The distribution of plant consumption traits across habitat types and the patterns of fruit availability suggest a mechanism of coexistence of two sympatric frugivorous mammals

Tédonzong, L. R. D.; Willie, J.; Tagg, N.; Tchamba, M. N.; Angwafo, T. E.; Keuko, A. M. P.; Kuenbou, J. K.; Petre, Charles-Albert; Lens, L.

doi:10.1002/ece3.5017

Article (Scientific journals)

The distribution of plant consumption traits across habitat types and the patterns of fruit availability suggest a mechanism of coexistence of two sympatric frugivorous mammals

Tédonzong, L. R. D.; Willie, J.; Tagg, N. et al.

2019 • In Ecology and Evolution, 9 (8), p. 4473-4494

Peer Reviewed verified by ORBi

Permalink
https://hdl.handle.net/2268/266368

DOI
10.1002/ece3.5017

Files (1)Send to Details Statistics Bibliography Similar publications

Files

Full Text

Ecology and Evolution - 2019.pdf

Publisher postprint (1.45 MB)

Download

This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

All documents in ORBi are protected by a user license.

Send to

RIS BibTex APA Chicago Permalink X Linkedin

Details

Keywords :

Niche partitioning in primates

Abstract :

[en] Understanding the mechanisms governing the coexistence of organisms is an important question in ecology, and providing potential solutions contributes to conservation science. In this study, we evaluated the contribution of several mechanisms to the coexistence of two sympatric frugivores, using western lowland gorillas (Gorilla gorilla gorilla) and central chimpanzees (Pan troglodytes troglodytes) in a tropical rainforest of southeast Cameroon as a model system. We collected great ape fecal samples to determine and classify fruit species consumed; we conducted great ape nest surveys to evaluate seasonal patterns of habitat use; and we collected botanical data to investigate the distribution of plant species across habitat types in relation to their “consumption traits” (which indicate whether plants are preferred or fallback for either gorilla, chimpanzee, or both). We found that patterns of habitat use varied seasonally for both gorillas and chimpanzees and that gorilla and chimpanzee preferred and fallback fruits differed. Also, the distribution of plant consumption traits was influenced by habitat type and matched accordingly with the patterns of habitat use by gorillas and chimpanzees. We show that neither habitat selection nor fruit preference alone can explain the coexistence of gorillas and chimpanzees, but that considering together the distribution of plant consumption traits of fruiting woody plants across habitats as well as the pattern of fruit availability may contribute to explaining coexistence. This supports the assumptions of niche theory with dominant and subordinate species in heterogeneous landscapes, whereby a species may prefer nesting in habitats where it is less subject to competitive exclusion and where food availability is higher. To our knowledge, our study is the first to investigate the contribution of plant consumption traits, seasonality, and habitat heterogeneity to enabling the coexistence of two sympatric frugivores. OPEN RESEARCH BADGES: This article has earned an Open Data Badge for making publicly available the digitally-shareable data necessary to reproduce the reported results. The data is available at https://datadryad.org/resource/doi:10.5061/dryad.ms65f29. © 2019 The Authors. Ecology and Evolution published by John Wiley & Sons Ltd.

Disciplines :

Environmental sciences & ecology

Author, co-author :

Tédonzong, L. R. D.; Projet Grands Singes (PGS), Cameroun, Centre for Research and Conservation (CRC), Royal Zoological Society of Antwerpen (RZSA), Antwerpen, Belgium, Terrestrial Ecology Unit (TEREC), Department of Biology, Ghent University (UGent), Ghent, Belgium, Department of Forestry, University of Dschang, Dschang, Cameroon

Willie, J.; Projet Grands Singes (PGS), Cameroun, Centre for Research and Conservation (CRC), Royal Zoological Society of Antwerpen (RZSA), Antwerpen, Belgium, Terrestrial Ecology Unit (TEREC), Department of Biology, Ghent University (UGent), Ghent, Belgium

Tagg, N.; Projet Grands Singes (PGS), Cameroun, Centre for Research and Conservation (CRC), Royal Zoological Society of Antwerpen (RZSA), Antwerpen, Belgium

Tchamba, M. N.; Department of Forestry, University of Dschang, Dschang, Cameroon

Angwafo, T. E.; Department of Forestry, University of Dschang, Dschang, Cameroon, Department of Fundamental Sciences, The University of Bamenda, HTTTC, Bambili, Cameroon

Keuko, A. M. P.; Projet Grands Singes (PGS), Cameroun, Centre for Research and Conservation (CRC), Royal Zoological Society of Antwerpen (RZSA), Antwerpen, Belgium, Terrestrial Ecology Unit (TEREC), Department of Biology, Ghent University (UGent), Ghent, Belgium, Department of Forestry, University of Dschang, Dschang, Cameroon

Kuenbou, J. K.; Projet Grands Singes (PGS), Cameroun, Centre for Research and Conservation (CRC), Royal Zoological Society of Antwerpen (RZSA), Antwerpen, Belgium, Terrestrial Ecology Unit (TEREC), Department of Biology, Ghent University (UGent), Ghent, Belgium, Department of Forestry, University of Dschang, Dschang, Cameroon

Petre, Charles-Albert ; Université de Liège - ULiège

Lens, L.; Terrestrial Ecology Unit (TEREC), Department of Biology, Ghent University (UGent), Ghent, Belgium

Language :

English

Title :

The distribution of plant consumption traits across habitat types and the patterns of fruit availability suggest a mechanism of coexistence of two sympatric frugivorous mammals

Publication date :

2019

Journal title :

Ecology and Evolution

eISSN :

2045-7758

Publisher :

John Wiley and Sons Ltd

Volume :

Issue :

Pages :

4473-4494

Peer reviewed :

Peer Reviewed verified by ORBi

Funders :

Chesapeake Research Consortium

Available on ORBi :

since 22 December 2021

Statistics

Number of views

34 (2 by ULiège)

Number of downloads

57 (2 by ULiège)

More statistics

Scopus citations^®

Scopus citations^®
without self-citations

OpenCitations

OpenAlex citations

Bibliography

Amarasekare, P. (2003). Competitive coexistence in spatially structured environments: A synthesis. Ecology Letters, 6, 1109–1122. https://doi.org/10.1046/j.1461-0248.2003.00530.x
Amarasekare, P. (2009). Competition and coexistence in animal communities. In S. A. Levin, S. R. Carpenter, H. C. J. Godfray, A. P. Kinzig, M. Loreau, J. B. Losos, B. Walker, & D. S. Wilcove (Eds.), The Princeton guide to ecology (pp. 196–201). UK: Princeton University Press.
Amarasekare, P., Hoopes, M. F., Mouquet, N., & Holyoak, M. (2004). Mechanisms of coexistence in competitive metacommunities. The American Naturalist, 164, 310–326. https://doi.org/10.1086/422858
Anderson, M. J., & Walsh, D. C. I. (2013). PERMANOVA, ANOSIM, and the Mantel test in the face of heterogeneous dispersions: What null hypothesis are you testing? Ecological Monographs, 83, 557–574. https://doi.org/10.1890/12-2010.1
Arnhem, E., Dupain, J., Drubbel, R. V., Devos, C., & Vercauteren, M. (2008). Selective logging, habitat quality and home range use by sympatric gorillas and chimpanzees: a case study from an active logging concession in Southeast Cameroon. Folia Primatologica, 79, 4473–14. https://doi.org/10.1159/000107664
Basabose, A. K. (2005). Ranging patterns of chimpanzees in a Montane forest of Kahuzi, Democratic Republic of Congo. International Journal of Primatology, 26, 33–54. https://doi.org/10.1007/s10764-005-0722-1
Basabose, A. K., & Yamagiwa, J. (2002). Factors affecting nesting site choice in chimpanzees at Tshibati, Kahuzi-Biega National Park: Influence of sympatric gorillas. International Journal of Primatology, 23, 263–282. https://doi.org/10.1023/A:1013879427335
Benítez-López, A., Viñuela, J., Suárez, F., Hervás, I., & García, J. T. (2014). Niche-habitat mechanisms and biotic interactions explain the coexistence and abundance of congeneric sandgrouse species. Oecologia, 176, 193–206. https://doi.org/10.1007/s00442-014-3010-y
Bermejo, M. (1999). Status and conservation of primates in Odzala National Park, Republic of the Congo. Oryx, 33, 323–331. https://doi.org/10.1046/j.1365-3008.1999.00081.x
Brown, J. S. (1989). Desert rodent community structure: a test of four mechanisms of coexistence. Ecological Monographs, 59, 4473–20. https://doi.org/10.2307/2937289
Calenge, C. (2006). The package “adehabitat” for the R software: A tool for the analysis of space and habitat use by animals. Ecological Modelling, 197, 516–519. https://doi.org/10.1016/j.ecolmodel.2006.03.017
Casanoves, F., Di Rienzo, J. A., Balzarini, M. G., Gonzalez, L., Tablada, M., & Robledo, C. W. (2012). InfoStat. User Manual, Córdoba, Argentina.
Chapman, C. A., Chapman, L. J., & Wrangham, R. W. (1995). Ecological constraints on group size: An analysis of spider monkey and chimpanzee subgroups. Behavioral Ecology and Sociobiology, 36, 59–70. https://doi.org/10.1007/bf00175729
Chapman, C. A., Chapman, L. J., Zanne, A. E., Poulsen, J. R., & Clark, C. J. (2005). A 12-Year Phenological Record of Fruiting: Implications for Frugivore Populations and Indicators of Climate Change. In J. L. Dew, & J. P. Boubli (Eds.), Tropical Fruits and Frugivores: The Search for Strong Interactors (pp. 75–92). Dordrecht Netherlands: Springer. https://doi.org/10.1007/1-4020-3833-x_5
Chapman, C. A., Wrangham, R., & Chapman, L. J. (1994). Indexes of habitat-wide fruit abundance in tropical forests. Biotropica, 26, 160–171. https://doi.org/10.2307/2388805
de Longh, H. H., de Jong, C. B., van Goethem, J., Klop, E., Brunsting, A. M. H., Loth, P. E., & Prins, H. H. T. (2011). Resource partitioning among African savanna herbivores in North Cameroon: The importance of diet composition, food quality and body mass. Journal of Tropical Ecology, 27, 503–513. https://doi.org/10.1017/S0266467411000307
Deblauwe, I. (2009). Temporal variation in insect-eating by Chimpanzees and Gorillas in Southeast Cameroon: Extension of niche differentiation. International Journal of Primatology, 30, 229–252. https://doi.org/10.1007/s10764-009-9337-2
Djoufack, S. D., Nkongmeneck, B. A., Dupain, J., Bekah, S., Bombome, K. K., Epanda, M. A., & Van Elsacker, L. (2007). Manuel d'identification des fruits consommés par les gorilles et les chimpanzés des basses terres de l'Ouest; Espèces de l’écosystème du Dja (Cameroun). Rapport de recherche, PGS.
Doran, D., & Greer, D. (2002). The influence of swamp use and fruit consumption on western gorilla (Gorilla gorilla gorilla) ranging behavior at Mondika Research Center. American Journal of Physical Anthropology, 117, 64–65. https://doi.org/10.1002/ajpa.20011
Doran, D., & Mcneilage, A. (1999). Diet of western lowland gorillas in south-west Central African republic: Implications for subspecific variation in gorilla grouping and ranging patterns. American Journal of Physical Anthropology, 108, 121–121.
Doran, D. M., McNeilage, A., Greer, D., Bocian, C., Mehlman, P., & Shah, N. (2002). Western lowland gorilla diet and resource availability: New evidence, cross-site comparisons, and reflections on indirect sampling methods. American Journal of Primatology, 58, 91–116. https://doi.org/10.1002/ajp.10053
Doran-Sheehy, D. M., Greer, D., Mongo, P., & Schwindt, D. (2004). Impact of ecological and social factors on ranging in western gorillas. American Journal of Primatology, 64, 207–222. https://doi.org/10.1002/ajp.20075
Doran-Sheehy, D., Mongo, P., Lodwick, J., & Conklin-Brittain, N. L. (2008). The role of leaves and herbs as fallback foods in Gorilla gorilla diet at Mondika: An examination of nutrient content and seasonal variation in intake. American Journal of Physical Anthropology, 135, 92–92. https://doi.org/10.1002/ajpa.20806
Doran-Sheehy, D., Mongo, P., Lodwick, J., & Conklin-Brittain, N. L. (2009). Male and female Western Gorilla diet: Preferred foods, use of fallback resources, and implications for ape versus old world monkey foraging strategies. American Journal of Physical Anthropology, 140, 727–738. https://doi.org/10.1002/ajpa.21118
Dupain, J., Guislain, P., Nguenang, G. M., De Vleeschouwer, K., & Van Elsacker, L. (2004). High chimpanzee and gorilla densities in a non-protected area on the northern periphery of the Dja Faunal Reserve, Cameroon. Oryx, 38, 209–216. https://doi.org/10.1017/s0030605304000365
Etiendem, D. N., & Tagg, N. (2013). Feeding ecology of cross river Gorillas (Gorilla gorilla diehli) at Mawambi Hills: The influence of resource seasonality. International Journal of Primatology, 34, 1261–1280. https://doi.org/10.1007/s10764-013-9739-z
Fay, J. M., & Agnagna, M. (1992). Census of gorillas in northern Republic of Congo. American Journal of Primatology, 27, 275–284. https://doi.org/10.1002/ajp.1350270405
Fayolle, A., Swaine, M. D., Bastin, J.-F., Bourland, N., Comiskey, J. A., Dauby, G., … Plumptre, A. J. (2014). Patterns of tree species composition across tropical African forests. Journal of Biogeography, 41, 2320–2331. https://doi.org/10.1111/jbi.12382
Felton, A. M., Felton, A., Raubenheimer, D., Simpson, S. J., Foley, W. J., Wood, J. T., … Lindenmayer, D. B. (2009). Protein content of diets dictates the daily energy intake of a free-ranging primate. Behavioral Ecology, 20, 685–690. https://doi.org/10.1093/beheco/arp021
Furuichi, T., Hashimoto, C., & Tashiro, Y. (2001). Fruit availability and habitat use by chimpanzees in the Kalinzu Forest, Uganda: Examination of fallback foods. International Journal of Primatology, 22, 929–945. https://doi.org/10.1023/A:1012009520350
Gaston, K. J., Blackburn, T. M., & Lawton, J. H. (1997). Interspecific abundance-range size relationships: An appraisal of mechanisms. Journal of Animal Ecology, 66, 579–601. https://doi.org/10.2307/5951
Gregory, R. D., & Gaston, K. J. (2000). Explanations of commonness and rarity in British breeding birds: Separating resource use and resource availability. Oikos, 88, 515–526. https://doi.org/10.1034/j.1600-0706.2000.880307.x
Grether, G. F., Losin, N., Anderson, C. N., & Okamoto, K. (2009). The role of interspecific interference competition in character displacement and the evolution of competitor recognition. Biological Reviews, 84, 617–635. https://doi.org/10.1111/j.1469-185X.2009.00089.x
Harrison, M. E., & Marshall, A. J. (2011). Strategies for the use of Fallback foods in Apes. International Journal of Primatology, 32, 531–565. https://doi.org/10.1007/s10764-010-9487-2
Head, J. S., Boesch, C., Makaga, L., & Robbins, M. M. (2011). Sympatric Chimpanzees (Pan troglodytes troglodytes) and Gorillas (Gorilla gorilla gorilla) in Loango National Park, Gabon: Dietary composition, seasonality, and intersite comparisons. International Journal of Primatology, 32, 755–775. https://doi.org/10.1007/s10764-011-9499-6
Head, J. S., Robbins, M. M., Mundry, R., Makaga, L., & Boesch, C. (2012). Remote video-camera traps measure habitat use and competitive exclusion among sympatric chimpanzee, gorilla and elephant in Loango National Park, Gabon. Journal of Tropical Ecology, 28, 571–583. https://doi.org/10.1017/S0266467412000612
Hill, M. O. (1974). Correspondence analysis: A neglected multivariate method. Applied Statistics, 23, 340–354. https://doi.org/10.2307/2347127
Hutchinson, G. E. (1957). Concluding remarks. Cold Spring Harbor Symposia on Quantitative Biology, 22, 415–427.
Hutchinson, G. E. (1961). The paradox of the plankton. The American Naturalist, 95, 137–145. https://www.jstor.org/stable/2458386.
Kalan, A. K., Madzoké, B., & Rainey, H. J. (2010). A Preliminary report on feeding and nesting behavior of swamp Gorillas in the lac tele community reserve. Mammalia, 74, 439–442. https://doi.org/10.1515/mamm.2010.047
Kamilar, J. M., & Ledogar, J. A. (2011). Species co-occurrence patterns and dietary resource competition in primates. American Journal of Physical Anthropology, 144, 131–139. https://doi.org/10.1002/ajpa.21380
Kinahan, A. A., & Pillay, N. (2008). Does differential exploitation of folivory promote coexistence in an African Savanna Granivorous rodent community? Journal of Mammalogy, 89, 132–137. https://doi.org/10.1644/06-MAMM-A-381.1
Kleynhans, E. J., Jolles, A. E., Bos, M. R. E., & Olff, H. (2011). Resource partitioning along multiple niche dimensions in differently sized African savanna grazers. Oikos, 120, 591–600. https://doi.org/10.1111/j.1600-0706.2010.18712.x
Kotler, B. P., & Brown, J. S. (1988). Environmental heterogeneity and the coexistence of desert rodents. Annual Review of Ecology and Systematics, 19, 281–307. https://doi.org/10.1146/annurev.es.19.110188.001433
Kotler, B. P., & Brown, J. S. (2007). Community Ecology. In D. W. Stephens, J. S. Brown, & R. C. Ydenberg (Eds.), Foraging: Behavior and Ecology (pp. 397–434). Chicago, USA: University of Chicago Press.
Kühl, H., Maisels, F., Ancrenaz, M., & Williamson, E. A. (2008). Best practice guidelines for surveys and monitoring of great ape populations. Gland, Switzerland: IUCN SSC Primate Specialist Group.
Lambert, J. E., & Rothman, J. M. (2015). Fallback foods, optimal diets, and nutritional targets: Primate responses to varying food availability and quality. Annual Review of Anthropology, 44, 493–512. https://doi.org/10.1146/annurev-anthro-102313-025928
Leach, K., Montgomery, W. I., & Reid, N. (2016). Modelling the influence of biotic factors on species distribution patterns. Ecological Modelling, 337, 96–106. https://doi.org/10.1016/j.ecolmodel.2016.06.008
Lehmann, J., & Boesch, C. (2004). To fission or to fusion: Effects of community size on wild chimpanzee (Pan troglodytes verus) social organisation. Behavioral Ecology and Sociobiology, 56, 207–216. https://doi.org/10.1007/s00265-004-0781-x
Lehmann, J., & Dunbar, R. (2009). Implications of body mass and predation for ape social system and biogeographical distribution. Oikos, 118, 379–390. https://doi.org/10.1111/j.1600-0706.2008.16382.x
Lepš, J., & Šmilauer, P. (2003). Multivariate analysis of ecological data using CANOCO. New York, NY: Cambridge University Press.
Manly, B. F. J., McDonald, L. L., Thomas, D. L., McDonald, T. L., & Erickson, W. P. (2002). Resource Selection by Animals: Statistical Design and Analysis for Field Studies. Netherlands: Springer, Kluwer Academic Publishers.
Martin, R. A., & Garnett, S. C. (2013). Relatedness and resource diversity interact to influence the intensity of competition. Biological Journal of the Linnean Society, 110, 689–695. https://doi.org/10.1111/bij.12146
Masi, S., & Breuer, T. (2018). Dialium seed coprophagy in wild western gorillas: Multiple nutritional benefits and toxicity reduction hypotheses. American Journal of Primatology, 80, e22752. https://doi.org/10.1002/ajp.22752
Masi, S., Cipolletta, C., Ortmann, S., Mundry, R., & Robbins, M. M. (2009). Does a More Frugivorous Diet Lead to an Increase in Energy Intake and Energy Expenditure? The Case of the Western Lowland Gorillas at Bai-Hokou, Central African Republic. In F. Scalfari, R. Bigazzi, L. Sineo, & C. Veracini (Eds.), 19th Meeting of the Italian Primatological Association (pp. 372–373). Asti: Folia Primatologica.
Masi, S., Mundry, R., Ortmann, S., Cipolletta, C., Boitani, L., & Robbins, M. M. (2015). The influence of seasonal frugivory on nutrient and energy intake in Wild Western Gorillas. PLoS ONE, 10, e0129254. https://doi.org/10.1371/journal.pone.0129254
Morgan, D., & Sanz, C. M. (2006). Chimpanzee feeding ecology and comparisons with sympatric gorillas in the Goualougo Triangle, Republik of Congo. In G. Hohmann, M. M. Robbins, & C. Boesch (Eds.), Feeding Ecology in Apes and Other Primates: Ecological, Physical, Behavioral aspects (pp. 97–122). New York, USA: Cambridge University Press.
Morgan, D., Sanz, C., Onononga, J. R., & Strindberg, S. (2006). Ape abundance and habitat use in the Goualougo Triangle, Republic of Congo. International Journal of Primatology, 27, 147–179. https://doi.org/10.1007/s10764-005-9013-0
Myers, J. A., & Harms, K. E. (2009). Seed arrival, ecological filters, and plant species richness: A meta-analysis. Ecology Letters, 12, 1250–1260. https://doi.org/10.1111/j.1461-0248.2009.01373.x
Neu, C. W., Byers, C. R., & Peek, J. M. (1974). A technique for analysis of utilization-availability data. Journal of Wildlife Management, 38, 541–545. https://doi.org/10.2307/3800887
Nishihara, T. (1995). Feeding ecology of Western Lowland Gorillas in the Nouabale-Ndoki National-Park, Congo. Primates, 36, 151–168. https://doi.org/10.1007/Bf02381342
Oelze, V. M., Head, J. S., Robbins, M. M., Richards, M., & Boesch, C. (2014). Niche differentiation and dietary seasonality among sympatric gorillas and chimpanzees in Loango National Park (Gabon) revealed by stable isotope analysis. Journal of Human Evolution, 66, 95–106. https://doi.org/10.1016/j.jhevol.2013.10.003
Ogawa, H., Yoshikawa, M., & Idani, G. (2014). Sleeping site selection by savanna chimpanzees in Ugalla, Tanzania. Primates, 55, 269–282. https://doi.org/10.1007/s10329-013-0400-4
Oksanen, J., Blanchet, F. G., Friendly, M., Kindt, R., Legendre, P., McGlinn, D., …Wagner, H. (2018). vegan: Community Ecology Package. R package version 2.5-2. https://CRAN.R-project.org/package=vegan (accessed 25 June 2018).
Owen-Smith, N., Martin, J., & Yoganand, K. (2015). Spatially nested niche partitioning between syntopic grazers at foraging arena scale within overlapping home ranges. Ecosphere, 6, 4473–17. https://doi.org/10.1890/ES14-00487.1
Perrin, M. R., & Kotler, B. P. (2005). A test of five mechanisms of species coexistence between rodents in a southern African savanna. African Zoology, 40, 55–61. https://doi.org/10.1080/15627020.2005.11407309
Petre, C.-A. (2016). Effectiveness of Western Lowland Gorilla (Gorilla Gorilla Gorilla) Seed Dispersal and Plant-Gorilla Mutualism in Southeast Cameroon, Gembloux Agro-Bio Tech. Belgium: Université de Liège.
Pianka, E. R. (1981). Competition and niche theory. In R. M. May (Ed.), Theoretical Ecology Principles and Applications, 2nd ed. (pp. 167–196). Sunderland, MA: Sinauer Associates.
Pla, L., Casanoves, F., & Rienzo, J. D. (2012). Quantifying Functional Biodiversity. New York: Springer.
Potts, K. B., Watts, D. P., & Wrangham, R. W. (2011). Comparative feeding ecology of two communities of Chimpanzees (Pan troglodytes) in Kibale National Park, Uganda. International Journal of Primatology, 32, 669–690. https://doi.org/10.1007/s10764-011-9494-y
Poulsen, J. R., & Clark, C. J. (2004). Densities, distributions, and seasonal movements of gorillas and chimpanzees in swamp forest in Northern Congo. International Journal of Primatology, 25, 285–306. https://doi.org/10.1023/B:IJOP.0000019153.50161.58
Quinn, G. P., & Keough, M. J. (2002). Experimental Design and Data Analysis for Biologists. New York, NY: Cambridge University Press.
R Core Team, (2018). R: A language and environment for statistical computing. https://www.R-project.org/accessed 25 June 2018.
Rainey, H. J., Iyenguet, F. C., Malanda, G. A. F., Madzoke, B., Dos Santos, D., Stokes, E. J., … Strindberg, S. (2010). Survey of Raphia swamp forest, Republic of Congo, indicates high densities of Critically Endangered western lowland gorillas Gorilla gorilla gorilla. Oryx, 44, 124–132. https://doi.org/10.1017/S003060530999010x
Remis, M. J. (1997). Western lowland gorillas (Gorilla gorilla gorilla) as seasonal frugivores: Use of variable resources. American Journal of Primatology, 43, 87–109.
Remis, M. J., Dierenfeld, E. S., Mowry, C. B., & Carroll, R. W. (2001). Nutritional Aspects of Western Lowland Gorilla (Gorilla gorilla gorilla) Diet During Seasons of Fruit Scarcity at Bai Hokou, Central African Republic. International Journal of Primatology, 22, 807–836. https://doi.org/10.1023/a:1012021617737
Ritchie, M. (2002). Competition and coexistence in mobile animals. In U. Sommer, & B. Worm (Eds.), Competition and Coexistence (pp. 109–131). Berlin Heidelberg: Springer-Verlag. https://doi.org/10.1007/978-3-642-56166-5_5
Rogers, M. E., Abernethy, K., Bermejo, M., Cipolletta, C., Doran, D., McFarland, K., … Tutin, C. E. G. (2004). Western gorilla diet: A synthesis from six sites. American Journal of Primatology, 64, 173–192. https://doi.org/10.1002/ajp.20071
Rogers, M. E., Voysey, B. C., McDonald, K. E., Parnell, R. J., & Tutin, C. E. G. (1998). Lowland gorillas and seed dispersal: The importance of nest sites. American Journal of Primatology, 45, 45–68. https://doi.org/10.1002/(SICI)1098-2345(1998)45:1<45:AID-AJP5>3.0.CO;2-W
Rosenzweig, M. L. (1981). A Theory of Habitat Selection. Ecology, 62, 327–335. https://doi.org/10.2307/1936707
Sanz, C., Morgan, D., Strindberg, S., & Onononga, J. R. (2007). Distinguishing between the nests of sympatric chimpanzees and gorillas. Journal of Applied Ecology, 44, 263–272. https://doi.org/10.1111/j.1365-2664.2007.01278.x
Schreier, B. M., Harcourt, A. H., Coppeto, S. A., & Somi, M. F. (2009). Interspecific competition and niche separation in primates: A global analysis. Biotropica, 41, 283–291. https://doi.org/10.1111/j.1744-7429.2008.00486.x
Sinclair, A. R. E., Fryxell, J. M., & Caughley, G. (2006). Wildlife ecology, conservation, and management, 2nd ed. Oxford, UK: Blackwell Publishing Ltd.
Sonké, B., & Couvreur, T. L. P. (2014). Tree diversity of the Dja Faunal Reserve, southeastern Cameroon. Biodiversity Data Journal, 2, e1049. https://doi.org/10.3897/BDJ.2.e1049
Stanford, C. B. (2006). The behavioral ecology of sympatric African apes: Implications for understanding fossil hominoid ecology. Primates, 47, 91–101. https://doi.org/10.1007/s10329-005-0148-6
Stanford, C. B., & Nkurunungi, J. B. (2003). Behavioral ecology of sympatric Chimpanzees and Gorillas in Bwindi Impenetrable National Park, Uganda: Diet. International Journal of Primatology, 24, 901–918. https://doi.org/10.1023/a:1024689008159
Steinmetz, R., Garshelis, D. L., Chutipong, W., & Seuaturien, N. (2013). Foraging ecology and coexistence of Asiatic black bears and sun bears in a seasonal tropical forest in Southeast Asia. Journal of Mammalogy, 94, 4473–18. https://doi.org/10.1644/11-MAMM-A-351.1
Sushma, H. S., & Singh, M. (2006). Resource partitioning and interspecific interactions among sympatric rain forest arboreal mammals of the Western Ghats, India. Behavioral Ecology, 17, 479–490. https://doi.org/10.1093/beheco/arj058
Sutherland, W. J., Freckleton, R. P., Godfray, H. C. J., Beissinger, S. R., Benton, T., Cameron, D. D., … Wiegand, T. (2013). Identification of 100 fundamental ecological questions. Journal of Ecology, 101, 58–67. https://doi.org/10.1111/1365-2745.12025
Syms, C. (2008). Ordination. In S. E. Jørgensen, & B. D. Fath (Ed.), Encyclopedia of Ecology (pp. 2572–2581). Oxford: Academic Press. https://doi.org/10.1016/B978-008045405-4.00524-3
Tagg, N., & Willie, J. (2013). The influence of transect use by local people and reuse of transects for repeated surveys on nesting in Western Lowland Gorillas (Gorilla gorilla gorilla) and Central Chimpanzees (Pan troglodytes troglodytes) in Southeast Cameroon. International Journal of Primatology, 34, 554–570. https://doi.org/10.1007/s10764-013-9681-0
Tagg, N., Willie, J., Petre, C. A., & Haggis, O. (2013). Ground night nesting in Chimpanzees: New insights from Central Chimpanzees (Pan troglodytes troglodytes) in South-East Cameroon. Folia Primatologica, 84, 362–383. https://doi.org/10.1159/000353172
Takenoshita, Y., Ando, C., Iwata, Y., & Yamagiwa, J. (2008). Fruit phenology of the great ape habitat in the Moukalaba-Doudou National Park, Gabon. African Study Monographs, 39, 23–39. https://doi.org/10.14989/66240
Tédonzong, L. R. D., Willie, J., Keuko, A. M. P., Kuenbou, J. K., Njotah, G., Tchamba, M. N., … Lens, L. (2018). Using abundance and habitat variables to identify high conservation value areas for threatened mammals. Biodiversity and Conservation, 27, 1115–1137. https://doi.org/10.1007/s10531-017-1483-9
Tédonzong, L. R. D., Willie, J., Tagg, N., Tchamba, M. N., Angwafo, T. E., Keuko, A. M. P., …Lens, L. (2019). Data from: The distribution of plant consumption traits across habitat types and the patterns of fruit availability suggest a mechanism of coexistence of two sympatric frugivorous mammals. Dryad Digital Repository, https://doi.org/10.5061/dryad.ms65f29
Thomas, D. L., & Taylor, E. J. (2006). Study designs and tests for comparing resource use and availability II. Journal of Wildlife Management, 70, 324–336. https://doi.org/10.2193/0022-541x(2006)70[324:Sdatfc]2.0.Co;2
Tutin, C. E. G., & Fernandez, M. (1993). Composition of the diet of Chimpanzees and comparisons with that of sympatric Lowland Gorillas in the Lope Reserve, Gabon. American Journal of Primatology, 30, 195–211. https://doi.org/10.1002/ajp.1350300305
Tutin, C. E. G., Fernandez, M., Rogers, M. E., Williamson, E. A., & Mcgrew, W. C. (1991). Foraging profiles of sympatric Lowland Gorillas and Chimpanzees in the Lope Reserve, Gabon. Philos T Roy Soc B, 334, 179–186. https://doi.org/10.1098/rstb.1991.0107
Tutin, C. E. G., Ham, R. M., White, L. J. T., & Harrison, M. J. S. (1997). The primate community of the Lopé reserve, Gabon: Diets, responses to fruit scarcity, and effects on biomass. American Journal of Primatology, 42, 4473–24. https://doi.org/10.1002/(SICI)1098-2345(1997)42:1<1:AID-AJP1>3.0.CO;2-0
Tweheyo, M., & Lye, K. A. (2003). Phenology of figs in Budongo Forest Uganda and its importance for the chimpanzee diet. African Journal of Ecology, 41, 306–316. https://doi.org/10.1111/j.1365-2028.2003.00475.x
Tweheyo, M., & Lye, K. A. (2005). Patterns of frugivory of the Budongo forest chimpanzees, Uganda. African Journal of Ecology, 43, 282–290. https://doi.org/10.1111/j.1365-2028.2005.00566.x
Vélez, J., Espelta, J. M., Rivera, O., & Armenteras, D. (2017). Effects of seasonality and habitat on the browsing and frugivory preferences of Tapirus terrestris in north-western Amazonia. Journal of Tropical Ecology, 33, 395–406. https://doi.org/10.1017/S0266467417000359
Vleut, I., Galindo-González, J., de Boer, W. F., Levy-Tacher, S. I., & Vazquez, L. B. (2015). Niche Differentiation and its Relationship with Food Abundance and Vegetation Complexity in Four Frugivorous Bat Species in Southern Mexico. Biotropica, 47, 606–615. https://doi.org/10.1111/btp.12238
Walter, G. H. (1991). What is resource partitioning? Journal of Theoretical Biology, 150, 137–143. https://doi.org/10.1016/S0022-5193(05)80327-3
White, L., & Edwards, A. (2000). Conservation Research in the African Rain Forests: A Technical Handbook. New York: Wildlife Conservation Society.
Williamson, E. A., Tutin, C. E. G., Rogers, M. E., & Fernandez, M. (1990). Composition of the diet of Lowland Gorillas at Lope in Gabon. American Journal of Primatology, 21, 265–277. https://doi.org/10.1002/ajp.1350210403
Willie, J., Petre, C. A., Tagg, N., & Lens, L. (2013). Density of herbaceous plants and distribution of western gorillas in different habitat types in south-east Cameroon. African Journal of Ecology, 51, 111–121. https://doi.org/10.1111/aje.12014
Willie, J., Tagg, N., Petre, C. A., Pereboom, Z., & Lens, L. (2014). Plant selection for nest building by western lowland gorillas in Cameroon. Primates, 55, 41–49. https://doi.org/10.1007/s10329-013-0363-5
Yamagiwa, J., & Basabose, A. K. (2009). Fallback foods and dietary partitioning among pan and Gorilla. American Journal of Physical Anthropology, 140, 739–750. https://doi.org/10.1002/ajpa.21102
Yamagiwa, J., Basabose, A. K., Kaleme, K. P., & Yumoto, T. (2008). Phenology of fruits consumed by a sympatric population of Gorillas and Chimpanzees in Kahuzi-Biega National Park, Democratic Republic of Congo. African Study Monographs, 39, 3–4494. https://doi.org/10.14989/66241.
Yamagiwa, J., Maruhashi, T., Yumoto, T., & Mwanza, N. (1996). Dietary and ranging overlap in sympatric gorillas and chimpanzees in Kahuzi-Biega National Park, Zaire. In W. C. McGrew, L. F. Marchant, & T. Nishida (Eds.), Great ape societies (pp. 82–98). Cambridge: Cambridge University Press.