Scrub jays (Aphelocoma coerulescens) form integrated memories of the multiple features of caching episodes

Four experiments examined whether food-storing scrub jays remember when and where they cached different foods. The scrub jays cached and recovered perishable and nonperishable foods in visuospatially distinct and trial-unique cache sites. They rapidly learned to avoid searching for foods that had perished by the time of recovery, while continuing to search for the same foods after shorter retention intervals when the foods were still fresh. The temporal control of searching at recovery was also observed when the familiarity of cache sites did not provide any information about the time of caching and when the same food was cached in distinct sites at different times. The authors argue that the jays formed an integrated memory for the location and time of caching of particular foods.     

Food caching by western scrub-jays (Aphelocoma californica) is sensitive to the conditions at recovery

Western scrub-jays (Aphelocoma californica) cached perishable and nonperishable food items, which they could recover after both short and long retention intervals. When perishable items were always degraded at recovery, jays decreased the number of perishable items cached and increased their caching of nonperishable items, relative to a control group whose caches were always fresh at recovery. Jays reduced the number of nonperishable items cached, however, when highly preferred food items were degraded only after the long retention intervals. The findings are discussed in terms of the role of retrospective and prospective processes in the control of caching.     

The control of food-caching behavior by Western scrub-jays (Aphelocoma californica)

Western scrub-jays (Aphelocoma californica) did not show extinction when caching behavior was never rewarded and they had no choice of where to cache the food. However, when the jays had the choice of caching items in 2 different locations or during 2 successive episodes, and only 1 of each was always rewarded at recovery, they rapidly learned to cache in the rewarded location or episode. When the jays had learned during training trials that their caches were always moved to 1 of 2 locations they did not cache in, then on the test trial they cached in the location that had been previously rewarded. To test whether these jays avoided the location in which their caches had been pilfered or chose the rewarded location, the procedure was repeated to include a 3rd location that was never rewarded. The jays avoided the pilfered location but cached equally in the rewarded and nonrewarded locations.     

Western scrub-jays (<Emphasis Type="Italic">Aphelocoma californica</Emphasis>) use cognitive strategies to protect their caches from thieving conspecifics

Food caching birds hide food and recover the caches when supplies are less abundant. There is, however, a risk to this strategy because the caches are susceptible to pilfering by others. Corvids use a number of different strategies to reduce possible cache theft. Scrub-jays with previous experience of pilfering other's caches cached worms in two visuospatially distinct caching trays either in private or in the presence of a conspecific. When these storers had cached in private, they subsequently observed both trays out of reach of a conspecific. When these storers had cached in the presence of a conspecific, they subsequently watched the observer pilfering from one of the trays while the other tray was placed in full view, but out of reach. The storers were then allowed to recover the remaining caches 3 h later. Jays cached more worms when they were observed during caching. At the time of recovery, they re-cached more than if they had cached in private, selectively re-caching outside of the trays in sites unbeknown to potential thieves. In addition, after a single pilfering trial, the jays switched their recovery strategy from predominantly checking their caches (i.e. returning to a cache site to see whether the food remained there) to predominantly eating them. Re-caching remained constant across the three trials. These results suggest that scrub-jays use flexible, cognitive caching and recovery strategies to aid in reducing potential future pilfering of caches by conspecifics.     

Eurasian jays (Garrulus glandarius) conceal caches from onlookers

Animals that cache food risk having their stored food pilfered by conspecifics. Previous research has shown that a number of food-caching species of corvid use strategies that decrease the probability of conspecifics pilfering their caches. In this experiment, we investigated whether Eurasian jays (Garrulus glandarius) would choose between caching behind an opaque and caching behind a transparent barrier whilst being observed by a conspecific. If caching in out-of-sight locations is a strategy to prevent conspecifics from pilfering these caches, then the jays should place a greater proportion of caches behind the opaque barrier when being observed than when caching in private. In accordance with this prediction, jays cached a greater proportion of food behind the opaque barrier when they were observed than when they cached in private. These results suggest that Eurasian jays may opt to cache in out-of-view locations to reduce the likelihood of conspecifics pilfering their caches.     

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

Episodic memory, as defined by Tulving, can be described in terms of behavioural elements (what, where and when information) but it is also accompained 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.     

How western scrub-jays (Aphelocoma californica) select a nut: effects of the number of options, variation in nut size, and social competition among foragers

Western scrub-jays (Aphelocoma californica) often visually assess and handle several whole (unshelled) peanuts before selecting one to transport and cache; this behavior is a search for a preferred heavy nut. I repeatedly video-taped individually identifiable jays as they landed on a feeding platform and chose from presentations of peanuts that varied in the number of items or in the distribution of sizes. I examined how differences among these presentations and a bird’s social status affected the amount of assessment and the economic consequences of choice. I also examined the specific patterns of handling peanuts, called sampling, to quantify the degree to which sampling sequences were typified by repeated comparisons among sampled peanuts (retrospective sampling), or sequential assessment and rejection of peanuts (prospective sampling). Peanut assessment was more extensive and prospective when there were many options from which to choose than when there were few. Peanut assessment was more extensive and retrospective when options were similar in size than when they varied. Scrub-jays were more likely to make repeated comparisons immediately before selecting a peanut than elsewhere in a sampling sequence. Subordinate scrub-jays, who were at the greatest risk of pre-emption by competitors, assessed peanuts less extensively and were more prospective in their sampling than dominants. Unless peanuts were very similar in size, jays were more accurate at selecting a high-quality peanut and achieved a higher rate of food storage than if they had not assessed. These results show that scrub-jays can adaptively modify how they search to improve their rate of food storage, and also suggest some of the specific search tactics used by jays when assessing peanuts. Received: 26 April 1999 / Accepted after revision: 10 October 1999     

Rhesus monkeys (Macaca mulatta) demonstrate robust memory for what and where,but not when,in an open-field test of memory

We adapted a paradigm developed by Clayton and Dickinson (1998), who demonstrated memory for what, where, and when in scrub jays, for use with rhesus monkeys. In the study phase of each trial, monkeys found a preferred and a less-preferred food reward in a trial-unique array of three locations in a large room. After 1 h, monkeys returned to the test room, where they found foods placed as during study. Twenty-five hours after the study phase monkeys again searched the room, but now the preferred food was replaced with a distasteful food remnant, while the less-preferred food was still present. Although monkeys remembered the locations of the foods for up to 25 h, they did not learn that the preferred food was available after the short, but not after the long delay. Thus, monkeys demonstrated long-term memory for the type and location of food but failed to demonstrate sensitivity to when they acquired that knowledge.     

Sun compass orientation in seed-caching corvids: its role in spatial memory

The role of sun compass orientation in spatial memory of Clark’s nutcrackers, Nucifraga columbiana, and pinyon jays, Gymnorhinus cyanocephalus, was studied in a series of cache recovery experiments. Birds were tested in an octagonal outdoor aviary with sand-filled cups inserted in the floor. For caching, only 12 such cups in a 90° sector were available, while for recovery 4–7 days later all 48 cups in the entire aviary were open. In control tests, the birds concentrated their search activity in the sector where they had cached. When their internal clock was shifted 6 h between caching and recovery, pinyon jays shifted their search activity to the 90° adjacent sector, as predicted if the sun compass was used. Clark’s nutcrackers did not respond to the first clock-shift; however, they, too, shifted their search activity after a second clock-shift back to normal. This suggests that the sun compass is a component of spatial memory in both species. Clark’s nutcrackers, however, seem to rely on their sun compass to a lesser degree than pinyon jays or the previously studied scrub jays. A comparison of the findings indicates that the role of the sun in spatial memory might reflect differences in habitat and ecology of the three corvid species. Received: 18 February 1999 / Accepted after revision: 17 September 1999     

Caching at a distance: a cache protection strategy in Eurasian jays

A fundamental question about the complexity of corvid social cognition is whether behaviours exhibited when caching in front of potential pilferers represent specific attempts to prevent cache loss (cache protection hypothesis) or whether they are by-products of other behaviours (by-product hypothesis). Here, we demonstrate that Eurasian jays preferentially cache at a distance when observed by conspecifics. This preference for a ‘far’ location could be either a by-product of a general preference for caching at that specific location regardless of the risk of cache loss or a by-product of a general preference to be far away from conspecifics due to low intra-species tolerance. Critically, we found that neither by-product account explains the jays’ behaviour: the preference for the ‘far’ location was not shown when caching in private or when eating in front of a conspecific. In line with the cache protection hypothesis we found that jays preferred the distant location only when caching in front of a conspecific. Thus, it seems likely that for Eurasian jays, caching at a distance from an observer is a specific cache protection strategy.     

Context effects on remembering and knowing: the expectancy heuristic

Three experiments are reported examining the effect of context on remember-know judgments. In Experiments 1 and 2, medium-frequency words were intermixed with high-frequency or low-frequency words at study or at test, respectively. Remember responses were greater for medium-frequency targets when they were studied or tested among high-frequency, as compared with low-frequency, words. The authors proposed a decision-based mechanism called "the expectancy heuristic" to explain why remember responses were more likely when items were studied or tested in the context of words that were relatively less distinct. According to the expectancy heuristic, when items on a recognition test exceed an expected level of memorability they will be given a remember judgment but when they do not, but are still more familiar than new words, they will be given a know judgment. Experiment 3, which varied expectancies about the strength of tested targets, demonstrated the use of the expectancy heuristic, indicating that it operates by selectively influencing the remember criterion rather than by influencing recollection of studied items.     

Early Stage Alzheimer's Disease Disrupts Encoding of Contextual Information

Two experiments examined whether impairments in recognition memory in early stage Alzheimer's disease (AD) were due to deficits in encoding contextual information. Normal elderly (NE) and patients diagnosed with mild stage AD learned one of two tasks. In Experiment 1 correct recognition memory required participants to remember not only what items they had experienced on a given trial but also when they had experienced them; Experiment 2 required that participants remember only what they had seen, not when they had seen it. Large recognition memory differences were found between the AD and NE groups in the experiment where time tagging was crucial for successful performance. An error analysis indicated that this was not due to the perseveration of previous learned responses. In Experiment 2, the only requisite for successful recognition was remembering what one had experienced; memory of the temporal record was not necessary for successful performance. In this instance, recognition memory for the NE and AD groups was identical. Taken together these results suggest that memory deficits found in early stage AD are partly due to impaired processing of contextual cues that provide crucial information about when events occur.     

Cognitive effort and recollective experience in recognition memory

The difficulty of the cognitive operations required to process study items was manipulated in two experiments investigating recollective experience. In subsequent recognition tests, subjects indicated whether their recognition judgements for items processed in these tasks were based on recollection ("remember" responses) or on familiarity ("know" responses). In Experiment 1 target items were presented in the context of a category decision task. It was found that remember responses increased with the difficulty of the category decision. For positive instances, remember responses were greater for items of low instance frequency than for items of high instance frequency, while for negative instances remember responses were greater for items from similar categories than for items from dissimilar categories. These effects were not present in know responses. In Experiment 2, remember responses were more frequent when study items had been presented in the form of anagrams to be solved than when they had been presented in the form of words to be read aloud. The incidence of know responses was not affected by the format in which study items were presented. Source judgements were also more accurate when recognition was based on recollection. It is argued that the type of conscious awareness experienced during recognition is determined by the knowledge activated by items presented in the recognition test, which in turn is determined by the nature of the operations engaged at encoding.     

Pilfering Eurasian jays use visual and acoustic information to locate caches

Pilfering corvids use observational spatial memory to accurately locate caches that they have seen another individual make. Accordingly, many corvid cache-protection strategies limit the transfer of visual information to potential thieves. Eurasian jays (Garrulus glandarius) employ strategies that reduce the amount of visual and auditory information that is available to competitors. Here, we test whether or not the jays recall and use both visual and auditory information when pilfering other birds’ caches. When jays had no visual or acoustic information about cache locations, the proportion of available caches that they found did not differ from the proportion expected if jays were searching at random. By contrast, after observing and listening to a conspecific caching in gravel or sand, jays located a greater proportion of caches, searched more frequently in the correct substrate type and searched in fewer empty locations to find the first cache than expected. After only listening to caching in gravel and sand, jays also found a larger proportion of caches and searched in the substrate type where they had heard caching take place more frequently than expected. These experiments demonstrate that Eurasian jays possess observational spatial memory and indicate that pilfering jays may gain information about cache location merely by listening to caching. This is the first evidence that a corvid may use recalled acoustic information to locate and pilfer caches.     

Remembrance of remembrance past

Arnold and Lindsay (2002) found that individuals more often failed to remember they had previously recalled an item if that item had been cued in a qualitatively different way on two recall occasions: the "forgot-it-all-along" (FIA) effect. Experiment 1 was designed to determine if the FIA effect arises because participants incorrectly believe they have not been previously tested for an item, or because they incorrectly believe they have failed to recall the item when previously tested. Experiment 2 measured participants' confidence in their incorrect prior-recall judgements, and Experiment 3 tested participants' ability to "recover" their previous recollection when the prior-recall context was restored. Results indicated that participants usually believed they had not previously been cued for the items they failed to remember previously recalling; they were often confident in their incorrect judgements of prior non-remembering; and re-introducing the context of prior remembering sometimes enabled them to recapture their memories of previous recall.     

Audience effects on food caching in grey squirrels (<Emphasis Type="Italic">Sciurus carolinensis</Emphasis>): evidence for pilferage avoidance strategies

If food pilferage has been a reliable selection pressure on food caching animals, those animals should have evolved the ability to protect their caches from pilferers. Evidence that animals protect their caches would support the argument that pilferage has been an important adaptive challenge. We observed naturally caching Eastern grey squirrels (Sciurus carolinensis) in order to determine whether they used any evasive tactics in order to deter conspecific and heterospecific pilferage. We found that grey squirrels used evasive tactics when they had a conspecific audience, but not when they had a heterospecific (corvid) audience. When other squirrels were present, grey squirrels spaced their caches farther apart and preferentially cached when oriented with their backs to other squirrels, but no such effect was found when birds were present. Our data provide the first evidence that caching mammals are sensitive to the risk of pilferage posed by an audience of conspecifics, and that they utilise evasive tactics that should help to minimise cache loss. We discuss our results in relation to recent theory of reciprocal pilferage and compare them to behaviours shown by caching birds.     

Gist-based memory for prices and “better buys” in younger and older adults

Ageing typically leads to various memory deficits which results in older adults’ tendency to remember more general information and rely on gist memory. The current study examined if younger and older adults could remember which of two comparable grocery items (e.g., two similar but different jams) was paired with a lower price (the “better buy”). Participants studied lists of grocery items and their prices, in which the two items in each category were presented consecutively (Experiment 1), or separated by intervening items (Experiment 2). At test, participants were asked to identify the “better buy” and recall the price of both items. There were negligible age-related differences for the “better buy” in Experiment 1, but age-related differences were present in Experiment 2 when there were greater memory demands involved in comparing the two items. Together, these findings suggest that when price information of two items can be evaluated and compared within a short period of time, older adults can form stable gist-based memory for prices, but that this is impaired with longer delays. We relate the findings to age-related changes in the use of gist and verbatim memory when remembering prices, as well as the associative deficit account of cognitive ageing.     

What–Where–When memory in magpies (Pica pica)

Some animals have been shown to be able to remember which type of food they hoarded or encountered in which location and how long ago (what–where–when memory). In this study, we test whether magpies (Pica pica) also show evidence of remembering these different aspects of a past episode. Magpies hid red- and blue-dyed pellets of scrambled eggs in a large tray containing wood shavings. They were allowed to make as many caches as they wanted. The birds were then returned either the same day or the next day to retrieve the pellets. If they returned the same day, one colour of pellets was replaced with wooden beads of similar size and colour, while if they returned the next day this would happen to the other colour. Over just a few trials, the birds learned to only search for the food pellets, and ignore the beads, of the appropriate colour for the given retention interval. A probe trial in which all items were removed showed that the birds persisted in searching for the pellets and not the beads. This shows that magpies can remember which food item they hoarded where, and when, even if the food items only differ from each other in their colour and are dispersed throughout a continuous caching substrate.     

A comparison of four corvid species in a working and reference memory task using a radial maze

Birds were tested in an open-room radial maze with learned spatial locations that varied from trial to trial (working memory) and locations that remained spatially stable (reference memory). Three of the species, the Clark's nutcracker (Nucifraga columbiana), pinyon jay (Gymnorhinus cyanocephalus), and Western scrub jay (Aphelocoma coerulescens) store food to varying degrees. The other species, the Eurasian jackdaw (Corvus monedula) does not. Pinyon jays and scrub jays performed better than the nutcrackers and jackdaws in both working and reference memory components of the maze. The pinyon jay and jackdaw performed as would be expected on the basis of their natural history and previous research, but the scrub jay and nutcracker did not. Results are consistent with phylogenetic relationships among the 4 species, but could also be explained by differences in response strategies or interference in processing both types of memory components of the maze.