International Journal of Primatology

, Volume 33, Issue 2, pp 479–488 | Cite as

Genetic Sampling of Unhabituated Chimpanzees (Pan troglodytes schweinfurthii) in Gishwati Forest Reserve, an Isolated Forest Fragment in Western Rwanda

  • Rebecca L. Chancellor
  • Kevin Langergraber
  • Sergio Ramirez
  • Aaron S. Rundus
  • Linda Vigilant
Article

Abstract

Many primate populations currently live in forest fragments. These populations are often unhabituated, elusive, and contain few individuals, making them difficult to study through direct observation. Noninvasive genetic methods are useful for surveying these unhabituated populations to infer the number and sex of individuals and the genetic diversity of the population. We conducted genetic analysis on 70 fecal samples from eastern chimpanzees (Pan troglodytes schweinfurthii) in Gishwati Forest Reserve, a forest fragment in western Rwanda. We genotyped all but two of these samples using 12 autosomal and 13 Y-chromosome microsatellite markers previously used in analyses of other chimpanzee populations. The genetic data show that these samples represent a minimum of 19 individuals (7 females, 12 males). However, because we may not have sampled all individuals in the population, we also performed mark-recapture analysis with the genetic data and found that the entire population likely numbers between 19 and 29 individuals. These results are consistent with opportunistic observations of at least 19 individual chimpanzees. Levels of variation at the Y-chromosome microsatellites were similar to those observed in other chimpanzee communities, suggesting that the chimpanzees in this forest are members of a single community. These results provide a baseline count of the number of male and female chimpanzees in the Gishwati Forest Reserve, and the data provide the potential for follow-up studies aimed at tracking individuals over time, thus aiding conservation management of this unhabituated population.

Keywords

Genotyping Mark recapture Noninvasive sampling Pan troglodytes schweinfurthii Y-chromosome 

Supplementary material

10764_2012_9591_MOESM1_ESM.docx (31 kb)
ESM 1(DOCX 31 kb)

References

  1. Anderson, J., Rowcliffe, J. M., & Cowlishaw, G. (2007). The Angola black-and-white colobus (Colobus angolensis palliatus) in Kenya: historical range contraction and current conservation status. American Journal of Primatology, 69, 664–680.PubMedCrossRefGoogle Scholar
  2. Arandjelovic, M., Guschanski, K., Schubert, G., Harris, T. R., Thalmann, O., Siedel, H., & Vigilant, L. (2009). Two-step multiplex polymerase chain reaction improves the speed and accuracy of genotyping using DNA from noninvasive and museum samples. Molecular Ecology Resources, 9, 28–36.PubMedCrossRefGoogle Scholar
  3. Arandjelovic, M., Head, J., Kühl, H., Boesch, C., Robbins, M. M., Maisels, F., & Vigilant, L. (2010). Effective non-invasive genetic monitoring of multiple wild western gorilla groups. Biological Conservation, 143, 1780–1791.CrossRefGoogle Scholar
  4. Arandjelovic, M., Head, J., Rabanal, L. I., Schubert, G., Mettke, E., Boesch, C., Robbins, M. M., & Vigilant, L. (2011). Non-invasive genetic monitoring of wild central chimpanzees. PLoS ONE, 6, e14761.PubMedCrossRefGoogle Scholar
  5. Archie, E. A., Moss, C. J., & Alberts, S. C. (2005). The ties that bind: genetic relatedness predicts the fission and fusion of social groups in wild African elephants. Proceedings of the Royal Society B: Biological Sciences, 273, 513–522.CrossRefGoogle Scholar
  6. Arrendal, J., Vila, C., & Bjorklund, M. (2007). Reliability of noninvasive genetic census of otters compared to field censuses. Conservation Genetics, 8, 1097–1107.CrossRefGoogle Scholar
  7. Barakabuye, N., Mulindahabi, F., Plumptre, A. J., Kaplin, B., Munanura, I., Ndagijimana, D., et al. (2007). Conservation of chimpanzees in the Congo-Nile Divide forests of Rwanda and Burundi. Unpublished report to U.S. Fish and Wildlife Service. No. 98210-G- GO95/GA 0282.Google Scholar
  8. Baranga, D., Chapman, C. A., & Kasenene, J. M. (2009). The structure and status of forest fragments outside protected areas in central Uganda. African Journal of Ecology, 47, 664–669.CrossRefGoogle Scholar
  9. Bergl, R. A., & Vigilant, L. (2007). Genetic analysis reveals population structure and recent migration within the highly fragmented range of the Cross River gorilla (Gorilla gorilla diehli). Molecular Ecology, 16, 501–516.PubMedCrossRefGoogle Scholar
  10. Bergl, R., Bradley, B. J., Nsubuga, A. M., & Vigilant, L. (2008). Genetic effects of habitat fragmentation, population size and demographic history on primate populations: the Cross River gorilla in a comparative context. American Journal of Primatology, 70, 848–859.PubMedCrossRefGoogle Scholar
  11. Bertolani, P., & Boesch, C. (2008). Habituation of wild chimpanzees (Pan troglodytes) of the South Group at Taï Forest, Côte d’Ivoire: empirical measure of progress. Folia Primatologica, 79, 162–171.CrossRefGoogle Scholar
  12. Blom, A., Cipolletta, C., Brunsting, A. M. H., & Prins, H. H. T. (2004). Behavioral responses of gorillas to habituation in the Dzanga-Ndoki National Park, Central African Republic. International Journal of Primatology, 25, 179–196.CrossRefGoogle Scholar
  13. Boesch, C., Kohou, G., Néné, H., & Vigilant, L. (2006). Male competition and paternity in wild chimpanzees of the Taï forest. American Journal of Physical Anthropology, 130, 103–115.PubMedCrossRefGoogle Scholar
  14. Boesch, C., Head, J., Tagg, N., Arandjelovic, M., Vigilant, L., & Robbins, M. (2007). Fatal chimpanzee attack in Loango National Park, Gabon: Observational and genetic evidence. International Journal of Primatology, 28, 1025–1034.CrossRefGoogle Scholar
  15. Bradley, B. J., Chambers, K., & Vigilant, L. (2001). Accurate DNA-based sex identification of apes using non-invasive samples. Conservation Genetics, 2, 179–181.CrossRefGoogle Scholar
  16. Bradley, B. J., Doran-Sheehy, D. M., & Vigilant, L. (2008). Genetic identification of elusive animals: re-evaluating tracking and nesting data for wild western gorillas. Journal of Zoology, 275, 333–340.CrossRefGoogle Scholar
  17. Chancellor, R. L., Rundus, A. S., & Nyandwi, S. (2012). The influence of seasonal variation on chimpanzee (Pan troglodytes schweinfurthii) fallback food consumption, nest group size, and habitat use in Gishwati, a montane rainforest fragment in Rwanda. International Journal of Primatology, 33, 115–133.Google Scholar
  18. Chapman, C. A., Naughton-Treves, L., Lawes, M. J., Wasserman, M. D., & Gillespie, T. R. (2007). Population declines of colobus in western Uganda and conservation value of forest fragments. International Journal of Primatology, 28, 513–528.CrossRefGoogle Scholar
  19. Cowlishaw, G. (1999). Predicting the pattern of decline of African primate diversity: an extinction debt from historical deforestation. Conservation Biology, 13, 1183–1193.CrossRefGoogle Scholar
  20. Cullen, L., Jr., Bodmerand, R. E., & Pádua, C. V. (2000). Effects of hunting in habitat fragments of the Atlantic forests, Brazil. Biological Conservation, 95, 49–56.CrossRefGoogle Scholar
  21. Doran-Sheehy, D., Derby, A. M., Greer, D., & Mongo, P. (2007). Habituation of western gorillas: the process and factors that influence it. American Journal of Primatology, 69, 1–16.CrossRefGoogle Scholar
  22. Excoffier, L., Laval, G., & Schneider, S. (2005). Arlequin ver. 3.0: an integrated software package for population genetics data analysis. Evolutionary Bioinformatics Online, 1, 47–50.Google Scholar
  23. Frankham, R. (2005). Genetics and extinction. Biological Conservation, 126, 131–140.CrossRefGoogle Scholar
  24. Gibbons, M. A., & Harcourt, A. H. (2009). Biological correlates of extinction and persistence of primates in small forest fragments: a global analysis. Tropical Conservation Science, 2, 388–403.Google Scholar
  25. Goldberg, T. L., & Wrangham, R. W. (1997). Genetic correlates of social behavior in wild chimpanzees: evidence from mitochondrial DNA. Animal Behaviour, 54, 559–570.PubMedCrossRefGoogle Scholar
  26. Goldberg, T. L., Gillespie, T. R., Rwego, I. B., Estoff, E. L., & Chapman, C. A. (2008). Forest fragmentation as cause of bacterial transmission among nonhuman primates, humans, and livestock, Uganda. Emerging Infectious Diseases, 14, 1375–1382.PubMedCrossRefGoogle Scholar
  27. Goossens, B., Setchell, J. M., Vidal, C., Dilambaka, E., & Jamart, A. (2003). Successful reproduction in wild-released orphan chimpanzees (Pan troglodytes troglodytes). Primates, 44, 67–69.PubMedGoogle Scholar
  28. Hájková, P., Zemanová, B., Roche, K., & Hájek, B. (2009). An evaluation of field and noninvasive genetic methods for estimating Eurasian otter population size. Conservation Genetics, 10, 1667–1681.CrossRefGoogle Scholar
  29. Johns, B. G. (1996). Responses of chimpanzees to habituation and tourism in the Kibale Forest, Uganda. Biological Conservation, 78, 257–262.CrossRefGoogle Scholar
  30. Johnson, W. E., Onorato, D. P., Roelke, M. E., Land, E. D., Cunningham, M., Belden, R. C., McBride, R., Jansen, D., Lotz, M., Shindle, D., Howard, J., Wildt, D. E., Penfold, L. M., Hostetler, J. A., Oli, M. K., & O’Brien, S. J. (2010). Genetic restoration of the Florida panther. Science, 24, 1641–1645.CrossRefGoogle Scholar
  31. Kohn, M. H., & Wagne, R. K. (1997). Facts from feces revisited. Trends in Ecology and Evolution, 12, 223–227.PubMedCrossRefGoogle Scholar
  32. Lacy, R. C. (1997). The importance of genetic variation to the viability of mammalian populations. Journal of Mammalogy, 78, 320–335.CrossRefGoogle Scholar
  33. Lande, R., & Barrowclough, G. (1987). Effective population size, genetic variation and their use in population management. In M. E. Soulé (Ed.), Viable populations for conservation (pp. 87–124). New York: Cambridge University Press.CrossRefGoogle Scholar
  34. Langergraber, K. E., Siedel, H., Mitani, J. C., Wrangham, R. W., Reynolds, V., Hunt, K. D., & Vigilant, L. (2007a). The genetic signature of sex-biased migration in patrilocal chimpanzees and humans. PLoS One, 10, e973.CrossRefGoogle Scholar
  35. Langergraber, K. E., Mitani, J. C., & Vigilant, L. (2007b). The limited impact of kinship on cooperation in wild chimpanzees. Proceedings of the National Academy of Sciences of the USA, 104, 7786–7790.PubMedCrossRefGoogle Scholar
  36. McGrew, W. C., Ensminger, A. L., Marchant, L. F., Pruetz, J. D., & Vigilant, L. (2004). Genotyping aids field study of unhabituated wild chimpanzees. American Journal of Primatology, 63, 87–93.PubMedCrossRefGoogle Scholar
  37. Miller, L., Savage, A., & Giraldo, H. (2004). Quantifying remaining forested habitat within the historic distribution of the cotton-top tamarin (Saguinus oedipus) in Colombia: Implications for long-term conservation. American Journal of Primatology, 64, 451–457.PubMedCrossRefGoogle Scholar
  38. Miller, C. R., Joyce, P., & Waits, L. P. (2005). A new method for estimating the size of small populations from genetic mark-recapture data. Molecular Ecology, 14, 1991–2005.PubMedCrossRefGoogle Scholar
  39. Nei, M. (1987). Molecular evolutionary genetics. New York: Columbia University Press.Google Scholar
  40. Nsubuga, A. M., Robbins, M. M., Roeder, A., Morin, P., Boesch, C., & Vigilant, L. (2004). Factors affecting the amount of genomic DNA extracted from ape feces and the identification of an improved sample storage method. Molecular Ecology, 13, 2089–2094.PubMedCrossRefGoogle Scholar
  41. Oates, J. F. (1996). Habitat alteration, hunting, and the conservation of folivorous primates in African forests. Australian Journal of Ecology, 21, 1–9.CrossRefGoogle Scholar
  42. Onderdonk, D. A., & Chapman, C. A. (2000). Coping with forest fragmentation: the primates of Kibale National Park, Uganda. International Journal of Primatology, 21, 587–611.CrossRefGoogle Scholar
  43. Plumptre, A. J., Masozera, M., & Vedder, A. (2001). The impact of civil war on the conservation of protected areas in Rwanda. Washington, DC: Biodiversity Support Program.Google Scholar
  44. Pope, T. R. (1996). Socioecology, population fragmentation, and patterns of genetic loss in endangered primates. In J. C. Avise & J. L. Hamrick (Eds.), Conservation genetics: Case histories from nature (pp. 119–159). New York: Chapman & Hall.Google Scholar
  45. Schwartz, M. K., Luikart, G., & Waples, R. S. (2007). Genetic monitoring as a promising tool for conservation and management. Trends in Ecology & Evolution, 22, 25–33.CrossRefGoogle Scholar
  46. Sommer, V., Adanub, J., Fauchera, I., & Fowler, A. (2004). Nigerian chimpanzees (Pan troglodytes vellerosus) at Gashaka: two years of habituation efforts. Folia Primatologica, 75, 295–316.CrossRefGoogle Scholar
  47. Taberlet, P., Camarra, J. J., Griffin, S., Uhrès, E., Hanotte, O., Waits, L. P., Dubois-Paganon, C., Burke, T., & Bouvet, J. (1997). Noninvasive genetic tracking of the endangered Pyrenean brown bear population. Molecular Ecology, 6, 869–876.PubMedCrossRefGoogle Scholar
  48. Tutin, C. E. G., & Fernandez, M. (1991). Responses of wild chimpanzees and gorillas to the arrival of primatologists: Behaviour observed during habituation. In H. O. Box (Ed.), Primate responses to environmental change (pp. 187–197). New York: Chapman & Hall.CrossRefGoogle Scholar
  49. van Oven, M., Hämmerle, J. M., van Schoor, M., Kushnick, G., Pennekamp, P., Zega, I., Lao, O., Brown, L., Kennerknecht, I., & Kayser, M. (2011). Unexpected island effects at an extreme: reduced Y chromosome and mitochondrial DNA diversity in Nias. Molecular Biology and Evolution, 28, 1349–1361.PubMedCrossRefGoogle Scholar
  50. Williamson, E. A., & Feistner, A. T. C. (2003). Habituating primates: Processes, techniques, variables and ethics. In J. M. Setchell (Ed.), Field and laboratory methods in primatology: A practical guide (pp. 25–39). Cambridge, UK: Cambridge University Press.Google Scholar
  51. Yamagiwa, J., Mwanza, N., Spangenberg, A., Maruhashi, T., Yumoto, T., Fischer, A., Steinhauer-Burkart, B., & Refisch, J. (1992). Population density and ranging pattern of chimpanzees in Kahuzi-Biega National Park, Zaire: a comparison with a sympatric population of gorillas. African Study Monographs, 13, 217–230.Google Scholar
  52. Zhan, X., Li, M., Zhang, Z., Goossens, B., Chen, Y., Wang, H., Bruford, M. W., & Wei, F. (2006). Molecular censusing doubles giant panda population estimate in a key nature reserve. Current Biology, 16, 451–452.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2012

Authors and Affiliations

  • Rebecca L. Chancellor
    • 1
    • 2
  • Kevin Langergraber
    • 3
    • 4
  • Sergio Ramirez
    • 3
  • Aaron S. Rundus
    • 1
    • 5
  • Linda Vigilant
    • 3
  1. 1.Great Ape TrustDes MoinesUSA
  2. 2.Department of AnthropologyUniversity of California, DavisDavisUSA
  3. 3.Primatology DepartmentMax Planck Institute for Evolutionary AnthropologyLeipzigGermany
  4. 4.Department of AnthropologyBoston UniversityBostonUSA
  5. 5.Department of PsychologyWest Chester UniversityWest ChesterUSA

Personalised recommendations