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An Emerging Role of Zoos to Conserve Biodiversity

  • Species360, (former International Species Information System) and University of Southern Denmark
  • International Species Information System


Roughly one in seven threatened terrestrial vertebrate species are held in captivity, a resource for ex situ conservation efforts.
A t the October 2010 meeting of the
Convention on Biological Diversity
(CBD) in Nagoya, Japan, delegates
discussed a plan to reduce pressures on the
planet’s biodiversity. Key targets include
expanding coverage of protected areas, halv-
ing the rate of loss of natural habitats, and
preventing extinction of threatened species
( 1). For species whose habitat is severely
threatened, however, the outlook is so bleak
that the International Union for Conservation
of Nature (IUCN), the U.S. Endangered Spe-
cies Act, and the CBD (Article 9) recognize
that in situ conservation actions (i.e., in the
species’ natural habitat) will need to be com-
bined with ex situ approaches, such as captive
breeding in zoos, aquariums, and so on ( 2, 3).
Captive breeding may be the only short-
term practical conservation option for species
confi ned to dwindling habitats ( 4). However,
captive breeding is absent or plays a minor
role in the policies of most governments, con-
servation organizations, and multilateral insti-
tutions. To shed light on the state of captive
breeding and its potential to contribute to con-
servation goals, we estimate the number of
threatened species already held in captivity.
Captive Breeding
Although ecosystem health should be a con-
servation priority, a recent evaluation of the
status of the world’s vertebrates ( 5) noted that
captive breeding played a major role in the
recovery of 17 of the 68 species whose threat
level was reduced [e.g., Przewalski’s wild
horse (Equus ferus przewalskii) ( 6), black-
footed ferret (Mustela nigripes) ( 7), and Cal-
ifornia condor (Gymnogyps californianus)
( 8)]. Captive breeding has the potential to
maintain targeted populations as an “insur-
ance policy” against threats like disease or
pressure from nonnative species [e.g., egg
predators on islands ( 9)] until reintroduction
into the wild is possible. A striking example
is the increase of amphibian collections in
zoos ( 10) as a response to chytridiomycosis,
a fungal infection responsible for precipitous
global amphibian population declines ( 11).
Captive breeding for reintroduction has
downsides. Sociopolitical factors can deter-
mine the success of programs. For example,
reintroduction of Arabian oryx (Oryx leu-
coryx) in central Oman was hampered by
poaching, partly because local communities
were insuffi ciently involved in conser vation
efforts ( 12, 13). Furthermore, captive breed-
ing is costly, and technical diffi culties can
arise such as hybridization [breeding among
different species ( 14), e.g., if current cryp-
tic species are managed as one species, but
are later split into several species according
to new taxonomic information]. The abil-
ity of individuals to learn crucial skills that
allow them to survive in the wild (e.g., fear
of humans or predators) may be compro-
mised. In many cases, these diffi culties have
been overcome by creative and species-spe-
cifi c measures. For example, it was feared
that Puerto Rican parrots (Amazona vittata)
would be unable to escape predators in the
wild, but this problem was solved with a pre-
release aviary-based stimulation and exercise
program ( 15). Because ex situ conservation
programs can be challenged when called into
action at the last possible moment with only a
few remaining individuals of a species, cap-
tive breeding should not simply be seen as
“emergency-room treatment.” It is a tool that
should be considered before the species has
reached the point of no return.
Counting Threatened Species in Captivity
We used the International Species Informa-
tion System (ISIS) database to estimate the
number of threatened species already held in
captivity. ISIS is an organization that holds
the most comprehensive information on
animals held in zoos and aquariums world-
wide, with records of ~2.6 million individu-
als shared among ~800 member institutions
( 16). From the IUCN Red List of Threatened
Species ( 17), we obtained the threat category
of each terrestrial vertebrate species repre-
sented in ISIS ( 18). [See supporting online
materials (SOM) for details.]
One-quarter of the world’s described bird
species and almost 20% of the mammal spe-
cies are held in ISIS zoos (table S1). Only
12% of the described reptile species are rep-
resented and 4% of amphibians. Our primary
focus is on species of conservation concern;
for mammals, roughly one-fi fth to one-quar-
ter of threatened ( 19) and Near-Threatened
species are represented in ISIS zoos (see
the fi gure) (table S1). With the exception of
Critically Endangered species, which only
have a 9% representation (tables S1 and S2),
the picture is similar for birds. For amphib-
ians, the representation of threatened spe-
cies is much lower (~3%); this is a concern
because amphibians are a highly threatened
group, with 41% of described species listed
as threatened or Extinct in the Wild (EW) ( 5).
The IUCN threat-level assessment for rep-
tiles has not been completed, so our results
should be interpreted with caution, but of the
1672 species already evaluated, zoos hold
37% of threatened and 18% of Near-Threat-
ened species.
Overall, zoos and aquariums hold roughly
one in seven threatened species (15%), but it
is important to consider also the number of
individuals held. Although individual zoos
might not have large populations of a par-
ticular species, collectively, zoos hold siz-
able populations of certain species, including
highly threatened ones (see the fi gure). Zoos,
as a global network, should strive to ensure
that their populations of threatened species
can survive in the long term. However, each
zoo may make a larger conservation contri-
bution by specializing in breeding a few at-
risk targeted species, rather than aiming to
increase its species diversity, as specialization
increases breeding success ( 4).
Ultimately, success of conservation
actions depends on the extent to which birth
and death rates permit populations to survive
in the wild ( 8). Population viability analyses
(PVAs) are used to forecast the probability of
population extinction for conservation pro-
grams ( 20), but these require parameteriza-
tion with data on age-specifi c birth and death
rates ( 21). Adequate data from natural envi-
ronments are often unavailable, especially for
threatened species ( 20). The zoo network has
large long-term data sets, including data such
as average litter size, interval between succes-
sive litters, and age at maturity, which could
be used to fi ll these gaps. Of course, zoo data
should be used with caution because they
An Emerging Role of Zoos
to Conserve Biodiversity
D. A. Conde,
1 * N. Flesness, 2 F. Colchero,
1 O. R. Jones,
1 A. Scheuerlein
Roughly one in seven threatened terrestrial
vertebrate species are held in captivity,
a resource for ex situ conservation efforts.
*Author for correspondence:
1Max Planck Institute for Demographic Research, Rostock
18057, Germany. 2International Species Information Sys-
tem, Eagan, MN 55121, USA.
Published by AAAS
on September 28, 2012www.sciencemag.orgDownloaded from SCIENCE VOL 331 18 MARCH 2011 1391
Number of species
Number of individuals
Percentage of
pecies per interval
25% 24% 23%
19% 100%
In zoos
21 27 25 27
Species (ranked by number of individuals)
9% 100%
840 29 23
28% 51% 0%
640 32 22
6% 4% 2% 3% 50%
24 10 18 48
NT: Near threatened VU: Vulnerable EN: Endangered CR: Critically endangered EW: Extinct in the wild
do not necessarily refl ect the situation in the
wild, such as population fl exibility in the face
of changing conditions.
Despite their current and potential contri-
butions to species conservation, ISIS zoos are
concentrated in temperate regions, whereas
most threatened species are tropical ( 5, 22)
(fi g. S1). This mismatch between the areas
where captive populations are held and their
native range poses a challenge for imple-
mentation of effective conservation actions.
Acclimatization to a new home is likely to be
faster for animals raised in conditions similar
to those where they are to be released. This
is one reason that it is suggested that captive
breeding be done in the country of the spe-
cies’ origin ( 2).
There are large parts of the world with high
biodiversity value, yet whose zoos are not
well represented in a global network (fi g. S1).
Given the importance of having data avail-
able for design of conservation programs,
policy-makers must encourage and facilitate
the participation of zoos from regions with
high levels of biodiversity threat in global
networks, such as ISIS and the World Asso-
ciation of Zoos and Aquariums (WAZA).
The potential for zoos to contribute to
conservation is not a new concept for the zoo
community. Zoos and aquariums have devel-
oped conservation projects in the wild, along-
side research and education programs ( 23).
For exam ple, mem bers of WAZA collectively
spend ~U.S. $350 million per year on conser-
vation actions in the wild, which makes them
the third major contributor to conservation
worldwide after the Nature Conservancy and
the World Wildlife Fund global network ( 24).
Given the scale of the biodiversity challenge,
it is vital that conservation bodies and policy-
makers consider the potential that zoos as a
global network can provide.
References and Notes
1. D. Normile, Science Insider, 29 October 2010; http://
2. Convention on Biological Diversity, Article 9, United
Nations—Treaty Series, pp. 149 and 150 (1993).
3. IUCN, IUCN Technical Guidelines on the Management of
Ex Situ Populations for Conservation (IUCN, Gland, Swit-
zerland, 2002), p. 4.
4. W. G. Conway, Zoo Biol. 30, 1 (2011).
5. M. Hoffmann et al., Science 330, 1503 (2010).
6. M. C. Van Dierendonck, M. F. Wallis de Vries, Conserv.
Biol. 10, 728 (1996).
7. J. Belant, P. Gober, D. Biggins, in IUCN Red List of Threat-
ened Species, Version 2010.4 (IUCN, Gland, Switzerland,
8. V. J. Meretsky, N. F. R. Snyder, S. R. Beissinger, D. A. Clen-
denen, J. W. Wiley, Conserv. Biol. 14, 957 (2000).
9. J.-C. Thibault, J.-Y. Meyer, Oryx 35, 73 (2001).
10. Amphibian Ark,
11. L. F. Skerratt et al., EcoHealth 4, 125 (2007).
12. J. A. Spalton, M. W. Lawerence, S. A. Brend, Oryx 33, 168
13. V. Morell, Science 320, 742 (2008).
14. R. Barnett, N. Yamaguchi, I. Barnes, A. Cooper, Conserv.
Genet. 7, 507 (2006).
15. T. H. White, J. A. Collazo, F. J. Vilella, Condor 107, 424
16. International Species Information System,
17. IUCN, IUCN Red List of Threatened Species, Version 3.1
(IUCN, Gland, Switzerland, 2009);
18. ISIS and IUCN information were matched on the species
level using the Catalogue of Life (F. A. Bisby et al., Eds.);
19. Threatened species are those listed as Critically Endan-
gered (CR), Endangered (EN), or Vulnerable (VU) by IUCN.
20. T. Coulson, G. M. Mace, E. Hudson, H. Possingham,
Trends Ecol. Evol. 16, 219 (2001).
21. J. M. Reed et al., Conserv. Biol. 16, 7 (2002).
22. R. Grenyer et al., Nature 444, 93 (2006).
23. WAZA, Building a Future for Wildlife: The World Zoo and
Aquarium Conservation Strategy (WAZA, Berne, Switzer-
land, 2005).
24. M. Gusset, G. Dick, Zoo Biol., 6 December 2010 (http://
25. We thank J. Vaupel, M. Gusset, C. D. L. Orme, D. Levitis,
D. de Man, W. van Lint, K. Zippel, S. Möller, J. Runge, E.
Brinks, G. Fiedler, P. Kutter, and F. Quade. We also thank
three anonymous referees.
Endangered species in zoos. (Top) The number of
species with IUCN status, globally described (color
bars) and in ISIS zoos (black bars). (Bottom) The
number of individuals in ISIS zoos for species listed
by IUCN—for mammals (142 species), birds (83 spe-
cies), reptiles (90 species), and amphibians (29 spe-
cies). The vertical broken lines show the boundaries
by 250, 50, and 10 individuals. The large numbers of
individuals classifi ed as Vulnerable and Near Threat-
ened are omitted for clarity. See SOM for details.
Supporting Online Material
Published by AAAS
on September 28, 2012www.sciencemag.orgDownloaded from
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Population viability analysis ( PVA) has become a commonly used tool in endangered species management. There is no single process that constitutes PVA, but all approaches have in common an assessment of a population's risk of extinction (or quasi extinction) or its projected population growth either under current conditions or expected from proposed management. As model sophistication increases, and software programs that facilitate PVA without the need for modeling expertise become more available, there is greater potential for the misuse of models and increased confusion over interpreting their results. Consequently, we discuss the practical use and limitations of PVA in conservation planning, and we discuss some emerging issues of PVA. We review extant issues that have become prominent in PVA, including spatially explicit modeling, sensitivity analysis, incorporating genetics into PVA, PVA in plants, and PVA software packages, but our coverage of emerging issues is not comprehensive. We conclude that PVA is a powerful tool in conservation biology for comparing alternative research plans and relative extinction risks among species, but we suggest caution in its use: (1) because PVA is a model, its validity depends on the appropriateness of the model's structure and data quality; (2) results should be presented with appropriate assessment of confidence; (3) model construction and results should be subject to external review, and (4) model structure, input, and results should be treated as hypotheses to be tested. We also suggest (5) restricting the definition of PVA to development of a formal quantitative model, (6) focusing more research on determining how pervasive density-dependence feedback is across species, and (7) not using PVA to determine minimum population size or (8) the specific probability of reaching extinction. The most appropriate use of PVA may be for comparing the relative effects of potential management actions on population growth or persistence. Resumen: El análisis de viabilidad poblacional (AVP) es una herramienta de uso común en el manejo de especies en peligro. No hay un proceso único que constituya al AVP, pero todos los enfoques tienen en común la estimación del riesgo de extinción (o cuasi extinción) o la proyección del crecimiento poblacional, ya sea bajo las condiciones actuales o las esperadas del manejo propuesto. A medida que aumenta la sofisticación del modelo, y que se dispone de programas de cómputo que facilitan el AVP sin necesidad de experiencia en modelaje, hay una mayor posibilidad de desaprovechar el modelo y una mayor confusión en la interpretación de los resultados. En consecuencia, discutimos el uso práctico y las limitaciones del AVP en la planificación de conservación y discutimos algunos temas emergentes del AVP. Revisamos temas vigentes que son prominentes en el AVP, incluyendo el modelaje espacialmente explícito, el análisis de sensibilidad, la inclusión de la genética en el AVP, AVP en plantas y paquetes de cómputo de AVP, sin embargo nuestra revisión de los temas emergentes no es amplia. Concluimos que el AVP es una herramienta poderosa para la biología de la conservación para comparar planes de investigación alternos y los riesgos de extinción entre especies, pero sugerimos precaución en su uso: (1) porque el AVP es un modelo cuya validez depende en la eficacia de la estructura del modelo y la calidad de los datos, (2) los resultados deberían presentarse con la evaluación de su confiabilidad, (3) la construcción del modelo y sus resultados deberían ser sometidos a revisión externa y (4) la estructura del modelo, los datos y los resultados deberían ser tratadas como hipótesis a probar. También sugerimos (5) restringir la definición del AVP para desarrollar un modelo cuantitativo formal, (6) realizar más investigación para determinar que tan extensa es la reacción de las especies a la denso-dependencia y (7) no utilizar el AVP para determinar el tamaño poblacional mínimo u (8) la probabilidad específica de extinción. El uso más adecuado del AVP puede ser para comparar los efectos relativos de las acciones de manejo sobre el crecimiento de la población o su persistencia.
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Global conservation strategies commonly assume that different taxonomic groups show congruent geographical patterns of diversity, and that the distribution of extinction-prone species in one group can therefore act as a surrogate for vulnerable species in other groups when conservation decisions are being made. The validity of these assumptions remains unclear, however, because previous tests have been limited in both geographical and taxonomic extent. Here we use a database on the global distribution of 19,349 living bird, mammal and amphibian species to show that, although the distribution of overall species richness is very similar among these groups, congruence in the distribution of rare and threatened species is markedly lower. Congruence is especially low among the very rarest species. Cross-taxon congruence is also highly scale dependent, being particularly low at the finer spatial resolutions relevant to real protected areas. `Hotspots' of rarity and threat are therefore largely non-overlapping across groups, as are areas chosen to maximize species complementarity. Overall, our results indicate that `silver-bullet' conservation strategies alone will not deliver efficient conservation solutions. Instead, priority areas for biodiversity conservation must be based on high-resolution data from multiple taxa.
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We report first-year survival for 34 captive-reared Puerto Rican Parrots (Amazona vittata) released in the Caribbean National Forest, Puerto Rico between 2000 and 2002. The purpose of the releases were to increase population size and the potential number of breeding individuals of the sole extant wild population, and to refine release protocols for eventual reintroduction of a second wild population elsewhere on the island. After extensive prerelease training, we released 10 parrots in 2000, 16 parrots in 2001, and eight parrots in 2002 ranging in age from 1-4 years old. All birds were equipped with radio-transmitters to monitor survival. The overall first-year survival estimate for the 34 parrots was 41 % (Cl 22%-61%). Only one parrot died within the first week postrelease, with most (94%) surviving for at least eight weeks after release. Most (54%) documented mortalities were due to raptor predation, which claimed 21 % of all released parrots. A captive-reared bird (male, age one), released in 2001, paired with a wild female and fledged two young in 2004. We also calculated survival based on 0% and 50% of observed predation losses and found hypothetical survival rates of 72% and 54%, respectively. Rigorous prerelease training and acclimation was believed to have improved initial postrelease parrot survival, and releasing mixed age-class groups suggests the potential for shortening the time to recruitment.
Experiences with the réintroduction of the takhi, or Przewalski horse (Equus fcrus przewalskit), in Mongolia can serve as valuable lessons for réintroduction of ungulates in general. We discuss the present taxonoinic, historical, and biological evidence and conclude that the takhi should be viewed as a typical steppe herbivore. Its last refuge, the Dzungarian Gobi, should therefore be seen as a marginal habitat because it consists mainly of desert and semidcsert. Since 1992 two réintroduction projects have been in the acclimatization phase in Mongolia. Despite promising developments, problems with cooperation, management, habitat choice, insufficient knowledge of the ethology of the species, and current land use within the different project areas could jeopardize the successful réintroduction of takhi. We review the conditions required for a potentially successful ungulate réintroduction. Ttie planning of a reintroduction within the framework of safeguarding an entire ecosystem with an integrated management plan appears essential. Each potential réintroduction site should be assessed thoroughly for its suitability, including size, habitat types, current land use, socioeconotnics, legislation, and potential problems. Each site should be provided with one or more acclimatization facilities to harbor genetically and physically healthy, socially adapted animals in biologically sound groups. An organization structure should be established for each reintroduction site. Its objective should be to develop an effective management plan and to carefully monitor the population and its surrounding ecosystem. Special attention should be given to local socioeconomic situations, community participation, and train- . ing of staff for management, research, and ranger and warden activities.
The return of the Arabian oryx Oryx leucoryx to Oman symbolized the success of a new approach to species conservation and established reintroduction as a conservation tool. Ten years after the species had been exterminated in the wild by poaching, the first 10 founder oryx, descendants of the ‘World Herd’, were reintroduced to the desert in central Oman in January 1982. A second release followed in 1984 and the population grew slowly through a 3-year drought that was broken by rain in June 1986. Further years of good rainfall and more founders meant that by April 1990 there were over 100 oryx in the wild, independent of supplementary feed and water, and using a range of over 11,000 sq km. At that time a new monitoring programme was implemented that allowed the transition from individual- to population-based monitoring and management. The population continued to grow and by October 1995 numbered approximately 280 in the wild (of which 22 were surviving founders) and used over 16,000 sq km of the Arabian Oryx Sanctuary. However, in February 1996 poaching resumed and oryx were captured for sale as live animals outside the country. Despite the poaching the population continued to increase and by October 1996 was estimated to be just over 400. However, poaching intensified and continued through late 1996 and 1997. By September 1998 it had reduced the wild population to an estimated 138 animals, of which just 28 were females. The wild population was no longer considered viable and action was taken to rescue some of the remaining animals from the wild to form a captive herd.
Four species of monarchs (Pomarea spp.) presently inhabit French Polynesia, one on Tahiti and three on the Marquesas Islands. Although all species populations were abundant during the nineteenth century or at the beginning of the twentieth century, their range and population numbers have recently decreased dramatically: intensive field surveys conducted between 1998 and 2000 reveal that four subspecies are now extinct from five islands in the Marquesas in the last decades. Introduction of the black rat is the major cause of extinction and decline, now amplified by new threats such as aggressive introduced birds and invasive alien plants reducing suitable habitats for breeding.
The remnant wild population of California Condors (Gymnogyps californianus) of the 1980s exhibited a rapid population decline caused by high mortality rates among adult and immature birds. The most prominent mortality factor was lead poisoning resulting from ingestion of bullet fragments in carcasses. Successful captive breeding has allowed many birds to be released to the wild since 1992, based originally on an assumption that exposure to lead could be prevented by food subsidy. The mortality of released birds, however, has generally exceeded levels needed for population stability calculated from simple population models. Collision with overhead wires was the most frequent cause of death in releases before 1994. Lead poisoning again surfaced as a problem starting in 1997 as older birds began feeding on carcasses outside the subsidy program. Although poisonings have been treated successfully by chelation therapy in recaptured birds, food subsidy is proving an ineffective solution to lead exposure. The best long-term solution appears to be either the creation of large reserves where hunting is prohibited or the restriction of hunting to nontoxic ammunition in release areas. Until sources of lead contamination are effectively countered, releases cannot be expected to result in viable populations. In addition, problems involving human-oriented behavior have resulted in the permanent removal of many released birds from the wild. The most promising reduction in human-oriented behavior has been achieved in one release of aversively conditioned, parent-reared birds. Rigorous evaluation of the factors reducing attraction to humans and human structures has been hampered by confounding of techniques in releases. Behavioral problems could be more quickly overcome by adoption of a comprehensive experimental approach.