Abstract
Maintaining social cohesion through coordinating traveling time and direction is a primary benefit of group living in mammals. During a 15-month study, we investigated socioecological factors underlying leadership of collective group movements in three multimale–multifemale groups of black howler monkeys (Alouatta pigra) at Palenque National Park (PNP), Mexico. A total of 691 independent group movements across a variety of contexts were collected. Leadership of group movements was partially shared, with adult females initiating and leading group movements significantly more often than did adult males and juveniles, an outcome that has been observed among a diverse set of group living taxa. Adult females did not lead their group more often to feeding sites nor did they lead group movements more frequently when pregnant or lactating compared to when cycling, providing little evidence that energetic demands were the primary drivers underlying female leadership in this primate species. Instead, only one adult female in each social group was identified as a habitual leader of their group. These ‘leader’ females had the highest centrality eigenvectors among the adult group members in their group, suggesting an embedded leadership with the spatially widest connected adult group member emerging as recurrent leader of collective group movements.
Similar content being viewed by others
References
Altmann J (1974) Observational study of behavior: sampling methods. Behaviour 69:227–267
Barelli C, Boesch C, Heistermann M, Reichard UH (2008) Female white-handed gibbons (Hylobates lar) lead group movements and have priority of access to food resources. Behaviour 145:965–981
Boinski S (1991) The coordination of spatial position: a field study of the vocal behaviour of adult female squirrel monkeys. Anim Behav 41:89–102
Boinski S (1993) Vocal coordination of troop movement among white-faced capuchin monkeys, Cebus capucinus. Am J Primatol 30:85–100
Boinski S, Garber PA (2000) On the move: how and why animals travel in groups. The University of Chicago Press, Chicago
Bonanni R, Cafazzo S, Valsecchi P, Natoli E (2010) Effect of affiliative and agonistic relationships on leadership behaviour in free-ranging dogs. Anim Behav 79:981–991
Borgatti SP, Everett MG, Freeman LC (2002) Ucinet for Windows: software for social network analysis. Analytic Technologies, Harvard
Byrne RW (1989) Social relationships of mountain baboons: leadership and affiliation in a non-female-bonded monkey. Am J Primatol 18:191–207
Carpenter CR (1934) A field study of the behavior and social relations of howling monkeys. Comp Psychol Monogr 10:1–168
Chapman CA (1990) Association patterns of spider monkeys: the influence of ecology and sex on social organization. Behav Ecol Sociobiol 26:409–414
Conradt L, Roper TJ (2003) Group decision-making in animals. Nature 421:155–158
Conradt L, Roper TJ (2005) Consensus decision making in animals. Trends Ecol Evol 20:449–456
Conradt L, Roper TJ (2007) Democracy in animals: the evolution of shared group decisions. Proc Roy Soc B 274:2317–2326
Dias PAD, Rangel-Negrín A, Canales-Espinosa D (2011) Effects of lactation on the time-budgets and foraging patterns of female black howlers (Alouatta pigra). Am J Phys Anthropol 145:137–146
Díaz Gallegos JR (1996) Estructura y composición florística de la vegetación del Parque Nacional Zona Arqueológica de Palenque, Chiapas, México. Bs. Thesis. Universidad Juárez Autónoma de Tabasco, Mexico
Dyer JRG, Johansson A, Helbing D, Couzin ID, Krause J (2009) Leadership, consensus decision making and collective behaviour in humans. Phil Trans R Soc B 364:781–789
Erhart EM, Overdorff DJ (1999) Female coordination of group travel in wild Propithecus and Eulemur. Int J Primatol 20:927–940
Estrada A, Castellanos L, Ibarra A, Garcia del Valle Y, Muñoz D, Rivera A, Franco B, Fuentes E, Jiménez C (2002) Survey of the population of the black howler monkey, Alouatta pigra, at the Mayan site of Palenque, Chiapas, Mexico. Primates 44:51–58
Fichtel C, Pyritz L, Kappeler PM (2011) Coordination of group movements in non-human primates. In: Boos M, Kolbe M, Kappeler PM, Ellwart T (eds) Coordination in human and non-human primate groups. Springer, Heidelberg, pp 37–56
Fischhoff IR, Sundaresan SR, Cordingley J, Larkin HM, Sellier MJ, Rubenstein DI (2007) Social relationship and reproductive state influence leadership roles in movements of plains zebra, Equus burchellii. Anim Behav 73:825–831
Holekamp KE, Boydston EE, Smale L (2000) Group travel in social carnivores. In: Boinski S, Garber PA (eds) One the move: how and why animals travel in groups. University of Chicago Press, Chicago, pp 587–627
Horwich RH (1983) Breeding behaviors in the black howler monkey (Alouatta pigra) of Belize. Primates 24:222–230
Ihl C, Bowyer TR (2011) Leadership in mixed-sex groups of muskoxen during the snow-free season. J Mammal 92:819–827
Jacobs A, Maumy M, Petit O (2008) The influence of social organisation on leadership in brown lemurs (Eulemur fulvus fulvus) in a controlled environment. Behav Process 79:111–113
Jacobs A, Sueur C, Deneubourg JL, Petit O (2011) Social network influences decision making during collective movements in brown lemurs (Eulemur fulvus fulvus). Int J Primatol 32:721–736
Kiflawi M, Mazeroll AI (2006) Female leadership during migration and the potential for sex-specific benefits of mass spawning in the brown surgeonfish (Acanthurus nigrofuscus). Environ Biol Fish 76:19–23
King AJ (2010) Follow me! I'm a leader if you do; I'm a failed initiator of you don't? Behav Process 84:671–674
King AJ, Sueur C (2011a) Where next? Group coordination and collective decision making in primates. Int J Primatol 32:1245–1267
King AJ, Sueur C (2011b) A rule-of-thumb based on social affiliation explains collective movements in desert baboons. Anim Behav 82:1337–1345
King AJ, Douglas CMS, Huchard E, Isaac NJB, Cowlishaw G (2008) Dominance and affiliation mediate despotism in a social primate. Curr Biol 18:1833–1838
King AJ, Johnson DDP, Van Vugt M (2009) The origins and evolution of leadership. Minireview. Curr Biol 19:911–916
Kitchen DM (2004) Alpha male black howler monkey responses to loud calls: effect of numeric odds, male companion behaviour and reproductive investment. Anim Behav 67:125–139
Kitchen DM (2006) Experimental test of female black howler monkey (Alouatta pigra) responses to loud calls from potentially infanticidal males: effects of numeric odds, vulnerable offspring, and companion behavior. Am J Phys Anthropol 131:73–83
Kitchen DM, Horwich RH, James RA (2004) Subordinate male black howler monkey (Alouatta pigra) responses to loud calls: experimental evidence for the effects of intra-group male relationships and age. Behaviour 141:703–723
Kummer H (1968) Social organization of hamadryas baboons. A field study. University of Chicago Press, Chicago
Leca JB, Gunst N, Thierry B, Petit O (2003) Distributed leadership in semi-free ranging white-faced capuchin monkeys. Anim Behav 66:1045–1052
Lewis JS, Wartzok D, Heithaus MR (2011) Highly dynamic fission-fusion species can exhibit leadership when traveling. Behav Ecol Sociobiol 65:1061–1069
Milton K (2000) Quo vadis? Tactics of food search and group movement in primates and other animals. In: Boinski S, Garber PA (eds) One the move: how and why animals travel in groups. University of Chicago Press, Chicago, pp 375–417
Neville MK (1972) Social relations within troops of red howler monkeys (Alouatta seniculus). Folia Primatol 18:47–77
Overdorff DJ, Erhart EM, Mutschler T (2005) Does female dominance facilitate feeding priority in black-and-white ruffed lemurs (Varecia variegata) in southeastern Madagascar? Am J Primatol 66:7–22
Pavelka MSM (2011) Mechanisms of cohesion in black howler monkeys. In: Sussman RW, Cloninger CR (eds) Origins and altruism and cooperation, developments in primatology: progress and prospects. Springer, New York, pp 167–178
Peterson RO, Jacobs AK, Drummer TD, Mech LD, Smith DW (2002) Leadership behavior in relation to dominance and reproductive status in gray wolves, Canis lupus. Can J Zool 80:1405–1412
Petit O, Bon R (2010) Decision-making processes: the case of collective movements. Behav Process 84:635–647
Prins HHT (1996) Ecology and behaviour of the African buffalo. Chapman and Hall, London
Pyritz LW, King AJ, Sueur C, Fichtel C (2011a) Reaching a consensus: terminology and concepts used in coordination and decision-making research. Int J Primatol 32:1268–1278
Pyritz LW, Kappeler PM, Fichtel C (2011b) Coordination of group movements in wild red-fronted lemurs (Eulemur rufifrons): processes and influence of ecological and reproductive seasonality. Int J Primatol 32:1325–1347
Ramseyer A, Boissy A, Thierry B, Dumont B (2009) Individual and social determinants of spontaneous group movements in cattle and sheep. Animal 3:1319–1326
Rasa OA (1987) The dwarf mongoose: a study of behaviour and social structure in relation to ecology in a small social carnivore. Adv Study Behav 17:121–163
Stewart KJ, Harcourt AH (1994) Gorilla's vocalisations during rest periods: signals of impending departure? Behaviour 130:29–40
Stueckle S, Zinner D (2008) To follow or not to follow: decision making and leadership during the morning departure in chacma baboons. Anim Behav 756:1995–2004
Sueur C, Petit O (2008) Organization of group members at departure is driven by social structure in Macaca. Int J Primatol 29:1085–1098
Sueur C, Petit O, Deneubourg JL (2009) Selective mimetism at departure in collective movements of Macaca tonkeana: an experimental and theoretical approach. Anim Behav 785:1087–1095
Trillmich J, Fichtel C, Kappeler PM (2004) Coordination of group movements in wild Verreaux'c sifakas (Propithecus verreauxi). Behaviour 141:1103–1120
Van Belle S, Estrada A (2006) Demographic features of Alouatta pigra populations in extensive and fragmented forests. In: Estrada A, Garber PA, Pavelka MSM, Leucke LG (eds) New perspectives in the study of Mesoamerican primates: distribution, ecology, behavior, and conservation. Springer, New York, pp 121–142
Van Belle S, Estrada A, Strier KB (2008) Social relationships among male Alouatta pigra. Int J Primatol 29:1481–1498
Van Belle S, Estrada A, Ziegler TE, Strier KB (2009) Social and hormonal mechanisms underlying male reproductive strategies in black howler monkeys (Alouatta pigra). Horm Behav 56:355–363
Van Belle S, Estrada A, Strier KB (2011) Insights into social relationships among female black howler monkeys, Alouatta pigra, at Palenque National Park, Mexico. Curr Zool 57:1–7
Viljoen PJ (1990) Daily movements of dessert-dwelling elephants in the northern Namib desert. S Afr J Wildl Res 20:69–72
Wang E, Milton K (2003) Intragroup social relationships of male Alouatta palliata on Barro Colorado Island, Republic of Panama. Int J Primatol 24:1227–1243
Acknowledgments
This manuscript is part of a postdoctoral research project of SVB supervised by PAG. We thank the Mexican government (CONANP and INAH) for granting research permission to AE to work in PNP. Financial and logistic support was provided by the Universidad Nacional Autónoma de México (UNAM). E. Pain, B. Thomas, E. Thom, P. Boone, L. Cervera, T. Roberts, S. Schindel, M. Groenenberg, P. Gabant, A. Moldawer, K. Wellens, K. Amato, and B. Wilkinson provided support in the field. We thank Dr. David Watts and three anonymous reviewers for their constructive comments on an earlier version of the manuscript. PAG wishes to thank Chrissie, Sara, and Jenni.
Conflict of interest
None.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by D. P. Watts
Ethnical standards
The research complied with protocols of the Animal Care Committee of the University of Illinois, Urbana-Champaign and adhered to the legal requirements of Mexico.
Rights and permissions
About this article
Cite this article
Van Belle, S., Estrada, A. & Garber, P.A. Collective group movement and leadership in wild black howler monkeys (Alouatta pigra). Behav Ecol Sociobiol 67, 31–41 (2013). https://doi.org/10.1007/s00265-012-1421-5
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00265-012-1421-5