Dozens of previously undocumented wild species—including some known to be susceptible to SARS-CoV-2—were on sale at markets across Wuhan in the months leading up to the pandemic, a new study shows.

As researchers across the world call for a careful investigation into the origins of the pandemic, the findings add more clarity into how SARS-CoV-2 might have jumped from a wild population of animals into humans.

“This report clearly places [SARS-CoV-2] susceptible animals smack in the middle of Wuhan,” says Robert Garry, a virologist at Tulane University who has written about the origins of the COVID-19, but was not involved in the research.

From early in the pandemic, virologists suspected that animals traded at wet markets in Wuhan—one of China’s biggest transit hubs—had carried SARS-CoV-2. Although the term “wet market” has been exoticized, it basically refers to something like a large farmers market, where individual vendors sell fresh fish, produce, and meat. In some instances, vendors will deal—legally or otherwise—in live wild animals, though that’s by no means the rule.

But those wild animals are often the sources of new diseases. SARS, the earlier cousin of SARS-CoV-2, originated in bats, then spilled into masked palm civets. Some of those civets were sold in markets in Guangdong province, where the disease then made the leap to humans. In the case of other diseases, like Ebola, scientists have never fully determined the animal reservoir.

Many of the earliest cases of COVID-19 in January of 2020 were traced back to a location called the Huanan seafood market, but a subsequent investigation by the World Health Organization documented links to several other Wuhan markets. Other patients had no contact at all with the markets. Still, the presence of SARS-CoV-2 in swabs taken from surfaces at the Huanan market suggested that it had played a role as a super-spreader location.

A May publication by Garry—which did not go through peer-review—argued that the genetic diversity of early COVID-19 cases indicated a spillover related to the wildlife trade. Two distinct lineages of the virus appeared at different wildlife markets, which Garry argues is best explained by an animal-to-human spillover further up the supply chain.

[Related: The virus that causes COVID-19 has been silently brewing in bats for decades]

The new study of wildlife sales, published this week in Scientific Reports, came out of a survey from May 2017 to November 2019. The research team, which included scientists from China, Canada, and the UK, was actually hunting for the source of a tick-borne illness that had caused a deadly outbreak in the Wuhan area 2009 and 2010.

Over the course of the survey, the lead author conducted monthly interviews with vendors at 17 shops across four markets, documenting 47,381 individual animals from 38 different species. Two of those species, civets and raccoon dogs (an East Asian canine most closely related to foxes), are suspected vectors for SARS-CoV-2. Vendors also sold mink, which both harbor and transmit the virus. Over the course of the pandemic, SARS-CoV-2 has killed thousands of farmed minks in nine countries, including the United States. In Denmark, outbreaks on mink farms ended up jumping back into humans.

A third of the mammals the researchers examined showed signs of having been illegally caught in the wild, and “almost all animals were sold alive, caged, stacked and in poor condition,” a recipe for the exchange of infectious diseases.

The new report notes that many of the animals were priced as luxury goods: $70 per kilogram for a sharp-nosed pit viper and $25 per kilogram for a Himalayan marmot (about $30 and $11 per pound, respectively).

Bats and pangolins were not for sale, however. That’s important because horseshoe bats are known to harbor coronaviruses, while pangolins were briefly suspected to be an intermediate host. This survey of wildlife markets further suggests that neither animal was involved in the Wuhan outbreak.

Researchers still suspect that bats were the original hosts of the virus, as they were for SARS-1, even if they didn’t directly infect people in Wuhan. A new study published Wednesday in Cell documented four coronaviruses in Southern China that were about 95 percent genetically identical to SARS-CoV-2.

Vendors were transparent with researchers about illegally dealing in animals. Of the 38 species documented, 31 were protected, and none of the 17 shops posted required documentation on the animals. “Vendors freely disclosed a variety of protected species on sale illegally in their shops,” the authors write, “therefore they would not benefit from specifically concealing pangolin trade or the trade in any particular species, and so we are confident this list is complete.”

That transparency means the study could be a key piece in determining the origins of SARS-CoV-2. The Chinese government closed the Huanan market on January 1, and by the time the World Health Organization’s investigators arrived in Wuhan in January of 2021, the wares had been cleared out.

The findings of the WHO investigation have been criticized for being too quick to rule out lab involvement in the origins of SARS-CoV-2. But it’s now clear that the investigation also didn’t get a full picture of Wuhan’s wildlife trade. By their own account, the investigators only interviewed two vendors at the Huanan market.

“It means that the WHO report is incorrect about which animals were for sale at the Huanan market and other wet markets in Wuhan,” Garry says. He also points out that the findings appear to contradict more recent Chinese government assertions that the virus was related to frozen fish sales.
The findings also provide a roadmap for further investigations of SARS-CoV-2’s origins, although the prospects for international cooperation have been muddied by political posturing. As Eddie Holmes, an Australian virologist who studies emerging diseases, told the Guardian in May, “The key step is to determine what animals, particularly mammals, were present in the market between August to December 2019. … Once these animals are identified, their sources — farms, traders and even wild source locations — need to be traced and all animals at those locations tested using a variety of approaches.”