1921
Volume 92, Issue 4
  • ISSN: 0002-9637
  • E-ISSN: 1476-1645

Abstract

Abstract.

Understanding the effects of land-use change on zoonotic disease risk is a pressing global health concern. Here, we compare prevalence of , 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, , in agricultural habitats. There was mixed support for rodent species diversity negatively impacting 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.

Loading

Article metrics loading...

/content/journals/10.4269/ajtmh.14-0504
2015-04-01
2017-09-20
Loading full text...

Full text loading...

/deliver/fulltext/14761645/92/4/776.html?itemId=/content/journals/10.4269/ajtmh.14-0504&mimeType=html&fmt=ahah

References

  1. Jones KE, Patel NG, Levy MA, Storeygard A, Balk D, Gittleman JL, Daszak P, , 2008. Global trends in emerging infectious diseases. Nature 451: 990993.[Crossref]
  2. Morens DM, Folkers GK, Fauci AS, , 2004. The challenge of emerging and re-emerging infectious diseases. Nature 430: 242249.[Crossref]
  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: 25872595.[Crossref]
  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: 97103.[Crossref]
  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: 345370.[Crossref]
  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.[Crossref]
  7. Fratkin E, , 2001. East African pastoralism in transition: Maasai, Boran, and Rendille cases. Afr Stud Rev 44: 125.[Crossref]
  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: 1254412549.[Crossref]
  9. Homewood KM, , 2004. Policy, environment and development in African rangelands. Environ Sci Policy 7: 125143.[Crossref]
  10. Mills JN, , 2006. Biodiversity loss and emerging infectious disease: an example from the rodent-borne hemorrhagic fevers. Biodiversity 7: 917.[Crossref]
  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: 113.[Crossref]
  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: 311.
  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: 41214133.[Crossref]
  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: 945954.[Crossref]
  15. Keesing F, Holt RD, Ostfeld RS, , 2006. Effects of species diversity on disease risk. Ecol Lett 9: 485498.[Crossref]
  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: 70367041.[Crossref]
  17. Randolph SE, Dobson A, , 2012. Pangloss revisited: a critique of the dilution effect and the biodiversity-buffers-disease paradigm. Parasitology 139: 847863.[Crossref]
  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: 679686.[Crossref]
  19. Young H, Griffin RH, Wood CL, Nunn CL, , 2013. Does habitat disturbance increase infectious disease risk for primates? Ecol Lett 16: 656663.[Crossref]
  20. Wood CL, Laffert KD, DeLeo G, Young HS, Hudson PJ, Kuris AM, , 2014. Does biodiversity protect humans against infectious disease? Ecology 95: 817832.[Crossref]
  21. Salkeld DJ, Lane RS, , 2010. Community ecology and disease risk: lizards, squirrels, and the Lyme disease spirochete in California, USA. Ecology 91: 293298.[Crossref]
  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: 315324.[Crossref]
  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: 133141.[Crossref]
  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: 778781.
  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: 263268.[Crossref]
  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: 196212.[Crossref]
  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: 736738.[Crossref]
  28. Davis S, Trapman P, Leirs H, Begon M, Heesterbeek J, , 2008. The abundance threshold for plague as a critical percolation phenomenon. Nature 454: 634637.[Crossref]
  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: 1311013115.[Crossref]
  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: 1424714250.[Crossref]
  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.[Crossref]
  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.[Crossref]
  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: 33973420.[Crossref]
  34. Lambin EF, Geist HJ, Lepers E, , 2003. Dynamics of land-use and land-cover change in tropical regions. Annu Rev Environ Resour 28: 205241.[Crossref]
  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: 99109.[Crossref]
  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: 224232.[Crossref]
  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, 138.
  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: 16.
  39. Mwalyosi R, , 1981. Ecological changes in Lake Manyara National Park. Afr J Ecol 19: 201204.[Crossref]
  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: 582591.[Crossref]
  41. Musser G, Carleton M, Wilson DE, Reeder DM, , 2005. Order Rodentia. , eds. Mammal Species of the World: A Taxonomic and Geographic Reference, Vol 2. Baltimore, MD: Johns Hopkins University Press, 7451600.
  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: 2375.
  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: 420469.[Crossref]
  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: 348360.[Crossref]
  45. Sikes RS, Gannon WL, , 2011. Guidelines of the American Society of Mammalogists for the use of wild mammals in research. J Mammal 92: 235253.[Crossref]
  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: 10301041.[Crossref]
  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: 463466.
  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: 15491551.[Crossref]
  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, 6163.
  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: 567571.[Crossref]
  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: 23272333.[Crossref]
  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: 492500.[Crossref]
  54. Bahmanyar M, Cavanaugh DC, , 1976. Plague Manual. Geneva, Switzerland: World Health Organization, 176.
  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: 14531459.[Crossref]
  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: 215227.[Crossref]
  57. Gratz N, , 1999. Plague manual: epidemiology, distribution, surveillance and control. World Health Organ Tech Rep Ser 99: 6396.
  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: 949956.
  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: 253257.[Crossref]
  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: 263265.[Crossref]
  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, 339350.[Crossref]
  62. LaDeau SL, Kilpatrick AM, Marra PP, , 2007. West Nile virus emergence and large-scale declines of North American bird populations. Nature 447: 710713.[Crossref]
  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: 975984.[Crossref]
  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: 296299.[Crossref]
  65. Dirzo R, Young H, Galetti M, Ceballos G, Isaac NJB, Collen B, , 2014. Defaunation in the Anthropocene. Science 345: 401406.[Crossref]
  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: 718724.[Crossref]
  67. Schmidt KA, Ostfeld RS, , 2001. Biodiversity and the dilution effect in disease ecology. Ecology 82: 609619.[Crossref]
  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: 699708.[Crossref]
  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: 250259.[Crossref]
  70. Leirs H, Verheyen W, Verhagen R, , 1996. Spatial patterns in Mastomys natalensis in Tanzania (Rodentia, Muridae). Mammalia 60: 545556.[Crossref]
  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: 367375.[Crossref]
  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: 213220.[Crossref]
  73. Leirs H, , 1995. Population ecology of Mastomys natalensis (Smith, 1834) multimammate rats: possible implications for rodent control in Africa. Agricul Ed 35: 1737.
  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: 1721.[Crossref]
  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: 98112.[Crossref]
  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: 435442.[Crossref]
  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.[Crossref]
  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: 687693.[Crossref]
http://instance.metastore.ingenta.com/content/journals/10.4269/ajtmh.14-0504
Loading
/content/journals/10.4269/ajtmh.14-0504
Loading

Data & Media loading...

Supplementary Data

Supplementary PDF

  • Received : 08 Aug 2014
  • Accepted : 14 Jan 2015

Most Cited This Month

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error