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.

References:

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.