Cited by 244Primate Behavior and EcologyMemory Processes and InfluencesChild and Animal Learning Development

The DOI matches its Crossref record; 69 of the 69 references it cites were found in a registry or an index; none of the 47 sources its claims cite is checked for support yet.

Keeping track of time: evidence for episodic-like memory in great apes

Open access

Martin-Ordas, Gema, Haun, Daniel, Colmenares, Fernando, Call, Josep·2010·Animal Cognition

DOI 10.1007/s10071-009-0282-4PMC PMC2822233

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Abstract

Episodic memory, as defined by Tulving, can be described in terms of behavioural elements (what, where and when information) but it is also accompanied by an awareness of one's past (chronesthesia) and a subjective conscious experience (autonoetic awareness). Recent experiments have shown that corvids and rodents recall the where, what and when of an event. This capability has been called episodic-like memory because it only fulfils the behavioural criteria for episodic memory. We tested seven chimpanzees, three orangutans and two bonobos of various ages by adapting two paradigms, originally developed by Clayton and colleagues to test scrub jays. In Experiment 1, subjects were fed preferred but perishable food (frozen juice) and less preferred but non-perishable food (grape). After the food items were hidden, subjects could choose one of them either after 5 min or 1 h. The frozen juice was still available after 5 min but melted after 1 h and became unobtainable. Apes chose the frozen juice significantly more after 5 min and the grape after 1 h. In Experiment 2, subjects faced two baiting events happening at different times, yet they formed an integrated memory for the location and time of the baiting event for particular food items. We also included a memory task that required no temporal encoding. Our results showed that apes remember in an integrated fashion what, where and when (i.e., how long ago) an event happened; that is, apes distinguished between different events in which the same food items were hidden in different places at different times. The temporal control of their choices was not dependent on the familiarity of the platforms where the food was hidden. Chimpanzees' and bonobos' performance in the temporal encoding task was age-dependent, following an inverted U-shaped distribution. The age had no effect on the performance of the subjects in the task that required no temporal encoding.

AI snapshot

Written from the paper’s full text.

TL;DR

Great apes remembered what, where, and when food was hidden in an integrated fashion, choosing perishable frozen juice more after 5 min and non-perishable grape after 1 h. Performance on this episodic-like memory task followed an inverted U-shaped age pattern, while a non-temporal memory task showed no age effect.

Key findings

In Experiment 1, apes chose frozen juice significantly more often after a 5-min retention interval than after 1 h (Wilcoxon: z = 2.55, p = 0.011, n = 12); 4 of 12 subjects showed this reversal individually.
In the pre-test requiring no temporal encoding, apes remembered food location above chance across delays (Wilcoxon: z = 3.12, p = 0.002, n = 12), with no age effect (r_s = 0.08, p = 0.41).
Experiment 1 www-memory performance showed an inverted U-shaped age trend (permutation test: c² = −0.142, p = 0.0682, n = 12); for chimpanzees and bonobos alone this was significant (c² = −0.026, p = 0.002, n = 9).
In Experiment 2, subjects chose frozen juice significantly more often from the platform baited last than from the platform baited first (Wilcoxon: z = 1.79, p = 0.037, one-tailed, n = 5), supporting integrated what–where–when memory.

Methods

Experiment 1 tested 7 chimpanzees, 3 orangutans, and 2 bonobos (12 total; ages 6–31 years) at the Wolfgang Köhler Primate Research Centre, using a platform with three possible baiting sites and two food types: preferred perishable frozen juice and less preferred non-perishable grape.
Subjects chose after 5-min or 1-h retention intervals; analyses used Wilcoxon tests, Pearson chi-square, and permutation-based quadratic models of age effects.
Experiment 2 tested 5 successful subjects (2 bonobos, 2 chimpanzees, 1 orangutan; ages 10–14 years) with two baiting events separated by 1 h and choice tests 5 min after the second event, analyzed with a one-tailed Wilcoxon test.

Limitations

The paper states that the reduced sample size did not allow more fine-grained analyses to distinguish differences between great ape species or developmental patterns.
The paper states that the data do not allow the conclusion that apes are actually recalling the baiting episode, and the mechanism used to keep track of time remains undetermined.
The paper notes that orangutan performance could reflect species differences or simply that the tested orangutans were too young or too old; more broadly, the study assesses behavioral criteria for episodic-like memory, not autonoetic awareness.

Model-written summary. Check it against the paper before relying on it.

Integrity signals

Registry

Crossref · 10.1007/s10071-009-0282-4

Cites

69 of 69 references verified0 citation errors · 0 not checkable

Statistics

Claims the paper makes

0 of 47 cited sources checked · 0 supported · 0 flagged

A result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“there was no change in performance across ages (r s=0.08, p = 0.41, n = 12).”
- Also stated in: § Abstract · plain
  “The age had no effect on the performance of the subjects in the task that required no temporal encoding.”
§ Keeping track of time: evidence for episodic-like memory in great apes > Experiment 1: content of memories > Results
Strength:plain· not yet calibratedn = 12
Tests✓ Asserted: passes✓ Checkable: passes? Load-bearing: unclear✓ Based: passes
A result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“In Experiment 2, subjects faced two baiting events happening at different times, yet they formed an integrated memory for the location and time of the baiting event for particular food items.”
§ Keeping track of time: evidence for episodic-like memory in great apes > Abstract
Load-bearingStrength:plain· not yet calibratedCausal:direct· not yet calibrated
Tests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes✓ Based: passes
- Rests on an assumption: Frozen juice remains available/edible after 5 min but melts and becomes unobtainable after 1 h.
A result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“Apes chose the frozen juice significantly more after 5 min and the grape after 1 h.”
- Also stated in: § Results · plain
  “Subjects chose the frozen juice significantly more often after the 5-min interval than after the 1-h interval (Wilcoxon test: z = 2.55, p = 0.011, n = 12; Fig. 2).”
§ Keeping track of time: evidence for episodic-like memory in great apes > Abstract
Load-bearingStrength:plain· not yet calibratedCausal:correlational· not yet calibratedn = 12
Tests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes✓ Based: passes
- Rests on an assumption: Frozen juice remains available/edible after 5 min but melts and becomes unobtainable after 1 h.
- Rests on an assumption: The grape is a non-perishable food.
A result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“Focusing solely on members of the genus Pan (chimpanzees and bonobos) confirmed this result (permutation test: c 2 = −0.026, p = 0.002, n = 9).”
- Also stated in: § Abstract · plain
  “Chimpanzees’ and bonobos’ performance in the temporal encoding task was age-dependent, following an inverted U-shaped distribution.”
§ Keeping track of time: evidence for episodic-like memory in great apes > Experiment 1: content of memories > Results
Strength:plain· not yet calibratedCausal:correlational· not yet calibratedn = 9
Tests✓ Asserted: passes✓ Checkable: passes? Load-bearing: unclear✓ Based: passes
A result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“Additionally, apes’ performance in the www-memory task showed an inverted U-shaped curve in which middle-age subjects performed better than the youngest and oldest subjects.”
- Also stated in: § General discussion · plain
  “Additionally, subjects’ performance in the www-memory task showed an age-dependent inverted U-shaped curve.”
§ Keeping track of time: evidence for episodic-like memory in great apes > Experiment 1: content of memories > Discussion
Strength:plain· not yet calibratedCausal:correlational· not yet calibrated
Tests✓ Asserted: passes✓ Checkable: passes? Load-bearing: unclear✓ Based: passes

Show all 42 claims

It may state two separate claims as one. 14
The quote only partly states this claim. 1
Probably not a substantial claim. 30

None of the sources cited for this claim have been checked yet.
In the paper
“Clayton and colleagues have shown that scrub jays flexibly integrated memories for the what, where and when of an event (Clayton and Dickinson 1998, 1999; Clayton et al. 2001, 2003b).”
§ Keeping track of time: evidence for episodic-like memory in great apes > Introduction
What the sources say
- Not checked yetcites Clayton and Dickinson 1998 source
- Not checked yetcites Clayton et al. 2001 source
- Not checked yetcites Clayton et al. 2003b
Strength:boosted· not yet calibratedCausal:direct· not yet calibrated
Tests✓ Asserted: passes✓ Checkable: passes✗ Load-bearing: fails✓ Based: passes
Probably not a substantial claim. The paper’s conclusions may not depend on it.
In the paper
“Therefore, one weakness in Clayton’s experimental approach is that it does not measure memory for unique experiences because they require training.”
§ Keeping track of time: evidence for episodic-like memory in great apes > Introduction
What the sources say
- Not checked yetcites Zentall et al. 2001 source
Strength:plain· not yet calibratedCausal:direct· not yet calibrated
Tests✓ Asserted: passes✓ Checkable: passes✗ Load-bearing: fails✓ Based: passes
Probably not a substantial claim. The paper’s conclusions may not depend on it.
In the paper
“However, their subjects were asked to remember these three elements in separate occasions, raising doubts about the integration of the components.”
§ Keeping track of time: evidence for episodic-like memory in great apes > Introduction
What the sources say
- Not checked yetcites Hoffman et al. 2009
Load-bearingStrength:plain· not yet calibratedCausal:direct· not yet calibrated
Tests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes✓ Based: passes
It may state two separate claims as one.
None of the sources cited for this claim have been checked yet.
In the paper
“recent experimental studies have shown evidence for planning in chimpanzees, bonobos and orangutans”
§ Keeping track of time: evidence for episodic-like memory in great apes > Introduction
What the sources say
- Not checked yetcites Mulcahy and Call 2006 source
- Not checked yetcites Dufour and Sterck 2008 source
- Not checked yetcites Osvath and Osvath 2008 source
Load-bearingStrength:plain· not yet calibratedCausal:correlational· not yet calibrated
Tests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes✓ Based: passes
Probably not a substantial claim.
None of the sources cited for this claim have been checked yet.
In the paper
“An alternative approach suggested by Eacott et al. (2005) challenged the main role of the “when” component in episodic-like memory.”
§ Keeping track of time: evidence for episodic-like memory in great apes > Introduction
What the sources say
- Not checked yetcites Eacott et al. 2005 source
- Not checked yetcites Friedman 1993 source
Load-bearingStrength:hedged· not yet calibratedCausal:direct· not yet calibrated
Tests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes✓ Based: passes
Probably not a substantial claim. It may state two separate claims as one.
In the paper
“The results from these experiments showed that rats were sensitive not only to the location of the objects, but also to the temporal order in which they were presented. These results led the authors to conclude that rats integrated what, where and when an event happened.”
§ Keeping track of time: evidence for episodic-like memory in great apes > Introduction
What the sources say
- Not checked yetcites Kart-Teke et al. 2006 source
Strength:plain· not yet calibratedCausal:direct· not yet calibrated
Tests✓ Asserted: passes✓ Checkable: passes✗ Load-bearing: fails✓ Based: passes
Probably not a substantial claim. The paper’s conclusions may not depend on it. It may state two separate claims as one.
None of the sources cited for this claim have been checked yet.
In the paper
“Other bird and mammal species have also been shown to possess such type of memory”
§ Keeping track of time: evidence for episodic-like memory in great apes > Introduction
What the sources say
- Not checked yetcites Babb and Crystal 2005 source
- Not checked yetcites Henderson et al. 2006 source
- Not checked yetcites Hampton et al. 2005 source
Strength:plain· not yet calibrated
Tests✓ Asserted: passes✓ Checkable: passes✗ Load-bearing: fails✓ Based: passes
Probably not a substantial claim. The paper’s conclusions may not depend on it.
In the paper
“Interestingly, longitudinal and cross-sectional studies in human memory have reported an inverted U-shaped curve as a function of age for episodic memory and no age effect for long-term memory (Bialystok and Craik 2006 for a review).”
§ Keeping track of time: evidence for episodic-like memory in great apes > Experiment 1: content of memories > Discussion
What the sources say
- Not checked yetcites Bialystok and Craik 2006 source
Strength:plain· not yet calibratedCausal:correlational· not yet calibrated
Tests✓ Asserted: passes✓ Checkable: passes✗ Load-bearing: fails✓ Based: passes
Probably not a substantial claim. The paper’s conclusions may not depend on it. It may state two separate claims as one.
In the paper
“Recently, Hoffman et al. 2009 examined working memory (Baddeley 2000) for what, where and when information in rhesus monkeys using a new paradigm based on a computer task and found positive evidence for episodic-like memory.”
§ Keeping track of time: evidence for episodic-like memory in great apes > Introduction
What the sources say
- Not checked yetcites Hoffman et al. 2009
Strength:plain· not yet calibrated
Tests✓ Asserted: passes✓ Checkable: passes✗ Load-bearing: fails✓ Based: passes
Probably not a substantial claim. The paper’s conclusions may not depend on it.
None of the sources cited for this claim have been checked yet.
In the paper
“The trial-unique learning paradigm has been successfully implemented in rodents (rats: Kart-Teke et al. 2006; mice: Dere et al. 2005) and birds (Zentall et al. 2001).”
§ Keeping track of time: evidence for episodic-like memory in great apes > Introduction
What the sources say
- Not checked yetcites Kart-Teke et al. 2006 source
- Not checked yetcites Dere et al. 2005 source
- Not checked yetcites Zentall et al. 2001 source
Strength:plain· not yet calibrated
Tests✓ Asserted: passes✓ Checkable: passes✗ Load-bearing: fails✓ Based: passes
Probably not a substantial claim. The paper’s conclusions may not depend on it.
None of the sources cited for this claim have been checked yet.
In the paper
“However, as pointed out by Crystal (2009), episodic memory is defined as a long-term memory system and the unexpected question experiment carried out by Zentall et al. (2001) only deals with short-time delays between the encoding event and the experimental question.”
§ Keeping track of time: evidence for episodic-like memory in great apes > Introduction
What the sources say
- Not checked yetcites Crystal 2009 source
- Not checked yetcites Zentall et al. 2001 source
Strength:plain· not yet calibrated
Tests✓ Asserted: passes✓ Checkable: passes? Load-bearing: unclear✓ Based: passes
It may state two separate claims as one.
None of the sources cited for this claim have been checked yet.
In the paper
“It has also been argued that episodic memory and future planning depend on common processes”
§ Keeping track of time: evidence for episodic-like memory in great apes > Introduction
What the sources say
- Not checked yetcites Mulcahy and Call 2006 source
- Not checked yetcites Dufour and Sterck 2008 source
- Not checked yetcites Osvath and Osvath 2008 source
Strength:hedged· not yet calibratedCausal:correlational· not yet calibrated
Tests✗ Asserted: fails✓ Checkable: passes✗ Load-bearing: fails✓ Based: passes
Probably not a substantial claim. The authors may not put it forward as true. The paper’s conclusions may not depend on it.
In the paper
“The results from this experiment showed that pigeons were able to report which action they performed in the past.”
§ Keeping track of time: evidence for episodic-like memory in great apes > Introduction
What the sources say
- Not checked yetcites Zentall et al. 2001 source
Strength:plain· not yet calibrated
Tests✓ Asserted: passes✓ Checkable: passes✗ Load-bearing: fails✓ Based: passes
Probably not a substantial claim. The paper’s conclusions may not depend on it.
In the paper
“Rats’ success in this task allowed the authors to conclude that rats recollected the what, where and which of a past episode.”
§ Keeping track of time: evidence for episodic-like memory in great apes > Introduction
What the sources say
- Not checked yetcites Eacott et al. 2005 source
Strength:plain· not yet calibratedCausal:direct· not yet calibrated
Tests✓ Asserted: passes✓ Checkable: passes✗ Load-bearing: fails✓ Based: passes
Probably not a substantial claim. The paper’s conclusions may not depend on it.
A conclusion the paper draws from its own results — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“Likewise, they chose more often the frozen juice in the platform baited last because the frozen juice was hidden 5 min ago and was, therefore, still edible.”
§ Keeping track of time: evidence for episodic-like memory in great apes > Experiment 2: structure of memories > Discussion
Load-bearingStrength:plain· not yet calibratedCausal:direct· not yet calibrated
Tests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes✓ Based: passes
It may state two separate claims as one.
- Rests on an assumption: Frozen juice hidden 1 h earlier had melted and was not edible, while frozen juice hidden 5 min earlier was still edible.
In the paper
“Familiarity is a recognition process that provides a temporal cue for knowing which food item will be available without actually recollecting the past event (Kort et al. 2005).”
§ Keeping track of time: evidence for episodic-like memory in great apes > General discussion
What the sources say
- Not checked yetcites Kort et al. 2005 source
Load-bearingStrength:plain· not yet calibratedCausal:direct· not yet calibrated
Tests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes✓ Based: passes
Probably not a substantial claim.
In the paper
“Friedman (1993) described three types of information that humans (but also animals) could process: temporal locations, which refer to when an event took place within a time pattern; temporal distances, implying how long ago an event occurred and before–after relations or order of events.”
§ Keeping track of time: evidence for episodic-like memory in great apes > General discussion
What the sources say
- Not checked yetcites Friedman 1993 source
Strength:plain· not yet calibrated
Tests✓ Asserted: passes✓ Checkable: passes✗ Load-bearing: fails✓ Based: passes
Probably not a substantial claim. The paper’s conclusions may not depend on it.
None of the sources cited for this claim have been checked yet.
In the paper
“Research on memory for the past events in humans has shown that there is no evidence that events are coded by the times of their occurrence or that memory is temporally organised (Friedman 1993, 2004).”
§ Keeping track of time: evidence for episodic-like memory in great apes > General discussion
What the sources say
- Not checked yetcites Friedman 1993 source
- Not checked yetcites Friedman 2004 source
Strength:plain· not yet calibrated
Tests✓ Asserted: passes✓ Checkable: passes✗ Load-bearing: fails✓ Based: passes
Probably not a substantial claim. The paper’s conclusions may not depend on it. It may state two separate claims as one.

37 of 37

The paper relies on this without support.
Frozen juice remains available/edible after 5 min but melts and becomes unobtainable after 1 h.
“The frozen juice was still available after 5 min but melted after 1 h and became unobtainable.”
“After 1 h, the frozen juice melted and became unobtainable, but it was still edible if chosen after 5 min.”
The paper relies on this without support.
The grape is a non-perishable food.
“less preferred but non-perishable food (grape)”
The paper relies on this without support.
Chimpanzees, bonobos and orangutans represent our closest and most distant great ape relatives, respectively.
“We tested chimpanzees, bonobos and orangutans because they represent our closest and most distant great ape relatives, respectively.”
The paper relies on this without support.
Frozen juice hidden 1 h earlier had melted and was not edible, while frozen juice hidden 5 min earlier was still edible.
“the frozen juice hidden in that platform was baited 1 h earlier and, therefore, had melted”
“the frozen juice was hidden 5 min ago and was, therefore, still edible”
The paper relies on this without support.
Apes prefer frozen juice over grapes when both are available.
“they should preferentially choose the frozen juice in the table baited last but the grape in the table baited first”
The paper relies on this without support.
The orangutan's significant reversal of choices in the last round of Experiment 1 indicates that her choices were based on how long ago the baiting event took place.
“We included one of the orangutans because in the last round of Experiment 1 she significantly reversed her choices (χ 2 = 6, p = 0.014; see table 1 for more details).”

6 of 6

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

Statistics recomputed

Every reported test result, recomputed from its test statistic and degrees of freedom. A result shows as not adding up only once an independent check has confirmed it.

Consistentz = 3.12reported p = .002 · recomputed p = .002
“z = 3.12, p = .002”
Consistentz = 2.55reported p = .011 · recomputed p = .011
“z = 2.55, p = .011”
Consistentz = 1.79reported p = .037 · recomputed p = .073
“z = 1.79, p = .037”
The paper states a one-tailed test

3 of 3

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

Each contradiction between two passages listed here was confirmed by an independent check.

The 24-hour pre-test was less accurate than the 2-minute pre-test
Major
Table 1 shows 100% accuracy at 2 minutes for every subject, but several subjects scored below 100% at 24 hours. The claim of equal accuracy underpins the paper's argument that there was no noticeable forgetting.
Experiment 2 percentages for Fifi do not fit six trials
Minor
Each Experiment 2 trial included a choice from both platforms, so six trials would yield six choices for each reported platform percentage. Fifi's reported 80% and 20% are not possible proportions of six choices; they correspond to proportions of five.

2 of 2

The episodic buffer: a new component of working memory?
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“Recently, Hoffman et al. 2009 examined working memory (Baddeley 2000) for what, where and when information in rhesus monkeys using a new paradigm based on a computer task and found positive evidence for episodic-like memory.”
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Self-citation
Notes
Pereltsvaig, A. M. (2026) · Cambridge University Press eBooks · doi:10.1017/9781009658256.014

Authors: Martin-Ordas, G., Haun, D., Colmenares, F., & Call, J.
Affiliations: Max Planck Institute for Evolutionary Anthropology (DE)
Universidad Complutense de Madrid (ES)
ORCID: Haun, Daniel
Colmenares, Fernando
Call, Josep
Venue: Animal Cognition
Publisher: Springer Science and Business Media LLC
Published: 2009-09-27
Volume: 13
Issue: 2
Pages: 331-340
ISSN: 1435-9448 (ISSN-L)
1435-9456
DOI: 10.1007/s10071-009-0282-4
PMC: PMC2822233
OpenAlex: W2165494708
Semantic Scholar: 448390e361ed5bf7a1a2721c8b62068b1f5cf1b0
Cited by: 244
References: 69
Citations by year: 2026: 14 · 2025: 9 · 2024: 11 · 2023: 14 · 2022: 12 · 2021: 22 · 2020: 14 · 2019: 35 · 2018: 8 · 2017: 23 · 2016: 6 · 2015: 14 · 2014: 17 · 2013: 10 · 2012: 12
FWCI: 15.04
Type: journal article
Language: en
Open access: hybrid
doi.org
Licence: cc-by-nc
creativecommons.org/licenses/by-nc/2.0 (tdm)
Locations: Animal Cognition (publishedVersion, cc-by-nc)
PubMed Central (publishedVersion, cc-by-nc)
PubMed (publishedVersion)
Max Planck Institute for Plasma Physics (submittedVersion)
Max Planck Digital Library (submittedVersion, other-oa)
MPG.PuRe (Max Planck Society) (submittedVersion, other-oa)
MPG.PuRe (Max Planck Society) (submittedVersion)
Topics: Life Sciences › Agricultural and Biological Sciences › Ecology, Evolution, Behavior and Systematics › Primate Behavior and Ecology
Life Sciences › Neuroscience › Cognitive Neuroscience › Memory Processes and Influences
Social Sciences › Psychology › Developmental and Educational Psychology › Child and Animal Learning Development
Keywords: episodic-like memory, great apes, chimpanzees, bonobos, orangutans, temporal memory, temporal coding, age differences
MeSH terms: Animals, Pan troglodytes, Feeding Behavior, Female, Food Preferences, Male, Pongo pygmaeus, Mental Recall, Time Factors, Time Perception, Hominidae, Pan paniscus

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Keeping track of time: evidence for episodic-like memory in great apes

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