PATTERNS OF MORTALITY IN FREE-RANGING CALIFORNIA CONDORS (GYMNOGYPS CALIFORNIANUS)

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: [email protected])

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


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9-M

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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

.


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

.


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

.


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


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

57-D

ec-

08

MU

nkn

ow

n,

mis

sin

g,

susp

ect

edp

red

atio

nb

yco

yote

Un

kn

ow

nN

PN

DN

AN

AN

A

372

28-A

pr-

05

23-M

ar-0

9F

Un

kn

ow

n,

scav

enged

,su

spect

edco

yote

pre

dat

ion

Un

kn

ow

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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.


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).


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


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


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.

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Submitted for publication 13 December 2010.Accepted 31 August 2011.


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PATTERNS OF MORTALITY IN FREE-RANGING CALIFORNIA CONDORS (GYMNOGYPS CALIFORNIANUS)