FRANK RIETKERK 1 &JEFFREY J. M. PEREBOOM 2,3

EDITORIAL: CONSERVATION OF GREAT APES 9 Int. Zoo Yb. (2018) 52: 9 15 DOI:10.1111/izy.12202 Editorial: Conservation of Great Apes Zoo contributions towards improving management and well-being of great apes: augmenting knowledge to safeguard our closest relatives FRANK RIETKERK 1 &JEFFREY J. M. PEREBOOM 2,3 1 Zoological Director, Stichting Apenheul, J.C. Wilslaan 21, 7313 HK Apeldoorn, The Netherlands, 2 Research Manager, Antwerp Zoo Centre for Research and Conservation, Royal Zoological Society of Antwerp, Koningin Astridplein 26, 2018 Antwerpen, Belgium, and 3 Evolutionary Ecology Group, University of Antwerp, Universiteitsplein 1, 2610 Antwerpen, Belgium E-mail: f.rietkerk@apenheul.nl, zjef.pereboom@kmda.org This volume of the International Zoo Yearbook aims to address the plight of some of the most charismatic and iconic animals we know the non-human great apes by highlighting the contributions that zoological institutions and their like-minded collaborators and partners have made to great ape husbandry, health and welfare, scientific research and conservation. As the current extinction crisis is faced, many species are threatened with extinction and great ape species are no exception. Each species of great ape, comprising Chimpanzees Pan troglodytes spp, Bonobos Pan paniscus, gorillas Gorilla spp and orangutans Pongo spp, are under threat from hunting for subsistence and trade, disease, and deforestation and habitat loss, and almost all are classed as either Endangered or Critically Endangered in the International Union for Conservation of Nature (IUCN) Red List (IUCN, 2017). The world s zoos, together with many stakeholders involved in great ape conservation, make valuable contributions towards limiting the negative consequences of those threats, including improving scientific understanding of this fascinating group of animals; refining ex situ breeding programmes; generating public awareness regarding the issues these species face and the urgency with which action must be taken; and supporting and undertaking direct conservation actions in the field. With this great ape special issue, the aim is to showcase the work carried out by zoological institutions, sanctuaries and their conservation partners towards improving the management, well-being and protection of great ape species both in captivity and in the wild. The selection of contributions to this volume highlights the latest achievements in great ape research, health and nutrition, animal management, in situ conservation and ex situ breeding programmes, and provides examples of how zoos can contribute to addressing the challenges and difficulties experienced when dealing with husbandry and population management linked to captive breeding, and in ensuring the protection of wild great apes and their habitats. By focusing attention on great ape conservation and the important role played by zoological institutions, the hope is that this volume will inspire additional zoos to take

10 EDITORIAL: CONSERVATION OF GREAT APES Plate 1. Bonobo Pan paniscus at Stichting Apenheul, The Netherlands. Ronald van der Beek, Stichting Apenheul. action, and help to inform future conservation initiatives and, ultimately, improve the survival of the great apes and protection of their habitats. (Plate 1.) This special issue should of course start with an historical overview and update on the latest ideas about the taxonomy of the non-human great apes. Who other than the late Colin Groves, controversial as his ideas sometimes might be, could provide such an up-to-date description of current understanding of great ape taxonomy (Groves, 2018)? Taxonomy is of course of considerable relevance to conservation, either for population-management purposes in zoo breeding programmes, for protecting great apes in their natural habitats or for reintroduction planning. For example, in orangutans Pongo spp the discussion on reconsidering subspecies and/or geographic variation may greatly influence the decision-making process when releasing rescued individuals of different origins within Borneo (Banes et al., 2016, 2018; Groves, 2018). In addition, as Groves correctly argues in his article, enhanced understanding about the taxonomy of great apes also has great importance to ex situ populations, and may help augment the welfare of great apes in zoos and as such improve survival and reproductive prospects, and the outcomes of conservation efforts. The paper by Marques-Bonet & Hvilsom (2018) on genomic variation in the great apes delves a bit deeper into the use of novel technologies, exploiting whole genome sequences to study taxonomy and evolutionary relationships, and how this can contribute to conservation planning for great apes. In particular for breeding programmes the latest developments in genomics may result in a fundamental shift in how zoo populations are managed in the future. Genome studies make it possible to identify the origin of individuals, particularly founders, which is especially important when setting up the parameters to manage (sub)populations, as well as allowing a better comparison of wild great ape populations with managed zoo populations. Such information will inform breeding-programme coordinators about genetic diversity, population structure, detailed assessments of relatedness or inbreeding, and whether the population goals can be achieved. At the time of writing, genomic tools are frequently used to add such a genetic overlay to the management of the ex situ programmes for chimpanzees Pan spp in European zoos, Bonobos in the EAZA Ex situ Programme (EEP) and Species Survival Plan (SSP) populations, and the Western lowland gorilla Gorilla gorilla gorilla (Marques- Bonet & Hvilsom, 2018) within the European Association of Zoos and Aquaria (EAZA) and the Association of Zoos and Aquariums (AZA), but similar efforts are being developed in other regions, and for orangutans Pongo spp and other species. For example, the Latin American Zoo & Aquarium Association (ALPZA) and the South East Asian Zoo Association (SEAZA) are

EDITORIAL: CONSERVATION OF GREAT APES 11 working towards establishing ex situ management programmes for several of the great ape species. In their paper on changing perceptions of keeping apes in Asian zoos, Banes and colleagues highlight the benefits of using genetics for species determination and for the development of population management based on genomic data as part of the SEAZA Species Management Programme (SSMP) for Bornean orangutans Pongo pygmaeus (Banes et al., 2018). The authors report convincingly that Asian zoos have made significant advances in orangutan care and population management; for example, orangutans serve as model species for the recently developed Regional Species Management Programme (RSMP) for primates, and future regional management programmes will likely be modelled according to the orangutan example. Although the advances in using genetics and genomics in population management and species conservation herald a new and exciting era, the bulk of coordinated breeding programmes still use studbook-based population management. The paper by Moreno Rivas et al. (2018) offers an excellent example of how studbook data from the EEP and SSP for Western lowland gorillas are used for demographic and genetic analyses to inform transfer and breeding recommendations, with the ultimate goal of safeguarding the longterm sustainability of genetically and demographically healthy zoo populations. Record keeping for individual wild animals managed by zoos and aquariums is an essential component of population management, not only at the institutional level but also to ensure long-term health and viability of species populations regionally and globally. Fisken et al. (2018) present a series of international and regional short reports for the great apes, including population-records updates (as at 31 December 2016). IMPROVING THE WELL-BEING AND HEALTH OF GREAT APES IN ZOOS The welfare and health of great apes in zoo environments are of considerable concern, and are subject to much debate and study. First and foremost, providing the right conditions is required to ensure optimal wellbeing. This includes enclosure design, accommodating behavioural needs, stimulating species-specific natural behaviours, providing adequate nutrition and ensuring the physical and psychological health of the animals. A critical requirement for effectively housing great apes is providing the right species-specific social environment. Studying the details of social interactions during group formation in zoos contributes to increasing the understanding of group dynamics, and ultimately enhances individual quality of life. Huskisson & Chism (2018) report on the development of social relationships during the establishment of a new group of Western lowland gorillas at Riverbanks Zoo, Columbia, SC, USA. In this case study, the group exhibited speciestypical interactions and appeared to be adjusting well to their new physical and social environments. Case studies such as these are fundamental for enhancing current understanding of the social repertoire of gorillas and contributing to available knowledge regarding the development of social relationships in a zoo during an introductory period. Cabana et al. (2018) address the issue of nutrition, as all great ape species in captivity are affected by a variety of abnormal behaviours and health conditions that are influenced by inadequate diets. Generally, the nutrient content of food items consumed by great apes in the wild is very unlike the food items typically fed in captivity, such as commercially bred fruits that have been selected for increased palatability and sweetness. This study by Cabana and colleagues aims to assess the effects of reducing carbohydrate content and increasing fibre concentrations of great ape diets, and to evaluate the behavioural and physiological responses of these species to the dietary changes. Based on their study, the authors conclude that excluding commercial fruits from great ape diets has many health and behavioural benefits, which may lead to

12 EDITORIAL: CONSERVATION OF GREAT APES decreased medical interventions and better well-being for great apes in zoos. Although diet also has an effect upon the occurrence of regurgitation and reingestion, a commonly observed abnormal behaviour pattern in great apes, there are other factors (e.g. temporal, seasonal, social, medical, individual personality) that should also be considered. Hill (2018) provides an excellent review of what is known about this behaviour at the time of writing, touching not only upon nutritional factors but also on behavioural and social elements. A major health concern for all zoohoused great apes is cardiovascular disease, which is associated with significant mortality and morbidity, particularly in Chimpanzees, Bonobos and Western lowland gorillas. This volume of the International Zoo Yearbook features three excellent papers on the topic, and all three stress the lack of contemporary understanding about epidemiology, pathogenesis, diagnosis, treatment and prevention of heart disease in great apes. The first paper (Strong, Martin, et al., 2018) describes a retrospective study on the frequency and patterns of cardiovascular disease-associated mortality in zoohoused great apes, and highlights several potential risk factors involved in great ape cardiovascular disease epidemiology and pathogenesis. The paper by Murphy et al. (2018) describes the Great Ape Heart Project (GAHP), which focuses on the detection and treatment of cardiovascular disease in great apes housed in zoos in the United States. A primary goal of the GAHP is to implement regular and advanced cardiac-health monitoring and evaluation of post-mortem protocols, to provide support to zoo staff by giving them access to a network of experts conversant with the best possible veterinary care, and to develop a robust cardiac-health database to increase the understanding and treatment of cardiac disease in all the great ape species. To this end the GAHP works with standardized protocols for consistent cardiac post-mortem examination, data collection and research in AZA-member zoos. In Europe, however, such standardization with regard to data collection, comprehensive clinical and pathological databases, and coordinated research activities does not appear to exist (Strong, Sheppard, et al., 2018). In this third paper, the authors stress the critical need for improvements in the consistency and quality of cardiovascular post-mortem examination sampling and reporting of the great ape heart across European zoological collections, to enhance the understanding about cardiovascular disease in these species. UNDERSTANDING SPECIES BIOLOGY Zoos can provide excellent opportunities for basic research into species biology, such as behaviour, life history, evolutionary processes, morphology, physiology and many other scientific fields of interest that are difficult to study in the wild. Two papers, one by Behringer et al. (2018) and the other by Gartner & Weiss (2018), highlight several benefits of using zoo animals for scientific research into physiology, behaviour and development, and demonstrate that research carried out within zoos contributes substantially to the advancement of fundamental scientific knowledge and literature. Moreover, the outcomes of basic research in zoos can have great added value in applied settings; for example, for the management, welfare and conservation of great apes. Using their investigations into the growth, physiology and endocrinology of Bonobos and Chimpanzees in zoos, Behringer et al. (2018) show that apart from generating an increased understanding of basic physiological processes in great apes, these studies contribute to the development, validation and fine-tuning of novel techniques for monitoring health and well-being in zoo-based Chimpanzees and Bonobos, as well as other primates, and provide new scientific tools for data collection and analyses. Similarly, Gartner & Weiss (2018) explain how well-planned and relevant

EDITORIAL: CONSERVATION OF GREAT APES 13 studies into great ape personality, behaviour and cognition carried out in zoos not only add to the scientific literature but also provide a solid foundation for animal-management protocols, and contribute to the physical and psychological well-being of animals in human care. Most importantly, the authors of both papers argue that studies of great apes, such as those presented here, and other species more generally, can provide a benchmark for improved understanding and protection of their wild conspecifics. CONSERVATION OF GREAT APES Next to implementing and supporting fundamental and applied research projects in their collections and the science-based management of coordinated breeding programmes, the world s zoos and their conservation partners make valuable contributions towards protecting great apes in their natural habitats; for example, by supporting and undertaking direct conservation actions in the field. Breuer et al. (2018) provide several examples of strategic collaborations between zoos and the Mbeli Bai Study (MBS) field-conservation project, in their paper on the conservation of Western lowland gorillas in the Republic of Congo, highlighting the various ways zoos and field-conservation projects can and do collaborate. In particular the authors focus on showcasing examples of how such partnerships can be a win-win for both parties. Zoos generally provide financial and logistical support, and focus on conservation education and raising public awareness. Zoos can also play an important role in the training of field-conservation staff, through capacity building and providing transferable skills. Field projects can inform and assist the work carried out in zoos by undertaking scientific research for field conservation and to inform captive management. Along a similar line, Ancrenaz et al. (2018) discuss the importance of zoos contributing to species conservation through species-management and conservationbreeding skills, capacity building, technical expertise, and advocacy and outreach activities to the wider public. In this paper on the conservation of wild orangutans Pongo spp, the authors correctly argue that rehabilitation and reintroduction of orangutans is insufficient and can even be counterproductive for the long-term survival of wild orangutan populations and their habitats. Longterm preservation of most orangutan populations will only be possible by improving the management of non-protected forests and by minimizing losses among remaining orangutan populations; for example, by taking a landscape level approach aimed at protecting and reconnecting patches of forest rather than trying to retain and protect isolated areas. Ancrenaz and colleagues argue that zoos have a responsibility and are well placed to take a leading role in such conservation initiatives. Zoos can and should become one of the key players involved in influencing people s attitude towards species conservation and sustainable development, and contribute to new approaches that have a positive impact on the survival of wild orangutan populations. Many of the world s zoos already play a crucial role in the long-term protection of wild great apes; for example, by addressing and mitigating the massive, widespread and accelerating threat from hunting and illegal trade. An excellent example of such an initiative is provided in the paper by Tagg et al. (2018). This study, led by a consortium of zoos and conservation non-governmental organizations (NGOs), offers highly relevant and detailed information on the main actors involved in the trafficking of chimpanzee and gorilla bushmeat around the Dja Biosphere Reserve in Cameroon, including aspects of their motivations, financial gains and profit, and the main routes involved in the commodity chain associated with the trade. The findings of this study resulted in the formulation of a number of practical recommendations to wildlife authorities and local governments aimed at improving law enforcement, the

14 EDITORIAL: CONSERVATION OF GREAT APES development of social programmes to provide alternative sources of income for hunters and traders, and more effective monitoring and research specifically to identify and understand the drivers of the consumption of great ape meat by urban consumers. Of course zoos, conservation NGOs, and academic and research institutions are not the only players involved in conservation research and the protection of great apes. A significant conservation role is played by the numerous primate rescue and rehabilitation centres providing sanctuary to primates, and focusing on primate welfare and conservation. The paper by Stokes et al. (2018) highlights the crucial role members of the Pan African Sanctuary Alliance (PASA) play in providing a safe haven for primates in Africa, supplying medical treatment and long-term care, and facilitating integration into social groups in large forest enclosures, and how PASA strengthens its member sanctuaries. PASA not only is the unified voice of the 23 primate sanctuaries in Africa but also improves animal welfare, ensures high standards of care, and contributes to primate-care training and capacity building of sanctuary staff. The primates within these sanctuaries have been either confiscated from the illegal wildlife trade or orphaned by bushmeat hunters, and many of these individuals were rescued in collaboration with law-enforcement agencies. In addition to playing an essential role in primate welfare and conservation, almost all PASA sanctuaries are involved in research activities, law-enforcement programmes, conservation education and awareness campaigns, and community-based projects, in similar ways and very often in close collaboration with the world s zoos. However, without structural support and assistance from zoos much of PASA s work would not be possible, and PASA and its members are passionate about continuing their long-standing collaborations with zoos worldwide and developing new partnerships, ultimately aiming to improve further great ape welfare and conservation. WE CAN MAKE A DIFFERENCE In this volume of the International Zoo Yearbook, the Editors have tried to bring together a selection of articles that focuses on the different actions zoological institutions and their conservation and academic partners have taken to contribute to the husbandry, health and welfare, scientific research and conservation of great apes. Primates, and in particular the non-human great apes, are our closest relatives. These species have always attracted a lot of scientific interest for many different reasons, resulting in a large and extensive body of scientific literature covering all aspects of great ape biology, in particular on their behaviour, ecology, evolution and physiology. Furthermore, there is an even larger amount of specialized literature focusing on the applied knowledge we have acquired about great apes through scientific and non-scientific research and/or studies. Nevertheless, this huge body of knowledge has not been enough to prevent each species of great ape from coming under severe threat from extinction. There is always much more to know, much more to understand and much more to do in order to prevent this wonderful group of primates from vanishing off the face of the earth. The world s zoos can and should take an active role in saving the great apes and other species, by generating additional knowledge, raising more awareness, promoting better welfare, further improving husbandry, and generating extra funds that will help the many advocates and supporters of great ape conservation to step up their game, and really make a difference. REFERENCES ANCRENAZ, M., BARTON, C., RIGER, P. & WICH, S. (2018): Building relationships: how zoos and other partners can contribute to the conservation of wild orangutans Pongo spp. International Zoo Yearbook 52: 164 172. BANES, G. L., GALDIKAS, B. M. F. & VIGILANT, L. (2016): Reintroduction of confiscated and displaced mammals risks outbreeding and introgression in natural populations, as evidenced by orang-utans of divergent subspecies. Scientific Reports 6: Art. 22026.

EDITORIAL: CONSERVATION OF GREAT APES 15 BANES, G. L., CHUA, W., ELDER, M.& KAO, J. (2018): Orang-utans Pongo spp in Asian zoos: current status, challenges and progress towards long-term population sustainability. International Zoo Yearbook 52: 150 163. BEHRINGER, V., STEVENS, J. M. G., DESCHNER, T. & HOHMANN, G. (2018): Getting closer: contributions of zoo studies to research on the physiology and development of bonobos Pan paniscus, chimpanzees Pan troglodytes and other primates. International Zoo Yearbook 52: 34 47. BREUER, T., MANGUETTE, M. & GROENENBERG, M. (2018): Gorilla Gorilla spp conservation from zoos to the field and back: examples from the Mbeli Bai Study. International Zoo Yearbook 52: 137 149. CABANA, F., JASMI, R. & MAGUIRE, R. (2018): Great ape nutrition: low-sugar and high-fibre diets can lead to increased natural behaviours, decreased regurgitation and reingestion, and reversal of prediabetes. International Zoo Yearbook 52: 48 61. FISKEN, F. A., CARLSEN, F., ELDER, M., DE JONGH, T., PEREBOOM, J. J. M., POHL, B., RIETKERK, F., ROSS, S. & TANIGUCHI, A. (2018): Global population records and managed-programme updates for the great apes: short report. International Zoo Yearbook 52: 212 226. GARTNER, M. C.& WEISS, A. (2018): Studying primate personality in zoos: implications for the management, welfare and conservation of great apes. International Zoo Yearbook 52: 79 91. GROVES, C. P. (2018): The latest thinking about the taxonomy of great apes. International Zoo Yearbook 52: 16 24. HILL, S. P. (2018): Regurgitation and reingestion (R/ R) in great apes: a review of current knowledge. International Zoo Yearbook 52: 62 78. HUSKISSON, S. M. & CHISM, J. L. (2018): Emerging relationships in a new group of western lowland gorillas Gorilla gorilla gorilla at Riverbanks Zoo & Garden, Columbia, SC. International Zoo Yearbook 52: 92 102. IUCN (2017): The IUCN Red List of Threatened Species. Gland, Switzerland, and Cambridge, UK: International Union for Conservation of Nature. Available at http://www.iucnredlist.org MARQUES-BONET, T. & HVILSOM, C. (2018): Genomic variation of the great apes and the application to conservation. International Zoo Yearbook 52: 25 33. MORENO RIVAS, M., RODRIGUEZ TEIJEIRO, J. D. & ABELLO, Mª. T. (2018): Genetic and demographic analysis of European Endangered Species Programme (EEP) and Species Survival Plan (SSP) western lowland gorilla Gorilla gorilla gorilla populations. International Zoo Yearbook 52: 194 211. MURPHY, H. W., DANFORTH, M. D. & CLYDE, V. L. (2018): The Great Ape Heart Project. International Zoo Yearbook 52: 103 112. STOKES, R., TULLY, G. & ROSATI, A. G. (2018): Pan African Sanctuary Alliance: securing a future for the African great apes. International Zoo Yearbook 52: 173 181. STRONG, V. J., MARTIN, M., REDROBE, S., WHITE, K.& BAIKER, K. (2018): A retrospective review of great ape cardiovascular disease epidemiology and pathology. International Zoo Yearbook 52: 113 125. STRONG, V. J., SHEPPARD, M. N., REDROBE, S.& BAI- KER, K. (2018): Guidelines for consistent cardiovascular post-mortem examination, sampling and reporting of lesions in European zoo-housed great apes. International Zoo Yearbook 52: 126 136. TAGG, N., MADDISON, N., DUPAIN, J., MCGILCHRIST, L., MOUAMFON, M., MCCABE, G., NGO BADJECK, M. M., TCHOUANKEP, M., MBOHLI, D., EPANDA, M. A., RANSOM, C. & FA, J. E. (2018): A zoo-led study of the great ape bushmeat commodity chain in Cameroon. International Zoo Yearbook 52: 182 193.