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.

Parasites and Predators: Partners in Crime

This week, I wanted to post about a paper that was just too sexy to resist blogging about.  However, as I was writing my post, I stumbled across Jeremy Yoder’s even better post about the paper.  So, you should click through to the Denim and Tweed blog, read his post, and then admire my only best attempt at drawing a flea.

Raveh et al. (2011) performed an experiment where gerbils were either infested or uninfested with fleas.  They put the gerbils in field enclosures, and then exposed the gerbils to a muzzled fox predator for half of the nights that the gerbils were in the enclosures.  Gerbils were provided with sand boxes containing buried seeds, and the gerbils had to balance foraging in the sand boxes for seeds and avoiding getting pounced on by the fox.  Among other things, Raveh et al. (2011) measured the “giving up density” in the sand boxes.  That is, how much food remained in the sand box when the gerbils left the food patch?  Higher giving up densities meant that the gerbils spent less time foraging, which would be bad news for gerbil seed consumption and storage.

Gerbils infested with high densities of fleas left food patches at higher giving up densities than gerbils without fleas.  And when gerbils had fleas and a fox was present, the gerbils left food patches at the highest giving up densities.  So, fleas distracted/irritated gerbils so much that the gerbils spent less time foraging for food, and that change in foraging behavior was amplified when both parasites and predators were present.  In a world full of things trying to eat gerbils, how’s a gerbil gonna eat?

Here are some things that I liked about this paper:

  1. Beautiful, mathy hypothesis testing.  Seriously, go read this paper.
  2. In the wild, 97-100% of gerbils have fleas!  Wow!
  3. Parasites may facilitate predation on the host, even when the parasites aren’t trophically transmitted.
  4. This relates to my post about vicious circles of body condition (or susceptibility) and parasite infection.  If gerbils with many fleas forage less than gerbils with few/no fleas, their body condition might decline.  And if their body condition declines, they might be more susceptible to fleas.  Etc.  This might lead to vicious circles of declining health/fitness.  Or, perhaps the vicious circles don’t have much time to act, because foxes come along and eat the distracted gerbils.

Serious business.


Raveh, A., B. P. Kotler, Z. Abramsky, and B. R. Krasnov. 2011. Driven to distraction: detecting the hidden costs of flea parasitism through foraging behaviour in gerbils. Ecology letters 14:47–51.

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.

Rove Beetles Eat Parasites (mind=blown)!

I found a big rove beetle in my yard today, and I decided to take some photos of its giant mandibles.  It was behaving oddly – maybe just because it didn’t like my attentions, or maybe because it was parasitized.  I decided to do some research into rove beetle parasites, and I discovered something tangential that blew my mind: rove beetles eat parasites!!

As I might have mentioned before, I’m really interested in predation on parasites, and I have a special soft spot for mutualistic organisms that eat parasites.  It turns out that there is a whole group of rove beetles (Amblyopinus) that live on rodents and in their nests.  These beetles were originally classified as parasites of rodents, but Ashe and Timm (1987) argued that they didn’t appear to be parasitic; rodents did not try to groom off their rove beetles, and beetles were never seen damaging host tissues.  Instead, Ashe and Timm (1987) found that the rove beetles hang out in the rodents’ nests during the day, eating ectoparasites, and hang out on the rodents at night so that they get free transportation among nests.  AWESOME!

I think that this is the first time I’ve heard of multicellular symbionts of mammals that eat parasites.  Can you think of any others? Remoras on cetaceans?



Ashe, J.S., and R.M. Timm. 1987. Probable mutualistic association between staphylinid beetles (Amblyopinus) and their rodent hosts.  Journal of Tropical Ecology, 3(2): 177-181.