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PATTERNS OF MORTALITY IN FREE-RANGING CALIFORNIA
CONDORS (GYMNOGYPS CALIFORNIANUS)
Bruce A. Rideout,1,16 Ilse Stalis,1 Rebecca Papendick,1 Allan Pessier,1 Birgit Puschner,2
Myra E. Finkelstein,3 Donald R. Smith,3 Matthew Johnson,4 Michael Mace,5 Richard Stroud,6
Joseph Brandt,7 Joe Burnett,8 Chris Parish,9 Jim Petterson,10 Carmel Witte,1
Cynthia Stringfield,11 Kathy Orr,12 Jeff Zuba,13 Mike Wallace,14 and Jesse Grantham15
1 Wildlife Disease Laboratories, Institute for Conservation Research, San Diego Zoo Global, PO Box 120551, San Diego,California 92112, USA2 Toxicology Laboratory, California Animal Health and Food Safety Laboratory, University of California Davis, Davis,California 95616, USA3 Microbiology and Environmental Toxicology Department, University of California, Santa Cruz, California 95064, USA4 U.S. Geological Survey, Forest and Rangeland Ecosystem Science Center, 3200 SW Jefferson Way, Corvallis, Oregon97331, USA5 Bird Department, San Diego Zoo Safari Park, 15500 San Pasqual Valley Road, Escondido, California 92027, USA6 U.S. Fish and Wildlife Service National Wildlife Forensic Lab, Ashland, Oregon, USA7 U.S. Fish and Wildlife Service, Hopper Mountain National Wildlife Refuge Complex, California Condor RecoveryProgram, PO Box 5839, Ventura, California 93005, USA8 Ventana Wildlife Society, 19045 Portola Dr. Ste. F-1, Salinas, California 93908, USA9 The Peregrine Fund, 5668 West Flying Hawk Lane, Boise, Idaho 83709, USA10 National Park Service, Pinnacles National Monument, 5000 Highway 146, Paicines, California 95043, USA11 Moorpark College, 7075 Campus Road, Moorpark, California 93021, USA12 Phoenix Zoo, 455 North Galvin Parkway, Phoenix, Arizona 85008-3431, USA13 Veterinary Services, San Diego Zoo Safari Park, 15500 San Pasqual Valley Road, Escondido, California 92027, USA14 Applied Animal Ecology, Institute for Conservation Research, San Diego Zoo Global, 15600 San Pasqual Valley Road,Escondido, California 92027, USA15 U.S. Fish and Wildlife Service, California Condor Recovery Program, 2493 Portola Road, Suite A, Ventura, California,93003, USA16 Corresponding author (email: brideout@sandiegozoo.org)
ABSTRACT: We document causes of death in free-ranging California Condors (Gymnogypscalifornianus) from the inception of the reintroduction program in 1992 through December 2009 toidentify current and historic mortality factors that might interfere with establishment of self-sustaining populations in the wild. A total of 135 deaths occurred from October 1992 (the first post-release death) through December 2009, from a maximum population-at-risk of 352 birds, for acumulative crude mortality rate of 38%. A definitive cause of death was determined for 76 of the 98submitted cases, 70% (53/76) of which were attributed to anthropogenic causes. Trash ingestion wasthe most important mortality factor in nestlings (proportional mortality rate [PMR] 73%;8/11), while lead toxicosis was the most important factor in juveniles (PMR 26%; 13/50) and adults(PMR 67%; 10/15). These results demonstrate that the leading causes of death at all CaliforniaCondor release sites are anthropogenic. The mortality factors thought to be important in the declineof the historic California Condor population, particularly lead poisoning, remain the most importantdocumented mortality factors today. Without effective mitigation, these factors can be expected tohave the same effects on the sustainability of the wild populations as they have in the past.
Key words: California Condor, Cathartidae, lead toxicosis, mortality, pathology, reintroduction.
INTRODUCTION
The California Condor (Gymnogypscalifornianus) went through a severepopulation decline in the late 20th century(Wilbur, 1978; Snyder and Snyder, 2000).In 1980, an expanded field research effortled by the US Fish and Wildlife Serviceand the National Audubon Society wasinitiated to try and save the species. By1982, intensive field surveys determinedthere were only 23 individuals left in the
wild population. Between 1982 and 1987,eggs, chicks, and adults were removed fromthe wild for a captive breeding program.When the last bird was trapped from thewild on April 19, 1987, the total worldpopulation stood at 27 individuals, all incaptivity (Grantham, 2007). The originalcauses for the decline were not fullyelucidated. Intentional shooting, lead poi-soning from ingestion of spent ammunitionin carcasses, egg collecting, and strychninepoisoning had been documented (Wilbur,
Journal of Wildlife Diseases, 48(1), 2012, pp. 95–112# Wildlife Disease Association 2012
95
1978; Janssen et al., 1986; Wiemeyer et al.,1988) but their relative importance was notfully known.
The conservation breeding programthat followed was very successful, produc-ing sufficient numbers of birds for rein-troductions to begin in Southern Califor-nia in 1992 (Kuehler et al., 1991; Snyderand Snyder, 2000; Grantham, 2007). Thereintroduction program expanded to in-clude additional sites in Arizona in 1996,Central California in 1997, and BajaCalifornia, Mexico in 2003 (Grantham,2007; Fig. 1).
A basic tenet of reintroduction biology isthat wildlife reintroductions should notbegin until the original causes of declinehave been mitigated (IUCN, 1998). How-ever, the original causes of decline may bepoorly documented, as was the case withthe California Condor. In these situations,establishing specific causes of death inreleased individuals is especially important.
It not only can reveal reasons for reintro-duction failures but can also providecircumstantial evidence regarding originalcauses of decline that might still prevail.
We documented causes of death in free-ranging California Condors at all releasesites from the inception of the reintroduc-tion program in 1992 through December2009 to provide baseline data for futureanalyses of the impact of these mortalityfactors on the establishment of self-sustaining populations in the wild.
MATERIALS AND METHODS
All mortalities from the inception of therelease program in 1992 through 31 Decem-ber 2009 were evaluated. Birds were includedin the study if they were found dead in thewild, were brought in from the wild for a life-threatening medical condition and died ofcauses directly or indirectly related to themedical problem being treated, or weremissing and presumed dead. Nestlings weredefined as birds ,6 mo old that had not yet
FIGURE 1. Map of California Condor release locations (numbered 1–8) and current range (shaded) in thesouthwestern United States and northwestern Mexico.
96 JOURNAL OF WILDLIFE DISEASES, VOL. 48, NO. 1, JANUARY 2012
fledged; juveniles as fledged birds from 6 mothrough 5 yr old; and adults as birds $6 yr old.The maximum population at risk consisted of49 chicks hatched in the wild and 303 juvenileor adult birds released during the studyperiod. The cumulative crude mortality ratewas defined as the total number of mortalitiesdivided by the combined maximum populationat risk for the study period. Proportionalmortality rates (PMR) were calculated foreach age class by dividing the number ofmortalities from a specific cause by allmortalities with a known cause.
Carcasses were recovered as quickly aspossible and delivered to the Wildlife DiseaseLaboratories, San Diego Zoo, San Diego,California, USA for complete post-mortemexaminations, with the exception of casesthought to involve intentional killing, whichwere delivered to the US Fish and WildlifeService Forensics Laboratory. Postmortemexams at the San Diego Zoo consisted ofwhole body dorsoventral and lateral x-rays, inmost cases, followed by an external exam andcomplete necropsy. Samples of all identifiabletissues were fixed in 10% neutral-bufferedformalin. Body condition was scored qualita-tively as good, fair, or poor based on total bodyfat deposits and pectoral muscle mass.
Liver samples from each case where liverwas available were frozen at 220 C for heavy-metal analysis (Toxicology Laboratory, Cali-fornia Animal Health and Food Safety Labo-ratory, Davis, California). Kidney sampleswere used when liver was not available (threecases). Samples were digested with nitric acidand analyzed for lead, manganese, iron,mercury, arsenic, molybdenum, zinc, copper,and cadmium by inductively coupled argonplasma emission spectrometry (ICP-AES;ARL, Accuris Model, Thermo Optek Corpo-ration, Franklin, Massachusetts, USA). Accu-racy of ICP was measured by analyzingstandard reference materials (SRM) such asbovine liver (National Institute of Standardsand Technology, SRM 1577b) and lobsterhepatopancreas (National Research Councilof Canada TORT-2). Data were accepted ifanalyzed standard reference material valueswere within two standard deviations of thecertified reference value. Metal concentrationswere determined and are expressed on a wet-weight basis. Feather and bone samplescollected post-mortem from one bird (422)were processed using trace metal cleantechniques and analyzed for lead concentra-tions according to the methods of Finkelsteinet al. (2010). Lead concentrations weredetermined using a Finnigan MAT Elementmagnetic sector-inductively coupled plasma
mass spectrometer (ICP-MS; Finnigan MAT, Inc.,San Jose, California, USA), measuring masses of206Pb, 207Pb, 208Pb, and 205Tl (the latter as aninternal standard), as described (Finkelstein etal., 2010). Normal values for heavy metals inliver (in mg/kg wet weight) were based on datafrom California Condors in the breeding flocks(copper mean 35 mg/kg, STD 29 mg/kg, n58;zinc mean 38 mg/kg, STD 17 mg/kg, n58;other values not shown) as well as comparisonswith Turkey Vultures (Risebrough, unpubl.)and published data from other avian species(Puls, 1994). Levels of manganese, iron,mercury, arsenic, molybdenum, and cadmiumwere interpreted as noncontributory and arenot shown.
Fixed tissues were processed routinely,sectioned at 5 mm, and stained with hematox-ylin and eosin for histopathologic examination.The cause of death in each case was defined asthe causal factor or factors responsible forinitiating the sequence of events that ultimate-ly led to death. It represents the professionaljudgment of the pathologist based on anintegration of the field history, antemortemclinical and laboratory findings (when avail-able), results of the post-mortem examination,and any ancillary diagnostic results. It includessupporting evidence as well as evidenceexcluding other causes. Cases were assigneda suspected cause of death when there washistoric or physical evidence pointing to acause, but the carcass was too autolyzed toconfirm the cause or the evidence did notmeet the full case definition. Cases wereassigned an unknown cause of death when thecarcass was missing, not submitted, scavenged,too autolyzed for evaluation, or when evidencepointing to a particular cause could not beidentified or was only speculative. A number ofpathologists have worked on condor cases overthe years of the program, but each case wasreviewed by a single pathologist (B.R.) toensure consistency. In some cases, the originalcause of death was revised based on new data oron a more-comprehensive review of the datathan was possible at the time the original reportwas written.
Lead toxicosis was diagnosed when antemor-tem blood lead concentrations were .50 mg/dl(determined in the field using LeadCare I or IIpoint-of-care devices; Magellan Biosciences,Chelmsford, Massachusetts, USA) based onclinical experience and previously publishedreports, (e.g., De Francisco et al., 2003) or onpost-mortem liver or kidney lead concentra-tions .6 mg/kg wet weight (Franson, 1996).Zinc toxicosis was diagnosed when hepaticzinc concentrations were .1,000 mg/kg wetweight and when (in cases with adequate cell
RIDEOUT ET AL.—CALIFORNIA CONDOR MORTALITY 97
preservation) there was histologic evidence ofindividual cell necrosis in acinar regions of thepancreas, individual cell necrosis in the liver,hemosiderosis in hepatocytes and Kupffer cells,and acute tubular necrosis in the kidney (Puls,1994; Puschner et al., 1999). Methods fordiagnosis of ethylene glycol toxicosis werepreviously reported (Murnane et al., 1995).Power line trauma or electrocution was diag-nosed when there were compatible traumaticinjuries, regionally singed or discolored feath-ers or skin, and a history of being found in theimmediate vicinity of power lines, often withfeathers adhered to the power lines.
West Nile virus infection was diagnosed byimmunohistochemistry on heart and brain(California Animal Health and Food SafetyLaboratory) in conjunction with compatiblelesions such as nonsuppurative inflammationand hemorrhage. All other causes of deathrelied on standard case definitions. Anthro-pogenic causes of death were defined as thoseattributable to man-made structures or hu-man activities (lead toxicosis, environmentaltrash, power lines, diseases introduced byhuman activity [e.g., West Nile Virus], andintentional killing). Nonanthropogenic mor-talities include all other causes such aspredator trauma, accidental drowning, andpoor body condition.
RESULTS
For the entire release program, 135deaths occurred from October 1992 (thefirst post-release death) through Decem-ber 2009, from a maximum population-at-risk of 352 birds, for a cumulative crudemortality rate of 38%. One-hundredcarcasses were recovered and 98 weresubmitted for necropsy (92 to the SanDiego Zoo and six to the US Fish andWildlife Service Forensics Laboratory;two were not submitted due to poorcondition of the carcasses).
A definitive cause of death was deter-mined for 76 of the 98 submitted cases,70% (53/76) of which were attributed toanthropogenic causes. All mortalities arepresented in Tables 1–3, in chronologicalorder by age-class and release location,but the most important mortality factorsare summarized below for the releasedpopulation as a whole. Figure 1 illustratesthe release locations and current ranges.
Nestling mortalities
Sixteen nestling deaths occurred from anat-risk population of 49 wild-hatched nest-lings (cumulative crude mortality rate 33%).A definitive cause of death was determinedfor 11 of 16 nestlings submitted, of which82% (9/11) were anthropogenic.
Trash ingestion was the cause of deathin eight cases, making it the most impor-tant mortality factor in nestlings, with aPMR of 73% (8/11). The trash generallyconsisted of bottle caps and small pieces ofbroken glass, plastic, and metal. In condor285, trash ingestion was the primaryproblem, but the immediate cause ofdeath was secondary zinc toxicosis. Thepresumed source of zinc was a galvanizedmetal washer (Fig. 2). Condor 308 wasbrought to the Los Angeles Zoo fortreatment of trash ingestion but wassubsequently euthanized because of sec-ondary respiratory aspergillosis unrespon-sive to therapy. West Nile virus infectionwith secondary respiratory aspergillosiswas the cause of death in one nestlingthat had not yet been vaccinated againstWest Nile Virus.
Juvenile and adult mortalities
A definitive cause of death was deter-mined for 65 of the 85 juveniles or adultssubmitted, of which 68% (44/65) wereanthropogenic. The most common mor-tality factors for juveniles and adults fellinto the categories of toxicosis, trauma oraccident, inanition, intentional killing,infectious disease, and trash ingestion.
There were 23 confirmed cases of leadtoxicosis (PMR 35%; 23/65) and one ofethylene glycol toxicosis. In some cases,lead toxicosis was diagnosed antemortembased on blood lead levels, but chelationtherapy resulted in hepatic lead levelsfalling below the diagnostic threshold bythe time of death. Eight of the leadtoxicosis cases from Arizona had metalfragments in the gastrointestinal (GI) tracton antemortem radiographs (n53) or leadammunition fragments in the GI tract
98 JOURNAL OF WILDLIFE DISEASES, VOL. 48, NO. 1, JANUARY 2012
TA
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RIDEOUT ET AL.—CALIFORNIA CONDOR MORTALITY 99
SB
Hat
chd
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ease
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tion
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sibly
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21
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Con
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.
100 JOURNAL OF WILDLIFE DISEASES, VOL. 48, NO. 1, JANUARY 2012
SB
Hat
chd
ate
Deat
hd
ate
Rel
ease
loca
tion
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ofd
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nd
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201
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-01
SoC
alM
Pow
erlin
eco
llisi
on,
elec
troc
ution
Non
eN
PN
D41.2
,1
37.4
233
9-M
ay-0
017-M
ay-0
2C
en
Cal
FU
nkn
own,
mis
sin
gU
nkn
ow
nN
PN
DN
AN
AN
A212
25-M
ay-9
930-N
ov-
02
Cen
Cal
FP
ower
line
colli
sion
,el
ectr
ocution
Non
eR
ub
ber
weat
her
stri
pp
ing
ND
25.9
,1
50.3
254
13-M
ay-0
119-F
eb
-03
Cen
Cal
MP
ower
line
colli
sion
,el
ectr
ocution
Non
eN
PN
D33.4
,1
34.1
260
1-J
un
-01
20-M
ay-0
3C
en
Cal
MP
oor
bod
yco
nditio
nas
soci
ated
with
poo
rfe
edin
gre
spon
sepos
t-re
leas
e
Non
eN
PN
D69.4
,1
124
267
5-A
pr-
02
19-J
ul-
03
SoC
alM
Tra
um
a,p
red
ator
(poss
ible
can
id)
Poo
rbod
yco
nd
itio
n,
elev
ated
liver
copp
erN
PN
D141
,1
77.1
202
18-A
pr-
99
26-O
ct-0
3S
oC
alM
Un
kn
ow
n,
mis
sin
gB
rush
fire
NP
ND
NA
NA
NA
268
6-A
pr-
02
26-O
ct-0
3S
oC
alF
Un
kn
ow
n,
mis
sin
gB
rush
fire
NP
ND
NA
NA
NA
256
13-M
ay-0
115-N
ov-
03
Cen
Cal
FU
nkn
own,
scav
enge
dN
on
eN
PN
DN
AN
AN
A179
30-M
ar-9
820-D
ec-
03
SoC
alM
Un
kn
ow
n,
mis
sin
gB
rush
fire
NP
ND
NA
NA
NA
277
24-A
pr-
02
5-J
an-0
6S
oC
alF
Un
kn
ow
n,
mis
sin
gU
nkn
ow
nN
PN
DN
AN
AN
A376
3-M
ay-0
56-J
ul-
06
Cen
Cal
MP
ow
er
lin
eco
llis
ion
,ele
ctro
cuti
on
Non
eN
PN
D57.7
,1
55
363
14-A
pr-
05
14-J
ul-
06
Cen
Cal
MP
oor
bod
yco
nd
itio
nas
soci
ated
wit
hp
oor
feed
ing
resp
on
sep
ost
-rele
ase
Ele
vate
dli
ver
lead
Cell
op
han
eN
eg
57.1
1.5
219
TA
BL
E1.
Con
tin
ued
.
RIDEOUT ET AL.—CALIFORNIA CONDOR MORTALITY 101
SB
Hat
chd
ate
Deat
hd
ate
Rel
ease
loca
tion
Sex
Pri
mar
yca
use
ofd
eath
Ad
dit
ion
alfi
nd
ings
Gas
tric
fore
ign
bod
ies
WN
V
Liv
erb
(mg/k
g,
ww
)
Co
pp
er
Lead
Zin
c
417
9-M
ay-0
612-M
ay-0
7C
en
Cal
FT
rau
ma,
pre
dat
or
(US
FW
SF
ore
nsi
cL
ab)
Poss
ible
hem
oly
tic
anem
iaN
PN
DN
A,
0.- 2
-5
NA
301
20-A
pr-
03
16-M
ay-0
7C
en
Cal
MP
ower
line
colli
sion
,tr
aum
aan
del
ectr
ocution
Non
eN
PN
D24
,1
47.8
307
5-M
ay-0
316-M
ay-0
7C
en
Cal
FR
attl
esn
ake
bit
eN
on
eN
PN
D45.3
,1
62.6
356
25-M
ar-0
51-O
ct-0
7C
en
Cal
FU
nkn
ow
n,
scav
en
ged
Un
kn
ow
nN
PN
DN
AN
AN
A429
8-A
pr-
07
4-D
ec-
07
Cen
Cal
FU
nkn
ow
n,
mis
sin
gU
nkn
ow
nN
PN
DN
AN
AN
A402
14-A
pr-
06
8-J
an-0
8S
oC
alF
Tra
um
a,p
red
ator,
mou
nta
inli
on
Non
eN
PN
D3.6
,1
21
377
4-M
ay-0
525-J
un
-08
Cen
Cal
FU
nkn
ow
n,
mis
sin
gB
rush
fire
NP
ND
NA
NA
NA
336
28-A
pr-
04
7-S
ep
-08
Cen
Cal
FT
oxi
cosi
s,le
adP
oor
bod
yco
nd
itio
nN
PN
D110
11
80
450
15-M
ay-0
712-D
ec-
08
SoC
alF
Wes
tN
ilevi
rus
infe
ctio
n(v
acci
nat
edtw
ice)
Asp
erg
illo
sis,
ele
vate
dli
v-er
cop
per
NP
Pos
210
,1
40
475
20-A
pr-
08
19-D
ec-
08
Cen
Cal
MT
rau
ma,
pre
sum
ed
con
speci
fic
Ele
vate
dli
ver
cop
per
NP
Neg
150
,1
78
474
21-A
pr-
08
7-M
ar-0
9S
oC
alF
Tra
um
a,co
nsp
ecific
Han
dli
ng
for
flu
idth
era
py
NP
Neg
98
,1
41
422
14-M
ay-0
69-J
ul-
09
Cen
Cal
FT
oxi
cosi
s,le
ad(s
ee
figu
re3)
Un
kn
ow
nN
PN
DN
AN
AN
A
358
30-M
ar-0
511-J
ul-
09
SoC
alM
Acc
iden
tal
stra
ngu
lation
with
8m
mro
pe
Non
eN
PN
D14
,1
37
Ad
ult
s(6
yran
dold
er)
105
18-A
pr-
94
30-J
ul-
00
SoC
alM
Un
kn
ow
n,
mis
sin
gU
nkn
ow
nN
PN
DN
AN
AN
A102
28-M
ar-9
424-S
ep
-00
SoC
alM
Un
kn
ow
n,
scav
en
ged
Un
kn
ow
nN
PN
DN
AN
AN
A101
28-A
pr-
94
6-O
ct-0
0S
oC
alF
Un
kn
ow
n,
auto
lysi
sN
on
eN
PN
D120
,1
44.9
100
27-M
ar-9
419-S
ep
-02
SoC
alM
Un
kn
ow
n,
mis
sin
gU
nkn
ow
nN
PN
DN
AN
AN
A12
1-J
an-7
613-F
eb
-03
SoC
alF
Gu
nsh
ot
(US
FW
SF
ore
nsi
csL
ab)
Un
kn
ow
nN
PN
DN
AN
AN
A
170
23-M
ay-9
715-J
un
-03
Cen
Cal
MT
oxic
osis
,le
ad(a
nte
mor
tem
dia
gnos
is,
under
trea
t-m
ent)
Vis
cera
lgou
tas
soci
ated
wit
hch
ela
tion
thera
py
NP
ND
12
,1
19.8
61-J
an-7
627-S
ep
-05
SoC
alM
Poor
bod
yco
nd
tion
Un
kn
ow
nN
PN
DN
AN
AN
A164
19-A
pr-
97
30-S
ep
-05
Cen
Cal
MU
nkn
ow
n,
scav
en
ged
Un
kn
ow
nN
PN
DN
AN
AN
A
TA
BL
E1.
Con
tin
ued
.
102 JOURNAL OF WILDLIFE DISEASES, VOL. 48, NO. 1, JANUARY 2012
SB
Hat
chd
ate
Deat
hd
ate
Rel
ease
loca
tion
Sex
Pri
mar
yca
use
ofd
eath
Ad
dit
ion
alfi
nd
ings
Gas
tric
fore
ign
bod
ies
WN
V
Liv
erb
(mg/k
g,
ww
)
Co
pp
er
Lead
Zin
c
245
25-A
pr-
01
14-A
ug-0
7S
oC
alF
Tox
icos
is,
lead
(ante
mor
tem
dia
gnos
is,
under
trea
t-m
ent)
Vis
cera
lgou
tas
soci
ated
wit
hch
ela
tion
thera
py
NP
ND
53.8
223.1
238
28-M
ar-0
110-M
ay-0
8S
oC
alM
Tox
icos
is,
lead
(ante
mor
tem
dia
gnos
is,
under
trea
t-m
ent)
Vis
cera
lgou
tas
soci
ated
wit
hch
ela
tion
thera
py
On
en
on
lead
meta
llic
pell
et
inan
tem
or-
tem
x-ra
y
ND
11
,1
24
278
24-A
pr-
02
25-J
un
-08
Cen
Cal
MU
nkn
ow
n,
mis
sin
gB
rush
fire
NP
ND
NA
NA
NA
286
16-M
ay-0
211-M
ay-0
9C
en
Cal
MT
oxic
osis
,le
ad(a
nte
mor
tem
dia
gnos
is,
under
trea
t-m
ent)
Pn
eu
mon
ia,
en
doca
rdit
is,
poor
bod
yco
nd
itio
n;
gu
nsh
ot.
NP
ND
12
,1
18
303
22-A
pr-
03
23-O
ct-0
9C
en
Cal
FT
oxi
cosi
s,le
ad(a
nte
mor-
tem
dia
gn
osi
s,u
nd
er
treat
men
t)
Non
eN
PN
D24
3.7
2.1
aS
B5
Stu
db
oo
kn
um
ber;
So
Cal
5S
ou
thern
Cal
ifo
rnia
;C
en
Cal
5C
en
tral
Cal
ifo
rnia
;M
5m
ale;
F5
fem
ale;
Un
k5
un
kn
ow
n;
US
FW
S5
Un
ited
Sta
tes
Fis
han
dW
ild
life
Serv
ice;
NA
5n
ot
app
lica
ble
;N
D5
no
td
on
e;
ww
5w
et
weig
ht;
Po
s5
po
siti
ve;
Neg
5n
egat
ive.
bR
esu
lts
inb
old
fro
mkid
ney.
cN
P5
no
tp
rese
nt.
dN
D5
no
td
on
e.
TA
BL
E1.
Con
tin
ued
.
RIDEOUT ET AL.—CALIFORNIA CONDOR MORTALITY 103
TA
BL
E2.
Cal
iforn
iaC
on
dor
mort
alit
ies
inA
rizo
na
1996–2010.a
SB
Hat
chd
ate
Deat
hd
ate
Sex
Pri
mar
yca
use
ofdea
thA
dd
itio
nal
fin
din
gs
Gas
tric
fore
ign
bod
ies
WN
V
Liv
erb
(mg/k
g,
ww
)
Co
pp
er
Lead
Zin
c
Nest
lin
gs
(,6
mo)
527
7-M
ay-0
921-J
ul-
09
Un
kU
nkn
own,
mis
sing
Un
kn
ow
nN
Pc
ND
dN
AN
AN
A
Juve
nile
s(6
mo–
5yr
)
142
29-M
ay-9
67-J
an-9
7M
Tra
um
a,gold
en
eag
leN
on
eN
PN
D29
,1
52
151
2-J
un
-96
18-M
ay-9
7F
Pow
erlin
eco
llisi
on,
trau
ma
Non
eN
PN
D39.6
,1
64.1
128
19-A
pr-
95
14-J
ul-
97
FU
nkn
ow
n,
mis
sin
gU
nkn
ow
nN
PN
DN
AN
AN
A169
20-M
ay-9
73-O
ct-9
8M
Un
kn
ow
n,
scav
en
ged
Un
kn
ow
nN
PN
DN
AN
AN
A177
28-M
ar-9
824-D
ec-
98
MU
nkn
own,
mis
sing,
susp
ecte
dco
yote
pre
dat
ion
Un
kn
ow
nN
PN
DN
AN
AN
A
124
4-A
pr-
95
13-M
ar-9
9F
Gu
nsh
ot
Un
kn
ow
nN
PN
DN
DN
DN
D207
4-M
ay-9
915-J
an-0
0M
Asp
irat
ion
pneu
mon
iaan
dai
rsac
culit
is,
idio
pat
hic
Sep
tice
mia
(bac
teri
alro
ds)
NP
ND
23.7
,1
27.9
197
24-M
ar-9
94-F
eb
-00
FSusp
ecte
dgo
lden
eagl
eat
tack
Non
eN
PN
D94.6
,1
29.6
116
13-A
pr-
95
2-M
ar-0
0M
Tox
icos
is,l
ead
(USF
WS
For
ensi
csL
ab)
Un
kn
ow
nN
PN
DN
A32
NA
211
23-M
ay-9
921-A
pr-
00
Un
kU
nkn
own,
mis
sing
Un
kn
ow
nN
PN
DN
AN
AN
A165
20-A
pr-
97
12-J
un
-00
MT
oxic
osis
,le
adN
on
e12
Lea
dsh
otgu
npel
lets
(2si
zes)
ND
25.3
34
35.8
191
10-M
ay-9
816-J
un
-00
FT
oxic
osis
,le
adA
nem
ia,
poor
bod
yco
nd
itio
n,
ele
vat-
ed
live
rco
pp
er
NP
ND
181
17
178
182
2-A
pr-
98
22-J
un
-00
FU
nkn
own,
scav
enge
dU
nkn
ow
nN
PN
DN
AN
AN
A150
29-M
ay-9
623-J
un
-00
FU
nkn
own,
mis
sing
Un
kn
ow
nN
PN
DN
AN
AN
A184
11-A
pr-
98
9-S
ep
-00
FU
nkn
own,
scav
enge
dU
nkn
ow
nN
PN
D61.4
,1
52.7
228
28-A
pr-
009-
Feb
-01
FP
oor
bod
yco
nditio
nE
leva
ted
live
rzi
nc
and
lead
NP
ND
85.6
1116
252
11-M
ay-0
122
-Feb
-02
MU
nkn
own,
scav
enge
dU
nkn
ow
nN
PN
DN
AN
AN
A
240
11-A
pr-
01
26-A
ug-
02M
Un
kn
ow
nU
nkn
ow
nC
orr
od
ed
lead
pell
ets
inb
od
yca
vity
(US
FW
SF
ore
nsi
csL
ab)
ND
NA
NA
NA
104 JOURNAL OF WILDLIFE DISEASES, VOL. 48, NO. 1, JANUARY 2012
SB
Hat
chd
ate
Deat
hd
ate
Sex
Pri
mar
yca
use
ofdea
thA
dd
itio
nal
fin
din
gs
Gas
tric
fore
ign
bod
ies
WN
V
Liv
erb
(mg/k
g,
ww
)
Co
pp
er
Lead
Zin
c
186
15-A
pr-
98
31-A
ug-
02M
Sh
otby
arro
w(U
SF
WS
For
ensi
csL
ab)
Un
kn
ow
nN
PN
DN
AN
AN
A
258
25-M
ay-0
125
-Oct
-02
MG
unsh
ot(U
SF
WS
For
ensi
csL
ab)
Un
kn
ow
nN
PN
DN
AN
AN
A
198
31-M
ar-9
916-S
ep
-03
MU
nkn
ow
n,
auto
lysi
sN
on
eP
iece
of
bla
ckru
bb
er
hose
ND
45.9
,1
36.6
176
19-M
ar-9
811-F
eb
-04
FU
nkn
ow
n,
mis
sin
gU
nkn
ow
nN
PN
DN
AN
AN
A235
18-M
ay-0
012-J
an-0
5F
Tox
icos
is,
lead
Non
eA
sph
alt
or
rock
ND
49.2
24
28.2
249
9-M
ay-0
123-J
an-0
5M
Tox
icos
is,
lead
Non
e2
lead
shotg
un
pell
ets
ND
30.7
48
40.6
305
3-M
ay-0
329-M
ar-0
5M
Poor
bod
yco
nd
itio
nE
leva
ted
live
rle
adN
PN
D49.7
2.8
65.3
347
17-M
ay-0
49-A
pr-
05
MP
oor
bod
yco
nditio
n(p
ossi
ble
poo
rfo
ragi
ng
skill
sor
feed
ing
resp
onse
)
Non
eN
PN
D88.6
,1
162
300
18-A
pr-
03
20-M
ay-0
5F
Un
kn
ow
n,
mis
sin
gU
nkn
ow
nN
PN
DN
AN
AN
A291
27-M
ar-0
31-N
ov-
05
MU
nkn
ow
n,
auto
lysi
sU
nkn
ow
nN
PN
D14.8
,1
37.8
304
24-A
pr-
03
16-M
ar-0
6M
Tox
icos
is,
lead
(ante
mor
tem
dia
gnos
is,
under
trea
tmen
t)P
oor
bod
yco
nd
itio
n,
crop
stas
is,
elev
at-
ed
live
rco
pp
er
1m
eta
llic
pell
et
inan
tem
ort
em
x-ra
y
ND
133
2.7
127
353
7-J
un
-04
10-J
un
-06
FU
nkn
ow
n,
mis
sin
gU
nkn
ow
nN
PN
DN
AN
AN
A248
8-M
ay-0
110-J
an-0
7F
Toxi
cosi
s,le
adN
on
eL
ead
amm
un
itio
nfr
agm
en
tN
D27.6
32
39.5
343
13-M
ay-0
4M
arch
07
FU
nkn
ow
n,
mis
sin
gU
nkn
ow
nN
PN
DN
AN
AN
A281
2-M
ay-0
223-A
pr-
08
FT
rash
ingest
ion
wit
hse
con
dar
yzi
nc
toxi
cosi
sP
oss
ible
ren
algou
tan
dp
oor
bod
yco
nd
itio
n
8p
en
nie
s,2
pen
-n
yfr
agm
en
ts,
on
ed
ime,
and
on
eq
uar
ter
ND
2.2
,1
1800
384
15-M
ay-0
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tin
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.
RIDEOUT ET AL.—CALIFORNIA CONDOR MORTALITY 105
SB
Hat
chd
ate
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hd
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Sex
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use
ofd
eath
Ad
dit
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nd
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tric
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(mg/k
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)
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106 JOURNAL OF WILDLIFE DISEASES, VOL. 48, NO. 1, JANUARY 2012
post-mortem (n55). Condor 259 fromBaja California died of lead toxicosisduring treatment after accidental inges-tion of a 22-caliber bullet not known to bepresent in a donkey carcass fed to the free-ranging birds. This bird also had evidenceof focal inflammation of the brain, butWest Nile virus testing was inconclusivedue to advanced autolysis. In condor 422,feather analysis indicated at least four leadexposure events since release approxi-mately 180 days earlier with one of theexposure events producing an estimatedpeak blood lead concentration of 300 mg/dl(Fig. 3). The final lead exposure eventimmediately prior to death resulted inan estimated blood lead concentration of60 mg/dl. Three of the confirmed leadtoxicosis mortalities from California and onefrom Baja California were complicated by
visceral gout associated with chelation treat-ment. The only consistent histologic findingassociated with lead toxicosis was Kupffer cellerythrophagocytosis and hemosiderosis.
There were 22 confirmed cases oftrauma or other accident (PMR 29%;22/76) with power line collision traumaor electrocution the most important cause(11 confirmed; 7 electrocutions and 4collisions). Other causes of trauma includ-ed five confirmed predator trauma cases(two thought to be a coyote [Canis latrans]or other canid and one each of mountainlion (Puma concolor), Golden Eagle (Aq-uila chrysaetos), and undetermined).
Nine birds died from inanition, two ofwhich had a history of poor feedingresponse after release. A third was killedby a coyote, but poor body condition andsecondary ventricular candidiasis were
TABLE 3. California Condor mortalities in Baja California 2003–2010.a
SB Hatch date Death date SexPrimary cause
of deathAdditional
findings
Gastricforeignbodies
Liver (mg/kg, ww)
Copper Lead Zinc
Nestlings (,6 mo)
437 20-Apr-07 21-May-07 Unk Unknown,missing
Unknown NPb NA NA NA
531 14-May-09 20-Oct-09 Unk Trashingestion
Unknown NP NA NA NA
Juveniles (6 mo–5 yr)
279 28-Apr-02 Nov. 2004 M Unknown,missing
Unknown NP NA NA NA
338 4-May-04 7-Feb-06 Unk Unknown,scavenged
Unknown NP NA NA NA
259 26-May-01 7-Jun-06 M Toxicosis,lead
Focal en-cephalitis
22-caliberleadbullet
18.5 98 33
315 19-May-03 22-Jul-06 M Unknown,scavenged
Unknown NP NA NA NA
390 28-May-05 14-Nov-07 Unk Unknown,scavenged
Unknown NP 28 ,1 39
325 9-Apr-04 6-Dec-07 M Toxicosis,lead (antemor-tem diagnosis,under treat-ment)
Visceral goutassociatedwith chela-tion thera-py
NP 7.9 ,1 24
407 22-Apr-06 13-Dec-08 F Unknown,scavenged
Unknown NP NA NA NA
a SB 5 Studbook number; M 5 male; F 5 female; Unk 5 unknown; NA 5 not applicable; ND 5 not done; ww 5 wetweight.
b NP 5 not present.
RIDEOUT ET AL.—CALIFORNIA CONDOR MORTALITY 107
considered the primary factors. Four birdswere killed by gunshot and another byarrow. One of the gunshot birds died ofidiopathic interstitial pneumonia while be-ing treated for a severe, open, comminutedfracture of the distal right tarsometatarsuscaused by the gunshot. One additional birdhad evidence of nonfatal gunshot, withshotgun pellets embedded in the body andone wing. The only confirmed infectiousdisease was a West Nile virus infection,complicated by secondary respiratory asper-gillosis, that was the cause of death in onesubadult (450) that had been vaccinatedagainst West Nile virus (see Chang et al.,2007). Two females had ingested a variety ofsmall trash items (see Table 2), includingzinc-core pennies, which led to secondaryzinc toxicosis as the immediate cause ofdeath. Nine birds, three of them nestlings,had hepatic copper concentrations morethan four standard deviations above themean for the captive flock, but none hadlesions suggestive of copper toxicosis (e.g.,inanition and bile stasis in the liver). Two ofthem had ingested metallic trash. One bird(260) had evidence of zinc exposure butwith no ingested foreign bodies present atnecropsy.
DISCUSSION
The leading causes of death at allCalifornia Condor release sites were
anthropogenic and include lead toxicosis,power line collisions and electrocutions,trash ingestion, intentional killing, andWest Nile virus infection. The mostimportant mortality factor for the com-bined free-ranging populations was leadtoxicosis with a PMR of 26% (13/50) forjuveniles and 67% (10/15) for adults. Theevidence that the principal source ofexposure was lead ammunition is over-whelming and includes the recovery oflead shotgun pellets and bullet fragmentsfrom the upper GI tract where lead isreadily absorbed (Mautino and Bell,1986), tissue lead isotope signatures thatmatch lead ammunition and not othersources of lead (Church et al., 2006;Finkelstein et al., 2010), confirmed expo-sures from a pig carcass containing spentammunition (Finkelstein et al., 2010),
FIGURE 2. Gizzard content from condor 285.The presumed source of zinc toxicosis was thegalvanized split-metal washer at center.
FIGURE 3. Condor 422’s feather lead and esti-mated blood lead concentrations, versus estimateddays of feather growth following release into the wild,for two primary feathers collected post-mortem, leftprimary 4 (LP4; triangles) and left primary 10 (LP10;circles). Feathers were estimated to have grown overdifferent time periods following release into the wildand, combined, reflect ,160 days of growth anddocument four lead exposure events with oneexposure resulting in an estimated blood lead of,300 mg/dl (LP4). LP10 appeared to be growing atthe time of death, and the most-recent feathersection indicates condor 422 was exposed to lead justprior to death with a blood lead estimated at ,60mg/dl. Blood lead concentrations were estimatedfrom measured feather lead concentrations using ablood:feather lead concentration relationship of,20:1 (Finkelstein et al., 2010). Days of feathergrowth were determined as described by Finkelsteinet al. (2010).
108 JOURNAL OF WILDLIFE DISEASES, VOL. 48, NO. 1, JANUARY 2012
exposures coinciding with the huntingseason and foraging activity in popularhunting areas (Hunt et al., 2007; Greenet al., 2009; Parish et al., 2009), the highprevalence of bullet fragments in hunter-killed carcasses and gut piles from field-dressed kills (Hunt et al., 2006), a lack ofother plausible sources of ingestible leadthat would occur across such diversehabitats (e.g., Eisler, 1988), and the factthat mortality is rare from exposure tononmetallic sources of lead (such as paintchips and ceramic glazes; Pattee et al.,1990). Although birds from Californialacked recoverable lead ammunition inthe GI tract post-mortem, lead ammuni-tion has been recovered antemortem fromtwo California birds that survived leadtoxicosis with treatment (and are, there-fore, not part of this study) and fromanother fatal lead toxicosis case after thisstudy was completed. Three Arizona birdswith metallic densities in the GI tract onantemortem radiographs had passed thefragments by the time of the post-mortemexam. Taken together, these findingssuggest that many birds probably ingestminute lead fragments, found alongwound channels (Hunt et al., 2006), whichare then completely absorbed or partiallyabsorbed and passed by the time the birddies. A nonammunition source of leadremains a possibility in some cases, but nosuch source has yet been confirmed.
The number of lead-associated deathswould undoubtedly be higher if not forsupplemental provision of lead-free calfcarcasses at the California and Arizonarelease sites and intensive monitoring andrepeated chelation treatment of the wildpopulation for lead exposure. A specificchelation protocol was associated withfour cases of visceral gout in this study.As a result, this protocol has beendiscontinued. In spite of these lossesduring therapy, chelation has been verysuccessful overall as a treatment for acutelead toxicosis in California Condors. How-ever, prerequisite monitoring and treat-ment requires substantial investment of
resources that is not in accord withestablishment of self-sustaining popula-tions.
Power line collisions and electrocutionwere a frequent problem in California.Because of that, power pole aversiontraining began in 1994 in an attempt tokeep birds away from power lines and toreduce perching on man-made objects(Mee and Snyder, 2007). Power poleaversion training gives birds a mild shockwhen landing on power pole replicas.Visual bird-flight diverters were alsoinstalled on power lines in high risk areas,but the effectiveness of visual divertersmight be species-dependent (Martin andShaw, 2010). One collision has occurred ata power line with diverters, but thenumber of deaths attributable to powerline collisions and electrocution has de-clined significantly and no fatal collisionsor electrocutions have occurred since2007. The low number of power linefatalities noted in Arizona and BajaCalifornia is presumably due to thepresence of fewer power lines in therelease areas. Whether power line colli-sions and electrocutions contributed to thedecline of the original wild populationremains uncertain.
Parent-feeding of trash to nestlings wasthe most important cause of death in thisage class. Clearing nest caves of trash priorto hatching, and periodically throughoutthe nestling stage, has reduced but noteliminated the occurrence of foreign bodyingestion, which suggests that the majorityof foreign material is brought by the adultsto be fed to the nestlings (Mee et al.,2007). The reason(s) for this aberrantbehavior remain open to speculation, butone plausible hypothesis is that it reflectsmisdirected attempts to provide bone ormollusk shell fragments as a calciumsource for nestlings (Mee et al., 2007).Others have proposed that trash is fed toneonates as a substitute for small stonesand sticks (‘‘rangle’’) normally fed as an aidto digestion (Benson et al., 2004; Houstonet al., 2007). Polished bone fragments are
RIDEOUT ET AL.—CALIFORNIA CONDOR MORTALITY 109
now being provided as a calcium sourcefor adults to feed to nestlings. Historicaccounts suggest that this problem did notoccur to this extent prior to the releaseprogram, although some trash was foundin nests of the original wild population andthe problem has been reported to occurin some Old World Gyps spp. vulturepopulations (Snyder et al., 1986; Meeet al., 2007). Trash ingestion by nestlingsis, therefore, not likely to have been afactor in the original population decline.
West Nile virus infection is an emergingmortality factor for young, wild-hatchedbirds. Mitigating this risk is an ongoingchallenge. An experimental DNA vaccineagainst West Nile virus has been usedsuccessfully in the institutional breedingflocks (Chang, 2007) and in wild birds, butit is not protective in all individuals.Although offspring of vaccinated adultfemales with high antibody titers havepassive maternal immunity through yolkantibodies, such passive immunity wouldbe waning in many nestlings before thepeak of mosquito activity in summer,making them vulnerable to infection.Vaccination of nestlings will, therefore,continue to be required indefinitely atnest sites where West Nile virus isprevalent unless other prevention strate-gies become available.
The significance of the apparent eleva-tion of hepatic copper concentrations insome birds also remains to be clarified.There was no definitive evidence ofcopper toxicosis in any individual, butthe signs of copper toxicosis can be vagueand nonspecific. One possible coppersource would be livers from neonatal dairycalves provided as supplemental food inCalifornia and Arizona, as neonates tendto have higher hepatic copper and zincconcentrations than do adult cattle(Puschner et al., 2004a; Puschner et al.,2004b). However, if dairy calves were thesource of copper, we would have expectedto see a correlation between hepaticcopper and zinc concentrations in thesecondors, and this was not observed.
Another possible source of copper isponds and water troughs for beef cattle,as these water sources are frequentlytreated with copper sulfate in Californiato control algal growth; but this would notexplain the two juvenile birds fromArizona with apparent elevations in he-patic copper. Two nestlings with elevatedhepatic copper had ingested metallicforeign bodies, some of which could havecontained copper. However, metallic cop-per is poorly absorbed from the gastroin-testinal tract in birds (Ledoux et al., 1991).This, combined with the lack of correla-tion between hepatic copper and lead,suggests that copper jacketing on bullets isnot a likely source. Additional monitoringwill be required to determine the sourcesand significance of hepatic copper accu-mulation in free-ranging condors.
The cause of death in one condor inCalifornia was ethylene glycol toxicosis(Murnane et al., 1995). The most commonsource of ethylene glycol is automobileantifreeze. However, propylene glycol wasalso present in the kidney sample from thisindividual. Because propylene glycol is notused in combination with ethylene glycol byany antifreeze manufacturer (Dow Chem-ical technical support, pers. comm., 2009),finding both compounds together suggeststhat a possible source of exposure was anindustrial motor using ethylene glycol as acoolant and propylene glycol as a hydraulicfluid. Alternatively, exposure might haveoccurred through a carcass intentionallylaced with ethylene glycol and pesticides(which might have used propylene glycol asa vehicle) intended to kill coyotes.
The number of birds reported missingor with unknown causes of death due topoor carcass condition at recovery is high,but may be unavoidable due to the remotelocations and rugged conditions of therelease sites, particularly the Baja Califor-nia release site. These carcass-recoverydifficulties introduce a sampling bias thatcould cause over-representation of mortal-ity factors that operate in less-remote areas.Power line collisions and electrocutions, for
110 JOURNAL OF WILDLIFE DISEASES, VOL. 48, NO. 1, JANUARY 2012
example, are far more likely to be encoun-tered than most poisonings because of theproximity of power lines to roads. Deter-mining whether additional mortality factorsare operating in more-remote locations willrequire more intensive field monitoringand carcass recovery efforts.
In conclusion, the mortality factorsthought to be important in the decline ofthe historic California Condor population,particularly lead poisoning, are still im-portant. Because the risk of lead exposurefrom ammunition was likely just as greatduring the decline of the original wildpopulation (see, for example, CaliforniaDepartment of Fish and Game, 2010),these findings provide additional circum-stantial evidence that lead toxicosis wasthe primary cause of the decline of thehistoric California Condor populationthrough the mid- to late 20th century.The cumulative crude mortality rate forthe free-ranging population was 38%
during this study. In comparison, thecumulative crude mortality rate for theNorth American captive population was8% (28 nestling and 10 juvenile or adultmortalities from a maximum population-at-risk of 485). Additional investigationswill be required to determine annualpopulation-specific mortality rates andtheir projected impact on populationsustainability but, without effective miti-gation, the principal anthropogenic mor-tality factors will likely continue to havethe same impacts on population sustain-ability as they have in the past.
ACKNOWLEDGMENTS
We thank the Institute for ConservationResearch, San Diego Zoo Global, for fundingthis study and the many pathologists andveterinarians who have volunteered time tosupport the California Condor recovery pro-gram. We acknowledge the contributions ofthe many dedicated field biologists, pathologytechnicians, veterinary technicians, clinicallaboratory technicians, and support staff thatmade this work possible. We specifically thankRobert Risebrough for access to unpublisheddata and helpful comments on the manuscript;April Gorow, Julie Albright, Marc Hammond,
Yvonne Cates, Jamie Koyama, and JulieMedlock for technical and administrativeassistance; and Ken Convey and Devon Langfor map preparation. Any use of trade or firmnames is for descriptive purposes only anddoes not imply endorsement by the USGovernment.
LITERATURE CITED
BENSON, P. C., I. PLUG, AND J. C. DOBBS. 2004. Ananalysis of bones and other materials collectedby Cape Vultures at the Kransberg and Bloubergcolonies, Limpopo Province, South Africa. Os-trich 75: 118–132.
CALIFORNIA DEPARTMENT OF FISH AND GAME. 2010.Hunting license statistics by decade, http://www.dfg.ca.gov/licensing/statistics/statistics.html. Ac-cessed August 2011.
CHANG, G. J., B. S. DAVIS, C. STRINGFIELD, AND C.LUTZ. 2007. Prospective immunization of theendangered California Condors (Gymnogypscalifornianus) protects this species from lethalWest Nile virus infection. Vaccine 25: 2325–2330.
CHURCH, M. E., R. GWIAZDA, R. W. RISEBROUGH, K.SORENSON, C. P. CHAMBERLAIN, S. FARRY, W.HEINRICH, B. A. RIDEOUT, AND D. R. SMITH.2006. Ammunition is the principal source oflead accumulated by California Condors re-introduced to the wild. Environmental Scienceand Technology 40: 6143–6150.
DE FRANCISCO, N., J. D. RUIZ TROYA, AND E. I.AGUERA. 2003. Lead and lead toxicity in domesticand free living birds. Avian Pathology 32: 3–13.
EISLER, R. 1988. Lead hazards to fish, wildlife, andinvertebrates: A synoptic review. US Fish andWildlife Service Biological Report 85 (1.14), 94pp.
FINKELSTEIN, M. E., D. GEORGE, S. SCHERBINSKI, R.GWIAZDA, M. JOHNSON, J. BURNETT, J. BRANDT, S.LAWREY, A. P. PESSIER, M. CLARK, J. WYNNE, J.GRANTHAM, AND D. R. SMITH. 2010. Feather leadconcentrations and (207)Pb/(206)Pb ratios re-veal lead exposure history of California Condors(Gymnogyps californianus). Environmental Sci-ence and Technology 44: 2639–2647.
FRANSON, J. C. 1996. Interpretation of tissue leadresidues in birds other than waterfowl. InEnvironmental contaminants in wildlife: Inter-preting tissue concentrations, W. N. Beyer,G. H. Heinz and A. W. Redmon-Norwood(eds.). CRC Press, Boca Raton, Florida,pp. 265–279.
GRANTHAM, J. 2007. Reintroduction of CaliforniaCondors into their historical range: The recoveryprogram in California. In California Condors inthe 21st Century, A. Mee, L. S. Hall and J.Grantham (eds.). Series in Ornithology, No. 2.American Ornithologists Union, Washington,
RIDEOUT ET AL.—CALIFORNIA CONDOR MORTALITY 111
DC, and Nuttall Ornithological Club, Cam-bridge, Massachusetts, pp. 123–138.
GREEN, R., W. G. HUNT, C. N. PARISH, AND I.NEWTON. 2009. Effectiveness of action to reduceexposure of free-ranging California Condors inArizona and Utah to lead from spent ammuni-tion. In Proceedings of the conference: Ingestionof lead from spent ammunition: Implications forwildlife and humans, R. T. Watson, M. Fuller,M. Pokras and G. Hunt (eds.). The PeregrineFund, Boise, Idaho, pp. 240–253.
HOUSTON, D. C., A. MEE, AND M. MCGRADY. 2007.Why do condors and vultures eat junk?: Theimplications for conservation. Journal of RaptorResearch 41: 235–238.
HUNT, W. G., W. BURNHAM, C. N. PARISH, K. K.BURNHAM, B. MUTCH, AND J. L. OAKS. 2006.Bullet fragments in deer remains: Implicationsfor lead exposure in avian scavengers. WildlifeSociety Bulletin 34: 167–170.
———, C. N. PARISH, S. C. FARRY, T. G. LORD, AND
R. SEIG. 2007. Movements of introduced Cali-fornia Condors in Arizona in relation to leadexposure. In California Condors in the 21stCentury, A. Mee, L. S. Hall and J. Grantham(eds.). Series in Ornithology, No. 2. AmericanOrnithologists Union, Washington, DC, andNuttall Ornithological Club, Cambridge, Massa-chusetts, pp. 79–96.
INTERNATIONAL UNION FOR THE CONSERVATION OF
NATURE (IUCN). 1998. Guidelines for reintro-ductions. Prepared by the IUCN/SSC reintro-duction specialist group. IUCN, Gland, Switzer-land and Cambridge, UK, 10 pp.
JANSSEN, D. L., J. E. OOSTERHUIS, J. L. ALLEN, M. P.ANDERSON, D. G. KELTS, AND S. N. WIEMEYER.1986. Lead poisoning in free ranging CaliforniaCondors. Journal of the American VeterinaryMedical Association 189: 1115–1117.
KUEHLER, C. M., D. J. STERNER, D. S. JONES, R. L.USNIK, AND S. KASIELKE. 1991. Report on captivehatches of California Condors (Gymnogypscalifornianus): 1983–1990. Zoo Biology 10: 65–68.
LEDOUX, D. R., P. R. HENRY, C. B. AMMERMAN, P. V.RAO, AND R. D. MILES. 1991. Estimation of therelative bioavailability of inorganic copper sourc-es for chicks using tissue uptake of copper.Journal of Animal Science 69: 215–222.
MARTIN, G. R., AND J. M. SHAW. 2010. Bird collisionswith power lines: Failing to see the way ahead?Biological Conservation 143: 2695–2702.
MAUTINO, M., AND J. U. BELL. 1986. Experimentallead toxicity in the Ring-necked Duck. Environ-mental Research 41: 538–545.
MEE, A., AND N. F. R. SNYDER. 2007. CaliforniaCondors in the 21st Century—Conservationproblems and solutions. In California Condorsin the 21st Century, A. Mee, L. S. Hall and J.Grantham (eds.). Series in Ornithology, No. 2.
American Ornithologists Union, Washington,DC, and Nuttall Ornithological Club, Cam-bridge, Massachusetts, pp. 243–279.
———, B. A. RIDEOUT, J. A. HAMBER, J. N. TODD, G.AUSTIN, M. CLARK, AND M. P. WALLACE. 2007.Junk ingestion and nestling mortality in areintroduced population of California CondorsGymnogyps californianus. Bird ConservationInternational 17: 119–130.
MURNANE, R. D., G. MEERDINK, B. A. RIDEOUT, AND
M. P. ANDERSON. 1995. Ethylene glycol toxicosisin a captive-bred released California Condor(Gymnogyps californianus). Journal of Zoo andWildlife Medicine 26: 306–310.
PARISH, C. N., W. G. HUNT, E. FELTES, R. SEIG, AND
K. ORR. 2009. Lead exposure among a reintro-duced population of California Condors innorthern Arizona and southern Utah. In Pro-ceedings of the conference: Ingestion of leadfrom spent ammunition: Implications for wildlifeand humans, R. T. Watson, M. Fuller, M. Pokrasand G. Hunt (eds.). The Peregrine Fund, Boise,Idaho, pp. 259–264.
PATTEE, O., P. BLOOM, J. SCOTT, AND M. SMITH. 1990.Lead hazards within the range of the CaliforniaCondor. Condor 92: 931–937.
PULS, R. 1994. Mineral levels in animal health.Sherpa International, Clearbrook, Canada, pp.294–296.
PUSCHNER, B., J. ST. LEGER, AND F. D. GALEY. 1999.Normal and toxic zinc concentrations in serum/plasma and liver of psittacines with respect togenus differences. Journal of Veterinary Diag-nostic Investigation 11: 522–527.
———, Y. K. CHOI, J. H. TEGZES, AND M. C.THURMOND. 2004a. Influence of age, sex, andproduction class on liver zinc concentration incalves. Journal of Veterinary Diagnostic Investi-gation 16: 278–282.
———, M. C. THURMOND, AND Y. K. CHOI. 2004b.Influence of age and production type on livercopper concentrations in calves. Journal ofVeterinary Diagnostic Investigation 16: 382–387.
SNYDER, N., AND H. SNYDER. 2000. The CaliforniaCondor. A saga of natural history and conservation.Academic Press, San Diego, California, 410 pp.
———, R. R. RAMEY, AND R. C. SIBLEY. 1986. Nest-site biology of the California Condor. Condor 88:228–241.
WILBUR, S. 1978. The California Condor, 1966–1976:A look at its past and future. United StatesDepartment of the Interior, Fish and WildlifeService. North American Fauna 72: 1–142.
WIEMEYER, S. N., J. M. SCOTT, M. P. ANDERSON, P. H.BLOOM, AND C. J. STAFFORD. 1988. Environmen-tal contaminants in California Condors. Journalof Wildlife Management 52: 238–247.
Submitted for publication 13 December 2010.Accepted 31 August 2011.
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