Temporal dynamics of nutrition, parasitism, and stress in colobus monkeys: Implications for population regulation and conservation

American Journal of Physical Anthropology

Volumn 134, Issue 2, 2007, Pages 240-250

  Chapman, Colin A ^a,b,c   Saj, Tania L ^a   Snaith, Tamaini V ^a  

^a MCGILL UNIVERSITY   (Canada)

^b WILDLIFE CONSERVATION SOCIETY   (United States)

^c MCGILL UNIVERSITY   (Canada)

Author keywords

Colobus; Cortisol; Kibale national park; Parasitism; Population regulation; Primate conservation; Within group competition

Indexed keywords

HYDROCORTISONE;

ARTICLE; COLOBINAE; CONSERVATION BIOLOGY; DIETARY INTAKE; FERTILITY; FOOD QUALITY; MONKEY; MORTALITY; NONHUMAN; NUTRITION; PARASITISM; PARASITOSIS; POPULATION BIOLOGY; POPULATION DENSITY; POPULATION DYNAMICS; STRESS; UGANDA;

ANIMAL NUTRITION PHYSIOLOGY; ANIMALS; COLOBUS; CONSERVATION OF NATURAL RESOURCES; DIET; FEEDING BEHAVIOR; FEMALE; HYDROCORTISONE; MALE; POPULATION DENSITY; POPULATION DYNAMICS; STRESS;

EID: 34548800764     PISSN: 00029483     EISSN: 10968644     Source Type: Journal    
DOI: 10.1002/ajpa.20664     Document Type: Article

References (87)

1. Abbott DH, Keverne EB, Bercovitch FB, Shipley CA, Mendoza SP, Saltzman W, Snowdon CT, Ziegler TE, Banjevic E, Garland T, Sapolsky RM. 2003. Are suborbinates always stressed? A comparative analysis of rank differences in Cortisol levels among primates. Horm Behav 43:67-82.
2. Bercovitch FB, Clarke AS. 1995. Dominance ranks, cortisol concentrations, and reproductive maturation in male rhesus macaques. Physiol Behav 58:215-221.
3. Bercovitch FB, Ziegler TE. 2002. Current topics in primate socioendrocrinology. Ann Rev Anthropol 31:45-67.
4. Blanchard DC, Spencer RL, Weiss SM, Blanchard RJ, McEwan B, Sakai RR. 1995. Visible burrow system as a model of chronic social stress: behavioral and neuroendocrine correlates. Psychoneuroendocrinology 20:117-134.
5. Boonstra R, Singleton GR. 1993. Population declines in the snowshoe hare and the role of stress. Gen Comp Endocrinol 91:126-143.
6. Chapman CA, Chapman LJ. 2002. Foraging challenges of red colobus monkeys: influence of nutrients and secondary compounds. Comp Biochem Physiol A Physiol 133:861-875.
7. Chapman CA, Chapman LJ, Bjorndal KA, Onderdonk DA. 2002. Application of protein-to-fiber ratios to predict colobine abundance on difference spatial scales. Int J Primatol 23:283-310.
8. 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.
9. Chapman CA, Peres CA. 2001. Primate conservation in the new millennium: the role of scientists. Evol Anthropol 10:16-33.
10. Chapman CA, Rothman JM, Hodder SAM. Can parasites limit primate group size? A test with red colobus. In: Huffman MA, Chapman CA, editors. Primate parasite ecology: the dynamics and study of host-parasite relationships. Cambridge: Cambridge University Press (in press).
11. Chapman CA, Speirs ML, Gillespie TR, Holland T, Austad K. 2005. Life on the edge: gastrointestinal parasites from forest edge and interior primate groups. Am J Primatol 68:1-12.
12. Chapman CA, Wasserman MD, Gillespie TR, Speirs ML, Lawes MJ, Saj TL, Ziegler TE. 2006. Do nutrition, parasitism, and stress have synergistic effects on red colobus populations living in forest fragments? Am J Phys Anthropol 131:525-534.
13. Collias N, Southwick C. 1952. A field study of population density and social organization in howling monkeys. Proc Natl Acad Sci USA 96:143-156.
14. Coop RL, Holmes PH. 1996. Nutrition and parasite interaction. Int J Parasitol. 26:951-962.
15. Cote IM, Poulin R. 1995. Parasitism and group size in social animals: a meta-analysis. Behav Ecol 6:159-165.
16. Creel S, Fox JE, Hardy J, Sands B, Garrot B, Peterson RO. 2002. Snowmobile activity and glucocorticoid stress responses in wolves and elk. Conserv Biol 16:809-814.
17. Despommier DD, Gwazda RW, Hotez PJ. 1995. Parasitic diseases. New York: Springer-Verlag.
18. Dunbar RIM. 1987. Habitat quality, population dynamics and group composition in colobus monkeys (Colobus guereza). Int J Primatol 8:299-322.
19. Ezenwa VO. 2003. Habitat overlap and gastrointestinal parasitism in sympatric African bovids. Parasitology 126:379-388.
20. Ezenwa VO. 2004. Host social behavior and parasitic infection: a multifactorial approach. Behav Ecol 15:446-454.
21. Feigler F, Anger V. 1966. Replacement of bensidine by copper ethylacetoacetate and tetra-base as spot-test reagent for hydrogen cyanide and cyanogens. Analyst 91:282-284.
22. Ferin M. 1999. Stress and the reproductive cycle. J Clin Endocrinol Metab 84:1768-1774.
23. Foley CAH, Papageorge S, Wasser SK. 2001. Noninvasive stress and reproductive measures of social and ecological pressures in free-ranging African elephants. Conserv Biol 15:1134-1142.
24. Freeland WJ. 1979. Primate social groups as biological islands. Ecology 60:719-728.
25. Gallaher R, Weldon C, Futral JG. 1975. An aluminum block digester for plant and soil analysis. Soil Sci Soc Am Proc 39:803-806.
26. Ganzhorn JU. 1992. Leaf chemistry and the biomass of folivorous primates in tropical forests: tests of a hypothesis. Oecologia 91:540-547.
27. Ganzhorn JU. 2002. Distribution of a folivorous lemur in relation to seasonally varying food resources: integrating quantitative and qualitative aspects of food characteristics. Oecologia 131:427-435.
28. Gatti S, Swiercynski G, Robinson F, Anselmi M, Corrales J, Moreira J, Montalvo G, Bruno A, Maserati F, Bisoffi Z, Scaglia M. 2002. Amoebic infections due to the Entamoeba histolytica-Entamoeba dispar complex: a study of the incidence in a remote rural area of Ecuador. Am J Trop Med Hyg 67:123-127.
29. Gesquiere LR, Altmann J, Khan MZ, Couret J, Yu JC, Endres CS, Lynch JW, Ogola P, Fox EA, Alberts SC, Wango EO. 2005. Coming of age: steroid hormones of wild immature baboons (Papio cynocephalus). Am J Primatol 67:83-100.
30. Gillespie TR, Chapman CA. 2001. Determinants of group size in the red colobus monkey (Procolobus badius): an evaluation of the generality of the ecological-constraints model. Behav Ecol Sociobiol 50:329-338.
31. Gillespie TR, Chapman CA, Greiner EC. 2005a. Effects of logging on gastrointestinal parasite infections and infection risk in African primates. J Appl Ecol 42:699-707.
32. Gillespie TR, Greiner EC, Chapman CA. 2005b. Gastrointestinal parasites of the colobus monkeys of Uganda. J Parasitol 91:569-573.
33. Gulland FMD. 1992. The role of nematode parasites in Soay sheep (Ovis aries L.) mortality during a population crash. Parasitol Res 105:493-503.
34. Hadley ME. 1996. Endocrinology. Upper Saddle River: Prentice Hall.
35. Harris TR 2005. Roaring, intergroup aggression, and feeding competition in black and white colobus monkeys (Colobus guereza) at Kanyawara, Kibale National Park, Uganda. New Haven: Yale University.
36. Holmes JC. 1995. Population regulation: a dynamic complex of interactions. Wild Res 22:11-20.
37. Horowitz W. 1970. Official methods of analysis of the Association of Official Analytical Chemists, 11th ed. Washington, DC: AOAC.
38. Hoste H, Jackson F, Athanasiadou S, Thamsborg SM, Hoskin SO. 2006. The effects of tannin-rich plants on parasitic nematodes in ruminants. Trends Parasitol 22:253-261.
39. Hudson PJ. 1986. The effect of a parasitic nematode on the breeding population of red grouse. J Anim Ecol 55:85-92.
40. Hudson PJ, Dobson AP, Newborn D. 1992. Do parasites make prey vulnerable to predation: red grouse and parasites. J Anim Ecol 61:681-692.
41. Huffman MA, Gotoh S, Turner LA, Hamai M, Yoshida K. 1997. Seasonal trends in intestinal nematode infection and medicinal plant use among chimpanzees in the Mahale Mountains, Tanzania. Primates 38:111-125.
42. Ilmonen P, Taarna T, Hasselquist D. 2000. Experimentally activated immune defense in female pied flycatchers results in reduced breeding success. Proc R Soc Lond 267:665-670.
43. Isbell LA. 1991. Contest and scramble competition: patterns of female aggression and ranging behaviour among primates. Behav Ecol 2:143-155.
44. Kaplan JE, Hu DU, Holmes KK, Jaffe HW, Masur H, Cock KM. 1996. Preventing opportunistic infections in human immunodeficiency virus-infected persons: implications for the developing world. Am J Trop Med Hyg 55:1-11.
45. Kingsolver JG, Schemske DW. 1991. Path analysis of selection. Trends Ecol Evol 6:276-280.
46. Koenig A. 2000. Competitive regimes in forest-dwelling Hanuman langur females (Semnopithecus entellus). Behav Ecol Sociobiol 48:93-109.
47. Koenig A, Borries C. 2002. Feeding competition and infanticide constrain group size in wild Hanuman langurs. Am J Primatol 57:33-34.
48. Milton K. 1979. Factors influencing leaf choice by howler monkeys: a test of some hypotheses of food selection by generalist herbivores. Am Nat 114:363-378.
49. Milton K. 1996. Effects of bot fly (Alouattamyia baeri) parasitism on a free-ranging howler (Alouatta palliata) population in Panama. J Zool Soc Lond 239:39-63.
50. Min BR, Hart SP. 2003. Tannins for suppression of internal parasites. J Anim Sci 81:102-109.
51. Moberg GP. 1985. Influence of stress on reproduction: measure of well-being. In: Moberg GP, editor. Animal stress. Bethesda, Maryland: American Physiological Society. p 245-267.
52. Muehlenbein MP. 2006. Intestinal parasite infections and fecal steroid levels in wild chimpanzees. Am J Phys Anthropol 130:546-550.
53. Munck A, Guyne P, Holbrook N. 1984. Physiological functions of glucocorticoids in stress and their relation to pharmacological action. Endocr Rev 5:25-44.
54. Munger JC, Karasov WH. 1989. Subleathal parasites and host energy budgets: tapeworm infection in white-footed mice. Ecology 70:904-921.
55. Munger JC, Karasov WH. 1994. Costs of bot-fly infection n white-footed mice: energy and mass flow. Can J Zool 72:166-176.
56. Murray DL, Keith LB, Cary JR. 1998. Do parasitism and nutritional status interact to affect production in snowshoe hares? Ecology 79:1209-1222.
57. Nunn CL, Altizer S. 2006. Infectious diseases in primates: behavior, ecology and evolution. Oxford: Oxford University Press.
58. Oates JF. 1996. Habitat alteration, hunting, and the conservation of folivorous primates in African forests. Aust J Ecol 21:1-9.
59. Oates JF, Whitesides GH, Davies AG, Waterman PG, Green SM, DaSilva GL, Mole S. 1990. Determinants of variation in tropical forest primate biomass: new evidence from West Africa. Ecology 71:328-343.
60. Parraga IM, Assis AO, Parado MS. 1996. Gender differences in growth of school-aged children with schistosomiasis and geohelminth infection. Am J Trop Med Hyg 55:150-156.
61. Pollard TM. 1995. Use of cortisol as a stress marker: practical and theoretical problems. Am J Human Biol 7:267-274.
62. Poulin R. 1991. Group-living and the richness of the parasite fauna in Canadian freshwater fishes. Oecologia 86:390-394.
63. Pride RE. 2005a. Foraging success, agonism, and predator alarms: behavioral predictors of Cortisol in Lemur catta. Int J Primatol 26:295-319.
64. Pride RE. 2005b. High faecal glucocorticoid levels predict mortality in ring-tailed lemurs (Lemur catta). Biol Lett 1:60-63.
65. Pride RE. 2005c. Optimal group size and seasonal stress in ring-tailed lemurs (Lemur catta). Behav Ecol 16:550-560.
66. Robbins CT. 1993. Wildlife feeding and nutrition. New York: Academic Press.
67. Romero LM, Wikelski M. 2001. Corticosterone levels predict survival probabilities of Galapagos marine iguanas during El Nino events. Proc Natl Acad Sci 98:7366-7370.
68. Saj TL, Marteinson S, Chapman CA, Sicotte P. Controversy over the application of current socioecological model to folivorous primates: Colobus vellerosus fits the predictions. Am J Phys Anthropol (in press).
69. Saj TL, Sicotte P. Scramble competition in Colobus vellerosus at Biabeng-Fiema, Ghana. Int J Primatol (in press).
70. Sapolsky RM. 1992. Neuroendocrinology of the stress-response. In: Becker JB, Breedlove SM, Crews D, editors. Behavioral Endocrinology. Cambridge, MA: MIT. p 287-566.
71. Shipley B. 1999. Testing causal explanations in organismal biology: causation, correlation and structural equation modeling. Oikos 86:374-382.
72. Sloss MW, Kemp RL, Zajac AM. 1994. Veterinary clinical parasitology. Ames: Iowa State University Press.
73. 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. Behav Ecol Sociobiol 25:185-190.
74. Snaith TV, Chapman CA. Primate group size and socioecological models: do folivores really play by different rules? Evol Anthropol (in press).
75. Solomons NW, Scott ME. 1994. Nutrition status of host populations influences parasitic infections. In: Scott ME, Smith G, editors. Parasitic and infectious diseases. New York: Academic Press. p 101-114.
76. Sousa MBC, Ziegler TE. 1998. Diurnal variation on the excretion patterns of fecal steroids in common marmoset (Callithrix jacchus) females. Am J Primatol 46:105-117.
77. Sterck EHM, Watts DP, van Schaik CP. 1997. The evolution of female social relationships in nonhuman primates. Behav Ecol Sociobiol 41:291-309.
78. Struhsaker TT. 1975. The red colobus monkey. Chicago: University of Chicago Press.
79. Struhsaker TT. 1976. A further decline in numbers of Amboseli vervet monkeys. Biotropica 8:211-214.
80. Struhsaker TT, Pope TR. 1991. Mating system and reproductive success - a comparison of 2 African forest monkeys (Colobus badius and Cercopithecus ascanius). Behaviour 117:182-205.
81. van Soest P. 1963. Use of detergents in the analysis of fibrous feeds. II. A rapid method for the determination of fiber and lignin. J Assoc Off Agric Chem 46:829-835.
82. Vitone ND, Altizer S, Nunn CL. 2004. Body size, diet and sociality influence the species richness of parasitic worms in anthropoid primates. Evol Ecol Res 6:183-189.
83. Wasser SK, Bevis K, King G, Hanson E. 1997. Noninvasive physiological measures of disturbance in Northern spotted owl. Conserv Biol 11:1019-1022.
84. Waterman PG. 1993. Methods in plant biochemistry, Vol. 8. New York: Academic Press.
85. Waterman PG, Ross JAM, Bennet EL, Davies AG. 1988. A comparison of the floristics and leaf chemistry of the tree flora in two Malaysian rain forests and the influence of leaf chemistry on populations of colobine monkeys in the Old World. Biol J Linn Soc 34:1-32.
86. Wrangham RW. 1980. An ecological model of female-bonded primate groups. Behaviour 75:262-300.
87. Ziegler TE, Scheffler G, Snowdon CT. 1995. The relationship of cortisol levels to social environment and reproductive functioning in female cotton-top tamarins. Saguinus oedipus. Horm Behav 29:407-424.