Environmental Health Perspectives Volume
103, Supplement 4, May 1995
[Citation
in PubMed] [Related
Articles]
Contaminants and Sea Ducks in Alaska and the Circumpolar Region
Charles J. Henny,1 Deborah D. Rudis,2 Thomas
J. Roffe,3 and Everett Robinson-Wilson4
1National Biological Survey, Forest and Rangeland Ecosystem
Science Center, Corvallis, Oregon; 2U.S. Fish and Wildlife Service,
Juneau, Alaska; 3National Biological Survey, National Wildlife
Health Center, Madison, Wisconsin; 4U.S. Fish and Wildlife Service,
Anchorage, Alaska
Abstract
We review nesting sea duck population declines in Alaska during recent
decades and explore the possibility that contaminants may be implicated.
Aerial surveys of the surf scoter (Melanitta perspicillata), white-winged
scoter (M. fusca), black scoter (M. nigra), oldsquaw (Clangula
hyemalis), spectacled eider (Somateria fischeri), and Steller's
eider (Polysticta stelleri) show long-term breeding population declines,
especially the latter three species. The spectacled eider was recently classified
threatened under the Endangered Species Act. In addition, three other diving
ducks, which commonly winter in coastal areas, have declined from unknown
causes. Large die-offs of all three species of scoters during molt, a period
of high energy demand, were documented in August 1990, 1991, and 1992 at
coastal reefs in southeastern Alaska. There was no evidence of infectious
diseases in those scoters. The die-offs may or may not be associated with
the long-term declines. Many scoters had elevated renal concentrations of
cadmium (high of 375 µg/g dry weight [dw]). Effects of cadmium in
sea ducks are not well understood. Selenium concentrations in livers of
nesting white-winged scoters were high; however, the eggs they laid contained
less selenium than expected based on relationships for freshwater bird species.
Histological evaluation found a high prevalence of hepatocellular vacuolation
(49%), a degenerative change frequently associated with sublethal toxic
insult. Cadmium and selenium mean liver concentrations were generally higher
in those birds with more severe vacuolation; however, relationships were
not statistically significant. We do not know if sea duck population declines
are related to metals or other contaminants.
-- Environ Health Perspect 103(Suppl 4):00-00 (1995)
Key words: Alaska, eiders, scoters, oldsquaw, cadmium, selenium,
metals, population declines, endangered species
This paper was presented at the Conference on Environmentally
Induced Alterations in Development: A Focus on Wildlife held 10-12 December
1993 in Racine, Wisconsin.
We thank Don and Lahoma Leishman for bringing the scoter
mortality at Cape Yakataga to our attention each year. Herman Griese (Alaska
Department of Fish and Game) and Tim Bowman (U.S. Fish and Wildlife Service
(USFWS), Cordova, Alaska) visited mortality sites in 1990 and 1991. Pilot
Steve Ranney provided logistics support. Personnel at the National Wildlife
Health Center (National Biological Survey), including J. Christian Franson,
provided necropsy reports and advice. Mike Vivion, pilot-biologist, provided
logistics and expertise for collecting scoters on Yukon Flats National
Wildlife Refuge (NWR). Ted Heuer and Leslie Kerr of Yukon Flats NWR were
instrumental in guiding our field collection on the refuge. Russell Oates,
Kim Trust, Bruce Conant, and John Hodges from the Alaska Region, USFWS,
provided additional information on waterfowl in Alaska. Joseph P. Skorupa,
USFWS, Sacramento, California, kindly provided unpublished information.
The manuscript was improved by the comments of W. Nelson Beyer, Lawrence
J. Blus, John E. Elliott, Gary H. Heinz, and David J. Hoffman.
Address correspondence to Dr. Charles J. Henny, National
Biological Survey, Forest and Rangeland Ecosystem Science Center, 3080
SE Clearwater Drive, Corvallis, OR 97333. Telephone (503) 757-4840. Fax
(503) 757-4845.
Introduction
Contamination of the environment with organic pollutants and metals is
worldwide; however, only limited information is available on the relationship
between con- taminants and effects on individual animals or animal populations,
especially for the arctic. Changes in population size, age and sex composition,
and reproductive success should be monitored to provide baseline data against
which to evaluate possible impacts on populations caused by contaminants
(1). The sea ducks discussed in this report have all experienced
serious population declines in Alaska and perhaps elsewhere during the last
several decades; the cause is unknown. The locations of sites discussed
in Alaska are shown in Figure 1.
Figure 1. Reference
locations for sea ducks in Alaska.
Surf scoters wintering in Oregon and Washington in 1984 to 1985, which
perhaps nest in Alaska, contained elevated concentrations of cadmium (2).
Surf scoter body weights in late January were negatively correlated with
cadmium concentrations, and this initially focused our attention on cadmium.
Sublethal effects of cadmium toxicity include growth retardation, anemia,
testicular damage, hypertrophy of the heart, and renal dysfunction (3).
Organic compounds received less attention in this evaluation because in
1992, 19 addled spectacled eider eggs from the Yukon Delta, Alaska, showed
organochlorine pesticides (<0.05 µg/g dry weight [dw]) and polychlorinated
biphenyls (PCBs; <0.30 µg/g dw) below detection limits (K Trust,
personal communication).
Benthic feeding surf scoters eat bivalves along with gastropods and crustaceans,
some plants, algae, insects, polychaetes, and fish. This diet is similar
to that of the benthic feeding spectacled eider which was recently classified
as a threatened species by the United States Fish and Wildlife Service (USFWS)
throughout its range in Alaska and Russia (4). About 50,000 pairs
of spectacled eider, half the estimated world population, nested on the
Yukon- Kuskokwim Delta in 1971; in 1992, the population was estimated at
1721 pairs (5). The Steller's eider shares the same breeding range
as the spectacled eider (Alaska and Russia), is also declining in Alaska
and is a candidate for endangered species status. Possible reasons for the
eider declines, in addition to contaminants, include parasites and disease,
subsistence harvest, predation during broodrearing, habitat change, and
alteration of Bering Sea food resources (5,6).
The purpose of this paper is to a) review the status of breeding
populations of scoters, eiders, and oldsquaws in Alaska and document the
large die-offs of scoters at coastal areas during molt; b) evaluate
the availability of metals in the arctic and their accumulation in sea ducks;
c) evaluate results of histological examinations of liver, kidney,
and testes to reveal indications of tissue damage associated with elevated
levels of metals; and d) lay out a research strategy to further investigate
the cause(s) of the population declines.
Materials and Methods
The USFWS has studied waterfowl populations throughout much of North
America using strip transect aerial surveys since 1955 (7,8) and
in Alaska since 1957, as well as using field studies of individual populations.
Waterfowl survey information was obtained from published reports and
an unpublished manuscript prepared by personnel of the USFWS. Established
strata (routes) flown in Alaska since 1957 provide the long-term data set
used to assess population changes in this report (9). Scoter numbers
in Alaska and Yukon Territory were not separated into species during aerial
surveys. The survey plane was changed in 1977 to a Turbo-Beaver which flies
slower and has much better visibility. Aerial counts were adjusted for observer
visibility and for the change in aircraft type.
In 1990, 1991, and 1992, we responded to reports of scoters dying during
the August molt at Cape Yakataga and Cape Suckling in southeastern Alaska.
Dead scoters were counted, and fresh carcasses were collected for necropsy
and residue analyses. The number of live scoters in each region was also
documented.
Analyses of water and sediment indicate the extent of metal contamination,
but reveal little about the bioavailability of metals to biota. Quantification
of metal concentrations in indigenous relatively
sessile, benthic organisms such as mussels, can be used to assess the bioavailability
of metals (10). Mussels become particularly meaningful when they
form a substantial portion of the diet of the species of interest, which
they do for scoters (2,11). Blue mussels (Mytilus trossulus)
were collected at five sites between Cordova and Yakutat, Alaska, in 1992
where scoters were dying during the molt. Usually three pools of mussels
varying from 19 to 33 individuals each were analyzed for residues (without
the shell), since shells contain very low cadmium concentrations (12).
We collected (shot) 37 white-winged scoters from a nesting population
on the Yukon Flats National Wildlife Refuge (NWR) in interior Alaska (early
June 1993) to a) evaluate metals in liver and kidneys; b)
identify and evaluate metals in stomach contents; and c) evaluate
metals with respect to hepatic, renal, and testicular condition as determined
by histopathology.
Liver and kidney samples were analyzed at Environmental Trace Substances
Research Center, Columbia, Missouri. Samples were weighed and frozen prior
to homogenization. An aliquot of each sample was weighed, freeze-dried,
and rehomogenized. Tissue subsamples were digested by nitric acid reflux
for mercury using cold vapor atomic absorption with a Perkin-Elmer Model
403 AA. Hydride generation required nitric-perchloric digestion for arsenic
and selenium. Samples analyzed by inductively coupled plasma (ICP) using
a Jarrell-Ash Model 1100 Mark III were also acid digested. Three times the
standard deviation of the mean was used as the detection limit for each
sample; Al 3.0, As 0.2, B 2.0, Ba 0.1, Be 0.01, Cd 0.02-0.03, Cr 0.1, Cu
0.2-0.3, Fe 0.9-1.0, Hg 0.01-0.04, Mg 0.3-0.4, Mn 0.2, Mo 1.0, Ni 0.1, Pb
0.4-0.5, Se 0.2-2, Sr 0.09-0.1, V 0.3-0.4, Zn 0.9-1.0. All trace elements
are reported as µg/g dry weight.
Three- to 4-millimeter cross-sections of kidney and testes, and similar
sections through the liver lobe, were preserved in Bouin's solution (accessions
1-7) or 10% buffered neutral formalin (accessions 8-37). Sections were paraffin-embedded,
sectioned at 5 µ, and stained with hematoxylin and eosin (H&E).
Oil-red-O stain was applied to fresh cut formalin-fixed tissues where H&E
indicated potential lipid inclusions. The relationship between histopathologic
findings and metal concentrations (cadmium, selenium, copper, zinc) were
analyzed using univariate analysis of variance (ANOVA) for each metal. All
metals were transformed to geometric scale (log10). Trends between
degree of vacuolation and metal concentrations were evaluated using linear
contrasts with ANOVA.
The first eider carcasses were obtained for residue analyses in 1991.
These included three birds confiscated after they were illegally shot and
an eider that flew into a tower during a storm.
Results
Review of Sea Duck Status in Alaska
Black scoters, surf scoters, white-winged scoters, and oldsquaw nest
at freshwater lakes and ponds in Alaska, with the breeding range of the
latter three species extending into adjacent Canada, and with all species
wintering along the Pacific and Atlantic coasts (13). Spectacled
eiders breed discontinuously along the coast of Alaska, historically on
St. Lawrence Island, and along the Arctic coast of Russia from the Chukotsk
Peninsula west to the Yana Delta (14). Spectacled eiders apparently
winter in the central and northwestern Bering Sea. The king eider (S.
spectabilis), common eider (S. mollissima), and Steller's eider
also nest near the Alaska coast.
According to Hodges et al. (9), scoter populations have declined
since the aerial survey began in 1957, with an estimated decline of 30%
during the 36-year period. Oldsquaw numbers were probably unchanged prior
to 1977 and then declined precipitously. In this 16-year period, oldsquaw
declined an estimated 75%. The eider breeding population on the Yukon-Kuskokwim
Delta (spectacled, Steller's, and a few common eiders) decreased 93% from
1957 to 1992. The spectacled eider is now classified as threatened under
the Endangered Species Act with a 94 to 98% decline in its principal breeding
range (5), and the Steller's eider is also a candidate species. The
Steller's eider was apparently extirpated in 1975 as a breeding bird on
the Yukon-Kuskokwim Delta, one of two areas in Alaska where it was a regular
breeder, and it is now restricted to a small breeding area near Barrow (6).
Monthly Steller's eider counts in winter at Izembek Lagoon on the Aleutian
Islands (mostly breeding birds from Siberia) averaged for the period 1986
to 1990, when compared with the same monthly averages during 1975 to 1985,
show an overall population decline of more than 50% (6). Thus, the
Steller's eider decline is more widespread than North American breeding
populations.
Alaska breeding populations of three other diving ducks that commonly
winter in coastal areas, the common goldeneye (Bucephala clangula),
Barrow's goldeneye (B. islandica), and bufflehead (B. albeola)
have declined. The two goldeneye species declined 45% and the bufflehead
42% since 1977 (9).
Scoter Die-offs on Alaska Molting Grounds
Citizens reported on 20 August 1990 that scoters had been dying at Cape
Yakataga (located in southeastern Alaska between Cordova and Yakutat) for
about 2 weeks. A beach survey of about 2.5 km was made at Cape Yakataga
on 21-22 August and revealed carcasses of 235 white-winged scoters, 28 surf
scoters, and 5 unidentified scoters. About 20 obviously weakened scoters
were observed on the beach and 150 to 200 live scoters were seen offshore.
Much higher numbers of dead birds had been observed by D. Leishman 2 days
before the Alaska Department of Fish and Game visit; high tides apparently
refloated and removed many carcasses. On 25 August, an Alaska Law Enforcement
Agent recorded at least 200 dead scoters on the beach at two locations between
the Tsiu and Kallakh Rivers west of Cape Yakataga.
Seven emaciated carcasses were collected for necropsy. No gross lesions
or evidence of infectious diseases were found. Bacterial and viral isolations
from multiple tissues were negative. Cape Yakataga is a reef area that seems
to attract molting scoters in August, perhaps because scoter prey (mussels,
clams, crustaceans, etc.) associate with rocky outcroppings.
Scoters again were reported dead and dying on 7 August 1991 at Cape Yakataga.
Tim Bowman, a USFWS wildlife biologist, Cordova, found 100 dead scoters
and another 100 obviously weak scoters near shore. All were molting and
flightless, and all scoters had died within the previous 2 days. About 90%
were white-winged scoters and 10% were black scoters. Several hundred scoters
were alive and apparently healthy offshore at the Cape. On 19 August 1991,
200 dead scoters were found on the beach at Cape Yakataga.
On 15 August 1991, Bowman flew to Cape Suckling, which is similar to
Cape Yakataga, and captured by hand 10
molting white-winged scoters. The birds were emaciated, weak, and relatively
easy to capture. Six dead scoters were found by walking about 3 km of shoreline.
More than 1000 live scoters were observed offshore at Cape Suckling.
Scoters were reported dying at Cape Yakataga on 18 August 1992. Weather
did not permit us to visit the region until 26 August, when 58 dead scoters
were counted at Cape Suckling (56 white-winged scoters, 1 surf scoter, and
1 unidentified scoter). Fifty-one of the birds had molted and were flightless
and five had retained their primaries. During a beach survey at Cape Yakataga
and north of the Cape, we counted 53 dead white-winged scoters, 2 surf scoters,
and 9 unidentified scoters. They were all emaciated and some had been dead
for many days. At Cape Yakataga, 275 to 300 live scoters were offshore.
Between Cape Suckling and Cape Yakataga, an additional 1870 live scoters
were counted.
No dead scoters were reported in southeastern Alaska in 1993. A visit
to Cape Yakataga and Cape Suckling on 18-19 August 1993 revealed about 400
and 1200 live scoters, respectively, with no dead birds along the shoreline.
All scoters could fly and had not yet initiated the molt.
Metals Accumulation in Sea Ducks and Prey
Molting Scoters from Southeast Alaska. Scoters found moribund
or dead in southeastern Alaska in 1990, 1991, and 1992 were analyzed for
a series of metals (Table 1). Most of these scoters were molting in late
summer at reef areas associated with Capes and died shortly after their
arrival. Cadmium concentrations were especially high in kidneys from Cape
Suckling scoters in 1991.
Mussels from Southeast Alaska. Mussels, prey species for
scoters, were analyzed from the region of the August die-offs (between Cordova
and Yakatat, Alaska) as were mussels and whelks from Oregon in 1992 (Table
2). Geometric mean cadmium concentrations (whole body, without shell) of
blue mussels (Mytilus trossulus) in this study were 2.5 to 5.9 µg/g
dw. M. trossulus collected at Cape Yakataga in 1975 (15) had
nearly identical concentrations of cadmium as in 1992 (5 µg/g vs 5.9
µg/g). Whelks (Nucella emarginata) from Waldport Bay, Oregon,
contained five times more cadmium than mussels at the same site. The whelks
analyzed included mostly foot rather than whole body, but Streit and Winter
(16) reported in Anodonta anatina that the lowest concentrations
were found in the foot, gut/gonad complex, and muscle tissue, which would
tend to minimize the real species difference.
Nesting Scoters from Interior Alaska. Thirty-seven nesting
white-winged scoters collected on the Yukon Flats NWR in early June 1993
were analyzed for a series of metals (Table 3). The 11 females contained
eggs at various stages of development, including eggs in the oviduct ready
to be laid in two birds. Fourteen of 18 scoters analyzed in southeastern
Alaska also were white-winged scoters (Table 1), and residue comparisons
can be made. In general, the livers of scoters that died during the molt
(Table 1) contained higher concentrations of cadmium, copper, mercury, iron,
and zinc. Magnesium and manganese were similar in both series, while selenium
was higher in the livers of breeding birds on the Yukon Flats NWR (geometric
mean 54 vs 22 µg/g dw). The selenium concentrations from the Yukon
Flats are potentially troublesome.
Eiders from Alaska. Three adult spectacled eiders were
shot illegally on St. Lawrence Island in November 1991 and were seized by
law enforcement personnel. An additional Steller's eider collided with a
tower at Togiak NWR in September 1991. These four carcasses provide the
only carcass residue data available for the species (Table 1).
Mercury in 19 addled spectacled eider eggs collected on the Yukon Delta
in 1992 ranged from nondetection (<0.03) up to 0.41 (geom. mean 0.07)
µg/g dw, while selenium ranged from 1.8 to 5.3 (geo mean 3.3) µg/g
dw (K Trust, personal communication).
Metals and Histopathology of Nesting White-winged Scoters
Kidney sections often contained tissue changes associated with parasitism.
These lesions were characterized by small, well defined granulomatous or
pyogranulomatous foci containing central debris and larval nematode remains
and were distributed throughout the renal cortex. Syncytia were common.
The lesions varied from mild to severe and may have hampered observation
of degenerative changes that could potentially be associated with metals.
Degenerative and necrotic lesions not associated with parasitic lesions
occurred in six sections and were very localized and minor. These changes
did not correlate with the tissue residue levels of contaminants we examined.
Vacuolation of hepatic cytoplasm was common (18/37=49%). Vacuoles varied
from an indistinct mildly foamy cytoplasm to clear, distinct, round, singular
to multiple vacuoles. Oil-red-O stain indicated lipid was responsible for
only a small portion of the vacuolation in some scoters. The degree of vacuolation
varied from mild to severe. Generally, mean liver concentrations of cadmium
and selenium were higher in birds with more severely affected liver sections.
However, no significant relationship was found between cadmium concentration
and hepatocellular vacuolation and only a marginally significant relationship
was found between selenium and vacuolation (F 2.84, p=0.10) (Table
4). There was no relationship between presence and severity of vacuolation
and sex of the bird, mean liver copper concentration, or mean liver zinc
concentration. Occasional granulomatous parasitic foci were observed in
liver sections.
No significant lesions were observed in sections of testes.
Discussion
Long-term Metals Availability in the Arctic
If cadmium, selenium, or other metals are currently affecting sea duck
populations, the question we immediately ask becomes, why at this time?
Of course, the population data for scoters and eiders provide evidence of
long-term population declines and not strictly a recent event. What is the
source and long-term pattern of pollution in Alaska sea ducks? Norheim (17)
studied seabirds and reported the presence of cadmium in both the arctic
and antarctic environments, but did not know to what extent long-distance
transport of air pollution contributed to this load. In arctic terrestrial
ecosystems lichens constitute a large portion of the tundra vegetation,
and they readily absorb atmospheric contaminants, including cadmium (18).
Therefore, barren-ground caribou (Rangifer tarandus) with a preferred
food in arctic Canada of lichens, were evaluated (19). Gamberg and
Scheuhammer (19) reported elevated concentrations of cadmium in caribou
kidneys (high of 166 µg/g dw, and most above 40 µg/g, especially
older animals) but with no significant differences among the three herds
sampled. They suggested that it was unlikely that herds were exposed to
cadmium from point-source pollution. Gamberg and Scheuhammer further pointed
out that in more pristine areas, contamination is primarily from long-range
transport with large air masses, but in some locations, differences in buffering
capacity and degree of environmental acidification may also contribute to
site differences in cadmium accumulation by herbivorous wildlife. Plants
accumulate cadmium, especially where soil acidification has occurred. In
addition, acidification increases concentrations of cadmium in surface waters
(20). Cadmium enrichment of food chains caused by acid rain may be
important in portions of the arctic. Like Norheim (17) for seabirds,
Gamberg and Scheuhammer (19) did not know whether the cadmium was
primarily of natural origin in the terrestrial arctic ecosystem or whether
it was mainly from atmospheric deposition.
Increased cadmium in remote ice fields seems to coincide with human industrialization
(21,22). Cadmium in wheat samples from 1972 was found to be twice
that reported in samples from 1916 at the same location near Uppsala, Sweden
(23). However, Boutron et al. (24) more recently observed
decreased concentrations of lead, cadmium, and zinc in the central Greenland
snows from 1967 to 1989, and suggested that pollution of the troposphere
of the northern hemisphere has significantly decreased for the three metals.
However, Furness et al. (25) reported that attempts to quantify changes
in heavy metal concentrations with ice cores or snow samples have been hindered
by extremely low concentrations. They recommended using plants and animals
because metal concentrations are increased by five to nine orders of magnitude
over those of snow or ice. Unfortunately, few long-term suitable series
of biological samples are available for analysis, especially for cadmium,
which concentrates in the liver and kidney (26).
Metals and Their Source in Migratory Sea Ducks
Migratory sea ducks present another confounding issue in that the accumulation
of metals may occur at a number of places including both the breeding and
wintering grounds. When cadmium concentrations in kidneys of hatch-year
(HY) birds collected in October (1.13 µg/g, dw) were compared with
adults (after hatch year, AHY) collected at the same time (33.8 µg/g),
it was apparent that surf scoters wintering in Oregon and Washington accumulated
cadmium during their life (2). Data showed that cadmium increased
significantly (p<0.001) in kidneys from October to January in
HY surf scoters collected at two of the sites in Oregon and Washington (0.94
vs 5.18 µg/g dw) (2). No HYs were collected at the third site
in January. Thus, it is important to recognize that cadmium was accumulated
by HY surf scoters at a rate of about 1.4 µg/g per month on the wintering
grounds. The maximum longevity for surf scoters is unknown, but for the
similar-sized white-winged scoter, it is 15 years 7 months (27),
and cadmium is generally believed to accumulate throughout life (28).
However, cadmium did not increase in the liver or kidney tissue of herring
gulls (Larus argentatus) between 4 and 11 years of age (29).
Hontelez et al. (30) reported cadmium concentrations in common
eiders from the Netherlands and reviewed European literature. He reported
median concentrations (dw) in livers and kidneys, respectively, as follows:
Netherlands, 6.5 and 15.3 µg/g; Norway, 13 and 25 µg/g; Denmark,
12.6 and 38.1 µg/g; Sweden, 6.7 and 21.8 µg/g; Svalbard, 13.2
and 48.7 to 59.8 µg/g. Differences between studies may possibly be
explained by differences in age of the birds investigated. For example,
the HY eiders from Denmark contained 9 and 26 µg/g cadmium in liver
and kidney respectively, while AHYs contained 17 and 52 µg/g (31).
Oldsquaws from Sweden contained even higher median levels of cadmium in
kidneys (est. 41.4 µg/g dw, max. 90 µg/g) than eiders (32).
Residue concentrations of cadmium in eiders from Alaska were similar
to those in scoters (Table 1); however, common eiders from Europe seemed
to contain slightly lower concentrations. Common eiders were recommended
for biomonitoring cadmium in the aquatic environments of Sweden and the
Netherlands (30,32).
Interpretation of Metals Concentrations
Nicholson et al. (33) studied seabirds at St. Kilda with mean
cadmium kidney concentrations of 100 to 200 µg/g dw and mean mercury
concentrations of 5 to 13 µg/g dw and concluded that cadmium concentrations
at which damage began and at which biochemical changes could be detected
were below those presently considered relatively safe for humans (200 µg/g
wet weight [ww] renal cortex, i.e., >600 µg/g dw). In humans, cadmium
is stored mainly in the renal cortex, the metal level of which is about
twice as high as the medulla (34). Elinder et al. (35) found
histopathological changes in horse kidneys associated with cadmium as low
as 75 to 125 µg/g ww. Elliott et al. (36) reported Leach's
storm petrels (Oceanodroma leucorhoa) with similar kidney cadmium
concentrations (129-183 µg/g dw) to Nicholson's seabirds but observed
few histological lesions in the tissues examined; none were similar to the
lesions previously associated with poisoning by or high residue concentrations
of cadmium or mercury. We did not find histopathological changes associated
with the level of cadmium in scoter livers and kidneys. On the basis of
broad ecological judgments, Nicholson et al. (33) concluded that
animals exposed to high levels of metals for a long time have evolved mechanisms
to minimize the effects on breeding potential. Tolerance to high tissue
cadmium levels is thought to be made possible by the cellular production
of the metal binding protein metallothionein (36). Metallothionein
is thought to be important in the normal metabolism of essential trace metals
(zinc and copper) and to afford protection against nonessential metals (cadmium
and mercury) by sequestering them in a form that renders them incapable
of interacting with enzymes and other macromolecules (36). In their
study, Elliott et al. (36) observed a highly significant positive
correlation between renal cadmium and metallothionein.
Foulkes (37) points out that the rate at which cadmium can be
sequestered in the presumably inert metallothionein complex depends upon
the rate of cadmium uptake by the kidney and the net rate of renal metallothionein
synthesis. It is likely, a priori, that following acute exposure to cadmium,
a higher fraction of tissue cadmium will be present in nonmetallothionein
and therefore probably a more toxic form than is the case after more chronic
low-level exposure. Cadmium-induced metallothionein has been shown to bind
not only cadmium, but also copper and zinc, which can lead to increased
concentrations of these metals in kidney and liver tissue (38-40).
As predicted, we found significant positive correlations between log10
cadmium and log10 copper (r2=0.41, p=0.004)
and between log10 cadmium and log10 zinc (r2=0.29,
p=0.02) in the livers of scoters found dead during the molt (Table
1) and in scoters collected on the breeding grounds (Table 5). However,
neither copper nor zinc were positively correlated with increasing hepatic
vacuolation.
Several protective mechanisms may operate to diminish effects of metals.
For 10 seabird species, the highest correlation coefficients were observed
when the molar concentrations of cadmium plus mercury and selenium plus
zinc were used in the calculations (17). Norheim (17) cited
several papers where selenium and zinc reduced the toxic effect of cadmium
and mercury and concluded that the penguins and other birds studied have
protective mechanisms that most probably diminish any effect of metals.
Adult mallards fed 15 µg/g dietary cadmium for 90 days had 54.3
µg/g ww in their kidneys or about 175 µg/g dw, and no lesions
were found in the kidneys. A few males showed slight to moderate gonad alterations,
and spermatogenesis appeared to have ceased (41). Mild to severe
kidney lesions were found in mallard ducklings fed 14.6 µg/g (42).
But perhaps more important is the altered avoidance behavior in the form
of hyperresponsiveness observed in young black ducks (Anas rubripes)
produced from parents fed only 4 µg/g dietary cadmium for about 4
months before egg laying (43). Most mussels collected in coastal
Alaska and Oregon contained at least 4 µg/g cadmium (Table 2). Cadmium
mainly accumulates in soft body parts of mussels by means of metallothioneins,
and excretion appears to be very slow in contrast to that of other metals
(44). The giant snail (Neptunea spp.) collected near Yakutat
in 1975 contained much higher cadmium concentrations that ranged from 49.5
to 142.5 µg/g dw (15).
Selenium concentrations in livers of nesting white-winged scoters collected
on the Yukon Flats NWR were high. The 54 µg/g dw selenium (geometric
mean) was higher than in scoters found dead during the molt in southeast
Alaska (Table 1), lower than in surf scoters collected on the wintering
grounds in Oregon and Washington (2), but similar to surf scoters
collected on wintering grounds in San Francisco Bay, California (45,46).
Mallards with relatively low liver selenium concentrations are known to
have impaired reproductive success (47). We also found an apparent
relationship between liver selenium concentrations and hepatocellular pathology
(vacuolation) that warrants further investigation.
We anticipated selenium concentrations would be much lower on the Yukon
Flats NWR by assuming levels would quickly decline if scoters were no longer
in a selenium-enriched area. Liver loss of selenium (in the absence of selenium
in the diet) was rapid and described by an exponential equation in mallards
(48). Perhaps a selenium source exists on the Yukon Flats.
The interpretation of selenium concentrations in birds has been primarily
based on egg concentrations. Ohlendorf et al. (49) showed selenium
concentrations in eggs reflect dietary selenium levels, and adverse selenium
effects on reproduction begin at about 10 µg/g dw in the egg, or perhaps
a little lower. Heinz (50), under controlled laboratory conditions,
reported selenium concentrations above 12 µg/g dw in eggs reduced
hatching success. To better interpret the 54 µg/g dw selenium in livers
at Yukon Flats NWR, we need to estimate selenium concentrations in eggs
laid by the white-winged scoters. A number of paired sets of selenium concentrations
(livers and eggs) of waterbirds (all freshwater species) from Kesterson
NWR, California, and Carson Lake, Nevada, are available (Table 6). These
freshwater species provide evidence that selenium concentrations in eggs
can be estimated from selenium concentrations in livers. Based on these
data, an estimated 29.2 µg/g dw was expected in the white-winged scoter
eggs. Using a similar approach, but another more comprehensive database
of 42 paired sets of livers and eggs (unpublished, all freshwater species),
a regression equation was used to estimate 21.3 µg/g dw selenium in
white-winged scoter eggs (JP Skorupa, personal communication). Eggs from
two white-winged scoter hens shot on the Yukon Flats NWR with eggs in their
oviducts contained 3.05 and 2.74 µg/g dw selenium; less developed
eggs from other white-winged scoters collected at the same time contained
2.85, 2.99, 3.39, and 4.70 µg/g dw. These low egg values were nearly
10-fold less than concentrations predicted by the two approaches based on
relationships for freshwater species (21.3-29.2 µg/g dw) and well
below egg concentrations known to affect freshwater species. Therefore,
the use of selenium concentration in livers (based on freshwater species)
as a measure of potential reproductive problems for sea ducks and perhaps
other seabirds may be in error. More selenium research is needed on liver-egg
relationships for seabirds and sea ducks.
Mercury and selenium concentrations in eggs laid by spectacled eiders
(geometric means 0.07 and 3.3 µg/g dw, respectively) were low. Higher
concentrations of mercury in eggs (above 3 µg/g dw) were needed to
show behavioral changes in mallard ducklings in controlled laboratory studies
(54) and, as mentioned earlier, higher concentrations of selenium
are also needed to reduce hatching success.
At the present stage of our investigations, we have not found evidence
of cadmium, selenium, or mercury adversely impacting the sea duck populations
in Alaska. We believe these contaminants were the most logical to evaluate
first. Also, limited evidence (spectacled eider eggs) suggests that organochlorine
pesticides and PCB concentrations were low. The need to further evaluate
organochlorine pesticides and PCBs for the other sea duck species (except
eider) still exist because they winter in bays and estuaries south of Alaska
where these contaminants persist at higher concentrations. The eiders, with
very low organochlorine pesticides and PCBs, do not migrate south of Alaska.
Although all sea ducks generally feed on benthic organisms, the timing and
magnitude of population declines suggest that the cause of decline is not
the same for all species. Sea ducks in general, and scoters in particular,
are the least understood waterfowl in North America. Little biological and
ecological research has been conducted on these species. For example, we
do not know if the nesting and molting scoter populations we sampled are
the same population. To our knowledge, only one detailed nesting study of
scoters has been conducted in North America (55). Nesting is generally
considered one of the weakest links in the life cycle, especially with regard
to contaminant effects. There are potentially many critical points and environmental
exposures in the life history of sea duck species. Because of this lack
of information on these species, particularly movement and migration patterns,
we believe the next step is to focus on a more complete understanding of
their ecology. Such information will help identify critical life stages
and potentially harmful environmental exposures and will allow us to generate
testable hypotheses regarding population declines.
We know that many of the sea duck species are declining, especially spectacled
and Steller's eiders. The USFWS has stewardship responsibilities for these
species in the United States. Additional biological, ecological, and contaminant
research is required for the service to effectively discharge those responsibilities.
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