Ecotoxicology (2014) 23:349–356 DOI 10.1007/s10646-014-1192-z
Blood lead concentrations in Alaskan tundra swans: linking breeding and wintering areas with satellite telemetry Craig R. Ely • J. Christian Franson
Accepted: 7 January 2014 / Published online: 28 January 2014 Ó Springer Science+Business Media New York (outside the USA) 2014
Abstract Tundra swans (Cygnus columbianus) like many waterfowl species are susceptible to lead (Pb) poisoning, and Pb-induced mortality has been reported from many areas of their wintering range. Little is known however about Pb levels throughout the annual cycle of tundra swans, especially during summer when birds are on remote northern breeding areas where they are less likely to be exposed to anthropogenic sources of Pb. Our objective was to document summer Pb levels in tundra swans throughout their breeding range in Alaska to determine if there were population-specific differences in blood Pb concentrations that might pose a threat to swans and to humans that may consume them. We measured blood Pb concentrations in tundra swans at five locations in Alaska, representing birds that winter in both the Pacific Flyway and Atlantic Flyway. We also marked swans at each location with satellite transmitters and coded neck bands, to identify staging and wintering sites and determine if winter site use correlated with summer Pb concentrations. Blood Pb levels were generally low (\0.2 lg/ml) in swans across all breeding areas. Pb levels were lower in cygnets than adults, suggesting that swans were likely exposed to Pb on wintering areas or on return migration to Alaska, rather than on the summer breeding grounds. Blood Pb levels varied significantly across the five breeding areas, with highest concentrations in birds on the North Slope of Alaska (wintering in the Atlantic Flyway), and lowest in birds C. R. Ely (&) Alaska Science Center, U.S. Geological Survey, 4210 University Drive, Anchorage, AK 99508, USA e-mail: [email protected] J. C. Franson National Wildlife Health Center, U.S. Geological Survey, 6006 Schroeder Rd, Madison, WI 53711, USA
from the lower Alaska Peninsula that rarely migrate south for winter. Keywords Alaska Lead Migration Satellite telemetry Subsistence Tundra swan
Introduction Swans (genus Cygnus), like many species of waterfowl, are susceptible to lead (Pb) poisoning (Sanderson and Bellrose 1986; Blus 1994). Pb poisoning mortality in waterfowl, generally characterized by blood Pb concentrations [1.0 lg/ml (Franson and Pain 2011), has historically been most commonly associated with ingestion of Pb from spent shot from shotgun shells (Sanderson and Bellrose 1986). However, swans and other waterbirds may be exposed to toxic levels of Pb from the ingestion of fishing weights and other tackle and when foraging in habitats exposed to sediments contaminated by Pb due to mining and smelting activities (Sears 1988; Blus et al. 1991; Franson et al. 2003). Swans are especially likely to be exposed to waterborne contaminants as they are highly dependent on wetland habitats for foraging and roosting, and wetlands are known to accumulate heavy metals from a variety of sources, including atmospheric deposition and riverine or marine inputs. Tundra swans (Cygnus columbianus) in the Pacific Flyway have long suffered from Pb toxicosis due to ingestion of Pb shot in Washington and British Columbia (Kendall and Driver 1982; Degernes et al. 2006), and exposure to high Pb levels in river sediments downstream from mining and smelting activities in northern Idaho (Blus et al. 1991, 1999; Beyer et al. 2000; Sileo et al. 2001). Tundra swans migrate through northern Idaho primarily during spring, and exposure there is believed to be both
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temporally and geographically restricted because of the migratory habits of the swans. The shot shell-related poisoning in Washington and British Columbia also affects trumpeter swans (Cygnus buccinator), and occurs throughout the winter, when thousands of swans are likely exposed to high concentrations of Pb. Of 1,727 swan carcasses (mainly trumpeter swans) examined from this area during 1999–2008, 1,376 (80 %) of the mortalities were attributed to Pb poisoning (Wilson et al. 2009). Although swan mortality from concentrated point sources of Pb has been well documented, we know little about normal ‘background levels’ of Pb in tundra swans, as most studies have focused on documenting the severity of poisoning of swans associated with morbidity or mortality events, rather than routinely sampling healthy wild birds. A better understanding of baseline Pb levels in wild birds will provide a context for categorizing sub-clinical levels and a more meaningful interpretation of the magnitude of Pb levels in adversely affected swans. Previous investigations of Pb poisoning in migratory waterfowl have primarily focused on wintering birds, but birds may also be exposed to Pb on the breeding grounds. Several species of waterfowl have been reported with elevated blood Pb concentrations in Alaska (Brown et al. 2006), including spectacled eiders (Somateria fischeri) on the Yukon–Kuskokwim (Y–K) Delta (Franson et al. 1995; Flint et al. 1997). In the latter instance mortality associated with the ingestion of Pb shot is thought to have led to a decline in the breeding population (Ely et al. 1994; Flint et al. 1997). Tundra swans on the Y–K Delta may also be exposed to Pb via shot pellets, as they nest sympatrically with, and use many of the same wetlands as spectacled eiders. Documentation of Pb levels in tundra swans in summer is additionally important as they are one of the primary species of birds harvested by subsistence hunters in western Alaska (Wentworth 2004). The degree of exposure to contaminants in migrating birds is undoubtedly related to distribution and habitat use; hence population differences in migratory pathways and winter distribution could lead to differential exposure to contaminants (Lavoie et al. 2012). To explore the possible relationships between blood Pb concentrations and migratory movements, we tracked swans via implanted satellite transmitters and observations of coded neck bands. We were particularly interested whether tundra swans that wintered and staged in areas that have a high incidence of Pb toxicity, such as the Pacific Northwest (WA, ID, BC), were more likely to have higher blood Pb levels during the summer than tundra swans wintering elsewhere in North America. We also wanted to determine whether tundra swans using wintering areas with a history of Pb-related mortality were from a single, or multiple breeding areas.
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Fig. 1 Locations in Alaska where tundra swans were sampled for Pb and implanted with satellite transmitters. Stippled area indicates approximate breeding distribution in Alaska. Dotted line near Point Hope indicates approximate boundary between birds belonging to the Eastern and Western populations
Study area Tundra swans were captured at five different breeding areas in Alaska in 2007 and 2008 (Fig. 1). Our sampling sites encompassed nearly the entire breeding range of tundra swans in Alaska (Bellrose 1980), and include locations on the: (1) lower Alaska Peninsula near Cold Bay; (2) upper Alaska Peninsula (Bristol Bay Lowlands) near King Salmon; (3) Y–K Delta in western Alaska; (4) Kotzebue Sound and Koyukuk River drainage in northwestern Alaska; and (5) the Colville River Delta on the arctic coastal plain of northern Alaska.
Methods Sample collection Molting tundra swans were captured when flightless during July and August. The sex of captured birds was determined based on cloacal characteristics (Bellrose 1980). Birds were determined to be either locals (i.e. cygnets), second year birds (SY; birds hatched the previous year), or after second year birds (ASY). SY birds were distinguished from ASY birds by the presence of grey feathering on their head and neck, and sometimes, backs (Bellrose 1980). At times it was difficult to determine whether the grey coloring on swans was due to feather color or mud; in these cases we also used the smaller lore size of SY birds to make an age
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determination (Dau, unpublished data). Blood was collected via jugular venipuncture with plastic syringes (Becton, Dickinson, Franklin Lakes, NJ) and *4 cc were placed in lithium heparinized evacuated glass tubes (Becton, Dickinson, Franklin Lakes, NJ). Samples were kept in a cooler until transported to a freezer at the end of each day, and later shipped to the National Wildlife Health Center (NWHC) in Madison, Wisconsin USA. We abdominally implanted (Korschgen et al. 1996) ten birds from each breeding location with satellite transmitters using propofol for anesthesia (Machin and Caulkett 2000). The 58 g transmitters (platform transmitting terminals [PTTs]; Microwave Telemetry, Columbia, MD) were used to track the movement of staging and wintering swans relative to where they were marked in Alaska. Although site use was determined after sampling blood Pb concentrations, swans are very highly site faithful and use wintering sites consistently across years (Rees 1987). PTTs were programmed to transmit once every 1–4 days depending on the season and designed to function for 2 years (Ramey et al. 2012). The Argos Data Collection and Location System (CLS America 2007) was used to obtain information on latitude and longitude, date, time, and quality of locations of swans instrumented with PTTs. We filtered unlikely locations based on rate and angle of movement (Douglas 2006) and the highest quality locations were used to represent daily position. We also fitted tundra swans with coded plastic neck bands (Sladen 1973), and received location information on neck-banded birds from a network of cooperators and volunteers, and via reports to the U.S. Geological Survey Bird Banding Laboratory (compiled through June 2012).
The lower level of detection for Pb in blood was 0.02 lg/ml, mean relative percent difference of duplicates was 6.6 %, and the mean recovery from spiked samples and standard reference materials was 94.7 and 97.9 %, respectively.
Animal care and use
We obtained blood samples from 653 adult (SY or ASY) tundra swans in 2007 and 2008 at five different breeding areas in Alaska (Table 1). We also obtained blood samples from 50 pre-fledged cygnets from the Colville River Delta in late August and early September 2007. Because of the difficulty in identifying second year (SY) birds (see ‘‘Methods’’ section), second year birds may be under represented in our analysis and included in the ASY category.
This study was approved by the Institutional Animal Care and Use Committees (IACUC) of the U.S. Fish and Wildlife Service Region 7, and the U.S. Geological Survey (USGS), Alaska Science Center (ASC), under Federal Permit #s MB124771 (2006) and MB789758 (2007–2010), and ASC IACUC permit # 2008–2015 (2009–2010). Blood samples were also collected under the authority of Federal Bird Banding Permit #20022 from the U.S. Department of Interior. Analytical methods Whole heparinized blood was prepared for analysis according to Fernandez and Hilligoss (1982), except that samples were diluted tenfold, rather than fivefold. Pb concentrations were determined at NWHC using a Thermo Jarrell Ash (TJA) model 188 graphite furnace with a TJA DS-2000 autosampler coupled to a TJA Scan-1 atomic absorption spectrophotometer (Thermo Jarrell Ash Corporation, Franklin, MA, USA).
Statistical analysis To determine if blood Pb concentrations were normally distributed we first plotted the raw data, identifying outliers (Minitab 2005), and then log-transformed the data (Helsel 2012). We found the data were not normally distributed, even after a log transformation, so we used nonparametric analyses based on ranks (Sokal and Rohlf 2012; Samuel and Bowers 2000; Helsel 2012). Our a priori assumption was that swans wintering predominantly in the Pacific Northwest would have higher blood levels than birds wintering elsewhere in the Pacific Flyway, so this test was one-tailed (significance level of 0.1); all other tests were two-tailed. We used the Kruskal–Wallis (K–W) test to determine the effects of location, age and sex on blood Pb levels. We followed-up significant K–W tests with paired comparisons using a Mann–Whitney U test with a Bonferroni adjustment based on the number of follow-up tests. Since the lower limit of detection was 0.02 lg Pb/ml blood, we assigned all samples with concentrations B0.02 lg/ml a value of 0.019 lg/ml, and they assumed equal ranks in our nonparametric analysis (Helsel 2012).
Results Capture and sampling
Blood lead concentrations There were no differences in blood Pb concentrations between years (K–W test on ranks; P = 0.094, adjusted for ties), sexes (K–W test on ranks: average ranks F = 323.7, M = 335.7, P = 0.342 adjusted for ties), or between SY or ASY birds (K–W test on ranks: average rank ASY = 321.7, SY = 353.5, P = 0.127 adjusted for ties) so data for age (ASY and SY), sex and year were combined for analysis. Blood Pb levels did vary significantly among sampling locations (K–W test on ranks: average rank
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Table 1 Age and sex of tundra swans sampled for blood lead levels in Alaska, 2007–2008 Location
2007
2008
Female ASY
Male SY
ASY
Total
Female SY
Male
ASY
SY
ASY
SY
Cold Bay
48
7
6
0
23
0
13
5
104a
King Salmon
17
13
9
4
7
2
2
5
62b
Yukon Delta Kotzebue Sound
37 58
2 0
27 30
0 3
28 126
22 20
22 73
4 8
142 320c
0
0
0
0
8
4
10
3
25d
Colville River a
Includes two ASY birds of unknown sex sampled in 2007
b
Includes three ASY birds of unknown sex sampled in 2007
c
Includes one ASY bird of unknown sex and one bird of unknown age and sex sampled in 2008
d
Does not include 50 hatch year birds sampled at the Colville River Delta in 2007—see text
range of locals 0.019–0.031 lg/ml, mean of SY/ ASY = 0.044 lg/ml). Cygnets were sampled 29 August–2 September when they would have been *2 months old. Winter distribution
Fig. 2 Concentration of lead in the blood of adult tundra swans from five different breeding areas in Alaska, 2007–2008. Top and bottom of boxes represent 3rd and 1st quartiles, respectively. Horizontal line through box is median value, top of whisker is the highest datum within 1.5 inter quartile range; asterisks are outliers. Sample sizes are in parentheses
Colville = 523.6, Y–K Delta = 358.0, Kotzebue Sound = 348.4, King Salmon = 277.3, and Cold Bay = 201.0; P \ 0.001; Fig. 2). Blood Pb concentrations were highest in adult birds on the Colville River Delta, even though no individuals sampled there had blood Pb values [0.20 lg/ ml. This was because nearly every adult Colville bird sampled had blood Pb concentrations well above the detectable level (0.02 lg/ml). Four of the birds with the highest Pb levels were from the region of Kotzebue Sound and one was from the Y–K Delta. Birds from King Salmon and Cold Bay had the lowest blood Pb concentrations (Fig. 2). Lead levels in the blood of 2-month old tundra swan cygnets (n = 50) from the Colville Delta in 2007 were significantly lower than that of older birds (SY and ASY) sampled on the Colville Delta in 2008 (K–W rank test: average rank SY/ASY = 63.0, HY = 25.5; P \ 0.001;
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The migration corridors and wintering areas of marked swans differed by capture location, with the exception of swans from the Y–K Delta and Kotzebue Sound region which had nearly identical distributions (Fig. 3). Birds from these two areas migrated down the east side of the Rocky Mountains before stopping in Utah on the way to wintering in the Central Valley of California. Birds from the Colville River Delta migrated east, to the Atlantic Coast, whereas birds from the southern Alaska Peninsula were largely non-migratory. Swans marked on the northern Alaska Peninsula (Bristol Bay Lowlands) migrated predominantly down the west coast of Canada and wintered in the Pacific Northwest, although the southern route of a few birds did overlap with the Y–K Delta/Kotzebue birds. Observations of neck-banded birds in the years following sampling showed a distribution pattern nearly identical to that of the PTT-marked birds.
Discussion Blood Pb concentrations The concentrations of Pb in the blood of swans was quite low in nearly every population (Fig. 2). Only 5 of 653 (0.77 %) tundra swans had blood Pb levels that were high enough to be considered characteristic of exposed birds, or indicative of subclinical poisoning (0.20–0.50 lg/ml), and no swans had Pb levels consistent with clinical poisoning ([0.50 lg/ml; Franson and Pain 2011).
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Fig. 3 Distribution of PTTmarked tundra swans marked in Alaska in 2008. Colored lines depict major migration corridors used from July 2008 to June 2009. Straight dashed line represents approximate division between Western and Eastern populations of tundra swans. Asterisks identify locations of documented occurrences of lead poisoning from spent shot in northern Washington/southern British Columbia (double asterisks—Degernes et al. 2006) and mine effluent in northern Idaho (single asterisks—Blus et al. 1999) (Color figure online)
Geographic variation in Pb concentrations Blood Pb concentrations of swans varied significantly across the five Alaska breeding areas which correlated with the widely divergent wintering areas used by birds from the different sites. The low Pb levels in adult swans from the lower Alaska Peninsula was expected given that most of these birds do not migrate south and therefore may not be as likely to be exposed to Pb as other populations that winter in areas closer to anthropogenic sources of lead. However the low levels of Pb in the blood of birds from the Bristol Bay Lowlands is somewhat surprising given that they winter in the Pacific Northwest (Fig. 3), a region with known Pb exposure and poisoning in swans (Blus 1994). The low blood Pb values in our sample from this region may be related to the fact that Pb poisoning in swans in the Pacific Northwest is reported to be more of an issue for trumpeter swans than tundra swans (Smith et al. 2009). It is also possible that by the time we sampled birds in July and August elevated blood Pb from wintering areas had already declined, or that tundra swans with elevated Pb levels were not fit enough to migrate to Alaska. Possible support for the latter possibility is the death of a PTT-marked King Salmon swan in late April en route to the Alaska Peninsula after stopping for 3 weeks in eastern Washington, a region
near extensive mining operations (Blus et al. 1999). This bird was one of five King Salmon PTT-marked birds that traversed this region during the three springs PTT swans were monitored (2009–2011). The higher levels of Pb in adult swans from the Colville River Delta is especially of interest as these birds winter along the Atlantic coast, primarily in coastal North Carolina and Maryland. In a review of Pb poisoning in swans, Blus (1994) reported that Atlantic coast tundra swans suffered high Pb related mortality, with thousands of birds dying annually in parts of eastern North Carolina in the 1970s. However, there have been few reported cases of Pb poisoning in swans from this region in subsequent decades, likely due to regulations banning the use of Pb shot for waterfowl hunting in 1991 (Management Plan for the Eastern Population of Tundra Swans 2007). Tundra swans wintering in the Chesapeake Bay region could still be exposed to elevated levels of Pb, as heavy metal concentrations in portions of the Bay still remain high (Conrad et al. 2007). The higher blood Pb levels in swans wintering on the east coast could also be related to the nature of the wetlands they use on their long cross-country journey compared to the shorter migration routes of Western Population tundra swans that use wetlands less proximate to urban or industrial areas (Petrie and Wilcox 2003; Ramey
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et al. 2012). The Eastern Population of swans may also have had higher Pb levels because the Colville River Delta is the most human-impacted breeding area in Alaska due to its proximity (\20 km) to the Prudhoe Bay Oil Field, although an earlier study concluded that Pb exposure rates in eiders breeding in the Prudhoe Bay Oil Field were not high enough to be of major concern (Wilson et al. 2004). Our data showing low blood Pb concentrations in cygnets from the Colville River Delta indicates that anthropogenic sources on the breeding grounds may not be contributory. Individual tundra swans from the vicinity of Kotzebue Sound had the highest blood Pb levels, with one bird having 0.40 lg/ml. However many more birds were sampled from Kotzebue Sound than from other regions (Table 1), so a greater range of values would be expected. Migration patterns of Kotzebue Sound and Y–K Delta swans were nearly identical outside Alaska (Fig. 3), so if Pb accumulation is primarily on wintering areas, exposure rates would be expected to be similar between the two areas, as was found. Origin of Pb in sampled swans It is difficult to assess the origin of lead contamination in transitory species without linking stable Pb isotope ratios of blood Pb to a point source (e.g., Tsuji et al. 2008). Concentrations of Pb in the blood of swans in Alaska are seemingly indicative of Pb exposure on wintering and staging areas as opposed to local Pb exposure. Although experimental Pb shot dosing studies typically indicate no shot retention after about 30 days, blood Pb concentrations remain high post exposure for variable lengths of time (Franson et al. 1984; Rodrı´guez et al. 2010). Thus, 27 and 30 days after dosage with 1 No. 4 lead shot pellet, the mean blood Pb concentration was about 0.6 lg/ml in canvasbacks (Aythya valisineria) and 2 lg/ml in mallards (Anas platyrhynchos), respectively (Franson et al. 1984; Rodrı´guez et al. 2010). Furthermore, blood Pb concentrations remained elevated compared to controls for an estimated 48 days in canvasbacks and 120 days in mallards (Franson et al. 1984; Rodrı´guez et al. 2010). However, Pb tends to accumulate in bone over the lifetime of birds and is considered to be relatively immobile [although fluctuations of Pb in bones of laying females are associated with eggshell formation (Franson and Pain 2011)]. Another indication that Pb may persist once ingested is that there is little evidence that eggs and growing feathers are major excretory routes for Pb, as they are for some other metals (Pattee 1984; Scheuhammer 1987). Hence, the Pb levels in birds we sampled in July and August, after egg laying and during the period of wing molt, could still have been reflective of Pb from staging and wintering sites or from areas where swans are harvested by subsistence hunters in May and June rather than local exposure; a conclusion supported by
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the near absence of blood Pb in cygnets on the Colville River Delta. Similarly, DeStefano et al. (1992) examined blood lead levels of Canada geese (Branta canadensis) on their breeding grounds in Canada, and attributed the higher blood lead levels of adults compared to goslings to exposure during previous seasons. Comparison with other species in Alaska In contrast to the high levels of Pb exposure and associated mortalities reported for spectacled eiders on the Y–K Delta (Franson et al. 1995; Flint et al. 1997) blood Pb levels were comparatively low in tundra swans sampled in this region. Although most of the tundra swans we sampled were from inland sites near Bethel as opposed to the more coastal areas where eiders were sampled, blood Pb levels were also low (\0.08 lg/ml) for the few swans (n = 6) sampled near the Kashunuk River where spectacled eiders were studied earlier (Petersen et al. 2011). Brown et al. (2006) found \3 % of Steller’s eiders (Polysticta stelleri) and black scoters (Melanitta americana) sampled during spring and summer in Alaska had been exposed ([0.20 lg/ml) to Pb. Black scoters from that study were sampled during summer on the Y–K Delta at sites more inland than where spectacled eiders were sampled (Brown et al. 2006), and in between our two Y–K Delta sampling locations. Background blood Pb concentrations in swans and potential exposure to humans Swans are good sentinels of ecosystem contamination by Pb, as they feed on submerged aquatic vegetation rooted in wetland sediments where lead may accumulate (Sileo et al. 2001). Our data show that blood Pb concentrations in swans sampled on their breeding grounds in Alaska are generally well below the value of 0.20 lg/ml known to cause physiological effects in waterfowl and some other birds and commonly used as a threshold level for lead exposure (Franson and Pain 2011). Blood concentrations \0.20 lg/ml, sometimes referred to as ‘‘background’’ concentrations, are typically found in birds in environments removed from sources of lead emissions and exposure. However, it is well known that even low levels of Pb affect brain development (Lanphear et al. 2000), and cognitive function in adult humans (Murata et al. 2009) and blood Pb concentrations as low as 0.050 lg/ml adversely affect brain function in children and adolescents (Lanphear et al. 2000). Neurobehavioral deficits have also been noted in herring gull chicks at elevated, but environmentally realistic, Pb exposure levels (Burger and Gochfeld 2005). Reduced brain weight has been reported in studies of lead exposure in young mallards and American kestrels (Falco sparverius) (Hoffman et al. 1985; Douglas-Stroebel et al. 2004).
Blood lead concentrations in Alaskan tundra swans
Mute swans (Cygnus olor) that collided with power lines, cables, or other objects had elevated blood Pb levels (O’Halloran et al. 1989; Kelly and Kelly 2005). Additional research is needed to determine the impacts of low levels of contaminants on long-lived wildlife such as swans, as it is not known whether birds respond similarly to humans in being behaviorally affected by low levels of Pb, and if so, whether there is a concomitant reduction in survival. From a human health perspective, the low blood Pb concentrations in Alaskan tundra swans indicate that the corresponding levels in other tissues (e.g., liver or muscle) should pose little or no threat to consumers. Previous studies reporting elevated Pb concentrations in game harvested with Pb ammunition and elevated blood levels in people that consumed hunter-shot animals (Scheuhammer et al. 1998; Le´vesque et al. 2003; Tsuji et al. 2008; Verbrugge et al. 2009) attributed elevated Pb levels to the ingestion of lead ammunition fragments in edible parts of game, not from eating tissues with elevated lead levels. Hence it is unlikely that consumption of tundra swans poses a health risk to subsistence users unless spent shot is also ingested.
Conclusions Blood Pb levels in tundra swans in Alaska are generally low, and values are lower in cygnets than adults. The winter distribution of tundra swans varies according to breeding site, and differences in blood Pb concentrations across breeding areas is likely influenced by differential exposure on staging and wintering areas. Blood Pb concentrations were lowest in swans from the lower Alaska Peninsula, a population that is only semi-migratory, and highest in birds that breed on the Colville River Delta and winter on the East Coast. The concentration of Pb in the blood of tundra swans in Alaska is low enough as to represent little risk to human consumers. Acknowledgments We are grateful to numerous biologists and veterinarians who assisted in the capture and bleeding of molting tundra swans in Alaska. Laboratory analysis was conducted by D. Finley (USGS). D. Helsel assisted with statistical analysis. Any use of trade, firm, or product names is for descriptive purposes only and does not imply endorsement by the U.S. Government. Earlier versions of the manuscript benefitted from reviews by C. Van Hemert, and J. Pearce, and J. Ackerman. Conflict of interest of interest.
The authors declare that they have no conflict
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C. R. Ely, J. C. Franson Samuel MD, Bowers EF (2000) Lead exposure in American black ducks after implementation of non-toxic shot. J Wildl Manag 64:947–953 Sanderson GC, Bellrose FC (1986) A review of the problem of lead poisoning in waterfowl, vol 4. Illinois Natural History Survey, Champaign. Special Publication, p 34 Scheuhammer AM (1987) The chronic toxicity of aluminum, cadmium, mercury, and lead in birds: a review. Environ Pollut 46:263–295 Scheuhammer AM, Perrault JA, Routhier E, Braune BM, Campbell GD (1998) Elevated lead concentrations in edible portions of game birds harvested with lead shot. Environ Pollut 102: 251–257 Sears J (1988) Regional and seasonal variations in lead poisoning in the mute swan Cygnus olor in relation to the distribution of lead and lead weights, in the Thames area, England. Biol Conserv 46:115–134 Sileo L, Creekmore LH, Audet DJ, Snyder MR, Meteyer CU, Franson JC, Locke LN, Smith MR, Finley DL (2001) Lead poisoning of waterfowl by contaminated sediment in the Coeur d’Alene River. Arch Environ Contam Toxicol 41:364–368 Sladen WJ (1973) A continental study of whistling swans using neck collars. Wildfowl 24:8–14 Smith MC, Davison MA, Schexnider CM, Wilson L, Bohannon J, Grassley JM, Krage DK, Boyd WS, Smith BD, Jordan M, Grue C (2009) Lead shot poisoning in swans: sources of pellets within Whatcom county, WA, USA and Sumas Prairie, BC, Canada. Extended abstract. In: Watson RT, Fuller M, Pokras M, Hunt WG (eds) Ingestion of lead from spent ammunition: implications for wildlife and humans. The Peregrine Fund, Boise. doi:10. 4080/isla.2009.0120 Sokal RR, Rohlf FJ (2012) Biometry, 4th edn. W. H. Freeman, New York Tsuji LJS, Wainman BC, Martin ID, Weber J-P, Sutherland C, Liberda EN, Nieboer E (2008) Elevated blood-lead levels in first nation people of Northern Ontario Canada: policy implications. Bull Environ Contam Toxicol 80:14–18 Verbrugge LA, Wenzel SG, Berner JE, Matz AC (2009) Human exposure to lead from ammunition in the circumpolar north. Extended abstract. In: Watson RT, Fuller M, Pokras M, Hunt WG (eds) Ingestion of lead from spent ammunition: implications for wildlife and humans. The Peregrine Fund, Boise. doi:10. 4080/isla.2009.0110 Wentworth F (2004) Subsistence migratory bird harvest surveys, Yukon–Kuskokwim Delta, 1993–2002, Bristol Bay, 1995–2001. U.S. Fish and Wildlife Service, Anchorage Wilson HM, Petersen MR, Troy D (2004) Concentrations of metals and trace elements in blood of spectacled and king eiders in northern Alaska, USA. Environ Toxicol Chem 23:408–414 Wilson LK, Grigg G, Forsyth R, Tolksdorf M, Bowes V, Smith M, Scheuhammer A (2009) Lead poisoning of trumpeter swans in the Pacific Northwest: can recovered shot help to elucidate the source? Extended abstract. In: Watson RT, Fuller M, Pokras M, Hunt WG (eds) Ingestion of lead from spent ammunition: implications for wildlife and humans, The Peregrine Fund, Boise. doi:10.4080/isla.2009.0120
Blood lead concentrations in Alaskan tundra swans: linking breeding and wintering areas with satellite telemetry Craig R. Ely • J. Christian Franson
Accepted: 7 January 2014 / Published online: 28 January 2014 Ó Springer Science+Business Media New York (outside the USA) 2014
Abstract Tundra swans (Cygnus columbianus) like many waterfowl species are susceptible to lead (Pb) poisoning, and Pb-induced mortality has been reported from many areas of their wintering range. Little is known however about Pb levels throughout the annual cycle of tundra swans, especially during summer when birds are on remote northern breeding areas where they are less likely to be exposed to anthropogenic sources of Pb. Our objective was to document summer Pb levels in tundra swans throughout their breeding range in Alaska to determine if there were population-specific differences in blood Pb concentrations that might pose a threat to swans and to humans that may consume them. We measured blood Pb concentrations in tundra swans at five locations in Alaska, representing birds that winter in both the Pacific Flyway and Atlantic Flyway. We also marked swans at each location with satellite transmitters and coded neck bands, to identify staging and wintering sites and determine if winter site use correlated with summer Pb concentrations. Blood Pb levels were generally low (\0.2 lg/ml) in swans across all breeding areas. Pb levels were lower in cygnets than adults, suggesting that swans were likely exposed to Pb on wintering areas or on return migration to Alaska, rather than on the summer breeding grounds. Blood Pb levels varied significantly across the five breeding areas, with highest concentrations in birds on the North Slope of Alaska (wintering in the Atlantic Flyway), and lowest in birds C. R. Ely (&) Alaska Science Center, U.S. Geological Survey, 4210 University Drive, Anchorage, AK 99508, USA e-mail: [email protected] J. C. Franson National Wildlife Health Center, U.S. Geological Survey, 6006 Schroeder Rd, Madison, WI 53711, USA
from the lower Alaska Peninsula that rarely migrate south for winter. Keywords Alaska Lead Migration Satellite telemetry Subsistence Tundra swan
Introduction Swans (genus Cygnus), like many species of waterfowl, are susceptible to lead (Pb) poisoning (Sanderson and Bellrose 1986; Blus 1994). Pb poisoning mortality in waterfowl, generally characterized by blood Pb concentrations [1.0 lg/ml (Franson and Pain 2011), has historically been most commonly associated with ingestion of Pb from spent shot from shotgun shells (Sanderson and Bellrose 1986). However, swans and other waterbirds may be exposed to toxic levels of Pb from the ingestion of fishing weights and other tackle and when foraging in habitats exposed to sediments contaminated by Pb due to mining and smelting activities (Sears 1988; Blus et al. 1991; Franson et al. 2003). Swans are especially likely to be exposed to waterborne contaminants as they are highly dependent on wetland habitats for foraging and roosting, and wetlands are known to accumulate heavy metals from a variety of sources, including atmospheric deposition and riverine or marine inputs. Tundra swans (Cygnus columbianus) in the Pacific Flyway have long suffered from Pb toxicosis due to ingestion of Pb shot in Washington and British Columbia (Kendall and Driver 1982; Degernes et al. 2006), and exposure to high Pb levels in river sediments downstream from mining and smelting activities in northern Idaho (Blus et al. 1991, 1999; Beyer et al. 2000; Sileo et al. 2001). Tundra swans migrate through northern Idaho primarily during spring, and exposure there is believed to be both
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temporally and geographically restricted because of the migratory habits of the swans. The shot shell-related poisoning in Washington and British Columbia also affects trumpeter swans (Cygnus buccinator), and occurs throughout the winter, when thousands of swans are likely exposed to high concentrations of Pb. Of 1,727 swan carcasses (mainly trumpeter swans) examined from this area during 1999–2008, 1,376 (80 %) of the mortalities were attributed to Pb poisoning (Wilson et al. 2009). Although swan mortality from concentrated point sources of Pb has been well documented, we know little about normal ‘background levels’ of Pb in tundra swans, as most studies have focused on documenting the severity of poisoning of swans associated with morbidity or mortality events, rather than routinely sampling healthy wild birds. A better understanding of baseline Pb levels in wild birds will provide a context for categorizing sub-clinical levels and a more meaningful interpretation of the magnitude of Pb levels in adversely affected swans. Previous investigations of Pb poisoning in migratory waterfowl have primarily focused on wintering birds, but birds may also be exposed to Pb on the breeding grounds. Several species of waterfowl have been reported with elevated blood Pb concentrations in Alaska (Brown et al. 2006), including spectacled eiders (Somateria fischeri) on the Yukon–Kuskokwim (Y–K) Delta (Franson et al. 1995; Flint et al. 1997). In the latter instance mortality associated with the ingestion of Pb shot is thought to have led to a decline in the breeding population (Ely et al. 1994; Flint et al. 1997). Tundra swans on the Y–K Delta may also be exposed to Pb via shot pellets, as they nest sympatrically with, and use many of the same wetlands as spectacled eiders. Documentation of Pb levels in tundra swans in summer is additionally important as they are one of the primary species of birds harvested by subsistence hunters in western Alaska (Wentworth 2004). The degree of exposure to contaminants in migrating birds is undoubtedly related to distribution and habitat use; hence population differences in migratory pathways and winter distribution could lead to differential exposure to contaminants (Lavoie et al. 2012). To explore the possible relationships between blood Pb concentrations and migratory movements, we tracked swans via implanted satellite transmitters and observations of coded neck bands. We were particularly interested whether tundra swans that wintered and staged in areas that have a high incidence of Pb toxicity, such as the Pacific Northwest (WA, ID, BC), were more likely to have higher blood Pb levels during the summer than tundra swans wintering elsewhere in North America. We also wanted to determine whether tundra swans using wintering areas with a history of Pb-related mortality were from a single, or multiple breeding areas.
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Fig. 1 Locations in Alaska where tundra swans were sampled for Pb and implanted with satellite transmitters. Stippled area indicates approximate breeding distribution in Alaska. Dotted line near Point Hope indicates approximate boundary between birds belonging to the Eastern and Western populations
Study area Tundra swans were captured at five different breeding areas in Alaska in 2007 and 2008 (Fig. 1). Our sampling sites encompassed nearly the entire breeding range of tundra swans in Alaska (Bellrose 1980), and include locations on the: (1) lower Alaska Peninsula near Cold Bay; (2) upper Alaska Peninsula (Bristol Bay Lowlands) near King Salmon; (3) Y–K Delta in western Alaska; (4) Kotzebue Sound and Koyukuk River drainage in northwestern Alaska; and (5) the Colville River Delta on the arctic coastal plain of northern Alaska.
Methods Sample collection Molting tundra swans were captured when flightless during July and August. The sex of captured birds was determined based on cloacal characteristics (Bellrose 1980). Birds were determined to be either locals (i.e. cygnets), second year birds (SY; birds hatched the previous year), or after second year birds (ASY). SY birds were distinguished from ASY birds by the presence of grey feathering on their head and neck, and sometimes, backs (Bellrose 1980). At times it was difficult to determine whether the grey coloring on swans was due to feather color or mud; in these cases we also used the smaller lore size of SY birds to make an age
Blood lead concentrations in Alaskan tundra swans
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determination (Dau, unpublished data). Blood was collected via jugular venipuncture with plastic syringes (Becton, Dickinson, Franklin Lakes, NJ) and *4 cc were placed in lithium heparinized evacuated glass tubes (Becton, Dickinson, Franklin Lakes, NJ). Samples were kept in a cooler until transported to a freezer at the end of each day, and later shipped to the National Wildlife Health Center (NWHC) in Madison, Wisconsin USA. We abdominally implanted (Korschgen et al. 1996) ten birds from each breeding location with satellite transmitters using propofol for anesthesia (Machin and Caulkett 2000). The 58 g transmitters (platform transmitting terminals [PTTs]; Microwave Telemetry, Columbia, MD) were used to track the movement of staging and wintering swans relative to where they were marked in Alaska. Although site use was determined after sampling blood Pb concentrations, swans are very highly site faithful and use wintering sites consistently across years (Rees 1987). PTTs were programmed to transmit once every 1–4 days depending on the season and designed to function for 2 years (Ramey et al. 2012). The Argos Data Collection and Location System (CLS America 2007) was used to obtain information on latitude and longitude, date, time, and quality of locations of swans instrumented with PTTs. We filtered unlikely locations based on rate and angle of movement (Douglas 2006) and the highest quality locations were used to represent daily position. We also fitted tundra swans with coded plastic neck bands (Sladen 1973), and received location information on neck-banded birds from a network of cooperators and volunteers, and via reports to the U.S. Geological Survey Bird Banding Laboratory (compiled through June 2012).
The lower level of detection for Pb in blood was 0.02 lg/ml, mean relative percent difference of duplicates was 6.6 %, and the mean recovery from spiked samples and standard reference materials was 94.7 and 97.9 %, respectively.
Animal care and use
We obtained blood samples from 653 adult (SY or ASY) tundra swans in 2007 and 2008 at five different breeding areas in Alaska (Table 1). We also obtained blood samples from 50 pre-fledged cygnets from the Colville River Delta in late August and early September 2007. Because of the difficulty in identifying second year (SY) birds (see ‘‘Methods’’ section), second year birds may be under represented in our analysis and included in the ASY category.
This study was approved by the Institutional Animal Care and Use Committees (IACUC) of the U.S. Fish and Wildlife Service Region 7, and the U.S. Geological Survey (USGS), Alaska Science Center (ASC), under Federal Permit #s MB124771 (2006) and MB789758 (2007–2010), and ASC IACUC permit # 2008–2015 (2009–2010). Blood samples were also collected under the authority of Federal Bird Banding Permit #20022 from the U.S. Department of Interior. Analytical methods Whole heparinized blood was prepared for analysis according to Fernandez and Hilligoss (1982), except that samples were diluted tenfold, rather than fivefold. Pb concentrations were determined at NWHC using a Thermo Jarrell Ash (TJA) model 188 graphite furnace with a TJA DS-2000 autosampler coupled to a TJA Scan-1 atomic absorption spectrophotometer (Thermo Jarrell Ash Corporation, Franklin, MA, USA).
Statistical analysis To determine if blood Pb concentrations were normally distributed we first plotted the raw data, identifying outliers (Minitab 2005), and then log-transformed the data (Helsel 2012). We found the data were not normally distributed, even after a log transformation, so we used nonparametric analyses based on ranks (Sokal and Rohlf 2012; Samuel and Bowers 2000; Helsel 2012). Our a priori assumption was that swans wintering predominantly in the Pacific Northwest would have higher blood levels than birds wintering elsewhere in the Pacific Flyway, so this test was one-tailed (significance level of 0.1); all other tests were two-tailed. We used the Kruskal–Wallis (K–W) test to determine the effects of location, age and sex on blood Pb levels. We followed-up significant K–W tests with paired comparisons using a Mann–Whitney U test with a Bonferroni adjustment based on the number of follow-up tests. Since the lower limit of detection was 0.02 lg Pb/ml blood, we assigned all samples with concentrations B0.02 lg/ml a value of 0.019 lg/ml, and they assumed equal ranks in our nonparametric analysis (Helsel 2012).
Results Capture and sampling
Blood lead concentrations There were no differences in blood Pb concentrations between years (K–W test on ranks; P = 0.094, adjusted for ties), sexes (K–W test on ranks: average ranks F = 323.7, M = 335.7, P = 0.342 adjusted for ties), or between SY or ASY birds (K–W test on ranks: average rank ASY = 321.7, SY = 353.5, P = 0.127 adjusted for ties) so data for age (ASY and SY), sex and year were combined for analysis. Blood Pb levels did vary significantly among sampling locations (K–W test on ranks: average rank
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Table 1 Age and sex of tundra swans sampled for blood lead levels in Alaska, 2007–2008 Location
2007
2008
Female ASY
Male SY
ASY
Total
Female SY
Male
ASY
SY
ASY
SY
Cold Bay
48
7
6
0
23
0
13
5
104a
King Salmon
17
13
9
4
7
2
2
5
62b
Yukon Delta Kotzebue Sound
37 58
2 0
27 30
0 3
28 126
22 20
22 73
4 8
142 320c
0
0
0
0
8
4
10
3
25d
Colville River a
Includes two ASY birds of unknown sex sampled in 2007
b
Includes three ASY birds of unknown sex sampled in 2007
c
Includes one ASY bird of unknown sex and one bird of unknown age and sex sampled in 2008
d
Does not include 50 hatch year birds sampled at the Colville River Delta in 2007—see text
range of locals 0.019–0.031 lg/ml, mean of SY/ ASY = 0.044 lg/ml). Cygnets were sampled 29 August–2 September when they would have been *2 months old. Winter distribution
Fig. 2 Concentration of lead in the blood of adult tundra swans from five different breeding areas in Alaska, 2007–2008. Top and bottom of boxes represent 3rd and 1st quartiles, respectively. Horizontal line through box is median value, top of whisker is the highest datum within 1.5 inter quartile range; asterisks are outliers. Sample sizes are in parentheses
Colville = 523.6, Y–K Delta = 358.0, Kotzebue Sound = 348.4, King Salmon = 277.3, and Cold Bay = 201.0; P \ 0.001; Fig. 2). Blood Pb concentrations were highest in adult birds on the Colville River Delta, even though no individuals sampled there had blood Pb values [0.20 lg/ ml. This was because nearly every adult Colville bird sampled had blood Pb concentrations well above the detectable level (0.02 lg/ml). Four of the birds with the highest Pb levels were from the region of Kotzebue Sound and one was from the Y–K Delta. Birds from King Salmon and Cold Bay had the lowest blood Pb concentrations (Fig. 2). Lead levels in the blood of 2-month old tundra swan cygnets (n = 50) from the Colville Delta in 2007 were significantly lower than that of older birds (SY and ASY) sampled on the Colville Delta in 2008 (K–W rank test: average rank SY/ASY = 63.0, HY = 25.5; P \ 0.001;
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The migration corridors and wintering areas of marked swans differed by capture location, with the exception of swans from the Y–K Delta and Kotzebue Sound region which had nearly identical distributions (Fig. 3). Birds from these two areas migrated down the east side of the Rocky Mountains before stopping in Utah on the way to wintering in the Central Valley of California. Birds from the Colville River Delta migrated east, to the Atlantic Coast, whereas birds from the southern Alaska Peninsula were largely non-migratory. Swans marked on the northern Alaska Peninsula (Bristol Bay Lowlands) migrated predominantly down the west coast of Canada and wintered in the Pacific Northwest, although the southern route of a few birds did overlap with the Y–K Delta/Kotzebue birds. Observations of neck-banded birds in the years following sampling showed a distribution pattern nearly identical to that of the PTT-marked birds.
Discussion Blood Pb concentrations The concentrations of Pb in the blood of swans was quite low in nearly every population (Fig. 2). Only 5 of 653 (0.77 %) tundra swans had blood Pb levels that were high enough to be considered characteristic of exposed birds, or indicative of subclinical poisoning (0.20–0.50 lg/ml), and no swans had Pb levels consistent with clinical poisoning ([0.50 lg/ml; Franson and Pain 2011).
Blood lead concentrations in Alaskan tundra swans
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Fig. 3 Distribution of PTTmarked tundra swans marked in Alaska in 2008. Colored lines depict major migration corridors used from July 2008 to June 2009. Straight dashed line represents approximate division between Western and Eastern populations of tundra swans. Asterisks identify locations of documented occurrences of lead poisoning from spent shot in northern Washington/southern British Columbia (double asterisks—Degernes et al. 2006) and mine effluent in northern Idaho (single asterisks—Blus et al. 1999) (Color figure online)
Geographic variation in Pb concentrations Blood Pb concentrations of swans varied significantly across the five Alaska breeding areas which correlated with the widely divergent wintering areas used by birds from the different sites. The low Pb levels in adult swans from the lower Alaska Peninsula was expected given that most of these birds do not migrate south and therefore may not be as likely to be exposed to Pb as other populations that winter in areas closer to anthropogenic sources of lead. However the low levels of Pb in the blood of birds from the Bristol Bay Lowlands is somewhat surprising given that they winter in the Pacific Northwest (Fig. 3), a region with known Pb exposure and poisoning in swans (Blus 1994). The low blood Pb values in our sample from this region may be related to the fact that Pb poisoning in swans in the Pacific Northwest is reported to be more of an issue for trumpeter swans than tundra swans (Smith et al. 2009). It is also possible that by the time we sampled birds in July and August elevated blood Pb from wintering areas had already declined, or that tundra swans with elevated Pb levels were not fit enough to migrate to Alaska. Possible support for the latter possibility is the death of a PTT-marked King Salmon swan in late April en route to the Alaska Peninsula after stopping for 3 weeks in eastern Washington, a region
near extensive mining operations (Blus et al. 1999). This bird was one of five King Salmon PTT-marked birds that traversed this region during the three springs PTT swans were monitored (2009–2011). The higher levels of Pb in adult swans from the Colville River Delta is especially of interest as these birds winter along the Atlantic coast, primarily in coastal North Carolina and Maryland. In a review of Pb poisoning in swans, Blus (1994) reported that Atlantic coast tundra swans suffered high Pb related mortality, with thousands of birds dying annually in parts of eastern North Carolina in the 1970s. However, there have been few reported cases of Pb poisoning in swans from this region in subsequent decades, likely due to regulations banning the use of Pb shot for waterfowl hunting in 1991 (Management Plan for the Eastern Population of Tundra Swans 2007). Tundra swans wintering in the Chesapeake Bay region could still be exposed to elevated levels of Pb, as heavy metal concentrations in portions of the Bay still remain high (Conrad et al. 2007). The higher blood Pb levels in swans wintering on the east coast could also be related to the nature of the wetlands they use on their long cross-country journey compared to the shorter migration routes of Western Population tundra swans that use wetlands less proximate to urban or industrial areas (Petrie and Wilcox 2003; Ramey
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et al. 2012). The Eastern Population of swans may also have had higher Pb levels because the Colville River Delta is the most human-impacted breeding area in Alaska due to its proximity (\20 km) to the Prudhoe Bay Oil Field, although an earlier study concluded that Pb exposure rates in eiders breeding in the Prudhoe Bay Oil Field were not high enough to be of major concern (Wilson et al. 2004). Our data showing low blood Pb concentrations in cygnets from the Colville River Delta indicates that anthropogenic sources on the breeding grounds may not be contributory. Individual tundra swans from the vicinity of Kotzebue Sound had the highest blood Pb levels, with one bird having 0.40 lg/ml. However many more birds were sampled from Kotzebue Sound than from other regions (Table 1), so a greater range of values would be expected. Migration patterns of Kotzebue Sound and Y–K Delta swans were nearly identical outside Alaska (Fig. 3), so if Pb accumulation is primarily on wintering areas, exposure rates would be expected to be similar between the two areas, as was found. Origin of Pb in sampled swans It is difficult to assess the origin of lead contamination in transitory species without linking stable Pb isotope ratios of blood Pb to a point source (e.g., Tsuji et al. 2008). Concentrations of Pb in the blood of swans in Alaska are seemingly indicative of Pb exposure on wintering and staging areas as opposed to local Pb exposure. Although experimental Pb shot dosing studies typically indicate no shot retention after about 30 days, blood Pb concentrations remain high post exposure for variable lengths of time (Franson et al. 1984; Rodrı´guez et al. 2010). Thus, 27 and 30 days after dosage with 1 No. 4 lead shot pellet, the mean blood Pb concentration was about 0.6 lg/ml in canvasbacks (Aythya valisineria) and 2 lg/ml in mallards (Anas platyrhynchos), respectively (Franson et al. 1984; Rodrı´guez et al. 2010). Furthermore, blood Pb concentrations remained elevated compared to controls for an estimated 48 days in canvasbacks and 120 days in mallards (Franson et al. 1984; Rodrı´guez et al. 2010). However, Pb tends to accumulate in bone over the lifetime of birds and is considered to be relatively immobile [although fluctuations of Pb in bones of laying females are associated with eggshell formation (Franson and Pain 2011)]. Another indication that Pb may persist once ingested is that there is little evidence that eggs and growing feathers are major excretory routes for Pb, as they are for some other metals (Pattee 1984; Scheuhammer 1987). Hence, the Pb levels in birds we sampled in July and August, after egg laying and during the period of wing molt, could still have been reflective of Pb from staging and wintering sites or from areas where swans are harvested by subsistence hunters in May and June rather than local exposure; a conclusion supported by
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the near absence of blood Pb in cygnets on the Colville River Delta. Similarly, DeStefano et al. (1992) examined blood lead levels of Canada geese (Branta canadensis) on their breeding grounds in Canada, and attributed the higher blood lead levels of adults compared to goslings to exposure during previous seasons. Comparison with other species in Alaska In contrast to the high levels of Pb exposure and associated mortalities reported for spectacled eiders on the Y–K Delta (Franson et al. 1995; Flint et al. 1997) blood Pb levels were comparatively low in tundra swans sampled in this region. Although most of the tundra swans we sampled were from inland sites near Bethel as opposed to the more coastal areas where eiders were sampled, blood Pb levels were also low (\0.08 lg/ml) for the few swans (n = 6) sampled near the Kashunuk River where spectacled eiders were studied earlier (Petersen et al. 2011). Brown et al. (2006) found \3 % of Steller’s eiders (Polysticta stelleri) and black scoters (Melanitta americana) sampled during spring and summer in Alaska had been exposed ([0.20 lg/ml) to Pb. Black scoters from that study were sampled during summer on the Y–K Delta at sites more inland than where spectacled eiders were sampled (Brown et al. 2006), and in between our two Y–K Delta sampling locations. Background blood Pb concentrations in swans and potential exposure to humans Swans are good sentinels of ecosystem contamination by Pb, as they feed on submerged aquatic vegetation rooted in wetland sediments where lead may accumulate (Sileo et al. 2001). Our data show that blood Pb concentrations in swans sampled on their breeding grounds in Alaska are generally well below the value of 0.20 lg/ml known to cause physiological effects in waterfowl and some other birds and commonly used as a threshold level for lead exposure (Franson and Pain 2011). Blood concentrations \0.20 lg/ml, sometimes referred to as ‘‘background’’ concentrations, are typically found in birds in environments removed from sources of lead emissions and exposure. However, it is well known that even low levels of Pb affect brain development (Lanphear et al. 2000), and cognitive function in adult humans (Murata et al. 2009) and blood Pb concentrations as low as 0.050 lg/ml adversely affect brain function in children and adolescents (Lanphear et al. 2000). Neurobehavioral deficits have also been noted in herring gull chicks at elevated, but environmentally realistic, Pb exposure levels (Burger and Gochfeld 2005). Reduced brain weight has been reported in studies of lead exposure in young mallards and American kestrels (Falco sparverius) (Hoffman et al. 1985; Douglas-Stroebel et al. 2004).
Blood lead concentrations in Alaskan tundra swans
Mute swans (Cygnus olor) that collided with power lines, cables, or other objects had elevated blood Pb levels (O’Halloran et al. 1989; Kelly and Kelly 2005). Additional research is needed to determine the impacts of low levels of contaminants on long-lived wildlife such as swans, as it is not known whether birds respond similarly to humans in being behaviorally affected by low levels of Pb, and if so, whether there is a concomitant reduction in survival. From a human health perspective, the low blood Pb concentrations in Alaskan tundra swans indicate that the corresponding levels in other tissues (e.g., liver or muscle) should pose little or no threat to consumers. Previous studies reporting elevated Pb concentrations in game harvested with Pb ammunition and elevated blood levels in people that consumed hunter-shot animals (Scheuhammer et al. 1998; Le´vesque et al. 2003; Tsuji et al. 2008; Verbrugge et al. 2009) attributed elevated Pb levels to the ingestion of lead ammunition fragments in edible parts of game, not from eating tissues with elevated lead levels. Hence it is unlikely that consumption of tundra swans poses a health risk to subsistence users unless spent shot is also ingested.
Conclusions Blood Pb levels in tundra swans in Alaska are generally low, and values are lower in cygnets than adults. The winter distribution of tundra swans varies according to breeding site, and differences in blood Pb concentrations across breeding areas is likely influenced by differential exposure on staging and wintering areas. Blood Pb concentrations were lowest in swans from the lower Alaska Peninsula, a population that is only semi-migratory, and highest in birds that breed on the Colville River Delta and winter on the East Coast. The concentration of Pb in the blood of tundra swans in Alaska is low enough as to represent little risk to human consumers. Acknowledgments We are grateful to numerous biologists and veterinarians who assisted in the capture and bleeding of molting tundra swans in Alaska. Laboratory analysis was conducted by D. Finley (USGS). D. Helsel assisted with statistical analysis. Any use of trade, firm, or product names is for descriptive purposes only and does not imply endorsement by the U.S. Government. Earlier versions of the manuscript benefitted from reviews by C. Van Hemert, and J. Pearce, and J. Ackerman. Conflict of interest of interest.
The authors declare that they have no conflict
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