Skip to main content

Landscape Attributes Affecting the Natural Hybridization of Mexican Howler Monkeys

  • Chapter
Primates in Fragments

Abstract

Natural hybridization can be affected by genetic and environmental factors. For instance, genetic incompatibilities may impede the formation of hybrids, or cause infertility of hybrid offspring, whereas anthropogenic habitat disturbance can promote the contact between formerly isolated species, and therefore, increase the probabilities of hybrid formation. Although there are a number of studies addressing endogenous factors affecting hybridization, little is known about the effects of environmental factors, such as habitat fragmentation, on hybridization in animals. Here we evaluate whether habitat configuration in a fragmented landscape affects the process of natural hybridization between Mexican howler monkeys (Alouatta palliata and Alouatta pigra), and which attributes of the fragmented landscape, if any, are likely responsible for this effect. Based on the genetic and morphological identification of purebred and hybrid individuals, we assessed the relationship between several metrics of habitat configuration (number of habitat fragments, fragment size, fragment isolation, and fragment shape) and the demographic characteristics and occupancy patterns of groups in areas where exclusively purebred individuals occur and in areas of hybridization in Macuspana, Tabasco. Our results indicate that forest fragmentation is more severe where hybridization occurs, where there is a larger number of small, though less isolated, fragments. Additionally, there are differences in group size and composition between purebred groups in areas with just purebred animals and in areas where hybridization is occurring. In areas of hybridization, purebred groups tended occupy the largest fragments, whereas in the only area where groups of the two parental species and hybrids co-exist, groups that included hybrid individuals tended to occupy more isolated fragments than groups of purebreds. These results are congruent with the hypothesis that hybridization between Mexican howlers is facilitated in fragmented landscapes. Although we could not discover the mechanisms that underlie this hypothesis, it is possible that in a landscape with more fragments, which are also smaller but rather connected, individuals move more frequently between forest remnants, increasing the probabilities of interspecific encounters.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Anderson E (1948) Hybridization of the habitat. Evolution 2:19

    Article  Google Scholar 

  • Arnold ML (1997) Natural hybridization and evolution. Oxford University Press, New York

    Google Scholar 

  • Arroyo-Rodríguez V, Dias PAD (2010) Effects of habitat fragmentation and disturbance on howler monkeys: a review. Am J Primatol 72:1–16

    Article  PubMed  Google Scholar 

  • Arroyo-Rodríguez V, Mandujano S, Benítez-Malvido J (2008) Landscape attributes affecting patch occupancy by howler monkeys (Alouatta palliata mexicana) at Los Tuxtlas, Mexico. Am J Primatol 70:69–77

    Article  PubMed  Google Scholar 

  • Asensio N, Arroyo-Rodríguez V, Dunn JC, Cristóbal-Azkarate J (2009) Conservation value of landscape supplementation for howler monkeys living in forest patches. Biotropica 41:768–773

    Article  Google Scholar 

  • Balcells CD, Veà JJ (2009) Developmental stages in the howler monkey, subspecies Alouatta palliata mexicana: a new classification using age-sex categories. Neotrop Primates 16:1–8

    Article  Google Scholar 

  • Barton NH, Hewitt GM (1985) Analysis of hybrid zones. Annu Rev Ecol Syst 16:113–148

    Article  Google Scholar 

  • Bleeker W, Hurka H (2001) Introgressive hybridization in Rorippa (Brassicaceae): gene flow and its consequences in natural and anthropogenic habitats. Mol Ecol 10:2013–2022

    Article  CAS  PubMed  Google Scholar 

  • Chapman CA, Pavelka MSM (2005) Group size in folivorous primates: ecological constraints and the possible influence of social factors. Primates 64:1–9

    Article  Google Scholar 

  • Clarke MR, Crockett CM, Zucker EL, Zaldivar M (2002) Mantled howler population of Hacienda La Pacifica, Costa Rica, between 1991 and 1998: effects of deforestation. Am J Primatol 56:155–163

    Article  PubMed  Google Scholar 

  • Cortés-Ortiz L (2003) Evolution of Howler monkeys, Genus Alouatta. Dissertation, University of East Anglia. 130 pp

    Google Scholar 

  • Cortés-Ortiz L, Bermingham E, Rico C, Rodríguez-Luna E, Sampaio I, Ruiz-García M (2003) Molecular systematics and biogeography of the Neotropical monkey genus, Alouatta. Mol Phylogenet Evol 26:64–81

    Article  PubMed  Google Scholar 

  • Cortés-Ortiz L, Duda TF, Canales-Espinosa D, García-Orduña F, Rodríguez-Luna E, Bermingham E (2007) Hybridization in large-bodied New World primates. Genetics 176:2421–2425

    Article  PubMed Central  PubMed  Google Scholar 

  • Cortés-Ortiz L, Mondragón E, Cabotage J (2010) Isolation and characterization of microsatellite loci for the study of Mexican howler monkeys, their natural hybrids, and other Neotropical primates. Conserv Genet Resour. doi:10.1007/s12686-009-9124-6

    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. Am J Primatol 67:209–222

    Article  PubMed  Google Scholar 

  • Cruzan MB, Arnold ML (1993) Ecological and genetic associations in an Iris hybrid zone. Evolution 47:1432–1445

    Article  Google Scholar 

  • Detwiler KM, Burrell AS, Jolly CJ (2005) Conservation implications of hybridization in African cercopithecine monkeys. Int J Primatol 26:661–684

    Article  Google Scholar 

  • Di Fiore A, Campbell CJ (2007) The Atelines: variation in ecology, behavior, and social organization. In: Campbell CJ, Fuentes A, MacKinnon KC, Panger M, Bearder SK (eds) Primates in perspective. Oxford University Press, New York, pp 155–185

    Google Scholar 

  • Docker MF, Dale A, Heath DD (2003) Erosion of interspecific reproductive barriers resulting from hatchery supplementation of rainbow trout sympatric with cutthroat trout. Mol Ecol 12:3515–3521

    Article  CAS  PubMed  Google Scholar 

  • Ellsworth JA, Hoelzer GA (2006) Genetic evidence on the historical biogeography of Central American howler monkeys. In: Lehman SM, Fleagle JG (eds) Primate biogeography: progress and prospects. Springer, New York, pp 81–103

    Chapter  Google Scholar 

  • Estrada A, Mendoza A, Castellanos L, Pacheco R, Van Belle S, García Y, Munoz D (2002) Population of the black howler monkey (Alouatta pigra) in a fragmented landscape in Palenque, Chiapas, Mexico. Am J Primatol 58:45–55

    Article  PubMed  Google Scholar 

  • Ewers RM, Didham RK (2006) Confounding factors in the detection of species responses to habitat fragmentation. Biol Rev 81:117–142

    Article  PubMed  Google Scholar 

  • Fahrig L (2003) Effects of habitat fragmentation on biodiversity. Annu Rev Ecol Evol Syst 34:487–515

    Article  Google Scholar 

  • Forman RTT, Godron M (1986) Landscape ecology. Wiley, New York

    Google Scholar 

  • Heath D, Bettles CM, Roff D (2010) Environmental factors associated with reproductive barrier breakdown in sympatric trout populations on Vancouver Island. Evol Appl 3:77–90

    Article  PubMed Central  PubMed  Google Scholar 

  • Horwich RH, Brockett RC, Jones CB (2000) Alternative male reproductive behaviors in the Belizean black howler monkey (Alouatta pigra). Neotrop Primates 8:95–98

    Google Scholar 

  • Jones CB (1995) Alternative reproductive behaviour in the mantled monkey (Alouatta palliata Gray): testing Carpenters hypothesis. Bio Primatol Lat 5:1–5

    Google Scholar 

  • Kelaita M, Dias PAD, Aguilar-Cucurachi MS, 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. Am J Phys Anthropol 146:179–187

    Article  PubMed  Google Scholar 

  • Keller B, Wolinska J, Manca M, Spaak P (2008) Spatial, environmental and anthropogenic effects on the taxon composition of hybridizing Daphnia. Phil Trans R Soc B Biol Sci 363:2943–2952

    Article  Google Scholar 

  • Lamont BB, He T, Enright NJ, Krauss SL, Miller B (2003) Anthropogenic disturbance promotes hybridization between Banksia species by altering their biology. J Evol Biol 16:551–557

    Article  CAS  PubMed  Google 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, México. Univ Ciencia SI II:11–21

    Google Scholar 

  • McCann C, Williams-Guillén K, Koontz FW, Roque-Espinoza AA, Martínez-Sánchez JC, Koontz C (2003) Shade coffee plantations as wildlife refuge for mantled howler monkeys (Alouatta palliata) in Nicaragua. In: Marsh LK (ed) Primates in fragments: ecology and conservation. Kluwer Academics, New York, pp 321–341

    Chapter  Google Scholar 

  • Motulsky HJ, Christopoulos A (2003) Fitting models to biological data using linear and nonlinear regression. A practical guide to curve fitting. GraphPad Software, San Diego

    Google Scholar 

  • Nunn CL (1999) The number of males in primate social groups: a comparative test of the socioecological model. Behav Ecol Sociobiol 46:1–13

    Article  Google Scholar 

  • Pozo-Montuy G, Serio-Silva JC, Bonilla-Sánchez YM, Bynum N, Landgrave R (2008) Current status of the habitat and population of the black howler monkey (Alouatta pigra) in Balancán, Tabasco, Mexico. Am J Primatol 70:1169–1176

    Article  PubMed  Google Scholar 

  • Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure from multilocus genotype data. Genetics 155:945–959

    CAS  PubMed Central  PubMed  Google Scholar 

  • Rodríguez-Luna E, Cortés-Ortiz L (1995) Consideraciones en relación a la translocación de un grupo de monos aulladores (Alouatta palliata). In: Rodríguez-Luna E, Cortés-Ortiz L, Contreras JM (eds) Estudios Primatológicos en México, vol 2. Universidad Veracruzana, Xalapa, pp 81–95

    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. Dissertation, Universidad de San Carlos, Guatemala

    Google Scholar 

  • Rzedowski J (2006) Vegetación de México. 1ra edición digital, CONABIO, México

    Google Scholar 

  • Sánchez-Colón S, Flores-Martínez A, Cruz-Leyva IA, Velázquez A (2009) Estado y transformación de los ecosistemas terrestres por causas humanas. In: Dirzo R, González R, March IJ (eds) Capital Natural de México, vol. 2. CONABIO, México, pp 75–129

    Google Scholar 

  • Schwarz D, McPheron BA (2007) When ecological isolation breaks down: sexual isolation is an incomplete barrier to hybridization between Rhagoletis species. Evol Ecol Res 9:829–841

    Google Scholar 

  • Smith JD (1970) The systematic status of the black howler monkey, Alouatta pigra Lawrence. J Mammal 51:358–369

    Article  Google Scholar 

  • Steinberg ER, Cortés-Ortiz L, Nieves M, Bolzán AD, García-Orduña F, Hermida-Lagunes J, Canales- Espinosa D, Mudry MD (2008) The karyotype of Alouatta pigra (Primates: Platyrrhini): mitotic and meiotic analyses. Cytogenet Genome Res 122:103–109

    Article  CAS  PubMed  Google Scholar 

  • Van Belle S, Estrada A (2006) Demographic features of Alouatta pigra populations in extensive and fragmented forests. In: Estrada A, Garber PA, Pavelka MSM, Luecke LG (eds) New perspectives in the study of Mesoamerican primates. Springer, New York, pp 121–142

    Chapter  Google Scholar 

Download references

Acknowledgments

We are indebted to A. Coyohua for his help during the censuses. We thank G. Muntané, R.A. Candelero, M.G. Cárdenas, A.L. Tapia, F. Burnonville, and E. Zacarías for their assistance during the collection of demographic data. Sampling for genetic data was conducted with the invaluable assistance of the personnel of the Instituto de Neuroetología, particularly J. Hermida, M.S. Aguilar, and F. García. We thank V. Arroyo-Rodríguez for his comments and suggestions on an earlier version of the manuscript. This research was made possible for P.A.D. Dias by Idea Wild and Universidad Veracruzana, and for L. Cortés-Ortiz by PROMEP UVER, Universidad Veracruzana, OVPR at the University of Michigan, NSF DEB-0640519 and NSF BCS-0962807. Procedures for capturing and handling primates were approved by the University Committee on Use and Care of Animals (UCUCA) at the University of Michigan and complied with all Mexican and US laws.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Pedro Américo D. Dias .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2013 Springer Science+Business Media New York

About this chapter

Cite this chapter

Dias, P.A.D., Alvarado-Serrano, D., Rangel-Negrín, A., Canales-Espinosa, D., Cortés-Ortiz, L. (2013). Landscape Attributes Affecting the Natural Hybridization of Mexican Howler Monkeys. In: Marsh, L., Chapman, C. (eds) Primates in Fragments. Developments in Primatology: Progress and Prospects. Springer, New York, NY. https://doi.org/10.1007/978-1-4614-8839-2_28

Download citation

Publish with us

Policies and ethics