We collected data on orangutan translocation events between March 15, 2020 and March 14, 2021. To obtain these data we reviewed online newspapers, government reporting, and reporting by non-governmental organizations (NGOs) focused on orangutan rescue, rehabilitation and release. We searched the department of Natural Resources and Ecosystem Conservation [Konservasi Sumber Daya Alam dan Ekosistem (KSDAE)] newsblog, and Indonesian newspaper websites ANTARA News, Prokal, TribunNews, Kompas, and The Jakarta Post, using the search term “orangutan” to capture any relevant news published during the study period. We also performed a Google Advanced Search for news results in both English and Bahasa Indonesia for the search term “orangutan” published during this period. The term “orangutan” is typically spelled the same in both languages, although searches for “orangutan” also returned results for the alternate spelling “orang-utan.” We compiled reported information from the ten organizations that held and released orangutans within Indonesia as of 2020, namely Bornean Orangutan Survival Foundation, Centre for Orangutan Protection/Borneo Orangutan Rescue Alliance, International Animal Rescue-Ketapang, Orangutan Foundation International, Orangutan Foundation–UK, Orangutan Information Centre, Sintang Orangutan Centre, Yayasan Jejak Pulang, and government facility BKSDA Tenggarong. Provincial departments of KSDAE, the Balai Konservasi Sumber Daya Ekosistem (BKSDA) also rescue and release orangutans and may temporarily hold them but do not operate long-term captive care facilities. Data on BKSDA releases were collated from the KSDAE online newsblog, and from online newspaper sources. Data on NGO releases were collected from these organizations' newsblogs, press releases, social media posts, annual reports, monitoring reports. Articles in Bahasa Indonesia were translated using Google translate, and we referred questions on meaning or nuance to Indonesian speaking authors of this paper.

For each record referencing orangutan translocations, we extracted any available data on: (1) rescue and release dates; (2) number of animals; (3) individual animal's age, sex, name, physical condition; (4) any description of health checks and post-release monitoring; (5) the origin and release locations; and (6) the entities conducting the translocation. Wherever possible we analyzed multiple sources to confirm data and address gaps within individual records. We excluded any possible duplicate records by reviewing for repeat mentions of combinations of available information on release date; animal name, age, and sex; and the translocation location and circumstances. We excluded all records where it was unclear if the animal had been previously counted. Releases were classified as: (1) reintroduction/reinforcements if they involved ex-captive orangutans that spent 6 months or more in rehabilitation facilities, or (2) wild-to-wild translocation if they involved wild orangutans captured and released within six months or less. Re-releases of previously released and recaptured orangutans were classified as the type of release originally conducted.

Release rates are the annual sums of individual animals released by release classification. For comparison of release rates before the COVID-19 pandemic, we used our published data on orangutan rescues and releases from 2007–2017 (4), and authors' dataset on 2018–2019 rescues and releases (Sherman, Ancrenaz and Meijaard unpublished data, Jaya unpublished data). The collection methods for these data are the same as described here for 2020 data.

The authors comprise a group of wildlife health, conservation and orangutan experts including orangutan translocation practitioners, orangutan conservation practitioners, and specialists in orangutan population, socioecology, health, and welfare. These practitioners considered the research questions of whether orangutan translocations can pose disease transmission and conservation risks, and specifically COVID-19 transmission risks. We followed the problem description questions posed by the OIE and IUCN Manual on Procedures for Wildlife Disease Risk Analysis (2014) in considering these queries. A problem description identifies the questions and issues being considered, assesses the cultural, political and social contexts that affect these issues, and identifies potential pathways by which risk is introduced (37). Here, we reviewed data to identify four elements of potential risk: (1) is the problem (pathogen transmission and conservation risk) potentially occurring?; (2) in which ways could the problem occur?; (3) what is the scope and context of the problem?; and (4) how should the problem description inform action? Some authors of this paper will also participate in the upcoming orangutan Disease Risk Analysis workshops, while others are not part of the workshop group, and serve here to provide external, independent views on the problem description. Having separate and independent problem description and hazard identification/DRA processes has been recommended to prevent political and social biases (38).

To determine whether transmission is potentially occurring (element 1 of potential risks, as described above), we reviewed the available data on orangutan translocations during the COVID-19 era (Orangutan Translocation Data Collection and Analysis). To examine which ways the problem could occur (element 2), we used published literature and author's expert knowledge to identify the “risk pathways” –logical routes by which pathogens could be introduced to orangutans from humans, or vice versa, or could spread amongst orangutans in captivity or in the wild (Table 1). It was necessary to answer OIE and IUCN (36) problem description questions separately for each translocation type (reinforcement, reintroduction, and wild-to-wild translocation), as each translocation type has a distinct set of risks and uncertainties. Element 3 required consideration of the conservation, policy and cultural contexts underpinning orangutan translocations, using published literature and author's unpublished data. Elements 1–3 are summarized in Table 2, a matrix of answers to the OIE and IUCN (36) problem description questions.

To exemplify how the problem description could inform decision making and action (element 4), we used SARS-CoV-2—an example of a human to non-human primate transmissible pathogen—to develop the qualitative risk matrix tool (Figure 5). We considered published data on COVID-19 disease presence in humans and great apes, and in other wildlife and domestic animals. We used qualitative categories of risk because data were not available for captive and wild orangutan exposure and transmission of the SARS-CoV-2 pathogen in Indonesia, and to make the matrix more useful to the diverse array of orangutan translocation stakeholders and decision makers (38). We made a logical stepwise matrix of risk categories based on the likelihood of active infection; exposure of susceptible individuals; and consequences of susceptible recipients becoming infected, getting sick or dying, and spreading the disease (28, 32). The risk matrix is based on Risk = Likelihood × Consequences. Likelihood and consequence category definitions are provided in the cells bounding the risk matrix. Category definitions are based on human health and safety risk likelihood and consequence definitions (47, 48). We also factored in mitigations including personal protective equipment (PPE), disease testing, and vaccination, as well as uncertainties about disease transmission and its consequences (28, 33). We weighed associated conservation risks using the IUCN precautionary principles, which state that great ape releases should not endanger wild conspecifics, other taxa within the release habitat, or habitat ecosystem functions (1, 3).

Our results suggest that the problem—pathogen transmission between humans and orangutans—is potentially occurring. Orangutans are being handled by or are in physical proximity with humans for extended periods. Translocated orangutans are highly likely to be in contact with wild orangutans after release. Other than the two sites in Sumatra, where wild-to-wild translocated and rehabilitated orangutans are reintroduced within historical range but outside current distribution (49), orangutans are purposefully released into wild populations, or into areas where they have the potential to disperse into existing wild populations (4, 50, 51).

Orangutan translocations decreased in frequency but continued throughout the COVID-19 pandemic. We identified releases of at least 15 rehabilitated ex-captive orangutans (reintroductions or reinforcements), and 27 wild-to-wild translocations in Indonesia from March 15, 2020 to March 14, 2021 (Table 3). At least two wild-to-wild translocations occurred during the March–May 2020 Indonesian government moratorium on captive wildlife releases. Three wild orangutans, one P. pygmaeus, one P. abelii and one P. tapanuliensis, were translocated multiple times during the study period. Total orangutan releases declined 74% and wild-to-wild translocations declined 64% during the study period compared to the average annual rate over the 5 years before COVID (2015–2019) (Figure 1). Notably the number of wild-to-wild translocations was highest in 2015, likely induced by the greater incidence of fires during the El Nino phase that year. The annual wild-to-wild translocation rate dropped from 155 in 2015 to 61 in 2016, and varied between 57 and 26 between 2017 and 2019.

In March 2020, IUCN Primate and Wildlife Health specialist groups recommended halting all releases of great apes in light of the extraordinary risk posed by the potential transmission of COVID-19 from humans to non-human great apes (30, 33). The Indonesian government prohibited captive wildlife releases in mid-March 2020 to prevent disease transmission to wild populations (71, 72). On May 20, 2020, the Indonesian Ministry of Environment and Forestry released a circular lifting this moratorium and providing technical instructions for wildlife releases during the COVID-19 pandemic (73, 74). The circular stipulates that all animals, including wild individuals that have been near humans, must go through medical examination and receive a certificate of health from KSDAE prior to release, and that the number of personnel involved in the release should be limited to the smallest number feasible to safely conduct release activities (73). All wildlife rescues and releases are conducted by Indonesian government personnel from the KSDAE (75, 76). Results of the implementation of the circular were not publicly available.

While some safety measures have been taken to prevent the spread of COVID during translocations, these measures have been inconsistent and insufficient to avoid potential pathogen exposure risk to wild populations. Photographs in news and social media reports showed some precautionary measures such as personal protective equipment (PPE) were applied during the study period (57, 67, 77), but use was not consistent. Photographs show many people present at releases, often in direct contact with orangutans (Figure 2). Some examples include: (1) a wild-to-wild translocated P. tapanuliensis surrounded by seven people, four of whom were not wearing any PPE (70); (2) a wild-to-wild translocation during the captive wildlife release moratorium (March 23, 2020) with at least 10 people present, and three people wearing masks below their nose or mouth (52); and (3) two people next to an anesthetized wild-to-wild translocated orangutan, both with masks below their chins (69). Such situations also occurred in release records prior to COVID (78–80) (Figure 3). We could not assess the proportion of releases during the study period with adequate vs. inadequate protective measures because published photographs were not available for every translocation event, and when available do not capture every aspect of the entire procedure. However, the available images illustrate the reality of the disease transmission risks during orangutan translocation.

Pathogen transmission can occur via numerous pathways inherent in the orangutan rescue, rehabilitation and translocation process (Table 2). This includes consideration of transmission risks posed by exposure times, e.g., 15 min or longer for COVID-19 (39). The table addresses pathways for other pathogens of concern that can cause morbidity or mortality in orangutans, can be transmitted to wild orangutans, and have been identified in captive orangutans. Examples of these pathogens include members of the viral families Hepadnaviridae, Picornaviridae, Phabdoviridae (81, 82), bacteria such as Streptococcus sp, Burkholderia pseudomallei (82) and Mycobacterium tuberculosis complex (83), and parasite species including Plasmodium sp. (including strains that also infect other non-human primate species and humans) (84), Entamoeba histolytica and Strongyloides sp, that would all likely result from contact or proximity to humans (84). Pathways of zoonotic disease transmission between humans and orangutans or among orangutans include direct and indirect contacts (abiotic transfer via fomites and other transmission ways), and animal vectors.

Based on evidence that the problem can potentially occur through a variety of pathways inherent in the orangutan translocation process, we developed a problem description (Table 2). We included data presented in this study, along with contextual information on conservation, socioeconomic, political, and ethical considerations from published literature (see discussion) to answer the problem description questions posed by OIE and IUCN (36). This problem description highlights a large number of data gaps and assumptions, indicating that a qualitative method of assessment based on the precautionary principle will likely be needed in the first iteration of a DRA for orangutan translocation.

We used the data summarized in the problem statement to make a qualitative risk assessment matrix that can be used by practitioners to consider overall threats associated with orangutan translocations (Figure 4). Likelihood for transmission from humans multiplies as more people interact with or are in proximity to the orangutan, and as exposure times lengthen. We also considered available information on mitigation measures and uncertainties, all of which modify likelihoods and consequences.

The risk of catastrophic consequences is highest for wild-to-wild translocation of Tapanuli orangutans. Tapanuli orangutans are the world's rarest great ape species, with a population of <800 individuals under significant threat from human activities (8). The capture and release of these orangutans puts them at risk of exposure to the virus from infected humans. COVID-19 is uncontrolled in Indonesia at the time of writing, with only 17% of the population vaccinated (85), and it is possible that humans in proximity to translocated animals will not use adequate disease risk mitigation measures (Figures 2, 3). Translocation of these animals into a small, geographically constrained wild population that is susceptible and non-immune to COVID-19, and already at serious risk of extinction, poses marked risks. Slightly lower but still severe risk is posed by wild-to-wild translocation of P. abelii and P. pygmeaus, or their release to reinforce wild populations, again due to known susceptibility of the species to the COVID-19 pathogen, likely exposure of translocated orangutans to humans without protective measures, and that wild and formerly released animals are non-immune.

Reintroduction of rehabilitated ex-captive orangutans is somewhat lower risk due to extensive protective measures available for captive animals and staff. Nonetheless, the risk remains high due to pathways for infection during captivity or release, or following release (at provisioning or observation sites), and subsequent risk of pathogen transmission to susceptible and non-immune conspecifics at the release site. Captive orangutans pose a moderate risk overall, as protective measures can be employed consistently. As with reintroduction, opportunities for infection during captivity still persist due to human contact and proximity.

Populations of all three species of orangutans are declining, primarily due to forest loss and killing (6). The underlying drivers of these threats complicate efforts to conserve orangutans. Poverty and well-being are significant concerns across much of Indonesia, particularly in rural areas with limited access to markets (91). Expansion of palm oil production, including in orangutan range, has been championed by industry and government as a solution for poverty alleviation, despite mixed results for human livelihoods and well-being (92). Results for orangutans, on the other hand, have been markedly poor (40, 41). However, conservation and management of orangutan populations within forest reserves and forested patches in palm oil plantations is possible if killing is avoided (5, 43, 93).

Where forests are cleared for agriculture, agro-forestry, natural resource extraction, or human settlements, orangutans are often driven out of their original habitats or have easier access to human crops (94–96). This can lead to conflicts with people when orangutans are found crop foraging or using human-occupied areas. Orangutans are often injured or killed by humans in these situations (4, 97). Orangutans are also killed for food, for traditional medicine, or to obtain live infants for pets (98).

Capturing infant orangutans nearly always necessitates killing the mother (99). Although illegal, keeping infant orangutans as pets is common in Indonesia, as is injury or harassment of wild orangutans found in human-occupied areas (4, 99). On average, more than 115 wild or illegally captive orangutans are being surrendered, confiscated or otherwise rescued by wildlife rescue organizations and government annually (4). Many Indonesians who buy or take an infant orangutan are motivated to “save” or care for the animal, although most privately held animals are rescued from malnourishment and often horrific conditions (4, 100).

Against this background of poverty, strong demand for forest lands, high killing rates and consistent local demand for pet orangutans, translocation is often marketed to the public as a means to “save” orangutans (4). Investments into orangutan rescue, rehabilitation and release total millions of dollars annually, but have not halted the continued decline in species populations (44), although these investments have prevented losses from being even greater (Santika et al., in prep). Orangutan releases are considered a conservation necessity by some (101), while others note that releases do not address the taxon's most urgent conservation needs, namely preventing deforestation and fragmentation of natural forest habitats, and forestalling the loss of wild orangutans by addressing killing and capture (9, 44). Rehabilitation and release also cost more than 12 times as much per orangutan as improved habitat protection (45). Nonetheless, releasing captive orangutans back to the wild is considered the only ethical option by many practitioners (46). Orangutan release also presents an ostensibly “quick and easy solution,” while habitat protection or community engagement to address killing requires longer term investment and effort, particularly in lowlands where stakeholders with complex and vested interests exist (Santika et al., in prep). Reintroduction of orangutans into historical range but outside current distribution has resulted in establishment of two new Sumatran orangutan populations, which are projected to become self-sustaining over time if releases continue over the next ten years and habitat loss and killing are prevented (102). Notably, habitat incursion and human-orangutan conflict are pressing concerns in at least one of these areas (103). Rehabilitated ex-captive and wild-to-wild translocated orangutans have also been released to reinforce viable and some small non-viable wild populations in both Kalimantan and Sumatra (4).

Orangutans metapopulations are multiple interacting individual orangutan populations bounded by geographic barriers. These metapopulations are projected to continue declining despite release activities, due to habitat fragmentation, forest loss and orangutan killing or removal (102). This is partly explained by the fact that releases do not represent net additions of orangutans to wild populations. Most ex-captive orangutans represent a net loss of at least two wild orangutans from the source population (the mother, likely killed, and the captured infant), with the rehabilitated former infant released after years of rehabilitation into another population (4). Wild-to-wild translocations thus represent a lateral movement comprised of removal of the wild orangutan from one local population, and its release into another.

Orangutan behavior and socioecology pose challenges for rehabilitation and survival of released orangutans, further complicating the potential for releases to boost wild populations (87). Wild adults of both sexes face difficulties in establishing a home range and adapting socially if translocated to a new location where the local orangutan population is unfamiliar to them. Wild-to-wild translocations are a particular concern in this regard, as they capture and remove wild orangutans from their metapopulation, disrupting the breeding and social structures of dispersed males and resident females (5). Importantly, different forest types within orangutan range differ in their seasonal, annual and spatial distribution of fruit and other food resources (104, 105), meaning orangutans may not know where and when to find important foods if they are translocated to unfamiliar locations (4). This may explain why wild-to-wild translocated orangutans often return to their capture site from following release, resulting in some animals being recaptured and moved multiple times (Table 3). Finding food in an unfamiliar habitat could also pose energetic stresses. Orangutans can exhibit decreased body weights and depleted fat stores during periods of low fruit availability (106). Wild orangutans with low body weights found foraging in oil palm plantations or other human crops are often considered to be starving and in need of being moved to new habitats, but instead may in some cases be going through a natural cycle of muscle catabolism during low fruit availability.

All this wicked complexity (9, 11) is happening in a context of limited information on orangutan disease surveillance and risk management. Orangutan veterinarians and rescue, rehabilitation and release NGOs and government agency staff are part of a long-running capacity development project, the Orangutan Veterinary Advisory Group (OVAG). OVAG provides capacity building on disease diagnosis and treatment, surveillance, risk management, and development of DRAs. Studies have been conducted on outbreaks in orangutan rehabilitation facilities (107, 108), and there have been instances of orangutans released with transmissible pathogens (109). Surveillance for wild orangutan diseases, zoonotic pathogen transfer, disease spillover and emerging diseases is limited, and indeed most wild populations are not surveilled. We are not aware of any DRA for orangutan translocation, and there is a paucity of data available on the management and risk abatement of pathogens that could infect orangutans.

Practitioners may perceive zoonotic disease transmission as less likely for orangutans than for other great apes, because of orangutan's semi-solitary lifestyle, more arboreal behavior in natural conditions, and the lack of clear examples of diseases wiping out orangutan populations following releases (23, 24, 110). But orangutans do come to the ground (111) and can contract human carried diseases, especially those transmitted via the fecal-oral or airborne transmission routes, respiratory viruses and bacteria in particular (110). Respiratory ailments sinusitis, airsacculitis and pneumonia are of particular concern for orangutans (112, 113). Further, males may travel among wild populations to find females (5, 105). This underscores the suggestion that individual orangutans can be disease superspreaders among conspecifics (114). Importantly, orangutans captured due to their proximity to humans may have already been exposed to human diseases. For example, orangutans have been observed using small puddles and human-constructed drains as water sources, which are highly likely to be contaminated with human waste (Oram, unpublished data) and which can also facilitate infections such as malaria from insect vectors (108).

Active COVID-19 infections are circulating among humans in Indonesia at a reported rate of 2,931 average daily cases and 182 average deaths daily as of September 2021 (85). At least one COVID-19 variant of concern, the more transmissible Alpha (formerly B.1.1.7), was verified in Indonesia as of March 16, 2021 (115). Although orangutan-specific consequences of SARS-CoV-2 remain unknown, extensive contact with caretakers during rehabilitation, the number of people involved in orangutan care and release, and occasional contact or proximity with humans through post-release monitoring, field research activities, provisioning or tourism potentially exposes orangutans to becoming asymptomatic carriers of contagious diseases, including SARS-CoV-2 (21–24, 31). Humans can transmit COVID-19 several days prior to being symptomatic, as occurred with captive gorillas (116). Transmission from humans to apes is thus classified as “likely” (Figure 4). Although rescue practitioners regularly use disease mitigation measures, wild-to-wild translocated orangutans are exposed to extensive human interactions that likely include humans without PPE or testing. Rehabilitation of ex-captive orangutans includes episodes of frequent exposure to human interaction over long periods (4), but likely with consistently applied mitigation measures, hence with lower overall risk. Nevertheless, there are unknowns for all releases including the potential for people to transmit disease even while using PPE or after vaccination.

Rescue centers mitigate many risks via disease surveillance and testing for likely zoonotic diseases in rehabilitated ex-captive orangutans, and government policies require proof of disease testing results, including for SARS-CoV-2, prior to release of ex-captives. Specifically regarding COVID-19, orangutan rescue organizations reported making significant efforts and financial outlays to implement precautionary protocols such as regular COVID-19 antigen testing for staff, use of PPE, and closures to tourism and volunteers (74, 117–125). Rescue organization personnel are also getting vaccinated against COVID-19. Vaccination has been successful in preventing COVID-19 infections in captive populations of black-footed ferrets, an endangered species susceptible to the disease (126). In the United States some captive populations of orangutans and other great apes have been vaccinated (116) and vaccination of captive Indonesian orangutans may become an option. However, species-specific healthcare and disease risk management expertise varies across orangutan facilities and personnel, as do efficacy of diagnostic tests and vaccines, and exposure of orangutans to humans. In particular, wild orangutans captured and translocated during the COVID-19 pandemic may be at greater risk of exposure per the World Health Organization's (WHO) definition (39): During the process of capture, examination, transport, and release, these animals are in direct contact with humans and at distances of <2 m from people, many without any PPE (Figures 2, 3), for more than 15 min. In some cases, there are large numbers of people without PPE in contact or close proximity to the animals (Figures 2, 3).

It is likely that any infected orangutans released into wild or reintroduced populations could spread SARS-CoV2 among conspecifics, thus consequences qualify as at least “significant” (Figure 4). SARS CoV2 affects multiple species, meaning likelihood of further species spillover is high (31, 127). Such spillover could pose catastrophic consequences to species, ecosystems and potentially humans (Figure 4). These considerations are applicable to any other transmissible diseases that could affect orangutans.