Use of space in two neighboring groups of the howler monkey Alouatta palliata mexicana (Primates: Atelidae): overlap and home range size

Authors

  • Paulo Cesar Quintana-Morales UNIVERSIDAD VERACRUZANA
  • Jorge E. Morales-Mávil UNIVERSIDAD VERACRUZANA
  • Mateo Escobar-Aliaga INSTITUTO TECNOLÓGICO DE SAN ANDRÉS.
  • Rocio Bravo-Xicotencatl

Keywords:

Monos aulladores, interacciones espaciales, traslape de ámbito hogareño, distancia intergrupal, competencia.

Abstract

The interaction between primate groups and the dynamics involved in the use of space are important factors affecting both competition for resources and intergroup dominance. In the present study we analyzed the differences in home range overlap and intergroup size, as well as the diversity of tree species within the home range, the Value Index for the key tree species, and the daily activity pattern of two neighboring groups of the howler monkey Alouatta palliata. From March 2002 to June 2003, the behavior and location of two groups of monkeys (G1, two adult males, four adult females and four infants; G2, six adult males, five adult females, one juvenile and three infants) were recorded in the same forest patch at Los Tuxtlas Biosphere Reserve, Veracruz, Mexico. Using the Minimum Convex Polygon (100 %), grid (100 m), and Kernel (adapted and fixed) methods, as well as transect sampling, significant differences (F1, 20 = 14.45, P = 0.001) were found in the home range size of the groups, being greater in G2. The habitat in the G2 home range had greater richness and diversity of tree species, as well as a higher Importance Value Index for the key tree species (Ficus spp.) included in the howler monkey diet. On the other hand, significant differences between groups (Mann-Whitney U = 38, P < 0.05) were found only as regards locomotion behavior, likely due to a behavioral adaptation to optimize food resource use or search. The two groups displayed a similar use of food resources; however, there was a slight overlap in the home range between both groups with no direct aggression, likely because their habitat included sufficient space and food. Our data suggest that the reduced overlap may vary between neighboring groups because of factors such as group size. However, groups could weigh various factors to avoid home-range overlap.

Author Biographies

Paulo Cesar Quintana-Morales, UNIVERSIDAD VERACRUZANA

Doctorado en Neuroetología por la Universidad Veracruzana. Laboratorio de Biología de la Conducta. Académico de Tiempo Completo. Profesor de Estadística, Sistemas de Información Geográfica y Experiencia Recepcional en Universidad Veracruzana y Posgrado en Neuroetología. Temas de interés: Primatología, Ecología, Sistemas de Información Geográfica, Etología y Fragmentación del hábitat.

Jorge E. Morales-Mávil, UNIVERSIDAD VERACRUZANA

Laboratorio de Biología de la Conducta. Académico de Tiempo Completo. Profesor de Ecología Conductual en Universidad Veracruzana y Posgrado en Neuroetología. Temas de interés: Ecología, Ecología Conductual, Matozoología, y herpetología.

Mateo Escobar-Aliaga, INSTITUTO TECNOLÓGICO DE SAN ANDRÉS.

Doctor en Etología por la Universidad de Barcelona, España. Profesor en el Instituto Tecnológico de San Andrés, Veracruz, México.

Rocio Bravo-Xicotencatl

Doctora en Etología por la Universidad de Barcelona, España.

References

Altmann, J. 1974. Observational study of behavior: sampling methods. Behaviour 49:227-267.

Amsler, S. J. 2010. Energetics costs of territorial boundary patrols by wild chimpanzees. American Journal of Primatology 72:93-103.

Asencio, N., J. Cristóbal-Azkarate, P. A. Duarte-Dias, J. J. Véa, and E. Rodríguez-Luna. 2007. Foraging habits of Alouatta palliata mexicana in three forest fragments. Folia Primatologica 78:141-153.

Baldwin, J. D., and J. I. Baldwin. 1972. Population density and use of space in howling monkeys (Alouatta villosa) in southwestern Panama. Primates 13:371-379.

Börger, L., B. D. Dalziel, and J. M. Fryxell. 2008. Are there general mechanisms of animal home range behaviour? A review and prospects for future research. Ecology Letters 11:637–650.

Campera, M., V. Serra, M. Balestri, M. Barresi, M. Ravaolahy, F. Randriatafika, and G. Donati. 2014. Effects of Habitat Quality and Seasonality on Ranging Patterns of Collared Brown Lemur (Eulemur collaris) in Littoral Forest Fragments. International Journal of Primatology 35:957-975.

Campos, F. A., M. L. Bergstrom, A. Childers, J. D. Hogan, K. M. Jack, A. D. Melin, K. N. Mosdossy, M. S. Myers, N. A. Parr, E. Sargeant, V. A. M. Schoof, and L. M. Fedigan. 2014. Drivers of home range characteristics across spatiotemporal scales in a Neotropical primate, Cebus capucinus. Animal Behaviour 91:93-109.

Castillo-Campos, G., and J. Laborde. 2004. La vegetación. Pp. 231-265, in Los Tuxtlas: El paisaje de la sierra (Guevara, S. J., J. Laborde, and G. Sánchez-Ríos, eds.). Instituto de Ecología/Unión Europea. Xalapa, México.

Chao, A., and T. J. Shen. 2010. SPADE (Species prediction and diversity estimation) v6 Program distributed by the author. Institute of Statistics. National Tsing Hua University. Hsin-Chu, Taiwan.

Chapman, C. A., and L. J. Chapman. 2000. Determinants of group size in primates: The importance of travel cost. Pp. 24-42, in On the move, how and why animals travel in groups (Boinski, S. y P. A. Garber, eds.). Universidad de Chicago. Chicago, U. S. A.

Chapman, C. A., R. W. Wrangham, and L. J. Chapman. 1995. Ecological constraints on group size: An analysis of spider monkey and chimpanzee subgroups. Behavioral Ecology and Sociobiology 36:59-70.

Chapman, C.A., and M. S. Pavelka. 2005. Group size in folivorous primates: ecological constraints and the possible influence of social factors. Primates 46:1-9.

Clarke, M.R. 1990. Behavioral development and socialization of infants in a free-ranging group of howling monkeys (Alouatta palliata). Folia Primatologica 54:1–15.

Colias, N. E., and C. Southwick. 1952. A Field study of population density and social organization in howling monkeys. Proceedings of the American Philosophical Society 96:143-156.

Coroi, M., M. Sheehy-Skeffington, P. Giller, C. Smith, M. Gormally, and G. O’Donovan. 2004. Vegetation diversity and stand structure in streamside forests in the south of Ireland. Forest Ecology and Management 202:39-57.

Cristóbal-Azkarate, J., P. A. D. Dias, and J. J. Veà . 2004. Causes of intraspecific aggression in Alouatta palliata mexicana: Evidence from injuries, demography, and habitat. International Journal of Primatology 25: 939-953.

Cristóbal-Azkarate, J., and V. Arroyo-Rodríguez. 2007. Diet and activity pattern of howler monkeys (Alouatta palliata) in Los Tuxtlas, Mexico: Effects of habitat fragmentation and implications for conservation. American Journal of Primatology 69:1013–1029.

Dias, P.A., and A. Rangel-Negrín. 2015. Diets of howler monkeys. Pp. 21-56, in Howler monkeys behavior, ecology, and conservation developments in primatology: Progress and prospects vol. 2 (Kowalewski, M. M., P. A. Garber, L. Cortés-Ortiz, B. Urbani, and D. Youlatos, eds.). Springer. New York, U. S. A.

Domingo-Balcells, C., and J. J. Véa-Baró. 2009. Developmental stages in the howler monkey, subspecies Alouatta palliata mexicana: a new classification using age-sex categories. Neotropical Primates 16:1–8.

Dunn, J. C., J. Cristóbal-Azkarate, and J. Veà . 2009. Differences in diet and activity pattern between two groups of Alouatta palliata associated with the availability of big trees and fruit of top food taxa. American Journal of Primatology 71:654–662.

Esri. 1999. ArcView v3.2 para Windows. Environmental Systems Research Institute. California, U. S. A.

Estrada, A. 1984. Resource use by howler monkeys (Alouatta palliata) in the rain forest of Los Tuxtlas, Veracruz, Mexico. International Journal of Primatology 5:105-131.

Glessner, K. D. G., and A. Britt. 2005. Population density and home range size of Indri indri in a protected low altitude rain forest. International Journal of Primatology 26:855-872.

Hopkins, M. E. 2013. Relative dominance and resource availability mediate mantled howler (Alouatta palliata) spatial responses to neighbors’ loud calls. International Journal of Primatology 34:1032-1054.

IBM Corp. Released. 2011. IBM SPSS Statistics para Windows v20.0. Nueva York, U. S. A.

Kernohan, B. J., R. A. Gitzen, and J. J. Millspaugh. 2001. Analysis of animal space use and movements. Pp. 125-166, in Radio tracking and animal populations (Millspaugh, J. J., and J. M. Marzluff, eds.). Academic. San Diego, U. S. A.

Kodric-Brown, A., and J. H. Brown. 1978. Influence of economics, interspecific competition, and sexual dimorphism on territoriality of migrant rufous hummingbirds. Ecology 59:285–296.

Laver, P. N., and M. J. Kelly. 2008. A critical review of home range studies. The Journal of Wildlife Management 72:209-298.

Lopez-Darias, M., T. W. Schoener, D. A. Spiller, and J. B. Losos. 2012. Predators determine how weather affects the spatial niche of lizard prey: exploring niche dynamics at a fine scale. Ecology 93:2512–2518.

Martin, P., and P. Bateson. 1993. Measuring behavior: An introductory guide. Universidad de Cambridge. Cambridge, United Kindom.

Mendoza, E., J. Fay, and R. Dirzo. 2005. A quantitative analysis of forest fragmentation in Los Tuxtlas, southeast Mexico: patterns and implications for conservation. Revista Chilena de Historia Natural 78:451-467.

Milton, K. 1980. The foraging strategy of howler monkeys: A study in primate economics. Universidad de Columbia. Nueva York, U. S. A.

Milton, K. 1984. Habitat, diet and activity patterns of free-ranging woolly spider monkeys (Brachyteles arachnoides E. Geoffroy 1806). International Journal of Primatology 5:491-514.

Mittermeier, R. 1973. Group activity and population dynamics of the howler monkeys of Barro Colorado Island. Primates 14:1-19.

Moreno, C. E., F. Barragán-Pavón, E. Pineda, and N. P. Pavón. 2011. Reanálisis de la diversidad alfa: alternativas para interpretar y comparar información sobre comunidades ecológicas. Revista Mexicana de Biodiversidad 82:1249-1261.

Nicholson, A. J. 1954. An outline of the dynamics of animal populations. Australian Journal of Zoology 2:9-65.

Pearce, F., C. Carbone, G. Cowlishaw, and N. J. B. Isaac. 2013. Space-use scaling and home range overlap in primates. Proceedings of the Royal Society B 280:1-6.

Pebsworth, P. A., A. J. J. MacIntosh, H. R. Morgan, and M. A. Huffman. 2012. Factors Influencing the ranging behavior of chacma baboons (Papio hamadryas ursinus) living in a human-modified habitat. International Journal of Primatology 33:872-887.

Pyritz, L. W., P. M. Kappeler, and C. Fichtel. 2011. Coordination of group movements in wild red-fronted lemurs (Eulemur rufifrons): processes and influence of ecological and reproductive seasonality. International Journal of Primatology 32:1325-1347.

Robbins, A. M., T. S. Stoinski, K. A. Fawcett, and M. M. Robbins. 2009. Socioecological influences on the dispersal of female mountain gorillas, evidence of a second folivore paradox. Behavioral Ecology and Sociobiology 63:477-489.

Rodgers, A. R., and A. P. Carr. 1998. HRE: The Home Range Extension for ArcView. Program distributed by the author. Ministry of Natural Resources. Centre for Northern Forest Ecosystem Research. Ontario, Canadá.

Rodríguez-Luna, E., L. E. Domínguez-Domínguez, J. E. Morales-Mávil, and M. Martínez-Morales. 2003. Foraging strategy changes in an Alouatta palliata mexicana troop released on an island. Pp. 229-250, in Primates in fragments: Ecology and conservation (Marsh, L. K., ed.). Kluwer Academic/ Plenum. Nueva York, U. S. A.

Serio-Silva, J. C., V. Rico-Gray, L. T. Hernández-Salazar, and R. Espinosa-Gómez. 2002. The role of Ficus (Moraceae) in the diet and nutrition of a troop of Mexican howler monkeys, Alouatta palliata mexicana, released on an island in southern Veracruz, Mexico. Journal of Tropical Ecology 18:1-16.

Seth, P. K., and S. Seth. 1986. Ecology and behaviour of rhesus monkeys in India. Pp. 89-104, in Primate ecology and conservation (Else, J. G., and P. C. Lee, eds.). Universidad de Cambridge. Cambridge, United Kindom.

Shaffer, C. A. 2014. Spatial Foraging in Free Ranging Bearded Sakis: Traveling Salesmen or Lévy Walkers? American Journal of Primatology 76:472–484.

Solórzano-García, B., E. A. Ellis, and E. Rodríguez-Luna. 2012. Deforestation and primate habitat availability in Los Tuxtlas Biosphere Reserve, Mexico. International Journal of Ecosystem 2:61-66.

Soto, M. 2004. El clima. Pp.195-200, in Los Tuxtlas, el paisaje de la sierra (Guevara, S. J., J. Laborde, and G. Sánchez-Ríos, eds.). Instituto de Ecología/Unión Europea. Xalapa, México.

Van-Schaik, C. P., and P. M. Kappeler. 1993. Life history, activity period and lemur social systems. Pp. 241-260, in Lemur social systems and their ecological basis (Kappeler, P. M., and J. U. Ganzhorn, eds.). Plenum. New York, U. S. A.

Williams-Guillén, K., C. McCann, J. C. Martínez-Sánchez, and F. Koontz. 2006. Resource availability and habitat use by mantled howling monkeys in a Nicaraguan coffee plantation: can agroforests serve as core habitat for a forest mammal? Animal Conservation 9:331-338.

Worton, B. J. 1989. Kernel methods for estimating the utilization distribution in home-range studies. Ecology 70:164-168.

Wrangham, R. W., G. L. Gittleman, and C. A. Chapman. 1993. Constraints on group size in primates and carnivores: population density and day-range as assays of exploitation competition. Behavioral Ecology and Sociobiology 32:199-209.

Downloads

Published

2017-03-13

Issue

Section

Articles