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POLICYFORUM

CONSERVATION

An Emerging Role of Zoos to Conserve Biodiversity


D. A. Conde,1* N. Flesness,2 F. Colchero,1 O. R. Jones,1 A. Scheuerlein1

Roughly one in seven threatened terrestrial vertebrate species are held in captivity, a resource for ex situ conservation efforts.

Captive Breeding

Although ecosystem health should be a conservation priority, a recent evaluation of the status of the worlds 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., Przewalskis wild horse (Equus ferus przewalskii) (6), blackfooted ferret (Mustela nigripes) (7), and California condor (Gymnogyps californianus) (8)]. Captive breeding has the potential to maintain targeted populations as an insurance 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
1

Counting Threatened Species in Captivity

Max Planck Institute for Demographic Research, Rostock 18057, Germany. 2International Species Information System, Eagan, MN 55121, USA. *Author for correspondence: conde@demogr.mpg.de

We used the International Species Information 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 worldwide, with records of ~2.6 million individuals 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 represented in ISIS (18). [See supporting online materials (SOM) for details.] One-quarter of the worlds described bird species and almost 20% of the mammal species are held in ISIS zoos (table S1). Only 12% of the described reptile species are rep-

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t the October 2010 meeting of the Convention on Biological Diversity (CBD) in Nagoya, Japan, delegates discussed a plan to reduce pressures on the planets biodiversity. Key targets include expanding coverage of protected areas, halving 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 Species Act, and the CBD (Article 9) recognize that in situ conservation actions (i.e., in the species natural habitat) will need to be combined with ex situ approaches, such as captive breeding in zoos, aquariums, and so on (2, 3). Captive breeding may be the only shortterm practical conservation option for species conned to dwindling habitats (4). However, captive breeding is absent or plays a minor role in the policies of most governments, conservation organizations, and multilateral institutions. To shed light on the state of captive breeding and its potential to contribute to conservation goals, we estimate the number of threatened species already held in captivity.

global amphibian population declines (11). Captive breeding for reintroduction has downsides. Sociopolitical factors can determine the success of programs. For example, reintroduction of Arabian oryx (Oryx leucoryx) in central Oman was hampered by poaching, partly because local communities were insufciently involved in conservation efforts (12, 13). Furthermore, captive breeding is costly, and technical difculties can arise such as hybridization [breeding among different species (14), e.g., if current cryptic species are managed as one species, but are later split into several species according to new taxonomic information]. The ability of individuals to learn crucial skills that allow them to survive in the wild (e.g., fear of humans or predators) may be compromised. In many cases, these difculties have been overcome by creative and species-specic 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 prerelease 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, captive 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.

resented and 4% of amphibians. Our primary focus is on species of conservation concern; for mammals, roughly one-fth to one-quarter of threatened (19) and Near-Threatened species are represented in ISIS zoos (see the 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 amphibians, the representation of threatened species 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 reptiles 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-Threatened 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 particular species, collectively, zoos hold sizable populations of certain species, including highly threatened ones (see the 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 contribution by specializing in breeding a few atrisk 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 programs (20), but these require parameterization with data on age-specic birth and death rates (21). Adequate data from natural environments 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 successive litters, and age at maturity, which could be used to ll these gaps. Of course, zoo data should be used with caution because they

POLICYFORUM
Mammals 800 Described In zoos Birds Reptiles Amphibians

Number of species

600

400

200 25% 0 NT 5000 VU EN CR 24% 23% 19% 100% EW

18% 17% 17% 9% NT VU EN CR 100% EW 18% NT VU 37% 28% EN 51% CR 0% EW 6% NT 4% VU 2% EN 3% CR 50% EW

Number of individuals

250 500 50 50 10

250 50 10

250 50 10

250 50 10

5 1

Percentage of species per interval

21

27

25

27

40

29

23

40

32

22

24

10 18

48

Species (ranked by number of individuals)


NT: Near threatened VU: Vulnerable EN: Endangered CR: Critically endangered EW: Extinct in the wild

Threatened

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 IUCNfor mammals (142 species), birds (83 species), reptiles (90 species), and amphibians (29 species). The vertical broken lines show the boundaries by 250, 50, and 10 individuals. The large numbers of individuals classied as Vulnerable and Near Threatened are omitted for clarity. See SOM for details.

do not necessarily reect the situation in the wild, such as population exibility in the face of changing conditions. Despite their current and potential contributions to species conservation, ISIS zoos are concentrated in temperate regions, whereas most threatened species are tropical (5, 22) (g. S1). This mismatch between the areas where captive populations are held and their native range poses a challenge for implementation 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 species origin (2). There are large parts of the world with high biodiversity value, yet whose zoos are not well represented in a global network (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 Association 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 developed conservation projects in the wild, alongside research and education programs (23). For example, members of WAZA collectively spend ~U.S. $350 million per year on conservation 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 policymakers consider the potential that zoos as a global network can provide.
References and Notes
1. D. Normile, Science Insider, 29 October 2010; http:// news.sciencemag.org/scienceinsider/2010/10/negotiators-agree-on-biodiversity.html. 2. Convention on Biological Diversity, Article 9, United NationsTreaty Series, pp. 149 and 150 (1993). 3. IUCN, IUCN Technical Guidelines on the Management of Ex Situ Populations for Conservation (IUCN, Gland, Switzerland, 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 Threatened Species, Version 2010.4 (IUCN, Gland, Switzerland, 2010). 8. V. J. Meretsky, N. F. R. Snyder, S. R. Beissinger, D. A. Clendenen, J. W. Wiley, Conserv. Biol. 14, 957 (2000). 9. J.-C. Thibault, J.-Y. Meyer, Oryx 35, 73 (2001). 10. Amphibian Ark, www.amphibianark.org. 11. L. F. Skerratt et al., EcoHealth 4, 125 (2007). 12. J. A. Spalton, M. W. Lawerence, S. A. Brend, Oryx 33, 168 (1999). 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 (2005). 16. International Species Information System, www.isis.org. 17. IUCN, IUCN Red List of Threatened Species, Version 3.1 (IUCN, Gland, Switzerland, 2009); www.iucnredlist.org. 18. ISIS and IUCN information were matched on the species level using the Catalogue of Life (F. A. Bisby et al., Eds.); www.catalogueoife.org. 19. Threatened species are those listed as Critically Endangered (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, Switzerland, 2005). 24. M. Gusset, G. Dick, Zoo Biol., 6 December 2010 (http:// onlinelibrary.wiley.com/doi/10.1002/zoo.20369/ abstract). 25. We thank J. Vaupel, M. Gusset, C. D. L. Orme, D. Levitis, D. de Man, W. van Lint, K. Zippel, S. Mller, J. Runge, E. Brinks, G. Fiedler, P. Kutter, and F. Quade. We also thank three anonymous referees.

Supporting Online Material


www.sciencemag.org/cgi/content/full/331/6023/1390/DC1 10.1126/science.1200674

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Supporting Online Material for


An Emerging Role of Zoos to Conserve Biodiversity
D. A. Conde,* N. Flesness, F. Colchero, O. R. Jones, A. Scheuerlein *To whom correspondence should be addressed. E-mail: conde@demogr.mpg.de
Published 18 March 2011, Science 331, 1390 (2011) DOI: 10.1126/science.1200674

This PDF file includes Materials and Methods SOM Text Fig. S1 Tables S1 and S2 References Other Supporting Online Material for this manuscript includes the following: (available at www.sciencemag.org/cgi/content/full/331/6023/1390/DC1) Data file containing presence or absence data for terrestrial vertebrate species in the IUCN Red List (ver 3.2) and in each ISIS zoo, including ancillary information on their threat category and number of specimens held per zoo.

Conde et al. SOM, page 1

Materials and Methods


To quantify the number of species and individuals from each IUCN category held in ISIS zoos, we matched the species-level data in ISISs freely available online global zoo and aquarium living inventory (S1), with the IUCN Red List (RL) assessment data version 3.1 (S2). We used the RL search tool to download a table with the assessment for terrestrial vertebrates: mammals, birds, reptiles, and amphibians (S3). We carried out the taxonomic name matching at the species level. Where the ISIS and IUCN taxonomic names differed, we used the Catalogue of Life (S4) for taxonomic synonyms. We used the taxonomic names given in the IUCN data sets as the basis for our analysis. In total, we assessed 3977 species and 624,227 individuals registered in 837 ISIS zoos, excluding the births in the past 12 months. We broke this information down by taxonomic class (mammal, bird, reptile, and amphibian) and by IUCN RL threat category (Tables S1 and S2 and Figure 1). The output data from our matching procedure is available in the SOM data file: ISIS.IUCN.Matching.xls. For mammals, birds, and amphibians, we further calculated the species richness (number of species) of threatened species for each zoo. We excluded reptiles from this part of the analysis because the IUCN Red List evaluation for this group is not yet complete. To map the distribution of threatened species across ISIS zoos (Fig. S1), we obtained the latitude and longitude of each zoo by using the GPS Visualizer multiple addresses geocode function (S5). We generated a vector file (i.e., shape file) that contained the data for each zoos geographical position and the total number of threatened species associated with it. To produce Fig. S1, we compared this distribution with the global distribution of wild threatened species given in Grenyer et al. (S6). The underlying data for these were kindly provided by one of the authors, C. D. L. Orme. All of our figures and maps were produced using R (S7).

Fig S1. Species richness map for threatened mammals, birds and amphibians within ISIS zoos (top) and globally (bottom) [modified from (S6)]. Zoo species richness is represented by points colored to indicate the number of species within individual zoos; global species richness corresponds to the number of species occurring within a 1q latitude by 1q longitude cell. Reptiles are omitted because the IUCN assessment is still incomplete.

Conde et al. SOM, page 2 Table S1. Total number of species described per class of terrestrial vertebrates in the IUCN (version 3.1) and ISIS databases and the number in each of the following IUCN Red List categories: LC, Least Concern; NT, Near Threatened; VU, Vulnerable; EN, Endangered; CR, Critically Endangered; and EW, Extinct in the Wild and DD, Data Deficient. For each category, we show the total number of species described in the IUCN Red List and the number in the ISIS database.
AMPHIBIA REPTILIA AVES MAMMALIA

LC NT VU EN CR EW DD TOTAL

IUCN ISIS IUCN ISIS IUCN ISIS IUCN ISIS IUCN ISIS IUCN ISIS IUCN ISIS IUCN ISIS

2372 141 382 22 657 28 754 13 484 15 2 1 1634 26 6285 246

761 180 80 15 226 87 150 43 93 48 1 0 366 72 1677 445

7735 1956 838 152 669 115 362 62 192 18 4 3 198 1 9998 2307

3099 606 320 81 503 122 447 104 187 36 2 2 907 28 5465 979

Conde et al. SOM, page 3 Table S2. Species categorized by the IUCN as Extinct in the Wild.
Class AMPHIBIA Species Name Anaxyrus baxteri Nectophrynoides asperginis REPTILIA Nilssonia nigricans In ISIS Zoos No Yes No Notes
Restricted to the Laramie Basin, Wyoming, USA. (S8). In 2 ISIS Zoos

IUCN Web Source for further information http://www.iucnredlist.org/ apps/redlist/details/54583 /0 http://www.iucnredlist.org/ apps/redlist/details/54837 /0 http://www.iucnredlist.org/ apps/redlist/details/2173/ 0 http://www.iucnredlist.org/ apps/redlist/details/14117 8/0 http://www.iucnredlist.org/ apps/redlist/details/14354 7/0 http://www.iucnredlist.org/ apps/redlist/details/14384 1/0 http://www.iucnredlist.org/ apps/redlist/details/14667 3/0 http://www.iucnredlist.org/ apps/redlist/details/7121/ 0 http://www.iucnredlist.org/ apps/redlist/details/15568 /0

AVES

Mitu mitu Zenaida graysoni Gallirallus owstoni Corvus hawaiiensis

Yes Yes Yes Yes Yes

Is known to occur only in a single artificial temple pond near Chittagong, Bangladesh (S9). In 3 ISIS Zoos

In 20 ISIS Zoos

In 15 ISIS Zoos

In one ISIS Zoo

MAMMALIA

Elaphurus davidianus

In 56 ISIS Zoos

Oryx dammah

Yes

In 103 ISIS Zoos

Conde et al. SOM, page 4

References and Notes


S1. ISIS, www.isis.org/Pages/findanimals.aspx; accessed April 2010. S2. IUCN, IUCN Red List of Threatened Species, Version 3.1 (IUCN, Gland, Switzerland, 2009); www.iucnredlist.org, accessed April 2010. S3. We used the other search options tool from the main IUCN RL Web page, detailed information on how to download IUCN RL data tables could be obtained from www.iucnredlist.org/news/iucn-red-list-site-made-easy-guide. S4. F.A. Bisby et al., Eds., Catalogue of Life (www.catalogueoflife.org/), accessed from May to July 2010. S5. GPS Visualizer, www.gpsvisualizer.com/geocoder/; accessed September 2010. S6. R. Grenyer et al., Nature 444, 93 (2006). S7. R Development Core Team, R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, Vienna, Austria, 2010); www.R-project.org. S8. G. Hammerson assessor in 2004, Anaxyrus baxteri. in IUCN Red List of Threatened Species, Version 2010.4 (IUCN, Gland Switzerland, 2010); www.iucnredlist.org, accessed on 28 February 2011. S9. G. S. M. Asmat assessor in 2002, Nilssonia nigricans. in IUCN Red List of Threatened Species, Version 2010.4 (IUCN, Gland Switzerland, 2010); www.iucnredlist.org, accessed on 28 February 2011.