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. 2021 Jan 5;83(2):e23228. doi: 10.1002/ajp.23228

Opportunities for respiratory disease transmission from people to chimpanzees at an East African tourism site

Darcey B Glasser 1, Tony L Goldberg 2, Nelson Guma 3, Godfrey Balyesiima 3, Hillary Agaba 3, Simplicious J Gessa 3, Jessica M Rothman 3,4,5,✉
PMCID: PMC7883129  PMID: 33400317

Abstract

Respiratory illnesses, including COVID‐19, present a serious threat to endangered wild chimpanzee (Pan troglodytes) populations. In some parts of sub‐Saharan Africa, chimpanzee tracking is a popular tourism activity, offering visitors a chance to view apes in their natural habitats. Chimpanzee tourism is an important source of revenue and thus benefits conservation; however, chimpanzee tracking may also increase the risk of disease transmission from people to chimpanzees directly (e.g., via aerosol transmission) or indirectly (e.g., through the environment or via fomites). This study assessed how tourist behaviors might facilitate respiratory disease transmission at a chimpanzee tracking site in Kibale National Park, Uganda. We observed tourists, guides, and student interns from the time they entered the forest to view the chimpanzees until they left the forest and noted behaviors related to disease transmission. Common behaviors included coughing, sneezing, and urinating, which respectively occurred during 88.1%, 65.4%, and 36.6% of excursions. Per excursion, individuals touched their faces an average of 125.84 ± 34.45 times and touched large tree trunks or branches (which chimpanzees might subsequently touch) an average of 230.14 ± 108.66 times. These results show that many pathways exist by which pathogens might move from humans to chimpanzees in the context of tourism. Guidelines for minimizing the risk of such transmission should consider tourist behavior and the full range of modes by which pathogen transmission might occur between tourists and chimpanzees.

Keywords: conservation, tourist behavior, zoonotic

Chimpanzee (Pan troglodytes) observed during study.

graphic file with name AJP-83-e23228-g001.jpg

Highlights

Great ape tourism presents risk for reverse zoonotic infection.

Future guidelines for great ape tourism should take into consideration the behavioral propensities of individual tourists.

1. INTRODUCTION

Human respiratory illnesses have caused significant mortality in wild African great ape populations, all of which are endangered (Kaur et al., 2018; Negrey et al., 2019; Palacios et al., 2011; Spelman et al., 2013). In the Kanyawara community of chimpanzees in Kibale National Park, Uganda, for example, respiratory illness has been the leading cause of death for over 31 years (Emery Thompson et al., 2018). Human metapneumovirus (HMPV) in Tanzania (Kaur et al., 2018), HMPV and human respirovirus 3 virus (HRV3) in Uganda (Negrey et al., 2019), rhinovirus C in Uganda (Scully et al., 2018), and coronavirus OC43 (Patrono et al., 2018) have been implicated in at least 84 individual wild chimpanzee deaths from 1968 to 2013.

These examples show that chimpanzees are susceptible to most, if not all, human respiratory pathogens. Although SARS‐CoV‐2 has not yet been documented in wild primates, it is considered a serious threat to great ape populations nonetheless (Melin et al., 2020). Human angiotensin‐converting enzyme‐2 (ACE2) has twelve key amino acid residuals on its surface, critical to SARS‐CoV‐2 infection (Melin et al., 2020). Apes, including chimpanzees, share those same key amino acid residuals, suggesting a similar susceptibility (Melin et al., 2020). Furthermore, wild chimpanzees have been infected with another human‐origin coronavirus, OC43, in Côte d'Ivoire in 2016 (Patrono et al., 2018). During this outbreak, samples of OC43 taken from infected chimpanzees proved genetically identical to samples taken from asymptomatic humans with access to the park, despite quarantine before and after the visit (Patrono et al., 2018).

Great ape tourism is a popular activity that offers tourists the opportunity for tourists to learn from and engage with nature (Williamson & Macfie, 2014). It also provides a source of income that can be used to further great ape conservation efforts (Litchfield, 2001). When properly regulated, great ape tourism can benefit visitors, local communities, and hosting governments, and apes. However, tourism can also have negative consequences, in particular, increased disease risk to the apes (Muehlenbein & Wallis, 2014), which could cause dramatic population declines (Leendertz et al., 2006). To mitigate these risks, rules for great ape tourism by government agencies and the International Union for Conservation of Nature (IUCN), include preventing sick tourists and researchers from going into the field, maintaining proper distance from apes, controlling the duration of ape viewing, and practicing good biosecurity and hygiene, but these rules can be difficult to enforce (Hanes et al., 2018; Nakamura & Nishida, 2009; Weber et al., 2020), and with the emergence of SARS‐CoV‐2, have already been reevaluated (Gillespie & Leendertz, 2020; IPS, 2020; Reid, 2020; Williamson & Macfie, 2014). For example, tourists visiting the chimpanzees at Mahale Mountains National Park, Tanzania were closer to chimpanzees than stipulated regulations and some tourists were seen coughing near the chimpanzees (Nakamura & Nishida, 2009).

Building on previous research, the objective of this study was to record human behavior during chimpanzee tracking that might affect the risk of reverse zoonotic disease transmission. In Uganda, the Kanyanchu community of chimpanzees is visited by approximately 10,000 tourists per year from locations around the world (Kibale National Park General Management Plan, 2015). During these 1‐h excursions, tourists are assigned to groups of six to visit a subgroup from a community that contains over 120 individual chimpanzees. Although visitors and guides are usually conservation‐minded (Bulbeck, 2005), we hypothesized that they might engage in behaviors that could inadvertently expose the chimpanzees to reverse zoonotic pathogens. We also examined the number of tourists per group, their distance from chimpanzees, and the overall time spent viewing chimpanzees to assess compliance with current regulations.

2. METHODS

2.1. Ethical statement

Our research adhered to the legal requirements of Uganda, as well as the Principles for Ethical Treatment of Nonhuman Primates formulated by the American Society of Primatologists. The Institutional Review Board at Hunter College reviewed this study and they determined that it was exempt from review because the research involved observation of public behavior. The tourists were informed that a researcher was present during their visit. The identities of tourists were not recorded.

2.2. Study site

Kibale National Park, Uganda is a mid‐altitude forested park approximately 795 km2 (Chapman et al., 2005). The park is managed by the Uganda Wildlife Authority. We collected observational data on visitors during tourist excursions to the Kanyanchu chimpanzee community. The community's home range is approximately 50 km2. This community is visited by tourists, whereas other habituated chimpanzee communities in the park are the subjects of long‐term research (Wrangham & Ross, 2008).

2.3. Behavioral observations

We collected data from June 14th to August 12th, 2018, for a total of 101 excursions over 52 days during the high tourist season (when the majority of tourist excursions occur). Excursions were led by staff of the Uganda Wildlife Authority and occurred three times daily: 8 am (morning), 11 am (mid‐morning), and 2 pm (afternoon), each lasting 2‐5 h, with 1 h for viewing the chimpanzees. Our sampling effort was distributed evenly among these different viewing times.

Before excursions began, tourists presented their permits or payments and listened to a short safety briefing. This briefing included the following information: basic park information (history, species present, etc.), rules and regulations (no eating, flash photography, littering, etc.), chimpanzee specific information (community composition, typical behaviors, habituation process, etc.), and activity information (length of activity, what to wear or carry, etc.). Tourist groups were then divided and mandated to have no more than six people per group, including their guide and any interns, students, or researchers. Groups departed simultaneously, often from different trail entrances and remained in contact via radio. When chimpanzees were spotted, guides communicated through radios to ensure all tourists were able to view chimpanzees, occasionally leading to group “merges.”

Behavioral data on visitors including park guides (n = 15), interns (n = 10), and tourists (n = 459), were collected using a prescribed ethogram as well as additional relevant behaviors (Table 1) continuously during the track and ad libitum; in addition, any miscellaneous behaviors deemed relevant to disease transmission were recorded. Human behaviors were grouped into six categories: self‐grooming, bodily functions, eating, forest interactions, interpersonal interactions, and miscellaneous potential concerns. Guide safety warnings to tourists during excursions were recorded under miscellaneous potential concerns to account for tourist behaviors that guides actively tried to end. All occurrences of a behavior in the ethogram by any individual were recorded during the excursion. The following visitor group metrics were also recorded: initial group size, group size if merged with other visitors, distance while viewing arboreal and terrestrial chimpanzees, and time spent viewing chimpanzees. Merging was defined as when two excursion groups met in the forest and remained together for longer than 5 min.

Table 1.

Total instances of recorded human behaviors during 101 visitor excursions, grouped by six behavioral categories

Category # Instances # Excursions % Excursions
Self‐grooming 12,654 101 100.0
Aerosol sunscreen/bug spray 2 10 9.9
Biting/cleaning fingernails 32 32 31.7
Chapstick/lipstick 2 2 2.0
Eye drops 1 1 1
Hand‐to‐face contact 12,584 94 94.1
Face wipes 1 1 1.0
Hand sanitizer 5 5 5.0
Q‐tip (twig) 1 1 1.0
Toothpick (twig) 25 25 24.8
Wash hands 1 1 1.0
Bodily functions 965 95 94.1
Bleeding 4 4 4.0
Coughing 733 89 88.1
Defecating 1 1 1.0
Sneezing 154 66 65.4
Spitting 16 13 12.9
Urinating 57 37 36.6
Eating 42 17 16.8
Breakfast foods (bread, eggs, millet) 5 7 6.9
Leaves 1 1 1.0
Lunch items (sandwiches, potatoes) 20 11 10.9
Snack Foods (protein bars, crackers, g‐nuts, gum) 16 25 24.8
Miscellaneous potential concerns 398 70 69.3
Age/12‐year old 1 1 1.0
Approaching chimps 30 21 20.8
Dehydration 1 1 1.0
Dropped gun 1 1 1.0
Earphones while walking 1 1 1.0
Falling 21 18 17.8
Flash camera 21 21 20.8
Gloves 15 15 14.9
Guide safety warnings 279 30 29.7
Handle feces 1 1 1.0
Ill/sick 4 4 4.0
Imitating chimp calls 20 20 19.8
Lighter 1 1 1.0
Phone call 1 1 1.0
Tourist lost 1 1 1.0
Direct forest interactions 23,669 100 99.0
Drop forest object after touching (fruit, leaves, feathers, snake skins) 83 60 59.4
Kiss tree 1 1 1.0
Littering 7 6 5.9
Removed fruit 1 1 1.0
Sitting on forest floor 561 79 78.2
Touching large tree trunks or branches 23,014 98 97.0
Using a branch as a walking stick 1 1 1.0
Wiping hands on leaves 1 1 1.0
Interpersonal interactions 170 54 53.5
Hand holding 160 53 52.5
Kissing 10 7 6.9
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This article is being made freely available through PubMed Central as part of the COVID-19 public health emergency response. It can be used for unrestricted research re-use and analysis in any form or by any means with acknowledgement of the original source, for the duration of the public health emergency.

2.4. Data analysis

Human behaviors were displayed as frequency distributions and standardized as a proportion by dividing by the number of excursions (N = 101). The following parameters were analyzed using one‐sample t tests: initial group size, group size while merged, distance while viewing both arboreal and terrestrial chimpanzees (A&T), distance while viewing arboreal chimpanzees (A), distance while viewing terrestrial chimpanzees (T), and time spent viewing chimpanzees. The null hypotheses for t tests were values recommended by the International Union for the Conservation of Nature (Gilardi et al., 2015) and Uganda Wildlife Authority (UWA) guidelines (Kibale National Park General Management Plan, 2015–2025).

3. RESULTS

A total of 15 park guides, 10 interns, and 434 tourists (N = 459) visited the chimpanzees during the chimpanzee tracks. “Self‐Grooming” occurred during all excursions (100.0%), followed by “Direct Forest Interactions” (99.0%), and “Bodily Functions” (94.1%) (Table 1). Across categories, touching large tree trunks or branches was the most frequent human behavior, followed by hand‐to‐face contact Table 2.

Table 2.

Visitor group size, distance to chimpanzees and time spent visiting chimpanzees in Kibale National Park, Uganda

Group characteristic: Recommended value Observed value Std. Dev. t df p α
1 Mean initial group size (# of persons) 6.0 6.0 1.2 0.3 100.0 .80 .05
2 Mean group size while merged (# of persons) 6.0 18.3 5.2 23.1 93.0 p < .001 .05
3 Mean distance while viewing (m) 8.0 13.7 6.3 8.8 96.0 p < .001 .05
4 Mean distance while viewing arboreal chimpanzees (m) 8.0 21.3 9.5 13.0 86.0 p < .001 .05
5 Mean distance while viewing terrestrial chimpanzees (m) 8.0 6.7 2.3 5.2 87.0 p < .001 .05
6 Mean time spent viewing (min) 60.0 79.1 22.0 8.7 100.0 p < .001 .05
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This article is being made freely available through PubMed Central as part of the COVID-19 public health emergency response. It can be used for unrestricted research re-use and analysis in any form or by any means with acknowledgement of the original source, for the duration of the public health emergency.

The total number of groups embarking at any given time ranged from 1 to 6, for a range of 3 to 60 individuals in the forest at the same time. On average, tourist groups merged during 40% of the total excursion time (55.5 ± 32.0) and the mean group size while merged (18.3 ± 5.2) was larger than IUCN recommendation of six people per group, t (93) = 23.1, p < .001. Mean distance while viewing chimpanzees on the ground (6.7 ± 2.3) was closer than the IUCN recommended 8.0 meters, t (87) = 5.2, p < .001. Time spent viewing chimpanzees regardless of terrestrial or arboreal position was longer than the 60 min viewing time recommended by IUCN, t (100) = 8.7, p < .001.

4. DISCUSSION

Great ape tourism is a “double‐edged sword” in that it simultaneously provides economic incentives for conserving apes while also putting them at risk for reverse zoonotic infections. Although visitors and guides are usually conservation‐minded, we hypothesized that they might engage in behaviors that could inadvertently expose chimpanzees to reverse zoonotic pathogens. Therefore, our study quantifies potential modes of transmission from humans to chimps that could inform disease risk prevention strategies. Self‐grooming and direct forest interactions were the two most common behavioral categories recorded. Each singular instance of hand‐to‐face contact or touching forest objects could lead to the deposition of infectious agents on fingers and fomites, respectively, even if the person is not clinically ill (Edemekong & Huang, 2019). Using twigs as Q‐tips or toothpicks, spitting, bleeding, coughing, sneezing, urinating, defecating, eating, and depositing food scraps on the forest floor, and handling or tasting forest fruits pose risks of depositing infectious agents into the forest as well, with heightened probabilities that chimpanzees will encounter them later. These observed high‐risk behaviors support our hypothesis that apes could come into contact with zoonoses if measures are not taken to mitigate these behaviors.

Knowing that nonhuman primates can be infected by many human respiratory pathogens and that great apes are likely susceptible to SARS‐CoV‐2, it is important to consider the ways in which transmission of these agents might occur (Melin et al., 2020). Airborne transmission and direct contact are modes of reverse zoonotic disease transmission (Epstein & Price, 2009). However, infection through fomites and the environment could also occur as has been suggested by other ape researchers (Gilardi et al., 2005). Some pathogens can remain viable for days after they are deposited into the environment (Baek et al., 2020; Chan et al., 2011; Edemekong & Huang, 2019; Kampf et al., 2020), which could facilitate transmission to chimpanzees long after infected people depart. Patrono et al. (2018) suggested that human coronavirus OC43 in wild chimpanzees in Cote d'Ivore may have been inadvertently introduced into the forest via asymptomatic shedding, which highlights this risk for coronavirus. As a result of the SARS‐CoV‐2 pandemic, new guidelines are being implemented to protect apes in Uganda (IPS, 2020). These include mandatory face masks for visitors and park staff, handwashing/sanitation facilities at the entrances of all its premises and protected areas, temperature checks for tourists, and maintenance of at least a 10‐meter distance from chimpanzees during visits (UWA, 2020). More effectively framed communications from the guides to tourists may also help promote safe tourists behaviors as they did in a study of mountain gorillas in Uganda (Gessa & Rothman, 2016). We hope that the results presented herein will enhance the comprehensiveness of these guidelines.

We note certain limitations to this study. Specifically, observations were recorded at only one tourism site in one country over a short period of time, such that their generality to other settings and seasons remains to be seen. Also, no biological samples were collected to document actual instances of infection. Nevertheless, to the extent that our findings from Kanyanchu prove representative of other great ape tourism sites, we suggest that future guidelines for ape tourism take into consideration the behavioral propensities of individual tourists, and actively discourage these high‐risk behaviors.

ACKNOWLEDGMENTS

We thank the Uganda Wildlife Authority staff at Kanyanchu and Kanyawara for logistical support. The Animal Behavior and Conservation Program at Hunter College of the City University of New York for funding and support as well as NSF 1521528 to JMR. We thank the Uganda Wildlife Authority and the Uganda National Council of Science and Technology for permission to conduct this study.

Glasser DB, Goldberg TL, Guma N, et al. Opportunities for respiratory disease transmission from people to chimpanzees at an East African tourism site. Am J Primatol. 2021;83:e23228 10.1002/ajp.23228

DATA AVAILABILITY STATEMENT

The data that support the findings of this study are available from the corresponding author upon reasonable request.

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Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Data Availability Statement

The data that support the findings of this study are available from the corresponding author upon reasonable request.

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