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.     

Indirect effects on fitness between individuals that have never met via an extended phenotype

Interactions between organisms are ubiquitous and have important consequences for phenotypes and fitness. Individuals can even influence those they never meet, if they have extended phenotypes that alter the environments others experience. North American red squirrels (Tamiasciurus hudsonicus) guard food hoards, an extended phenotype that typically outlives the individual and is usually subsequently acquired by non‐relatives. Hoarding by previous owners can, therefore, influence subsequent owners. We found that red squirrels breed earlier and had higher lifetime fitness if the previous hoard owner was a male. This was driven by hoarding behaviour, as males and mid‐aged squirrels had the largest hoards, and these effects persisted across owners, such that if the previous owner was male or died in mid‐age, subsequent occupants had larger hoards. Individuals can, therefore, influence each other's resource‐dependent traits and fitness without ever meeting, such that the past can influence contemporary population dynamics through extended phenotypes.     

Dissecting the decision making process of scatter‐hoarding rodents

Many animals scatter‐hoard seeds to ensure an even supply of food throughout the year and this behavior requires similar foraging decisions. Seed‐traits have been shown to affect the final foraging decision but little is known about the decision process itself. Here, we first defined four sequential steps comprising the decision process of scatter‐hoarding rodents: 1) upon encountering a seed, should it be ignored or manipulated; 2) if manipulated, should it be eaten in situ or removed elsewhere; 3) upon removal, how far away should it be carried; and finally 4) whether to eat or cache the removed seed. Using experimental seeds with controlled differences in size, tannin and nutrient content, we evaluated how different traits influence each step in this decision process. We found that different traits had distinct effects on each step. Seed size affected all four steps, while nutrient and tannin content primarily affected the first and third steps. By dissecting foraging behavior in relation to experimentally controlled seed‐traits, we have created an effective framework within which to understand the unique relationship between scatter‐hoarding rodents that both predate and disperse plant seeds.     

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.     

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.     

Seed caching and cache pilferage by three rodent species in a temperate forest in the Xiaoxinganling Mountains

Although differences in food-hoarding tactics both reflect a behavioral response to cache pilferage among rodent species and may help explain their coexistence, differentiation in cache pilfering abilities among sympatric rodents with different hoarding strategies is seldom addressed. We carried out semi-natural enclosure experiments to investigate seed hoarding tactics among three sympatric rodent species (Tamias sibiricus, Apodemus peninsulae and Clethrionomys rufocanus) and the relationship of their pilfering abilities at the inter- and intraspecific levels. Our results showed that T. sibiricus exhibited a relatively stronger pilfering ability than A. peninsulae and C. rufocanus, as indicated by its higher recovery rate of artificial caches. Meanwhile A. peninsulae showed a medium pilfering ability and C. rufocanus displayed the lowest ability. We also noted that both cache size and cache depth significantly affected cache recovery in all three species. T. sibiricus scatter-hoarded more seeds than it larder-hoarded, A. peninsulae larder-hoarded more than scatter-hoarded, and C. rufocanus acted as a pure larder-hoarder. In T. sibiricus, individuals with lower pilfering abilities tended to scatter hoard seeds, indicating an intraspecific variation in hoarding propensity. Collectively, these results indicated that sympatric rodent species seem to deploy different food hoarding tactics that allow their coexistence in the temperate forests, suggesting a strong connection between hoarding strategy and pilfering ability.     

Hyper-dispersed cache distributions reduce pilferage: a laboratory study

Many animals use hoarding as a long-term strategy to ensure a food supply at times of shortage. We suggest that long-term scatter hoarders, whose caches are vulnerable to potentially high pilferage, should hoard in ways to reduce cache loss. This could be achieved by manipulating the density and dispersal patterns of caches to reduce the foraging efficiency of pilferers. This study explores the effect of distribution patterns on cache loss in the laboratory. We recorded the discovery of food items in different dispersal patterns by two bird species: coal tits Periparus ater (a hoarder) and great tits Parus major (a non-hoarder). Hyper-dispersed distributions reduced foraging efficiency because both species used systematic local search patterns. This study shows that hyper-dispersed distributions would be advantageous to hoarding animals to reduce cache loss.     

A Miocene rodent nut cache in coastal dunes of the Lower Rhine Embayment, Germany

A fossil burrow system containing a food cache was discovered in coastal facies in the Lower Rhine Embayment near Cologne, Germany, in the lignite sequences of the Garzweiler open-pit mine. Because these sediments are of Burdigalian age (late Early Miocene), this cache appears to be the geologically oldest food cache to date. The burrow occurs in the Morken Sand beds (horizon 5D), and it is hypothesized here that it was excavated by a Miocene burrowing animal from the surface of a palaeosol into the underlying dune sand in an interdune area. Based on the morphology of the burrow system and the size of the galleries, the burrow was made by a rodent, most likely a large hamster (e.g. Lartetomys or Karydomys ) or, conceivably, a large ground squirrel. The chambers, and sometimes the galleries, of the burrow were filled with a monospecific cache of considerable size, estimated here as a minimum of 1800 nuts, although it was probably much larger. This food cache, a larder hoard, consisted of the three-dimensionally preserved nuts of Castanopsis pyramidata (Fagaceae). Because many extant rodents are long-term larder hoarders in regions experiencing seasonal food shortages (e.g. those with cold winter conditions or a dry season), the occurrence of this type of food cache in the Early Miocene implies an acute or chronic scarcity of food resources which, in turn, may be linked to either seasonal cycles in food availability in the backbeach environment or, plausibly, may possibly foretell the onset of climatic seasonality in the entire region.     

Homogénéité ou hétérogénéité dans le métal des dépôts de l’Âge du Bronze : estimations sur leur formation à partir des isotopes du plomb

Lead isotope analysis was applied to three representative Late Bronze Age hoards from the Iberian Peninsula, for all of which compositional analyses are available. Unpublished isotopic evidence from the cave of Muricecs (Lleida) and the settlement of Las Lunas (Toledo) are compared to the published results for weapons from the Ría de Huelva, one of the most important Late Bronze Age hoards from Western Europe. Lead isotope analysis can tell us the sources of the metal used to make the artifacts in each hoard. The limited number of geologic reference points makes it difficult to determine all of the ore sources, but the analyses do give us evidence about the degree of homogeneity of the metal in the artifacts. As a result, one can separate metallic composition from artifact typology and thereby evaluate how the hoards were formed and what their functions were. Elemental analysis is unsuitable for this purpose because Late Bronze Age metals from Iberia are very homogenous and have few impurities.     

Effects of food value, predation risk, and pilferage on the caching decisions of Dipodomys merriami

Animals that scatter cache their food face a trade-off betweenthe benefits of protecting caches from pilferers and the costsassociated with caching. Placing food into a large number ofwidely spaced caches helps to protect it from pilferage butalso involves costs such as greater exposure to predators. Ipredicted that animals would disperse food into a larger numberof more widely spaced caches when caching (1) a preferred foodversus a less preferred food and (2) under conditions of lowpredation risk versus high predation risk. To test these predictions,I examined the scatter-caching decisions of Merriam's kangaroorats (Dipodomys merriami). D. merriami distributed caches inclumped patterns, regardless of food preference, but they showeda tendency to invest more in a preferred food by distributingcaches more widely. Under the relative safety of the new moon,they did not disperse caches more widely, rather they partitionedthe same amount of food into a larger number of caches thanthey did under the full moon, when predation risk is higher.To examine whether their cache spacing decisions had a significantimpact on the success of cache pilferers, I measured discoveryby pilferers of artificial caches of two food types at differentcaching distances. Results indicate that the cache spacing behaviorof D. merriami functions to protect caches from pilferers, becauseincreased spacing of artificial caches decreased the probabilityof pilferage for both types of food.     

Stochastic dietary restriction using a Markov-chain feeding protocol elicits complex, life history response in medflies

Lifespan in individually housed medflies (virgins of both sexes) and daily reproduction for females were studied following one of 12 dietary restriction (DR) treatments in which the availability of high-quality food (yeast-sugar mixture) for each fly was based on a Markov chain feeding scheme--a stochastic dietary regime which specifies that the future dietary state depends only on the present dietary state and not on the path by which the present state was achieved. The stochastic treatments consisted of a combination of one of four values of a 'discovery' parameter and one of three values of a 'persistence' parameter. The results supported the hypotheses that: (i) longevity is extended in most medfly cohorts subject to stochastic DR; and (ii) longevity is more affected by the patch discovery than the patch persistence parameter. One of the main conclusions of the study is that, in combination with the results of earlier dietary restriction studies on the medfly, the results reinforce the concept that the details of the dietary restriction protocols have a profound impact on the sign and magnitude of the longevity extension relative to ad libitum cohorts and that a deeper understanding of the effect of food restriction on longevity is not possible without an understanding of its effect on reproduction.     

Nectar provisioning close to host patches increases parasitoid recruitment,retention and host parasitism

In the adult stage, many parasitoids require hosts for their offspring growth and plant-derived food for their survival and metabolic needs. In agricultural fields, nectar provisioning can enhance biological control by increasing the longevity and fecundity of many species of parasitoids. Provided in a host patch, nectar can also increase patch quality for parasitoids and affect their foraging decisions, patch time residence, patch preference or offspring allocation. The aim of this study was to investigate the impact of extrafloral nectar (EFN) provisioning close to hosts on parasitoid aggregation in patches. The aphid parasitoid Diaeretiella rapae (M’Intosh) was released inside or outside patches containing Brassica napus L. infested by Brevicoryne brassicae L. aphids and Vicia faba L. with or without EFN. When parasitoids were released outside patches, more parasitoids were observed in patches with EFN than in patches deprived of EFN. This higher recruitment could be linked to a higher attraction of a combination of host and food stimuli or a learning process. A release–recapture experiment of labeled parasitoids released within patches showed the higher retention of parasitoids in patches providing EFN and hosts, suggesting that food close to the host patch affects patch residence time. Both attractiveness and patch retention could be involved in the higher number of parasitoids foraging in host patches surrounded by nectar and for the higher parasitism recorded. Nectar provisioning in host patches also affected female offspring allocation inside the patch.     

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.     

Spacing Behavior of a Non‐Larder‐Hoarding Tamiasciurus: A Study of Mearns's Squirrels in Xeric Coniferous Forests

In ecosystems with seasonal fluctuations in food supply many species use two strategies to store food: larder hoarding and scatter hoarding. However, because species at different geographic locations may experience distinct environmental conditions, differences in hoarding behavior may occur. Tree squirrels in the genus Tamiasciurus display variation in hoarding behavior. Whereas red (Tamiasciurus hudsonicus) and Douglas's (Tamiasciurus douglasii) squirrels in mesic coniferous forests defend territories centered around larder hoards maintaining non‐overlapping home ranges, red squirrels in deciduous forests defend small scatter‐hoarded caches of cones maintaining overlapping home ranges. As in other rodent species, variation in hoarding behavior appears to influence the spacing behavior of red and Douglas's squirrels. In contrast, Mearns's squirrels (Tamiasciurus mearnsi) in xeric coniferous forests neither rely on larder hoards nor appear to display territorial behavior. Unfortunately, little is known about the ecology of this southernmost Tamiasciurus. Using radiotelemetry, we estimated home‐range size, overlap, and maximum distance traveled from nest to examine the spacing behavior of Mearns's squirrels. Similar to scatter‐hoarding rodents, maximum distance traveled from nest was greater for males during mating season, whereas those of females were similar year round. Although no seasonal differences were detected, male home ranges were three times larger during mating season, whereas those of females were smaller and displayed a minor variation between seasons. Home ranges were overlapped year round but contrary to our expectations, overlap was greater during mating season for both sexes, with no detectable relationship between male home‐range size and the number of females overlapped during mating season. Overall, the results appear to support our hypothesis that in the absence of larder hoards, the spacing behavior of Mearns's squirrels should be different from larder‐hoarding congeners and more similar to scatter‐hoarding rodents.     

Climate change and the demographic demise of a hoarding bird living on the edge

Population declines along the lower-latitude edge of a species' range may be diagnostic of climate change. We report evidence that climate change has contributed to deteriorating reproductive success in a rapidly declining population of the grey jay (Perisoreus canadensis) at the southern edge of its range. This non-migratory bird of boreal and subalpine forest lives on permanent territories, where it hoards enormous amounts of food for winter and then breeds very early, under still-wintry conditions. We hypothesized that warmer autumns have increased the perishability of hoards and compromised subsequent breeding attempts. Our analysis confirmed that warm autumns, especially when followed by cold late winters, have led to delayed breeding and reduced reproductive success. Our findings uniquely show that weather months before the breeding season impact the timing and success of breeding. Warm autumns apparently represent hostile conditions for this species, because it relies on cold storage. Our study population may be especially vulnerable, because it is situated at the southern edge of the range, where the potential for hoard rot is most pronounced. This population's demise may signal a climate-driven range contraction through local extinctions along the trailing edge.     

The Value of a hoard: not just energy

We present a stochastic dynamic programming model of the contributionof stored food to winter survival. Using the acorn woodpecker(Melanerpes formtcivorus) as a model organism, we demonstratethat a hoard of small energetic value can impart considerableimprovement in the probability of surviving the winter and soimprove fitness. With this model we hope to resolve Koenig andMumme's paradox, that acorn woodpeckers expend much time andeffort to create and maintain hoards of acorns which provideno more that 16% of their energetic needs over the period inwhich they are used. We further demonstrate that the contributionof hoarded acorns to survival depends on the variability inforaging outcome, independently of the energetic value of thehoard in absolute terms. We point out that the results applyin principle to all hoarding animals and suggest a number offurther elaborations of the model.     

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     

Food hoarding behaviour of large field mouseApodemus peninsulae

An important behavioural adaptation for animal species with variable or unpredictable food availability is storing food. Food availability for large field mouseApodemus peninsulae (Thomas, 1907) is not reliable. We conducted a series of tests with the large field mouse to determine food hoarding behaviour, response when their hoarded food was removed, and whether perishable foods were treated different than non perishable foods. The study was conducted in four semi-natural enclosures (4 × 3 × 1 m), established on the Donglingshan Mountain near Beijing, China. Thirteen large field mice were placed in enclosures and offered wild apricotPrunus armeniaca seeds and Liaodong oakQuercus liaotungensis acorns. Our results indicated that although large field mice hoarded seeds in larder and scatter patterns, they more frequently exhibited larder hoarding. Liadong oak acorns were generally consumed near the feeder, whereas apricot seeds were more frequently transported to the nest box. Only apricot seeds were scattered among hoard sites. When seeds were removed from hoarding sites the mice responded by taking increased amounts of seeds to their nest for larder and scatter hoarding. Hoarding sites were not randomly distributed throughout the enclosure.     

围栏条件下岩松鼠对核桃的贮藏

许多动物都能够贮藏食物以应对一定时期的食物短缺。岩松鼠是中国特有的一种啮齿动物,主要分布于华北山地和丘陵地区,对于其食物贮藏行为还了解不多。我们在北京东灵山地区建立了半自然围栏,在围栏一角设置一木质巢箱供其休息,在围栏中心设一食盘(给食处),就岩松鼠对核桃(已预先标记)的贮藏特征进行了观察。每只受试动物在实验开始前6 h断食,于13∶ 00 左右,随机选择1 只岩松鼠,将其放入围栏中适应2 ～ 3 h。随后,在给食处放置20 枚已标记的核桃。于第二天同一时间进入围栏,检查并记录岩松鼠对核桃的处理情况,将埋藏、取食和剩余的核桃全部移出,另置20 枚新的核桃,继续实验。第三天,重复上述检查和记录,将岩松鼠及被其处理的核桃全部移出,清理巢箱、整理围栏。随后放入第二只岩松鼠,重复上述实验过程,如遇恶劣气候,则实验顺延,直至实验结束。结果表明:岩松鼠兼具集中贮藏和分散贮藏两种食物贮藏方式,并且分散方式是其主要的食物贮藏方式;岩松鼠在围栏中选择一定的位置贮藏食物;文中还讨论了可能影响岩松鼠食物贮藏的因素。     

Repeated radicle pruning of Quercus mongolica acorns as a cache management tactic of Siberian chipmunks

Many rodents hoard seeds as a means of ensuring food availability during scarcity. Siberian chipmunks (Tamias sibiricus) feed on acorns of white oak Quercus mongolica and hoard them for future use. Such caches may deteriorate due to the early germination of the acorns in autumn, which can be inhibited by radicle pruning or embryo excision. Siberian chipmunks are found to frequently prune the radicles of germinated acorns of Q. mongolica; however, whether this behavior is a kind of cache management tactic remains unclear. Here, we performed semi-natural enclosure and field experiments to test the role of radicle pruning in cache management of T. sibiricus. We found that T. sibiricus preferred non-germinated acorns and tended to prune radicles of germinating acorns when scatter-hoarding them, but did not perform the behavior of embryo excision by squirrels. Both semi-natural enclosure and field experiments showed that T. sibiricus not only pruned radicles repeatedly but removed radicles varied in length from acorns, which significantly postponed acorn germination and radicle growth. These observations suggest that radicle pruning would be an evolutionary tactic for cache management of Siberian chipmunks.