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POLICYFORUM UNTIL 2:00 PM US ET THURSDAY, 17 MARCH 2011
                EMBARGOED
       CONSERVATION


       An Emerging Role of Zoos                                                                                     Roughly one in seven threatened terrestrial
                                                                                                                    vertebrate species are held in captivity,

       to Conserve Biodiversity
                                                                                                                    a resource for ex situ conservation efforts.


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




       A
                 t the October 2010 meeting of the                global amphibian population declines (11).        resented and 4% of amphibians. Our primary
                 Convention on Biological Diversity                   Captive breeding for reintroduction has       focus is on species of conservation concern;
                 (CBD) in Nagoya, Japan, delegates                downsides. Sociopolitical factors can deter-      for mammals, roughly one-fifth to one-quar-
       discussed a plan to reduce pressures on the                mine the success of programs. For example,        ter of threatened (19) and Near-Threatened
       planet’s biodiversity. Key targets include                 reintroduction of Arabian oryx (Oryx leu-         species are represented in ISIS zoos (see
       expanding coverage of protected areas, halv-               coryx) in central Oman was hampered by            the figure) (table S1). With the exception of
       ing the rate of loss of natural habitats, and              poaching, partly because local communities        Critically Endangered species, which only
       preventing extinction of threatened species                were insufficiently involved in conservation      have a 9% representation (tables S1 and S2),
       (1). For species whose habitat is severely                 efforts (12, 13). Furthermore, captive breed-     the picture is similar for birds. For amphib-
       threatened, however, the outlook is so bleak               ing is costly, and technical difficulties can     ians, the representation of threatened spe-
       that the International Union for Conservation              arise such as hybridization [breeding among       cies is much lower (~3%); this is a concern
       of Nature (IUCN), the U.S. Endangered Spe-                 different species (14), e.g., if current cryp-    because amphibians are a highly threatened
       cies Act, and the CBD (Article 9) recognize                tic species are managed as one species, but       group, with 41% of described species listed
       that in situ conservation actions (i.e., in the            are later split into several species according    as threatened or Extinct in the Wild (EW) (5).
       species’ natural habitat) will need to be com-             to new taxonomic information]. The abil-          The IUCN threat-level assessment for rep-
       bined with ex situ approaches, such as captive             ity of individuals to learn crucial skills that   tiles has not been completed, so our results
       breeding in zoos, aquariums, and so on (2, 3).             allow them to survive in the wild (e.g., fear     should be interpreted with caution, but of the
           Captive breeding may be the only short-                of humans or predators) may be compro-            1672 species already evaluated, zoos hold
       term practical conservation option for species             mised. In many cases, these difficulties have     37% of threatened and 18% of Near-Threat-
       confined to dwindling habitats (4). However,               been overcome by creative and species-spe-        ened species.
       captive breeding is absent or plays a minor                cific measures. For example, it was feared            Overall, zoos and aquariums hold roughly
       role in the policies of most governments, con-             that Puerto Rican parrots (Amazona vittata)       one in seven threatened species (15%), but it
       servation organizations, and multilateral insti-           would be unable to escape predators in the        is important to consider also the number of
       tutions. To shed light on the state of captive             wild, but this problem was solved with a pre-     individuals held. Although individual zoos
       breeding and its potential to contribute to con-           release aviary-based stimulation and exercise     might not have large populations of a par-
       servation goals, we estimate the number of                 program (15). Because ex situ conservation        ticular species, collectively, zoos hold siz-
       threatened species already held in captivity.              programs can be challenged when called into       able populations of certain species, including
                                                                  action at the last possible moment with only a    highly threatened ones (see the figure). Zoos,
       Captive Breeding                                           few remaining individuals of a species, cap-      as a global network, should strive to ensure
       Although ecosystem health should be a con-                 tive breeding should not simply be seen as        that their populations of threatened species
       servation priority, a recent evaluation of the             “emergency-room treatment.” It is a tool that     can survive in the long term. However, each
       status of the world’s vertebrates (5) noted that           should be considered before the species has       zoo may make a larger conservation contri-
       captive breeding played a major role in the                reached the point of no return.                   bution by specializing in breeding a few at-
       recovery of 17 of the 68 species whose threat                                                                risk targeted species, rather than aiming to
       level was reduced [e.g., Przewalski’s wild                 Counting Threatened Species in Captivity          increase its species diversity, as specialization
       horse (Equus ferus przewalskii) (6), black-                We used the International Species Informa-        increases breeding success (4).
       footed ferret (Mustela nigripes) (7), and Cal-             tion System (ISIS) database to estimate the           Ultimately, success of conservation
       ifornia condor (Gymnogyps californianus)                   number of threatened species already held in      actions depends on the extent to which birth
       (8)]. Captive breeding has the potential to                captivity. ISIS is an organization that holds     and death rates permit populations to survive
       maintain targeted populations as an “insur-                the most comprehensive information on             in the wild (8). Population viability analyses
       ance policy” against threats like disease or               animals held in zoos and aquariums world-         (PVAs) are used to forecast the probability of
       pressure from nonnative species [e.g., egg                 wide, with records of ~2.6 million individu-      population extinction for conservation pro-
       predators on islands (9)] until reintroduction             als shared among ~800 member institutions         grams (20), but these require parameteriza-
       into the wild is possible. A striking example              (16). From the IUCN Red List of Threatened        tion with data on age-specific birth and death
       is the increase of amphibian collections in                Species (17), we obtained the threat category     rates (21). Adequate data from natural envi-
       zoos (10) as a response to chytridiomycosis,               of each terrestrial vertebrate species repre-     ronments are often unavailable, especially for
       a fungal infection responsible for precipitous             sented in ISIS (18). [See supporting online       threatened species (20). The zoo network has
                                                                  materials (SOM) for details.]                     large long-term data sets, including data such
       1
         Max Planck Institute for Demographic Research, Rostock       One-quarter of the world’s described bird     as average litter size, interval between succes-
       18057, Germany. 2International Species Information Sys-    species and almost 20% of the mammal spe-         sive litters, and age at maturity, which could
       tem, Eagan, MN 55121, USA.                                 cies are held in ISIS zoos (table S1). Only       be used to fill these gaps. Of course, zoo data
       *Author for correspondence: conde@demogr.mpg.de            12% of the described reptile species are rep-     should be used with caution because they

1390                                                   18 MARCH 2011 VOL 331 SCIENCE www.sciencemag.org
POLICYFORUM
                                                           EMBARGOED UNTIL 2:00 PM US ET THURSDAY, 17 MARCH 2011
                                           Mammals                                                      Birds                                     Reptiles                               Amphibians
                           800
                                                                 Described
                                                                 In zoos
                           600
  Number of species




                           400


                           200                                                        18%
                                          24%        23%                                       17%
                                  25%                                                                                                        37%
                                                                                                      17%
                                                            19%                                                9%                                   28%    51%                      6%       4%                3%
                                                                       100%                                           100%          18%                                  0%                             2%            50%
                             0
                                    NT     VU        EN         CR      EW            NT        VU      EN      CR        EW            NT   VU      EN        CR        EW         NT       VU         EN     CR      EW
                          5000

                                         250                                          250                                          250                                                     250
  Number of individuals




                           500
                                                     50                                                 50                                          50                                           50

                            50                                   10                                                  10                                             10                                   10


                             5

                             1
     Percentage of
species per interval                21          27         25           27            8         40            29          23        6        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                                           able for design of conservation programs,                           7. J. Belant, P. Gober, D. Biggins, in IUCN Red List of Threat-
species with IUCN status, globally described (color                                       policy-makers must encourage and facilitate                            ened Species, Version 2010.4 (IUCN, Gland, Switzerland,
                                                                                                                                                                 2010).
bars) and in ISIS zoos (black bars). (Bottom) The                                         the participation of zoos from regions with                         8. V. J. Meretsky, N. F. R. Snyder, S. R. Beissinger, D. A. Clen-
number of individuals in ISIS zoos for species listed                                     high levels of biodiversity threat in global                           denen, J. W. Wiley, Conserv. Biol. 14, 957 (2000).
by IUCN—for mammals (142 species), birds (83 spe-                                         networks, such as ISIS and the World Asso-                          9. J.-C. Thibault, J.-Y. Meyer, Oryx 35, 73 (2001).
cies), reptiles (90 species), and amphibians (29 spe-                                                                                                        10. Amphibian Ark, www.amphibianark.org.
                                                                                          ciation of Zoos and Aquariums (WAZA).                              11. L. F. Skerratt et al., EcoHealth 4, 125 (2007).
cies). The vertical broken lines show the boundaries
by 250, 50, and 10 individuals. The large numbers of
                                                                                               The potential for zoos to contribute to                       12. J. A. Spalton, M. W. Lawerence, S. A. Brend, Oryx 33, 168
individuals classified as Vulnerable and Near Threat-                                     conservation is not a new concept for the zoo                          (1999).
                                                                                                                                                             13. V. Morell, Science 320, 742 (2008).
ened are omitted for clarity. See SOM for details.                                        community. Zoos and aquariums have devel-                          14. R. Barnett, N. Yamaguchi, I. Barnes, A. Cooper, Conserv.
                                                                                          oped conservation projects in the wild, along-                         Genet. 7, 507 (2006).
                                                                                          side research and education programs (23).                         15. T. H. White, J. A. Collazo, F. J. Vilella, Condor 107, 424
                                                                                                                                                                 (2005).
do not necessarily reflect the situation in the                                           For example, members of WAZA collectively                          16. International Species Information System, www.isis.org.
wild, such as population flexibility in the face                                          spend ~U.S. $350 million per year on conser-                       17. IUCN, IUCN Red List of Threatened Species, Version 3.1
of changing conditions.                                                                   vation actions in the wild, which makes them                           (IUCN, Gland, Switzerland, 2009); www.iucnredlist.org.
                                                                                                                                                             18. ISIS and IUCN information were matched on the species
    Despite their current and potential contri-                                           the third major contributor to conservation                            level using the Catalogue of Life (F. A. Bisby et al., Eds.);
butions to species conservation, ISIS zoos are                                            worldwide after the Nature Conservancy and                             www.catalogueoflife.org.
concentrated in temperate regions, whereas                                                the World Wildlife Fund global network (24).                       19. Threatened species are those listed as Critically Endan-
                                                                                                                                                                 gered (CR), Endangered (EN), or Vulnerable (VU) by IUCN.
most threatened species are tropical (5, 22)                                              Given the scale of the biodiversity challenge,                     20. T. Coulson, G. M. Mace, E. Hudson, H. Possingham,
(fig. S1). This mismatch between the areas                                                it is vital that conservation bodies and policy-                       Trends Ecol. Evol. 16, 219 (2001).
where captive populations are held and their                                              makers consider the potential that zoos as a                       21. J. M. Reed et al., Conserv. Biol. 16, 7 (2002).
                                                                                                                                                             22. R. Grenyer et al., Nature 444, 93 (2006).
native range poses a challenge for imple-                                                 global network can provide.                                        23. WAZA, Building a Future for Wildlife: The World Zoo and
mentation of effective conservation actions.                                                                                                                     Aquarium Conservation Strategy (WAZA, Berne, Switzer-
Acclimatization to a new home is likely to be                                                  References and Notes                                              land, 2005).
                                                                                            1. D. Normile, Science Insider, 29 October 2010; http://         24. M. Gusset, G. Dick, Zoo Biol., 6 December 2010 (http://
faster for animals raised in conditions similar                                                news.sciencemag.org/scienceinsider/2010/10/negotia-               onlinelibrary.wiley.com/doi/10.1002/zoo.20369/
to those where they are to be released. This                                                   tors-agree-on-biodiversity.html.                                  abstract).
is one reason that it is suggested that captive                                             2. Convention on Biological Diversity, Article 9, United         25. We thank J. Vaupel, M. Gusset, C. D. L. Orme, D. Levitis,
breeding be done in the country of the spe-                                                    Nations—Treaty Series, pp. 149 and 150 (1993).                    D. de Man, W. van Lint, K. Zippel, S. Möller, J. Runge, E.
                                                                                            3. IUCN, IUCN Technical Guidelines on the Management of              Brinks, G. Fiedler, P. Kutter, and F. Quade. We also thank
cies’ origin (2).                                                                              Ex Situ Populations for Conservation (IUCN, Gland, Swit-          three anonymous referees.
    There are large parts of the world with high                                               zerland, 2002), p. 4.
biodiversity value, yet whose zoos are not                                                  4. W. G. Conway, Zoo Biol. 30, 1 (2011).                       Supporting Online Material
                                                                                            5. M. Hoffmann et al., Science 330, 1503 (2010).
well represented in a global network (fig. S1).                                             6. M. C. Van Dierendonck, M. F. Wallis de Vries, Conserv.
                                                                                                                                                           www.sciencemag.org/cgi/content/full/331/6023/1390/DC1
Given the importance of having data avail-                                                     Biol. 10, 728 (1996).                                                                                  10.1126/science.1200674


                                                                        www.sciencemag.org SCIENCE VOL 331 18 MARCH 2011                                                                                                          1391

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Conde 03-18-11

  • 1. POLICYFORUM UNTIL 2:00 PM US ET THURSDAY, 17 MARCH 2011 EMBARGOED CONSERVATION An Emerging Role of Zoos Roughly one in seven threatened terrestrial vertebrate species are held in captivity, to Conserve Biodiversity a resource for ex situ conservation efforts. D. A. Conde,1* N. Flesness,2 F. Colchero,1 O. R. Jones,1 A. Scheuerlein1 A t the October 2010 meeting of the global amphibian population declines (11). resented and 4% of amphibians. Our primary Convention on Biological Diversity Captive breeding for reintroduction has focus is on species of conservation concern; (CBD) in Nagoya, Japan, delegates downsides. Sociopolitical factors can deter- for mammals, roughly one-fifth to one-quar- discussed a plan to reduce pressures on the mine the success of programs. For example, ter of threatened (19) and Near-Threatened planet’s biodiversity. Key targets include reintroduction of Arabian oryx (Oryx leu- species are represented in ISIS zoos (see expanding coverage of protected areas, halv- coryx) in central Oman was hampered by the figure) (table S1). With the exception of ing the rate of loss of natural habitats, and poaching, partly because local communities Critically Endangered species, which only preventing extinction of threatened species were insufficiently involved in conservation have a 9% representation (tables S1 and S2), (1). For species whose habitat is severely efforts (12, 13). Furthermore, captive breed- the picture is similar for birds. For amphib- threatened, however, the outlook is so bleak ing is costly, and technical difficulties can ians, the representation of threatened spe- that the International Union for Conservation arise such as hybridization [breeding among cies is much lower (~3%); this is a concern of Nature (IUCN), the U.S. Endangered Spe- different species (14), e.g., if current cryp- because amphibians are a highly threatened cies Act, and the CBD (Article 9) recognize tic species are managed as one species, but group, with 41% of described species listed that in situ conservation actions (i.e., in the are later split into several species according as threatened or Extinct in the Wild (EW) (5). species’ natural habitat) will need to be com- to new taxonomic information]. The abil- The IUCN threat-level assessment for rep- bined with ex situ approaches, such as captive ity of individuals to learn crucial skills that tiles has not been completed, so our results breeding in zoos, aquariums, and so on (2, 3). allow them to survive in the wild (e.g., fear should be interpreted with caution, but of the Captive breeding may be the only short- of humans or predators) may be compro- 1672 species already evaluated, zoos hold term practical conservation option for species mised. In many cases, these difficulties have 37% of threatened and 18% of Near-Threat- confined to dwindling habitats (4). However, been overcome by creative and species-spe- ened species. captive breeding is absent or plays a minor cific measures. For example, it was feared Overall, zoos and aquariums hold roughly role in the policies of most governments, con- that Puerto Rican parrots (Amazona vittata) one in seven threatened species (15%), but it servation organizations, and multilateral insti- would be unable to escape predators in the is important to consider also the number of tutions. To shed light on the state of captive wild, but this problem was solved with a pre- individuals held. Although individual zoos breeding and its potential to contribute to con- release aviary-based stimulation and exercise might not have large populations of a par- servation goals, we estimate the number of program (15). Because ex situ conservation ticular species, collectively, zoos hold siz- threatened species already held in captivity. programs can be challenged when called into able populations of certain species, including action at the last possible moment with only a highly threatened ones (see the figure). Zoos, Captive Breeding few remaining individuals of a species, cap- as a global network, should strive to ensure Although ecosystem health should be a con- tive breeding should not simply be seen as that their populations of threatened species servation priority, a recent evaluation of the “emergency-room treatment.” It is a tool that can survive in the long term. However, each status of the world’s vertebrates (5) noted that should be considered before the species has zoo may make a larger conservation contri- captive breeding played a major role in the reached the point of no return. bution by specializing in breeding a few at- recovery of 17 of the 68 species whose threat risk targeted species, rather than aiming to level was reduced [e.g., Przewalski’s wild Counting Threatened Species in Captivity increase its species diversity, as specialization horse (Equus ferus przewalskii) (6), black- We used the International Species Informa- increases breeding success (4). footed ferret (Mustela nigripes) (7), and Cal- tion System (ISIS) database to estimate the Ultimately, success of conservation ifornia condor (Gymnogyps californianus) number of threatened species already held in actions depends on the extent to which birth (8)]. Captive breeding has the potential to captivity. ISIS is an organization that holds and death rates permit populations to survive maintain targeted populations as an “insur- the most comprehensive information on in the wild (8). Population viability analyses ance policy” against threats like disease or animals held in zoos and aquariums world- (PVAs) are used to forecast the probability of pressure from nonnative species [e.g., egg wide, with records of ~2.6 million individu- population extinction for conservation pro- predators on islands (9)] until reintroduction als shared among ~800 member institutions grams (20), but these require parameteriza- into the wild is possible. A striking example (16). From the IUCN Red List of Threatened tion with data on age-specific birth and death is the increase of amphibian collections in Species (17), we obtained the threat category rates (21). Adequate data from natural envi- zoos (10) as a response to chytridiomycosis, of each terrestrial vertebrate species repre- ronments are often unavailable, especially for a fungal infection responsible for precipitous sented in ISIS (18). [See supporting online threatened species (20). The zoo network has materials (SOM) for details.] large long-term data sets, including data such 1 Max Planck Institute for Demographic Research, Rostock One-quarter of the world’s described bird as average litter size, interval between succes- 18057, Germany. 2International Species Information Sys- species and almost 20% of the mammal spe- sive litters, and age at maturity, which could tem, Eagan, MN 55121, USA. cies are held in ISIS zoos (table S1). Only be used to fill these gaps. Of course, zoo data *Author for correspondence: conde@demogr.mpg.de 12% of the described reptile species are rep- should be used with caution because they 1390 18 MARCH 2011 VOL 331 SCIENCE www.sciencemag.org
  • 2. POLICYFORUM EMBARGOED UNTIL 2:00 PM US ET THURSDAY, 17 MARCH 2011 Mammals Birds Reptiles Amphibians 800 Described In zoos 600 Number of species 400 200 18% 24% 23% 17% 25% 37% 17% 19% 9% 28% 51% 6% 4% 3% 100% 100% 18% 0% 2% 50% 0 NT VU EN CR EW NT VU EN CR EW NT VU EN CR EW NT VU EN CR EW 5000 250 250 250 250 Number of individuals 500 50 50 50 50 50 10 10 10 10 5 1 Percentage of species per interval 21 27 25 27 8 40 29 23 6 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 able for design of conservation programs, 7. J. Belant, P. Gober, D. Biggins, in IUCN Red List of Threat- species with IUCN status, globally described (color policy-makers must encourage and facilitate ened Species, Version 2010.4 (IUCN, Gland, Switzerland, 2010). bars) and in ISIS zoos (black bars). (Bottom) The the participation of zoos from regions with 8. V. J. Meretsky, N. F. R. Snyder, S. R. Beissinger, D. A. Clen- number of individuals in ISIS zoos for species listed high levels of biodiversity threat in global denen, J. W. Wiley, Conserv. Biol. 14, 957 (2000). by IUCN—for mammals (142 species), birds (83 spe- networks, such as ISIS and the World Asso- 9. J.-C. Thibault, J.-Y. Meyer, Oryx 35, 73 (2001). cies), reptiles (90 species), and amphibians (29 spe- 10. Amphibian Ark, www.amphibianark.org. ciation of Zoos and Aquariums (WAZA). 11. L. F. Skerratt et al., EcoHealth 4, 125 (2007). cies). The vertical broken lines show the boundaries by 250, 50, and 10 individuals. The large numbers of The potential for zoos to contribute to 12. J. A. Spalton, M. W. Lawerence, S. A. Brend, Oryx 33, 168 individuals classified as Vulnerable and Near Threat- conservation is not a new concept for the zoo (1999). 13. V. Morell, Science 320, 742 (2008). ened are omitted for clarity. See SOM for details. community. Zoos and aquariums have devel- 14. R. Barnett, N. Yamaguchi, I. Barnes, A. Cooper, Conserv. oped conservation projects in the wild, along- Genet. 7, 507 (2006). side research and education programs (23). 15. T. H. White, J. A. Collazo, F. J. Vilella, Condor 107, 424 (2005). do not necessarily reflect the situation in the For example, members of WAZA collectively 16. International Species Information System, www.isis.org. wild, such as population flexibility in the face spend ~U.S. $350 million per year on conser- 17. IUCN, IUCN Red List of Threatened Species, Version 3.1 of changing conditions. vation actions in the wild, which makes them (IUCN, Gland, Switzerland, 2009); www.iucnredlist.org. 18. ISIS and IUCN information were matched on the species Despite their current and potential contri- the third major contributor to conservation level using the Catalogue of Life (F. A. Bisby et al., Eds.); butions to species conservation, ISIS zoos are worldwide after the Nature Conservancy and www.catalogueoflife.org. concentrated in temperate regions, whereas the World Wildlife Fund global network (24). 19. Threatened species are those listed as Critically Endan- gered (CR), Endangered (EN), or Vulnerable (VU) by IUCN. most threatened species are tropical (5, 22) Given the scale of the biodiversity challenge, 20. T. Coulson, G. M. Mace, E. Hudson, H. Possingham, (fig. S1). This mismatch between the areas it is vital that conservation bodies and policy- Trends Ecol. Evol. 16, 219 (2001). where captive populations are held and their makers consider the potential that zoos as a 21. J. M. Reed et al., Conserv. Biol. 16, 7 (2002). 22. R. Grenyer et al., Nature 444, 93 (2006). native range poses a challenge for imple- global network can provide. 23. WAZA, Building a Future for Wildlife: The World Zoo and mentation of effective conservation actions. Aquarium Conservation Strategy (WAZA, Berne, Switzer- Acclimatization to a new home is likely to be References and Notes land, 2005). 1. D. Normile, Science Insider, 29 October 2010; http:// 24. M. Gusset, G. Dick, Zoo Biol., 6 December 2010 (http:// faster for animals raised in conditions similar news.sciencemag.org/scienceinsider/2010/10/negotia- onlinelibrary.wiley.com/doi/10.1002/zoo.20369/ to those where they are to be released. This tors-agree-on-biodiversity.html. abstract). is one reason that it is suggested that captive 2. Convention on Biological Diversity, Article 9, United 25. We thank J. Vaupel, M. Gusset, C. D. L. Orme, D. Levitis, breeding be done in the country of the spe- Nations—Treaty Series, pp. 149 and 150 (1993). D. de Man, W. van Lint, K. Zippel, S. Möller, J. Runge, E. 3. IUCN, IUCN Technical Guidelines on the Management of Brinks, G. Fiedler, P. Kutter, and F. Quade. We also thank cies’ origin (2). Ex Situ Populations for Conservation (IUCN, Gland, Swit- three anonymous referees. There are large parts of the world with high zerland, 2002), p. 4. biodiversity value, yet whose zoos are not 4. W. G. Conway, Zoo Biol. 30, 1 (2011). Supporting Online Material 5. M. Hoffmann et al., Science 330, 1503 (2010). well represented in a global network (fig. S1). 6. M. C. Van Dierendonck, M. F. Wallis de Vries, Conserv. www.sciencemag.org/cgi/content/full/331/6023/1390/DC1 Given the importance of having data avail- Biol. 10, 728 (1996). 10.1126/science.1200674 www.sciencemag.org SCIENCE VOL 331 18 MARCH 2011 1391