, Volume 59, Issue 3, pp 301–311 | Cite as

The influence of anthropogenic edge effects on primate populations and their habitat in a fragmented rainforest in Costa Rica

  • Laura M. BoltEmail author
  • Amy L. Schreier
  • Kristofor A. Voss
  • Elizabeth A. Sheehan
  • Nancy L. Barrickman
  • Nathaniel P. Pryor
  • Matthew C. Barton
Original Article


When a forest is fragmented, this increases the amount of forest edge relative to the interior. Edge effects can lead to loss of animal and plant species and decreased plant biomass near forest edges. We examined the influence of an anthropogenic forest edge comprising cattle pasture, coconut plantations, and human settlement on the mantled howler (Alouatta palliata), white-faced capuchin (Cebus capucinus), Central American spider monkey (Ateles geoffroyi), and plant populations at La Suerte Biological Research Station (LSBRS), Costa Rica. We predicted that there would be lower monkey encounter rate, mean tree species richness, and diameter at breast height (DBH) in forest edge versus interior, and that monkeys would show species-specific responses to edge based on diet, body size, and canopy height preferences. Specifically, we predicted that howler monkeys would show positive or neutral edge effects due to their flexible folivorous diet, large body size, and preference for high canopy, capuchins would show positive edge effects due to their diverse diet, small body size, and preference for low to middle canopy, and spider monkeys would show negative edge effects due their reliance on ripe fruit, large body size, and preference for high upper canopy. We conducted population and vegetation surveys along edge and interior transects at LSBRS. Contrary to predictions, total monkey encounter rate did not vary between the forest edge and forest interior. Furthermore, all three species showed neutral edge effects with no significant differences in encounter rate between forest edge and interior. Interior transects had significantly higher mean tree species richness than edge transects, and interior trees had greater DBH than edge trees, although this difference was not significant. These results suggest that forest edges negatively impact plant populations at La Suerte but that the monkeys are able to withstand these differences in vegetation.


Edge effects Costa Rica Anthropogenic Forest fragmentation Alouatta Ateles Cebus 



We are grateful to Renee Molina and the Maderas Rainforest Conservancy for their support and facilitation of our research at the La Suerte Biological Research Station, Costa Rica. We thank Renate Schlaht for sharing feeding tree data, Palomo Aguilar, Marie-dominique Franco, Arlene Ruddy, and Caleb Garzanelli for help mapping and clearing transects, Michael Ennis for population survey data collection, Nicholas Hug for GIS assistance, and Ryan Janzen for technological consultation. We also thank Madison Azzara, Troy Levinson, Tim Cooney, Tianna Wagner, Macy Cox, Natalie Lopez-Esquibel, Katie Pepperl, and Renate Schlaht for help conducting vegetation surveys. Finally, we thank the Primates associate editor and reviewers Kimberley Hockings and Giuseppe Donati for their helpful comments which have improved this paper. Our research complies with the ethical standards in the treatment of animals corresponding with the guidelines laid down by the Primate Society of Japan, NIH (US), and EC. This research protocol was approved by the Regis University Animal Care Committee and was conducted with the permission of the Costa Rican government, the Maderas Rainforest Conservancy, and the Molina family. This research was supported by University Research and Scholarship Council (URSC) Faculty and Student Research and Scholarship Grants (Regis University) and the Maderas Rainforest Conservancy.


  1. Arroyo-Rodriguez V, Dias P (2010) Effects of habitat fragmentation and disturbance on howler monkeys: a review. Am J Primatol 72:1–16CrossRefPubMedGoogle Scholar
  2. Arroyo-Rodriguez V, Mandujano S (2006) Forest fragmentation modifies habitat quality for Alouatta palliata. Int J Primatol 27:1079–1096CrossRefGoogle Scholar
  3. Arroyo-Rodriguez V, Mandujano S (2009) Conceptualization and measurement of habitat fragmentation from the primates’ perspective. Int J Primatol 30:497–514CrossRefGoogle Scholar
  4. Asensio N, Cristobal-Azkarate J, Dias P, Vea J, Rodriguez-Luna E (2007) Foraging habits of Alouatta palliata mexicana in three forest fragments. Folia Primatol 78:141–153CrossRefPubMedGoogle Scholar
  5. Balme G, Slotow R, Hunter L (2010) Edge effects and the impact of non-protected areas in carnivore conservation: leopards in the Phinda-Mkhuze Complex, South Africa. Anim Conserv 13:315–323CrossRefGoogle Scholar
  6. Bates D, Maechler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48CrossRefGoogle Scholar
  7. Boyle S, Lourenco W, Da Silva L (2009) Travel and spatial patterns change when Chiropotes satanas chiropotes inhabit forest fragments. Int J Primatol 30:515–531CrossRefGoogle Scholar
  8. Brodie J, Giordano A, Ambu L (2015) Differential responses of large mammals to logging and edge effects. Mammal Biol 80:7–13CrossRefGoogle Scholar
  9. Burke R, Lehman S (2014) Edge effects on morphometrics and body mass in two sympatric species of mouse lemurs in Madagascar. Folia Primatol 85:277–291CrossRefPubMedGoogle Scholar
  10. Canale G, Kierulff M, Chivers D (2013) A critically endangered capuchin monkey (Sapajus xanthosternos) living in a highly fragmented hotspot. In: Marsh L, Chapman C (eds) Primates in fragments. Springer, New York, pp 299–311CrossRefGoogle Scholar
  11. Chapman C (1988) Patterns of foraging and range use by three species of Neotropical primates. Primates 29:177–194CrossRefGoogle Scholar
  12. Chapman C, Wrangham R, Chapman L (1995) Ecological constraints on group size: an analysis of spider monkey and chimpanzee subgroups. Behav Ecol Sociobiol 36:59–70CrossRefGoogle Scholar
  13. Chen J, Franklin J, Spies T (1992) Vegetation response to edge environments in old-growth Douglas fir forests. Ecol Appl 2:387–396CrossRefPubMedGoogle Scholar
  14. Cunha A, Vieira M, Grelle C (2006) Preliminary observations on habitat, support use and diet in two non-native primates in an urban Atlantic forest fragment: the capuchin monkey (Cebus sp.) and the common marmoset (Callithrix jacchus) in the Tijuca forest, Rio de Janeiro. Urban Ecosyst 9:351–359CrossRefGoogle Scholar
  15. de Vries M (2017) How “edgy” are tamarins? A preliminary investigation of spatial variation in the behaviour of two sympatric callitrichids. Department of Anthropology, University of Toronto, TorontoGoogle Scholar
  16. Defler T, Rodriguez J, Hernandez-Camacho J (2003) Conservation priorities for Colombian primates. Primate Conserv 19:10–18Google Scholar
  17. di Fiore A, Link A, Campbell C (2011) The atelines: behavioral and sociological diversity in a New World monkey radiation. In: Campbell C, Fuentes A, MacKinnon K, Panger M, Bearder S (eds) Primates in perspective. Oxford University Press, New York, pp 155–188Google Scholar
  18. Estrada A (1984) Resource use by howler monkeys in the rain forest of Los Tuxtlas, Veracruz, Mexico. Int J Primatol 5:105–131CrossRefGoogle Scholar
  19. Estrada A (2015) Conservation of Alouatta: social and economic drivers of habitat loss, information vacuum, and mitigating population declines. In: Kowalewski M, Garber P, Cortes-Ortiz L, Urbani B, Youlatos D (eds) Howler monkeys, developments in primatology: progress and prospects. Springer, New York, pp 383–409Google Scholar
  20. Estrada A, Coates-Estrada R (1996) Tropical rain forest fragmentation and wild populations of primates at Los Tuxtlas, Mexico. Int J Primatol 17:759–783CrossRefGoogle Scholar
  21. Estrada A, Anzures A, Coates-Estrada R (1999) Tropical rain forest fragmentation, howler monkeys (Alouatta palliata), and dung beetles at Los Tuxtlas, Mexico. Am J Primatol 48:253–262CrossRefPubMedGoogle Scholar
  22. Estrada A, Garber PA, Rylands AB, Roos C, Fernandez-Duque E, Di Fiore A, Li B (2017) Impending extinction crisis of the world’s primates: why primates matter? Sci Adv 3:e1600946CrossRefPubMedPubMedCentralGoogle Scholar
  23. Fleagle J, Mittermeier R (1980) Locomotor behavior, body size, and comparative ecology of seven Surinam monkeys. Am J Phys Anth 52:301–314CrossRefGoogle Scholar
  24. Ford S, Davis L (1992) Systematics and body size: implications for feeding adaptations in New World monkeys. Am J Phys Anth 88:415–468CrossRefGoogle Scholar
  25. Freese C (1983) Cebus capucinus. In: Jazen D (ed) Costa Rican natural history. Cambridge University Press, Cambridge, pp 458–460Google Scholar
  26. Ganzhorn J (1995) Low-level forest disturbance effects on primary production, leaf chemistry, and lemur populations. Ecology 76:2084–2096CrossRefGoogle Scholar
  27. Garber P, Kowalewski M (2015) New challenges in the study of howler monkey behavioral ecology and conservation: where we are and where we need to go? In: Kowalewski M, Garber P, Cortes-Ortiz L, Urbani B, Youlatos D (eds) Howler monkeys, developments in primatology: progress and prospects. Springer, New York, pp 413–428Google Scholar
  28. Garber P, Estrada A, Pavelka M (2006) New perspectives in the study of Mesoamerican primates: concluding comments and conservation priorities. 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 563–584CrossRefGoogle Scholar
  29. Garber P, Molina A, Molina R (2010) Putting the community back in community ecology and education: the role of field schools and private reserves in the ethical training of primatologists. Am J Primatol 72:785–793CrossRefPubMedGoogle Scholar
  30. Gibson L, Lynam A, Bradshaw C, He F, Bickford D, Woodruff D, Laurance W (2013) Near-complete extinction of native small mammal fauna 25 years after forest fragmentation. Science 341:1508–1510CrossRefPubMedGoogle Scholar
  31. Glander K (1982) The impact of plant secondary compounds on primate feeding behavior. Yearbook Phys Anth 15:1–18Google Scholar
  32. Glanz W (1990) Neotropical mammal densities: how unusual is the community on Barro Colorado Island, Panama? In: Gentry A (ed) Four Neotropical rainforests. Yale University Press, New Haven, pp 287–313Google Scholar
  33. Haddad NM, Brudwig LA, Clobert J, Davies KF, Gonzalez A, Holt RD, Townshend JR (2015) Habitat fragmentation and its lasting impact on Earth’s ecosystems. Sci Adv 1:e1500052CrossRefPubMedPubMedCentralGoogle Scholar
  34. Harris L (1988) Edge effects and conservation of biotic diversity. Conserv Biol 2:330–332CrossRefGoogle Scholar
  35. Klein L, Klein D (1977) Feeding behaviour of the Colombian spider monkey. In: Clutton-Brock T (ed) Primate ecology: studies of the feeding and ranging behavior in lemurs, monkeys and apes. Academic Press, London, pp 153–181Google Scholar
  36. Kulp J, Heymann E (2015) Ranging, activity budget, and diet composition of red titi monkeys (Callicebus cupreus) in primary forest and forest edge. Primates 56:273–278CrossRefPubMedPubMedCentralGoogle Scholar
  37. Laurance W (1991) Edge effects in tropical forest fragments: application of a model for the design of nature reserves. Biol Conserv 57:205–219CrossRefGoogle Scholar
  38. Laurance W, Yensen E (1991) Predicting the impacts of edge in fragmented habitats. Biol Conserv 55:77–92CrossRefGoogle Scholar
  39. Lehman S (2007) Spatial variations in Eulemur fulvus rufus and Lepilemur mustelinus densities in Madagascar. Folia Primatol 78:46–55CrossRefPubMedGoogle Scholar
  40. Lehman S, Rajaonson A, Day S (2006a) Edge effects on the density of Chierogaleus major. Int J Primatol 27:1569–1588CrossRefGoogle Scholar
  41. Lehman S, Rajaonson A, Day S (2006b) Edge effects and their influence on lemur density and distribution in southeast Madagascar. Am J Phys Anthropol 129:232–241CrossRefPubMedGoogle Scholar
  42. Lehman S, Rajaonson A, Day S (2006c) Lemur responses to edge effects in the Vohibola III classified forest, Madagascar. Am J Primatol 68:293–299CrossRefPubMedGoogle Scholar
  43. Lenz B, Jack K, Spironello W (2014) Edge effects in the primate community of the biological dynamics of Forest Fragments Project, Amazonas, Brazil. Am J Phys Anth 155:436–446CrossRefGoogle Scholar
  44. Lidicker W (1999) Responses of mammals to habitat edges: an overview. Landscape Ecol 14:333–343CrossRefGoogle Scholar
  45. Lovejoy T, Bierregaard R, Rylands A, Malcolm J, Quintela C, Harper L, Brown K, Powell A, Powell G, Schubart H, Hays M (1986) Edge and other effects of isolation on Amazon forest fragments. In: Soule M (ed) Conservation biology: the science of scarcity and diversity. Sunderland/Sinauer, New York, pp 257–285Google Scholar
  46. Marsh C, Link A, King-Bailey G, Donati G (2016) Effects of fragment and vegetation structure on the population abundance of Ateles hybridus, Alouatta seniculus and Cebus albifrons in Magdalena Valley, Colombia. Folia Primatol 87:17–30CrossRefPubMedGoogle Scholar
  47. Martin L, Blossey B, Ellis E (2012) Mapping where ecologists work: biases in the global distribution of terrestrial ecological observations. Front Ecol Environ 10:195–201CrossRefGoogle Scholar
  48. Mbora D, Meikle D (2004) Forest fragmentation and the distribution, abundance and conservation of the Tana River red colobus (Procolobus rufomitratus). Biol Conserv 118:67–77CrossRefGoogle Scholar
  49. McGoogan K (2011) Edge effects on the behaviour and ecology of Propithecus coquereli in northwest Madagascar. Department of Anthropology, University of Toronto, TorontoGoogle Scholar
  50. McKinney T, Westin J, Serio-Silva J (2015) Anthropogenic habitat modification, tourist interactions and crop-raiding in howler monkeys. In: Kowalewski M, Garber P, Cortes-Ortiz L, Urbani B, Youlatos D (eds) Howler monkeys, developments in primatology: progress and prospects. Springer, New York, pp 281–311Google Scholar
  51. McLennan M, Spagnoletti N, Hockings K (2017) The implications of primate behavioral flexibility for sustainable human-primate coexistence in anthropogenic habitats. Int J Primatol 38:105–121CrossRefGoogle Scholar
  52. Milton K (1979) Factors influencing leaf choice by howler monkeys: a test of some hypotheses of food selection by generalist herbivores. Am Nat 114:362–378CrossRefGoogle Scholar
  53. Mittermeier R, Schwitzer C, Rylands A, Taylor L, Chiozza F, Williamson E, Wallis J (2012) Primates in peril: the world’s 25 most endangered primates 2012–2014. IUCN/SSC Primate Specialist Group (PSG), International Primatological Society (IPS), Conservation International (CI), Bristol Conservation and Science Foundation, Bristol, pp 1–40Google Scholar
  54. Molina M (2015) A brief history of the Molina family, and the birth of the Maderas Rainforest Conservancy at the La Suerte and Ometepe Field Stations—a narrative. In: Huettman F (ed) Central American biodiversity: conservation, ecology and a sustainable future. Springer Science + Business Media, New York, pp 199–214CrossRefGoogle Scholar
  55. Munoz D, Estrada A, Naranjo E, Ochoa S (2006) Foraging ecology of howler monkeys in a cacao (Theobroma cacao) plantation in Comalcalco, Mexico. Am J Primatol 68:127–142CrossRefPubMedGoogle Scholar
  56. Myers N, Mittermeier R, Mittermeier C, Fonseca G, Kent J (2000) Biodiversity hotspots for conservation priorities. Nature 403:853–858CrossRefPubMedGoogle Scholar
  57. Occhibove F, Ferro C, Campera M, Liponi G, Borgognini-Tarli S, Ganzhorn J, Donati G (2015) Living in islands of forests: nutritional ecology of the howler monkey (Alouatta palliata) at La Suerte Biological Field Station, North-eastern Costa Rica. In: Huettman F (ed) Central American biodiversity: conservation, ecology and a sustainable future. Springer Science + Business Media, New York, pp 525–538CrossRefGoogle Scholar
  58. Peres C (1999) General guidelines for standardizing line-transect surveys of tropical forest primates. Neotrop Primates 7:11–15Google Scholar
  59. Peres C, Dolman P (2000) Density compensation in Neotropical primate communities: evidence from 56 hunted and non-hunted Amazonian forests of varying productivity. Oecologia 122:175–189CrossRefPubMedGoogle Scholar
  60. Perry S (1997) Male-female social relationships in wild white-faced capuchins (Cebus capucinus). Behaviour 134:477–510CrossRefGoogle Scholar
  61. Pollock S, Nielsen S, St. Clair C (2017) A railway increases the abundance and accelerates the phenology of bear-attracting plants in a forested, mountain park. Ecosphere 8:e01985CrossRefGoogle Scholar
  62. Pruetz J, Leasor H (2002) Densities of primate species in forest fragments at La Suerte Biological Field Station, Costa Rica. Neotrop Primates 10:4–9Google Scholar
  63. R Core Team (2016) R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing. Available from:
  64. Ramsay M, Razafindrakoto A, Lehman S (2017) The effects of a national highway on the endangered golden-brown mouse lemur Microcebus ravelobensis in Ankarafantsika National Park, Madagascar. Oryx. Google Scholar
  65. Reis L, Fletcher R, Battin J, Sisk T (2004) Ecological responses to habitat edges: mechanisms, models, and variability explained. Annu Rev Ecol Syst 35:491–522CrossRefGoogle Scholar
  66. Rose L (1994) Sex differences in diet and foraging behaviour in white-faced capuchins (Cebus capucinus). Int J Primatol 15:95–114CrossRefGoogle Scholar
  67. Rose L (1997) Vertebrate predation and food-sharing in Cebus and Pan. Int J Primatol 18:727–765CrossRefGoogle Scholar
  68. Ryan S, Starks P, Milton K, Getz W (2008) Intersexual conflict and group size in Alouatta palliata: a 23-year evaluation. Int J Primatol 29:405–420CrossRefGoogle Scholar
  69. Saunders D, Hobbs R, Margules C (1991) Biological consequences of ecosystem fragmentation: a review. Conserv Biol 5:18–32CrossRefGoogle Scholar
  70. Shimooka Y (2004) Seasonal variation in association patterns of wild spider monkeys (Ateles belzebuth belzebuth) at La Macarena, Colombia. Am J Primatol 52:13–29Google Scholar
  71. Shimooka Y (2005) Sexual differences in ranging of Ateles belzebuth belzebuth at La Macarena, Colombia. Int J Primatol 26:385–406CrossRefGoogle Scholar
  72. Skrinyer AJ (2016) Living on the edge: an assessment of habitat disturbance and primate use on the Osa Peninsula, Costa Rica. MA Thesis: Kent State UniversityGoogle Scholar
  73. Stevens S, Husband T (1998) The influence of edge on small mammals: evidence from Brazilian Atlantic forest fragments. Biol Conserv 85:1–8CrossRefGoogle Scholar
  74. Stevenson P, Link A, Ramirez B (2005) Frugivory and seed fate in Bursera inversa at Tinigua National Park, Colombia: implications for primate conservation. Biotropica 37:431–438CrossRefGoogle Scholar
  75. van Roosmalen M (1985) Habitat preferences, diet, feeding strategy and social organization of the black spider monkey (Ateles paniscus paniscus Linnaeus 1758) in Surinam. Acta Amazonica 15:1–238Google Scholar
  76. Zárate D, Andresen E, Estrada A, Serio-Silva J (2014) Black howler monkey (Alouatta pigra) activity, foraging and seed dispersal patterns in shaded cocoa plantations versus rainforest in southern Mexico. Am J Primatol 76:890–899CrossRefPubMedGoogle Scholar

Copyright information

© Japan Monkey Centre and Springer Japan KK, part of Springer Nature 2018

Authors and Affiliations

  • Laura M. Bolt
    • 1
    • 4
    Email author
  • Amy L. Schreier
    • 2
    • 4
  • Kristofor A. Voss
    • 2
  • Elizabeth A. Sheehan
    • 2
    • 4
  • Nancy L. Barrickman
    • 3
    • 4
  • Nathaniel P. Pryor
    • 2
    • 4
  • Matthew C. Barton
    • 2
    • 4
  1. 1.Department of AnthropologyUniversity of TorontoTorontoCanada
  2. 2.Department of BiologyRegis UniversityDenverUSA
  3. 3.Salt Lake Community CollegeSalt Lake CityUSA
  4. 4.The Maderas Rainforest ConservancyMiamiUSA

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