The influence of natural diet composition, food intake level, and body size on ingesta passage in primates

Comparative Biochemistry and Physiology - A Molecular and Integrative Physiology

Volumn 150, Issue 3, 2008, Pages 274-281

  Clauss, Marcus ^a   Streich, W Jürgen ^b   Nunn, Charles L ^c   Ortmann, Sylvia ^b   Hohmann, Gottfried ^c   Schwarm, Angela ^b   Hummel, Jürgen ^d  

^a VETSUISSE FACULTY UNIVERSITY OF ZURICH   (Switzerland)

^b LEIBNIZ INSTITUTE FOR ZOO AND WILDLIFE RESEARCH   (Germany)

^c MAX PLANCK INSTITUTE FOR EVOLUTIONARY ANTHROPOLOGY   (Germany)

^d UNIVERSITY OF BONN   (Germany)

Author keywords

Digestive anatomy; Digestive physiology; Feeding ecology; Foregut fermenter; Herbivory; Ingesta passage; Mean retention time

Indexed keywords

ARTICLE; BODY MASS; BODY SIZE; DIGESTION; FERMENTATION; FOOD COMPOSITION; FOOD INTAKE; HERBIVORE; NONHUMAN; PHYLOGENY; PRIMATE; STOMACH;

MAMMALIA; PRIMATES;

EID: 44749094454     PISSN: 10956433     EISSN: 15314332     Source Type: Journal    
DOI: 10.1016/j.cbpa.2008.03.012     Document Type: Article

References (95)

1. Aiello L.C., and Wheeler P. The expensive tissue hypothesis: the brain and the digestive system in human and primate evolution. Curr. Anthropol. 36 (1995) 199-221
2. Barboza P.S., and Bowyer R.T. Sexual segregation in dimorphic deer: a new gastrocentric hypothesis. J. Mammal. 81 (2000) 473-489
3. Behrend A., Lechner-Doll M., Streich W.J., and Clauss M. Seasonal faecal excretion, gut fill, liquid and particle marker retention in mouflon (Ovis ammon musimon), and a comparison with roe deer (Capreolus capreolus). Acta Theriol. 49 (2004) 503-515
4. Bell R.H.V. A grazing ecosystem in the Serengeti. Sci. Am. 225 (1971) 86-93
5. Bininda-Emonds O.R.P., Cardillo M., Jones K.E., MacPhee R.D.E., Beck R.M.D., Grenyer R., Price S.A., Vos R.A., Gittleman J.L., and Purvis A. The delayed rise of present-day mammals. Nature 446 (2007) 507-512
6. Blomberg S.P., Garland T., and Ives A.R. Testing for phylogenetic signal in comparative data: behavioral traits are more labile. Evolution 57 (2003) 717-745
7. Brotoisworo E., and Dirgayusa I.W.A. Ranging and feeding behavior of Presbythis christata in the Pangandaran Nature Reserve, West Java, Indonesia. In: Ehara A., Kimura T., Takenaka O., and Iwamoto M. (Eds). Primatology today (1991), Elsevier Science, Amsterdam 115-118
8. Calder W.A. Size, function, and life history (1984), Harvard University Press, Cambridge, MA
9. Campbell J.L., Eisemann J.H., Glander K.E., and Crissey S.D. Intake, digestibility, and passage of a commercially designed diet by two propithecus species. Am. J. Primatol. 48 (1999) 237-246
10. Campbell J.L., Williams C.V., and Eisemann J.H. Fecal inoculum can be used to determine the rate and extent of in vitro fermentation of dietary fiber sources across three lemur species that differ in dietary profile: Varecia variegata, Eulemur fulvus and Hapalemur griseus. J. Nutr. 132 (2002) 3073-3080
11. Campbell J.L., Williams C.V., and Eisemann J.H. Use of total dietary fiber across four lemur species (Propithecus cerreauxi coquereli, Hapalemur griseus griseus, Varecia variegata, and Eulemur fulvus): does fiber type affect digestive efficiency?. Am. J. Primatol. 64 (2004) 323-335
12. Caton J. Digestive strategy of the Asian colobine genus Trachypithecus. Primates 40 (1999) 311-325
13. Caton J.M., and Hume I.D. The digestive strategies of marmosets and tamarins. Proc. Comp. Nutr. Soc. 1 (1996) 18-20
14. Caton J.M., Hill D.M., Hume I.D., and Crook G.A. The digestive strategy of the common marmoset (Callithrix jacchus). Comp. Biochem. Physiol. A 114 (1996) 1-8
15. Caton J.M., Hume I.D., Hill D.M., and Harper P. Digesta retention in the gastro-intestinal tract of the orangutan (Pongo pygmaeus). Primates 40 (1999) 551-558
16. Caton J.M., Lawes M., and Cunningham C. Digestive strategy of the south-east African lesser bushbaby (Galago moholi). Comp. Biochem. Physiol. A 127 (2000) 39-48
17. Chapman C.A., Walker S., and Lefebvre L. Reproductive strategies of primates: the influence of body size and diet on litter size. Primates 31 (1990) 1-13
18. Chapman C.A., Chapman L.J., Gautier-Hion A., Lambert J.E., Rode K., Tutin C.E.G., and White L.J.T. Variation in the diet of Cercopithecus monkeys: differences within forests, among forests, and across species. In: Glenn M., and Cords M. (Eds). The guenons: diversity and adaptation in African monkeys (2002), Kluwer Academic Press, New York 319-344
19. Chivers D.J. Functional anatomy of the gastrointestinal tract. In: Davies A.G., and Oates J.F. (Eds). Colobine monkeys (1995), Cambridge University Press, Cambridge 205-226
20. Chivers D.J., and Hladik C.M. Morphology of the gastrointestinal tract in primates: comparisons with other mammals in relation to diet. J. Morph. 166 (1980) 337-386
21. Clauss M., and Hummel J. The digestive performance of mammalian herbivores: why big may not be that much better. Mammal. Rev. 35 (2005) 174-187
22. Clauss M., and Lechner-Doll M. Differences in selective reticulo-ruminal particle retention as a key factor in ruminant diversification. Oecologia 129 (2001) 321-327
23. Clauss M., Frey R., Kiefer B., Lechner-Doll M., Loehlein W., Polster C., Rössner G.E., and Streich W.J. The maximum attainable body size of herbivorous mammals: morphophysiological constraints on foregut, and adaptations of hindgut fermenters. Oecologia 136 (2003) 14-27
24. Clauss M., Schwarm A., Ortmann S., Alber D., Flach E.J., Kühne R., Hummel J., Streich W.J., and Hofer H. Intake, ingesta retention, particle size distribution and digestibility in the hippopotamidae. Comp. Biochem. Physiol. A 139 (2004) 449-459
25. Clauss M., Froeschle T., Castell J., Hummel J., Hatt J.M., Ortmann S., and Streich W.J. Fluid and particle retention times in the black rhinoceros (Diceros bicornis), a large hindgut-fermenting browser. Acta Theriol. 50 (2005) 367-376
26. Clauss M., Robert N., Walzer C., Vitaud C., and Hummel J. Testing predictions on body mass and gut contents: dissection of an African elephant (Loxodonta africana). Eur. J. Wildlife Res. 51 (2005) 291-294
27. Clauss M., Hummel J., and Streich W.J. The dissociation of the fluid and particle phase in the forestomach as a physiological characteristic of large grazing ruminants: an evaluation of available, comparable ruminant passage data. Eur. J. Wildlife Res. 52 (2006) 88-98
28. Clauss M., Schwarm A., Ortmann S., Streich W.J., and Hummel J. A case of non-scaling in mammalian physiology? Body size, digestive capacity, food intake, and ingesta passage in mammalian herbivores. Comp. Biochem. Physiol. A 148 (2007) 249-265
29. Clauss M., Streich W.J., Schwarm A., Ortmann S., and Hummel J. The relationship of food intake and ingesta passage predicts feeding ecology in two different megaherbivore groups. Oikos 116 (2007) 209-216
30. Clutton-Brock T.H., and Harvey P.H. Primates, brains and ecology. J. Zool. (Lond.) 190 (1980) 309-323
31. Clutton-Brock T.H., and Harvey P.H. The functional significance of variation in body size among mammals. Special Publications of the American Society of Mammalogy vol. 7 (1983) 632-663
32. Cork S. Digestive constraints on dietary scope in small and moderately-small mammals: how much do we really understand?. In: Chivers D.J., and Langer P. (Eds). The digestive system of mammals: food, form and function (1994), Cambridge University Press, Cambridge 337-369
33. Courts S.E. Dietary strategies of Old World fruit bats: how do they obtain sufficient protein?. Mammal. Rev. 28 (1998) 185-194
34. Danish L., Chapman C.A., Hall M.B., Rode K.D., and O'Driscoll Worman C. The role of sugar in diet selection in redtail and red colobus monkeys. In: Hohmann G., Robbins M.M., and Boesch C. (Eds). Feeding Ecology in Apes and Other Primates (2006), Cambridge University Press, Cambridge 473-488
35. Demment M.W. Feeding ecology and the evolution of body size of baboons. Afr. J. Ecol. 21 (1983) 219-233
36. Demment M.W., and Van Soest P.J. A nutritional explanation for body-size patterns of ruminant and nonruminant herbivores. Am. Nat. 125 (1985) 641-672
37. Dierenfeld E.S., Hintz H.F., Robertson J.B., Van Soest P.J., and Oftedal O.T. Utilization of bamboo by the giant panda. J. Nutr. 112 (1982) 636-641
38. Dierenfeld E.S., Koontz F.W., and Goldstein R.S. Feed intake, digestion and passage of the proboscis monkey (Nasalis larvatus) in captivity. Primates 33 (1992) 399-405
39. Edwards M.S., and Ullrey D.E. Effect of dietary fiber concentration on apparent digestibility and digesta passage in non-human primates. I. Ruffed lemurs (Varecia variegata variegata and V. v. rubra). Zool. Biol. 18 (1999) 529-536
40. Edwards M.S., and Ullrey D.E. Effect of dietary fiber concentration on apparent digestibility and digesta passage in non-human primates. II. Hindgut- and foregut-fermenting folivores. Zoo. Biol. 18 (1999) 537-549
41. Felsenstein J. Phylogenies and the comparative method. Am. Nat. 125 (1985) 1-15
42. Foose, T.J., 1982. Trophic strategies of ruminant versus nonruminant ungulates. PhD. University of Chicago, Chicago
43. Fryxell J.M., Vamosi S.M., Walton R.A., and Doucet C.M. Retention time and the functional response of beavers. Oikos 71 (1994) 207-214
44. Garland T., Harvey P.H., and Ives A.R. Procedures for the analysis of comparative data using phylogenetically independent contrasts. Syst. Biol. 4 (1992) 18-32
45. Gaulin S.J.C. A Jarman-Bell model of primate feeding niches. Human Ecol. 7 (1979) 1-20
46. Gautier-Hion A., Emmons L.H., and Dubost G. A comparison of the diets of three major groups of primary consumers of Gabon (primates, squirrels and ruminants). Oecologia 45 (1980) 182-189
47. Goodall J. The chimpanzees of Gombe: patterns of behavior (1996), Belknap Press of Harvard University Press, Cambridge
48. Hara C. "Pygathrix nemaeus" (On-line), Animal Diversity Web (2003). http://animaldiversity.ummz.umich.edu/site/accounts/information/Pygathrix_nemaeus.html Accessed May 19, 2007 at http://animaldiversity.ummz.umich.edu/site/accounts/information/Pygathrix_nemaeus.html
49. Harvey P.H., and Pagel M.D. The comparative method in evolutionary biology (1991), Oxford University Press, Oxford
50. Hofmann R.R. Evolutionary steps of ecophysiological adaptation and diversification of ruminants: a comparative view of their digestive system. Oecologia 78 (1989) 443-457
51. Hummel J., Nogge G., Clauss M., Norgaard C., Johanson K., Nijboer J., and Pfeffer E. Energetic nutrition of the okapi in captivity: fermentation characteristics of feedstuffs. Zool. Biol. 25 (2006) 251-266
52. Hummel J., Südekum K.H., Streich W.J., and Clauss M. Forage fermentation patterns and their implications for herbivore ingesta retention times. Funct. Ecol. 20 (2006) 989-1002
53. Illius A.W., and Gordon I.J. Modelling the nutritional ecology of ungulate herbivores: evolution of body size and competitive interactions. Oecologia 89 (1992) 428-434
54. Janis C. The evolutionary strategy of the equidae and the origins of rumen and caecal digestion. Evolution 30 (1976) 757-774
55. Jarman P.J. The social organization of antelope in relation to their ecology. Behaviour 48 (1974) 215-266
56. Karasov W.H., and Martínez del Rio C. Physiological ecology: how animals process energy, nutrients, and toxins (2007), Princeton University Press, Princeton, New Jersey, USA
57. Kirkpatrick R.C., Zou R.J., Dierenfeld E.S., and Zhou H.W. Digestion of selected foods by Yunnan snub-nosed monkey (Rhinopithecus bieti). Am. J. Phys. Anthropol. 114 (2001) 156-162
58. Kool K.M. The diet and feeding behavior of the Silver leaf monkey (Trachypithecus auratus sondaicus) in Indonesia. Int. J. Primatol. 14 (1993) 667-700
59. Lambert J.E. Primate digestion: interactions among anatomy, physiology, and feeding ecology. Evol. Anthropol. 7 (1998) 8-20
60. Lambert J.E. Digestive retention times in forest guenons (Cercopithecus spp.) with reference to chimpanzees (Pan troglotydes). Int. J. Primatol. 23 (2002) 1169-1185
61. Maddison W.P., and Maddison D.R. Mesquite: a modular system for evolutionary analysis (2006). http://mesquiteproject.org http://mesquiteproject.org
62. McNab B.K. The physiological ecology of vertebrates. A view from energetics (2002), Cornell University Press, Ithaca
63. Meyers D.M., and Wright P.C. Resource tracking: food availability and Propithecus seasonal reproduction. In: Kappeler P.M., and Ganzhorn J.U. (Eds). Lemur social systems and their ecological basis (1993), Plenum Press, New York 179-192
64. Midford P.E., Garland T., and Maddison W.P. PDAP Package of Mesquite (2005) Version 1.07. In:
65. Milton K. Distribution patterns of tropical plant foods as an evolutionary stimulus to primate mental development. Am. Anthropol. 83 (1981) 534-548
66. Milton K. The role of food-processing factors in primate food choice. In: Rodman P.S., and Cant J.G.H. (Eds). Adaptations for foraging in nonhuman primates (1984), Columbia University Press, New York 249-279
67. Milton K. Physiological ecology of howlers (Alouatta): energetic and digestive considerations and comparison with the colobinae. Int. J. Primatol. 19 (1998) 513-548
68. Milton K., and Demment M.W. Digestion and passage kinetics of chimpanzees fed high and low fibre diets and comparisons with human data. J. Nutr. 118 (1988) 1082-1088
69. Nelson S.L., Kunz T.H., and Humphrey S.R. Folivory in fruit bats: leaves provide a natural source of calcium. J. Chem. Ecol. 31 (2005) 1683-1691
70. Nijboer, J., Clauss, M., 2006. The digestive physiology of colobine primates. In: Nijboer J. Fibre intake and faeces quality in leaf-eating monkeys. PhD thesis, University of Utrecht, The Netherlands 9-28.
71. Nijboer J., Clauss M., Van de Put K., Van der Kuilen J., Wouterse H., and Beynen A.C. Influence of two different diets on fluid and particle retention time in Javan langur (Trachypithecus auratus auratus). Zool. Gart. N.F. 77 (2007) 36-46
72. Nunn C.L., and Barton R.A. Comparative methods for studying primate adaptation and allometry. Evol. Anthropol. 10 (2001) 81-98
73. Oates J.F. The guereza and its food. In: Clutton-Brock T.H. (Ed). Primate ecology (1977), Academic Press, London 275-321
74. Oftedal O. The nutritional consequences of foraging in primates: the relationship of nutrient intakes to nutrient requirements. Phil. Trans. R. Soc. Lond. B 334 (1991) 161-170
75. Parra R. Comparison of foregut and hindgut fermentation in herbivores. In: Montgomery G.G. (Ed). The ecology of arboreal folivores (1978), Smithsonian Institution Press, Washington DC 205-229
76. Pavelka M.S.M., and Knopff K.H. Diet and activity in black howler monkeys (Alouatta pigra) in southern Belize: does degree of frugivory influence activity level?. Primates 45 (2004) 105-111
77. Pérez-Barbería F.J., Elston D.A., Gordon I.J., and Illius A.W. The evolution of phylogenetic differences in the efficiency of digestion in ruminants. Proc. R. Soc. Lond. B 271 (2004) 1081-1090
78. Petraitis P.S., Dunham A.E., and Niewlarowski P.H. Inferring multiple causality: the limitations of path analysis. Funct. Ecol. 10 (1996) 421-431
79. Reid E.D., and Brooks R.J. Effect of water on retention time and food consumption in deer mice. Can. J. Zool. 72 (1994) 1711-1714
80. Remis M.J. Initial studies on the contributions of body size and gastrointestinal passage rates to dietary flexibility among gorillas. Am. J. Phys. Anthropol. 112 (2000) 171-180
81. Rice W.R., and Gaines S.D. 'Heads I win, tails you lose': testing directional alternative hypotheses in ecological and evolutionary research. Trends Ecol. Evol. 9 (1994) 235-237
82. Sailer L.D., Gaulin S.J., Boster J.S., and Kurland J.A. Measuring the relationship between dietary quality and body size in primates. Primates 26 (1985) 14-27
83. Sakaguchi E., Suzuki K., Kotera S., and Ehara A. Fibre digestion and digesta retention time in macaque and colobus monkeys. In: Ehara A., Kimura T., Takenaka O., and Iwamoto M. (Eds). Primatology today (1991), Elsevier Science, New York 671-674
84. Sibly R. Strategies of digestion and defecation. In: Townsend C., and Calow P. (Eds). Physiological ecology: an evolutionary approach to resource utilization (1981), Blackwell Scientific, Oxford 109-139
85. Silva M., and Downing J.A. CRC handbook of mammalian body masses (1995), CRC Press, Bota Racon
86. Simmen B., Hladik A., and Ramasiarisoa P. Food intake and dietary overlap in native Lemur catta and Propithecus verreauxi and introduced Eulemur fulvus at Berenty, Southern Madagascar. Int. J. Primatol. 24 (2003) 949-968
87. Snodgrass J.J., Leonard W.R., and Robertson M.L. Primate bioenergetics: an evolutionary perspective. In: Ravosa J.R., and Dagosto M. (Eds). Primate origins: adaptations and evolution (2007), Springer, New York 703-737
88. Stalinski J. Digestion, defecation and food passage rate in the insectivorous bat Myotis myotis. Acta Theriol. 39 (1994) 1-11
89. Stevens C.E., and Hume I.D. Contributions of microbes in vertebrate gastrointestinal tract to production and conservation of nutrients. Physiol. Revs. 78 (1998) 393-427
90. Stokke S., and du Toit J.T. Sex and size related differences in the dry season feeding patterns of elephants in Chobe National Park, Botswana. Ecography 23 (2000) 70-80
91. Tan C.L. Group composition, home range size, and diet of three sympatric bamboo lemur species (Genus Hapalemur) in Ranomafana National Park, Madagascar. Int. J. Primatol. 20 (1999) 547-566
92. Udén P., Rounsaville T.R., Wiggans G.R., and Van Soest P.J. The measurement of liquid and solid digesta retention in ruminants, equines and rabbits given timothy (Phleum pratense) hay. Br. J. Nutr. 48 (1982) 329-339
93. Warner A.C.I. Rate of passage through the gut of mammals and birds. Nutr. Abstr. Revs. B 51 (1981) 789-820
94. Xiang Z.F., Huo S., Xiao W., Quan R.C., and Grueter C.C. Diet and feeding behavior of Rhinopithecus bieti at Xiaochangdu, Tibet: adaptations to a marginal environment. Am. J. Primatol. 69 (2007) 1-18
95. Yeager C.P. Feeding ecology of the proboscis monkey (Nasalis larvatus). Int. J. Primatol. 10 (1989) 497-530