Abstract
The conservation of endangered species can benefit from a clear understanding of the quantity and distribution of their main foods. The population of mountain gorillas (Gorilla beringei beringei) living in the Virunga Massif of Rwanda, Uganda, and Democratic Republic of Congo has doubled in size since the 1980s, due to success in conservation efforts in and around their habitat. However, this increase in population size along with pressures on gorilla habitat raises concerns about spatial-temporal changes in the gorillas’ food plants. This study modelled the abundance and distribution of gorilla food species in the Virunga Massif. A total of 1050 vegetation recordings were collected on five plant species that are known to be frequently consumed by gorillas in one region of the Virungas, the Karisoke area. Two types of datasets collected along vegetation zones were combined: one with plant abundance expressed with Braun-Blanquet scores; and the other with abundance expressed as biomass. Moreover, ecological characteristics of locations where these species occur were extracted from satellite imagery. Analysis of variance and linear regression models were used to examine relationships between food species abundances and predictor variables. Subsequently, maps for the food species were created using boosted regression trees (BRTs). The abundance of species differed across vegetation zones, and the differences were statistically significant among vegetation zones with enough species observations. The accuracy of the BRTs indicated greater than random predictions (AUC > 0.65). This study shows the suitable areas for these gorilla food species and relevant ecological variables determining their distribution. The results provide insights into habitat occupancy by mountain gorillas, and help to design a baseline for monitoring changes in the abundance of gorilla food species under changing climate and anthropogenic pressure.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
The georeferenced distribution maps for each of the targeted food species are submitted as electronic supplementary material and will be made available online as raster data (Online Resource 6).
References
Albeare SM (2009) Comparisons of Boosted Regression Tree, GLM and GAM performance in the standardization of yellowfin tuna catch-rate. Data from the Gulf of Mexico longline fishery. Dissertation, Louisiana State University
Allouche O, Tsoar A, Kadmon R (2006) Assessing the accuracy of species distribution models: prevalence, kappa and the true skill statistic (TSS). J Appl Ecol 43(6):1223–1232. https://doi.org/10.1111/j.1365-2664.2006.01214.x
Bader MY, Ruijten JJA (2008) A topographic-based model of forest cover at the alpine tree line in the tropical Andes. Biodiversity 35:711–723. https://doi.org/10.1111/j.1365-2699.2007.01818.x
Belfiore N, Seimon A, Picton PG, Basabose A, Gray M, Masinde I, Elliott J, Thorne JH, Seo CW, Muruthi P (2015) The implications of global climate change for mountain gorilla conservation in the Albertine Rift. A white paper prepared by the African Wildlife Foundation, the International Gorilla Conservation Programme and EcoAdapt. Kigali, Rwanda
Bergseng E, Ørka HO, Næsset E, Gobakken T (2015) Assessing forest inventory information obtained from different inventory approaches and remote sensing data sources. Ann For Sci 72(1):33–45. https://doi.org/10.1007/s13595-014-0389-x
Blanca M, Alarcón R, Arnau J, Bono R, Bendayan R (2017) Non-normal data: is ANOVA still a valid option? Psicothema 29(4):552–557. https://doi.org/10.7334/psicothema2016.383
Chen I, Shiu H, Benedick S, Holloway JD, Khen V, Barlow HS, Hill JK, Thomas CD (2009) Elevation increases in moth assemblages over 42 years on a tropical mountain. Proc Natl Aacd Sci USA 106(5):1479–1483
De’ath G (2007) Boosted trees for ecological modelling and prediction. Ecol Soc Am 88(1):243–251
De’ath G, Fabricius KE (2013) Classification and regression trees: a powerful yet simple technique for ecological data analysis. Ecol Soc Am 81(11):3178–3192
Dondeyne S, Deckers JA, Chapelle J (1993) The soils and vegetation of the Bisoke volcano (Rwanda): habitat of mountain gorillas. Pedologie 43:301–322
Duque-Lazo J, van Gils H, Groen TA, Navarro-Cerrillo RM (2016) Transferability of species distribution models: the case of Phytophthora cinnamomi in Southwest Spain and Southwest Australia. Ecol Model 320:62–70. https://doi.org/10.1016/j.ecolmodel.2015.09.019
Elith J, Leathwick JR (2009) Species distribution models: ecological explanation and prediction across space and time. Annu Rev Ecol Evolut Syst. https://doi.org/10.1146/annurev.ecolsys.110308.120159
Elith J, Leathwick JR, Hastie T (2008) A working guide to boosted regression trees. J Anim Ecol 77(4):802–813. https://doi.org/10.1111/j.1365-2656.2008.01390.x
Ellenberg D, Mueller-Dombois D (1974) Community sampling: the relevé method. Aims and methods of vegetation ecology. New York-London-Sydney-Toronto, John Wiley and Sons
Field A (2009) Discovering statistics using SPSS, 3rd edn. SAGE Publications, Los Angeles
Fossey D (1974) Observations on the home range of one group of mountain gorillas (Gorilla gorilla beringei). Anim Behav 22(3):568–581. https://doi.org/10.1016/S0003-3472(74)80002-3
Foster P (2001) The potential negative impacts of global climate change on tropical montane cloud forests. Earth-Sci Rev 55(1–2):73–106. https://doi.org/10.1016/S0012-8252(01)00056-3
Ganas J, Robbins MM, Nkurunungi JB, Kaplin BA, McNeilage A (2004) Dietary variability of mountain gorillas in Bwindi Impenetrable National Park, Uganda. Int J Primatol 25(5):1043–1072. https://doi.org/10.1023/B:IJOP.0000043351.20129.44
Goodall J (1977) Feeding and ranging behaviour of a mountain gorilla group (Gorilla gorilla beringei) in the Tshibinda-Kahuzi Region (Zaïre). In: Clutton-Brock TH (ed) Primate ecology: studies of feeding and ranging behaviour in lemurs, monkeys and apes. University of Chicago Press, Chicago, pp 449–479
Granjon AC, Robbins M, Arinaitwe J, Cranfield M, Eckardt W, Mburanumwe I, Musana A, Robbins A, Roy J, Vigilant L, Hickey J (2019) Increased survey effort and intrinsic growth contribute to the largest recorded mountain gorilla population. Anim Conserv, in review
Gray M, McNeilage A, Fawcett K, Robbins MM, Ssebide B, Mbula D, Uwingeli P (2010) Censusing the mountain gorillas in the Virunga Volcanoes: complete sweep method versus monitoring. Afr J Ecol 48(3):588–599. https://doi.org/10.1111/j.1365-2028.2009.01142.x
Gray M, Roy J, Vigilant L, Fawcett K, Basabose A, Cranfield M, Uwingeli P, Mburanumwe I, Kagoda E, Robbins MM (2013) Genetic census reveals increased but uneven growth of a critically endangered mountain gorilla population. Biol Conserv 158:230–238. https://doi.org/10.1016/j.biocon.2012.09.018
Grueter CC, Ndamiyabo F, Plumptre AJ, Abavandimwe D, Mundry R, Fawcett K, Robbins MM (2013) Long-term temporal and spatial dynamics of food availability for endangered mountain gorillas in Volcanoes National Park, Rwanda. Am J Primatol 75(3):267–280. https://doi.org/10.1002/ajp.22102
Grueter CC, Deschner T, Behringer V, Fawcett K, Robbins MM (2014) Socioecological correlates of energy balance using urinary C-peptide measurements in wild female mountain gorillas. Physiol Behav 127:13–19. https://doi.org/10.1016/j.physbeh.2014.01.009
Grueter CC, Wright E, Abavandimwe D, Ortmann S, Mudakikwa A, Musana A, Uwingeli P, Ngagijimana F, Vecellio V, Stoinski TS, Robbins MM (2018) Going to extremes for sodium acquisition: use of community land and high-altitude areas by mountain gorillas Gorilla beringei in Rwanda. Biotropica 50(5):826–834. https://doi.org/10.1111/btp.12598
Guisan A, Zimmermann NE (2000) Predictive habitat distribution models in ecology. Ecol Model 135:147–186. https://doi.org/10.1016/S0304-3800(00)00354-9
Hanley AJ, McNeil JB (1982) The meaning and use of the area under a receiver operating characteristic (ROC) curve. Radiol 143:29–36. https://doi.org/10.1148/radiology.143.1.7063747
Hermes C, Segelbacher G, Schaefer HM (2018) A framework for prioritizing areas for conservation in tropical montane cloud forests. Ecoscience 25(1):97–108. https://doi.org/10.1080/11956860.2017.1419787
Hickey JR, Basabose A, Gilardi KV, Greer D, Nampindo S, Robbins MM, Stoinski TS (2018) Gorilla beringei ssp. The IUCN Red List of Threatened Species 2018. E.T39999A17989719, 8235. IUCN Red List. https://doi.org/10.2305/IUCN.UK.2018-2.RLTS.T39999A17989719.en
Hitimana J, Namara A, Sengalama T (2006) Community-based natural resource management plan (CBNRM). Report prepared for the International Gorilla Conservation Programme, Kigali
IUCN (2019) The IUCN Red List of Threatened Species. Version 2019-1. https://www.iucnredlist.org/. Accessed 05 May 2019
Joshi C, De Leeuw J, van Andel J, Skidmore AK, Lekhak HD, van Duren IC, Norbu N (2006) Indirect remote sensing of a cryptic forest understorey invasive species. For Ecol Manag 225(1–3):245–256. https://doi.org/10.1016/j.foreco.2006.01.013
Kalpers J, Williamson EA, Robbins MM, McNeilage A, Nzamurambaho A, Lola N, Mugiri G (2003) Gorillas in the crossfire: population dynamics of the Virunga mountain gorillas over the past three decades. Oryx 37(03):326–337. https://doi.org/10.1017/S0030605303000589
Kayijamahe E (2008) Spatial modelling of mountain gorilla (Gorilla beringei beringei) habitat suitability and human impact. Dissertation, University of Twente, Faculty of Geo-information Science and Earth Observation (ITC)
Kübler D, Hildebrandt P, Günter S, Stimm B, Weber M, Mosandl R, Muñoz J, Cabrera O, Anguirre N, Zeilinger J, Silva B (2015) Assessing the importance of topographic variables for the spatial distribution of tree species in a tropical mountain forest. Erdkunde 70(1):19–47. https://doi.org/10.3112/erdkunde.2016.01.03
Leathwick JR, Elith J, Francis MP, Hastie T, Taylor P (2006) Variation in demersal fish species richness in the oceans surrounding New Zealand: an analysis using boosted regression trees. Mar Ecol Prog Ser 321:267–281. https://doi.org/10.3354/meps321267
Liu C, White M, Newell G (2011) Measuring and comparing the accuracy of species distribution models with presence-absence data. Ecography 34(2):232–243. https://doi.org/10.1111/j.1600-0587.2010.06354.x
Liu C, White M, Newell G (2013) Selecting thresholds for the prediction of species occurrence with presence-only data. J Biogeogr 40(4):778–789. https://doi.org/10.1111/jbi.12058
Lowman MD (1986) Light interception and its relation to structural differences in three Australian rainforest canopies. Aust J Ecol 11(2):163–170. https://doi.org/10.1111/j.1442-9993.1986.tb01387.x
McGahey DJ, Williams DG, Muruthi P, Loubser DI (2013) Investigating climate change vulnerability and planning for adaptation: learning from a study of climate change impacts on the mountain gorilla in the Albertine Rift. Nat Sci 5(5):10–17
McNeilage AJ (1995) Mountain gorillas in the Virunga Volcanoes: ecology and carrying capacity. Dissertation, University of Bristol
McNeilage A (2001) Diet and habitat use of two mountain gorilla groups in contrasting habitats in the Virungas. In: Robbins MM, Sicotte P, Stewart KJ (eds) Mountain gorillas. Cambridge University Press, Cambridge, pp 265–292. https://doi.org/10.1017/CBO9780511661631.011
Owiunji I, Nkuutu D, Kujirankwinja D, Liengola I, Plumptre AJ, Nsanzurwimo A, Fawcett K, McNeilage A (2005) The biodiversity of the Virunga Volcanoes. Report by WCS, IGCP, DFGFI, ITFC. Kigali, Rwanda
Phillips SJ, Anderson RP, Schapire RE (2006) Maximum entropy modelling of species geographic distributions. Ecol Model 190(3–4):231–259. https://doi.org/10.1016/j.ecolmodel.2005.03.026
Piedallu C, Gégout J (2008) Efficient assessment of topographic solar radiation to improve plant distribution models. Agric For Meteorol 148(11):1696–1706. https://doi.org/10.1016/j.agrformet.2008.06.001
Plumptre AJ (1991) Plant-herbivore dynamics in the Birungas. Dissertation, University of Bristol
Plumptre AJ, Williamson AE (2001) Conservation-oriented research in the Virunga region. In: Robbins MM, Sicotte P, Kelly J (eds) Mountain gorillas: three decades of research at Karisoke. Cambridge University Press, Cambridge, pp 361–390
Quinn GP, Keough MJ (2002) Experimental design and data analysis for biologists. Cambridge University Press, New York. https://doi.org/10.1016/S0022-0981(02)00278-2
R Development Core Team R (2014) R: a language and environment for statistical computing. R foundation for statistical computing. http://www.r-project.org/. Accessed 9 January 2019
REMA (2011) Atlas of Rwandaʼs changing environment: implications for climate change resilience. Kigali, Rwanda. https://na.unep.net/siouxfalls/publications/REMA.pdf. Accessed 01 June 2015
Robbins MM, Gray M, Fawcett K, Nutter FB, Uwingeli P, Mburanumwe I, Kagoda E, Basabose A, Stoinski TS, Cranfield MR, Byamukama J, Spelman LH, Robbins AM (2011) Extreme conservation leads to recovery of the Virunga mountain gorillas. PLoS ONE 6:e19788. https://doi.org/10.1371/journal.pone.0019788
Rothman JM, Plumptre AJ, Dierenfeld ES, Pell AN (2007) Nutritional composition of the diet of the gorilla (Gorilla beringei): a comparison between two montane habitats. J Trop Ecol 23(6):673–682. https://doi.org/10.1017/S0266467407004555
Seiler N, Boesch C, Mundry R, Stephens C, Robbins MM, Seiler N (2017) Space partitioning in wild, non-territorial mountain gorillas: the impact of food and neighbours. R Soc Open Sci 4:170720
Smith JBM (1977) Vegetation and microclimate of east and west-facing slopes in the grasslands of Mt Wilhelm Papua New Guinea. J Ecol 65(1):39–53
Spinage CA (1972) The ecology and problems of the Volcanoes National Park, Rwanda. Biol Conserv 4(3):194–204. https://doi.org/10.1016/0006-3207(72)90169-3
Tanner EVJ, Vltousek PM, Cuevas E (1998) Experimental investigation of nutrient limitation of forest growth on wet tropical mountains. Ecol 79(1):10–22. https://doi.org/10.2307/176860
Tuyisingize D (2010) Terrestrial small mammal community composition in the Volcanoes National Park, Rwanda. Dissertation, University of Cape Town
van Gils H, Kayijamahe E (2010) Sharing natural resources: mountain gorillas and people in the Parc National des Volcans, Rwanda. Afr J Ecol 48(3):621–627. https://doi.org/10.1111/j.1365-2028.2009.01154.x
Vedder AL (1984) Movement patterns of a group of free-ranging mountain gorillas (Gorilla gorilla beringei) and their relation to food availability. Am J Primatol 7(2):73–88. https://doi.org/10.1002/ajp.1350070202
Watts DP (1984) Composition and variability of mountain gorilla diets in the Central Virungas. Am J Primatol 7(4):323–356. https://doi.org/10.1002/ajp.1350070403
Watts DP (1998) Long-term habitat use by mountain gorillas (Gorilla gorilla beringei). 1. Consistencey, variation, and home range size and stability. Int J Primatol 19(4):651–679
Weber AW, Vedder AL (1983) Population dynamics of the Virunga gorillas: 1959–1978. Biol Conserv 26(4):341–366. https://doi.org/10.1016/0006-3207(83)90096-4
Wikum DA, Shanholtzer GF (1978) Application of Braun-Blaquet cover-abundance scale for vegetation analysis in land-development studies. Environ Manag 2(4):323–329. https://doi.org/10.1007/bf01866672
Williamson EA, Fawcett K (2008) Long-term research and conservation of the Virunga mountain gorillas. In: Wrangham R, Ross E (eds) Science and conservation in African forests: the benefits of long-term research. Cambridge University Press, Cambridge, pp 213–229. https://doi.org/10.1017/CBO9780511754920
Wright E, Grueter CC, Seiler N, Abavandimwe D, Stoinski TS, Ortmann S, Robbins MM (2015) Energetic responses to variation in food availability in the two mountain gorilla populations (Gorilla beringei beringei). Am J Phys Anthropol 158(3):487–500. https://doi.org/10.1002/ajpa.22808
Acknowledgements
Special thanks are addressed to the Dutch Government, for an MSc grant to the main author of this paper. The constructive comments from the anonymous reviewers that helped to improve the manuscript are very much appreciated. Deep gratitude to Mr Télesphore Ngoga and Mr Abel Musana from Rwanda Development Board for assisting with getting permission and logistics for this research. Thanks to Dr Winnie Eckardt from the Karisoke Research Centre in Rwanda for facilitating the data sharing. An additional dataset used in this study was made available from the Dian Fossey Gorilla Fund (DFGF). We are very grateful to Mr Félix Ndagijimana, the Director of Karisoke in Rwanda and Dr Tara Stoinski, the President and Chief Scientific Officer of DFGF based in Atlanta, United States of America.
Funding
This study was funded by Grant No. (NFP-MA.14/5718).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Communicated by Xiaoli Shen.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Akayezu, P., van Duren, I.C., Groen, T.A. et al. Abundance and spatial distribution of the main food species for mountain gorillas in the Virunga Massif, Rwanda. Biodivers Conserv 28, 3597–3620 (2019). https://doi.org/10.1007/s10531-019-01838-0
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10531-019-01838-0