Skip to main content

Advertisement

Log in

The Challenge of Coexistence: Changes in Activity Budget and Ranging Behaviour of Brown Howler Monkeys in Response to the Presence of Conspecifics and Heterospecifics

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

Abstract

The presence of other animals, both conspecifics and heterospecifics, is a major driving force for how animals organize themselves in space and time. Although theoretical models are available to explain the role of each in animal movement, fine-scale assessments of daily movement are scarce, particularly for primates. Hence, our goal was to assess whether and how the presence of conspecifics and heterospecifics influence spatiotemporal landscape use in two, wild, howler monkey (Alouatta guariba) groups. We followed the groups for 14 months in a large, continuous forest, during which we recorded their daily path length (DPL), home range, activity budget, feeding, and the presence of other groups (conspecifics) and other species (heterospecifics). The two groups differed in DPL, home range, proportion of fruits ingested, and time devoted to moving and resting. Partial least squares path modelling showed that variation in DPL was explained by the percentage of leaves or fruits ingested and by the presence of conspecifics, but not of heterospecifics. Group differences in several ecological variables emphasise the need to conduct further studies of space use with more groups in the same area to understand the underlying mechanisms of these differences. Moreover, our analysis shows that within-species interactions may be a stronger force in spatiotemporal organisation than interspecies interactions, at least in this folivorous primate. This is relevant from both a theoretical standpoint, and also when considering the consequences of habitat fragmentation and reduction. Deforestation leads to decreased resource availability and increased likelihood of encounters with conspecifics, which ultimately alters the proportion of food items ingested and increases the DPL, disrupting energy balance.

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. (1995). Foraging strategies of Yakushima macaques (Macaca fuscata yakui). International Journal of Primatology, 16(4), 595–609.

    Article  Google Scholar 

  • Agostini, I. (2009). Ecology and behavior of two howler monkey species (Alouatta guariba clamitans and Alouatta caraya) living in sympatry in northeastern Argentina. PhD dissertation, Università degli Studi di Roma “La Sapienza”, Rome, Italy.

  • Agostini, I., Holzmann, I., & Di Bitetti, M. S. (2010a). Ranging patterns of two syntopic howler monkey species (Alouatta guariba and A. caraya) in Northeastern Argentina. International Journal of Primatology, 31, 363–381. https://doi.org/10.1007/s10764-010-9390-x.

    Article  Google Scholar 

  • Agostini, I., Holzmann, I., & Di Bitetti, M. S. (2010b). Are howler monkey species ecologically equivalent? Trophic niche overlap in syntopic Alouatta guariba clamitans and Alouatta caraya. American Journal of Primatology, 72(2), 173–186. https://doi.org/10.1002/ajp.20775.

    Article  PubMed  Google Scholar 

  • Agostini, I., Holzmann, I., & Di Bitetti, M. S. (2012). Influence of seasonality, group size, and presence of a congener on activity patterns of howler monkeys. Journal of Mammalogy, 93(3), 645–657. https://doi.org/10.1644/11-MAMM-A-070.1.

    Article  Google Scholar 

  • Alba-Mejia, L., Caillaud, D., Montenegro, O. L., Sánchez-Palomino, P., & Crofoot, M. C. (2013). Spatiotemporal interactions among three neighboring groups of free-ranging white-footed tamarins (Saguinus leucopus) in Colombia. International Journal of Primatology, 34(6), 1281–1297. https://doi.org/10.1007/s10764-013-9740-6.

    Article  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Amato, K. R., Leigh, S. R., Kent, A., Mackie, R. I., Yeoman, C. J., Stumpf, R. M., ... & Garber, P. A. (2015). The gut microbiota appears to compensate for seasonal diet variation in the wild black howler monkey (Alouatta pigra). Microbial Ecology, 69(2), 434-443.

  • Aristizabal, J. F., Rothman, J. M., García-Fería, L. M., & Serio-Silva, J. C. (2016). Contrasting time-based and weight-based estimates of protein and energy intake of black howler monkeys (Alouatta pigra). American Journal of Primatology, 79(4), e22611. https://doi.org/10.1002/ajp.22611.

    Article  CAS  Google Scholar 

  • Arroyo-Rodríguez, V., & Mandujano, S. (2006). Forest fragmentation modifies habitat quality for Alouatta palliata. International Journal of Primatology, 27(4), 1079–1096.

    Article  Google Scholar 

  • Back, J. P., & Bicca-Marques, J. C. (2019). Supplemented howler monkeys eat less wild fruits, but do not change their activity budgets. American Journal of Primatology, 81(9), e23051. https://doi.org/10.1002/ajp.23051.

    Article  CAS  PubMed  Google Scholar 

  • Behie, A. M., & Pavelka, M. S. (2015). Fruit as a key factor in howler monkey population density: conservation implications. In M. M. Kowalewski, P. A. Garber, L. Cortés-Ortiz, B. Urbani, & D. Youlatos (Eds.), Howler monkeys Behavior, Ecology, and Conservation (pp. 357–382). Springer.

    Chapter  Google Scholar 

  • Behie, A. M., Pavelka, M. S., & Chapman, C. A. (2010). Sources of variation in fecal cortisol levels in howler monkeys in Belize. American Journal of Primatology, 72(7), 600–606. https://doi.org/10.1002/ajp.20813.

    Article  PubMed  Google Scholar 

  • Benítez-Malvido, J., & Martínez-Ramos, M. (2003). Impact of forest fragmentation on understory plant species richness in Amazonia. Conservation Biology, 17(2), 389–400.

    Article  Google Scholar 

  • Bersacola, E., Svensson, M. S., & Bearder, S. K. (2015). Niche partitioning and environmental factors affecting abundance of strepsirrhines in Angola. American Journal of Primatology, 77(11), 1179–1192. https://doi.org/10.1002/ajp.22457.

    Article  PubMed  Google Scholar 

  • Bestley, S., Jonsen, I. D., Hindell, M. A., Harcourt, R. G., & Gales, N. J. (2015). Taking animal tracking to new depths: synthesizing horizontal–vertical movement relationships for four marine predators. Ecology, 96(2), 417–427. https://doi.org/10.1890/14-0469.1

  • Bicca-Marques, J. C. (2003). How do howler monkeys cope with habitat fragmentation? In M. K. Larsh (Ed.), Primates in Fragments: Ecology and Conservation (pp. 283–303). Springer.

    Chapter  Google Scholar 

  • Bicca-Marques, J. C., Chaves, Ó. M., & Hass, G. P. (2020). Howler monkey tolerance to habitat shrinking: Lifetime warranty or death sentence? American Journal of Primatology, 82(4), 1–9. https://doi.org/10.1002/ajp.23089.

    Article  Google Scholar 

  • Bolt, L. M., Russell, D. G., & Schreier, A. L. (2021). Anthropogenic edges impact howler monkey (Alouatta palliata) feeding behaviour in a Costa Rican rainforest. Primates, 62(4), 647–657.

    Article  PubMed  Google Scholar 

  • Bonadonna, G., Zaccagno, M., Torti, V., Valente, D., De Gregorio, C., Randrianarison, R. M., Tan, C., Gamba, M., & Giacoma, C. (2020). Intra-and intergroup spatial dynamics of a pair-living singing primate, Indri indri: a multiannual study of three indri groups in Maromizaha Forest, Madagascar. International Journal of Primatology, 41(2), 224–245. https://doi.org/10.1007/s10764-019-00127-5

  • Bonvicino, C. R. (1989). Ecologia e comportamento de Alouatta belzebul (Primates: Cebidae) na mata atlântica. Revista Nordestina de Bilogia, 6, 149–179.

    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. https://doi.org/10.1023/A:1024680806342

  • Bryson-Morrison, N., Tzanopoulos, J., Matsuzawa, T., & Humle, T. (2017). Activity and habitat use of chimpanzees (Pan troglodytes versus) in the anthropogenic landscape of Bossou, Guinea, West Africa. American Journal of Primatology, 38(2), 282–302.

    Article  Google Scholar 

  • Buss G, Oklander LI, Bicca Marques JC, Hirano ZB, Chaves OM, Mendes SL et al., (2019). Brown howler monkey: Alouatta guariba Humboldt, 1812. In: Primates in Peril. The world’s 25 most endangered primates 2018-2020.

  • Caillaud, D., Crofoot, M. C., Scarpino, S. V., Jansen, P. A., Garzon-Lopez, C. X., et al (2010). Modelling the spatial distribution and fruiting pattern of a key tree species in a neotropical forest: methodology and potential applications. PLoS One, 5(11), e15002. https://doi.org/10.1371/journal.pone.0015002.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Carvalho Jr., O., Ferrari, S. F., & Strier, K. B. (2004). Diet of a muriqui group (Brachyteles arachnoides) in continuous primary forest. Primates, 45(3), 201–204. https://doi.org/10.1007/s10329-004-0079-7.

    Article  PubMed  Google Scholar 

  • Ceccarelli, E., Negrín, A. R., Coyohua-Fuentes, A., Canales-Espinosa, D., & Dias, P. A. D. (2019). An exploration of the factors influencing the spatial behavior of mantled howler monkeys (Alouatta palliata). International Journal of Primatology, 40(2), 197–213. https://doi.org/10.1007/s10764-018-0075-1.

    Article  Google Scholar 

  • Chapman, C. A. (1990). Ecological constraints on group size in three species of neotropical primates. Folia Primatologica, 55, 1–9.

    Article  CAS  Google Scholar 

  • Chapman, C. A., Chapman, L. J., Wangham, R., Hunt, K., Gebo, D., & Gardner, L. (1992). Estimators of fruit abundance of tropical trees. Biotropica, 527–531.

  • Chapman, C. A., Wrangham, R. W., & Chapman, L. J. (1995). Ecological constraints on group size: an analysis of spider monkey and chimpanzee subgroups. Behavioral Ecology and Sociobiology, 36, 59–70.

    Article  Google Scholar 

  • Chaves, Ó. M., Fernandes, F. A., Oliveira, G. T., & Bicca-Marques, J. C. (2019). Assessing the influence of biotic, abiotic, and social factors on the physiological stress of a large Neotropical primate in Atlantic forest fragments. Science of the Total Environment, 690, 705–716. https://doi.org/10.1016/j.scitotenv.2019.07.033.

    Article  CAS  PubMed  Google Scholar 

  • Chiarello, A. G. (1992). Dieta, padrão de atividades e área de vida de um grupo de bugios (Alouatta fusca) na Reserva de Santa Genebra, Campinas, SP. Masters' dissertation. Universidade Estadual de Campinas, Campinas, Brazil.

  • Clutton-Brock, T. H., & Harvey, P. H. (1977). Primate ecology and social organization. Journal of Zoology, 183(1), 1–39. https://doi.org/10.1111/j.1469-7998.1977.tb04171.x.

    Article  Google Scholar 

  • Clutton-Brock, T. H., Rose, K. E., & Guinness, F. E. (1997). Density–related changes in sexual selection in red deer. Proceedings of the Royal Society B: Biological Sciences, 264(1387), 1509–1516.

    Article  CAS  PubMed Central  Google Scholar 

  • Cooke, S. J., Hinch, S. G., Wikelski, M., Andrews, R. D., Kuchel, L. J., Wolcott, T. G., & Butler, P. J. (2004). Biotelemetry: a mechanistic approach to ecology. Trends in Ecology & Evolution, 19(6), 334–343.

    Article  Google Scholar 

  • Cornick, L. A., & Markowitz, H. (2002). Diurnal vocal patterns of the black howler monkey (Alouatta pigra) at Lamanai, Belize. Journal of Mammalogy, 83(1), 159–166. https://doi.org/10.1644/1545-1542(2002)083<0159:DVPOTB>2.0.CO;2.

    Article  Google Scholar 

  • Cortés-Ortiz, L., Bermingham, E., Rico, C., Rodrıguez-Luna, E., Sampaio, I., & Ruiz-Garcıa, M. (2003). Molecular systematics and biogeography of the Neotropical monkey genus, Alouatta. Molecular Phylogenetics and Evolution, 26(1), 64–81.

    Article  PubMed  Google Scholar 

  • Courbin, N., Fortin, D., Dussault, C., & Courtois, R. (2014). Logging-induced changes in habitat network connectivity shape behavioral interactions in the wolf–caribou–moose system. Ecological Monographs, 84(2), 265–285. https://doi.org/10.1890/12-2118.1

  • Creel, S., & Creel, N. M. (1995). Communal hunting and pack size in African wild dogs, Lycaon pictus. Animal Behaviour, 50(5), 1325–1339.

    Article  Google Scholar 

  • Cristóbal-Azkarate, J., Urbani, B., & Asensio, N. (2015). Interactions of howler monkeys with other vertebrates: a review. In M. M. Kowalewski, P. A. Garber, L. Cortés-Ortiz, B. Urbani, & D. Youlatos (Eds.), Howler Monkeys: Behavior, Ecology, and Conservation (pp. 141–164). Springer.

    Chapter  Google Scholar 

  • Cunha, R. G. T., & Jalles-Filho, E. (2007). The roaring of southern brown howler monkeys (Alouatta guariba clamitans) as a mechanism of active defence of borders. Folia Primatologica, 78(4), 259–271. https://doi.org/10.1159/000105545.

    Article  Google Scholar 

  • Cunningham, E., & Janson, C. (2007). Integrating information about location and value of resources by white faced-saki monkeys (Pithecia pithecia). Animal Cognition, 10, 293–304.

    Article  PubMed  Google Scholar 

  • Dasilva, G. L. (1992). The western black-and-white colobus as a low-energy strategist: activity budgets, energy expenditure and energy intake. Journal of Animal Ecology, 61, 79–91. https://doi.org/10.2307/5511.

    Article  Google Scholar 

  • de Cunha, R. G. T., de Oliveira, D. A. G., Holzmann, I., & Kitchen, D. M. (2015). Production of loud and quiet calls in howler monkeys. In M. M. Kowalewski, P. A. Garber, L. Cortés-Ortiz, B. Urbani, & D. Youlatos (Eds.), Howler monkeys: Adaptive radiation, systematics, and morphology (pp. 337–369). Springer.

    Chapter  Google Scholar 

  • Di Bitetti, M. S., Di Blanco, Y. E., Pereira, J. A., Paviolo, A., & Pírez, I. J. (2009). Time partitioning favors the coexistence of sympatric crab-eating foxes (Cerdocyon thous) and pampas foxes (Lycalopex gymnocercus). Journal of Mammalogy, 90(2), 479–490.

    Article  Google Scholar 

  • Di Fiore, A., Link, A., & Campbell, C. J. (2011). The atelines: behavioral and socioecological diversity in a New World monkey radiation. In C. J. Campbell, A. Fuentes, M. C. Mackinnon, S. K. Bearder, & R. M. Stumpf (Eds.), Primates in Perspective (pp. 155–188). Oxford University Press.

    Google Scholar 

  • Dias, L. G., & Strier, K. B. (2000). Agonistic encounters between muriquis, Brachyteles arachnoides hypoxanthus (Primates, Cebidae), and other animals at the Estação Biológica de Caratinga, Minas Gerais, Brazil. Neotropical Primates, 8, 138–141.

    Google Scholar 

  • dos Santos-Barnett, T. C., Cavalcante, T., Boyle, S. A., Matte, A. L., Bezerra, B. M., de Oliveira, T. G., & Barnett, A. A. (2022). Pulp fiction: why some populations of ripe-fruit specialists Ateles chamek and A. marginatus prefer insect-infested foods. International Journal of Primatology. https://doi.org/10.1007/s10764-022-00284-0.

  • Falótico, T., Mendonça-Furtado, O., Fogaça, M. D., Tokuda, M., Ottoni, E. B., & Verderane, M. P. (2021). Wild robust capuchin monkey interactions with sympatric primates. Primates, 62, 659–666. https://doi.org/10.1007/s10329-021-00913-x.

    Article  PubMed  Google Scholar 

  • Ferreguetti, A. C., Oliveira, A., Pereira, B. C., Santori, R. T., Geise, L., & Bergallo, H. G. (2020). Encounter rate and behavior of Alouatta guariba clamitans in the Ilha Grande State Park, Rio de Janeiro State, Brazil. Zoologia (Curitiba), 37, e36846. https://doi.org/10.3897/zoologia.37.e36846.

    Article  Google Scholar 

  • Fortes, V. B., Bicca-Marques, J. C., Urbani, B., Fernández, V. A., & Da Silva Pereira, T. (2015). Ranging behavior and spatial cognition of howler monkeys. In M. M. M. Kowalewski, P. A. Garber, L. Cortés-Ortiz, B. Urbani, & D. Youlatos (Eds.), Howler Monkeys: Behavior, Ecology, and Conservation (pp. 219–258). Springer.

    Chapter  Google Scholar 

  • Gibson, L., & Koenig, A. (2012). Neighboring groups and habitat edges modulate range use in Phayre’s leaf monkeys (Trachypithecus phayrei crepusculus). Behavioral Ecology and Sociobiology, 66(4), 633–643. https://doi.org/10.1007/s00265-011-1311-2.

    Article  Google Scholar 

  • Gómez-Posada, C., & Londoño, J. M. (2012). Alouatta seniculus: density, home range and group structure in a bamboo forest fragment in the Colombian Andes. Folia Primatologica, 83(1), 56–65. https://doi.org/10.1159/000339803

  • González-Solís, J., Guix, J. C., Mateos, E., & Llorens, L. (2001). Population density of primates in a large fragment of the Brazilian Atlantic rainforest. Biodiversity and Conservation, 10(8), 1267–1282. https://doi.org/10.1023/A:1016678126099.

    Article  Google Scholar 

  • Goodale, E., Beauchamp, G., & Ruxton, G. (2017). Mixed-species groups of animals: behavior, community structure, and conservation. Academic Press.

    Google Scholar 

  • Gross, M. (2017). Primates in peril. Current Biology, 27(12), 573–576. https://doi.org/10.1016/j.cub.2017.06.002.

    Article  CAS  Google Scholar 

  • Harris, T. R., & Chapman, C. A. (2007). Variation in diet and ranging of black and white colobus monkeys in Kibale National Park, Uganda. Primates, 48(3), 208–221.

    Article  PubMed  Google Scholar 

  • Hartig, F. (2017). DHARMa: Residual diagnostics for hierarchical (multi-level/mixed) regression models. https://cran.r-project.org/package=DHARMa. Accessed Mar 2023

  • Heymann, E. W., & Buchanan-Smith, H. M. (2000). The behavioural ecology of mixed-species troops of callitrichine primates. Biological Reviews, 75(2), 169–190.

    Article  CAS  PubMed  Google Scholar 

  • Hladik, C. M. (1978). Adaptive strategies of primates in relation to leaf eating. In G. G. Montgomery (Ed.), The Ecology of arboreal Folivores (pp. 373–395). Smithsonian Institution Press.

    Google Scholar 

  • Hobson, K. A., Norris, D. R., Kardynal, K. J., & Yohannes, E. (2019). Animal migration: a context for using new techniques and approaches. In Tracking animal migration with stable isotopes (pp. 1–23). Academic Press.

    Google Scholar 

  • Houle, A., Chapman, C. A., & Vickery, W. L. (2010). Intratree vertical variation of fruit density and the nature of contest competition in frugivores. Behavioral Ecology and Sociobiology, 64(3), 429–441.

    Article  Google Scholar 

  • Isbell, L. A. (1991). Contest and scramble competition: patterns of female aggression and ranging behavior among primates. Behavioral Ecology, 2(2), 143–155. https://doi.org/10.1093/beheco/2.2.143.

    Article  Google Scholar 

  • Izar, P., Verderane, M. P., Peternelli-Dos Santos, L., Mendonça-Furtado, O., Presotto, A., Tokuda, M., et al (2012). Flexible and conservative features of social systems in tufted capuchin monkeys: comparing the socioecology of Sapajus libidinosus and Sapajus nigritus. American Journal of Primatology, 74(4), 315–331. https://doi.org/10.1002/ajp.20968.

    Article  PubMed  Google Scholar 

  • Janmaat, K. R., de Guinea, M., Collet, J., Byrne, R. W., Robira, B., van Loon, E., Jang, H., Biro, D., Ramos-Fernandez, G., Ross, C., Presotto, A., Allritz, M., Alavi, S., & van Belle, S. (2021). Using natural travel paths to infer and compare primate cognition in the wild. Iscience, 24(4), 102343.

    Article  PubMed  PubMed Central  Google Scholar 

  • Janson, C. (1985). Aggressive competition and individual food consumption in wild brown capuchin monkeys (Cebus apella). Behavioral Ecology and Sociobiology, 18(2), 125–138.

    Article  Google Scholar 

  • Janson, C. H., & Van Schaik, C. P. (1988). Recognizing the many faces of primate food competition: methods. Behaviour, 105(1/2), 165–186.

    Google Scholar 

  • Jerusalinsky, L., Bicca-Marques, J.C., Neves, L.G., Alves, S.L., Ingberman, B., Buss, G., Fries, B.G., Alonso, A.C., da Cunha, R.G.T., Miranda, J.M.D., Talebi, M., de Melo, F.R., Mittermeier, R.A. & Cortes-Ortíz, L. (2021). Alouatta guariba (amended version of 2020 assessment). The IUCN Red List of Threatened Species. https://doi.org/10.2305/IUCN.UK.2021-1.RLTS.T39916A190417874.en

  • Jung, L., Mourthe, I., Grelle, C. E., Strier, K. B., & Boubli, J. P. (2015). Effects of local habitat variation on the behavioral ecology of two sympatric groups of brown howler monkey (Alouatta clamitans). PLoS One, 10(7), e0129789. https://doi.org/10.1371/journal.pone.0129789.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kamilar, J. M., & Beaudrot, L. (2013). Understanding primate communities: Recent developments and future directions. Evolutionary Anthropology, 22(4), 174–185. https://doi.org/10.1002/evan.21361.

    Article  PubMed  Google Scholar 

  • Kernohan, B. J., Gitzen, R. A., & Millspaugh, J. J. (2001). Analysis of animal space use and movements. In J. J. Millspaugh & J. M. Marzluff (Eds.), Radio tracking and animal populations (pp. 125–166). Academic Press.

    Chapter  Google Scholar 

  • Kitchen, D. W., Cunha, R. G. T., Holzmann, I., & Oliveira, D. A. G. (2015). Function of loud calls in howler monkeys. In M. M. Kowalewski, P. A. Garber, L. Cortés-Ortiz, B. Urbani, & D. Youlatos (Eds.), Howler monkeys: adaptive radiation, systematics, and morphology (pp. 369–402). Springer.

    Chapter  Google Scholar 

  • Knowlton, J. L., & Graham, C. H. (2010). Using behavioral landscape ecology to predict species’ responses to land-use and climate change. Biological Conservation, 143(6), 1342–1354. https://doi.org/10.1016/j.biocon.2010.03.011.

    Article  Google Scholar 

  • Kowalewski, M. M. (2007). Patterns of affiliation and co-operation in howler monkeys: an alternative model to explain social organization in non-human primates. PhD dissertation, University of Illinois, Urbana, USA.

  • Kurihara, Y., & Muto, H. (2021). Behavioral responses of Japanese macaques to playback-simulated intergroup encounters. Behavioural Processes, 182, 104279.

    Article  PubMed  Google Scholar 

  • Laundré, J. W., Hernández, L., & Ripple, W. J. (2010). The landscape of fear: ecological implications of being afraid. The Open Ecology Journal, 3, 1–7.

    Article  Google Scholar 

  • Markham, A. C., Alberts, S. C., & Altmann, J. (2012). Intergroup conflict: ecological predictors of winning and consequences of defeat in a wild primate population. Animal Behaviour, 84(2), 399–403. https://doi.org/10.1016/j.anbehav.2012.05.009.

    Article  Google Scholar 

  • Martins, M. M. (2008). Fruit diet of Alouatta guariba and Brachyteles arachnoides in Southeastern Brazil: comparison of fruit type, color, and seed size. Primates, 49(1), 1–8.

    Article  PubMed  Google Scholar 

  • Matsuda, I., Clauss, M., Tuuga, A., Sugau, J., Hanya, G., Yumoto, T., ... & Hummel, J. (2017). Factors affecting leaf selection by foregut-fermenting proboscis monkeys: new insight from in vitro digestibility and toughness of leaves. Scientific Reports, 7(1), 1-10.

  • Mendes, S. L. (1989). Estudo ecológico de Alouatta fusca (Primates: Cebidae) na Estação Biológica de Caratinga, MG. Revista Nordestina de Biologia, 71–104.

  • Milton, K. (1979). Factors influencing leaf choice by howler monkeys: a test of some hypotheses of food selection by generalist herbivores. The American Naturalist, 114(3), 362–378.

    Article  CAS  Google Scholar 

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

    Google Scholar 

  • Milton, K. (1998). Physiological ecology of howlers (Alouatta): energetic and digestive considerations and comparison with the Colobine. International Journal of Primatology, 19, 513–548. https://doi.org/10.1023/A:1020364523213.

    Article  Google Scholar 

  • Miranda, J., & Passos, F. C. (2004). Hábito alimentar de Alouatta guariba (Humboldt)(Primates, Atelidae) em Floresta de Araucária, Paraná, Brasil. Revista Brasileira de Zoologia, 21(4), 821–826.

    Article  Google Scholar 

  • Morellato, L. P. C., Talora, D. C., Takahasi, A., Bencke, C. C., Romera, E. C., & Zipparro, V. B. (2000). Phenology of Atlantic rain forest trees: a comparative study. Biotropica, 32(4b), 811–823. https://doi.org/10.1111/j.1744-7429.2000.tb00620.x.

    Article  Google Scholar 

  • Müller, C. A., & Manser, M. B. (2007). ‘Nasty neighbours’ rather than ‘dear enemies’ in a social carnivore. Proceedings of the Royal Society B: Biological Sciences, 274(1612), 959–965. https://doi.org/10.1098/rspb.2006.0222.

    Article  PubMed Central  Google Scholar 

  • Nagy, K. A., & Milton, K. (1979). Energy metabolism and food consumption by wild howler monkeys (Alouatta palliata). Ecology, 60(3), 475–480.

    Article  Google Scholar 

  • Nathan, R., et al (2022). Big-data approaches lead to an increased understanding of the ecology of animal movement. Science, 375(6582), eabg1780.

    Article  CAS  PubMed  Google Scholar 

  • Oklander L. I., Buss G., Bicca-Marques J.C., Hirano Z. B., Chaves O. M., Jardim M. M. A., Valença-Montenegro M. M., Mendes S. L., Neves L. G., Kowalewski M., Melo F. R., Rylands A. B., Jerusalinsky L. (2022). Brown howler monkey: Alouatta guariba Humboldt, 1812. In: Primates in Peril. The world’s 25 most endangered primates 2020-2022.

  • Pinto, L. P., Barnett, A. A., Bezerra, B. M., Boubli, J.-P., Bowler, M., Cardoso, N., Castelli, C., Rodriguez, M. J. O., Santos, R. R., Setz, E. Z., & Veiga, L. M. (2013). Why we know so little: the challenges of fieldwork on the pitheciines. In L. Veiga, A. Barnett, S. Ferrari, & M. Norconk (Eds.), Evolutionary Biology and Conservation of Titis, Sakis and Uacaris (pp. 145–150). Cambridge University Press.

    Chapter  Google Scholar 

  • Pisciotta, K. (2002). The Paranapiacaba forest fragment. In E. Mateos, J. C. Guix, A. Serra, & K. Pisciotta (Eds.), Censuses of vertebrates in a Brazilian Atlantic rainforest area: The Paranapiacaba fragment. University of Barcelona.

    Google Scholar 

  • Plano de Manejo. (2015). Plano de Manejo Parque Estadual Carlos Botelho. Unidades de Terreno do Parque. Available in <http://observatorio.wwf.org.br/site_media/upload/gestao/planoManejo/PM_PECarlosBotelho_parte_002.pdf>. Accessed: August 2021.

  • Powell, R. A. (2000). Animal home ranges and territories and home range estimators. In L. Boitoni & T. K. Fuller (Eds.), Research techniques in animal ecology: controversies and consequences (pp. 65–110). Columbia University Press.

    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. https://doi.org/10.1007/s10764-008-9257-6

  • Pruetz, J. D., & Isbell, L. A. (2000). Correlations of food distribution and patch size with agonistic interactions in female vervets (Chlorocebus aethiops) and patas monkeys (Erythrocebus patas) living in simple habitats. Behavioral Ecology and Sociobiology, 49(1), 38–47.

    Article  Google Scholar 

  • Prugh, L. R., Sivy, K. J., Mahoney, P. J., Ganz, T. R., Ditmer, M. A., van de Kerk, M., ... & Montgomery, R. A. (2019). Designing studies of predation risk for improved inference in carnivore-ungulate systems. Biological Conservation, 232, 194-207.

  • Pyke, G. (2019). Animal movements: an optimal foraging approach. In Encyclopedia of animal behavior (pp. 149–156). Elsevier Academic Press.

    Chapter  Google Scholar 

  • R Core Team. (2019). R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing https://www.R-project.org. Accessed Mar 2023

  • Raño, M., Kowalewski, M. M., Cerezo, A. M., & Garber, P. A. (2016). Determinants of daily path length in black and gold howler monkeys (Alouatta caraya) in northeastern Argentina. American Journal of Primatology, 78(8), 825–837. https://doi.org/10.1002/ajp.22548.

    Article  PubMed  Google Scholar 

  • Reynoso-Cruz, J. E., Rangel-Negrín, A., Coyohua-Fuentes, A., Canales-Espinosa, D., & Dias, P. A. D. (2016). Measures of food intake in mantled howling monkeys. Primates, 57(2), 161–166. https://doi.org/10.1007/s10329-016-0513-7.

    Article  PubMed  Google Scholar 

  • Ribeiro, M. C., Metzger, J. P., Martensen, A. C., Ponzoni, F. J., & Hirota, M. M. (2009). The Brazilian Atlantic Forest: How much is left, and how is the remaining forest distributed? Implications for conservation. Biological Conservation, 142(6), 1141–1153. https://doi.org/10.1016/j.biocon.2009.02.021.

    Article  Google Scholar 

  • Ries, L., & Sisk, T. D. (2004). A predictive model of edge effects. Ecology, 85(11), 2917–2926.

    Article  Google Scholar 

  • Rímoli, J., Nantes, R. D. S., & Júnior, A. L. (2012). Diet and activity patterns of black howler monkeys Alouatta caraya (Humboldt, 1812, Primates, Atelidae) in ecotone Cerrado-Pantanal in the left bank of Aquidauana River, Mato Grosso do Sul, Brazil. Oecologia Australis, 16, 933–948. https://doi.org/10.4257/oeco.2012.1604.15.

    Article  Google Scholar 

  • Rosa, M. R., Brancalion, P. H., Crouzeilles, R., Tambosi, L. R., Piffer, P. R., Lenti, F. E., ... & Metzger, J. P. (2021). Hidden destruction of older forests threatens Brazil’s Atlantic Forest and challenges restoration programs. Science Advances, 7(4), eabc4547. https://doi.org/10.1126/sciadv.abc4547

  • Rose, L. M., Perry, S., Panger, M. A., Jack, K., Manson, J. H., Gros-Louis, J., Mackinnon, C. K., & Vogel, E. (2003). Interspecific interactions between Cebus capucinus and other species: data from three Costa Rican sites. International Journal of Primatology, 24(4), 759–796. https://doi.org/10.1023/A:1024624721363

  • Rosenberger, A. L., & Strier, K. B. (1989). Adaptive radiation of the ateline primates. Journal of Human Evolution, 18(7), 717–750.

    Article  Google Scholar 

  • Rowley, M. H., & Christian, J. J. (1976). Interspecific aggression between Peromyscus and Microtus females: A possible factor in competitive exclusion. Behavioral Biology, 16(4), 521–525.

    Article  CAS  PubMed  Google Scholar 

  • Sanchez, G. (2013). PLS Path Modeling with R. Trowchez Editions. Berkeley, 2013. Available in: http://www.gastonsanchez.com/PLS Path Modeling with R.pdf. Accessed October 2022.

  • Sanz, C. M., Strait, D., Ayina, C. E., Massamba, J. M., Ebombi, T. F., Kialiema, S. N., ... & Morgan, D. B. (2022). Interspecific interactions between sympatric apes. Iscience, 25(10), 105059.

  • Scarry, C. J. (2013). Between-group contest competition among tufted capuchin monkeys, Sapajus nigritus, and the role of male resource defence. Animal Behavior, 85(5), 931–939. https://doi.org/10.1016/j.anbehav.2013.02.013.

    Article  Google Scholar 

  • Schoener, T. W. (1974). Resource Partitioning in Ecological Communities: Research on how similar species divide resources helps reveal the natural regulation of species diversity. Science, 185(4145), 27–39.

    Article  CAS  PubMed  Google Scholar 

  • Schreier, A. L., Bolt, L. M., Russell, D. G., Readyhough, T. S., Jacobson, Z. S., Merrigan-Johnson, C., & Coggeshall, E. M. (2021). Mantled howler monkeys (Alouatta palliata) in a Costa Rican forest fragment do not modify activity budgets or spatial cohesion in response to anthropogenic edges. Folia Primatologica, 92(1), 49–57. https://doi.org/10.1159/000511974.

    Article  Google Scholar 

  • Sekulic, R. (1982). The function of howling in red howler monkeys (Alouatta seniculus). Behaviour, 38-54. https://doi.org/10.1163/156853982X00517.

  • Sha, J. C. M., & Hanya, G. (2013). Diet, activity, habitat use, and ranging of two neighboring groups of food-enhanced long-tailed macaques (Macaca fascicularis). American Journal of Primatology, 75(6), 581–592. https://doi.org/10.1002/ajp.22137.

    Article  PubMed  Google Scholar 

  • Sih, A. (2005). Predator-prey space use as an emergent outcome of a behavioral response race. Ecology of Predator-Prey Interactions, 256, 78.

    Google Scholar 

  • Singh, M. R., Singh, M., Ananada Kumar, M., Kumar, H. N., Sharma, A. K., & Sushma, H. S. (2000). Niche separation in sympatric lion-tailed macaques (Macaca silenus) and Nilgiri langur (Presbytis johnii) in an Indian tropical rain forest. Primate Report, 58, 83–95. http://repository.ias.ac.in/89653/1/13p.pdf. Accessed Mar 2023

  • Snaith, T. V., & Chapman, C. A. (2007). Primate group size and interpreting socioecological models: do folivores really play by different rules? Evolutionary Anthropology, 16(3), 94–106. https://doi.org/10.1002/evan.20132.

    Article  Google Scholar 

  • Sobral, G., Siqueira Martins, G., & Oliveira, C. A. (2022). Thermal imaging aids behavioural studies: the case of a diurnal neotropical primate. Mastozoologia Neotropical, 29(1), e0622. https://doi.org/10.31687/saremMN.22.29.1.07.e0622.

    Article  Google Scholar 

  • Sobroza, T. V., Pequeno, P. A. C. L., Gordo, M., Kinapp, N. M., Barnett, A. A., & Spironello, W. (2021). Does co-occurrence drive vertical niche partitioning in parapatric tamarins (Saguinus spp.)? Austral Ecology, 46, 1335–1342. https://doi.org/10.1111/aec.13085.

    Article  Google Scholar 

  • Strier, K. B. (1987). Ranging behavior of woolly spider monkeys, or muriquis, Brachyteles arachnoides. International Journal of Primatology, 8(6), 575–591.

    Article  Google Scholar 

  • Strier, K. B. (1989). Effects of patch size on feeding associations in muriquis (Brachyteles arachnoides). Folia Primatologica, 52, 70–77. https://doi.org/10.1159/000156383.

    Article  CAS  Google Scholar 

  • Talebi, M., Bastos, A., & Lee, P. C. (2005). Diet of southern muriquis in continuous Brazilian Atlantic Forest. International Journal of Primatology, 26(5), 1175–1187. https://doi.org/10.1007/s10764-005-6463-3.

    Article  Google Scholar 

  • Teichroeb, J. A., & Sicotte, P. (2009). Test of the ecological-constraints model on ursine colobus monkeys (Colobus vellerosus) in Ghana. American Journal of Primatology, 71(1), 49–59. https://doi.org/10.1002/ajp.20617.

    Article  PubMed  Google Scholar 

  • Temeles, E. J. (1994). The role of neighbours in territorial systems: when are they'dear enemies'? Animal Behavior, 47(2), 339–350. https://doi.org/10.1006/anbe.1994.1047.

    Article  Google Scholar 

  • Terborgh, J. (2014). Five new world primates. Princeton University Press.

    Google Scholar 

  • Van Belle, S., & Estrada, A. (2020). The influence of loud calls on intergroup spacing mechanism in black howler monkeys (Alouatta pigra). International Journal of Primatology, 41(2), 265–286.

    Article  Google Scholar 

  • Van Belle, S., Estrada, A., & Garber, P. A. (2013). Spatial and diurnal distribution of loud calling in black howlers (Alouatta pigra). International Journal of Primatology, 34(6), 1209–1224. https://doi.org/10.1007/s10764-013-9734-4.

    Article  Google Scholar 

  • Vogel, E. R., & Janson, C. H. (2007). Predicting the frequency of food-related agonism in white-faced capuchin monkeys (Cebus capucinus), using a novel focal-tree method. American Journal of Primatology, 69(5), 533–550. https://doi.org/10.1002/ajp.20368.

    Article  CAS  PubMed  Google Scholar 

  • Walter, H. (1973). Vegetation of the Earth in Relation to Climate and the Eco-Physiological Conditions. Springer.

    Google Scholar 

  • Worton, B. J. (1995). A convex hull-based estimator of home-range size. Biometrics, 51, 1206–1215. https://doi.org/10.2307/2533254.

    Article  Google Scholar 

Download references

Acknowledgments

A preliminary version of this paper was presented to a committee in partial fulfilment of the requirements for the PhD degree. Hence, we are indebted to committee members J.C. Bicca-Marques, P. Izar, R. G. Ferreira, and A. Araújo for their important suggestions, which greatly increased the quality increase of this paper. We are also thankful to A. Caccavo for producing the home range figure; I. Campell from Stackoverflow for enabling the calculation of DPL using a simple R code. We would also thank L. Wiseman-Jones for her help in proofreading the English language of this paper. Finally, the authors thank the anonymous referees, the Associate Editor and the Editor-in-Chief, for reviews that greatly enhanced the quality of the manuscript. Fieldwork was conducted within the current legal norms in Brazil (Instituto Chico Mendes de Conservação da Biodiversidade License number 55826-1; Secretaria do Meio Ambiente - Fundação Florestal authorisantion number 009.188/2016; SISGEN register number A165E11).

Inclusion and diversity statement

• One or more of the authors of this paper self-identifies as an underrepresented ethnic minority in science.

• One or more of the authors of this paper self-identifies as a member of the LGBTQ+ community.

• While citing references scientifically relevant for this work, we also actively worked to promote gender balance in our reference list.

Funding

This study was financed in part by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior – Brasil (CAPES) – Finance Code 001 (to GS), and part by FAPESP (#2017/07954-0) (to LFF).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Gisela Sobral.

Additional information

Handling Editor: Addisu Mekonnen

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Sobral, G., Fuzessy, L.F. & de Oliveira, C.A. The Challenge of Coexistence: Changes in Activity Budget and Ranging Behaviour of Brown Howler Monkeys in Response to the Presence of Conspecifics and Heterospecifics. Int J Primatol 44, 558–580 (2023). https://doi.org/10.1007/s10764-023-00359-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10764-023-00359-6

Keywords

Navigation