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Wild capuchin monkeys anticipate the amount of ripe fruit in natural trees

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Abstract

Tropical forests have a high diversity of tree species which have very low densities and vary across time in their seasons of peak fruiting and maturation rates. As evidence of the ability of primates to track or anticipate changes in fruit production at individual trees, researchers have used the increased speed of primate groups toward more rewarding food patches. We analyzed the speed of approach to natural trees of wild capuchin monkeys under the effect of scramble competition, after excluding any plausible visual, olfactory and auditory cues. We conducted all-day group follows of three habituated capuchin groups at Iguazú National Park, Argentina, collecting data on ranging behavior and patterns of visits to fruit trees in relation with their location and fruit availability. Travel speed varied according to the expected reward at a feeding tree, increasing as rewards increased from low values, but decreasing again at very high values. Also, travel speed varied with time of day, decreasing from the time of first activity as the monkeys became less hungry, and increasing again toward late afternoon. Measures of unripe fruit cover did not explain variation in travel speed at any distance from a focal tree. Our data imply that, after excluding sensory cues, capuchins appear to anticipate time-varying ripe fruit quantity of natural resources, suggesting that they use memory of tree location and anticipation of fruit maturation. We also confirm that speed is a good measure about expectations of resources, as has been shown in previous studies.

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References

  • Anzelc A (2009) The foraging and travel patterns of white-faced sakis in Brownsberg Nature Park, Suriname: preliminary evidence for goal-directed foraging behavior. Master of Arts Thesis, Kent State University, pp 194. Unpublished

  • Ban SD, Boesch C, Janmaat KRL (2014) Taï chimpanzees anticipate revisiting high-valued fruit trees from further distances. Anim Cognit 17(6):1353–1364

    Article  Google Scholar 

  • Barr DJ, Levy R, Scheepers C, Tily HJ (2013) Random effects structure for confirmatory hypothesis testing: keep it maximal. J Mem Lang 68:255–278

    Article  Google Scholar 

  • Bates D, Maechler M, Bolker B, Walker S, Christensen RH B, Singmann H, Dai B, Grothendieck G (2015) lme4: linear mixed-effects models using ‘Eigen’ and S4. https://cran.r-project.org/web/packages/lme4/index.html

  • Bicca-Marques JC, Garber PA (2004) Use of spatial, visual, and olfactory information during foraging in wild nocturnal and diurnal anthropoids: a field experiment comparing Aotus, Callicebus, and Saguinus. Am J Primatol 62:171–187

    Article  PubMed  Google Scholar 

  • Bolen RM, Green SM (1997) Use of olfactory cues in foraging by owl monkeys (Aotus nancymai) and capuchin monkeys (Cebus apella). J Comp Psychol 111(2):152–158

    Article  CAS  PubMed  Google Scholar 

  • Brown AD, Zunino GE (1990) Dietary variability in Cebus apella in extreme habitats: evidence of adaptability. Folia Primatol 54:187–195

    Article  CAS  PubMed  Google Scholar 

  • Chapman CA, Fedigan LM (1990) Dietary differences between neighboring groups Cebus capucinus groups: local traditions, food availability or responses to food profitability? Folia Primatol 54:177–186

    Article  CAS  PubMed  Google Scholar 

  • 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. Am J Primatol 24:317–333

    Google Scholar 

  • Cunningham E, Janson CH (2007) Integrating information about location and value of resources in white-faced saki monkeys (Phitecia phitecia). Anim Cognit 10:293–304

    Article  Google Scholar 

  • De Oliveira Oyama S, de Souza LA (2011) Morphology and anatomy of the developing fruit of Maclura tinctoria, Moraceae. Rev Bras Bot 34(2):187–195

    Article  Google Scholar 

  • Di Bitetti MS (1997) Evidence for an important social role of allogrooming in a platyrrhine primate. Anim Behav 54(1):199–211

    Article  Google Scholar 

  • Di Bitetti MS (2001) Home-range use by the tufted capuchin monkey (Cebus apella nigritus) in a subtropical rainforest of Argentina. J Zool 253:33–45

    Article  Google Scholar 

  • Di Bitetti MS, Janson CH (2001) Social foraging and the finder’s share in capuchin monkeys, Cebus apella. Anim Behav 62:47–56

    Article  Google Scholar 

  • Felton AM, Felton A, Lindenmayer DB, Foley WJ (2009) Nutritional ecology: nutritional goals of wild primates. Funct Ecol 23:70–78

    Article  Google Scholar 

  • Gallistel CR, Gibbon J (2000) Time, rate and conditioning. Psychol Rev 107(2):289–344

    Article  CAS  PubMed  Google Scholar 

  • Garber PA (1989) Role of spatial memory in primate foraging patterns: Saguinus mystax and Saguinus fuscicollis. Am J Primatol 19:203–216

    Article  Google Scholar 

  • Garber PA, Dolins FL (1996) Testing learning paradigms in the field: evidence for use of spatial and perceptual information and rule-based foraging in wild moustached tamarins. In: Norconk MA, Rosenberger AL, Garber PA (eds) Adaptive radiations of Neotropical primates. Plenum Press, New York, pp 201–216

    Chapter  Google Scholar 

  • Garber P, Pacuilli LM (1997) Experimental field study of spatial memory and learning in wild capuchin monkeys (Cebus capuchinus). Folia Primatol 68:236–253

    Article  CAS  PubMed  Google Scholar 

  • Gendron RP, Staddon JER (1983) Searching for cryptic prey: the effect of search rate. Am Nat 121:172–186

    Article  Google Scholar 

  • Gibeault S, MacDonald SE (2000) Spatial memory and foraging competition in captive western lowland gorillas (Gorilla gorilla gorilla). Primates 41(2):147–160

    Article  Google Scholar 

  • Hirsch BT, Tujague MP, Di Blanco YE, Di Bitetti MS, Janson CH (2013) Comparing capuchins and coatis: causes and consequences of differing movement ecology in two sympatric mammals. Anim Behav 86:331–338

    Article  Google Scholar 

  • Houle A, Chapman CA, Vickery WL (2007) Intratree variation in fruit production and implications for primate foraging. Int J Primatol 28:1197–1217

    Article  Google Scholar 

  • Janmaat KRL, Byrne RW, Zuberbühler K (2006) Evidence for a spatial memory of fruiting states of rainforest trees in wild mangabeys. Anim Behav 72:797–807

    Article  Google Scholar 

  • Janmaat KRL, Chapman CA, Meijer R, Zuberbühler K (2012) The use of fruiting synchrony by foraging mangabey monkeys: a ‘simple tool’ to find fruit. Anim Cognit 15:83–96

    Article  CAS  Google Scholar 

  • Janmaat KRL, Polanskya L, Ban SD, Boesch C (2014) Wild chimpanzees plan their breakfast time, type, and location. Proc Natl Acad Sci USA 111(46):16343–16348

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Janson CH (1985) Aggressive competition and individual food consumption in wild brown capuchin monkeys (Cebus apella). Behav Ecol Sociobiol 18:125–138

    Article  Google Scholar 

  • Janson CH (1988) Food competition in brown capuchin monkeys (Cebus apella): quantitative effects of group size and tree productivity. Behaviour 105:53–76

    Article  Google Scholar 

  • Janson CH (1990) Social correlates of individual spatial choice in foraging groups of brown capuchin monkeys, Cebus apella. Anim Behav 40:910–921

    Article  Google Scholar 

  • Janson CH (1998) Experimental evidence for spatial memory in foraging wild capuchin monkeys, Cebus apella. Anim Behav 55:1229–1243

    Article  CAS  PubMed  Google Scholar 

  • Janson CH (2000) Spatial movement strategies: theory, evidences and challenges. In: Boinski S, Garber PA (eds) On the move: how and why animals travel in groups. University of Chicago Press, Chicago, pp 165–203

    Google Scholar 

  • Janson CH (2007) Experimental evidence for route integration and strategic planning in wild capuchin monkeys. Anim Cognit 10(3):341–356

    Article  Google Scholar 

  • Janson CH (2016) Capuchins, space, time and memory: an experimental test of what-where-when memory in wild monkeys. Proc R Soc B. doi:10.1098/rspb.2016.1432

    PubMed  Google Scholar 

  • Janson CH, Byrne R (2007) What wild primates know about resources: opening up the black box. Anim Cognit 10:357–367

    Article  Google Scholar 

  • Janson CH, Di Bitetti MS (1997) Experimental analysis of food detection in capuchin monkeys: effects of distance, travel speed and resource size. Behav Ecol Sociobiol 41:17–24

    Article  Google Scholar 

  • Janson CH, Goldsmith ML (1995) Predicting group size in primates: foraging costs and predation risks. Behav Ecol 6(3):326–336

    Article  Google Scholar 

  • Janson CH, van Schaik CP (1988) Recognizing the many faces of primate food competition: methods. Behaviour 105:165–186

    Article  Google Scholar 

  • Janson CH, Vogel ER (2006) Hunger and aggression in capuchin monkeys. In: Hohmann G, Boesch C, Nebel C (eds) Feeding ecology in apes and other primates. Cambridge University Press, Cambridge, pp 285–312

    Google Scholar 

  • Janson CH, Baldovino MC, Di Bitetti MS (2012) The group life cycle and demography of brown capuchin monkeys (Cebus [apella] nigritus) in Iguazú National Park, Argentina. In: Kappeler P, Watts D (eds) Long-term field studies of primates. Springer-Verlag, Heidelberg, pp 185–214

    Chapter  Google Scholar 

  • Laska M, Freyer D (1997) Olfactory discrimination ability for aliphatic esters in Squirrel monkeys and humans. Chem Senses 22:457–465

    Article  CAS  PubMed  Google Scholar 

  • Laska M, Wieser A, Rivas Bautista RM, Hernandez Salazar LT (2004) Olfactory sensitivity for carboxylic acids in Spider monkeys and Pigtail macaques. Chem Senses 29:101–109

    Article  PubMed  Google Scholar 

  • Maarse H (1991) Volatile Compounds in foods and beverages. Marcel Dekker, New York

    Google Scholar 

  • MacDonald SE (1994) Gorillas’ (Gorilla gorilla gorilla) spatial memory in a foraging task. J Comp Psychol 108:107–113

    Article  CAS  PubMed  Google Scholar 

  • MacDonald SE, Agnes MM (1999) Orangutan (Pongo pygmaeus abelii) spatial memory and behavior in a foraging task. J Comp Psychol 113:213–217

    Article  Google Scholar 

  • MacDonald SE, Wilkie DM (1990) Yellow-nosed monkey’s (Cercopithecus ascanius whitesidei) spatial memory in a simulated foraging environment. J Comp Psychol 104:382–387

    Article  Google Scholar 

  • MacDonald SE, Pang JC, Gibeault S (1994) Marmoset (Callithrix jacchus jacchus) spatial memory in a foraging task: win-stay versus win-shift strategies. J Comp Psychol 108:328–334

    Article  CAS  PubMed  Google Scholar 

  • Menzel EW (1973) Chimpanzee spatial memory organization. Science 182(4115):943–945

    Article  CAS  PubMed  Google Scholar 

  • Menzel CR (1991) Cognitive aspects of foraging in Japanese monkeys. Anim Behav 41:397–402

    Article  Google Scholar 

  • Milton K (1981) Distribution patterns of tropical plant foods as an evolutionary stimulus to primate mental development. Am Anthropol New Ser 83:534–548

    Article  Google Scholar 

  • Milton K (2000) Quo vadis? Tactics of food search and group movement in primates and other animals. In: Boinski S, Garber PA (eds) On the move: How and why animals travel in groups. University of Chicago Press, Chicago, pp 375–417

    Google Scholar 

  • Noser R, Byrne RW (2007) Travel routes and planning of visits to out-of-sight resources in wild chacma baboons, Papio urcinus. Anim Behav 73:257–266

    Article  Google Scholar 

  • Noser R, Byrne RW (2010) How do wild baboons (Papio ursinus) plan the routes? Travel among multiple high-quality food sources with inter-group competition. Anim Cognit 13:145–155

    Article  Google Scholar 

  • Placci LG, Arditi SI, Ciotek LE (1994) Productividad de hojas, flores y frutos en el Parque Nacional Iguazú. Yvyrareta 5:49–56

    Google Scholar 

  • Platt ML, Brannon EM, Briese TL, French JA (1996) Differences in feeding ecology predict differences in performance between golden lion tamarins (Leontopithecus rosalia) and Wied’s marmosets (Callithrix kuhli) on spatial and visual memory tasks. Anim Learn Behav 24(4):384–393

    Article  Google Scholar 

  • Pochron ST (2001) Can concurrent speed and directness of travel indicate purposeful encounter in the yellow baboons (Papio hamadryas cynocephalus) of Ruaha National Park, Tanzania? Int J Primatol 22(5):773–785

    Article  Google Scholar 

  • R Development Core Team (2011) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  • Roberts WA, Mitchell S, Phelps MT (1993) Foraging in laboratory trees: spatial memory in squirrel monkeys. In: Zendall TR (ed) Animal cognition: A tribute to Donald A. Riley. Lawrence Erlbaum, Hillsdale, pp 131–151

    Google Scholar 

  • Scheumann M, Call J (2006) Sumatran orangutans and a yellow-cheeked crested gibbon know what is where. Int J Primatol 27(2):575–602

    Article  Google Scholar 

  • Sigg J, Stolba J (1981) Home range and daily March in a hamadryas baboon troop. Folia Primatol 36:40–75

    Article  CAS  PubMed  Google Scholar 

  • Stephens DW, Krebs JR (1983) Foraging theory. Princeton University Press, Princeton

    Google Scholar 

  • Suarez SA (2014) Ecological factors predictive of wild Spider monkey (Ateles belzebuth) foraging decisions in Yasuní, Ecuador. Am J Primatol 76:1185–1195

    Article  PubMed  Google Scholar 

  • Tujague MP (2013) Comportamiento espacial y memoria en el mono caí (Cebus apella) en contexto de grupo: semejanzas entre primates no humanos y humanos. Ph.D. dissertation, University of La Plata, Argentina, p 201. Unpublished

  • Tujague MP, Janson CH (in press). Foraging cognition in Neotropical primates: integrating studies from wild and captivity. In Kowalewski M, Oklander L (eds) Primatology in Argentina I. Editorial SAREM, Buenos Aires

  • Tujague MP, Bacigalupe MA, Lahitte HB, Janson CH (2016) Memoria espacial en monos capuchinos de Argentina: un estudio observacional en vida silvestre. Revista Argentina de Antropología Biológica 18(1):1–13

    Article  Google Scholar 

  • 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 24:265–276

    Article  Google Scholar 

  • Vogel ER (2005) Rank differences in energy intake rates in white-faced capuchin monkeys, Cebus capucinus: the effects of contest competition. Behav Ecol Sociobiol 58:333–344

    Article  Google Scholar 

  • Vogel ER, Janson CH (2007) Predicting the frequency of food-related agonism in white-faced capuchin monkeys (Cebus capucinus), using a novel focal-tree method. Am J Primatol 69:1–18

    Article  Google Scholar 

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Acknowledgements

We wish to thank Administración de Parques Nacionales and Centro de Investigaciones Ecológicas Subtropicales for granting permission to conduct this study. This work would not have been possible without field assistance from Alex Alcocer Aldunate, Ana Alvarez, María Celia Baldovino, María Verónica Cifre, Lara Coleselli, Emanuel Galetto, Juan Garibaldi, Luis Molina, Natalia Gomez de Oliveira, Elizabeth Gonzáles Valentín, Rocío Fernández Quintero, Daniel Lambruschi, Ricardo Melzew, Juan Pablo Peretti, Noelia Rivas, Taylor Rubin, Clara Scarry and Fermino Silva

Funding

This study was funded by a dissertation fellowship from the Argentine Research Council (CONICET) to M.P.T., as well as grants from Idea Wild and the American Society of Mammalogists (no grant numbers available).

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Authors and Affiliations

  1. Instituto de Biología Subtropical (IBS), Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Universidad Nacional de Misiones (UNaM), Bertoni 85, CP3370, Puerto Iguazú, Misiones, Argentina

    María Paula Tujague

  2. Asociación Civil Centro de Investigaciones del Bosque Atlántico (CeIBA), Puerto Iguazú, Argentina

    María Paula Tujague

  3. Division of Biological Sciences, The University of Montana, Missoula, USA

    Charles H. Janson

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  1. María Paula Tujague
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  2. Charles H. Janson
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Correspondence to María Paula Tujague.

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All applicable international, national and/or institutional guidelines for the care and use of animals were followed. All research reported in this manuscript adhered to the International Primatological Society and the American Society of Primatologists Principles for the Ethical treatment of Non-human Primates, and complied with the protocols approved by the Animal Care and Use Committee and the Argentine Research Council (CONICET). It also adhered to the legal requirements of Argentina.

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Tujague, M.P., Janson, C.H. Wild capuchin monkeys anticipate the amount of ripe fruit in natural trees. Anim Cogn 20, 841–853 (2017). https://doi.org/10.1007/s10071-017-1105-7

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