Foraging and ranging behavior during a fallback episode: Hylobates albibarbis and Pongo pygmaeus wurmbii compared

American Journal of Physical Anthropology

Volumn 140, Issue 4, 2009, Pages 716-726

  Vogel, Erin R ^a,b   Haag, Livia ^b   Mitra Setia, Tatang ^c   Van Schaik, Carel P ^b   Dominy, Nathaniel J ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF ZURICH   (Switzerland)

^c Universitas Nasional   (Indonesia)

Author keywords

Dental morphology; Food mechanics; Forest structure; Locomotion; Primate diet

Indexed keywords

ADAPTATION; ANATOMY; ANIMAL BEHAVIOR; ANTHROPOIDEA; APE; BARK; CANOPY; CONFERENCE PAPER; DIET; DIGESTION; FOOD; FOOD INTAKE; FORAGING; FOREST STRUCTURE; FRUIT; HAPLORHINI; HYLOBATES ALBIBARBIS; INDONESIA; LOCOMOTION; MOLAR TOOTH; NONHUMAN; ORANG UTAN; PRESSURE; PRIMATE; RAIN FOREST; SOUTHEAST ASIA;

ANALYSIS OF VARIANCE; ANIMALS; APPETITIVE BEHAVIOR; CUSPID; DIET; FOOD HABITS; FRUIT; HYLOBATES; INDONESIA; MOLAR; MOTOR ACTIVITY; PONGO PYGMAEUS; SPECIES SPECIFICITY;

HAPLORHINI; HYLOBATES; PONGO; PONGO PYGMAEUS; PRIMATES; SIMIIFORMES;

EID: 70449109373     PISSN: 00029483     EISSN: 10968644     Source Type: Journal    
DOI: 10.1002/ajpa.21119     Document Type: Conference Paper

References (106)

1. Ashton PS, Givnish TJ, Appanah S. 1988. Staggered flowering in the Dipterocarpaceae: new insights into floral induction and the evolution of mast fruiting in the aseasonal tropics. Am Nat 132:44-66. (Pubitemid 19323994)
2. Bartlett TQ. 2009. The gibbons of Khao Yai: seasonal variation in behavior and ecology. Upper Saddle River: Pearson.
3. Bell RHV. 1971. A grazing ecosystem in the Serengeti. Sci Am 225:86-93.
4. Cannon CH, Curran LM, Marshall AJ, Leighton M. 2007a. Beyond mast-fruiting events: community asynchrony and individual dormancy dominate woody plant reproductive behavior across seven Bornean forest types. Curr Sci 93: 1558-1566.
5. Cannon CH, Curran LM, Marshall AJ, Leighton M. 2007b. Long-term reproductive behaviour of woody plants across seven Bornean forest types in the Gunung Palung National Park (Indonesia): suprannual synchrony, temporal productivity and fruiting diversity. Ecol Lett 10:956-969. (Pubitemid 47383381)
6. Cannon CH, Leighton M. 1994. Comparative locomotor ecology of gibbons and macaques: selection of canopy elements for crossing gaps. Am J Phys Anthropol 93:505-524. (Pubitemid 24104774)
7. Cant JGH. 1987. Positional behavior of female Bornean orangutans Pongo pygmaeus. Am J Primatol 12:71-90.
8. Chivers DJ. 1977. The feeding behavior of siamang (Symphalangys syndactylus). In: Clutton-Brock TH, editor. Primate ecology: studies of feeding and ranging behaviour in lemurs, monkeys and apes. London: Academic Press. p 355-382.
9. Chivers DJ. 1984. Feeding and ranging in gibbons: a summary. In: Preuschoft H, Chivers DJ, Brockelman WY, Creel N, editors. The lesser apes: evolutionary and behavioural biology. Edinburgh: Edinburgh University Press. p 267-281.
10. Clutton-Brock TH. 1977. Some aspects of intraspecific variation in feeding and ranging behaviour in primates. In: Clutton- Brock TH, editor. Primate ecology. London: Academic Press. p 539-556.
11. Curran LM, Leighton M. 2000. Vertebrate responses to spatio-temporal variation in seed production of mast-fruiting diptero-carpaceae. Ecol Monogr 70:101-128. (Pubitemid 30096344)
12. Delgado RA, van Schaik CP. 2000. The behavioral ecology and conservation of the orangutan (Pongo pygmaeus): a tale of two islands. Evol Anthropol 9:201-218.
13. Dial R, Bloodworth B, Lee A, Boyne P, Heys J. 2004. The distribution of free space and its relation to canopy composition at six forest sites. Forest Sci 50:312-325. (Pubitemid 39009358)
14. Dominy NJ, Lucas PW. 2004. Significance of color, calories, and climate to the visual ecology of catarrhines. Am J Primatol 62:189-207.
15. Dominy NJ, Lucas PW, Wright SJ. 2003b. Mechanics and chemistry of rain forest leaves: canopy and understorey compared. J Exp Bot 54:2007-2014.
16. Dominy NJ, Svenning J-C, Li W-H. 2003a. Historical contingency in the evolution of primate color vision. J Hum Evol 44:25-45.
17. Dominy NJ, Vogel ER, Yeakel JD, Constantino P, Lucas PW. 2008. Mechanical properties of plant underground storage organs and implications for dietary models of early hominins. Evol Biol 35:159-175.
18. Dudley R, DeVries PJ. 1990. Tropical rain forest structure and the geographical distribution of gliding vertebrates. Biotropica 22:432-434.
19. Elton S, Foley R, Ulijaszek SJ. 1998. Habitual energy expenditure of human climbing and clambering. Ann Hum Biol 25:523-531.
20. Emmons LH, Gentry AH. 1983. Tropical forest structure and the distribution of gliding and prehensile-tailed vertebrates. Am Nat 121:513-524.
21. Fan P-F, Jiang X-L. 2008. Effects of food and topography on ranging behavior of black crested gibbon (Nomascus concolor jingdongensis) in Wuliang Mountain, Yunnan, China. Am J Primatol 70:871-878.
22. Fleagle JG. 1976. Locomotion and posture of the Malayan siamang and implications for hominoid evolution. Folia Primatol 26:245-269.
23. Fleagle JG, Mittermeier RA. 1980. Locomotor behavior, body size and comparative ecology of seven Surinam monkeys. Am J Phys Anthropol 52:301-314.
24. Frisch JE. 1963. Sex-differences in the canines of the gibbon (Hylobates lar). Primates 4:1-10.
25. Frisch JE. 1973. The hylobatid dentition. In: Rumbaugh DM, editor. Gibbon and siamang, Vol.2: anatomy, dentition, taxonomy, molecular evolution, and behavior. Basel: S. Karger. p 56-95.
26. Gaulin SJC. 1979. A Jarman/Bell model of primate feeding niches. Hum Ecol 7:1-20.
27. Gautier-Hion A, Gautier JP, Quirs R. 1981. Forest structure and fruit availability as complementary factors influencing habitat use by a troop of monkeys (Cercopithecus cephus). Rev Ecol (Terre Vie) 35:511-536.
28. Gittins SP. 1980. Territorial behavior in the agile gibbon. Int J Primatol 1:381-399.
29. Gittins SP. 1983. The use of the forest canopy by the agile gibbon. Folia Primatol 40:134-144.
30. Gittins SP, Raemaekers J. 1980. Siamang, lar and agile gibbons. In: Chivers DJ, editor. Malayan forest primates: ten years' study in tropical rain forest. New York: Plenum Press. p 63-105.
31. Grand TI. 1984. Motion economy within the canopy: four strategies for mobility. In: Rodman PS, Cant JGH, editors. Adaptations for foraging in non-human primates. New York: Columbia University Press. p 54-72.
32. Grant PR, Grant BR. 2002. Unpredictable evolution in a 30- year study of Darwin's finches. Science 296:707-711.
33. Hanna JB, Schmitt D, Griffin TM. 2008. The energetic cost of climbing in primates. Science 320:898.
34. Hemingway CA, Bynum N. 2005. The influence of seasonality on primate diet and ranging. In: van Schaik CP, Brockman DK, editors. Seasonality in primates. Cambridge: Cambridge University Press. p 58-104.
35. Houle A, Chapman CA, Vickery WL. 2007. Intratree variation in fruit production and implications for primate foraging. Int J Primatol 28:1197-1217. (Pubitemid 50003056)
36. Hunt KD. 1995. Body size effects on vertical climbing among chimpanzees. Int J Primatol 16:855-865.
37. Jarman PJ. 1974. The social organization of antelope in relation to their ecology. Behaviour 48:215-256.
38. Jungers WL, Stern JT. 1984. Kinesiological aspects of brachiation in lar gibbons. In: Preuschoft H, Chivers DJ, Brockelman WY, Creel N, editors. The lesser apes: evolutionary and behavioural biology. Edinburgh: Edinburgh University Press. p 119-134.
39. Kay RF. 1981. The nut-crackers - a new theory of the adaptations of the Ramapithecinae. Am J Phys Anthropol 55:141-151.
40. Kay RF. 1985. Dental evidence for the diet of Australopithecus. Annu Rev Anthropol 14:315-341.
41. Kelley J. 1995. Sexual dimorphism in canine shape among extant great apes. Am J Phys Anthropol 96:365-389.
42. Kinzey WG. 1978. Feeding behaviour and molar features in two species of titi monkeys. In: Chivers J, Herbert J, editors. Recent advances in primatology. New York: Academic Press. p 373-385.
43. Kinzey WG. 1992. Dietary and dental adaptations in the Pitheciinae. Am J Phys Anthropol 88:499-514.
44. Kinzey WG, Norconk MA. 1990. Hardness as a basis of fruit choice in two sympatric primates. Am J Phys Anthropol 81: 5-15.
45. Kinzey WG, Norconk MA. 1993. Physical and chemical properties of fruit and seeds eaten by Pithecia and Chiropotes in Surinam and Venezuela. Int J Primatol 14:207-227.
46. Knott CD. 1998. Changes in orangutan caloric intake, energy balance, and ketones in response to fluctuating fruit availability. Int J Primatol 19:1061-1079.
47. Kono RT, Suwa G. 2008. Enamel distribution patterns of extant human and hominoid molars: occlusal versus lateral enamel thickness. Bull Natl Mus Nat Sci D 34:1-9.
48. Laden G, Wrangham RW. 2005. The rise of the hominids as an adaptive shift in fallback foods: plant underground storage organs (USOs) and australopith origins. J Hum Evol 49:482-498.
49. Lambert JE, Chapman CA, Wrangham RW, Conklin-Brittain NL. 2004. Hardness of cercopithecine foods: implications for the critical function of enamel thickness in exploiting fallback foods. Am J Phys Anthropol 125:363-368.
50. Leighton DR. 1987. Gibbons: territoriality and monogamy. In: Smuts BB, Cheney DL, Seyfarth RM, Wrangham RW, Struhsaker TT, editors. Primate societies. Chicago: University of Chicago Press. p 135-145.
51. Leighton M, Leighton DR. 1983. Vertebrate responses to fruiting seasonality within a Bornean rain forest. In: Sutton SL, Whitmore TC, Chadwick AC, editors. Tropical rain forest: ecology and management. Oxford: Blackwell. p 181-196.
52. Lucas PW. 2004. Dental functional morphology: How teeth work. Cambridge: Cambridge University Press.
53. Lucas PW, Beta T, Darvell BW, Dominy NJ, Essackjee HC, Lee PKD, Osorio D, Ramsden L, Yamashita N, Yuen TD. 2001. Field kit to characterize physical, chemical and spatial aspects of potential primate foods. Folia Primatol 72:11-25. (Pubitemid 32247414)
54. Lucas PW, Constantino P, Wood B, Lawn B. 2008. Dental enamel as a dietary indicator in mammals. BioEssays 30:374-385.
55. Lucas PW, Peters CR, Arrandale SR. 1994. Seed-breaking forces exerted by orang-utans with their teeth in captivity and a new technique for estimating forces produced in the wild. Am J Phys Anthropol 94:365-378.
56. MacKinnon J. 1974. The behaviour and ecology of wild orangutans (Pongo pygmaeus). Anim Behav 22:3-74.
57. Marshall AJ, Boyko CM, Feilen KL, Boyko RH, Leighton M. 2009a. Defining fallback foods and assessing their importance in primate ecology and evolution. Am J Phys Anthropol 140: 603-614.
58. Marshall AJ, Cannon CH, Leighton M. 2009b. Competition and niche overlap between gibbons (Hylobates albibarbis) and other frugivorous vertebrates in Gunung Palung National Park, West Kalimantan. In: Lappan SM, Whittaker DL, Geissmann T, editors. The gibbons: new perspectives on small ape socioecology and population biology. New York: Springer (in press).
59. Marshall AJ, Leighton M. 2006. How does food availability limit the population density of white-bearded gibbons? In: Hohmann G, Robbins MM, Boesch C, editors. Feeding ecology in apes and other primates: ecological, physical and behavioral aspects. Cambridge: Cambridge University Press. p 313-335.
60. Marshall AJ, Wrangham RW. 2007. Evolutionary consequences of fallback foods. Int J Primatol 28:1219-1235.
61. Masterson TJ. 1997. Sexual dimorphism and interspecific cranial form in two capuchin species: Cebus albifrons and C. apella. Am J Phys Anthropol 104:487-511.
62. McConkey KR, Ario A, Aldy F, Chivers DJ. 2003. Influence of forest seasonality on gibbon food choice in the rain forests of Barito Ulu, Central Kalimantan. Int J Primatol 24:19-32. (Pubitemid 36117320)
63. M'Kirera F, Ungar PS. 2003. Occlusal relief changes with molar wear in Pan troglodytes troglodytes and Gorilla gorilla gorilla. Am J Primatol 60:31-41. (Pubitemid 36832435)
64. Nagatoshi K. 1990. Molar enamel thickness in European Miocene and extant hominoidea. Int J Primatol 11:283-295.
65. Olejniczak AJ, Tafforeau P, Feeney RNM, Martin LB. 2008. Three-dimensional primate molar enamel thickness. J Hum Evol 54:187-195. (Pubitemid 351189106)
66. Parker GG, Russ ME. 2004. The canopy surface and stand development: assessing forest canopy structure and complexity with near-surface altimetry. Forest Ecol Manag 189:307-315.
67. Pettersson, J. 2007. Between year differences and similarities of female orangutan home ranges. Masters thesis, Universitz of Uppsala, Sweden.
68. Plavcan JM, Ruff CB. 2008. Canine size, shape, and bending strength in primates and carnivores. Am J Phys Anthropol 136:65-84.
69. Plavcan JM, van Schaik CP. 1992. Intrasexual competition and canine dimorphism in anthropoid primates. Am J Phys Anthropol 87:461-477.
70. Plavcan JM, van Schaik CP. 1997. Interpreting hominid behavior on the basis of sexual dimorphism. J Hum Evol 32:345-374. (Pubitemid 127420701)
71. Pontzer H, Wrangham RW. 2004. Climbing and the daily energy cost of locomotion in wild chimpanzees: implications for hominoid locomotor evolution. J Hum Evol 46:315-333. (Pubitemid 38454210)
72. Preuschoft H, Demes B. 1984. Biomechanics of brachiation. In: Preuschoft H, Chivers DJ, Brockelman WY, Creel N, editors. The lesser apes: evolutionary and behavioral biology. Edinburgh: Edinburgh University Press. p 96-118.
73. Raemaekers J. 1980. Causes of variation between months in the distance traveled daily by gibbons. Folia Primatol 34:46-60.
74. Remis MJ. 1999. Tree structure and sex differences in arboreality among western lowland gorillas (Gorilla gorilla gorilla) at Bai Hokou, Central African Republic. Primates 40:383-396. (Pubitemid 29437697)
75. Robinson BW, Wilson DS. 1998. Optimal foraging, specialization, and a solution to Liem's paradox. Am Nat 151:223-235.
76. Rosenberger AL, Kinzey WG. 1976. Functional patterns of molar occlusion in platyrrhine primates. Am J Phys Anthropol 45:281-298.
77. Sakai S. 2002. General flowering in lowland mixed dipterocarp forests of South-east Asia. Biol J Linn Soc 75:233-247. (Pubitemid 35056730)
78. Sakai S, Momose K, Yumoto T, Nagamitsu T, Nagamasu H, Hamid AA, Nakashizuka T. 1999. Plant reproductive phenology over four years including an episode of general flowering in a lowland dipterocarp forest, Sarawak, Malaysia. Am J Bot 86:1414-1436. (Pubitemid 30811538)
79. Schaefer HM, Schmidt V, Wesenberg J. 2002. Vertical stratification and caloric content of the standing fruit crop in a tropical lowland forest. Biotropica 34:244-253. (Pubitemid 34763192)
80. Schultz AH. 1944. Age changes and variability in gibbons: a morphological study on a population sample of a man-like ape. Am J Phys Anthropol 2:1-129.
81. Shellis RP, Beynon AD, Reid DJ, Hiiemae KM. 1998. Variations in molar enamel thickness among primates. J Hum Evol 35:507-522.
82. Singleton IS, van Schaik CP. 2001. Orangutan home range size and its determinants in a Sumatran swamp forest. Int J Primatol 22:877-911.
83. Taylor AB. 2006. Feeding behavior, diet, and the functional consequences of jaw form in orangutans, with implications for the evolution of Pongo. J Hum Evol 50:377-393.
84. Taylor AB, van Schaik CP. 2007. Variation in brain size and ecology in Pongo. J Hum Evol 52:59-71.
85. Taylor AB, Vogel ER, Dominy NJ. 2008. Masticatory biomechanics and food mechanical properties in large-bodied hominoids. J Hum Evol 55:604-616.
86. Temerin LA, Cant JGH. 1983. The evolutionary divergence of Old World monkeys and apes. Am Nat 122:335-351.
87. Terborgh J. 1983. Five new world primates: a study in comparative ecology. Princeton: Princeton University Press.
88. Thorpe SKS, Crompton RH. 2005. Locomotor ecology of wild orangutans Pongo pygmaeus abelii in the Gunung Leuser Ecosystem, Sumatra, Indonesia: a multivariate analysis using log-linear modelling. Am J Phys Anthropol 127:58-78.
89. Thorpe SKS, Crompton RH, Alexander RM. 2007a. Orangutans use compliant branches to lower the energetic cost of locomotion. Biol Lett 3:253-256.
90. Thorpe SKS, Holder RL, Crompton RH. 2007b. Origin of human bipedalism as an adaptation for locomotion on flexible branches. Science 316:1328-1331.
91. Tuttle RH, Cortright GW. 1988. Positional behavior, adaptive complexes, and evolution. In: Schwartz JH, editor. Orang-utan biology. Oxford: Oxford University Press. p 311-330.
92. Ungar PS. 2007. Dental functional morphology: the known, the unknown, and the unknowable. In: Ungar PS, editor. Evolution of the human diet: the known, the unknown, and the unknowable. Oxford: Oxford University Press. p 39-55.
93. Ungar PS, M'Kirera F. 2003. A solution to the worn tooth conundrum in primate functional anatomy. Proc Natl Acad Sci USA 100:3874-3877. (Pubitemid 36418124)
94. van Schaik CP. 1999. The socioecology of fission-fusion sociality in orangutans. Primates 40:73-90.
95. van Schaik CP, Brockman DK. 2005. Seasonality in primate ecology, reproduction, and life history: an overview. In: van Schaik CP, Brockman DK, editors. Seasonality in Primates. Cambridge: Cambridge University Press. p 3-20.
96. van Schaik CP, Terborgh JW, Wright SJ. 1993. The phenology of tropical forests: adaptive significance and consequences for primary consumers. Annu Rev Ecol Syst 24:353-377. (Pubitemid 2022115)
97. van Schaik CP, van Noordwijk MA, Wich SA. 2006. Innovation in wild Bornean orangutans (Pongo pygmaeus wurmbii). Behaviour 143:839-876.
98. van Woerden JT. 2007. The behavioral change of wild Bornean orangutans (P. p. wurmbii): a comparison to wild Sumatran orangutans (P. abelii). M.Sc. thesis, University of Utrecht.
99. Vogel ER, van Woerden JT, Lucas PW, Utami Atmoko SS, van Schaik CP, Dominy NJ. 2008. Functional ecology and evolution of hominoid molar enamel thickness: Pan troglodytes schwein-furthii and Pongo pygmaeus wurmbii. J Hum Evol 55:60-74.
100. Weishampel JF, Godin JR, Henebry GM. 2001. Pantropical dynamics of 'intact' rain forest canopy texture. Glob Ecol Biogeogr 10:389-398.
101. Whitten AJ. 1980. Arenga fruit as a food for gibbons. Principes 24:143-146.
102. Wiens JA. 1977. On competition and variable environments. Am Sci 65:590-597.
103. Wich SA, van Schaik CP. 2000. The impact of El Niño on mast fruiting in Sumatra and elsewhere in Malesia. J Trop Ecol 16:563-577.
104. Wrangham R, Conklin-Brittain N, Hunt K. 1998. Dietary response of chimpanzees and cercopithecines to seasonal variation in fruit abundance. I. Antifeedants. Int J Primatol 19:949-970. (Pubitemid 29051795)
105. Wright BW. 2005. Craniodental biomechanics and dietary toughness in the genus Cebus. J Hum Evol 48:473-492.
106. Zar JH. 1999. Biostatistical analysis, 4th ed. Upper Saddle River: Prentice Hall.