Memory for what, where, and when in the black-capped chickadee (Poecile atricapillus)
Abstract
Episodic memory is the ability to remember personally experienced past events (Tulving in Organization of memory. Academic Press, San Diego, pp. 381-403, 1972). In non-human animals, the behavioural criterion for episodic-like memory is remembering "what" occurred in conjunction with "when" and "where" (Clayton and Dickinson in Nature 395:272-274, 1998). We conducted tests for "what, where, and when" memory in a food-storing bird, the black-capped chickadee (Poecile atricapillus). In Experiment 1, chickadees found sunflower seeds and mealworms in concealed sites in their home cage. Birds later re-visited these sites after either a short (3 h) or long (123 h) retention interval. Chickadees normally prefer mealworms, but at the long retention interval mealworms were degraded in taste and appearance. Chickadees showed some memory for what kind of food they had encountered and where, but no memory for when food had previously been found. Experiment 2 followed a similar procedure, except that chickadees searched for hidden sunflower seeds and mealworms in trees in an indoor aviary. These more natural conditions increased both the spatial scale of the task and the effort required to find food. In this experiment, birds showed evidence for all three components of what-where-when memory. Unlike some previous studies of episodic-like memory, birds' behaviour cannot be accounted for by differential memory strength for more recent events. The results show that memory for what, where, and when occurs in food-storing birds outside the corvid family, does not require food caching or retrieval, and that remembering "when" can depend on the nature of the task.
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Chickadees failed to recall 'when' information when tested in non-natural settings.
“chickadees failed to recall ‘when’ information when tested in non-natural settings [62].”
From Is episodic-like memory <i>like</i> episodic memory? (2024) · cites this paper as [62]
Some experiments required birds to remember details of caches they did not make themselves, but this is still within their naturally occurring behavioural repertoire.
“While some of these experiments required the birds to remember details of caches that they did not make themselves [62,92], this is still under the remit of their naturally occurring behavioural repertoire.”
From Is episodic-like memory <i>like</i> episodic memory? (2024) · cites this paper as [62]
Cites
(1983) · Medical Entomology and Zoology · Cited by 6,051 · see citing works
Episodic memory: from mind to brain
Tulving, E. (2002) · Annual Review of Psychology · doi:10.1146/annurev.psych.53.100901.135114 · Cited by 4,950 · see citing works
(2007) · Cognitive Psychology · doi:10.4135/9781446212967.n15 · Cited by 3,749 · see citing works
The evolution of foresight: What is mental time travel, and is it unique to humans?
Suddendorf, T., & Corballis, M. C. (2007) · Behavioral and Brain Sciences · doi:10.1017/s0140525x07001975 · Cited by 2,031 · see citing works
How many memory systems are there?
Tulving, E. (1985) · American Psychologist · doi:10.1037/0003-066x.40.4.385 · Cited by 1,909 · see citing works
Episodic-like memory during cache recovery by scrub jays
Clayton, N. S., & Dickinson, A. (1998) · Nature · doi:10.1038/26216 · Cited by 1,464 · see citing works
Battig, W. F., Tulving, E., & Donaldson, W. (1973) · The American Journal of Psychology · doi:10.2307/1421962 · Cited by 1,428 · see citing works
Mental time travel and the evolution of the human mind.
Suddendorf, T., & Corballis, M. C. (1997) · PubMed · Cited by 1,053 · see citing works
Memory for the time of past events.
Friedman, W. J. (1993) · Psychological Bulletin · doi:10.1037/0033-2909.113.1.44 · Cited by 639 · see citing works
Food-Caching Western Scrub-Jays Keep Track of Who Was Watching When
Dally, J. M., Emery, N. J., & Clayton, N. S. (2006) · Science · doi:10.1126/science.1126539 · Cited by 501 · see citing works
Roberts, W. A. (2002) · Psychological Bulletin · doi:10.1037/0033-2909.128.3.473 · Cited by 432 · see citing works
Self-citationAlternative representations of time, number, and rate
Church, R. M., & Broadbent, H. A. (1990) · Cognition · doi:10.1016/0010-0277(90)90018-f · Cited by 362 · see citing works
Episodic-like Memory in the Rat
Babb, S. J., & Crystal, J. D. (2006) · Current Biology · doi:10.1016/j.cub.2006.05.025 · Cited by 308 · see citing works
Recalling yesterday and predicting tomorrow
Grant, J. B., & Suddendorf, T. (2005) · Cognitive Development · doi:10.1016/j.cogdev.2005.05.002 · Cited by 278 · see citing works
Western Scrub-Jays Anticipate Future Needs Independently of Their Current Motivational State
Correia, S. P. C., Dickinson, A., & Clayton, N. S. (2007) · Current Biology · doi:10.1016/j.cub.2007.03.063 · Cited by 258 · see citing works
Wistar rats show episodic-like memory for unique experiences
KARTTEKE, E., DESOUZASILVA, M., HUSTON, J., & DERE, E. (2006) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2005.10.002 · Cited by 250 · see citing works
Integrated memory for objects, places, and temporal order: Evidence for episodic-like memory in mice
Dere, E., Huston, J. P., & De Souza Silva, M. A. (2005) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2005.07.002 · Cited by 243 · see citing works
Episodic-like memory in mice: Simultaneous assessment of object, place and temporal order memory
Dere, E., Huston, J. P., & Silva, M. A. D. S. (2005) · Brain Research Protocols · doi:10.1016/j.brainresprot.2005.08.001 · Cited by 242 · see citing works
Clayton, N. S., Yu, K. S., & Dickinson, A. (2001) · Journal of Experimental Psychology: Animal Behavior Processes · doi:10.1037//0097-7403.27.1.17 · Cited by 238 · see citing works
Clayton, N. S., & Dickinson, A. (1999) · Journal of Comparative Psychology · doi:10.1037/0735-7036.113.4.403 · Cited by 227 · see citing works
Episodic-like memory in rats: is it based on when or how long ago?
Roberts, W. A., Feeney, M. C., MacPherson, K., Petter, M., McMillan, N., & Musolino, E. (2008) · Science · doi:10.1126/science.1152709 · Cited by 191 · see citing works
Cowie, R. J., Krebs, J. R., & Sherry, D. F. (1981) · Animal Behaviour · doi:10.1016/s0003-3472(81)80077-2 · Cited by 187 · see citing works
Self-citationFood storage by black-capped chickadees: Memory for the location and contents of caches
Sherry, D. F. (1984) · Animal Behaviour · doi:10.1016/s0003-3472(84)80281-x · Cited by 183 · see citing works
Self-citationEcology and Evolution of Food-storage Behavior in Conifer-seed-caching Corvids
Wall, S. B. V., & Balda, R. P. (2010) · Zeitschrift für Tierpsychologie · doi:10.1111/j.1439-0310.1981.tb01298.x · Cited by 183 · see citing works
Discrimination of what, when, and where: Implications for episodic-like memory in rats
Babb, S. J., & Crystal, J. D. (2005) · Learning and Motivation · doi:10.1016/j.lmot.2005.02.009 · Cited by 181 · see citing works
Episodic-like memory in pigeons
Zentall, T. R., Clement, T. S., Bhatt, R. S., & Allen, J. (2001) · Psychonomic Bulletin & Review · doi:10.3758/bf03196204 · Cited by 178 · see citing works
An evolutionary perspective on caching by corvids
de Kort, S. R., & Clayton, N. S. (2005) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2005.3350 · Cited by 159 · see citing works
Dally, J. M., Emery, N. J., & Clayton, N. S. (2005) · Animal Behaviour · doi:10.1016/j.anbehav.2005.02.009 · Cited by 157 · see citing works
Timing in Free-Living Rufous Hummingbirds, Selasphorus rufus
Henderson, J., Hurly, T. A., Bateson, M., & Healy, S. D. (2006) · Current Biology · doi:10.1016/j.cub.2006.01.054 · Cited by 140 · see citing works
What–Where–When memory in magpies (Pica pica)
Zinkivskay, A., Nazir, F., & Smulders, T. V. (2009) · Animal Cognition · doi:10.1007/s10071-008-0176-x · Cited by 139 · see citing works
Long-term memory for cache sites in the black-capped chickadee
Hitchcock, C. L., & Sherry, D. F. (1990) · Animal Behaviour · doi:10.1016/s0003-3472(05)80699-2 · Cited by 136 · see citing works
Self-citationHampton, R. R., Hampstead, B. M., & Murray, E. A. (2005) · Learning and Motivation · doi:10.1016/j.lmot.2005.02.004 · Cited by 128 · see citing works
Interval Timing by an Invertebrate, the Bumble Bee Bombus impatiens
Boisvert, M. J., & Sherry, D. F. (2006) · Current Biology · doi:10.1016/j.cub.2006.06.064 · Cited by 122 · see citing works
Self-citationThe comparative study of mental time travel
Roberts, W. A., & Feeney, M. C. (2009) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2009.03.003 · Cited by 111 · see citing works
Self-citationRetrospective cognition by food-caching western scrub-jays
de Kort, S. R., Dickinson, A., & Clayton, N. S. (2005) · Learning and Motivation · doi:10.1016/j.lmot.2005.02.008 · Cited by 107 · see citing works
Ferkin, M. H., Combs, A., delBarco‐Trillo, J., Pierce, A. A., & Franklin, S. (2007) · Animal Cognition · doi:10.1007/s10071-007-0101-8 · Cited by 107 · see citing works
Episodic-like memory in a gorilla: A review and new findings
Schwartz, B. L., Hoffman, M. L., & Evans, S. (2005) · Learning and Motivation · doi:10.1016/j.lmot.2005.02.012 · Cited by 96 · see citing works
Bird, L. R., Roberts, W. A., Abroms, B. D., Kit, K. A., & Crupi, C. (2003) · Journal of comparative psychology · doi:10.1037/0735-7036.117.2.176 · Cited by 92 · see citing works
Self-citationEpisodic-like memory: Pigeons can report location pecked when unexpectedly asked
Zentall, T. R., Singer, R. A., & Stagner, J. P. (2008) · Behavioural Processes · doi:10.1016/j.beproc.2008.05.003 · Cited by 84 · see citing works
Memory for “what”, “where”, and “when” information in rhesus monkeys (Macaca mulatta).
Hoffman, M. L., Beran, M. J., & Washburn, D. A. (2009) · Journal of Experimental Psychology Animal Behavior Processes · doi:10.1037/a0013295 · Cited by 79 · see citing works
Brodin, A., & Ekman, J. B. (1994) · Nature · doi:10.1038/372510a0 · Cited by 72 · see citing works
Black-capped Chickadee (Poecile atricapillus)
Foote, J. R., Mennill, D. J., Ratcliffe, L. M., et al. (2005) · The Birds of North America Online · doi:10.2173/bna.39 · Cited by 65 · see citing works
What-where-when memory in pigeons.
Skov-Rackette, S. I., Miller, N. Y., & Shettleworth, S. J. (2006) · Journal of Experimental Psychology Animal Behavior Processes · doi:10.1037/0097-7403.32.4.345 · Cited by 65 · see citing works
Episodic-like memory in crossbred Yucatan minipigs (Sus scrofa)
Kouwenberg, A., Walsh, C. J., Morgan, B. E., & Martin, G. M. (2009) · Applied Animal Behaviour Science · doi:10.1016/j.applanim.2009.01.005 · Cited by 62 · see citing works
Are there alternatives to traditional polygraph procedures?
Bashore, T. R., & Rapp, P. E. (1993) · Psychological Bulletin · doi:10.1037/0033-2909.113.1.3 · Cited by 57 · see citing works
Naqshbandi, M., Feeney, M. C., McKenzie, T. L. B., & Roberts, W. A. (2006) · Behavioural Processes · doi:10.1016/j.beproc.2006.10.010 · Cited by 55 · see citing works
Self-citationAnnual Cycle of the Black-Capped Chickadee: Seasonality of Food-Storing and the Hippocampus
Hoshooley, J. S., Phillmore, L. S., Sherry, D. F., et al. (2006) · Brain Behavior and Evolution · doi:10.1159/000096984 · Cited by 54 · see citing works
Self-citationMacDougall‐Shackleton, S. A., Sherry, D. F., Clark, A. P., et al. (2003) · Animal Behaviour · doi:10.1006/anbe.2003.2113 · Cited by 53 · see citing works
Self-citationFloral reward production is timed by an insect pollinator
Boisvert, M. J., Veal, A. J., & Sherry, D. F. (2007) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2007.0445 · Cited by 33 · see citing works
Self-citationNeurobiology of spatial behavior
Sherry, D. F., & Hoshooley, J. S. (2007) · Oxford University Press eBooks · doi:10.1093/acprof:oso/9780198569992.003.0002 · Cited by 33 · see citing works
Self-citationAnimal Memory: Episodic-like Memory in Rats
Roberts, W. A. (2006) · Current Biology · doi:10.1016/j.cub.2006.07.001 · Cited by 30 · see citing works
Self-citationSpatial list learning in black-capped chickadees
Crystal, J. D., & Shettleworth, S. J. (1994) · Animal Learning & Behavior · doi:10.3758/bf03199958 · Cited by 28 · see citing works
Black-capped Chickadee (Poecile atricapillus)
Smith, S. M. (1993) · The Birds of North America Online · doi:10.2173/bna.039 · Cited by 7 · see citing works
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Allen, T. A., & Fortin, N. J. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1301199110 · Cited by 350 · see citing works
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Holland, S. M., & Smulders, T. V. (2011) · Animal Cognition · doi:10.1007/s10071-010-0346-5 · Cited by 61 · see citing works
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Zhou, W., & Crystal, J. D. (2011) · Animal Cognition · doi:10.1007/s10071-010-0367-0 · Cited by 60 · see citing works
Davies, J. R., Garcia-Pelegrin, E., & Clayton, N. S. (2024) · PLOS ONE · doi:10.1371/journal.pone.0301298 · Cited by 31 · see citing works
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Takagi, S., Tsuzuki, M., Chijiiwa, H., Arahori, M., Watanabe, A., Saito, A., & Fujita, K. (2017) · Behavioural Processes · doi:10.1016/j.beproc.2016.12.014 · Cited by 19 · see citing works
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Self-citation
- Authors
- Feeney, M. C., Roberts, W. A., & Sherry, D. F.
- Affiliations
- Western University (CA)
- Corresponding author
- Feeney, Miranda C.
- Venue
- Animal Cognition
- Published
- 2009-05-23
- Volume
- 12
- Issue
- 6
- Pages
- 767-777
- ISSN
- 1435-9448 (ISSN-L)
- 1435-9456
- OpenAlex
- W2103274435
- Cited by
- 101
- References
- 54
- Citations by year
- 2026: 1 · 2025: 6 · 2024: 6 · 2023: 4 · 2022: 5 · 2021: 7 · 2020: 7 · 2019: 3 · 2018: 2 · 2017: 12 · 2016: 6 · 2015: 8 · 2014: 6 · 2013: 7 · 2012: 5
- FWCI
- 3.39
- Type
- journal article
- Language
- en
- Open access
- closed
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Animal Cognition (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory Processes and Influences
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Social Sciences › Psychology › Developmental and Educational Psychology › Child and Animal Learning Development
- Keywords
- episodic-like memory, black-capped chickadee, food storage, food caching, retention interval, spatial memory, temporal memory, avian cognition
- MeSH terms
- Animals, Feeding Behavior, Memory, Retention, Psychology, Songbirds
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