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The Influence of Loud Calls on Intergroup Spacing Mechanism in Black Howler Monkeys (Alouatta pigra)

Abstract

Long-distance vocalizations form an integral part of intergroup spacing mechanisms. The decision to approach, retreat, or ignore loud calls of neighboring groups might be influenced by resource availability, location in the home range, presence of fertile females or infants, or differential resource-holding potentials, and can alter intergroup encounter rates. During a 19-mo study (February 2016–August 2017), we examined navigation decisions relative to neighbor’s loud calls for five groups of black howler monkeys (Alouatta pigra) in Palenque National Park, Mexico. Study groups encountered any of their neighbors at a mean rate of one every 3.5 days and the same neighbor at a mean rate of one every 16.7 days, which was significantly more frequent than would be expected based on a simulation model that randomized observed daily paths. These results are consistent with mutual attraction. Based on 368 travel bouts relative to nearby (50–300 m) calls of neighbors, study groups were more likely to approach calls of neighbors than would be expected by chance, but only when neighbors were close by (50–150 m), suggesting that the imminence of threat by opponents played a role. Of the nine social and ecological predictor variables considered, availability of ripe fruits and of flowers was an important driver of their navigation choices and groups were more likely to move toward neighbors’ calls when ripe fruits were scarce and to move away when flowers were abundant. We found no evidence that the presence of fertile females or unweaned infants influenced navigation decisions. Nor did relative competitive abilities of opposing groups, measured as numeric superiority in group size or male group size, affect navigation decisions. This study provides evidence that black howler monkeys incorporate information on resource availability and neighbors’ current locations into their navigation decisions and intergroup spacing patterns.

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References

  1. Amato, K. R., & Garber, P. A. (2014). Nutrition and foraging strategies of the black howler monkey (Alouatta pigra) in Palenque National Park, Mexico. American Journal of Primatology, 76, 774–787.

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

  3. Barrett, L., & Lowen, C. B. (1998). Random walks and the gas model: spacing behaviour of grey-cheeked mangabeys. Functional Ecology, 12, 857–865.

  4. Beehner, J., & Kitchen, D. (2007). Factors affecting individual participation in group-level aggression among non-human primates. Behaviour, 144, 1551–1581.

  5. Behie, A. M., & Pavelka, M. S. M. (2015). Fruit as 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, Developments in Primatology: Progress and Prospects (pp. 357–382). New York: Springer Science+Business Media.

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

  7. Brown, M. (2013). Food and range defence in group-living primates. Animal Behaviour, 85, 807–816.

  8. Brown, M. (2014). Patch occupation time predicts responses by grey-cheeked mangabeys (Lophocebus albigena) to real and simulated neighboring groups. International Journal of Primatology, 35, 491–508.

  9. Brown, M., & Waser, P. M. (2018). Group movements in response to competitors’ calls indicate conflicts of interest between male and female grey-cheeked mangabeys. American Journal of Primatology, 80, e22918.

  10. Burnham, K. P., & Anderson, D. R. (2002). Model selection and multimodel inference: A practical information-theoretical approach (2nd ed.). New York: Springer-Verlag.

  11. Carpenter, C. R. (1934). A field study of the behavior and social relations of howling monkeys. Comparative Psychology Monographs, 10, 1–168.

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

  13. Chivers, D. J. (1969). On the daily behaviour and spacing of howling monkey groups. Folia Primatologica, 10, 48–102.

  14. Cornick, L. A., & Markowitz, H. (2002). Diurnal vocal patterns of the black howler monkeys (Alouatta pigra) at Lamanai, Belize. Journal of Mammalogy, 83, 159–166.

  15. Crockett, C. M. (2003). Re-evaluating the sexual selection hypothesis for infanticide by Alouatta males. In C. B. Jones (Ed.), Sexual selection and reproductive competition in primates: New perspectives and directions (pp. 327–365). Norman, OK: American Society of Primatologists.

  16. Crofoot, M. C., & Gilby, I. C. (2012). Cheating monkeys undermine group strength in enemy territory. Proceedings of the National Academy of Sciences of the USA, 109, 501–505.

  17. 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.

  18. Croissant, Y. (2013). mlogit: multinomial logit model. https://CRAN.R-project.org/package=mlogit

  19. 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.

  20. da 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, 259–271.

  21. de Guinea, M., Estrada, A., Nekaris, K. A. I., & Van Belle, S. (2019). Arboreal route navigation in a Neotropical mammal: energetic implications associated with tree monitoring and landscape attributes. Movement Ecology, 7, 39. https://doi.org/10.1186/s40462-019-0187-z

  22. Delgado, R. A. (2006). Sexual selection in the loud calls of male primates: Signal content and function. International Journal of Primatology, 27, 5–25.

  23. Días, P. A. D., & Rangel-Negrín, A. (2015). Diets of howler monkeys. In M. M. Kowalewski, P. A. Garber, L. Cortés-Ortiz, B. Urbani, & D. Youlatos (Eds.), Howler monkeys: Behavior, ecology, and conservation, Developments in Primatology: Progress and Prospects (pp. 21–56). New York: Springer Science+Business Media.

  24. Díaz Gallegos, J. R. (1996). Estructura y composición floristico de la vegetación del Parque Nacional Zona Arqueológica de Palenque, Chiapas, México. Bs. thesis, Universidad Juárez Autónoma de Tabasco.

  25. Dormann, C. F., Elith, J., Bacher, S., Buchmann, C., Carl, G., et al (2013). Collinearity: A review of methods to deal with it and a simulation study evaluating their performance. Ecography, 36, 27–46.

  26. Erb, W. M., Hodges, J. K., & Hammerschmidt, K. (2013). Individual, contextual, and age-related acoustic variation in simakobu (Simias concolor) loud calls. PLoS ONE, 8(12), e83131.

  27. Estrada, A., Castellanos, L., Ibarra, A., García del Valle, Y., Muñoz, D., & Rivera, A. (2002). Survey of the population of the black howler monkey, Alouatta pigra, at the Mayan site of Palenque, Chiapas, Mexico. Primates, 44, 51–58.

  28. Fischer, J., Kitchen, D. M., Seyfarth, R. M., & Cheney, D. L. (2004). Baboon loud calls advertise male quality: Acoustic features and their relation to rank, age, and exhaustion. Behavioral Ecology and Sociobiology, 56, 140–148.

  29. Furuichi, T. (In press). Variations in intergroup relationships among species and among and within local populations of African great apes. International Journal of Primatology.

  30. Garber, P. A., Pruetz, J. D., & Isaacson, J. (1993). Patterns of range use, range defense, and intergroup spacing in moustached tamarin monkeys (Saguinus mystax). Primates, 34, 11–25.

  31. Harrison, M. J. S. (1983). Territorial behaviour in the green monkey, Cercopithecus sabaeus: Seasonal defense of local food supplies. Behavioral Ecology and Sociobiology, 12, 85–94.

  32. 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.

  33. 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.

  34. Horwich, R. H., & Gebhard, K. (1983). Roaring rhythms in black howler monkeys (Alouatta pigra) in Central America. Primates, 24, 290–296.

  35. Howard, A. M., Nibbelink, N. P., Madden, M., Young, L. A., Bernardes, S., & Fragaszy, D. M. (2015). Landscape influences on the natural and artificially manipulated movements of bearded capuchin monkeys. Animal Behaviour, 106, 59–70.

  36. Hutchinson, J. M. C., & Waser, P. M. (2007). Use, misuse, and extensions of “ideal gas” models of animal encounters. Biological Reviews, 82, 335–359.

  37. 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.

  38. Kitchen, D. M., da Cuhna, R. G. T., Holzmann, I., & de Oliviera, 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, Developments in Primatology: Progress and Prospects (pp. 369–399). New York: Springer Science+Business Media.

  39. 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, Developments in Primatology: Progress and Prospects (pp. 165–189). New York: Springer Science+Business Media.

  40. Kumara, H. N., Singh, M., Sharma, A. K., Santhosh, K., & Pal, A. (2014). Impact of forest fragment size and between-group encounters in loin-tailed macaques. Primates, 55, 543–548.

  41. Lewis, J. R., Sandel, A. A., Hilty, S., & Barnett, S. E. (In press). Sex differences explain participation but not outcome of intergroup encounters in a monomorphic primate (Propithecus verreauxi). International Journal of Primatology.

  42. Li, Z., Ding, B., Wu, F., Lei, T. K. H., Kays, R., & Crofoot, M. C. (2015). Attraction and avoidance detection from movements. Proceedings of the VLDB Endowment, 7, 157–168.

  43. Majolo, B., de Bortoli, A., Martinez Inigo, L., & Lehmann, J. (In press). The effect of group size and individual characteristics on intergroup encounters in primates. International Journal of Primatology.

  44. Milton, K. (2000). Quo vadis? Tactics of food search and group movement in primates and other animals. In S. Boinski & P. A. Garber (Eds.), On the move: How and why animals travel in groups (pp. 375– 418). Chicago: University of Chicago Press.

  45. Mirville, M. O., Ridley, A. R., Samedi, J. P. M., Vecellio, V., Ndagijimana, F., et al (In press). Intragroup behavioral changes following intergroup conflict in mountain gorillas (Gorilla beringei beringei). International Journal of Primatology.

  46. Mitani, J. C. (1985). Sexual selection and adult male orangutan long calls. Animal Behavior, 33, 272–283.

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

  48. Scarry, C. J., & Tujague, P. (2012). Consequences of lethal intragroup aggression and alpha male replacement on intergroup relations and home range use in tufted capuchin monkeys (Cebus apella nigritus). American Journal of Primatology, 74, 804–810.

  49. Sekulic, R. (1982). Daily and seasonal patterns of roaring and spacing in four red howler (Alouatta seniculus) troops. Folia Primatologica, 39, 22–48.

  50. Sekulic, R., & Chivers, D. J. (1986). The significance of call duration in howler monkeys. International Journal of Primatology, 7, 183–190.

  51. Southwick, C. H. (1962). Patterns of intergroup social behavior in primates, with special reference to rhesus and howling monkeys. Annals of the New York Academy of Sciences, 102, 436–454.

  52. Spiegel, O., Leu, S. T., Sih, A., & Bull, C. M. (2016). Socially interacting or indifferent neighbors? Randomization of movement paths to tease apart social preference and spatial constraints. Methods in Ecology and Evolution, 7, 971–979.

  53. Sugiura, M., Saito, C., Sato, S., Agetsuma, N., Takahashi, H., et al (2000). Variation in intergroup encounters in two populations of Japanese macaques. International Journal of Primatology, 21, 519–535.

  54. 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. Behavioral Ecology and Sociobiology, 65, 13–21.

  55. Van Belle, S., Estrada, A., & Garber, P. A. (2013a). Spatial and diurnal distribution of loud calling in black howlers (Alouatta pigra). International Journal of Primatology, 34, 1209–1224.

  56. Van Belle, S., Estrada, A., & Garber, P. A. (2013b). Collective group movement and leadership in wild black howler monkeys (Alouatta pigra). Behavioral Ecology and Sociobiology, 67, 31–41.

  57. Van Belle, S., Estrada, A., & Garber, P. A. (2014). The function of loud calls in black howler monkeys (Alouatta pigra): Food, mate, or infant defense? American Journal of Primatology, 76, 1196–1206.

  58. Van Belle, S., Kulp, A. E., Thiessen-Bock, R., Garcia, M., & Estrada, A. (2010). Observed infanticides following a male immigration event on black howler monkeys, Alouatta pigra, at Palenque National Park, Mexico. Primates, 51, 279–284.

  59. Van Belle, S., & Scarry, C. J. (2015). Individual participation in intergroup contests is mediated by numerical assessment strategies in black howler and tufted capuchin monkeys. Philosophical Transactions of the Royal Society B: Biological Sciences, 370, 20150007.

  60. Vercauteren Drubbel, R., & Gautier, J. P. (1993). On the occurrence of nocturnal and diurnal loud calls, differing in structure and duration, in red howlers (Alouatta seniculus) of French Guyana. Folia Primatologica, 60, 195–209.

  61. Waser, P. M. (1976). Cercocebus albigena: Site attachment, avoidance, and intergroup spacing. American Naturalist, 110, 911–935.

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

  63. 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. Behaviour, 108, 73–103.

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

  65. Wich, S. A., Assink, P. R., Becher, F., & Sterck, E. H. M. (2002). Playbacks of long-distance calls to wild Thomas langurs (Primates; Presbytis thomasi): The effect of familiarity. Behaviour, 139, 79–87.

  66. 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. Behavioral Ecology and Sociobiology, 52, 474–484.

  67. Wilson, M. L., Kahlenberg, S. M., Wells, M., & Wrangham, R. W. (2012). Ecological and social factors affect the occurrence and outcomes of intergroup encounters in chimpanzees. Animal Behaviour, 83, 277–291.

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Acknowledgments

We thank the Mexican government (CONANP and INAH) for granting research permission to work in Palenque National Park. Our research was supported by a research grant from Universidad Nacional Autónoma de México (PAPIIT-UNAM project IN200216). We also thank the numerous research assistants who provided support in the field, especially Elsa Barrios, Anaid Cardenas, Dallas Levey, and Miguel de Guinea. We thank Takeshi Furuichi, Joanna Setchell, and two anonymous reviewers for their constructive comments on previous versions of the manuscript.

Author information

SVB and AE conceived and designed the research. SVB conducted field work, performed statistical analyses, and wrote the manuscript. AE provided editorial advice.

Correspondence to Sarie Van Belle.

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Handling Editor: Takeshi Furuichi

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Van Belle, S., Estrada, A. The Influence of Loud Calls on Intergroup Spacing Mechanism in Black Howler Monkeys (Alouatta pigra). Int J Primatol (2019) doi:10.1007/s10764-019-00121-x

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Keywords

  • Ideal gas model
  • Intergroup encounters
  • Mutual attraction
  • Mutual avoidance
  • Navigation
  • Vocal communication