There was something wrong with the chimpanzees. For weeks, a community of 205 animals in Uganda’s Kibale National Park had been coughing, sneezing and looking generally miserable. But no one could say for sure what ailed them, even as the animals began to die.Necropsies can help to identify a cause of death, but normally, the bodies of chimps that succumb to disease are found long after decomposition has set in, if at all. So when Tony Goldberg, a US wildlife epidemiologist visiting Kibale, got word that an adult female named Stella had been found freshly dead, Goldberg knew this was a rare opportunity to look for an answer.Goldberg and two Ugandan veterinary colleagues drove for two hours to a remote part of the park, then lugged their gear for another hour by foot through the hilly, forested terrain to where Stella’s body lay in the underbrush. They lifted the 45-kilogram animal onto a tarpaulin, and got to work. As they crouched over the chimp, sweat pooled beneath their full-body protective suits and their goggles fogged in the humid air. They meticulously worked their way through Stella’s organ systems, collecting samples and recording data on visible pathology. Not knowing what had killed her was “unnerving”, Goldberg recalls. “It could have been Ebola.”As the necropsy progressed, however, Goldberg began to see telltale signs of a familiar disease: fluid build-up in Stella’s chest cavity and around her heart. Lung tissue that was dark red, consolidated and marked with lesions. It looked, in other words, like the chimp had died of severe pneumonia.Months later, molecular testing revealed the culprit behind the outbreak: human metapneumovirus, which causes run-of-the-mill respiratory infections in people but is “a well-known killer” in our closest primate relatives, says Goldberg, a researcher at the University of Wisconsin–Madison. More than 12% of the community that Stella belonged to ended up dying in the outbreak, which occurred in 2017. More animals were indirectly lost as a result of being orphaned1. “Stella had a baby that was clinging to her body for a while after she died,” Goldberg says. “The baby subsequently died.”
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This phenomenon of animals catching diseases from humans, called reverse zoonoses, affects species around the world — from mussels contaminated with hepatitis A virus and cheetahs that come down with influenza A, to the parasite Giardia duodenalis passed on to African painted dogs (Lycaon pictus) and tuberculosis transmitted to Asian elephants2. But because of their evolutionary closeness to humans, great apes tend to be most vulnerable to our diseases. “We share over 98% of our genetic material with gorillas and chimpanzees, so we can easily make them sick,” says Gladys Kalema-Zikusoka, a wildlife veterinarian and founder of Conservation Through Public Health, a non-profit group in Entebbe, Uganda, dedicated to promoting the coexistence of people and animals.For some great ape populations that live in protected areas, reverse zoonoses are an even bigger threat than habitat loss or poaching. This is the case for most, if not all, of the chimp communities in Kibale. In a group at Kanyawara, for example, respiratory pathogens such as human rhinovirus C and human metapneumovirus have been the leading chimp killers for more than 35 years, accounting for almost 59% of deaths from a known cause3. Despite the seriousness of this problem across Africa, Goldberg says, it’s hardly studied compared with other conservation issues, and public awareness is likewise scant.Goldberg was shaken by what he saw at Kibale, and decided he would focus on finding ways to reduce the risk of such outbreaks happening in the future. He was concerned for the chimps, an endangered species, but more than that, he was perplexed by the lack of epidemiological understanding of how, exactly, wild animals contract human diseases. This insight, he knew, is needed to develop effective solutions. “I realized this is not just something that happens now and then,” he says. “It’s a major problem and we should formalize the study of it.”
Tony Goldberg puts on protective gear to conduct a necropsy of a dead chimpanzee.Credit: Ronan Donovan
Many other scientists and conservationists agree that human diseases pose one of the greatest risks to African great apes today — and there are a few efforts under way to use a research-based approach to mitigate this problem. After a nearly decade-long hiatus, for example, the International Union for Conservation of Nature (IUCN) is releasing its latest disease-prevention guidelines for great ape tourism. And last July, a working group that aims to bring together scientists, conservationists, community developers, tour operators and government officials in Uganda met to talk about better enforcement of responsible tourism practices and standardization of educational content for tourists.There still is a need, however, for all parties — including scientists — to pay much more attention to this issue, says Fabian Leendertz, director of the Helmholtz Institute for One Health in Greifswald, Germany. “The more concrete evidence we have about how transmission happens and where the risk factors are, the better and sharper the hygiene measures that we take can be,” he says. “This would also make the arguments stronger to convince tour operators and other stakeholders to adhere to those guidelines.”Public health for primates Most people who have heard of reverse zoonoses have probably done so in the context of the coronavirus SARS-CoV-2, which humans have transmitted to a panoply of species, from pets to exotic zoo animals. Most recently, SARS-CoV-2 has spread into white-tailed deer (Odocoileus virginianus) across North America, providing the virus with a new wild reservoir4. “The nightmare scenario is deer-vid emerging as a new variant,” Goldberg says.Long before people heard about tigers and mink coming down with COVID-19, however, researchers were observing the same phenomenon happening with different human diseases in dozens of captive and wild species. Some of the first records in great apes were made by British primatologist Jane Goodall, who in 1966 recorded ten chimps who seemed to have contracted poliovirus after an outbreak in a nearby human community. In her 1986 book, The Chimpanzees of Gombe, Goodall also noted that chimps “quite often” had colds and coughs, and “with very few exceptions they can contract the same contagious diseases as humans”. To Goodall’s heartbreak, David Graybeard — the first chimp to befriend her, and her favourite — succumbed to one such respiratory outbreak in 1968.Goodall suspected that the chimps were being made unwell by people. But evidence of this didn’t arrive until 2008, when Leendertz and his colleagues used molecular tools to show that human viruses were to blame for a decade’s worth of major respiratory disease outbreaks in chimps in Taï National Park, Côte d’Ivoire5. The paper was a wake-up call, Leendertz says. Although zoo keepers and field conservationists had long been aware anecdotally of the threat that human pathogens pose to great apes, many government officials and tour operators “wouldn’t listen to all the warnings until we published the scientific evidence”, he says.In the years since the paper came out, habitat destruction, human encroachment, climate change and globalization have only accelerated, and all of Africa’s great ape species are now decreasing. Eastern and western gorillas are both critically endangered, while chimpanzees and bonobos are endangered. The fact that human diseases can take out significant proportions of great ape communities makes the pathogens a dire threat to all four species, in particular. “Great ape populations can’t afford these sorts of losses,” Goldberg says. “Their populations are already so small, fragmented and declining that they just don’t have the ability to rebound or adapt.”
An aerial photograph of Kibale National Park in western Uganda shows the border between intact forest and agricultural fields, which have encroached on and shrunk the habitat for chimpanzees in the park.Credit: Ronan Donovan
In a 2018 literature review, researchers documented 33 probable or confirmed pathogen transmission events from humans to chimpanzees or mountain gorillas (Gorilla beringei beringei), a subspecies of eastern gorilla with only around 1,000 individuals. Those events included deadly cases of measles, human metapneumovirus and the bacterium Streptococcus pneumoniae6.Many of the pathogens cause infections that, in a person, would result in an annoying but mild cold. In great apes, however, these diseases can be deadly, because the animals have no immunity or evolved genetic resistance. Once a chimpanzee or gorilla becomes unwell, there is usually little that can be done to help. There is also no vaccine for most common cold viruses.What could work, Goldberg realized, was a public-health approach: finding the source of pathogens and preventing them from getting into the populations in the first place.Perverse incentives A Facebook post this year summed up the problem all too well. One day in October, Taylor Weary, an epidemiologist who recently graduated from Goldberg’s lab and a soon-to-be veterinarian, examined a photograph that had been shared by a 30-something man after his visit to Kibale. He is in the forest, grinning with his mask pulled down, squatting a metre or two in front of a chimp.Seeing the photo, Weary sighs: “This is really illustrative of what not to do.”In 2015, the IUCN released guidelines for great ape tourism, which recommended that people stay at least 7 metres away from the animals and that tour groups limit their size and exclude people who feel unwell. The guidelines also specified that all visitors wear face masks. Although these rules are clear on paper, they can only reduce disease risk if they are actually enforced by guides and followed by tourists on the ground.
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There are obvious reasons why that doesn’t always happen. For one, counting on all international visitors to be honest about whether they’re feeling unwell before their trek is not realistic. “Imagine you’re an American tourist, you’ve gone all the way to Africa, and this is your bucket-list trip,” Goldberg says. “Now you’ve got a stomach ache — and you’re not going to go see the gorillas? Of course you are.”Like the person in the Facebook post, tourists also break rules while out in the field, either because of excitement in the moment or owing to wilful disregard. “Some tourists just don’t listen,” Kalema-Zikusoka says — and their African guides might or might not correct them. “They don’t want to be rude, and they find it hard to manage tourists sometimes.”Guides might also refrain from reproaching visitors for fear of losing a potential tip. Some guides “get tips that are twice the monthly salary of typical villagers in the area”, Goldberg says. “There’s all these perverse incentives.”In a 2020 study, Kalema-Zikusoka and her colleagues observed 53 gorilla treks at Uganda’s Bwindi Impenetrable National Park, and found that the 7-metre rule was violated on almost every occasion, with tourists sometimes getting within 3 metres of the animals7. Another 2020 study that analysed 282 YouTube videos of mountain gorilla tourism found that 40% depicted humans within arm’s reach of gorillas or engaging in physical contact with the animals8.In a third 2020 study, Darcey Glasser, then a graduate student at Hunter College of the City University of New York, joined 101 chimp treks at Kibale. Groups often merged, growing from the six-person limit to an average of 18 individuals crowded around one or several chimps9. Glasser observed tourists coughing during 88% of excursions; sneezing in 65%; urinating in 37%; eating in 17%; and spitting in 13% (see ‘Passing on pathogens’). She also found that tourists touched trees an average of 230 times per excursion. “Everyone’s touching everything,” she says. Whereas all this might seem innocent, such behaviours can inadvertently create fomites — inanimate objects that carry infectious agents. Fomites sprinkled along forest paths might represent an important but overlooked source of infection for great apes.
Source: Ref. 9
Glasser presented her findings to wildlife officials in Uganda, who responded encouragingly, she says, by adding hand-sanitizing stations at the start of trails. In general, however, officials tend to avoid imposing strict rules that they think might impact visitors’ experiences. Mask wearing is a good example, Goldberg says. Although masks were recommended in the IUCN guidelines in 2015, “for years before COVID-19, it was an epic battle to try to convince people in ape-range countries to mandate wearing face masks”.Officials at the Uganda Wildlife Authority, which oversees the country’s national parks and all tourism activity in them, did not respond to Nature’s e-mails, texts or phone calls requesting an interview for this article. Great ape tourism is a key source of revenue for the 13 African countries where it occurs, Leendertz says, so reverse zoonosis is “not always an easy topic, because they’re afraid of losing tourists”.Early this year, the existing IUCN tourism guidelines will be republished with a post-pandemic addendum that is meant to reduce the risk of SARS-CoV-2 finding its way into wild great ape populations and, potentially, into other species. “If a great ape dies of SARS-CoV-2 and a leopard finds it, it could cause a circulation in wildlife,” says Leendertz, who is one of the co-authors of the guidelines. Not surprisingly, the addendum provides a stronger emphasis on mask wearing — something that previously reluctant tourism authorities have begun to enforce since the COVID-19 pandemic, Leendertz says.Hidden transmission Ecotourism represents one serious disease risk for great apes, but it cannot account for all cases of reverse zoonoses. Some great ape populations never see a tour group — Stella’s community among them — yet they still experience deadly outbreaks of human pathogens.Scientists are another possible culprit, but there are relatively few in the field and they usually follow strict biosecurity measures, including quarantining after arriving at the station, health screening before entering the forest, always wearing masks in the field and keeping a certain distance from any animals they encounter. “People have an impression of this research based on things they’ve seen from old Jane Goodall photo shoots,” says Melissa Emery Thompson, an anthropologist at the University of New Mexico in Albuquerque and co-director of the Kibale Chimpanzee Project. “But there’s absolutely no contact that happens with any great ape research in the wild.”
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As Goldberg thought about how to tackle this problem, he noticed a perplexing pattern in the list of human pathogens that typically afflict great apes: they’re also those that are the bane of primary schools worldwide. They’re the infections that, like clockwork, young children catch when they go back to school, and then bring home. “These viruses live in kids, but kids have parents, and kids are always transmitting the viruses to parents and adult companions,” Goldberg says.Great apes, it occurred to him, could be catching diseases from adults who go into the forest after catching pathogens from their children. The idea seemed even more plausible when Goldberg realized that adults infected with these “sniffle germs” often show no symptoms, even as they shed copious viral particles.It was a compelling hypothesis, but it needed to be tested. So Goldberg secured a grant to recruit Weary as the graduate student leading the investigation. From 2019 to 2021, she and Patrick Tusiime, the health coordinator for the Kasiisi Project, a non-profit group that supports primary schools around Kibale, began collecting monthly nasal swabs of 203 children enrolled at 3 primary schools near the national park. Thirty-one were children of adults who worked in the forest, who also had their noses swabbed during the testing. The team collected faecal samples from 55 chimps to test for human pathogens, and combined these data with observations about the animals’ health from chimp trackers: specialized field assistants who are employed by the Kibale Chimpanzee Project to collect daily health and behavioural data for an ongoing, 35-year-long monitoring project.The findings, which are currently in review for publication, confirmed Goldberg’s original hypothesis about the link between ill children, asymptomatic adults and reverse zoonoses in chimps. Every respiratory pathogen that has caused a chimp outbreak in Kibale was present in children living nearby. They were 3.5 times more likely than adults to be symptomatic, but their infections tracked with those of both their parents and the chimps. Respiratory outbreaks occurred in chimps in October 2019 and January 2020, but during Uganda’s most stringent COVID-19 pandemic lockdown between March and September 2020, the researchers observed an “extraordinarily clear” drop in infections across the board, Goldberg says, suggesting that schools are indeed a major source of transmission.The message, Goldberg says, was clear: “To save the chimps, we have to make kids healthier.”Catalysing change One big takeaway from the findings was that the current model is inadequate to reduce the risk of reverse zoonoses in Kibale’s chimpanzees, and also probably in great apes in Africa as a whole. It hinges on stopping symptomatic people from going into the forest, but infected adults are usually asymptomatic. Simply updating this policy to forbid guides and trackers from going to work whenever their children are ill isn’t a solution, Goldberg says, because kids being kids, they “are sick all the time”.Banning tourism also wouldn’t work. Parks depend on visitor fees to pay salaries, maintain local support for conservation and justify the cost of setting land aside for wildlife. “When I was growing up, the perception was that chimps are bad,” says Tusiime, who was born in a rural village near Kibale. “Now there’s a shift to a positive attitude towards chimpanzees because they bring in tourists, they bring in revenue.”
Contact between people and chimpanzees has led to problems in Uganda. This home was abandoned after chimps killed a child living there.Credit: Ronan Donovan
Tourism is necessary for conservation, Kalema-Zikusoka adds, “but it needs to be done carefully, otherwise we won’t have these animals around”.Abiding by existing biosecurity rules for rangers, guides and tourists would probably go a long way to reducing reverse zoonoses. Enforcement is complex, however, and working out how to do it well “will require a more focused effort of experts and African governments coming together and making decisions that are good for the apes and good for tourism”, says Cristina Gomes, a wildlife conservationist at Florida International University in Miami who helped to launch the working group that met last July to identify creative ways to implement best practices for wildlife tourism in Uganda. The group plans to seek funding to hold a workshop series with government officials, rangers and tour operators, and to make educational videos to standardize explanations and instructions that tourists receive before going into the field.One idea the group supports, for example, is to entitle guides who work with chimps to paid sick days — a luxury most currently do not have. Another suggestion is to create an accreditation programme that certifies companies that follow best practices, justifying a slightly higher fee for their services. “If we could reward tourism companies for caring, I think that’s a way to incentivize change,” Weary says.Teaching children and adults who live near great apes about how microbial transmission works, and then empowering them with the resources to put that knowledge to use, is also a promising path forward, she adds. Some of this is already happening as a direct result of the team’s research. They found, for example, that children enrolled at one of the three rural primary schools in the project stood out for their high rates of infection. That school turned out to be the most unhygienic, with up to 76 children crowded into a single, dirt-floored classroom. When Weary and Tusiime presented this finding to the district health office, officials responded by building extra classrooms and covering the floors with cement. The Kasiisi Project is installing hand-washing facilities at schools around Kibale and arranging educational programmes to teach children simple ways to reduce viral transmission, such as sneezing into their arm rather than their hands.A new initiative called Healthy Children, Healthy Apes is also being implemented by different teams at three further sites in Uganda to see whether the findings from Kibale apply to other places where chimps and gorillas live.Some early results suggest they do. Last October, in Goldberg’s fluorescent-lit laboratory in Wisconsin, a next-generation DNA deep sequencer used for virus hunting beeped to life, ready to process a batch of nasal swab samples collected from this latest phase of the project. So far, the analysis has confirmed that the same common cold viruses found in children at Kibale and worldwide occur in children who live near other field sites around Uganda. “There’s very good reason to believe we can extrapolate to all sub-Saharan African great ape sites that have been plagued by respiratory disease,” says Weary.Tusiime, visiting from Uganda, was present in Madison to witness the latest phase of the project. He’d joined Goldberg and the team for a month to gain a deeper understanding of the analytical work and build relationships with colleagues over plates of fried cheese curds. Insight from the US side of the project will be invaluable, he says, for liaising back home with project participants, institutional review boards and officials. “Hopefully I can advocate for us to have this equipment in Uganda so we can do these tests there in the future,” he says. “It’s very relevant to our community.”Reverse zoonoses can never be completely prevented. Common cold viruses cannot be eradicated, and people and great apes won’t be staying apart any time soon. Testifying to this, Goldberg says, outbreaks of respiratory disease were documented in chimps in at least five locations throughout sub-Saharan Africa in 2023 alone.The hope, however, is that incidents such as these will become rarer as scientists, officials, rural residents and tourists gain a deeper understanding and awareness of the problem. “Behavioural change takes time, but if you’re committed, it eventually happens,” Tusiime says. “So we need to start now.” More
