International Journal of Primatology

, Volume 40, Issue 3, pp 374–392 | Cite as

Patterns of Sleeping Site and Sleeping Tree Selection by Black-and-Gold Howler Monkeys (Alouatta caraya) in Northern Argentina

  • Melina V. BrividoroEmail author
  • Martin M. Kowalewski
  • Clara J. Scarry
  • Luciana I. Oklander


The selection of sleeping sites and sleeping trees in nonhuman primates is related to social and ecological factors. We investigate the role of body stability, risk of parasite infection, access to food, and range defense in the sleeping behavior of black-and-gold howler monkeys (Alouatta caraya) in northern Argentina. We collected data for 4 groups over 12 mo (198 study days). Black-and-gold howlers used 12 of 36 available tree species as sleeping trees. In comparison to the available trees, sleeping trees had a larger diameter at breast height, greater total height, and greater height of the lowest branch. Monkeys used large branches to sleep more frequently than small branches. Our results suggest that howlers avoided using the same sleeping tree on consecutive nights. At sleeping trees, individuals descended to lower branches to defecate. Sleeping sites were close to morning feeding sites. More sleeping sites were located in areas of range overlap between groups (75%) than in exclusive-use areas (25%), and sleeping sites located in overlapping areas were used more frequently when neighboring groups were nearby than when they were far away. Our results suggest that body stability, parasite avoidance, access to food, and range defense all affect the selection of sleeping sites.


Feeding sites Parasite avoidance Range defense Sleeping habits Stability 



We are grateful to our field assistants and professionals and technicians of the EBCo for their help in the collection of data: V. González, R. Martinez, T. Martinez, M. Martinez, L. Ramos, Y. Rodríguez, S. van Remoortere, M. L. Gelín, D. Fergnani, S. Pérez Salles, L. B. Boccolini, V. Manrique Bustamante, and P. Fernandez. We thank Ilaria Agostini for constructive comments and editorial corrections. We thank the editors and reviewers for their contributions on earlier drafts of the manuscript. This project was supported by the ABS Developing Nations Award to M. V. Brividoro and doctoral fellowship CONICET to M. V. Brividoro. L. I. Oklander and M. M. Kowalewski are members of Carrera de Investigador Científico CONICET. M. M. Kowalewski wants to acknowledge Bruno K. for help in exploring infant sleeping patterns. M. V. Brividoro thanks Ariel and Lorenzo for their love and patience.

Author Contributions

MVB, MMK, LIO originally formulate the idea, MVB conducted fieldwork, MVB, MMK, CJS performed statistical analyses and MVB, MMK, CJS and LIO wrote the manuscript.


  1. Albert, A., Savini, T., & Huynen, M. C. (2011). Sleeping site selection and presleep behavior in wild pigtailed macaques. American Journal of Primatology, 73, 1222–1230.CrossRefGoogle Scholar
  2. Altmann, S. A. (1974a). Baboon, space, time, and energy. American Zoologist, 14, 221–248.CrossRefGoogle Scholar
  3. Altmann, J. (1974b). Observational study of behavior: Sampling methods. Behaviour, 49, 227–267.CrossRefGoogle Scholar
  4. Anderson, D. J. (1982). The home range: A new nonparametric estimation technique. Ecology, 63, 103–112.CrossRefGoogle Scholar
  5. Anderson, J. R. (1984). Ethology and ecology of sleep in monkeys and apes. Advances in the Study of Behavior, 14, 165–229.CrossRefGoogle Scholar
  6. Anderson, J. R. (1998). Sleep, sleeping sites, and sleep-related activities: Awakening to their significance. American Journal of Primatology, 46, 63–75.CrossRefGoogle Scholar
  7. Anderson, J. R., & Mc Grew, W. C. (1984). Guinea baboons (Papio papio) at a sleeping site. American Journal of Primatology, 6(1), 1–14.CrossRefGoogle Scholar
  8. Aquino, R., & Encarnacion, F. (1986). Characteristics and use of sleeping sites in Aotus (Cebidae: Primates) in the Amazon lowlands of Peru. American Journal of Primatology, 11, 319–331.CrossRefGoogle Scholar
  9. Barnett, A. A., Shaw, P., Spironello, W. R., MacLarnon, A., & Ross, C. (2012). Sleeping site selection by golden-backed uacaris, Cacajao melanocephalus ouakary (Pitheciidae), in Amazonian flooded forests. Primates, 53, 273–285.CrossRefGoogle Scholar
  10. Bergeson, D. J. (1998). Patterns of Suspensory Feeding in Alouatta palliata, Ateles geoffroyi, and Cebus capucinus. In: E. Strasser, J.G. Fleagle, A.L. Rosenberger, H.M. McHenry (Eds.). Primate Locomotion. Boston: Springer.Google Scholar
  11. 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 Antropology, 106, 533–546.CrossRefGoogle Scholar
  12. Braza, F., Alvarez, F., & Azcarate, T. (1981). Behaviour of the red howler monkey (Alouatta seniculus) in the llanos of Venezuela. Primates, 22(4), 459–473.CrossRefGoogle Scholar
  13. Brividoro, M. V. (2018). Influencia de factores socio-ecológicos en el agrupamiento para el descanso nocturno y la selección y uso de sitios dormideros del mono carayá (Alouatta caraya). PhD thesis, Universidad Nacional de La Plata-Facultad de Ciencias Naturales y Museo.Google Scholar
  14. Brotcorne, F., Maslarov, C., Wandia, I. N., Fuentes, A., Beudels-Jamar, R. C., & Hiynen, M. C. (2014). The role of anthropic, ecological, and social factors in sleeping site choice by long-tailed macaques (Macaca fascicularis). American Journal of Primatology, 76, 1140–1150.CrossRefGoogle Scholar
  15. Capellini, I., Nunn, C. L., McNamara, P., Preston, B. T., & Barton, R. A. (2008). Energetic constraints, not predation, influence the evolution of sleep patterning in mammals. Functional Ecology, 22, 847–853.CrossRefGoogle Scholar
  16. Chapman, C. A. (1989). Primate seed dispersal: The fate of dispersed seeds. Biotropica, 21(2), 148–154.CrossRefGoogle Scholar
  17. Cheyne, S. M., Höing, A., Rinear, J., & Sheeran, L. K. (2012). Sleeping site selection by agile gibbons: The influence of tree stability, fruit availability and predation risk. Folia Primatologica, 83(3–6), 299–311.CrossRefGoogle Scholar
  18. Day, R. T., & Elwood, R. W. (1999). Sleeping site selection by the golden-handed tamarin Saguinus midas midas: The role of predation risk, proximity to feeding sites, and territorial defence. Ethology, 105, 1035–1051.CrossRefGoogle Scholar
  19. Di Bitetti, M. S., Luengos Vidal, E. M., Baldovino, M. C., & Benesovsky, V. (2000). Sleeping site preferences in tufted capuchin monkeys (Cebus apella nigritus). American Journal of Primatology, 50, 257–274.CrossRefGoogle Scholar
  20. Di Fiore, A. (2002). Predator sensitive foraging in ateline primates. In L. E. Miller (Ed.), Eat or be eaten: Predator sensitive foraging among primates (pp. 242–267). Cambridge: Cambridge University Press.CrossRefGoogle Scholar
  21. Di Fiore, A., & Campbell, C. J. (2007). The Atelines: 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: Oxford University Press.Google Scholar
  22. Di Fiore, A., Link, A., & Campbell, C. J. (2011). The Atelines: Behavioral and socioecological diversity in a New World monkeys radiation. In C. J. Campbell, A. Fuentes, K. C. MacKinnon, S. Bearder, & R. Stumpf (Eds.), Primates in Perspective, part two: The Primates (2nd ed., pp. 155–188). Oxford: Oxford University Press.Google Scholar
  23. Duszynski, W. D., Wilson, W. D., Upton, S. J., & Levine, N. D. (1999). Coccidia (Apicomplexa: Eimeriidae) in the primates and the Scandentia. International Journal of Primatology, 20(5), 761–795.CrossRefGoogle Scholar
  24. Fan, P. F., & Jiang, X. L. (2008). Sleeping sites, sleeping trees, and sleep-related behaviors of black crested gibbons (Nomascus concolor jingdongensis) at Mt. Wuliang, Central Yunnan, China. American Journal of Primatology, 70, 153–160.CrossRefGoogle Scholar
  25. Fei, H. L., Scott, M. B., Zhang, W., Ma, C. Y., Xiang, Z. F., & Fan, P. F. (2012). Sleeping tree selection of Cao Vit gibbon (Nomascus nasutus) living in degraded karst Forest in Bangliang, Jingxi, China. American Journal of Primatology, 74, 998–1005.CrossRefGoogle Scholar
  26. Feilen, K. L., & Marshall, A. J. (2014). Sleeping site selection by proboscis monkeys (Nasalis larvatus) in West Kalimantan, Indonesia. American Journal of Primatology, 76(12), 1127–1139.CrossRefGoogle Scholar
  27. Fernández, V. A. (2014). Ecología nutricional del monos aullador negro y dorado (Alouatta caraya) en el límite sur de su distribución. PhD thesis, Universidad Nacional de Buenos Aires, Facultad de Ciencias Exactas y Naturales.Google Scholar
  28. Freeland, W. J. (1976). Pathogens and the evolution of primate sociality. Biotropica, 8(1), 12–24.CrossRefGoogle Scholar
  29. Freeland, W. J. (1980). Mangabey (Cerocebus Albigena) movement patterns in relation to food availability and fecal contamination. Ecology, 61(6), 1297–1303.CrossRefGoogle Scholar
  30. Fruth, B., & McGrew, W. C. (1998). Resting and nesting in primates: Behavioral ecology of inactivity. American Journal of Primatology, 46, 3–5.CrossRefGoogle Scholar
  31. Garber, P. A., & Kowalewski, M. K. (2011). Collective action and male affiliation in howler monkeys (Alouatta caraya). In R. W. Sussman & C. R. Cloninger (Eds.), Origins of altruism and cooperation (pp. 145–165). New York: Springer Science+Business Media.CrossRefGoogle Scholar
  32. Gauthier-Clerc, M., Tamisier, A., & Cézilly, F. (2000). Sleep-vigilance trade-off in gadwall during the winter period. Condor, 102, 307–313.CrossRefGoogle Scholar
  33. Gennuso, M. S., Brividoro, M., Pavé, R., Raño, M., & Kowalewski, M. (2018). Social play among black and gold howler monkey (Alouatta caraya) immatures during intergroup encounters. American Journal of Primatology, 80, e22909. Scholar
  34. Gilbert, K. A. (1997). Red howling monkey use of specific defecation sites as a parasite avoidance strategy. Animal Behavior, 54, 451–455.CrossRefGoogle Scholar
  35. Hausfater, G., & Meade, B. J. (1982). Alternation of sleeping groves by yellow baboons (Papio cynocephalus) as strategy for parasite avoidance. Primates, 23(2), 287–297.CrossRefGoogle Scholar
  36. Heymann, E. W. (1995). Sleeping habits of tamarins, Saguinus mystax and Saguinus fuscicollis (Mammalia; primates; Callitrichidae), in North-Eastern Peru. Journal of Zoology, 237, 211–226.CrossRefGoogle Scholar
  37. Holzmann, I., Agostini, I., & Di Bitetti, M. S. (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.CrossRefGoogle Scholar
  38. 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(1), 125–139.CrossRefGoogle Scholar
  39. Kowalewski, M. M., & Garber, P. A. (2010). Mating promiscuity and reproductive tactics in female black and gold howler monkeys (Alouatta caraya) inhabiting an island on the Parana River, Argentina. American Journal of Primatology, 72, 734–748.CrossRefGoogle Scholar
  40. Kowalewski, M. M., & Garber, P. A. (2015). Solving the collective action problem during intergroup encounters: The case of black and gold howler monkeys (Alouatta caraya). In M. M. Kowalewski, P. A. Garber, L. Cortés-Ortiz, B. Urbani, & D. Youlatos (Eds.), Howler monkeys: Behavior, ecology, and conservation (pp. 165–189). Developments in Primatology: Progress and Prospects). New York: Springer Science+Business Media.CrossRefGoogle Scholar
  41. Kowalewski, M. M., & Gillespie, T. R. (2009). Ecological and anthropogenic influences on patterns of parasitism in free-ranging primates: A meta-analysis of the genus Alouatta. In P. Garber, A. Estrada, J. C. Bicca-Marques, E. W. Heymann, & K. B. Strier (Eds.), South American primates Developments in primatology: Progress and prospects (pp. 433–461). New York: Springer Science+Business Media.Google Scholar
  42. Kowalewski, M., & Zunino, G. E. (2005). The parasite behavior hypothesis and the use of sleeping sites by black howler monkeys (Alouatta caraya) in a discontinuous forest. Neotropical Primates, 13(1), 22–26.CrossRefGoogle Scholar
  43. Li, D., Grueter, C. C., Ren, B., Qihai, Z., Ming, L. I., Peng, Z., & Wei, F. (2006). Characteristics of night-time sleeping places selected by golden monkeys (Rhinopithecus bieti) in the Samage Forest, Baima Snow Mountain nature reserve, China. Integrative Zoology, 1, 141–152.CrossRefGoogle Scholar
  44. Martines-Mota, R. (2015). The effects of habitat disturbance, host traits, and host physiology on patterns of gastrointestinal parasite infection in black howler monkeys (Alouatta pigra). PhD thesis, University of Illinois at Urbana-Champaign.Google Scholar
  45. Mendes Pontes, A. R., & Soares, M. L. (2005). Sleeping sites of common marmosets (Callithrix jacchus) in defaunated urban forest fragments: A strategy to maximize food intake. Journal of Zoology, 266, 55–63.CrossRefGoogle Scholar
  46. Milton, K. (1980). The foraging strategy of howler monkeys: A study in primate economics. New York: Columbia University Press.Google Scholar
  47. Mittermeier, R. A. (1973). Group activity and population dynamics of the howler monkey on Barro Colorado Island. Primates, 14(1), 1–19.CrossRefGoogle Scholar
  48. Oklander, L. I., Kowalewski, M., & Corach, D. (2014). Male reproductive strategies in black and gold howler monkeys (Alouatta caraya). American Journal of Primatology, 76(1), 43–55.CrossRefGoogle Scholar
  49. Phoonjampa, R., Koenig, A., Borries, C., Gale, G. A., & Savini, T. (2010). Selection of sleeping trees in pileated gibbons (Hylobates pileatus). American Journal of Primatology, 72, 617–625.Google Scholar
  50. R Core Team. (2016). R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing.Google Scholar
  51. Ramakrishnan, U., & Coss, R. G. (2001). Strategies used by bonnet macaques (Macaca radiata) to reduce predation risk while sleeping. Primates, 42(3), 193–206.CrossRefGoogle Scholar
  52. 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.CrossRefGoogle Scholar
  53. Reichard, U. (1998). Sleeping sites, sleeping places, and presleep behavior of gibbons (Hylobates lar). American Journal of Primatology, 46, 35–62.CrossRefGoogle Scholar
  54. Rumiz, D. I. (1990). Alouatta caraya: Population density and demography in northern Argentina. American Journal of Primatology, 21, 279–294.CrossRefGoogle Scholar
  55. Sekulic, R. (1982). Daily and seasonal patterns of roaring and spacing in four red howler Alouatta seniculus troops. Folia Primatologica, 39, 22–48.CrossRefGoogle Scholar
  56. Siegel, J. M. (2001). The REM sleep-memory consolidation hypothesis. Science, 294, 1058–1063.CrossRefGoogle Scholar
  57. Siegel, J. M. (2005). Clues to the functions of mammalian sleep. Nature, 437(7063), 1264–1271.CrossRefGoogle Scholar
  58. Smith, A. C., Knogge, C., Huck, M., Lottker, P., Buchanan-Smith, H. M., & Heymann, E. W. (2007). Long-term patterns of sleeping site use in wild saddleback (Saguinus fuscicollis) and mustached tamarins (S. mystax): Effects of foraging, thermoregulation, predation, and resource defense constraints. American Journal of Physical Anthropology, 134(3), 340–353.CrossRefGoogle Scholar
  59. Smith, R. L., Hayes, S. E., Smith, P., & Dickens, J. K. (2017). Sleeping site preferences in Sapajus cay Illiger 1815 (primates: Cebidae) in a disturbed fragment of the upper Paraná Atlantic Forest, rancho Laguna Blanca, eastern Paraguay. Primates, 59(1), 79–88.CrossRefGoogle Scholar
  60. Stuart, M. D., Greenspan, L. L., Glander, K. E., & Clarke, M. R. (1990). A coprological survey of parasites of wild mantled howling monkeys, Alouatta palliata palliata. Journal of Wildlife Diseases, 26(84), 547–549.CrossRefGoogle Scholar
  61. Takahashi, H. (1997). Huddling relationships in night sleeping groups among wild Japanese macaques in Kinkazan Island during winter. Primates, 38(1), 57–68.CrossRefGoogle Scholar
  62. Teichroeb, J. A., Holmes, T. D., & Sicotte, P. (2012). Use of sleeping trees by ursine colobus monkeys (Colobus vellerosus) demonstrates the importance of nearby food. Primates, 53(3), 287–296.CrossRefGoogle Scholar
  63. Tenaza, R., & Tilson, R. L. (1985). Human predation and Kloss’s gibbon (Hylobates klossii) sleeping trees in Siberut Island, Indonesia. American Journal of Primatology, 8, 299–308.CrossRefGoogle Scholar
  64. Van Belle, S., Estrada, A., Ziegler, T. E., & Strier, K. B. (2009). Sexual behavior across ovarian cycles in wild black howler monkeys (Alouatta pigra): Male mate guarding and female mate choice. American Journal of Primatology, 71, 153–164.CrossRefGoogle Scholar
  65. von Hippel, F. A. (1998). Use of sleeping trees by black and white colobus monkeys (Colobus guereza) in the Kakamega Forest, Kenya. American Journal of Primatology, 45, 281–290.CrossRefGoogle Scholar
  66. Zhang, S. Y. (1995). Sleeping habits of brown capuchin monkeys (Cebus apella) in French Guiana. American Journal of Primatology, 36, 327–335.CrossRefGoogle Scholar
  67. Zunino, G. E., Bravo, S. P., Murad Ferreira, F., & Reisenman, C. (1996). Characteristics of two types of habitat and the status of the howler monkey (Alouatta caraya) in northern Argentina. Neotropical Primates, 4(2), 48–50.Google Scholar
  68. Zunino, G. E., González, V., Kowalewsk, M. M., & Bravo, S. P. (2001). Alouatta caraya relations among habitat, density and social organization. Primate Report, 61, 37–45.Google Scholar
  69. Zunino, G. E., Kowalewski, M. M., Oklander, L. I., & Gonzalez, V. (2007). Habitat fragmentation and population size of the black and gold howler monkey (Alouatta caraya) in a semideciduous forest in northern Argentina. American Journal of Primatology, 69, 1–10.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Asociación Civil Centro de Investigaciones del Bosque AtlánticoPuerto IguazúArgentina
  2. 2.Estación Biológica Corrientes, Museo Argentino de Ciencias NaturalesCONICETCorrientesArgentina
  3. 3.Department of AnthropologyCalifornia State UniversitySacramentoUSA
  4. 4.Instituto de Biología SubtropicalUniversidad Nacional de Misiones, CONICETPuerto IguazúArgentina

Personalised recommendations