Effects of Land Use on Plague (Yersinia pestis) Activity in Rodents in Tanzania

Douglas J. McCauley Department of Ecology, Evolution and Marine Biology, University of California Santa Barbara, Santa Barbara, California; Woods Institute for the Environment, Department of Biology, Department of Environmental Earth System Science, and Department of Medicine, Stanford University, Stanford, California; Department of Biology, Colorado State University, Fort Collins, Colorado; Division of Mammals, National Museum of Natural History, Smithsonian Institution, Washington, District of Columbia; Department of Biology, Northern Virginia Community College, Springfield, Virginia; Sokoine University of Agriculture, Morogoro, Tanzania

Search for other papers by Douglas J. McCauley in
Current site
Google Scholar
PubMed Close
,
Daniel J. Salkeld Department of Ecology, Evolution and Marine Biology, University of California Santa Barbara, Santa Barbara, California; Woods Institute for the Environment, Department of Biology, Department of Environmental Earth System Science, and Department of Medicine, Stanford University, Stanford, California; Department of Biology, Colorado State University, Fort Collins, Colorado; Division of Mammals, National Museum of Natural History, Smithsonian Institution, Washington, District of Columbia; Department of Biology, Northern Virginia Community College, Springfield, Virginia; Sokoine University of Agriculture, Morogoro, Tanzania

Search for other papers by Daniel J. Salkeld in
Current site
Google Scholar
PubMed Close
,
Hillary S. Young Department of Ecology, Evolution and Marine Biology, University of California Santa Barbara, Santa Barbara, California; Woods Institute for the Environment, Department of Biology, Department of Environmental Earth System Science, and Department of Medicine, Stanford University, Stanford, California; Department of Biology, Colorado State University, Fort Collins, Colorado; Division of Mammals, National Museum of Natural History, Smithsonian Institution, Washington, District of Columbia; Department of Biology, Northern Virginia Community College, Springfield, Virginia; Sokoine University of Agriculture, Morogoro, Tanzania

Search for other papers by Hillary S. Young in
Current site
Google Scholar
PubMed Close
,
Rhodes Makundi Department of Ecology, Evolution and Marine Biology, University of California Santa Barbara, Santa Barbara, California; Woods Institute for the Environment, Department of Biology, Department of Environmental Earth System Science, and Department of Medicine, Stanford University, Stanford, California; Department of Biology, Colorado State University, Fort Collins, Colorado; Division of Mammals, National Museum of Natural History, Smithsonian Institution, Washington, District of Columbia; Department of Biology, Northern Virginia Community College, Springfield, Virginia; Sokoine University of Agriculture, Morogoro, Tanzania

Search for other papers by Rhodes Makundi in
Current site
Google Scholar
PubMed Close
,
Rodolfo Dirzo Department of Ecology, Evolution and Marine Biology, University of California Santa Barbara, Santa Barbara, California; Woods Institute for the Environment, Department of Biology, Department of Environmental Earth System Science, and Department of Medicine, Stanford University, Stanford, California; Department of Biology, Colorado State University, Fort Collins, Colorado; Division of Mammals, National Museum of Natural History, Smithsonian Institution, Washington, District of Columbia; Department of Biology, Northern Virginia Community College, Springfield, Virginia; Sokoine University of Agriculture, Morogoro, Tanzania

Search for other papers by Rodolfo Dirzo in
Current site
Google Scholar
PubMed Close
,
Ralph P. Eckerlin Department of Ecology, Evolution and Marine Biology, University of California Santa Barbara, Santa Barbara, California; Woods Institute for the Environment, Department of Biology, Department of Environmental Earth System Science, and Department of Medicine, Stanford University, Stanford, California; Department of Biology, Colorado State University, Fort Collins, Colorado; Division of Mammals, National Museum of Natural History, Smithsonian Institution, Washington, District of Columbia; Department of Biology, Northern Virginia Community College, Springfield, Virginia; Sokoine University of Agriculture, Morogoro, Tanzania

Search for other papers by Ralph P. Eckerlin in
Current site
Google Scholar
PubMed Close
,
Eric F. Lambin Department of Ecology, Evolution and Marine Biology, University of California Santa Barbara, Santa Barbara, California; Woods Institute for the Environment, Department of Biology, Department of Environmental Earth System Science, and Department of Medicine, Stanford University, Stanford, California; Department of Biology, Colorado State University, Fort Collins, Colorado; Division of Mammals, National Museum of Natural History, Smithsonian Institution, Washington, District of Columbia; Department of Biology, Northern Virginia Community College, Springfield, Virginia; Sokoine University of Agriculture, Morogoro, Tanzania

Search for other papers by Eric F. Lambin in
Current site
Google Scholar
PubMed Close
,
Lynne Gaffikin Department of Ecology, Evolution and Marine Biology, University of California Santa Barbara, Santa Barbara, California; Woods Institute for the Environment, Department of Biology, Department of Environmental Earth System Science, and Department of Medicine, Stanford University, Stanford, California; Department of Biology, Colorado State University, Fort Collins, Colorado; Division of Mammals, National Museum of Natural History, Smithsonian Institution, Washington, District of Columbia; Department of Biology, Northern Virginia Community College, Springfield, Virginia; Sokoine University of Agriculture, Morogoro, Tanzania

Search for other papers by Lynne Gaffikin in
Current site
Google Scholar
PubMed Close
,
Michele Barry Department of Ecology, Evolution and Marine Biology, University of California Santa Barbara, Santa Barbara, California; Woods Institute for the Environment, Department of Biology, Department of Environmental Earth System Science, and Department of Medicine, Stanford University, Stanford, California; Department of Biology, Colorado State University, Fort Collins, Colorado; Division of Mammals, National Museum of Natural History, Smithsonian Institution, Washington, District of Columbia; Department of Biology, Northern Virginia Community College, Springfield, Virginia; Sokoine University of Agriculture, Morogoro, Tanzania

Search for other papers by Michele Barry in
Current site
Google Scholar
PubMed Close
, and
Kristofer M. Helgen Department of Ecology, Evolution and Marine Biology, University of California Santa Barbara, Santa Barbara, California; Woods Institute for the Environment, Department of Biology, Department of Environmental Earth System Science, and Department of Medicine, Stanford University, Stanford, California; Department of Biology, Colorado State University, Fort Collins, Colorado; Division of Mammals, National Museum of Natural History, Smithsonian Institution, Washington, District of Columbia; Department of Biology, Northern Virginia Community College, Springfield, Virginia; Sokoine University of Agriculture, Morogoro, Tanzania

Search for other papers by Kristofer M. Helgen in
Current site
Google Scholar
PubMed Close
DOI:
https://doi.org/10.4269/ajtmh.14-0504
Volume/Issue:
Volume 92: Issue 4
Page(s):
776–783
Restricted access
Get Permissions

Understanding the effects of land-use change on zoonotic disease risk is a pressing global health concern. Here, we compare prevalence of Yersinia pestis, the etiologic agent of plague, in rodents across two land-use types—agricultural and conserved—in northern Tanzania. Estimated abundance of seropositive rodents nearly doubled in agricultural sites compared with conserved sites. This relationship between land-use type and abundance of seropositive rodents is likely mediated by changes in rodent and flea community composition, particularly via an increase in the abundance of the commensal species, Mastomys natalensis, in agricultural habitats. There was mixed support for rodent species diversity negatively impacting Y. pestis seroprevalence. Together, these results suggest that land-use change could affect the risk of local transmission of plague, and raise critical questions about transmission dynamics at the interface of conserved and agricultural habitats. These findings emphasize the importance of understanding disease ecology in the context of rapidly proceeding landscape change.

    • Supplemental Materials (PDF 471 KB)

Author Notes

* Address correspondence to Hillary S. Young, Bldg. 569, Rm. 1101, University of California, Santa Barbara, CA 93106-9620. E-mail: hillary.young@lifesci.ucsb.edu
† These authors contributed equally.

Financial support: This project was supported by the James Smithson Fund of the Smithsonian Institution, the National Geographic Society (Grants 4691-91, 8846-10, 9106-12), the National Science Foundation (DEB-0909670), the Woods Institute for the Environment at Stanford University, the Smithsonian Barcode Network grant, and the Smithsonian Women's Committee (SWC 44).

Authors' addresses: Douglas J. McCauley and Hillary S. Young Department of Ecology, Evolution, and Marine Biology, University of California Santa Barbara, Santa Barbara, CA, E-mails: douglas.mccauley@lifesci.ucsb.edu and hillary.young@lifesci.ucsb.edu. Daniel J. Salkeld, Rodolfo Dirzo, Eric F. Lambin, Lynnee Gaffikin, Michele Barry, Woods Institute for the Environment, Department of Medicine, Stanford University, Stanford, CA, E-mails: dansalkeld@gmail.com, rdirzo@stanford.edu, elambin@stanford.edu, earthlg@gmail.com, and michele.barry@stanford. Rhodes Makundi, Sokoine University of Agriculture, Morogoro, Tanzania, E-mail: rmakundi@yahoo.com. Ralph P. Eckerlin, Natural Sciences Division, Northern Virginia Community College, Annandale, VA, E-mail: reckerlin@nvcc.edu. Kristofer M. Helgen, Division of Mammals, Smithsonian Institution, Washington, DC, E-mail: helgenk@si.edu.

Copyright:
© The American Society of Tropical Medicine and Hygiene 2015
Received:
08 Aug 2014
|
Accepted:
14 Jan 2015
|
Published Online:
01 Apr 2015
Cover The American Journal of Tropical Medicine and Hygiene
The American Journal of Tropical Medicine and Hygiene
Print ISSN:
0002-9637
Online ISSN:
1476-1645
  • 1.

    Jones KE, Patel NG, Levy MA, Storeygard A, Balk D, Gittleman JL, Daszak P, 2008. Global trends in emerging infectious diseases. Nature 451: 990–993.

  • 2.

    Morens DM, Folkers GK, Fauci AS, 2004. The challenge of emerging and re-emerging infectious diseases. Nature 430: 242–249.

  • 3.

    Dunn RR, Davies TJ, Harris NC, Gavin MC, 2010. Global drivers of human pathogen richness and prevalence. Proc R Soc Lond B Biol Sci 277: 2587–2595.

  • 4.

    Neerinckx S, Bertherat E, Leirs H, 2010. Human plague occurrences in Africa: an overview from 1877 to 2008. Trans R Soc Trop Med Hyg 104: 97–103.

  • 5.

    Thiberville SD, Moyen N, Dupuis-Maguiraga L, Nougairede A, Gould EA, Roques P, de Lamballerie X, 2013. Chikungunya fever: epidemiology, clinical syndrome, pathogenesis and therapy. Antiviral Res 99: 345–370.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 6.

    Sindato C, Karimuribo ED, Pfeiffer DU, Mboera LEG, Kivaria F, Dautu G, Bernard B, Paweska JT, 2014. Spatial and temporal pattern of Rift Valley fever outbreaks in Tanzania; 1930 to 2007. PLoS ONE 9: e88897.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 7.

    Fratkin E, 2001. East African pastoralism in transition: Maasai, Boran, and Rendille cases. Afr Stud Rev 44: 1–25.

  • 8.

    Homewood K, Lambin EF, Coast E, Kariuki A, Kikula I, Kivelia J, Said M, Serneels S, Thompson M, 2001. Long-term changes in Serengeti-Mara wildebeest and land cover: pastoralism, population, or policies? Proc Natl Acad Sci USA 98: 12544–12549.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 9.

    Homewood KM, 2004. Policy, environment and development in African rangelands. Environ Sci Policy 7: 125–143.

  • 10.

    Mills JN, 2006. Biodiversity loss and emerging infectious disease: an example from the rodent-borne hemorrhagic fevers. Biodiversity 7: 9–17.

  • 11.

    Lambin EF, Tran A, Vanwambeke SO, Linard C, Soti V, 2010. Pathogenic landscapes: interactions between land, people, disease vectors, and their animal hosts. Int J Health Geogr 9: 1–13.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 12.

    Vittor AY, Gilman RH, Tielsch J, Glass G, Shields T, Lozano WS, Pinedo-Cancino V, Patz JA, 2006. The effect of deforestation on the human-biting rate of Anopheles darlingi, the primary vector of falciparum malaria in the Peruvian Amazon. Am J Trop Med Hyg 74: 3–11.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 13.

    Chasar A, Loiseau C, Valkiūnas G, Iezhova T, Smith TB, Sehgal RNM, 2009. Prevalence and diversity patterns of avian blood parasites in degraded African rainforest habitats. Mol Ecol 18: 4121–4133.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 14.

    Pongsiri MJ, Roman J, Ezenwa VO, Goldberg TL, Koren HS, Newbold SC, Ostfeld RS, Pattanayak SK, Salkeld DJ, 2009. Biodiversity loss affects global disease ecology. Bioscience 59: 945–954.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 15.

    Keesing F, Holt RD, Ostfeld RS, 2006. Effects of species diversity on disease risk. Ecol Lett 9: 485–498.

  • 16.

    Young HS, Dirzo R, Helgen KM, McCauley DJ, Billeter SA, Kosoy MY, Osikowicz LM, Salkeld DJ, Young TP, Dittmar K, 2014. Declines in large wildlife increase landscape-level prevalence of rodent-borne disease in Africa. Proc Natl Acad Sci USA 111: 7036–7041.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 17.

    Randolph SE, Dobson A, 2012. Pangloss revisited: a critique of the dilution effect and the biodiversity-buffers-disease paradigm. Parasitology 139: 847–863.

  • 18.

    Salkeld DJ, Padgett KA, Jones JH, 2013. A meta-analysis suggesting that the relationship between biodiversity and risk of zoonotic pathogen transmission is idiosyncratic. Ecol Lett 16: 679–686.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 19.

    Young H, Griffin RH, Wood CL, Nunn CL, 2013. Does habitat disturbance increase infectious disease risk for primates? Ecol Lett 16: 656–663.

  • 20.

    Wood CL, Laffert KD, DeLeo G, Young HS, Hudson PJ, Kuris AM, 2014. Does biodiversity protect humans against infectious disease? Ecology 95: 817–832.

  • 21.

    Salkeld DJ, Lane RS, 2010. Community ecology and disease risk: lizards, squirrels, and the Lyme disease spirochete in California, USA. Ecology 91: 293–298.

  • 22.

    Piudo L, Monteverde MJ, Walker RS, Douglass RJ, 2011. Rodent community structure and Andes virus infection in sylvan and peridomestic habitats in northwestern Patagonia, Argentina. Vector Borne Zoonotic Dis 11: 315–324.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 23.

    Davis S, Makundi R, Machang'u R, Leirs H, 2006. Demographic and spatio-temporal variation in human plague at a persistent focus in Tanzania. Acta Trop 100: 133–141.

  • 24.

    Ogen-Odoi A, Mbidde EK, Lutwama J, Wamala J, Mucunguzi A, Mugagga M, Kagirita A, Lukwago L, Musanza MM, Talisuna A, 2009. Bubonic and pneumonic plague—Uganda, 2006. MMWR 58: 778–781.

  • 25.

    McCauley DJ, Keesing F, Young T, Dittmar K, 2008. Effects of the removal of large herbivores on fleas of small mammals. J Vector Ecol 33: 263–268.

  • 26.

    Laudisoit A, Leirs H, Makundi R, Krasnov BR, 2009. Seasonal and habitat dependence of fleas parasitic on small mammals in Tanzania. Integr Zool 4: 196–212.

  • 27.

    Davis S, Begon M, De Bruyn L, Ageyev VS, Klassovskiy NL, Pole SB, Viljugrein H, Stenseth NC, Leirs H, 2004. Predictive thresholds for plague in Kazakhstan. Science 304: 736–738.

  • 28.

    Davis S, Trapman P, Leirs H, Begon M, Heesterbeek J, 2008. The abundance threshold for plague as a critical percolation phenomenon. Nature 454: 634–637.

  • 29.

    Stenseth NC, Samia NI, Viljugrein H, Kausrud KL, Begon M, Davis S, Leirs H, Dubyanskiy VM, Esper J, Ageyev VS, 2006. Plague dynamics are driven by climate variation. Proc Natl Acad Sci USA 103: 13110–13115.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 30.

    Salkeld DJ, Salathé M, Stapp P, Jones JH, 2010. Plague outbreaks in prairie dog populations explained by percolation thresholds of alternate host abundance. Proc Natl Acad Sci USA 107: 14247–14250.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 31.

    Moore SM, Monaghan A, Griffith KS, Apangu T, Mead PS, Eisen RJ, 2012. Improvement of disease prediction and modeling through the use of meteorological ensembles: human plague in Uganda. PLoS ONE 7: e44431.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 32.

    Andrianaivoarimanana V, Kreppel K, Elissa N, Duplantier JM, Carniel E, Rajerison M, Jambou R, 2013. Understanding the persistence of plague foci in Madagascar. PLoS Negl Trop Dis 7: e2382.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 33.

    Serneels S, Said M, Lambin E, 2001. Land cover changes around a major east African wildlife reserve: the Mara Ecosystem (Kenya). Int J Remote Sens 22: 3397–3420.

  • 34.

    Lambin EF, Geist HJ, Lepers E, 2003. Dynamics of land-use and land-cover change in tropical regions. Annu Rev Environ Resour 28: 205–241.

  • 35.

    Ogutu J, Owen-Smith N, Piepho H, Said M, 2011. Continuing wildlife population declines and range contraction in the Mara region of Kenya during 1977–2009. J Zool 285: 99–109.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 36.

    Beale CM, Rensberg SV, Bond WJ, Coughenour M, Fynn R, Gaylard A, Grant R, Harris B, Jones T, Mduma S, 2013. Ten lessons for the conservation of African savannah ecosystems. Biol Conserv 167: 224–232.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 37.

    Olson JM, 2004. The Spatial Patterns and Root Causes of Land Use Change in East Africa. LUCID Project. Nairobi, Kenya: International Livestock Research Institute, 1–38.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 38.

    Kilonzo B, Mbise T, Mwalimu D, Kindamba L, 2006. Observations on the endemicity of plague in Karatu and Ngorongoro, northern Tanzania. Tanzan J Health Res Bull 8: 1–6.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 39.

    Mwalyosi R, 1981. Ecological changes in Lake Manyara National Park. Afr J Ecol 19: 201–204.

  • 40.

    Ondrejicka DA, Locke SA, Morey K, Borisenko AV, Hanner RH, 2014. Status and prospects of DNA barcoding in medically important parasites and vectors. Trends Parasitol 30: 582–591.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 41.

    Musser G, Carleton M, 2005. Order Rodentia. Wilson DE, Reeder DM, eds. Mammal Species of the World: A Taxonomic and Geographic Reference, Vol 2. Baltimore, MD: Johns Hopkins University Press, 745–1600.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 42.

    Verheyen W, Hulselmans JLT, Dierckx T, Mulungu L, Liers H, Corti M, Verheyen E, 2007. The characterization of the Kilimanjaro Lophuromys aquilus True, 1892 population and the description of five new Lophuromys species (Rodentia, Muridae). Bulletin van het Koninklijk Belgisch Instituut voor Natuurwetenschappen, Biologie 77: 23–75.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 43.

    Carleton MD, Stanley WT, 2012. Species limits within the Praomys delectorum group (Rodentia: Muridae: Murinae) of East Africa: a morphometric reassessment and biogeographical implications. Zool J Linn Soc 165: 420–469.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 44.

    Young HS, McCauley DJ, Dirzo R, Goheen JR, Agwanda B, Brook C, Castillo EO, Ferguson A, Kinyua SN, McDonough MM, Palmer TM, Pringle RM, Young TP, Helgen KM, 2015. Context-dependent effects of large wildlife declines on small mammal communities in central Kenya. Ecol Appl 25: 348–360.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 45.

    Sikes RS, Gannon WL, 2011. Guidelines of the American Society of Mammalogists for the use of wild mammals in research. J Mammal 92: 235–253.

  • 46.

    Young HS, McCauley DJ, Helgen KM, Goheen JR, Otárola-Castillo E, Palmer TM, Pringle RM, Young TP, Dirzo R, 2013. Effects of mammalian herbivore declines on plant communities: observations and experiments in an African savanna. J Ecol 101: 1030–1041.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 47.

    Williams JE, Gentry MK, Braden CA, Leister F, Yolken RH, 1984. Use of an enzyme-linked immunosorbent assay to measure antigenaemia during acute plague. Bull World Health Organ 62: 463–466.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 48.

    Esamaeili S, Azadmanesh K, Naddaf SR, Rajerison M, Carniel E, Mostafavi E, 2013. Serologic survey of plague in animals, western Iran. Emerg Infect Dis 19: 1549–1551.

  • 49.

    Chu MC, 2000. Laboratory Manual of Plague Diagnostic Tests. Atlanta, GA: U.S. Department of Health and Human Services, Centers for Disease Control and Prevention and World Health Organization, 61–63.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 50.

    LoGiudice K, Ostfeld RS, Schmidt KA, Keesing F, 2003. The ecology of infectious disease: effects of host diversity and community composition on Lyme disease risk. Proc Natl Acad Sci USA 100: 567–571.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 51.

    Kilpatrick AM, Daszak P, Jones MJ, Marra PP, Kramer LD, 2006. Host heterogeneity dominates West Nile virus transmission. Proc R Soc Lond B Biol Sci 273: 2327–2333.

  • 52.

    R Development Core Team, 2014. R: A Language and Environment for Statistical Computing. Vienna, Austria: The R Foundation for Statistical Computing.

  • 53.

    Neerinckx S, Peterson AT, Gulinck H, Deckers J, Kimaro D, Leirs H, 2010. Predicting potential risk areas of human plague for the Western Usambara Mountains, Lushoto District, Tanzania. Am J Trop Med Hyg 82: 492–500.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 54.

    Bahmanyar M, Cavanaugh DC, 1976. Plague Manual. Geneva, Switzerland: World Health Organization, 1–76.

  • 55.

    Zimba M, Loveridge J, Davies DM, Mukaratirwa S, 2012. Seasonal abundance and epidemiologial indices of potential plague vectors Dinopysyllus lypusus (Siphonaptera: Hystrichopsyllidae) and Ctenophthalmus calceatus (Siphonaptera: Ctenophthalmidae) on rodents captured from three habitat types of Hatcliffe and Dzivarasekwa suburbs of Harare, Zimbabwe. J Med Ent 49: 1453–1459.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 56.

    Kilonzo B, Mvena Z, Machangu R, Mbise T, 1997. Preliminary observations on factors responsible for long persistence and continued outbreaks of plague in Lushoto district, Tanzania. Acta Trop 68: 215–227.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 57.

    Gratz N, 1999. Plague manual: epidemiology, distribution, surveillance and control. World Health Organ Tech Rep Ser 99: 63–96.

  • 58.

    Eisen RJ, Borchert JN, Holmes JL, Amatre G, Van Wyk K, Enscore RE, Babi N, Atiku LA, Wilder AP, Vetter SM, 2008. Early-phase transmission of Yersinia pestis by cat fleas (Ctenocephalides felis) and their potential role as vectors in a plague-endemic region of Uganda. Am J Trop Med Hyg 78: 949–956.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 59.

    Makundi RH, Massawe AW, Mulungu LS, Katakweba A, Mbise TJ, Mgode G, 2008. Potential mammalian reservoirs in a bubonic plague outbreak focus in Mbulu District, northern Tanzania, in 2007. Mammalia 72: 253–257.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 60.

    Monath T, Newhouse VF, Kemp GE, Setzer HW, Cacciapuoti A, 1974. Lassa virus isolation from Mastomys natalensis rodents during an epidemic in Sierra Leone. Science 185: 263–265.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 61.

    Denys C, Koulémou K, Soropogui B, Koivogui L, Doré A, Meulen JT, Akoua-Koffi C, Camara MD, Allali BK, Calvet E, Sylla O, Kouassi-Kan S, Kourouma F, Lecompte E, 2005. Community analysis of Muridae (Mammalia, Rodentia) diversity in Guinea: a special emphasis on Mastomys species and Lassa fever distributions. New York, NY: Springer US. African Biodiversity, 339–350.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 62.

    LaDeau SL, Kilpatrick AM, Marra PP, 2007. West Nile virus emergence and large-scale declines of North American bird populations. Nature 447: 710–713.

  • 63.

    Streicker DG, Fenton A, Pedersen AB, 2013. Differential sources of host species heterogeneity influence the transmission and control of multihost parasites. Ecol Lett 16: 975–984.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 64.

    Dornelas M, Gotelli NJ, McGill B, Shimadzu H, Moyes F, Sievers C, Magurran AE, 2014. Assemblage time series reveal biodiversity change but not systematic loss. Science 344: 296–299.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 65.

    Dirzo R, Young H, Galetti M, Ceballos G, Isaac NJB, Collen B, 2014. Defaunation in the Anthropocene. Science 345: 401–406.

  • 66.

    Amatre G, Babi N, Enscore RE, Ogen-Odoi A, Atiku LA, Akol A, Gage KL, Eisen RJ, 2009. Flea diversity and infestation prevalence on rodents in a plague-endemic region of Uganda. Am J Trop Med Hyg 81: 718–724.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 67.

    Schmidt KA, Ostfeld RS, 2001. Biodiversity and the dilution effect in disease ecology. Ecology 82: 609–619.

  • 68.

    Allan BF, Langerhans RB, Ryberg WA, Landesman WJ, Griffin NW, Katz RS, Oberle BJ, Schutzenhofer MR, Smyth KN, Maurice AS, 2009. Ecological correlates of risk and incidence of West Nile virus in the United States. Oecologia 158: 699–708.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 69.

    Clay CA, Lehmer EM, Jeor SS, Dearing MD, 2009. Testing mechanisms of the dilution effect: deer mice encounter rates, Sin Nombre virus prevalence and species diversity. EcoHealth 6: 250–259.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 70.

    Leirs H, Verheyen W, Verhagen R, 1996. Spatial patterns in Mastomys natalensis in Tanzania (Rodentia, Muridae). Mammalia 60: 545–556.

  • 71.

    Stenseth NC, Leir H, Skonhoft A, Davis SA, Pech RP, Andreassen HP, Singleton GR, Lima M, Machang'u RS, Makundi RH, 2003. Mice, rats, and people: the bio-economics of agricultural rodent pests. Front Ecol Environ 1: 367–375.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 72.

    Vibe-Petersen S, Leirs H, Bruyn LD, 2006. Effects of predation and dispersal on Mastomys natalensis population dynamics in Tanzanian maize fields. J Anim Ecol 75: 213–220.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 73.

    Leirs H, 1995. Population ecology of Mastomys natalensis (Smith, 1834) multimammate rats: possible implications for rodent control in Africa. Agricul Ed 35: 1–737.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 74.

    Makundi RH, Massawe AW, Mulungu LS, 2007. Breeding seasonality and population dynamics of three rodent species in the Magamba Forest Reserve, Western Usambara Mountains, north-east Tanzania. Afr J Ecol 45: 17–21.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 75.

    Fa JE, Purvis A, 1997. Body size, diet and population density in afrotropical forest mammals: a comparison with neotropical species. J Anim Ecol 66: 98–112.

  • 76.

    MacMillan K, Enscore RE, Ogen-Odoi A, Borchert JN, Babi N, Amatre G, Atiku LA, Mead PS, Gage KL, Eisen RJ, 2011. Landscape and residential variables associated with plague-endemic villages in the West Nile region of Uganda. Am J Trop Med Hyg 84: 435–442.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 77.

    Eisen RJ, Borchert JN, Mpanga JT, Atiku LA, MacMillian K, Boegler KA, Montenieri JA, Monaghan A, Gage KL, 2012. Flea diversity as an element for persistence of plague bacteria in an East African plague focus. PLoS ONE 7: e35598.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 78.

    Laudisoit A, Leir H, Makundi RH, Van Dongen S, Davis S, Neerinckx S, Deckers J, Libois R, 2007. Plague and the human flea, Tanzania. Emerg Infect Dis 13: 687–693.

Past two years Past Year Past 30 Days
Abstract Views 510 308 9
Full Text Views 689 18 0
PDF Downloads 293 19 0
 

 

 

 
 
Affiliate Membership Banner
 
 
Research for Health Information Banner
 
 
CLOCKSS
 
 
 
Society Publishers Coalition Banner
Save