Abstract
Both in captivity and the wild, primates are found to travel mostly to the nearest available resource, but they may skip over the closest resource and travel to more distant resources, which are often found to be more productive. This study examines the tradeoff between distance and reward in the foraging choices of one group of wild capuchin monkeys (Cebus apella nigritus) using feeding platforms in large-scale foraging experiments conducted over four years. Three feeding sites were arrayed in an oblique triangle, such that once the monkey group had chosen one site to feed, they had a choice between two remaining sites, a close one with less food and the other up to 2.3 times as far away but with more food. Sites were provisioned once per day. The capuchins generally chose the closer feeding site, even when the more distant site offered up to 12 times as much food. The distances to, rewards of, or various profitability measures applied to each alternative site individually did not explain the group’s choices in ways consistent with foraging theory or principles of operant psychology. The group’s site choices were predicted only by comparing efficiency measures of entire foraging pathways: (1) direct travel to the more rewarding distant site, versus (2) the longer ‘detour’ through the closer site on the way to the more distant one. The group chose the detour more often when the reward was larger and the added detour distance shorter. They appeared to be more sensitive to the absolute increase in detour distance than to the relative increase compared to the straight route. The qualitative and quantitative results agree with a simple rule: do not use the detour unless the energy gain from extra food outweighs the energy cost of extra travel. These results suggest that members of this group integrate information on spatial location, reward, and perhaps potential food competition in their choice of multi-site foraging routes, with important implications for social foraging.
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References
Anderson JD (1983) Optimal foraging and the traveling salesman. Theo Pop Biol 24:145–159
Baker RR (1978) The evolutionary ecology of animal migration. Hodder and Stoughton, London
Baum WM, Schwendiman JW, Bell KE (1999) Choice, contingency discrimination, and foraging theory. J Exp Anal Behav 71:355–373
Boesch C, Boesch H (1984) Mental map in wild chimpanzees: an analysis of hammer transports for nut cracking. Primates 25:160–170
Brown AD, Zunino GE (1990) Dietary variability in Cebus apella in extreme habitats: evidence for adaptability. Folia primatologica 54:187–195
Bugnyar T, Heinrich B (2005) Ravens, Corvus corax, differentiate between knowledgeable and ignorant competitors. Proc Roy Soc London B-Biol Sci 272:1641–1646
Christophides N (1985) Vehicle routing. In: Lawler EL, Lenstra JK, Rinnooy Kan AHG, Shmoys DB (eds) The traveling salesman problem. Wiley, Chichester, pp 431–448
Clayton NS, Dickinson A (1998) Episodic-like memory during cache recovery by scrub jays. Nature 395:272–274
Clayton NS, Griffiths DP, Emery NJ, Dickinson A (2001) Elements of episodic-like memory in animals. Philos Trans Roy Soc London B-Biol Sci 356:1483–1491
Clayton NS, Bussey TJ, Dickinson A (2003a) Can animals recall the past and plan for the future? Nat Rev Neurosci 4:685–691
Clayton NS, Bussey TJ, Emery NJ, Dickinson A (2003b) Prometheus to Proust: the case for behavioural criteria for ‘mental time travel’. Trends Cognit Sci 7:436–437
Couzin ID, Krause J, Franks NR, Levin SA (2005) Effective leadership and decision making in animal groups on the move. Nature 433:513–516
Cramer AE, Gallistel CR (1997) Vervet monkeys as travelling salesmen. Nature 387:464–464
Cunningham EP (2003) The use of memory in Pithecia pithecia’s foraging strategy. Ph.D dissertation, Anthropology, City University of New York. Available from: University Microfilms, Ann Arbor, 64–03:973
Cunningham EP, Janson CH (2007a) Integrating information about location and value of resources by white faced-saki monkeys (Pithecia pithecia). Anim Cogn doi:10.1007/s10071-007-0077-4
Cunningham E, Janson C (2007b) A socioecological perspective on primate cognition, past and present. Anim Cogn doi:10.1007/s10071-007-0078-3
DiBitetti MS (2001a) Food-associated calls in the tufted capuchin monkey (Cebus apella). Ph.D. Thesis, Department of Ecology and Evolution. Stony Brook University, Stony Brook, 258 p
DiBitetti MS, Janson CH (2001) The finder’s share in foraging groups of brown capuchin monkeys (Cebus apella). Anim Behav 62:47–56
DiBitetti MS, Vidal EML, Baldovino MC, Benesovsky V (2000) Sleeping site preferences in tufted capuchin monkeys (Cebus apella nigritus). Amer J Primatol 50:257–274
Ducoing AM, Thierry B (2003) Withholding information in semifree-ranging Tonkean macaques (Macaca tonkeana). J Comp Psych 117:67–75
Dumont B, Hill DRC (2004) Spatially explicit models of group foraging by herbivores: what can Agent-Based Models offer? Anim Res 53:419–428
Emery NJ, Clayton NS (2001) Effects of experience and social context on prospective caching strategies by scrub jays. Nature 414:443–446
Emery NJ, Dally JM, Clayton NS (2004) Western scrub-jays (Aphelocoma californica) use cognitive strategies to protect their caches from thieving conspecifics. Anim Cogn 7:37–43
Fantino E, Goldshmidt JN (2000) Differences, not ratios, control choice in an experimental analogue to foraging. Psychol Sci 11:229–233
Fragaszy D, Johnson-Pynn J, Hirsh E, Brakke K (2003) Strategic navigation of two-dimensional alley mazes: comparing capuchin monkeys and chimpanzees. Anim Cogn 6:149–160
Garber PA (1988) Foraging decisions during nectar-feeding by tamarin monkeys (Saguinus mystax and Saguinus fuscicollis). Biotropica 20:100–106
Garber PA (1989) Role of spatial memory in primate foraging patterns: Saguinus mystax and Saguinus fuscicollis. Amer J Primatol 19:203–216
Gebhardt SE, Thomas RG (2002) Nutritive value of foods. Home and garden bulletin. US Department of Agriculture, Agricultural Research Service: Washington, DC, v + 95
Golden BL, Stewart WR (1985) Empirical analysis of heuristics. In: Lawler EL, Lenstra JK, Rinooy Kan AHG, Shmoys DB (eds) The traveling salesman problem. Wiley, Chichester, pp 207–249
Grace RC (1999) The matching law and amount-dependent exponential discounting as accounts of self-control choice. J Exp Anal Behav 71:27–44
Grace RC, Savastano HI (2000) The relationship between value and temporal context is an empirical question: a reply to Fantino (2000). J Exp Psych-General 129:447–448
Green L, Myerson J, Holt DD, Slevin JR, Estle SJ (2004) Discounting of delayed food rewards in pigeons and rats: is there a magnitude effect? J Exp Anal Behav 81:39–50
Hall CL, Fedigan LM (1997) Spatial benefits afforded by high rank in white-faced capuchins. Anim Behav 53:1069–1082
Hare B, Call J, Agnetta B, Tomasello M (2000) Chimpanzees know what conspecifics do and do not see. Anim Behav 59:771–785
Hare B, Call J, Tomasello M (2001) Do chimpanzees know what conspecifics know? Anim Behav 61:139–151
Haynes KE, Fotheringham AS (1984) Gravity and spatial interaction models. Sage Publication, Newbury Park
Janson CH (1985) Aggressive competition and individual food intake in wild brown capuchin monkeys. Behav Ecol Sociobiol 18:125–138
Janson CH (1988) Food competition in brown capuchin monkeys (Cebus apella): quantitative effects of group size and tree productivity. Behaviour 105:53–76
Janson CH (1990) Social correlates of individual spatial choice in foraging brown capuchin monkeys (Cebus apella). Anim Behav 38:910–921
Janson CH (1996) Toward an experimental socioecology of primates: examples from Argentine brown capuchin monkeys (Cebus apella nigritus). In: Norconk MA, Rosenberger AL, Garber PA (eds) Adaptive radiations of neotropical primates. Plenum, New York, pp 309–325
Janson CH (1998) Experimental evidence for spatial memory in foraging wild capuchin monkeys, Cebus apella. Anim Behav 55:1229–1243
Janson CH (2000) Spatial movement strategies: theory, evidence, and challenges. In: Boinksi S, Gaber PA (eds) On the move: how and why animals travel in groups. Chicago University Press, Chicago, pp 165–203
Janson CH, Byrne RW (2007) What wild primates know about resources—opening up the black box. Anim Cogn doi:10.1007/s10071-007-0080-9
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
Johnson DS, Papadimitriou CH (1985) Computational complexity. In: Lawler EL, Lenstra JK, Rinnoy Kan AHG, Shmoys DB (eds) The traveling salesman problem. A guided tour of combinatorial optimization. Wiley, Chichester, pp 37–85
MacDonald SE, Wilkie DM (1990) Yellow-nosed monkeys’ (Cercopithecus ascanius whitesidei) spatial memory in a simulated foraging environment. J Comp Psych 104:382–387
Mazur JE (2000) Tradeoffs among delay, rate, and amount of reinforcement. Behav Process 49:1–10
Menzel EW Jr (1973) Chimpanzee spatial memory organization. Science 182:943–45
Menzel CR, Beck BB (2000) Homing and detour behavior in golden lion tamarin social groups. In: Boinski S, Garber PA (eds) On the move: how and why animals travel in groups. University of Chicago Press, Chicago, pp 299–326
Menzel EW Jr, Juno C (1985) Social foraging in marmoset monkeys and the question of intelligence. Philos Trans R Soc Lond B 308:145–158
Milton K (1981) Distribution patterns of tropical food plants as an evolutionary stimulus to primate mental development. Amer Anthropol 83:534–548
Mitchell RW, Anderson JR (1997) Pointing, withholding information, and deception in capuchin monkeys (Cebus apella). J Comp Psych 111:351–361
Noser R, Byrne RW (2007) Mental maps in chacma baboons (Papio ursinus) using intergroup encounters as a natural experiment. Anim Cogn doi:10.1007/s10071-007-0068-x
Placci LG, Arditi SI, Ciotek LE (1994) Productividad de hojas, flores y frutos en el Parque Nacional Iguazu. Yvyrareta 5:49–56
Poti P (2000) Aspects of spatial cognition in capuchins (Cebus apella): frames of reference and scale of space. Anim Cogn 3:69–77
Rachlin H, Raineri A, Cross D (1991) Subjective probability and delay. J Exp Anal of Behav 55:233–244
Savastano HI, Fantino E (1996) Differences in delay, not ratios, control choice in concurrent chains. J Exp Anal Behav 66:97–116
Schwagmeyer PL (1995) Searching today for tomorrow’s mates. Anim Behav 50:759–767
Shettleworth SJ (1998) Cognition, evolution, and behavior. Oxford University Press, New York
Sigg H, Stolba A (1981) Home range and daily march in a Hamadryas baboon troop. Folia primatol. 36:40–75
Stephens DW, Krebs JR (1987) Foraging theory. Princeton University Press, Princeton, NJ
Stephens DW, Lynch JF, Sorensen AE, Gordon C (1986) Preference and profitability: theory and experiment. Amer Natur 127:533–553
Steudel K (2000) The physiology and energetics of movement: effects on individuals and groups. In: Boinksi S, Garber PA (eds) On the move: how and why animals travel in groups. The University of Chicago Press, Chicago, pp 9–23
Stevens JR, Hallinan EV, Hauser MD (2005a) The ecology and evolution of patience in two New World monkeys. Biol Lett 1:223–226
Stevens JR, Rosati AG, Ross KR, Hauser MD (2005b) Will travel for food: Spatial discounting in two new world monkeys. Curr Biol 15:1855–1860
Tobin H, Logue AW (1994) Self-control across species (Columba livia, Homo sapiens, and Rattus norvegicus). J Comp Psych 108:126–133
Tobin H, Logue AW, Chelonis JJ, Ackerman KT (1996) Self-control in the monkey Macaca fascicularis. Anim Learn Behav 24:168–174
Acknowledgments
I am grateful for the expert assistance and collaboration of many, among them Dr. Lisa Rose, Dr. Mario Di Bitetti, Celia Baldovino, Ben Hirsch, Brandon Wheeler, Ingrid Holzmann, and Viviana Benesovsky. None of this work would have been remotely possible without Fermino DaSilva, our tree climber. I thank the Argentine National Park Service and the Delegacion Tecnica Regional Nordeste for permission to work at the field station and to Karina Schiaffino for helping to solve many field station problems. This work was supported by NSF grants IBN-9511642 and BNS-9870909, and by a grant from the Committee on Research and Exploration of the National Geographic Society. All research protocols described here were approved by Stony Brook University’s Institutional Animal Care and Use Committee in the years performed.
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This contribution is part of the special issue “ A Socioecological Perspective on Primate Cognition” (Cunningham and Janson 2007b).
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Janson, C.H. Experimental evidence for route integration and strategic planning in wild capuchin monkeys. Anim Cogn 10, 341–356 (2007). https://doi.org/10.1007/s10071-007-0079-2
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DOI: https://doi.org/10.1007/s10071-007-0079-2