Advertisement

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

  • Juan Carlos Serio-SilvaEmail author
  • Ricarda Ramírez-Julián
  • Timothy M. Eppley
  • Colin A. Chapman
Chapter

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.

Keywords

Terrestrial locomotion Forest fragments Vegetation remnants Water intake Drinking 

Notes

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.

References

  1. 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 YorkGoogle Scholar
  2. 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 13:1–3CrossRefGoogle Scholar
  3. 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 28:637–655CrossRefGoogle Scholar
  4. Bicca-Marques JC, Calegaro-Marques C (1995) Drinking behavior of the black howler monkey (Alouatta caraya). Folia Primatol 58:107–111CrossRefGoogle Scholar
  5. 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 33:233–245CrossRefGoogle Scholar
  6. Brussard PF (1985) Minimum viable populations: how many are too few? Restor Manag Notes 3(1):21–25Google Scholar
  7. 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: 1039–1051CrossRefGoogle Scholar
  8. Chalise MK (2013) Fragmented primate populations of Nepal. In: Marsh LK, Chapman CA (eds) Primates in fragments: complexity and resilience. Springer, New York, pp 329–356CrossRefGoogle Scholar
  9. Chapman CA, Chapman LJ, Wrangham RW, Hunt K, Gebo D, Gardner L (1992) Estimators of fruit abundance of tropical trees. Biotropica 24:527–531CrossRefGoogle Scholar
  10. 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 23:513–578CrossRefGoogle Scholar
  11. 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 YorkGoogle Scholar
  12. da Silva EC (1981) A preliminary survey of brown howler monkeys (Alouatta fusca) at the Cantareira Reserve (Sao Paulo, Brazil). Rev Bras Biol 41:897–909Google Scholar
  13. 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 YorkGoogle Scholar
  14. Estrada A (1984) Resource use by howling monkeys (Alouatta palliata) in the rain forest of Los Tuxtlas, Veracruz, Mexico. Int J Primatol 5:105–131CrossRefGoogle Scholar
  15. Estrada A, Coates-Estrada R (1984) Some observations on the present distribution and conservation of Alouatta and Ateles in Southern Mexico. Am J Primatol 7:133–137CrossRefGoogle Scholar
  16. Forman RTT, Godron M (1986) Landscape ecology. Wiley, New YorkGoogle Scholar
  17. Gebo DL, Sargis EJ (2005) Terrestrial adaptations in the postcranial skeletons of guenons. Am J Phys Anthropol 93:341–371CrossRefGoogle Scholar
  18. Gentry AH (1982) Patterns of neotropical plant species diversity. Evol Biol 15:1–84Google Scholar
  19. Gilbert KA, Stouffer PC (1989) Use of a ground water source by mantled howler monkeys (Alouatta palliata). Biotropica 21:380CrossRefGoogle Scholar
  20. 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 37–57Google Scholar
  21. Glander KE (1978) Drinking from arboreal water sources by mantled howling monkeys (Alouatta palliata gray). Folia Primatol 29:206–217CrossRefGoogle Scholar
  22. 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.1244693CrossRefPubMedPubMedCentralGoogle Scholar
  23. Harcourt AH, Doherty DA (2005) Species-area relationships of primates in tropical forest fragments: a global analysis. J Appl Ecol 42:630–637CrossRefGoogle Scholar
  24. Laurance WF, Vasconcelos HL, Lovejoy TE (2000) Forst loss and fragmentation in the Amazon: implications for wildlife conservation. Oryx 34:39–45CrossRefGoogle Scholar
  25. 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. LouisGoogle Scholar
  26. Marsh LK, Chapman CA (2013) Primates in fragments: complexity and resilience. Springer, New YorkCrossRefGoogle Scholar
  27. Mendoza E, Dirzo R (1999) Deforestation in Lacandonia (southeast Mexico): evidence for the declaration of the northernmost tropical hot-spot. Biodivers Conserv 8:1621–1641CrossRefGoogle Scholar
  28. Milton K (1980) The foraging strategies of howler monkeys: a study in primate economics. Columbia University Press, New YorkGoogle Scholar
  29. Milton K, Van Soest P, Robertson JB (1980) Digestive efficiencies of wild howler monkeys. Physiol Zool 53:402–409CrossRefGoogle Scholar
  30. 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 349–453Google Scholar
  31. 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 YorkGoogle Scholar
  32. Onderdonk DA, Chapman CA (2000) Coping with forest fragmentation: the primates of Kibale National Park, Uganda. Int J Primatol 21:587–611CrossRefGoogle Scholar
  33. 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 45:105–111CrossRefGoogle Scholar
  34. 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, MexicoGoogle Scholar
  35. 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 22:53–66Google Scholar
  36. 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 48:102–107CrossRefGoogle Scholar
  37. 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 70:1–8CrossRefGoogle Scholar
  38. 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 52:139–147CrossRefGoogle Scholar
  39. Racenis J (1951) Some observations on the red howling monkey (Alouatta seniculus) in Venezuela. J Mammology 33:114–115CrossRefGoogle Scholar
  40. Reyes-Castillo P (1978) La fauna silvestre en el Plan Balancán Tenosique. INIREB. Biblioteca del Instituto de Ecologia Xalapa, MexicoGoogle Scholar
  41. Serio-Silva JC, Rico-Gray V (2000) Use of a stream by Mexican howler monkeys. Southwest Nat 45:332–333CrossRefGoogle Scholar
  42. 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):29–35CrossRefGoogle Scholar
  43. Terborgh J (1983) Five new world primates. Princeton University Press, PrincetonGoogle Scholar
  44. Tutin CEG, White LJT, Mackanga-Missandzou A (1997) The use of rainforest mammals of natural forest fragments in an equatorial African savanna. Conserv Biol 11:1190–1203CrossRefGoogle Scholar
  45. 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 121–142CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Juan Carlos Serio-Silva
    • 1
    Email author
  • Ricarda Ramírez-Julián
    • 2
  • Timothy M. Eppley
    • 3
  • Colin A. Chapman
    • 4
    • 5
    • 6
  1. 1.Red DE Biología y Conservación de VertebradosInstituto de Ecología A.C.VeracruzMexico
  2. 2.POSGRADO Instituto de Ecología, A.C.VeracruzMexico
  3. 3.San Diego Zoo Global – Institute for Conservation ResearchSan DiegoUSA
  4. 4.Department of AnthropologyMcGill UniversityMontrealCanada
  5. 5.School of Life SciencesUniversity of KwaZulu-NatalScottsvilleSouth Africa
  6. 6.Shaanxi Key Laboratory for Animal ConservationNorthwest UniversityXi’anChina

Personalised recommendations