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.     

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.     

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.     

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.     

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.     

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.     

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.     

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.     

An apparatus for studying operant activity of captive coyotes

We describe a portable apparatus designed to examine the free-operant food preferences of captive coyotes in their home kennels. Because leverpressing for food access was the dependent variable, we measured food preference independently of food ingestion. Using successive approximation, we trained 8 out of 19 coyotes (42%) to use the apparatus. This percentage is similar to training rates for dogs. We used fixed and variable ratio schedules of reinforcement to further test 4 of the trained coyotes. All 4 produced response curves similar to those of other species on similar schedules of reinforcement.     

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.     

Cache decision making: the effects of competition on cache decisions in Merriam's kangaroo rat (Dipodomys merriami)

Caching food is an economic, decision-making process that requires animals to take many factors into account, including the risk of pilferage. However, little is known about how food-storing animals determine the risk of pilferage. In this study, the authors examined the effect of a dominant competitor species on the caching and behavior of Merriam's kangaroo rat (Dipodomys merriami). The authors found that, as with conspecific competitors, kangaroo rats did not alter caching in response to the mere presence of a heterospecific competitor, but moved caches to an unpreferred area when the competitor's presence was paired with pilferage. These data suggest that Merriam's kangaroo rat assesses pilfer risk from actual pilferage by a competitor and adaptively alters cache strategy to minimize future risk.     

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.     

Effects of novelty and familiarity on illness-induced aversions to food and place cues in coyotes (Canis latrans)

Two experiments investigated the effects of novelty and familiarity on illness-induced aversions to taste and place cues in coyotes (Canis latrans). Coyotes were made ill on familiar food laced with lithium chloride in a novel place and then received preference tests. In Experiment 1, coyotes avoided the previously poisoned familiar food in the novel treatment place but readily ate the same familiar food in a familiar safe place. In Experiment 2, the results of Experiment 1 were replicated, and it was found that coyotes would eat a different familiar food in the novel treatment place. On the basis of the results of this and other studies, a model for averting animals from places where they are not wanted is presented.     

Cache protection strategies of a non-social food-caching corvid,Clark’s nutcracker (<Emphasis Type="Italic">Nucifraga</Emphasis><Emphasis Type="Italic">columbiana</Emphasis>)

Clark’s nutcrackers (Nucifraga columbiana), a non-social corvid, cache much of their food in order to survive periods of resource uncertainty. These caches are at risk as they are subject to pilferage from other animals including conspecifics. Potentially, nutcrackers can ensure the safety of these caches by keeping track of whether they have been observed making a cache and subsequently engage in cache protection strategies—strategies that have been shown by other members of the corvid family (e.g., scrub-jays and ravens). Behaviors including creating more caches, eating a higher proportion of seeds, and re-caching existing compromised sites have been shown in laboratory settings with social corvids and have provided preliminary evidence of the complex cognitive abilities of corvids. In the present study, Clark’s nutcrackers are shown to engage in similar cache protection behaviors when observed by a conspecific. Furthermore, we show that these behaviors are a result of social, rather than associative, cues.     

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     

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.     

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.     

Short-term observational spatial memory in Jackdaws (<Emphasis Type="Italic">Corvus monedula</Emphasis>) and Ravens (<Emphasis Type="Italic">Corvus corax</Emphasis>)

Observational spatial memory (OSM) refers to the ability of remembering food caches made by other individuals, enabling observers to find and pilfer the others' caches. Within birds, OSM has only been demonstrated in corvids, with more social species such as Mexican jays (Aphelocoma ultramarine) showing a higher accuracy of finding conspecific' caches than less social species such as Clark's nutcrackers (Nucifraga columbiana). However, socially dynamic corvids such as ravens (Corvus corax) are capable of sophisticated pilfering manoeuvres based on OSM. We here compared the performance of ravens and jackdaws (Corvus monedula) in a short-term OSM task. In contrast to ravens, jackdaws are socially cohesive but hardly cache and compete over food caches. Birds had to recover food pieces after watching a human experimenter hiding them in 2, 4 or 6 out of 10 possible locations. Results showed that for tests with two, four and six caches, ravens performed more accurately than expected by chance whereas jackdaws did not. Moreover, ravens made fewer re-visits to already inspected cache sites than jackdaws. These findings suggest that the development of observational spatial memory skills is linked with the species' reliance on food caches rather than with a social life style per se.     

Pilfering ravens, Corvus corax, adjust their behaviour to social context and identity of competitors

Like other corvids, food-storing ravens protect their caches from being pilfered by conspecifics by means of aggression and by re-caching. In the wild and in captivity, potential pilferers rarely approach caches until the storers have left the cache vicinity. When storers are experimentally prevented from leaving, pilferers first search at places other than the cache sites. These behaviours raise the possibility that ravens are capable of withholding intentions and providing false information to avoid provoking the storers' aggression for cache protection. Alternatively, birds may refrain from pilfering to avoid conflicts with dominants. Here we examined whether ravens adjust their pilfer tactics according to social context and type of competitors. We allowed birds that had witnessed a conspecific making caches to pilfer those caches either in private, together with the storer, or together with a conspecific bystander that had not created the caches (non-storer) but had seen them being made. Compared to in-private trials, ravens delayed approaching the caches only in the presence of storers. Furthermore, they quickly engaged in searching away from the caches when together with dominant storers but directly approached the caches when together with dominant non-storers. These findings demonstrate that ravens selectively alter their pilfer behaviour with those individuals that are likely to defend the caches (storers) and support the interpretation that they are deceptively manipulating the others' behaviour.This contribution is part of the special issue “Animal Logics” (Watanabe and Huber 2006).     

Foraging behaviour in domestic pigs (Sus scrofa): remembering and prioritizing food sites of different value

This experiment investigated whether domestic pigs can remember the locations of food sites of different relative value, and how a restricted retrieval choice affects their foraging behaviour. Nine juvenile female pigs were trained to relocate two food sites out of a possible eight in a spatial memory task. The two baited sites contained different amounts of food and an obstacle was added to the smaller amount to increase handling time. On each trial, a pig searched for the two baited sites (search visit). Once it had found and eaten the bait, it returned for a second (relocation) visit, in which the two same sites were baited. Baited sites were changed between trials. All subjects learnt the task. When allowed to retrieve both baits, the subjects showed no preference for retrieving a particular one first (experiment 1). When they were allowed to retrieve only one bait, a significant overall preference for retrieving the larger amount emerged across subjects (experiment 2). To test whether this preference reflected an avoidance of the obstacle with the smaller bait, 15 choice-restricted control trials were conducted. In control trials obstacles were present with both baits. Pigs continued to retrieve the larger bait, indicating they had discriminated between the two food sites on the basis of quantity or profitability and adjusted their behaviour accordingly when the relocation choice was restricted. This suggests for the first time that domestic pigs have the ability to discriminate between food sites of different relative value and to remember their respective locations.