Plague: many European epidemics and many introductions from Central Asia

A few years ago, I stumbled across a paper whose very title blew my mind. Using archeological evidence, the authors claimed that, “Rats cannot have been intermediate hosts for Yersinia pestis during medieval plague epidemics in Northern Europe.” (You can see more about their awesome work here.) That paper was the first one to really pique my interest in the medieval plague epidemics, but it wasn’t the last:

Most people only know about the most famous plague epidemic in Europe – the Black Death – but there were actually many European plague epidemics. We know that plague didn’t originate in Europe, though. The first introduction is thought to have come from Asia. After that initial introduction, the plague might have hung out in reservoir hosts in between outbreaks in Europe. That’s what people used to think, anyways. But the reservoir host that was typically implicated was the black rat (see my previous post), and recent evidence suggests that the black rat couldn’t be responsible for many of the epidemics that occurred. So, where the heck did the plague come from in all of those epidemics?

Schmid et al. (2015) combed thousands of records of plague outbreaks in medieval towns that were near areas for which climate proxies (e.g., tree ring records) exist. The vast majority of those outbreaks occurred shortly after a neighboring town had an outbreak, which might suggest that town-to-town transmission by people is a more reasonable cause for most outbreaks than a rodent reservoir. However, some out the outbreaks didn’t follow outbreaks in neighboring towns, and they occurred in maritime towns. In those cases, plague might have been introduced into towns via ships.

But where was the plague coming from? Well, there are really only two options. The ships could be bringing in the plague from other European towns, or they could be bringing the plague from someplace else, like Asia. And interestingly, Schmid et al. (2015) found a relationship between a climate proxy in Asia (tree ring growth in juniper trees in the Karakorum mountains) and plague outbreaks that occurred ~15 years later in Europe.

Here’s what Schmid et al. (2015) hypothesize was happening in a typical plague cycle: in years that were climatically favorable, rodent populations in Central Asia boomed. Gerbils were living fast and loose, making babies and spreading fleas and plague amongst themselves. The flea populations responded to the sudden spike in host density by making lots of flea babies. So, there were lots of gerbils and lots of fleas. Then the climate shifted to something less favorable, there wasn’t enough food to go around, and the giant gerbil population crashed. That was no good for the fleas, who suddenly found themselves homeless. The fleas then had to go find different hosts – such as camels or humans – and they took the plague with them to their new hosts. (By the way, a similar thing might happen with Lyme Disease: acorn mast years might cause large mouse and tick populations, and after subsequent declines in the mouse populations, hungry ticks go looking for other hosts, including humans.)

So, you’re thinking, “Uh, yeah, so a few years after Central Asia is the Land of Plenty for gerbils, a billion hungry, plague-y fleas and go looking for other hosts in Central Asia. How does the plague repeatedly travel 4000km from Central Asia to the Black Sea to hop on a boat to Europe?” Uhhhh… good question. One hypothesis is that the plague traveled the Silk Road along with the caravans via humans and camels for ~10-12 years, eventually reaching the Black Sea. This is an area of study that people are focusing on now.

So, when the mainstream media picked this story up, they had all these witty lines about how people are all prejudiced against black rats, when really it’s the innocent-looking gerbils who are to blame for the plague. (Have you ever seen a black rat being wrongly interrogated by the authorities? It’s terrifying.)  I can’t think of anything wittier to say, but I made a cartoon of a gerbil wearing a blonde wig. You’re welcome.



Schmid, BV, U Buntgen, WR Easterday, C Ginzler, L Walloe, B Bramanti, and NC Stenseth. 2015. Climate-driven introduction of the Black Death and successive plague reintroductions into Europe. PNAS.

Plague in prairie dogs

Black-tailed prairie dogs are ground squirrels that live in the North American grasslands. Prairie dogs are important parts of grassland ecosystems because (1) their burrows are habitats for other species and (2) they are important prey for a variety of predators, including the endangered black-footed ferret. Prairie dogs are highly susceptible to sylvatic plague (caused by the Yersinia pestis bacteria), which causes nearly 100% mortality in infected prairie dogs. When epidemics wipe out entire prairie dog colonies, it is bad news for predators that rely on prairie dog prey. Therefore, there has been a lot research on sylvatic plague transmission, where the hope is that one day we will be able to fully understand and control prairie dog plague epidemics. I think this research tells a really cool story about the role of vectors and alternative hosts in parasite transmission, so I’m going to blog about some of that work today.


For a long time, plague transmission to prairie dogs was assumed to occur primarily through “blocked” fleas. Fleas infected by the Y. pestis bacteria develop a blockage in their digestive system that prevents them from feeding. Afterwards, when they’re trying and failing to feed on their hosts, they repeatedly attempt to regurgitate the blockage, and this injects the Y. pestis bacteria into the host. (Mmm.) But there’s a problem with this story: the fleas that live on prairie dogs (Oropsylla hirsuta) only occasionally become blocked, and it takes a long time for this blockage to occur. Therefore, it didn’t seem like fully blocked fleas could be responsible for the very rapid epidemics and die offs that often occur in prairie dog populations (Webb et al. 2006).

The Y. pestis bacteria might also be transmitted by other routes. For instance, direct contact with infectious droplets (i.e., airborne transmission), consumption of infectious tissue/cadavers, and bites from unblocked fleas might transmit Y. pestis to susceptible prairie dogs. To evaluate the plausibility of those possibilities, Webb et al. (2006) did a really cool modeling study. They found that transmission from blocked fleas and airborne transmission couldn’t be the sole cause of epidemics in prairie dogs, unless the rates of transmission were increased several orders of magnitude above the rates that people have observed in the field. Instead, Webb et al. (2006) suggested that some kind of short term reservoir must be playing a role in transmission – such as unblocked fleas, consumption of infectious cadavers, or alternative rodent hosts (e.g., grasshopper mice).

Shortly after, Eisen et al. (2006) found that transmission of Y. pestis from unblocked Oropsylla hirsuta is possible. In fact, transmission by unblocked fleas can occur very soon after infection – resulting in faster transmission – and infected fleas survive for a long time when unblocked, allowing them to continue to transmit the bacteria for longer than blocked fleas. Neat!

But what about the role of alternative rodent hosts in transmission of plague to prairie dogs? One long-standing hypothesis is that less susceptible rodent species maintain the Y. pestis bacteria enzootically (=without big epidemics) all the time, and then epidemics occur in prairie dog populations when the Y. pestis spills over from the reservoir host into prairie dog populations.  For instance, Jones and Britten (2010) found that when prairie dogs populations are genetically structured among regions, their fleas did not have genetically distinct populations, which suggests that other rodent species might disperse fleas (and Y. pestis) among prairie dog colonies. (See last week’s post for more examples where people used host and parasite population genetic structure to infer intra and interspecific transmission rates.)

But that only explains how alternative reservoir hosts, such as grasshopper mice, play a role in causing the start of prairie dog epidemics. Do grasshopper mice play any role in transmission among prairie dogs during plague epidemics?  Stapp et al. (2009) found that the number of prairie dog fleas increases on grasshopper mice during plague epidemics, probably because the fleas are forced to find new hosts when their prairie dog hosts die. Therefore, grasshopper mice can be short term hosts for infected prairie dog fleas. Additionally, grasshopper mice frequently go into prairie dog burrows, and their ranges can include burrows from 12-23 different prairie dog coteries, which are distinct social units that prairie dogs interact within (Kraft and Stapp 2013). Therefore, while the plague might remain enzootic in prairie dog colonies with very few or no grasshopper mice because the plague would rarely have opportunities to spread among coteries, grasshopper mice can greatly increase the rate of transmission in prairie dog colonies by spreading fleas and Y.pestis into multiple coteries (Kraft and Stapp 2013, Salkeld et al. 2010).

So, we have a bacteria that is vectored by fleas and alternative rodent hosts that can spread the fleas within and among prairie dog populations, thereby causing and exacerbating plague epidemics in prairie dogs. How do we control a pathogen like this? Two methods are currently being used. The first is treating the entrances to prairie dog burrows with insecticides in order to kill off the flea vectors. The second is a vaccine that provides prairie dogs with immunity to Y. pestis. However, dusting burrow entrances and catching and vaccinating individual animals takes a lot of time and money. Fortunately, people are working on an oral vaccine that can be put out in bait, like the oral vaccine for fox rabies that is air-dropped in bait by planes. The oral vaccine for prairie dogs will hopefully be more effective and cheaper than existing control strategies.


Eisen, R.J., Bearden, S.W., Wilder, A.P., Montenieri, J.A., Antolin, M.F. & Gage, K.L. (2006). Early-phase transmission of Yersinia pestis by unblocked fleas as a mechanism explaining rapidly spreading plague epizootics. PNAS 103:15380–15385.

Jones, P.H., and H.B. Britten. 2010. The absence of concordant population genetic structure in the black-tailed prairie dog and the flea, Oropsylla hirsuta, with implications for the spread of Yersinia pestis. Molecular Ecology 19: 2038–2049.

Kraft, J.P., and P. Stapp. 2013. Movements and burrow use by northern grasshopper mice as a possible mechanism of plague spread in prairie dog colonies. Journal of Mammalogy 94(5):1087–1093.

Salkeld, D.J., M. Salathe, P. Strapp, and J.H. Jones. 2010. Plague outbreaks in prairie dog populations explained by percolation thresholds of alternate host abundance. PNAS 107(32): 14247-14250.

Stapp, P., D.J. Salkeld, H.A. Franklin, J.P. Kraft, D.W. Tripp, M.F. Antolin, and K.L. Gage. 2009. Evidence for the involvement of an alternate rodent host in the dynamics of introduced plague in prairie dogs. Journal of Animal Ecology 78(4): 807-817.

Webb, C.T., C.P. Brooks, K.L. Gage, and M.F. Antolin. 2006. Classic flea-borne transmission does not drive plague epizootics in prairie dogs. PNAS 103(16): 6236-6241.

Did Rats Spread the Black Death?

Everyone knows that black rats harboring fleas infected with Yersinia pestis (the bacterium that causes bubonic plague) were transported on ships throughout medieval Europe, spreading the Black Death and killing maybe half of the population.  Right?  Since Paul-Louis Simond proposed the idea in 1898, there’s mostly been agreement that rat fleas from black rats were the main vector of plague transmission.

Last week, I was lit searching something unrelated when I stumbled across an April 2013 paper entitled, “Rats cannot have been intermediate hosts for Yersinia pestis during medieval plague epidemics in Northern Europe.”  Wow!  In the paper, Hufthammer and Walloe (2013) argue that archaeological evidence suggests that the black rat was not widespread or abundant in Northern Europe at the time of the Black Death, so fleas from rats couldn’t be the main vector of plague.  I’m not an archaeologist, so I can’t really judge the archaeological evidence presented by Hufthammer and Walloe (2013).  But I was fascinated by the literature review that they presented, and I wanted to share some of their ideas on the blog.  Here are some of the arguments against rat-facilitated transmission, as expressed by Hufthammer and Wallow (2013) and other sources:

  1. Many rodent species can be infected by the plague, and rodent species vary in their ability to tolerate the plague.  For instance, mice and voles don’t tend to die when infected with the plague, while black rats are killed by the plague.  Apparently black rats don’t just quietly die, either – they get really sick and behave abnormally, so it would be hard not to notice the diseased rats.  If black rats were experiencing a plague epidemic, then massive mortality events should have been observed in black rat populations.  Therefore, if there are written accounts of plague epidemics in humans that do not include notes about how massive number of black rats also recently experienced horrific deaths, then black rats probably weren’t involved in the spread of the plague.  Similarly, there should be archaeological records (i.e., rat bones) of black rat population declines coinciding with human plague epidemics.  But in many cases, there aren’t! I find that fascinating!
  2. If the plague kills rats within a few weeks, then rat populations carrying the plague wouldn’t be able to survive any ship voyages that long. (Is your mind blown yet?!)
  3. In many places, the plague spread so quickly that it does not seem possible that rats could have been the cause of transmission.  The rats would need to travel to the new town and die of infection before the rat fleas left the rats to bite and infect humans.  Apparently that process takes several weeks, which is just too slow to explain how rapidly the bubonic plague spread among towns.
  4.  The human flea (Pulex irritans) can be infected with the plague.  In present-day Tanzania, where the plague occurs in humans, human fleas are the most common fleas in households (Laudisoit et al. 2007).  Furthermore, towns that frequently have plague epidemics also have greater proportions of houses containing human fleas.  So, perhaps human fleas play(ed) a role in plague transmission?
  5. The human body louse (Pediculus humanus) can also become infected with and transmit the plague (Ayyadurai et al. 2010).

Does that mean that rats and rat fleas never caused plague epidemics?  Nope.  There is evidence of rat plague epidemics before human plague epidemics in some locations.  Similarly, the plague has proceeded slowly enough in some locations that rat-facilitated transmission is feasible.  But in other places, like Northern Europe, the evidence may be iffy.  Perhaps rat fleas originally brought the plague to the region, but then the main vectors were human ectoparasites?

This is all fascinating, and I hope we see more related research in the future!



Ayyadurai, S., F. Sebbane, D. Raoult, and M. Drancourt. 2010. Body lice, yersinia pestis orientalis, and black death. Emerging infectious diseases 16:892–3.

Hufthammer, A. K., and L. Walløe. 2013. Rats cannot have been intermediate hosts for Yersinia pestis during medieval plague epidemics in Northern Europe. Journal of Archaeological Science 40:1752–1759.

Laudisoit, A., H. Leirs, R. H. Makundi, S. Van Dongen, S. Davis, S. Neerinckx, J. Deckers, and R. Libois. 2007. Plague and the human flea, Tanzania. Emerging infectious diseases 13:687–93.