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Lead Exposure in Bald Eagles from Big Game Hunting,
the Continental Implications and Successful Mitigation
Efforts
Bryan Bedrosian*, Derek Craighead, Ross Crandall
Craighead Beringia South, Kelly, Wyoming, United States of America
Abstract
Studies suggest hunter discarded viscera of big game animals (i.e., offal) is a source of lead available to scavengers. We
investigated the incidence of lead exposure in bald eagles in Wyoming during the big game hunting season, the influx of
eagles into our study area during the hunt, the geographic origins of eagles exposed to lead, and the efficacy of using non-
lead rifle ammunition to reduce lead in eagles. We tested 81 blood samples from bald eagles before, during and after the
big game hunting seasons in 2005–2010, excluding 2008, and found eagles had significantly higher lead levels during the
hunt. We found 24% of eagles tested had levels indicating at least clinical exposure (.60 ug/dL) during the hunt while no
birds did during the non-hunting seasons. We performed driving surveys from 2009–2010 to measure eagle abundance and
found evidence to suggest that eagles are attracted to the study area during the hunt. We fitted 10 eagles with satellite
transmitters captured during the hunt and all migrated south after the cessation of the hunt. One returned to our study area
while the remaining nine traveled north to summer/breed in Canada. The following fall, 80% returned to our study area for
the hunting season, indicating that offal provides a seasonal attractant for eagles. We fitted three local breeding eagles with
satellite transmitters and none left their breeding territories to feed on offal during the hunt, indicating that lead ingestion
may be affecting migrants to a greater degree. During the 2009 and 2010 hunting seasons we provided non-lead rifle
ammunition to local hunters and recorded that 24% and 31% of successful hunters used non-lead ammunition, respectively.
We found the use of non-lead ammunition significantly reduced lead exposure in eagles, suggesting this is a viable solution
to reduce lead exposure in eagles.
Citation: Bedrosian B, Craighead D, Crandall R (2012) Lead Exposure in Bald Eagles from Big Game Hunting, the Continental Implications and Successful
Mitigation Efforts. PLoS ONE 7(12): e51978. doi:10.1371/journal.pone.0051978
Editor: Christopher James Johnson, USGS National Wildlife Health Center, United States of America
Received January 2, 2012; Accepted November 14, 2012; Published December 19, 2012
Copyright: ß2012 Bedrosian et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits
unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Funding: Funding was provided by 1% for the Tetons, Engelhard Foundation, Community Foundation of Jackson Hole, the Hewlett Foundation, the Peregrine
Fund, the Packard Foundation, R. and L. Haberfeld, Y. and M. Chouinard, A. and B. Hirschfield, H. Luther, G. Ordway, and P. Van Roijen. The funders had no role in
study design, data collection and analysis, decision to publish, or preparation of the manuscript.
Competing Interests: The authors have declared that no competing interests exist.
* E-mail: bryan@beringiasouth.org
Introduction
Lead exposure in terrestrial birds has received much attention in
recent years both in North America and Europe (for reviews, see
[1], [2]). There are studies that describe lead fragmentation of rifle
bullets in the carcasses and offal (i.e., gut piles) of ground squirrels
(Spermophilus richardsonii), prairie dogs (Cynomys ludovicianus), deer
(Odocioleus spp.), roe deer (Capreolus capreolus), elk, fallow deer, and
red deer (Cervus spp), [3–7], and all make the argument that these
lead fragments pose a hazard to scavenging species. Several studies
have focused on lead ingestion of rifle bullet fragments in the
critically endangered California Condors (Gymnogyps californianus)
because of the large percentage of free-flying condors that have
symptoms of and/or have died from lead poisoning (e.g., [8–10]).
There is isotopic evidence that the majority of lead ingested by
condors originates from spent rifle bullets in offal and shot big
game un-retrieved by hunters [8], thus substantiating the earlier
suppositions that avian scavengers can incur lead poisoning from
big game hunting practices [11–13], [7]. Similarly, Common
Ravens (Corvus corax) and Turkey Vultures (Cathartes aura) have
significantly higher blood lead levels during big game hunting
seasons than non-hunting periods [6], [14], [15] offering further
evidence that lead ingestion from offal poses a risk to all avian
scavengers.
There have been several studies on lead exposure in eagles
across North America. The incidence of lead ingestion in both
bald eagles (Haliaeetus leucocephalus) and golden eagles (Aquila
chrysaetos) did not change after the ban of lead shot for waterfowl
hunting [16], suggesting offal as an alternate source of lead
exposure. Two studies [13], [17] both found high incidence of lead
poisoning in eagles and found that the times and areas of high
exposure were not correlated to waterfowl hunting for both the
western US and the Great Plains. Both studies suggested that big
game hunting may be a significant source of dietary lead exposure
for eagles. A spatial-temporal association with lead exposure and
big game hunting seasons has been found for both bald and golden
eagles in California, the Pacific Northwest, and the Midwest, [12],
[18], [19], respectively. Most recently, bald eagle admission to
rehabilitation facilities in the Midwest have indicated a positive
relationship of lead exposure to the rifle hunting season and zones
from 1996–2009 as well as a correlation between lead and copper
exposure in the eagles, further suggesting big-game hunting
ammunition as the source [20]. While all of these studies on lead
exposure in eagles support the hypothesis that big game hunting is
PLOS ONE | www.plosone.org 1 December 2012 | Volume 7 | Issue 12 | e51978
a significant source of lead exposure for eagles, the data are
correlative. No experimental data exist to determine if reducing
the amount of lead ammunition used reduces lead exposure in
eagles.
Few studies have examined blood lead levels of live, free-
ranging eagles. Lead exposure has been found in 36% of 162
golden eagles sampled year-round [12], but the majority of
exposure occurred during the deer hunting season. Eighty-six
percent of migrant bald eagles in Montana (n = 37) were found
with elevated lead levels [21], but there was a lower exposure rate
for migrant golden eagles (56%; n = 86). Bald eagles sampled from
two different sites in Saskatchewan and Montana during the
autumn had 18% and 8% exposure rates [13] (n = 97 and 81,
respectively). Golden eagles sampled from recent years in
California were found with a 77% lead exposure rate that
dropped to 37% following lead rifle ammunition regulation [22].
Most recently, free-ranging bald eagles captured in southwest
Montana had significantly higher lead exposure rates in the fall
than birds sampled in winter and spring [23]. This study also
found eagles sampled in recent years had higher lead loads than
eagles sampled after the ban of lead shotgun ammunition for
waterfowl hunting, further suggesting lead exposure is likely from
rifle ammunition sources.
Recent legislation in California banning the use of non-lead rifle
ammunition in the range of the California condor is estimated by
the CA Fish and Game Commission to have 80–95% compliance.
This appears to be successful in reducing the incidence of lead
ingestion by some avian scavengers [22], but not condors [24].
Similarly, a voluntary non-lead bullet program has been in place
since 2005 in the Kaibab Plateau of Arizona’s condor range and
compliance is estimated at 85% [25] but condor deaths from lead
ingestion continues ([26], C. Parish pers. comm.). This lack of
response from condor populations is because of the large home
ranges of condors, due to the temporal variation in their food
sources, and the difficulties in controlling for recreational and
predator hunting in field studies [27]. However, this lack of
response means that more evidence is needed to convince the
general public that non-lead programs can be effective in reducing
deaths from lead ingestion in scavenging species such as condors
and eagles.
To examine the relationship between lead ammunition and bald
eagles, we were interested in addressing the following questions: 1)
are bald eagles in the upper Snake River ecosystem being exposed
to lead at a higher rate during (or as a result of) the local hunting
season 2) can bald eagle blood lead levels be reduced by increasing
the amount of non-lead ammunition used by hunters. To address
these questions, we sampled blood lead levels of eagles before,
during, and after annual big game hunts and nestling bald eagles
within this area as a control. We investigated the spatial and
temporal exposure risks by satellite tracking eagles and performing
regular driving surveys to measure eagle abundance within our
study area. To test if lead exposure in bald eagles can be reduced
by using non-lead rifle ammunition alternatives, we provided
hunters with free or discounted non-lead ammunition (ammuni-
tion with copper or gilding metal bullets) and surveyed the
proportion of successful hunters using non-lead for two years.
Using these data, we modeled the lead levels of bald eagles during
this time period to investigate the efficacy of our program.
Materials and Methods
Ethics Statement
Animal capture, handling, and sampling protocols were covered
under federal and state permits (U.S. Geological Survey bird
banding permit #22637; National Park Service scientific collect-
ing permit #GRTE SCI-003; US Dept. of Interior – National Elk
Refuge Station #61550, Permit #11-06; Wyoming Game and
Fish Department scientific collecting permit #293). The study was
approved by the Craighead Beringia South Institutional Animal
Care and Use Committee (protocol #CBS04-005-01).
Study Area
Eagles were studied and captured within the Jackson Hole
valley of northwestern Wyoming (43u919N, 110u409W). Jackson
Hole is an inter-mountain valley (elevation of the valley floor
approx. 2300 m) and comprises the headwaters of the Snake River
drainage. The valley is composed of mainly public lands including
Grand Teton National Park, the National Elk Refuge, and 3
wilderness areas in the surrounding 4 national forests (Bridger-
Teton, Targhee, Caribou, and Shoshone). Elk, deer, moose, and
bison (Bison bison) hunting occurs annually within the valley and
most hunters leave offal from their kills in the field (see [6] for a
detailed description). Hunting for elk and bison is permitted on the
National Elk Refuge and Grand Teton National Park has an elk
reduction program. There are roughly 3000 big game animals
harvested annually within and directly surrounding the study area
[6]. The big game hunting seasons for elk began the second
weekend in September and ended the second weekend in
December. Little to no recreational or predator hunting occurs
outside of the big game hunting season due to the protection
afforded by the national park and refuge.
Capture and Handling
Eagles were captured during and after the hunting seasons using
net launchers (CODA Ent., Mesa, AZ and Trapping Innovations,
LLC, Kelly, WY). Eagles were baited with road-killed carrion or
with existing gut piles opportunistically found in the study area.
We captured eagles during the hunting seasons of 2005–07 and
2009–2010 (N = 5, 22, 9, 12, and 7, respectively) and post-hunt in
2007–08 (N = 7 and 4, respectively). Resident eagles were captured
pre-hunt in 2010 (N = 7) using a floating noose fish [28] on the
Snake River in Jackson Hole. Blood samples from nestlings (N = 8)
were taken in cooperation with Grand Teton National Park and
A. Harmata (Montana State University) within the Jackson Hole
valley during the 2006 nesting season.
Once captured, each eagle received a United States Geological
Survey band, was aged, measured, and 2.5 cc of blood was drawn
from the brachial vein. Bald Eagles were aged up to six years-old
[29] and sex was determined using bill depth and mass [30]. A
large portion of the blood sample (2.0 cc) was placed in EDTA
storage tubes (Becton, Dickinson, and Company, Kranklin Lakes,
NJ) for analysis of blood lead levels (BLL) by inductively coupled
plasma mass spectrometry (ICMPS) by the Diagnostic Center for
Population and Animal Health (Michigan State University,
Lansing, MI). The lower detection level for blood lead levels via
ICPMS was 0.1 ug/dL. The remainder of the blood sample was
stored in lysis buffer [31] for later DNA analysis. Blood samples
from recaptures (n = 2) collected at least three weeks apart were
considered independent samples because the lead depuration rate
for birds is approximately three weeks [32], [6]. We also confirmed
this depuration rate by holding one sub-adult bald eagle with toxic
levels for 17 d during which time its’ BLL dropped from 113 ug/
dL to below 25 ug/dL. Because of this depuration rate, we did not
collect blood samples from mid-December through early-January
to prevent ambiguity in the hunting and post-hunting season
comparison.
Lead Exposure in Bald Eagles from Rifle Ammunition
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Non-Lead Ammunition Program
During the hunting season in 2009 we gave away free non-lead
ammunition to hunters in Grand Teton National Park and the
National Elk Refuge and in 2010 we sold this ammunition at a
discount to all hunters in the Jackson Hole region. We purchased
FederalHammunition packed with BarnesHTSX or TTSX
bullets, WinchesterHE-tip, and HornadyHGMX ammunition
from Cabela’s IncHfor our distribution program. We collected
survey information from Grand Teton National Park and the
National Elk Refuge in all years to determine the number of elk
harvested and the number of successful hunters using lead and
non-lead ammunition. All successful Park and Refuge elk hunters
are required to turn in a hunting survey. Because bison hunters are
not required to turn in a hunt survey, we extrapolated the annual
percentage of elk hunters using non-lead ammunition to the total
bison harvest within the National Elk Refuge (bison hunting is not
allowed in Grand Teton National Park).
Satellite Tracking
During the 2009/10 hunting season we fit 10 eagles, 9 migrant
and one local, with 65 g satellite platform terminal transmitters
(PTTs; Wildlife Computers) using a backpack style harness with
Teflon ribbon and breakaway stitching [33]. During the summer
of 2010 we fit 3 additional local breeding eagles to determine their
seasonal movements. We reduced the dataset to location accuracy
class 3-1 [34] and analyzed the locations in ArcMap 9.3.
Driving Surveys
From August 2009 through March 2011, we performed 126
driving surveys for all corvids and raptors across our study area
[35]. Surveys were performed only to detect seasonal abundance
shifts within the study area as they relate to the big game hunting
season and not density of the species being counted due to several
potential biases that exist in raptor road counts [35], such as
monitoring only from roads and distribution of elk kills during the
hunting season. Weekly surveys were performed seven weeks
before and after the hunting season and for the 10 and 11 weeks
during each of the hunting seasons in 2009 and 2010, respectively.
Surveys were performed bi-weekly during the spring and summer
(mid-February through mid-August). We surveyed two different
routes (14.5 km and 17.1 km) that bisected our study area on each
survey day for a total of 63 repetitions per transect (Figure 1).
Routes were chosen to minimize paralleling power lines because of
a potential for bias for perching raptors, such as eagles. Driving
speed was maintained at 32 km/hr. A team of 2 authors
performed the surveys. We alternated starting points to reduce
potential time-of-day bias and we recorded species, age, distance
to the bird, height of the bird (when first sighted), activity (i.e.,
perched, flying, feeding, and aggregation) and if it was perched on
a power pole.
Data Analysis
D’Agostino-Pearson normality tests indicated that the blood
lead level data were right skewed (P,0.001), so we log transformed
the data to achieve a normal distribution (P = 0.378) and used
those data in parametric tests. We first tested for differences
between age and sex since these variables have influenced lead
exposure in other species [36], [6]. We categorized age into adult
(.5 yrs.) and sub-adult (0–5 yrs.) and tested for a difference
between categories of both age and sex using t-tests. To examine
potential differences between hunting and non-hunting seasons,
we excluded nestling samples and used a generalized linear mixed
model test using blood lead level as the dependent variable and
age class, hunt vs non-hunting season, year captured and gender as
independent variables with capture date as the random-effects
variable. Following the mixed-effects model, we tested for
differences between years of any significant factors using an
ANVOA. We tested the difference in blood lead levels between the
hunting seasons, non-hunting seasons, and nestling lead levels
using an ANOVA with post-hoc t-test comparisons. We also tested
the proportion of samples during the hunting and non-hunting
seasons in lead exposure categories (background, sub-clinical,
clinical, and acute exposure) versus expected using a chi-square
test.
We were interested in the relative abundance (not density) of
eagles within our study area to determine if there was an influx of
eagles during the hunting season, so we analyzed the survey data
using eagles detected/km. We combined survey data from all non-
hunting season surveys (pre and post 2009 and 2010 hunting
seasons, N = 42) into one non-hunt abundance sample. We also
combined data from both 2009 and 2010 hunts (N = 21) for a
hunting season abundance measure. We tested for differences in
abundance between the hunting and non-hunting seasons using a
Mann-Whitney test because both datasets exhibited non-normal
distributions.
We used linear mixed-effects models to examine the relation-
ships between eagle lead levels, harvest, age and sex using capture
date as a random effect. The total number of harvested game
annually can influence annual blood lead levels of scavenger
populations [14], so it is important to adjust for the annual harvest
rate when comparing between-year variation in blood lead levels.
To test the efficacy of our non-lead program on reducing lead
ingestion rates in 2009 and 2010 compared to earlier years, we
assessed model fit of mean annual log-transformed lead levels
between the total elk and bison harvest and total harvest from
hunters using lead ammunition only (discounting the non-lead
ammunition harvest). We predicted that if the annual mean
population lead level was directly related to the amount of lead
ammunition used by hunters (i.e., more lead ammunition = higher
lead levels), then the models including the lead ammunition only
would have a better fit than the models using total harvest (lead
and non-lead harvest combined). We evaluated sex proportion and
eagle age structure (as a binary variables; adult and non-adult) to
determine if they improved model fit for both harvest models. We
used Pearson’s goodness-of-fit coefficients to assess relationship
between explanatory variables and blood lead levels. We used
Akiake’s information criterion (DAIC) [37] to choose top models
describing the relationship between our chosen variables and
blood lead levels to determine if our non-lead program decreased
eagle lead levels (i.e., the lead-only harvest model had a better fit
relative to the model using total harvest rate).
Results
We tested 81 blood samples for blood lead concentrations from
71 free-flying eagles, including two recaptures .3 weeks after
initial capture and 8 nestlings (Table 1). Based on the background
exposure level criterion of 10 ug/dL [15] and sub-clinical, clinical,
and acute levels [38] we found 93% (N = 68) of all non-nestling
eagles tested had been exposed to lead. Thirty-three percent of
samples (N = 14) exhibited at least clinical lead exposure (.60 ug/
dL) and all were sampled during the hunting season. All nestling’s
sampled (N = 8) were below 1.0 ug/dL (Table 2) and one nestling
had blood lead levels below the detectability threshold.
In 2009, we distributed one free box of non-lead ammunition
from 14 different caliber rifles to a total of 194 hunters from Grand
Teton National Park (GTNP) and the National Elk Refuge (NER).
Lead Exposure in Bald Eagles from Rifle Ammunition
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All successful hunters in GTNP and all hunters on the NER
(whether successful or not) are required to turn in hunt surveys. In
2009, 24.5% of successful hunters (n = 331) in GTNP and 34% in
the NER (n = 143) used non-lead ammunition for their hunt.
Combining both hunt areas, a total of 24% of all successful hunters
used non-lead ammunition in 2009. In 2010, we sold non-lead
ammunition at a reduced rate to hunters. That year, a total of
31% of hunters in GTNP (n = 340) and 33% of hunters on the
NER (n = 221) indicated they used non-lead for their successful
harvest. Figure 2.
We found no difference in lead levels by sex (t = 21.56,
P = 0.12) or age (t = 1.41; P = 0.16), so we pooled those data for the
remainder of the analyses. We found that blood lead levels were
higher during the hunting season than outside the hunting season
(z = 3.06, P = 0.002) while no other variable tested (age, year
captured, and sex) had a significant effect on lead levels (all
P.0.3). We found that neither hunting nor non-hunting seasons
were significantly different between sampling years (P = 0.373 and
0.396, respectively). Nestlings had lower levels of lead than non-
nestlings tested during the non-hunting season (t = 10.68,
P,0.001) and eagles sampled during the non-hunting seasons
had lower lead levels than those tested during the hunting season
(t = 24.65, P,0.001). We found that eagles had lead levels lower
than expected during the non-hunting season and higher than
expected during the hunt (P,0.001) (Table 2).
We found some evidence to suggest that there was an increase in
the abundance of eagles within our study area during the hunting
seasons as compared to the non-hunting seasons (W = 1265.5,
P = 0.06). From our driving surveys, we found an average of 0.09
eagles/km during the non-hunting seasons (range = 0–0.85 eagles/
km; SD = 0.17) and 0.28 eagles/km during the hunting season
(range = 0–1.63 eagles/km; SD = 0.43).
Nine of 10 tagged eagles migrated from the study area after the
cessation of the hunting season. The majority (n = 6) wintered in
Figure 1. Study area with eagle count transects. Boundary (red) and land ownership of the study area. Eagle count transects outlined in black.
The majority of elk harvest in Grand Teton National Park occurs within the study area boundary and the study area includes all hunt zones on the
National Elk Refuge.
doi:10.1371/journal.pone.0051978.g001
Table 1. Blood lead level (mg/dL) descriptive statistics for bald
eagles in Jackson Hole, Wyoming, USA (2005–2007, 2009–10).
n
mean SE median range
Nestling Controls 8 0.29 0.09 0.25 non-detect - 0.8
All Non-Nestlings 73 77.73 13.94 40 2.0–717.9
Non-Hunting Season 18 23.03 3.76 21.4 2.0–53.7
Hunting Season 55 95.63 17.84 55.9 4.3–717.9
doi:10.1371/journal.pone.0051978.t001
Lead Exposure in Bald Eagles from Rifle Ammunition
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Utah, one each in Montana, Arizona, and Colorado (Figure 2).
Almost all of the eagles (n = 9) summered in central Canada while
one sub-adult summered in the vicinity of our study area (Figure 3).
While in Canada, 4 transmitters stopped working, fell off or the
eagle died (unknown since unrecovered) which left 5 functioning
transmitters. During the fall migration in 2010, four of the five
eagles returned directly to our study area stopping for no more
than two days at a time. Once in the study area, they remained for
the entire hunting season before continuing their southerly
migration [Figure 4]. We fit three adult, breeding eagles within
the study area with PTT transmitters during the late summer of
2010 to assess their movement during the hunting season. The
Table 2. Percentage and number (N) of bald eagle samples in four exposure categories captured between November – January in
Jackson Hole, Wyoming, USA from 2005–07, 2009–10.
Background
Sub-Clinical
Exposure
Clinical
Exposure
Acute
Exposure
,
10 ug/dL 10–59 ug/dL 60–100 ug/dL
.
100 ug/dL
Nestlings 100 (8) 0 0 0
All non-nestlings 7 (5) 60 (44) 14 (10) 19 (14)
Non-Hunting Season 22 (4) 78 (14) 0 0
Hunting Season 2 (1) 55 (30) 18 (10) 25 (14)
Blood lead levels ,10 mg/dL = background, 10–59 mg/dL = exposed, 60–99 mg/dL = clinically affected, and .100= acute lead exposure (guidelines based on Redig 1984
and Kelly et al. 2011).
doi:10.1371/journal.pone.0051978.t002
Figure 2. Big game harvest and eagle blood lead levels. Total big game harvest (lead and non-lead) by year (black bars, 2005–2008, 2009–
2010) and harvest of big game using only lead-based ammunition (white bars) in Jackson Hole, Wyoming. Log transformed mean seasonal blood lead
levels of bald eagles (gray line). Note the x-axis is not time contiguous since eagles were not sampled during the 2008 hunting season.
doi:10.1371/journal.pone.0051978.g002
Lead Exposure in Bald Eagles from Rifle Ammunition
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average distance from these nests to the nearest hunt zone was
2.3 km (range 1.55–2.83). None of these three individuals left their
breeding areas (ca. 55 km
2
) along the Snake River during the
hunting season.
Our models suggest that the total amount of elk and bison
harvested with non-lead bullets influenced the mean annual lead
level (Table 3, Figure 3). The model fit improved when we used
the harvest rate with only animals taken using lead ammunition
Figure 3. Summer and wintering locations of bald eagles. Winter (2009–2010) and summer locations (2010) of 10 bald eagles fitted with
satellite transmitters during the 2009 big game hunting season in Jackson Hole, Wyoming.
doi:10.1371/journal.pone.0051978.g003
Lead Exposure in Bald Eagles from Rifle Ammunition
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Figure 4. Bald eagle fall migration routes. Fall migratory (August 2010– January 2011) routes of bald eagles captured the previous fall (2009) in
Jackson Hole, Wyoming. Four of the five eagles returned to Jackson Hole during the big game hunting season a year after being tagged.
doi:10.1371/journal.pone.0051978.g004
Lead Exposure in Bald Eagles from Rifle Ammunition
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(total harvest – non-lead harvest), as compared to the model using
the total harvest (lead harvest+non-lead harvest). There was no
relationship between mean lead levels and total harvest across
years (P = 0.661, se = .001, coef. ,0.001). However, we did find
that the mean annual lead level of eagles was related to the level of
lead-only harvest (total harvest – non-lead harvest; P = 0.035,
se = .001, coef. = 0.002). Neither sex nor age composition helped
improve the model fit for either the total harvest or lead-only
harvest models.
Discussion
Most studies on lead ingestion in scavengers have focused on
spatial (i.e., hunting zones) or temporal (i.e., hunting seasons)
correlations with lead levels or deaths caused by lead poisoning.
Our data suggest a causative relationship between lead rifle
ammunition use and lead ingestion in bald eagles. Our study area
is devoid of other potential sources of lead ingestion by bald eagles,
thereby making it possible to experimentally reduce the potential
of lead ingestion by eagles. Because of the protection afforded by
the National Elk Refuge and the National Park Service, there is no
recreational varmint or predator shooting and no waterfowl or
upland game hunting is permitted. Fishing with live bait is also
prohibited in the study area, reducing the possibility of the use of
lead-based fishing tackle by anglers. Further reducing the
possibility of lead exposure through angling is the fact that all
sport fish within the study area are in the Salmonidae family, which
are almost always fished for using non-lead based tackle (i.e., fly-
fishing) and virtually no fishing exists during the big-game hunting
season due to ice formation on the lakes and rivers within the study
area. In our study area, almost all hunters field dress their harvest
and leave the gutpile (both thoracic and abdominal organs) at the
site of the kill, making it available to scavengers. Thus, by reducing
lead ammunition in our study area, we were able to experimen-
tally reduce lead exposure in bald eagles. Our models of lead
ingestion in the bald eagle populations of northwestern Wyoming
before and after non-lead ammunition was promoted, indicate that
lead exposure in eagles can be effectively reduced through the use
of non-lead bullets.
Our study area was unique in that for many years it has
supported large and concentrated elk and bison herds [39].
Roughly 3,000 elk are harvested within our study area each fall
between mid-October and mid-December [6], making a consistent
and long-time source of carrion for eagles, not unlike a salmon
spawning stream. Our road surveys and satellite tracking data
indicate a temporal and spatial shift of eagles into our study area
each fall in response to this food source. Bald eagles typically
forage and exhibit linear movement patterns associated with rivers
and creeks during the summer months within our study area [40].
Our surveys were completed from the roadway with only a portion
closely paralleling riparian corridors (Figure 1) so we cannot
determine if there was less use of river corridors during the hunting
season. However, the data clearly indicate greater eagle use of
non-riparian habitats during the big-game hunting season in
response to the distribution of offal across the study area.
The local population of breeding bald eagles within our study
has been stable (S. Patla, WY Game & Fish Dept., pers. comm.).
Fall and winter use areas for the resident eagles were small in
comparison to the migrant birds that used the study area in its
entirety. The resident use areas were centered along the Snake
River near their nest sites where we presume the birds continued
to feed primarily on fish and waterfowl. This supposition is also
supported by the lack of lead detected in local, nestling bald eagles
(Table 2). The big game hunting season in our study area does not
overlap the nesting period for bald eagles so the resident adults are
likely foraging on food sources not contaminated with lead, such as
fish, and feeding the nestlings those prey. It remains unknown if
adults mobilize lead stored in bone during egg production since
lead can replace calcium reserves in bone [41]. Since blood lead
levels only reflect ingestion within the previous two weeks [6] and
the eaglets were tested well after hatching, our results cannot help
elucidate that theory but do indicate that breeding adults are
foraging on prey with little to no lead contamination.
In our study, most satellite tracked migrants returned to central
Canada for the spring and summer and returned the following
year to Jackson Hole during the hunting season (Figure 4). While
we have no information about the health of northern breeding
populations, it is germane that lead and its toxic effects are
cumulative from year to year [42].
While there is no consensus on background or lethal concen-
trations of lead for most raptors, most researchers consider a blood
concentration .100 ug/dL to indicate acute poisoning. We
measured a blood lead concentration of 717 ug/dL in an eagle
that subsequently migrated south to Colorado and then north to
Northwest Territories, Canada. While several eagles have been
found dead with confirmed lead poisoning (liver lead concentra-
tions .6 ppm ww) during the hunting season within our study
area (S. Patla pers. comm.), it appears there is large variation
among individuals in the amount of lead that can be tolerated. We
did not detect any clinical signs of lead toxicity in captured eagles.
Eagles were only handled for a short amount of time during a
period of induced stress due to capture and handling so clinical
signs of lead intoxication may have been overlooked. Our tracking
data coupled with high lead burdens indicates more studies need
to be conducted on lethal levels and lead burdens that can be
tolerated by this species. Cumulative effects on longevity,
behaviors, and breeding success remain unknown and may be a
significant source of mortality.
Recently, there have been studies linking the lead isotopic ratios
in feathers of exposed condors with ammunition sources [8], [43].
Such studies would likely be relevant for eagles to further elucidate
the direct link between lead-based rifle ammunition and lead
ingestion in scavengers, such as bald eagles. In addition to linking
lead-based rifle ammunition to exposure in eagles, several recent
studies have raised concern for human health implications arising
from lead-based rifle bullets [44], [45]. Fragments from lead-based
rifle bullets are not only left in the gutpiles of field dressed big-
game, but are also present in packaged meat [44] and may prove
useful for investigating this potential source of human dietary lead
exposure.
Table 3. Top-ranked models (out of 10 considered) of eagle
blood lead levels in relation to harvest with lead-based bullets
by age, and sex from 2005–2007, 2009–2010 in Jackson
Hole,Wyoming, USA.
Model DAIC Akaike weight
Lead-Only Harvest
a
0 0.75
Total Harvest 3.46 0.13
Lead-Only Harvest, Age 4.34 0.09
Lead-Only Harvest, Age, Sex 7.64 0.02
Total Harvest, Age 7.72 0.02
a
AIC = 13.48.
doi:10.1371/journal.pone.0051978.t003
Lead Exposure in Bald Eagles from Rifle Ammunition
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Unlike many environmental problems there is a straightforward
and easy solution to toxic lead exposure in wildlife from rifle
ammunition: non-lead alternative ammunition. In our study many
hunters quickly made this transition voluntarily, 24% and 31% the
first and second year, respectively and this resulted in immediate,
measurably lower lead levels of eagles. This was accomplished with
modest public awareness and by making non-lead ammunition
more readily available. There remains a majority of hunters who
have not changed and for whom additional and persuasive
education and positive incentives will be necessary. In Arizona, a
similar program with state support and funding to offer free non-
lead ammunition to all hunters obtained an annual average of
85% voluntary compliance [25]. For a state or national program
to succeed it will take a concerted and coordinated effort of state
and federal wildlife and natural resource agencies and other
interested organizations to educate hunters about the superior
ballistic performance and environmental benefits of non-lead rifle
ammunition. Without proper education, support for and compli-
ance of non-lead regulations will fall short of the thresholds needed
to effectively remove this source of lead contamination from
wildlife and wildlands.
Acknowledgments
We thank S. Cain, E. Cole, S. Craighead, E. Curran, M. Cuthill, J. Hatch,
D. Huckel, L. Iverson, S. Kallin, J. M. Learned, M. Meyer, C. N. Parish,
M. D. Parrish, S. Patla, E. Patterson, P. Popinchalk, H. Quigley, T.
Rogers, S. Wolff, and many others who helped support this project. The
Wyoming Game and Fish Department, Grand Teton National Park, The
National Elk Refuge, U.S. Forest Service, and the Wyoming Department
of Transportation helped provide access and carrion for trapping. Nestling
blood samples were kindly provided by G. Montopoli and A. Harmata.
Author Contributions
Conceived and designed the experiments: BB DC. Performed the
experiments: BB RC DC. Analyzed the data: BB RC. Contributed
reagents/materials/analysis tools: BB DC. Wrote the paper: BB RC DC.
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