Changes in spatial memory mediated by experimental variation in food supply do not affect hippocampal anatomy in mountain chickadees (Poecile gambeli)

Earlier reports suggested that seasonal variation in food-caching behavior (caching intensity and cache retrieval accuracy) might correlate with morphological changes in the hippocampal formation, a brain structure thought to play a role in remembering cache locations. We demonstrated that changes in cache retrieval accuracy can also be triggered by experimental variation in food supply: captive mountain chickadees (Poecile gambeli) maintained on limited and unpredictable food supply were more accurate at recovering their caches and performed better on spatial memory tests than birds maintained on ad libitum food. In this study, we investigated whether these two treatment groups also differed in the volume and neuron number of the hippocampal formation. If variation in memory for food caches correlates with hippocampal size, then our birds with enhanced cache recovery and spatial memory performance should have larger hippocampal volumes and total neuron numbers. Contrary to this prediction we found no significant differences in volume or total neuron number of the hippocampal formation between the two treatment groups. Our results therefore indicate that changes in food-caching behavior and spatial memory performance, as mediated by experimental variations in food supply, are not necessarily accompanied by morphological changes in volume or neuron number of the hippocampal formation in fully developed, experienced food-caching birds.     

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     

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.     

The relationship between dominance, corticosterone, memory, and food caching in mountain chickadees (Poecile gambeli)

It has been hypothesized that in avian social groups subordinate individuals should maintain more energy reserves than dominants, as an insurance against increased perceived risk of starvation. Subordinates might also have elevated baseline corticosterone levels because corticosterone is known to facilitate fattening in birds. Recent experiments showed that moderately elevated corticosterone levels resulting from unpredictable food supply are correlated with enhanced cache retrieval efficiency and more accurate performance on a spatial memory task. Given the correlation between corticosterone and memory, a further prediction is that subordinates might be more efficient at cache retrieval and show more accurate performance on spatial memory tasks. We tested these predictions in dominant-subordinate pairs of mountain chickadees (Poecile gambeli). Each pair was housed in the same cage but caching behavior was tested individually in an adjacent aviary to avoid the confounding effects of small spaces in which birds could unnaturally and directly influence each other's behavior. In sharp contrast to our hypothesis, we found that subordinate chickadees cached less food, showed less efficient cache retrieval, and performed significantly worse on the spatial memory task than dominants. Although the behavioral differences could have resulted from social stress of subordination, and dominant birds reached significantly higher levels of corticosterone during their response to acute stress compared to subordinates, there were no significant differences between dominants and subordinates in baseline levels or in the pattern of adrenocortical stress response. We find no evidence, therefore, to support the hypothesis that subordinate mountain chickadees maintain elevated baseline corticosterone levels whereas lower caching rates and inferior cache retrieval efficiency might contribute to reduced survival of subordinates commonly found in food-caching parids.     

Clark's Nutcracker (Aves: Corvidae) Spatial Memory: Interference Effects on Cache Recovery Performance?

Clark's nutcrackers, Nucifraga columbiana, accurately v recover thousands of caches per year in the field. Previous experiments have confirmed that these birds possess excellent, long-lasting spatial-memory capabilities. We tested whether resistance to interference is one of the features of nutcracker spatial memory. Experiment 1 tested retroactive interference. Nutcrackers showed no decrease in accuracy overall but performed relatively poorly in their final recovery session. Interference is unlikely to have caused these sites to be poorly remembered because they had fewer neighbouring cache sites than better-remembered sites. Experiment 2 tested for proactive interference. Interference would have caused the experimental birds to be less accurate than control birds. Instead then were slightly more accurate. In experiment 3, nutcrackers were allowed to repeatedly view their cache sites from a cage between caching and recovery. Nutcrackers were less accurate when recovering from cache sites they had viewed. This effect may be due to changes in motivation. Order of caching had no effect on accuracy but nutcrackers were more accurate when recovering caches from central than from peripheral areas of experimental rooms. In summary, these experiments provide further evidence of the remarkable spatial-memory abilities of Clark's nutcrackers and demonstrate that these birds are highly resistant to interference effects on spatial memory. Comparative tests will be needed to test if specialized food storers are exceptionally resistant to interference in spatial memory.     

Long-term moderate elevation of corticosterone facilitates avian food-caching behaviour and enhances spatial memory

It is widely assumed that chronic stress and corresponding chronic elevations of glucocorticoid levels have deleterious effects on animals' brain functions such as learning and memory. Some animals, however, appear to maintain moderately elevated levels of glucocorticoids over long periods of time under natural energetically demanding conditions, and it is not clear whether such chronic but moderate elevations may be adaptive. I implanted wild-caught food-caching mountain chickadees (Poecile gambeli), which rely at least in part on spatial memory to find their caches, with 90-day continuous time-release corticosterone pellets designed to approximately double the baseline corticosterone levels. Corticosterone-implanted birds cached and consumed significantly more food and showed more efficient cache recovery and superior spatial memory performance compared with placebo-implanted birds. Thus, contrary to prevailing assumptions, long-term moderate elevations of corticosterone appear to enhance spatial memory in food-caching mountain chickadees. These results suggest that moderate chronic elevation of corticosterone may serve as an adaptation to unpredictable environments by facilitating feeding and food-caching behaviour and by improving cache-retrieval efficiency in food-caching birds.     

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.     

Mechanisms of Cache Retrieval in the Group Nesting Southern Flying Squirrel (Glaucomys volans)

We examined the proximate mechanisms of cache retrieval in the group‐living, southern flying squirrel, Glaucomys volans, through a series of behavioral experiments conducted in a large indoor arena. The effectiveness of several retrieval mechanisms was determined including spatial memory, olfaction, random searching and a heuristic under different environmental conditions. Our goal was to elucidate the hoarding strategy of individuals in a nest group and to address whether food storing individuals possess a retrieval advantage over pilfering nestmates. A storer's retrieval advantage is necessary for scatter hoarding to be an evolutionarily stable strategy (ESS) within aggregations of unrelated individuals. Our previous work has shown that, G. volans lives in such groups, and consequently it was important to address the storer's retrieval advantage under a range of environmental conditions. Initially in our baseline experiment, we developed methods to eliminate olfactory‐based retrieval and to control for random searching. Subsequently, we experimentally determined the effectiveness of cache retrieval via spatial memory, a heuristic and olfaction. We examined the mechanisms of cache retrieval in three additional experiments using two independent subject populations and found that under dry, odorless conditions spatial memory was the most effective retrieval mechanism in support of a storer's retrieval advantage. In a fifth experiment we examined cache retrieval under wet environmental conditions and showed that olfactory‐based retrieval was effective and the storer's advantage was reduced. We interpret these laboratory results based on considerations of natural environmental conditions and game theory. We propose a conditional ESS strategy where animals store and retrieve their own caches as the primary food hoarding tactic and opportunistically pilfer caches as a secondary tactic.     

The effect of social dominance on fattening and food-caching behaviour in Carolina chickadees, Poecile carolinensis

Subordinates often have to wait for dominants to obtain food. As a result, their foraging success should be less predictable and they should therefore maintain a higher level of energy reserves compared with dominants. A corollary of this prediction is that subordinates should gain mass earlier in the day and maintain higher mass than dominants. We tested these predictions with captive Carolina chickadees. In two different experiments (one where birds were given ad libitum access to food and the other with food access limited to 60 min/day), we formed social flocks of two previously unfamiliar birds and compared their energy management (body fat and food caches) while they were in the flock with energy management when housed alone. Results from both experiments failed to support the predictions. Of all the parameters of body mass and food caching we measured only the following results were significant: (1) On the ad libitum food schedule, both subordinates and dominants accumulated more mass over the day when in a flock compared with when they were solitary, and there were no differences in mass gain between dominants and subordinates. (2) When analysed separately, dominants showed a higher evening mass in the flock compared with the solitary condition, a trend that runs opposite to the prediction. Our results suggest that when in favourable foraging conditions, social interactions might cause dominant and subordinate birds to accumulate more energy reserves as a result of competition. On the other hand, if food supply is limited, both dominants and subordinates may be forced to maintain similar fat reserves as an insurance against increased risk of starvation. Copyright 2000 The Association for the Study of Animal Behaviour.     

贮食动物的盗食与反盗食行为策略

食物贮藏是许多动物应对食物短缺、保障其生存和繁衍的一种适应性行为。保护好贮藏食物以供食物短缺期利用,是食物贮藏成功的标志和进化动力。同种或异种动物盗食是贮藏食物损失的重要原因。嗅觉、视觉与空间记忆、随机搜寻等是动物搜寻和盗取食物的重要手段;避免盗食、阻止盗食和容忍盗食是动物反盗食的重要策略。动物通常采用多种行为策略进行盗食和反盗食,分配食物资源,形成相对稳定的种内、种间关系。盗食与反盗食互作及其对贮食行为进化的意义已成为行为生态学的研究热点和前沿之一,针对鸟类和哺乳类动物的研究尤为丰富。本文总结了贮食动物常见的盗食和反盗食行为策略及其相互作用的研究进展,主要内容涉及贮食动物利用嗅觉、视觉与空间记忆、随机搜寻等盗取其他个体食物的盗食策略,以及通过隐藏、转移、保卫、容忍等方式减少被盗食,保护贮藏食物的行为策略。针对现有研究状况,从种间盗食与反盗食及其与物种共存的关系,种间非对称盗食关系及其适应意义,盗食与反盗食最适行为策略及其与贮食动物适合度的关系等方面对今后研究提出了建议。     

Seasonal hippocampal plasticity in food-storing birds

Both food-storing behaviour and the hippocampus change annually in food-storing birds. Food storing increases substantially in autumn and winter in chickadees and tits, jays and nutcrackers and nuthatches. The total size of the chickadee hippocampus increases in autumn and winter as does the rate of hippocampal neurogenesis. The hippocampus is necessary for accurate cache retrieval in food-storing birds and is much larger in food-storing birds than in non-storing passerines. It therefore seems probable that seasonal change in caching and seasonal change in the hippocampus are causally related. The peak in recruitment of new neurons into the hippocampus occurs before birds have completed food storing and cache retrieval for the year and may therefore be associated with spacing caches, encoding the spatial locations of caches, or creating a neuronal architecture involved in the recollection of cache sites. The factors controlling hippocampal plasticity in food-storing birds are not well understood. Photoperiodic manipulations that produce change in food-storing behaviour have no effect on either hippocampal size or neuronal recruitment. Available evidence suggests that changes in hippocampal size and neurogenesis may be a consequence of the behavioural and cognitive involvement of the hippocampus in storing and retrieving food.     

Clark's Nutcrackers Nucifraga columbiana Remember the Size of Their Cached Seeds

Clark's nutcrackers ( Nucifraga columbiana ) hide thousands of seeds in subterranean caches that they later recover using spatial information about cache location. In two experiments, we tested whether nutcrackers also remember another type of information regarding their caches – the size of the seeds in each cache. We videotaped birds during cache recovery and then measured their bill gape during probing behaviour as captured on the videotape. In experiment one, six birds each experienced two treatments: one that allowed them to cache and then recover large seeds, and the other, an identical treatment using small seeds. During this experiment, all six birds used a wider gape when attempting to recover seeds during the large-seed treatment than during the small-seed treatment, and gape width was significantly correlated with seed size. During experiment two, we presented birds with both large and small seeds within the same caching session. We also increased the retention interval between caching and recovery. These modifications increased the difficulty of the task. Six of the seven birds used a wider gape during seed recovery when digging for caches that contained large seeds than they did when searching for small seeds. The ability to remember the size of seeds placed within caches may serve to increase the likelihood of speedy and successful recovery. It also allows the birds another level of organization of their food supply. These are the first experiments to suggest that Clark's nutcrackers remember more about their caches than location alone.     

Rapid effects of corticosterone on cache recovery in mountain chickadees (Parus gambeli)

Environmental perturbations increase adrenal activity in several vertebrates. Increases in corticosterone may serve as a proximate trigger whereby organisms can rapidly adapt their behavior to survive environmental fluctuations. In food-caching songbirds, inclement weather may present the need to alter caching and/or retrieval behaviors to ensure food supplies. We hypothesized that corticosterone may increase the rate of caching and/or retrieval behaviors in the mountain chickadee, a food-storing songbird, and tested if these potential effects were mediated by alterations in appetite, activity, or memory for cache sites. Corticosterone or vehicle was administered to subjects 5 min prior to either caching or recovery in a naturalistic laboratory paradigm during which we recorded the number of caching events, sites visited, and seeds eaten (caching) or caches recovered, total sites visited, cache-related visits, and non-cache-related visits (recovery). Data were analyzed using nested ANOVA for treatment within sequential trial. There was no effect on any caching behaviors following treatment. However, birds treated with corticosterone during retrieval recovered more seeds and tended to visit more cache-related sites than did controls. Since groups did not differ in the number of seeds eaten or the total number of sites visited, it seems unlikely that corticosterone affected appetite or activity. Rapid surges in corticosterone may increase the efficacy of an underlying memory process for cache sites which is reflected in higher cache recovery in corticosterone-treated birds than in controls. Thus, rapid alterations in plasma corticosterone following environmental change may alter memory-reliant behaviors which promote survival in the food-caching mountain chickadee.     

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.     

Ravens, Corvus corax, differentiate between knowledgeable and ignorant competitors

Human social behaviour is influenced by attributing mental states to others. It is debated whether and to what extent such skills might occur in non-human animals. We here test for the possibility of ravens attributing knowledge about the location of food to potential competitors. In our experiments, we capitalize on the mutually antagonistic interactions that occur in these birds between those individuals that store food versus those that try to pilfer these caches. Since ravens' pilfer success depends on memory of observed caches, we manipulated the view of birds at caching, thereby designing competitors who were either knowledgeable or ignorant of cache location and then tested the responses of both storers and pilferers to those competitors at recovery. We show that ravens modify their cache protection and pilfer tactics not simply in response to the immediate behaviour of competitors, but also in relation to whether or not they previously had the opportunity of observing caching. Our results suggest that the birds not only recall whom they had seen during caching, but also know that obstacles can obstruct the view of others and that this affects pilfering.     

Effect of watercourse characteristics on food-caching behaviour by European beaver, Castor fiber

We studied the relations between watercourse depth and width, and the occurrence, time of initiation and finite size of beaver food caches. Water depth was significantly greater by lodges with a food cache than at lodges lacking a food cache. There was no significant difference in watercourse width between the two groups. Date of initiation of the food cache was not related to water depth, but beavers living by wider watercourses started constructing food caches before those living on narrow watercourses. Finite size of food caches was significantly related to watercourse width and time of initiation. Results are discussed in the contexts of behavioural plasticity in overwintering strategies and habitat selection.     

Placement, Retrieval, and Memory of Caches by Thirteen-Lined Ground Squirrels

Mechanisms governing placement and retrieval of scatter hoards were investigated in 13-lined ground squirrels ( Spermophilus tridecemlineatus ). The squirrels used several placement tactics, including relatively deep burial of seeds, avoidance of prominent objects, and cryptic placement, which would reduce chance discovery by competitors but that might also increase the difficulty of retrieval for the hoarder. Nevertheless, scatter hoards were unfailingly retrieved within a day or two after placement, despite experimental elimination or displacement of local sensory cues emanating from the sites. Artificial caches placed close to true caches were not discovered, indicating that recovery attempts were quite precise. These results imply that 13-lined ground squirrels rely heavily on spatial memory for retrieval and are the first experimental demonstration of the importance of memory for cache recovery in a natural population of mammals.     

Population genetic structure and its implications for adaptive variation in memory and the hippocampus on a continental scale in food-caching black-capped chickadees

Food-caching birds rely on stored food to survive the winter, and spatial memory has been shown to be critical in successful cache recovery. Both spatial memory and the hippocampus, an area of the brain involved in spatial memory, exhibit significant geographic variation linked to climate-based environmental harshness and the potential reliance on food caches for survival. Such geographic variation has been suggested to have a heritable basis associated with differential selection. Here, we ask whether population genetic differentiation and potential isolation among multiple populations of food-caching black-capped chickadees is associated with differences in memory and hippocampal morphology by exploring population genetic structure within and among groups of populations that are divergent to different degrees in hippocampal morphology. Using mitochondrial DNA and 583 AFLP loci, we found that population divergence in hippocampal morphology is not significantly associated with neutral genetic divergence or geographic distance, but instead is significantly associated with differences in winter climate. These results are consistent with variation in a history of natural selection on memory and hippocampal morphology that creates and maintains differences in these traits regardless of population genetic structure and likely associated gene flow.     

A dynamic model of short-term energy management in small food-caching and non-caching birds

The survival of small birds in winter is critically dependenton the birds' ability to accumulate and maintain safe levelsof energy reserves. In some species, food caching facilitatesenergy regulation by providing an energy source complementaryto body fat. We present a dynamic optimization model of short-term,diurnal energy management for both food-caching and non-caching birds in which only short-day, winter conditions are considered.We assumed that birds can either rest, forage and eat, forageand cache, or retrieve existing caches (the two latter optionsare available only to caching birds). The model predicted thatwhen there is variability in foraging success (here modeledstrictly as within-day variability), both caching and non-caching birds should increase their fat reserves almost linearly inthe morning slowing down toward late afternoon, a result consistentwith field data but different than the result of a previousdynamic program. Non-cachers were predicted to carry higherfat levels than cachers especially when the variability inforaging success is high. Probability of death for non-caching birds was predicted to be higher than that for cachers, especiallyat higher levels of variability in foraging success. Amongcaching birds, an increase in number of caches and fat reserveswas also predicted if: (1) mean foraging success was decreased,(2) variability in foraging success was increased, and (3)energy expenditure at night was increased over our baselineconditions. Under the conditions simulated in our model, birdswere predicted to cache only if cache half-life (i.e., timeinterval over which 50% of the caches are forgotten or lostto pilferage) exceeded 2.5 days, indicating that low pilferagerate and long memory favor more caching. Finally, we showedthat such daily patterns of energy management do not necessarilyrequire relaxing assumptions about mass-dependent predationrisk.     

Song as an honest signal of past developmental stress in the European starling (Sturnus vulgaris)

Bird song is a sexually selected male trait where females select males on the basis of song quality. It has recently been suggested that the quality of the adult male song may be determined by nutritional stress during early development. Here, we test the 'nutritional-stress hypothesis' using the complex song of the European starling. Fledgling starlings were kept under experimental treatment (unpredictable short-term food deprivations) or control conditions (ad libitum food supply), for three months immediately after independence. We measured their physiological and immune responses during the treatment and recorded song production during the following spring. Birds in the experimental group showed increased mass during the treatment and also a significantly suppressed humoral response compared with birds in the control group. There was no difference between the groups in the cell-mediated response. Next spring, males in the experimental group spent less time singing, sang fewer song bouts, took longer to start singing and also sang significantly shorter song bouts. These data support the hypothesis that both the quality and quantity of song produced by individual birds reflect past developmental stress. The results also suggest the 'nutritional-stress hypothesis' is best considered as a more general 'developmental-stress hypothesis'.