B I O L O G I C A L C O N S E R VAT I O N 1 2 9 ( 2 0 0 6 ) 1 3 4 –1 4 8

. sc iencedi rec t .com

ava i lab le at www

journal homepage: www.elsevier .com/ locate /b iocon

Population management of threatened taxa in captivitywithin their natural ranges: Lessons from Andeanbears (Tremarctos ornatus) in Venezuela

Kathryn M. Rodrıguez-Clark *, Ada Sanchez-Mercado

Laboratorio de Ecologıa y Genetica de Poblaciones, Centro de Ecologıa, Instituto Venezolano de Investigaciones Cientıficas,

Apartado 21827, Caracas 1020-A, Venezuela

A R T I C L E I N F O

Article history:

Received 16 June 2005

Received in revised form

31 August 2005

Accepted 17 October 2005

Available online 6 December 2005

Keywords:

Andean bear

Tremarctos ornatus

Captive breeding

Range country

Demographic and genetic

management

0006-3207/$ - see front matter � 2005 Elsevidoi:10.1016/j.biocon.2005.10.037

* Corresponding author: Tel.: +58 212 504 188E-mail address: kmrodriguezclark@gmail

A B S T R A C T

Populations of threatened taxa in captivity within their natural ranges can make important

contributions to conservation, but these may be compromised by the inappropriate appli-

cation of population management goals developed in other contexts. We conducted demo-

graphic, genetic, and population viability analyses on the captive population of Andean

bears (Tremarctos ornatus) in Venezuela to investigate the management of within-range cap-

tive populations in general, and to better integrate this population into the conservation of

Andean bears in particular. We found that although the present population is very small

and not internally self-sustaining, incorporation of confiscated wild individuals has

resulted in a low average number of generations in captivity and low inbreeding, with mod-

erate gene diversity and a high probability of future population persistence. However, past

imports from extra-range populations have been from over-represented lineages of

unknown origin, which have mixed with under-represented Venezuelan ones, reducing

the future value of the Venezuelan population as a source for founder stock. Our analyses

indicate that the rate of incorporation of wild recruits is a major factor influencing proxy

measures of conservation value, and distinguishing within- from extra-range populations.

This implies that, contrary to conventional wisdom, internal self-sustainability can be a

misguided goal in within-range populations, which furthermore may not be suitable desti-

nations for surplus animals from captive populations elsewhere.

� 2005 Elsevier Ltd. All rights reserved.

1. Introduction

With the resources required for conservation of the world�s

biodiversity far outstripping present allocations, there is an

urgent need to ensure not only that new investments are se-

cured, but that already-dedicated investments are made effi-

ciently (Balmford et al., 2003). One conservation sector which

has made advances in this area is that dealing with captive

populations, which may aid conservation through education,

fundraising, research, and breeding for release into the wild

er Ltd. All rights reserved

9; fax: +58 212 504 1617..com (K.M. Rodrıguez-Cla

(Hutchins et al., 1995). For example, the American Zoo and

Aquarium Association (AZA) and the European Association

of Zoos and Aquaria (EAZA), respectively, manage over 390

and 250 species for conservation purposes, compared with

just a handful in 1965 (AZA, 2005; EAZA, 2005). Zoo associa-

tions in Australia, Japan, and India are making similar ad-

vances; however, much untapped potential remains

elsewhere (WAZA, 2005).

A part of this potential is represented by threatened taxa

already in captivity within their natural ranges. In general,

.rk).

B I O L O G I C A L C O N S E R VAT I O N 1 2 9 ( 2 0 0 6 ) 1 3 4 –1 4 8 135

holding threatened taxa can be an efficient use of zoo re-

sources, since populations may be managed simultaneously

for a wider range of conservation goals than may non-threa-

tened taxa (Hutchins et al., 1995). Furthermore, within-range

captive populations of such groups may present distinct

advantages over extra-range ones. For example, native envi-

ronmental conditions may be easier to replicate, improving

welfare, reproduction, and ease of reintroduction, while min-

imizing exposure to non-native pathogens; location close to

human threats to species allows educational messages to

reach the most important target audiences; and captive

capacity close to natural populations may facilitate rescue

and rehabilitation of valuable wild specimens (e.g. Sanz and

Grajal, 1998; Wilcken et al., 2000).

However, worldwide, threatened species are presently dis-

tributed where present zoo capacity is not (Baillie et al., 2004;

WAZA, 2005). For example, just 9% of the AZA�smost intensive

programsare focusedon threatenedor endangered speciesna-

tive to North America (AZA, 2005). Even in the relatively pros-

perous Australasian region, whose zoo association focuses

54% of its 98 conservation breeding programs on native taxa,

thereare less thana thirdof thezoos inNorthAmerica–despite

the fact that Australasia has more than double the threatened

species (Johnson et al., 2005; AZA, 2005; IUCN, 2005). The situa-

tion is even more unbalanced in South America and Africa.

In recognition of the potential advantages of within-range

captive populations, extra-range programs for threatened

taxa may seek deliberately to develop within-range compo-

nents (e.g. US Fish and Wildlife Service, 2004; Tilson, 1998).

However, many within-range captive populations of threa-

tened taxa were initiated with no particular conservation

goals in mind. The broad aim of this paper is to consider

the value of such �happenstance� populations: how should

they be managed for maximal conservation impact, particu-

larly if extra-range programs already exist?

One approach is to apply management techniques devel-

oped largely in the context of extra-range populations. In gen-

eral, such management aims to maximize the probability of

population persistence (Ballou et al., 1995). Demographically,

the aim is often self-sustainability, in order to minimize the

need to import wild-caught individuals (Ballou and Foose,

1996). This is achieved by controlling age/sex composition,

population growth rate, and size, by manipulating parameters

under managerial control (primarily breeding opportunities,

acquisitions, and transfers), while taking into account less

easily manipulated deterministic and stochastic factors (neo-

natal mortality, litter size, age at first reproduction, etc.; Foose

and Ballou, 1988). At the same time, genetic management

aims to maximize the retention of gene diversity, and thereby

minimize inbreeding, in order to minimize inbreeding depres-

sion – and in the case of threatened taxa destined for reintro-

duction, also minimize adaptation to captivity and loss of

evolutionary potential (Rodrıguez-Clark, 1999).

However, while applying these techniques, it is important

to ask: how might differences between within-range and ex-

tra-range populations be relevant? For example, is self-sus-

tainability always a valid demographic goal? How can

exchanges between within-and extra-range populations help

or hinder management goals? The interaction of demo-

graphic and genetic forces, compounded with uncertainty

about the future, may obscure the answers to these questions,

and there are few published examples for guidance (e.g.

Frantzen et al., 2001).

Here we help fill this gap by analyzing the case of captive

Andean bears (Tremarctos ornatus) in Venezuela, to illustrate

how within-range populations in general differ in their popu-

lationmanagement, and at the same time to address a priority

identified by the action plan for T. ornatus: the integration of

the Venezuelan captive population into the conservation goals

for the species as a whole (Peyton, 1999). Our additional spe-

cific objectives for this study were therefore: (1) to determine

the age structure and growth rate of the Venezuelan captive

population, and the major factors influencing them; (2) to

determine the genetic status of the population, in terms of

inbreeding, kinship, and lineage distribution, relative to larger

extra-range captive populations; (3) to determine the impact

of past and possible future exchanges with other populations

(in North America, Europe, Colombia, and the wild in Ven-

ezuela); and (4) to identify opportunities and constraints im-

posed by these characteristics, in order to facilitate setting

realistic conservation goals for this species in captivity in

Venezuela.

2. Methods

2.1. Wild Andean bears

The Andean bear (T. ornatus) is distributed throughout the An-

des, from the Argentina/Bolivia border to Venezuela and the

Darien region of Panama, principally between 1000 and

3600 m (Peyton, 1980; Mondolfi, 1989; Suarez, 1988). Current

population estimates are based on extrapolations of data

from other bear species, and suggest a total population size

of �20,000, with the number in Venezuela less than 1000 (Pey-

ton, 1999; Kattan et al., 2004).

The distribution and generalist diet of T. ornatus have put it

in conflict with humans since pre-Colombian times, and up to

75% of range countries� human populations are concentrated

in present and former bear habitat areas (Peyton, 1999). Prin-

ciple threats in Venezuela include hunting because of per-

ceived threats to livestock and crops, as well as habitat

conversion and fragmentation due to agriculture and urbani-

zation (Goldstein, 1991; Yerena and Torres, 1994; Kattan et al.,

2004). The species was first classified as internationally

vulnerable in 1982, and is presently classified as endangered

in Venezuela (Thornback and Jenkins, 1982; Rodrıguez and

Rojas-Suarez, 1999). Because wildlife law enforcement is vari-

able, in practice T. ornatus� survival in Venezuela depends on

animals located in areas that remain inaccessible to humans

(Peyton, 1999). Although Venezuela boasts a greater propor-

tion of bear habitat under official protection than in any other

range country, rural poverty and encroachment in these lar-

gely unmarked parks threaten this protection (Rodrıguez

et al., 2003).

Information about vital rates in the wild is virtually non-

existent, since T. ornatus� mountainous habitat and shy char-

acter make habituation and radiotracking studies difficult.

Behavioral mechanisms mediating connectivity between sub-

populations, such as territoriality and dispersal, are similarly

unknown. To date, subspecies status has never been sug-

136 B I O L O G I C A L C O N S E R VAT I O N 1 2 9 ( 2 0 0 6 ) 1 3 4 –1 4 8

gested for any subpopulation (Kitchener, 1994). However,

though neighboring subpopulations such as Venezuela and

Colombia are genetically similar, significant divisions appear

to exist between these groups and those in Ecuador, Bolivia

and Peru (Ruiz-Garcıa et al., 2005).

2.2. Andean bears in captivity: North America and Europe

The earliest records of Andean bears in captivity are from

the San Diego Zoo (USA), in 1938. By 2002, there were

approximately 277 live animals in 122 institutions world-

wide, principally in North America, Europe, and South

America (Rosenthal, 2003). The American Zoo Association

(AZA) 2004–2005 Species Survival PlanTM for this species cov-

ers 73 animals (males and females = 45.28), with the follow-

ing management goals: (1) achievement of self-sustaining

demographic stability, (2) expansion to 100 individuals;

and (3) maintenance of 90% of wild genetic variation for

100 years (Long and Silver, 2005). Goals for the present

European population of 73 animals (34.36.3) are similar,

with a greater emphasis on inbreeding avoidance (Kolter,

L., personal communication). Analyses conducted below

on these populations are based on data from Rosenthal

(2003), since no births and few deaths have occurred in

these populations in recent years (Kolter, L., Weinhardt,

D., personal communication).

2.3. Andean bears in captivity in the Northern Andes:Data collection

Although organization of breeding efforts and population

records were first initiated in Venezuela over twenty years

ago (e.g. Restrepo-Valencia, 1984), and have continued at

some level since then (e.g. Torres, 1991; Bracho, 1999), there

has been little institutional structure in place to maintain

continuity. The recent creation of the Asociacion Venezolana

de Zoologicos y Acuarios (AVZA), directed by member zoos

and aquaria, may allow for a more coordinated approach.

Within the AVZA, the Grupo de Trabajo de Osos Frontinos de

Venezuela (GTOV) identified the need for the present study

(Pernalete, 2004).

To update information on Venezuelan captive bears, we

combined studbook data current to 29 July 2003 from

Rosenthal (2003) with interviews conducted with members

of the GTOV and other sources. All data were recorded in

the SPARKS database software (Scobie et al., 2004). We also

conducted a space survey using similar techniques, in order

to project capacity within the six Venezuelan institutions

able to house bears in the next 10 years. We updated stud-

book information for specimens in Colombia using similar

methods, for two reasons. First, including this population

enlarged the sample of bears in South American institu-

tions for estimates of demographic parameters. More

importantly, it allowed us to examine the potential effect

of future international exchanges on the Venezuelan popu-

lation. Colombia, as the most geographically and genetically

close population, is a natural partner to consider for such

exchanges. Data collected from both countries was subse-

quently submitted to the International Studbook for T.

ornatus.

2.4. Demographic analyses

For each management population identified (North America,

Europe, Venezuela, Colombia), we conducted analyses by

exporting data from SPARKS to Population Management

2000 (Pollak et al., 2002). We defined the Venezuelan manage-

ment population, for example, as all bears held for more than

a few months in a Venezuelan institution between January 1,

1900 and May 31, 2005.

Age-and sex-specific fecundity (Mx) was calculated as

the ratio of the number of births of one sex in a given

age class, to the total number of specimens of that sex

passing through that age class. Annual survival (Px) was

calculated similarly, replacing births with deaths, and sub-

tracting the resulting amount from 1 (except in the 0–1

age class, in which only captive-born individuals were used,

so as to not bias estimates downward by omitting unknown

mortality rates in wild-caught individuals). Wild-caught ani-

mals estimated to be over a year at capture were excluded

from demographic analyses, so that ages of all individuals

included were accurate to within a year. Estimates were

smoothed by calculating a running average across groups

of three consecutive age classes, except the first class (Wi-

ese, 2000).

Three annual percents of population change were then

projected from life tables: one for each sex, including only

births and deaths (kb), and one for both sexes combined,

including births, deaths, imports, and exports, averaged geo-

metrically over the past 10 years (kbi10). In addition, for each

population, we tallied total population size, sex ratio, annual

importation rate in the last 25 years (i25), and the stable age

distribution. Finally, we calculated the average number of

generations in captivity in each population, by assigning a

generation of 0 to each wildcaught animal, and assigning

each captive-born animal the average of the generations of

its parents, plus one.

2.5. Genetic analyses

We conducted genetic analyses using PM2000, considering

only live, reproductive individuals and their direct ancestors

(Lacy and Ballou, 2002). Colombia was the only population

with a significant proportion of animals with unknown ances-

try (5 of 30 reproductive animals); because it had many indi-

viduals from the wild (‘‘founders’’), we conservatively

assumed that those with unknown ancestry were not foun-

ders, thus excluding them from further analyses (Willis, 1993).

Genetic analyses included tallying the total number of ac-

tual and potential founders of each population, and calculat-

ing the relative contribution of each founder to the present

population (‘‘founder representation’’), along with the propor-

tion of each founder�s alleles that still survive in the present

population (‘‘maximum potential allelic retention’’), using a

gene drop analysis (Ballou and Foose, 1996). To maintain a

captive genetic profile as close as possible to the wild, the

present representation of each founder should be propor-

tional to the relative maximum potential allelic retention of

that founder. We thus calculated the percent excess or deficit

of representation of each founder as the difference between

its actual and ideal representation.

B I O L O G I C A L C O N S E R VAT I O N 1 2 9 ( 2 0 0 6 ) 1 3 4 –1 4 8 137

We then calculated four interrelated measures of genetic

uniformity and variability, from population pedigrees using

algorithms provided in PM2000 (Lacy, 1995): average inbreed-

ing coefficient ð�F ; Falconer and MacKay, 1996), mean kinship

ðMK, the average kinship of each individual to all others in

the living population; Ballou and Lacy, 1995), gene diversity

(GD, equivalent to expected heterozygosity; Nei, 1973), and

founder genome equivalents (FGEs, the number of idealized

wild individuals that have the same GD as the present popu-

lation; Lacy, 1989). All were calculated relative to a hypothet-

ical base population from which founders are drawn at

random and are assumed to be unrelated. In analyses of ex-

tra-range populations, living, wild-caught animals are nor-

mally excluded to avoid artificially inflating diversity

measures, because their presence is a usually a rare event

(Lacy and Ballou, 2002). However, we included them in our

analysis since the incorporation of wild animals is regular

occurrence in Venezuela and Colombia.

2.6. Future projections and management alternatives

In order to explore the impacts of future management alter-

natives on the Venezuelan population, we used PM2000 to

first project the expected deterministic changes in population

size and demographic structure over the next 10 years, begin-

ning with present age structures and assuming that the his-

toric importation rates and that age-and sex-specific

mortalities remained unchanged. We then compared these

projections to the number of births or imports needed to grow

from the current population size and structure to a demo-

graphically stable age distribution of the size predicted by

our space survey.

We next used the metapopulation viability analysis soft-

ware VORTEX (Lacy et al., 2005) to model the effect of a series

of management scenarios on future changes in the conserva-

tion value of our populations. We chose probability of persis-

tence, (Pp), GD, and �F as proxy indicators of value, estimating

means from 10,000 replicate runs of each scenario. While

higher quantities for the first two and lower quantities for

the last correspond to a higher conservation value, thresholds

commonly employed include maintaining Pp above 95%, GD

above 90% and �F below 12.5% for 100 years (Faust and Earn-

hardt, 2004; Ballou and Foose, 1996; Ballou et al., 2001; Allen-

dorf and Ryman, 2002).

In all scenarios, starting populations had the age struc-

tures and sizes of populations used in genetic analyses,

along with their historic pedigree relationships and mortality

rates. Age-specific fecundities were calculated from data be-

tween 1970 and 1995, to exclude the effect of fecundity re-

stricted by imperfect husbandry in early years and by

deliberate management in recent years (Long and Silver,

2005). In this dataset, 98 females bred out of 201 attaining

breeding age, so a state variable of 0 or 1 was randomly as-

signed to each female at birth or arrival into the metapopu-

lation, to select which individuals would eventually breed.

We used program default values to model the effects of

inbreeding depression, and restricted future breeding to

model optimal genetic management (using the �static list

option�; Miller and Lacy, 2005), tracking gene diversity and

inbreeding via 20 hypothetical loci.

Sensitivity analysis was then used to investigate the rela-

tive influence of variation in two factors: population size,

and origin of new members of the population (via import

from the wild, captive reproduction, or inter-population dis-

persal). In our base scenario, we used the average historical

recruitment of wild animals, and based dispersal between

North America and Europe on the 16 animals in total that

moved between these two populations in the past 60 years.

Dispersal from North America and Europe to Venezuela was

based on the recent historical rate of one animal from each

population in the last 10 years, which is roughly when these

populations began to experience surpluses. A dispersal mod-

ifier function furthermore reproduced historical patterns by

weighting dispersal among all groups toward the 0–1 age

class. Finally, we varied parameters systematically with re-

spect to the base scenario, as described in Section 3 below.

The VORTEX project file including all input values used is

available at http://www.vortex9.org/projects/venbear.vpj.

3. Results

3.1. Demographic analyses

The earliest record of an Andean bear in captivity in Venezu-

ela is at the Zoologico Las Delicias, in Maracay in 1947 (Torres,

1991). Since then, 37 animals have been held in six Venezue-

lan institutions; one of these came from the North American

population (195), and one from the European (397) (Fig. 1). As

of August, 2005, the Venezuelan population consisted of 13

live animals in four institutions. Four of these were wild-

caught males from Venezuela (orphaned cubs that hunters

had either sold or attempted to keep as pets), and nine were

captive-bred either in Europe or Venezuela.

Despite its small size, the present Venezuelan population

has a reasonably balanced distribution of sexes and age clas-

ses; North American, European and Colombian populations

are all larger, but are missing individuals in the youngest

age classes (Fig. 2). Considering all 551 individuals analyzed

together, annual survival was low in neonates (59–64%) but

high throughout peak reproductive years, with declines

beginning after about 15 years, and accelerating after 25

(Fig. 3). Fecundity peaked higher and sooner for females than

males, who experienced more balanced fecundity through-

out their lives. Fecundity and survivorship estimates were

similar in the Venezuelan population considered alone, but

small sample sizes in each age class prohibited rigorous

comparison.

When only births and deaths were considered across all

data, the average annual proportional increase projected from

life tables (kb) very slightly exceeded 1 in both males and fe-

males (1.002 and 1.007, respectively), indicating that Andean

bears are in theory capable of sustaining themselves demo-

graphically in captivity (Table 1). Rates within individual pop-

ulations varied greatly, however, from 0.82 and 0.79 in

Colombian males and females, respectively, to 1.03 and 1.02

in Europe. The average rate of wild imports over the past 25

years has differed also, with Venezuela, at 0.36 bears/year,

falling between 1.32 bears/year in Colombia and none in Eur-

ope and North America. These averages furthermore obscure

considerable within-population variation: in Venezuela, for

Fig. 1 – Pedigree of all Andean bears ever in captivity in Venezuela as of April 2005, and their direct ancestors. Captions list

international studbook numbers, house name if any (with country of origin if not Venezuela and known), and year of birth.

Females are represented by circles, males by squares, and individuals of unknown sex by diamonds. Parents are connected

by a single horizontal or diagonal line, with offspring connected via branching perpendicular lines and twins by double lines.

Bears presently or at one time in Venezuela are indicated in white (with live specimens outlined in bold); those from

European and North American institutions are in dark and light grey, respectively. Venezuelan bears with no ancestors

indicated are from the wild in Venezuela, unless otherwise noted. Individuals that are or have the potential to be genetic

founders in the Venezuelan population are indicated with a bullet point.

138 B I O L O G I C A L C O N S E R VAT I O N 1 2 9 ( 2 0 0 6 ) 1 3 4 –1 4 8

example, although nine wild animals entered the population

between 1980 and 2005, six of these were prior to 1993, and

three were in 2004–2005.

When wild captures were considered in addition to births,

population growth rates over the last 10 years (kbi10) were

much higher in Venezuela and Colombia than North America

or Europe (Table 1). Broadly speaking, therefore, North Amer-

ica and European populations have maintained themselves

entirely by reproduction, Columbia substantially by imports

from the wild, and Venezuela by a mix of the two. As a result,

the average number of generations in captivity was quite low

in Colombia (0.33), intermediate in Venezuela (0.81), and high-

er in North America and Europe (1.59 and 2.38, respectively).

3.2. Genetic analyses

Before conducting genetic analyses, we removed all females

over 25 and all males over 27 from consideration, since anal-

yses above indicated zero probability of reproduction above

these ages (Fig. 3A). Analyses below are thus based on 13 liv-

ing animals in Venezuela, 30 in Colombia, 69 in Europe, 67 in

North America, and 179 in all combined.

The unusual combination of a small size and a regular in-

put of wild founders meant that the genetic characteristics of

the living Venezuelan population compared favorably to the

other three populations analyzed in some respects, but not

others (Table 2). In just 13 animals, the Venezuelan popula-

tion carries the genetic equivalent of 4.5 hypothetical wild

founders – as compared for example with just 5.2 wild foun-

ders represented by all 69 animals considered in Europe. On

the other hand, the Venezuelan population has retained just

89% of wild genetic diversity, and MK in the Venezuelan pop-

ulation is high (0.11).

Three principal effects of historical exchange between

Venezuela and extra-range populations were clear from ge-

netic analyses: increased potential for future inbreeding ð�F Þ,the presence of highly over-represented lineages, and the

mixing of over-and under-represented lineages. �F was 3.1%

in the Venezuelan population (Table 2); however, this was

due entirely to the presence of a single individual imported

from Europe (#397; Fig. 1), whose inbreeding coefficient was

an incredible 39.8%. (All others had an F of zero). At the time

of his move, #397 was in fact the most inbred Andean bear in

captivity, with the third-highest mean kinship in Europe.

The second major effect of past exchanges was a highly

unbalanced representation of founders within the Venezue-

lan population (Fig. 4). All founders should be represented

in proportion to their maximum potential allelic retention,

such that the ideal balance of representation changes with

the reference population. Considering the Venezuelan popu-

lation in isolation, for example, (Fig. 4A) #350 (a wildcaught

Venezuelanmale) was quite over-represented, by 15.9%, while

A. Venezuela: 13 animals (8.5.0)

20

15

5

10

Males Females01234567 6 754321

Age class

C. North America: 75 animals (48.27.0) D. Europe: 73 animals (34.36.3)

B. Colombia: 33 animals (20.13.0)

20

15

5

10

Males Females01234567 7654321

Age class

unknown age (adults)

20

15

5

10

Number of individuals Number of individuals

Number of individuals Number of individuals

Males Females01234567 7 7654321

Age class

20

15

5

10

Males Females01234567 654321

Age class

Fig. 2 – Age and sex distribution of Andean bears in captivity in four regions. Actual distributions are indicated with bars, and

theoretically stable age distributions with lines.

0.05

0.00

0.10

0.15

0.20

0 2 4 6 8 10 12 14 16 18 20 22 24 26 28 30

0.0

0.2

0.4

0.6

0.8

1.0

0 2 4 6 8 10

12

14

16

18

20

22

24

26

28

30

32

34

36

38

40

A. Fecundity (Mx) B. Annual survival (Px)

%

Age class

Fig. 3 – Estimated age- and sex-specific demographic parameters in 551 Andean bears captive between January 01 1900 and

May 31, 2005 in North America, Europe, Venezuela, and Colombia. Males curves are indicated with black lines, females with

grey.

B I O L O G I C A L C O N S E R VAT I O N 1 2 9 ( 2 0 0 6 ) 1 3 4 –1 4 8 139

Table 2 – Genetic characteristics of Andean bears in four captive populations

Population N Founders �F MK GD

Actual Potential FGEs

Venezuela 13 9 11 4.49 0.031 0.11 0.89

Colombia 30 8 20 15.56 0.000 0.03 0.97

North America 67 22 22 8.74 0.009 0.06 0.94

Europe 69 19 19 5.19 0.041 0.10 0.91

All 179 36 51 15.32 0.020 0.03 0.97

N is the number of living animals considered in the analysis, while actual founders are the number of wild animals in the history of the

population that have reproduced. Potential founders furthermore include living, wild-caught, reproductive animals that have not yet repro-

duced. FGEs indicate founder genome equivalents, �F is average inbreeding, MK is average mean kinship, and GD is gene diversity.

Table 1 – Demographic population descriptors for Andean bears in four captive populations

Population kb (M) kb (F) i25 (bears/year) kbi10 Tc (generations)

Venezuela 0.87 1.02 0.36 1.09 0.81

Colombia 0.82 0.79 1.32 1.07 0.33

North America 1.00 1.01 0 1.01 1.59

Europe 1.03 1.02 0 1.02 2.38

All 1.00 1.01 1.68 1.01 1.77

kb, M and kb, F indicate the annual percent change in males and females, respectively, for a stable population with the fecundity and mortality

equivalent to those in each population since 1900, while i25 is the importation rate into the population in bears/year in the past 25 years. kbi10 is

the geometric mean percent change in population size over the last 10 years, considering imports and exports as well as births and deaths. Tc is

average number of generations the population has been in captivity.

140 B I O L O G I C A L C O N S E R VAT I O N 1 2 9 ( 2 0 0 6 ) 1 3 4 –1 4 8

#7 and #34 (European-population ancestors of #397) were

slightly under-represented. However, viewing these founders

in the context of their donor populations changed the picture

considerably (Fig. 4B and C). In fact, six of the nine founders

currently contributing to the Venezuelan population were

also themost over-represented founders in each of their donor

populations and were nearly so also in all three populations

considered as a whole (Fig. 4D). These highly over-represented

founders included not only the ancestors of the European

population�s donation to Venezuela; the ancestors of the

North American donation to Venezuela were the two foun-

ders with the highest absolute representation in the entire

population (#25 and #66).

Finally, the third effect of past exports to Venezuela was

the mixing of lineages in two undesirable ways. First, the ori-

gin of the European founders represented in the Venezuelan

population is unknown, andmay derive fromwild subpopula-

tions that are genetically differentiated from the Venezuelan/

Colombian one. If these lineages are interbred with the pres-

ent population, the only known pure Venezuelan/Colombian

subpopulation in captivity will be lost. Secondly, because

the North American bear #195 and her offspring have been

the only reproductive females in Venezuela, the very most

over-represented lineages have beenmixedwith the most un-

der-represented ones, represented by Venezuela�s wildcaught

males (Fig. 4D). This mixing cannot be remedied in the case of

#350, which is no longer alive; the only way his representation

can be increased is by also increasing that of the over-repre-

sented #66 and #25.

3.3. Future projections and management alternatives

Given the present age structure (Fig. 2) and estimated historic

vital rates (Fig. 3C and D), and assuming unlimited space and

no changes (nor random variation) in management practices,

by 2015 the Venezuelan captive population of Andean bears is

expected to grow from 13 to 22 individuals, assuming wild im-

ports continue at historical rates (henceforth referred to as

the ‘‘Base’’ scenario; Fig. 5). However, our survey of space

availability in Venezuela revealed that the current population

in fact exceeds the present capacity of suitable spaces by one

individual, and that this capacity is expected to change only

slightly in the next 10 years, with space for a total of just 15

animals projected to be available by the year 2015.

To meet this target without having to cull animals, one

obvious management intervention would be to increase the

captive capacity in Venezuela. However, this would be among

the most costly of options, and sensitivity analysis revealed

that capacity changes would have little impact on GD and �F

relative to the base scenario: even doubling capacity to 30

individuals increased GD from 89% to just 90.5% and affected

inbreeding hardly at all over the 100 years simulated (data not

shown). Similarly, the probability of population persistence

for 100 years (Pp), changed little with increases in captive

capacity.

With new recruits entering the Venezuelan popula-

tion from internal reproduction, from the wild, and from

abroad, another management option would be to eliminate

or reduce one of these sources. In contrast to changes in

-0.20

-0.10

0.00

0.10

0.20A. Venezuela

International studbook number

Rel

ativ

eex

cess

orde

ficit

ofre

pres

enta

tion

Box surroundscurrent foundersof Venezuelanpopulation.

-0.04

-0.02

0.00

0.02

0.04B. North America

-0.04

0.00

0.04

0.08C. Europe

Wild1f

363f7f 34m

25m66f

350m424m

509m479m

734m29f

54m50m

3m 4f 22m42f

33m55f

32f67m

28m63m

68f36m

35f146f

77f122f

-0.04

-0.02

0.00

0.02

0.04 D. All three

Fig. 4 – Relative excess or deficit of wild founder representation for four groupings of Andean bears. Positive values indicate

an excess in representation; negative values a deficit. Animals are arranged by descending overall representation, within two

groups: founders contributing to the Venezuelan population (inside gray box), and all others. Letters following each studbook

number indicate sex. See text for calculation of relative excess or deficit.

B I O L O G I C A L C O N S E R VAT I O N 1 2 9 ( 2 0 0 6 ) 1 3 4 –1 4 8 141

captive capacity, such changes in the origin of new recruits

had a strong influence on Pp, GD and �F in Venezuela (Fig. 6).

Some of these differences are straightforward to interpret;

for example, a self-sustaining population of 15 would have

just four females and four males of reproductive age

(Fig. 2A), and would be expected to lose GD at 6% per genera-

tion (�10 years) on average. With no influx of individuals from

elsewhere to contribute new alleles and alleviate inbreeding,

a self-sustaining population would thus be the worst possible

scenario for both GD and �F (Fig. 6A and B). Furthermore,

although this scenario is theoretically possible, random vari-

ations in demographic outcomes are important at such a

small size, and resulted in a Pp of virtually zero.

At another extreme, accomplishing population additions

entirely as imports from the wild at historical rates had sim-

ilarly straightforward impacts: it would eliminate inbreeding

entirely (by definition; Fig. 6B), and increase GD in the short

term and prevent it falling much below present levels in the

long term. However, Pp under this scenario was only 86%, as

historical survivorship and the rate of wild additions resulted

in a long-term expected population size of just five. Thus

combining these two sources of new recruits (the ‘‘base

Year

2005 2006 2007 2008 2009 2010 2011 2012 2013 2014 2015

Num

ber

of a

nim

als

0

2

4

6

8

10

12

14

16

18

20

22

24

juvenile

high reproductive

low reproductive

senescent

projectedcapacity

Fig. 5 – Projected number of Andean bears in captivity in Venezuela 2005–2015. Imported animals are assumed to be wild

cubs less than one year old, and are assumed to have the same vital rates as captive-born animals. Graphs are divided into

approximate age classes for ease of interpretation; juveniles are 0 through 2 years, high reproductives are 3 through 15, low

reproductives are 16 through 25, and senescent animals are 26 or older.

142 B I O L O G I C A L C O N S E R VAT I O N 1 2 9 ( 2 0 0 6 ) 1 3 4 –1 4 8

scenario’’) was better than either alone for maintaining a pop-

ulation size close to carrying capacity with a high GD, a rea-

sonable �F , and a high Pp (Fig. 6A and B).

The influence of the third possible origin for new recruits,

international imports, was more subtle, and depended

strongly on the relative sizes of the populations exchanging

individuals, the rates of movement between them, and the

selection criteria of individuals to be moved. Given the genet-

ic impacts of past imports from North America and Europe

(‘‘NAE imports’’) outlined above, it was perhaps expected that

replacing these imports with otherwise equivalent animals

from Colombia resulted in a higher GD in the Venezuelan

population (Fig. 6C) (also a lower �F ; data not shown). More

surprising, however, was the fact that NAE imports were ben-

eficial in Venezuela relative to the base scenario, at least in

the short and medium term: even lineages that were over-

represented elsewhere were better than insufficient recruits

or marginal additional internal reproduction within such a

small population (Fig. 6C).

Even more surprising than the potential benefit of NAE im-

ports to Venezuela, however, was their potential detriment to

North America and Europe themselves. A final possible man-

agement strategy to cope with potential future surpluses in

Venezuela is of course to export individuals. When Venezuela

was assumed to provide one individual to North America

every 10 years, in accordance with AZA recommendations

for that population (Long and Silver, 2005), NAE imports were

beneficial to Venezuela, all other things being equal (Fig. 6C).

However, such movements resulted in more rapid declines in

GD in North America relative to the base scenario: lineages

sent to Venezuela were simply reimported a few years later,

and resulted in lower GD and higher Pp in North America in

the long term (Fig. 6D).

Of all realistic scenarios examined, the one that performed

the best for maintenance of high GD and Pp with low �F in Ven-

ezuela combined: (1) continued incorporation of individuals

from the wild at historical rates, with (2) halved mortality

for those wild imports, (3) imports of cubs from Colombia at

a rate of one individual every five years, and (4) internal Ven-

ezuelan reproduction to maintain carrying capacity and pro-

duce sufficient individuals for export (Fig. 7A and B). (In

fact, under these conditions, the Venezuelan population

would be capable of producing two surplus animals every 10

years to send to Europe and/or North America). In spite of

the modest improvements of this optimum over the base sce-

nario, it remained highly sensitive to the number of animals

recruited from the wild (Fig. 7A and B)

4. Discussion

4.1. Management implications for within-rangepopulations

The present study highlights a central difference between

within-range and extra-range captive populations of threa-

tened taxa, which, if not taken into account in the application

of standardmanagementpractices, could reduce theconserva-

tion value of within-range populations. This difference, in the

probabilityof receiving recruits fromthewild,has at least three

general management implications. The first is the for impor-

tance of achieving demographic self-sustainability in within-

range populations; the second is for their suitability as a

location for surplus animals from captive populations else-

where; and the third is for the importance of planning for

uncertainty.

Although in theory the captivepopulations of Andeanbears

in both Venezuela and Colombia could be self-sustaining

(Fig. 3), at present they are not (Table 1). Being self-sustaining

is so central a goal in extra-rangemanagement that it has been

suggested that non-self-sustaining zoo populations should be

eliminated, even when they are valuable as visitor attractions

and are endangered in the wild (e.g. Wiese, 2000; Rees, 2003).

A. Origin of recruits within Venezuela:effect on Venezuelan GD and Pp

B. Origin of recruits within Venezuela:effect on Venezuelan F

C. Origin of foreign recruits to Venezuela:effect on Venezuelan GD

D. Origin of foreign recruits to Venezuela:effect on North American GD and Pp

Years in the future

Years in the future

0.72

0.76

0.80

0.84

0.88

0.92

0.96

1.00

Base (wild + internal); Pp = 0.93

Wild; Pp = 0.86

Internal; Pp = 0

Colombian

NAE

Base Colombian;Pp = 0.2

NAE; Pp = 0.1

Base

0 20 40 60 80 1000.00

0.04

0.08

0.12

0.16

0.20

0.24

0.28

0 20 40 60 80 100

Internal

Base

WildWild

0.72

0.76

0.80

0.84

0.88

0.92

0.96

1.00

0 20 40 60 80 100

0.72

0.76

0.80

0.84

0.88

0.92

0.96

1.00

0 20 40 60 80 100

Gen

edi

vers

ityor

inbr

eedi

ng

Fig. 6 – Sensitivity of gene diversity and inbreeding in captive populations of Andean bears to the origin of new recruits.

Base = as described in text. Wild = recruits to Venezuela arrive from the wild at historical rates; Internal = Internal

reproduction in Venezuela at maximal historical rates, or at whatever lower rate is sufficient to fill carrying capacity left

unfilled by other sources. NAE = North America and Europe provide imports to Venezuela at historical rates, at random with

respect to mean kinship and inbreeding, with age-dependence equal to that in historical exchanges between North America

and Europe. Colombia = equivalent to NAE, except that imports are provided by Colombia to Venezuela. Pp is the probability of

population persistence for 100 years.

B I O L O G I C A L C O N S E R VAT I O N 1 2 9 ( 2 0 0 6 ) 1 3 4 –1 4 8 143

Clearly, however, filling scarce Venezuelan capacity with cap-

tive-bred individuals makes little sense; it would increase �F

while reducing GD and Pp relative to a continuation of present

trends (Fig. 6). Requiring the Venezuelan population to be self-

sustaining would also prevent it from performing a function

uniquely suited towithin-range captive populations: receiving

confiscated or problem specimens which would otherwise be

destroyed. Accepting confiscated animals on a regular basis

is simply not legally and logistically feasible for most extra-

range populations, and the risk of supporting to an illegal mar-

ket by doing so is very real. These barriers may bemuch smal-

ler within range countries, however. Furthermore, the regular

influx of wild founders can allow within-range populations to

retain a given GD and Pp with a smaller population size, allow-

ing them to contribute to a broader range of conservation goals

without raising costs (in the spirit of the ‘‘nucleus population’’

concept; Willis and Wiese, 1993).

The higher flow of wild animals into within-range popula-

tions has a second major management implication: they are

not suitable as destinations for surplus animals from other

A. Mean gene diversity in Venezuela B. Mean inbreeding in Venezuela

Years in the future

Optimal; Pp = 0.99

Op 1/2; Pp = 0.96

Base

Op 1/4; Pp = 0.83

Op 0;Pp = 0

Optimal

Op 1/2

Base

Op 1/4

Op 0

Gen

edi

vers

ityor

inbr

eedi

ng

0.52

0.56

0.60

0.64

0.68

0.72

0.76

0.80

0.84

0.88

0.92

0.96

1.00

0 20 40 60 80 1000.00

0.04

0.08

0.12

0.16

0.20

0.24

0.28

0.32

0.36

0.40

0.44

0.48

20 40 60 80 1000

Fig. 7 – Sensitivity of gene diversity and inbreeding in the Venezuelan captive population of Andean bears to changes in

recruitment from the wild. Base is the same as in Fig. 6; Optimal is as described in the text. Values in bold indicate the rate of

imports from the wild relative to the Optimal scenario.

144 B I O L O G I C A L C O N S E R VAT I O N 1 2 9 ( 2 0 0 6 ) 1 3 4 –1 4 8

breeding programs. As captive populations are increasingly

managed for conservation goals, there are inevitably animals

superfluous to genetic and demographic aims. Given limited

space and the need to balance the welfare of individuals with

the long-term viability of captive populations, numerous

solutions have been proposed, including contraception,

euthanasia, and reintroduction – all of which may present

logistical or moral challenges (Asa et al., 1996). Placement of

individuals in ‘‘foreign zoos’’ has to date been viewed as one

of the best options, with concerns about care standards and

space availability being the primary obstacles to its wide-

spread use (Graham, 1996). However, the export of surplus

individuals from extra-range to within-range populations

may exacerbate the very management problems that they

were intended to solve. This is because international ex-

changes are used not only to alleviate ‘‘surplus animal’’ prob-

lems; they also may be sought to reduce inbreeding, increase

relative gene diversity, and reduce differentiation from wild

populations (Norton and Ashley, 2004). Past North American

and European exports of genetically undesirable individuals

to Venezuela may have relieved those regions of surplus,

but they also increased the potential for inbreeding in Vene-

zuela, introduced over-represented lineages, and mixed these

lineages with under-represented ones (Table 2, Fig. 4). While

these genetic changes are (perhaps surprisingly) not very

problematic from a strictly Venezuelan perspective (Fig. 6C),

they are from an international one. A prime potential source

for needed new founder lineages (Long and Silver, 2005) has

been made less valuable, and will become even less so if ex-

ports of surplus to Venezuela continue (Fig. 6D). A unified

way to avoid such problems in the future would be to intro-

duce truly global, rather than simply regional, captive popula-

tion management (Olney, 2005, Section 4.6). However, in the

case of T. ornatus, the considerable institutional and financial

commitments required for such management do not seem to

exist at present. For example, the international studbook kee-

per position for the species has remained vacant since 2003.

A final consequence of the increased probability of wild re-

cruits into within-range captive populations is that it adds an-

other source of uncertainty, and hence increases difficulty in

population management. Small population size combined

with large individual body size in the case of Andean bears

in Venezuela means that the difference of a few wild recruits

can have large demographic and logistical impacts: the rate of

arrival of wild recruits appears to be one of the most impor-

tant factors affecting Pp, GD, and �F (Fig. 7). In Venezuela, var-

iation in wild recruitment has been due to changing political

and legal circumstances, which are difficult to predict and

prepare for. For example, when legal changes increased the

penalty for bear poaching from a fine to up to 18 months in

jail (MARN, 1992), there was a long hiatus in confiscations

(Fig. 1) – not apparently because poaching itself lessened (Yer-

ena, 1994), but perhaps because of increased incentives to not

get caught or to repent of an illegal acquisition. Whatever its

root cause, variation in wild recruitment rates implies that

adaptive management may be more important in within-

B I O L O G I C A L C O N S E R VAT I O N 1 2 9 ( 2 0 0 6 ) 1 3 4 –1 4 8 145

range populations – ironically, even though they may have the

fewest resources to cope with such uncertainty.

The regular incorporation of wild individuals is not pres-

ently a general characteristic of many within-range captive

populations of threatened taxa managed for conservation

purposes. Such populations are primarily in North America,

Europe, and Australia, where native threatened taxa are al-

ready at very low numbers in the wild. However, it is likely

to become more of an issue as institutions in Africa, Asia,

and South America organize to manage their captive threa-

tened taxa, since many wild populations of threatened taxa

in these regions are still large enough to support illicit trade

or to come in conflict with humans. In fact, institutions in

these regions already face a flood of confiscated and problem

wildlife (e.g. Cuaron, 2005), which in more affluent regions of

the world are dealt with by dedicated wildlife rehabilitation

centers. Overwhelmed, institutions may not have the re-

sources to single out threatened taxa for special treatment.

The incorporation of wild individuals into captive populations

thus may remain most important in a well-defined set of cir-

cumstances: when taxa are threatened in the wild and main-

taining a captive population advances clear conservation

goals; when confiscations are relatively regular and in smaller

numbers; when immediate rehabilitation and release is not

desirable or feasible; and when receiving confiscations in no

way risks contributing to illicit trade or hunting.

4.2. Setting goals for the Venezuelan captive population

In addition to revealing general implications for the manage-

ment of within-range populations, our analyses highlight

three sets of observations relevant to themanagement of Ven-

ezuelan captiveAndeanbears in particular. First, in spite of the

population�s small size, bears in Venezuela retain a relatively

high number of founder genome equivalents, with a low aver-

agenumberof generations in captivity and low inbreeding, and

a high probability of population persistence as long as recruits

continue. Second, animals imported into Venezuela from ex-

tra-range populations have been from over-represented lin-

eages, (in one case of unknown geographic origin, with high

inbreeding), and these lineages have irrevocably mixed with

underrepresented wild-caught Venezuelan lineages. Finally, if

past trends continue, the populationwill expand to 22 individ-

uals by 2015, when only 15 spaces are predicted to be available.

How do these characteristics affect the range of possible con-

servation (and thus management) goals available to Andean

bears in captivity in Venezuela? Below we consider three such

conservation goals, which have successively more stringent

population management repercussions.

One potential conservation goal, which has been identified

as important for Andean bears elsewhere, is the reduction of

losses in the wild from conflict with humans (Peyton, 1999;

Rodrıguez et al., 2003). The captive population could advance

this goal in Venezuela in three ways, via education, research

and monitoring of poaching activities, and rescue of confis-

cated individuals. The location of some Venezuelan institu-

tions close to areas where conflicts occur (and of others

close to institutions where conservation policy is set and en-

forced) position them to reach out to these and other actors

with targeted educational messages, for which captive speci-

mens could be ambassadors. Investments made to reach

these groups, as well as NGOs involved in field conservation,

furthermore could facilitate the discovery of poaching inci-

dents and surviving orphans, placing zoos strategically to

aid in research about this problem (Cuaron, 2005). Finally,

confiscated orphans could be rehabilitated by zoos and main-

tained in captivity, temporarily or permanently depending on

other conservation goals. If this goal were to be adopted, pop-

ulation management aims would include maintaining a high

Pp in strategically located institutions, along with sufficient

physical and logistical capacity to receive unpredictable num-

bers of wild recruits. While the former appears to be feasible

in the Venezuelan population under a relatively wide range of

circumstances, the present small captive capacity might rep-

resent a constraint to the latter.

A second possible conservation goal for the captive popula-

tion is to directly increase small population sizes in thewild by

release of rescued individuals or their captive-bred offspring

(Harcourt, 1987). Such a goal might be controversial, as it has

been identified as important for this species in some analyses

(Rodrıguez et al., 2003), but not others (Peyton, 1999). Further-

more,while supplementationhas been considered extensively

in theory (e.g. Pedrono et al., 2004; Tenhumberg et al., 2004),

there are few published empirical studies demonstrating

cost-effectiveness and concrete conservation benefits (Fischer

and Lindenmayer, 2000), and the conditions under which suc-

cess is likely are restricted (Kleiman, 1996). For example, when

habitat loss and fragmentation are threats (as for Andean

bears), available habitat may be saturated, and the potential

genetic benefits of reducing isolation through releases (e.g,

Land and Lacy, 2000) may be outweighed by the genetic risk

of reducing the effective population size in the wild (Tufto

andHindar, 2003). Nonetheless, translocation ofwild individu-

als has been shown to be technically feasible with other bear

species, and groups are experimenting with rehabilitation

and release techniques in Andean bears where confiscations

are common (e.g. Clark et al., 2002; Castellanos, 2004). Setting

more general concerns aside, this goal would be facilitated in

the Venezuelan captive population by the populationmanage-

ment aims described above, as well as bymaintenance of pop-

ulation growth rates sufficient to sustain releases, of a low

number of generations in captivity, and of genetic stock in cap-

tivity similar to that in areas for planned releases (Kleiman,

1996). In this context, predicted surpluses in the Venezuelan

captive population and a history of receiving wild recruits rep-

resent opportunities, while the presence of genetic lineages of

unknown origin are a constraint.

A third prospective conservation goal is for the population

to serve as long-term insurance against future extinction.

Although this goal is almost universally adopted for threa-

tened taxa in captivity, the population management aims it

implies are among the most difficult to attain, including

maintenance of high Pp and GD, and avoiding high F, over long

time horizons (Ballou and Foose, 1996). Our analyses indicate,

perhaps surprisingly, that these aims are not impossible for

the Venezuelan population, again thanks largely to wild re-

cruits (Fig. 7A). While the past mixing of common and rare

lineages in the Venezuelan population may represent the

largest single inherent constraint, the same inter-institu-

tional contact that resulted in less-than-perfect exchanges

146 B I O L O G I C A L C O N S E R VAT I O N 1 2 9 ( 2 0 0 6 ) 1 3 4 –1 4 8

in the past may present an opportunity for the future. These

contacts may enhance the ability of the Venezuelan popula-

tion to further the �insurance� value of the entire captive pop-

ulation if future exchanges are made in the context of truly

global management, and include accepting surplus wild ani-

mals from Colombia, and supplying founder stock to popula-

tions in North America and Europe (Fig. 7).

Our analysis of captive Andean bears in Venezuela is thus

consistent with observations of other authors: genetic and

demographic factors may present fewer inherent obstacles

to achieving conservation goals than do logistical factors,

(such as the constantly shifting resources and personnel of

institutions), and basic biological unknowns, (such as deter-

minants of infant mortality) (Peyton et al., 1999; Frantzen

et al., 2001). While the small captive capacity in Venezuela

means that population management should ideally be nimble

and intensive (Earnhardt et al., 2001), the regular arrival of

wild recruits make the conservation value of the population

relatively robust to lapses in such management. Simple steps

that could further minimize the impact of such lapses include

continuing to improve record-keeping, confiscation protocols,

and interinstitutional communication. Given the importance

of within-range populations to the future of the global captive

Andean bear population, extra-range institutions could more-

over contribute by providing grants, organizing meetings, pro-

viding training opportunities, and by continuing to make their

own population analyses and goals readily available.

Acknowledgements

Wearegrateful tomanypeopleforhelpinguslocate information

and references for thepresentwork, includingAndres Brachoof

theRedTremarctos, LydiaKolterand JennyVanLeeuwenofEAZA,

CarolineLeesofARAZPA,andMarkRosenthalDianaWeinhardt,

BobWiese, and KevinWillis of the AZA, aswell as the dozens of

individuals at Venezuelan and Colombian zoos who provided

information about their specimens. We thank Laurie Bing-

aman-Lackey of ISIS and Robert C. Lacy of the Chicago Zoologi-

cal Society for their patient help with SPARKS, PM2000, and

VORTEX. An earlier version of this manuscript was read and

greatly improved by comments from Jon Paul Rodrıguez, Robert

C. Lacy, and two anonymous reviewers. Financial support for

this studywasprovided by ClevelandMetroparks Zoo, the Insti-

tuto Venezolano de Investigaciones Cientıficas, FONACIT grant

F-2001000902, and the Wildlife Conservation Society/Bronx

Zoo, who sponsored our copy of SPARKS.

R E F E R E N C E S

Allendorf, F.W., Ryman, N., 2002. The role of genetics inpopulation viability analysis. In: Beissinger, S.R., McCullough,D.R. (Eds.), Population Viability Analysis. Chicago UniversityPress, Chicago, pp. 50–85.

Asa, C.S., Porton, I., Baker, A.M., Plotka, E.D., 1996. Contraceptionas a management tool for controlling surplus animals. In:Kleiman, D.G., Allen, M.E., Thompson, K.V., Lumpkin, S. (Eds.),Wild Mammals in Captivity. University of Chicago Press,Chicago, pp. 451–467.

AZA, 2005. Website of the American Zoo and AquariumAssociation. Available from: http://www.aza.org/ accessed on10 March 2005.

Baillie, J.E.M., Hilton-Taylor, C., Stuart, S.N., 2004. 2004 IUCN RedList of Threatened Species: A Global Species Assessment.IUCN, Gland, Switzerland and Cambridge, UK.

Ballou, J.D., Earnhardt, J.M., Thompson, S.D., 2001. MateRX:Genetic Management Software. Smithsonian Institution,National Zoological Park, Washington, DC.

Ballou, J.D., Foose, T.J., 1996. Demographic and geneticmanagement of captive populations. In: Kleiman, D.G., Allen,M.E., Thompson, K.V., Lumpkin, S. (Eds.), Wild Mammals inCaptivity. University of Chicago Press, Chicago, pp. 263–283.

Ballou, J.D., Gilpin, M., Foose, T.J., 1995. Population Managementfor Survival and Recovery: Analytical Methods and Strategiesin Small Population Conservation. Columbia University Press,New York.

Ballou, J.D., Lacy, R.C., 1995. Identifying genetically importantindividuals for management of genetic variation in pedigreedpopulations. In: Ballou, J.D., Gilpin, M., Foose, T.J. (Eds.),Population Management for Survival and Recovery: AnalyticalMethods and Strategies in Small Population Conservation.Columbia University Press, New York, pp. 76–111.

Balmford, A., Gaston, K.J., Blyth, S., James, A., Kapos, V., 2003.Global variation in terrestrial conservation costs, conservationbenefits, and unmet conservation needs. Proceedings of theNational Academy of Sciences of the United States of America100, 1046–1050.

Bracho, A., 1999. Spectacled bears (Tremarctos ornatus) in theGustavo Rivera Zoological Park. In: Rosenthal, M.A. (Ed.),International Studbook for the Spectacled Bear 1997–1999.Lincoln Park Zoological Gardens, Chicago, IL, p. p. 239.

Castellanos, A., 2004. Andean Bear Research in the Intag Region,Ecuador. International Bear News 13, 26.

Clark, J.E., van Manen, F.T., Pelton, M.R., 2002. Correlates ofsuccess for on-site releases of nuisance black bears in GreatSmoky Mountains National Park. Wildlife Society Bulletin 30,104–111.

Cuaron, A.D., 2005. Further role of zoos in conservation:Monitoring wildlife use and the dilemma of receiving donatedand confiscated animals. Zoo Biology 24, 115–124.

Earnhardt, J.M., Thompson, S.D., Marhevsky, E.A., 2001.Interactions of target population size, population parameters,and program management on viability of captive populations.Zoo Biology 20, 169–183.

EAZA, 2005. Website of the European Association of Zoos andAquaria. Available from: http://www.eaza.net/ accessed on 10March 2005.

Falconer, D.S., MacKay, T.F.C., 1996. Introduction to QuantitativeGenetics, fourth ed. Addison Wesley Longman Limited, Essex,England.

Faust, L.J., Earnhardt, J.M., 2004. ZooRisk: A Risk Assessment Tool.Version 1.0 User�s Manual. Lincoln Park Zoo, Chicago, IL.

Fischer, J., Lindenmayer, D.B., 2000. An assessment of thepublished results of animal relocations. BiologicalConservation 96, 1–11.

Foose, T.J., Ballou, J.D., 1988. Management of small populations.International Zoo Yearbook 27, 26–41.

Frantzen, M.A.J., Ferguson, J.W.H., de Villiers, M.S., 2001. Theconservation role of captive African wild dogs (Lycaon pictus).Biological Conservation 100, 253–260.

Goldstein, I., 1991. Spectacled bear predation and feedingbehavior on livestock in Venezuela. Studies on NeotropicalFauna and Environment 26, 231–235.

Graham, S., 1996. Issues of surplus animals. In: Kleiman, D.G.,Allen, M.E., Thompson, K.V., Lumpkin, S. (Eds.), WildMammals in Captivity. University of Chicago Press, Chicago,pp. 290–296.

B I O L O G I C A L C O N S E R VAT I O N 1 2 9 ( 2 0 0 6 ) 1 3 4 –1 4 8 147

Harcourt, A.H., 1987. Options for unwanted or confiscatedprimates. Primate Conservation 8, 111–113.

Hutchins, M., Willis, K., Wiese, R.J., 1995. Strategic collectionplanning: theory and practice. Zoo Biology 14, 5–25.

IUCN, 2005. 2004 IUCN Red List of Threatened Species. Availablefrom http://www.iucnredlist.org accessed on 23 May 2005.

Johnson, K., Ford, C., Lees, C., 2005. Australasian SpeciesManagement Program: Regional Census and Plan, 15th ed.Australasian Regional Association of Zoological Parks andAquaria, Sydney, Australia.

Kattan, G., Hernandez, O.L., Goldstein, I., Rojas, V., Murillo, O.,et al, 2004. Range fragmentation in the spectacled bearTremarctos ornatus in the northern Andes. Oryx 38, 155–163.

Kitchener, A.C., 1994. A review of the evolution, systematics,functional morphology, distribution and status of the Ursidae.International Zoo News 242, 4–24.

Kleiman, D.G., 1996. Reintroduction programs. In: Kleiman, D.G.,Allen, M.E., Thompson, K.V., Lumpkin, S. (Eds.), WildMammals in Captivity. University of Chicago Press, Chicago,pp. 297–305.

Lacy, R.C., 1989. Analysis of founder representation in pedigrees:Founder equivalents and founder genome equivalents. ZooBiology 8, 111–124.

Lacy, R.C., 1995. Clarification of genetic terms and their use inthe management of captive populations. Zoo Biology 14,565–578.

Lacy, R.C., Ballou, J.D., 2002. Population Management 2000: User�sManual. Chicago Zoological Society, Brookfield, IL.

Lacy, R.C., Borbat, M., Pollak, J.P., 2005. Vortex: A StochasticSimulation of the Extinction Process. Version 9.51. ChicagoZoological Society, Brookfield, IL.

Land, E.D., Lacy, R.C., 2000. Introgression level achieved throughFlorida panther genetic restoration. Endangered SpeciesUpdate: University of Michigan School of Natural Resources17, 100–105.

Long, S., Silver, S.C., 2005. Spectacled Bear (Tremarctos ornatus)Species Survival Plan. Population Management Center, LincolnPark Zoo, Chicago, IL.

MARN (Ministerio del Ambiente y Recursos Naturales deVenezuela), 1992. Ley Penal del Ambiente. Gaceta Oficial No.4358.

Miller, P.S., Lacy, R.C., 2005. Vortex: A Stochastic Simulation of theExtinction Process. Version 9.51 User�s Manual. ConservationBreeding Specialist Group (SSC/IUCN), Apple Valley, MN.

Mondolfi, E., 1989. Notes on the distribution, habitat, food-habits,status and conservation of the spectacled bear (Tremarctosornatus Cuvier) in Venezuela. Mammalia 53, 525–544.

Nei, M., 1973. Analysis of gene diversity in subdividedpopulations. Proceedings of the National Academy of Sciencesof the United States of America 70, 3321–3323.

Norton, J.E., Ashley, M.V., 2004. Genetic variability and populationdifferentiation in captive Baird�s tapirs (Tapirus bairdii). ZooBiology 23, 521–531.

Olney, P.J.S. (Ed.), 2005. Building a Future for Wildlife: The WorldZoo and Aquarium Conservation Strategy. World Associationof Zoos and Aquaria, Berne, Switzerland.

Pedrono, M., Smith, L.L., Clobert, J., Massot, M., Sarrazin, F., 2004.Wild-captive metapopulation viability analysis. BiologicalConservation 119, 463–473.

Pernalete, J.M., 2004. Grupo de Trabajo de Osos Frontinos deVenezuela: Acta Constitutiva, Estatutos, y Minuta No. 1. Page 9.Asociacion Venezolana de Parques Zoologicos y Acuarios,Barquisimeto.

Peyton, B., 1980. Ecology, distribution, and food habits ofspectacled bears, Tremarctos ornatus, in Peru. Journal ofMammalogy 61, 639–652.

Peyton, B., 1999. Spectacled bear conservation action plan. In:Servheen, C., Herrero, S., Peyton, B. (Eds.), Bears: Status Survey

and Conservation Action Plan. IUCN, Gland, Switzerland, pp.157–198.

Peyton, B., Servheen, C., Herrero, S., 1999. An overview of bearconservation planning and implementation. In: Servheen, C.,Herrero, S., Peyton, B. (Eds.), Bears: Status Survey andConservation Action Plan. IUCN, Gland, Switzerland, pp. 8–24.

Pollak, J.P., Lacy, R.C., Ballou, J.D., 2002. Population Management2000, version 1.16. Chicago Zoological Society, Brookfield, IL.

Rees, P.A., 2003. Asian elephants in zoos face global extinction:should zoos accept the inevitable? Oryx 37, 20–21.

Restrepo-Valencia, N., 1984. Propuesta para la creacion de uncentro de crıa en cautiverio para el oso deanteojos (Tremarctosornatus). In: Weinhardt, D. (Ed.), International Studbook forthe Spectacled Bear. Lincoln Park Zoological Gardens, Chicago,pp. 94–115.

Rodrıguez, D., Cuesta, F., Goldstein, I., Bracho, A., Naranjo, L.G.,et al. 2003. Estrategia ecorregional para la conservacion del osoAndino (Tremarctos ornatus) en los Andes del Norte. WWFColombia, EcoCiencia, Fundacion Wii, Wildlife ConservationSociety, Cali, Colombia, p. 72.

Rodrıguez, J.P., Rojas-Suarez, F., 1999. El Libro Rojo de la FaunaVenezolana, segundaedicion. Provita-FundacionPolar,Caracas.

Rodrıguez-Clark, K.M., 1999. Genetic theory and evidencesupporting current practices in captive breeding forconservation. In: Dobson, A.P., Landwebber, L.F. (Eds.),Genetics and the Extinction of Species: DNA and theConservation of Biodiversity. Princeton University Press,Princeton, NJ, pp. 47–73.

Rosenthal, M., 2003. International Studbook for the Andean Bear(Tremarctos ornatus) 2000–2002. Lincoln Park Zoo, Chicago, IL.

Ruiz-Garcıa, M., Orozco-Terwengel, P., Castellanos, A., Arias, L.,2005. Microsatellite analysis of the spectacled bear (Tremarctosornatus) across its range distribution. Genes and GeneticSystems 80, 57–69.

Sanz, V., Grajal, A., 1998. Successful reintroduction of captive-raised yellow-shouldered Amazon parrots on Margarita Island,Venezuela. Conservation Biology 12, 430–441.

Scobie, P.N., Lackey, L.B., Porter, S., Princee, F. 2004. SPARKS: SinglePopulation Analysis and Record Keeping System, Version 1.5.International Species Information Systems, Eagan, Minnesota,USA.

Suarez, L., 1988. Seasonal distribution and food-habits ofspectacled bears (Tremarctos ornatus) in the highlands ofEcuador. Studies on Neotropical Fauna and Environment 23,133–136.

Tenhumberg, B., Tyre, A.J., Shea, K., Possingham, H.P., 2004.Linking wild and captive populations to maximize speciespersistence: Optimal translocation strategies. ConservationBiology 18, 1304–1314.

Thornback, J., Jenkins, M., 1982. The IUCNMammal Red Data Book:The Americas and Australasia. IUCN, Gland, Switzerland.

Tilson, R. 1998. American Zoo and Aquarium Association (AZA)North American Amur (Siberian) Tiger Species Survival Plan(SSP) Master Plan – 1998. Minnesota Zoo, Apple Valley,Minnesota, p. 56.

Torres, D.A., 1991. Management of the spectacled bear inVenezuelan zoological parks (F. Cuvier, 1825). In: Weinhardt, D.(Ed.), International Studbook of the Spectacled Bear Tremarctosornatus. Lincoln Park Zoological Gardens, Chicago, pp. 83–103.

Tufto, J., Hindar, K., 2003. Effective size in management andconservation of subdivided populations. Journal of TheoreticalBiology 222, 273–281.

US Fish andWildlife Service, 2004. Draft Revised Recovery Plan forthe Sihek or guam Micronesian Kingfisher (Halcyoncinnamomina cinnamomina). Portland, OR. Ix + 99 pages.

WAZA, 2005. Membership list of the World Association of Zoosand Aquariums. Available from: http://www.waza.org/network/index.php?main=zoos&view=namerica, http://

148 B I O L O G I C A L C O N S E R VAT I O N 1 2 9 ( 2 0 0 6 ) 1 3 4 –1 4 8

www.waza.org/network/index.php?main=zoos&view=samerica,http://www.waza.org/network/index.php?main=zoos&view=europe, http://www.waza.org/network/index.php?main=zoos&view=asia, http://www.waza.org/network/index.php?main=zoos&view=africa, http://www.waza.org/network/index.php?main=zoos&view=oceania accessed on 10 March 2005.

Wiese, R.J., 2000. Asian elephants are not self-sustaining in NorthAmerica. Zoo Biology 19, 299–309.

Wilcken, J., Johnson, K., Lees, C. (Eds.), 2000. Australasian SpeciesManagement Program: Regional Census and Plan, 10th ed.Australasian Regional Association of Zoological Parks andAquaria, Sydney, Australia.

Willis, K., 1993. Use of animals with unknown ancestries inscientifically managed breeding programs. Zoo Biology 12,161–172.

Willis, K., Wiese, R.J., 1993. Effect of new founders on retentionof gene diversity in captive populations: A formalization of thenucleus population concept. Zoo Biology 12, 535–548.

Yerena, E., 1994. Parques nacionales y conservacion ambiental:corredores ecologicos en los Andes de Venezuela. FundacionPolar, Caracas.

Yerena, E., Torres, D.A., 1994. Spectacled bear conservation anddispersal corridors in Venezuela. International Conference ofBear Research and Management 9, 169–172.