Before the coronavirus pandemic shut down Wuhan’s wildlife markets in 2020, it was common to see dozens of species and hundreds of wild animals crammed into cages, stacked one on top of the other.

A walk through the Huanan Wholesale Seafood Market revealed king rat snakes (Elaphe carinata), bamboo rats (Rhizomys sinensis), Amur hedgehogs (Erinaceus amurensis), raccoon dogs (Nyctereutes procyonoides) and hog badgers (Arctonyx albogularis) peering out from wire and glass cages. Marmots (Marmota himalayana), sold for food, commanded more than $25 per kilogram ($11 per pound). Hedgehogs cost just $2 per kilo (90 cents a pound). All held the possibility of being a vector for zoonotic disease.

Between May 2017 and November 2019 — the point at which the SARS-CoV-2 virus is presumed to have spilled over into humans from an unknown animal host — more than 47,000 individual animals, including 31 protected species, were sold in Wuhan’s markets. Multiply that by the uncounted wildlife markets across Asia, Africa, Latin America and elsewhere, and the scale of risk to humanity becomes clear.

But although almost 90% of the 180 recognized RNA viruses that can harm humans are zoonotic in origin, meaning they come from a nonhuman animal, disease surveillance of the world’s wildlife markets and trade is largely absent, according to experts.

There is no internationally recognized standard for managing the legal wildlife trade based on disease risk, and no global pathogen screening measures are currently in place for wildlife or products consumed as food or transported around the world. Multilateral treaties like CITES do regulate the international trade in endangered plants and animals to safeguard imperiled species, but few equivalent regulations exist to protect human health, and only a handful of countries exercise strict veterinary import controls over wildlife.

In response, scientists around the world are now calling for increased biosurveillance and regulation of the world’s wildlife markets and wildlife trade to prevent future zoonotic spillover events and pandemics. Failure to act now could be catastrophic to humanity.

Bringing biosurveillance to biodiversity hotspots

Following a series of zoonotic spillovers linked to bats — Nipah, SARS, MERS, Hendra and Ebola — researchers monitored a single cave in southwest China for four years. Their work turned up 11 novel coronaviruses. Subsequently, between 2015 and 2017, 0.6% of rural residents in the provinces of Yunnan, Guangxi and Guangdong in southern China tested positive for prior bat coronavirus antibodies, indicating close interaction between species.

This and other evidence has caused scientists with the Wildlife Disease Surveillance Focus Group to urge that countries significantly ramp up wildlife testing in areas with a high risk of emerging infectious diseases and implement advanced screening technology. The focus group is composed of experts from the University of Edinburgh, University of Melbourne, the Natural History Museum of Vienna, the San Diego Zoo Wildlife Alliance, and Washington University in Saint Louis.

But such careful surveillance will require bold new financial, political and systems development commitments. There are currently just 125 reference laboratories around the world certified to screen for one or more target animal pathogens. However, these labs don’t conduct sweeping surveys of potential pathogens, and the distribution of the facilities doesn’t reflect the realities of disease risk: more than half are concentrated in Europe and North America, while Southeast Asia, Africa, and Central and South America pose a much higher risk of being the source of emerging infectious zoonotic diseases.

“There are places with incredible biodiversity where you have many potential targets for diseases to jump from one species to another,” explains Mrinalini Erkenswick Watsa, a researcher with the San Diego Zoo Wildlife Alliance and a focus group member. But there are few labs located at these critical human-wildlife interfaces to screen for pathogens, creating a serious biosurveillance bottleneck.

There is evidence that centralized surveillance facilities can yield good results, asserts the focus group. For example, PREDICT, a project of USAID’s Emerging Pandemic Threats program, was launched in 2009 with the aim of serving as an early-warning system for zoonotic spillover. Researchers ultimately screened 164,000 animals and humans and detected 949 novel viruses in zoonotic hotspots across 30 countries.

But the world’s epidemiological labs are also subject to political whims. In late 2019, the Trump administration ended federal funding for PREDICT.

“We need to do more broad-scale surveillance,” says Watsa. “It cannot only be left in the hands of governments because governments are political and funding is tied to that.”

Watsa and her colleagues argue that the first step must be to establish a cost-effective, decentralized disease biosurveillance system that would allow public health professionals and wildlife scientists in remote areas, especially near booming wildlife markets, to test for pathogens year-round, at source, with modern mobile technologies that allow for whole genome sequencing, metagenomic analysis, and metabarcoding of pathogens. As things stand, restricting these activities to a few central labs impedes global surveillance efforts, possibly delaying rapid response to a spillover event.

This year, Watsa, working with the San Diego Zoo Wildlife Alliance and the Amazon Conservation Association, along with other partners, established an in situ laboratory at Los Amigos Biological Station in southeastern Peru. The Biosafety Level 2 lab will screen animals in the surrounding rainforest for viruses and parasites to establish a general picture of which kinds of pathogens and parasites are present in different species. The facility has already taken samples from nearly 1,000 mark and recapture animals, including primates, bats and frogs. Scientists will use this information to develop rapid tests for targeted infectious diseases that can then be used to screen wildlife far away from a lab (in wildlife markets, for example), in hopes of generating a faster global response to potential spillover events.

This approach, Watsa says, is more proactive than updating international regulations or creating new treaties, which takes significant time. “This is something we can do right now to make [markets] safer for people consuming food and safer for wildlife.”

Monitoring the global legal wildlife trade

Even with stricter surveillance of wildlife markets, the spread of pathogens could still evade detection, say some experts, partly due to the illegal wildlife trade which sees millions of animals trafficked across international borders annually. Of 17 shops inspected at the Wuhan wet market, for example, none posted origin or quarantine certificates, indicating some animals were potentially there illegally. Indeed, in the months following the coronavirus outbreak, environmental groups pointed a finger at the illegal trade, estimated to be worth as much as $23 billion, and its associated spillover risks.

But importantly, scientists argue that the legal wildlife trade poses a far greater risk to humanity. “Even though we only see a small part of the illegal wildlife trade, the legal wildlife trade is substantially larger by at least [three] orders of magnitude,” says Vincent Nijman, an anthropologist at Oxford Brookes University who studies the wildlife trade.

One significant surveillance gap within the legal trade: Shipments often aren’t properly inspected. Instead, border agents, often lacking in sufficient numbers and in technical training, conduct superficial sweeps of declared goods to ensure that cargo descriptions match contents — that a spiny softshell turtle (Apalone spinifera) isn’t actually a vulnerable Chinese softshell turtle (Pelodiscus sinensis), for example. But such inspections only capture about 10% of the trade, says Nijman, and possible infection in a transported species is rarely monitored.

“Most countries have health and quarantine facilities at ports of entry, but not all of these are effective,” confirms Chris Shepherd, executive director of Monitor, a wildlife trade-focused nonprofit. Moreover, many animals never cross international borders; they’re hunted in the wild and moved within a country’s boundaries. “The legal trade is considered low risk and so some countries don’t take these issues very seriously,” Shepherd says. As a result, zoonotic disease spillover and spread can become well established inside a country before being identified — with the rest of the world a mere airplane flight away.

At market, animals are kept in conditions Shepherd describes as “horrific.” Cages, containing a myriad of species are typically piled high, with the animals in the bottom row covered in feces and other body excretions that could carry disease. Some animals are sold as pets, others for food. “In the open meat markets, like in Myanmar, Cambodia, or Laos, the hygienic conditions are terrifying. There are not effective measures in place to ensure these places aren’t hubs of disease,” Shepherd says. “These markets are a ticking time bomb.”

Gaps in sanitation, inspection and surveillance have left the door wide open for future zoonotic spillover events. “Parasites and diseases don’t read documents — they don’t care if something is traded legally or illegally,” says Nijman, who adds that “Where we’ve gone in the wrong direction is focusing entirely on the illegal trade in wild animals. We can make massive [public health] gains by looking at the legal trade and scaling up inspections.”

Rapidly assessing risky business

Earlier this year, researchers working with WWF and universities in Hong Kong released a rapid risk assessment tool for use in wildlife markets in the Asia-Pacific region in hopes of improving on-the-ground monitoring as countries work toward broader regulatory treaties.

“A complete shutdown [of the legal wildlife trade] would be ideal, but it’s not realistic,” explains Eric Wikramanayake of WWF’s Asia-Pacific Counter-Illegal Wildlife Trade Hub and the paper’s lead author. “There are so many wildlife markets, ranging from small villages to wildlife restaurants to large urban markets, and some communities are dependent on wildlife products for nutrition.”

Though there’s a push for better hygiene in markets — separating animals and increasing hand-washing by butchers — sanitation improvements can only marginally reduce spillover risk. “All wildlife carry some kind of virus or bacteria or pathogen, but some are more virulent than others,” explains Wikramanayake. In other words, if high disease-risk taxa are being traded, it doesn’t matter how clean someone’s hands are. Monitoring is vital.

The new assessment tool, a risk matrix, will help government authorities in public health and wildlife sectors assess markets and trade situations for zoonotic disease risk, based on the kind of trade and the particular wildlife taxa available for sale.

Wikramanayake and his colleagues first established 11 generalized trade situations, determined by three variables: transmission risk, spread potential, and zoonotic virus risk. These variables rely on elements such as market size, hygiene, animal stress, the turnover of people moving through a market, and how far buyers might travel after visiting a market. Each scenario is given a qualitative score representing risk.

Next, the team ranked disease risk from different taxonomic groups. Recent studies have found that just 26.5% of mammal species in the wildlife trade host three-quarters of known zoonotic viruses. Because we know that HIV originated in nonhuman primates, and Ebola came from bats, these groups — along with small rodents, pangolins, Viverridae (civets and mongooses), wild birds, and Mustelidae (weasels and badgers) — are deemed to be in the high-risk category, while reptiles, fish, amphibians and elephants are considered low risk.

Trade situations and taxonomic risk are then combined in a matrix to help officials assess the spillover risk associated with specific wildlife markets. Using these criteria, small town markets were found to be of consistently high risk, while large urban markets, like the one in Wuhan, were generally of medium risk. A primate or bat (a high-risk species) sold in a small village market (where risk is greater), would therefore be deemed one of the highest-risk scenarios for zoonotic spillover.

It’s now possible to create effective risk assessment tools like this one, Wikramanayake says, due to the rapid increase in the number of studies dealing with emerging infectious diseases. “Thirty years ago, that information would not have been available,” he says. But the 2003 SARS outbreak spurred great advancements in research on zoonotic spillover, though regulation has lagged.

Wikramanayake hopes this and other field evaluation tools can be deployed in hotspots around the globe. WWF is now working with the Association of Southeast Asian Nations (ASEAN) and the World Organisation for Animal Health to implement the new tool.

“Given the opposition to wildlife trade bans, it is more likely that more nuanced approaches will emerge that balance market risk levels with subsistence hunting and use of wildlife by rural people,” notes the OneHealth study.

An outright ban?

Not everyone agrees that shutting down the legal wildlife trade writ large is an impossible or undesirable strategy. Sue Lieberman is vice president of international policy for the Wildlife Conservation Society and previously served as chief of the U.S. Government CITES Scientific Authority. She says that increased surveillance and species-by-species restrictions aren’t sufficient.

“If you’re only screening for known viruses or only looking at the riskiest species, you’re going to miss things,” she says. “We need to look at the whole commercial trade in wildlife and ask why we should continue using [wild animals] for human consumption. The risk is just too high.”

Lieberman rejects the notion that the legal wildlife trade is meeting significant nutritional demands that can’t be easily replaced. “It is a source of food security for a small percentage of people, but it’s a non-essential luxury for many. In the markets in Wuhan, Indonesia, Kinshasa, or Brazzaville, it’s cheaper to get chicken or fish. Wildlife is a specialty item.”

In response to the COVID-19 outbreak, China temporarily banned the consumption of most wildlife for food. Then, in 2021, it cemented that decision in a new law. The government is in the process of buying out wildlife farms, though China’s new regulation contains loopholes. It doesn’t, for example, apply to wildlife used in traditional medicine. “This [ban] hasn’t affected food security — it’s not causing hunger in China,” Lieberman notes.

Indeed, some countries are taking an ambitious approach to shutting down the wildlife trade. Gabon banned the sale and consumption of bats and pangolins in March 2020. Vietnam cracked down on wildlife imports into the country and stopped the movement of wildlife between provinces. And at the end of August 2021, Hong Kong’s legislature passed a bill to consider wildlife smuggling as organized crime, meaning traffickers will now be subject to harsher penalties and authorities will be permitted to conduct in-depth investigations.

At the international level, the World Health Organization (WHO) in April asked governments to stop the trade in live wild-caught mammals. And 25 heads of government are urging the WHO to create an international pandemic treaty, albeit one to deal with vaccine rollout and prevent spillovers from escalating into pandemics. Lieberman hopes the WHO will consider greater at-source protections to prevent spillover in the first place. “For health and disease, it makes more sense to ban it all,” she says.

“Even if it’s a one in a million chance that a virus will jump from an animal to people … we believe any level of risk is not acceptable,” says Lieberman. “Look at COVID-19. Look at how many millions have died and the devastating economic losses. All wildlife are a risk.”

Citations:

Hu, B., Zeng, L., Yang, X., Ge, X., Zhang, W., Li, B., … Shi, Z. (2017). Discovery of a rich gene pool of bat SARS-related coronaviruses provides new insights into the origin of SARS coronavirus. PLOS Pathogens, 13(11), e1006698. doi:10.1371/journal.ppat.1006698

Li, H., Mendelsohn, E., Zong, C., Zhang, W., Hagan, E., Wang, N., … Daszak, P. (2019). Human-animal interactions and bat coronavirus spillover potential among rural residents in southern China. Biosafety and Health, 1(2), 84-90. doi:10.1016/j.bsheal.2019.10.004

Nijman, V. (2021). Illegal and legal wildlife trade spreads zoonotic diseases. Trends in Parasitology, 37(5), 359-360. doi:10.1016/j.pt.2021.02.001

Shivaprakash, K. N., Sen, S., Paul, S., Kiesecker, J. M., & Bawa, K. S. (2021). Mammals, wildlife trade, and the next global pandemic. Current Biology, 31(16), 3671-3677.e3. doi:10.1016/j.cub.2021.06.006

Tighter wildlife disease monitoring needed to prevent future pandemics. (2020). Veterinary Record, 187(3). doi:10.1136/vr.m2896

Watsa, M., & Wildlife Disease Surveillance Focus Group. (2020). Rigorous wildlife disease surveillance. Science, 369(6500), 145-147. doi:10.1126/science.abc0017

Wikramanayake, E., Pfeiffer, D. U., Magouras, I., Conan, A., Ziegler, S., Bonebrake, T. C., & Olson, D. (2021). A tool for rapid assessment of wildlife markets in the Asia-Pacific region for risk of future zoonotic disease outbreaks. One Health, 13, 100279. doi:10.1016/j.onehlt.2021.100279

Wikramanayake, E., Pfeiffer, D., Magouras, I., Conan, A., Ziegler, S., Bonebrake, T. C., … Olson, D. (2021). Evaluating wildlife markets for pandemic disease risk. The Lancet Planetary Health, 5(7), e400-e401. doi:10.1016/s2542-5196(21)00143-1

Xiao, X., Newman, C., Buesching, C. D., Macdonald, D. W., & Zhou, Z. (2021). Animal sales from Wuhan wet markets immediately prior to the COVID-19 pandemic. Scientific Reports, 11(1). doi:10.1038/s41598-021-91470-2

Banner image: A caged baby monkey in Jatinegara Market, East Jakarta, Indonesia. Image by Wolf Gordon Clifton/Animal People, Inc. via Flickr (CC BY-NC 2.0).

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