High altitude diets: Implications for the feeding and nutritional ecology of mountain gorillas

High Altitude Primates

Volumn , Issue , 2014, Pages 247-264

  Rothman, Jessica M ^a   Nkurunungi, John Bosco ^b   Shannon, Bianca F ^a   Bryer, Margaret A H ^a  

^a CITY UNIVERSITY OF NEW YORK   (United States)

^b MBARARA UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Uganda)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 85007335001     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1007/978-1-4614-8175-1_14     Document Type: Chapter

References (89)

1. Aiba, S., & Kitayama, K. (1999). Structure, composition and species diversity in an altitudesubstrate matrix of rain forest tree communities on Mount Kinabalu, Borneo. Plant Ecology, 140, 139-157.
2. Barton, R. A., Whiten, A., Byrne, R. W., & English, M. (1993). Chemical composition of baboon plant foods: implications for the interpretation of intraspecific and interspecific differences in diet. Folia Primatologica, 61, 1-20.
3. Basabose, A. K. (2002). Diet composition of chimpanzees inhabiting the montane forest of Kahuzi, Democratic Republic of Congo. American Journal of Primatology, 58, 1-21.
4. Blanco, M. B., & Rahalinarivo, V. (2010). First direct evidence of hibernation in an eastern dwarf lemur species (Cheirogaleus crossleyi) from the high-altitude forest of Tsinjoarivo, centraleastern Madagascar. Naturwissenschaften, 97, 945-950.
5. Bruijnzeel, L. A., & Veneklaas, E. J. (1998). Climatic conditions and tropical montane forests. Ecology, 79, 3-9.
6. Butynski, T. M., & Kalina, J. (1993). Three new mountain national parks for Uganda. Oryx, 27, 214-224.
7. Byrne, R. W., Whiten, A., Henzi, S. P., & McCulloch, F. M. (1993). Nutritional constraints on mountain baboons (Papio ursinus): Implications for baboon socioecology. Behavioral Ecology and Sociobiology, 33, 233-246.
8. Calvert, J. J. (1985). Food selection by western gorillas (Gorilla gorilla gorilla) in relation to food chemistry. Oecologia, 65, 236-246.
9. Carlson, B. A., Rothman, J. M., & Mitani, J. C. (2013). Diurnal variation in nutrients and chimpanzee foraging behavior. American Journal of Primatology, 75, 342-349.
10. Casimir, M. J. (1975). Feeding ecology and nutrition of an eastern gorilla group in Mt. Kahuzi region (Republique du Zaire). Folia Primatologica, 24, 81-136.
11. Chapman, C. A., Chapman, L. J., Rode, K. D., Hauck, E. M., & McDowell, L. R. (2003). Variation in the nutritional value of primate foods: among trees, time periods, and areas. International Journal of Primatology, 24, 317-333.
12. Conklin-Brittain, N. L., Wrangham, R. W., & Hunt, K. (1998). Dietary response of chimpanzees and cercopithecines to seasonal variation in fruit abundance II Macronutrients. International Journal of Primatology, 19, 971-997.
13. Danish, L., Chapman, C. A., Hall, M. B., Rode, K. D., & Worman, C. (2006). The role of sugar in diet selection in redtail and red colobus monkeys. In G. Hohmann, M. M. Robbins, & C. Boesch (Eds.), Feeding ecology in apes and other primates: Ecological, physical, and behavioural aspects (pp. 471-487). Cambridge: Cambridge University Press.
14. Dearing, M. D., Mangione, A. M., & Karasov, W. H. (2000). Diet breadth of mammalian herbivores: Nutrient verses detoxification constraints. Oecologia, 123, 397-405.
15. Doran, D. M., & McNeilage, A. (1998). Gorilla ecology and behavior. Evolutionary Anthropology, 6, 120-131.
16. Doran, D. M., 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 verses old world monkey foraging strategies. American Journal of Physical Anthropology, 140, 727-238.
17. Dunbar, R. (1992). A model of the gelada socio-ecological system. Primates, 33, 69-83.
18. Dunbar, R. (1998). Impact of global warming on the distribution and survival of the gelada baboon: A modelling approach. Global Change Biology, 4, 293-304.
19. Fimbel, C., Vedder, A., Dierenfeld, E., & Mulindahabi, F. (2001). An ecological basis for large group size in Colobus angolensis in the Nyungwe Forest, Rwanda. African Journal of Ecology, 39, 83-92.
20. Friend, A., Woodward, F., & Switsur, V. (1989). Field measurements of photosynthesis, stomatal conductance, leaf nitrogen and d 13 C along altitudinal gradients in Scotland. Functional Ecology, 3, 117-122.
21. Ganas, J., Robbins, M. M., Nkurunungi, J. B., Kaplin, B. A., & McNeilage, A. (2004). Dietary variability of mountain gorillas in Bwindi Impenetrable National Park, Uganda. International Journal of Primatology, 25, 1043-1072.
22. Ganas, J., Ortmann, S., & Robbins, M. M. (2008). Food preferences of wild mountain gorillas. American Journal of Primatology, 70, 927-938.
23. Ganzhorn, J. U. (1995). Low level forest disturbance effects on primary production, leaf chemistry, and lemur populations. Ecology, 76, 2084-2096.
24. Ganzhorn, J. U., & Wright, P. C. (1994). Temporal patterns in primate leaf eating: The possible role of leaf chemistry. Folia Primatologica, 63, 203-208.
25. Goldsmith, M.L., Taylor, A.B., & Goldsmith, M.L. (2003) Comparative behavioral ecology of a lowland and highland gorilla population: Where do Bwindi gorillas fit?, Gorilla biology: a multidisciplinary perspective (pp. 358-384). Cambridge: Cambridge University Press.
26. Goodall, A. G. (1977). Feeding and ranging behaviour of a mountain gorilla group (Gorilla gorilla beringei) in the Tshibinda-Kahuzi region (Zaire). In T. Clutton Brock (Ed.), Primate Ecology: Studies of Feeding and Ranging Behaviour in Lemurs, Monkeys and Apes (pp. 450-479). London: Academic Press.
27. Guo, X. S., Ding, L. M., Long, R. J., Qi, B., Shang, Z. H., Wang, Y. P., et al. (2012). Changes of chemical composition to high altitude results in Kobresia littledalei growing in alpine meadows with high feeding values for herbivores. Animal Feed Science Technology, 173, 186-193.
28. Hanya, G., Noma, N., & Agetsuma, N. (2003). Altitudinal and seasonal variations in the diet of Japanese macaques in Yakushima. Primates 44, 51-59.
29. Hamilton, A. (1975). A quantitative analysis of altitudinal zonation in Uganda forests. Plant Ecology, 30, 99-106.
30. Hikosaka, K., Nagamatsu, D., Ishii, H. S., & Hirose, T. (2002). Photosynthesis-nitrogen relationships in species at different altitudes on Mount Kinabalu, Malaysia. Ecological Research, 17, 305-313.
31. Hodkinson, I. D. (2005). Terrestrial insects along elevation gradients: Species and community responses to altitude. Biological Reviews, 80, 489-513.
32. Iwamoto, T., & Dunbar, R. (1983). Thermoregulation, habitat quality and the behavioural ecology of gelada baboons. The Journal of Animal Ecology, 53, 357-366.
33. Kirkpatrick, R. C., & Grueter, C. C. (2010). Snub-nosed monkeys: Multilevel societies across varied environments. Evolutionary Anthropology: Issues, News, and Reviews, 19, 98-113.
34. Kitayama, K., & Aiba, S.-I. (2002). Ecosystem structure and productivity of tropical rain forests along altitudinal gradients with contrasting soil phosphorus pools on Mount Kinabalu, Borneo. Journal of Ecology, 90, 37-51.
35. Körner, C. (1989). The nutritional status of plants from high altitudes. Oecologia, 81, 379-391.
36. Mau, M., Südekum, K. H., Johann, A., Sliwa, A., & Kaiser, T. M. (2009). Saliva of the graminivorous Theropithecus gelada lacks proline-rich proteins and tannin-binding capacity. American Journal of Primatology, 71, 663-669.
37. Mehlman, P. (1988). Food resources of the wild Barbary macaque (Macaca sylvanus) in highaltitude fir forest, Ghomaran Rif, Morocco. Journal of Zoology, 214, 469-490.
38. McNeilage, A., Robbins, M. M., Sicotte, P., & Stewart, K. J. (2001). Diet and habitat use of two mountain gorilla groups in contrasting habitats in the Virungas, Mountain gorillas: three decades of research at Karisoke (pp. 263-292). Cambridge: Cambridge University Press.
39. Ménard, N. (2002). Ecological plasticity of Barbary macaques (Macaca sylvanus). Evolutionary Anthropology: Issues, News, and Reviews, 11(S1), 95-100.
40. Mendiratta, U., Kumar, A., Mishra, C., & Sinha, A. (2009). Winter ecology of the Arunachal macaque Macaca munzala in Pangchen Valley, western Arunachal Pradesh, northeastern India. American Journal of Primatology, 71, 939-947.
41. Mertl-Millhollen, A. S., Moret, E. S., Felantosoa, D., Rasamimanana, H., Blumenfeld-Jones, K. C., & Jolly, A. (2003). Ring- tailed lemur home ranges correlate with food abundance and nutritional content at a time of environmental stress. International Journal of Primatology, 24, 965-985.
42. Milton, K. (1999). Nutritional characteristics of wild primate foods: Do the diets of our closest living relatives have lessons for us? Nutrition, 15, 488-498.
43. Oates JF, Sunderland-Groves J, Bergl R, Dunn A, Nicholas A, Takang E, Omeni F, Imong I, Fotso R, Nkembi L & Williamson EA (2007) Regional Action Plan for the Conservation of the Cross River Gorilla (Gorilla gorilla diehli). IUCN/SSC Primate Specialist Group and Conservation International. Arlington, VA, 36 pp.
44. Oftedal, O. T. (1992). The nutritional consequences of foraging in primates: The relationship of nutrient intakes to nutrient requirements. Philosophical Transactions of the Royal Society B, 334, 161-170.
45. Pellissier, L., Fiedler, K., Ndribe, C., Dubuis, A., Pradervand, J.-N., Guisan, A., et al. (2012). Shifts in species richness, herbivore specialization, and plant resistance along elevation gradients. Ecology and Evolution, 2, 1818-1825.
46. Popovich, D. G., Jenkins, D. J. A., Kendall, C. W. C., Dierenfeld, E. S., Carroll, R. W., Tariq, N., et al. (1997). The western lowland gorilla diet has implications for the health of humans and other hominoids. Journal of Nutrition, 127, 2000-2005.
47. Proctor, J., Edwards, I., Payton, R., & Nagy, L. (2007). Zonation of forest vegetation and soils of Mount Cameroon, West Africa. Plant Ecology, 192, 251-269.
48. Rahbek, C. (1995). The elevational gradient of species richness: a uniform pattern? Ecography, 18, 200-205.
49. Remis, M. J. (1997). Western lowland gorillas (Gorilla gorilla gorilla) as seasonal frugivores: Use of variable resources. American Journal of Primatology, 43, 87-109.
50. Remis, M. J. (2000). Initial studies on the contributions of body size and gastrointestinal passage rates to dietary flexibility among gorillas. American Journal of Physical Anthropology, 112, 171-180.
51. Remis, M. J., & Kerr, M. E. (2002). Taste responses to fructose and tannic acid among gorillas (Gorilla gorilla gorilla). International Journal of Primatology, 23, 251-261.
52. 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.
53. Remis, M. J., Taylor, A. B., & Goldsmith, M. L. (2003). Are gorillas vacuum cleaners of the forest floor? The roles of body size, habitat, and food preferences on dietary flexibility and nutrition, Gorilla Biology: A multidisciplinary perspective (pp. 385-404). Cambridge:Cambridge University Press.
54. Richardson, A. D. (2004). Foliar chemistry of balsam fir and red spruce in relation to elevation and the canopy light gradient in the mountains of northeastern United States. Plant and Soil, 260, 291-299.
55. Robbins, M. M., & McNeilage, A. (2003). Home range and frugivory patterns of mountain gorillas in Bwindi Impenetrable National Park, Uganda. International Journal of Primatology, 24, 467-491.
56. Robbins, M. M., Nkurunungi, J. B., & McNeilage, A. (2006). Variability of the feding ecology of eastern gorillas. In G. Hohmann, M. M. Robbins, & C. Boesch (Eds.), Feeding ecology in apes and other primates (pp. 25-48). Cambridge, U.K.,: Cambridge University Press.
57. Rogers, M. E., & Williamson, E. A. (1987). Density of herbaceous plants eaten by gorillas in Gabon- some preliminary data. Biotropica, 19, 278-281.
58. Rogers, M. E., Maisels, F., Williamson, E. A., Fernandez, M., & Tutin, C. E. G. (1990). Gorilla diet in the Lope Reserve, Gabon- A nutritional analysis. Oecologia, 84, 326-339.
59. Rogers, M. E., Abernethy, K., Bermejo, M., Cipolletta, C., Doran, D., McFarland, K., et al. (2004). Western gorilla diet: A synthesis from six sites. American Journal of Primatology, 64, 173-192.
60. Rothman, J. M., Dierenfeld, E. S., Molina, D. O., Shaw, A. V., Hintz, H. F., & Pell, A. N. (2006a). Nutritional chemistry of foods eaten by gorillas in Bwindi Impenetrable National Park, Uganda. American Journal of Primatology, 68, 675-691.
61. Rothman, J. M., Pell, A. N., Nkurunungi, J. B., Dierenfeld, E. S., Newton-Fisher, N. E., Notman, H., et al. (2006b). Nutritional aspects of the diet of wild gorillas: How do Bwindi gorillas compare? Primates of Western Uganda. New York: Kluwer Academic.
62. Rothman, J. M., Van Soest, P. J., & Pell, A. N. (2006c). Decaying wood is a sodium source for mountain gorillas. Biology Letters, 2, 321-324.
63. Rothman, J. M., Plumptre, A. J., Dierenfeld, E. S., & Pell, A. N. (2007). Nutritional composition of the diet of the gorilla (Gorilla beringei): A comparison between two mountain habitats. Journal of Tropical Ecology, 23, 673-682.
64. Rothman, J. M., Chapman, C. A., & Pell, A. N. (2008a). Fiber-bound protein in gorilla diets:implications for estimating the intake of dietary protein by primates. American Journal of Primatology, 70, 690-694.
65. Rothman, J. M., Dierenfeld, E. S., Hintz, H. F., & Pell, A. N. (2008b). Nutritional quality of gorilla diets: Consequences of age, sex and season. Oecologia, 155, 111-122.
66. Rothman, J. M., Chapman, C. A., Hansen, J. L., Cherney, D. J., & Pell, A. N. (2009). Rapid assessment of the nutritional value of foods eaten by mountain gorillas: Applying nearinfrared reflectance spectroscopy to primatology. International Journal of Primatology, 30, 729-742.
67. Rothman, J. M., Raubenheimer, D., & Chapman, C. A. (2011). Nutritional geometry: Gorillas prioritize non-protein energy while consuming surplus protein. Biology Letters, 7, 847-849.
68. Rothman, J. M., Chapman, C. A., & Van Soest, P. J. (2012). Methods in primate nutritional ecology: A user's guide. International Journal of Primatology, 33, 542-566.
69. Ryan, A. M., Chapman, C. A., & Rothman, J. M. (2013). How do differences in species and part consumption affect diet nutrient concentrations? A test with red colobus monkeys in Kibale National Park, Uganda. African Journal of Ecology, 51, 1-10.
70. Schmid, J., & Ganzhorn, J. (2009). Optional strategies for reduced metabolism in gray mouse lemurs. Naturwissenschaften, 96, 737-741.
71. Schmitt, C. B., Denich, M., Demissew, S., Friis, I., & Boehmer, H. J. (2010). Floristic diversity in fragmented Afromontane rainforests: Altitudinal variation and conservation importance. Applied Vegetation Science, 13, 291-304.
72. Sharma, C. M., Suyal, S., Gairola, S., & Ghildiyal, S. K. (2009). Species richness and diversity along an altitudinal gradient in moist temperate forest of Garhwal Himalaya. Journal of American Science, 5, 119-128.
73. 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.
74. Tanner, E. V. J., Vitousek, P. M., & Cuevas, E. (1998). Experimental investigation of the nutrient limitation of forest growth on wet tropical mountains. Ecology, 79, 10-22.
75. Tchouto, M., De Boer, W., De Wilde, J., & Van der Maesen, L. (2006). Diversity patterns in the flora of the Campo-Ma'an rain forest, Cameroon: Do tree species tell it all? Forest diversity and management (pp. 293-314). Netherlands: Springer.
76. Twinomugisha, D., Chapman, C. A., Lawes, M., Worman, C. O., Danish, L. M., Newton-Fisher, N. E., et al. (2006). How does the golden monkey of the Virungas cope in a fruit scarce environment? Primates of Western Uganda. New York: Kluwer Academic.
77. Vázquez, J. A., & Givnish, T. J. (1998). Altitudinal gradients in tropical forest composition, structure, and diversity in the Sierra de Manantlán. Journal of Ecology, 86, 999-1020.
78. Waterman, P. G., Choo, G. M., Vedder, A. L., & Watts, D. (1983). Digestibility, digestion inhibitors and nutrients of herbaceous foliage and green stems from an African montane flora and comparison with other tropical flora. Oecologia, 60, 244-249.
79. Watts, D. P. (1984). Composition and variability of mountain gorilla diets in the central Virungas. American Journal of Primatology, 7, 323-356.
80. Watts, D. P. (1998). Seasonality in the ecology and life histories of mountain gorillas (Gorilla gorilla beringei). International Journal of Primatology, 19, 929-948.
81. Whiten, A., Byrne, R., & Henzi, S. (1987). The behavioral ecology of mountain baboons. International Journal of Primatology, 8, 367-388.
82. Worman, C. O., & Chapman, C. A. (2005). Seasonal variation in the quality of tropical ripe fruit and the response of three frugivores. Journal of Tropical Ecology, 21, 689-697.
83. Reiner, W.B., Petzinger, C., Power, M.L., Rothman, J.M., in review. Fatty acids in mountain gorilla diets: Implications for primate nutrition and health. American Journal of Primatology.
84. Xiang, Z., Huo, S., Xiao, W., Quan, R., & Grueter, C. C. (2007). Diet and feeding behavior of Rhinopithecus bieti at Xiaochangdu, Tibet: Adaptations to a marginal environment. American Journal of Primatology, 69, 1141-1158
85. Xiang, Z., Liang, W. B., Nie, S. G., & Li, M. (2012). Diet and feeding behavior of Rhinopithecus brelichi at Yangaoping, Guizhou. American Journal of Primatology, 74, 551-560.
86. Yamagiwa, J., & Mwanza, N. (1994). Day-journey length and daily diet of solitary male gorillas in lowland and highland habitats. International Journal of Primatology, 15(2), 207-224.
87. Yamagiwa, J., Kahekwa, J., & Basabose, A. K. (2003). Intra-specific variation in social organization of gorillas: Implications for their social evolution. Primates, 44, 359-369.
88. Yiming, L. (2006). Seasonal variation of diet and food availability in a group of Sichuan snubnosed monkeys in Shennongjia Nature Reserve, China. American Journal of Primatology, 68, 217-233.
89. Zhuang, L., Tian, Z., Chen, Y., Li, W., Li, J., & Lu, S. (2012). Community characteristics of wild fruit forests along elevation gradients and the relationships between the wild fruit forests and environments in the Keguqin Mountain region of Iii. Journal of Mountain Science, 9, 115-126.