The Specialist Capuchin? Using Ecological Niche Models to Compare Niche Breadth in Mesoamerican Primates

  • Steig E. JohnsonEmail author
  • Kerry A. Brown
Part of the Developments in Primatology: Progress and Prospects book series (DIPR)


The high degree of dietary breadth and flexibility in capuchins (Cebus and Sapajus), coupled with their advanced cognitive abilities, is well documented. Owing to these characteristics, capuchins may be considered highly adaptable generalists, capable of occupying a wide range of habitats. The Panamanian white-throated capuchin (Cebus (capucinus) imitator) coexists with several other primate genera in Mesoamerica. Some taxa, such as the mantled howler monkey (Alouatta palliata) and Geoffroy’s spider monkey (Ateles geoffroyi), have broader geographic ranges than C. imitator. This may be due to historical biogeography (e.g. earlier colonization of the region by Ateles and Alouatta) or, alternatively, because some habitats may be less suitable for capuchins. We investigated the latter hypothesis using ecological niche models (ENMs) to predict range extent based on climate and elevation, as well as niche breadth. Our results suggest a narrow climate niche relative to the more wide-ranging Ateles geoffroyi, as well as Alouatta spp. Precipitation in the coldest quarter and temperature seasonality were the two most important climate variables for determining C. imitator habitat suitability. These findings may have implications for capuchins’ ability to persist through environmental changes (climate change and forest degradation, and loss) and warrant consideration in assessing their extinction risk.


Niche models Mesoamerica Capuchin Howler monkey Spider monkey 



We would like to thank Tracy Wyman for assistance with analyses and figures. In addition, we wish to express our appreciation to the editors and two anonymous reviewers for helpful improvements to the manuscript. We are also very grateful to the organizers of the Festschrift conference, held in Banff, Alberta, on December 2–3, 2016, for the opportunity to participate in this wonderful celebration of Dr. Fedigan’s distinguished career.

This paper evolved from discussions following various committee meetings, exams, and defences of several of Dr. Fedigan’s graduate students over the years and happily brought a lemurologist momentarily back to his capuchin roots. This is just one example of the great privilege and pleasure I (SEJ) have had to work with Linda over the past dozen years, and her intellectual inspiration long preceded that; I am grateful for her mentorship, leadership, and friendship.

Supplementary material (1.1 mb)
Fig. S15.1 Effect of each predictor variable on habitat suitability (probability of presence) in ENMs for Alouatta palliata. Curves indicate how habitat suitability changes according to the particular variable, maintaining other variables at their average sample value. The red lines indicate the mean response of the five replicate Maxent runs, and the blue bands represent +/− one standard deviation (EPS 20318 kb) (1.5 mb)
Fig. S15.2 Effect of each predictor variable on habitat suitability (probability of presence) in ENMs for Alouatta pigra . Curves indicate how habitat suitability changes according to the particular variable, maintaining other variables at their average sample value. The red lines indicate the mean response of the five replicate Maxent runs, and the blue bands represent +/− one standard deviation (EPS 22670 kb) (1.1 mb)
Fig. S15.3 Effect of each predictor variable on habitat suitability (probability of presence) in ENMs for Ateles geoffroyi . Curves indicate how habitat suitability changes according to the particular variable, maintaining other variables at their average sample value. The red lines indicate the mean response of the five replicate Maxent runs, and the blue bands represent +/− one standard deviation (EPS 20274 kb) (1.1 mb)
Fig. S15.4 Effect of each predictor variable on habitat suitability (probability of presence) in ENMs for Cebus imitator . Curves indicate how habitat suitability changes according to the particular variable, maintaining other variables at their average sample value. The red lines indicate the mean response of the five replicate Maxent runs, and the blue bands represent +/− one standard deviation (EPS 20337 kb)


  1. Amato KR, Garber PA (2014) Nutrition and foraging strategies of the black howler monkey (Alouatta pigra) in Palenque National Park, Mexico. Am J Primatol 76(8):774–787. CrossRefPubMedGoogle Scholar
  2. Baumgarten A, Williamson GB (2007) The distributions of howling monkeys (Alouatta pigra and A. palliata) in southeastern Mexico and Central America. Primates 48(4):310–315. CrossRefPubMedGoogle Scholar
  3. Behie AM, Pavelka MSM (2005) The short-term effects of a hurricane on the diet and activity of black howlers (Alouatta pigra) in Monkey River, Belize. Folia Primatol 76:1–9CrossRefGoogle Scholar
  4. Blair ME, Sterling EJ, Dusch M, Raxworthy CJ, Pearson RG (2013) Ecological divergence and speciation between lemur (Eulemur) sister species in Madagascar. J Evol Biol 26:1790–1801. CrossRefPubMedGoogle Scholar
  5. Bonilla-Sánchez YM, Serio-Silva JC, Pozo-Montuy G, Chapman CA (2012) Howlers are able to survive in Eucalyptus plantations where remnant and regenerating vegetation is available. Int J Primatol 33(1):233–245. CrossRefGoogle Scholar
  6. Boubli JP, Rylands AB, Farias IP, Alfaro ME, Alfaro JL (2012) Cebus phylogenetic relationships: a preliminary reassessment of the diversity of the untufted capuchin monkeys. Am J Primatol 74(4):381–393. CrossRefPubMedGoogle Scholar
  7. Brown JL, Yoder AD (2015) Shifting ranges and conservation challenges for lemurs in the face of climate change. Ecol Evol 5(6):1131–1142. CrossRefPubMedPubMedCentralGoogle Scholar
  8. Cai W, Borlace S, Lengaigne M, van Rensch P, Collins M, Vecchi G, Timmermann A, Santoso A, McPhaden MJ, Wu L, England MH, Wang G, Guilyardi E, Jin F-F (2014) Increasing frequency of extreme El Niño events due to greenhouse warming. Nat Clim Chang 4(2):111–116. CrossRefGoogle Scholar
  9. Campos FA, Fedigan LM (2009) Behavioral adaptations to heat stress and water scarcity in white-faced capuchins (Cebus capucinus) in Santa Rosa National Park, Costa Rica. Am J Phys Anthropol 138(1):101–111. CrossRefPubMedGoogle Scholar
  10. Campos FA, Bergstrom ML, Childers A, Hogan JD, Jack KM, Melin AD, Mosdossy KN, Myers MS, Parr NA, Sargeant E, Schoof VAM, Fedigan LM (2014) Drivers of home range characteristics across spatiotemporal scales in a Neotropical primate, Cebus capucinus. Anim Behav 91:93–109. CrossRefGoogle Scholar
  11. Campos FA, Jack KM, Fedigan LM (2015) Climate oscillations and conservation measures regulate white-faced capuchin population growth and demography in a regenerating tropical dry forest in Costa Rica. Biol Conserv 186:204–213. CrossRefGoogle Scholar
  12. Carnegie SD, Fedigan LM, Melin AD (2011) Reproductive seasonality in female capuchins (Cebus capucinus) in Santa Rosa (Area de Conservación Guanacaste), Costa Rica. Int J Primatol 32(5):1076. CrossRefGoogle Scholar
  13. Chapman CA (1987) Flexibility in diets of three species of Costa Rican primates. Folia Primatol 49(2):90–105CrossRefGoogle Scholar
  14. Chapman CA (1988) Patterns of foraging and range use by three species of neotropical primates. Primates 29(2):177–194CrossRefGoogle Scholar
  15. Chapman CA, Fedigan LM (1990) Dietary differences between neighboring Cebus capucinus groups: local traditions, food availability or responses to food profitability? Folia Primatol 54:177–186CrossRefGoogle Scholar
  16. Chapman CA, Chapman L, Glander KE (1989) Primate populations in northwestern Costa Rica: potential for recovery. Primate Conserv 10:37–44Google Scholar
  17. Collins AC, Dubach JM (2000) Biogeographic and ecological forces responsible for speciation in Ateles. Int J Primatol 21(3):421–444. CrossRefGoogle Scholar
  18. Cortés-Ortiz L, Bermingham E, Rico C, Rodrıguez-Luna E, Sampaio I, Ruiz-Garcıa M (2003) Molecular systematics and biogeography of the Neotropical monkey genus, Alouatta. Mol Phylogenet Evol 26(1):64–81. CrossRefPubMedGoogle Scholar
  19. de Albuquerque FS, Benito B, Beier P, Assunção-Albuquerque MJ, Cayuela L (2015) Supporting underrepresented forests in Mesoamerica. Nat Conservacao 13(2):152–158. CrossRefGoogle Scholar
  20. DeClerck FAJ, Chazdon R, Holl KD, Milder JC, Finegan B, Martinez-Salinas A, Imbach P, Canet L, Ramos Z (2010) Biodiversity conservation in human-modified landscapes of Mesoamerica: past, present and future. Biol Conserv 143(10):2301–2313. CrossRefGoogle Scholar
  21. Defler TR (1985) Contiguous distribution of two species of Cebus monkeys in El Tuparro National Park, Colombia. Am J Primatol 8:101–112CrossRefGoogle Scholar
  22. Dunham AE, Erhart EM, Overdorff DJ, Wright PC (2008) Evaluating effects of deforestation, hunting, and El Nino events on a threatened lemur. Biol Conserv 141(1):287–297. CrossRefGoogle Scholar
  23. Dunham AE, Erhart EM, Wright PC (2011) Global climate cycles and cyclones: consequences for rainfall patterns and lemur reproduction in southeastern Madagascar. Glob Chang Biol 17(1):219–227. CrossRefGoogle Scholar
  24. Elith J, Leathwick JR (2009) Species distribution models: ecological explanation and prediction across space and time. Annu Rev Ecol Evol Syst 40:677–697. CrossRefGoogle Scholar
  25. Elith J, Graham CH, Anderson RP, Dudik M, Ferrier S, Guisan A, Hijmans RJ, Huettmann F, Leathwick JR, Lehmann A, Li J, Lohmann LG, Loiselle BA, Manion G, Moritz C, Nakamura M, Nakazawa Y, Overton JM, Peterson AT, Phillips SJ, Richardson K, Scachetti-Pereira R, Schapire RE, Soberon J, Williams S, Wisz MS, Zimmermann NE (2006) Novel methods improve prediction of species’ distributions from occurrence data. Ecography 29:129–151CrossRefGoogle Scholar
  26. Elith J, Phillips SJ, Hastie T, Dudik M, Chee YE, Yates CJ (2011) A statistical explanation of MaxEnt for ecologists. Divers Distrib 17:43–57. CrossRefGoogle Scholar
  27. Fedigan LM, Jack K (2001) Neotropical primates in a regenerating Costa Rican dry forest: a comparison of howler and capuchin population patterns. Int J Primatol 22(5):689–713. CrossRefGoogle Scholar
  28. Fedigan LM, Rose LM, Avila RM (1996) See how they grow: tracking capuchin monkey (Cebus capucinus) populations in a regenerating Costa Rican dry forest. In: Norconk MA, Rosenberger AL, Garber PA (eds) Adaptive radiations of Neotropical Primates. Springer, Boston, pp 289–307. CrossRefGoogle Scholar
  29. Fielding AH, Bell JF (1997) A review of methods for the assessment of prediction errors in conservation presence/absence models. Environ Conserv 24(1):38–49CrossRefGoogle Scholar
  30. Ford SM (2006) The biogeographic history of Mesoamerican primates. In: Estrada A, Garber PA, Pavelka MSM, Luecke L (eds) New perspectives in the study of Mesoamerican Primates: distribution, ecology, behavior, and conservation. Springer, New York, pp 81–114CrossRefGoogle Scholar
  31. Fragaszy DM, Visalberghi E, Robinson JG (1990) Variability and adaptability in the genus Cebus. Folia Primatol 54:114–118CrossRefGoogle Scholar
  32. Fragaszy DM, Visalberghi E, Fedigan LM (2004) The complete capuchin: the biology of the genus Cebus. Cambridge University Press, CambridgeGoogle Scholar
  33. Fragaszy DM, Liu Q, Wright BW, Allen A, Brown CW, Visalberghi E (2013) Wild bearded capuchin monkeys (Sapajus libidinosus) strategically place nuts in a stable position during nut-cracking. PLoS One 8(2):e56182. CrossRefPubMedPubMedCentralGoogle Scholar
  34. Gause GF (1934) The struggle for existence. Williams and Wilkins, BaltimoreCrossRefGoogle Scholar
  35. Hardin G (1960) The competitive exclusion principle. Science 131(3409):1292–1297. CrossRefPubMedGoogle Scholar
  36. Hijmans RJ, Cameron SE, Parra JL, Jones P, Jarvis A (2005) Very high resolution interpolated climate surfaces for global land areas. Int J Climatol 25:1965–1978CrossRefGoogle Scholar
  37. Holzmann I, Agostini I, DeMatteo K, Areta JI, Merino ML, Di Bitetti MS (2015) Using species distribution modeling to assess factors that determine the distribution of two parapatric howlers (Alouatta spp.) in South America. Int J Primatol 36(1):18–32. CrossRefGoogle Scholar
  38. Ingram JC, Dawson TP (2005) Climate change impacts and vegetation response on the island of Madagascar. Phil Trans R Soc A 363:55–59CrossRefGoogle Scholar
  39. IUCN (2017) The IUCN red list of threatened species. Accessed 14 July 2017
  40. Janson CH (1998) Experimental evidence for spatial memory in foraging in wild capuchin monkeys (Cebus apella). Anim Behav 55:1229–1243CrossRefGoogle Scholar
  41. Johnson SE, Delmore KE, Brown KA, Wyman TM, Louis EE (2016) Niche divergence in a brown lemur (Eulemur spp.) hybrid zone: using ecological niche models to test models of stability. Int J Primatol 37(1):69–88. CrossRefGoogle Scholar
  42. Junker J, Blake S, Boesch C, Campbell G, Ld T, Duvall C, Ekobo A, Etoga G, Galat-Luong A, Gamys J, Ganas-Swaray J, Gatti S, Ghiurghi A, Granier N, Hart J, Head J, Herbinger I, Hicks TC, Huijbregts B, Imong IS, Kuempel N, Lahm S, Lindsell J, Maisels F, McLennan M, Martinez L, Morgan B, Morgan D, Mulindahabi F, Mundry R, N’Goran KP, Normand E, Ntongho A, Okon DT, Petre C-A, Plumptre A, Rainey H, Regnaut S, Sanz C, Stokes E, Tondossama A, Tranquilli S, Sunderland-Groves J, Walsh P, Warren Y, Williamson EA, Kuehl HS (2012) Recent decline in suitable environmental conditions for African great apes. Divers Distrib 18(11):1077–1091. CrossRefGoogle Scholar
  43. Kamilar JM, Ledogar JA (2011) Species co-occurrence patterns and dietary resource competition in primates. Am J Phys Anthropol 144(1):131–139. CrossRefPubMedGoogle Scholar
  44. Kamilar JM, Tecot SR (2016) Anthropogenic and climatic effects on the distribution of Eulemur species: an ecological niche modeling approach. Int J Primatol 37(1):47–68. CrossRefGoogle Scholar
  45. Kamilar JM, Blanco MB, Muldoon KM (2016) Ecological niche modeling of mouse lemurs (Microcebus spp.) and its implications for their species diversity and biogeography. In: Lehman SM, Radespiel U, Zimmermann E (eds) The dwarf and mouse lemurs of Madagascar: biology, behavior and conservation biogeography of the Cheirogaleidae. Cambridge University Press, Cambridge, pp 449–461CrossRefGoogle Scholar
  46. Lawler JJ, White D, Neilson RP, Blaustein AR (2006) Predicting climate-induced range shifts: model differences and model reliability. Glob Chang Biol 12(8):1568–1584. CrossRefGoogle Scholar
  47. Levins R (1968) Evolution in changing environments: some theoretical explorations. Monographs in population biology. Princeton University Press, PrincetonGoogle Scholar
  48. Lobo JM, Jiménez-Valverde A, Real R (2008) AUC: a misleading measure of the performance of predictive distribution models. Glob Ecol Biogeogr 17(2):145–151. CrossRefGoogle Scholar
  49. Lynch Alfaro JW, Boubli JP, Olson LE, Di Fiore A, Wilson B, Gutiérrez-Espeleta GA, Chiou KL, Schulte M, Neitzel S, Ross V, Schwochow D, Nguyen MTT, Farias I, Janson CH, Alfaro ME (2012) Explosive Pleistocene range expansion leads to widespread Amazonian sympatry between robust and gracile capuchin monkeys. J Biogeogr 39(2):272–288. CrossRefGoogle Scholar
  50. Milton K (1981) Food choice and digestive strategies by two sympatric primate species. Am Nat 117:496–505CrossRefGoogle Scholar
  51. Milton K, Giacalone J (2014) Differential effects of unusual climatic stress on capuchin (Cebus capucinus) and howler monkey (Alouatta palliata) populations on Barro Colorado Island, Panama. Am J Primatol 76(3):249–261. CrossRefPubMedGoogle Scholar
  52. Morales-Jimenez AL, Cortés-Ortiz L, Di Fiore A (2015) Phylogenetic relationships of Mesoamerican spider monkeys (Ateles geoffroyi): molecular evidence suggests the need for a revised taxonomy. Mol Phylogenet Evol 82(Part B):484–494. CrossRefPubMedGoogle Scholar
  53. Mosdossy KN, Melin AD, Fedigan LM (2015) Quantifying seasonal fallback on invertebrates, pith, and bromeliad leaves by white-faced capuchin monkeys (Cebus capucinus) in a tropical dry forest. Am J Phys Anthropol 158(1):67–77. CrossRefPubMedGoogle Scholar
  54. Nakazato T, Warren DL, Moyle LC (2010) Ecological and geographic modes of species divergence in wild tomatoes. Am J Bot 97(4):680–693CrossRefGoogle Scholar
  55. Nascimento FF, Lazar A, Seuanez HN, Bonvicino CR (2015) Reanalysis of the biogeographical hypothesis of range expansion between robust and gracile capuchin monkeys. J Biogeogr 42:1349–1363CrossRefGoogle Scholar
  56. Pearson RG, Raxworthy CJ, Nakamura M, Peterson AT (2007) Predicting species distributions from small numbers of occurrence records: a test case using cryptic geckos in Madagascar. J Biogeogr 34:102–117CrossRefGoogle Scholar
  57. Peers MJL, Thornton DH, Murray DL (2013) Evidence for large-scale effects of competition: niche displacement in Canada lynx and bobcat. P Roy Soc B-Biol Sci 280(1773):1–10. CrossRefGoogle Scholar
  58. Phillips SJ, Anderson RP, Schapire RE (2006) Maximum entropy modeling of species geographic distributions. Ecol Model 190:231–259CrossRefGoogle Scholar
  59. Pittman SJ, Brown KA (2011) Multi-scale approach for predicting fish species distributions across coral reef seascapes. PLoS One 6(5):e20583. CrossRefPubMedPubMedCentralGoogle Scholar
  60. Rose LM (1994) Sex differences in diet and foraging behavior in white-faced capuchins (Cebus capucinus). Int J Primatol 15(1):95–114. CrossRefGoogle Scholar
  61. Ruiz-Garcia M, Castillo MI, Ledezma A, Leguizamon N, Sánchez R, Chinchilla M, Gutierrez-Espeleta GA (2012) Molecular systematics and phylogeography of Cebus capucinus (Cebidae, Primates) in Colombia and Costa Rica by means of the mitochondrial COII gene. Am J Primatol 74(4):366–380. CrossRefPubMedGoogle Scholar
  62. Rylands AB, Groves CP, Mittermeier RA, Cortés-Ortiz L, Hines JJH (2006) Taxonomy and distributions of Mesoamerican primates. In: Estrada A, Garber PA, Pavelka MSM, Luecke L (eds) New perspectives in the study of Mesoamerican primates: distribution, ecology, behavior, and conservation. Springer US, Boston, pp 29–79. CrossRefGoogle Scholar
  63. van Schaik CP, Pfannes KR (2005) Tropical climates and phenology: a primate perspective. In: Brockman DK, van Schaik CP (eds) Seasonality in primates: studies of living and extinct human and non-human primates. Cambridge University Press, New York, pp 23–54CrossRefGoogle Scholar
  64. Syfert MM, Smith MJ, Coomes DA (2013) The effects of sampling bias and model complexity on the predictive performance of MaxEnt species distribution models. PLoS One 8(2):e55158. CrossRefPubMedPubMedCentralGoogle Scholar
  65. van Schaik CP, Terborgh JW, Wright SJ (1993) The phenology of tropical forests: adaptive significance and consequences for primary consumers. Annu Rev Ecol Syst 24:353–377CrossRefGoogle Scholar
  66. Warren DL, Glor RE, Turelli M (2010) ENMTools: a toolbox for comparative studies of environmental niche models. Ecography 33(3):607–611. CrossRefGoogle Scholar
  67. Wiederholt R, Post E (2010) Tropical warming and the dynamics of endangered primates. Biol Lett 6(2):257–260. CrossRefPubMedGoogle Scholar
  68. Wiederholt R, Post E (2011) Birth seasonality and offspring production in threatened neotropical primates related to climate. Glob Chang Biol 17(10):3035–3045. CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2018

Authors and Affiliations

  1. 1.Department of Anthropology and ArchaeologyUniversity of CalgaryCalgaryCanada
  2. 2.Department of Geography and GeologyKingston UniversityKingston Upon ThamesUK

Personalised recommendations