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Kathy Traylor‑Holzer1 and Jonathan D. Ballou2 Is Conservation Really Black and White?

Giant pandas. Most people, daresay The Past – the 1970s (Nicholls 2011). The resulting everyone reading this article, have an the 1980s and before state gifts and eventual breeding loans immediate internal response to this of panda pairs have had widespread species. What is your initial reaction? The has long been international impacts beyond the sur- Is it positive? Or negative? Conserva- shrouded in mystery. Restricted to vival of this single species and helped tion success, or failure? How much remote mountainous areas of west- to open to the world. do you really know about this unique ern China, amazingly this species was species and its journey toward pres- unknown to all except local residents For receiving these high profile ervation? until 1869, even within China. This animals, however, breeding giant carnivore that eats bamboo and ap- pandas posed challenges. Difficulties Few species spark as much emotion pears to have an opposable‘ thumb’ in breeding a solitary species with a and debate, and frequent misper- confused taxonomists and challenged short breeding season (1–2 day estrus ception, as the giant panda. Among early attempts to maintain captive once a year) and delayed implantation, © Kathy Traylor‑Holzer the general public it is a much loved specimens, adding to its mystic. Few combined with behavioral issues such Pan Pan (ISB# 308), a 30-year‑old wild‑caught founder now retired at the Dujiang- yan giant panda base, was an infamously prolific male, siring 29 cubs in 17 litters icon subject to frequent anthropo- individuals made it out of China for as inexperience, incompatibility and and accounting for 9% of the genetic composition of the current ex situ population. morphism and occasional fanaticism. decades, making it a rare and little disinterest, led to frequent repro- The Beginning – the 1990s Biologists often think of it as a spe- understood curiosity. All of that ductive failure. Newborn cubs are cies fraught with reproductive issues changed with Mao Zedong. extremely small and altricial, which At first, successful reproduction was and by State Forestry Administration 61 giant pandas at the major Chinese and restrictive dietary requirements contributed to low survival. Public slow and there were few surviving (SFA) facilities such as Wolong. While breeding facilities during 1998-2000 that threaten its survival. For many Its striking physical appeal and en- perception was, and often still is, that cubs. By 1980 the worldwide captive institutions from these two different identified behavioral, nutritional and conservationists, it is viewed as a demism combined with its absence giant pandas reproduce poorly and population had grown to 100 pandas, government ministries cooperated, health issues contributing to low drain on limited resources for conser- from historic Chinese culture such as are not viable long term in captivity. but most of the population was wild there was no single, overall manage- reproductive success. Additional col- vation with little return. But for many paintings and literature placed the gi- That indeed was the case at one time. born. Population size remained at ment strategy. Recognizing the need laborations addressed health, capac- of us close to this species, the giant ant panda in a unique position during All that has changed – and it is due 100-115 pandas for many years, with for a scientifically‑based captive man- ity building and other issues. This fed panda is an emerging conservation the Culture Revolution. While Mao primarily to extensive collaboration on births just compensating for fewer agement plan, Chinese managers into a CBSG‑led workshop in early success story that demonstrates the declared a‘ war against nature’ and re- an international scale toward com- captures from the wild to prevent invited the IUCN SSC Conservation 2002 that established the structure benefits of comprehensive planning jected most cultural icons such as the mon conservation goals and fueled by decline. But in 1997 something Breeding Specialist Group (CBSG) to of a Chinese scientific management and extensive collaboration that can Chinese (Shapiro 2001), the giant science. Each of the many partners in noteworthy happened – for the first facilitate the development of such a committee that meets annually to conserve a species, and possibly even panda was embraced as a symbol of this decades‑long effort has its own time, and ever since, the number of plan. No stranger to China, CBSG had share management and research more. Let us explain. modern China and acted as a catalyst, rich story to tell. Here we present one captive‑born giant pandas in captivity facilitated the development of a stud- achievements and to develop each along with table tennis, to bridge rela- aspect in which we have been involved exceeded the number of wild‑born in- book and masterplan for the Critically year’s breeding plan (see Wildt et al. tions between China and the West in as population management advisors dividuals. Soon after, the population Endangered South China tiger just 2006 for more details). to the global ex situ population. began to grow and become demo- a year earlier in 1995. In late 1996, a graphically sustainable. The future of CBSG‑led team headed to Chengdu We (the authors) were fortunate the species in zoos was changed by to begin this process for giant pandas. enough to participate in that inaugu- a series of collaborative events that ral 2002 meeting and have provided Figure 1 began in 1996 in Chengdu, China. Chinese workshop participants population management advice to acknowledged their challenges and the global giant panda program each Census of the giant panda By the mid-1990s, several Chinese agreed that their goal was “to de- year thereafter. Along the way we global captive population by origin from the 2015 facilities were breeding giant pandas. velop a self‑sustaining population of have witnessed its transformation International Studbook However, only a few adults were suc- giant pandas that will assist support- into a well‑managed, viable popula- (data from Xie 2015). cessful breeders, thereby failing to ing a long‑term, viable population tion that can contribute to the secu- capture genes from most wild‑caught in the wild” – a vision beyond the rity and recovery of this endangered pandas and limiting population exhibition of pandas in zoos. Interna- species. growth. Neonatal mortality, nutrition tional experts assisted in the analysis and health issues also plagued the of problems related to reproduction population. A further complication and health as well as infrastructure was that captive pandas in China and capacity building needs. While 1 IUCN SSC Conservation were managed both in zoological the challenges were great, so was the Breeding Specialist Group institutions (by the Chinese Associa- potential for success, and motiva- 2 Smithsonian Conservation tion of Zoological Gardens – CAZG) tion was high. A biomedical survey of Biology Institute 4 WAZA 1/16 WAZA 1/16 5

North America 17 pandas China 366 pandas • Jinbao Paradise • Wenzhou Zoological Gardens • San Diego | US • Anji Bamboo Gardens • Langzhong Panda Paradise • Wolong Gengda • Memphis Zoo | US • Anyang Zoological Garden • Lanzhou Zoo Giant Panda Base • Zoo Atlanta | US • Baoxing Education Center • Linyi Botanical Garden • Wolong Hetaoping • National Zoological Park | US • Beijing Zoological Gardens • Liugongdao Park Giant Panda Base • Toronto Zoo | Canada • Changsha Ecological Zoo • Liuzhou Zoo • Wuhan Zoo • Chapultapec Zoo | Mexico • Chengdu Research Base • Nanchang Zoological Garden • Wuxi Zoological Garden of Giant Panda Breeding • • Xiazhuhu National Europe 11 pandas • Chengdu Zoological Garden • Ningbo Zoological Garden Everglade Park • Edinburgh Zoo | Scotland • Chongqing Zoological Garden • Northeast Tiger Garden • Xiuning Giant Panda • Pairi Daiza Zoo | Belgium • Dafeng Zoo • Panyu Xiangjiang Safari Park Ecological Park • Tiergarten Schönbrunn | Austria • Dalian Forest Zoo • Zoological Gardens • Xixiakou Wild Animal Park • Zoo de Beauval | France • Dujiangyan Giant Panda Base • Sanjiang Ecological Tourism • Ya’an Bifengxia • Zoo Aquarium de Madrid | Spain • Emei Xianzhizhujian Zone Giant Panda Base Ecological Park • Shanghai Wild Animal Park • Yangzhou Zoological Garden Asia outside of mainland China • Fuzhou Giant Panda • Shanghai Zoological Garden • Yichang Children’s + Australia & Oceania • Shanxi Rare Wildlife Research Zoological Garden 27 pandas Research Center • Guangzhou Zoological Garden Center • Zibo Yuanshan National • Ocean Park | Hong Kong • Shenzhen Safari Park Forest Park • Seac Pai Van Park | Macau • Guilin Qixing Park Zoo • Guizhou Forest • Shijizhuang Zoo Figure 2 • Zoo | • Taihu Everglade Park • Chiangmai Zoo | Thailand Wild Animal Park • Hangzhou Wild Animal Park • Taiyuan Zoological Garden Giant pandas currently • Zoo Negara | Malaysia • Tianjin Fude Zoo in zoos worldwide. • River Safari | Singapore • Hangzhou Zoological Garden • Hefei Wild Animal Park • Tianjin Zoological Park • Tokyo Ueno Zoo | • Tianmuhu Garden • Kobe Oji Zoo | Japan • Huaying Mountain Giant Panda Wild Training Base • Wenling Changyu Dongtian • Adventure World | Japan Scenic Spot • Adelaide Zoo | Australia • Jinan Zoo

The Present – 2000 to 2015 A One Plan Approach

Over the past 14 years the giant Improved understanding of factors An important aspect in the success Resolving any demographic chal- Since the 1996 workshop, giant Management of the ex situ popula- panda population has developed into affecting reproductive success has of the giant panda population is the lenges to promote growth is essential panda managers viewed the ex situ tion is a shared collaboration be- a demographically stable population, played a role, especially for females. concentration of pandas in a few for population viability, but it can population as a tool to support pan- tween the CAZG zoos and the State expanding from 152 pandas in 19 in- Promoting successful mating behav- large breeding centers in China. be easier behaviorally, logistically das in the wild. The current officially Forestry Administration. Annual stitutions in 2002 to the current (No- ior in males continues to be a chal- Within each breeding center lies and even politically than managing stated goal of the ex situ program is: giant panda conferences intersperse vember 2015) population of 423 indi- lenge, and the extremely short estrus a vast body of expertise in husbandry, it genetically. Working to produce presentations on the status, research viduals in 78 institutions worldwide of each female leaves little time for veterinary care, and reproduction. more little baby pandas is motivating. The maintenance of a sustainable ex and management of wild pandas (Figure 1). While the rescue of an adaptive learning. The development A large number of individuals within Purposefully reducing the number situ giant panda population that is with those of the ex situ population. occasional wild individual occurs, of successful artificial insemination a single facility provide options for of cubs in favor of greater emphasis genetically and demographically viable Disease centers focus on the health of 92% of the ex situ population is cap- (AI) procedures for giant pandas has mates when initial pairing attempts on breeding genetically valuable ani- and can provide animals for release to both captive and wild pandas, and ex tive born. Annual growth ranged from provided a safety net. Most mat- fail. Three Chinese facilities ac- mals is more difficult to explain and support the wild population. situ facilities provide staging grounds 9–15% except when intentionally ings involve either natural mating counted for 80% of the births since enforce. As with most ex situ popula- for individuals transitioning between slowed. This demographically healthy by 2–3 males or natural mating by 2002 and are the heart of the ex situ tions, reproductive success rates are Recognized conservation roles of the these environments. population has a well‑balanced age a single male followed by AI from population. often lower with individuals near the ex situ population and related contri- and sex structure that is the envy of multiple male donors, with relatively top of the mean kinship list, and the butions of the ex situ community to Perseverance has been strong, and many managed programs. few matings relying solely on AI. Sub- Strong population growth and high temptation to rely on good yet ge- giant panda conservation are: was needed when the May 2008 sequent genetic testing verifies the levels of gene diversity retained netically over‑represented breeders earthquake hit the Wolong breeding A variety of factors led to this strong paternity of offspring, and show that (97%) allowed the setting of a lofty is strong, and especially so for giant • Source of giant pandas for center in the mountains of , population growth. Improvements in when both natural mating and AI are quantitative goal for this population pandas. In recent years the mantra reintroduction needs home to 63 giant pandas at that time. nutrition and veterinary care im- used, it is almost invariably the males that is seldom achievable or even “quality over quantity” has dominated • Insurance population against popu- The amazing dedication of and rescue proved overall survival, and rearing that naturally mated with the female considered – the retention of at least the annual giant panda conferences lation decline or loss in the wild efforts by the Wolong staff during protocols have increased neonatal that are the offsprings’ sires. While 90% gene diversity for 200 years, as and technical meetings. The genetic • Research opportunities this tragedy meant that only three survival. About 50% of litters consist natural mating behavior is preferred, originally recommended for captive value of mated pairs (i. e., those with (e.g., disease prevention) pandas were lost in the resulting of twins vs single cubs, yet it is diffi- AI offers opportunities for reproduc- populations by Soule et al. (1986). low Mate Suitability Index scores) • Resource for developing techniques landscapes that destroyed the breed- cult for females to rear two such altri- ing genetic valuable non‑breeding About 500 pandas (400–600, depend- is reported and applauded by both that can support wild panda con- ing center and 120,000 ha of giant cial young that are only about 1/1000 males and for cross‑institutional ing upon the intensity of genetic CAZG and SFA. While this change in servation in China (e. g., censusing, panda habitat. of the size of the female at birth. The transfers of sperm instead of living management) are needed to achieve priorities, from the number of baby health status) practice of periodically switching animals. In 2015 the first transfer of this genetic goal set by the giant pandas to the genetic value of those • Economic and political benefits The rapid improvement in the vi- siblings between the mother and the sperm from China to the US dem- panda scientific committee in 2009; cubs, took several years before it to support wild population ability of the ex situ population over nursery (with always one cub in each) onstrated the potential value of this the population is now approaching its was embraced, it now is accepted conservation the past two decades has been allows both twins to survive and yet technique for long‑distance transfers. target size and can realistically meet practice. As a result, gene diversity • Resource for public education matched by similar improvements in reap the benefits of being mother All of these achievements were the this goal. has not only been maintained but has and public awareness the wild. The 2015 census, the fourth reared. result of strong collaborations among increased from 96.9% in 2002 derived such National Giant Panda Survey dedicated managers, researchers from 41 founders to 97.4% derived completed every 10 years, estimates and veterinarians within China and from 52 founders. the wild population at 1,864 pandas, partner holding institutions around representing a 17% increase over the world. the past decade. Advancements 6 WAZA 1/16 WAZA 1/16 7

© ZoosDalian Victoria Forest Zoo Participants of the 2015 Annual Conference of the Chinese Committee of Breeding Techniques for giant pandas, representing many of the hundreds of individuals and institutions collaborating for the conservation of the giant panda. References

• Li, B. V. and Pimm, S. L. 2015. Conserving Pandas China’s endemic vertebrates sheltering under the protective The giant panda serves as an um- Can giant pandas be conserved in umbrella of the giant panda. Con‑ brella species for the conservation of long‑term, viable populations both servation Biology. DOI: 10. 1111/ © Kathy Traylor‑Holzer China’s biodiversity. China’s remain- in situ and ex situ? Should they be cobi. 12618. One of the 96 pandas at the Chengdu Research ing endemic species are concentrated conserved? We think so. Long‑term • Nicholls, H. 2011. The Way of the Base of Giant Panda Breeding, one of the primarily in mountainous areas less success appears achievable, and Panda. Pegasus Books: New York. The Future primary breeding centers for the species. impacted by human activities, much the benefits likely extend beyond • Shaprio, J. 2001. Mao’s War of which coincides with wild giant this species – to increased capacity, Against Nature. Cambridge Uni- have also occurred in the ecological The last 20 years have seen the devel- Wild pandas may face new challenges panda range. Over 96% of panda increased habitat and biodiversity versity Press: Cambridge. understanding and management opment of a strong, demographically as habitat and land use patterns habitat overlaps with centers for en- protection, and increased inter‑agen- • Soule, M., Gilpin, M., Conway, W. of wild giant panda populations. and genetically healthy giant panda change with climate change. Other demic mammal, bird and amphibian cy and international collaborations and Foose, T. 1986. The millen- Wei et al. 2015 detail conservation ex situ population and significant threats such as emerging diseases species in need of protection (Li and with the goal of conservation. Could nium ark: how long a voyage, efforts by the Chinese government protection of wild panda habitat may come into play. Fragmentation Pimm 2015). Protection of any panda resources be better invested across how many staterooms, how that have halted population decline and populations. Some challenges and genetic isolation may become habitat therefore benefits many other a wider range of species? Probably. many passengers? Zoo Biology and outline ecological research that remain, however, and new ones are the biggest threat, increasing the endemic species. But the reality is that, at least for now, 5(2): 101–113. inform effective management actions, emerging. For ex situ populations, conservation value of population giant pandas are a high profile and • Traylor‑Holzer, K. and Ballou, J. D. including the creation of 67 protected more improvements are needed to reinforcement through transloca- Likewise, the giant panda ex situ pro- attractive species that resonates with 2016. 2016 Breeding and Manage‑ areas based on habitat models. This increase natural mating behavior tion and the need for management gram is serving as a ground‑breaking people across the globe, and conser- ment Recommendations and Sum‑ represents ~12% increase in giant and parental rearing opportunities. at the meta‑population level. With a model for the scientific genetic vation efforts seem to be working. mary of the Status of the Giant panda geographic range since 2003 Timely paternity testing in cases of third of the wild population living in management of ex situ populations in Panda Ex situ Population. IUCN (WWF 2015). multiple possible sires will be impor- non‑protected areas, the expansion China. Our work with the giant panda Our role has been a small one in this Conservation Breeding Specialist tant to maximize effective genetic of protected areas would be benefi- program has led to a series of capac- journey, and it has been our pleasure Group: Apple Valley, MN. These simultaneous achievements management. The development of a cial. The large body of knowledge and ity building efforts for CAZG in collec- to watch the progress unfold around • Wei, F., Swaisgood, R., Hu, Y., Nie, have laid the foundation for the next formal genome resource bank (GRB) research on the wild population pro- tion planning, studbook development, us. We thank the hundreds of incred- Y., Li, Y., Zhang, Z., Qi, D. and Zhu, phase – the evolution of the ex situ strategy for the systematic collection, vides real opportunities for adaptive advanced population management ibly knowledgeable and dedicated in- L. 2015. Progress in the ecology population as a source population storage and use of sperm (and other management to address issues such and masterplanning, and to a dividuals, and especially our Chinese and conservation of giant pan- for release to reinforce existing wild biosamples) with respect to clearly as habitat quality, fragmentation, dedication by CAZG to expand sound colleagues, for allowing us to join in das. Conservation Biology 29(6): panda population and/or establish defined goals is recommended to and climate change (Wei et al. 2015). population management to more on the adventure, and cheer them on 1497–1507. new ones through reintroduction. provide additional management op- These efforts can paint a brighter species within Chinese zoos. Panda to even greater future success. • Wildt, D. E., Zhang, A., Zhang, H., A few trial releases have taken place tions and security. And of course, new future for wild giant pandas – but the breeding centers are considering Janssen, D. L., and Ellis, S. (eds.). since 2012 to investigate release opportunities await on the horizon for benefits do not stop there. expanding their population manage- 2006. Giant Pandas: Biology, training strategy. Now each year a the development of effective reintro- ment strategies from giant pandas to Veterinary Medicine and Man‑ few females are purposefully bred duction and reinforcement to support their red panda populations. The suc- agement. Cambridge University to produce offspring surplus to the wild populations. cess of this biologically and politically Press: New York. needs of the ex situ population and complex species program provides • Xie, Z. 2015. International Giant are reared and trained for release. the tools and instills the confidence Panda Studbook. Chinese As- This fledgling program is expected to to consider intensive management sociation of Zoological Gardens: expand and provide direct support to for other species. Beijing. the wild population.