Small folivorous primate groups exhibit behavioral and physiological effects of food scarcity

Behavioral Ecology

Volumn 21, Issue 1, 2010, Pages 46-56

  Harris, Tara R ^a,b   Chapman, Colin A ^c,d   Monfort, Steven L ^b  

^a MAX PLANCK INSTITUTE FOR EVOLUTIONARY ANTHROPOLOGY   (Germany)

^b SMITHSONIAN CONSERVATION BIOLOGY INSTITUTE   (United States)

^c MCGILL UNIVERSITY   (Canada)

^d WILDLIFE CONSERVATION SOCIETY   (United States)

Author keywords

Black and white colobus monkeys; Feeding competition; Folivores; Food availability; Group size; Primates

Indexed keywords

BEHAVIORAL RESPONSE; FOOD LIMITATION; GROUP SIZE; LACTATION; NATIONAL PARK; PEPTIDE; PHYSIOLOGICAL RESPONSE; PRIMATE; SCRAMBLE COMPETITION; SELECTION;

KIBALE NATIONAL PARK; UGANDA; WESTERN PROVINCE [UGANDA];

COLOBINAE; COLOBUS; COLOBUS GUEREZA; COLOBUS SP.; PRIMATES;

EID: 72649102784     PISSN: 10452249     EISSN: 14657279     Source Type: Journal    
DOI: 10.1093/beheco/arp150     Document Type: Article

References (73)

1. Borries C, Larney E, Lu A, Ossi K, Koenig A. 2008. Costs of group size: lower developmental and reproductive rates in larger groups of leaf monkeys. Behav Ecol. 19:1186-1191.
2. Bradbury JW, Vehrencamp SL. 1976. Social organization and foraging in emballonurid bats, II: a model for the determination of group size. Behav Ecol Sociobiol. 1:383-404.
3. Chapman CA, Chapman LJ, Bjorndal KA, Onderdonk DA. 2002. Application of protein to fiber ratios to predict colobine abundance on different spatial scales. Int J Primatol. 23:283-310.
4. Chapman CA, Chapman LJ, Gillespie TR. 2002. Scale issues in the study of primate foraging: red colobus of Kibale National Park. Am J Phys Anthropol. 117:349-363.
5. Chapman CA, Chapman LJ, Naughton-Treves L, Lawes MJ, McDowell LR. 2004. Predicting folivorous primate abundance: validation of a nutritional model. Am J Primatol. 62:55-69.
6. Chapman CA, Gillespie TR, Speirs ML. 2005. Parasite prevalence and richness in sympatric colobines: effects of host density. Am J Prima-tol. 67:259-266.
7. Chapman CA, Lambert JA. 2000. Habitat alteration and the conservation of African primates: case study of Kibale National Park, Uganda. Am J Primatol. 50:169-185.
8. Chapman CA, Pavelka MSM. 2005. Group size in folivorous primates: ecological constraints and the possible influence of social factors. Primates. 46:1-9.
9. Chapman CA, Wasserman MD, Gillespie TR, Speirs ML, Lawes MJ, Saj TL, Ziegler TE. 2006. Do nutrition, parasitism, and stress have syn-ergistic effects on red colobus populations living in forest fragments? Am J Phys Anthropol. 131:525-534.
10. Clutton-Brock TH. 1974. Primate social organization and ecology. Nature. 250:539-542.
11. Coop RL, Holmes PH. 1996. Nutrition and parasite interaction. Int J Parasitol. 26:951-962.
12. Crockett CM, Janson CH. 2000. Infanticide in red howlers: female group size, male composition, and a possible link to folivory. In: van Schaik CP, Janson CH, editors. Infanticide by males and its implications. Cambridge: Cambridge University Press. p. 75-98.
13. Crook JH, Gartlan JS. 1966. Evolution of primate societies. Nature. 210:1200-1203.
14. Deschner T, Kratzsch J, Hohmann G. 2008. Urinary C-peptide as a method for monitoring body mass changes in captive bonobos (Pan paniscus). Horm Behav. 54:620-626.
15. Eisenberg JF, Muckenhirn NA, Rudran R. 1972. The relation between ecology and social structure in primates. Science. 176:863-874.
16. Emery Thompson M, Knott CD. 2008. Urinary C-peptide of insulin as a non-invasive marker of energy balance in wild orangutans. Horm Behav. 53:526-535.
17. Emery Thompson M, Muller MN, Wrangham RW, Lwanga JS, Potts KB. 2009. Urinary C-peptide tracks seasonal and individual variation in energy balance in wild chimpanzees. Horm Behav. 55:299-305.
18. Fashing PJ. 2001. Activity and ranging patterns of guerezas in the Kakamega forest: intergroup variation and implications for intra-group feeding competition. Int J Primatol. 22:549-577.
19. Fashing PJ. 2007. African colobine monkeys: patterns of between-group interaction. In: Campbell C, Fuentes A, MacKinnon A, Panger M, Bearder S, editors. Primates in perspective. Oxford: Oxford University Press. p. 201-224.
20. Freeland WJ. 1979. Primate social groups as biological islands. Ecology. 60:719-728.
21. Ganas J, Robbins MM. 2005. Ranging behavior of the mountain gorillas (Gorilla beringei beringei) in Bwindi Impenetrable National Park, Uganda: a test of the ecological constraints model. Behav Ecol Sociobiol. 58:277-288.
22. Ganzhorn JU. 1992. Leaf chemistry and the biomass of folivorous primates in tropical forests. Oecologia. 91:540-547.
23. Glander KE. 1982. The impact of plant secondary compounds on primate feeding behavior. Yearb Phys Anthropol. 25:1-18.
24. Harris TR. 2005. Roaring, intergroup aggression, and feeding competition in black and white colobus monkeys (Colobus guereza) at Kanyawara, Kibale National Park, Uganda [dissertation]. [New Haven (CT)]: Yale University. p. 253.
25. Harris TR. 2006. Evidence for between group contest competition for food in a highly folivorous population of black and white colobus monkeys (Colobus guereza). Behav Ecol Sociobiol. 61:317-329.
26. Harris TR, Caillaud D, Chapman CA, Vigilant L. 2009. Neither genetic nor observational data alone are sufficient for understanding sex-biased dispersal in a social-group-living species. Mol Ecol. 18: 1777-1790.
27. Harris TR, Chapman CA. 2007. Variation in diet and ranging of black and white colobus monkeys in Kibale National Park, Uganda. Primates. 48:208-221.
28. Havel PJ. 2001. Peripheral signals conveying metabolic information to the brain: short-term and long-term regulation of food intake and energy homeostasis. Exp Biol Med. 226:963-977.
29. Hemingway CA, Bynum N. 2005. The influence of seasonality on primate diet and ranging. In: Brockman DK, van Schaik CP, editors. Seasonality in primates. Cambridge: Cambridge University Press. p. 57-104.
30. Ilmonen P, Hakkarainen H, Koivunen V, Korpimaki E, Mullie A, Shutler D. 1999. Parental effort and blood parasitism in Teng-malm's owl: effects of natural and experimental variation in food abundance. Oikos. 86:79-86.
31. Isbell LA. 1991. Contest and scramble competition: patterns of female aggression and ranging behavior among primates. Behav Ecol. 2:143-155.
32. Janson CH. 1998. Testing the predation hypothesis for vertebrate sociality: prospects and pitfalls. Behaviour. 135:389-410.
33. Janson C, Goldsmith ML. 1995. Predicting group size in primates: foraging costs and predation risks. Behav Ecol. 6:326-336.
34. Jarman PJ. 1974. The social organization of antelope in relation to their ecology. Behaviour. 48:215-267.
35. Kasenene J. 1987. The influence of mechanized selective logging, felling intensity and gap-size on the regeneration of a tropical moist forest in the Kibale Forest Reserve, Uganda [dissertation]. East Lansing, Michigan: Michigan State University.
36. Kay RNB, Davies AG. 1994. Digestive physiology. In: Davies AG, Oates JF, editors. Colobine monkeys: their ecology, behaviour and evolution. Cambridge: Cambridge University Press. p. 229-249.
37. Koenig A. 2002. Competition for resources and its behavioral consequences among female primates. Int J Primatol. 23:759-783.
38. Koenig A, Beise J, Chalise MK, Ganzhorn JU. 1998. When females should contest for food 6 testing hypotheses about resource density, distribution, size, and quality with Hanuman langurs (Presbytis entellus). Behav Ecol Sociobiol. 42:225-237.
39. Korstjens AH, Dunbar RIM. 2007. Time constraints limit group sizes and distribution in red and black-and-white colobus. Int J Primatol. 28:551-575.
40. Korstjens AH, Sterck EHM, Noë R. 2002. How adaptive or phyloge-netically inert is primate social behavior? A test with two sympatric colobines. Behaviour. 139:203-225.
41. Macdonald DW. 1983. The ecology of carnivore social behavior. Nature. 301:379-384.
42. Milton K. 1979. Factors influencing leaf choice by howler monkeys: a test of some hypotheses of food selection by generalist herbivores. Am Nat. 114:362-378.
43. Milton K. 1980. The foraging strategy of Howler monkeys: a study in primate economics. New York: Columbia University Press.
44. Mitani JC, Sanders WJ, Lwanga JS, Windfelder TL. 2001. Predatory behavior of crowned hawk-eagles (Stephanoaetus coronatus) in Kibale National Park, Uganda. Behav Ecol Sociobiol. 49:187-195.
45. Oates JF. 1974. The ecology and behaviour of the black-and-white colobus Monkey (Colobus guereza Ruppell) in East Africa [dissertation]. London: University of London.
46. Oates JF. 1977a. The guereza and its food. In: Clutton-Brock TH, editor. Primate ecology: studies of feeding and ranging behavior in lemurs, monkeys, and apes. New York: Academic Press. p. 275-321.
47. Oates JF. 1977b. The social life of a black-and-white colobus monkey, Colobus guereza. Z Tierpsychol. 45:1-60.
48. Oates JF, Davies AG, Delson E. 1994. The diversity of living colobines. In: Davies AG, Oates JF, editors. Colobine monkeys: their ecology, behaviour and evolution. Cambridge: Cambridge University Press. p. 45-73.
49. Pond CM. 1977. The significance of lactation in the evolution of mammals. Evolution. 31:177-199.
50. Rode KD, Chapman CA, Chapman LJ, McDowell LR. 2003. Mineral resource availability and consumption by colobus in Kibale National Park, Uganda. Int J Primatol. 24:541-573.
51. Robbins MM, Robbins AM, Gerald-Steklis N, Steklis HD. 2007. Socio-ecological influences on the reproductive success of female mountain gorillas (Gorilla beringei beringei ). Behav Ecol Sociobiol. 61: 919-931.
52. Saj TL, Marteinson S, Chapman CA, Sicotte P. 2007. Controversy over the application of current socioecological models to folivorous primates: Colobus vellerosus fits the predictions. Am J Phys Anthropol. 133:994-1003.
53. Sherry DS, Ellison PT. 2007. Potential applications of urinary C-peptide of insulin for comparative energetics research. Am J Phys Anthropol. 133:771-778.
54. Sloss MW, Kemp RL, Zajac AM. 1994. Veterinary clinical parasitology. Ames (IA): Iowa State University Press.
55. Snaith TV, Chapman CA. 2005. Towards an ecological solution to the folivore paradox: patch depletion as an indicator of within-group scramble competition in red colobus monkeys (Piliocolobus tephro-sceles). Behav Ecol Sociobiol. 59:185-190.
56. Snaith TV, Chapman CA. 2007. Primate group size and interpreting socioecological models: do folivores really play by different rules? Evol Anthropol. 16:94-106.
57. Snaith TV, Chapman CA. 2008. Red colobus monkeys display alternative behavioral responses to the costs of scramble competition. Be-hav Ecol. 19:1289-1296.
58. Sokal RR, Rohlf FJ. 1995. Biometry. New York: W.H. Freeman and Company.
59. Steenbeek R, van Schaik CP. 2001. Competition and group size in Thomas's langurs (Presbytis thomasi): the folivore paradox revisited. Behav Ecol Sociobiol. 49:100-110.
60. Struhsaker TT. 1975. The red colobus monkey. Chicago: University of Chicago Press.
61. Struhsaker TT. 1997. Ecology of an African rain forest: logging in Kibale and the conflict between conservation and exploitation. Gainesville (FL): University Press of Florida.
62. Struhsaker TT, Leakey M. 1990. Prey selectivity by crowned hawk-eagles on monkeys in the Kibale Forest, Uganda. Behav Ecol Socio-biol. 26:435-443.
63. Struhsaker T, Leland L. 1979. Socioecology of five sympatric monkey species in the Kibale Forest, Uganda. Adv Study Behav. 9:159-228.
64. Struhsaker T, Leland L. 1987. Colobines: infanticide by adult males. In: Smuts BB, Cheney DL, Seyfarth RM, Wrangham RW, Struhsaker TT, editors. Primate societies. Chicago: University of Chicago Press. p. 83-97.
65. Tappen M, Wrangham RW. 2000. Recognizing hominoid-modified bones: the taphonomy of colobus bones partially digested by free-ranging chimpanzees in the Kibale Forest, Uganda. Am J Phys Anthropol. 113:217-234.
66. Taussky HH. 1954. A microcolorimetric determination of creatine in urine by the Jaffe reaction. J Biol Chem. 208:853-861.
67. Teichroeb JA, Sicotte P. 2008. Test of the ecological-constraints model on Ursine colobus monkeys (Colobus vellerosus) in Ghana. Am J Primatol. 70:1-11.
68. van Schaik CP. 1989. The ecology of social relationships amongst female primates. In: Standen V, Foley RA, editors. Comparative socioecology: the behavioral ecology of humans and other mammals. Oxford: Blackwell Scientific. p. 195-218.
69. van Schaik CP, Pfannes KR. 2005. Tropical climates and phenology: a primate perspective. In: Brockman DK, van Schaik CP, editors. Seasonality in primates. Cambridge: Cambridge University Press. p. 23-54.
70. 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.
71. Watts DP, Mitani JC. 2002. Hunting behavior of chimpanzees at Ngogo, Kibale National Park, Uganda. Int J Primatol. 23:1-28.
72. Wing LD, Buss IO. 1970. Elephants and forests. Wildl Monogr. 19:3-92.
73. Wrangham RW. 1980. An ecological model of female-bonded primate groups. Behaviour. 75:262-299.