Animal Cognition

, 12:575

Metamemory in tufted capuchin monkeys (Cebus apella)

Original Paper


Whereas evidence for metacognition by nonhuman primates has been obtained in great apes and old world monkeys, it is weaker in new world monkeys. For instance, capuchin monkeys may fail to recognize their own knowledge of the location of invisible bait. In the present study, we tested whether tufted capuchin monkeys would flexibly change their behavior in a delayed matching-to-sample (DMTS) test depending upon the strength of their memory trace of the sample. In Experiment 1, two monkeys were tested on a modified 9-alternative DMTS task with various delays on a computerized display. In some trials, the monkeys could choose whether to go for a memory test or for a simple key touch as an escape from the test. In other trials, they were forced to go for the memory test. Both monkeys escaped from the memory test more often when their matching accuracy on forced tests was lower. In one of the monkeys, the matching accuracies on chosen memory tests decreased more slowly as a function of delay length, and were higher after long delays than those on forced memory tests. This suggests that at least one capuchin monkey was able to recognize the strength of his own memory trace. Experiment 2 employed occasional no-sample tests, in which the monkeys faced the task choice without presentation of any sample for the trial. The monkey who was successful in Experiment 1 declined the memory test more often in no-sample trials than regular trials, further indicating metamemory in this individual. In Experiment 3, this successful monkey received a task, in which he was sometimes able to choose between shape MTS or texture MTS tasks. However, his matching accuracies did not differ between chosen tasks and forced tasks. Thus, the metamemory possessed by this new world monkey species may be more like a flag, showing strength of memory trace, than an elaborate representation showing details of the memory trace.


Metamemory Metacognition Memory trace Delayed matching-to-sample Tufted capuchin monkeys 


  1. Babb SJ, Crystal JD (2006) Discrimination of what, when, and where is not based on time of day. Learn Motiv 34:124–130Google Scholar
  2. Basile, BM, Hampton, RR, Suomi, SJ, Murra, EA (2008). An assessment of memory awareness in tufted capuchin monkeys (Cebus apella). Anim Cogn. doi:10.1007/s10071-008-0180-1
  3. Call J (2005) The self and other: a missing link in comparative social cognition. In: Terrace HS, Metcalfe J (eds) The missing link in cognition: origins of self-reflective consciousness. Oxford University Press, New York, pp 321–341Google Scholar
  4. Call J, Carpenter M (2001) Do apes and children know what they have seen? Anim Cogn 4:207–220CrossRefGoogle Scholar
  5. Clayton NS, Dickinson A (1998) Episodic-like memory during cache recovery by scrub jays. Nature 395:272–274PubMedCrossRefGoogle Scholar
  6. Dunlosky J, Bjork RA (2008) Handbook of metamemory and memory. Psychology Press, NewYorkGoogle Scholar
  7. Ferkin MH, Combs A, delBarco-Trillo J, Pierce AA, Franklin S (2008) Meadow voles, Microtus pennsylvanicus, have the capacity to recall the “what”, “where”, and “when” of a single past event. Anim Cogn 11:147–159PubMedCrossRefGoogle Scholar
  8. Foote AL, Crystal JD (2007) Metacognition in the rat. Cur Biol 17:551–555CrossRefGoogle Scholar
  9. Fragaszy DM, Izar P, Visalberghi E, Ottoni EB, de Oliveira MG (2004) Wild capuchin monkeys (Cebus libidinosurs) use anvils and stone pounding tools. Am J Primatol 64:359–366PubMedCrossRefGoogle Scholar
  10. Fujita K, Giersch A (2005) What perceptual rules do capuchin monkeys (Cebus apella) follow in completing partly occluded figures? J Exp Psychol Anim Behav Process 31:387–398PubMedCrossRefGoogle Scholar
  11. Fujita K, Kuroshima H, Masuda T (2002) Do tufted capuchin monkeys (Cebus apella) spontaneously deceive opponents? A preliminary analysis of an experimental food-competition contest between monkeys. Anim Cogn 5:19–25PubMedCrossRefGoogle Scholar
  12. Fujita K, Kuroshima H, Asai S (2003) How do tufted capuchin monkeys (Cebus apella) understand causality involved in tool use? J Exp Psychol Anim Behav Process 29:233–242PubMedCrossRefGoogle Scholar
  13. Hampton RR (2001) Rhesus monkeys know when they remember. Proc Natl Acad Sci USA 98:5359–5362PubMedCrossRefGoogle Scholar
  14. Hampton RR (2005) Can rhesus monkeys discriminate between remembering and forgetting? In: Terrace H, Metcalfe J (eds) The missing link in cognition: origins of self-reflective consciousness. Oxford University Press, New York, pp 272–295Google Scholar
  15. Hampton RR, Zivin A, Murray EA (2004) Rhesus monkeys (Macaca mulatta) discriminate between knowing and not knowing and collect information as needed before acting. Anim Cogn 7:239–254PubMedCrossRefGoogle Scholar
  16. Hattori Y, Kuroshima H, Fujita K (2005) Cooperative problem solving by tufted capuchin monkeys (Cebus apella): Spontaneous division of labor, communication, and reciprocal altruism. J Comp Psychol 119:335–342PubMedCrossRefGoogle Scholar
  17. Hattori Y, Kuroshima H, Fujita K (2007) I know you are not looking at me: capuchin monkeys’ (Cebus apella) sensitivity to human attentional states. Anim Cogn 10:141–148PubMedCrossRefGoogle Scholar
  18. Inman A, Shettleworth SJ (1999) Detecting metamemory in nonverbal subjects: a test with pigeons. J Exp Psychol Anim Behav Process 25:389–395CrossRefGoogle Scholar
  19. Itakura S (1996) An exploratory study of gaze-monitoring in nonhuman primates. Jpn Psychol Res 38:174–180CrossRefGoogle Scholar
  20. Jensen K, Call J, Tomasello M (2007) Chimpanzees are rational maximizers in an ultimatum game. Science 318:107–109PubMedCrossRefGoogle Scholar
  21. Kaminski J, Call J, Tomasello M (2004) Body orientation and face orientation: two factors controlling apes’ begging behavior from humans. Anim Cogn 7:216–223PubMedCrossRefGoogle Scholar
  22. Kornell N, Son LK, Terrace HS (2007) Transfer of metacognitive skills and hint seeking in monkeys. Psychol Sci 18:64–71PubMedCrossRefGoogle Scholar
  23. Kuroshima H, Fujita K, Masuda T (2002) Understanding of the relationship between seeing and knowing by capuchin monkeys (Cebus apella). Anim Cogn 5:41–48PubMedCrossRefGoogle Scholar
  24. Kuroshima H, Fujita K, Adachi I, Iwata K, Fuyuki A (2003) A capuchin monkey (Cebus apella) understands when people do and do not know the location of food. Anim Cogn 6:283–291PubMedCrossRefGoogle Scholar
  25. Mazzoni G, Nelson TO (1998) Metacognition and cognitive neuropsychology. Lawrence Erlbaum Associates, MahwahGoogle Scholar
  26. Metcalfe J, Shimamura AP (1994) Metacognition: knowing about knowing. The MIT Press, CamridgeGoogle Scholar
  27. Ottoni EB, Mannu M (2001) Semifree-ranging tufted capuchin monkeys (Cebus apella) spontaneously use tools to crack open nuts. Int J Primatol 22:347–358CrossRefGoogle Scholar
  28. Paukner A, Anderson JR, Fujita K (2005) Redundant food searches by capuchin monkeys (Cebus apella): a failure of metacognition? Anim Cogn 9:110–117PubMedCrossRefGoogle Scholar
  29. Povinelli DJ, Eddy TJ (1996). What young chimpanzees know about seeing. Monogr Soc Res Child Dev 61(3):i–vi, 1–152Google Scholar
  30. Silk JB, Brosnan SF, Vonk J, Henrich J, Povinelli DJ, Richardson AS, Lambeth SP, Mascaro J, Schapiro SJ (2005) Chimpanzees are indifferent to the welfare of unrelated group members. Nature 437:1357–1359PubMedCrossRefGoogle Scholar
  31. Smith JD, Schull J, Strote J, McGee K, Egnor R, Erb L (1995) The uncertain reponse in the bottlenosed dolphin (Tursiops truncatus). J Exp Psychol Gen 124:391–408PubMedCrossRefGoogle Scholar
  32. Smith JD, Shields WE, Schull J, Washburn DA (1997) The uncertain response in humans and animals. Cognition 62:75–97PubMedCrossRefGoogle Scholar
  33. Smith JD, Shields WE, Washburn DA (2003) The comparative psychology of uncertainty monitoring and metacognition. Behav Brain Sci 26:317–373PubMedGoogle Scholar
  34. Son LK, Kornell N (2005) Metacognitive judgments in rhesus macaques: Explicit versus implicit mechanisms. In: Terrace H, Metcalfe J (eds) The missing link in cognition: origins of self-reflective consciousness. Oxford University Press, New York, pp 296–320Google Scholar
  35. Suda-King C (2008) Do orangutans (Pongo pygmaeus) know when they do not remember? Anim Cogn 11:21–42Google Scholar
  36. Vick S-J, Anderson JR (2000) Learning and limits of use of eye gaze by capuchin monkeys (Cebus apella) in an object-choice task. J Comp Psychol 114:200–207PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2009

Authors and Affiliations

  1. 1.Department of Psychology, Graduate School of LettersKyoto UniversityKyotoJapan

Personalised recommendations