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EcoHealth

DOI: 10.1007/s10393-015-1096-2

Ó 2016 International Association for Ecology and Health

Original Contribution

Effects of Lead Exposure, Flock Behavior, and Management


Actions on the Survival of California Condors (Gymnogyps
californianus)

Victoria J. Bakker,1 Donald R. Smith,2 Holly Copeland,3 Joseph Brandt,4


Rachel Wolstenholme,5 Joe Burnett,6 Steve Kirkland,4 and Myra E. Finkelstein2
1
Department of Ecology, Montana State University, Bozeman, MT 59717
2
Microbiology and Environmental Toxicology Department, University of California Santa Cruz, 1156 High St, Santa Cruz, CA 95064
3
The Nature Conservancy, 258 Main Street, Lander, WY 82520
4
United States Fish and Wildlife Service, 2493 Portola Rd. Suite B, Ventura, CA 93003
5
National Park Service, Pinnacles National Park, 5000 Highway 146, Paicines, CA 95043
6
Ventana Wildlife Society, 19045 Portola Dr. Ste. F-1, Salinas, CA 93908

Abstract: Translocation is an increasingly important tool for managing endangered species, but factors
influencing the survival of translocated individuals are not well understood. Here we examine intrinsic and
extrinsic drivers of survival for critically endangered California condors (Gymnogyps californianus) whose wild
population recovery is reliant upon releases of captively bred stock. We used known fate models and infor-
mation-theoretic methods to compare the ability of hypothesized covariates, most of which serve as proxies for
lead exposure risk, to predict survival rates of condors in California. Our best supported model included the
following predictors of survival: age of the recovery program, precipitation, proportion of days observed
feeding on proffered carcasses, maximum blood lead concentration over the preceding 18 months, and time
since release. We found that as flocks have increased in size and age, condors are increasingly likely to range
more widely and less likely to be observed feeding on proffered food, and these ‘‘wilder’’ behaviors were
associated with lower survival. After accounting for these behaviors, we found a positive survival trend, which
we attribute to ongoing improvements in management. Our findings illustrate that the survival of translocated
animals, such as highly social California condors, is influenced by behaviors that change through time.

Keywords: lead exposure, survival, California condor, management actions, flock, precipitation, translocation

INTRODUCTION Grenier et al. 2007; island fox, Coonan et al. 2010). Similarly,
averting extinctions of species threatened by climate change
Recovery of critically endangered species often depends upon may require translocating individuals to new habitats (Hoegh-
releases of captively bred individuals (e.g., black-footed ferret, Guldberg et al. 2008). These released animals, however, must
Electronic supplementary material: The online version of this article (doi:10.1007/
navigate a novel environment and unfamiliar social structure,
s10393-015-1096-2) contains supplementary material, which is available to autho- which can increase their mortality rates compared to residents,
rized users. especially shortly after release (Shier 2006; Bakker et al. 2009;
Pinter-Wollman et al. 2009).
Correspondence to: Myra E. Finkelstein, e-mail: myraf@ucsc.edu
V. Bakker et al.

The wild population of critically endangered California ulations and hunting (Rivrud et al. 2014). Indeed, mule
condors (Gymnogyps californianus) is supported by releases deer harvest and population sizes in arid southern Cali-
of captively bred stock and closely monitored (USFWS fornia are positively correlated to past precipitation (Mar-
2013), providing a unique opportunity to examine factors shal et al. 2002; Marshal and Bleich 2011). Finally, the
affecting post-translocation survival. After the population Condor Recovery Program has been actively attempting to
declined to *22 individuals by 1982, all condors were ta- reduce lead exposure and other threats to condors, and
ken into captivity, and releases of captive-bred individuals institutional learning may have generated a temporal trend
began in 1992 (USFWS 2013). We consider these releases in survival rates.
and the re-releases of individuals after extended stays in Here we examine how lead exposure, management
captivity as ‘‘translocations.’’ To help facilitate monitoring actions (e.g., proffered feeding stations and rearing meth-
and management of this population composed largely of od), the age of the recovery program, flock size, precipi-
translocated individuals, proffered carcasses are maintained tation, and individual factors (e.g., age and time since
at established sites, although condors also forage upon non- release) influence the survival of condors in California. Our
proffered carcasses across the landscape. Lead poisoning prior work has investigated the effect of lead on condor
from ingesting spent ammunition while feeding on non- population health (Finkelstein et al. 2012), and our current
proffered carcasses is the leading cause of mortality in free- analysis expands upon this effort to represent a compre-
flying juvenile and adult California condors (Cade 2007; hensive assessment of how multiple temporally dynamic
Finkelstein et al. 2012; Rideout et al. 2012), whereas trash factors influence annual survival. Because condors are
ingestion is a primary cause of mortality for wild nestlings highly managed and monitored on a near-daily basis, they
(Rideout et al. 2012). provide an ideal case study to examine how intrinsic and
Intrinsic factors unique to individual condors may extrinsic factors affect survivorship in translocated species.
increase lead exposure risk and thus mortality risk. For
example, Kelly et al. (2014) reported that a condor’s blood
lead level increased with decreasing use of proffered car- METHODS
casses. Additionally, some individuals may exhibit unrec-
ognized behavioral patterns that increase their exposure Management and Monitoring Data
risk. If so, lead exposure history should predict future Proffered feeding stations are used for management and
exposure risk and thus future survival. A history of elevated monitoring purposes including re-trapping for routine
blood lead may also directly contribute to death due to the health checks. Free-flying birds are monitored on a near-
toxicity of lead on multiple physiological systems (Skerfv- daily basis via visual observation of patagial tags on con-
ing and Bergdahl 2014). dors at proffered feeding stations or via detection of signals
Group size and dynamics may promote risky behaviors from radio (VHF) and/or GPS transmitters. Condors are
for condors, which are highly social and forage and roost also trapped approximately semi-annually for physical
communally (Sheppard et al. 2013). In particular, the flock checkups including blood lead assessment, and, if indicated
may function as an information center for the location of by health status, transferred to captive facilities for ex-
food (Brown 1986; Marzluff et al. 1996; Buckley 1997; tended treatment (Grantham 2007; Walters et al. 2010).
Wright et al. 2003). Because condors were re-introduced to Nests are managed to reduce trash-related mortalities
a landscape devoid of conspecifics, they have been building through actions such as trash removal from the nest
social hierarchies and knowledge of the landscape largely de vicinity and nestling examinations to detect trash impac-
novo, although a few original members of the wild flock tion (Walters et al. 2010; USFWS 2012).
have been re-released. Blood lead concentrations used in this study were
Extrinsic factors, including not only anthropogenic measured by certified commercial laboratories (ANTECH
threats, but also natural conditions such as weather, may Diagnostics, Louisiana Animal Disease Diagnostic Labora-
influence the frequency of lead-contaminated carcasses in tory, and/or California Animal Health and Food Safety
the environment, thereby increasing a condor’s lead Laboratory, University of California, Davis). Typically,
exposure risk and decreasing survival. Precipitation, for birds with blood lead concentrations > 35 lg/dL received
example, can drive relationships between vertebrate pop- clinical management (e.g., chelation therapy).
Factors Affecting California Condor Survival

Model Variables (See Also Table 1) poisoning events. We tallied these variables through the
interval prior to the survival prediction interval, with the
We included every condor free-flying in California or held
aim of excluding blood lead values and/or chelation treat-
in zoos from the start of the reintroduction program in
ments directly associated with the proximate cause of
1992 through August 2013. Free-flying (FF) and zoo (Zoo)
death.
birds were assessed as separate attribute groups, and year
We included time since release from captivity, both as
was also considered a group to allow tests of annual vari-
a binary (e.g., RelLT1yr for birds in the first year after re-
ation in survival. We considered unchanging intrinsic fac-
lease), and as a continuous variable (RelTime). We con-
tors that may influence a condor’s behavior and survival as
sidered changes in survival probability with age, including
time-invariant individual covariates: sex, rearing location
continuous linear and quadratic year effects (Age, Age2), as
(wild vs. captive, assessed using the binary variable, Wild-
well as functional forms in which survival stabilizes as birds
Rear), and rearing method (Parent, Foster, Hand) (Mer-
mature (e.g., Agethru2yr:FF indicates survival changes with
etsky et al. 2000; Utt et al. 2008).
age up through 2 years and then is constant with respect to
We investigated changing intrinsic factors that could
age for free-flying birds).
influence mortality risk as time-varying individual covari-
Extrinsic factors that change through time and could
ates, with a focus on variables hypothesized to influence
influence behaviors and lead exposure risks of entire flocks
lead exposure risk. Feeding on non-proffered food often
were considered. We assessed the predictive strength
goes undetected by biologists, but other observable
of short-term precipitation, which may influence the
behaviors may serve as proxies, such as frequency of use of
dynamics of small mammals, by evaluating cumulative
proffered food (FedProffered) or proportion of monitoring
precipitation in the previous year, and the predictive
days an individual is undetected (Absent) and thus far from
strength of longer-term precipitation, which has been
management areas. The presence of condors utilizing
linked to deer dynamics (Marshal et al. 2002; Marshal and
proffered food is recorded only if a carcass is present and
Bleich 2011), by assessing cumulative precipitation in the
thus this data collection method helps account for variation
previous 5 years (CentralRain1, CentralRain5, South-
in carcass placement rates.
ernRain1, SouthernRain5). Because longer-term rainfall
Condors using coastal areas are known to feed on
should influence condors primarily during the hunting
beach-cast marine mammals (Burnett et al. 2013), which
season, we assessed models in which cumulative rainfall
are typically uncontaminated by lead-based ammunition.
5 years prior to the fall hunting season (before September)
Thus, to evaluate the potential for differences in probabil-
influenced only the fall survival intervals (September–
ities of encountering lead-contaminated carcasses on the
October, November–December, CentralRain5Fall, South-
coast, we included the proportion of free-flying days an
ernRain5Fall).
individual was observed near the coast (Coastal). Condors
Additional extrinsic factors included indices of leg-
in California are currently spatially segregated into two
islative and management changes. Specifically, we consid-
fairly distinct flocks, one in southern California managed
ered a binary variable indicating time intervals subsequent
by the U.S. Fish and Wildlife Service, and another in central
to a partial ban on lead-based ammunition in condor
California managed by Pinnacles National Park and Ven-
habitat in California that went into effect July 2008 (Ridley-
tana Wildlife Society. As these two flocks may experience
Tree Conservation Act 2008, PostBan). A year trend vari-
different risks, we included a binary variable indicating
able indicating number of years since the release program
flock membership (Central), which was generally consistent
started (ProgramAge) was considered as a composite index
throughout a bird’s lifetime.
of ongoing efforts to improve management to enhance
To investigate relationships between known lead
survival rates [e.g., changes in release strategies, power pole
exposure history as identified via blood lead monitoring
aversion training, and nest monitoring practices to remove
and survival, we included two covariates. We used natural
trash (Walters et al. 2010)]. Finally, we considered year-
log of the maximum blood lead concentration in the pre-
specific effects and screened for survival differences in time
ceding 18 months (MaxPb) to assess the effect of previous
intervals when management changed substantively, such as
blood lead concentrations and lifetime number of chela-
increased nest monitoring in 2007 (USFWS 2012).
tions (Cheln) to assess the effect of cumulative detected lead
V. Bakker et al.

Table 1. Variables Considered in Survival Analysis for California Condors

Factor Description
Group variables
Zoo 1992–2013 Individuals were considered Zoo birds if they remained in captivity 1 year
FF < 1995, 1996–2013 Free-flying individuals. Individuals were considered FF upon release from captive breeding facilities
or hatching in the wild. They retained FF status even with short to moderate length stays in
captivity (<1 year) in release site field pens or zoos. However, the proportion of time in captivity
was considered as a covariate
To allow comparisons of models with and without variance in annual survival, each year (Jan 1–
Dec 31) was considered a group for both FF and Zoo, except that the periods from 1992 to 1995
were combined into one interval due to small sample sizes (1–15 individuals tracked per year
versus 21–141 in subsequent years)
Invariant individual covariates
Foster Binary variable indicating if individual was reared by foster parents
Hand Binary variable indicating if individual was reared by zookeepers
Parent Binary variable indicating if individual was reared by genetic parents
Sex (M, F, U) Male, Female, Unknown. Binary variables indicating sex
WildRear Binary variable indicating if individual was reared in the wild
Time-varying individual covariates
Absent Proportion of free-flying days in which an individual was absent from monitoring (not visually
sighted or observed via radio-telemetry) in previous two-month interval
Age Age in years. Functional forms considered include linear and quadratic terms and age-variation
Agethruyr:FF terminating with maturity
Agethrumo:Zoo Age of free-flying birds (FF) in years, and age of zoo birds (Zoo) in months. For example,
Agethru2yr:FF indicates survival changes with age up through 2 years then is constant with respect
to age
Cheln Cumulative number of recorded chelations (used in clinical therapy for lead poisoning) in an
individual’s lifetime excluding the current two-month interval
Coastal The proportion of free-flying days that an individual was observed near the coast (i.e., observed
visually or by telemetry signal in the Big Sur California area). This variable was applied only to
birds in the central flock
Central Binary variable indicating if individual was part of the central California flock in the current two-
month interval. Generally constant throughout a bird’s lifetime
FamDeath Binary variable indicating if mate, sire or dam died in previous bimonthly interval. Because family
members may forage together or in the same areas, this variable was intended to assess the degree
to which social networks influence lead exposure risk
FedProffered Proportion of free-flying days observed feeding at proffered feeding stations in previous two-month
interval
FlockSize Number of individuals > 6 months old in the individual’s flock (central vs. southern) in a given
year
MaxPb Natural log of the maximum blood lead in the 9 bimonthly intervals (18 months) prior to and up
through the interval previous to the estimation interval. For Figure 2, MaxPb was rescaled by
multiplying by 10
RelLT0.5yr Binary variables indicating time interval shortly after initial release from captive breeding facility
RelLT1yr (i.e., within 0.5, 1, or 2 years)
RelLT2yr Number of bimonthly intervals since an individual’s initial release from captivity, up to a maxi-
RelTime mum of 30 (i.e., 5 years). Wild hatched individuals assigned a value of 30
Factors Affecting California Condor Survival

Table 1. continued

Factor Description
Time-varying covariates
CentralRain1 Cumulative precipitation, in meters, for the 1-year and 5-year intervals preceding the survival
CentralRain5 interval, based on monthly totals. Rainfall for the central flock (CentralRain1, CentralRain5) was
CentralRain5Fall applied to central flock individuals and likewise southern rain (SouthernRain1, SouthernRain5)
SouthernRain1 was applied to southern flock individuals. Because cumulative 5-year rainfall is correlated with
SouthernRain5 deer harvest, we also used models in which we calculated the accumulated rainfall for the 5 years
SouthernRain5Fall prior to start of the hunting season (survival interval 5, Sep/Oct) and assessed its ability to predict
survival in intervals 5 and 6 (Nov/Dec) to test for a hunting season effect (CentralRain5Fall,
SouthernRain5Fall). CentralRain obtained from monitoring at Pinnacles National Park (NCDC
Climate Data Online, COOP station: 046926). SouthernRain obtained from PRISM time series
dataset for the 4 km pixel centered at Bitter Creek National Wildlife Refuge (PRISM Group
2015). Missing data for a small number of months (10/318) at Pinnacles were obtained from a
nearby station (Panoche 2w COOP 046675). For Figure 2, SouthernRain5Fall was divided by 5 to
express a mean annual rain over 5 years
PostBan Binary variable indicating time intervals after the implementation of the Ridley-Tree Condor
Preservation Act restricting lead ammunition for hunting in condor territory in California
(Ridley-Tree Condor Preservation Act 2008), which was assumed to be in full effect in 2009
ProgramAge Number of years since start of release program. For Figure 2, ProgramAge was divided by 10 and
thus indicates decadal change

Statistical Analyses summarized over the previous 18 months (i.e., 9 two-month


intervals) because blood lead monitoring often occurred at
We estimated annual survival rates and assessed factors driv-
approximately annual intervals in the first decade of the
ing them for both zoo and free-flying groups. Known fate
recovery program.
models in Program MARK (Cooch and White 2010) were
Two datasets were analyzed. First, to assess effects of
used to evaluate bimonthly mortality data from near daily
observed blood lead levels on future survival, we used the
radio-telemetry checks and direct observations. We assessed
subset of data for which MaxPb was available for all two-
the strength of covariates (Table 1) in predicting survival, with
month intervals in the year for each individual (i.e., Pb
a primary focus on free-flying birds, considering plausible
dataset). Second, to ensure that survival rates estimated
interactions and functional forms of these variables. Model
using the Pb dataset were not biased by omitting individ-
selection was based on quasi-Akaike Information Criterion
uals missing lead data (e.g., fledglings were often missing
corrected for small sample sizes (AICc, Lebreton et al. 1992).
lead data) and that the best model forms were selected, we
Individuals moving from long-term captivity in zoos to
also estimated survival rates with all data (i.e., full dataset),
the wild and vice versa were transferred among groups (Zoo
excluding specific models that used MaxPb, and compared
and FF), and their encounter histories right or left censored
model rankings and estimates based on each dataset.
to reflect their altered status. Individuals transferred to
Model selection was guided by AICc and approached
Mexico or Arizona were removed from the sample at the
in a two-step process. First, we identified the best model
time of transfer (i.e., right censored).
structure considering only year, age, and sex effects. Next,
To minimize the conflation of behaviors likely to predict
we assessed covariate effects for their ability to add
future lead exposure and those that may arise as a result of
explanatory power to this basic model structure or to ac-
lead exposure, time-varying individual covariates (i.e.,
count for annual variation. We considered interactions
Coastal, Absent, FedProffered, MaxPb, and Cheln, Table 1)
with ProgramAge, Central, Coastal, and Age if they im-
were summarized only up through the two-month interval
proved model fit. Because of inherent limitations to
preceding the survival prediction interval. Most variables
estimates of AICc-based variable importance when repre-
were summarized over one two-month interval, but to
sentation of variables is unbalanced (Burnham and
maximize data completeness, lead exposure (MaxPb) was
V. Bakker et al.

Figure 1. Mean estimated annual survival (±SE) of California condors greater than 2 years of age free-flying in California (filled triangle).
Estimates were based on the best model with temporal and age structure using the full dataset (Yr + Agethru2yrs:FF + Agethru1mo:Zoo,
Table S2). Also shown are flock-specific estimates for the central (open circle) and southern (filled circle) flocks using full dataset and based on
model Yr + Agethru2yrs:FF + Agethru1mo:Zoo + Central + Yr*Central + Yr*Agethru2yrs:FF (Table S2). Numbers indicate samples sizes
(number of individuals in the sample, all ages), with central flock sample sizes shown in italics and southern flock shown in bold text.

Anderson 2002), we indexed variable importance simply as


the proportion of plausible models (DAICc < 7, Burnham
et al. 2011) containing the variable.
To assist in interpreting our results, we analyzed how
foraging and ranging behaviors (i.e., FedProffered and Ab-
sent) changed with bird age, flock size, and program age,
using observations at the time of each independent lead test
(1689 observations, 195 individuals). We employed general
estimating equations to predict these binomial response
variables in R (geepack package, Halekoh et al. 2006),
including bird ID as a repeated measure (autoregressive
correlation structure, ar1) and flock location (Central) as a
factor, and used Wald tests and a quasi-information criterion Figure 2. Beta coefficients (±SE) for the best model predicting
(MuMIn package, Pan 2001) to guide model selection. annual survival of California condors in California using the Pb
dataset (Table 2, model 1). See Table 1 for variable descriptions.

RESULTS
age in the youngest age classes then became constant at older
ages, and this structure fit better than a quadratic age function
Basic Model Structure
(Figures 2, 3, and 4, Tables S1–S2). For free-flying birds,
The best basic model structure, considering only age and year survival peaked and stabilized at age 2 years (Figure 1), while
effects, included annually varying survival for free-flying for zoo birds survival became constant after the first month of
California condors (Figure 1), and constant survival for zoo life at an annual survival rate of 0.989 (95% CI 0.984–0.992).
condors, with age effects for both (i.e., Yr + Ageth- For free-flying and zoo birds, no sex effect was retained in the
ru2yrs:FF + Agethru1mo:Zoo). This basic structure was sup- best basic models except for an effect of unknown sex, with
ported using either the full (n = 4507 annual encounter such birds having lower survival (Table S2), which is unsur-
histories, 1361 FF, 3146 Zoo) or Pb (n = 4106 annual prising given that sex is unknown primarily for birds that die
encounter histories, 960 FF, 3146 Zoo) datasets (Tables S1– very young (e.g., <6 months) (Rideout et al. 2012). To avoid
S2). As expected, birds housed in zoos survived at higher rates biasing estimates high by excluding birds of unknown sex, no
than free-flying birds. For both groups, survival increased with sex effect was included in final model-building.
Factors Affecting California Condor Survival

Figure 3. Effects of proffered feeding rate (FedProffered, Table 1), time since release, and age on annual survival rates of free-flying California
condors for the southern and central California flocks. Shown are survival predictions for individuals with high proffered feeding rates, or the
proportion of free-flying days observed feeding on proffered carcasses equal to 0.3 (high rate), and low proffered feeding rates, or the proportion
of free-flying days observed feeding on proffered carcasses equal to 0.05 (low rate). For both high and low feeding rates, survival predictions are
shown for wild-born birds, or equivalently, birds released more than 5 years ago (wild birds), and for birds released 6 months ago (released
birds). Predictions are based on best model fit to the Pb dataset (Table 2; Figure 2) and parameterized with observed conditions for 2011
through 2013 for rainfall (SouthernRain5Fall = 1.32 m, CentralRain1 = 0.39 m, ProgramAge = 22), and the median maximum observed blood
lead in the previous 9 bimonthly intervals for birds >1 year old (27 lg/dL).

Figure 4. Effects of precipitation, previous lead exposure history, and age on annual survival rates of free-flying California condors for the southern
and central California flocks based on the best predictive model using the Pb dataset (Table 2; Figure 2). Predictions are based on two scenarios for
lead: maximum observed blood lead in the previous 9 bimonthly intervals was low (10 lg/dL, Low MaxPb) or high (100 lg/dL, High MaxPb).
Predictions also assume two scenarios for precipitation based on first and third quartiles of precipitation during the study period. For the southern
flock, cumulative precipitation for the previous 5 years, SouthernRain5Fall, was 1.37 m (low rainfall) and 1.71 m (high rainfall), and fall survival
is shown expressed as an annual rate. For the central flock, cumulative rainfall in the previous 1 year, CentralRain1, of 0.34 m (low rainfall)
and 0.51 m (high rainfall). Scenarios shown assume a wild-born individual with a proffered feeding rate of 0.05 in the year 2013.

Environmental and behavioral covariate models were better supported than models with year effects.
Among plausible model forms (DAICc < 7), all included a
We next considered whether environmental and behavioral
positive annual trend in survival (ProgramAge, Table 2,
covariates added additional explanatory power, and if they
Tables S1–S2). When ProgramAge was considered without
could account for annual variance in survival of free-flying
other covariates, a negative ProgramAge2 variable was
birds. Several covariates accounted for enough annual
strongly supported, indicating a plateauing of the annual
variance in survival that model forms with these covariates
Table 2. Model Selection for Estimating the Annual Survival of California Condors Based on the Pb Dataset, for the Top 28 Models

ProgramAge Central FedProffered CentralRain1 Southern Rel MaxPb Coastal Absent Wild FedProffered* ProgramAge* ProgramAge* Absent* AICc DAICc Model wi
Rain5Fall Time Rear Central FedProffered Central Central
V. Bakker et al.

1.0 1.0 1.0 1.0 0.82 0.76 0.67 0.31 0.29 0.22 0.16 0.14 0.14 0.04
+ - + + - + - + 1165.33 0.00 0.08
+ - + + - + - 1165.57 0.24 0.07
+ - + + - + - - 1166.31 0.98 0.05
+ - + + - - + 1166.55 1.22 0.04
+ - + + + - + 1166.57 1.24 0.04
+ - + + - - 1166.57 1.24 0.04
+ - + + - + - + 1166.95 1.62 0.04
+ - + + - - - 1167.03 1.70 0.03
+ - + + - + - + 1167.10 1.77 0.03
+ - + + - + - + + 1167.12 1.79 0.03
+ - + + + - 1167.22 1.89 0.03
+ - + + - + - - + 1167.32 1.99 0.03
+ - + + - + - + 1167.38 2.05 0.03
+ - + + - + - - 1167.57 2.24 0.03
+ - + + - 1167.61 2.28 0.03
+ - + + - - + 1167.83 2.50 0.02
+ - + + + - - 1167.83 2.50 0.02
+ - + + - + - + - 1168.06 2.73 0.02
+ - + + - + - - - 1168.28 2.95 0.02
+ - + + + - + 1168.37 3.04 0.02
+ - + + - - + 1168.48 3.15 0.02
+ - + + - + + 1168.55 3.22 0.02
+ - + + - + - + + 1168.58 3.25 0.02
+ - + + - + - 1168.63 3.30 0.02
+ - + + - + 1168.73 3.40 0.01
+ - + + - + - - - 1168.88 3.55 0.01
+ - + + - + - + + 1168.90 3.57 0.01
+ - + + - + - - + 1168.94 3.61 0.01

Signs indicate presence of variable in model and direction of relationship with survival. Final column is model AICc weight (Model wi), a measure of the probability of the model given the data and other
candidate models. The first row shows an index of variable importance based on the proportion of all plausible models (i.e., all models with DAICc < 7, which account for *99% of the AICc weight) that
contain the effect. Effects shown here only applied to free-flying condors. All models shown also include an intercept and an age effect (Agethru2yr:FF, Figure 2)
Factors Affecting California Condor Survival

survival trend (Tables S1–S2). However, ProgramAge2 was tral) indicated a tendency for undetected central flock
not included in the best models with other covariates, individuals to experience relatively greater mortality risk.
suggesting that the long-term survival trend persisted after Finally, there was some support for a negative interaction
accounting for changes in variables that increase risk of between years since the start of the release program and
mortality, as described below (Figure 5). central flock (ProgramAge*Central) such that the increasing
survival trend was slower for the central flock.
Lead exposure
Flock Size and Experience
All plausible models included a positive effect on survival of
frequent feeding on proffered carcasses (FedProffered, Fig- As the flocks have grown in size, individuals have reduced
ures 2, 3), and most also included a negative survival effect their proffered feeding frequency (FedProffered * Flock-
related to the maximum blood lead concentration in the size, Flocksize = -0.026, P  0.001, Figure 6a) and in-
previous 18 months (MaxPb, Table 2; Figures 2, 4). We creased their absences from the monitoring area
found support for a positive interaction of FedProffered and (Absent * Flocksize, Flocksize = 0.017, P  0.001, Fig-
ProgramAge suggesting that the beneficial effects of prof- ure 6b). Although bird age also predicted decreases in
fered feeding are increasing through time. Several sup- FedProffered and increases in Absent (FedProffered * Age,
ported models included a negative effect of absence from Age = -0.05, P  0.001, Absent * Age, Age = 0.014,
the monitoring area (Absent) and a positive effect of P < 0.001), with older birds being absent from feeding
presence near the coast (Coastal) on survival. stations and the monitoring area more often, age was a
weaker predictor than flock size. For FedProffered, models
Precipitation with both FlockSize and Age were supported over models
with either variable alone, and both QIC and Wald tests
All plausible models included a positive effect of precipi- indicated stronger support for models including FlockSize
tation in the previous year on central flock (CentralRain1) (FedProffered * FlockSize + Age, FlockSize = -0.021,
survival. Nearly all models also included a negative effect of P  0.001, Age = -0.014, P = 0.036). Thus, when flock
cumulative precipitation in the previous five years on fall sizes are larger, birds decrease their FedProffered rates at
survival of the southern flock (SouthernRain5Fall) (Table 2; earlier ages. The best model for Absent includes only
Figure 4, Fig. S1). When considered in combination with FlockSize, suggesting bird age has limited influence on ab-
one-year precipitation, a significant negative effect of five- sence from the observation area. In all models, there was a
year precipitation was also found for the central flock but positive effect of Central on FedProffered and negative effect
not supported in the best models (Tables S1-S2), suggesting on Absent, indicating central flock birds were more likely to
that when the positive effect of one-year precipitation was be observed at feeding stations and less likely to be absent
controlled for, high precipitation in the previous 5 years from the monitoring area, which may be partly
also lowered survival in the central flock. attributable to monitoring intensity. Flock size and years
since the release program started (ProgramAge) are highly
Central Versus Southern California Flocks correlated (r = 0.948), and not surprisingly given this
correlation, ProgramAge showed similar patterns to Flock-
Although all plausible models included a negative effect for Size in predicting FedProffered and Absent. Because Pro-
individuals in the central flock (Central), this should be gramAge was better supported by AICc in survival models,
viewed in conjunction with the positive precipitation effect, we only considered ProgramAge in final model selection.
such that survival is higher among central birds under
median precipitation conditions (Figure 4). Several inter- Other Factors
actions indicated a greater influence of behavior on central
flock survival. The positive interaction between observed Most supported models contained a positive effect of time
feeding and central (FedProffered*Central) indicated the since release from captivity (RelTime), and several included
safety associated with proffered feeding was greater in the a positive effect of being reared in the wild (WildRear).
central flock, while the negative interaction between ab- There was little to no support for other effects considered,
sence from the monitoring area and central (Absent*Cen- including rearing method, death of a family member,
V. Bakker et al.

Figure 5. Factors predicting positive and negative effects on survival


of free-flying California condors in California (CA) and hypothesized
relationships between these factors and the probability of lead
exposure (Lead exposure risk), which is the leading cause of
mortality in free-flying condors. We do not link age or time since
release to probability of lead exposure because we do not consider
the influences of these factors on survival to be mediated through
lead exposure risk. For predictors of survival, line width indicates the
proportion of plausible models (DAICc < 7) containing effect.
Figure 6. Changes in behavior with changing flock sizes of
proportion of time captive, and a bird’s lifetime cumulative California condors in California. Shown are mean and 95%
number of chelations (Tables S1–S2). confidence intervals of the proportion of free-flying days that
individuals are a observed feeding at proffered feeding stations
(FedProffered) and b absent from the management area during
DISCUSSION
monitoring checks (Absent).

Many of the factors influencing the survival of California


condors are temporally dynamic, underscoring the need for et al. 2008; Kelly et al. 2014; Finkelstein et al. 2015), but no
adaptive approaches to managing translocated wild ani- studies to our knowledge have linked temporally varying
mals. The primary factors correlated with an individual causal factors for lead poisoning to annual survival rates
condor’s survival rate, based on the best supported model and trends. A recent study by Kelly et al. (2015) uses Cox
(Figure 2), were age of the recovery program, proportion of regression and a dataset similar to ours to evaluate variables
free-flying days observed feeding at proffered carcasses, associated with mortality in California condors subsequent
maximum blood lead concentration in the previous to release or fledging, but this approach cannot estimate
18 months, time since initial release from captivity, and annual survival rates and trends while accounting for
precipitation. Although the importance of some of these multiple time-varying factors operating on different tem-
factors is not surprising (e.g., tendency to feed on proffered poral scales (Fieberg and DelGiudice 2009). Because cor-
carcasses), others were unexpected (e.g., precipitation). rectly understanding how changing behaviors and threats
Most factors predicting survival have clear hypothesized influence survival is critical to assessing management effi-
links to lead exposure risk (Figure 5). cacy for a re-introduced species such as the California
Lead is the leading cause of mortality among free-fly- condor, we use MLE general linear models to account for
ing condors (Rideout et al. 2012) and several publications time-varying covariates and set our models on the time
have investigated predictors of lead exposure (e.g., Green scale of the condor program. The Cox regression approach
Factors Affecting California Condor Survival

likewise is not able to account for mortality factors whose yet resulted in detectable reductions in condor lead expo-
strength varies through time, as our analysis indicates they sure rates (Finkelstein et al. 2012, Kelly et al. 2014).
do, and indeed such changes violate the proportional Interestingly, in the absence of covariates, the best
hazard assumption of Cox regression. model forms indicate that survival rate gains have peaked
and may be declining, but with covariates, survival main-
Individual Traits tains a positive linear trend. One likely explanation for this
pattern is that condors are increasingly expressing behav-
As documented for many other translocated animals, iors that place them at risk of mortality. For example, for a
younger birds and birds more recently released had reduced given rate of feeding on proffered carcasses, predicted
survival rates, a pattern attributed to lack of familiarity with survival has increased through time, but proffered feeding
the environment (Shier 2006; Bakker et al. 2009; Pinter- rates have not stayed constant. Indeed, as the flock has
Wollman et al. 2009). Similarly, wild-reared birds had aged, individual condors have clearly increased their wild
higher survival rates than released captive-reared birds. type behaviors—feeding less often on proffered food and
This elevated risk for young and inexperienced birds could spending more days absent from observation (Figure 6). In
result from general naı̈vete in the face of a broad range of addition, as the flock has grown, a declining rate of prof-
potential threats, such as predator attacks, collisions, and fered food availability on a per bird basis might have
electrocutions. Thus, the time period shortly after release encouraged foraging for non-proffered carcasses.
should be prioritized for monitoring and management Others have identified age as a main factor responsible
actions. for condors feeding less at proffered stations (Kelly et al.
Several behaviors likely to predict lead exposure risk 2014) or becoming more wide-ranging (Rivers et al. 2014);
had a strong influence on the survival of free-flying con- however, our analyses indicate that flock size and age of the
dors. Frequent feeding at proffered feeding stations was condor recovery program are stronger predictors. If social
consistently supported and was clearly protective against scavenging birds gain information on food sources from
mortality (Figure 3), and this behavior became more the flock (Buckley 1997; Wright et al. 2003), larger, more
important through time. Similarly, the proportion of days age-diverse, and more wide-ranging flocks should con-
absent from the monitoring area predicted lower survival. tribute to increased discovery and use of non-proffered
Taken together, these results indicate that, in the current food sources as observed here (Figure 6, Figure S2).
environment, as condors develop more wild behaviors (e.g., Analyses of movement data support the hypothesis that
feeding more on non-proffered carcasses), they are at individual birds have become more wide-ranging as the
greater risk of mortality, which we attribute to an increased flock has aged, with mean home range size (95% kernel
probability of lead exposure associated with these behaviors density estimates) increasing from 2003 through 2013 and
(Figure 5). showing a positive association with program age, especially
The best supported models included a positive annual for the southern California flock (H. Copeland, unpub-
trend in condor survival rates over the course of the release lished data).
program (ProgramAge), which likely reflects the results of
ongoing efforts to adaptively steward this species and
Extrinsic Factors
manage mortality risks. In fact, over the course of the
reintroduction program, survival was better predicted by Because ingestion of spent lead ammunition is the principal
an annual trend than by the binary variable denoting a source of lead exposure to condors (Finkelstein et al. 2012),
restriction on lead-based ammunition in condor territory. years of high deer or pig harvest as well as predator or
The observation that annual trend was a better predictor of ground squirrel control should result in higher lead expo-
survival underscores the importance of comprehensive sure and mortality risks. The contrasting influences of
conservation efforts (e.g., refined release methods, nest precipitation on survival rates suggest different lead expo-
monitoring, and lead awareness efforts) of which the sure sources for the central and southern California flocks.
restriction of lead-based ammunition is just one (Walters For the southern flock, cumulative precipitation in the
et al. 2010) and supports other observations that legislative 5 years prior to the fall hunting season is the strongest
restrictions on lead ammunition use in California have not weather-related predictor of survival. This precipitation
V. Bakker et al.

covariate, which predicts low survival in fall season only, is that the hazard of death was 1.8 times higher in southern
also correlated with mule deer harvests in California, versus central California flocks, but they did not account
especially in the arid southern region (Marshal et al. 2002; for the effects of year, age, or changing behaviors and
Marshal and Bleich 2011). For the central flock, however, precipitation. Our models indicate the regional comparison
the dominant influence of precipitation is lower survival is far more context dependent, and in many conditions,
the year following low precipitation. The reason why low condors in southern California have higher survival than
rainfall conditions reduce condor survival in central Cali- those in central California.
fornia is unknown, but may be related to an increase in lead
exposure due to rain-mediated changes in the dynamics or
CONCLUSION
behavior of hunted or depredated mammals, or of hunters
themselves (Rivrud et al. 2014).
Here we investigated the individual and environmental
The finding that birds with higher blood lead in the
factors that influence the survival rates of California con-
previous 18 months had lower survival suggests some
dors in an evolving setting spanning 22 years of recovery
individuals may regularly express behaviors that elevate
program efforts. We found that the survival of newly re-
their lead exposure risk or that lead exposure directly re-
leased individuals is reduced, highlighting the need for
duces a bird’s future survival. The relationship between
ongoing attention to releases. Most importantly, as condor
lead history and survival should not be interpreted as the
flocks grow, they are increasingly expressing behaviors
probability of an individual surviving a high lead exposure
typical of wild condors, which range widely and feed on
event as any condor detected with high lead values (e.g.,
non-proffered carcasses. In the current environment, these
>35 lg/dL) typically received clinical treatment for lead
behaviors are strongly associated with a higher risk of
poisoning. The intent of this analysis was not to estimate
mortality, which we suggest is related to a higher likelihood
the probability of direct mortality from a lead poisoning
of feeding on carcasses contaminated with lead-based
event but to estimate future survival after experiencing a
ammunition. More broadly, our results illustrate that while
high lead exposure and surviving this exposure with
translocation is an important tool in the conservation
treatment. Further, our blood lead dataset likely missed
toolbox, translocated animals require special attention to
numerous exposure events because feather lead analysis has
managing changing mortality risks through time as indi-
shown periodic blood lead monitoring to be a relatively
viduals and populations alter the ways in which they
poor indicator of lead exposure history (Finkelstein et al.
interact with their new environment.
2010; Finkelstein et al. 2012). In light of these data limi-
tations, it is notable that we were nonetheless able to detect
a clear influence of past lead exposure on future survival. ACKNOWLEDGMENTS
An important consideration when evaluating the effect
of extrinsic factors on condor survival is that the central We thank the United States Fish and Wildlife Service
and southern California flocks are managed by different California Condor Recovery Program, The Nature Con-
organizations—U.S. Fish and Wildlife Service for the servancy, The Zoological Society of London, and field crews
southern flock and Pinnacles National Park and Ventana associated with Pinnacles National Park, Ventana Wildlife
Wildlife Society for the central flock. We include a binary Society, and the Hopper Mountain National Wildlife
variable to assess differences in survival between flocks after Refuge Complex. Special thanks to T. Kelly, D. Moen, B.
accounting for other variables. However, because condors Rideout, S. Scherbinski, and A. Welch for their important
released in central California have merged into one flock, contributions to this study. We are also grateful to D. Doak
we are unable to separate survival impacts attributable to and three anonymous reviewers for providing helpful
differing management approaches within this flock. In comments on an earlier manuscript draft. This project
addition, we are not able to detect subtle influences of was supported by the U.S. Fish and Wildlife Service. The
management if they are correlated with environmental findings and conclusions in this article are those of the
(e.g., precipitation) or intrinsic (e.g., age structure) vari- authors and do not necessarily represent the views of the
ables that also influence survival. Kelly et al. (2015) report U.S. Fish and Wildlife Service.
Factors Affecting California Condor Survival

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