Skip to main content
SpringerLink
Log in

Terrestrial Locomotion and Other Adaptive Behaviors in Howler Monkeys (Alouatta pigra) Living in Forest Fragments

  • Chapter
  • First Online:
Movement Ecology of Neotropical Forest Mammals

Abstract

Habitat loss threatens many primate species, yet some can thrive in small forest fragments. As forest loss increases due to anthropogenic land conversion or climate change, understanding the adaptive behaviors that facilitate the use of fragments becomes critical in predicting which species will be most likely to survive. To address this issue, we quantified apparent adaptive behaviors of five groups of howler monkey (Alouatta pigra) living in small fragments located in cattle pastures in Balancán, Tabasco, Mexico. Here we report on two potentially adaptive behaviors that may facilitate their ability to survive in forest fragments: terrestrial locomotion and drinking water directly from sources, such as tree hollows. We examined associations between these behaviors and characteristics of fragment vegetation, as well as howler diet and general activity. In 1117 h of observation, 63 terrestrial events were observed, which mainly involved traveling to isolated trees. We hypothesized that larger groups would use larger areas and engage in more terrestrial locomotion because of the greater number of individuals; also larger groups might be less vulnerable to predation. However, there was no relationship between group size and the number of terrestrial events. There was a significant relationship between the cumulative distances traveled on the ground and the first principal component (PC 1) of general behavior during the dry season. Most of the 18 drinking events unexpectedly occurred in the rainy season and only 7 during dry season, and, counter to our expectation, their occurrence was not related to what plant parts were being eaten. We use this research to discuss a conservation action plan we have put in place for this howler population at a landscape level involving protected areas, education, policy development, and knowledge dissemination.

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

Access this chapter

Log in via an institution
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
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

  • Aggimarangsee N (2013) Status monitoring of isolated populations of macaques and other non-human primates in Thailand. In: Marsh LK, Chapman CA (eds) Primates in fragments: complexity and resilience. Springer, New York

    Google Scholar 

  • Almeida-Silva B, Guedes PG, Boubli JP, Strier KB (2005) Deslocamento terrestre e o comportamento de beber em um groupo de barbados (Alouatta guarida clamitan Cabrera, 1940) en Ninas Gerais, Brasil. Neotropical Primates 13:1–3

    Article  Google Scholar 

  • Anderson J, Cowlishaw G, Rowcliffe JM (2007) Effects of forest fragmentation on the abundance of Colobus angolensis palliatus in Kenya’s coastal forests. Int J Primatol 28:637–655

    Article  Google Scholar 

  • Bicca-Marques JC, Calegaro-Marques C (1995) Drinking behavior of the black howler monkey (Alouatta caraya). Folia Primatol 58:107–111

    Article  Google Scholar 

  • Bonilla-Sanchez YM, Serio-Silva JC, Pozo-Montuy G, Chapman CA (2012) Does the expansion of Eucalyptus plantations signal hope or despair for black howler monkeys? Int J Primatol 33:233–245

    Article  Google Scholar 

  • Brussard PF (1985) Minimum viable populations: how many are too few? Restor Manag Notes 3(1):21–25

    Google Scholar 

  • Campbell CJ, Aureli F, Chapman CA, Ramos-Fernandez G, Matthews K, Russo SE, Suarez S, Vick L (2005) Terrestrial behavior of Ateles spp. Int J Primatol: 26: 1039–1051

    Article  Google Scholar 

  • Chalise MK (2013) Fragmented primate populations of Nepal. In: Marsh LK, Chapman CA (eds) Primates in fragments: complexity and resilience. Springer, New York, pp 329–356

    Chapter  Google Scholar 

  • Chapman CA, Chapman LJ, Wrangham RW, Hunt K, Gebo D, Gardner L (1992) Estimators of fruit abundance of tropical trees. Biotropica 24:527–531

    Article  Google Scholar 

  • Chapman CA, Naughton-Treves L, Lawes MJ, Wasserman MD, Gillespie TR (2007) The conservation value of forest fragments: explanations for population declines of the colobus of western Uganda. Int J Primatol 23:513–578

    Article  Google Scholar 

  • Chapman CA, Ghai RR, Jacob AL, Koojo SM, Reyna-Hurtado R, Rothman JM, Twinomugisha D, Wasserman MD, Goldberg TL (2013) Going, going, gone: a 15-year history of the decline of primates in forest fragments near Kibale National Park, Uganda. In: Marsh LK, Chapman CA (eds) Primates in fragments: complexity and resilience. Springer, New York

    Google Scholar 

  • da Silva EC (1981) A preliminary survey of brown howler monkeys (Alouatta fusca) at the Cantareira Reserve (Sao Paulo, Brazil). Rev Bras Biol 41:897–909

    Google Scholar 

  • deVleeschower KM, Raboy BE (2013) Multi-level and multi-disciplinary approaches to understanding endangered primates in complex landscapes: golden-headed lion tamarins in Southern Bahia, Brazil. In: Marsh LK, Chapman CA (eds) Primates in fragments: complexity and resilience. Springer, New York

    Google Scholar 

  • Estrada A (1984) Resource use by howling monkeys (Alouatta palliata) in the rain forest of Los Tuxtlas, Veracruz, Mexico. Int J Primatol 5:105–131

    Article  Google Scholar 

  • Estrada A, Coates-Estrada R (1984) Some observations on the present distribution and conservation of Alouatta and Ateles in Southern Mexico. Am J Primatol 7:133–137

    Article  PubMed  Google Scholar 

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

    Google Scholar 

  • Gebo DL, Sargis EJ (2005) Terrestrial adaptations in the postcranial skeletons of guenons. Am J Phys Anthropol 93:341–371

    Article  Google Scholar 

  • Gentry AH (1982) Patterns of neotropical plant species diversity. Evol Biol 15:1–84

    Google Scholar 

  • Gilbert KA, Stouffer PC (1989) Use of a ground water source by mantled howler monkeys (Alouatta palliata). Biotropica 21:380

    Article  Google Scholar 

  • Glander KE (1975) Habitat description and resource utilization: an ecological view of social organization in mantled howler monkeys. In: Tuttle RH (ed) Socioecology and psychology of primates. Mouton, The Hague, pp 37–57

    Google Scholar 

  • Glander KE (1978) Drinking from arboreal water sources by mantled howling monkeys (Alouatta palliata gray). Folia Primatol 29:206–217

    Article  CAS  Google Scholar 

  • Hansen MC, Potapov PV, Moore R, Hancher M, Turubanova SA, Tyukavina A, Thau D, Stehman SV, Goetz SJ, Loveland TR, Kommareddy A, Egorov A, Chini L, Justice CO, Townshend JRG (2013) High-resolution global maps of 21st-century forest cover change. Science 342:850–853. https://doi.org/10.1126/Science.1244693

    Article  CAS  PubMed  Google Scholar 

  • Harcourt AH, Doherty DA (2005) Species-area relationships of primates in tropical forest fragments: a global analysis. J Appl Ecol 42:630–637

    Article  Google Scholar 

  • Laurance WF, Vasconcelos HL, Lovejoy TE (2000) Forst loss and fragmentation in the Amazon: implications for wildlife conservation. Oryx 34:39–45

    Article  Google Scholar 

  • Marsh LK (1999) Ecological effect of the black howler monkey (Alouatta pigra) on fragmented forests in Community Baboon Sanctuary, Belize. Ph.D. Thesis, University of Washington, St. Louis

    Google Scholar 

  • Marsh LK, Chapman CA (2013) Primates in fragments: complexity and resilience. Springer, New York

    Book  Google Scholar 

  • Mendoza E, Dirzo R (1999) Deforestation in Lacandonia (southeast Mexico): evidence for the declaration of the northernmost tropical hot-spot. Biodivers Conserv 8:1621–1641

    Article  Google Scholar 

  • Milton K (1980) The foraging strategies of howler monkeys: a study in primate economics. Columbia University Press, New York

    Google Scholar 

  • Milton K, Van Soest P, Robertson JB (1980) Digestive efficiencies of wild howler monkeys. Physiol Zool 53:402–409

    Article  Google Scholar 

  • Neville MK, Glander KE, Braza F, Ryland AB (1988) The howling monkeys, genus Alouatta. In: Mittermeier RA, Rylands AB, Coimbra-Filho AF, Da Fonseca GAB (eds) Ecology and behavior of neotropical primates, vol 2. WWF-US, Washington, DC, pp 349–453

    Google Scholar 

  • Nijman V (2013) One hundred years of solitude: effects of long-term forest fragmentation on the primate community of Java, Indonesia. In: Marsh LK, Chapman CA (eds) Primates in fragments: complexity and resilience. Springer, New York

    Google Scholar 

  • Onderdonk DA, Chapman CA (2000) Coping with forest fragmentation: the primates of Kibale National Park, Uganda. Int J Primatol 21:587–611

    Article  Google Scholar 

  • Pavelka MSM, Knopff KH (2004) Diet and activity in black howler monkeys (Alouatta pigra) in southern Belize: does degree of frugivory influence activity level? Primates 45:105–111

    Article  PubMed  Google Scholar 

  • Pozo-Montuy G (2003) Comportamiento de monos aulladores (Alouatta pigra) en habitat fragmentado, en la Rancheria Leona Vicario, Balancan, Tabasco. Universidad Juarez Autonoma de Tabasco, Mexico

    Google Scholar 

  • Pozo-Montuy G, Serio-Silva JC (2006) Comportamiento alimentario de monos aulladores negros (Alouatta pigra Lawrence, Cebidae) en hábitat fragmentado en Balancán, Tabasco, México. Acta Zool Mex 22:53–66

    Google Scholar 

  • Pozo-Montuy G, Serio-Silva JC (2007) Movement and resource use by a group of Alouatta pigra in a forest fragment in Balancan, Mexico. Primates 48:102–107

    Article  PubMed  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 70:1–8

    Article  Google Scholar 

  • Pozo-Montuy G, Serio-Silva JC, Bonilla-Sanchez YM (2011) Influence of the landscape matrix on the abundance of arboreal primates in fragmented landscapes. Primates 52:139–147

    Article  PubMed  Google Scholar 

  • Racenis J (1951) Some observations on the red howling monkey (Alouatta seniculus) in Venezuela. J Mammology 33:114–115

    Article  Google Scholar 

  • Reyes-Castillo P (1978) La fauna silvestre en el Plan Balancán Tenosique. INIREB. Biblioteca del Instituto de Ecologia Xalapa, Mexico

    Google Scholar 

  • Serio-Silva JC, Rico-Gray V (2000) Use of a stream by Mexican howler monkeys. Southwest Nat 45:332–333

    Article  Google Scholar 

  • Serio-Silva JC, Olguín EJ, Garcia-Feria L, Tapia-Fierro K, Chapman CA (2015) Cascading impacts of anthropogenically driven habitat loss: deforestation, flooding, and possible lead poisoning in howler monkeys (Alouatta pigra). Primates 56(1):29–35

    Article  PubMed  Google Scholar 

  • Terborgh J (1983) Five new world primates. Princeton University Press, Princeton

    Google Scholar 

  • Tutin CEG, White LJT, Mackanga-Missandzou A (1997) The use of rainforest mammals of natural forest fragments in an equatorial African savanna. Conserv Biol 11:1190–1203

    Article  Google Scholar 

  • van Belle S, Estrada A (2006) Demographic features of Alouatta pigra populations in extensive and fragmented forest. In: Estrada A, Garber P, Pavelka M, Luecke L (eds) New perspectives in the study of Mesoamerican Primates: distribution, ecology, behavior and conservation. Kluwer Academic/Plenum Publishers, New York, pp 121–142

    Chapter  Google Scholar 

Download references

Acknowledgments

We are grateful to Consejo Nacional de Ciencia y Tecnología (CONACyT) for the graduate studies scholarship (204435) awarded to RR-J for her master studies. The Instituto de Ecología AC (INECOL) provided the opportunity for graduate studies and a knowledge-rich environment. NSERC and CRC grants helped fund the writing stage. We thank Gilberto Pozo and Magali Bonilla for their generous support while RR-J was in Balancán. The Pozo Family and, especially, Mr. Paco Pozo and Mr. Rufino Gómez for their help with the fieldwork, and with great affection RR-J thanks Charo Mosqueda for unconditional support. Nelly Jiménez kindly assisted with plant identification and Valerie Schoof provided valuable comments on the project.

Author information

Authors and Affiliations

  1. Red DE Biología y Conservación de Vertebrados, Instituto de Ecología A.C., Veracruz, Mexico

    Juan Carlos Serio-Silva

  2. POSGRADO Instituto de Ecología, A.C., Veracruz, Mexico

    Ricarda Ramírez-Julián

  3. San Diego Zoo Global – Institute for Conservation Research, San Diego, CA, USA

    Timothy M. Eppley

  4. Department of Anthropology, McGill University, Montreal, QC, H3A 2A7, Canada

    Colin A. Chapman

  5. School of Life Sciences, University of KwaZulu-Natal, Scottsville, Pietermaritzburg, South Africa

    Colin A. Chapman

  6. Shaanxi Key Laboratory for Animal Conservation, Northwest University, Xi’an, China

    Colin A. Chapman

Authors
  1. Juan Carlos Serio-Silva
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ricarda Ramírez-Julián
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Timothy M. Eppley
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Colin A. Chapman
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Juan Carlos Serio-Silva .

Editor information

Editors and Affiliations

  1. El Colegio de la Frontera Sur (ECOSUR), Department of Biodiversity Conservation, Lerma, Campeche, Mexico

    Rafael Reyna-Hurtado

  2. Department of Anthropology, McGill University, Montreal, QC, Canada

    Colin A. Chapman

Rights and permissions

Reprints and permissions

Copyright information

© 2019 Springer Nature Switzerland AG

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Serio-Silva, J.C., Ramírez-Julián, R., Eppley, T.M., Chapman, C.A. (2019). Terrestrial Locomotion and Other Adaptive Behaviors in Howler Monkeys (Alouatta pigra) Living in Forest Fragments. In: Reyna-Hurtado, R., Chapman, C. (eds) Movement Ecology of Neotropical Forest Mammals. Springer, Cham. https://doi.org/10.1007/978-3-030-03463-4_9

Download citation

Publish with us

Policies and ethics

Search

Navigation