Cute but deadly? (Image: Natural Visions/Alamy)

Most would choose the cuddly gerbil over the much-maligned rat. But the latter’s bad reputation may not be fully deserved. Central Asian rodents, not rats, prospering under warm variations in climate, could have been to blame for the arrival of the Black Death in Europe in 1347 and for repeated outbreaks of plague over the next four centuries that killed millions of people.

The plague is caused by the Yersinia pestis bacterium, which is carried by fleas and mostly affects rodents. Plague has hit Europe a number of times, but the second pandemic – the one that caused the Black Death – remains the most notorious today. Believed to have originally come to Europe from Asia via the Silk Road trading route, it was thought that the repeated plague outbreaks that followed the Black Death epidemic were caused by rodent reservoirs in Europe – bacteria-infested fleas hiding out in rats.

But Nils Christian Stenseth at the University of Oslo, Norway, and colleagues say that instead of rats, it is their furry counterparts in central Asia that are to blame. The team analysed 4119 historical records of post-Black Death plague outbreaks and found that the vast majority were probably caused by similar outbreaks nearby. But they were able to identify 61 outbreaks that took place in 17 harbour areas, including London, Hamburg, Barcelona and Dubrovnik, that were likely to have been caused by maritime imports from Asia.


By comparing these cases with historical records, Stenseth’s team were able to identify 16 years within the period from 1346 to 1837 in which brand new introductions of Y. pestis are likely to have been responsible for plague outbreaks, as opposed to infection from neighbouring regions or local trade partners.

Feeling the heat

When they compared the dates of these outbreaks with tree ring data, they did not find a correlation with European climate patterns. However, climate fluctuations in Asia – above average temperatures followed by sudden drops – consistently preceded plague reintroductions in Europe by around 15 years. In other words, the new plague outbreaks were linked to Asian rodents, not rats living in Europe, as had been thought.

“Warmer climate increases the activity of fleas and their ability to spread the bacterium from individual to individual,” says Stenseth. “We have previously shown that an increase of 1 °C doubles the prevalence [of plague] in wild rodents in central Asia.”

Under such conditions, not only do the fleas become more active, but the rodents they live on – most likely gerbils and marmots – become more numerous. When the temperature suddenly falls again, as indicated by a change in the thickness of tree rings, rodent populations crash, and their fleas are forced to find new hosts – perhaps camels, perhaps humans.

“The study is interesting and convincing,” says Hartmut Dunkelberg of the University of Goettingen in Germany. “Climate influences different factors such as the development of fleas and the distribution of plague reservoirs. Many human infections are seasonal.”

Stenseth’s team believe the 15-year time lag between such crashes and the introduction of new plague-ridden fleas to Europe comprised three stages: a couple of years finding new hosts and coming into contact with humans, around 10 years travelling westward along trade routes such as the Silk Road, and finally the plague’s reintroduction to Europe via marine trading harbours.

Camel ride

The long, middle stage across central Asia may have involved camels, says Stenseth, who could have caught fleas from gerbils and passed them on to humans.

This explanation for where fresh European plague outbreaks came from explains how countries like Norway, which did not have rat populations at the time, could have suffered repeated outbreaks.

Today, climate fluctuations are likely to affect wildlife plague reservoirs in different ways, depending on their location, says Stenseth. “In central Asia and northern China, the current climate change is likely to increase the occurrence of plague, whereas in the southern part of China it is likely to decrease.”

Dunkelberg says that individual cases of plague could occur in Europe, but that outbreaks would be unlikely. “I cannot see any greater risk of an epidemic outbreak.”

Journal reference: PNAS, DOI: 10.1073/pnas.1412887112