Skip to main content
×
×
Home

Effects of anthropogenic and demographic factors on patterns of parasitism in African small mammal communities

  • JOHANNA S. SALZER (a1) (a2) (a3), DARIN S. CARROLL (a2) (a3), AMANDA JO WILLIAMS-NEWKIRK (a1) (a2) (a4), STEFANIE LANG (a2), JULIAN KERBIS PETERHANS (a5) (a6), INNOCENT B. RWEGO (a2) (a7) (a8), SANDRA OCKERS (a7) and THOMAS R. GILLESPIE (a1) (a2) (a7)...
Summary

Habitat disturbance often results in alterations in community structure of small mammals. Additionally, the parasites harboured by these small mammals may be impacted by environmental changes or indirectly affected by changes in available hosts. To improve our understanding of this interplay, we examined the patterns of parasitism in small mammal communities from a variety of habitats in forested Uganda. Small mammals were collected from areas experiencing variable habitat disturbance, host density and species richness. The analysis focused on 3 most abundant rodent species, Lophuromys aquilus, Praomys jacksoni and Hylomyscus stella, and a diverse group of parasites they harbour. The impact of various habitat and host community factors on parasite prevalence was examined using linear regression and Spearman's rank-order correlation. We further investigated the parasite communities associated with each individual using correspondence analysis. We determined that, parasite prevalence and richness may be occasionally influenced by community and habitat factors, but taxonomy is a driving force in influencing the parasite community harboured by an individual host. Ultimately, applying general principles across a broad range of disturbance levels and diverse host communities needs to be approached with caution in complex communities.

Copyright
Corresponding author
* Corresponding author. Program in Population Biology, Ecology, and Evolution, Emory University, 1462 Clifton Road, Atlanta, Georgia 30322, USA; Department of Environmental Sciences, Emory University, 400 Dowman Drive, Atlanta, Georgia 30322, USA; and Department of Environmental Health, Rollins School of Public Health, Emory University, 1518 Clifton Road, Atlanta, Georgia 30322, USA. E-mail: Thomas.Gillespie@emory.edu
References
Hide All
Alvarado-Otegui, J. A., Ceballos, L. A., Orozco, M. M., Enriquez, G. F., Cardinal, M. V., Cura, C., Schijman, A. G., Kitron, U. and Gurtler, R. E. (2012). The sylvatic transmission cycle of Trypanosoma cruzi in a rural area in the humid Chaco of Argentina. Acta Tropica 124, 7986.
Anderson, D. R., Burnham, K. P., White, G. C. and Otis, D. L. (1983). Density-estimation of small-mammal populations using a trapping web and distance sampling methods. Ecology 64, 674680.
Arneberg, P. (2002). Host population density and body mass as determinants of species richness in parasite communities: comparative analyses of directly transmitted nematodes of mammals. Ecography 25, 8894.
Beldomenico, P. M. and Begon, M. (2010). Disease spread, susceptibility and infection intensity: vicious circles? Trends in Ecology and Evolution 25, 2127.
Bellier, E. (2012). D. Borcard, F. Gillet, P. Legendre: Numerical Ecology with R. Journal of Agricultural, Biological, and Environmental Statistics 17, 308309.
Bush, S. E. (2009). Field Guide to Collecting Parasites. Natural History Museum, University of Kansas, Lawrence, Kansas, USA.
Bush, S. E., Reed, M. and Maher, S. (2013). Impact of forest size on parasite biodiversity: implications for conservation of hosts and parasites. Biodiversity and Conservation 22, 13911404.
Chapman, C. A. and Lambert, J. E. (2000). Habitat alteration and the conservation of African primates: case study of Kibale National Park, Uganda. American Journal of Primatology 50, 169185.
Chapman, C. A., Balcomb, S. R., Gillespie, T. R., Skorupa, J. P. and Struhsaker, T. T. (2000). Long-term effects of logging on African primate communities: a 28-year comparison from Kibale National Park, Uganda. Conservation Biology 14, 207217.
Daszak, P., Cunningham, A. A. and Hyatt, A. D. (2000). Wildlife ecology – emerging infectious diseases of wildlife - threats to biodiversity and human health. Science 287, 443449.
Delany, M. J. (1975). The Rodents of Uganda, Trustees of the British Museum (Natural History), London, UK.
Dobigny, G., Poirier, P., Hima, K., Cabaret, O., Gauthier, P., Tatard, C., Costa, J. M. and Bretagne, S. (2011). Molecular survey of rodent-borne Trypanosoma in Niger with special emphasis on T. lewisi imported by invasive black rats. Acta Tropica 117, 183188.
Dobson, A. (2004). Population dynamics of pathogens with multiple host species. American Naturalist 164, S64S78.
Dobson, A., Lafferty, K. D., Kuris, A. M., Hechinger, R. F. and Jetz, W. (2008). Homage to Linnaeus: how many parasites? How many hosts? Proceedings of the National Academy of Sciences of the United States of America 105, 1148211489.
Dranzoa, C. (1998). The avifauna 23 years after logging in Kibale National park, Uganda. Biodiversity and Conservation 7, 777797.
Fain, A. (1994). Adaptation, specificity, and host-parasite coevolution in mites (Acari). International Journal for Parasitology 24, 12731283.
Froeschke, G., van der Mescht, L., McGeoch, M. and Matthee, S. (2013). Life history strategy influences parasite responses to habitat fragmentation. International Journal for Parasitology 43, 11091118.
Gillespie, T. R. and Chapman, C. A. (2006). Prediction of parasite infection dynamics in primate metapopulations based on attributes of forest fragmentation. Conservation Biology 20, 441448.
Gillespie, T. R. and Chapman, C. A. (2008). Forest fragmentation, the decline of an endangered primate, and changes in host–parasite interactions relative to an unfragmented forest. American Journal of Primatology 70, 222230.
Gillespie, T. R., Chapman, C. A. and Greiner, E. C. (2005). Effects of logging on gastrointestinal parasite infections and infection risk in African primates. Journal of Applied Ecology 42, 699707.
Hartter, J. (2009). Attitudes of rural communities toward wetlands and forest fragments around Kibale National Park, Uganda. Human Dimensions of Wildlife 14, 433447.
Hartter, J., Ryan, S. J., Southworth, J. and Chapman, C. A. (2011). Landscapes as continuous entities: forest disturbance and recovery in the Albertine Rift landscape. Landscape Ecology 26, 877890.
Isabirye-Basuta, G. and Kasenene, J. M. (1987). Small rodent populations in selectively felled and mature tracts of Kibale Forest, Uganda. Biotropica 19, 260266.
Johnson, P. T. J., Preston, D. L., Hoverman, J. T. and Richgels, K. L. D. (2013). Biodiversity decreases disease through predictable changes in host community competence. Nature 494, 230233.
Kasenene, J. M. (1984). The influence of selective logging on rodent populations and the regeneration of selected tree species in the Kibale Forest, UgandaTropical Ecology 179195.
Keesing, F., Belden, L. K., Daszak, P., Dobson, A., Harvell, C. D., Holt, R. D., Hudson, P., Jolles, A., Jones, K. E., Mitchell, C. E., Myers, S. S., Bogich, T. and Ostfeld, R. S. (2010). Impacts of biodiversity on the emergence and transmission of infectious diseases. Nature 468, 647652.
Krasnov, B. R., Korallo-Vinarskaya, N. P., Vinarski, M. V., Shenbrot, G. I., Mouillot, D. and Poulin, R. (2008). Searching for general patterns in parasite ecology: host identity versus environmental influence on gamasid mite assemblages in small mammals. Parasitology 135, 229242.
Lafferty, K. D. (2010). Interacting parasites. Science 330, 187188.
Lafferty, K. D. (2012). Biodiversity loss decreases parasite diversity: theory and patterns. Philosophical Transactions of the Royal Society B: Biological Sciences 367, 28142827.
Lane, R. P., Crosskey, R. W. (Ed.) (1993). Medical Insects and Arachnids. Kluwer Academic Publishers, Dordrecht, Netherlands.
Lange, M. (2005). Ecological laws: what would they be and why would they matter? Oikos 110, 394403.
Lawton, J. H. (1999). Are there General Laws in Ecology? Oikos 84, 177192.
Lwanga, J. (1994). The role of seed and seedling predators, and browsers on the regeneration of two forest canopy species (Mimusops Bagshawei and Strombosia Scheffleri) in Kibale Forest, Reserve, Uganda. Ph.D. thesis, University of Florida, Gainsville.
Mills, J. N., Childs, J. E., Ksiazek, T. G. and Peters, C. J. (1995). Methods for Trapping and Sampling Small Mammals for Virologic Testing, US Department of Health and Human Services, Public Health Service, CDC, Atlanta, Georgia.
Mills, J. N., Yates, T. L., Ksiazek, T. G., Peters, C. J. and Childs, J. E. (1999). Long-term studies of hantavirus reservoir populations in the southwestern United States: rationale, potential, and methods. Emerging Infectious Diseases 5, 95101.
Nagorsen, D. W. and Peterson, R. L. (1980). Mammal Collector's Manual. Royal Ontario Museum, Toronto.
Noyes, H. A., Stevens, J. R., Teixeira, M., Phelan, J. and Holz, P. (1999). A nested PCR for the ssrRNA gene detects Trypanosoma binneyi in the platypus and Trypanosoma sp. in wombats and kangaroos in Australia. International Journal for Parasitology 29, 331339.
Noyes, H. A., Ambrose, P., Barker, F., Begon, M., Bennet, M., Bown, K. J. and Kemp, S. J. (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, 185190.
Ostfeld, R. S., Keesing, F. and Eviner, V. T. (2008). Infectious Disease Ecology: Effects of Ecosystems on Disease and of Disease on Ecosystems. Princeton University Press, Princeton, New Jersey, USA.
Peppers, L. L., Carroll, D. S. and Bradley, R. D. (2002). Molecular systematics of the genus Sigmodon (Rodentia: Muridae): evidence from the mitochondrial cytochrome-b gene. Journal of Mammalogy 83, 396407.
Poulin, R. (2007). Are there general laws in parasite ecology? Parasitology 134, 763776.
R Core Team (2013). R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria.
Randolph, S. E. and Dobson, A. D. M. (2012). Pangloss revisited: a critique of the dilution effect and the biodiversity-buffers-disease paradigm. Parasitology 139, 847863.
Roche, B., Dobson, A. P., Guegan, J. F. and Rohani, P. (2012). Linking community and disease ecology: the impact of biodiversity on pathogen transmission. Philosophical Transactions of the Royal Society B: Biological Sciences 367, 28072813.
Salkeld, D. J., Padgett, K. A. and Jones, J. H. (2013). A meta-analysis suggesting that the relationship between biodiversity and risk of zoonotic pathogen transmission is idiosyncratic. Ecology Letters 16, 679686.
Salyer, S. J., Gillespie, T. R., Rwego, I. B., Chapman, C. A. and Goldberg, T. L. (2012). Epidemiology and molecular relationships of Cryptosporidium spp. in people, primates, and livestock from Western Uganda. PLoS Neglected Tropical Diseases 6, e1597.
Salzer, J. S., Rwego, I. B., Goldberg, T. L., Kuhlenschmidt, M. S. and Gillespie, T. R. (2007). Giardia sp and Cryptosporidium sp infections in primates in fragmented and undisturbed forest in western Uganda. Journal of Parasitology 93, 439440.
Salzer, J. S., Carroll, D. S., Rwego, I. B., Li, Y., Falendysz, E. A., Shisler, J. L., Karem, K. L., Damon, I. K. and Gillespie, T. R. (2013). Serologic evidence for circulating Orthopoxviruses in peridomestic rodents from rural Uganda. Journal of Wildlife Diseases 49, 125131.
Seavy, N. E. and Apodaca, C. K. (2002). Raptor abundance and habitat use in a highly-disturbed-forest landscape in western Uganda. Journal of Raptor Research 36, 5157.
Struhsaker, T. T. (1997). Ecology of an African Rain Forest: Logging in Kibale and the Conflict between Conservation and Exploitation. University of Florida, Gainsville, Florida.
Telfer, S., Lambin, X., Birtles, R., Beldomenico, P., Burthe, S., Paterson, S. and Begon, M. (2010). Species interactions in a parasite community drive infection risk in a wildlife population. Science 330, 243246.
Thorn, E. and Kerbis Peterhans, J. (2009). Small Mammals of Uganda, Booner Zoologische Monographien, Bonn, Germany.
Torchin, M. E., Lafferty, K. D., Dobson, A. P., McKenzie, V. J. and Kuris, A. M. (2003). Introduced species and their missing parasites. Nature 421, 628630.
Woolhouse, M. E. J., Dye, C., Etard, J. F., Smith, T., Charlwood, J. D., Garnett, G. P., Hagan, P., Hii, J. L. K., Ndhlovu, P. D., Quinnell, R. J., Watts, C. H., Chandiwana, S. K. and Anderson, R. M. (1997). Heterogeneities in the transmission of infectious agents: implications for the design of control programs. Proceedings of the National Academy of Sciences of the United States of America 94, 338342.
Young, H., Griffin, R. H., Wood, C. L. and Nunn, C. L. (2013). Does habitat disturbance increase infectious disease risk for primates? Ecology Letters 16, 656663.
Recommend this journal

Email your librarian or administrator to recommend adding this journal to your organisation's collection.

Parasitology
  • ISSN: 0031-1820
  • EISSN: 1469-8161
  • URL: /core/journals/parasitology
Please enter your name
Please enter a valid email address
Who would you like to send this to? *
×

Keywords

Metrics

Altmetric attention score

Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed