Scatter-hoarding Animals Research Articles

A non-memory-based functional neural framework for animal caching behavior

The brain’s extraordinary abilities are often attributed to its capacity to learn and adapt. But memory has its limitations, especially when faced with tasks such as retrieving thousands of food items—a common behavior in scatter-hoarding animals. Here, we propose a brain mechanism that may facilitate caching and retrieval behaviors, with a focus on hippocampal spatial cells. Rather than memorizing the locations of their caches, as previously hypothesized, we suggest that cache-hoarding animals employ a static mechanism akin to hash functions commonly used in computing. Our mathematical model aligns with the activity of hippocampal spatial cells, which respond to an animal’s positional attention. We know that the region that activates each spatial cell remains consistent across subsequent visits to the same area but not between areas. This remapping, combined with the uniqueness of cognitive maps, produces persistent hash functions that can serve both food caching and retrieval. We present a simple neural network architecture that can generate such a probabilistic hash that is unique to the animal and not sensitive to environmental changes. This mechanism could serve a virtually boundless capacity for the encoding of any structured data.

Substrate scent-induced disproportionate seed dispersal by rodents.

Conspecific adults impose strong negative density-dependent effects on seed survival nearby parent trees, however, the underlying mechanisms are diversified and remain unclear. In this study, we presented consistent evidence that parent-scented forest floor masked seed odor, reduced cache recovery rate by scatter-hoarding animals, and then increased seed dispersal far away from mother trees. Our results showed that seed odors of Korean pine Pinus koraiensis match well with the volatile profile of their forest floor. Moreover, scatter-hoarding animals selectively transported P. koraiensis seeds toward the areas where seed odor was more contrasting against the background substrate, possibly due to the fact that accumulation of conspecific volatile compounds in caches hindered seed detection by scatter-hoarding animals. Our study provides insight into the role of leaf litter in directing seed dispersal process, representing a novel mechanism by which P. koraiensis increases selection for seed dispersal far away from the parent tree.

Gut microbiota is associated with spatial memory and seed-hoarding behavior of South China field mice (Apodemus draco).

Scatter-hoarding animals store food in multiple locations within their home range and rely on spatial memory for subsequent localization and retrieval. The relationship between memory and scatter-hoarding behavior has been widely demonstrated, but the association of gut microbiota with spatial memory and seed-hoarding behavior of animals remains unclear. In this study, by using enclosure behavior tests, memory tests including an object location test (OLT) and a novel object recognition test (NORT), and fecal microbiota transplantation (FMT) experiment, we evaluated the role of gut microbiota in affecting the memory and seed-hoarding behavior of rodents. According to their scatter-hoarding intensity, South China field mice (Apodemus draco) were divided into scatter-hoarding group (SG) and non-scatter-hoarding group (NG). We found that the SG performed better than the NG in the NORT. FMT from SG donor mice altered the NG recipient mice's gut microbiota structure. Further tests demonstrated FMT from SG donor mice increased memory of NG recipient mice in laboratory tests and seed larder hoarding intensity of NG recipient mice in enclosures. Our results suggest gut microbiota could modulate the memory and seed-hoarding behavior of animals.

Spatial decision-making in acorn dispersal by Eurasian jays around the forest edge: Insights into oak forest regeneration mechanisms

Seed dispersal is key to forest regeneration and often depends on the behavior of seed scatter-hoarding animals. However, our understanding of the decision-making of scatter-hoarders and how vegetation structure at different spatial scales affects dispersal patterns remains limited. We studied seed dispersal at the forest edge across multiple spatial scales (habitat, sub-habitat, microsites) between and within habitats with distinct vegetation structure. Our model system is a mixed-oak forest dominated by holm oak (Quercus ilex) and an adjacent shrubland dominated by the shrub Retama sphaerocarpa. For three years, we tracked the movement of acorns by a keystone scatter-hoarder, the Eurasian jay (Garrulus glandarius). At the coarse scale, jays did not show a preference for caching acorns either in the forest or in the shrubland when the source tree was within the forest. However, when the source tree was on the forest edge or was an isolated oak tree in the shrubland at < 200 m from the forest, jays showed a preference for caching in the forest. Conversely, when isolated oak trees were > 200 m from the forest, all acorns were dispersed in the shrubland. Dispersal distances were shorter within the forest than within the shrubland. At an intermediate scale, within the shrubland jays preferred to cache acorns under large retamas while avoiding gaps. In the forest, jays also avoided gaps and preferred certain woody species and vertical vegetation structures, although these preferences varied across feeders. At the finest scale, jays selected stones as cache microsites. Thus, the selection of acorn caching sites followed a hierarchical and selective top-down process across different spatial scales. The position of the source trees in the landscape determined habitat preference and dispersal distance. We detected different preferences in response to similar vegetation structure and composition, indicating that the decision-making process is flexible at an intermediate scale that generates diverse spatial patterns of dispersal. This study sheds light on the intricate decision-making process of seed caching by scatter-hoarders, and the consequences for the spatial patterns of seed dispersal as well as the expansion and regeneration of oak forests.

Preferences of avian seed-hoarders in advance of potential American chestnut reintroduction

Nut-bearing trees such as oaks (Quercus genus) and American chestnut (Castanea dentata, hereafter: chestnut) rely on scatter-hoarding animals for seed dispersal. With the pursuit of blight-resistant chestnuts for eventual reintroduction into eastern hardwood forests of the United States, it becomes important to understand how foraging preferences of avian seed-hoarders will influence chestnut dispersal in oak-dominated forests. Using six seed selection trials over three years and two “seasons” (early fall and late fall), we assess the relative seed preferences – when gathering seeds for hoarding or consumption – of five species of avian seed dispersers in southeast Ohio. In each trial, we presented an equal number of chestnuts and two species of common acorns, black (Q. velutina) and white oak (Q. alba), to wild birds on feeding platforms monitored by cameras. We used Bayesian discrete choice models to determine preferences of each species, and estimate the influence of natural variation in background mast availability (i.e., different years and seasons). Blue Jays (Cyanocitta cristata) showed a consistent preference for the seeds of black oak over chestnut over white oak, and the strength of preference for black oak increased in late season when acorns were scarce. Other species showed variable preferences, with White-breasted Nuthatch (Sitta carolinensis) the only species to prefer chestnuts over both acorns, though sample size was small (n = 26 selections). Our results suggest chestnuts are used by a host of avian seed-hoarders that may facilitate dispersal of chestnut, particularly in years of black oak mast failure.

Palatability and profitability of co-occurring seeds alter indirect interactions among rodent-dispersed trees.

Beyond direct species interactions, seed dispersal is potentially affected by indirect seed-seed interactions among co-occurring nut-bearing trees which are mediated by scatter-hoarding animals as shared seed dispersers. A relevant question in such systems is to what extent different functional traits related to food palatability and profitability affect the kinds of indirect interactions that occur among co-occurring seeds, and the consequences for seed dispersal. We used field experiments to track seed dispersal with individually tagged seeds in both monospecific and mixed seed communities. We measured indirect effects based on 3 seed-seed species pairs from the family Fagaceae with contrasting seed size, tannin level, and dormancy in a subtropical forest in Southwest China. When all else was equal, the presence of adjacently placed seeds with contrasting seed traits created different indirect effects measured through a variety of dispersal-related indicators. Apparent mutualism was reciprocal due to increasing seed dispersal in mixed seed patches with mixed differences in seed tannins and dormancy. However, differences in either seed size or dormancy in co-occurring adjacently placed seeds caused apparent competition with reduced seed removal or seed dispersal (distance) in at least one species. Our study supports the hypothesis that different functional traits related to food palatability and profitability in co-occurring seeds modify foraging decisions of scatter-hoarding animals, and subsequently cause indirect effects on seed dispersal among rodent-dispersed trees. We conclude that such indirect effects mediated by shared seed dispersers may act as an important determinant of seed dispersal for co-fruiting animal-dispersed trees in many natural forests.

Great tits who remember more accurately have difficulty forgetting, but variation is not driven by environmental harshness

The causes of individual variation in memory are poorly understood in wild animals. Harsh environments with sparse or rapidly changing food resources are hypothesized to favour more accurate spatial memory to allow animals to return to previously visited patches when current patches are depleted. A potential cost of more accurate spatial memory is proactive interference, where accurate memories block the formation of new memories. This relationship between spatial memory, proactive interference, and harsh environments has only been studied in scatter-hoarding animals. We compare spatial memory accuracy and proactive interference performance of non-scatter hoarding great tits (Parus major) from high and low elevations where harshness increases with elevation. In contrast to studies of scatter-hoarders, we did not find a significant difference between high and low elevation birds in their spatial memory accuracy or proactive interference performance. Using a variance partitioning approach, we report the first among-individual trade-off between spatial memory and proactive interference, uncovering variation in memory at the individual level where selection may act. Although we have no evidence of harsh habitats affecting spatial memory, our results suggest that if elevation produced differences in spatial memory between elevations, we could see concurrent changes in how quickly birds can forget.

High-valued seeds are remembered better: evidence for item-based spatial memory of scatter-hoarding rodents

Episodic memory of scatter-hoarding animals involves encoding and storage of memories of cached food items, in conjunction with subsequent retrieval or recovery. Although the reward values mediate the interaction of item memory and source memory, whether nonhuman animals divide their spatial memory resources between cached items of different values has never been tested. Here, we used a unique scatter-hoarder/seed system to test our ‘cache value hypothesis’, which proposes that scatter-hoarding animals will preferentially allocate spatial memory resources towards higher-valued caches. By making Edwards's long-tailed rats, Leopoldamys edwardsi , anosmic, using Triton X-100, we showed that L. edwardsi recovered more caches containing large nuts than those containing small ones, although the two kinds of nuts were equivalently cached. Our results therefore support the hypothesis that scatter-hoarding animals allocate more spatial memory resources to caches containing high-valued items. This is one of the few studies to investigate how item memory regulates source memory (order information) in the context of food storing and recovery by animals, especially by scatter-hoarding rodents. That high-valued items were remembered better than low-valued ones in our study suggests that item memory appears to be contextually associated with order information of items in animal memory processes, which is not in agreement with a previous suggestion that order information is independent of content or item information. • We used a scatter-hoarding rodent to test episodic memory. • Edward's long-tailed rats allocated more memory on high-valued caches. • High-valued items were remembered better than low-valued ones. • The rats know ‘what food’ was cached ‘where’ or ‘when’.

Olfaction alters spatial memory strategy of scatter-hoarding animals.

Although it has been suggested that olfaction is closely interconnected with hippocampal systems, whether olfaction regulates spatial memory strategy remains never known. Furthermore, no study has examined how olfaction mediates spatial memory established on the external objects, for example, caches made by scatter-hoarding animals. Here, we experimentally induced nondestructive and reversible olfaction loss of a scatter-hoarding animal Leopoldamys edwardsi, to test whether and how olfaction regulates spatial memory to mediate cache recovery and pilferage. Our results showed that the normal L. edwardsi preferred to pilfer caches of others rather than to recover their own using accurate spatial memory (35.7% vs. 18.6%). Anosmic L. edwardsi preferred to recover the caches they made prior to olfaction loss rather than to pilfer from others relied on spatial memory (54.2% vs. 36.0%). However, L. edwardsi with anosmia showed no preference either to the caches they established after olfaction loss or caches made by others (25.8% vs. 29.1%). These collectively indicate that olfaction loss has a potential to affect new memory formation but not previously established spatial memory on caches. Our study first showed that olfaction modified spatial memory strategy in cache recovery and pilferage behaviors of scatter-hoarding animals. We suggest that future studies pay more attention to the evolution of olfaction and its relationship with spatial memory strategy.

Rodent-mediated plant community competition: what happens to the seeds after entering the adjacent stands?

BackgroundSeed dispersal by scatter-hoarding animals can affect the developmental dynamics of plant communities. However, how animals might participate in plant inter-community competition has rarely been investigated. Forest community junction is an area where the competition between plant communities is most prominent and animal activity is more frequent. At present, little is known about how scatter-hoarding animals might assist competitions by adjacent plant communities. Thus, for 3 years (2015–2017), we tracked the fate of 2880 tagged seeds (Quercus aliena var. acuteserrata, Pinus tabuliformis, and P. armandii seed) placed near an edge where the forest composition changes from a pine forest to an oak forest in northwestern China.ResultsWe found that the seed fates differed when Quercus and Pinus seeds entered adjacent stands. In contrast to Pinus seeds, acorns that entered pine forests were characterized by higher caching rates and longer dispersal distances. Pinus seeds had the highest probability of being predated (85%) by rodents, and eleven Q. aliena var. acuteserrata seedlings were established in pine forests, although none survived in the later stages. In addition, rodents exhibited obvious selectivity in terms of the microhabitats for the seed caching sites.ConclusionsSeed fates differed when Quercus and Pinus seeds entered adjacent stands. The predation pressure by rodents on the seeds of Pinus species limited the germination of seeds and seedling establishment in oak forests. The different seed fates after their bidirectional dispersal could affect the differences in natural regeneration between pine and oak forests, and they might increase the recruitment rates for oak at the edge of an adjacent community. Rodent-mediated seed dispersal could potential unintentionally affect the competition between plant communities.

Cache placement near nests by a multiple-prey loader, the Siberian chipmunk

The rapid sequestering hypothesis predicts that scatter-hoarding animals quickly sequester food items by storing seeds in caches near seed sources to reduce competition. However, tests of this hypothesis usually use food-hoarding animals with a single load or a small load size. How multiple-load animals place their caches between food sources and nests remains largely unknown. Here, we hypothesized that multiple-load animals, compared to single-load animals, may not necessarily sequester food items but adopt alternative hoarding strategies due to their multiple-load ability. In this study, we presented seeds at different distances from the nests of the multiple-loading Siberian chipmunk, Tamias sibiricus, and mapped the spatial distribution of their caches in multiple-compartment enclosures to test our hypothesis that a multiple-prey loader will consistently establish caches near nests rather than rapidly sequester near the seed source. By using multiple-compartment enclosures with different distances between the seed source and nests, and given potential intra- and interspecific competition, we found chipmunks consistently placed their caches near nests but away from the seed source. Cache placement near nests may serve as an alternative strategy that not only guarantees a maximum harvest rate at the seed source but also ensures effective cache defence near nests. Moreover, scatter-hoarding seeds near nests may alternatively guarantee a food supply if larder-hoarded seeds are depleted or lost. Unlike seeds sequestered near food sources, caches near nests imply long dispersal distances for seeds in our study. Therefore, scatter hoarding by multiple-prey loaders is expected to be ecologically important for the structure and function of tree communities, especially in ecosystems in which seeds depend on food-hoarding animals for dispersal and germination.

Seed harvest by scatter-hoarding yellow pine chipmunks (Tamias amoenus)

Seed-caching rodents store large quantities of seeds during the summer and autumn but the number of stored seeds has rarely been estimated. Understanding how many seeds each individual stores has implications for energetics during the period of food scarcity, and the number of seeds scatter hoarded has implications for how well animals disperse the seed of plants and thereby effect ecological processes. The number of seeds of antelope bitterbrush (Purshia tridentata) and Jeffrey pine (Pinus jeffreyi) scatter hoarded by yellow pine chipmunks (Tamias amoenus) was estimated in a year of good seed production. Both of these plant species are adapted for seed dispersal by scatter-hoarding animals. Individual chipmunks scatter hoarded an estimated 29,629 bitterbrush seeds and 5,945 Jeffrey pine seeds each year. These estimates are likely underestimates and do not include the many thousands of seeds eaten during the harvest period. Combined, the number of seeds of these two species that chipmunks scatter hoard in soil provided 2.8 times more energy than required to survive the autumn and winter. Populations of yellow pine chipmunks have the potential to scatter hoard nearly a million seeds per hectare in good seed years.

Evidence of high individual variability in seed management by scatter-hoarding rodents: does ‘personality’ matter?

The predation and dispersal of seeds by scatter-hoarding animals is one of the most studied processes in the context of animal–plant interactions. Seed management by these animals has been traditionally approached at the population level: the patterns documented in the field are assumed to be similar for all individuals of the population and the variability within the population is considered to be random noise. However, little is known about to what extent this variability responds to different and consistent behaviours between individuals. The aim of this study was to analyse the individual variation and consistency in behaviour of scatter-hoarding rodents within a population. As our model we used the wood mouse, Apodemus sylvaticus, a key disperser of holm oak acorns, Quercus ilex, which, in turn, suffers high predation pressure by the common genet, Genetta genetta. In two sets of laboratory experiments, we compared the variance and consistency in behaviours and acorn management due to individual differences with that due to manipulation, using genet scents, of the perceived predation risk. Genet scents reduced the activity (i.e. time out of the refuge) in all wood mice, but the differences and consistency in activity between individuals accounted for most of the variance. Also, mice showed different and consistent stress or relaxed behaviours. Most of the variance in seed management variables, such as dispersal distance and seed size selection, was explained by consistent differences between individuals across scent treatments. The increase in stress behaviours and decrease in relaxed behaviours were positively related to dispersal ability (i.e. longer distances and larger acorns). Our study highlights the importance of considering the individual component of behaviour in scatter-hoarding rodents. This fine-scale level, largely overlooked in the ecological framework, will help to increase our understanding of seed management by scatter-hoarding animals.

Seed value influences cache pilfering rates by desert rodents.

Some rodents gather and store seeds. How many seeds they gather and how they treat those seeds is largely determined by seed traits such as mass, nutrient content, hardness of the seed coat, presence of secondary compounds, and germination schedule. Through their consumption and dispersal of seeds, rodents act as agents of natural selection on seed traits, and those traits influence how rodents forage. Many seeds that are scatter-hoarded by rodents are pilfered, or stolen, by other rodents, and seed traits also likely influence pilfering rates and seed fates of pilfered seeds. To clarify coevolutionary relationships between rodents and the plants that they disperse, one needs to understand the role of seed traits in rodent foraging decisions. We compared how the seeds of 4 species of plants that are dispersed by scatter-hoarding animals and that differ in value (singleleaf piñon pine, Pinus monophylla; desert peach, Prunus andersonii; antelope bitterbrush, Purshia tridentata; Utah juniper, Juniperus osteosperma) were pilfered and recached by rodents. One hundred artificial caches of the 4 seed species (25 per species) were prepared, and removal by rodents was monitored. Rodents pilfered high-value seeds more rapidly than the other seeds. Desert peach seeds, which contain toxic secondary compounds, were more frequently recached. Relatively low value seeds like Utah juniper and antelope bitterbrush were pilfered more slowly and were sometimes left at cache sites, and seeds of the latter species were transported shorter distances to new cache sites. The background density of seeds also appeared to influence the relative value of seeds.

Effects of rodent abundance and richness on cache pilfering.

Scatterhoarding is a common behavioral strategy to conserve food during periods of scarcity, but this type of food storage is vulnerable to theft or pilferage. A variety of environmental factors and cache characteristics influence the rate of pilferage. Here we investigate 2 environmental factors, which heretofore have not received much attention: the abundance and species richness of scatterhoarding animals in the vicinity of scatterhoarded seeds. We measured the rate of cache pilferage at 7 sites that differed in the number and species composition of granivorous rodents in western Nevada using local native seeds and sunflower seeds. We found that there was no difference between the pilferage rate of native seeds and sunflower seeds, but that sites with different rodent abundances had different pilferage rates. Pilferage rates were proportional to the abundance of scatterhoarding rodents. Scatterhoarding rodents removed seeds at the rate of 1.3%/day/rodent individual. Species richness of scatterhoarding rodents was not correlated with rates of pilferage. These results suggest that density-dependent competition for scatterhoarded seeds is a strong determinant of pilferage rates.

Scatter-hoarding animal places more memory on caches with weak odor

Although spatial memory and olfaction are crucial for cache recovery, the knowledge of whether scatter-hoarding rodents place different memories on caches with different seed odors is still lacking. We used Siberian chipmunk Tamias sibiricus and peanut kernel system to test how scatter-hoarding rodents trade off spatial memory and olfaction when retrieving paired artificial caches emitting either strong or weak odor. T. sibiricus preferred to first recover caches with strong odor across trials both in the impoverished and enriched environments. With the establishment of spatial memory on the artificial caches following the 5-day trials, time spent on retrieving the two caches significantly decreased. Although strong-odor caches were preferred to be recovered during the trials, T. sibiricus selectively searched the caches previously containing peanut kernel emanating weak odor when the odor cues were removed in the final day test in the impoverished environments, indicating that chipmunks may have associated cache odor and cache location based on previous experience in the trials. However, with the spatial and odor cues removed, all tested chipmunks failed to search the caches previously containing peanut kernels in the enriched conditions, suggesting the importance of spatial memory in directing the cache locations. These data collectively indicate that T. sibiricus may place more memory on their caches emitting weak odor for later recovery. To our best knowledge, this is the first study shows whether scatter-hoarding animals trade off spatial memory on their caches emitting different seed odors, which will help us better understand the mechanisms of cache recovery by scatter-hoarding animals. Although scatter-hoarding animals show advantage over naive animals to relocate their caches based on spatial memory, we lack the knowledge of how scatter-hoarding animals place weight on spatial memory and olfaction during recovery of cached seeds. Our results show first evidence that scatter-hoarding animals tend to place more spatial memory on caches with weak odor. Our results provide new insight into the mechanisms of how scatter-hoarding animals trade off spatial memory on their caches emanating different seed odors, which will help us better understand the mechanisms of cache recovery by scatter-hoarding animals.

Fragmentation modifies seed trait effects on scatter-hoarders’ foraging decisions

Scatter-hoarding animals are crucial in seed dispersal of nut-bearing plants. We used the holm oak Quercus ilex—wood mouse Apodemus sylvaticus mutualism as a model system to evaluate the relative importance of seed size and fat content on scatter-hoarders’ foraging decisions influencing oak dispersal and potential recruitment. We performed a field experiment in which we offered holm oak acorns with contrasting seed size (2 vs 5 g) and fat content (3 vs 11%). Moreover, to test if the strength of these seed trait effects was context-dependent, experimental acorns were placed in small fragments, where natural regeneration is scarce or absent, and forest habitats. In small fragments, rodents had to face increased intraspecific competition for acorns and reduced anti-predator cover during transportation. As a result, they became more selective to ensure rapid acquisition of most valuable food items but, in turn, transported seeds closer to avoid unaffordable predation risks. During harvesting and caching, larger acorns were prioritized and preferentially cached. Fat content only had a minor effect in harvesting preferences. In contrast, in forest sites, where rodent abundance was four times lower and understory cover was well-developed, rodents were not selective but provided enhanced dispersal services to oaks (caching rates were 75% higher). From the plants’ perspective, our results imply that the benefits of producing costly seeds are context-dependent. Seed traits modified harvesting and caching rates only when rodents were forced to forage more efficiently in response to increased intraspecific competition. However, when landscape traits limited cache protection strategies, a more selective foraging behavior by scatter-hoarders did not result in enhanced dispersal services. Overall, our result shows that successful dispersal of acorns depends on how specific traits modulate their value and how landscape properties affect rodents’ ability to safeguard them for later consumption.

Reciprocal pilfering in a seed-caching rodent community: implications for species coexistence

Cache pilfering rates have been reported to be unsustainably high in many seed-caching rodent communities, but the dynamics of pilfering is largely unknown at the community level. In this study, we examined rates of seed-cache pilfering in a species-rich community of granivorous rodents in pair-wise trials. We compared the ability of each species to pilfer from conspecifics as well as heterospecifics to determine if pilfering is symmetrical or asymmetrical in the community. During the study, pilfering was more or less symmetrical among three scatter-hoarding species of rodents, averaging 28% (SD = 26%) of caches pilfered in 24 h, while the lone larder-hoarding species was unable to pilfer and experienced cache loss at the rate of 16 ± 14% of caches in 24 h to the other species. Pilfering was reciprocal among the scatter-hoarding species among conspecifics and heterospecifics despite differences in caching behavior (cache depth, size, and location). These finding support the hypothesis of reciprocal pilfering and are consistent with theories of the coexistence of ecologically similar species by lessening the effects of competition among species at the resource level and demonstrate that species with a pilfering disadvantage may need to exhibit different caching behaviors (e.g., larder-hoarding) to prevent competitive exclusion. Many rodents scatter-hoard seeds to survive periods when other food is scarce. Because these caches are usually undefended, individuals may experience significant theft of seeds. We reasoned that individuals that scatter-hoard seeds extensively are likely to have many of their caches pilfered, and that to counteract this loss, they should also be very effective pilferers of other animal’s caches. Conversely, animals that seldom scatter-hoard seeds are likely to be poor pilferers. This suggests that the ability to pilfer is part of the adaptive strategy of scatter-hoarding animals and that the more they scatter-hoard, the more they pilfer. Individuals that are unable to replace lost caches may not survive periods of food scarcity. There should be intense competition for stored seeds within communities of scatter-hoarding rodents, and this competition is manifested not only at the time of seed harvest but also as pilferage of cached seeds. In such communities, we expect pilferage to be reciprocal, or nearly equal among scatter-hoarding species, and thereby contribute to coexistence.

Caching for where and what: evidence for a mnemonic strategy in a scatter-hoarder.

Scatter-hoarding animals face the task of maximizing retrieval of their scattered food caches while minimizing loss to pilferers. This demand should select for mnemonics, such as chunking, i.e. a hierarchical cognitive representation that is known to improve recall. Spatial chunking, where caches with the same type of content are related to each other in physical location and memory, would be one such mechanism. Here we tested the hypothesis that scatter-hoarding eastern fox squirrels (Sciurus niger) are organizing their caches in spatial patterns consistent with a chunking strategy. We presented 45 individual wild fox squirrels with a series of 16 nuts of four different species, either in runs of four of the same species or 16 nuts offered in a pseudorandom order. Squirrels either collected each nut from a different location or collected all nuts from a single location; we then mapped their subsequent cache distributions using GPS. The chunking hypothesis predicted that squirrels would spatially organize caches by nut species, regardless of presentation order. Our results instead demonstrated that squirrels spatially chunked their caches by nut species but only when caching food that was foraged from a single location. This first demonstration of spatial chunking in a scatter hoarder underscores the cognitive demand of scatter hoarding.

Effective nut dispersal by magpies (Pica pica L.) in a Mediterranean agroecosystem.

Scatter-hoarding animals such as corvids play a crucial role in the dispersal of nut-producing tree species. This interaction is well known for some corvids, but remains elusive for other species such as the magpie (Pica pica), an abundant corvid in agroecosystems and open landscapes of the Palearctic region. In addition, the establishment of the individual dispersed seeds-a prerequisite for determining seed-dispersal effectiveness-has never before been documented for the interaction between corvids and nut-producing trees. We analyzed walnut dispersal by magpies in an agroecosystem in southern Spain. We used several complementary approaches, including video recording nut removal from feeders, measuring dispersal distance using radio tracking (with radio transmitters placed inside nuts), and monitoring the fate of dispersed nuts to the time of seedling emergence. Magpies were shown to be highly active nut dispersers. The dispersal distance averaged 39.6±4.5m and ranged from 4.1 to 158.5m. Some 90% of the removed walnuts were cached later, and most of these (98%) were buried in the soil or hidden under plant material. By the time of seedling emergence, ca. 33% of nuts remained at the caching location. Finally, 12% of the cached nuts germinated and 4% yielded an emerged seedling, facilitating the transition to the next regeneration stage. The results demonstrate for the first time that magpies can be an effective scatter-hoarding disperser of a nut-producing tree species, suggesting that this bird species may play a key role in the regeneration and expansion of broadleaf forests in Eurasia.