, Volume 55, Issue 3, pp 345–352 | Cite as

Mammal assemblages in forest fragments and landscapes occupied by black howler monkeys

  • Ariadna Rangel-NegrínEmail author
  • Alejandro Coyohua-Fuentes
  • Domingo Canales-Espinosa
  • Pedro Américo D. Dias
News and Perspectives


Species assemblages in disturbed habitats vary as a function of the interaction between species requirements and the spatial configuration of the habitat. There are many reports accounting for the presence of howler monkeys in fragments where other mammals are absent, suggesting that they are more resilient. In the present study we explored this idea and predicted that if howler monkeys were more resilient to habitat loss and fragmentation than other mammals, mammal assemblages in fragments occupied by howler monkeys should include fewer species with decreasing amount of habitat (smaller fragment size and less habitat in the landscape) and increasing number of forest fragments. We explored these relationships by additionally considering the feeding and life habits of mammal species, as well as the isolation and proximity of each fragment to human settlements and roads. We sampled the presence of mammals in five fragments occupied by black howler monkeys (Alouatta pigra) in the Mexican state of Campeche. Through direct sights performed during 240 h in each fragment, we observed 23 species. At the landscape scale, higher fragmentation was associated with a decrease in herbivores, omnivores and total number of species. At the fragment scale semiarboreal, omnivore, and total number of species increased with increasing fragment size. This study supports the idea that howler monkeys are more resilient to forest loss and fragmentation than other native mammals, and our exploratory analyses suggest that the specific mammal assemblages that are found in fragments are related to both landscape and fragment scale spatial attributes, as well as with species-specific characteristics.


Alouatta Fragment size Landscape spatial attributes Mexico Trophic level 



We thank all the students and volunteers that helped during fieldwork. The following people and institutions granted permission to work in their properties and facilitated our fieldwork: Comisarios Ejidales de Abelardo Domínguez, Calax, Conhuas, Plan de Ayala, and Carmén Gómez; Ayuntamiento de Calakmul; Lic. C. Vidal and Lic. L. Álvarez, INAH Campeche; Biól. F. Durand Siller, Reserva de la Biósfera Calakmul, CONANP; Ing. V. Olvera, El Álamo. This study was supported by CFE (RGCPTTP-UV-001/04), Universidad Veracruzana, Conacyt (Grant Number: 235839; i010/458/2013 C-703/2013) and Idea Wild. Some of the ideas included in this paper were presented at the “II Congresso Latino Americano & XV Congresso Brasileiro de Primatologia” (Recife, Brasil, August 2013). We thank conference participants for stimulating discussions, and L.K. Marsh for very constructive comments on a previous version of the manuscript. A. Rangel-Negrín and P.A.D. Dias thank Mariana for support during the writing of this paper.


  1. Arroyo-Rodríguez, Cuesta-del Moral E, Mandujano S, Chapman CA, Reyna-Hurtado R, Fahrig L (2013) Assessing habitat fragmentation effects on primates: the importance of evaluating questions at the correct scale. In: Marsh L, Chapman CA (eds) Primates in fragments: complexity and resilience. Springer, New York, pp 13–28Google Scholar
  2. Asensio N, Cristóbal-Azkarate J, Dias PAD, Veà JJ, Rodríguez-Luna E (2007) Foraging habits of Alouatta palliata mexicana in three forest fragments. Folia Primatol 78:141–153PubMedCrossRefGoogle Scholar
  3. Asensio N, Arroyo-Rodríguez V, Dunn J, Cristóbal-Azkarate J (2009) Conservation value of landscape supplementation for howler monkeys living in forest patches. Biotropica 41:768–773CrossRefGoogle Scholar
  4. Bicca-Marques JC (2003) How do howler monkeys cope with habitat fragmentation? In: Marsh LK (ed) Primates in fragments: ecology and conservation. Kluwer Academic/Plenum Publishers, New York, pp 283–303CrossRefGoogle Scholar
  5. Bolger DT, Suarez AV, Crooks KR, Morrison SA, Case TJ (2000) Arthropods in urban habitat fragments in southern California: area, age, and edge effects. Ecol Appl 10:1230–1248CrossRefGoogle Scholar
  6. Canale GR, Peres CA, Guidorizzi CE, Gatto CAF, Kierulff MCM (2012) Pervasive defaunation of forest remnants in a tropical biodiversity hotspot. PLoS One 7:e41671PubMedCentralPubMedCrossRefGoogle Scholar
  7. Cardillo M, Mace GM, Jones KE, Bielby J, Bininda-Emonds ORP, Sechrest W, Orme CDL, Purvis A (2005) Multiple causes of high extinction risk in large mammal species. Science 309:1239–1241PubMedCrossRefGoogle Scholar
  8. Cristóbal-Azkarate J, Arroyo-Rodríguez V (2007) Diet and activity pattern of howler monkeys (Alouatta palliata) in Los Tuxtlas, Mexico: effects of habitat fragmentation and implications for conservation. Am J Primatol 69:1013–1029PubMedCrossRefGoogle Scholar
  9. Crooks KR (2002) Relative sensitivities of mammalian carnivores to habitat fragmentation. Conserv Biol 16:488–502CrossRefGoogle Scholar
  10. Crooks KR, Soulé ME (1999) Mesopredator release and avifaunal extinctions in a fragmented system. Nature 400:563–565CrossRefGoogle Scholar
  11. Daily GC, Ceballos G, Pacheco J, Suzan G, Sánchez-Azofeifa A (2002) Countryside biogeography of Neotropical mammals: conservation opportunities in agricultural landscape of Costa Rica. Conserv Biol 17:1814–1826CrossRefGoogle Scholar
  12. Didham RK, Hammond PM, Lawton JH, Eggleton P, Stork NE (1998) Beetle species responses to tropical forest fragmentation. Ecol Monogr 68:295–323CrossRefGoogle Scholar
  13. Driscoll DA, Weir T (2005) Beetle responses to habitat fragmentation depend on ecological traits, habitat condition and remnant size. Conserv Biol 19:182–194CrossRefGoogle Scholar
  14. Dunning JB, Danielson BJ, Pulliam HR (1992) Ecological processes that affect populations in complex landscapes. Oikos 65:169–175CrossRefGoogle Scholar
  15. Engeman RM, Massei G, Sage M, Gentle MN (2013) Monitoring wild pig populations: a review of methods. Environ Sci Pollut R 20:8077–8091CrossRefGoogle Scholar
  16. Frair JL, Merrill EH, Visscher DR, Fortin D, Beyer HL, Morales JM (2005) Scales of movement by elk (Cervus elaphus) in response to heterogeneity in forage resources and predation risk. Landsc Ecol 20:273–287CrossRefGoogle Scholar
  17. Galetti M, Dirzo R (2013) Ecological and evolutionary consequences of living in a defaunated world. Biol Conserv 163:1–6CrossRefGoogle Scholar
  18. Gaulin SJC, Knight DH, Gaulin CK (1980) Local variance in Alouatta group size and food availability on Barro Colorado Island. Biotropica 12:137–143CrossRefGoogle Scholar
  19. Guzmán-Soriano D, Retana-Guiascón OG, Cú-Vizcarra JD (2013) Lista de los mamíferos terrestres del estado de Campeche, México. Acta Zool Mex 29:105–128Google Scholar
  20. Hamel S, Killengreen ST, Henden JA, Eide NE, Roed-Eriksen L, Ims RA, Yoccoz NG (2013) Towards good practice guidance in using camera-traps in ecology: influence of sampling design on validity of ecological inferences. Methods Ecol Evol 4:105–113CrossRefGoogle Scholar
  21. Jorge MLSP, Galetti M, Ribeiro MC, Ferraz KMPMB (2013) Mammal defaunation as surrogate of trophic cascades in a biodiversity hotspot. Biol Conserv 163:49–57CrossRefGoogle Scholar
  22. Komonen A, Penttilä R, Lindgren M, Hanski I (2000) Forest fragmentation truncates a food chain based on an old-growth forest bracket fungus. Oikos 90:119–126CrossRefGoogle Scholar
  23. Krebs D (1998) Ecological methodology, 2nd edn. Benjamin/Cummings, Menlo ParkGoogle Scholar
  24. Laurance W, Laurance SG, Hilbert DH (2008) Long-term dynamics of a fragmented rainforest mammal assemblage. Conserv Biol 22:1154–1164PubMedCrossRefGoogle Scholar
  25. Lindenmayer DB, Cunningham RB, Donnelly CF, Nix H, Lindenmayer BD (2002) Effects of forest fragmentation on bird assemblages in a novel landscape context. Ecol Monogr 72:1–18CrossRefGoogle Scholar
  26. McKinney ML (2002) Urbanization, biodiversity, and conservation. Bioscience 52:883–890CrossRefGoogle Scholar
  27. Mittermeier RA, van Roosmalen MGM (1981) Preliminary observations on habitat utilization and diet in eight Surinam monkeys. Folia Primatol 36:1–39PubMedCrossRefGoogle Scholar
  28. Olson ZH, Beasley JC, DeVault TL, Rhodes OE Jr (2012) Scavenger community response to the removal of a dominant scavenger. Oikos 121:77–84CrossRefGoogle Scholar
  29. Peres CA, Palacios E (2007) Basin-wide effects of game harvest on vertebrate population densities in Amazonian forests: implications for animal-mediated seed dispersal. Biotropica 39:304–315CrossRefGoogle Scholar
  30. Pozo-Montuy G, Serio-Silva JC, Chapman CA, Bonilla-Sánchez YM (2013) Resource use in a landscape matrix by an arboreal primate: evidence of supplementation in Alouatta pigra. Int J Primatol 34:714–731CrossRefGoogle Scholar
  31. Schwarzkopf L, Rylands AB (1989) Primate species richness in relation to habitat structure in Amazonian rainforest fragments. Biol Conserv 48:1–12CrossRefGoogle Scholar
  32. Swihart RK, Gehring TM, Kolozsvary MB (2003) Responses of ‘resistant’ vertebrates to habitat loss and fragmentation: the importance of niche breadth and range boundaries. Divers Distrib 9:1–18CrossRefGoogle Scholar
  33. Terborgh J, Lopez L, Nuñez VP, Rao M, Shahabuddin G, Orihuela G, Riveros M, Ascanio R, Adler GH, Lambert TD, Balbas L (2001) Ecological meltdown in predator-free forest fragments. Science 294:1923–1926PubMedCrossRefGoogle Scholar
  34. Van Belle S, Estrada A (2006) Demographic features of Alouatta pigra populations in extensive and fragmented forest. In: Estrada A, Garber PA, Pavelka MSM, Luecke L (eds) New perspectives in the study of Mesoamerican primates: distribution, ecology, behavior and conservation, Kluwer Academic/Plenum Publishers, New York, pp 121–142Google Scholar
  35. Wright SJ (2003) The myriad consequences of hunting for vertebrates and plants in tropical forests. Perspect Plant Ecol 6:73–86CrossRefGoogle Scholar

Copyright information

© Japan Monkey Centre and Springer Japan 2014

Authors and Affiliations

  • Ariadna Rangel-Negrín
    • 1
    Email author
  • Alejandro Coyohua-Fuentes
    • 1
  • Domingo Canales-Espinosa
    • 1
  • Pedro Américo D. Dias
    • 1
  1. 1.Instituto de NeuroetologíaUniversidad VeracruzanaXalapaMexico

Personalised recommendations