Scrub jays (Aphelocoma coerulescens) remember the relative time of caching as well as the location and content of their caches

Two experiments examined whether food-storing scrub jays (Aphelocoma coerulescens) could remember when they cached particular food items as well as what they cached and where. In Experiment 1, scrub jays cached and recovered perishable "wax worms" (wax moth larvae) and nonperishable peanuts in 2 visuospatially distinct and trial-unique trays. The birds searched preferentially for fresh wax worms if they had cached them 4 hr earlier but rapidly learned to search for peanuts and avoid decayed wax worms that had been cached 124 hr previously. This pattern also was observed when the food items were removed before recovery on test trials. These results were replicated in Experiment 2 using a procedure in which both types of food were cached in different sides of the same caching tray: On the basis of a single, trial-unique experience, scrub jays could remember the relative time of caching as well as what type of food was cached in each cache site.     

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.     

Corvid caching: Insights from a cognitive model

Caching and recovery of food by corvids is well-studied, but some ambiguous results remain. To help clarify these, we built a computational cognitive model. It is inspired by similar models built for humans, and it assumes that memory strength depends on frequency and recency of use. We compared our model's behavior to that of real birds in previously published experiments. Our model successfully replicated the outcomes of two experiments on recovery behavior and two experiments on cache site choice. Our "virtual birds" reproduced declines in recovery accuracy across sessions, revisits to previously emptied cache sites, a lack of correlation between caching and recovery order, and a preference for caching in safe locations. The model also produced two new explanations. First, that Clark's nutcrackers may become less accurate as recovery progresses not because of differential memory for different cache sites, as was once assumed, but because of chance effects. And second, that Western scrub jays may choose their cache sites not on the basis of negative recovery experiences only, as was previously thought, but on the basis of positive recovery experiences instead. Alternatively, both "punishment" and "reward" may be playing a role. We conclude with a set of new insights, a testable prediction, and directions for future work.     

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     

Interacting Cache memories: evidence for flexible memory use by Western Scrub-Jays (Aphelocoma californica)

When Western Scrub-Jays (Aphelocoma californica) cached and recovered perishable crickets, N. S. Clayton, K. S. Yu, and A. Dickinson (2001) reported that the jays rapidly learned to search for fresh crickets after a 1-day retention interval (RI) between caching and recovery but to avoid searching for perished crickets after a 4-day RI. In the present experiments, the jays generalized their search preference for crickets to intermediate RIs and used novel information about the rate of decay of crickets presented during the RI to reverse these search preferences at recovery. The authors interpret this reversal as evidence that the birds can integrate information about the caching episode with new information presented during the RI.     

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.     

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.     

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.     

The effects of cache modification on food caching and retrieval behavior by rats

Rats cached pieces of cheese on four different arms of an eight-arm radial maze. On a retrieval test given 45 min later, rats learned to return to arms where food was cached before arms where food had not been cached. Tests were then performed in which cache sites on one side of the maze were always modified (pilfered or degraded), but cache sites on the other side of the maze were left intact. In all of these tests, it was found over repeated trials that rats continued to distribute cached food equally between the two sides of the maze. Measures of the order in which arms were visited showed no caching preference but a preference in food retrieval for the side of the maze where food caches were not altered. These findings suggest that rats’ caching behavior is not affected by its consequences.     

Memory development in the second year: for events or locations?

We employed an object-placement/object-removal design, inspired by recent work on 'episodic-like' memory in scrub jays (Clayton, N. S., & Dickinson, A. (1998). Episodic-like memory during cache recovery by scrub jays. Nature, 395, 272-274), to examine the possibility that children in the second year of life have event-based memories. In one task, a successful search could have been due to the recall of an object-removal event. In the second task, a successful search could only have been caused by recall of where objects were located. Success was general in the oldest group of children (21-25 months), while performance was broadly similar on the two tasks. The parsimonious interpretation of this outcome is that the first task was performed by location memory, not by event memory. We place these data in the context of object permanence development.     

Do Clark’s nutcrackers demonstrate what-where-when memory on a cache-recovery task?

What-where-when (WWW) memory during cache recovery was investigated in six Clark’s nutcrackers. During caching, both red- and blue-colored pine seeds were cached by the birds in holes filled with sand. Either a short (3 day) retention interval (RI) or a long (9 day) RI was followed by a recovery session during which caches were replaced with either a single seed or wooden bead depending upon the color of the cache and length of the retention interval. Knowledge of what was in the cache (seed or bead), where it was located, and when the cache had been made (3 or 9 days ago) were the three WWW memory components under investigation. Birds recovered items (bead or seed) at above chance levels, demonstrating accurate spatial memory. They also recovered seeds more than beads after the long RI, but not after the short RI, when they recovered seeds and beads equally often. The differential recovery after the long RI demonstrates that nutcrackers may have the capacity for WWW memory during this task, but it is not clear why it was influenced by RI duration.     

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.     

Hiding and searching strategies of adult humans in a virtual and a real-space room

Adults searched for or cached three objects in nine hiding locations in a virtual room or a real-space room. In both rooms, the locations selected by participants differed systematically between searching and hiding. Specifically, participants moved farther from origin and dispersed their choices more when hiding objects than when searching for hidden objects. In addition, in both virtual and real-space rooms, prior experience in the hiding task increased the distance participants traveled from origin and the dispersion of their choices during searching. Furthermore, gender differences appeared in the virtual room but not in the real-space room. Specifically, during hiding females travelled farther from origin than males and during searching they dispersed their choices more than males. Overall, the results suggest that strategies used by adult humans for searching and caching are consistent with those seen in non-human animals and children.     

Food caching in captive coyotes: stereotypy of action sequence and spatial distribution of cache sites

This paper describes some aspects of the food caching behaviour of four captive coyotes. Detailed observations of the actions used by coyotes to cache food revealed them to be strikingly similar to those previously described for timber wolves. The similarities included the identity of the movements used, their temporal sequencing, and their susceptibility to interruption. This suggests that there exists a stereotypy across canids in the action sequences used in caching. Second, an examination of the distribution of cache sites revealed that each coyote scattered cache sites widely within a wooded region of their enclosure and preferentially in terrains close to exposed tree roots.     

Serial reversal learning and the evolution of behavioral flexibility in three species of North American corvids (Gymnorhinus cyanocephalus, Nucifraga columbiana, Aphelocoma californica)

In serial reversal learning, subjects learn to respond differentially to 2 stimuli. When the task is fully acquired, reward contingencies are reversed, requiring the subject to relearn the altered associations. This alternation of acquisition and reversal can be repeated many times, and the ability of a species to adapt to this regimen has been considered as an indication of behavioral flexibility. Serial reversal learning of 2-choice discriminations was contrasted in 3 related species of North American corvids: pinyon jays (Gymnorhinus cyanocephalus), which are highly social; Clark's nutcrackers (Nucifraga columbiana), which are relatively solitary but specialized for spatial memory; and western scrub jays (Aphelocoma californica), which are ecological generalists. Pinyon jays displayed significantly lower error rates than did nutcrackers or scrub jays after reversal of reward contingencies for both spatial and color stimuli. The effect was most apparent in the 1st session following each reversal and did not reflect species differences in the rate of initial discrimination learning. All 3 species improved their performance over successive reversals and showed significant transfer between color and spatial tasks, suggesting a generalized learning strategy. The results are consistent with an evolutionary association between behavioral flexibility and social complexity.     

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.     

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.     

Mental time travel in animals?

Are humans alone in their ability to reminisce about the past and imagine the future? Recent evidence suggests that food-storing birds (scrub jays) have access to information about what they have stored where and when. This has raised the possibility of mental time travel (MTT) in animals and sparked similar research with other species. Here we caution that such data do not provide convincing evidence for MTT. Examination of characteristics of human MTT (e.g. non-verbal declaration, generativity, developmental prerequisites) points to other avenues as to how a case for animal MTT could be made. In light of the current lack of evidence, however, we maintain that MTT is a uniquely human characteristic.