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Dietary Profile, Food Composition, and Nutritional Intake of Female White-Faced Capuchins

  • Mackenzie L. Bergstrom
  • Amanda D. Melin
  • Monica S. Myers
  • Linda M. Fedigan
Chapter
Part of the Developments in Primatology: Progress and Prospects book series (DIPR)

Abstract

Seasonal variation in food availability and nutritional intake can ultimately affect female reproductive success. Although many primate studies have looked at foraging behaviour as a measure of diet, nutritional ecology and associated physiological consequences are a relatively new area of research. We present data on variation in the dietary profiles, foraging behaviour, and nutritional intake of female white-faced capuchins (Cebus capucinus imitator) in response to temporal variation in food abundance within the home ranges of three groups in the Área de Conservación Guanacaste, Sector Santa Rosa, Costa Rica. We estimated nutritional requirements based on published laboratory research and nutritional standards to determine whether females meet requirements in the face of seasonal variation in food abundance. Our results show that fruit contributed most to overall energy gain despite females devoting a greater proportion of foraging time to invertebrates; thus time spent foraging does not accurately reflect energy intake. On a dry matter basis, fruits provided the most important source of water-soluble carbohydrates, whereas high proportions of protein intake came from invertebrates, particularly when fruit availability was low. However, the greater weight of fruit items compared to invertebrates on a dry matter basis likely contributed to females’ ability to consume macronutrients at higher rates while foraging on fruit due to higher mass intake per unit time. Requirement estimates and observed intake revealed that there are times during low-fruit seasons in which females do not appear to meet their minimum nutritional requirements, warranting further investigation into the physiological consequences of this shortfall.

Keywords

Nutrition Diet Seasonal variation Food availability Neotropical primate 

Notes

Acknowledgements

Thank you to the Ministry of Environment, Energy and Technology (MINAET) of Costa Rica and the Animal Care Committee at the University of Calgary for permissions to conduct research. This project was also supported by Sr. R Blanco, MM Chavarria, and the staff of the Área de Conservación Guanacaste. Many field assistants and friends aided in the collection of valuable data for this project including M Myers, B Thankey, H Clouse, C Lees, B Kowalzik, Dr. C Turner Hogan, and S Chevez. R Espinoza, A Guadamuz, J Vargas, and R Franco provided valuable assistance with the identification of plant and invertebrate samples. We thank G Bridgett for logistical help with permits and Dr. J Addicott and J McQuade for assistance with data organization and database design. Thank you to Dr. E Vogel for contributing nutritional data and Drs. E Wikberg and F Campos for statistical guidance. The authors were supported by the following funding organizations: To MLB: The Leakey Foundation, Alberta Innovates Technology Futures, International Primatological Society, Animal Behaviour Society, Sigma Xi, and University of Calgary. To ADM: Natural Sciences and Engineering Research Council of Canada (NSERC) and Canada Research Chairs Program. To LMF: NSERC and Canada Research Chairs Program.

Supplementary material

432332_1_En_11_MOESM1_ESM.docx (48 kb)
Appendices A to D (DOCX 47 kb)

References

  1. Altmann J (1974) Observational study of behavior: sampling methods. Behaviour 49:227–265PubMedCrossRefPubMedCentralGoogle Scholar
  2. Altmann SA (1991) Diets of yearling female primates (Papio cynocephalus) predict lifetime fitness. Proc Natl Acad Sci U S A 88(2):420–423PubMedPubMedCentralCrossRefGoogle Scholar
  3. Altmann SA (1998) Foraging for survival: yearling baboons in Africa. University of Chicago Press, ChicagoGoogle Scholar
  4. ANKOM Technology (2011) Method 6: neutral detergent fiber in feeds - filter bag technique (for A200 and A200I). https://www.ankom.com/sites/default/files/document-files/Method_6_NDF_A200.pdf. Accessed 31 Jan 2017
  5. Antonow-Schlorke I, Schwab M, Cox LA, Li C, Stuchlik K, Witte OW, Nathanielsz PW, McDonald TJ (2011) Vulnerability of the fetal primate brain to moderate reduction in maternal global nutrient availability. Proc Natl Acad Sci U S A 108(7):3011–3016PubMedPubMedCentralCrossRefGoogle Scholar
  6. AOAC International (2012a) AOAC official method 942.05 ash of animal feed. In: Latimer G (ed) Official methods of analysis of AOAC International, 19th edn. AOAC International, GaithersburgGoogle Scholar
  7. AOAC International (2012b) Official method 2003.05 crude fat in feeds, cereal grains, and forages. In: Latimer G (ed) Official methods of analysis of AOAC International, 19th edn. AOAC International, GaithersburgGoogle Scholar
  8. AOAC International (2012c) Official method 992.23 crude protein in cereal grains and oilseeds: generic combustion method. In: Latimer G (ed) Official methods of analysis of AOAC International, 19th edn. AOAC International, GaithersburgGoogle Scholar
  9. AOAC International (2012d) Official method 992.15 crude protein in meat and meat products including pet foods. In: Latimer G (ed) Official methods of analysis of AOAC International, 19th edn. AOAC International, GaithersburgGoogle Scholar
  10. AOAC International (2012e) Official method 930.15 loss on drying (moisture) for feeds (at 135 for 2 hours), dry matter on oven drying for feeds (at 135 for 2 hours). In: Latimer G (ed) Official methods of analysis of AOAC International, 19th edn. AOAC International, GaithersburgGoogle Scholar
  11. AOAC International (2012f) Official method 990.03 protein (crude) in animal feed: combustion method. In: Latimer G (ed) Official methods of analysis of AOAC International, 19th edn. AOAC International, GaithersburgGoogle Scholar
  12. Ausman LM, Hegsted DM (1980) Protein requirements of adult cebus monkeys (Cebus albifrons). Am J Clin Nutr 33(12):2551–2558PubMedCrossRefGoogle Scholar
  13. Bell RHV (1971) A grazing ecosystem in the Serengeti. Sci Am 225:86–93CrossRefGoogle Scholar
  14. Bentley GR (1999) Aping our ancestors: comparative aspects of reproductive ecology. Evol Anthr 7(5):175–185CrossRefGoogle Scholar
  15. Bergstrom ML, Fedigan LM (2010) Dominance among female white-faced capuchin monkeys (Cebus capucinus): hierarchical linearity, nepotism, strength and stability. Behaviour 147(7):899–931CrossRefGoogle Scholar
  16. Bergstrom ML (2015) Seasonal effects on the nutrition and energetic condition of female white-faced capuchin monkeys. Dissertation, University of CalgaryGoogle Scholar
  17. Bronson FH (1985) Mammalian reproduction: an ecological perspective. Biol Reprod 32(1):1–26PubMedCrossRefGoogle Scholar
  18. 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 91:93–109CrossRefGoogle Scholar
  19. Campos, FA (2018, this volume) A synthesis of long-term environmental change in Santa Rosa, Costa Rica. In: Kalbitzer U, Jack KM (eds) Primate life histories, sex roles, and adaptability - Essays in honour of Linda M. Fedigan. Developments in primatology: progress and prospects. Springer, New York, pp 331–354Google Scholar
  20. Carnegie SD, Fedigan LM, Melin AD (2011a) Reproductive seasonality in female capuchins (Cebus capucinus) in Santa Rosa (Area de Conservación Guanacaste), Costa Rica. Int J Primatol 32(5):1076–1090CrossRefGoogle Scholar
  21. Carnegie SD, Fedigan LM, Ziegler TE (2011b) Social and environmental factors affecting fecal glucocorticoids in wild, female white-faced capuchins (Cebus capucinus). Am J Primatol 73(9):861–869PubMedPubMedCentralCrossRefGoogle Scholar
  22. CEM Corportation (2014) Method notes: digestion of alfalfa. http://cem.com/en/digestion-of-alfalfa-80ml-quartz. Accessed 31 Jan 2017
  23. CEM Corportation (2016) Methods notes: digestion of feed grain. http://cem.com/en/digestion-of-feed-grain. Accessed 31 Jan 2016
  24. Chapman CA, Fedigan LM (1990) Dietary differences between neighboring Cebus capucinus groups: local traditions, food availability or responses to food profitability? Folia Primatol 54:177–186PubMedCrossRefGoogle Scholar
  25. Chapman CA, Chapman LJ, Rode KD, Hauck EM, McDowell LR (2003) Variation in the nutritional value of primate foods: among trees, time periods, and areas. Int J Primatol 24(2):317–333CrossRefGoogle Scholar
  26. Chivers DJ, Hladik CM (1980) Morphology of the gastrointestinal tract in primates: comparisons with other mammals in relation to diet. J Morphol 166:337–386PubMedCrossRefGoogle Scholar
  27. Clutton-Brock TH, Harvey PH (1977) Species differences in feeding and ranging behavior in primates. In: Clutton-Brock TH (ed) Primate ecology. Academic Press, London, pp 557–584Google Scholar
  28. Clutton-Brock TH, Guinness FE, Albon SD (1982) Red deer: behavior and ecology of two sexes. Edinburgh University Press, EdinburghGoogle Scholar
  29. Conklin-Brittain NL, Knott CD, Wrangham RW (2006) Energy intake by wild chimpanzees and orangutans: methodological considerations and a preliminary comparison. In: Hohmann G, Robbins MM, Boesch C (eds) Feeding ecology in apes and other primates. Cambridge University Press, Cambridge, pp 445–471Google Scholar
  30. Cummings JH, Jenkins DJ, Wiggins HS (1976) Measurement of the mean transit time of dietary residue through the human gut. Gut 17:210–218PubMedPubMedCentralCrossRefGoogle Scholar
  31. Fedigan LM, Rose LM (1995) Interbirth interval variation in three sympatric species of neotropical monkey. Am J Primatol 37(1):9–24CrossRefGoogle Scholar
  32. Felton AM, Felton A, Lindenmayer DB, Foley WJ (2009a) Nutritional goals of wild primates. Funct Ecol 23(1):70–78CrossRefGoogle Scholar
  33. Felton AM, Felton A, Raubenheimer D, Simpson SJ, Foley WJ, Wood JT, Wallis IR, Lindenmayer DB (2009b) Protein content of diets dictates the daily energy intake of a free-ranging primate. Behav Ecol 20(4):685–690CrossRefGoogle Scholar
  34. Finke MD (2007) Estimate of chitin in raw whole insects. Zoo Biol 26(2):105–115PubMedCrossRefGoogle Scholar
  35. Ford SM, Davis LC (1992) Systematics and body size: implications for feeding adaptations in New World monkeys. Am J Phys Anthropol 88(4):415–468PubMedCrossRefGoogle Scholar
  36. Fragaszy DM (1990) Sex and age differences in the organization of behavior in wedge-capped capuchins, Cebus olivaceus. Behav Ecol 1(1):81–94CrossRefGoogle Scholar
  37. Fragaszy DM, Boinski S (1995) Patterns of individual diet choice and efficiency of foraging in wedge-capped capuchin monkeys (Cebus olivaceus). J Comp Psychol 109(4):339–348PubMedCrossRefGoogle Scholar
  38. Fragaszy D, Visalberghi E, Fedigan LM (2004) The complete capuchin: the biology of the genus Cebus. Cambridge University Press, CambridgeGoogle Scholar
  39. Hall MB, Hoover WH, Jennings JP, Miller Webster TK (1999) A method for partitioning neutral detergent-soluble carbohydrates. J Sci Food Agr 79:2079–2086CrossRefGoogle Scholar
  40. Harborne JB (1984) Phytochemical methods: a guide to modern techniques of plant analysis. Chapman and Hall, LondonCrossRefGoogle Scholar
  41. Hinde K, Milligan LA (2011) Primate milk: proximate mechanisms and ultimate perspectives. Evol Anthropol 20:9–23PubMedCrossRefGoogle Scholar
  42. Hladik CM (1977) A comparative study of the feeding strategies of two sympatric species of leaf monkeys: Presbytis senex and Presbytis entellus. In: Clutton-Brock TH (ed) Primate ecology: studies of feeding and ranging behavior in lemurs, monkeys and apes. Academic Press, London, pp 324–353Google Scholar
  43. Isbell LA (1991) Contest and scramble competition: patterns of aggression and ranging behavior among primates. Behav Ecol 2:143–155CrossRefGoogle Scholar
  44. Irwin MT, Raharison J, Raubenheimer DR, Chapman CA, Rothman J (2015) The nutritional geometry of resource scarcity: effects of lean seasons and habitat disturbance on nutrient intakes and balancing in wild sifakas. PLoS One 10(6):e0128046PubMedPubMedCentralCrossRefGoogle Scholar
  45. Izar P, Verderane MP, Peternelli-dos-Santos L, Mendonça-Furtado O, Presotto A, Tokuda M, Visalberghi E, Fragaszy D (2012) Flexible and conservative features of social systems in tufted capuchin monkeys: comparing the socioecology of Sapajus libidinosus and Sapajus nigritus. Am J Primatol 74(4):315–331PubMedCrossRefGoogle Scholar
  46. Janson CH (1985) Aggressive competition and individual food consumption in wild brown capuchin monkeys (Cebus apella). Behav Ecol Sociobiol 18:125–138CrossRefGoogle Scholar
  47. Janson CH (1988) Experimental evidence for spatial memory in wild brown capuchin monkeys (Cebus apella). Anim Behav 55:1229–1243CrossRefGoogle Scholar
  48. Johnson CA, Raubenheimer D, Rothman JM, Clarke D, Swedell L (2013) 30 days in the life: daily nutrient balancing in a wild chacma baboon. PLoS One 8(7):e70383PubMedPubMedCentralCrossRefGoogle Scholar
  49. Kay RF, Madden RH, Van Schaik C, Higdon D (1997) Primate species richness is determined by plant productivity: implications for conservation. P Natl Acad Sci USA 94(24):13023–13027CrossRefGoogle Scholar
  50. Key C, Ross C (1999) Sex differences in energy expenditure in non-human primates. P R Soc London B Bio 266(1437):2479–2485CrossRefGoogle Scholar
  51. Koenig A (2002) Competition for resources and its behavioral consequences among female primates. Int J Primatol 23:759–783CrossRefGoogle Scholar
  52. Lucas A (1998) Programming by early nutrition: an experimental approach. J Nutr 128(2):401S–406SPubMedCrossRefGoogle Scholar
  53. MacKinnon KC (2006) Food choice by juvenile capuchin monkeys (Cebus capucinus) in a tropical dry forest. In: Estrada A, Pavelka M, Garber P, Luecke L (eds) New perspectives in the study of Mesoamerican primates: distribution, ecology, behavior, and conservation. Springer Press, New York, pp 349–366CrossRefGoogle Scholar
  54. Matthews L (2009) Activity patterns, home range size, and intergroup encounters in Cebus albifrons support existing models of capuchin socioecology. Int J Primatol 30(5):709–728CrossRefGoogle Scholar
  55. McCabe GM (2005) Diet and nutrition in white-faced capuchins (Cebus capucinus): effects of group, sex and reproductive state. Thesis, University of CalgaryGoogle Scholar
  56. McCabe GM, Fedigan LM (2007) Effects of reproductive status on energy intake, ingestion rates, and dietary composition of female Cebus capucinus at Santa Rosa, Costa Rica. Int J Primatol 28:837–851CrossRefGoogle Scholar
  57. McCabe GM, Emery Thompson M (2013) Reproductive seasonality in wild Sanje mangabeys (Cercocebus sanjei), Tanzania: relationship between the capital breeding strategy and infant survival. Behaviour 150(12):1399–1429CrossRefGoogle Scholar
  58. McCabe G, Fernàndez D (2018, this volume) Patterns of infant mortality and seasonality in wild Sanje mangabeys, Cercocebus sanjei. In: Kalbitzer U, Jack KM (eds) Primate life histories, sex roles, and adaptability - Essays in honour of Linda M. Fedigan. Developments in primatology: progress and prospects. Springer, New York, pp 57–70Google Scholar
  59. Melin, AD, Webb SE, Williamson RE, Chiou K (2018) Data Collection in Field Primatology: A Renewed Look at Measuring Foraging Behaviour. In: Kalbitzer U, Jack KM (eds) Primate life histories, sex roles, and adaptability - Essays in honour of Linda M. Fedigan. Developments in primatology: progress and prospects. Springer, New York, pp 161–187Google Scholar
  60. Melin A, Fedigan L, Hiramatsu C, Hiwatashi T, Parr N, Kawamura S (2009) Fig foraging by dichromatic and trichromatic Cebus capucinus in a tropical dry forest. Int J Primatol 30(6):753–775CrossRefGoogle Scholar
  61. Melin AD, Fedigan LM, Young HC, Kawamura S (2010) Can color vision variation explain sex differences in invertebrate foraging by capuchin monkeys? Curr Zool 56(3):300–312Google Scholar
  62. Melin AD, Hiramatsu C, Parr NA, Matsushita Y, Kawamura S, Fedigan LM (2014a) The behavioral ecology of color vision: considering fruit conspicuity, detection distance, and dietary importance. Int J Primatol 35(1):258–287CrossRefGoogle Scholar
  63. Melin AD, Young HC, Mosdossy KN, Fedigan LM (2014b) Seasonality, extractive foraging and the evolution of primate sensorimotor intelligence. J Hum Evol 71(0):77–86PubMedCrossRefGoogle Scholar
  64. Melin Meachem AD (2011) Polymorphic colour vision and foraging in white-faced capuchins: insights from field research and simulations of monkey vision. Dissertation, University of CalgaryGoogle Scholar
  65. Merrill AL, Watt BK (1955) Derivation of current calorie factors. In: USDA ARS (ed) Agricultural handbook no. 74: energy value of foods, basis and derivation. U.S. Government Printing Office, Washington D.C., p 24–43. https://naldc.nal.usda.gov/download/CAT40000007/. Accessed 31 Jan 2017
  66. Miller KE, Bales KL, Ramos JH, Dietz JM (2006) Energy intake, energy expenditure, and reproductive costs of female wild golden lion tamarins (Leontopithecus rosalia). Am J Primatol 68(11):1037–1053PubMedCrossRefGoogle Scholar
  67. Milton K (1981) Food choice and digestive strategies of two sympatric primate species. The Am Nat 117(4):496–505CrossRefGoogle Scholar
  68. Milton K (1984) The role of food-processing factors in primate food choice. In: Rodman PS, Cant JGH (eds) Adaptations for foraging in nonhuman primates: contributions to an organismal biology of prosimians, monkeys and apes. Columbia University Press, New York, pp 249–279Google Scholar
  69. Milton K (1987) Primate diets and gut morphology: implications for hominid evolution. In: Harris M, Ross EB (eds) Food and evolution: toward a theory of food habits. Temple University Press, Philadelphia, pp 93–115Google Scholar
  70. 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 150:67–77CrossRefGoogle Scholar
  71. Mott GE, Jackson EM, McMahan CA, McGill HC Jr (1990) Cholesterol metabolism in adult baboons is influenced by infant diet. J Nutr 120(3):243–225PubMedCrossRefGoogle Scholar
  72. Mott GE, Lewis DS, McGill HC Jr (1991) Programming of cholesterol metabolism by breast or formula feeding. Ciba Found Symp 156:56–76PubMedGoogle Scholar
  73. Moura ACdA (2004) The capuchin monkey and the Caatinga dry forest: a hard life in a harsh habitat. Dissertation, University of CambridgeGoogle Scholar
  74. National Research Council (2003) Nutrient requirements of nonhuman primates. National Academy Press, Washington, DCGoogle Scholar
  75. Norconk MA, Wright BW, Conklin-Brittain NL, Vinyard CJ (2009) Mechanical and nutritional properties of food as factors in platyrrhine dietary adaptations. In: Garber PA, Estrada A, Bicca-Marques JC, Heymann EW, Strier KB (eds) South American primates: comparative perspectives in the study of behavior, ecology, and conservation. Springer Science+Business Media, LLC, New York, pp 279–319CrossRefGoogle Scholar
  76. O’Malley R, Fedigan L (2005) Variability in food-processing behaviour among white-faced capuchins (Cebus capucinus) in Santa Rosa National Park, Costa Rica. Am J Phys Anthropol 128:63–73PubMedCrossRefGoogle Scholar
  77. Oftedal OT, Whiten A, Southgate DAT, Van Soest P (1991) The nutritional consequences of foraging in primates: the relationship of nutrient intakes to nutrient requirements. Philos T R Soc B 334(1270):161–170CrossRefGoogle Scholar
  78. Perry S (1996) Female-female social relationships in wild white-faced capuchin monkeys, Cebus capucinus. Am J Primatol 40(2):167–182CrossRefGoogle Scholar
  79. Peters RH, Cloutier S, Dubé D, Evans A, Hastings P, Kaiser H, Kohn D, Sarwer-Foner B (1988) The allometry of the weight of fruit trees and shrubs in Barbados. Oecologia 74(4):612–616PubMedCrossRefGoogle Scholar
  80. Raubenheimer D (2011) Toward a quantitative nutritional ecology: the right-angled mixture triangle. Ecol Monogr 81(3):407–427CrossRefGoogle Scholar
  81. Raubenheimer D, Simpson SJ (1993) The geometry of compensatory feeding in the locust. Anim Behav 45:953–964CrossRefGoogle Scholar
  82. Raubenheimer D, Rothman JM, Pontzer H, Simpson SJ (2014) Macronutrient contributions of insects to the diets of hunter–gatherers: a geometric analysis. J Hum Evol 71(0):70–76PubMedCrossRefGoogle Scholar
  83. Rose LM (1994) Sex differences in diet and foraging behavior in white-faced capuchins (Cebus capucinus). Int J Primatol 15(1):95–114CrossRefGoogle Scholar
  84. Rothman JM, Raubenheimer D, Chapman CA (2011) Nutritional geometry: gorillas prioritize non-protein energy while consuming surplus protein. Biol Lett 7:847–849PubMedPubMedCentralCrossRefGoogle Scholar
  85. Rothman JM, Raubenheimer D, Bryer MAH, Takahashi M, Gilbert CC (2014) Nutritional contributions of insects to primate diets: implications for primate evolution. J Hum Evol 71:59–69PubMedCrossRefGoogle Scholar
  86. Schulke O, Chalise MK, Koenig A (2006) The importance of ingestion rates for estimating food quality and energy intake. Am J Phys Anthropol 68:951–965Google Scholar
  87. Simpson SJ, Raubenheimer D (1993) A multi-level analysis of feeding behaviour: the geometry of nutritional decisions. Philos T R Soc B 342(1302):381–402CrossRefGoogle Scholar
  88. Smith RJ, Jungers WL (1997) Body mass in comparative primatology. J Hum Evol 32(6):523–559PubMedCrossRefGoogle Scholar
  89. Sterck EHM, Watts DP, van Schaik CP (1997) The evolution of female social relationships in non-human primates. Behav Ecol Sociobiol 41:291–309CrossRefGoogle Scholar
  90. Tardif SD, Jaquish CE (1997) Number of ovulations in the marmoset monkey (Callithrix jacchus): relation to body weight, age and repeatability. Am J Primatol 42(4):323–329PubMedCrossRefGoogle Scholar
  91. Terborgh J (1983) Five New World primates. Princeton University Press, PrincetonGoogle Scholar
  92. United States Department of Agriculture (2014) The PLANTS Database. http://plants.usda.gov. Accessed 7 Jul 2014
  93. van Schaik CP, van Noordwijk MA (1989) The special role of male cebus monkeys in predation avoidance and its effect on group composition. Behav Ecol Sociobiol 24(5):265–276CrossRefGoogle Scholar
  94. 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(1):353–377CrossRefGoogle Scholar
  95. Van Soest PJ, Robertson JB, Lewis BA (1991) Methods for dietary fiber, neutral deterent fiber, and nonstarch polysaccharides in relation to animal nutrition. J Dairy Sci 74(10):3583–3597PubMedCrossRefGoogle Scholar
  96. Vogel ER (2004) The ecological basis of aggression in white-faced capuchin monkeys, Cebus capucinus, in a Costa Rican dry forest. Dissertation, Stony Brook UniversityGoogle Scholar
  97. Vogel ER (2005) Rank differences in energy intake rates in white-faced capuchin monkeys, Cebus capucinus: the effects of contest competition. Behav Ecol Sociobiol 58:333–344CrossRefGoogle Scholar
  98. Vogel ER, Janson CH (2006) Predicting the frequency of food related agonism in white-faced capuchin monkeys (Cebus capucinus), using a novel focal tree method. Am J Primatol 69(5):533–550CrossRefGoogle Scholar
  99. Voland E (1998) Evolutionary ecology of human reproduction. Annu Rev Anthropol 27:347–374PubMedCrossRefGoogle Scholar
  100. Wrangham RW (1980) An ecological model of female-bonded primate groups. Behaviour 75:262–300CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2018

Authors and Affiliations

  • Mackenzie L. Bergstrom
    • 1
  • Amanda D. Melin
    • 1
    • 2
    • 3
  • Monica S. Myers
    • 1
  • Linda M. Fedigan
    • 1
  1. 1.Department of Anthropology and ArchaeologyUniversity of CalgaryCalgaryCanada
  2. 2.Department of Medical GeneticsUniversity of CalgaryCalgaryCanada
  3. 3.Alberta Children’s Hospital Research Institute, University of CalgaryCalgaryCanada

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