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.     

Problems faced by food-caching corvids and the evolution of cognitive solutions

The scatter hoarding of food, or caching, is a widespread and well-studied behaviour. Recent experiments with caching corvids have provided evidence for episodic-like memory, future planning and possibly mental attribution, all cognitive abilities that were thought to be unique to humans. In addition to the complexity of making flexible, informed decisions about caching and recovering, this behaviour is underpinned by a motivationally controlled compulsion to cache. In this review, we shall first discuss the compulsive side of caching both during ontogeny and in the caching behaviour of adult corvids. We then consider some of the problems that these birds face and review the evidence for the cognitive abilities they use to solve them. Thus, the emergence of episodic-like memory is viewed as a solution for coping with food perishability, while the various cache-protection and pilfering strategies may be sophisticated tools to deprive competitors of information, either by reducing the quality of information they can gather, or invalidating the information they already have. Finally, we shall examine whether such future-oriented behaviour involves future planning and ask why this and other cognitive abilities might have evolved in corvids.     

Scatter‐hoarding and cache pilfering of rodents in response to seed abundance

Seed caching and reciprocal cache pilferage play an important role in the coexistence of food‐hoarding animals. Understanding what affects seed caching and how cache pilferage occurs is an important question in seed dispersal ecology. However, tracking seed fate and cache pilferage presents substantial practical difficulties. Siberian chipmunks Tamias sibiricus always remove the entire pericarp when scatter‐hoarding acorns of Mongolian oak Quercus mongolica, whereas wood mice Apodemus peninsulae often store whole acorns in their caches. These differences in behavior provide an opportunity to investigate unilateral cache pilferage of T. sibiricus from A. peninsulae in response to seed abundance. In this study, tagged acorns were released at the peak and end periods of seed rain from Q. mongolica. This allowed us to investigate seed caching and unilateral cache pilferage at different seed abundances. We found that a higher proportion of acorns were cached at lower level of seed abundance (toward the end of seed rain), mainly because T. sibiricus rather than A. peninsulae scatter‐hoarded significantly more acorns at this time. Cache distances decreased with increasing seed abundance, indicating that acorns were cached further away and into smaller caches at lower seed abundance. Unexpectedly, unilateral cache pilferage by T. sibiricus was not significantly influenced by seed abundance—remaining at around 28% during both periods of high and low seed abundance.     

Evidence of Social Influences on Cache‐Making by Grey Squirrels (Sciurus carolinensis)

Many studies have found that scatter‐hoarding animals change their behaviour when storing food in the presence of conspecifics to minimize the likelihood that their caches will be pilfered; they refrain from caching, move away from conspecifics or choose visually obscured sites. This study reports the first evidence that the presence of conspecifics continues to influence the caching behaviour of a scatter‐hoarding mammal, the grey squirrel, after a suitable cache site has been selected and the hoarder is filling and covering its cache. Wild grey squirrels were filmed when storing preferred and less preferred nuts and when they were alone or with conspecifics present. In line with previous findings, squirrels spent longer travelling from the nut patch and were more vigilant when conspecifics were present. However, squirrels also spent longer disguising their caches and were more likely to stop digging and become vigilant when conspecifics were present than when they were alone. In particular, they were most likely to curtail their digging when storing their preferred nuts in the presence of conspecifics. The results indicate that caching squirrels remain sensitive to the presence of conspecifics until the cache is complete and that they respond flexibly to conspecifics according to the type of food they are storing.     

Mountain chickadees discriminate between potential cache pilferers and non-pilferers

Evolution of complex cognition in animals has been linked to complex social behaviour. One of the costs of sociality is increased competition for food which may be reduced by food caching, but cache theft may undermine the benefits of caching. In birds, sophisticated food-caching-related cognition has been demonstrated only for corvids and attributed to their highly social behaviour. Many non-corvid food-caching species exhibit similar complex social behaviour and here I provide experimental evidence that mountain chickadees (Poecile gambeli) adjust their caching strategies depending on social context. Chickadees were allowed to cache seeds in the presence of potential cache pilferer, either conspecific or heterospecific (red-breasted nuthatch, Sitta canadensis) and a non-pilferer (dark-eyed junco, Junco hyemalis) positioned at the opposite sides of the experimental arena. Available caching sites were either exposed to these observers or hidden from their view while the cacher could always see both observers. Chickadees chose caching sites that were hidden from direct view of the potential pilferers while caching in direct view of the non-pilferers. When no pilferers were present, chickadees made equal use of all available caching substrates and there were no differences in the amount of caching in the presence or absence of pilferers. These results suggest that (i) chickadees may be able to recognize potential cache thieves, both conspecific and heterospecific, and adjust their caching strategies to minimize potential cache pilferage and (ii) chickadees appear to discriminate between caching sites that can or cannot be seen by observers, which may allow them to control visual information available to potential pilferers.     

食干果鸟对种子传播的作用

食干果鸟对种子传播的作用鲁长虎袁力（东北林业大学,哈尔滨１５００４０）ＥｆｆｅｃｔｏｆＤｒｙ＿ｆｒｕｉｔＥａｔｉｎｇＢｉｒｄｓｔｏＳｅｅｄＤｉｓｐｅｒｓａｌ．Ｌｕｃｈａｎｇｈｕ,ＹｕａｎＬｉ（ＮｏｒｔｈｅａｓｔＦｏｒｅｓｔｒｙＵｎｉｖｅｒｓｉｔｙ,...     

The placement, recovery, and loss of scatter hoards by eastern chipmunks,Tamias striatus

Although eastern chipmunks typically larder hoard food in theirburrows, some scatter hoarding occurs, especially by newly emergedjuveniles and by females with young. To examine patterns ofscatter hoard placement and their adaptive significance, weused standard food provisioning tests followed by continuousmonitoring to determine the longevity and fate of scatter hoards.Longevity of scatter hoards was low (median 74 min) and pilferagewas high (46%). Chipmunks placed scatter hoards away from thepatch, closer to their burrow and within the defended area ofprimary use. Scatter hoard placement was affected by the numberof competitors at the patch. However, juveniles and femaleswith young differed slightly in their responses. competitorsthat approached scatteihoards were sometimes chased away bythe scatter hoard's owner, and the scatter hoard was moved toanother location by the owner. Females with young recoveredtheir largest scatter hoards first, but there was little additionalpattern in scatter hoard recovery. An experiment using simulatedscatter hoards showed that scatter hoards farther from a patchof food lasted longer and that disturbing and marking scatterhoards reduced their longevity. These observations indicate:(1) that scatter hoard placement is more related to avoidingpilferage of completed caches than to rapidly sequestering fooditems from an ephemeral patch and (2) that optimal cache distributionmay be affected by the cache-defense ability of individuals,by the relationship between competitor density and cache securitynear the patch, and by the territorial behavior of neighboringconspecifics.     

Social influences on food caching in willow tits: a field experiment

We studied the food hoarding behavior of willow tits (Parusmontanus), a scatter-hoarding passerine wintering in dominance-structuredflocks. We examined social influences on microhabitat selectionand spatial cache distribution at temporary feeders. Dominantadult males stored food closer to die feeder and at a greaterrate than did subordinates. When alone, the birds stored foodcloser to the feeder than when accompanied by conspecifics.Conifers were preferred over deciduous trees as cache trees.The subordinates cached more in die outer parts of branchesthan dominants. There were no significant differences in dierelative or absolute heights of die caches, nor in the verticalor horizontal hoarding niche breadths between dominants andsubordinates. We experimentally removed die dominants from dieflock for 90 min and recorded the behavior of die remainingsubordinates immediately after die removal. The removal resultedin a decrease in die hoarding distance of die remaining birds,indicating that die presence of dominants directly affecteddie behavior of subordinates and suggesting that kleptopar-asitismby dominants may be prevented by rarhing farther away. Withdie dominants removed, die subordinates cached at a greaterrate than before die removal. The decrease in die hoarding distanceand increase in die hoarding rate were die only significanteffects of die experiment, perhaps suggesting that, during ashort absence of dominants, die subordinates do not benefitfrom changing dieir caching microhabitat They might be excludedfrom those new, possibly safer, microhabitats after die dominantbird rejoins die flock.     

Memory and Brain in Food‐Storing Birds: Space Oddities or Adaptive Specializations?

Scatterhoarding birds that cache food items have become an important model system for the study of spatial memory and its correlates in the brain. In particular, it has been suggested that through adaptive specialization, species that cache food have better spatial memory and a relatively larger hippocampus than their non-caching relatives. Critics of this approach, dubbed neuroecology, maintain that neither of these hypotheses has been confirmed. Here, we review the evidence pertaining to a correlation between food-storing capability and the relative volume of the hippocampus. Hippocampal volume has been related to food-storing behaviour in comparisons between species, within species, or within individuals, but the evidence is not consistent. There are several possible reasons for this inconsistency, including: (1) food-hoarding birds may not always use memory for retrieval, (2) there may be systematic differences between data from North American and Eurasian species that affect the analysis, and (3) sample sizes have in many cases been too small. In addition, both the independent variable (degree of food-hoarding specialization) and the dependent variable (relative volume of the hippocampus) are not clearly and consistently defined. Alternatively, it is possible that the neuroecological hypothesis is false. Systematic empirical research is necessary to determine whether or not food-storing birds have evolved adaptive specializations in brain and cognition.     

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.     

The effects of cache loss on choice of cache sites in black-capped chickadees

Food-storing birds lose a great deal of their stored food toother animals. We examined whether blackcapped chickadees (Parusairicapillus) modify their choice of cache sites using informationthat predicts cache loss. In experiment 1, birds learned toavoid caching at spatial locations where cache loss had previouslyoccurred, but they did not avoid caching near local color cuesthat predicted cache loss. Birds did not modify their generaluse of space in the aviary. Birds also learned to reduce searchingfor caches where spatial location predicted cache loss. Experiment2 confirmed the birds’ ability to discriminate among thespatial locations and the local color cues used in experiment1. In experiment 3, learning a food-rewarded approach to potentialcache sites occurred without any change in the choice of sitesfor caching. We discuss how chickadees selectively associatethe choice of cache site with its consequences, even over delaysof several hours between caching and cache recovery.     

Seed caching by woylies Bettongia penicillata can increase sandalwood Santalum spicatum regeneration in Western Australia

Abstract The role a small marsupial, the woylie Bettongia penicillata, might play in the recruitment and regeneration of Western Australian sandalwood Santalum spicatum through its seed caching behaviour was investigated in this study. To determine the fate of the seeds, cotton thread was attached to the seeds and the trail followed. A total of 25 seed caches were located. All of the seeds were found in separate caches, which was consistent with scatter‐hoarding behaviour. The average distance from the source of the seeds to the cache was 43.1 m ± 5.8 m at Dryandra woodland and 29.1 m ± 3.8 m at Karakamia sanctuary. The mean cache depth was 4.3 cm ± 0.2 cm at Dryandra woodland compared with 4.6 cm ± 0.3 cm at Karakamia sanctuary. Significantly more seedlings and saplings grew away from sandalwood trees at sites where woylies were present than at sites with no woylies. In contrast, significantly more seedlings and saplings grew under adult sandalwood trees at the site without woylies than where they were present, although there were significantly lower rates of recruitment and sandalwood regeneration at these sites. In addition, significantly more whole, undisturbed sandalwood seeds were found under the parent trees at the woylie‐free site than at the site with woylies. These findings strongly suggest that little seed dispersal or regeneration of sandalwood occurs in the absence of woylies. Through scatter‐hoarding, woylies have the potential to disperse and cache sandalwood seeds away from the source and significantly alter the subsequent regeneration of sandalwood. Furthermore, by caching seeds large distances away from a source, woylies could modify the distribution of sandalwood in an area.     

啮齿动物的分散贮食行为

食物贮藏是许多动物重要的适应性行为,分散贮藏的食物以植物种子为主。每个贮藏点贮藏数量不等的食物项目。啮齿动物分散贮藏食物之后,可降低食物被其他个体获取的机率,提高对食物资源的控制能力,最终有利于自身的生存和繁殖成功。植物种子被贮藏之后,可减少非贮食鼠类对种子的取食。同时,合适的微生境和埋藏有利于种子萌发、幼苗建成和植物的更新;使植物的分布区得以扩展。探讨啮齿动物的分散贮食行为,能够更好地理解食物贮藏在啮齿动物生活史中的作用,进一步认识鼠类和植物的相互关系以及不同啮齿动物在群落形成中的潜在作用。本综述了啮齿动物分散贮食的研究进展,并提出今后工作中的几点建议。     

The ecology of the avian brain: food-storing memory and the hippocampus

Some species of birds store food, often hoarding several hundreds of seeds over a period of just a few weeks. Field and laboratory studies have demonstrated that food-storing species have an impressive memory and an enlarged region of the brain, the hippocampal region. Lesion experiments have shown that the hippocampus is important in accurate retrieval of stored food. Taken together, these results have led to the hypothesis that the enlarged hippocampus is associated with the memory requirements of retrieving stored food. In this review, we discuss four areas of study: comparative studies of the brain, comparative studies of behaviour, developmental plasticity and seasonal changes in food storing and the hippocampus.     

The ecology of the avian brain: food-storing memory and the hippocampus

Some species of birds store food, often hoarding several hundreds of seeds over a period of just a few weeks. Field and laboratory studies have demonstrated that food-storing species have an impressive memory and an enlarged region of the brain, the hippocampal region. Lesion experiments have shown that the hippocampus is important in accurate retrieval of stored food. Taken together, these results have led to the hypothesis that the enlarged hippocampus is associated with the memory requirements of retrieving stored food. In this review, we discuss four areas of study: comparative studies of the brain, comparative studies of behaviour, developmental plasticity and seasonal changes in food storing and the hippocampus.     

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.     

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。     

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.     

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.     

Is hippocampal volume affected by specialization for food hoarding in birds?

The hypothesis that spatial-memory specialization affects the size of the hippocampus has become widely accepted among scientists. The hypothesis comes from studies on birds primarily in two families, the Paridae (tits, titmice and chickadees) and the Corvidae (crows, nutcrackers, jays, etc.). Many species in these families store food and rely on spatial memory to relocate the cached items. The hippocampus is a brain structure that is thought to be important for memory. Several studies report that hoarding species in these families possess larger hippocampi than non-hoarding relatives, and that species classified as large-scale hoarders have larger hippocampi than less specialized hoarders. We have investigated the largest dataset on hippocampus size and food-hoarding behaviour in these families so far but did not find a significant correlation between food-hoarding specialization and hippocampal volume. The occurrence of such an effect in earlier studies may depend on differences in the estimation of hippocampal volumes or difficulties in categorizing the degree of specialization for hoarding or both. To control for discrepancies in measurement methods we made our own estimates of hippocampal volumes in 16 individuals of four species that have been included in previous studies. Our estimates agreed closely with previous ones, suggesting that measurement methods are sufficiently consistent. Instead, the main reasons that previous studies have found an effect where we did not are difficulties in assessing the degree of hoarding specialization and the fact that smaller subsets of species were compared than in our study. Our results show that a correlation between food-hoarding specialization and hippocampal volume cannot be claimed on the basis of present data in these families.