Abstract
Habitat disturbance and anthropogenic change are globally associated with extinctions and invasive species introductions. Less understood is the impact of environmental change on the parasites harbored by endangered, extinct, and introduced species. To improve our understanding of the impacts of anthropogenic disturbance on such host–parasite interactions, we investigated an invasive trypanosome (Trypanosoma lewisi). We screened 348 individual small mammals, representing 26 species, from both forested and non-forested habitats in rural Uganda. Using microscopy and PCR, we identified 18% of individuals (order Rodentia) as positive for trypanosomes. Further phylogenetic analyses revealed two trypanosomes circulating—T. lewisi and T. varani. T. lewisi was found in seven species both native and invasive, while T. varani was identified in only three native forest species. The lack of T. varani in non-forested habitats suggests that it is a natural parasite of forest-dwelling rodents. Our findings suggest that anthropogenic disturbance may lead to spillover of an invasive parasite (T. lewisi) from non-native to native species, and lead to local co-extinction of a native parasite (T. varani) and native forest-dwelling hosts.
Similar content being viewed by others
R eferences
Adams ER, Hamilton PB, Gibson WC (2010) African trypanosomes: celebrating diversity. Trends in Parasitology 26:324–328
Altizer S, Nunn CL, Lindenfors P (2007) Do threatened hosts have fewer parasites? A comparative study in primates. Journal of Animal Ecology 76:304–314
Anderson RM, May RM (1979) Population biology of infectious diseases: Part I. Nature 280:361–367
Averis S, Thompson RCA, Lymbery AJ, Wayne AF, Morris KD, Smith A (2009) The diversity, distribution and host–parasite associations of trypanosomes in Western Australian wildlife. Parasitology 136:1269–1279
Bush SE, Reed M, Maher S (2013) Impact of forest size on parasite biodiversity: implications for conservation of hosts and parasites. Biodiversity and Conservation 22:1391–1404
Carleton MD, Musser GG (2005) Order Rodentia. In: Mammal Species of the World: A Taxonomic and Geographic Reference, Wilson DE, Reeder DM (editors), Baltimore, MD: Johns Hopkins University Press, pp 745–752
Chapman CA, Balcomb SR, Gillespie TR, Skorupa JP, Struhsaker TT (2000) Long-term effects of logging on African primate communities: a 28-year comparison from Kibale National Park, Uganda. Conservation Biology 14:207–217
Chasar A, Loiseau UC, Valkiunas G, Iezhova T, Smith TB, Sehgal RNM (2009) Prevalence and diversity patterns of avian blood parasites in degraded African rainforest habitats. Molecular Ecology 18:4121–4133
Cottontail VM, Kalko EKV, Cottontail I, Wellinghausen N, Tschapka M, Perkins SL, et al. (2014) High local diversity of Trypanosoma in a common bat species, and implications for the biogeography and taxonomy of the T. cruzi clade. PLoS One 9:e108603
Delany MJ (1975) The Rodents of Uganda, London, UK: Trustees of the British Museum (Natural History)
Dobigny G, Poirier P, Hima K, Cabaret O, Gauthier P, Tatard C, et al. (2011) Molecular survey of rodent-borne Trypanosoma in Niger with special emphasis on T. lewisi imported by invasive black rats. Acta Tropica 117:183–188
Dobson A, Lafferty KD, Kuris AM, Hechinger RF, Jetz W (2008) Homage to Linnaeus: How many parasites? How many hosts? Proceedings of the National Academy of Sciences of USA 105:11482–11489
Drummond AJ, Ashton B, Buxton S, Cheung M, Cooper A, Duran C, et al. (2010) Geneious v5.5. Available: http://www.geneious.com
Dunn RR, Harris NC, Colwell RK, Koh LP, Sodhi NS (2009) The sixth mass coextinction: Are most endangered species parasites and mutualists? Proceedings of the Royal Society B: Biological Sciences 276:3037–3045
Dunne JA, Lafferty KD, Dobson AP, Hechinger RF, Kuris AM, Martinez ND, et al. (2013) Parasites affect food web structure primarily through increased diversity and complexity. PLoS Biology 11:e1001579
Gillespie TR, Chapman CA (2006) Prediction of parasite infection dynamics in primate metapopulations based on attributes of forest fragmentation. Conservation Biology 20:441–448
Hamilton PB, Gibson WC, Stevens JR (2007) Patterns of co-evolution between trypanosomes and their hosts deduced from ribosomal RNA and protein-coding gene phylogenies. Molecular Phylogenetics and Evolution 44:15–25
Hartter J (2009) Attitudes of rural communities toward wetlands and forest fragments around Kibale National Park, Uganda. Human Dimensions of Wildlife 14:433–447
Hoare CA (1972) The Trypanosomas of Mammals, Oxford, UK: Blackwell Scientific Publications
Keesing F, Holt RD, Ostfeld RS (2006) Effects of species diversity on disease risk. Ecology Letters 9:485–498
Koh LP, Dunn RR, Sodhi NS, Colwell RK, Proctor HC, Smith VS (2004) Species coextinctions and the biodiversity crisis. Science 305:1632–1634
May RM, Anderson RM (1991) Infectious Diseases of Humans: Dynamics and Control, Oxford, UK: Oxford University Press.
McCauley DJ, Salkeld DJ, Young HS, Makundi R, Dirzo R, Eckerlin RP, Lambin EF, Gaffikin L, Barry M, Helgen KM (2015) Effects of land use on plague (Yersinia pestis) activity in rodents in Tanzania. American Journal of Tropical Medicine and Hygiene 92:776–783
Mills JN, Yates TL, Ksiazek TG, Peters CJ, Childs JE (1999) Long-term studies of hantavirus reservoir populations in the southwestern United States: rationale, potential, and methods. Emerging Infectious Diseases 5:95–101
Milocco C, Kamyingkird K, Desquesnes M, Jittapalapong S, Herbreteau V, Chaval Y, et al. (2013) Molecular demonstration of Trypanosoma evansi and Trypanosoma lewisi DNA in wild rodents from Cambodia, Lao PDR and Thailand. Transboundary and Emerging Diseases 60:17–26
Molyneux DH (1969) Intracellular stages of Trypanosoma lewisi in fleas and attempts to find such stages in other trypanosome species. Parasitology 59:669–674
Noyes HA, Ambrose P, Barker F, Begon M, Bennet M, Bown KJ, et al. (2002) Host specificity of Trypanosoma (Herpetosoma) species: evidence that bank voles (Clethrionomys glareolus) carry only one T. (H.) evotomys 18S rRNA genotype but wood mice (Apodemus sylvaticus) carry at least two polyphyletic parasites. Parasitology 124:185–190
Pedersen AB, Jones KE, Nunn CL, Altizer S (2007) Infectious diseases and extinction risk in wild mammals. Conservation Biology 21:1269–1279
Peppers LL, Carroll DS, Bradley RD (2002). Molecular systematics of the genus Sigmodon (Rodentia: Muridae): evidence from the mitochondrial cytochrome-b gene. Journal of Mammalogy 83:396–407
Pinto CM, Ocana-Mayorga S, Lascano MS, Grijalva MJ (2006) Infection by trypanosomes in marsupials and rodents associated with human dwellings in Ecuador. Journal of Parasitology 92:1251–1255
Pinto CM, Kalko EK, Cottontail I, Wellinghausen N, Cottontail VM (2012) TcBat a bat-exclusive lineage of Trypanosoma cruzi in the Panama Canal Zone, with comments on its classification and the use of the 18S rRNA gene for lineage identification. Infection, Genetics and Evolution 12:1328–1332
Pumhom P, Pognon D, Yangtara S, Thaprathorn N, Milocco C, Douangboupha B, et al. (2014) Molecular prevalence of Trypanosoma spp. in wild rodents of Southeast Asia: influence of human settlement habitat. Epidemiology and Infection 142:1221–1230
Randolph SE, Dobson ADM (2012) Pangloss revisited: a critique of the dilution effect and the biodiversity-buffers-disease paradigm. Parasitology 139:847–863
Salkeld DJ, Padgett KA, Jones JH (2013) A meta-analysis suggesting that the relationship between biodiversity and risk of zoonotic pathogen transmission is idiosyncratic. Ecology Letters 16:679–686
Salzer JS, Carroll DS, Williams-Newkirk AJ, Lang S, Peterhans JK, Rwego IB, et al. (2015) Effects of anthropogenic and demographic factors on patterns of parasitism in African small mammal communities. Parasitology 142:512–522
Sato H, Ishita K, Matsuo K, Inaba T, Kamiya H, Ito M (2003) Persistent infection of Mongolian jirds with a non-pathogenic trypanosome, Trypanosoma (Herpetosoma) grosi. Parasitology 127:357–363
Sato H, Takano A, Kawabata H, Une Y, Watanabe H, Mukhtar MM (2009) Trypanosoma cf. varani in an imported ball python (Python reginus) from Ghana. Journal of Parasitology 95:1029–1033
Stamatakis A, Ludwig T, Meier H (2005) RAxML-II: a program for sequential, parallel and distributed inference of large phylogenetic. Concurrency and Computation: Practice and Experience 17:1705–1723
Struhsaker TT (1997) Ecology of an African Rain Forest: Logging in Kibale and the Conflict Between Conservation and Exploitation, Gainesville, FL: University of Florida Press
Truc P, Büscher P, Cuny G, Gonzatti MI, Jannin J, Joshi P, et al. (2013) Atypical human infections by animal trypanosomes. PLoS Neglected Tropical Diseases 7:e2256
Verma A, Manchanda S, Kumar N, Sharma A, Goel M, Banerjee PS, et al. (2011) Case report: Trypanosoma lewisi or T. lewisi-like infection in a 37-day-old Indian infant. American Journal of Tropical Medicine and Hygiene 85:221–224
Verneau O, Palacios C, Platt T, Alday M, Billard E, Allienne JF, et al. (2011) Invasive species threat: parasite phylogenetics reveals patterns and processes of host-switching between non-native and native captive freshwater turtles. Parasitology 138:1778–1792
Wanyonyi MG, Ng’wena AGM, Ngeiywa MM (2011) Prevalence of Trypanosoma and Plasmodium species’ parasites in small rodents of Kakamega Forest in western Kenya. African Journal of Health Sciences 19:61–67
Wenyon CM (1908) Report of the travelling pathologist and protozoologist. In: Third Report of the Wellcome Research Laboratories of the Gordon Memorial College, Balfour KAB (editor), London, UK: Tindall, Cox, pp 121–168
Wyatt KB, Campos PF, Gilbert MTP, Kolokotronis S-O, Hynes WH, DeSalle R, et al. (2008) Historical mammal extinction on Christmas Island (Indian Ocean) correlates with introduced infectious disease. PLoS One 3:e3602
Young H, Griffin RH, Wood CL, Nunn CL (2013) Does habitat disturbance increase infectious disease risk for primates? Ecology Letters 16:656–663
Young HS, Dirzo R, Helgen KM, McCauley DJ, Billeter SA, Kosoy MY, et al. (2014) Declines in large wildlife increase landscape-level prevalence of rodent-borne disease in Africa. Proceedings of the National Academy of Sciences of USA 111:7036–7041
Zhang J, Kapli P, Pavlidis P, Stamatakis A (2013) A general species delimitation method with applications to phylogenetic placements. Bioinformatics 29:2869–2876
A cknowledgments
This research was supported in part by the Emory Global Health Institute, Emory University Environmental Science Department, and the appointment of J.S.S. to the Research Participation Program administered by Oak Ridge Institute for Science and Education (ORISE) through an Interagency Agreement with CDC. The authors thank the Uganda Wildlife Authority, Uganda National Council for Science and Technology, Makerere University Biological Field Station and local authorities for permission to conduct this study. The authors are thankful to J. de Roode for his encouragement and interests in investigating blood-borne pathogens. The authors thank S. Ockers, C. Akora, and I. Mwesige who provided valuable assistance in the field and K. Cross for assistance in the laboratory. The authors also thank S. L. Perkins, J. N. Mills, I. K. Damon, W. Stanley, U. Kitron, R. R. Lash, and S. P. Montgomery for helpful comments, logistical, and/or analytical assistance.
Author information
Authors and Affiliations
Corresponding author
Additional information
The views expressed in this paper are solely those of the authors and do not represent those of the CDC, US Government, or any other entity which the authors may be affiliates.
Rights and permissions
About this article
Cite this article
Salzer, J.S., Pinto, C.M., Grippi, D.C. et al. Impact of Anthropogenic Disturbance on Native and Invasive Trypanosomes of Rodents in Forested Uganda. EcoHealth 13, 698–707 (2016). https://doi.org/10.1007/s10393-016-1160-6
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10393-016-1160-6