Lead Exposure in Free-Flying Turkey Vultures Is Associated with Big Game Hunting in California

Abstract

Predatory and scavenging birds are at risk of lead exposure when they feed on animals injured or killed by lead ammunition. While lead ammunition has been banned from waterfowl hunting in North America for almost two decades, lead ammunition is still widely used for hunting big game and small game animals. In this study, we evaluated the association between big game hunting and blood lead concentration in an avian scavenger species that feeds regularly on large mammals in California. We compared blood lead concentration in turkey vultures within and outside of the deer hunting season, and in areas with varying wild pig hunting intensity. Lead exposure in turkey vultures was significantly higher during the deer hunting season compared to the off-season, and blood lead concentration was positively correlated with increasing wild pig hunting intensity. Our results link lead exposure in turkey vultures to deer and wild pig hunting activity at these study sites, and we provide evidence that spent lead ammunition in carrion poses a significant risk of lead exposure to scavengers.

Full text

Lead Exposure in Free-Flying Turkey Vultures Is
Associated with Big Game Hunting in California
Terra R. Kelly*, Christine K. Johnson
School of Veterinary Medicine, Wildlife Health Center, University of California Davis, Davis, California, United States of America
Abstract
Predatory and scavenging birds are at risk of lead exposure when they feed on animals injured or killed by lead ammunition.
While lead ammunition has been banned from waterfowl hunting in North America for almost two decades, lead
ammunition is still widely used for hunting big game and small game animals. In this study, we evaluated the association
between big game hunting and blood lead concentration in an avian scavenger species that feeds regularly on large
mammals in California. We compared blood lead concentration in turkey vultures within and outside of the deer hunting
season, and in areas with varying wild pig hunting intensity. Lead exposure in turkey vultures was significantly higher during
the deer hunting season compared to the off-season, and blood lead concentration was positively correlated with
increasing wild pig hunting intensity. Our results link lead exposure in turkey vultures to deer and wild pig hunting activity
at these study sites, and we provide evidence that spent lead ammunition in carrion poses a significant risk of lead exposure
to scavengers.
Citation: Kelly TR, Johnson CK (2011) Lead Exposure in Free-Flying Turkey Vultures Is Associated with Big Game Hunting in California. PLoS ONE 6(4): e15350.
doi:10.1371/journal.pone.0015350
Editor: Andrew Iwaniuk, University of Lethbridge, Canada
Received August 19, 2010; Accepted November 10, 2010; Published April 6, 2011
Copyright: ß2011 Kelly, Johnson. 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: This research was funded by a State Wildlife Grant #T-12-1. 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: trkelly@ucdavis.edu
Introduction
Lead poisoning was recognized as an important cause of
mortality in wildlife in the late 1950s [1–3] when ingested spent
lead ammunition and fishing sinkers were linked to significant die-
offs in waterfowl [4]. In 1986, a phase-in of nontoxic ammunition
was initiated for waterfowl hunting in wetlands along the most
impacted flyways in North America, followed by a nationwide ban
of lead-based ammunition for waterfowl hunting in 1991 [5]. A
major impetus for this policy change was mortality in the
endangered bald eagle (Haliaeetus leucocephalus) population due to
secondary lead poisoning from feeding on waterfowl containing lead
ammunition [6–8]. While this regulation had a major impact on
decreasing lead-associated mortality in waterfowl [9], there was no
change in the prevalence of lead poisoning in eagles admitted to a
rehabilitation center in the Midwestern U.S. during the post-ban
period from 1991–1995. The authors attributed the lead poisoning
in these cases in part to lead ammunition used in deer hunting [8].
Studies have demonstrated that lead bullets, upon impact, can
produce hundreds of small fragments contaminating animal
carcasses and discarded viscera that serve as important food
sources for scavengers [10–13]. Predatory and scavenging birds
are at risk of lead exposure when they consume embedded lead
shot or bullet fragments in carcasses and gut-piles left in the field
by hunters [6,8,14–16]. Old and new world vultures may be at
increased risk of lead exposure because of their unique feeding
ecology as obligate scavengers.
Lead-related mortality was a factor in the decline of the
endangered California condor (Gymnogyps californianus) population in
the 1980s [17] and has undermined efforts to establish a naturally
sustainable population in the wild. California condors are monitored
for lead exposure and a high proportion of the population exhibits
elevated blood lead concentration during routine screening [18,19],
with some individuals requiring clinical intervention. The major
challenges facing the recovery of this species have brought significant
awareness to the policies surrounding the use of lead ammunition for
hunting in North America, and in 2008 led to a ban of lead
ammunition for most hunting activities within the California range
of the condor. This legislation has received scrutiny from opponents
who question whether lead exposure in wildlife is related to hunting
activities and from wildlife agencies considering similar regulations to
protect other vulnerable species.
Increased lead exposure during the deer hunting season has
been detected in condors [18–20] and golden eagles sampled in
the California range of the condor [21], however elevated blood
lead concentrations have also been noted outside of the deer
hunting season [21]. In Arizona and Utah, this seasonal increase
in blood concentration in condors coincides with movement of the
population to an area with high deer hunting pressure [20].
Temporal spatial correlations between big game hunting and lead
exposure have also been documented in common ravens (Corvus
corax) in the Greater Yellowstone Area. The ravens were observed
to have significantly higher blood lead concentrations during the
big game hunting season compared to the off season and lead
exposure was found to be temporally correlated with big game
hunting pressure [22]. In this study, food resources during the
hunting season were limited by harsh weather and landscape, and
hunter-killed prey was thought to be the primary food source
available to ravens.
In California, year-round food sources for avian scavengers
appear to be highly diverse due to a wide range of natural habitats,
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a mild climate, and a productive livestock economy. Turkey
vultures (Cathartes aura) in California feed on a wide array of
carrion including birds, reptiles, and small mammals, as well as
large mammals, such as domestic livestock, wild ungulates, and
beachcast marine animals [23]. Big game hunting in California is
presumed to supply a substantial food source to avian scavengers,
especially year-round wild pig hunting, which provides hunter-
killed carrion throughout the year to scavengers within the wild pig
range. Hunting activities vary by type and intensity throughout
California and there is considerable overlap of different hunting
seasons.
While previous studies have explored temporal and spatial
patterns of lead exposure in avian scavengers with respect to
confined hunting activities under conditions with limited food
resources, data is currently lacking on lead exposure in avian
scavengers in diverse habitats with varying big game hunting
activity and a range of available food resources. Furthermore,
blood lead concentrations have not been evaluated in association
with hunting activities in free-flying populations of turkey vultures,
an important scavenger in the Americas with excellent potential as
a sentinel species for monitoring the availability of lead
ammunition in carrion. In this study we tested the hypotheses
that: (1) turkey vulture blood lead concentrations are higher during
deer hunting season in an area with intense deer hunting
compared to outside of the deer hunting season at the same
location, and (2) turkey vulture blood lead concentrations are
positively correlated with wild pig hunting intensity. Our results
indicate that lead exposure in turkey vultures is highly associated
with big game hunting activity despite a naturally diverse field
setting and wide range of available food sources.
Materials and Methods
Ethics statement
Animal capture and sampling protocols were covered under
state and federal permits (United States Geological Survey federal
bird banding permit #20431 and California Department of Fish
and Game scientific collecting permit #000221) and approved by
the University of California, Davis Institutional Animal Care and
Use Committee (protocol #07-12955).
Study site selection
Deer and wild pig hunting constitute the majority of the total
statewide harvest of big game animals in California. Deer hunting
occurs in late summer and fall in discrete seasons that vary by
region. Pig hunting occurs year-round, although October through
May tends to be the most popular time for hunting since pigs are
most easily tracked in the wet season [24]. We evaluated the
distribution of deer and wild pig hunting activity in California by
overlaying county level harvest data from the 2006 game take
hunter survey [25] and hunting seasons reported in the California
mammal hunting regulations booklet [26]. The game take hunter
survey is conducted annually by the California Department of Fish
and Game and provides the best game harvest estimates for
California [25]. We calculated the proportion of total statewide
harvest for deer and wild pig hunting for each county as a relative
measure of local hunting intensity.
We selected our study sites to represent a range of hunting
activity in areas with a resident turkey vulture population. Turkey
vultures were sampled during discrete periods outside of the
reported turkey vulture migration [23] to ensure blood lead
concentration reflected local lead exposure. We assumed that
turkey vultures were feeding on hunter-killed carcasses and gut-
piles within an area roughly equivalent to their estimated home
range in each direction from our study sites [27]. We selected a site
at the University of California Hopland Research Extension
Center (HREC) in Mendocino County, California (38u599390N,
123u049020W) to evaluate the association between deer hunting
and blood lead concentration in turkey vultures. This is a rural
farming area situated amongst oak covered coastal foothills and is
characterized by high intensity deer hunting, with Mendocino
County accounting for the highest proportion of the deer harvest
in California in 2006. We sampled turkey vultures at this site on
two occasions; 1) a two week period beginning one week following
the opening day of the deer hunting season, and 2) a two week
period one month preceding the deer hunting season during the
following year. The only hunting activity that varied between
sampling efforts at this site was deer hunting. The black bear
hunting season occurs concurrently with the deer hunting season
in California. However, this site is not considered to be suitable
habitat for black bears and there were no reports of bears
harvested within our study area. Year-round hunting activities,
including wild pig, rabbits, and non-game (coyotes, ground
squirrels, skunks, opossum, starlings), were occurring during both
sampling periods. The seasons for upland game and waterfowl
hunting occur later in the fall and did not overlap with our
sampling activities at this site.
We also selected three study sites along a gradient of wild pig
hunting intensity in areas without other substantial hunting
activities occurring at the time of sampling. Our low wild pig
hunting intensity (LOW PIG) study site was located near Irvine
Lake, an urban area in Orange County, California (33u459440N,
117u429470W) (Fig. 1). This area accounted for ,1% of the total
statewide harvest for wild pig hunting. Our medium pig hunting
intensity (MED PIG) study site was located in Mendocino County
at the same site that we used to evaluate the association between
lead exposure and deer hunting (Fig. 1). This site accounted for
approximately 3% of the total statewide harvest for wild pig
hunting. Sampling occurred outside of the deer hunting season at
this site in order to assess lead exposure in vultures due to medium
intensity pig hunting. Lastly, our high intensity (HI PIG) study site
was located at the University of California Landels-Hill Big Creek
Reserve in Monterey County (36u039510N, 121u349280W) (Fig. 1),
an area characterized by rugged oak-covered coastal mountains
near the Big Sur coast surrounded by private and public land with
high intensity wild pig hunting. Monterey County had the highest
wild pig hunting pressure in 2006, accounting for greater than
15% of the total statewide reported pig harvest.
We focused our investigations on deer and wild pig hunting
activities by sampling outside of other big game, upland game, and
small mammal game hunting seasons. Year round non-game
hunting activities were occurring within all of our study areas,
however harvest rates were considerably lower than that for game
species with managed hunting seasons during confined time
periods. Furthermore, harvest data for non-game species was
similar among sites [25].
Sample collection and analysis
We captured turkey vultures in 2008 and 2009 using carrion
baited walk-in traps with a ‘‘lure’’ turkey vulture, drop-in traps,
and a ground net launcher (CODA Enterprises, Mesa, AZ). All
vultures underwent basic health screening at the time of capture.
Data collected on each vulture included capture location (GIS
coordinates), sex, age class, body weight, basic morphometric
measurements, and body condition score. The body condition
score was a subjective measure of body condition index based on
the contour of the pectoral muscle mass ranging from a score of 1
(emaciated) to 5 (obese). We determined the age class of each
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vulture as hatch year (HY), second year (SY), and after second year
(ASY) by coloration of the head and maxilla [28]. Turkey vultures
were marked with vinyl patagial tags or passive integrated
transponders (AVID microchip systemH, Avid Identification
Systems, Inc., CA) in order to identify specific individuals at our
study sites. We identified the sex of each vulture by polymerase
chain reaction analysis of chromosomal DNA in blood samples
(Sex Made Easy
TM
, Zoogen Incorporated, Davis, CA).
Blood lead concentration rises within days of exposure to lead
[29], thus serving as a relative indicator of the amount of lead
available in carrion food sources at each study site. We considered
blood lead concentrations #10 mg/dL as consistent with exposure
to environmental background sources of lead, and concentrations
.10 mg/dL indicating elevated exposure to a point source of lead,
as would occur with ingestion of lead fragments. This threshold
value was chosen based on blood lead concentrations ,2mg/dL
in control turkey vultures and ,10 mg/dL in control bald eagles in
experimental lead dosing studies [29,30], and lead concentrations
of ,4mg/dL in pre-release California condors in captivity [31].
Furthermore, free-flying common ravens sampled outside of the
big game hunting season had a median blood lead concentration
of1.8 mg/dL [22]. Blood was collected from the brachial vein into
lithium heparin blood tubes (Becton Dickinson, Franklin Lakes,
NJ) and stored at 280uC until analysis. Blood samples were
analyzed for lead concentration at the California Animal Health
and Food Safety Laboratory (CAHFS), University of California,
Davis using graphite atomic absorption spectrophotometry
(PerkinElmer Model AAnalyst 800 graphite furnace atomic
absorption spectrophotometer; PerkinElmer, Waltham, MA). To
ensure precision of results, all samples were run in duplicate and
results were considered acceptable when the relative standard
deviation was #10%. To ensure accuracy of results, a proficiency
testing blood sample from the Wisconsin State Laboratory of
Hygiene with a target lead value was analyzed with each set of
Figure 1. Map of study sites selected along a gradient of wild pig hunting intensity. The counties are shaded according to categories of
the proportion of total statewide harvest of wild pigs by county.
doi:10.1371/journal.pone.0015350.g001
Lead Exposure in Vultures Associated with Hunting
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blood samples. These WSLH samples were within one standard
deviation of the target value. The lower laboratory reporting limit
for blood lead concentration was 6 mg/dL.
Data analysis
Blood lead concentration data were left censored since
concentrations falling below the laboratory limit of 6 mg/dL were
reported as a ‘‘nondetect’’ (,6mg/dL). Data were therefore
analyzed using NADA (Nondetects And Data Analysis) [32], a
library package in R [33] that provides an analytical framework for
analyzing left-censored data. This framework allows for censored
data to be incorporated into computations of the statistics using
nonparametric and parametric methods. The probability distribu-
tion of the blood lead concentration data was assessed using
probability plots and the Shapiro-Wilks test. A significance level of
0.05 was used for all statistical analyses unless stated otherwise.
Because age and sex related differences in blood lead
concentrations have been reported in other studies [34–36], we
evaluated differences in median turkey vulture blood lead
concentration by sex using the Wilcoxon rank sum test, and age
class using the Kruskal-Wallis test with post hoc Mann- Whitney U
test comparisons, including correction for multiple comparisons of
the respective p-values [37].
We used linear regression models with maximum likelihood
estimation, that incorporate censored data points, to investigate
the relationship between vulture blood lead concentration and
deer hunting and wild pig hunting intensity, separately. To identify
the most parsimonious models, we used the likelihood-ratio test to
determine whether each variable and interaction term significantly
improved model fit (P,0.05), compared to a model without that
variable. Variables and interaction terms were retained in the
model if they improved model fit, while minimizing Akaike’s
information criterion (AIC), or were determined to be important
confounders based on a change in parameter estimates from the
crude parameter by at least 10% with addition of the variables to
the model. Overall model fit was assessed by evaluation of the
residual plots.
To further illustrate the association between vulture blood lead
exposure and hunting activity, we calculated the overall
prevalence of elevated blood lead exposure ($10 mg/dL), and
the prevalence for each study group of interest with estimates of
95% confidence intervals using binomial probability testing. We
also demonstrated a trend in blood lead concentration across levels
of wild pig hunting intensity using a nonparametric test for trend
[38].
Results
A total of 172 turkey vultures were captured for this study,
including 90 ASY females, 67 ASY males, 4 SY males, 8 HY
females, and 3 HY males. Age classifications were collapsed into
two categories, HY vultures and after hatch year (AHY), vultures
given that median blood lead concentrations did not differ
between second year vultures and adults. Overall, 48% (83/172,
95% CI = 41%–55%) of our turkey vultures had elevated blood
lead concentrations .10 mg/dL. Despite blood lead concentra-
tions consistent with acute lead toxicosis ($100 mg/dL) [39] in
some individuals, none of the vultures were showing signs of
intoxication at capture.
Effect of Deer Hunting Season on Blood Lead
Concentration
We sampled 34 vultures during the deer hunting season and 39
vultures outside of the deer hunting season at our site with high
intensity deer hunting. The median blood lead concentration was
15 mg/dL (range: 6–170 mg/dL) during deer hunting season
compared to 7 mg/dL (range: 6–36 mg/dL) outside of the deer
hunting season (Figure 2A). There was a significant relationship
between deer hunting and turkey vulture blood lead concentration
in our multivariable analysis (Likelihood Ratio Chi-Square test,
G = 20.64, d.f. = 3, P= 0.0001, Table 1A) and significantly higher
blood lead concentrations (3-fold difference in the geometric mean
blood lead concentration) during the deer hunting season
compared to outside of the deer hunting season (P,0.01). An
interaction term between deer hunting season and age class was fit
in the model to account for the difference in the effect of deer
hunting on blood lead concentration by age. Specifically, only
after hatch year vultures had higher blood lead concentrations
during the deer hunting season. We found no difference in blood
lead concentration between sexes among vultures captured at this
location. The prevalence of elevated blood lead exposure in
vultures sampled during the deer hunting season was 76% (26/34,
95% CI = 60%–88%), which was significantly higher than the
36% prevalence among vultures sampled outside of the deer
hunting season (14/39, 95% CI = 22%–51%). Twenty-one
percent of vultures (7/34, 95% CI = 9%–36%) sampled during
the deer hunting season had moderate levels of elevated blood lead
exposure ($60 mg/dL), and two of the vultures had blood lead
concentrations .100 mg/dL, which are levels consistent with
acute lead intoxication [39]. None of the vultures sampled outside
of the deer hunting season had blood lead concentrations $60
mg/dL.
Effect of Wild Pig Hunting Intensity on Blood Lead
Concentration
We sampled 52 vultures at our LOW PIG site, 39 vultures at
our MED PIG site and 47 at our HI PIG site. The median blood
lead level was 4 mg/dL (range: 6–38 mg/dL) at the LOW PIG site,
7mg/dL (range: 6–36 mg/dL) at the MED PIG site, and 14 mg/dL
(range: 6–76 mg/dL) at the HI PIG site (Figure 2B). We detected a
significant relationship between wild pig hunting intensity and
turkey vulture blood lead concentration in our age and sex
adjusted model (Likelihood Ratio Chi-Square test, G = 42.81,
d.f. = 4, P,0.0001, Table 1B). The geometric mean for blood lead
concentration (mg/dL) was higher at our MED PIG and HI PIG
sites compared to our LOW PIG site, by a factor of 2 and 3,
respectively. Age class and sex were incorporated in the model to
adjust for joint confounding. Males at these three sites had
significantly higher blood lead concentration compared to females
(P= 0.04). We also detected a positive trend in vulture lead
exposure across wild pig hunting intensity categories using the
non-parametric test for trend (z = 6.78, P,0.0001). The preva-
lence of elevated blood lead exposure (.10 mg/dL) was 13% (7/
52, 95% CI = 6%–24%) in vultures sampled at the LOW PIG site,
36% (14/39, 95% CI = 22%–52%) in vultures sampled at the
MED PIG site, and 66% (31/47, 95% CI =53%–78%) in vultures
sampled at the HI PIG site.
Discussion
Our findings provide evidence that big game hunting in
California increases the risk of lead exposure in avian scavengers
from ingestion of lead ammunition. Elevated blood lead
concentration in free-flying turkey vultures varied according to
deer and wild pig hunting activities occurring at our study sites.
Turkey vultures captured during the deer hunting season
experienced significantly higher levels of lead exposure compared
to vultures captured outside of the deer hunting season with
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concentrations consistent with intoxication in some individuals.
None of the vultures sampled outside of the deer hunting season at
the same location had similarly high levels. Turkey vulture blood
lead concentrations were also highly correlated with wild pig
hunting intensity with concentrations three times higher at our
high intensity wild pig hunting site compared to our site with low
wild pig hunting intensity. Capture locations used in our study
were carefully selected such that deer and wild pig hunting
activities were the major factors varying between sampling efforts.
We sampled outside of other big game, upland game, and small
mammal game hunting seasons and the total year-round harvest
reported for non-game species was similar among sites.
The elevated blood lead concentrations documented in turkey
vultures captured for our study is consistent with exposure to a
point source of concentrated lead during foraging. Unlike some
other contaminants, lead does not undergo biological magnifica-
tion in the food chain, or concentrate in animal blood or tissues at
levels high enough to cause significant secondary lead poisoning in
predators or scavengers. Lead concentration can achieve high
levels in the environment (water and soil) in small localized areas
around lead mines, smelters and industrial plants [40–44].
However, lead poisoning in wildlife from these concentrated
environmental sources is relatively rare in occurrence. Further-
more, there were no lead-related industrial activities in the vicinity
of our field sites, so these sources were not likely to have
contributed to lead exposure in the vultures captured for this
study. Instead, the patterns in lead exposure observed in our study
attribute the point source of elevated blood lead concentrations to
Figure 2. Distribution of blood lead concentrations (mg/dL) in turkey vultures across study sites with varying big game hunting
activities. The rectangle represents the interquartile range (IQR) from the first quartile (the 25th percentile) to the third quartile (the 75th percentile).
The whiskers extend out to the smallest value within 1.5 times the IQR from the first quartile and the largest value within 1.5 times the IQR from the
third quartile. The dots represent outlying data points. A. Turkey vultures sampled during the deer hunting season had significantly higher blood lead
concentration than vultures sampled outside of the deer hunting season (P,0.01). B. There was a significant positive trend in turkey vulture blood
lead concentrations across wild pig hunting intensity categories (P,0.0001).
doi:10.1371/journal.pone.0015350.g002
Table 1. Regression estimates for the effect of big game hunting activity on turkey vulture blood lead concentrations (mg/dL).
A. Deer Hunting Season Model: Parameter estimate* Standard error P-value
Intercept 2.01 0.16 ,0.001
Deer hunting season 1.06 0.23 ,0.001
Age class (hatch year) 0.82 0.92 0.300
Deer hunting season * age class (hatch year) 22.03 1.05 0.050
B. Wild Pig Hunting Intensity Model:
Intercept 1.49 0.15 ,0.001
Wild pig hunting (medium intensity) 0.45 0.19 0.010
Wild pig hunting (high intensity) 1 0.18 ,0.001
Sex (males) 0.26 0.14 0.040
Age class (hatch year) 20.61 0.45 0.100
*Presented on natural logarithmic scale.
doi:10.1371/journal.pone.0015350.t001
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lead fragments in hunted animal carcasses available to foraging
vultures during big game hunting activities.
During our field efforts, turkey vultures were observed feeding
on wild mammals and domestic animal carrion. Vultures at all
study sites had access to dead domestic animals from nearby
livestock operations; our LOW PIG and MED PIG sites were near
major cattle and sheep operations [45] and our HI PIG site was in
close proximity to designated California condor feeding stations
where dairy calf carcasses are put out as a source of food for
condors. All sites were also within flight distance to the coast where
beachcast marine animals are available to scavengers. Marine
mammals occasionally die with gunshot wounds [46], thus serving
as potential sources of lead exposure to scavengers. We assume
that the same is true for livestock in California; however we were
unable to find reports of gunshot wounds as a cause of mortality in
these animals [47–49]. Most likely, these occurrences are
comparatively infrequent and would only vary systematically
across our study locations along the gradient of big game hunting
intensity if accidental shooting of livestock increases during big
game hunting activities.
This study is the first to document blood lead concentrations in
wild populations of turkey vultures and measure an association
between lead exposure in turkey vultures and hunting activities. As
obligate scavengers, turkey vultures may be at higher risk of lead
exposure from ingestion of spent ammunition, compared to
predators and scavengers that do not rely on carrion as a sole food
source. Our findings suggest that turkey vultures rely heavily on
hunted wild animal carrion for food. Interestingly, deleterious
effects associated with elevated lead exposure were not observed in
captured turkey vultures, despite observed blood lead concentra-
tions in some individuals that have been reported to cause lead
toxicity and death [29]. However, intensive long term follow-up of
individual birds with telemetry and frequent recaptures would be
necessary to detect clinical signs associated with lead intoxication
and lead-associated decreases in survivorship. Experimental
intoxication of turkey vultures has shown that this species can
tolerate a substantial burden of lead exposure and must ingest
more lead to reach high levels in the blood and cause mortality
than levels that have been reported in other avian species [29].
While turkey vultures may be a poor physiological model for the
toxic effects of lead [29], they are good sentinels for monitoring
lead exposure from ingestion of lead ammunition in field settings
due to their feeding ecology and potentially high survival rates
despite high levels of lead exposure.
In studies of raptors and vultures collected in Canada, turkey
vultures had the highest tissue levels of lead compared to other
species [50,51]. Turkey vultures have been found to also have
significantly elevated bone lead concentrations, consistent with
chronic exposure [52]. Chronic lead exposure from prolonged or
repeated exposure at lower concentrations can have sublethal
effects in avian species by impairing reproductive success [53],
growth rate of young birds [54,55], neurobehavioral function
[56,57], immunity [58,59], and physiology [29,60]. Furthermore,
a number of sublethally-exposed birds likely die from other causes
in which lead could be a contributing factor. As a result of this
myriad of deleterious health effects, birds may be more susceptible
to other stressors and increased risk of predation and disease.
While the population impacts of acute and chronic lead exposure
are unknown for most wild bird populations, the effect of lead
exposure on long-term sustainability through direct mortality and
sublethal effects is a concern.
Ingestion of spent ammunition has been linked to lead exposure
and lead poisoning in a range of wildlife species worldwide [16,61–
63]. This study contributes to the growing body of literature
emphasizing the hazards that lead ammunition poses to both
wildlife and public health [63]. Non-lead ammunition alternatives
are increasingly available for both small and large game species.
Transition to alternatives for shooting game and non-game species
will benefit many wildlife species and will also eliminate the
potential risk to humans of accidental ingestion of lead in
harvested game [64].
Acknowledgments
We thank California Department of Fish and Game for providing harvest
data and resources needed to accomplish fieldwork and laboratory
analyses. We thank Y. Hernandez, N. Todd and Bloom Biologicals for
their expertise in turkey vulture capture. We thank S. Torres for
intellectual contribution to study design and for critical review of this
manuscript and A. Kent for technical assistance with figures. We also thank
the volunteers that helped with field studies. The California Raptor Center
housed and provided daily care to our lure vulture. B. Poppenga provided
guidance on interpretation of the blood lead data. The University of
California Hopland Extension Research Center, University of California
Landels-Hill Big Creek Reserve, and Irvine Ranch Land Conservancy
provided land access and hospitality during our field efforts.
Author Contributions
Conceived and designed the experiments: TRK CKJ. Performed the
experiments: TRK. Analyzed the data: TRK. Contributed reagents/
materials/analysis tools: TRK CKJ. Wrote the paper: TRK CKJ.
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