A review of research in primate sanctuaries

Abstract

While non-human primate studies have long been conducted in laboratories, and more recently at zoological parks, sanctuaries are increasingly considered a viable setting for research. Accredited sanctuaries in non-range countries house thousands of primates formerly used as subjects of medical research, trained performers or personal pets. In range countries, however, sanctuaries typically house orphaned primates confiscated from illegal poaching and the bushmeat and pet trafficking trades. Although the primary mission of these sanctuaries is to rescue and rehabilitate residents, many of these organizations are increasingly willing to participate in non-invasive research. Notably, from a scientific standpoint, most sanctuaries provide potential advantages over traditional settings, such as large, naturalistic physical and social environments which may result in more relevant models of primates' free-ranging wild counterparts than other captive settings. As a result, an impressive scope of research in the fields of primate behaviour, cognition, veterinary science, genetics and physiology have been studied in sanctuaries. In this review, we examine the range and form of research that has been conducted at accredited sanctuaries around the world. We also describe the potential challenges of sanctuary-based work and the considerations that external researchers may face when deciding to collaborate with primate sanctuaries on their research projects.

1. Introduction

For most of the past century, the vast majority of captive non-human primate (hereafter simply ‘primate’) research was concentrated in laboratory settings where academic and human health advancement was effectively the core impetus for housing those species in captivity. In 2010, United States research facilities were home to over 70 000 primates used in biomedical research [1], while even more were subjects of behavioural and cognitive studies in universities and other academic centres. But, increasingly over the past 40 years, the sites of captive primate research have begun to diversify. For instance, research in zoo settings continues to rise, and primates are often the most-studied taxa among the many species housed in these settings [2,3]. Hopper [4] provided a review of zoo-based cognitive research, finding the same high prevalence of primate-focused studies. In these settings, research typically falls alongside other institutional mission-based priorities such as education, leisure and conservation. As a result, researchers are just one group of stakeholders among many in zoos.

While primates have been housed in laboratories and zoos for over a century in many parts of the world, a more recent housing category is sanctuaries, where primates are rehomed from situations where they are orphaned or unable to survive on their own, no longer needed, wanted, or from which they require protection. In general, these organizations have categorically prioritized the care and wellbeing of resident primates above other potential interests, including research. Indeed, over a decade ago, Brent [5] stated ‘the scientific study of non-human primates in sanctuaries in the United States is virtually non-existent,' but nonetheless had the foresight to advocate for the growth in this area that has transpired recently. Brent [5] recognized the potential value that non-invasive studies could bring in terms of improving the care and management of sanctuary-housed primates, and advocated for collaborations between researchers and sanctuary staff. Today, many primate sanctuaries around the world are increasingly participating in non-invasive research [6], which contributes to new understanding about these animals, while preserving their commitment to the wellbeing of these residents.

In this review paper, we will examine the range of peer-reviewed research that has been conducted in primate sanctuary settings or with biosamples taken from sanctuary-housed primates. As with any review, we begin by deliberately drawing the boundaries of the scope of our search, which begins with consideration of what constitutes a sanctuary. Like the word zoo, the term sanctuary likely evokes a particular reaction from people; however, in practice, these organizations can vary broadly in mission, resources, sustainability and effectiveness. Here, we restrict our review, with only a few exceptions, to publications from captive research conducted in accredited sanctuary organizations: those that have met some particular set of guidelines for administrative functioning and are part of a community of like-minded organizations. There are several accrediting bodies for sanctuaries worldwide, including the Pan African Sanctuary Alliance (PASA) for African primate sanctuaries and the Global Federation of Animal Sanctuaries (GFAS) which accredits sanctuaries for a range of taxa around the world. In rarer circumstances, some sanctuaries are accredited by bodies typically associated with zoos, such as the Association of Zoos and Aquariums (AZA) in North America. The primary exceptions we made to the accreditation restriction are for organizations that broadly meet the criteria of sanctuaries, including a lack of breeding and a focus on rehoming primates in need (for example, Kumamoto Sanctuary in Japan and Fundación Mona in Spain).

The result of our selection criteria means that a comparatively small number of publications from reputable sanctuary organizations are not reported in this review. We chose not to include organizations such as Duke Lemur Center in this review as its primary mission is focused much more so on research than providing sanctuary for primates in need of rehoming. Similarly, we excluded sanctuaries at which most primates were only temporarily housed prior to being reintroduced back to the wild. For instance, the Orangutan Care Center and Quarantine (OCCQ) is excluded from this review for those reasons, despite past involvement in a variety of research initiatives. While these selection criteria exclude a small proportion of sanctuaries engaged in captive primate research, they do provide both a means by which to consistently frame the scope of research we review and ensure a high level of care is provided to the resident primates under study. Those organizations that do meet our criteria tend to be largely skewed towards research with great apes, in particular chimpanzees (Pan troglodytes), which to some degree also reflects the species distribution of sanctuary residents themselves. Specific interest in Pan spp. is not unlike that seen in other research settings and may be perpetuated by the fact that a robust set of scientific background information is readily available to support future studies [3].

The vast majority of captive primate research publications coming from sanctuary-based work are either from western-based scientists working in African sanctuaries or from a small handful of sanctuaries with heavy investment in behavioural sciences (e.g. Kumamoto Sanctuary and Fundación Mona). This uneven distribution could be influenced by the predetermined scope of our literature search (focusing only on captive research from sanctuaries that have attained accreditation status) or from our methodology (it is possible that there are non-English language reports that were not counted). A more parsimonious explanation is that our findings reflect the skewed distribution of current research interests and capacity in the sanctuary world. As most sanctuaries around the world are focused almost entirely on maintaining the rescue and rehabilitation operations of their organization, any potential investment in research activities may be seen as competing with those aims. While we describe several advantages to sanctuary research, we also acknowledge the historical, cultural and logistical barriers to these organizations reaching their research potential.

(a). Consideration of sanctuary-based research

Accredited primate sanctuaries exist around the world (figure 1), though there are important regional differences in terms of the organizational missions and how research is conducted therein. Range country primate sanctuaries in Africa, Asia and South and Central America are often in place to receive formerly wild primates displaced by illegal human activities, such as poaching, the bushmeat trade, pet trade trafficking, and via confiscation by a third party. Conversely, non-range country sanctuaries, located in North America and Europe, primarily receive primates who are voluntarily provided or legally facilitated from laboratories, owned as personal pets, or used in entertainment. For the purposes of this review, we, therefore, consider Kumamoto Sanctuary in Japan (a primate range country) as categorized with non-range country organizations because of the nature of their population.

Figure 1.

Locations and primary accreditors of the sanctuaries where research described in this review took place. AZA, Association of Zoos and Aquariums; GFAS, Global Federation of Animal Sanctuaries; PASA, Pan African Sanctuary Alliance.

(b). Housing and types of research

As we have described, the degree to which research opportunities compete alongside other aspects of an organization's mission varies both between and within housing categories. While animal care is an important aspect of research centres, the fundamental purpose of the primates living there is to participate in scientific studies. Accordingly, in laboratories, we see a greater range of studies that include not only non-invasive behavioural investigations but also invasive biomedical studies (those that may include non-care-related insertions, injections or incisions) that use primates as models for human health conditions. Indeed, in a review of primate research published in 2001, Carlsson et al. [7] found that the most common areas of research were those in which primates were used as models for human conditions, as well as neuroscience and biochemistry research, concluding that 14% of primate studies could be classified as non-invasive. Research based at zoological parks also varies considerably, though it is very rarely considered invasive in nature and generally focuses on determining positive applications for animals rather than humans. Stoinski et al. [2] surveyed AZA-accredited zoos and reported that the most commonly studied topics included reproduction, behaviour, physiology, conservation, husbandry, cognition, pathology, genetics and animal nutrition.

Primate sanctuaries are typically the most restrictive in terms of allowable research. For instance, the Global Federation of Animal Sanctuaries' Operations Standards [8] only allows research that does not negatively impact animal welfare, interfere with normal daily activities, or cause pain or distress (terms that are left undefined in this context). However, they also point out that exceptions may be made with the approval of an appropriate decision-making body if it is determined that the health and welfare interests of the animal(s) are best served by participating in the study, or if there will be a tangible benefit for the individual animal(s) involved. They also allow samples to be collected during routine examinations, enclosure cleaning and post-mortem. Some sanctuaries may insist that samples collected from their residents are neither used solely for human medical benefit nor to infect animals housed elsewhere. As such, while many sanctuaries will likely have a narrower scope of allowable research compared to zoos and laboratories, opportunities to conduct research at sanctuaries do indeed exist.

(c). Sanctuary research capacity

In addition to the type of research being conducted at the sanctuary, there are other considerations in play when considering sanctuary-based research. The first is the research capacity of the organization. With a few exceptions, most primate sanctuaries do not have full-time research staff and the burden of conducting research is, therefore, often carried by external researchers or non-research sanctuary staff or volunteers. In either case, this presents logistical challenges ranging from the time and effort involved in hosting external personnel on site, to the degree to which research activities reduce staff capacity for other core functions. Moreover, studies of complex cognitive abilities or involving the collection of certain biosamples may require greater expertise than some sanctuaries are able to provide, often resulting in a greater focus on observational behavioural research. Secondly, the degree to which animals are accessible for research may differ from more traditional settings. Enclosures at sanctuaries often tend to be larger than in laboratories (e.g. [9]) and, compared to many zoo exhibits, are not necessarily designed to facilitate behavioural observations. Some sanctuaries have attempted to overcome these challenges by installing elevated observation decks or a system of remote cameras. Hansen et al. [10] conducted an evaluation of such a camera system in a chimpanzee sanctuary and found that, although cameras provided narrower perspectives on animal subjects, the observer was able to view large enclosures at a much faster rate compared to in-person observations. Much larger multi-acre enclosures, such as those found in range-country sanctuaries, may, therefore, be even more difficult settings to conduct behavioural observations.

(d). Sanctuary populations

As discussed earlier, the nature of sanctuary populations may differ depending on the region in which the sanctuary is located (table 1). Broadly speaking, many range-country sanctuaries have a positive population flow in which the influx of primates (rescued from circumstances related to illegal poaching, pet trafficking and the bushmeat trade) is generally greater than the outflux, with recently placed younger individuals often outnumbering older residents. Such circumstances may create opportunities for developmental and longitudinal research, though many of the residents may have atypical early histories involving little parent-rearing or traumatic experiences. On the other hand, with most non-range sanctuaries, there is a population bias towards older individuals. Here, sanctuaries function primarily as end-of-life facilities in which there is no breeding and mortality rates reflect an aged population. As a result, research on ageing or studies leveraging post-mortem biosampling may be well suited to these facilities should they meet the research criteria of the organization. Furthermore, the source of incoming primates in non-range sanctuaries may be more varied, as individuals may arrive with histories as laboratory research subjects, personal pets, or commercial entertainers. While some research may focus specifically on the effects of these past experiences [11–13], the atypical social histories of many of these individuals may be an important consideration. While some studies report long-term impacts of atypical and traumatic early histories on sanctuary-housed chimpanzees [11,12,14,15], other findings suggest that (range-country) sanctuary apes are as mentally healthy as apes in other settings (e.g. zoos) and can be seen as a valuable resource for non-invasive research [16]. In range country sanctuaries, such developmental improvements are likely related to the young age of arrival as well as the institutional rehabilitation and care programmes in place for these individuals.

Table 1.

Primate species housed at each of the sanctuaries where research described in this review took place.

sanctuary	primate species housed
1. Chimpanzee Sanctuary Northwest	Pan troglodytes
2. Born Free USA Primate Sanctuary	Chlorocebus pygerthyrus; Macaca spp.; Papio spp.
3. Cleveland Amory Black Beauty Ranch	Cebus spp.; Hylobates spp.; Macaca spp.
4. Chimp Haven	Pan troglodytes
5. Ape Initiative	Pan paniscus
6. Jungle Friends Primate Sanctuary	Ateles spp.; Callithrix spp.; Cebus spp.; Saguinus spp.; Saimiri spp.
7. Center For Great Apes	Pan troglodytes; Pongo pygmaeus
8. Save the Chimps	Pan troglodytes
9. Fauna Foundation	Macaca mulatta; Pan troglodytes
10. Las Pumas Rescue Center	Ateles geoffroyi; Cebus capucinus
11. Fundación Mona	Macaca mulatta; Pan troglodytes
12. Tacugama Chimpanzee Sanctuary	Pan troglodytes
13. Chimpanzee Rehabilitation Project	Pan troglodytes
14. Chimpanzee Conservation Center	Pan troglodytes
15. Limbe Wildlife Centre	Cercocebus spp.; Cercopithecus spp.; Gorilla gorilla gorilla; Mandrillus spp.; Pan troglodytes; Papio anubis
16. Drill Ranch (Pandrillus)	Mandrillus leucophaeus; Pan troglodytes
17. Ape Action Africa	Cercocebus spp.; Cercopithecus spp.; Chlorocebus tantalus; Gorilla gorilla gorilla; Mandrillus sphinx; Pan troglodytes; Papio anubis
18. Sanaga-Yong Chimpanzee Rescue	Pan troglodytes
19. Parc de la Lékédi	Cercocebus spp.; Cercopithecus spp.; Colobus satanas; Erythrocebus patas; Gorilla gorilla gorilla; Lophocebus albigena; Mandrillus sphinx; Miopithecus ogouensis; Pan troglodytes
20. Tchimpounga Chimpanzee Rehabilitation Centre	Pan troglodytes
21. Lola Ya Bonobo	Pan paniscus
22. J.A.C.K. (Jeunes Animaux Confisques au Katanga)	Pan troglodytes
23. Ngamba Island Chimpanzee Sanctuary	Pan troglodytes
24. Sweetwaters Chimpanzee Sanctuary	Pan troglodytes
25. Chimfunshi Wildlife Orphanage	Chlorocebus pygerythrus; Pan troglodytes; Papio cynocephalus
26. Vervet Monkey Foundation	Chlorocebus pygerythrus
27. Kumamoto Sanctuary	Pan paniscus; Pan troglodytes

Note. Listed species are based on published research, sanctuary websites and personal communication. As sanctuary populations are variable, this table should be viewed as a guide rather than a conclusive list.

(e). Sanctuary affiliations

Research in sanctuary settings is not evenly distributed across organizations. Some sanctuaries are heavily invested in conducting research, and this is best illustrated by a trio of sanctuaries housing chimpanzees around the world. Kumamoto Sanctuary is unusual in that it is a chimpanzee sanctuary organization that maintained the facility, care staff and animals of a former biomedical research site. The sanctuary maintains an affiliation with a major university and has staff scientists on site to facilitate a wide range of biological, behavioural and cognitive research with the resident chimpanzees and bonobos (Pan paniscus) [17]. As such, the research productivity of this organization is quite high. In the United States, Chimp Haven was founded by scientists from the laboratory research community and continues to maintain a research department focused primarily on applied behavioural and welfare studies [18]. Here, additional research resources are facilitated though a collaboration with the research-oriented Lincoln Park Zoo in Chicago, IL [19]. In the central African country of Zambia, Chimfunshi Wildlife Orphanage (hereafter Chimfunshi) has conducted research for many years through collaborations with the Max Planck Institute for Evolutionary Anthropology in Germany and a core team of researchers primarily focused on cultural variation between the different chimpanzee communities.

2. Advantages of sanctuary-based research

While there are several factors requiring consideration in sanctuary-based primate research, there are also advantages relative to the more traditional laboratory settings and zoological parks. Investigations that prioritize subjects as models of free-ranging primates will often find the largest and most naturalistic enclosures in sanctuary settings—especially those in range countries [9]. In many of these environments, the primates themselves may well be considered attractive research models as the benefits of a free-ranging, naturalistic lifestyle are combined with some degree of control typical of captive settings. Likewise, large and species-typical social groups are important for the validity of much behavioural research [15], and larger sanctuary enclosures may facilitate such groupings of research subjects.

Additionally, while zoo settings may provide some degree of naturalism for some primates, the potential impact of visitors on behaviour and biology is always a consideration. Unfamiliar humans are a rarity in sanctuary settings, and thus may be more attractive to researchers interested in visitor effects (note [20] for potential impact of visitors in a sanctuary setting). Importantly, sanctuaries stand to benefit from research as well. The influx of expertise and academic support associated with research has the potential to bolster a sanctuary organization through greater visibility to global audiences, which could result in broader public support. Moreover, partnerships with sanctuary organizations in range countries can also help support their conservation initiatives as many organizations are involved in the reintroduction of primates to their natural habitats [21,22].

3. Review of research

To perform this review, we conducted a literature search with Google Scholar, using the name of each accredited sanctuary as search criteria to identify peer-reviewed articles as well as academic theses and dissertations. We also conducted broader searches using combinations of the words ‘sanctuary,’ ‘primate,’ ‘monkey’ and ‘ape,’ and then reviewed the methods section of each of these publications to confirm they included at least one sanctuary-housed primate or biosample (usually hair, saliva, urine or faeces) from a sanctuary-housed primate. Publications meeting these criteria were also classified based on subject matter under one of the following categories: behaviour and welfare, cognition, and, collectively, veterinary, genetic and physiology. Notably, many studies that include sanctuary-housed primates also include wild, zoo- or laboratory-housed subjects. Accordingly, while many of these studies occurred exclusively at sanctuaries or with samples from sanctuary-housed primates, a significant portion were collaborative efforts involving multiple institutions and/or field sites, with sanctuary-housed primates making up a subset of the subjects. Finally, we note our overt decision to avoid detailed descriptions of methodologies and research conclusions in this review to better emphasize the breadth of topics that have been explored with sanctuary-housed primates.

(a). Behaviour and welfare

Among the most obvious categories of research suited to sanctuaries are behavioural studies and those focused on welfare applications. Observational studies, in which resident primates are watched from afar without any disruption to their daily routine, are classically non-invasive in nature and the scientific investment to procure these data is relatively modest. Great ape (particularly chimpanzee) behavioural studies are typically the most prevalent in sanctuary settings, with studies focusing on activity budgets [23–25], grooming [26–29], locomotion [30,31] and space-use [32], sexual behaviour [33,34], social networks [35], play behaviour [36,37], behavioural flexibility [38], social interactions [39–41] and dominance hierarchies [42,43]. Specific behaviours may also be of particular interest in sanctuary settings given their relationship to care and management. At Chimpanzee Sanctuary Northwest in the United States, researchers examined the chimpanzees' acclimation to a novel outdoor environment [44], and although sanctuaries are typically not open to the public, there have nonetheless been several evaluations of the potential influence of visitors [20,45,46]. At both Chimp Haven [47] and Chimpanzee Sanctuary Uto (now Kumamoto Sanctuary) [48], nesting behaviour has been prioritized as a behaviour to be promoted with their resident chimpanzees, and studied intensively as a result.

Research on chimpanzee and bonobo communicative behaviour has also received significant attention, with studies of great ape communication conducted at Kumamoto [49,50], Ape Initiative in the United States [51–53] and Chimfunshi [54]. At Lola Ya Bonobo in the Democratic Republic of Congo (hereafter Lola), studies have focused on bonobos' copulation calls [55–58], gestures [59,60], vocal–gestural combinations in infants [61], sex signals [62], communication signals [63] and contest hoots [64]. Chimpanzee facial expressions have also been studied at both Ngamba Island in Uganda (hereafter Ngamba) [65] and Chimfunshi [66,67]. On the other hand, research on the behaviour of other sanctuary-housed primates, such as drills (Mandrillus leucophaeus) [68], capuchins (Cebus apella, Cebus capucinus) [69], and macaques (Macaca mulatta, Macaca fuscata) and olive baboons (Papio anubis) [70] is evident but was much rarer to find published in our search.

Measures of the welfare of sanctuary-housed primates have also received considerable research attention. Broad chimpanzee welfare assessments [71–73], as well as studies focusing on both positive [37] and negative [74,75] indicators of wellbeing, have been studied in sanctuary settings. Leveraging the diverse backgrounds of sanctuary primates, researchers have further explored the welfare effects of atypical early life histories, such as the sudden loss of parents by orphaned wild chimpanzees [76], or atypical exposure to humans on former pets or performers [11–13,77]. Given the often traumatic lives of primates prior to arriving at a sanctuary, the psychological health of sanctuary-housed great apes has also received attention. Studies at Save the Chimps [78] as well as at Lola and the Tchimpounga Chimpanzee Rehabilitation Center (hereafter Tchimpounga) in the Republic of Congo [16] broadly explored psychological health, while the effects of the bushmeat trade on chimpanzees have also been documented [79]. Other studies involving sanctuary chimpanzees have focused on mood disorders, such as signs of generalized anxiety and compulsive disorders [80–82] and post-traumatic stress disorder in chimpanzees at Fauna Foundation in Canada (hereafter Fauna) [83,84].

Associated with welfare studies are those investigations that overtly acknowledge and focus on anthropogenic impacts on apes. For instance, a study at Lola focused on the outcomes of human interactions with the resident bonobos [85], and another at Sweetwaters Chimpanzee Sanctuary in Kenya (hereafter Sweetwaters), examined the effect of being watched by humans on chimpanzee resource acquisition [86]. Similarly, at Fauna, chimpanzees' responses to sound [87] and caregiver interactions [70] have been studied to determine their effects on the chimpanzees.

In contrast to studies that focus on elements that are unique to captive conditions, other studies focus on the very naturalistic state of some sanctuary environments, especially those in range-country facilities that provide expansive, naturally forested areas and species-typical foraging opportunities. In these cases, resident primates may represent suitable proxies for behaviours typically studied with wild populations. Ecological studies, such as those focused on fruit-opening behaviours by chimpanzees at Chimfunshi [88] and feeding decisions when presented with contaminated foods by bonobos at Lola [89], leverage natural foraging conditions at these sanctuaries for research opportunities. Other naturalistic studies have looked at primate food preferences [90], reactions to novel foods [91], interactions with wildlife [92,93] and responses to deaths of groupmates [94–96].

Some behavioural studies, while still generally considered non-invasive in nature, nonetheless involve some manipulation of the primates themselves or their environment. Animals may be temporarily separated from their group, shifted to other areas of their housing, or provided with resources or objects that would otherwise not be present. For instance, the study of cooperative behaviours among great apes has been widespread in sanctuary settings, with studies involving chimpanzees at Ngamba [97–104], Tchimpounga [105–107] and Sweetwaters [108], as well as bonobos at Lola [105,109]. In addition to cooperation, chimpanzee resource competition [110,111], helping behaviour [112–114] and altruism [115] have also been studied. Such studies, as well as extensive research on prosociality with both chimpanzees [116–119] and bonobos [97,120–124], use behavioural measures to assess apes' cognitive abilities. For example, yawn contagion, frequently used as a measure of empathy, has been studied in chimpanzees at Tacugama Chimpanzee Sanctuary in Sierra Leone (hereafter Tacugama) [125] and bonobos at Lola [126].

(b). Cognition

Though behavioural studies are often considered best-suited for sanctuary settings because of their unobtrusive nature, the depth and range of cognitive studies conducted in primate sanctuaries, particularly in range countries, is impressive. An array of innovative and easy to implement methods to assess primate thinking, learning, perception and emotion have been used in sanctuaries, with many studies buoyed by access to large sample sizes typically unavailable in zoos or research centres.

Among the first sanctuaries to embrace collaborations with external researchers interested in primate cognition was Ngamba. Researchers from several European and American universities have travelled there to work alongside sanctuary staff and resident chimpanzees on a wide range of topics; including, social learning in ecological contexts [127,128], problem-solving of a trap-tube task [129], deception [130], quantitative abilities [131], reasoning and inference abilities [132–134], perspective taking [135], inhibitory control compared across the great apes and human children [136], imitation and emulation [137,138], and one study finding that dogs (Canis familiaris) but not chimpanzees comprehend imperative human pointing [139]. Work at other chimpanzee sanctuaries in Africa followed suit, emphasizing individual [140] and social learning [141] in addition to comparative cognition research involving multiple species [142–144]. Specifically, researchers have also investigated topics such as reciprocity of ‘favours' by chimpanzees [145], development of spatial memory [146], auditory sequence learning [147] and joint attention [148–150].

Studies of the ways in which sanctuary-housed primates, primarily chimpanzees, make decisions and solve problems have yielded numerous publications over the previous two decades. Cognitive development [41,125,146,151,152], decision-making [153–157] and tool-use [94,158–163] are some of the most commonly studied topics involving great apes. However, researchers have also investigated several more specific topics with sanctuary-housed chimpanzees, such as the influence of both social presence [164] and early rearing history [165] on problem-solving. Other problem-solving research has looked at chimpanzees' use of causal and arbitrary cues [166] as well as the role of visual feedback in the floating peanut task [167]. The performance of chimpanzees at Ngamba on the floating peanut task has also been studied comparatively with human children and non-sanctuary-housed gorillas (Gorilla gorilla gorilla) and orangutans (Pongo pygmaeus) [168]. Though cognitive research has typically focused on chimpanzees, the cognition of sanctuary-housed bonobos is also well studied. Lola, in particular, is responsible for a number of studies on wild-born bonobo cognition [169,170], frequently in collaboration with other institutions to compare performance across multiple species [144,151–155,158,171–175]. Captive-born bonobo cognition has also received attention at both Ape Initiative [148,176,177] and Kumamoto [178–180].

As in other settings, the methods to study cognition in sanctuaries are highly varied, ranging from puzzles [129,138,167,168] to video playbacks of conspecifics [181]. Among the most common studies, in both range- and non-range-country sanctuaries, are those focused on handedness and laterality [177,182–192], in part because of methodology that can be as simple as providing small PVC tubes from which the apes pick out sticky foods with their finger. On the opposite end of the technology spectrum, the utilization of infrared eye-tracking devices continues to grow. Researchers at Kumamoto, often in collaboration with the Wolfgang Kohler Primate Research Center in Leipzig, Germany, have used these devices to investigate anticipatory looking and false beliefs [193–197] to explore topics such as joint attention and theory of mind.

(c). Veterinary, genetic and physiology

Primate sanctuaries, particularly those in range countries, have also been used for myriad studies on veterinary topics, as well as genetic and physiological research. Procuring biosamples from wild-born, but sanctuary-housed, primates is often far simpler in these managed settings than from their counterparts in the wild, making sanctuaries a logistically attractive option for many researchers in this field.

A wide range of clinical conditions specific to primates have thus been studied in sanctuary settings. Cardiac function [198] and disease [199,200] have been investigated in both chimpanzees and bonobos, as well as improvements to cardiac monitoring [201] and heart rate responses to anaesthetic protocols [202]. At Kumamoto, clinical cases of maxillary sarcoma [203], leprosy [204] and Down syndrome [205] have all been reported in chimpanzees, while researchers have also investigated a non-invasive test for tuberculosis in PASA sanctuaries [206]. Parasitology research has been conducted at a number of PASA sanctuaries, including a multi-institutional investigation of Trypanosoma brucei, the parasite responsible for sleeping sickness [207], which used samples from sanctuary-housed gorillas at Limbe Wildlife Center in Cameroon (hereafter Limbe) and chimpanzees from several facilities. Predictably, Plasmodium falciparum, the parasite causing malaria, has been studied extensively in African sanctuaries, with researchers collaborating to analyse samples obtained from all four great ape species [208,209], while similar research has been conducted at Kumamoto [210]. Parasites responsible for schistosomiasis have also been studied at Ngamba [211–215], while other intestinal parasites have been researched in sanctuary-housed chimpanzees at Kumamoto [216,217], Limbe and Sweetwaters [218], as well as in chimpanzees and mandrills (Mandrillus sphinx) at Tchimpounga [219] and bonobos at Lola [220].

Sanctuary research has also contributed to virology, including the potentially worrisome confirmed transfer of a pathogen between sanctuary workers and great apes [221,222]. Further research has looked at samples from both living and deceased great apes to better understand adenoviruses [223], polyomaviruses [224], enterovirus [225–227], Epstein–Barr virus [228], cytomegaloviruses [229], herpesvirus [230], poliovirus [231], retroviruses [232], sapovirus [233] and pneumonia [234]. Hepatitis B has also been studied with sanctuary-housed chimpanzees and gorillas [235–237], while other studies have looked at viral infections in chimpanzees at Ngamba [238] and inflammatory disease risk in chimpanzees at Sweetwaters [239].

Sanctuary-based research on the primate microbiome has used samples from Limbe [218,240], Ngamba [241,242], Sweetwaters [218,243–245], Tacugama [246,247] and Lola [247]. One noteworthy finding from this microbiome research has been the extent to which captivity humanizes the microbiome of numerous primate species housed at a variety of institutions, including sanctuaries [248]. Researchers have also studied various bacteria using samples from chimpanzees at several African sanctuaries [221,249–252], as well as biomarkers [253] and blood groups [254] in sanctuary-housed great apes. One case study even describes blood transfusions to treat an anaemic chimpanzee at Tchimpounga [255]. Post-mortem reports from chimpanzees who died at GFAS-accredited sanctuaries have been reviewed [256], while longevity and mortality of captive chimpanzees in Japan, including at Kumamoto, has also been studied [257].

Hormones, in particular cortisol and testosterone, have also been studied with sanctuary-housed primates. Cortisol has been measured in chimpanzees as an indicator of stress at Ngamba [258], while several studies at Kumamoto have further explored cortisol levels obtained from hair samples and its associated effects in chimpanzees [259–262]. Testosterone has been assessed in chimpanzees at Ngamba [263,264] and Kumamoto [265], as well as in chimpanzees at Tchimpounga and bonobos at Lola [266], where the effects of testosterone on cognitive performance were also tested [267]. Additionally, testosterone and cortisol have been studied in bonobos at Lola in the context of food competition [268]. Other hormonal relationships, such as the effects of castration on macaque social behaviour [269] and the effect of ageing on chimpanzee fertility [270], have been conducted at American and African sanctuaries, respectively.

At Kumamoto, researchers have looked at chimpanzee morphology [271,272], chimpanzee and bonobo finger length proportions [273], and the skeletal material of deceased primates from several sanctuaries [274]. Other topics of study at Kumamoto include chimpanzee colour vision [275,276], taste receptors [277,278], growth [279,280] and reproductive biology [281]. There are relatively few biological studies of non-ape species, though researchers at the Vervet Monkey Foundation in South Africa have used subcutaneous thermal sensors to examine internal temperature variation in vervet monkeys (Chlorocebus pygerythrus) [282]. Thermal imaging has also been used by researchers to examine psycho-physiological responses of resident chimpanzees [181,283].

A number of studies have also explored the genetics of sanctuary-housed primates. Research involving the genetics of chimpanzees has been conducted at Kumamoto [284–288], Limbe [289,290] and Ngamba [291,292]. Several other studies have further explored great ape genetics at multiple PASA-accredited sanctuaries [247,293–297], while one study looked at the genetics of chimpanzee neuroticism at sanctuaries in Africa and Japan [298]. At Kumamoto, DNA was also recently used to estimate chimpanzee ages [299], while even the mitochondrial DNA of the chimpanzee louse has been studied at Tacugama [300].

4. The future of sanctuary-based research

Though captive primate research in sanctuary settings has been conducted for far shorter a time period than in laboratories and zoological parks, this review demonstrates the impressive growth and scope of those efforts. Importantly, many of the studies mentioned in this review are highly collaborative in nature. Relatively few sanctuaries employ staff scientists, and many of the studies described here are initiated ‘from the outside' by scientists and students seeking novel and appropriate subjects for their research. Such inter-institutional and collaborative investigations may be particularly powerful and demonstrate increased variation for the factors under study. Indeed, it is increasingly the case that different types of institutions are willing and able to work together to increase sample sizes and research relevancy. For instance, much of the research focused on using large samples of primates to assess influences on personality has successfully combined populations living across zoos, laboratories, sanctuaries and even the wild [301–307]. Other collaborative efforts, such as the research partnership between Lincoln Park Zoo and Chimp Haven [19], work to leverage the respective institutional strengths of two organizations. Most broadly, the ManyPrimates initiative [308] aims to facilitate collaboration among primate researchers working in a variety of settings, including sanctuaries, by pooling resources, standardizing study methods, and growing sample sizes to augment research potency. Collaborations in which investment burdens are shared, information is openly exchanged, and participants invest in the success of their partners and the project, are those that are most likely to succeed. Such partnerships begin with the consideration of a sanctuary organization as more than simply a research resource housing potential research subjects, and an acceptance that organizational priorities may differ from those of traditional research venues.

Along with the aforementioned benefits of conducting research in a sanctuary setting, there comes a number of potential challenges in considering the availability of study opportunities. Unlike in laboratory and zoo settings, where self-sustaining populations of primates remain available for research purposes, the primates replenishing sanctuary facilities for the future are usually by-products of other activities, such as medical research, the bushmeat or pet trafficking trades, or use in the entertainment business. As those activities wane, likely so too will the influx of primates into sanctuaries. For example, the vast majority of chimpanzees housed in accredited sanctuaries in the United States have been transferred into the sanctuary community after their usefulness as subjects of medical research or as pets and entertainers ended. The dissolution of these activities resulted in a huge growth in the sanctuary chimpanzee population over the past two decades, but projections point to a steady decline in that population as those chimpanzees age and eventually die out. With no breeding programmes in accredited sanctuary settings, it is reasonable to expect that those chimpanzee populations, and any associated research with them, will conclude in about 40 years' time (Faust, unpublished data). However, this is not necessarily the case for other regions or other species. In range countries, unfortunately, the illegal bushmeat and pet trades continue to produce orphaned primates, among which the most fortunate funnel into nearby accredited sanctuaries. In non-range countries, biomedical research with monkeys remains common; as such, one might expect a continued influx of monkeys to sanctuary settings [309] and growth in organizations that house those species. Given that their very existence depends on the decisions and activities of other organizations and industries, the long-term sustainability of sanctuaries, and their associated research programmes, is thus difficult to predict. Indeed, many sanctuaries are overt about their organization's philosophy to ‘be in business to be out of business.’

Regardless of the long-term outlook for sanctuary organizations, the idea that sanctuaries can aid research is no longer a niche concept [310]. While in some cases they may serve as a replacement for research opportunities that are no longer available in other settings, there may also be lines of scientific inquiry that are actually best suited for sanctuaries. For instance, without breeding programmes, many sanctuaries have an increasingly aged population of primates in residence and studies of ageing may, therefore, be particularly well-suited for these populations. This review demonstrates the perhaps surprising breadth and depth of research being conducted in sanctuary settings around the world. While relatively narrow in taxonomic scope, existing and emerging partnerships with sanctuaries have produced high-quality science with important application potential. Continued development of collaborations between scientists and sanctuaries is likely to be of benefit to both the academic and animal care communities alike.

Data accessibility

This article has no additional data.

Authors' contributions

S.R. conceived and wrote the review. J.L. wrote the review and created the figures.

Competing interests

We declare we have no competing interests.

Funding

This work was funded by the Women's Board of Lincoln Park Zoo.