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. 2015 Jan 8:8:11.
doi: 10.1186/s13071-014-0616-1.

Seasonal fluctuations of small mammal and flea communities in a Ugandan plague focus: evidence to implicate Arvicanthis niloticus and Crocidura spp. as key hosts in Yersinia pestis transmission

Sean M Moore  1   2   3 , Andrew Monaghan  4 , Jeff N Borchert  5 , Joseph T Mpanga  6 , Linda A Atiku  7 , Karen A Boegler  8 , John Montenieri  9 , Katherine MacMillan  10 , Kenneth L Gage  11 , Rebecca J Eisen  12
Affiliations

Seasonal fluctuations of small mammal and flea communities in a Ugandan plague focus: evidence to implicate Arvicanthis niloticus and Crocidura spp. as key hosts in Yersinia pestis transmission

Sean M Moore et al. Parasit Vectors. .

Abstract

Background: The distribution of human plague risk is strongly associated with rainfall in the tropical plague foci of East Africa, but little is known about how the plague bacterium is maintained during periods between outbreaks or whether environmental drivers trigger these outbreaks. We collected small mammals and fleas over a two year period in the West Nile region of Uganda to examine how the ecological community varies seasonally in a region with areas of both high and low risk of human plague cases.

Methods: Seasonal changes in the small mammal and flea communities were examined along an elevation gradient to determine whether small mammal and flea populations exhibit differences in their response to seasonal fluctuations in precipitation, temperature, and crop harvests in areas within (above 1300 m) and outside (below 1300 m) of a model-defined plague focus.

Results: The abundance of two potential enzootic host species (Arvicanthis niloticus and Crocidura spp.) increased during the plague season within the plague focus, but did not show the same increase at lower elevations outside this focus. In contrast, the abundance of the domestic rat population (Rattus rattus) did not show significant seasonal fluctuations regardless of locality. Arvicanthis niloticus abundance was negatively associated with monthly precipitation at a six month lag and positively associated with current monthly temperatures, and Crocidura spp. abundance was positively associated with precipitation at a three month lag and negatively associated with current monthly temperatures. The abundance of A. niloticus and Crocidura spp. were both positively correlated with the harvest of millet and maize.

Conclusions: The association between the abundance of several small mammal species and rainfall is consistent with previous models of the timing of human plague cases in relation to precipitation in the West Nile region. The seasonal increase in the abundance of key potential host species within the plague focus, but not outside of this area, suggests that changes in small mammal abundance may create favorable conditions for epizootic transmission of Y. pestis which ultimately may increase risk of human cases in this region.

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Figures

Figure 1
Figure 1
Monthly plague cases, precipitation, temperature, and crop harvests in West Nile region of Uganda. (A) Number of monthly suspected human plague cases in Arua and Zombo districts from 1999 to 2011. Averaged monthly (B) precipitation (mm) and (C) mean temperatures (°C) at field sites above and below 1300 m. Climate variables are long-term averages for 1999–2008 derived from Weather Research and Forecasting model simulations described in Monaghan et al. [35]. (D) Percentage of homesteads above 1300 m that report harvesting millet/maize, potatoes, pumpkins, beans, and ground nuts in each month.
Figure 2
Figure 2
Schematic of sampling design for a single homestead within a village.
Figure 3
Figure 3
Abundance (per 100 trap nights) above and below 1300 m of the eight most common small mammals. Error bars represent ±1 SE. *Indicates statistically significant difference (α = 0.05) between abundance above and below 1300 m using repeated measures analysis with a generalized linear mixed model.
Figure 4
Figure 4
Comparison of abundance of most common small mammals during and outside of the plague season. Abundance is mean adjusted abundance per homestead inside and outside of huts (per 100 trap nights). Error bars represent ±1 SE. *Indicates statistically significant difference (α = 0.05) between abundance during and outside of plague season using a generalized linear mixed model with homestead ID as a random effect.
Figure 5
Figure 5
Species richness, diversity, and abundance of small mammals and fleas inside and outside plague risk area. (A) Comparison of species richness of small mammals and fleas during and outside of plague season. Fleas-all is the number of flea species collected from both indoors and outdoors in a homestead, Fleas-outside is the number of flea species collected from outside of the huts in a homestead. (B) Species diversity of small mammals and fleas during and outside of plague season. (C) Total abundance of fleas per homestead and fleas per small mammal host during and outside of plague season. Error bars represent ±1 SE. *Indicates statistically significant difference (α = 0.05) between abundance during and outside of plague season.
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