Strategies of spatial learning for food storing in scrub jays

Western scrub jays (Aphelocoma californica) hide food and rely on spatial memory to recover their caches at a later date. To do this cache-and-recovery, they can use both spatial and site-specific cues. I examined these cues in an experimental setting. The experiment established that scrub jays, like other food storers, prefer to rely on the location of the caching tray rather than tray-specific cues. They could modify their preference for spatial cues through training in which spatial cues were made irrelevant. Even after such training, the spatial cues controlled the jays behaviour when the spatial and site-specific cues gave competitive information about the cached sites. Thus, the global spatial cues have priority but the jays use the local site-specific cues when the spatial cues do not give enough information about the cached site.     

Western scrub-jays conceal auditory information when competitors can hear but cannot see

Western scrub-jays (Aphelocoma californica) engage in a variety of cache-protection strategies to reduce the chances of cache theft by conspecifics. Many of these strategies revolve around reducing visual information to potential thieves. This study aimed to determine whether the jays also reduce auditory information during caching. Each jay was given the opportunity to cache food in two trays, one of which was filled with small pebbles that made considerable noise when cached in (‘noisy’ tray), whereas the other one contained soil that made little detectable noise when cached in (‘quiet’ tray). When the jays could be heard, but not seen, by a competitor, they cached proportionally less food items in the ‘noisy’ substrate than when they cached alone in the room, or when they could be seen and heard by competitors. These results suggest that western scrub-jays know when to conceal auditory information, namely when a competitor cannot see but can hear the caching event.     

The Effects of Social Context on the Food-Caching Behavior of Florida Scrub-Jays (Aphelocoma coerulescens)

Florida scrub‐jays are cooperative breeders that live in family groups consisting of a breeding pair, often with several non‐breeding helpers. Florida scrub‐jays cache food by scatter‐hoarding items for later consumption. Within family groups, members have the opportunity to observe and pilfer the caches of other members. We observed jays harvesting experimentally provisioned peanuts alone and in the presence of other family members, to determine whether jays modify their food‐handling behavior relative to social context. Non‐breeding helpers were less likely to cache in the presence of the dominant male breeder than when alone and all jays tended to cache out of sight when observed by another jay. These changes in caching behavior are consistent with cache protection strategies employed by other species. However, the adaptive value of such cache protection within a sedentary cooperatively breeding family group on a year‐round territory is unclear.     

Ontogeny of food-caching site preferences in young Florida Scrub-Jays: evidence of learning or changing social status?

Florida Scrub-Jays (Aphelocoma coerulescens) are cooperative breeders endemic to Florida’s oak scrub. In autumn, Florida Scrub-Jays cache thousands of acorns and exhibit behaviors that appear to balance cache site selection against food degradation or cache robbery. However, both experience and position within a social dominance hierarchy could affect individual cache preferences. We examined the cache site preferences of birds with differing levels of caching experience and at different strata within a complex social dominance hierarchy. Our objective was to determine how experience, social position, and social context when caching influenced microhabitat preferences, and if these change as jays age, gain experience, and their social position changes. Naïve first-year birds preferred to cache in well-hidden, densely vegetated sites with relatively high soil moisture content. Naïve birds also cached farther from provisioning points if observed by a socially dominant bird than when they were alone or in the presence of birds of equal social status. Experienced adults preferred to cache in open, dry sandy sites and social context at the time of caching did not influence their preferences. As naïve birds aged, they gained experience and their social position changed. Experienced second-year birds shifted their preference to more open, drier sites, and did so more often when they remained subordinate within their group rather than becoming dominant breeders. Second-year birds that remained subordinate did not alter their caching behavior if observed by dominant birds. These patterns suggest that after gaining experience, jays learned which sites were more appropriate for caching and shifted their preference, regardless of their changing social status. We suggest that the risk of cache loss to food degradation might be greater than the risk of pilfering for Florida Scrub-Jays, especially for birds in any social strata except the most subordinate, but this requires additional study.     

Mirror-mediated responses of California scrub jays (Aphelocoma californica) during a caching task and the mark test

Mirror self-recognition, as an index of self-awareness, has been proposed as a precursor for more complex social cognitive abilities, such as prosocial reasoning and cooperative decision-making. Indeed, evidence for mirror self-recognition has been shown for animals possessing complex social cognitive abilities such as great apes, dolphins, elephants and corvids. California scrub jays (Aphelocoma californica) have provided strong evidence that non-human animals are capable of mental state attribution. For instance, scrub jays are reported to use their experience stealing the food of others to infer that other birds may similarly intend to steal from them. If a concept of “self” is required for such complex social cognitive abilities, then scrub jays might be expected to show mirror self-recognition. Thus, we examined whether California scrub jays are capable of mirror self-recognition using two experimental contexts: a caching task and the mark test. During the caching task, we compared the extent to which scrub jays protected their food after caching alone, in the presence of a conspecific and in the presence of a mirror. The birds did not engage in more cache protection behaviours with a mirror present than when caching alone, suggesting scrub jays may have recognized their reflection and so did not expect cache theft. Alternative explanations for this behaviour are also discussed. During the mark test, the scrub jays were surreptitiously marked with a red or plumage-coloured control sticker. The scrub jays showed no evidence of mirror self-recognition during the mark test, as the birds did not preferentially attempt to remove the red mark in the presence of a mirror. Together, the results provide mixed evidence of the mirror self-recognition abilities of California scrub jays. We highlight the need to develop alternative approaches for evaluating mirror self-recognition in non-human animals to better understand its relationship with complex social cognition.     

Recaching Decisions of Florida Scrub‐Jays are Sensitive to Ecological Conditions

Food caching animals depend on their caches at times of low food availability. Because stored food is susceptible to being stolen or degraded, many species employ cache protection strategies such as ceasing caching in the presence of others or avoiding storing perishable items for long periods. Several species frequently recover their caches and recache, which may reduce pilferage or degradation of cached items. We studied the food handling decisions of Florida scrub‐jays (Aphelocoma coerulescens) after cache recovery to determine the roles that social and ecological environments play in post‐recovery decisions. Instead of reducing recaching in the presence of others, recovering jays flew away from the recovery site, allowing them to eat or recache a recovered item regardless of the social context. Microhabitat type and soil moisture of the recovery sites had a significant influence on whether recoveries were eaten or recached; most items that were recached had been recovered from bare sand sites or sites with low soil moisture. Taken together, our results suggest that food store management of Florida scrub‐jays are unaffected by the social context, but are strongly affected by the habitat conditions that influence the quality of caches.     

Motivational control of caching behaviour in the scrub jay, Aphelocoma coerulescens

We investigated the motivational control of caching behaviour in scrub jays using a two-stage procedure to examine the effects of prefeeding and/or precaching (stage 1) on subsequent caching behaviour (stage 2). Experiment 1 demonstrated that both prefeeding and precaching reduced the subsequent caching of both edible (peanuts) and inedible (stones) items. The reduction in caching was greatest when the items available for storing were the same in the two stages. This item specificity was confirmed in experiment 2 using two food types, peanuts and dog food kibbles. The final experiment demonstrated that the effect of prefeeding on subsequent caching can also be food specific, in that birds that received food in a powdered form that they could eat, but not cache in stage 1, showed a reduction in subsequent caching in stage 2 only when the food type was the same in the two stages. These results suggest that caching behaviour is controlled by both the feeding system and an independent caching system, and that this control is mediated by the incentive value of the specific items rather than by a general motivational state. Copyright 1999 The Association for the Study of Animal Behaviour.     

Does Seed‐Caching Experience Affect Spatial Memory Performance by Pinyon Jays?

Food‐storing birds use spatial memory to find previously cached food items. Throughout winter, pinyon jays (Gymnorhinus cyanocephalus) rely heavily on cached pinyon pine (Pinus edulis) seeds. Because of a recent severe drought, pinyon pine trees had not produced a significant seed crop for several years. Therefore, 1‐ and 2‐yr‐old birds never had the opportunity to cache and recover seeds and birds 4 or more years of age had not recovered seeds in 3 yr. This study examined whether natural but extreme variability in experience might result in differences in abstract spatial memory ability during a non‐cache recovery test of spatial memory. Three groups of jays were tested for spatial memory ability in an open room analog of the radial arm maze. Two of the groups were 8 mo old: young/minimally experienced birds which had 2 mo of experience in the wild, while young/experienced birds had 5 mo of experience in their natural habitat. The third group, adult, consisted of birds more than 3 yr old, with at least 3 yr of experience in their natural habitat. This was the only group with experience caching pine seeds. All three groups performed equally and well above chance. This suggests that spatial memory is fully developed by 8 mo of age and is not affected by extensive experience in the wild.     

Bolus recovery by gray jays: an experimental analysis

Gray jays (Perisoreus canadensis) typically store food boli in various sites on conifers. In a laboratory setting we determined whether gray jays recover stored boli by means of olfaction, trial-and-error search or spatial memory. Using an artificial tree with 52 possible caching sites, caching and/or recovery trials were performed with five captive gray jays for the following experiments: (1) no extra visual cues on tree; (2) extra visual cues (pine foliage) attached to tree; (3) pungent-smelling food hidden by observer; (4) one bird allowed to cache food but caches recovered by a second bird; (5) one bird allowed to observe another bird cache food and later permitted to recover those caches. Results supported the memory hypothesis, but cache site preferences were apparent for individual birds. To control for this, an additional experiment (6), in which cache site access was limited by the investigators, was conducted with two new birds. These results also indicated that gray jays use spatial memory to recover stored boli.     

Acorn dispersal by the blue jay (Cyanocitta cristata)

Summary Blue jays transported and cached 133,000 acorns from a stand of Quercus palustris trees in Blacksburg, Virginia, representing 54% of the total mast crop. A further 20% (49,000) of the mast crop was eaten by jays at the collecting site. A large proportion of the nuts remaining beneath the collecting trees was parasitized by curculionid larvae. The number of nuts transported per caching trip ranged from 1–5 with a mean of 2.2. Mean distance between seed trees and caches was 1.1 km (range: 100 m–1.9 km). Jays appeared to choose species with small- to medium-sized nuts (Quercus palustris, Q. phellos, Q. velutina, Fagus grandifolia) and avoided the larger nuts of Q. borealis and Q. alba.Nuts were cached singly within a few meters of each other and were always covered with debris. Covering may improve germination and early growth by protecting the nut and radicle from desiccation. The vegetation structure of most suburban caching sites was analogous to open, disturbed environments in more natural landscapes. The presence of numerous Quercus seedlings in jay caching sites and the tendency for jays to cache nuts in environments conducive to germination and early growth indicate that blue jays facilitate colonization of members of the Fagaceae.     

Species Differences in Spatial Memory Performance on a Three-dimensional Task

Three species of seed-caching corvids were tested in a spatial, three-dimensional analog of the radial maze. The apparatus consisted of five artificial trees, each with six branches. A wooden feeder could be attached to each branch. Each feeder contained a hole that could hold a pine seed. During the first 40 trials of acquisition testing, all three species improved rapidly with nutcrackers and pinyon jays performing at higher levels than scrub jays. Testing was then interrupted for 31 d. After the interruption, the two species of jays continued to improve but the nutcrackers did not. This species performed with only modest accuracy through the remainder of the experiment. Mixed-interval testing was done at 10, 60, 180, and 300 min. All species declined in accuracy with increased retention interval. However, at 10 and 180 min, pinyon jays performed significantly better than scrub jays. This is the fourth spatial memory task in which pinyon jays have out-performed scrub jays. The difference in performance between these two species provides more evidence for divergence in spatial cognition as a function of dependence on cached food.     

Dominance rank influences food hoarding in New Zealand Robins Petroica australis

Social interactions are thought to be an important determinant of food hoarding behaviour in birds. Theoretical work predicts that subordinate birds should cache more to offset losses to dominant birds. However, empirical support for this prediction is mixed. We evaluated whether social dominance influences the food hoarding behaviour of New Zealand Robins Petroica australis . Robins provide a unique opportunity to test food hoarding theory because they are fearless of humans and will cache food presented to them by hand. We offered mealworms to free-ranging male and female Robins to test whether (1) one sex was socially dominant, (2) the subordinate sex cached more frequently than the dominant sex and (3) birds cached more frequently when they were in the presence of a potential competitor. Our results indicate that males were dominant over females. Males acquired most of the prey offered to birds during trials and won all aggressive encounters observed between sexes. However, caching rates ran contrary to theoretical predictions. Males stored approximately twice as many mealworms as females. Both sexes also stored more food when they were alone than when they were accompanied by conspecifics. We interpret the reluctance of females and paired birds to hoard food as a strategy to avoid the loss of caches to competitors. Our overall results indicate that dominance rank strongly influences caching decisions, but that caching rates ran contrary to theoretical predictions.     

Cognitive representation in transitive inference: A comparison of four corvid species

During operant transitive inference experiments, subjects are trained on adjacent stimulus pairs in an implicit linear hierarchy in which responses to higher ranked stimuli are rewarded. Two contrasting forms of cognitive representation are often used to explain resulting choice behavior. Associative representation is based on memory for the reward history of each stimulus. Relational representation depends on memory for the context in which stimuli have been presented. Natural history characteristics that require accurate configural memory, such as social complexity or reliance on cached food, should tend to promote greater use of relational representation. To test this hypothesis, four corvid species with contrasting natural histories were trained on the transitive inference task: pinyon jays, Gymnorhinus cyanocephalus; Clark's nutcrackers, Nucifraga columbiana; azure-winged magpies, Cyanopica cyanus; and western scrub jays, Aphelocoma californica. A simplified computer model of associative representation displayed a characteristic pattern of accuracy as a function of position in the hierarchy. Analysis of the deviation of each subject's performance from this predicted pattern yielded an index of reliance on relational representation. Regression of index scores against rankings of social complexity and caching reliance indicated that both traits were significantly and independently associated with greater use of relational representation.     

Corvid re-caching without 'theory of mind': a model

Scrub jays are thought to use many tactics to protect their caches. For instance, they predominantly bury food far away from conspecifics, and if they must cache while being watched, they often re-cache their worms later, once they are in private. Two explanations have been offered for such observations, and they are intensely debated. First, the birds may reason about their competitors' mental states, with a 'theory of mind'; alternatively, they may apply behavioral rules learned in daily life. Although this second hypothesis is cognitively simpler, it does seem to require a different, ad-hoc behavioral rule for every caching and re-caching pattern exhibited by the birds. Our new theory avoids this drawback by explaining a large variety of patterns as side-effects of stress and the resulting memory errors. Inspired by experimental data, we assume that re-caching is not motivated by a deliberate effort to safeguard specific caches from theft, but by a general desire to cache more. This desire is brought on by stress, which is determined by the presence and dominance of onlookers, and by unsuccessful recovery attempts. We study this theory in two experiments similar to those done with real birds with a kind of 'virtual bird', whose behavior depends on a set of basic assumptions about corvid cognition, and a well-established model of human memory. Our results show that the 'virtual bird' acts as the real birds did; its re-caching reflects whether it has been watched, how dominant its onlooker was, and how close to that onlooker it has cached. This happens even though it cannot attribute mental states, and it has only a single behavioral rule assumed to be previously learned. Thus, our simulations indicate that corvid re-caching can be explained without sophisticated social cognition. Given our specific predictions, our theory can easily be tested empirically.     

Observational visuospatial encoding of the cache locations of others by western scrub-jays (<Emphasis Type="Italic">Aphelocoma californica</Emphasis>)

Western scrub-jays (Aphelocoma californica) hide food and rely on spatial memory to recover their caches at a later date. They also rely on observational spatial memory to steal caches made by other individuals. Successful pilfering may require an understanding of allocentric space because the observer will often be in a different position from the demonstrator when the caching event occurs. We compared cache recovery accuracy of pairs of observers that watched a demonstrator cache food. The pattern of recovery searches showed that observers were more accurate when they had observed the caching event from the same viewing direction as the demonstrator than when they had watched from the opposite direction. Search accuracy was not affected by whether or not the tray-specific local cues provided left–right landmark information (i.e. heterogeneous vs. homogeneous local cues), or whether or not the caching tray location was rotated. Taken together, these results suggest that observers have excellent spatial memory and that they have little difficulty with mental rotation.     

Social cognition by food-caching corvids. The western scrub-jay as a natural psychologist

Food-caching corvids hide food, but such caches are susceptible to pilfering by other individuals. Consequently, the birds use several counter strategies to protect their caches from theft, e.g. hiding most of them out of sight. When observed by potential pilferers at the time of caching, experienced jays that have been thieves themselves, take further protective action. Once the potential pilferers have left, they move caches those birds have seen, re-hiding them in new places. Naive birds that had no thieving experience do not do so. By focusing on the counter strategies of the cacher when previously observed by a potential pilferer, these results raise the intriguing possibility that re-caching is based on a form of mental attribution, namely the simulation of another bird's viewpoint. Furthermore, the jays also keep track of the observer which was watching when they cached and take protective action accordingly, thus suggesting that they may also be aware of others' knowledge states.     

Animal memory: episodic-like memory in rats

Recent experiments with rats on a radial maze indicate that they can remember what foods they encountered, and when and where they encountered them. These findings, and others with food-storing birds, challenge the idea that only humans have episodic memory.     

Are Cape Ground Squirrels (Xerus inauris) Sensitive to Variation in the Pay‐offs from Their Caches?

For food caching to be adaptive, the benefits of recovery must outweigh the costs of storing an item. One of the costs to cachers is the risk of theft, and therefore, it is predicted that individuals may be sensitive to this theft and show various behavioural strategies to minimise it. In this study, we gave wild Cape ground squirrels (Xerus inauris) a choice between two different coloured items of the same food type: one item with a specific colour that was always artificially removed when cached and the other item with a different colour that was not removed when cached. During the choice presentations, subjects reduced the amount they consumed and cached of the food items with the colour that was experimentally removed when cached, despite the two items only differing in caching pay‐off. This avoidance to choose the food with the colour that was removed occurred over time, which suggests that subjects were using information about the item's pay‐off during cache recovery and this then impacted on successive decisions. This study highlights how the sensitivity to a food item's pay‐off can affect an individual's choice towards items that offer the greater overall reward.     

Causes and consequences of pre‐laying weight gain in a food‐caching bird that breeds in late winter

Animals that reside at high latitudes and altitudes year‐round often use cached food to survive over the winter months, but a few species also rely on stored food to sustain them during the breeding season when the nutritional requirements of females are higher than normal. Gray jays Perisoreus canadensis rely on perishable cached food during the winter and females begin breeding in late winter when fresh food is rarely available. To examine pre‐laying patterns of weight gain, as well as the causes and consequences of weight gain among individuals, we weighed females regularly throughout the pre‐laying period. Females began increasing their weight approximately nine days prior to their first egg date, and on average increased their body weight by 25%, which is on par with other bird species that rely on non‐cached food. Final pre‐laying weight was positively influenced by the percent of conifers on territories, providing some support for previous results showing that coniferous trees are better able to preserve cached food. We also found that both final pre‐laying weight and the rate of weight gain were positively related to female age, supporting the hypothesis that female caching ability improves with age. With increasing final weight, females tended to lay larger clutches and hatched more nestlings, despite the fact that final weight was not influenced by weight at the beginning of the weighing period. Our results confirm that gray jays are able to reach breeding condition while relying primarily on food stored before winter, and suggest a novel mechanism by which habitat‐mediated carry‐over effects and female age may influence reproductive performance in a food‐caching animal.     

Sun compass orientation in seed-caching scrub jays (Aphelocoma coerulescens)

Summary In their natural environment, scrub jays harvest pinyon pine seeds and store them in subterranean caches. In our tests, the birds performed this behavior 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 the recovery session 4 to 6 days later all 48 cups in the entire aviary were open. In control tests, the birds concentrated their search in the sector where the seeds had been cached. When the internal clock of the birds was shifted 6 h between caching and recovery, they preferentially probed in the adjacent 90° sector. This indicated that they used sun compass information to relocate their caches, largely ignoring visual cues from surrounding landmarks.The dominant role of the sun compass which has a parallel in the orientation of homing pigeons, may reflect a general tendency to prefer compass information in spatial orientation tasks; it is in agreement with the model that birds generally have a directionally oriented view of space.Abbreviations OR Original caches - SH shifted caches