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

Published online by Cambridge University Press:  29 September 2014

JOHANNA S. SALZER ,
DARIN S. CARROLL ,
AMANDA JO WILLIAMS-NEWKIRK ,
STEFANIE LANG ,
JULIAN KERBIS PETERHANS ,
INNOCENT B. RWEGO ,
SANDRA OCKERS  and
THOMAS R. GILLESPIE
JOHANNA S. SALZER
Affiliation:
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 Poxvirus and Rabies Branch, Division of High-Consequence Pathogens and Pathology, Centers for Disease Control and Prevention, 1600 Clifton Road, Atlanta, Georgia 30333, USA
DARIN S. CARROLL
Affiliation:
Department of Environmental Sciences, Emory University, 400 Dowman Drive, Atlanta, Georgia 30322, USA Poxvirus and Rabies Branch, Division of High-Consequence Pathogens and Pathology, Centers for Disease Control and Prevention, 1600 Clifton Road, Atlanta, Georgia 30333, USA
AMANDA JO WILLIAMS-NEWKIRK
Affiliation:
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 Rickettsial Zoonoses Branch, Division of Vector-borne Diseases, Centers for Disease Control and Prevention, 1600 Clifton Road, Atlanta, Georgia 30333, USA
STEFANIE LANG
Affiliation:
Department of Environmental Sciences, Emory University, 400 Dowman Drive, Atlanta, Georgia 30322, USA
JULIAN KERBIS PETERHANS
Affiliation:
College of Professional Studies, Roosevelt University, 430 South Michigan Avenue, Chicago, Illinois 60605, USA Field Museum of Natural History, 1400 South Lake Shore Drive, Chicago, Illinois 60605, USA
INNOCENT B. RWEGO
Affiliation:
Department of Environmental Sciences, Emory University, 400 Dowman Drive, Atlanta, Georgia 30322, USA Department of Environmental Health, Rollins School of Public Health, Emory University, 1518 Clifton Road, Atlanta, Georgia 30322, USA Department of Biological Sciences, Makerere University, Kampala, Uganda
SANDRA OCKERS
Affiliation:
Department of Environmental Health, Rollins School of Public Health, Emory University, 1518 Clifton Road, Atlanta, Georgia 30322, USA
THOMAS R. GILLESPIE*
Affiliation:
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 Department of Environmental Health, Rollins School of Public Health, Emory University, 1518 Clifton Road, Atlanta, Georgia 30322, USA
*
* 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
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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.

Keywords

ectoparasitesfleasGiardiaKibale National ParklicemitesPraomysrodenttickstrypanosome
Type
Research Article
Information
Parasitology , Volume 142 , Issue 3 , March 2015 , pp. 512 - 522
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Copyright
Copyright © Cambridge University Press 2014 

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References

REFERENCES

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, 79–86.CrossRefGoogle Scholar
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, 674–680.CrossRefGoogle Scholar
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, 88–94.CrossRefGoogle Scholar
Beldomenico, P. M. and Begon, M. (2010). Disease spread, susceptibility and infection intensity: vicious circles? Trends in Ecology and Evolution 25, 21–27.Google Scholar
Bellier, E. (2012). D. Borcard, F. Gillet, P. Legendre: Numerical Ecology with R. Journal of Agricultural, Biological, and Environmental Statistics 17, 308–309.Google Scholar
Bush, S. E. (2009). Field Guide to Collecting Parasites. Natural History Museum, University of Kansas, Lawrence, Kansas, USA.Google Scholar
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, 1391–1404.Google Scholar
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, 169–185.Google Scholar
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, 207–217.Google Scholar
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, 443–449.Google Scholar
Delany, M. J. (1975). The Rodents of Uganda, Trustees of the British Museum (Natural History), London, UK.Google Scholar
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, 183–188.Google Scholar
Dobson, A. (2004). Population dynamics of pathogens with multiple host species. American Naturalist 164, S64–S78.Google Scholar
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, 11482–11489.Google Scholar
Dranzoa, C. (1998). The avifauna 23 years after logging in Kibale National park, Uganda. Biodiversity and Conservation 7, 777–797.Google Scholar
Fain, A. (1994). Adaptation, specificity, and host-parasite coevolution in mites (Acari). International Journal for Parasitology 24, 1273–1283.CrossRefGoogle ScholarPubMed
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, 1109–1118.Google Scholar
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, 441–448.Google Scholar
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, 222–230.Google Scholar
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, 699–707.CrossRefGoogle Scholar
Hartter, J. (2009). Attitudes of rural communities toward wetlands and forest fragments around Kibale National Park, Uganda. Human Dimensions of Wildlife 14, 433–447.Google Scholar
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, 877–890.CrossRefGoogle Scholar
Isabirye-Basuta, G. and Kasenene, J. M. (1987). Small rodent populations in selectively felled and mature tracts of Kibale Forest, Uganda. Biotropica 19, 260–266.Google Scholar
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, 230–233.Google Scholar
Kasenene, J. M. (1984). The influence of selective logging on rodent populations and the regeneration of selected tree species in the Kibale Forest, Uganda.  Tropical Ecology 179–195.Google Scholar
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, 647–652.Google Scholar
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, 229–242.Google Scholar
Lafferty, K. D. (2010). Interacting parasites. Science 330, 187–188.Google Scholar
Lafferty, K. D. (2012). Biodiversity loss decreases parasite diversity: theory and patterns. Philosophical Transactions of the Royal Society B: Biological Sciences 367, 2814–2827.CrossRefGoogle ScholarPubMed
Lane, R. P., Crosskey, R. W. (Ed.) (1993). Medical Insects and Arachnids. Kluwer Academic Publishers, Dordrecht, Netherlands.Google Scholar
Lange, M. (2005). Ecological laws: what would they be and why would they matter? Oikos 110, 394–403.Google Scholar
Lawton, J. H. (1999). Are there General Laws in Ecology? Oikos 84, 177–192.CrossRefGoogle Scholar
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.Google Scholar
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.Google Scholar
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, 95–101.Google Scholar
Nagorsen, D. W. and Peterson, R. L. (1980). Mammal Collector's Manual. Royal Ontario Museum, Toronto.CrossRefGoogle Scholar
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, 331–339.Google Scholar
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, 185–190.CrossRefGoogle Scholar
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.Google Scholar
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, 396–407.Google Scholar
Poulin, R. (2007). Are there general laws in parasite ecology? Parasitology 134, 763–776.CrossRefGoogle ScholarPubMed
R Core Team (2013). R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria.Google Scholar
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, 847–863.CrossRefGoogle ScholarPubMed
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, 2807–2813.Google Scholar
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, 679–686.Google Scholar
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.Google Scholar
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, 439–440.Google Scholar
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, 125–131.Google Scholar
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, 51–57.Google Scholar
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.Google Scholar
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, 243–246.Google Scholar
Thorn, E. and Kerbis Peterhans, J. (2009). Small Mammals of Uganda, Booner Zoologische Monographien, Bonn, Germany.Google Scholar
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, 628–630.Google Scholar
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, 338–342.CrossRefGoogle ScholarPubMed
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, 656–663.Google Scholar