Zookeeping: An Introduction to the Science and ...

53 Conservation Biology Gerald Dick and Markus Gusset

INTRODUCTION Conservation biology, a relatively new stage in the application of science to conservation problems, addresses the biology of species, communities, and ecosystems that are perturbed, either directly or indirectly, by human activities or other agents (Soulé 1985). Its goal is to provide principles and tools for preserving biological diversity. Caughley (1994) identified two dominant themes in the theoretical and methodological development of conservation biology as a scientific discipline: the “small population” and “declining population” paradigms. The former focuses on the dynamics and persistence of small populations, while the latter examines the factors that reduce populations to small sizes in the first place. Conservation biology thus provides an understanding of both threatening and mitigating factors in order to propose solutions for realworld conservation challenges. The aims of this chapter are to present an overview of • the definition of biodiversity conservation • global species crisis and conservation challenges • world zoo and aquarium conservation strategies • conservation through zoos and aquariums. WHAT IS BIODIVERSITY CONSERVATION? The following section is based on the introduction to “Building a Future for Wildlife: Zoos and Aquariums Committed to Biodiversity Conservation” (Dick and Gusset 2010) by Reid (2010). “Biodiversity” appears at first sight to be a fairly straightforward concept. In one context it refers to the immense global variety of wildlife, some of which is cared for in zoos and aquariums. But biodiversity can also be understood in terms of microorganisms and the complex genetic variation in animal and plant chromosomes, genes, DNA, and other biochemistry. Such intricate microscopic or molecular variation ultimately determines the uniqueness and success of individuals, species, and higher-level taxa. This contrasts

with an equally complex macroscopic biodiversity, including the large range of habitats, landscapes, and ecosystems. The focus on wildlife diversity has changed since the 18th century. Carolus Linnaeus (1707–78) described some 12,100 species in his lifetime, of which 4,400 were animals and 7,700 were plants. He confidently predicted that the complete eventual plant list would not exceed 10,000. However, the present rate of discovery of species is extremely high. At least 2,057 new vascular plants were named in 2006, along with 8,995 insects and 486 fishes. Since 2004 more than 13 new amphibian species have been recognized each month, with more than 6,000 named so far from a total list of perhaps 9,000 (Hilton-Taylor et al. 2009). Indeed, there has been an extraordinary explosion of knowledge across all major taxa, with new species being discovered daily. There is no absolutely agreed-upon projected total, nor any easy scientific means of establishing such a figure. The current global biodiversity assessment (see CBD 2010) recognizes 1.8 million described species as possibly being valid, with a final projected total of perhaps 14 million. If true, this means that less than 13 of all species have scientific names, and a staggering 12.2 million remain to be formally described. Considering also our limited knowledge of the world’s microscopic and macroscopic biodiversity, we have a heady brew of ignorance! For example, comparatively few vertebrate species have had their conservation status assessed in any scientific detail. While there are many notable species conservation successes, the general situation, as documented by the Convention on Biological Diversity (CBD), steadily gets worse with each advancing year (CBD 2010). Clearly, zoos and aquariums must do much more to conserve vertebrates, and must pay far more attention to equally imperiled invertebrates and plants. THE ROLE OF THE WORLD’S ZOOS IN CONSERVATION “Conservation” can be defined as action that substantially enhances the survival of species and habitats, whether con533

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ducted in or out of the natural habitat. From this, “United for Conservation” is a headline statement used to communicate the central purpose of the World Association of Zoos and Aquariums (WAZA). Certainly, a biodiversity conservation and environmental sustainability ethos pervades the vision, mission, and values of the separate membership components of WAZA, ranging from regional and national associations to individual institutions. Clearly, the 1,300 or more mainstream zoos and aquariums on our planet serve a vital and serious purpose that is not always well publicized. This substantial conservation role exists alongside providing the visiting public a fun-filled and educational day out in a leisure context. Collectively, this creates millions of dollars of income that is applied to worthwhile conservation projects at home and abroad that are either operated by zoos and aquariums or conducted in partnership with them. Such activities are often targeted directly at practical issues in biodiversity conservation both in nature (in situ) and outside of the natural habitat (ex situ), at home and abroad. Increasingly, these two different designations are dissolving into a continuum in which threatened species are managed extensively (mainly in the wild) and intensively (mainly in captivity), with every sort of management combination in between. To assess global zoo and aquarium attendance, the authors approached 12 national and regional zoo and aquarium associations, covering all regions of the world, to provide a figure for how many visitors their member institutions received in 2008 (Gusset and Dick 2011a). About 600 million people reportedly visited zoos and aquariums worldwide in 2008. A comparison of zoo and aquarium attendance in 1990, the year of the last global survey, and in 2008 (table 53.1) shows that those zoo and aquarium associations reporting higher numbers in the 2008 survey represent regions with established documenting structures (North America, Australasia, and Europe), thus suggesting a growing number of visits in these regions. Conversely, those associations reporting lower numbers in the current survey represent regions where obtaining comprehensive numbers is more challenging (Latin America, Africa, and Asia). While the 2008 survey was specifically aimed at collecting documented figures from the associations’ members— something that generally proved feasible for the former three regions—the 1990 survey (IUDZG/CBSG 1993) relied on the associations’ estimates of zoo and aquarium attendance. This may be more appropriate for Latin America, Africa, and Asia, given the underestimates in documented figures confirmed by the associations in those regions in the current survey. Considering this variation in reporting between the two surveys, and assuming a largely unchanged number of existing zoos and aquariums, it seems legitimate to adjust the results accordingly (table 53.1), in which case zoos and aquariums worldwide receive more than 700 million visits annually. This figure, which may include multiple individual visits, is most certainly an underestimate (WAZA 2009) and is unparalleled by any other group of conservation-oriented institutions. The authors also assessed the conservation expenditures of the world zoo and aquarium community, approaching the same 12 national and regional zoo and aquarium associations to provide a figure for how much money their member

TABLE 53.1. Annual number (in millions) of visits to zoos and aquariums worldwide in 1990 (IUDZG/CBSG 1993), 2008 (this survey), and adjusted. From Gusset and Dick 2011. 1990

2008

Adjusted

North America Latin America Africa Australasia Europe Asia

106 61 15 6 125 308

186 11 8 17 142 221

186 61 15 17 142 308

Global total

621

585

729



1990 figures for Latin America, Africa, and Asia. 2008 figures for North America, Australasia, and Europe.

institutions spent on wildlife conservation in 2008 (Gusset and Dick 2011a). (Wildlife conservation in this context encompasses in situ conservation of wild species and habitats, and also includes related ex situ work.) The world zoo and aquarium community reportedly spent about US$350 million on wildlife conservation in 2008. This amount includes the expenses of zoo-based conservation organizations, but given that only 7 of the 12 associations submitted figures on conservation expenditures, it is most certainly an underestimate. Across regions, zoos and aquariums in North America and Europe spent the most by far on wildlife conservation (97 of expenses reported). In relation to major international conservation organizations (figure 53.1), the world zoo and aquarium community is among the main providers of conservation funding. This growing vocational conservation-focused ethos reflects the many cooperative initiatives of zoos and aquariums in supporting threatened species and habitats (e.g., Zimmermann et al. 2007; Dick and Gusset 2010; Zimmermann 2010); it may, for example, involve breeding programs, studbook management, assisted reproduction, species reintroductions or translocations, educational outreach, and benign (noninvasive and nonintrusive) scientific research. Often this now involves an integrated approach that takes in rapidly advancing disciplines such as conservation medicine, ecological restoration, and the sociology, ethnology, and psychology of “human-wildlife conflict.” Sometimes this entails a need to address worldwide issues in human development and poverty alleviation, which are a major root cause of the global decline in biodiversity (Niekisch 2010). Strategy planning and stakeholder support for these exercises is often supplied by the Conservation Breeding Specialist Group (CBSG) and the Reintroduction Specialist Group (RSG) of the Species Survival Commission (SSC) of the International Union for Conservation of Nature (IUCN), while bulk electronic data handling is expertly covered through the Zoological Information Management System (ZIMS) of the International Species Information System (ISIS) organization (Althaus et al. 2010; Stuart et al. 2010). International studbooks, kept under the auspices of WAZA, represent the highest level of global monitoring and management. They are meant to provide a valuable service to the zoological community, offering the most complete

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Figure 53.1. Amount of money spent on wildlife conservation by major international conservation organizations (figures taken from annual reports) and the world zoo and aquarium community (this survey) in 2008, in thousands of US dollars (Gusset and Dick 2011).

and accurate global data on the ex situ population’s pedigree and demography, including husbandry and veterinary guidance where possible, thus enabling better management of the population through analysis of the data (Althaus et al. 2010). In most cases, the staff members of WAZA member institutions serve as studbook keepers. Within WAZA the international studbook program is overseen by the Committee for Population Management (CPM) and is coordinated by a nominated employee at the WAZA executive office, in collaboration with ISIS. The Zoological Society of London (ZSL) regularly publishes the updated list of current international studbooks in the International Zoo Yearbook. As of November 2011, there were 123 active international studbooks on 162 species or subspecies (some international studbooks cover more than one taxon). Conservation breeding programs typically are established and administered at the level and under the auspices of the regional associations. At its 2003 annual conference, WAZA adopted a procedure for establishing interregional programs, which may involve a number of species for which international studbooks have been established. These programs, now called Global Species Management Plans (GSMPs), are those officially recognized and endorsed by WAZA. As of November 2011, there were three such global programs: one each for the Sumatran tiger (Panthera tigris sumatrae) and the Javan gibbon (Hylobates moloch), and a combined program for African and Asian elephants (Loxodonta africana and Elephas maximus). Given the emerging challenges of keeping viable captive populations regionally (Gusset and Dick 2011b), additional GSMPs will be established in the near future. GLOBAL SPECIES CRISIS AND CONSERVATION CHALLENGES Human beings are becoming increasingly cut off from nature. More than 50 of the world’s population currently lives in cities, and 70 will live in cities by 2030 (Djoghlaf 2010). As

a result, the majority of the population does not appreciate that biodiversity is their ultimate source of goods such as food, timber, and medicines, and that it provides society with irreplaceable ecosystem services like crop pollination, air and water purification, erosion control, and the renewal of soil fertility. This estrangement from nature makes it difficult for people to see the dangers inherent in the ongoing loss of biodiversity. Human activities are currently driving species extinct at up to 1,000 times the prehuman background rate (see CBD 2010). The 2010 Living Planet Index showed that vertebrate population sizes have on average declined by almost 30 over the last 40 years (figure 53.2). In the long term, this loss will radically undermine the potential of sustainable development, exacerbating poverty and fostering conflicts over dwindling resources. The following section is based on a review of the global species crisis and conservation challenges by Stuart et al. (2010). The rapid disappearance of species, and thus biodiversity, is often referred to as one of the world’s greatest environmental concerns. The IUCN Red List of Threatened Species is the world’s most comprehensive data resource on the status of species, containing information and status assessments on more than 40,000 species of animals and plants (Vié et al. 2009). As well as measuring the extinction risk faced by each species, the IUCN Red List includes detailed species-specific information on distribution, threats, conservation measures, and other relevant factors. This list is increasingly used by scientists, governments, nongovernmental organizations, businesses, and civil society for a wide variety of purposes, including zoos and aquariums that want to educate their visitors about the extinction risks faced by the exhibited species. The IUCN Red List categories and criteria are the world’s most widely used system for gauging the extinction risk faced by species. Each species assessed is assigned to one of eight different categories (figure 53.3), based on a series of quantitative criteria. Species classified as Vulnerable, Endangered, and

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Figure 53.2. The Living Planet Index of global biodiversity, measured as the relative aggregate size of 7,953 populations of 2,544 vertebrate species across all regions of the world over time, with 1970 as the baseline (WWF International 2010).

Figure 53.3. Structure of the IUCN Red List categories (Vié et al. 2009).

Critically Endangered are all regarded as “threatened.” The Red List shows that the status of the world’s species is deteriorating in all regions and in all taxonomic groups. However, three major ongoing extinction crises stand out in particular: amphibians, corals, and Asian large animals. Nearly one-third of the planet’s amphibians (31.1), one-quarter of its reefbuilding corals (27), and nearly one-quarter of its mammals (22.2) are threatened or extinct (figure 53.4). AMPHIBIAN EXTINCTION CRISIS Amphibians, representing more than 6,200 species worldwide, are one of the most threatened major taxonomic groups on the IUCN Red List (Hilton-Taylor et al. 2009). At least 42 of amphibian species have populations that are declining, indicating that the percentage of threatened species will likely only rise in the future. In contrast, fewer than 1 of amphibian species have populations that are increasing. Overall, there is strong evidence that the pace of amphibian extinctions is increasing: of the 38 known extinctions since

Figure 53.4. Proportion of species threatened with extinction in different taxonomic groups. The total number of described species in each group is indicated in parentheses. Error bars show minimum and maximum estimates (Hilton-Taylor et al. 2009).

the year 1500, 11 have occurred since 1980. Also, 120 species of amphibians have been listed as possibly extinct, most having not been seen since 1980. The most severe impact has been in Mesoamerica, the northern Andes, and the Greater Antilles. Habitat loss is the greatest threat to amphibians, affecting nearly 61 of all known species and a very large percentage (87) of those species that are threatened. However, the fungal disease chytridiomycosis has been the major driver of known and suspected amphibian extinctions over the past three decades. The disease-causing pathogen (Batrachochytrium dendrobatidis) was probably introduced to the affected regions (e.g., the Americas, Australasia, and Europe) by international trade in African clawed frogs (Xenopus laevis), which were previously used for pregnancy assays in humans (Weldon et al. 2004). In response to the amphibian crisis, the IUCN/SSC Am-

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phibian Specialist Group (ASG) and other partners have developed the Amphibian Conservation Action Plan (Gascon et al. 2007), which provides a comprehensive framework for combating amphibian declines and extinctions. A major priority is to protect the habitat of the many threatened amphibian species that do not occur in any protected areas. Another priority is working with zoos, aquariums, and other centers to shelter and breed amphibians threatened by chytridiomycosis, which cannot yet be treated in the wild and which can cause up to 100 mortality in certain species. The Amphibian Ark (AArk) is a global program created by IUCN/SSC and WAZA to manage threatened amphibians in captivity until it is safe to reintroduce them into the wild. CORAL EXTINCTION CRISIS Warm-water, reef-building corals provide essential habitat for many species of fishes and invertebrates, making them the most biologically diverse ecosystems in the ocean. All 845 known species of reef-building corals in the world have been assessed on the IUCN Red List. More than one-quarter (27) have been listed as “threatened” or at a high risk of extinction, with an additional 20 listed as “near threatened” (Hilton-Taylor et al. 2009), meaning that they will likely join a threatened category in the future. Moreover, reef-building

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corals are declining at a faster rate than any other group of species currently on the IUCN Red List. Just 15 years ago the overall level of threat to reef-building corals was very low. The catastrophic decline in the abundance of reef-building corals stems primarily from increased bleaching (i.e., the stress-induced whitening of corals) and disease events linked to higher sea temperatures that result from global warming. Coastal development and other human activities such as coral extraction and pollution have also contributed to dramatic declines since the mid-1990s. Ocean acidification resulting from increased levels of atmospheric carbon dioxide (CO) is further impacting reef-building coral species by negatively affecting calcification. The highest number of threatened species according to the IUCN Red List is in the Indo-Malay-Philippine Archipelago, or “Coral Triangle,” which is the global epicenter of marine biodiversity, with the highest number of coral species. In all regions, the loss of coral ecosystems will have huge cascading effects for reef-dependent species as well as for the large number of people and nations that depend on coral reef resources for economic and food security. Ex situ conservation may be necessary for corals and other coral-dependent species (figure 53.5; see Penning 2010), since measures to reduce the level of CO in the atmosphere are still a long way from having an effect.

Figure 53.5. Ex situ propagation of corals at Oceanário de Lisboa in Portugal. Photograph by Gerald Dick.

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LARGE ANIMALS OF ASIA EXTINCTION CRISIS The third extinction crisis revealed by the IUCN Red List is for animals in Southeast Asia (Hilton-Taylor et al. 2009). Globally almost one-quarter of mammals (22.2) are threatened with extinction, but Asian countries are showing the most impact. Of the top 20 countries with threatened mammal populations, ten are in Asia, where there have been massive population declines over the past two decades. The Indo-Malayan region shows rapid declines in both birds and mammals, driven by deforestation, habitat loss, and high rates of hunting for mammals. Large-bodied taxa throughout Asia, including mammals, birds, fishes, and reptiles (such as turtles), are being impacted by massive and largely uncontrolled overexploitation. Two mammalian extinctions have likely resulted in the last few years: the baiji or Yangtze River dolphin (Lipotes vexillifer) in China and the kouprey (Bos sauveli), a forest-dwelling large ungulate once found mainly in Cambodia but also in Laos, Vietnam, and Thailand. There is an urgent need throughout Asia to address the overexploitation of wildlife through antipoaching measures and the control of trade in wildlife products. For example, the often unsustainable and illegal hunting of wild animals for meat—so-called bushmeat—does not only reduce populations of several species, including the great apes (Bennett et al. 2007). The consumption of great apes as bushmeat is also considered a vector of human immunodeficiency virus (HIV) and Ebola virus in Africa. Initiatives are needed that focus not only on antipoaching but also on providing alternative livelihoods for local people—allowing the root causes of poaching to be addressed through such measures as providing alternative protein sources (e.g., breeding of cane rats, Thryonomys spp.) and implementing capacity-building and training programs. The conversion of lowland forests for palm oil and other biofuels also needs to be urgently addressed, especially in Indonesia and Malaysia. There is growing evidence that climate change will become one of the major drivers of species extinction in the coming years. IUCN recently completed the first phase of a project to identify species most vulnerable to climate change (Foden et al. 2009). The results showed that 52 of all amphibian species and 71 of warm-water, reef-building corals are potentially susceptible. This information will highly influence our approach to species conservation in the future. However, other more “traditional” threats, such as habitat loss, invasive species, and overharvesting, remain critically important and should not be overlooked because of the current attention being given to climate change by many of the world’s leading environmental agencies and donors. Stemming the tide of global extinctions requires urgent action by all parts of society. Species are of enormous importance to human livelihoods, and the benefits they provide will continue in perpetuity if we learn to manage biodiversity sustainably. In the next decade the tide must turn for species conservation, and society must respond to the wake-up call that the IUCN Red List represents. This is the challenge we must all address in the next decade if future generations are to have the chance not only to enjoy the full diversity of the world’s species but, ultimately, to survive.

WORLD ZOO AND AQUARIUM CONSERVATION STRATEGIES The following section is based on a review of zoo and aquarium conservation strategies by Gipps (2010). The first World Zoo Conservation Strategy was published in 1993. It was jointly produced by the International Union of Directors of Zoological Gardens (IUDZG) and the IUCN/SSC Conservation Breeding Specialist Group (CBSG). In the foreword, HRH the Duke of Edinburgh, then president of WWF International, wrote the following: “Much can be done by establishing and managing protected areas, but there are many species whose natural habitats have already been degraded or destroyed. For these the only hope of survival is the direct stewardship and human care in zoological and botanical gardens in captive breeding centres.” Note the emphasis on “human care . . . in captive breeding centers.” The document itself contained eleven chapters: • Introduction: Zoos in a changing world • The world conservation strategy and zoos • The global zoo network • Education • Zoo animal collections and their conservation • Ex situ conservation of animal populations • Capacity: Space limitations and choice of species • Artificial reproduction and cryopreservation: Biotechnology in support of conservation • Back to nature: Animals for reintroduction and restocking • Knowledge and research • The way forward: Towards a new integration A notable feature of this list is that it concentrates almost exclusively on ways in which zoos can maintain sustainable populations within their institutions, with the notion that reintroductions or restocking are the principle [sic] objectives of the exercise. In 2002, the council of WAZA (formerly known as IUDZG) decided that the strategy needed substantial revision. At its annual conference that year, under the auspices of its newly formed Conservation Committee, a workshop was held to discuss what a new World Zoo and Aquarium Conservation Strategy might contain (Gipps 2010). The resulting strategy document, “Building a Future for Wildlife: The World Zoo and Aquarium Conservation Strategy” (WZACS), was published by WAZA in 2005. The chapters in that document, and the vision statements at the beginning of each chapter, are: 1. Integrating conservation: The major goal of zoos and aquariums will be to integrate all aspects of their work with conservation activities. The fundamental elements of each organization’s culture will be the values of sustainability and conservation,

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Good Practice Tip: All of a keeper’s daily work—for example, with regard to animal care, resource use, and public relations—should be conceived and designed to contribute to achieving the overall goal of conserving wild species and habitat.

and social and environmental responsibility. These values will permeate all areas of their work and will be understood and promoted by all those working within the WAZA network. 2. Conservation of wild populations: Zoos and aquariums will make further contributions to conservation in the wild by providing knowledge, skills, and resources through initiatives in zoo breeding, translocations and reintroduction, wildlife health, research, training, education, and by funding field activities. Zoos and aquariums will be an important force for worldwide conservation by their employment or support of field workers active in the conservation of wild animals and their habitats. 3. Science and research: Zoos and aquariums are fully and actively integrated into the research community and into public consciousness and understanding of science, as serious, respected scientific institutions that make significant contributions and sound scientific decisions for wildlife worldwide. 4. Population management: All zoos and aquariums will be primary centers of expertise in small population management and will be involved in global or regional cooperative breeding programs. All such programs will be based on sound knowledge using the latest available data on population management, reproductive biology, genetics, behavior, physiology, nutrition, veterinary care, and husbandry. 5. Education and training: Zoos and aquariums with their unique resource of live animals, their expertise, and their links to field conservation will be recognized as leaders and mentors in formal and informal education for conservation. The educational role of zoos and aquariums will be socially, environmentally, and culturally relevant, and by influencing people’s behavior and values, education will be seen as an important conservation activity. Zoos and aquariums will expand the training of their own staff and of others engaged in in situ and ex situ work. 6. Communication: Marketing and public relations: Zoos and aquariums and their national and regional associations will become highly effective in communicating conservation issues and their role in conservation. They will become better recognized as one of the major and most trusted voices speaking on behalf of wildlife and wild places.

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7. Partnerships and politics: Through increased cooperation and judicious encouragement, zoos and aquariums will continue to raise standards of animal management, educate the public to act on behalf of conservation issues, and assist in field projects. Partnerships will strengthen global cooperation and help all zoos, aquariums, and other conservation organizations to improve and to achieve their conservation goals. Zoos and aquariums will be encouraged to help one another, particularly those that have fewer resources and/or expertise. 8. Sustainability: All zoos and aquariums will work towards sustainability and reduce their “environmental footprint.” They will use natural resources in a way that does not lead to their decline, thus meeting the needs of the present without compromising future generations. All zoos and aquariums will serve as leaders by example, using green practices in all aspects of their operations and by demonstrating methods by which visitors can adopt sustainable lifestyles. 9. Ethics and animal welfare: All zoos and aquariums will follow ethical principles and maintain the highest standards of animal welfare in order to establish and sustain viable populations of healthy animals for conservation purposes and to convey credible conservation messages to the public. What is particularly striking about this list of chapters is that, although there is overlap with the contents of the 1993 strategy (particularly with respect to the conservation education role of zoos), there is also a strong degree of divergence. In particular, the conservation of wild populations has become a core element of the new strategy, because it is now a core element of the conservation work (both action and research) that zoos and aquariums do. The introduction to the 2005 strategy is littered with references to conservation in the wild. For example, the definition of conservation is given as “securing of longterm populations of species in natural ecosystems and habitats wherever possible.” This definition is followed by an explanatory note that says that the words “natural ecosystems and habitats” signify that “no amount of worthy endeavor is of ultimate value if it doesn’t translate into animals and plants surviving in the wild.” Apart from the change in emphasis of the 2005 strategy compared with that of 1993, the world has changed in another hugely important way; we now live in the age of the Internet. A few thousand copies of the World Zoo Conservation Strategy were printed in 1993 and basically, that was it. Most major zoos in the world bought several copies, and some copies went to government and nongovernment conservation agencies around the world. But, if you had not received a printed copy, you probably did not see it. The contrast between the 1993 and 2005 documents is astonishing. The WZACS has now been translated into Chinese, Czech, French, German, Hungarian, Polish, Portuguese, Russian, Spanish, and Swedish and has been

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downloaded from the WAZA website more than 250,000 times, in addition to 10,000 printed copies of the English version plus many more thousand copies in the other languages. Clearly, this is a document that has been seen and used by a very large number of people. Indeed, the conservation strategies of many regional zoo and aquarium associations, and many of their institutional members, are based on the WZACS. A subtheme of the WZACS is the “Global Aquarium Strategy for Conservation and Sustainability,” published by WAZA in 2009 (see Penning 2010). It is believed that the WZACS has been, at least in part, instrumental in the way that zoos and aquariums have changed how they view their role in the wider world of conservation. Zoos and aquariums all over the world now believe their role in helping to conserve wild populations of animals (and plants) to be as important as conservation breeding programs and the possibilities of reintroductions. Of course, the two processes remain inextricably linked; zoos and aquariums are, after all, an astonishingly powerful and large resource for maintaining assurance populations of species threatened in the wild. But, in the modern world, zoos and aquariums acknowledge that breeding programs and reintroductions are not, and never will be, enough. We know of no responsible zoo or aquarium director who would regard the existence of the last remnants of a species, held solely and permanently in human care, as any sort of success. Rather, the conservation world at large, which includes all those zoos and aquariums committed to conservation, would count that as a sad, and indeed abject, failure. CONSERVATION THROUGH ZOOS AND AQUARIUMS In the years 2000 and 2001, WAZA organized three workshops on how it should become more involved through in situ conservation. One recommendation was that with the goal of becoming an internationally recognized conservation organization, WAZA should brand suitable conservation projects. The idea behind the WAZA branding is to create a win-win situation: The brand promotes the project and also lets WAZA use it to convey what zoos and aquariums do for conservation globally. Projects or programs are branded on application, with three sets of endorsement criteria focusing on biological, operational, and institutional and partnership issues. Applications have to meet the criteria set forth by the WAZA executive office. Applications may be submitted by either the project receiving support from a member of WAZA or by a WAZA member providing support to the project. Since inception of the scheme in 2003, the number of WAZA-branded projects has steadily increased to 214 (in November 2011). The authors of this chapter compiled and assessed conservation projects supported by the world zoo and aquarium community, focusing on 113 WAZA-branded projects (Gusset and Dick 2010a, b). The majority of projects had their main focus on species protection. They mainly focused on mammals, and mostly on charismatic primates and carnivores. Most of the projects involved working with taxa classified as globally threatened with extinction according to the 2008

IUCN Red List of Threatened Species. Amphibians and fishes were underrepresented in the number of projects relative to the percentage of threatened species described in these taxa. The projects were primarily active in the Eurasian, subSaharan African, or Southeast Asian regions (figure 53.6). They focused strongly on terrestrial habitats, among them chiefly tropical and subtropical forests. Terrestrial habitats at high conservation risk, especially Mediterranean woodlands and temperate grasslands, were underrepresented. Project leaders typically applied for WAZA branding to increase their publicity or credibility or to attract support from zoos and aquariums. Later, these project leaders were generally undecided later about whether the WAZA branding had resulted in the desired outcome. Projects mainly each received support from one or two to five zoos and aquariums. Zoos and aquariums primarily became involved in projects either on their own initiative or because the projects had requested their support. The main form of project support they provided was monetary funding. Their contributions (including nonmonetary support) often covered more than half of a project’s annual financial expenditures. Most of the projects would not have been viable without the support from zoos and aquariums. Their financial expenditures were typically in the range of US $10,000 to $100,000 per year, with their duration often being longer than 10 years. In assessing these projects’ conservation impact, we also asked how much the projects improved the conservation status of their target species or habitats (Gusset and Dick 2010a, b). The projects, on average, reached a self-assessed impact score of three out of four possible points. We then did an evaluation of the concurrent influence of all of the above attributes on a project’s impact score. This analysis revealed that the higher a project’s financial expenditures and the higher the contribution made by zoos and aquariums to these financial expenditures, the higher was the project’s impact score. In the following section, conservation success stories are presented in which zoos and aquariums were heavily involved, the focus is on reintroduction projects where a direct link between ex situ and in situ conservation was often most visible and communicable to the public. These are classic examples of how conservation breeding programs in zoos and aquariums, when effectively coordinated with protective measures in the wild, can help re-diversify life on the planet (Stanley Price and Fa 2007; Earnhardt 2010). However, as is pointed out repeatedly throughout this chapter, zoos and aquariums need to move beyond the paradigm of captive breeding and reintroduction. The handful of iconic species in these projects includes the American bison (Bison bison), probably the first captive-bred animal to be reintroduced for conservation purposes back in 1907; the black-footed ferret (Mustela nigripes), for which removal from the wild for captive breeding started in 1985; the California condor (Gymnogyps californianus), which after being taken into captivity started to breed successfully in 1988; the Arabian oryx (Oryx leucoryx), released in Oman in 1982 using stock mainly from the United States; and the golden lion tamarin (Leontopithecus rosalia), which was the subject of great interzoo collaboration and successful release back into Brazil, starting from 1984.

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Figure 53.6. Geographic distribution of in situ conservation projects supported by the world zoo and aquarium community. The map shows major terrestrial habitat types, or biomes, of the world (Olson et al. 2001).

American bison once numbered in the tens of millions and ranged from Alaska to northern Mexico. They were then nearly eliminated by intensive hunting in the late 19th century. In 1906 only about 1,000 bison, captive and wild, remained in North America. One year later the American Bison Society, founded at New York’s Bronx Zoo, started reintroducing captive-bred bison into reserves in the western United States. In addition to approximately 500,000 bison in captive commercial populations, there are now about 30,000 bison in conservation herds. Mainly as a consequence of the degradation of the North American prairie ecosystem, only 18 black-footed ferrets remained in the wild by 1985. In the same year, a number of zoos and other organizations started collaborating on a captive breeding program with ferrets collected from the wild. After a period of prerelease conditioning, in which the ferrets lived in pens with prairie dog (Cynomys spp.) burrow systems, reintroduction started in 1991. About 1,000 black-footed ferrets now live in the wild. As a consequence of habitat destruction, poaching, and lead poisoning, the California condor declined to the extent that in 1981 only 22 birds remained in the wild. After the last remaining wild specimens were brought into captivity at the Los Angeles Zoo and San Diego Zoo’s Wild Animal Park in 1987, a captive breeding program was started through collaboration between zoos and various other organizations. From 1992 onwards, captive-bred condors have been reintroduced. Innovative methods include removing eggs from condor nests to encourage females to lay replacement eggs, using adult lookalike condor puppets to feed newly hatched chicks to prevent them from imprinting on humans, and aversive conditioning to avoid power lines and humans. About 170 California condors now live in the wild. The Arabian oryx was exterminated in the wild as a con-

sequence of intensive hunting, with the last animal shot in Oman in 1972. Luckily, a captive herd had been established in the early 1960s by the Phoenix Zoo. Other zoos in the United States and Europe joined the captive breeding program, and Arabian oryx have been released from 1978 onwards at several sites throughout the Arabian Peninsula. In addition to approximately 6,000 to 7,000 captive animals, about 1,100 Arabian oryx now live in the wild. Mainly as a consequence of habitat destruction, only a few hundred golden lion tamarins remained in the early 1970s. Starting in 1972, a captive population was built up at the Smithsonian’s National Zoological Park in Washington, DC, and in other zoos, in association with a primate center in Rio de Janeiro, Brazil. Before reintroduction started in 1984, the tamarins went through a prerelease training program during which the animals learned how to search for hidden food and how to use natural substrates for locomotion. The tamarins were subsequently acclimatized in enclosures built around natural vegetation at the release site, and were subjected to post-release training. About 1,000 golden lion tamarins now live in the wild. SUMMARY The goal of conservation biology is to provide principles and tools for preserving biological diversity. This biodiversity—the variety of genes, species, and ecosystems that constitute life on earth—is increasingly threatened by human activities. Zoos and aquariums are involved in numerous practical issues in biodiversity conservation both in nature (in situ) and outside the natural habitat (ex situ), at home and abroad. However, zoos and aquariums cannot leverage a conservation message when keeping animals in substandard conditions, and they cannot cultivate a conservation ethic in their visitors without

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doing business in a sustainable way. Integrated management between wild and captive populations is increasing, and we see it as a major niche on which zoos and aquariums should focus their conservation efforts, including the recovery and management of small populations and translocation biology. Zoos and aquariums, unlike other conservation organizations, enjoy the distinct advantage of having physical sites that people can visit. Can we envision a day when the zoo or aquarium becomes a conservation organization that exhibits animals as part of its mission to connect people to nature, and uses this connection to preserve species in the wild? A number of zoos and aquariums, keeping alive the flame of species conservation, are almost there. REFERENCES Althaus, Thomas, Laurie Bingaman-Lackey, Fiona A. Fisken, and Dave Morgan. 2010. The role of international studbooks in conservation breeding programmes. In Building a Future for Wildlife: Zoos and Aquariums Committed to Biodiversity Conservation, ed. Gerald Dick and Markus Gusset, 49–52. Gland: WAZA Executive Office. Bennett, Elizabeth L., Eric Blencowe, Katrina Brandon, David Brown, Robert W. Burn, Guy Cowlishaw, Glyn Davies, Holly Dublin, John E. Fa, E. J. Milner-Gulland, John G. Robinson, J. Marcus Rowcliffe, Fiona M. Underwood, and David S. Wilkie. 2007. Hunting for consensus: Reconciling bushmeat harvest, conservation, and development policy in West and Central Africa. Conservation Biology 21:884–87. Caughley, Graeme. 1994. Directions in conservation biology. Journal of Animal Ecology 63:215–44. CBD. 2010. Global biodiversity Outlook 3. Montreal: CBD Secretariat. Dick, Gerald, and Markus Gusset, eds. 2010. Building a Future for Wildlife: Zoos and Aquariums Committed to Biodiversity Conservation. Gland, Switzerland: WAZA Executive Office. Djoghlaf, Ahmed. 2010. Convention on Biological Diversity: Conservation of Biodiversity through 2010 and Beyond. In Building a Future for Wildlife: Zoos and Aquariums Committed to Biodiversity Conservation, ed. Gerald Dick and Markus Gusset, 17–20. Gland, Switzerland: WAZA Executive Office. Earnhardt, Joanne M. 2010. The role of captive populations in reintroduction programs. In Wild Mammals in Captivity: Principles and Techniques for Zoo Management, 2nd ed., ed. Devra G. Kleiman, Katerina V. Thompson, and Charlotte Kirk Baer, 268–80. Chicago: University of Chicago Press. Foden, Wendy B., Georgina M. Mace, Jean-Christophe Vié, Ariadne Angulo, Stuart H. M. Butchart, Lyndon DeVantier, Holly T. Dublin, Alexander Gutsche, Simon N. Stuart, and Emre Turak. 2009. Species susceptibility to climate change impacts. In Wildlife in a Changing World: An Analysis of the 2008 IUCN Red List of Threatened Species, ed. Jean-Christophe Vié, Craig Hilton-Taylor, and Simon N. Stuart, 77–87. Gland, Switzerland: IUCN. Gascon, Claude, James P. Collins, Robin D. Moore, Don R. Church, Jeanne E. McKay, and Joseph R. Mendelson III, eds. 2007. Amphibian Conservation Action Plan. Gland, Switzerland: IUCN. Gipps, Jo. 2010. The world zoo and aquarium conservation strategy: Where do we go from here? In Building a Future for Wildlife: Zoos and Aquariums Committed to Biodiversity Conservation, ed. Gerald Dick and Markus Gusset, 35–38. Gland, Switzerland: WAZA Executive Office. Gusset, Markus, and Gerald Dick. 2010a. ‘Building a Future for Wildlife’? Evaluating the contribution of the world zoo and aquarium community to in situ conservation. International Zoo Yearbook 44:183–91.

———. 2010b. Biodiversity conservation projects supported by the world zoo and aquarium community. In Building a Future for Wildlife: Zoos and Aquariums Committed to Biodiversity Conservation, ed. Gerald Dick and Markus Gusset, 57–60. Gland, Switzerland: WAZA Executive Office. ———. 2011a. The global reach of zoos and aquariums in visitor numbers and conservation expenditures. Zoo Biology 30:566–69. Gusset, Markus, and Gerald Dick, eds. 2011b. WAZA Magazine 12: Towards Sustainable Population Management. Gland, Switzerland: WAZA Executive Office. Hilton-Taylor, Craig, Caroline M. Pollock, Janice S. Chanson, Stuart H. M. Butchart, Thomasina E. E. Oldfield, and Vineet Katariya. 2009. State of the world’s species. In Wildlife in a Changing World: An Analysis of the 2008 IUCN Red List of Threatened Species, ed. Jean-Christophe Vié, Craig Hilton-Taylor, and Simon N. Stuart, 15–41. Gland, Switzerland: IUCN. IUDZG/CBSG. 1993. The World Zoo Conservation Strategy: The Role of the Zoos and Aquaria of the World in Global Conservation. Chicago: Chicago Zoological Society. Niekisch, Manfred. 2010. International conservation policy and the contribution of the zoo and aquarium community. In Building a Future for Wildlife: Zoos and Aquariums Committed to Biodiversity Conservation, ed. Gerald Dick and Markus Gusset, 45–48. Gland, Switzerland: WAZA Executive Office. Olson, David M., Eric Dinerstein, Eric D. Wikramanayake, Neil D. Burgess, George V. N. Powell, Emma C. Underwood, Jennifer A. D’Amico, Illanga Itoua, Holly E. Strand, John C. Morrison, Colby J. Loucks, Thomas F. Allnutt, Taylor H. Ricketts, Yumiko Kura, John F. Lamoreux, Wesley W. Wettengel, Prashant Hedao, and Kenneth R. Kassem. 2001. Terrestrial ecoregions of the world: A new map of life on earth. BioScience 51:933–38. Penning, Mark. 2010. Aquariums and the conservation of waterdependent species. In Building a Future for Wildlife: Zoos and Aquariums Committed to Biodiversity Conservation, ed. Gerald Dick and Markus Gusset, 35– 38. Gland, Switzerland: WAZA Executive Office. Reid, Gordon McGregor. 2010. Introduction. In Building a Future for Wildlife: Zoos and Aquariums Committed to Biodiversity Conservation, ed. Gerald Dick and Markus Gusset, 11– 14. Gland, Switzerland: WAZA Executive Office. Soulé, Michael E. 1985. What is conservation biology? BioScience 35:727–34. Stanley Price, Mark R., and John E. Fa. 2007. Reintroductions from zoos: A conservation guiding light or a shooting star? In Zoos in the 21st Century: Catalysts for Conservation? ed. Alexandra Zimmermann, Matthew Hatchwell, Lesley Dickie, and Chris West, 155–77. Cambridge: Cambridge University Press. Stuart, Simon N., Dena Cator, and Jane Smart. 2010. International Union for Conservation of Nature: Global species crisis and conservation challenges. In Building a Future for Wildlife: Zoos and Aquariums Committed to Biodiversity Conservation, ed. Gerald Dick and Markus Gusset, 21– 24. Gland, Switzerland: WAZA Executive Office. Vié, Jean-Christophe, Craig Hilton-Taylor, Caroline M. Pollock, James Ragle, Jane Smart, Simon N. Stuart, and Rashila Tong. 2009. The IUCN Red List: A key conservation tool. In Wildlife in a Changing World: An Analysis of the 2008 IUCN Red List of Threatened Species, ed. Jean-Christophe Vié, Craig Hilton-Taylor, and Simon N. Stuart, 1–13. Gland, Switzerland: IUCN. Weldon, Ché, Louis H. du Preez, Alex D. Hyatt, Reinhold Muller, and Rick Speare. 2004. Origin of the amphibian chytrid fungus. Emerging Infectious Diseases 10:2100–2105. WAZA. 2005. Building a Future for Wildlife: The World Zoo and Aquarium Conservation Strategy. Bern: WAZA Executive Office. ———. 2009. Turning the Tide: A Global Aquarium Strategy for Conservation and Sustainability. Bern: WAZA Executive Office.

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conservation biolo gy WWF International. 2010. Living Planet Report 2010. Gland, Switzerland: WWF International. Zimmermann, Alexandra. 2010. The role of zoos in contributing to in situ conservation. In Wild Mammals in Captivity: Principles and Techniques for Zoo Management, 2nd ed., ed. Devra G. Klei-

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