Group Structure and Dynamics in Black Howlers (Alouatta pigra): A 7-year Perspective
The long-term monitoring of group structure and dynamics is critical to the study of primate ecology and evolutionary processes, as well as to understand the responses of individuals to changes in their environments. We monitored individually recognized black howlers (Alouatta pigra) belonging to 11 groups for 7 yr in different habitats and landscapes in Campeche (Mexico). Our aims were 1) to describe group structure and dynamics; 2) to determine whether group structure and dynamics changed significantly over time; and 3) to evaluate which habitat and landscape-scale attributes best predicted variation among groups in structure and dynamics. Each year we surveyed the groups twice in each climatic season (wet and dry season), resulting in a total of 10,083 sampling days. Although group size increased over time, mostly as a result of moderate to high infant survival rates and increases in the number of juveniles in groups, other demographic parameters, such as the number of adults and infants per group, were stable. We observed no group takeovers involving two or more males and infrequent takeovers by solitary males; frequent disappearances of individuals of both sexes from their natal groups around the age of sexual maturation, suggesting a bisexual dispersal pattern; concentration of births in the wet season; male-biased sex ratios at birth but female-biased immature survival. Group structure and dynamics were affected by both habitat and landscape-scale attributes, but factors acting at the habitat scale had an overall higher impact on demographics. Besides reporting new life history and demographic data for this species, the results from this study suggest that black howlers may be more sensitive to habitat disturbance than previously reported.
KeywordsAlouatta pigra Campeche Census Demographics Group size and composition Long-term monitoring
This study would not have been possible without the efforts of 53 people that were involved in fieldwork. We thank all the students, volunteers, and researchers who helped with data collection. The following people and institutions granted permission to work in their properties and facilitated our fieldwork: Comisarios Ejidales de Abelardo Domínguez, Calax, Chekubul, Conhuas, Nvo. Ontario, Plan de Ayala, and Candelario Hernández Perera, Igor, Carmén Gómez and Ricardo Valencia; Ayuntamiento de Calakmul; Ing. A. Sánchez Martínez, El Tormento, INIFAP; Lic. C. Vidal and Lic. L. Álvarez, INAH Campeche; Biól. F. Durand Siller, Reserva de la Biósfera Calakmul, CONANP; Ing. V. Olvera, El Álamo. Climate data was kindly provided by CONAGUA. We thank the help of R. Mateo-Gutiérrez, S. Sinaca-Colín, C. Gutiérrez-Báez (Centro de Investigaciones Históricas y Sociales, UACM) and J. Salvador Flores-Guido (Facultad de Medicina Veterinaria y Zootecnia, UADY) in the identification of the plants. This study was supported by CFE (RGCPTTP-UV-001/04), Universidad Veracruzana, Conacyt (grant number 235839; grants i010/152/2014 and C-133/2014) and Idea Wild. We are indebted to V. Arroyo-Rodríguez for support with statistical analysis, and to F. Aureli, J. Setchell, and two anonymous reviewers for very constructive and helpful comments and suggestions that greatly improved the manuscript. P. A. D. Dias and A. Rangel-Negrín thank Mariana for being a constant source of inspiration for exploring primate behavior and ecology.
- Altmann, J. (1980). Baboon mothers and infants. Cambridge, MA: Harvard University Press.Google Scholar
- Behie, A. M., & Pavelka, M. S. M. (2015). Fruit as a key factor in howler monkey population density: conservation implications. In M. Kowalewski, P. A. Garber, L. Cortés-Ortiz, B. Urbani, & D. Youlatos (Eds.), Howler monkeys: Behavior, ecology and conservation (pp. 357–382). New York: Springer.CrossRefGoogle Scholar
- Brockett, R. C., Horwich, R. H., & Jones, C. B. (2000). Female dispersal of the Belizean black howling monkey (Alouatta pigra). Neotropical Primates, 8, 32–34.Google Scholar
- Burnham, K. P., & Anderson, D. R. (2002). Model selection and multimodel inference: A practical information-theoretic approach. New York: Springer Science+Business Media.Google Scholar
- Canty, A., & Ripley, B. (2014). boot: Bootstrap R (S-Plus) Functions. R package version 1.3-13. Available at: http://cran.r-project.org/web/packages/boot/boot.pdf (Accessed August 20, 2014).
- Clarke, M. R., Zucker, E. L., & Scott, N. J. J. (1986). Population trends of the mantled howler groups of La Pacifica, Guanacaste, Costa Rica. American Journal of Primatology, 11, 79–88.Google Scholar
- Collias, N., & Southwick, C. (1952). A field study of population density and social organization in howling monkeys. Proceedings of the American Philosophical Society, 96, 143–156.Google Scholar
- Crawley, M. J. (2002). Statistical computing: An introduction to data analysis using S-Plus. London: John Wiley & Sons.Google Scholar
- Cristóbal-Azkarate, J., Veà, J., Asensio, N., & Rodríguez-Luna, E. (2005). Biogeographical and floristic predictors of the presence and abundance of mantled howlers (Alouatta palliata mexicana) in rainforest fragments at Los Tuxtlas, Mexico. American Journal of Primatology, 67, 209–222.CrossRefPubMedGoogle Scholar
- Crockett, C. M. (1984). Emigration by female red howler monkeys and the case for female competition. In M. F. Small (Ed.), Female primates: Studies by women primatologists (pp. 159–173). New York: Alan R. Liss.Google Scholar
- 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.Google Scholar
- Crockett, C. M., & Janson, C. H. (2000). Infanticide in red howlers: Female group size, male membership and a possible link to folivory. In C. P. van Schaik & C. H. Janson (Eds.), Infanticide by males and its implications (pp. 75–98). Cambridge, U.K.: Cambridge University Press.CrossRefGoogle Scholar
- Crockett, C. M., & Sekulic, R. (1984). Infanticide in red howler monkeys (Alouatta seniculus). In G. Hausfater & S. B. Hrdy (Eds.), Infanticide: Comparative and evolutionary perspectives (pp. 173–191). New York: Aldine.Google Scholar
- Dias, P. A. D., Alvarado, D., Rangel-Negrín, A., Canales-Espinosa, D., & Cortés-Ortiz, L. (2013). Landscape attributes affecting the natural hybridization of Mexican howler monkeys. In L. Marsh & C. A. Chapman (Eds.), Primates in fragments: Complexity and resilience (pp. 423–435). New York: Springer.CrossRefGoogle 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, K. C. MacKinnon, S. K. Bearder, & R. M. Stumpf (Eds.), Primates in perspective (2nd ed., pp. 155–188). New York: Oxford University Press.Google Scholar
- Forman, R. T. T., & Godron, M. (1986). Landscape ecology. New York: John Wiley & Sons.Google Scholar
- Horwich, R. H., Brockett, R. C., James, R. A., & Jones, C. B. (2001). Population structure and group productivity of the Belizean black howling monkey (Alouatta pigra): Implications for female socioecology. Primate Report, 61, 47–64.Google Scholar
- Janson, C., & Verdolin, J. (2005). Seasonally of primate births in relation to climate. In D. K. Brockman & C. P. van Schaik (Eds.), Tropical fruits and frugivores: The search for strong interactors (pp. 307–350). Cambridge, U.K.: Cambridge University Press.Google Scholar
- Kelaita, M. A., Dias, P. A. D., Aguilar-Cucurachi, M. S., Canales-Espinosa, D., & Cortés-Ortiz, L. (2011). Impact of intra-sexual selection on sexual dimorphism and testes size in the Mexican howler monkeys Alouatta palliata and A. pigra. American Journal of Physical Anthropology, 146, 179–187.CrossRefPubMedGoogle Scholar
- Kitchen, D. M. (2000). Aggression and assessment among social groups of Belizean black howler monkeys (Alouatta pigra). Ph.D. thesis, University of Minnesota.Google Scholar
- Lumley, T. (2009). Package ‘LEAPS’: Regression subset selection. Available at: http://cran.r-project.org/web/packages/leaps/leaps.pdf (Accessed August 20, 2014).
- Mandujano, S., Escobedo-Morales, L., Palacios-Silva, R., Arroyo-Rodríguez, V., & Rodríguez-Toledo, E. M. (2006). A metapopulation approach to conserving howler monkey in a highly fragmented landscape in Los Tuxtlas, Mexico. In A. Estrada, P. A. Garber, M. S. M. Pavelka, & L. Luecke (Eds.), New perspectives in the study of Mesoamerican primates: Distribution, ecology, behavior, and conservation (pp. 513–538). New York: Springer Science+Business Media.CrossRefGoogle Scholar
- Mandujano, S., & Estrada, A. (2005). Detección de umbrales de área y distancia de aislamiento para la ocupación de fragmentos de selva por monos aulladores, Alouatta palliata, en Los Tuxtlas (pp. 11–21). II: México. Universidad y Ciencia.Google Scholar
- Marsh, L. K., Cuarón, A. D., Cortés-Ortiz, L., Shedden, A., Rodríguez-Luna, E., & de Grammont, P. C. (2008). Alouatta pigra. IUCN 2014 Red List of Threatened Species. Version 2013.1. Available at: http://www.iucnredlist.org (Accessed September 25, 2014).
- Milton, K. (1982). The role of resource seasonality in density regulation of a wild primate population. In E. G. Leigh, A. S. Rand, & D. M. Windsor (Eds.), The ecology of a tropical forest (pp. 273–289). Washington, DC: Smithsonian Institution Press.Google Scholar
- Milton, K., Giacalone, J., Wright, S. J., & Stockmayer, G. (2005). Do frugivore population fluctuations reflect fruit production? Evidence from Panama. In J. L. Dew & J. P. Boubli (Eds.), Tropical fruits and frugivores: The search for strong interactors (pp. 5–35). Berlin and Heidelberg: Springer Science+Business Media.CrossRefGoogle Scholar
- Neter, J., Wasserman, W., & Kutner, M. H. (1990). Applied linear statistical models. Chicago: Irwin.Google Scholar
- Ordóñez-Gómez, J. D., Arroyo-Rodríguez, V., Nicasio-Arzeta, S., & Cristóbal-Azkarate, J. (2014). Which is the appropriate scale to assess the impact of landscape spatial configuration on the diet and behavior of spider monkeys? American Journal of Primatology. doi: 10.1002/ajp.22310.PubMedGoogle Scholar
- Rangel-Negrín, A., Dias, P. A. D., & Canales-Espinosa, D. (2011). Impact of translocation on the behavior and health of black howlers. In L. Gama-Campillo, G. Pozo-Montuy, W. M. Contreras-Sánchez, & S. L. Arriaga-Weiss (Eds.), Perspectivas en primatología Mexicana (pp. 271–288). Villahermosa: Universidad Juárez Autónoma de Tabasco.Google Scholar
- Rosales-Meda, M. (2003). Abundancia, distribución y composición de tropas del mono aullador negro (Alouatta pigra) en diferentes remanentes de Bosque en la Eco-región Lachuá. B.Sc. dissertation, Guatemala: Universidad de San Carlos.Google Scholar
- Rosenberger, A. L., Tejedor, M. F., Cooke, S., Halenar, L., & Pekkar, S. (2009). Platyrrhine ecophylogenetics, past and present. In P. A. Garber, J. C. Bicca-Marques, E. W. Heymann, & K. B. Strier (Eds.), South American primates: Comparative perspectives in the study of behavior, ecology, and conservation (pp. 69–113). New York: Springer Science+Business Media.CrossRefGoogle Scholar
- Stouffer, P. C., & Borges, S. H. (2001). Conservation recommendations for understory birds in Amazonian forest fragments and secondary areas. In R. O. Bierregaard Jr., C. Gascon, T. E. Lovejoy, & R. Mesquita (Eds.), Lessons from Amazonia: The ecology and conservation of a fragmented forest (pp. 248–261). New Haven, CT: Yale University Press.Google Scholar