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Taï chimpanzees anticipate revisiting high-valued fruit trees from further distances

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Abstract

The use of spatio-temporal memory has been argued to increase food-finding efficiency in rainforest primates. However, the exact content of this memory is poorly known to date. This study investigated what specific information from previous feeding visits chimpanzees (Pan troglodytes verus), in Taï National Park, Côte d’Ivoire, take into account when they revisit the same feeding trees. By following five adult females for many consecutive days, we tested from what distance the females directed their travels towards previously visited feeding trees and how previous feeding experiences and fruit tree properties influenced this distance. To exclude the influence of sensory cues, the females’ approach distance was measured from their last significant change in travel direction until the moment they entered the tree’s maximum detection field. We found that chimpanzees travelled longer distances to trees at which they had previously made food grunts and had rejected fewer fruits compared to other trees. In addition, the results suggest that the chimpanzees were able to anticipate the amount of fruit that they would find in the trees. Overall, our findings are consistent with the hypothesis that chimpanzees act upon a retrieved memory of their last feeding experiences long before they revisit feeding trees, which would indicate a daily use of long-term prospective memory. Further, the results are consistent with the possibility that positive emotional experiences help to trigger prospective memory retrieval in forest areas that are further away and have fewer cues associated with revisited feeding trees.

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References

  • Baayen R (2008) Analyzing linguistic data. Cambridge University Press, Cambridge

    Book  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 (2012) lme4: linear mixed-effects models using S4 classes. R package version 0.999999-0

  • Boesch C (2008) Why do chimpanzees die in the forest? The challenges of understanding and controlling for wild ape health. Am J Primatol 70:722–726

    Article  PubMed  Google Scholar 

  • Boesch C, Boesch-Achermann H (2000) The Chimpanzees of the Taï Forest: behavioural ecology and evolution. Oxford University Press, Oxford

    Google Scholar 

  • Boesch C, Crockford C, Herbinger I, Wittig R, Moebius Y, Normand E (2008) Intergroup conflicts among chimpanzees in Taï National Park: lethal violence and the female perspective. Am J Primatol 70:519–532

    Article  PubMed  Google Scholar 

  • Byrne RW, Noser R, Bates LA, Jupp PE (2009) How did they get here from there? Detecting changes of direction in terrestrial ranging. Anim Behav 77:619–631

    Article  Google Scholar 

  • Carlson BA, Rothman JM, Mitani JC (2013) Diurnal variation in nutrients and chimpanzee foraging behavior. Am J Primatol 75:342–349

    Article  PubMed  Google Scholar 

  • Cavonius CR, Robbins DO (1973) Relationships between luminance and visual acuity in the rhesus monkey. J Psychol 232:239–246

    CAS  Google Scholar 

  • Chapman CA, Chapman LJ, Wrangham RW, Hunt K, Gebo D, Gardner L (1992) Estimators of fruit abundance of tropical trees. Biotropica 24:527–531

    Article  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

    Article  Google Scholar 

  • Cook RG, Brown MF, Riley DA (1985) Flexible memory processing by rats: use of prospective and retrospective information in the radial maze. J Exp Psychol Anim Behav Process 11:453–469

    Article  PubMed  CAS  Google Scholar 

  • Crystal JD (2013) Prospective memory. Curr Biol 23:750–751

    Article  Google Scholar 

  • Cunningham E, Janson C (2007) Integrating information about location and value of resources by white-faced saki monkeys (Pithecia pithecia). Anim Cogn 10:293–304

    Article  PubMed  Google Scholar 

  • Dobson A (2002) An introduction to generalized linear models. Chapman, Hall/CRC, Boca Raton

    Google Scholar 

  • Emlen JM (1966) The role of time and energy in food preference. Am Soc Nat 100:611–617

    Article  Google Scholar 

  • Fagan WF, Lewis MA, Auger-Méthé M et al (2013) Spatial memory and animal movement. Ecol Lett 16:1316–1329

    Article  PubMed  Google Scholar 

  • Fedurek P, Slocombe KE (2013) The social function of food-associated calls in male chimpanzees. Am J Primatol 75:726–739

    Article  PubMed  Google Scholar 

  • Field A (2005) Discovering statistics using spss. Sage, London

    Google Scholar 

  • Forstmeier W, Schielzeth H (2011) Cryptic multiple hypotheses testing in linear models: overestimated effect sizes and the winner’s curse. Behav Ecol Sociobiol 65:47–55

    Article  PubMed  PubMed Central  Google Scholar 

  • Fox J, Weisberg S (2011) An R companion to applied regression, 2nd edn. Sage, Thousand Oaks

    Google Scholar 

  • Garber PA (1988) Foraging decisions during nectar feeding by tamarin monkeys (Saguinus mystax and Saguinus fuscicollis, callitrichidae, primates) in Amazonian Peru. Biotropica 20:100–106

    Article  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 

  • Gill FB (1988) Trapline foraging by hermit hummingbirds: competition for an undefended, renewable resource. Ecology 69:1933–1942

    Article  Google Scholar 

  • Glander K (1978) Howling monkey feeding behavior and plant secondary compounds: a study of strategies. In: Montgomery G (ed) The ecology of arboreal folivores. The symposia of the National Zoological Park, Smithsonian Institution, Washington, pp 561–574

    Google Scholar 

  • Golla H, Ignashchenkova A, Haarmeier T, Thier P (2004) Improvement of visual acuity by spatial cueing: a comparative study in human and non-human primates. Vision Res 44:1589–1600

    Article  PubMed  Google Scholar 

  • Goné Bi ZB (2007) Régime alimentaire des chimpanzés, distribution spatiale et phénologie des plantes dont les fruits sont consommés par les chimpanzés du Parc National de Taï, en Côte d’Ivoire. PhD Dissertation, Université de Cocody, Abidjan, Côte d’Ivoire

  • Goodall J (1986) The chimpanzees of Gombe: patterns of behavior. Cambridge University Press, Harvard

    Google Scholar 

  • Guillaumet JL (1967) Recherches sur la végétation et la flore de la région du Bas-Cavally (Côte d’Ivoire). Mémoires ORSTOM, Paris, p 259

    Google Scholar 

  • Hamann SB, Ely TD, Grafton ST, Kilts CD (1999) Amygdala activity related to enhanced memory for pleasant and aversive stimuli. Nat Am 2:289–293

    CAS  Google Scholar 

  • Hauser DM (2000) The sound and the fury: primate vocalizations as reflections of emotion and thought. In: Nils L, Wallin BM, Steven B (eds) The origins of music. The MIT Press, Cambridge, pp 77–102

    Google Scholar 

  • Hauser DM, Wrangham RW (1987) Manipulation of food calls in captive chimpanzees. A preliminary report. Folia Primatol 48:207–210

    Article  PubMed  CAS  Google Scholar 

  • Hiramatsu C, Melin AD, Aureli F et al (2009) Interplay of olfaction and vision in fruit foraging of spider monkeys. Anim Behav 77:1421–1426

    Article  Google Scholar 

  • Hothorn T, Hornik K (2012) Exact distributions for rank and permutation tests. R package version 0.8-23

  • 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, Chancellor RL (2010) Exploring new areas: how important is long-term spatial memory for mangabey (Lophocebus albigena johnstonii) foraging efficiency? Int J Primatol 31:863–886

    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, Ban SD, Boesch C (2013a) Chimpanzees use long-term spatial memory to monitor large fruit trees and remember feeding experiences across seasons. Anim Behav 86:1183–1205

    Article  Google Scholar 

  • Janmaat KRL, Ban SD, Boesch C (2013b) Taï chimpanzees use botanical skills to discover fruit: what we can learn from their mistakes. Anim Cogn 6:851–860

    Article  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Janson CH, Chapman CA (1999) Resources and primate community structure. In: Fleagle JG, Janson C, Reed K (eds) Primate communities. Cambridge University Press, Cambridge, pp 237–267

    Chapter  Google Scholar 

  • Janson CH, DiBitetti 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 

  • Kane MJ, Engle RW (2000) Working-memory capacity, proactive interference, and divided attention: limits on long-term memory retrieval. J Exp Psychol Learn Mem Cogn 26:336–358

    Article  PubMed  CAS  Google Scholar 

  • Kano F, Tanaka M, Tomonaga M (2008) Enhanced recognition of emotional stimuli in the chimpanzee (Pan troglodytes). Anim Cogn 11:517–524

    Article  PubMed  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Laska M, Liesen A, Teubner P (1999) Enantioselectivity of odor perception in squirrel monkeys and humans. Am J Physiol 277:1098–1103

    Google Scholar 

  • Laska M, Seibt A, Weber A (2000) “Microsmatic” primates revisited: olfactory sensitivity in the squirrel monkey. Chem Senses 25:47–53

    Article  PubMed  CAS  Google Scholar 

  • Laska M, Teresa L, Salazar H, Luna ER (2003) Food preferences and nutrient composition in captive spider monkeys, Ateles geoffroyi. Physiol Behav 78:321–329

    Article  PubMed  CAS  Google Scholar 

  • Leighton M, Leighton DR (1982) The relationship of size of feeding aggregate to size of food patch: howler monkey (Alouatta palliata) feeding in Trichilia cipo fruit trees on Barro Colorado Island. Biotropica 14:81–90

    Article  Google Scholar 

  • Marler P, Tenaza R (1977) Signalling behavior of apes with special reference to vocalization. In: Sebeok TA (ed) How animals communicate. Indiana University Press, Bloomington, pp 965–1033

    Google Scholar 

  • Martin P, Bateson P (2007) Measuring behaviour. An introductory guide. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Martin-Ordas G, Haun D, Colmenares F, Call J (2010) Keeping track of time: evidence for episodic-like memory in great apes. Anim Cogn 13:331–340

    Article  PubMed  PubMed Central  Google Scholar 

  • McFarland Symington M (1988) Food competition and foraging party size in the black spider monkey (Ateles paniscus chamek). Behaviour 105:117–134

    Article  Google Scholar 

  • Merigan WH, Katz LM (1990) Spatial resolution across the macaque retina. Vis Res 30:985–991

    Article  PubMed  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Mulcahy NJ, Call J (2006) Apes save tools for future use. Science 312:1038–1040

    Article  PubMed  CAS  Google Scholar 

  • N’Goran PK, Boesch C, Mundry R, N’Goran EK, Herbinger I, Yapi FA, Kühl HS (2012) Hunting, law enforcement, and African primate conservation. Conserv Biol 26:565–571

    Article  PubMed  Google Scholar 

  • N’Guessan AK, Ortmann S, Boesch C (2009) Daily energy balance and protein gain among Pan troglodytes verus in the Taï National Park, Côte d’Ivoire. Int J Primatol 30:481–496

    Article  Google Scholar 

  • Normand E, Boesch C (2009) Sophisticated Euclidean maps in forest chimpanzees. Anim Behav 77:1195–1201

    Article  Google Scholar 

  • Normand E, Ban SD, Boesch C (2009) Forest chimpanzees (pan troglodytes verus) remember the location of numerous fruit trees. Anim Cogn 12:797–807

    Article  PubMed  PubMed Central  Google Scholar 

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

    Article  Google Scholar 

  • Parr LA (2001) Cognitive and physiological markers of emotional awareness in chimpanzees (Pan troglodytes). Anim Cogn 4:223–229

    Article  PubMed  CAS  Google Scholar 

  • Peres CA (1991) Ecology of mixed-species groups of tamarins in Amazonian Terra Firme Forests. PhD Dissertation, Cambridge University, Cambridge

  • Porter LM, Garber PA (2013) Foraging and spatial memory in wild weddell’s saddleback tamarins (Saguinus fuscicollis weddelli) when moving between distant and out-of-sight goals. Int J Primatol 34:30–48

    Article  Google Scholar 

  • Pyke GH, Pulliam HR, Charnov EL (1977) Optimal foraging: a selective review of theory and tests. Q Rev Biol 52:137–154

    Article  Google Scholar 

  • R Core Development Team (2013) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  • Rosati AG, Hare B (2012) Chimpanzees and bonobos exhibit divergent spatial memory development. Dev Sci 15:840–853

    Article  PubMed  Google Scholar 

  • Sayers K, Menzel CR (2012) Memory and foraging theory: chimpanzee utilization of optimality heuristics in the rank-order recovery of hidden foods. Anim Behav 84:795–803

    Article  PubMed  PubMed Central  Google Scholar 

  • Schel AM, Machanda Z, Townsend SW, Zuberbühler K, Slocombe KE (2013) Chimpanzee food calls are directed at specific individuals. Anim Behav 86:955–965

    Article  Google Scholar 

  • Schoener TW (1971) Theory of feeding strategies. Annu Rev Ecol Syst 2:369–404

    Article  Google Scholar 

  • Shettleworth SJ (2010) Cognition, evolution, and behavior. Oxford University Press, Oxford

    Google Scholar 

  • Slocombe EK, Zuberbühler K (2006) Food-associated calls in chimpanzees: responses to food types or food preferences? Anim Behav 72:989–999

    Article  Google Scholar 

  • Thorpe CM, Jacova C, Wilkie DM (2004) Some pitfalls in measuring memory in animals. Neurosci Biobehav Rev 28:711–718

    Article  PubMed  Google Scholar 

  • Van Schaik CP, Terborgh JW, Wright SJ (1993) The phenology of tropical forests: adaptive significance and consequences for primary consumers. Annu Rev Ecol Syst 24:353–377

    Article  Google Scholar 

  • Worman CO, Chapman CA (2005) Seasonal variation in the quality of a tropical ripe fruit and the response of three frugivores. J Trop Ecol 21:689–697

    Article  Google Scholar 

  • Wrangham RW, Conklin-brittain NL, Hunt KD (1998) Dietary response of chimpanzees and cercopithecines to seasonal variation in fruit abundance. I. Antifeedants. Int J Primatol 19:949–970

    Article  Google Scholar 

  • Zentall TR, Steirn JN, Jackson-Smith P (1990) Memory strategies in pigeons’ performance of a radial-arm-maze analog task. J Exp Psychol Anim Behav Process 16:358–371

    Article  Google Scholar 

  • Zuberbühler K, Janmaat KRL (2010) Foraging cognition in non-human primates. In: Platt ML, Ghazanfar AA (eds) Primate neuroethology. Oxford University Press, Oxford, pp 64–83

    Chapter  Google Scholar 

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Acknowledgments

We thank the Leakey Foundation (the Franklin Mosher Baldwin Memorial Fellowship), the Max Planck Institute for Evolutionary Anthropology (MPI), the Centre Suisse de Recherches Scientifiques (CSRS) and the Taï Chimpanzee Project (TCP) for providing funding for this study. We thank the Office Ivorien des Parcs et Réserves (OIPR), the Direction du Parc National de Taï and the Ministère de la Recherche Scientifique en Côte d’Ivoire and the Université Félix Houphouët Boigny for their permission to execute this research and logistical support. We thank C. Stephens and R. Mundry for statistical support and for writing programs in R to calculate the approach distances as well to determine the complete interval of revisits. We thank C. Stephens for proofreading. We are grateful to A. N’Guessan for sharing his data on the energy value of the chimpanzee foods. We are grateful also to J. Tahou, L.B. Bally, V. Gnagnon, R. Nabo and A. Siablo for assistance in field data collection. This study is based on non-invasive observations and complies with the laws of Côte d’Ivoire.

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Authors and Affiliations

  1. Max Planck Institute for Evolutionary Anthropology, Deutscher Platz 6, 04103, Leipzig, Germany

    Simone D. Ban, Christophe Boesch & Karline R. L. Janmaat

  2. Centre Suisse de Recherches Scientifiques, 01 BP 1303, Abidjan 01, Côte d’Ivoire

    Simone D. Ban

  3. UFR Biosciences, Université Félix Houphouët Boigny, 22 BP 1106, Abidjan 22, Côte d’Ivoire

    Simone D. Ban

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  1. Simone D. Ban
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Correspondence to Simone D. Ban.

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Ban, S.D., Boesch, C. & Janmaat, K.R.L. Taï chimpanzees anticipate revisiting high-valued fruit trees from further distances. Anim Cogn 17, 1353–1364 (2014). https://doi.org/10.1007/s10071-014-0771-y

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