Responses of Primates and Other Frugivorous Vertebrates to Plant Resource Variability over Space and Time at Gunung Palung National Park

International Journal of Primatology

Volumn 35, Issue 6, 2014, Pages 1178-1201

  Marshall, Andrew J ^a   Beaudrot, Lydia ^a   Wittmer, Heiko U ^b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b VICTORIA UNIVERSITY OF WELLINGTON   (New Zealand)

Author keywords

Frugivory; Habitat use; Hierarchical modeling; Ordination; Phenology; Primate population density; Vertebrate community ecology

Indexed keywords

COMMUNITY ECOLOGY; FRUGIVORY; HABITAT TYPE; NATIONAL PARK; PHENOLOGY; POPULATION DENSITY; PRIMATE; RESOURCE AVAILABILITY; SPATIOTEMPORAL ANALYSIS;

GUNUNG PALUNG NATIONAL PARK; INDONESIA; WEST KALIMANTAN;

PRIMATES; VERTEBRATA;

EID: 84914682698     PISSN: 01640291     EISSN: 15738604     Source Type: Journal    
DOI: 10.1007/s10764-014-9774-4     Document Type: Article

References (76)

1. Angiosperm Phylogeny Group. (2003). An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG II. Botanical Journal of the Linnean Society, 141, 399–436.
2. Ashton, P. S., Givnish, T. J., & Appanah, S. (1988). Staggered flowering in the Dipterocarpaceae: New insights into floral induction and the evolution of mast fruiting in the aseasonal tropics. American Naturalist, 132, 44–66.
3. Beaudrot, L., & Marshall, A. J. (2011). Primate communities are structured more by dispersal limitation than by niches. Journal of Animal Ecology, 80, 332–341.
4. Beaudrot, L., Struebig, M. J., Meijaard, E., van Balen, S., Husson, S., & Marshall, A. J. (2013a). Co-occurrence patterns of Bornean vertebrates suggest competitive exclusion is strongest among distantly related species. Oecologia, 173, 1053–1062.
5. Beaudrot, L., Struebig, M. J., Meijaard, E., van Balen, S., Husson, S., Young, C. F., & Marshall, A. J. (2013b). Interspecific interactions between primates, birds, bats, and squirrels may affect community composition on Borneo. American Journal of Primatology, 75, 170–185.
6. Blundell, A. G. (1996). A preliminary checklist of mammals at Cabang Panti Research Station, Gunung Palung National Park, West Kalimantan. Tropical Biodiversity, 3, 251–259.
7. Buckland, S. T., Anderson, D. R., Burnham, K. P., & Laake, J. L. (1993). Distance sampling: Estimating abundance of biological populations. London: Chapman & Hall.
8. Buij, R., Wich, S. A., Lubis, A. H., & Sterck, E. H. M. (2002). Seasonal movements in the Sumatran orangutan (Pongo pygmaeus abelii) and consequences for conservation. Biological Conservation, 107, 83–87.
9. Burnham, K. P., & Anderson, D. R. (2002). Model selection and multimodal inference: A practical information-theoretic approach. New York: Springer-Verlag.
10. Caldecott, J. O. (1980). Habitat quality and populations of two sympatric gibbons (Hylobatidae) on a mountain in Malaya. Folia Primatologica, 33, 291–309.
11. Cannon, C. H., Curran, L. M., Marshall, A. J., & Leighton, M. (2007a). Beyond mast-fruiting events: Community asynchrony and individual dormancy dominate woody plant reproductive behavior across seven Bornean forest types. Current Science, 93, 1558–1566.
12. Cannon, C. H., Curran, L. M., Marshall, A. J., & Leighton, M. (2007b). Long-term reproductive behavior of woody plants across seven Bornean forest types in the Gunung Palung National Park (Indonesia): Suprannual synchrony, temporal productivity, and fruiting diversity diversity. Ecology Letters, 10, 956–969.
13. Cannon, C. H., & Leighton, M. (1994). Comparative locomotory ecology of gibbons and macaques: Selection of canopy elements for crossing gaps. American Journal of Physical Anthropology, 93, 505–524.
14. Cannon, C. H., & Leighton, M. (2004). Tree species distributions across five habitats in a Bornean rain forest. Journal of Vegitation Science, 15, 257–266.
15. Chapman, C. A., Chapman, L. J., Bjorndal, K. A., & Onderdonk, D. A. (2002). Application of protein-to-fiber ratios to predict colobine abundance on different spatial scales. International Journal of Primatology, 23, 283–310.
16. Chapman, C. A., & Onderdonk, D. A. (1998). Forests without primates: Primate/plant codependency. American Journal of Primatology, 45, 127–141.
17. Chapman, C. A., Struhsaker, T. T., Skorupa, J. P., Snaith, T. V., & Rothman, J. M. (2010). Understanding long-term primate community dynamics: implications of forest change. Ecological Applications, 20, 179–191.
18. Cheyne, S. M., Thompson, C. J. H., & Chivers, D. J. (2013). Travel adaptations of Bornean agile gibbons Hylobates albibarbis (Primates: Hylobatidae) in a degraded secondary forest, Indonesia. Journal of Threatened Taxa, 5, 3963–3968.
19. Curran, L. M., & Leighton, M. (2000). Vertebrate responses to spatiotemporal variation in seed production of mast-fruiting Dipterocarpaceae. Ecological Monographs, 70, 101–128.
20. Curran, L. M., Trigg, S. N., McDonald, A. K., Astiani, D., Hardiono, Y. M., Siregar, P., et al (2004). Lowland forest loss in protected areas of Indonesian Borneo. Science, 303, 1000–1003.
21. Curran, L. M., & Webb, C. O. (2000). Experimental tests of the spatiotemporal scale of seed predation in mast-fruiting Dipterocarpaceae. Ecological Monographs, 70, 129–148.
22. Dennis, R. A., & Colfer, C. P. (2006). Impacts of land use and fire on the loss and degradation of lowland forest in 1983–2000 in East Kutai District, East Kalimantan, Indonesia. Singapore Journal of Tropical Geography, 27, 30–48.
23. Diamond, J. (1973). Distributional ecology of New Guinea birds. Science, 179, 759–769.
24. Fiske, I., & Chandler, R. B. (2011). Unmarked: An R package for fitting hierarchical models of wildlife occurrence and abundance. Journal of Statistical Software, 43, 1–23.
25. Fleagle, J., & Reed, K. (1996). Comparing primate communities: A multivariate approach. Journal of Human Evolution, 30, 489–510.
26. Fleagle, J. J., Janson, C., & Reed, K. E. (1999). Primate communities. Cambridge: Cambridge University Press.
27. French, A. R., & Smith, T. B. (2005). Importance of body size in determining dominance hierarchies among diverse tropical frugivores. Biotropica, 37, 96–101.
28. Fuller, D. O., Jessup, T. C., & Salim, A. (2004). Loss of forest over in Kalimantan, Indonesia, since the 1997–1998 El Niño. Conservation Biology, 18, 249–254.
29. Ganzhorn, J. U. (1999). Body mass, competition and the structure of primate communities. In J. J. Fleagle, C. Janson, & K. E. Reed (Eds.), Primate communities (pp. 141–157). Cambridge, U.K.: Cambridge University Press.
30. Gause, G. F. (1934). The struggle for existence. Baltimore: Williams & Wilkins.
31. Gautier-Hion, A., Duplantier, J. M., Quris, R., Feer, F., Sourd, C., Decoux, J. P., et al. (1985). Fruit characters as a basis of fruit choice and seed dispersal in a tropical forest vertebrate community. Oecologia, 65, 324–337.
32. Hamard, M., Cheyne, S. M., & Nijman, V. (2010). Vegetation correlates of gibbon density in the peat-swamp forest of the Sabangau catchment, Central Kalimantan, Indonesia. American Journal of Primatology, 72, 607–616.
33. Harrison, M. E., & Marshall, A. J. (2011). Strategies for the use of fallback foods in apes. International Journal of Primatology, 32, 531–565.
34. Haugaasen, T., & Peres, C. A. (2005). Primate assemblage structure in Amazonian flooded and unflooded forests. American Journal of Primatology, 67, 243–258.
35. Haugaasen, T., & Peres, C. A. (2007). Vertebrate responses to fruit production in Amazonian flooded and unflooded forests. Biodiversity and Conservation, 16, 4165–4190.
36. Hemingway, C. A., & Bynum, N. (2005). The influence of seasonality on primate diet and ranging. In D. K. Brockman & C. P. van Schaik (Eds.), Seasonality in primates: Studies of living and extinct human and non-human primates (pp. 57–104). Cambridge, U.K.: Cambridge University Press.
37. Houle, A., Chapman, C. A., & Vickery, W. L. (2010). Intratree vertical variation of fruit density and the nature of contest competition in frugivores. Behavioral Ecology and Sociobiology, 64, 429–441.
38. Hubbell, S. P. (2001). The unified nuetral theory of biodiversity and biogeography. Princeton, NJ: Princeton University Press.
39. Hutchinson, G. E. (1957). Concluding remarks. Population studies: Animal ecology and demography. Cold Spring Harbor Symposia on Quantitave Biology, 22, 415–427.
40. Kamilar, J. M. (2009). Environmental and geographic correlates of the taxonomic structure of primate communities. American Journal of Physical Anthropology, 139, 382–393.
41. Kamilar, J. M., & Beaudrot, L. (2013). Understanding primate communities: Recent developments and future directions. Evolutionary Anthropology, 22, 174–185.
42. 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.
43. Kappeler, M. (1984). The gibbon in Java. In H. Preuschoft, D. J. Chivers, W. Y. Brockelman, & N. Creel (Eds.), The lesser apes: Evolutionary and behavioural biology (pp. 19–31). Edinburgh: Edinburgh University Press.
44. Kay, R. F., Madden, R. H., van Schaik, C. P., & Higdon, D. (1997). Primate species richness is determined by plant productivity: Implications for conservation. Proceedings of the National Academy of Sciences of the USA, 94, 13023–13027.
45. Knott, C. D. (1998). Changes in orangutan caloric intake, energy balance, and ketones in response to fluctuating fruit availability. International Journal of Primatology, 19, 1061–1079.
46. Laman, T. G., Gaither, J. C., & Lukas, D. E. (1996). Rain forest bird diversity in Gunung Palung National Park, West Kalimantan, Indonesia. Tropical Biodiversity, 3, 281–296.
47. Laurance, W. F., Useche, D. C., Shoo, L. P., Herzog, S. K., Kessler, M., Escobar, F., et al. (2011). Global warming, elevational ranges and the vulnerability of taxa. Biological Conservation, 144, 548–557.
48. Legendre, P., & Gallagher, E. D. (2001). Ecologically meaningful transformations for ordination of species data. Oecologia, 129, 271–280.
49. Lehman, S. M. (2006). Nested distribution patterns and the historical biogeography of the primates of Guyana. In S. M. Lehman & J. G. Fleagle (Eds.), Primate biogeography (pp. 63–80). New York: Springer Science+Business Media.
50. Leighton, M., & Leighton, D. (1983). Vertebrate responses to fruiting seasonality within a Bornean rain forest. In S. L. Sutton, T. C. Whitmore, & A. C. Chadwick (Eds.), Tropical rain forest: Ecology and management (pp. 181–196). Boston: Blackwell Scientific.
51. Lwanga, J. S., Struhsaker, T. T., Struhsaker, P. J., Butynski, T. M., & Mitani, J. C. (2011). Primate population dynamics over 32.9 years at Ngogo, Kibale National Park, Uganda. American Journal of Primatology, 73, 997–1011.
52. Marshall, A. J. (2004). The population ecology of gibbons and leaf monkeys across a gradient of Bornean forest types. Ph.D. dissertation, Harvard University.
53. Marshall, A. J. (2009). Are montane forests demographic sinks for Bornean white-bearded gibbons (Hylobates albibarbis)? Biotropica, 41, 257–267.
54. Marshall, A. J. (2010). Effect of habitat quality on primate populations in Kalimantan: Gibbons and leaf monkeys as case studies. In J. Supriatna & S. L. Gursky (Eds.), Indonesian primates (pp. 157–177). New York: Springer Science+Business Media.
55. Marshall, A. J., Ancrenaz, M., Brearley, F. Q., Fredriksson, G., Ghaffar, N., Heydon, M., et al. (2009a). The effects of habitat quality, phenology, and floristics on populations of Bornean and Sumatran orangutans: Are Sumatran forests more productive than Bornean forests? In S. A. Wich, S. S. Utami Atmoko, T. Mitra Setia, & C. P. van Schaik (Eds.), Orangutans: Geographic variation in behavioral ecology and conservation (pp. 97–117). Oxford: Oxford University Press.
56. Marshall, A. J., Boyko, C. M., Feilen, K. L., Boyko, R. H., & Leighton, M. (2009b). Defining fallback foods and assessing their importance in primate ecology and evolution. American Journal of Physical Anthropology, 140, 603–614.
57. Marshall, A. J., Cannon, C. H., & Leighton, M. (2009c). Competition and niche overlap between gibbons (Hylobates albibarbis) and other frugivorous vertebrates in Gunung Palung National Park, West Kalimantan, Indonesia. In S. Lappan & D. Whittaker (Eds.), The gibbons: New perspectives on small ape socioecology and population biology (pp. 161–188). New York: Springer Science+Business Media.
58. Marshall, A. J., & Leighton, M. (2006). How does food availability limit the population density of white-bearded gibbons? In G. Hohmann, M. Robbins, & C. Boesch (Eds.), Feeding ecology of the apes and other primates (pp. 311–333). Cambridge, U.K.: Cambridge University Press.
59. Marshall, A. J., & Wich, S. A. (2013). Characterization of primate environments through assessment of plant phenology. In E. Sterling, M. Blair, & N. Bynum (Eds.), Primate ecology and conservation: A handbook of techniques (pp. 103–127). Oxford: Oxford University Press.
60. Marshall, A. J., & Wrangham, R. W. (2007). Evolutionary consequences of fallback foods. International Journal of Primtology, 28, 1219–1235.
61. O’Brien, T. G., Kinnaird, M. F., Nurcahyo, A., Iqbal, M., & Rusmanto, M. (2004). Abundance and distribution of sympatric gibbons in a threatened Sumatran rain forest. International Journal of Primatology, 25, 267–284.
62. Oksanen, J., Blanchet, F. G., Kindt, R., Legendre, P., Minchin, P. R., O’Hara, R. B., et al. (2013) vegan: Community Ecology Package. R package version 2.0–10.
63. Paoli, G. D., Curran, L. M., & Zak, D. R. (2006). Soil nutrients and beta diversity in the Bornean Dipterocarpaceae: Evidence for niche partitioning by tropical rain forest trees. Journal of Ecology, 94, 157–170.
64. Peres, C. A. (1993). Structure and organization of an Amazonian terra frime primate community. Journal of Tropical Ecology, 9, 259–276.
65. Peres, C. A. (1997). Primate community structure at twenty western Amazonian flooded and unflooded forests. Journal of Tropical Ecology, 13, 381–405.
66. Peres, C. A., & Janson, C. H. (1999). Species coexistence, distribution and environmental determinants of neotropical primate richness: A community-level zoogeographic analysis. In J. J. Fleagle, C. Janson, & K. E. Reed (Eds.), Primate communities (pp. 55–74). Cambridge, U.K.: Cambridge University Press.
67. Poulson, J. R., Clark, C. J., Connor, E. F., & Smith, T. B. (2002). Differential resource use by primates and hornbills: Implications for seed dispersal. Ecology, 83, 228–240.
68. R Core Team. (2013). R: A language and environment for statistical computing. Austria: R Foundation for Statistical Computing V. Available at http://www.R-project.org/.
69. Reed, K. E., & Bidner, L. R. (2004). Primate communities: past, present and possible future. Yearbook of Physical Anthropology, 47, 2–39.
70. Rodman, P. S. (1979). Synecology of Bornean primates I. A test for interspecific interactions in spatial distribution of five species. American Journal of Physical Anthropology, 38, 655–660.
71. Rodman, P. S. (1991). Structural differentiation of microhabitats on sympatric Macaca fascicularis and M. nemestrina in East Kalimantan, Indonesia. International Journal of Primatology, 12, 357–375.
72. Royle, J. A., Dawson, D. K., & Bates, S. (2004). Modeling abundance effects in distance sampling. Ecology, 85, 1591–1597.
73. Stevenson, P. R. (2011). The abundance of large ateline monkeys is positively associated with the diversity of plants regenerating in Neotropical forests. Biotropica, 43, 512–519.
74. ter Braak, C. J. F., & Šmilauer, P. (1998). CANOCO reference manual and user’s guide to Canoco for Windows (version 4). Ithaca, NY: Microcomputer Power.
75. Whittaker, R. H. (1960). Vegetation of the Siskiyou Mountains, Oregon and California. Ecological Monographs, 30, 279–338.
76. Wich, S. A., & van Schaik, C. P. (2000). The impact of El Niño on mast fruiting in Sumatra and eslewhere in Malesia. Journal of Tropical Ecology, 16, 563–577.