Abstract
Howler monkeys, genus Alouatta, are recognized as one of the most resistant primates to forest fragmentation. In this study a comparison of the home range, activity and diet of red howler monkeys (A. seniculus) was made between a continuous forest and a fragment in Meta, Colombia (Tinigua Park and Santa Rosa farm, respectively). Data was gathered on focal animals for 4-5 days per month, over 13 months in the continuous forest, and for six months in a 21-ha fragment. Home range areas were larger in the continuous forest. Resting was the most frequent activity in both places (58-59%), but individuals in the continuous forest moved more than those in the fragment (15 vs. 9%). In contrast, feeding was less frequent in the continuous forest (23 vs. 31%). Consumption of leaves was higher in the fragment (67%) than in the continuous forest (56%), contrasting with the pattern found for ripe fruit consumption (fragment: 32%, continuous forest: 44%). Results from phenological transects indicate that fruits were consumed in proportion to their abundance; however, the same was not true for young leaves. Due to increased production and tree species diversity, the number of fruit species consumed in the continuous forest was greater than in the fragment. No differences were found in feeding rates among group members, suggesting an egalitarian society in terms of resource acquisition. Results from this study show that fragmentation affects home range, moving patterns, and diet composition. Overall, the dietary and behavioral flexibility shown by howler monkeys allow them to live in fragments, and it is suggested that this is more likely in areas with high productivity and few competitors. © 2015. Acad. Colomb. Cienc. Ex. Fis. Nat.
References
ReferencesAgoramoorthy, G., & Rudran, R. (1993). Male dispersal among free-ranging red howler monkeys (Alouatta seniculus) in Venezuela. Folia Primatologica, 61: 92-96.
Andresen, E. (1999). Seed dispersal by monkeys and the fate of dispersed seeds in a Peruvian rain forest. Biotropica, 31: 145-158.
Arroyo-Rodriguez, V., & Mandujano, S. (2006). Forest frag-mentation modifies habitat quality for Alouatta palliata.International Journal of Primatology, 27: 1079-1096.
Asensio, N., Cristobal-Azkarate J., Dias P.A.D., Vea J.J., & Rodriguez-Luna, E. (2007). Foraging habits of Alouatta palliata mexicana in three forest fragments. Folia Primatologica, 78: 141-153.
Beltran, M.L., & Stevenson, P.R. (2012). Twins and infanticide in red howler monkeys inhabiting a fragment in Western Orinoquia. Neotropical Pirmates, 19(1): 41-42.
Bicca-Marques, J.C. (2003). How do howler monkeys cope with habitat fragmentation? In: L.K. Marsh (ed.) Primates in fragments: Ecology and conservation. (pp. 283-303). Kluwer Academics/Plenum Publishers, New York.
Bravo, S.P., & Sallenave, A. (2003). Foraging behavior and activity patterns of Alouatta caraya in the northeastern Argentinean flooded forest. International Journal of Primatology, 24: 825-846.
Carretero-P., X. (2008). Efecto de la disponibilidad de recursos sobre la ecología y comportamiento de Saimiri sicureus albigena en fragmentos de bosque de galería, San Martin (Meta- Colombia). MSc thesis. Pontificia Universidad Javeriana, Bogota.Chapman, C.A., & Balcomb, S.R. (1998). Population charac-teristics of howlers: Ecological conditions or group history. International Journal of Primatology, 19: 385-403.
Clarke, M.R., Collins, D.A., & Zucker, E.L. (2002). Responses to deforestation in a group of mantled howlers (Alouatta palliata) in Costa Rica. International Journal of Primatology, 23: 365-381.
Cristobal-Azkarate, J., & Arroyo-Rodriguez, V. (2007). Diet and activity pattern of howler monkeys (Alouatta palliata) in Los Tuxtlas, Mexico: Effects of habitat fragmentation and implications for conservation. AmericanJournal of Primatology,69: 1013-1029.
Crockett, C.M. (1996). The relation between red howler monkey (Alouatta seniculus) troop size and population growth in two habitats. In: M.A. Norconk, A.L. Rosenberger & P.A. Garber (eds.). Adaptive Radiations of Neotropical Primates. (pp. 489-510). Plenum Press, New York.
Crockett, C.M. (1998). Conservation biology of the genus Alouatta. International Journal of Primatology, 19: 549-578.
Crockett, C.M. (2003). Re-evaluating the sexual selection hypothesis for infanticide by Alouatta males. Special Topics in Primatology,3: 327-365.
Crockett, C.M., & Eisenberg, J.F. (1987). Howlers: Variations in group size and demography. In: B.B. Smuts, D.L. Cheney, R.M. Seyfarth, R.W. Wrangham & T.T. Struhsaker (eds.). Primate Societies. (p. 54-68), University of Chicago Press, Chicago.
Di Fiore, A., & Campbell, C.J. (2007). The Aletines: Variation in ecology, behavior, and social organization. In: C.J. Campbell, A. Fuentes, K.C. Mackinnon, M. Panger, & S.K. Bearder (eds.).Primates in Perspective. (pp. 155-185). Oxford University Press; Oxford.
Ganzhorn, J.U. (1992). Leaf chemistry and the biomass of folivorous primates in tropical forests: Test of a hypothesis. Oecologia, 91: 540-547.
Gaulin, S.J.C., & Gaulin, C.K. (1982). Behavioral ecology of Alouatta seniculus in Andean cloud forest. International Journal of Primatology, 3: 1-32.
Hobbs, R.J., & Yates, C.J. (2003). Impacts of ecosystem fragmentation on plant populations: generalizing the idiosyncratic. Australian Journal of Botany, 51: 471-488.
Isbell, L.A. (1991). Contest and scramble competition: patterns of female aggression and ranging behavior among primates. Behavioral Ecology, 2: 134-155.
Isbell, L.A., & van Vuren, D. (1996). Differential costs of locational and social dispersal and their consequences for female group-living primates. Behaviour,133: 1-36.
Izawa, K. (1993). Soil-eating by Alouatta and Ateles. International Journal of Primatology,14: 229-242.
Izawa, K. (1997). Social changes within a group of red howler monkeys, VI. Field Studies of Fauna and Flora La Macarena Colombia, 11: 19-34.
Izawa, K., & Lozano, H. (1992). Social changes within a group of red howler monkeys (Alouatta seniculus) IV. Field Studies of New World Monkeys La Macarena Colombia, 7: 15-27.
Juan, S., Estrada, A., & Coates-Estrada, R. (2000). Contrastes y similitudes en el uso de recursos y patrón general de actividades en tropas de monos aulladores (Alouatta palliata) en fragmentos de selva en Los Tuxtlas, México. Neotropical Primates, 8: 131-135.
Julliot, C. (1996). Seed dispersal by red howling monkeys (Alouatta seniculus) in the tropical rain forest of French Guiana. International Journal of Primatology,17: 239-258.
Julliot, C., & Sabatier, D. (1993). Diet of the red howler monkey (Alouatta seniculus) in French- Guiana. International Journal of Primatology, 14: 527-550.
Kimura, K. (1992). Demographic approach to the social group of wild red howler monkeys (Alouatta seniculus). Field Studies of New World Monkeys La Macarena Colombia, 7: 29-34.
Laurance, W.F., Lovejoy, T.E., Vasconcelos, H.L., Bruna, E.M., Didham, R.K., Stouffer, P.C.,et al. (2002). Ecosystem decay of Amazonian forest fragments: A 22-year investigation. Conservation Biology, 16: 605-618.
Marsh, L.K., & Loiselle, B.A. (2003). Recruitment of black howler fruit trees in fragmented forests of Northern Belize. International Journal of Primatology, 24: 65-86.
Milton, K. (1998). Physiological ecology of howlers (Alouatta): Energetic and digestive considerations and comparison with the Colobinae. International Journal of Primatology,19: 513-548.
Miranda, J.M.D., Bernardi, I.P., Abreu, K.C., & Passos, F.C.(2005). Predation on Alouatta guariba clamitans Cabrera (Primates, Atelidae) by Leopardus pardalis (Linnaeus) (Carnivora, Felidae). Revista Brasileira de Zoologia, 22: 793-795.
Oates, J.F., Whitesides, G.H., Davies, A.G., Waterman, P.G., Green, S.M., Dasilva, G.L., & Mole, S. (1990). Determinants of variation in tropical forest primate biomass - new evidence from West-Africa. Ecology, 71: 328-343.
Palma, A.C., Vélez, A., Gómez-Posada, C., López, H., Zárate-Caicedo, D. A., & Stevenson, P.R. (2011). Use of space, activity patterns, and foraging behavior of red howler monkeys (Alouatta seniculus) in an Andean forest fragment in Colombia. American Journal of Primatology, 73 (10), 1062-1071.
Peres, C.A. (1997). Effects of habitat quality and hunting pressure on arboreal folivore densities in Neotropical forests: A case study of howler monkeys (Alouatta spp.). Folia Primatologica, 68: 199-222.
Pope, T.R. (1990). The reproductive consequences of male cooperation in the red howler monkey: paternity exclusion in multimale and single-male troops using genetic markers. Behavioral Ecology and Sociobiology, 27: 439-446.
Pope, T.R. (1992). The Influence of dispersal patterns and mating system on genetic differentiation within and between populations of the red howler monkey (Alouatta seniculus). Evolution, 46: 1112-1128.
Rudran, R., & Fernandez-Duque, E. (2003). Demographic changes over thirty years in a red howler population in Venezuela. International Journal of Primatology, 24: 925-947.
Sallis, E.S.V., de Barros, V., Garmatz, S.L., Fighera, R.A., & Graca, D.L. (2003). A case of yellow fever in a brown howler (Alouatta fusca) in Southern Brazil. Journal of Veterinary Diagnostic Investigation, 15: 574-576.
Santamaría, M. (2004). The effect of home range reduction on the ecology of red howler monkeys in Central Amazonia. Doctoral thesis, University of Cambridge. Cambridge, UK.
Santamaría, M., & Rylands, A.B. (2003). Ecología básica de un grupo de Alouatta seniculus durante la estación seca en la Amazonia central brasilera. In: V. Pereira-Bengoa, F. Nassar-Montoya & A. Savage (eds.). Primatologia del Nuevo Mundo: Biología, medicina y conservación. (pp. 96-111). Centro de Primatologia Araguatos, Bogotá.
Saunders, D.A., Hobbs, R.J., & Margules, C.R. (1991). Biological consequences of ecosystem fragmentation: A review. Conservation Biology, 5: 18-32.
Sekulic, R. (1982). The function of howling in red howler monkeys (Alouatta seniculus). Behaviour, 81: 38-54.
Sterck, E.H.M., Watts, D.P., & van Schaik, C.P. (1997). The evolution of female social relationships in nonhuman primates. Behavioral Ecology & Sociobiology, 41: 291-309.
Stevenson, P.R. (2007). Estimates of the number of seeds dispersed by a population of primates in a lowland forest in western Amazonia. In: A.J. Dennis, E.W. Schupp, R.J. Green & D.W. Westcott (eds.). Seed dispersal: theory and its application in a changing world. (pp. 340-362). CAB International, Wallingford, UK.
Stevenson, P.R. (2010). Efectos de la fragmentación y de la producción de frutos en comunidades de primates Neotropicales. In: V. Pereira-Bengoa, P.R.
Stevenson, M.L. Bueno & F. Nassar (eds.). Avances en la Primatología del Nuevo Mundo. (pp. 239-257). Centro de Primatología Araguatos, Bogotá.
Stevenson, P.R., & Aldana, A.M. (2008). Potential effects of ateline extinction and forest fragmentation on plant diversity and composition in the Western Orinoco basin, Colombia.International Journal of Primatology, 29: 365-377.
Stevenson, P.R., Castellanos, M.C., Cortes, A.I., & Link, A. (2008). Flowering patterns in a seasonal tropical lowland forest in western Amazonia. Biotropica, 40: 559-567.
Stevenson, P.R., Castellanos, M.C., Pizarro, J.C., & Garavito, M. (2002). Effects of seed dispersal by three ateline monkey species on seed germination at Tinigua National Park, Colombia. International Journal of Primatology, 23:1187-1204.
Stevenson, P.R., & Link, A. (2010). Fruit preferences of Ateles belzebuth in Tinigua Park, Northwestern Amazonia. International Journal of Primatology,31: 393-407.
Stevenson, P.R., Quiñones, M.J., & Ahumada, J.A. (1998). Effects of fruit patch availability on feeding subgroup size and spacing patterns in four primate species at Tinigua National Park, Colombia. International Journal of Primatology,19: 313-324.
Stevenson, P.R., Quiñones, M.J., & Ahumada, J.A. (2000). Influence of fruit availability on ecological overlap among four Neotropical primates at Tinigua National Park, Colombia. Biotropica, 32: 533-544.
Stevenson, P.R., Suescún, M., & Quiñones, M.J. (2004). Characterization of forest types at the CIEM, Tinigua Park, Colombia. Field Studies of New World Monkeys La Macarena Colombia, 14: 1-19.
Terborgh, J., & Janson, C.H. (1986). The socioecology of primate groups. Annual Review of Ecology & Systematics,17: 111-135.
Thorington, R.W.J., Rudran, R., & Mack, D. (1979). Sexual dimorphism of Alouatta seniculus and observations on capture techniques. In: J.F. Eisenberg (ed.). VertebrateEcology in the Northern Neotropics. (pp. 97-106). Smithsonian Institution Press, Washington D. C., USA.
Torres-Neira, J.A. (2005). Historia natural de Cebus apella y patrones de asociación interespecífica con Saimiri sciureusen un bosque fragmentado (Meta, Colombia). B.Sc thesis. Universidad de Los Andes, Bogotá.
Treves, A., Drescher, A., & Ingrisano, N. (2001). Vigilance and aggregation in black howler monkeys (Alouatta pigra). Behavioral Ecology & Sociobiology, 50: 90-95.
van Schaik, C. (2000). Infanticide by male primates: the sexual selection hypothesis revisited. In: C. van Schaik & C.H. Janson (eds.). Infanticide by males and its implications. (pp. 27-60). Cambridge University Press, Cambridge, UK.
Wang, E., & Milton, K. (2003). Intragroup social relationships of male Alouatta palliata on Barro Colorado Island, Republic of Panama. International Journal of Primatology,24: 1227-1243.
This work is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License.
Copyright (c) 2015 Journal of the Colombian Academy of Exact, Physical and Natural Sciences