Fecal microbiomes of non-human primates in Western Uganda reveal species-specific communities largely resistant to habitat perturbation

American Journal of Primatology

Volumn 76, Issue 4, 2014, Pages 347-354

  Mccord, Aleia I ^a   Chapman, Colin A ^b,c   Weny, Geoffrey ^c   Tumukunde, Alex ^c   Hyeroba, David ^c   Klotz, Kelly ^a   Koblings, Avery S ^a   Mbora, David N M ^d   Cregger, Melissa ^e   White, Bryan A ^e   Leigh, Steven R ^e,f   Goldberg, Tony L ^a,c  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b MCGILL UNIVERSITY   (Canada)

^c MAKERERE UNIVERSITY   (Uganda)

^d WHITTIER COLLEGE   (United States)

^e UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^f UNIVERSITY OF COLORADO   (United States)

Author keywords

Cercopithecinae; Colobinae; Forest fragmentation; Microbiome; Non human primate; Uganda

Indexed keywords

CATTLE; FECES; FOREST; HABITAT; HABITAT FRAGMENTATION; LIVESTOCK; MEDICINE; MICROBIAL COMMUNITY; NATIONAL PARK; PERTURBATION; PHYSIOLOGY; PRIMATE; RELATEDNESS; SHEEP;

KENYA; KIBALE NATIONAL PARK; UGANDA;

ANIMALIA; BOS; BOS INDICUS; CAPRA HIRCUS; CERCOPITHECINAE; CERCOPITHECUS; CERCOPITHECUS ASCANIUS; COLOBINAE; COLOBUS; COLOBUS GUEREZA; OVIS ARIES; PRIMATES; PROCOLOBUS BADIUS; PROCOLOBUS RUFOMITRATUS; SUIDAE; SUS SCROFA;

BACTERIAL DNA;

ANIMAL; ARTICLE; CATTLE; CERCOPITHECUS; COLOBINAE; ECOSYSTEM; FECES; FOREST FRAGMENTATION; GENETICS; GOAT; HUMAN; MICROBIOLOGY; MICROBIOME; MICROFLORA; NON-HUMAN PRIMATE; SHEEP; SWINE; TREE; UGANDA;

CERCOPITHECINAE; COLOBINAE; FOREST FRAGMENTATION; MICROBIOME; NON-HUMAN PRIMATE; UGANDA;

ANIMALS; CATTLE; CERCOPITHECUS; COLOBUS; DNA, BACTERIAL; ECOSYSTEM; FECES; GOATS; HUMANS; MICROBIOTA; SHEEP; SWINE; TREES; UGANDA;

EID: 84895928084     PISSN: 02752565     EISSN: 10982345     Source Type: Journal    
DOI: 10.1002/ajp.22238     Document Type: Article

References (61)

1. Adams DA, Riggs MM, Donskey CJ. 2007. Effect of fluoroquinolone treatment on growth of and toxin production by epidemic and nonepidemic Clostridium difficile strains in the cecal contents of mice. Antimicrob Agents Chemother 51:2674-2678.
2. Amato KR, Yeoman CJ, Kent A, et al. 2013. Habitat degradation impacts black howler monkey (Alouatta pigra) gastrointestinal microbiomes. ISME J 7:1344-1353.
3. Arumugam M, Raes J, Pelletier E, et al. 2011. Enterotypes of the human gut microbiome. Nature 473:174.
4. Banks JC, Cary SC, Hogg ID. 2009. The phylogeography of Adelie penguin faecal flora. Environ Microbiol 11:577-588.
5. Bonnell TR, Sengupta RR, Chapman CA, Goldberg TL. 2010. An agent-based model of red colobus resources and disease dynamics implicates key resource sites as hot spots of disease transmission. Ecol Model 221:2491-2500.
6. Caporaso JG, Lauber CL, Costello EK, et al. 2011. Moving pictures of the human microbiome. Genome Biol 12:R50.
7. Chapman CA, Pavelka MS. 2005. Group size in folivorous primates: ecological constraints and the possible influence of social factors. Primates 46:1-9.
8. Chapman CA, Wasserman MD, Gillespie TR, et al. 2006. Do food availability, parasitism, and stress have synergistic effects on red colobus populations living in forest fragments? Am J Phys Anthropol 131:525-534.
9. Chapman CA, Ghai R, Jacob A, et al. 2012. Going, going, gone: a 15-year history of the decline of primates in forest fragments near Kibale National Park, Uganda. In: Marsh LK, editor. Primates in fragments. New York: Springer.
10. Chaves KE, Arroyo-Rodrigues VA. 2012. Differences in diet between spider monkey groups living in forest fragments and continuous forest in Mexico. Biotropica 44:105-113.
11. Chivers DJ. 1994. Functional anatomy of the gastrointestinal tract. In: Davies AG, Oates JF, editors. Colobine monkeys: Their ecology, behaviour and evolution. Cambridge: Cambridge University Press. p 205-228.
12. Clarke RN. 2001. PRIMER v5: user manual/tutorial, PRIMER-E. Plymouth, UK. p 91.
13. Costello EK, Lauber CL, Hamady M, et al. 2009. Bacterial community variation in human body habitats across space and time. Science 326:1694-1697.
14. Croswell A, Amir E, Teggatz P, Barman M, Salzman NH. 2009. Prolonged impact of antibiotics on intestinal microbial ecology and susceptibility to enteric Salmonella infection. Infect Immun 77:2741-2753.
15. Degnan PH, Pusey AE, Lonsdorf EV, et al. 2012. Factors associated with the diversification of the gut microbial communities within chimpanzees from Gombe National Park. Proc Natl Acad Sci USA 109:13034-13039.
16. Dethlefsen L, McFall-Ngai M, Relman DA. 2007. An ecological and evolutionary perspective on human-microbe mutualism and disease. Nature 449:811-818.
17. Dillon RJ, Vennard CT, Buckling A, Charnley AK. 2005. Diversity of locust gut bacteria protects against pathogen invasion. Ecol Lett 8:1291-1298.
18. Dominguez-Bello MG, Blaser MJ, Ley RE, Knight R. 2011. Development of the human gastrointestinal microbiota and insights from high-throughput sequencing. Gastroenterology 140:1713-1719.
19. Eckburg PB, Bik EM, Bernstein CN, urdom E, Dethlefesen L, Sargent M, Gill SR, Nelon KE, Relman DA. 2005. Diversity of the human intestinal microbial flora. Science 308:1635.
20. Ezenwa VO, Gerardo NM, Inouye DW, Medina M, Xavier JB. 2012. Animal behavior and the microbiome. Science 338:198-199.
21. Fisher MM, Triplett EW. 1999. Automated approach for ribosomal intergenic spacer analysis of microbial diversity and its application to freshwater bacterial communities. Appl Environ Microb 65:4630-4636.
22. Frey JC, Rothman JM, Pell AN, et al. 2006. Fecal bacterial diversity in a wild gorilla. Appl Environ Microb 72:3788-3792.
23. Goldberg TL, Gillespie TR, Rwego IB, Estoff EL, Chapman CA. 2008. Forest fragmentation and bacterial transmission among nonhuman primates, humans, and livestock, Uganda. Emerg Infect Dis 14:1375.
24. Goldberg TL, Paige SB, Chapman CA. 2012. The Kibale EcoHealth Project: exploring connections among human health, animal health, and landscape dynamics in western Uganda. In: Aguirre AA, Daszak P, Ostfeld RS, editors. New directions in conservation medicine: applied cases of ecological health. New York: Oxford University Press. p 452-465.
25. Groves CP. 2007. The taxonomic diversity of the Colobinae of Africa. J Anthropol Sci 85:7-34.
26. Johnston AR, Gillespie TR, Rwego IB, et al. 2010. Molecular epidemiology of cross-species Giardia duodenalis transmission in Western Uganda. PLoS Negl Trop Dis 4:e683.
27. Jones SE, McMahon KD. 2009. Species-sorting may explain an apparent minimal effect of immigration on freshwater bacterial community dynamics. Environ Microbiol 11:905-913.
28. Kliks MM. 1990. Helminths as heirlooms and souvenirs-a review of New-World paleoparasitology. Parasitol Today 6:93-100.
29. Koch H, Schmid-Hempel P. 2011. Socially transmitted gut microbiota protect bumble bees against an intestinal parasite. Proc Natl Acad Sci USA 108:19288-19292.
30. Koenig JE, Spor A, Scalfone N, et al. 2011. Succession of microbial consortia in the developing infant gut microbiome. Proc Natl Acad Sci US A108:4578-4585.
31. Ley RE, Hamady M, Lozupone C, et al. 2008a. Evolution of mammals and their gut microbes. Science 320:1647-1651.
32. Ley RE, Lozupone CA, Hamady M, Knight R, Gordon JI. 2008b. Worlds within worlds: evolution of the vertebrate gut microbiota. Nat Rev Microbiol 6:776-788.
33. McFall-Ngai MJ. 2002. Unseen forces: the influence of bacteria on animal development. Dev Biol 242:1-14.
34. McKenna P, Hoffmann C, Minkah N, et al. 2008. The macaque gut microbiome in health, lentiviral infection, and chronic enterocolitis. PLoS Pathog 4:e20.
35. McKenzie VJ, Bowers RM, Fierer N, Knight R, Lauber CL. 2012. Co-habiting amphibian species harbor unique skin bacterial communities in wild populations. ISME J 6:588-596.
36. Moran NA, McCutcheon JP, Nakabachi A. 2008. Genomics and evolution of heritable bacterial symbionts. Annu Rev Genet 42:165-190.
37. Muegge BD, Kuczynski J, Knights D, et al. 2011. Diet drives convergence in gut microbiome functions across mammalian phylogeny and within humans. Science 332:970-974.
38. Ochman H, Worobey M, Kuo CH, et al. 2010. Evolutionary relationships of wild hominids recapitulated by gut microbial communities. PLoS Biol 8:e1000546.
39. Onderdonk DA, Chapman CA. 2000. Coping with forest fragmentation: the primates of Kibale National Park, Uganda. Int J Primatol 21:587-611.
40. Owino AO, Oyugi JO. 2010. Assessment of forest patches' extents and land cover changes in the Tana River Primate National Reserve, 1994-2004. Afr J Ecol 48:546-550.
41. Perelman P, Johnson WE, Roos C, Seuanez HN, Horvath JE, Moreira MA, Kessing B, Pontius J, Roelke M, Rumpler Y, Schneider MP, Silva A, O'Brien SJ, Pecon-Slattery J. 2011. A molecular phylogeny of living primates. PLoS Genet 7:e1001342.
42. Phillips CD, Phelan G, Dowd SE, et al. 2012. Microbiome analysis among bats describes influences of host phylogeny, life history, physiology and geography. Mol Ecol 21:2617-2627.
43. Ramette A. 2007. Multivariate analyses in microbial ecology. FEMS Microbiol Ecol 62:142-160.
44. Robinson CJ, Bohannan BJM, Young VB. 2010. From structure to function: the ecology of host-associated microbial communities. Microbiol Mol Biol Rev 74:453.
45. Round JL, Mazmanian SK. 2009. The gut microbiota shapes intestinal immune responses during health and disease. Nat Rev Immunol 9:313.
46. Rwego IB, Gillespie TR, Isabirye-Basuta G, Goldberg TL. 2008. High rates of Escherichia coli transmission between livestock and humans in rural Uganda. J Clin Microbiol 46:3187-3191.
47. Salyer SJ, Gillespie TR, Rwego IB, Chapman CA, Goldberg TL. 2012. Epidemiology and molecular relationships of Cryptosporidium spp. in people, primates, and livestock from Western Uganda. PLoS Negl Trop Dis 6:e1597.
48. Salzer JS, Rwego IB, Goldberg TL, Kuhlenschmidt MS, Gillespie TR. 2007. Giardia sp and Cryptosporidium sp infections in primates in fragmented and undisturbed forest in Western Uganda. J Parasitol 93:439-440.
49. Shendure J, Ji HL. 2008. Next-generation DNA sequencing. Nat Biotechnol 26:1135-1145.
50. Smith P, Siddharth J, Pearson R, et al. 2012. Host genetics and environmental factors regulate ecological succession of the mouse colon tissue-associated microbiota. PLoS ONE 7:e30273.
51. Spor A, Koren O, Ley R. 2011. Unravelling the effects of the environment and host genotype on the gut microbiome. Nat Rev Microbiol 9:279-290.
52. Szekely BA, Singh J, Marsh TL, et al. 2010. Fecal bacterial diversity of human-habituated wild chimpanzees (Pan troglodytes schweinfurthii) at Mahale Mountains National Park, Western Tanzania. Am J Primatol 72:566-574.
53. Turnbaugh PJ, Ley RE, Hamady M, et al. 2007. The human microbiome project. Nature 449:804-810.
54. Turnbaugh PJ, Hamady M, Yatsunenko T, et al. 2009. A core gut microbiome in obese and lean twins. Nature 457:480-484.
55. Uenishi G, Fujita S, Ohashi G, et al. 2007. Molecular analyses of the intestinal microbiota of chimpanzees in the wild and in captivity. Am J Primatol 69:367-376.
56. Ursell LK, Metcalf JL, Parfrey LW, Knight R. 2012. Defining the human microbiome. Nutr Rev 70:S38-S44.
57. Walter J, Ley R. 2011. The human gut microbiome: ecology and recent evolutionary changes. In: Gottesman S, Harwood CS, editors. Annual review of microbiology, Vol. 65. Palo Alto: Annual Reviews. p 411-429.
58. Weins JA. 1995. Habitat fragmentation: island v landscape perspectives on bird conservation. IBIS 137:S97-S104.
59. Xu B, Huang ZX, Wang XY, et al. 2010. Phylogenetic analysis of the fecal flora of the wild pygmy loris. Am J Primatol 72:699-706.
60. Yeoman CJ, Chia N, Yildirim S, et al. 2011. Towards an evolutionary model of animal-associated microbiomes. Entropy 13:570-594.
61. Yildirim S, Yeoman CJ, Sipos M, et al. 2010. Characterization of the fecal microbiome from non-human wild primates reveals species specific microbial communities. PLoS ONE 5:e13963.