International Journal of Primatology

, Volume 36, Issue 2, pp 209–226 | Cite as

Modeling Primate Abundance in Complex Landscapes: A Case Study From the Udzungwa Mountains of Tanzania

  • Claudia BarelliEmail author
  • Roger Mundry
  • Alessandro Araldi
  • Keith Hodges
  • Duccio Rocchini
  • Francesco Rovero


With persistent degradation of tropical forests creating fragmented landscapes, the study of patterns of primate responses to habitat changes is of increasing conservation relevance. We modeled primate abundance in the Udzungwa Mountains of Tanzania through a landscape approach, i.e., one that includes a representative range of discrete forest blocks. The area is internationally recognized for biological endemism and is a primate hotspot in Africa. We targeted three predominantly arboreal monkeys: Udzungwa red colobus (Procolobus gordonorum), Peters’ Angola colobus (Colobus angolensis palliatus), and the Tanzania Sykes’ monkey (Cercopithecus mitis monoides). In each of the four forests (12–522 km2 in size), we counted primate groups along a grid of line transects (267 km walked) and sampled canopy trees in vegetation plots along the same transects (N = 408) to derive structural and floristic forest parameters and proxies of human impact. We found that elevation and the percentage of climber coverage on trees consistently emerged as significant predictors of primate abundance for all three species in spite of their differences in feeding habits, with a negative effect of elevation and a positive effect of climber coverage. This pattern held despite large variations in elevation, forest habitat, and human disturbance across the four forests surveyed. We conclude that arboreal primates in the Udzungwas are dependent on lowland and medium-elevation forests (ca. 300–1200 m a.s.l.) and show considerable resilience to moderate forest disturbance. However, agricultural intensification causes rapid forest degradation, with detrimental effects on primates that need to be prevented through increased protection and community conservation.


Eastern Arc Ecological models Forest disturbance Line transect Peters’ Angola colobus Rain forest Tanzania Sykes’ monkey Udzungwa red colobus 



We thank the Tanzania Commission for Science and Technology (COSTECH), Tanzania Wildlife Research Institute (TAWIRI), and Tanzania National Parks (TANAPA) for granting us permission to conduct the study (Costech Permits No. 2011-85-NA-2011-33; 2011-84-NA-2011-33; 2011-351-NA-2011-68; 2011-346-NA-2011-183). We are also grateful to the warden and staff of Udzungwa Mountains National Park, the Tanzanian field assistants for their valuable assistance throughout the study, and to J. F. Gallardo Palacios for conducting and managing most of the field work. We also thank S. Tenan, three anonymous reviewers, and the editor-in-chief Joanna Setchell for helpful comments on previous versions of the manuscript. Financial support was provided by the Provincia Autonoma di Trento and the EU (Marie Curie Actions COFUND, postdoctoral grant to C. Barelli), Rufford Small Grants Foundation (1033-C to F. Rovero), Idea Wild (to A. Araldi), and the German Primate Centre (DPZ).


  1. Aiken, L. S., & West, S. G. (1991). Multiple regression: Testing and interpreting interactions. Newbury Park, CA: SAGE.Google Scholar
  2. Araldi, A., Barelli, C., Hodges, K., & Rovero, F. (2014). Density estimation of the endangered Udzungwa red colobus (Procolobus gordonorum) and other arboreal primates in the Udzungwa Mountains using systematic distance sampling. International Journal of Primatology, 35, 941–956.Google Scholar
  3. Bakayoko, A., Martin, P., Chatelain, C., Traore, D., & Gautier, L. (2011). Diversity, family dominance, life forms and ecological strategies of forest fragments compared to continuous forest in Southwestern Côte d'Ivoire. Candollea, 66, 255–262.CrossRefGoogle Scholar
  4. Barelli, C., Gallardo Palacios, J. F., & Rovero, F. (2014). Variation in primate abundance along an elevational gradient in the Udzungwa Mountains of Tanzania. In N. Grow, S. Gursky-Doyen, & A. Krzton (Eds.), High-altitude primates. Developments in primatology: Progress and prospects (pp. 211–226). New York: Springer Science+Business Media.Google Scholar
  5. Bocian, C. M. (1997). Niche separation of black-and-white colobus monkeys (Colobus angolensis and C. guereza) in the Ituri Forest. Ph.D. dissertation, City University of New York.Google Scholar
  6. Bolliger, J. (2005). Simulating complex landscapes with a generic model: Sensitivity to qualitative and quantitative classifications. Ecological Complexity, 2, 131–149.CrossRefGoogle Scholar
  7. Bracebridge, C. E., Davenport, T. R., & Marsden, S. J. (2012). The impact of forest disturbance on the seasonal foraging ecology of a critically endangered african primate. Biotropica, 44, 560–568.CrossRefGoogle Scholar
  8. Brook, B. W., Sodhi, N. S., & Bradshaw, C. J. A. (2008). Synergies among extinction drivers under global change. Trends in Ecology & Evolution, 23, 453–460.CrossRefGoogle Scholar
  9. Busch, D. S., & Hayward, L. S. (2009). Stress in a conservation context: A discussion of glucocorticoid actions and how levels change with conservation-relevant variables. Biological Conservation, 142, 2844–2853.CrossRefGoogle Scholar
  10. Butynski, T. M. (1990). Comparative ecology of blue monkeys (Cercopithecus mitis) in high- and low-density subpopulations. Ecological Monographs, 60, 1–26.CrossRefGoogle Scholar
  11. Cardillo, M., Mace, G. M., Jones, K. E., Bielby, J., Bininda-Emonds, O. R. P., Sechrest, W., et al. (2005). Multiple causes of high extinction risk in large mammal species. Science, 309, 1239–1241.Google Scholar
  12. Chajewski, M. (2009). rela: Scale item analysis. R package version 4.1.Google Scholar
  13. Chapman, C. A., Balcomb, S. R., Gillespie, T. R., Skorupa, J. P., & 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.CrossRefGoogle Scholar
  14. Chapman, C. A., & 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.CrossRefPubMedGoogle Scholar
  15. Cowlishaw, G., & Dunbar, R. I. M. (2000). Primate conservation biology. Chicago: University of Chicago Press.Google Scholar
  16. Davenport, T. R. B., Nowak, K., & Perkin, A. (2013). Priority primate areas in Tanzania. Oryx, 48, 39–51.CrossRefGoogle Scholar
  17. Dobson, A. J. (2002). An introduction to generalized linear models. Boca Raton, FL: Chapman & Hall/CRC.Google Scholar
  18. Dunn, J. C., Asensio, N., Arroyo-Rodríguez, V., Schnitzer, S., & Cristóbal-Azkarate, J. (2012). The ranging costs of a fallback food: Liana consumption supplements diet but increases foraging effort in howler monkeys. Biotropica, 44, 705–714.CrossRefGoogle Scholar
  19. Fa, J. E., Ryan, S. F., & Bell, D. J. (2005). Hunting vulnerability, ecological characteristics and harvest rates of bushmeat species in afrotropical forests. Biological Conservation, 121, 167–176.CrossRefGoogle Scholar
  20. Fahrig, L. (2003). Effects of habitat fragmentation on biodiversity. Annual Review of Ecology, Evolution, and Systematics, 34, 487–515.CrossRefGoogle Scholar
  21. Field, A. (2005). Discovering statistics using SPSS. London: SAGE.Google Scholar
  22. Fimbel, C., Vedder, A., Dierenfeld, E., & Mulindahabi, F. (2001). An ecological basis for large group size in Colobus angolensis in the Nyungwe Forest, Rwanda. African Journal of Ecology, 39, 83–92.CrossRefGoogle Scholar
  23. Forstmeier, W., & Schielzeth, H. (2011). Cryptic multiple hypotheses testing in linear models: overestimated effect sizes and the winner’s curse. Behavioural Ecology and Sociobiology, 65, 47–55.CrossRefGoogle Scholar
  24. Fürtbauer, I., Mundry, R., Heistermann, M., Schülke, O., & Ostner, J. (2011). You mate, I mate: macaque females synchronize sex not cycles. PLoS ONE, e26144.Google Scholar
  25. Gelman, A., & Hill, J. (2007). Data analysis using regression and multilevel/hierarchical models. Cambridge, U.K.: Cambridge University Press.Google Scholar
  26. Gerwing, J. J., Schnitzer, S. A., Burnham, R. J., Bongers, F., Chave, J., DeWalt, S. J., et al. (2006). A standard protocol for liana censuses. Biotropica, 38, 256–261.CrossRefGoogle Scholar
  27. Hanya, G., & Bernard, H. (2012). Fallback foods of red leaf monkeys (Presbytis rubicunda) in Danum Valley, Borneo. International Journal of Primatology, 33, 322–337.CrossRefGoogle Scholar
  28. Hédl, R., Svátek, M., Dancak, M., Rodzay, A. W., Salleh, A. B. M., & Kamariah, A. S. (2009). A new technique for inventory of permanent plots in tropical forests: A case study from lowland dipterocarp forest in Kuala Belalong, Brunei Darussalam. Blumea, 54, 124–130.CrossRefGoogle Scholar
  29. Henle, K., Lindenmayer, D. B., Margules, C. R., Saunders, D. A., & Wissel, C. (2004). Species survival in fragmented landscapes: Where are we now? Biodiversity Conservation, 13, 1–8.CrossRefGoogle Scholar
  30. Johns, A. D., & Skorupa, J. P. (1987). Responses of rain-forest primates to habitat disturbance: A review. International Journal of Primatology, 8, 157–191.CrossRefGoogle Scholar
  31. Laurance, W. F., Useche, D. C., Rendeiro, J., Kalka, M., Bradshaw, C. J. A., et al. (2012). Averting biodiversity collapse in tropical forest protected areas. Nature, 489, 290–294.CrossRefPubMedGoogle Scholar
  32. Linder, J. M. (2013). African primate diversity threatened by “new wave” of industrial oil palm expansion. African Primates, 8, 25–38.Google Scholar
  33. Lovett, J. C. (1993). Eastern Arc moist forest flora. In J. C. Lovett & S. K. Wasser (Eds.), Biogeography and ecology of the rain forests of Eastern Africa (pp. 33–55). New York: Cambridge University Press.CrossRefGoogle Scholar
  34. Lovett, J. C., Marshall, A. R., & Carr, J. (2006). Changes in tropical forest vegetation along an altitudinal gradient in the Udzungwa Mountains National Park, Tanzania. African Journal of Ecology, 44, 478–490.CrossRefGoogle Scholar
  35. Mammides, C., Cords, M., & Peters, M. K. (2009). Effects of habitat disturbance and food supply on population densities of three primate species in the Kakamega Forest, Kenya. African Journal of Ecology, 47, 87–96.CrossRefGoogle Scholar
  36. Marsh, L. K. (2003). Primates in fragments: Ecology and conservation. New York: Plenum Press.CrossRefGoogle Scholar
  37. Marsh, L. K., & Chapman, C. (2013). Primates in fragments. Complexity and resilience. Developments in primatology: Progress and prospects. New York: Springer Science+Business Media.Google Scholar
  38. Marshall, A. R. (2007). Disturbance in the Udzungwas: responses of monkeys and trees to forest degradation. Ph.D. dissertation, University of York, Ann Arbor, MI.Google Scholar
  39. Marshall, A. R. (2008). Ecological report on Magombera forest. Unpublished report to WWFTPO. Retrieved from
  40. Marshall, A. R., Topp-Jørgensen, J. E., Brink, H., & Fanning, E. (2005). Monkey abundance and social structure in two high-elevation forest reserves in the Udzungwa Mountains of Tanzania. International Journal of Primatology, 26, 127–145.CrossRefGoogle Scholar
  41. Marshall, A. R., Jørgensbye, H. I. O., Rovero, F., Platts, P. J., White, P. C. L., & Lovett, J. C. (2010). The species-area relationship and confounding variables in a threatened monkey community. American Journal of Primatology, 72, 325–36.Google Scholar
  42. McCullagh, P., & Nelder, J. A. (2008). Generalized linear models. London: Chapman and Hall.Google Scholar
  43. McGregor, P. K. (1992). Quantifying responses to playback: One, many, or composite multivariate measures? In P. K. McGregor (Ed.), Playback and studies of animal communication (pp. 79–96). New York: Plenum Press.CrossRefGoogle Scholar
  44. National Bureau of Statistics. (2013). 2012 Population and housing census. Ministry of Finance, United Republic of Tanzania. Retrieved from
  45. Nowak, K., & Lee, P. C. (2013). Status of Zanzibar red colobus and Sykes's monkeys in two coastal forests in 2005. Primate Conservation, 27, 65–73.CrossRefGoogle Scholar
  46. 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
  47. Platts, P. J., Burgess, N. D., Gereau, R. E., Lovett, J. C., Marshall, A. R., McClean, C. J., et al. (2011). Delimiting tropical mountain ecoregions for conservation. Environmental Conservation, 38, 312–324.Google Scholar
  48. Plumptre, A. J., & Johns, A. G. (2001). Changes in primate communities following logging disturbance. In R. A. Fimbel, J. G. Robinson, & A. Grajal (Eds.), The cutting edge: Conserving wildlife in logged tropical forests (pp. 71–92). New York: Columbia University Press.Google Scholar
  49. Quinn, G. P., & Keough, M. J. (2002). Experimental designs and data analysis for biologists. Cambridge, U.K.: Cambridge University Press.CrossRefGoogle Scholar
  50. R Core Team. (2013). R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing.Google Scholar
  51. Rodgers, W. A., Homewood, K. M., & Hall, J. B. (1979). An ecological survey of Magombera forest reserve. Unpublished report, University of Dar es Salaam, Tanzania.Google Scholar
  52. Rovero, F., Marshall, A. R., Jones, T., & Perkin, A. (2009). The primates of the Udzungwa Mountains: Diversity, ecology and conservation. Journal of Anthropological Sciences, 87, 93–126.PubMedGoogle Scholar
  53. Rovero, F., Menegon, M., Fjeldså, J., Collett, L., Doggart, N., Leonard, C., Norton, G., Owen, N., Perkin, A., Spitale, D., Ahrends, A., & Burgess, N. D.  (2014). Targeted vertebrate surveys enhance the faunal importance and improve explanatory models within the Eastern Arc Mountains of Kenya and Tanzania. Diversity and Distributions, 20, 1438–1449.Google Scholar
  54. Rovero, F., Mtui, A., Kitegile, A. S., & Nielsen, M. R. (2012). Hunting or habitat degradation? Decline of primate populations in Udzungwa Mountains, Tanzania: An analysis of threats. Biological Conservation, 146, 89–96.CrossRefGoogle Scholar
  55. Rovero, F., & Struhsaker, T. T. (2007). Vegetative predictors of primate abundance: Utility and limitations of a fine-scale analysis. American Journal of Primatology, 69, 1242–1257.CrossRefPubMedGoogle Scholar
  56. Ryan, A. M., Chapman, C. A., & Rothman, J. M. (2013). How do differences in species and part consumption affect diet nutrient concentrations? A test with red colobus monkeys in Kibale National Park, Uganda. African Journal of Ecology, 51, 1–10.CrossRefGoogle Scholar
  57. Schielzeth, H. (2010). Simple means to improve the interpretability of regression coefficients. Methods in Ecology and Evolution, 1, 103–113.CrossRefGoogle Scholar
  58. Schipper, J., Chanson, J. S., Chiozza, F., Cox, N. A., Hoffmann, M., et al. (2008). The status of the world's land and marine mammals: Diversity, threat, and knowledge. Science, 322, 225–230.CrossRefPubMedGoogle Scholar
  59. Schnitzer, S. A., & Bongers, F. (2002). The ecology of lianas and their role in forests. Trends in Ecology and Evolution, 17, 223–230.CrossRefGoogle Scholar
  60. Schnitzer, S. A., & Bongers, F. (2011). Increasing liana abundance and biomass in tropical forests: Emerging patterns and putative mechanisms. Ecology Letters, 14, 397–406.CrossRefPubMedGoogle Scholar
  61. Schnitzer, S. A., & Carson, W. P. (2010). Lianas suppress tree regeneration and diversity in treefall gaps. Ecology Letters, 13, 849–857.CrossRefPubMedGoogle Scholar
  62. Shannon, C. (1948). A mathematical theory of communication. Bell System Technical Journal, 27, 379–423.CrossRefGoogle Scholar
  63. Siex, K. S., & Struhsaker, T. T. (1999). Colobus monkeys and coconuts: A study of perceived human–wildlife conflicts. Journal of Applied Ecology, 36, 1009–1020.CrossRefGoogle Scholar
  64. Simpson, E. H. (1949). Measurement of diversity. Nature, 163, 688.CrossRefGoogle Scholar
  65. Steel, R. I. (2012). The effects of habitat parameters on the behavior, ecology, and conservation of the Udzungwa red colobus monkey (Procolobus gordonorum). Ph.D. dissertation, Duke University.Google Scholar
  66. Struhsaker, T. T. (1997). Ecology of an African rain forest: Logging in Kibale and the conflict between conservation and exploitation. Gainesville: University Press of Florida.Google Scholar
  67. Struhsaker, T. T. (2010). The red colobus monkeys: Variation in demography, behavior, and ecology of endangered species. Oxford: Oxford University Press.CrossRefGoogle Scholar
  68. Vogel, E. R., Haag, L., Mitra-Setia, T., van Schaik, C. P., & Dominy, N. J. (2009). Foraging and ranging behavior during a fallback episode: Hylobates albibarbis and Pongo pygmaeus wurmbii compared. American Journal of Physical Anthropology, 140, 716–726.CrossRefPubMedGoogle Scholar
  69. Wong, S. N. P., Saj, T. L., & Sicotte, P. (2006). Comparison of habitat quality and diet of Colobus vellerosus in forest fragments in Ghana. Primates, 47, 365–373.CrossRefPubMedGoogle Scholar
  70. Zar, J. H. (1999). Biostatistical analysis. Upper Saddle River, NJ: Prentice Hall.Google Scholar

Copyright information

© Springer Science+Business Media New York 2015

Authors and Affiliations

  • Claudia Barelli
    • 1
    • 2
    • 3
    Email author
  • Roger Mundry
    • 4
  • Alessandro Araldi
    • 2
  • Keith Hodges
    • 2
  • Duccio Rocchini
    • 3
  • Francesco Rovero
    • 1
    • 5
  1. 1.Sezione di Biodiversità TropicaleMUSE - Museo delle ScienzeTrentoItaly
  2. 2.Reproductive Biology Unit, German Primate Centre (DPZ)Leibniz Institute for Primate ResearchGöttingenGermany
  3. 3.Biodiversity and Molecular Ecology DepartmentResearch and Innovation Centre - Fondazione Edmund MachTrentoItaly
  4. 4.Max Planck Institute for Evolutionary AnthropologyLeipzigGermany
  5. 5.Udzungwa Ecological Monitoring Centre (UEMC)Mang’ulaTanzania

Personalised recommendations