Skip to main content
Log in

An Exploration of the Factors Influencing the Spatial Behavior of Mantled Howler Monkeys (Alouatta palliata)

  • Published:
International Journal of Primatology Aims and scope Submit manuscript

Abstract

Space use patterns are the result of complex interactions between individuals and their environment. Although competition with conspecifics, the distribution and availability of food resources and climatic conditions may all influence space use by primates, these factors are usually addressed separately. Studies that integrate social, ecological, and physical factors have the potential to improve our understanding of variation in the spatial behavior of primates. We studied two groups of mantled howler monkeys (Alouatta palliata) in Los Tuxtlas, Mexico, to explore how intergroup competition, food availability, and ambient temperature influenced their use of space over 15 months. Loud calls produced by neighboring groups were a determining factor in the variation in the area used per month, daily ranging distance, and travel rate. Food availability did not influence any aspect of spatial behavior, but the distribution of feeding trees affected travel rate. Ambient temperature influenced the frequency and speed of travel. These results suggest that the spatial behavior of howler monkeys is influenced by social (intergroup competition), ecological (food distribution), and physical (ambient temperature) factors, and that the specific effects of these factors vary among measures of space use.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Agetsuma, N. (1995a). Foraging strategies of Yakushima macaques (Macaca fuscata yakui). International Journal of Primatology, 16, 595–609.

    Article  Google Scholar 

  • Agetsuma, N. (1995b). Dietary selection by Yakushima macaques (Macaca fuscata yakui): The influence of food availability and temperature. International Journal of Primatology, 16, 611–627.

    Article  Google Scholar 

  • Agetsuma, N., & Nakagawa, N. (1998). Effects of habitat differences on feeding behaviors of Japanese monkeys: Comparison between Yakushima and Kinkazan. Primates, 39, 275–289.

    Article  Google Scholar 

  • Agostini, I., Holzmann, I., & Di Bitetti, M. S. (2010). Ranging patterns of two syntopic howfler monkey species (Alouatta guariba and A. caraya) in northeastern Argentina. International Journal of Primatology, 31, 363–381.

    Article  Google Scholar 

  • Alcock, J. (1997). Animal behavior: An evolutionary approach (6th ed.). Sunderland, MA: Sinauer Associates.

    Google Scholar 

  • Altmann, J. (1974). Observational study of behavior: Sampling methods. Behaviour, 49, 227–267.

    Article  CAS  PubMed  Google Scholar 

  • Angilletta, M. J., Huey, R. B., & Frazier, M. R. (2010). Thermodynamic effects on organismal performance: Is hotter better? Physiological and Biochemical Zoology, 83, 197–206.

    Article  PubMed  Google Scholar 

  • Asensio, N., José-Domínguez, J. M., & Dunn, J. C. (2018). Socioecological factors affecting range defensibility among howler monkeys. International Journal of Primatology, 39, 90–104.

    Article  Google Scholar 

  • Aujard, F., & Vasseur, F. (2001). Effect of ambient temperature on the body temperature rhythm of male gray mouse lemurs (Microcebus murinus). International Journal of Primatology, 22, 43–56.

    Article  Google Scholar 

  • Bailey, D. M., & Johnston, I. A. (2005). Temperature acclimatization of swimming performance in the European queen scallop. Journal of Thermal Biology, 30, 119–124.

    Article  Google Scholar 

  • Baldwin, J. D., & Baldwin, J. I. (1976). Vocalizations of howler monkeys (Alouatta palliata) in southwestern Panama. Folia Primatologica, 26, 81–108.

    Article  CAS  Google Scholar 

  • Bale, J. S. (2002). Insects and low temperatures: From molecular biology to distributions and abundance. Philosophical Transactions of the Royal Society of London B : Biological Sciences, 357, 849–861.

  • Baoping, R., Ming, L., Yongcheng, L., & Fuwen, W. (2009). Influence of day length, ambient temperature, and seasonality on daily travel distance in the Yunnan snub-nosed monkey at Jinsichang, Yunnan, China. American Journal of Primatology, 71, 233–241.

    Article  PubMed  Google Scholar 

  • Barton, K. (2016). ‘MuMIn’: multi-model inference. R Package Version 1., 15, 6.

    Google Scholar 

  • Bates, D., Maechler, M., Bolker, B., & Walker, S. (2016). ‘lme4’: Linear mixed-effects models using ‘Eigen’ and S4. R Package Version, 1, 1–12.

    Google Scholar 

  • Bicca-Marques, J. C., & Azevedo, R. B. (2004). The thermoregulation hypothesis does not explain the evolution of sexual dichromatism in the brown howler monkey (Alouatta guariba clamitans). Folia Primatologica, 75, 236.

    Google Scholar 

  • Bicca-Marques, J. C., & Calegaro-Marques, C. (1994). Activity budget and diet of Alouatta caraya: An age–sex analysis. Folia Primatologica, 63, 216–220.

    Article  CAS  Google Scholar 

  • Bicca-Marques, J. C., & Calegaro-Marques, C. (1998). Behavioral thermoregulation in a sexually and developmentally dichromatic Neotropical primate, the black-and-gold howling monkey (Alouatta caraya). American Journal of Physical Anthropology, 106, 533–546.

    Article  CAS  PubMed  Google Scholar 

  • Bolyard, K. J., & Rowland, W. J. (2000). The effects of spatial context and social experience on the territorial aggression of male threespine stickleback. Behaviour, 137, 845–864.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Burnham, K. P., & Anderson, D. R. (2002). Model selection and multimodel inference: A practical information-theoretic approach (2nd ed.). New York: Springer Science+Business Media.

    Google Scholar 

  • Buzzard, P. J. (2006). Ranging patterns in relation to seasonality and frugivory among Cercopithecus campbelli, C. petaurista and C. diana in the Taï Forest. International Journal of Primatology, 27, 559–573.

    Article  Google Scholar 

  • Cabanac, M. (2006). Adjustable set point: To honor Harold T. Hammel. Journal of Applied Physiology, 100, 1338–1346.

    Article  PubMed  Google Scholar 

  • Cano-Huertes, B., Rangel-Negrín, A., Coyohua-Fuentes, A., Chavira-Ramírez, D. R., Canales-Espinosa, D., & Dias, P. A. D. (2017). Reproductive energetics of female mantled howler monkeys (Alouatta palliata). International Journal of Primatology, 5, 942–961.

    Article  Google Scholar 

  • Chapman, C. A. (1988). Patterns of foraging and range use by three species of Neotropical primates. Primates, 29, 177–194.

    Article  Google Scholar 

  • Chaves, O. M., & Bicca-Marques, J. C. (2016). Feeding strategies of brown howler monkeys in response to variations in food availability. PLoS One, 11, e0145819.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cheney, L., & Seyfarth, R. M. (2003). Signalers and receivers in animal communication. Annual Review of Psychology, 54, 145–173.

    Article  PubMed  Google Scholar 

  • Chiarello, A. G. (1995a). Grooming in brown howler monkeys, Alouatta fusca. American Journal of Primatology, 35, 73–81.

    Article  Google Scholar 

  • Chiarello, A. G. (1995b). Role of loud calls in brown howler monkeys, Alouatta fusca. American Journal of Primatology, 36, 213–222.

    Article  Google Scholar 

  • Cohen, J. A. (1960). A coefficient of agreement for nominal scales. Educational and Psychological Measurement, 20, 37–46.

    Article  Google Scholar 

  • Cristóbal-Azkarate, J., & Arroyo-Rodríguez, V. (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.

    Article  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Crockett, C. M., & Pope, T. (1988). Inferring patterns of aggression from red howler monkey injuries. American Journal of Primatology, 15, 289–308.

    Article  Google Scholar 

  • Crofoot, M. C., Gilby, I. C., Wikelski, M. C., & Kays, R. W. (2008). Interaction location outweighs the competitive advantage of numerical superiority in Cebus capucinus intergroup contests. Proceedings of the National Academy of Sciences of the USA, 105, 577–581.

    Article  PubMed  Google Scholar 

  • da Cunha, R. G. T., & Byrne, R. W. (2006). Roars of black howler monkeys (Alouatta caraya): Evidence for a function in inter-group spacing. Behaviour, 143, 1169–1199.

    Article  Google Scholar 

  • da Cunha, R. G. T., & Jalles-Filho, E. (2007). The roaring of southern brown howler monkeys (Alouatta guariba clamitans) as a mechanism of active defense of borders. Folia Primatology, 78, 259–271.

    Article  Google Scholar 

  • Darwin, C. (1859). On the origin of species. London: J Murray.

    Google Scholar 

  • Di Fiore, A., & Campbell, C. J. (2007). The atelines: Variations 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). New York: Oxford University Press.

    Google Scholar 

  • Doran, D. (1997). Influence of seasonality on activity patterns, feeding behavior, ranging and grouping patterns in Taï chimpanzees. International Journal of Primatology, 18, 183–206.

    Article  Google Scholar 

  • Dussault, C., Ouellet, J.-P., Courtois, R., Huot, J., Breton, L., & Jolicoeur, H. (2005). Linking moose habitat selection to limiting factors. Ecography, 28, 619–628.

    Article  Google Scholar 

  • Estrada, A., Juan-Solano, S., Martínez, T. O., & Coates-Estrada, R. (1999). Feeding and general activity patterns of a howler monkey (Alouatta palliata) troop living in a forest fragment at Los Tuxtlas, Mexico. American Journal of Primatology, 48, 167–183.

    Article  CAS  PubMed  Google Scholar 

  • Fan, P. F., Ni, Q. Y., Sun, G. Z., Huan, B., & Jiang, X. L. (2008). Seasonal variation in the activity budget of Nomascus concolor jingdongensis at Mt. Wuliang, Central Yunnan, China: Effect of diet and temperature. International Journal of Primatology, 29, 1047–1057.

    Article  Google Scholar 

  • Fashing, P. J., Mulindahabi, F., Gakima, J.-B., Masozera, M., Mununura, I., Plumptre, A. J., & Nguyen, N. (2007). Activity and ranging patterns of Colobus angolensis ruwenzorii in Nyungwe Forest, Rwanda: Possible costs of large group size. International Journal of Primatology, 28, 529–550.

    Article  Google Scholar 

  • Feighny, J. A., Williamson, K. E., & Clarke, J. A. (2006). North American elk bugle vocalizations: Male and female bugle call structure and context. Journal of Mammalogy, 87, 1072–1077.

    Article  Google Scholar 

  • Fortes, V. B., Bicca-Marques, J. C., Urbani, B., Fernández, V. A., & Pereira, T. S. (2015). Ranging behavior and spatial cognition of howler monkeys. In M. Kowalewski, P. A. Garber, L. Cortés-Ortiz, B. Urbani, & D. Youlatos (Eds.), Howler monkeys: Behavior, ecology, and conservation (pp. 219–255). New York: Springer Science+Business Media.

    Chapter  Google Scholar 

  • Fournier, L. A. (1978). Un método cuantitativo Para la medición de características fenológicas en árboles. Turrialba, 24, 422–423.

    Google Scholar 

  • Fox, J., & Weisberg, S. (2016). ‘Car’: Companion to applied regression. R Package Version, 2, 1–4.

    Google Scholar 

  • Ganzhorn, J. U. (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.

    Article  PubMed  Google Scholar 

  • Gentry, A. H. (1982). Patterns of Neotropical plant species diversity. Evolutionary Biology, 15, 1–84.

    Google Scholar 

  • Gese, E. M. (2001). Territorial defense by coyotes (Canis latrans) in Yellowstone National Park, Wyoming: Who, how, where, and why. Canadian Journal of Zoology, 79, 980–987.

    Article  Google Scholar 

  • Getz, W. M., Fortmann-Roe, S. B., Lyons, A., Ryan, S., & Cross, P. (2007). LoCoH methods for the construction of home ranges and utilization distributions. PLoS One, 2, e207.

    Article  PubMed  PubMed Central  Google Scholar 

  • Gorini, L., Linnell, J. D. C., May, R., Panzacchi, M., Boitani, L., et al (2012). Habitat heterogeneity and mammalian predator-prey interactions. Mammal Reviews, 42, 55–77.

    Article  Google Scholar 

  • Grinnell, J., Packer, C., & Pusey, A. E. (1995). Cooperation in male lions: Kinship, reciprocity, or mutualism? Animal Behaviour, 49, 95–105.

    Article  Google Scholar 

  • Gurski, S. (2000). Effect of seasonality on the behavior of an insectivorous primate, Tarsius spectrum. International Journal of Primatology, 21, 477–495.

    Article  Google Scholar 

  • Hanya, G. (2004). Seasonal variations in the activity budget of Japanese macaques in the coniferous forest of Yakushima: Effects of food and temperature. American Journal of Primatology, 63, 165–177.

    Article  PubMed  Google Scholar 

  • Harrington, F. H., & Mech, L. D. (1983). Wolf pack spacing: Howling as a territory-independent spacing mechanism in a territorial population. Behavioural Ecology and Sociobiology, 12, 161–168.

    Article  Google Scholar 

  • Harris, T. R. (2007). Testing mate, resource and infant defense functions of intergroup aggression in nonhuman primates: Issues and methodology. Behaviour, 144, 1521–1535.

    Article  Google Scholar 

  • Harrison, M. (1985). Time budget of the green monkey, Cercopithecus sabaeus: Some optimal strategies. International Journal of Primatology, 6, 351–376.

    Article  Google Scholar 

  • Hendershott, R., Rawson, B., & Behie, A. (2018). Home range size and habitat use by cat Ba langurs (Trachypithecus poliocephalus) in a disturbed and fragmented habitat. International Journal of Primatology, 39, 547–566.

    Article  Google Scholar 

  • Hey, E. (1975). Thermal neutrality. British Medical Bulletin, 31, 69–74.

    Article  CAS  PubMed  Google Scholar 

  • Hill, R. A. (2006). Thermal constraints on activity scheduling and habitat choice in baboons. American Journal of Physical Anthropology, 129, 242–249.

    Article  PubMed  Google Scholar 

  • Holzmann, I., Agostini, I., & Di Bitetti, M. (2012). Roaring behavior of two syntopic howler species (Alouatta caraya and A. guariba clamitans): Evidence supports the mate defense hypothesis. International Journal of Primatology, 33, 338–355.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Hopkins, M. E. (2016). Mantled howler monkey spatial foraging decisions reflect spatial and temporal knowledge of resource distributions. Animal Cognition, 19, 387–403.

    Article  PubMed  Google Scholar 

  • Horwich, R., & Lyon, J. (1990). A Belizean rain forest: The community baboon sanctuary. Gays Mills, WI: Orangutan Press.

    Google Scholar 

  • Hurtado, R. R., Teichroeb, J. A., Bonnell, T. R., Hernández-Sarabia, R. U., Vickers, S. M., et al (2017). Primates adjust movement strategies due to changing food availability. Behavioural Ecology, 29, 368–376.

    Article  Google Scholar 

  • Kaplin, B. A. (2001). Ranging behavior of two species of guenons (Cercopithecus lhoesti and C. mitis doggetti) in the Nyungwe Forest reserve, Rwanda. International Journal of Primatology, 22, 521–548.

    Article  Google Scholar 

  • Kitchen, D. M. (2000). Aggression and assessment among social groups of Belizean black howler monkeys (Alouatta pigra). PhD thesis, University of Minnesota, Minneapolis.

  • Kitchen, D. M. (2004). Alpha male black howler monkey responses to loud calls: Effect of numeric odds, male companion behaviour and reproductive investment. Animal Behaviour, 67, 125–139.

    Article  Google Scholar 

  • Kitchen, D. M., Cheney, D. L., & Seyfarth, R. M. (2004). Factors mediating inter-group encounters in savannah baboons (Papio cyanocephalus ursinus). Behaviour, 141, 197–218.

    Article  Google Scholar 

  • Krebs, J. R., & Davies, N. B. (1993). An introduction to behavioral ecology (3rd ed.). Oxford: Blackwell.

    Google Scholar 

  • Langbauer, W. R. (2000). Elephant communication. Zoo Biology, 19, 425–445.

    Article  Google Scholar 

  • Laundré, J. W., Hernández, L., & Altendorf, K. B. (2001). Wolves, elk, and bison: Reestablishing the “landscape of fear” in Yellowstone National Park, USA. Canadian Journal of Zoology, 79, 1401–1409.

    Article  Google Scholar 

  • Lazaro-Perea, C. (2001). Intergroup interactions in wild common marmosets, Calithrix jacchus: Territorial defence and assessment of neighbours. Animal Behaviour, 62, 11–21.

    Article  Google Scholar 

  • Matsuda, I., Tuuga, A., & Higashi, S. (2009). Ranging behavior of proboscis monkeys in a riverine forest with special reference to ranging in inland forest. International Journal of Primatology, 30, 313–325.

    Article  Google Scholar 

  • McComb, K., Packer, C., & Pusey, A. (1994). Roaring and numerical assessment in contests between groups of female lions, Panthera leo. Animal Behaviour, 47, 379–387.

    Article  Google Scholar 

  • McKechnie, A. E., & Wolf, B. O. (2004). Partitioning of evaporative water loss in white-winged doves: Plasticity in response to short-term thermal acclimation. Journal of Experimental Biology, 207, 203–210.

    Article  PubMed  Google Scholar 

  • Milton, K. (1980). The foraging strategy of howler monkeys: A study of primate economics. New York: Columbia University Press.

    Google Scholar 

  • Miranda, J. M. D. (2004). Ecologia e conservação de Alouatta Guariba clamitans Cabrera, 1940 em Floresta Ombrófila Mista no estado do Paraná, Brasil. Curitiba: Universidade Federal do Paraná.

    Google Scholar 

  • Mitchell, B. R., Makagon, M. M., Jaeger, M. M., & Barrett, R. H. (2006). Information content of coyote barks and howls. Bioacoustics, 15, 289–314.

    Article  Google Scholar 

  • Muhle, C. B., & Bicca-Marques, J. C. (2007). Comportamento de termorregulação de bugios-ruivos (Alouatta guariba clamitans Cabrera, 1940 – Primates, Atelidae) no Parque Zoológico de Sapucaia do Sul, RS. In J. C. Bicca-Marques. In A Primatologia no Brasil (Vol. 10, pp. 423–432). Porto Alegre: Sociedade Brasileira de Primatologia.

    Google Scholar 

  • Mundry, R. (2011). Issues in information theory-based statistical inference—A commentary from a frequentist’s perspective. Behavioural Ecology and Sociobiology, 65, 57–68.

    Article  Google Scholar 

  • Nakagawa, S., & Schielzeth, H. (2013). A general and simple method for obtaining R2 from generalized linear mixed-effects models. Methods in Ecology and Evolution, 4, 133–142.

    Article  Google Scholar 

  • Nathan, R., Wayne, M., Getz, W. M., Revilla, E., Holyoak, M., et al (2008). A movement ecology paradigm for unifying organismal movement research. Proceedings of the National Academy Sciences of the USA, 105, 19052–19059.

    Article  Google Scholar 

  • Noser, R., & Byrne, R. W. (2007). Mental maps in chacma baboons (Papio urisnus): Using inter-group encounters as a natural experiment. Animal Cognition, 10, 331–340.

    Article  PubMed  Google Scholar 

  • Nowack, J., Wippich, M., Mzilikazi, N., & Dausmann, K. H. (2013). Surviving the cold, dry period in Africa: Behavioral adjustments as an alternative to heterothermy in the African lesser bushbaby (Galago moholi). International Journal of Primatology, 34, 49–64.

    Article  Google Scholar 

  • Oliveira, D. A. G., & Ades, C. (2004). Long-distance calls in Neotropical primates. Anais da Academia Brasileira de Ciências, 76, 393–398.

    Article  PubMed  Google Scholar 

  • Oliveira, E. M. (2003). Ecologia de Alouatta guariba clamitans (Humboldt, 1812–Primates, Atelidae) em mata estacional semidecídua no sudeste do Brasil. Dissertação (Mestrado em Ecologia e Conservação de Recursos Naturais), Universidade Federal de Uberlândia.

  • Overdorff, D. J., Strait, S. G., & Telo, A. (1997). Seasonal variation in activity and diet in a small-bodied folivorous primate, Hapalemur griseus, in southeastern Madagascar. American Journal of Primatology, 43, 211–223.

    Article  CAS  PubMed  Google Scholar 

  • Owen-Smith, N. (1994). Foraging responses of kudus to seasonal changes in food resources: Elasticity in constraints. Ecology, 75, 1050–1062.

    Article  Google Scholar 

  • Packer, C., Scheel, C., & Pusey, A. E. (1990). Why lions form groups: Food is not enough. American Naturalist, 136, 1–19.

    Article  Google Scholar 

  • Palacios, E., & Rodríguez, A. (2001). Ranging pattern and use of space in a group of red howler monkeys (Alouatta seniculus) in a southeastern Colombian rainforest. American Journal of Primatology, 55, 233–251.

    Article  CAS  PubMed  Google Scholar 

  • Peng-Fei, F., Wen, X., Sheng, H., & Xue-Long, J. (2009). Singing behavior and singing functions of black-crested gibbons (Nomascus concolor jingdongensis) at Mt. Wuliang, Central Yunnan, China. American Journal of Primatology, 71, 539–547.

    Article  Google Scholar 

  • Perret, M., & Aujard, F. (2001). Regulation by photoperiod of seasonal changes in body mass and reproductive function in gray mouse lemurs (Microcebus murinus): Differential responses by sex. International Journal of Primatology, 22, 5–24.

    Article  Google Scholar 

  • Perry, S. (1996). Intergroup encounters in wild white-faced capuchins (Cebus capucinus). International Journal of Primatology, 17, 309–330.

    Article  Google Scholar 

  • Pfefferle, D., West, P. M., Grinnell, J., Packer, C., & Fischer, J. (2007). Do acoustic features of lion, Panthera leo, roars reflect sex and male condition? Journal of the Acoustical Society of America, 121, 3947–3953.

    Article  PubMed  Google Scholar 

  • Pinto, A. C. B., Azevedo-Ramos, C., & de Carvalho Jr., O. (2003). Activity patterns and diet of the howler monkey Alouatta belzebul in areas of logged and unlogged forest in eastern Amazonia. Animal Biodiversity and Conservation, 26, 39–49.

    Google Scholar 

  • Pörtner, H. O., Bennett, A. F., Bozinovic, F., Clarke, A., Lardies, M. A., et al (2006). Trade-offs in thermal adaptation: The need for a molecular to ecological integration. Physiological and Biochemical Zoology, 79, 295–313.

    Article  PubMed  Google Scholar 

  • Potts, K. B., Baken, E., Levang, A., & Watts, D. P. (2016). Ecological factors influencing habitat use by chimpanzees at Ngogo, Kibale National Park, Uganda. American Journal of Primatology, 78, 432–440.

    Article  PubMed  Google Scholar 

  • Prates, H. M., & Bicca-Marques, J. C. (2008). Age–sex analysis of activity budget, diet, and positional behavior in Alouatta caraya in an orchard forest. International Journal of Primatology, 29, 703–715.

    Article  Google Scholar 

  • QGIS Development Team (2014). QGIS geographic information system. Open Source Geospatial Foundation Project

  • R Core Team (2017). R: A language and environment for statistical computing. Vienna: R Foundation for Statistical Computing.

    Google Scholar 

  • Rezende, E. L., Chappell, M. A., & Hammond, K. A. (2004). Cold-acclimation in Peromyscus: Temporal effects and individual variation in maximum metabolism and ventilatory traits. Journal of Experimental Biology, 207, 295–305.

    Article  PubMed  Google Scholar 

  • Risch, D., Clark, C. W., Corkeron, P. J., Elepfandt, A., Kovacs, K. M., et al (2007). Vocalizations of male bearded seals, Erignathus barbatus: Classification and geographical variation. Animal Behaviour, 73, 747–762.

    Article  Google Scholar 

  • Saj, T. L., & Sicotte, P. (2007). Predicting the competitive regime of female Colobus vellerosus from the distribution of food resources. International Journal of Primatology, 28, 315–336.

    Article  Google Scholar 

  • Salomão, R., Santana, A., & Costa Neto, S. (2012). Construction of importance value index of species using multivariate analysis for phytosociological analysis of dense rain forest. Floresta, 42, 115–128.

    Article  Google Scholar 

  • Saulitis, E. L., Matkin, C. O., & Fay, F. H. (2005). Vocal repertoire and acoustic behavior of the isolated AT1 killer whale subpopulation in southern Alaska. Canadian Journal of Zoology, 83, 1015–1029.

    Article  Google Scholar 

  • Seebacher, F., Elsey, R. M., & Trosclair, P. L. I. I. I. (2003). Body temperature null-distributions in large reptiles: Seasonal thermoregulation in the American alligator (Alligator mississippiensis). Physiological and Biochemical Zoology, 76, 348–359.

    Article  PubMed  Google Scholar 

  • Sekulic, R. (1982). The function of howling in red howler monkeys (Alouatta seniculus). Behaviour, 81, 38–54.

    Article  Google Scholar 

  • Symonds, M. R. E., & Moussalli, A. (2011). A brief guide to model selection, multimodel inference and model averaging in behavioural ecology using Akaike’s information criterion. Behavioural Ecology and Sociobiology, 65, 13–21.

    Article  Google Scholar 

  • Szekely, M., Petervari, E., & Szelenyi, Z. (2004). Orexigenic vs. anorexigenic peptides and feeding status in the modulation of fever and hypothermia. Frontiers in Bioscience, 9, 2746–2763.

    Article  CAS  PubMed  Google Scholar 

  • Terrien, J., Perret, M., & Aujard, F. (2011). Behavioral thermoregulation in mammals: A review. Frontiers in Bioscience, 16, 1428–1444.

    Article  Google Scholar 

  • Thompson, C. L., Williams, S. H., Glander, K. E., Teaford, M. F., & Vinyard, C. J. (2014). Body temperature and thermal environment in a generalized arboreal anthropoid, wild mantled howling monkeys (Alouatta palliata). The American Journal of Physical Anthropology, 154, 1–10.

    Article  PubMed  Google Scholar 

  • Treves, A. (2001). Reproductive consequences of variation in the composition of howler monkey (Alouatta spp.) groups. Behavioural Ecology and Sociobiology, 50, 61–71.

    Article  Google Scholar 

  • Watanuki, Y., & Nakayama, Y. (1993). Age difference in activity pattern of Japanese monkeys: Effects of temperature, snow, and diet. Primates, 34, 419–430.

    Article  Google Scholar 

  • Watts, D. P. (1988). Environmental influences on mountain gorilla time budgets. American Journal of Primatology, 15, 195–211.

    Article  Google Scholar 

  • West, B. T., Welch, K. B., & Galecki, A. T. (2014). Linear mixed models: A practical guide using statistical software. Boca Raton, FL: Chapman & Hall.

    Book  Google Scholar 

  • Westerterp, K. R. (2004). Diet induced thermogenesis. Nutrition & Metabolism, 1, 1–5.

    Article  CAS  Google Scholar 

  • Westerterp-Plantenga, M. S. (1999). Effects of extreme environments on food intake in human subjects. Proceedings of the Nutrition Society, 58, 791–798.

    Article  CAS  PubMed  Google Scholar 

  • Whitehead, J. M. (1987). Vocally mediated reciprocity between neighboring groups of mantled howling monkeys, Alouatta palliata palliata. Animal Behaviour, 35, 1615–1627.

    Article  Google Scholar 

  • Whitehead, J. M. (1989). The effect of the location of a simulated intruder on responses to long-distance vocalizations of mantled howling monkeys, Alouatta palliata palliata. Behaviour, 108, 73–103.

    Article  Google Scholar 

  • Whitehead, J. M. (1995). Vox AIouattinae: A preliminary survey of the acoustic characteristics of long-distance calls of howling monkeys. International Journal of Primatology, 16, 121–144.

    Article  Google Scholar 

  • Whittaker, R. H., & Woodwell, G. M. (1968). Dimension and production relations of trees and shrubs in the Brookhaven Forest, New York. Journal of Ecology, 56, 1–25.

    Article  Google Scholar 

  • Wich, S. A., & Nunn, C. L. (2002). Do male “long-distance calls” function in mate defense? A comparative study of long-distance calls in primates. Behavioural Ecology and Sociobiology, 52, 474–484.

    Article  Google Scholar 

  • Zuur, A. F., Ieno, E. N., & Elphick, C. S. (2010). A protocol for data exploration to avoid common statistical problems. Methods in Ecology and Evolution, 1, 3–14.

    Article  Google Scholar 

Download references

Acknowledgements

We dedicate this study to our dear colleague and friend Diana Angeles Ramirez Saldivar, who dedicated her life to study and protect wildlife in Mexico and Malaysia. We thank P. Cruz Miros and several volunteers and students for their invaluable help during fieldwork. La Flor de Catemaco granted permission to work at this site, and Ing. J. L. Ponce Puente facilitated our work in a variety of ways. We thank C. M. Schaffner for her kind review of a previous version of the manuscript. J. M. Setchell and two anonymous reviewers provided very helpful feedback and corrections on previous versions of the manuscript. This study was supported by Universidad Veracruzana and Conacyt (beca doctoral 592163; proyecto ciencia básica 254217). A. Rangel Negrín and P. A. D. Dias were supported by a grant to CA-UV-25 from the Dirección General de Desarrollo Académico e Innovación Educativa, Universidad Veracruzana (México) while preparing this manuscript. A. Rangel-Negrín and P. A. D. Dias thank Mariana and Fernando for constant support and inspiration to study primate behavior.

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Enrico Ceccarelli or Pedro Américo D. Dias.

Additional information

Handling Editor: Joanna M. Setchell

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ceccarelli, E., Negrín, A.R., Coyohua-Fuentes, A. et al. An Exploration of the Factors Influencing the Spatial Behavior of Mantled Howler Monkeys (Alouatta palliata). Int J Primatol 40, 197–213 (2019). https://doi.org/10.1007/s10764-018-0075-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10764-018-0075-1

Keywords

Navigation