Skip to main content

Advertisement

Log in

Human proximity and habitat fragmentation are key drivers of the rangewide bonobo distribution

  • Original Paper
  • Published:
Biodiversity and Conservation Aims and scope Submit manuscript

Abstract

Habitat loss and hunting threaten bonobos (Pan paniscus), Endangered (IUCN) great apes endemic to lowland rainforests of the Democratic Republic of Congo. Conservation planning requires a current, data-driven, rangewide map of probable bonobo distribution and an understanding of key attributes of areas used by bonobos. We present a rangewide suitability model for bonobos based on a maximum entropy algorithm in which data associated with locations of bonobo nests helped predict suitable conditions across the species’ entire range. We systematically evaluated available biotic and abiotic factors, including a bonobo-specific forest fragmentation layer (forest edge density), and produced a final model revealing the importance of simple threat-based factors in a data poor environment. We confronted the issue of survey bias in presence-only models and devised a novel evaluation approach applicable to other taxa by comparing models built with data from geographically distinct sub-regions that had higher survey effort. The model’s classification accuracy was high (AUC = 0.82). Distance from agriculture and forest edge density best predicted bonobo occurrence with bonobo nests more likely to occur farther from agriculture and in areas of lower edge density. These results suggest that bonobos either avoid areas of higher human activity, fragmented forests, or both, and that humans reduce the effective habitat of bonobos. The model results contribute to an increased understanding of threats to bonobo populations, as well as help identify priority areas for future surveys and determine core bonobo protection areas.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Anderson RP, Gonzalez I (2011) Species-specific tuning increases robustness to sampling bias in models of species distributions: an implementation with Maxent. Ecol Model 222:2796–2811

    Article  Google Scholar 

  • Arroyo-Rodriguez V, Mandujano S, Benítez-Malvido J (2008) Landscape attributes affecting patch occupancy by howler monkeys (Alouatta palliata mexicana) at Los Tuxtlas, Mexico. Am J Primatol 70:69–77

    Article  PubMed  Google Scholar 

  • Beyers RL, Hart JA, Sinclair ARE, Grossmann F, Klinkenberg B, Dino S (2011) Resource wars and conflict ivory: the impact of civil conflict on elephants in the Democratic Republic of Congo—the case of the Okapi Reserve. PLoS One 6(11):e27129. doi:10.1371/journal.pone.0027129

    Article  PubMed  CAS  Google Scholar 

  • Blake S, Strindberg S, Boudjan P, Makombo C, Bila-Isia I et al (2007) Forest elephant crisis in the Congo Basin. PLoS Biol 5(4):e111. doi:10.1371/journal.pbio.0050111s

    Article  PubMed  Google Scholar 

  • Boubli JP, de Lima MG (2009) Modeling the geographical distribution and fundamental niches of Cacajao spp. and Chiropotes israelita in Northwestern Amazonia via a maximum entropy algorithm. International J Primatol 30:217–228

    Article  Google Scholar 

  • Campbell G, Kuehl HS, Diarrassouba A, N’Goran PK, Boesch C (2011) Long-term research sites as refugia for threatened and over-harvested species. Biol Lett 7:723–726

    Article  PubMed  CAS  Google Scholar 

  • DeLong ER, DeLong D, Clarke-Pearson D (1988) Comparing the areas under two or more correlated receiver operating characteristic curves: a nonparametric approach. Biometrics 44:837–845

    Article  PubMed  CAS  Google Scholar 

  • Draulans D, Van Krunkelsven E (2002) The impact of war on forest areas in the Democratic Republic of Congo. Oryx 36:35–40

    Article  Google Scholar 

  • Dupain J, Van Elsacker L (2001) The status of the bonobo in the Democratic Republic of Congo. In: Galdikas BMF, Briggs NE, Sheeran LK, Shapiro GL, Goodall J (eds) All Apes Great and Small Volume 1: African Apes. Kluwer Academic/Plenum Publishers, New York, pp 57–74

    Google Scholar 

  • Elith J, Graham CH, Anderson RP et al (2006) Novel methods improve prediction of species’ distributions from occurrence data. Ecography 29:129–151

    Article  Google Scholar 

  • Elith J, Phillips SJ, Hastie T, Dudík M, Chee YE, Yates C (2010) A statistical explanation of MaxEnt for ecologists. Divers Distrib 17:43–57

    Article  Google Scholar 

  • FAO (2000) Africover multipurpose land cover databases for Democratic Republic of Congo. Food and Agriculture Organization (FAO) of the United Nations, Rome. www.africover.org. Accessed 23 July 2011

  • Fruth B, Benishay JM, Bila-Isia I, Coxe S, Dupain J, Furuichi T, Hart J, Hart T, Hashimoto C, Hohmann G, Hurley M, Ilambu O, Mulavwa M, Ndunda M, Omasombo V, Reinartz G, Scherlis J, Steel L, Thompson J (2008) Pan paniscus. IUCN Red List of Threatened Species, Version 2010.4 (IUCN 2010). www.iucnredlist.org. Accessed 8 June 2011

  • Grossmann F, Hart J, Vosper A, Ilambu O (2008) Range occupation and population estimates of bonobos in the Salonga National Park: application to large-scale surveys of bonobos in the Democratic Republic of Congo. In: Furuichi T, Thompson J (eds) The bonobos behavior, ecology, and conservation. Springer, New York, pp 189–216

    Google Scholar 

  • Hansen MC, Roy D, Lindquist E, Adusei B, Justice CO, Altstatt AA (2008) A method for integrating MODIS and Landsat data for systematic monitoring of forest cover and change in the Congo Basin. Remote Sens Environ 112:2495–2513

    Article  Google Scholar 

  • Hart J, Grossmann F, Vosper A, Ilanga J (2008) Human hunting and its impact on bonobos in the salonga national park, Democratic Republic of Congo. In: Furuichi T, Thompson J (eds) The bonobos behavior, ecology, and conservation. Springer, New York, pp 245–271

    Google Scholar 

  • Hernandez PA, Graham CH, Master LL, Albert DL (2006) The effect of sample size and species characteristics on performance of different species distribution modeling methods. Ecography 29:773–785

    Article  Google Scholar 

  • Hickey JR (2012) Modeling bonobo (Pan paniscus) occurrence in relation to bushmeat hunting, slash-and-burn agriculture, and timber harvest: harmonizing bonobo conservation with sustainable development. Dissertation, University of Georgia

  • Hickey JR, Carroll JP, Nibbelink NP (2012) Applying landscape metrics to characterize potential habitat of bonobos (Pan paniscus) in the Maringa–Lopori–Wamba landscape, Democratic Republic of Congo. International J Primatol 33:381–400

    Article  Google Scholar 

  • Hijmans RJ, Cameron SE, Parra JL, Jones PG, Jarvis A (2005) Very high resolution interpolated climate surfaces for global land areas. International J Climatol 25:1965–1978

    Article  Google Scholar 

  • IUCN (2010) IUCN Red List of Threatened Species, Version 2010.4. www.iucnredlist.org. Accessed 7 Jun 2011

  • IUCN/SSC A.P.E.S. Database. http://apes.eva.mpg.de. Accessed 1 Feb 2011

  • Junker J, Blake S, Boesch C et al (2012) Recent decline in suitable environmental conditions of African great apes. Divers Distrib 18:1077–1091

    Article  Google Scholar 

  • McGarigal K, Cushman SA, Neel MC, Ene E (2002) FRAGSTATS: spatial pattern analysis program for categorical maps. Computer software program produced by the authors at the University of Massachusetts, Amherst. http://www.umass.edu/landeco/research/fragstats/fragstats.html

  • Mohneke M, Fruth B (2008) Bonobo (Pan paniscus) density estimation in the SW-salonga national park, Democratic Republic of Congo: common methodology revisited. In: Furuichi T, Thompson J (eds) The bonobos behavior, ecology, and conservation. Springer, New York, pp 151–166

    Google Scholar 

  • Mulavwa MN, Yangozene K, Yamba-Yamba M, Motema-Salo B, Mwanza NN, Furuichi T (2010) Nest groups of wild bonobos at Wamba: selection of vegetation and tree species and relationships between nest group size and party size. Am J Primatol 72:575–586

    PubMed  Google Scholar 

  • N’Goran PK, Boesch C, Mundry R, N’Goran EK, Herbinger I, Yapi FA, Kühl HS (2012) Hunting, law enforcement and African primate conservation. Conserv Biol 26:565–571

    Article  PubMed  Google Scholar 

  • OSFAC (Observatoire Satellital des forêts d’Afrique Central) (2010) Forêts d’Afrique centrale évaluées par télédétection (FACET): forest cover and forest cover loss in the Democratic Republic of Congo from 2000 to 2010. South Dakota State University and University of Maryland, Brookings and College Park. ISBN 978-0-9797182-5-0

    Google Scholar 

  • Phillips SJ (2006) A brief tutorial on Maxent. AT&T Research, Florham Park. http://www.cs.princeton.edu/~schapire/maxent/tutorial/tutorial.doc

  • Phillips SJ (2008) Transferability, sample selection bias and background data in presence-only modeling: a response to Peterson et al. (2007). Ecography 31:272–278

    Article  Google Scholar 

  • Phillips SJ, Anderson RP, Schapire RE (2006) Maximum entropy modeling of species geographic distributions. Ecol Model 190:231–259

    Article  Google Scholar 

  • Phillips SJ, Dudík M, Elith J, Graham CH, Lehmann A, Leathwich J, Ferrier S (2009) Sample selection bias and presence-only species distribution models: implications for background and pseudo-absence data. Ecol Appl 19:181–197

    Article  PubMed  Google Scholar 

  • Potapov P, Yaroshenko A, Turubanova S et al. (2008) Mapping the world’s intact forest landscapes by remote sensing. Ecol Soc 13(2):51. http://www.ecologyandsociety.org/vol13/iss2/art51/

    Google Scholar 

  • Reinartz GE, Guislain P, Mboyo Bolinga TD, Isomana E, Inogwabini B, Bokomo N, Ngamankosi M, Wema Wema L (2008) Ecological factors influencing bonobo density and distribution in the salonga national park: applications for population assessment. In: Furuichi T, Thompson J (eds) The bonobos: behavior, ecology, and conservation. Springer, New York, pp 167–188

    Google Scholar 

  • Robinson JG (1996) Hunting wildlife in forest patches: an ephemeral resource. In: Schelhas J, Greenberg R (eds) Forest Patches in Tropical Landscapes. Island Press, Washington, DC, pp 111–130

    Google Scholar 

  • Sanderson EW, Malanding J, Levy MA, Redford KH, Wannebo AV, Woolmer G (2002) The human footprint and the last of the wild. Bioscience 52:891–904

    Article  Google Scholar 

  • Stokes EJ, Strindberg S, Bakabana PC, Elkan PW, Iyenguet FC et al (2010) Monitoring great ape and elephant abundance at large spatial scales: measuring effectiveness of a conservation landscape. PLoS One 5(4):e10294. doi:10.1371/journal.pone.0010294

    Article  PubMed  Google Scholar 

  • Swenson JE (1982) Effects of hunting on habitat use by mule deer on mixed-grass prairie in Montana. Wildl Soc Bull 10:115–120

    Google Scholar 

  • Thompson-Handler N, Malenky RK, Reinartz GE (1995) Action plan for Pan paniscus: report on free ranging populations and proposals for their preservation. Zoological Society of Milwaukee County, Milwaukee

    Google Scholar 

  • Thorn JS, Nijman V, Smith D, Nekaris KAI (2009) Ecological niche modelling as a technique for assessing threats and setting conservation priorities for Asian slow lorises (Primates: nycticebus). Biodivers Distrib 15:289–298

    Article  Google Scholar 

  • Torres J, Brito JC, Vasconcelos MJ, Catarino L, Gonçalves J, Honrado J (2010) Ensemble models of habitat suitability relate chimpanzee (Pan troglodytes) conservation to forest and landscape dynamics in western Africa. Biolog Conserv 143:416–425

    Article  Google Scholar 

  • Tranquilli S, Abedi-Lartey M, Amsini F et al (2012) Lack of conservation effort rapidly increases African great ape extinction risk. Conserv Lett 5:48–55

    Article  Google Scholar 

  • UNDP (2011) Human development report 2011. United Nations development programme. Palgrave Macmillan, New York. ISBN: 9780230363311. http://hdr.undp.org/en/media/HDR_2011_EN_Complete.pdf

  • USAID (2010) Democratic Republic of Congo: biodiversity and tropical forestry assessment (118/119) final report. Prosperity, livelihoods and conserving ecosystems indefinite quantity contract (PLACE IQC) contract number EPP-I-03-06-00021-00. http://pdf.usaid.gov/pdf_docs/PNADS946.pdf

  • USGS (2000) HYDRO1k elevation derivative database. US geological survey earth resources observation and science (EROS) Center, Sioux Falls. http://eros.usgs.gov/#/Find_Data/Products_and_Data_Available/gtopo30/hydro/africa. Accessed 1 Sept 2010

  • van Engelen VWP, Verdoodt A, Dijkshoorn JA, Van Ranst E (2006) Soil and terrain database of central Africa (DR of Congo, Burundi and Rwanda). Report 2006/07, ISRIC World Soil Information, Wageningen. http://www.isric.org. Accessed 1 Sept 2010

  • VanDerWal J, Shoo LP, Graham C, Williams SE (2009) Selecting pseudo-absence data for presence-only distribution modeling: how far should you stray from what you know? Ecol Model 220:589–594

    Article  Google Scholar 

  • Veloz SD (2009) Spatially autocorrelated sampling falsely inflates measures of accuracy for presence-only niche models. J Biogeogr 36:2290–2299

    Article  Google Scholar 

  • Wich SA, Fredriksson GM, Usher G, Peters HH, Priatna D, Basalamah F, Susanto W, Kühl HS (2011) Hunting of Sumatran orang-utans and its importance in determining distribution and density. Biol Conserv 146:163–169

    Article  Google Scholar 

  • Wiley EO, McNyset KM, Peterson AT, Robins CR, Stewart AM (2003) Niche modeling and geographic range predictions in the marine environment using a machine-learning algorithm. Oceanography 16:120–127

    Article  Google Scholar 

  • Wilkie DS, Morelli GA, Shaw E, Rotberg F, Auzel P (2000) Roads, development and conservation in the Congo basin. Conserv Biol 14:1614–1622

    Article  Google Scholar 

  • WRI (2010) Interactive forest atlas for Democratic Republic of Congo (Atlas forestier interactif de la République Démocratique du Congo), version 1.0. World resources institute and the ministry of the environment. Conservation of Nature and Tourism of the Democratic Republic of Congo, Washington, DC, USA. http://www.wri.org/publication/interactive-forest-atlas-democratic-republic-of-congo

  • Yackulic CB, Chandler R, Zipkin EF, Royle JA, Nichols JD, Grant EHC, Veran S (2013) Presence-only modelling using MAXENT: when can we trust the inferences? Methods Ecol Evol 4:236–243

    Article  Google Scholar 

  • Yamagiwa J (2003) Bushmeat poaching and the conservation crisis in Kahuzi-Biega National Park, Democratic Republic of the Congo. J. Sustain For 16:111–130

    Article  Google Scholar 

Download references

Acknowledgments

We thank the Arcus Foundation, Columbus Zoo, Conservation International, European Union, Frankenberg Foundation, IUCN/SSC Primate Specialist Group, Margot Marsh Biodiversity Foundation Primate Action Fund, Max Planck Institute (MPI) for Evolutionary Anthropology, United States Agency for International Development (USAID) Central Africa Regional Program for the Environment (CARPE), United States Fish and Wildlife Service Great Apes Program, United States Forest Service, University of Georgia, University of Kent, Wildlife Conservation Society (WCS), Woodtiger Foundation, and World Wildlife Fund (WWF) for funding. MPI compiled the bonobo presence data through the IUCN/SSC A.P.E.S. database. Terese Hart (Lukuru Foundation), Jo Thompson (Lukuru Wildlife Research Project), Simeon Dino S’hwa (WCS and Lukuru Foundation) and Christine Tam (WWF) provided a portion of the bonobo presence data. The first author holds an American Fellowship with the American Association of University Women.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Jena R. Hickey.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1

The response curves of the relative suitability of conditions for bonobos and the predictor variables from the final rangewide MaxEnt model depict a negative relationship for forest fragmentation as measured by edge density (km/km2), and positive relationships for distance from river (km), distance from agriculture (km), and percent-forest landcover (TIFF 1300 kb)

Supplementary material 2

A comparison of the MaxEnt rangewide spatial predictions of relative suitability for bonobos (a) without elevation and (b) with elevation as a fifth variable, Democratic Republic of Congo (TIFF 7736 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Hickey, J.R., Nackoney, J., Nibbelink, N.P. et al. Human proximity and habitat fragmentation are key drivers of the rangewide bonobo distribution. Biodivers Conserv 22, 3085–3104 (2013). https://doi.org/10.1007/s10531-013-0572-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10531-013-0572-7

Keywords

Navigation