were not detected.
Average SCHL concentrations in Laysan albatross fat (319
ng/g) were significantly greater (p , 0.05) than those of toxaphene, while in blackfooted albatross, the reverse was observed (Table 1). The SCHL levels were fourfold less than
SDDT levels in Laysan albatross fat and sixfold less in blackfooted albatross.
The DDT-related compounds were detected in all fat and
egg samples with 3.5-fold greater concentrations of SDDT in
blackfooted than in Laysan albatross (Table 1). Fourfold lower
levels of SDDT were found in northern royal compared with
blackfooted albatross eggs (Table 1). In fat samples, SDDT
concentrations exceeded those of toxaphene by about fivefold
in both species. The 4,49-DDE was the major DDT component,
accounting for 78% of SDDT in blackfooted and 84% in Laysan albatross fat. Eggs also had high proportions of 4,49-DDE,
ranging from 82% in blackfooted albatross to 87% in northern
royal albatross. Both TCPMe and TCPMeOH, which are impurities in technical DDT and diclofol [36], were present at
low ng/g (wet wt) levels in all fat and egg samples in the north
Pacific species. Similar to toxaphene, but unlike 4,49-DDE and
chlordane-related compounds, levels of TCPMe and
TCPMeOH were higher in eggs than in fat (on a lipid wt basis).
Both TCPMe and TCPMeOH were significantly correlated (p
, 0.05) with 4,4-DDE in blackfooted albatross and with 4,49DDT, oxychlordane, cis-chlordane, and chlorobornanes B81413 and B8-1679 in Laysan albatross (Table 2).
The predominant HCH isomer in albatross fat and eggs was
b-HCH, the most recalcitrant component [37]. Mean concentrations of b-HCH were 10- to 12-fold greater than the sum
of a-HCH and g-HCH in samples from all three species. Unlike
the more recalcitrant compounds (DDT, CHL, toxaphene),
mean concentrations of SHCH did not differ significantly between blackfooted and Laysan albatross (p . 0.05). However,
blackfooted albatross eggs had 60 times higher levels of SHCH
than northern royal albatross (Table 1).
Mirex was a major individual OC in albatross fat and eggs,
exceeded in concentration only by oxychlordane, 4,49-DDT,
and 4,49-DDE among the 30 OC pesticides and metabolites
that were determined. Mirex levels in fat were significantly
higher in blackfooted than in Laysan albatross (p , 0.05). In
Laysan albatross, mirex was significantly correlated with recalcitrant OCs B8-1413, B9-1679, 4,49-DDE, 4,49-DDT, and
oxychlordane, but correlation coefficients were relatively small
(Table 2).
Mean HCB concentrations were twofold higher in blackfooted than in Laysan albatross. The HCB levels in northern
royal albatross eggs were 2.5-fold lower than in blackfooted
91.0
38.7
68.1
3.8
5.7
60.5
0.7
9.0
3.8
36.1
142
7.2
9.2
75.3
6.7
24.0
2.1
85.8
5.4
1,108
6.4
25.8
31.6
137
29.5
26.1
38.4
37.6
243
1,314
67.0
319
% Lipid
Dieldrin
Hexachlorobenzene
Octachlorostyrene
a-HCH
b-HCH
g-HCH
U82b
U83b
MC5b
Oxychlordane
trans-Chlordane
cis-Chlordane
trans-Nonachlor
cis-Nonachlor
cis-Heptachlor epoxide
Heptachlor
Mirex
o,p-DDE
p,p-DDE
o,p-DDD
p,p-DDD
o,p-DDT
p,p-DDT
TCPMec
TCPMeOHc
P26 (B8-1413)d
P50 (B9-1679)d
Toxaphene
SDDT
SHCH
SCHL
3.9
6.2
13.3
1.0
2.7
10.5
0.3
3.7
0.6
8.3
32.5
4.8
2.6
18.4
2.4
6.1
0.6
32.1
1.6
192
1.6
7.5
5.8
53.2
6.2
5.5
10.5
8.8
61.2
242
11.1
70
SD
84.2
28.1
39.9
2.1
2.7
40.1
0.5
3.4
2.7
21.3
67.8
3.6
5.8
47.7
3.5
12.5
1.0
44.1
2.9
679
4.1
18.1
20.1
66.6
19.9
15.5
20.4
20.9
143
813
43.5
180
96.6
49.3
95.2
6.1
12.0
81.7
1.5
15.2
5.1
57.2
223
22.1
15.2
122
12.4
37.5
3.1
209
8.6
1,527
10.2
40.3
42.2
295
39.0
37.8
55.8
52.9
348
1,922
86.3
507
Minimum Maximum
91.2
59.5
143
4.8
6.6
88.4
0.9
5.4
4.3
54.3
352
23.9
21.6
251
24.4
33.3
2.2
243
16.0
3,772
18.2
117
99.7
754
49.7
37.5
191
205
1,022
4,777
95.9
777
Mean
3.3
20.7
31.5
0.9
2.3
41.2
0.1
0.8
1.1
8.7
84.4
8.9
5.5
60.4
4.5
11.6
0.6
59.6
6.7
876
7.0
17.8
19.3
185.1
15.6
7.6
66.4
49.1
237
1,012
41.3
162
SD
85.0
30.1
86.0
3.7
3.9
40.4
0.8
4.4
2.7
39.4
194
16.8
16.6
178
20.2
15.3
1.5
156
9.4
2,217
11.4
90.3
70.3
514
25.4
28.2
64.0
111
551
2,914
46.6
495
94.4
85.0
177
6.1
10.7
152
0.1
6.7
5.8
63.6
436
41.4
30.5
343
30.1
48.0
3.1
313
27.2
4,610
29.8
144
120
944
63.1
46.2
258
255
1,229
5,819
157
970
Minimum Maximum
Blackfooted albatross, fat
(n 5 6)
13.0
4.2
12.2
0.3
0.4
5.5
0.1
0.1
0.4
0.3
15.5
0.9
2.0
14.7
1.7
3.4
0.0
24.0
1.0
233
2.0
2.9
6.4
47.8
42.3
38.9
61.7
99.6
513
293
5.9
39.4
Mean
11.7
3.2
8.0
0.5
0.5
4.6
0.1
0.1
0.3
0.3
7.9
0.5
1.0
7.0
0.9
2.3
0.0
12.7
1.5
326
2.6
4.4
9.7
82.6
35.5
36.5
64.0
140
611
427
5.2
20.3
14.3
5.3
16.4
0.1
0.2
6.3
0.1
0.1
0.6
0.3
23.1
1.4
3.0
22.4
2.6
4.6
0.0
35.2
0.5
139
1.4
1.4
3.0
13.0
49.2
41.2
59.5
58.9
415
158
6.6
58.6
Minimum Maximum
Blackfooted albatross, egg pool
(n 5 2)
7.06
—
5.01
—
0.008
0.081
0.018
—
—
—
—
0.06
0.27
—
—
1.17
—
—
—
57.9
—
2.35
—
0.04
6.18
—
—
—
—
66.4
0.10
—
Mean
1.53
—
1.96
—
0.004
0.027
0.009
—
—
—
—
0.03
0.13
—
—
0.51
—
—
—
40.5
—
2.26
—
0.02
5.35
—
—
—
—
46.6
0.03
—
SD
4.60
—
3.50
—
0.005
0.040
0.011
—
—
—
—
0.03
0.16
—
—
0.80
—
—
—
17.0
—
0.11
—
0.01
0.03
—
—
—
—
20.3
0.06
—
9.00
—
9.10
—
0.015
0.12
0.036
—
—
—
—
0.11
0.53
—
—
2.10
—
—
—
140
—
5.40
—
0.09
17.0
—
—
—
—
161
0.14
—
Minimum Maximum
Northern royal albatross,a eggs
(n 5 7)
b
Dashes indicate compound not determined.
U82 and U83 are octachlordanes identified in technical chlordane by Dearth and Hites [13] and by Karlsson et al. [28]. They were also identified in ringed seal fat by Muir et al. [34] as U6 and
U5, respectively. MC5 is also an octachlordane isomer [13].
c tris(p-Chlorophenyl)methane and tris(p-Chlorophenyl)methanol.
d P26 52-exo, 3-endo, 5-exo, 6-endo,8,8,10,10-octachlorobornane; P50 5 2-exo, 3-endo, 5-exo, 6-endo,8,8,9,10,10-nonachlorobornane; DDE 5 dichlorodiphenyldichloroethylene; DDD 5 dichlorodiphenyldichloroethane; TCPMe 5 tris(p-chlorophenyl)methane.
a
Mean
Statistic
Laysan albatross, fat
(n 5 20)
Table 1. Mean concentrations (ng/g wet wt) of organochlorine pesticides and related compounds in albatross fat and egg pools from the Midway Islands (1994–1995); SD 5 standard deviation
416
Environ. Toxicol. Chem. 21, 2002
D.C.G. Muir et al.
Toxaphene in albatrosses from the Pacific Ocean
Fig. 1. Chromatograms (gas chromatography-electron capture negative ion mass spectrometry [GC-ECNIMS]) of blackfooted and Laysan
albatross fat extracts and technical toxaphene standard. The chromatograms are the sum of selected Cl6, Cl7, Cl8, and Cl9 ions.
albatross (Table 1). Concentrations of HCB correlated with
most chlordane-, DDT-, and toxaphene-related compounds but
not with SHCH or octachlorostyrene (data not shown). Octachlorostyrene was detected in all egg and fat samples from
the north Pacific albatrosses but was a relatively minor contaminant (Table 1). Unlike HCB, mean octachlorostyrene levels were not significantly different between Laysan and blackfooted albatross (p . 0.05). In Laysan albatross, octachlorostyrene levels were significantly correlated with cis- and transnonachlor, dieldrin, 4,4-DDE, and b-HCH but not with
toxaphene, mirex, a-HCH, or g-HCH.
Dieldrin was a relatively minor OC pesticide in fat, ranging
from 38.7 ng/g (wet wt) in Laysan albatross to 49 ng/g in
blackfooted albatross (Table 1). Endrin, a related cyclodiene
pesticide, was not detected (,0.02 ng/g wet wt) in fat or eggs.
Similar to SHCH, dieldrin concentrations did not differ significantly between the two species (p . 0.05). However, concentrations of dieldrin were strongly correlated with b-HCH,
chlordane-, and DDT-related compounds but not with toxaphene (Table 2).
DISCUSSION
Toxaphene was found to be a major contaminant in blackfooted albatross eggs relative to most other OC pesticides.
Fig. 2. Selected ion chromatograms (gas chromatography-electron
capture negative ion mass spectrometry [GC-ECNIMS]) of hexa-,
hepta-, octa-, and nonachlorobornanes in Laysan albatross fat.
Environ. Toxicol. Chem. 21, 2002
417
Only SPCBs were present at greater concentrations than toxaphene or SDDT in blackfooted albatross eggs and in Laysan
albatross fat [25; D.C.G. Muir, unpublished data] (Table 3).
The recalcitrant nonachlorobornane (B9-1679) was present at
relatively high concentrations in both fat and egg samples and
was exceeded only by concentrations of 4,49-DDE in terms of
overall predominance of individual OC contaminants. All of
the five prominent chlorobornane congeners had chlorine substitution on the six-membered bornane ring, with the 2-exo,3endo,5-exo,6-endo pattern appearing to give rise to highly
recalcitrant structures. It has been shown that chlorobornanes
with this substitution pattern have higher heats of formation
than those with geminal dichloro substitution at the two or six
positions or with unsubstituted ring carbons [38]. Buser and
Müller [15] found a similar pattern of chlorobornanes in penguin (Pygoscelis adelis) fat to that observed in albatross in
the current study. They found two prominent, unidentified heptachlorobornanes as well as P26 and three other prominent
octachlorobornanes. In agreement with our observations, B91679 was the only prominent nonachlorobornane. Our results
for albatross are also consistent with the observation that B81413 and B9-1679 were not metabolized by Laysan albatross
liver microsomes [11]. Only P32, with geminal 2,2-,5-substitution on the six-member ring and single chlorines at C8 and
C9 was metabolized by albatross.
Toxaphene has rarely been reported in avian species (Table
3). This may be related to the major difference in the pattern
of chlorobornanes compared with technical toxaphene (Figs.
1 and 2), which creates analytical uncertainties. Several chlorobornanes have been determined in eggs of skuas (Catharacta
sp.) and penguins from the Antarctic [39]. These authors found
that B9-1679 was the most abundant chlorobornane in skua
eggs, followed by B8-1413, B9-1025, and B8-1412 (1–20 ng/
g wet wt). In penguin (Pygoscelis sp.,) eggs, B8-1413 was
present at greater concentrations than B9-1679, but both congeners were present at lesser concentrations (0.02–0.8 ng/g
wet wt) than in blackfooted albatross eggs [40].
Other studies have measured only total toxaphene in avian
samples. Jansson et al. [17] reported toxaphene concentrations
of 2,600 ng/g (lipid wt) in osprey (Pandion haliaetus) from
Sweden. These piscivorous birds are migratory, wintering in
west central Africa. Toxaphene concentrations in guillemots
collected in the 1970s from the Baltic Sea averaged 6,500 ng/
g (lipid wt) [41]. A pooled guillemot muscle sample from the
Barents Sea (Spitzbergen) collected in the early 1980s had a
toxaphene concentration of 4,100 ng/g lipid weight, indicating
the wide dispersion of toxaphene in northern Europe (Table
3). In contrast, nondetectable concentrations of toxaphene have
been reported in double-crested cormorant (Phalacrocorax auritus) eggs from Green Bay, Wisconsin, USA [42]. Nondetectable toxaphene was also reported in eggs of great egret
(Ardea alba) and black-crowned night heron (Nycticorax nycticorax) from the Rio Grande valley, while green heron (Butorides virescens) eggs had levels ranging from ,10 to 7,900
ng/g (wet wt) [43].
While there are no other reports, to our knowledge, of toxaphene concentrations in seabirds from the north Pacific, a
comparison of OC pesticides in beluga whales from North
American stocks found the lowest concentrations of toxaphene
in the isolated Cook Inlet (AK, USA) population of the northeast Pacific and the greatest concentrations in the eastern Canadian Arctic [44]. Concentrations of toxaphene in arctic
ringed seals, a widely distributed circumpolar species, also
0.324
0.378
0.564**
0.648**
0.426
0.734**
0.827**
0.256
0.875**
0.476*
0.382
0.436
Layson albatross (n 5 20)c
Dieldrin
0.262
TCPMe
0.433
TCPMeOH
0.589**
bHCH
0.546*
Oxychlordane
0.665**
0.447*
trans-CHL
0.512*
cis-CHL
0.441
trans-Nonachlor
0.479*
Mirex
0.447*
4,49-DDE
0.662**
4,49-DDT
0.928**
P26
0.828**
P50
0.869**
0.33
0.484*
0.256
0.498*
0.321
20.056
0.346
0.457*
0.451*
0.667**
0.941*
20.329
0.658
0.263
20.063
20.262
0.143
0.804
20.051
0.400
0.438
TCPMe
0.427
0.543*
0.229
0.407
0.309
0.214
0.402
0.477*
0.618**
0.765**
20.288
0.71
0.097
20.142
20.202
0.268
0.825*
0.053
0.459
0.489
TCPMeOH
0.539*
0.096
0.534*
0.542*
0.305
0.638**
0.348
0.531*
0.477*
0.401
0.522
0.776
0.957*
0.476
0.259
0.604
0.690
0.667
bHCH
0.572*
0.762**
0.675**
0.482*
0.84**
0.706**
0.630**
0.717**
0.612
0.545
0.498
0.747
0.97*
0.644
0.939*
0.949*
0.569*
0.405
0.037
0.394
0.229
0.506*
0.468*
0.916*
0.626
0.453
0.553
0.51
0.68
0.677
Oxychlordane trans-CHL
0.756**
0.253
0.818**
0.727**
0.539*
0.517*
0.865*
0.572
0.410
0.683
0.721
0.702
cis-CHL
0.231
0.879**
0.697**
0.449*
0.447*
0.571
0.34
0.685
0.756
0.727
trans-Nonachlor
0.472*
0.451*
0.482*
0.384
0.574
0.973*
0.75
0.74
Mirex
0.688**
0.479*
0.491*
0.441
0.865*
0.885*
4,49-DDE
0.546*
0.598**
0.716
0.698
4,49-DDT
b
a
TCPMe 5 tris(p-chlorophenyl)methane; TcPMeOH 5 tris(p-chlorophenyl)methanol; BHCH 5 hexachlorocyclohexanes; CHL 5 chlordane-related compounds; DDE 5 dichlorodiphenyldichloroethylene.
Pearson correlation coefficients (r) (df 5 4), where values of r . 0.81 are significant at p , 0.05 (*).
c Values of r . 0445 (df 5 8) are significant at p , 0.05 (*) and r . 0.56 at p , 0.01 (**).
0.054
0.056
0.874*
0.689
0.797
0.911*
0.94*
0.561
0.586
0.630
0.879*
0.863*
Dieldrin
Blackfooted albatross (n 5 6)b
Dieldrin
0.802*
TCPMe
0.493
TCPMeOH
0.562
0.612
bHCH
0.963*
Oxychlordane
0.600
trans-CHL
0.614
cis-CHL
0.661
trans-Nonachlor
0.737
Mirex
0.912*
4,49-DDE
0.672
4,49-DDT
0.988*
P26
0.993*
P50
Toxaphene
Table 2. Correlation coefficients for major individual organochlorine (OC) pesticide components in fat samples from two species of albatrossa
418
Environ. Toxicol. Chem. 21, 2002
D.C.G. Muir et al.
Toxaphene in albatrosses from the Pacific Ocean
Fig. 3. Profile of chlordane-related compounds in albatross fat compared with their proportions in technical chlordane.
appear to be greater in the European Arctic (Barents Sea) than
in the Canadian Arctic [45]. Combined with results for deposition of toxaphene in North America [46], the available
evidence suggests that the north Atlantic and eastern North
America show a greater degree of contamination with toxaphene than the north Pacific. This is consistent with the relatively great use of toxaphene in the 1970s on cotton in the
southeastern United States [6]. This use, which peaked in the
mid-1970s, represented a major portion of global emissions
[6].
The ratio of toxaphene in eggs to that in fat (lipid/lipid) in
blackfooted albatross averaged 3.6, while this ratio for SDDT,
SHCH, and SCHL was 0.45, 0.43, and 0.34, respectively. This
high ratio implies recent dietary exposure of the adult birds
and suggests an additional source of toxaphene for the females
relative to other OC pesticides. The possibility of local sources
of persistent organochlorines near the nesting sites of the
blackfooted albatross is unlikely [25]. Adult albatross are in
a fasting state for most of their stay on the atoll and travel
500 to 800 km north of the atoll to feed [22]. There are no
measurements, to our knowledge, of toxaphene in prey items
of the albatross or in seawater in the central Pacific Ocean that
would help explain the high egg/fat ratio. Toxaphene measurements in the northern Bering Sea show that it is a major
OC pesticide, present at concentrations about 20 times higher
than SDDT but 100 times lower than SHCH (T.F. Bidleman,
Environment Canada, Toronto, ON, personal communication).
The distribution of the Laysan and blackfooted albatross in
the north Pacific may help explain the greater concentrations
of OC pesticides in blackfooted albatross. The majority of adult
Laysan albatross are thought to feed between Japan, the Aleutians, and Hawaii, USA, in December to May and are more
commonly observed from June to August off the North American coast. In September to November, they are abundant in
the northwestern Hawaiian Islands as they return to their midPacific colonies. In contrast, adult blackfooted albatross are
most common in the eastern tropical north Pacific, frequenting
the North American coast from Baja California, Mexico, to
Canada, favoring offshore areas with strong upwelling currents. They spend December to February in central Pacific or
Hawaiian breeding colonies. Abundance closer to the North
American coast increases in March to May, with higher numbers seen off Canada and in the Gulf of Alaska in summer.
Blackfooted albatross are rare in the western north Pacific [22].
Environ. Toxicol. Chem. 21, 2002
419
Past emissions of DDT, toxaphene, and related organochlorine pesticides continue to give rise to elevated concentrations in resident top predators along the coast of California
[47]. The central valley of California was a major use area for
DDT, and there is evidence for continued emissions via volatilization from soils to air and long-range transport [48]. The
relatively high concentrations of SDDT and toxaphene in
blackfooted albatross may thus be related to heavy use of these
pesticides in agriculture in California in the 1960s and 1970s.
Concentrations of DDT and PCBs were generally greater in
piscivorous seabirds, such as guillemot (Uria aalge) and
Brant’s cormorant (Phalacrocorax penicillatus) from the Gulf
of the Farallones (San Francisco, CA, USA) [47], than in albatross when compared on a lipid basis (Table 3). Other piscivores, such as rhinoceros auklet (Cerorhinca monocerata)
feeding on the continental shelf off California and off Vancouver Island [49], had similar DDT and PCB concentrations
to blackfooted albatross but higher concentrations than Laysan
albatross (Table 3). Both species of albatross had greater concentrations of chlordane-related compounds and mirex in eggs
than planktivores, such as ancient murrelet (Synthilboramphus
antiquus), and piscivores, such as rhinoceros auklet and forktailed petrel (Oceanodroma furcata), sampled on the coast of
British Columbia in the 1980s [49]. Much greater concentrations of SDDT and PCBs were found in eggs of bald eagles
(Haliaeetus leucocephalus) from the Aleutian Islands [50]
than in albatross eggs (Table 3). However, the bald eagles feed
at a higher trophic level than albatross, with a diet including
mammals, fish, and seabirds.
The HCH isomers, dieldrin, and octachlorostyrene were the
only organochlorines that were not present at significantly
higher concentrations in blackfooted albatross compared with
Laysan albatross. This implies a more even distribution of
these chemicals between the western and eastern north Pacific.
The much lower SHCH concentrations in the northern royal
albatross also imply much lower levels in seawater in the
southern oceans. Our results are generally consistent with the
geographical trends of HCH isomers in the Pacific Ocean and
Indian Oceans in 1989 and 1990 measured by Iwata et al. [3].
They found the highest levels of SHCH in the north Pacific
(Bering Sea, Gulf of Alaska, Northwestern Pacific, USA;
means ranging from 1,000 to 1,900 ng/L), intermediate levels
in the central north Pacific (250 pg/L), and the lowest levels
in the southern Pacific Ocean (south of Australia; mean of 36
pg/L).
Both SHCH and SDDT have been reported as the predominant OC pesticides in resident and local migrant birds in south
India [51]. Some resident species had relatively high proportions of a- and g-HCH, implying recent exposure [51]. This
is quite different from measurements in birds from Europe and
North America, including the north Pacific albatrosses, where
PCBs and DDT predominate (Table 3) and only the recalcitrant
isomer b-HCH predominates. The results for the northern royal
albatross eggs were similar, with a general predominance of
b-HCH in these samples. These results illustrate that, where
HCH use is great, there can be significant accumulation in
birds, even migratory birds, which spend only a short time in
the greatest HCH exposure area. Our results also suggest that
albatross are not directly exposed to elevated HCH despite
frequenting offshore areas of the western Pacific. however,
exposure there (e.g., off China and southeast Asia) may be
greater than in North American waters.
Both HCB and octachlorostyrene concentrations were cor-
a
Eggs
Eggs
Eggs
1983
1985
1986
Muscle
Egg
Muscle
Muscle
Muscle
Muscle
Eggs
Eggs
Fat
Eggs
1983
1993–1994
1993–1994
1993–1994
Eggs
Eggs
1983–1985
1993–1994
35
4
1
1
6
5
10
10
1
6
6
16
3
9
?
10
11
5
20
6
2
2 pools
2 pools
1 pool
7
3
13
7
—
9.7
2.2
2.8
3.1
3.4
5.1
3.6
—
23.5
14
8.50
11
11.5
?
100
70
13
91
91
13
90
10
10
—
—
13.6
5
2,600
7,300
4,100
650
3,050
4,200
496
30
98
—
—
—
—
—
—
—
—
—
267
1,110
4,050
—
—
—
—
—
—
—
n or
Toxan in pool % Lipid phene
80,000
154,000
5,500
980
275,000
74,000
1,980
188
—
2,915
4,507
6,412
15,270
5,426
25,000
2,492,600
321
4,385
1,440
5,215
2,370
—
—
—
965
964
16,882
15,900
SDDT
97,000
340,000
12,000
2,600
280,000
100,000
3,520
19
—
4,723
4,336
10,390
35,360
7,178
22,000
490,000
207
2,769
—
—
—
2,700
1,985
6,880
758
790
12,147
15,000
SPCB
— 5 no data available; CHL 5 chlordane-related compounds; TCPMe 5 tris(p-chlorophenyl)methane; TCPMeOH 5 tris(p-chemophenyl)methanol.
Sweden
North Sweden
Muscle
1993–1994
Egg
Muscle
1993–1994
1989
Fat
Fat
Egg
Fat
Egg
Egg
Egg
Chick
Muscle
Muscle
1994–1995
1994–1995
1994–1995
1993–1994
1993–1994
1993–1994
1995–1998
1995–1998
1993–1994
1994–1994
Guillemot (Uria aalge)
1976–1978
Brunnich’s guillemot
1981
(Uria lomvi)
Guillemot (Uria aalge)
1980
Eider duck
1980
(Somateria molissima)
White-tailed sea eagle (Haliaetus
1982
albicilla)
Osprey (Pandion haliaetus)
1982
Skuas (Catharacta sp.)
Penguins (Pygoscelis sp.)
Adelie penguin
(Pygoscelis adelie)
Laysan albatross
Blackfooted albatross
Blackfooted albatross
Layson albatross
Laysan albatross
Blackfooted albatross
Northern royal albatross
Northern royal albatross
Guillemot (Uria aalge)
Brant’s cormorant
(Phalacrocorax penicillatus)
Rhinoceros auklet
(Cerorhinca monocerata)
Pigeon guillemot
(Cepphus columba)
Peregrine falcon
(Falco peregrinus anatum)
Bald eagle
(Haliaeetus leucocephalus)
Leach’s storm petrel
(Oceanodroma leucorhoa)
Fork-tailed storm petrel
(Oceanodroma furcata)
Glaucous-winged gull
(Larus glaucescens)
Rhinoceros auklet
(Cerorhinca monocerata)
Ancient murrelet
(Synthilboramphus antiquus)
Year(s)
199
—
—
—
—
—
425
32
—
91
229
241
164
309
3,400
—
23
168
350
849
291
—
—
—
—
—
175
1,530
—
—
—
—
—
—
—
—
—
—
—
—
—
—
—
1,655
—
—
61
95
623
—
—
—
—
—
—
—
—
—
—
—
—
—
—
—
—
21
21
88
45
170
470
—
—
—
94
266
177
—
—
—
—
—
—
—
[17]
[41]
[40]
[39]
[49]
[50]
[58]
This study; [23]
[23]
[47]
This study
This study
This study
[25]
Reference
Environ. Toxicol. Chem. 21, 2002
Spitzbergen, Norway
Spitzbergen, Norway
North Atlantic/Arctic/Baltic
Baltic
Baltic
Antarctic
Weddell Sea
Vancouver Island (BC, Canada)
Aleutian Islands (Kiska)
Central coast of California, USA
Gulf of Farallones (CA, USA)
Taiora Head, New Zealand
Midway Atoll
Pacific Ocean
Midway Atoll
Location
TCPMe
1
TCPMe
OH Mirex
SCHL
Table 3. Concentrations of toxaphene and other organochlorine (CO pesticide-related compounds as well as polychlorinated biphenyls (PCBs) in seabird eggs and tissues (1980–1990s); (ng/g lipid
wt) from the north Pacific Ocean; results for seabirds from other regions are included where toxaphene was reporteda
420
D.C.G. Muir et al.
Toxaphene in albatrosses from the Pacific Ocean
related (p , 0.01) in Laysan albatross fat; however, octachlorostyrene was also correlated with other recalcitrant OC pesticides. The similar concentrations in both species of albatross
imply an Asian source of octachlorostyrene for the Laysan
albatross. Little is known about global emissions of octachlorostyrene; however, magnesium production and chlorine manufacture were historically important sources (http://www.
epa.gov/grtlakes/bnsdocs/98summ/ocs/index.html) [52]. Maximum emissions of octachlorostyrene in the Great Lakes region
occurred in the 1960s (http://www.epa.gov/ grtlakes/bnsdocs/
98summ/ocs/index.html) [52], probably due to disposal of
wastes related to chlorine manufacture using graphite electrodes, a process abandoned in the 1970s. Both HCB and octachlorostyrene have been assumed to have similar sources
based on formation from successive two-carbon units
(www.epa.gov/grtlakes/bns/baphcb/tephcb.html) [53].
The proportion of various chlordane-related compounds in
the north Pacific albatross species was different from technical
chlordane (Fig. 3), reflecting a significant capacity to degrade
the major components to oxychlordane. The predominance of
oxychlordane in avian species has been observed in many
studies. Less well documented is the bioaccumulation of minor
components of technical chlordane such as the octachlordanes
U82, U83, and MC5. These compounds were found to biomagnify in the arctic cod–ringed seal–polar bear food web [34].
Fisk et al. [21] have shown that MC5 is a major octachlordane
in liver of seabirds from Northern Baffin Bay, Canada, present
at higher levels than cis- or trans-chlordane. The proportion
of MC5 relative to trans-chlordane was also elevated in penguin tissue; however, U82 and U83 were not observed in penguins [54]. While MC6 (or nonachlor III) was a major chlordane compound in polar bear [35], it was only a minor component in penguins and was undetectable in albatross fat (although small amounts could have been present and
undetectable due to coelution with PCB99), illustrating major
phylogenetic differences in degradative capacity toward chlordane-related compounds.
Despite recent use of DDT in China and southeast Asia
compared with North America [55] and evidence for transPacific transportation of DDT [48], Laysan albatross do not
show elevated concentrations of DDT-related compounds, including TCPMe, compared with blackfooted albatross. The
DDT contamination of marine food webs along the west coast
of North America remains relatively high [47,56] and, although
data for comparable species are limited, is higher than in marine food webs from the Asian coast of the Pacific [2,57]. The
TCPMe/OH concentrations also appear to be greater in North
American waters than in Asia [57,58]. The TCPMeOH was
elevated in peregrine falcon eggs from the central coast of
California, ranging from 250 to 5,300 ng/g lipid weight [58],
compared with 623 ng/g lipid in blackfooted albatross. The
ratio of TCPMe to SDDT was much greater in albatross eggs
(0.14) than in the peregrine falcon (0.007) [58] or white-tailed
sea eagle from the Baltic sea (0.004) [59]. This higher ratio
may be due to the lower trophic feeding level of albatross and
to a lesser degradative capacity compared with falcons and
eagles. Ratios of TCPMe to SDDT have also been reported
to be greater in fish (;0.01) than in marine mammals or fisheating birds [59].
It has previously been concluded that the 4,49-DDE concentrations in blackfooted albatross, which averaged 1,800 ng/
g (wet wt) compared with the 293 ng/g (wet wt) in the present
samples, were at the lower end of the range of possible effects
Environ. Toxicol. Chem. 21, 2002
421
on avian species [26]. Albatrosses were found to have relatively high levels of toxaphene compared with other OC pesticides, especially in eggs. Whether these levels represent significant toxicological threats to albatross is difficult to assess.
Toxaphene is not considered highly toxic to avian species [10].
Black ducks (Anas rubripes) fed toxaphene at 50 mg/kg for
19 months showed no significant effects on egg production,
growth, egg shell thickness, or chick survival compared with
controls [60]. There is a lack of toxicological information
available for individual congeners. Both B8-1413 and B9-1679
were not genotoxic in the Mutatoxt (Azur, Carlsbad, CA,
USA) assay, and albatross liver microsomes decreased the genotoxic response of technical toxaphene [11]. Given the significant levels of these 2-exo,3-endo,5-exo,6-endo-substituted
congeners, further work on tissues and eggs of fish-eating birds
should be carried out to develop more comprehensive data on
their concentrations. The availability of individual chlorobornane standards is likely to make this possible in the near future.
Given the upcoming global ban on toxaphene and several other
OC pesticides (http://irptc.unep.ch/pops/pops-gs/popsgs.html)
[4], future work should examine temporal trends of these contaminants in albatross at these remote locations in both hemispheres as a measure of the global response to the cessation
of use.
Acknowledgement—This research was conducted under a baseline
assessment of Global Marine Contamination, contract agreement
8200227010 between the U.S. Environmental Protection Agency and
the World Wildlife Fund USA. The invaluable assistance of the U.S.
Fish and Wildlife Service, Pacific Islands System (D.K. McDermond,
E. Flint), and the U.S. Navy (Lieutenant Commander M. Driggers,
Chief Warrant Officer Gregg Dafenderfer) is gratefully acknowledged.
Funding for the collection and analysis of south Pacific albatross
samples was provided by the Department of Conservation, Wellington,
New Zealand. We thank Lori Feyk for shipping and handling of samples, Dan Tretiak for sample extraction, and Norbert Grift for technical
supervision of all of the GC-ECD analysis. The authors wish to acknowledge the expertise of Scott Leathem, Tania Van Maanen, Bob
Symons, and the Institute for Environmental Science and Research,
Wellington, New Zealand, ultratrace analytical laboratory, who conducted the analyses of the northern royal albatross samples. We thank
Aaron Fisk for helpful review of the manuscript.
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