Biodiversity and Conservation

, Volume 22, Issue 13–14, pp 3085–3104 | Cite as

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

  • Jena R. Hickey
  • Janet Nackoney
  • Nathan P. Nibbelink
  • Stephen Blake
  • Aime Bonyenge
  • Sally Coxe
  • Jef Dupain
  • Maurice Emetshu
  • Takeshi Furuichi
  • Falk Grossmann
  • Patrick Guislain
  • John Hart
  • Chie Hashimoto
  • Bernard Ikembelo
  • Omari Ilambu
  • Bila-Isia Inogwabini
  • Innocent Liengola
  • Albert Lotana Lokasola
  • Alain Lushimba
  • Fiona Maisels
  • Joel Masselink
  • Valentin Mbenzo
  • Norbert Mbangia Mulavwa
  • Pascal Naky
  • Nicolas Mwanza Ndunda
  • Pele Nkumu
  • Valentin Omasombo
  • Gay Edwards Reinartz
  • Robert Rose
  • Tetsuya Sakamaki
  • Samantha Strindberg
  • Hiroyuki Takemoto
  • Ashley Vosper
  • Hjalmar S. Kühl
Original Paper

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.

Keywords

Bonobo Distribution Fragmentation Habitat Hunting IUCN/SSC A.P.E.S. database Pan paniscus 

Supplementary material

10531_2013_572_MOESM1_ESM.tif (1.3 mb)
Supplementary material 1The 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)
10531_2013_572_MOESM2_ESM.tif (7.6 mb)
Supplementary material 2A 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)

References

  1. Anderson RP, Gonzalez I (2011) Species-specific tuning increases robustness to sampling bias in models of species distributions: an implementation with Maxent. Ecol Model 222:2796–2811CrossRefGoogle Scholar
  2. 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 70:69–77PubMedCrossRefGoogle Scholar
  3. 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 PubMedCrossRefGoogle Scholar
  4. 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 PubMedCrossRefGoogle Scholar
  5. 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 30:217–228CrossRefGoogle Scholar
  6. 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 7:723–726PubMedCrossRefGoogle Scholar
  7. DeLong ER, DeLong D, Clarke-Pearson D (1988) Comparing the areas under two or more correlated receiver operating characteristic curves: a nonparametric approach. Biometrics 44:837–845PubMedCrossRefGoogle Scholar
  8. Draulans D, Van Krunkelsven E (2002) The impact of war on forest areas in the Democratic Republic of Congo. Oryx 36:35–40CrossRefGoogle Scholar
  9. 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 57–74Google Scholar
  10. Elith J, Graham CH, Anderson RP et al (2006) Novel methods improve prediction of species’ distributions from occurrence data. Ecography 29:129–151CrossRefGoogle Scholar
  11. Elith J, Phillips SJ, Hastie T, Dudík M, Chee YE, Yates C (2010) A statistical explanation of MaxEnt for ecologists. Divers Distrib 17:43–57CrossRefGoogle Scholar
  12. 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
  13. 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
  14. 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 189–216Google Scholar
  15. 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 112:2495–2513CrossRefGoogle Scholar
  16. 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 245–271Google Scholar
  17. 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 29:773–785CrossRefGoogle Scholar
  18. 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 GeorgiaGoogle Scholar
  19. 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 33:381–400CrossRefGoogle Scholar
  20. Hijmans RJ, Cameron SE, Parra JL, Jones PG, Jarvis A (2005) Very high resolution interpolated climate surfaces for global land areas. International J Climatol 25:1965–1978CrossRefGoogle Scholar
  21. IUCN (2010) IUCN Red List of Threatened Species, Version 2010.4. www.iucnredlist.org. Accessed 7 Jun 2011
  22. IUCN/SSC A.P.E.S. Database. http://apes.eva.mpg.de. Accessed 1 Feb 2011
  23. Junker J, Blake S, Boesch C et al (2012) Recent decline in suitable environmental conditions of African great apes. Divers Distrib 18:1077–1091CrossRefGoogle Scholar
  24. 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
  25. 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 151–166Google Scholar
  26. 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 72:575–586PubMedGoogle Scholar
  27. 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 26:565–571PubMedCrossRefGoogle Scholar
  28. 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 978-0-9797182-5-0Google Scholar
  29. Phillips SJ (2006) A brief tutorial on Maxent. AT&T Research, Florham Park. http://www.cs.princeton.edu/~schapire/maxent/tutorial/tutorial.doc
  30. Phillips SJ (2008) Transferability, sample selection bias and background data in presence-only modeling: a response to Peterson et al. (2007). Ecography 31:272–278CrossRefGoogle Scholar
  31. Phillips SJ, Anderson RP, Schapire RE (2006) Maximum entropy modeling of species geographic distributions. Ecol Model 190:231–259CrossRefGoogle Scholar
  32. 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 19:181–197PubMedCrossRefGoogle Scholar
  33. 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
  34. 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 167–188Google Scholar
  35. 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 111–130Google Scholar
  36. Sanderson EW, Malanding J, Levy MA, Redford KH, Wannebo AV, Woolmer G (2002) The human footprint and the last of the wild. Bioscience 52:891–904CrossRefGoogle Scholar
  37. 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 PubMedCrossRefGoogle Scholar
  38. Swenson JE (1982) Effects of hunting on habitat use by mule deer on mixed-grass prairie in Montana. Wildl Soc Bull 10:115–120Google Scholar
  39. 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, MilwaukeeGoogle Scholar
  40. 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 15:289–298CrossRefGoogle Scholar
  41. 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 143:416–425CrossRefGoogle Scholar
  42. Tranquilli S, Abedi-Lartey M, Amsini F et al (2012) Lack of conservation effort rapidly increases African great ape extinction risk. Conserv Lett 5:48–55CrossRefGoogle Scholar
  43. 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
  44. 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
  45. 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
  46. 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
  47. 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 220:589–594CrossRefGoogle Scholar
  48. Veloz SD (2009) Spatially autocorrelated sampling falsely inflates measures of accuracy for presence-only niche models. J Biogeogr 36:2290–2299CrossRefGoogle Scholar
  49. 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 146:163–169CrossRefGoogle Scholar
  50. 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 16:120–127CrossRefGoogle Scholar
  51. Wilkie DS, Morelli GA, Shaw E, Rotberg F, Auzel P (2000) Roads, development and conservation in the Congo basin. Conserv Biol 14:1614–1622CrossRefGoogle Scholar
  52. 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
  53. 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 4:236–243CrossRefGoogle Scholar
  54. Yamagiwa J (2003) Bushmeat poaching and the conservation crisis in Kahuzi-Biega National Park, Democratic Republic of the Congo. J. Sustain For 16:111–130CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2013

Authors and Affiliations

  • Jena R. Hickey
    • 1
  • Janet Nackoney
    • 2
  • Nathan P. Nibbelink
    • 3
  • Stephen Blake
    • 4
  • Aime Bonyenge
    • 5
  • Sally Coxe
    • 6
  • Jef Dupain
    • 7
  • Maurice Emetshu
    • 5
  • Takeshi Furuichi
    • 8
  • Falk Grossmann
    • 9
  • Patrick Guislain
    • 10
  • John Hart
    • 11
  • Chie Hashimoto
    • 8
  • Bernard Ikembelo
    • 5
  • Omari Ilambu
    • 12
  • Bila-Isia Inogwabini
    • 12
  • Innocent Liengola
    • 5
  • Albert Lotana Lokasola
    • 13
  • Alain Lushimba
    • 14
  • Fiona Maisels
    • 9
    • 15
  • Joel Masselink
    • 9
  • Valentin Mbenzo
    • 16
  • Norbert Mbangia Mulavwa
    • 17
  • Pascal Naky
    • 5
  • Nicolas Mwanza Ndunda
    • 17
  • Pele Nkumu
    • 5
  • Valentin Omasombo
    • 18
  • Gay Edwards Reinartz
    • 10
  • Robert Rose
    • 9
  • Tetsuya Sakamaki
    • 8
  • Samantha Strindberg
    • 9
  • Hiroyuki Takemoto
    • 8
  • Ashley Vosper
    • 19
  • Hjalmar S. Kühl
    • 20
  1. 1.Department of Natural ResourcesCornell UniversityIthacaUSA
  2. 2.Department of Geographical SciencesUniversity of MarylandCollege ParkUSA
  3. 3.Warnell School of Forestry and Natural ResourcesUniversity of GeorgiaAthensUSA
  4. 4.Max Planck Institute of OrnithologyRadolfzellGermany
  5. 5.Wildlife Conservation SocietyKinshasaDemocratic Republic of the Congo
  6. 6.Bonobo Conservation InitiativeWashingtonUSA
  7. 7.African Wildlife Foundation Conservation CentreNairobiKenya
  8. 8.Primate Research InstituteKyoto UniversityInuyamaJapan
  9. 9.Wildlife Conservation SocietyBronxUSA
  10. 10.Bonobo and Congo Biodiversity InitiativeZoological Society of MilwaukeeMilwaukeeUSA
  11. 11.Lukuru FoundationKinshasaDemocratic Republic of the Congo
  12. 12.World Wildlife Fund, DRCKinshasaDemocratic Republic of the Congo
  13. 13.Kokolopori Bonobo Nature ReserveKinshasaDemocratic Republic of the Congo
  14. 14.African Wildlife FoundationKinshasaDemocratic Republic of the Congo
  15. 15.School of Natural Sciences, Biological and Environmental SciencesUniversity of StirlingStirlingScotland, UK
  16. 16.Congo Basin Ecosystems Conservation Support Program (PACEBCo)KinshasaDemocratic Republic of the Congo
  17. 17.Center of Research in Ecology and Forestry (CREF)Ministry of Education and Scientific ResearchMabaliDemocratic Republic of the Congo
  18. 18.Congolese Institute for the Conservation of Nature (ICCN)KinshasaDemocratic Republic of the Congo
  19. 19.Wildlife Conservation SocietyZanagaDemocratic Republic of the Congo
  20. 20.Max Planck Institute for Evolutionary AnthropologyLeipzigGermany

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