experiencia laboral
35. Operación y mantenimiento
Our research in Kibale is ongoing, and we hope that we can make contributions both to conservation biology and to the theoretical fi elds of population biology and behavioral ecology. In general, our research into ecological determinants of folivore abundance provides support for the notion that the protein-to-fi ber ratio is a good predictor of food choice in colobines, but only partially supports the use of this index in predicting colobine biomass. The documentation of the role of parasites adds depth to our understanding of variation in primate abundance. As we have previously demonstrated that human modifi cations to landscapes can alter interac-tions between parasites and hosts (Chapman et al. 2005 ; Gillespie et al. 2005 ), this raises the intriguing question of what types of anthropogenic disturbances will lead to disease playing a more signifi cant role in determining primate population size. In the future, between-site comparisons should be carefully conducted to explore the effects of specifi c anthropogenic disturbances (e.g., forest fragmentation with or without elevated rates of human contact), because the focus has now shifted from whether anthropogenic habitat change alters primate–disease interactions to how anthropogenic change alters primate–disease interactions. Finally, if food competi-tion proves to be biologically signifi cant for folivores, our interpretacompeti-tions of primate behavior will need to be refi ned, and current theoretical models of primate social organization may need revision (see Snaith and Chapman 2007 ).
Perhaps the biggest gap in our understanding of folivore abundance and social organization stems from the fact that most socioecological studies conducted to date are based at the group level, and it has not been possible to examine individual strat-egies (but see Koenig et al. 1998 ; Koenig 2002 ). Furthermore, we are missing the critical connection between individual attributes (such as dominance, nutritional status, physiological stress, and parasite burden), and how they affect components of fi tness (such as survival probability and reproduction). For example, it would be very useful to assess individual differences in feeding effi ciency between groups of different sizes. Although direct measures of reproductive success would be ideal, differences in feeding effi ciency may be a suffi cient proxy and may help shed light on the costs of grouping in folivores. Following the predictions of the ecological constraints model (Chapman and Chapman 2000b ), females in larger groups should have lower caloric intake, consume foods of lower quality (particularly foods with lower protein-to-fi ber ratios), have longer day ranges (after controlling for
environmental conditions), and be in inferior physical condition relative to females in smaller groups, all else being equal. If the model is correct in linking group size and feeding effi ciency, not all females are expected to achieve their full reproductive potential and this may impact dispersal decisions. Our studies suggest that the eco-logical setting in which a primate population fi nds itself can strongly infl uence both its abundance and its social structure. We believe that the most exciting and interest-ing developments still await us as we come to understand how ecological variables determine individual strategies affecting the behavior and ecology of folivores.
Acknowledgments Funding for this research was provided by the Canada Research Chairs Program, Wildlife Conservation Society (WCS), Natural Science and Engineering Research Council (NSERC) Canada, and the National Science Foundation (NSF), U.S.A. (SBR- 990899).
J.F.G. was supported by a Graduate Research Fellowship from the National Science Foundation, the Canadian Institutes of Health Research’s Systems Biology Training Program, an Explorers Club–Eddie Bauer Youth Grant, and a Quebec Centre for Biodiversity Science Excellence Award.
Permission to conduct this research was given by the Offi ce of the President, Uganda, the National Council for Science and Technology, and the Uganda Wildlife Authority. Many people provided assistance or helpful comments on this research, including Lauren Chapman, Karen Bjorndal, Tom Gillespie, Ellis Greiner, Daphne Onderdonk, Mike Huffman, Mike Wasserman, and Toni Zeigler.
Ellis Greiner aided in parasite identifi cation.
References
Bell FR (1995) Perception of sodium appetite in farm animals. In: Phillips CJC, Chiy PC (eds) Sodium in agriculture. Chalcombe, Canterbury, pp 82–90
Bercovitch FB, Ziegler TE (2002) Current topics in primate socioendocrinology. Annu Rev Anthropol 31:45–67
Boesch C (1996) Social grouping in Tai chimpanzees. In: McGrew WC, Marchant LF, Nishida T (eds) Great ape societies. Cambridge University Press, Cambridge, pp 101–113
Boonstra R, Singleton GR (1993) Population declines in the snowshoe hare and the role of stress.
Gen Comp Endocrinol 91:126–143
Boutin S (1990) Food supplementation experiments with terrestrial vertebrates: patterns, prob-lems, and the future. Can J Zool 68:203–220
Butynski TM (1990) Comparative ecology of blue monkeys ( Cercopithecus mitis ) in high- and low-density sub-populations. Ecol Monogr 60:1–26
Camm JD, Norman SK, Polasky S, Solow AR (2002) Nature reserve site selection to maximize expected species covered. Oper Res 50:946–955
Chapman CA (1988) Patch use and patch depletion by the spider and howling monkeys of Santa Rosa National Park, Costa Rica. Behav Ecol 105:99–116
Chapman CA (1990) Association patterns of spider monkeys: the infl uence of ecology and sex on social organization. Behav Ecol Sociobiol 26:409–414
Chapman CA, Chapman LJ (1999) Implications of small scale variation in ecological conditions for the diet and density of red colobus monkeys. Primates 40:215–231
Chapman CA, Chapman LJ (2000a) Constraints on group size in red colobus and red-tailed guenons: examining the generality of the ecological constraints model. Int J Primatol 21:565–585
Chapman CA, Chapman LJ (2000b) Determinants of group size in primates: the importance of travel costs. In: Boinski S, Garber PA (eds) On the move: how and why animals travel in groups. University of Chicago Press, Chicago, pp 24–41
Chapman CA, Chapman LJ (2002) Foraging challenges of red colobus monkeys: infl uence of nutrients and secondary compounds. Comp Biochem Physiol A Physiol 133:861–875 Chapman CA, Fedigan LM (1990) Dietary differences between neighboring cebus monkey groups:
local traditions or responses to food availability? Folia Primatol (Basel) 54:177–186 Chapman CA, Gogarten JF (2012) Primate conservation: is the cup half empty or half full? Nature
Educ Knowl 3:7
Chapman CA, Lambert JE (2000) Habitat alterations and the conservation of African primates:
a case study of Kibale National Park, Uganda. Am J Primatol 50:169–186
Chapman CA, Peres CA (2001) Primate conservation in the new millennium: the role of scientists.
Evol Anthropol 10:16–33
Chapman CA, Wrangham RW, Chapman LJ (1995) Ecological constraints on group size: an analy-sis of spider monkey and chimpanzee subgroups. Behav Ecol Sociobiol 36:59–70
Chapman CA, Chapman LJ, Bjorndal KA, Onderdonk DA (2002a) Application of protein-to-fi ber ratios to predict colobine abundance on difference spatial scales. Int J Primatol 23:283–310 Chapman CA, Chapman LJ, Bjorndal KA, Onderdonk DA (2002b) Application of protein-to-fi ber
ratios to predict colobine abundance on different spatial scales. Int J Primatol 23:283–310 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 Chapman CA, Speirs ML, Gillespie TR, Holland T, Austad K (2005) Life on the edge:
gastrointes-tinal parasites from forest edge and interior primate groups. Am J Primatol 68:1–12
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
Chapman CA, Naughton-Treves L, Lawes MJ, Wasserman MD, Gillespie TR (2007) The conser-vation value of forest fragments: explanations for population declines of the colobus of western Uganda. Int J Primatol 23:513–578
Chapman CA, Struhsaker TT, Skorupa JP, Snaith TV, Rothman JM (2010) Understanding long- term primate community dynamics: implications of forest change. Ecol Appl 20:179–191 Chivers DJ, Hladik CM (1980) Morphology of the gastrointestinal tract in primates: comparisons
with other mammals in relation to diet. J Morphol 166:337–386
Clutton-Brock TH, Harvey PH (1977) Primate ecology and social organization. J Zool 183:1–39 Coley P (1983) Herbivory and defensive characteristics of tree species in a lowland tropical forest.
Ecol Monogr 53:209–233
Coop RL, Holmes PH (1996) Nutrition and parasite interaction. Int J Parasitol 26:951–962 Creel S (2001) Social dominance and stress hormones. Trends Ecol Evol 16:491–497
Creel S, Fox JE, Hardy J, Sands B, Garrot B, Peterson RO (2002) Snowmobile activity and gluco-corticoid stress responses in wolves and elk. Conserv Biol 16:809–814
Crockett CM, Janson CH (2000) Infanticide in red howlers: female group size, group composition, and a possible link to folivory. In: van Schaik CP, Janson CH (eds) Infanticide by males and its implications. Cambridge University Press, Cambridge, pp 75–98
Crompton DWT (1991) Nutritional interactions between hosts and parasites. In: Toft CA, Aeschlimann A, Bolis L (eds) Parasite–host associations: coexistence of confl ict. Oxford University Press, Oxford, pp 228–257
DaSilva GL (1992) The western black and white colobus as a low energy strategist: activity bud-get, energy expenditure and energy intake. J Anim Ecol 61:79–91
Davies AG (1994) Colobine populations. In: Davies AG, Oates JF (eds) Colobine monkeys. Their ecology, behaviour and evolution. Cambridge University Press, Cambridge, pp 285–310 Eisenberg JF, Muckenhirn NA, Rudran R (1972) The relation between ecology and social structure
in primates. Science 176:863–874
Fashing PJ, Dierenfeld E, Mowry CB (2007) Infl uence of plant and soil chemistry on food selec-tion, ranging patterns, and biomass of Colobus guereza in Kakamega Forest, Kenya. Int J Primatol 28:673–703
Fearer TM, Prisley SP, Stauffer DF, Keyser PD (2007) A method for integrating the Breeding Bird Survey and Forest Inventory and Analysis databases to evaluate forest bird–habitat relation-ships at multiple spatial scales. For Ecol Manag 243:128–143
Fimbel C, Vedder A, Dierenfeld E, Mulindahabi F (2001) An ecological basis for large group size in Colobus angolensis in the Nyungwe Forest, Rwanda. Afr J Ecol 39:83–92
Ganzhorn JU (2002) Distribution of a folivorous lemur in relation to seasonally varying food resources: integrating quantitative and qualitative aspects of food characteristics. Oecologia (Berl) 131:427–435
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
Gillespie TR, Chapman CA, Greiner EC (2005) Effects of logging on gastrointestinal parasite infections and infection risk in African primates. J Appl Ecol 42:699–707
Gogarten JF, Bonnell TR, Campenni M, Wasserman MD, Chapman CA (in review-a) Increasing group size alters behavior of a folivorous primate
Gogarten JF, Jacob AL, Ghai RR, Rothman JM, Twinomugisha D, Wasserman MD, Chapman CA (in review-b) Causes and consequences of changing group sizes in a primate community over 15+ years
Gogarten JF, Brown LM, Chapman CA, Marina C, Doran-Sheehy D, Fedigan LM, Grine FE, Perry S, Pusey AE, Sterck EHM, Wich SA, Wright PC (2012a) Seasonal mortality patterns in non- human primates: implications for variation in selection pressures across environments.
Evolution 66:3256–3266
Gogarten JF, Guzman M, Chapman CA, Jacob AL, Omeja PA, Rothman JM (2012b) What is the predictive power of the colobine protein-to-fi ber model and its conservation value? Trop Conserv Sci 5:381–393
Goldberg TL, Chapman CA, Cameron K, Saj S, Karesh W, Wolfe N, Wong SW, Dubois ME, Slifka MK (2008) Serologic evidence for a novel poxvirus in endangered red colobus monkeys.
Emerg Infect Dis 14:801–803
Goldberg TL, Sintasath DM, Chapman CA, Cameron KM, Karesh WB, Tang S, Wolfe ND, Rwego IB, Ting N, Switzer WM (2009) Co-infection of Ugandan red colobus ( Procolobus [ Piliocolobus ] rufomitratus tephrosceles ) with novel, divergent delta-, lenti-, and spumaretro-viruses. J Virol 83:11318–11329
Gulland FMD (1992) The role of nematode parasites in Soay sheep ( Ovis aries L.) mortality dur-ing a population crash. Parasitol Res 105:493–503
Harris TR (2005) Roaring, intergroup aggression, and feeding competition in black and white colobus monkeys ( Colobus guereza ) at Kanyawara, Kibale National Park, Uganda. Yale University, New Haven
Harris TR, Chapman CA, Monfort SL (2010) Small folivorous primate groups exhibit behavioral and physiological effects of food scarcity. Behav Ecol 21:46–56
Holmes JC (1995) Population regulation: a dynamic complex of interactions. Wildl Res 22:11–20
Hudson PJ, Dobson AP, Newborn D (1992) Do parasites make prey vulnerable to predation: red grouse and parasites. J Anim Ecol 61:681–692
Isbell LA (1991) Contest and scramble competition: patterns of female aggression and ranging behaviour among primates. Behav Ecol 2:143–155
Isbell LA, Young TP (2002) Ecological models of female social relationships in primates: similari-ties, disparities and some directions for future clarity. Behaviour 139:177–202
Janson CH, Goldsmith ML (1995) Predicting group size in primates: foraging costs and predation risks. Behav Ecol 6:326–336
Janson CH, van Schaik CP (1988) Recognizing the many faces of primate food competition:
methods. Behaviour 105:165–186
Kingsolver JG, Schemske DW (1991) Path analysis of selection. Trends Ecol Evol 6:276–280 Koenig A (2000) Competitive regimes in forest-dwelling hanuman langur females ( Semnopithecus
entellus ). Behav Ecol Sociobiol 48:93–109
Koenig A (2002) Competition for resources and its behavioral consequences among female pri-mates. Int J Primatol 23:759–783
Koenig A, Borries C (2002) Feeding competition and infanticide constrain group size in wild hanuman langurs. Am J Primatol 57:33–34
Koenig A, Beise J, Chalise MK, Ganzhorn JU (1998) When females should contest for food: test-ing hypotheses about resource density, distribution, size and quality with hanuman langurs ( Presbytis entellus ). Behav Ecol Sociobiol 42:225–237
Korstjens AH, Sterck EHM, Noe R (2002) How adaptive or phylogenetically inert is primate social behaviour? A test with two sympatric colobines. Behaviour 139:203–225
Kristan WB (2007) Expected effects of correlated habitat variables on habitat quality and bird distribution. Condor 109:505–515
Lee PY, Rotenberry JT (2005) Relationships between bird species and tree species assemblages in forested habitats of eastern North America. J Biogeogr 32:1139–1150
McDowell LR (1992) Minerals in animal and human nutrition. Academic Press, New York McKey DB, Gartlan JS, Waterman PG, Choo GM (1981) Food selection by black colobus
mon-keys ( Colobus satanas ) in relation to plant chemistry. Biol J Linn Soc 16:115–146
McNab BK (2002) The physiological ecology of vertebrates: a view from energetics. Cornell University Press, Cornell
Milton K (1979) Factors infl uencing leaf choice by howler monkeys: a test of some hypotheses of food selection by generalist herbivores. Am Nat 114:363–378
Milton K (1996) Effects of bot fl y ( Alouattamyia baeri ) parasitism on a free-ranging howler ( Alouatta palliata ) population in Panama. J Zool Soc Lond 239:39–63
Miyamoto MM, Allen JA, Ting N, Gogarten JF, Chapman CA (in press) Microsatellite DNA dem-onstrates different levels of genetic structure in two, unequally sized, neighboring groups of red colobus monkeys. Am J Primatol 75:478–490
Munger JC, Karasov WH (1989) Sublethal parasites and host energy budgets: tapeworm infection in white-footed mice. Ecology 70:904–921
Nunn CL (2011) The comparative approach in evolutionary anthropology and biology. University of Chicago Press, Chicago
Oates JF (1994) The natural history of African colobines. In: Davies AG, Oates JF (eds) Colobine monkeys: their ecology, behaviour and evolution. Cambridge University Press, Cambridge Oates JF, Davies AG (1994) What are the colobines. In: Oates JF, Davies AG (eds) Colobine
mon-keys: their ecology, behaviour and evolution. Cambridge University Press, Cambridge, pp 1–10 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
Omeja PA, Chapman CA, Obua J (2009) Enrichment planting does not promote native tropical tree restoration in a former pine plantation. Afr J Ecol 47:650–657
Robbins CT (1993) Wildlife feeding and nutrition. Academic, New York
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 Rothman JM, Chapman CA, van Soest PJ (2012) Methods in primate nutritional ecology: a user’s
guide. Int J Primatol 33:542–566
Sapolsky RM (1992) Neuroendocrinology of the stress-response. In: Becker JB, Breedlove SM, Crews D (eds) Behavioral endocrinology. MIT, Cambridge, pp 287–566
Siex K, Struhsaker TT (1999) Ecology of the Zanzibar red colobus monkey: demography variabil-ity and habitat stabilvariabil-ity. Int J Primatol 20:163–192
Skorupa JP (1988) The effect of selective timber harvesting on rain forest primates in Kibale Forest, Uganda. PhD Thesis, University of California, Davis
Smith WH (1976) Character and signifi cance of forest tree root exudates. Ecology 57:324–331 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 59:185–190
Snaith TV, Chapman CA (2007) Primate group size and socioecological models: do folivores really play by different rules? Evol Anthropol 16:94–106
Snaith TV, Chapman CA (2008) Red colobus monkeys display alternative behavioural responses to the costs of scramble competition. Behav Ecol 19:1289–1296
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
Sterck EHM, Watts DP, van Schaik CP (1997) The evolution of female social relationships in nonhuman primates. Behav Ecol Sociobiol 41:291–309
Struhsaker TT (1975) The red colobus monkey. University of Chicago Press, Chicago
Struhsaker TT (1997) Ecology of an African rain forest: logging in Kibale and the confl ict between conservation and exploitation. University of Florida Press, Gainesville
Struhsaker TT (2000) Variation in adult sex ratios of red colobus monkey social groups: implica-tions for interspecifi c comparisons. In: Kappeler PM (ed) Primate males: causes and conse-quences of variation in group composition. Cambridge University Press, Cambridge, pp 108–119
Struhsaker T (2008a) Procolobus rufomitratus ssp. tephrosceles . IUCN 2010 IUCN Red List of Threatened Species, Version 20104
Struhsaker TT (2008b) Demographic variability in monkeys: implication for theory and conserva-tion. Int J Primatol 28:19–34
Struhsaker TT (2010) The red colobus monkeys: variation in demography, behavior, and ecology of endangered species. Oxford University Press, Oxford
Struhsaker TT, Leland L (1987) Colobines: infanticide by adult males. In: Smuts BB, Cheney DL, Seyfarth RM, Wrangham RW, Struhsaker TT (eds) Primate societies. University of Chicago Press, Chicago, pp 83–97
Struhsaker TT, Marshall AR, Detwiler K, Siex K, Ehardt C, Lisbjerg DD, Butynski TM (2004) Demographic variation among Udzungwa red colobus in relation to gross ecological and socio-logical parameters. Int J Primatol 25:615–658
Terborgh J, Janson CH (1986) The socioecology of primate groups. Annu Rev Ecol Syst 17:111–135
van Schaik CP (1983) Why are diurnal primates living in groups? Behaviour 87:120–144 van Schaik CP (1999) The socioecology of fi ssion–fusion sociality in orangutans. Primates
40:69–86
van Schaik CP, van Hooff JARAM (1983) On the ultimate causes of primate social systems.
Behaviour 85:91–117
Van Soest PJ (1994) Nutritional ecology of the ruminant. Cornell University Press, Ithaca Wasser SK, Bevis K, King G, Hanson E (1997) Noninvasive physiological measures of disturbance
in the northern spotted owl. Conserv Biol 11:1019–1022
Wasserman MD, Chapman CA (2003) Determinants of colobine monkey abundance: the impor-tance of food energy, protein and fi bre content. J Anim Ecol 72:650–659
Waterman PG, Ross JAM, Bennett EL, Davies AG (1988) A comparison of the fl oristics and leaf chemistry of the tree fl ora in two Malaysian rain forests and the infl uence of leaf chemistry on populations of colobine monkeys in the Old World. Biol J Linn Soc 34:1–32
Wrangham RW (1980) An ecological model of female-bonded primate groups. Behaviour 75:262–300
Wrangham RW (2000) Why are male chimpanzees more gregarious than mothers? A scramble competition hypothesis. In: Kappeler PM (ed) Primate males: causes and consequences of variation in group composition. Cambridge University Press, Cambridge, pp 248–258 Wursig B, Wursig M (1979) Behaviour and ecology of the bottlenose dolphin, Tursiops truncatus ,
in the South Atlantic. Fish Bull 77:399–412
Yeager CP, Kirkpatrick CR (1998) Asian colobine social structure: ecological and evolutionary constraints. Primates 39:147–155
Yeager CP, Kool K (2000) The behavioral ecology of Asian colobines. In: Whitehead PF, Jolly CJ (eds) Old World monkeys. Cambridge University Press, Cambridge, pp 496–521
25