Forest Landscape Restoration Contributes to the Conservation of Primates in the Gishwati-Mukura Landscape, Rwanda

Deogratias Tuyisingize1,2, Winnie Eckardt1, Damien Caillaud3, M. Ngabikwiye1, Beth A. Kaplin4,2
1The Dian Fossey Gorilla Fund International, Karisoke Research Center, Musanze, Rwanda
2College of Science and Technology, University of Rwanda, Kigali, Rwanda
3Department of Anthropology, University of California, Davis, USA
4University of Massachusetts Boston, Boston, USA

Tóm tắt

Từ khóa


Tài liệu tham khảo

Arakwiye, B. (2020). Forest cover change in Western Rwanda during periods of wars and environmental policy shifts: Dynamics, drivers, and ecological outcomes. PhD Thesis, Clark University.

Arakwiye, B., Ogan, J., & Eastman, J. R. (2021). Thirty years of forest-cover change in Western Rwanda during periods of wars and environmental policy shifts. Regional Environmental Change, 21(2). https://doi.org/10.1007/s10113-020-01744-0.

Arroyo-Rodríguez, V., Cuesta-del Moral, E., Mandujano, S., Chapman, A. C., Reyna-Hurtado, R., & Fahrig, L. (2013). Assessing habitat fragmentation effects on primates: The importance of evaluating questions at the correct scale. In L. K. Marsh & C. A. Chapman (Eds.), Primates in fragments: Complexity and resilience (pp. 13–28). Springer. https://doi.org/10.1007/978-1-4614-8839-2_2.

Ayebare, S., Plumptre, A. J., Kujirakwinja, D., & Segan, D. (2018). Conservation of the endemic species of the Albertine Rift under future climate change. Biological Conservation, 220(June 2017), 67–75. https://doi.org/10.1016/j.biocon.2018.02.001.

Barakabuye, N., Mulindahabi, F., Plumptre, A. J., Kaplin, B., Munanura, I., Ndagijimana, D., & Ndayiziga, O. (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 Unpublished report to U.S. Fish and Wildlife Service.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.

Baranga, D., Basuta, G. I., Teichroeb, J. A., & Chapman, C. A. (2012). Crop raiding patterns of solitary and social groups of red-tailed monkeys on cocoa pods in Uganda. Tropical Conservation Science, 5(1), 104–111. https://doi.org/10.1177/194008291200500109.

Bicca-Marques, J. C. (2003). How do howler monkeys cope with habitat fragmentation? In L. K. Marsh (Ed.), Primates in fragments: Ecology and conservation (pp. 283–303). Kluwer Academic/Plenum Publishers. https://doi.org/10.1007/978-1-4757-3770-7_18.

Bizuru, E., Nyandwi, E., Nshutiyayesu, S., & Kabuyenge, J. P. (2015). Inventory and mapping of threatened remnant terrestrial ecosystems outside protected areas through Rwanda. Kigali.

Buckland, S. T., Plumptre, A. J., Thomas, L., & Rexstad, E. A. (2010a). Design and analysis of line transect surveys for primates. International Journal of Primatology, 31(5), 833–847. https://doi.org/10.1007/s10764-010-9431-5.

Buckland, S. T., Plumptre, A. J., Thomas, L., & Rexstad, E. A. (2010b). Line transect sampling of primates: Can animal-to-observer distance methods work? International Journal of Primatology, 31(3), 485–499. https://doi.org/10.1007/s10764-010-9408-4.

Buckland, S. T., Plumptre, A. J., Thomas, L., & Rexstad, E. A. (2010c). Design and analysis of line transect surveys for primates. International Journal of Primatology, 31(5), 833–847. https://doi.org/10.1007/s10764-010-9431-5.

Campbell-Smith, G., Simanjorang, H. V. P., Leader-Williams, N., & Linkie, M. (2010). Local attitudes and perceptions toward crop-raiding by orangutans (Pongo abelii) and other nonhuman primates in Northern Sumatra, Indonesia. American Journal of Primatology, 72(10), 866–876. https://doi.org/10.1002/ajp.20822.

Chancellor, R. L., Rundus, A. S., & Nyandwi, S. (2017). Chimpanzee seed dispersal in a montane forest fragment in Rwanda. American Journal of Primatology, 79(3), 1–8. https://doi.org/10.1002/ajp.22624.

Chancellor, R., Langergraber, K., Ramirez, S., Rundus, A. S., & Vigilant, L. (2012a). Genetic sampling of unhabituated chimpanzees (Pan troglodytes schweinfurthii) in Gishwati forest reserve, an isolated forest fragment in Western Rwanda. International Journal of Primatology, 33(2), 479–488. https://doi.org/10.1007/s10764-012-9591-6.

Chancellor, R., Rundus, A., & Nyandwi, S. (2012b). The influence of seasonal variation on Chimpanzee (Pan troglodytes schweinfurthii) fallback food consumption, nest group size, and habitat use in Gishwati, a montane rain forest fragment in Rwanda. International Journal of Primatology, 33(1), 115–133. https://doi.org/10.1007/s10764-011-9561-4.

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, 14(1), 207–217. https://doi.org/10.1046/j.1523-1739.2000.98592.x

Chapman, C. A., Cords, M., Gautier-Hion, A., Chapman, L. J., Gathua, J. M., Tutin, C. E. G., et al. (2002). Variation in the diets of Cercopithecus species: Differences within forests, among forests, and across species. In K. M. Glenn & M. Cords (Eds.), The guenons: Diversity and adaptation in african monkeys (pp. 325–350). Kluwer Academic/Plenum Publishers. https://doi.org/10.1007/0-306-48417-x_22

Chapman, C. A., Omeja, P. A., Kalbitzer, U., Fan, P., & Lawes, M. J. (2018). Restoration provides hope for faunal recovery: Changes in primate abundance over 45 years in Kibale National Park, Uganda. Tropical Conservation Science, 11, 1–5. https://doi.org/10.1177/1940082918787376.

Chazdon, R. L., Cullen, L., Padua, S. M., & Padua, C. V. (2020). People, primates and predators in the Pontal: From endangered species conservation to forest and landscape restoration in Brazil’s Atlantic Forest. Royal Society Open. Science, 7(12). https://doi.org/10.1098/rsos.200939rsos200939.

Chazdon, R. L., & Uriarte, M. (2016). Natural regeneration in the context of large-scale forest and landscape restoration in the tropics. Biotropica, 48(6), 709–715. https://doi.org/10.1111/btp.12409.

Clay, N. (2019). Fixing the ecosystem: Conservation, crisis and capital in Rwanda’s Gishwati Forest. Environment and Planning E: Nature and Space, 2(1), 23–46. https://doi.org/10.1177/2514848619826576.

Cowlishaw, G. (1999). Predicting the pattern of decline of African primate diversity: An extinction debt from historical deforestation. Conservation Biology, 13(5), 1183–1193. https://doi.org/10.1046/j.1523-1739.1999.98433.x.

Dias, P. C. (1996). Sources and sinks in population biology. Trends in Ecology and Evolution, 11(8), 326–330. https://doi.org/10.1016/0169-5347(96)10037-9.

Dunham, N. T. (2017). Feeding ecology and dietary flexibility of Colobus angolensis palliatus in relation to habitat disturbance. International Journal of Primatology, 38(3), 553–571. https://doi.org/10.1007/s10764-017-9965-x.

Easton, J., Chao, N., Mulindahabi, F., Ntare, N., Rugyerinyange, L., & Ndikubwimana, I. (2011). Status and conservation of the only population of the Vulnerable owl-faced monkey Cercopithecus hamlyni in Rwanda. Oryx, 45(3), 435–438. https://doi.org/10.1017/S0030605310001468.

Estrada, A., Garber, P. A., Rylands, A. B., Roos, C., Fernandez-duque, E., Di Fiore, A., et al (2017). Impending extinction crisis of the world’s primates: Why primates matter. Science Advances, 3(January), 1–16. https://doi.org/10.1126/sciadv.1600946.

Fahrig, L. (1997). Relative effects of habitat loss and fragmentation on population extinction. The Journal of Wildlife Management, 61(3), 603. https://doi.org/10.2307/3802168.

Fahrig, L. (2003). Effects of habitat fragmentation on biodiversity. Annual Review of Ecology, Evolution, and Systematics, 34(1), 487–515. https://doi.org/10.1146/annurev.ecolsys.34.011802.132419.

Fashing, P. J., Nguyen, N., Luteshi, P., Opondo, W., Cash, J. F., & Cords, M. (2012). Evaluating the suitability of planted forests for African forest monkeys: A case study from Kakamega forest. Kenya. American Journal of Primatology, 74(1), 77–90. https://doi.org/10.1002/ajp.21012.

Furuichi, T., Hashimoto, C., & Tashiro, Y. (2001). Extended application of a marked-nest census method to examine seasonal changes in habitat use by chimpanzees. International Journal of Primatology, 22(6), 913–928. https://doi.org/10.1023/A:1012057403512.

Goodall, J. (2015). Caring for people and valuing forests in Africa. In G. Wuerthner, E. Crist, & T. Butler (Eds.), Protecting the Wild. Island Press. https://doi.org/10.5822/978-1-61091-551-9_3.

Graham, T. L., Matthews, H. D., & Turner, S. E. (2016). A global-scale evaluation of primate exposure and vulnerability to climate change. International Journal of Primatology, 37(2), 158–174. https://doi.org/10.1007/s10764-016-9890-4.

Green, S. J., Boruff, B. J., & Grueter, C. C. (2020). From ridge tops to ravines: landscape drivers of chimpanzee ranging patterns. Animal Behaviour, 163, 51–60. https://doi.org/10.1016/j.anbehav.2020.02.016.

Hanya, G., Zamma, K., Hayaishi, S., Yoshihiro, S., Tsuriya, Y., Sugaya, S., et al (2005). Comparisons of food availability and group density of Japanese macaques in primary, naturally regenerated, and plantation forests. American Journal of Primatology, 66(3), 245–262. https://doi.org/10.1002/ajp.20142.

Hill, M. C. (1997). Crop-raiding by wild vertebrates: The farmer’s perspective in an agricultural community in western Uganda. International Journal of Pest Management, 43(1), 77–84. https://doi.org/10.1080/096708797229022.

Hill, M. C. (2000). Conflict of interest between people and baboons: Crop raiding in Uganda. International Journal of Primatology, 21(2), 299–315. https://doi.org/10.1023/A:1005481605637.

Hill, M. C. (2018). Crop foraging, crop rosses, and crop raiding. Annual Review of Anthropology, 47(1), 377–394. https://doi.org/10.1146/annurev-anthro-102317-050022.

Ickes, K., Roetgers, C., Quesada, M., Kalko, E., Kudavidanage, E., Mudappa, D., et al (2012). Averting biodiversity collapse in tropical forest protected areas. Nature, 489(7415), 290–294. https://doi.org/10.1038/nature11318.

Irwin, M. T. (2006). Ecological impacts of forest fragmentation on diademed sifakas (Propithecus diadema) at Tsinjoarivo, eastern Madagascar: Implications for conservation in fragmented landscapes. PhD Thesis, Stony Brook University

IUCN, & WRI. (2014). A guide to the restoration opportunities assessment methodology (ROAM): Assessing forest landscape restoration opportunities at the national or sub-national level. Working Paper (Road-test edition). Gland, Switzerland: IUCN. 125pp.

Kaplin, B. A. (2001). Ranging behavior of two species of guenons ( Cercopithecus lhoesti and C . mitis doggetti ) in the Nyungwe forest reserve. Rwanda. International Journal of Primatology, 22(4), 521–548. https://doi.org/10.1023/A:1010716001014.

Kaplin, B. A. (2014). Chimpanzee conservation in Nyungwe National Park, Rwanda: The impacts of buffer zone type and land use change. Final perfomance report to the U.S.

Kaplin, B. A., & Moermond, T. C. (2000). Foraging ecology of the mountain monkey (Cercopithecus l’hoesti): Implications for its evolutionary history and use of disturbed forest. American Journal of Primatology, 50(4), 227–246. https://doi.org/10.1002/(SICI)1098-2345(200004)50:4<227::AID-AJP1>3.0.CO;2-S.

Laurance, W., Lovejoy, T. E., Vasconcelos, H. L., Bruna, E. M., Didham, R. K., Stouffer, P. C., et al (2002). Ecosystem decay of amazonian forest fragments: A 22-year investigation. Conservation Biology, 16(3), 605–618. https://doi.org/10.1046/j.1523-1739.2002.01025.x.

Mansourian, S., Dudley, N., & Vallauri, D. (2017). Forest landscape restoration: Progress in the last decade and remaining challenges. Ecological Restoration, 35(4), 281–288. https://doi.org/10.3368/er.35.4.281.

Marchesi, P., Marchesi, N., Fruth, B., & Boesch, C. (1995). Census and distribution of chimpanzees in Côte D’Ivoire. Primates, 36(4), 591–607. https://doi.org/10.1007/BF02382880.

Marsh, L. K., & Chapman, C. A. (2013). Primates in fragments: Complexity and resilience. https://doi.org/10.1007/978-1-4614-8839-2.

McGuinness, S., & Taylor, D. (2014). Human dimensions of wildlife farmers ’ perceptions and actions to decrease crop raiding by forest-dwelling primates around a Rwandan forest fragment. Human Dimensions of Wildlife, 19(2), 179–190. https://doi.org/10.1080/10871209.2014.853330.

Mekonnen, A., Fashing, P. J., Bekele, A., Hernandez-Aguilar, R. A., Rueness, E. K., & Stenseth, N. C. (2018). Dietary flexibility of Bale monkeys (Chlorocebus djamdjamensis) in southern Ethiopia: Effects of habitat degradation and life in fragments. BMC Ecology, 18(1), 1–20. https://doi.org/10.1186/s12898-018-0161-4.

Merker, S., Yustian, I., & Mühlenberg, M. (2005). Responding to forest degradation: Altered habitat use by Dian’s tarsier Tarsius dianae in Sulawesi. Indonesia. Oryx, 39(2), 189–195. https://doi.org/10.1017/S0030605305000438.

Miller, D. L., Rexstad, E., Thomas, L., Laake, J. L., & Marshall, L. (2019). Distance sampling in R. Journal of Statistical Software, 89(1), 1–28. https://doi.org/10.18637/jss.v089.i01.

MINIRENA (2014). Forest landscape restoration opportunity assessment for Rwanda. Kigali.

Naughton-Treves, L. (1998). Predicting patterns of crop damage by wildlife around Kibale National Park. Uganda. Conservation Biology, 12(1), 156–168. https://doi.org/10.1046/j.1523-1739.1998.96346.x.

Nelson, F. (2010). Community Rights, Conservation and Contested Land. (F. Nelson, Ed.)Community Rights, Conservation and Contested Land. London: Earthscan. https://doi.org/10.4324/9781849775052

Newton-Fisher, N. E. (1999). The diet of chimpanzees in the Budongo forest reserve. Uganda. African Journal of Ecology, 37(3), 344–354. https://doi.org/10.1046/j.1365-2028.1999.00186.x.

Ngabikwiye, M. (2019). Feeding ecology , ranging patterns and composition of golden monkey group outside Gishwati protected area. BSc Thesis, University of Rwanda.

NISR. (2012). Rwanda fourth population and housing census. Thematic report: Population size, structure and distribution. https://www.statistics.gov.rw/publication/rphc4-atlas

Nyandwi, E., & Mukashema, A. (2011). Excessive deforestation of Gishwati mountainous forest and biodiversity changes. Participatory Geographic Information Systems (P-GIS) for natural resource management and food security in Africa, the ict4d article. Dakar.

Oldekop, J. A., Holmes, G., Harris, W. E., & Evans, K. L. (2016). A global assessment of the social and conservation outcomes of protected areas. Conservation Biology, 30(1), 133–141. https://doi.org/10.1111/cobi.12568.

Onderdonk, D. A., & Chapman, C. A. (2000). Coping with forest fragmentation: The primates of Kibale National Park, Uganda. International Journal of Primatology, 21(4), 587–611. https://doi.org/10.1023/A:1005509119693.

Peres, C. A. (1999). General guidelines for standardizing line-transect surveys of tropical forest. Neotropical Primates, 1(7), 11–16.

Plumptre, A. J., Davenport, T. R. B., Behangana, M., Kityo, R., Eilu, G., Ssegawa, P., et al (2007). The biodiversity of the Albertine Rift. Biological Conservation, 134(2), 178–194. https://doi.org/10.1016/j.biocon.2006.08.021.

Plumptre, A. J., Masozera, M., & Vedder, A. (2001). The impact of civil war on the conservation of protected areas in Rwanda. Washington, D.C.: Biodiversity Support Program. http://www.worldwildlife.org/bsp/publications/africa/141/CAR.pdf

Plumptre, A. J., & Reynolds, V. (1997). Nesting behavior of chimpanzees: Implications for censuses. International Journal of Primatology, 18(4), 475–485. https://doi.org/10.1023/A:1026302920674.

Ponce-Reyes, R., Plumptre, A. J., Segan, D., Ayebare, S., Fuller, R. A., Possingham, H. P., & Watson, J. E. M. (2017). Forecasting ecosystem responses to climate change across Africa’s Albertine Rift. Biological Conservation, 209, 464–472. https://doi.org/10.1016/j.biocon.2017.03.015.

REMA. (2015). Terrestrial ecosystems and species in need of protection in Rwanda. Technical report. Kigali, Rwanda.

Riley, E. P., Mackinnon, K. C., Fernandez-Duque, E., Setchell, J. M., & Garber, P. A. (2014). Code of best practices for field primatology. International Primatological Society and American Society of Primatologists Steering Committee, 1–17. https://doi.org/10.13140/2.1.2889.1847.

Robertson, B. A., & Hutto, R. L. (2006). Concepts & synthesis emphasizing new ideas to stimulate research in ecology a framework for understanding ecological traps and an evaluation of existing evidence. Ecology, 87(5), 1075–1085. https://doi.org/10.1890/0012-9658(2006)87[1075:AFFUET]2.0.CO;2.

Rundus, A., Chancellor, R., Nyandwi, S., & Johnston, A. (2022). Factors influencing chimpanzee (Pan troglodytes schweinfurthii) crop foraging in farmland outside of Gishwati Forest, Rwanda. International Journal of Primatology. https://doi.org/10.1007/s10764-022-00291-1.

Rylands, A. B., Williamson, E. A., Hoffmann, M., & Mittermeier, R. A. (2008). Primate surveys and conservation assessments. Oryx, 42(03), 313–314. https://doi.org/10.1017/s0030605308423050.

Salerno, J., Chapman, C. A., Diem, J. E., Dowhaniuk, N., Goldman, A., MacKenzie, C. A., et al (2018). Park isolation in anthropogenic landscapes: land change and livelihoods at park boundaries in the African Albertine Rift. Regional Environmental Change, 18(3), 913–928. https://doi.org/10.1007/s10113-017-1250-1.

Schwitzer, C., Glatt, L., Nekaris, K. A. I., & Ganzhorn, J. U. (2011). Responses of animals to habitat alteration: An overview focussing on primates. Endangered Species Research, 14(1), 31–38. https://doi.org/10.3354/esr00334.

Tutin, C. E. G., & Fernandez, M. (1984). Nationwide census of gorilla (gorilla g. gorilla) and chimpanzee (Pan t. troglodytes) populations in Gabon. American Journal of Primatology, 6(4), 313–336. https://doi.org/10.1002/ajp.1350060403.

Tuyisingize, D., Eckardt, W., Caillaud, D., & Kaplin., B. A. (2021). High flexibility in diet and ranging patterns in two golden monkey (Cercopithecus mitis kandti ) populations in Rwanda. American Journal of Primatology, e23347. https://doi.org/10.1002/ajp.23347.

Tuyisingize, D., Kaplin, B. A., Eckardt, W., Musana, A., & Caillaud, D. (2022). Distribution and conservation status of the golden monkey Cercopithecus mitis kandti in Rwanda. Oryx, 1–9. https://doi.org/10.1017/s0030605321001009.

Twinomugisha, D., Chapman, C. A., Lawes, M. J., O’Driscoll Worman, C., & Danish, L. M. (2007). How does the golden monkey of the Virungas cope in a fruit-scarce environment? In C. A. Chapman, M. J. Lawes, & L. Danish (Eds.), Primates of Western Uganda (pp. 45–60). Springer. https://doi.org/10.5860/choice.44-3872.

Ukizintambara, T. (2008). Edge effects on ranging and foraging behaviour of L’hoest’s monkey (Cercopithecus lhoesti) in Bwindi Impenetrable National Park, Uganda. Final report to the Rufford small grant foundation.

Vié, J.-C., Hilton-Taylor, C., & Stuart, S. N. (2009). Wildlife in a changing world – An analysis of the 2008 IUCN Red List of threatened species. Gland, Switzerland: IUCN. 180 pp.

Wallace, G. E., & Hill, C. M. (2016). Deterring crop-foraging wildlife. Lessons from farms in north-western Uganda. Oxford. https://doi.org/10.1080/17470218.2014.959534

White, L., & Edward, A. (2000). Conservation research in the African rain forests: A technical handbook. (L. White & A. Edward, Eds.). New York: Wildlife Conservation Society. https://pdf.usaid.gov/pdf_docs/Pnade111.pdf