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.     

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.     

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.     

Elements of episodic-like memory in animals

A number of psychologists have suggested that episodic memory is a uniquely human phenomenon and, until recently, there was little evidence that animals could recall a unique past experience and respond appropriately. Experiments on food-caching memory in scrub jays question this assumption. On the basis of a single caching episode, scrub jays can remember when and where they cached a variety of foods that differ in the rate at which they degrade, in a way that is inexplicable by relative familiarity. They can update their memory of the contents of a cache depending on whether or not they have emptied the cache site, and can also remember where another bird has hidden caches, suggesting that they encode rich representations of the caching event. They make temporal generalizations about when perishable items should degrade and also remember the relative time since caching when the same food is cached in distinct sites at different times. These results show that jays form integrated memories for the location, content and time of caching. This memory capability fulfils Tulving's behavioural criteria for episodic memory and is thus termed 'episodic-like'. We suggest that several features of episodic memory may not be unique to humans.     

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.     

Seed hoarding by rodents of the Monte Desert,Argentina

Food storage is an important adaptation of several animal species to the temporally variable or unpredictable food supplies that are typical of desert environments. In the present study, whether Eligmodontia typus and Graomys griseoflavus inhabiting sand dunes in the Monte desert displayed scatter‐hoarding was investigated. Both rodent species prepared surface caches by digging small holes (1–3 cm deep) in the soil. Caches were partially covered with sand and dry leaves, which meant that all of the cache sites at each station could be found. Most caches were found below shrubs, that is, in a sheltered microhabitat rather than near the food source. The mean distance between caches and seed sources was significantly higher than the mean distance from food sources to shrubs. The proportion of caches was significantly higher in shrubs with high safety cover. The adaptive significance of this foraging behaviour could be a competitive tactic for the rapid sequestering of food from a rich and ephemeral source. Such behaviour would reflect predation risk, which constitutes an important foraging cost in deserts, and could also influence plant community dynamics.     

Causes and consequences of variation in diet composition of nestling Canada jays

Diet quality during development can impact growth, physiology, behaviour and survival. The Canada jay is a resident boreal passerine that caches a wide variety of perishable food items in late summer and autumn for its over‐winter survival and late‐winter reproduction. A previous experiment found evidence that food supplementation of Canada jay pairs during the nestling period had a positive effect on the condition of their nestlings. However, given that foods cached by adults vary widely in nutritional content, the composition of nestling diets could also have an important influence on offspring development. In a population of Canada jays in Algonquin Provincial Park, Ontario, Canada, we investigated the influence of environmental conditions before and during the breeding season on nestling diet composition and the consequences of nestling diet composition on the body condition of nestlings and on their subsequent survival. Using stable‐carbon (δ¹³C) and ‐nitrogen (δ¹⁵N) isotopes, we estimated the proportion of three food groups (vertebrates + human food, invertebrates and plants) in feathers from almost 200 nestlings. Nestling diet in March and April was influenced by environmental conditions 5–6 months prior to hatching, with warmer and more variable autumn temperatures associated with a greater proportion of vertebrate flesh and human food in the diet. However, the proportion of vertebrates and human food in the diet had no influence on nestling body condition or whether an individual was observed the following fall. Our results, in conjunction with previous work on Canada jays, suggest that the quantity of food available to a nestling during development may be more important than diet composition.     

Reduced reproductive performance associated with warmer ambient temperatures during incubation in a winter‐breeding,food‐storing passerine

Timing of reproduction can influence individual fitness whereby early breeders tend to have higher reproductive success than late breeders. However, the fitness consequences of timing of breeding may also be influenced by environmental conditions after the commencement of breeding. We tested whether ambient temperatures during the incubation and early nestling periods modulated the effect of laying date on brood size and dominant juvenile survival in gray jays (Perisoreus canadensis), a sedentary boreal species whose late winter nesting depends, in part, on caches of perishable food. Previous evidence has suggested that warmer temperatures degrade the quality of these food hoards, and we asked whether warmer ambient temperatures during the incubation and early nestling periods would be associated with smaller brood sizes and lower summer survival of dominant juveniles. We used 38 years of data from a range‐edge population of gray jays in Algonquin Provincial Park, Ontario, where the population has declined over 50% since the study began. Consistent with the “hoard‐rot” hypothesis, we found that cold temperatures during incubation were associated with larger brood sizes in later breeding attempts, but temperatures had little effect on brood size for females breeding early in the season. This is the first evidence that laying date and temperature during incubation interactively influence brood size in any bird species. We did not find evidence that ambient temperatures during the incubation period or early part of the nestling period influenced summer survival of dominant juveniles. Our findings provide evidence that warming temperatures are associated with some aspects of reduced reproductive performance in a species that is reliant on cold temperatures to store perishable food caches, some of which are later consumed during the reproductive period.     

Memory for food caches: not just for retrieval

Many animals use hoarding as a long-term strategy to ensurea food supply at times of shortage. Hoarders employ strategiesthat enhance their ability to relocate caches such as rememberingwhere caches are located. Long-term scatterhoarders, whose cacheshave potentially high pilferage rates, should also hoard ina way to reduce potential cache pilferers' ability to find caches.Previous studies have demonstrated that this could be achievedby hyperdispersing caches to reduce the foraging efficiencyof pilferers. This study investigates whether coal tits (Parusater) indeed place their caches away from existing ones. Inour experiment, birds hoarded food in 3 conditions: when cachesfrom a previous storage session were still present, when cachesfrom a previous storage session were not present anymore becausethe bird had retrieved them, and when caches from a previousstorage session had been removed by the experimenter. We showthat coal tits hoard away from existing caches and that theydo not use cues from extant caches to do this. This evidenceis consistent with the use of memory for the locations of previouscaches when deciding where to place new caches. This findinghas important implications for our understanding of the selectivepressures that have shaped spatial memory in food-hoarding birds.     

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.     

Food storage by black-capped chickadees: Memory for the location and contents of caches

Black-capped chickadees (Parus atricapillus) store food in a scattered distribution in their winter home range. Several hundred food items may be stored in a day, each in a separate cache site. Previous studies of marsh tits (Parus palustris) and nutcrackers (Nucifraga spp.) have shown that spatial memory is used to relocate caches. Memory for storage sites, if used by black-capped chickadees, is predicted to have four properties. Birds should be able to: (1) accurately relocate cache sites, (2) recall which caches they have previously emptied, (3) recall which sites they have discovered empty (as a result of loss to other animals) and (4) recall what type of food is stored at a cache site. Laboratory experiments show that chickadees do incorporate these kinds of information in memory for cache sites.     

Mechanisms of cache retrieval in long-term hoarding birds

Food hoarding and memory have primarily been studied in two bird families, the Corvidae (crows, jays, nutcrackers, etc.) and the Paridae (tits, titmice and chickadees). In both families there are species that hoard large quantities of seeds and nuts in the autumn and depend on these stores during the winter. Caches are concealed or highly inconspicuous and the most efficient way to retrieve them is to remember the exact locations. However, a long-term memory for a large number of caches may be physiologically expensive, and especially after long retention intervals, an alternative strategy could be to retrieve caches by cheaper but less efficient methods. Very few studies have been designed to investigate the decay of the memory in birds, but both field observations and experiments point in the same direction: although long-term hoarding corvids seem to possess an accurate long-term memory, long-term hoarding parids do not appear to. I discuss possible reasons for this and suggest that differences between the families in their degree of dependence on stored food or/and size-related limitations of brain capacity may be important.     

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.     

Management of fat reserves and food caches in tufted titmice (Parus bicolor) in relation to unpredictable food supply

In the temperate zone, permanent-resident birds and mammalsthat do not hibernate must survive harsh winter conditions oflow ambient temperature, long nights, and reduced food levels.To understand the energy management strategy of food-hoardingbirds, it has been hypothesized that such birds respond to increasedstarvation risk by increasing the number of their hoards ratherthan by increasing their fat reserves and that they cache earlyin the day and retrieve their caches later to achieve fat reservesnecessary to survive the night We tested these hypotheses byobserving the responses in captivity of a caching bird, thetufted titmouse (Parus bicolor), to the combined influencesof reduced predictability of food and naturally occurring ambienttemperature and photoperiod. When the food supply was unpredictable,birds significantly increased both internal fat reserves atdusk and external food caches. Initially leaner birds tendedto increase their fat reserves to a greater extent and initiallyfatter birds tended to cache more food and to fly significantlyless. Half the birds also increased their dawn and mean dailybody mass. All birds tended to forage, gain body mass, and cachefood at significantly lower rates in the morning and at significantlyhigher rates in the evening. Cache retrieval showed the oppositetrend, with birds retrieving most of their caches in the morning.Our results do not support the hypothesis that caching birdsincrease caching rate but not body mass under an unpredictablefood regime. Instead fat reserves and food caches are both importantcomplementary sources of energy in food-hoarding birds. Energymanagement by wintering birds occurs in response to a numberof biotic and abiotic factors acting simultaneously; thus futuremodels must incorporate independent variables in addition tothe state of the food supply and time of day     

Florida Scrub-Jays (Aphelocoma coerulescens) are Sentinels More When Well-Fed (Even with no Kin Nearby)

Sentinels occupy high, exposed positions while other group members forage nearby. If sentinel behavior involves a foraging–predation risk trade‐off, animals should be sentinels more when fed supplemental food. When individual Florida scrub‐jays (Aphelocoma coerulescens) were fed fragments of peanuts, during the following 30 min they shifted 30% of their time from foraging to sentinel behavior. In a follow‐up experiment, we fed either one or two members in each group. As before, the jays reduced their foraging and spent much more time as sentinels when given supplemental food. In each treatment, pairs were sentinels simultaneously considerably less often than expected by chance. The dramatic shift from foraging to sentinel behavior suggests that for Florida scrub‐jays sentinel behavior brings substantial benefits for no greater cost than that of lost opportunities to forage. Because the results held for simple mated pairs of scrub‐jays, we argue that kin selection and social prestige are not necessary to explain sentinel behavior.     

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.     

Ravens judge competitors through experience with play caching

Complex social behavior builds on the mutual judgment of individuals as cooperation partners and competitors [1]. Play can be used for assessing the others' dispositions in humans and nonhuman mammals [2], whereas little is known about birds. Recently, food-caching corvids have been found to rival primates in their ability to judge the behaviors and intentions of others in competition for hidden food [3]. Here, we show that ravens Corvus corax quickly learn to assess the competitive strategies of unfamiliar individuals through interactions with them over caches with inedible items and subsequently apply this knowledge when caching food. We confronted birds with two human experimenters who acted differently when birds cached plastic items: the pilferer stole the cached objects, whereas the onlooker did not. Birds responded to the actions of both experimenters with changing the location of their next object caches, either away from or toward the humans, as if they were testing their pilfering dispositions. In contrast, ravens instantly modified their caching behavior with food, preventing only the competitive human from finding the caches. Playful object caching in a social setting could thus aid ravens in evaluating others' pilfering skills.     

Observational learning and the raiding of food caches in ravens, Corvus corax: is it ‘tactical’ deception?

Group-foraging ravens scatter-hoard when they are competing for food and, to some extent, also raid the caches made by others. We investigated the effects of observational spatial memory on individual caching and raiding tactics. With captive ravens, we found visual observation was essential for locating and raiding the caches of conspecifics. Both captive and free-ranging ravens, food cachers as well as potential cache raiders, responded to each other's presence. Cachers withdrew from conspecifics and most often placed their caches behind structures, obstructing the view of potential observers. Raiders watched inconspicuously and kept at a distance to cachers close to their cache sites. In response to the presence of potential raiders or because of their initial movements towards caches, the cachers frequently interrupted caching, changed cache sites, or recovered their food items. These results suggest that ravens, regardless of whether they act as cachers or raiders, are capable of withholding information about their intentions and, hence, manipulate the other bird's attention either to prevent or to achieve social-learning opportunities. Such interactions may qualify as ‘tactical’ deception and may have created a considerable pressure selecting for social cognition in ravens. Copyright 2002 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.     

Experimental evidence for a novel mechanism driving variation in habitat quality in a food-caching bird

Variation in habitat quality can have important consequences for fitness and population dynamics. For food-caching species, a critical determinant of habitat quality is normally the density of storable food, but it is also possible that quality is driven by the ability of habitats to preserve food items. The food-caching gray jay (Perisoreus canadensis) occupies year-round territories in the coniferous boreal and subalpine forests of North America, but does not use conifer seed crops as a source of food. Over the last 33 years, we found that the occupancy rate of territories in Algonquin Park (ON, Canada) has declined at a higher rate in territories with a lower proportion of conifers compared to those with a higher proportion. Individuals occupying territories with a low proportion of conifers were also less likely to successfully fledge young. Using chambers to simulate food caches, we conducted an experiment to examine the hypothesis that coniferous trees are better able to preserve the perishable food items stored in summer and fall than deciduous trees due to their antibacterial and antifungal properties. Over a 1–4 month exposure period, we found that mealworms, blueberries, and raisins all lost less weight when stored on spruce and pine trees compared to deciduous and other coniferous trees. Our results indicate a novel mechanism to explain how habitat quality may influence the fitness and population dynamics of food-caching animals, and has important implications for understanding range limits for boreal breeding animals.     

Caching behaviour of Red Squirrels Sciurus vulgaris under conditions of high food availability

Members of the genus Sciurus store seed when plentiful by scatterhoarding. Such caches are impossible to defend and vulnerable to both interspecific and intraspecific competitors. In view of the delicate position held by Red Squirrels Sciurus vulgaris L. in Britain it is of value to extend to this species studies of the methods whereby such competition is reduced. Caching behaviour in a population of Red Squirrels living in a protected reserve and receiving supplementary food was studied for 18 months. Two main aspects were investigated; their ability to find caches they had not made, and their efforts to reduce competition for caches they did make. Stapanian & Smith (1978) predicted that caches are made at an optimal density and that the entire 360d? arc around a resource is used. This study upheld this second prediction but not the first for the population of Red Squirrels in question. In addition, it is suggested that caching cannot be considered to be permanent under conditions of surplus food.