Scatter-hoarding Behavior Research Articles

Teasing apart the effects of seed size and energy content on rodent scatter-hoarding behavior.

Scatter-hoarding rodents are known to play a crucial role in the seed dispersal of many plant species. Numerous studies have indicated that both seed size and the energy content of seeds can affect rodent foraging behavior. However, seed size is usually associated with energy content per seed, making it difficult to isolate how seed size and energy affect rodent foraging preferences. This study used 99 treatments of artificial seeds (11 seed sizes×9 levels of energy content) to tease apart the effect of seed size and energy content on rodent seed-caching behavior. Both seed traits showed significant effects, but their details depended on the stage of the rodent foraging process. Seeds with higher energy content were harvested more rapidly while seed size only had a modest effect on harvest rate. However, after harvesting, seed size showed a much stronger effect on rodent foraging behavior. Rodents’ choice of which seeds to remove and cache, as well as seed dispersal distance, seemed to reflect an optimal seed size. Our findings could be adapted in future studies to gain a better understanding of scatter-hoarding rodent foraging behavior, and the co-evolutionary dynamics between plant seed production and seed dispersers.

The Interplay of Habitat and Seed Type on Scatterhoarding Behavior in a Fragmented Afromontane Forest Landscape

AbstractScatterhoarding by rodents, whereby seeds are collected and stored for later consumption, can result in seed dispersal. Seeds may be covered in litter on the forest floor (cached) or buried. This is particularly so in the Neotropics for large, nutritious seeds, and where primary dispersers are rare or missing. In African forests, contemporary anthropogenic pressures such as hunting, forest degradation, and fragmentation are contributing toward major declines in large frugivores, yet the potential for scatterhoarding to mitigate this loss is largely unknown. In this study, we used thread‐marked seed to explore the balance between seed predation and dispersal by rodents in Afromontane forest. We studied two tree species in three habitats: (1) continuous forest; (2) continuous forest edge, and (3) small, degraded riparian forest patches. We found that seed removal rates were high and almost the same in all three habitats for both tree species, but that the predation/dispersal balance differed among habitats. In continuous forest, more seeds of each species were scatterhoarded than depredated, and rates of scatterhoarding differed between the two species. In all habitats, burying seeds up to 2 cm belowground was more common than caching. Distances seeds were moved was approximately five times greater in continuous forest than in forest edge or riparian patches. We found strong evidence to suggest that the African pouched rat, Cricetomys sp. nov was responsible for the scatterhoarding.

Interactions between a seed-eating neotropical rodent, the Azara's agouti (Dasyprocta azarae), and the Brazilian ‘pine’Araucaria angustifolia

We studied the seed predation and scatter-hoarding behaviour of Azara's agoutis Dasyprocta azarae (Rodentia: Dasyproctidae) in relation to the seeds of the Brazilian ‘pine’, Araucaria angustifolia (Araucariaceae), the rodent's main winter food source. We compared seed-removal rates, seed-caching rates, cache distances and recovery rates between a summer period of food abundance (with a low demand for A. angustifolia seeds and no such seeds naturally available) and a winter period of food scarcity (with a high demand for A. angustifolia seeds). We investigated whether the relative seed value affected the rodent's seed-handling behaviour. We predicted that during the high seed-demand period (winter): (1) cache distances would be greater; (2) fewer seeds would be stored; (3) more seeds would be recovered and the seed-recovery time would be lower. In support of our first two predictions, the caching distances were greater in winter (mean ± SE = 15.67 ± 5.11 m) than in summer (9.40 ± 1.59 m), and agoutis hoarded >9 times more seeds in summer (55) than in winter (6). Our third prediction was not supported, and the proportion of unrecovered caches and buried seed recovery times did not differ between winter (mean ± SE = 3.00 ± 0.00 days, n = 5 seeds) and summer (11.05 ± 3.68 days, n = 20 seeds). The high resource density (during summer) rather than the density of A. angustifolia seeds likely influenced seed fate. Agoutis acted mainly as predators, leaving few intact seeds, caching a low proportion of handled seeds (≅ 8%) and rapidly consuming the caches. Agoutis may cache seeds to keep them safe from competitors on a short-term basis rather than maintaining medium- or long-term reserves for use during food-scarcity periods.

Scatter-Hoarding Rodents Prefer Slightly Astringent Food

The mutualistic interaction between scatter-hoarding rodents and their seed plants is highly complex yet poorly understood. Plants may benefit from the seed dispersal behavior of rodents, as long as seed consumption is minimized. In parallel, rodents may maximize foraging efficiency and cache high-quality resources for future consumption. Defensive compounds, such as tannins, are thought to be a major mechanism for plant control over rodent behavior. However, previous studies, using naturally occurring seeds, have not provided conclusive evidence supporting this hypothesis. Here, we test the importance of tannin concentrations on the scatter-hoarding behavior of rodents by using an artificial seed system. We combined feeding trials and field observations to examine the overall impact of seed tannin concentrations on rodent behavior and health. We found that rodents favored seeds with an intermediate amount of tannin (∼5%) in the field. Meanwhile, in rodents that were fed a diet with different tannin content, only diets with high tannin content (25%, 15%, and 10%) caused a significant negative influence on rodent survival and health. Significant differences were not found among treatments with tannin levels of 0–5%. In contrast to many existing studies, our results clearly demonstrate that scatter-hoarding rodents prefer slightly ‘astringent’ food. In the co-evolutionary arms race between plants and animals, our results suggest that while tannins may play a significant role in reducing general predation levels by the faunal community, they have no precise control over the behavior of their mutualistic partner. Instead, the two partners appear to have reached an evolutionary point where both parties receive adequate benefits, with the year-to-year outcome being dependent on a wide range of factors beyond the control of either partner.

Effects of seed quality and seed location on the removal of acorns and beechnuts

We examine whether different guilds of foragers remove seeds differentially according to seed quality (seed size and insect infestation) and seed location (habitat and microhabitat) in a mixed oak-beech forest. Video recordings indicated that the wood mouse (Apodemus sylvaticus) was first to encounter seeds. Foragers preferred acorns to beechnuts, large to small size and sound to infested. Nevertheless, infested seeds were removed by rodents even when sound seeds were present. Seeds that were not preferred by scatter-hoarding rodents remained longer on the ground and were more vulnerable to predation and desiccation (4% moisture loss per day). However, seeds that were removed by scatter-hoarders were moved away from their mother trees (96%) and cached individually (32%), increasing their moisture content (3% per day). Buried seeds, simulating scatter-hoarding behavior, experienced only a 17% removal after 4 months. Seed removal differences among habitats were not due to habitat attributes but to the spatial distribution of rodent-preferred microhabitats. Thus, a significant lower seed removal was observed under the tree canopy with no shrubs. However, seed removal in forest gaps with deadwood cover was not significantly different from the preferred microhabitat (under shrub cover). In pure beech forests, seed removal by rodents only occurred under Ilex aquifolium (the only perennial cover) and under woody debris. This study concludes that seed quality and seed location determine the contribution of different removers (predators vs. dispersers), their seed selection and their removal speed, leading to different seed fates which will eventually affect tree regeneration.

Effect of logging on rodent scatter‐hoarding dynamics in tropical forests: implications for plant recruitment

The present study tested the hypothesis that logging affects the scatter-hoarding behavior of rodents, which, in turn, negatively affects the quantity and quality of Pouteria campechiana (Sapotaceae) seed dispersal. A series of seed stations was established in logged and unlogged forests of ejido Señor, Yucatan Peninsula, and comparisons were made between logged and unlogged forests in terms of: (i) seed removal; (ii) number of seeds hoarded; (iii) hoarding distance; and (iv) the number of recruits and the survival of hoarded seeds. The number of both hoarded and removed seeds was significantly higher in unlogged sites. Furthermore, the mean distance of hoarding was greater in unlogged compared with logged sites. Although recruitment and survival were present in both logged and unlogged sites, there were more surviving seedlings in unlogged sites. The data indicate that both the quantity and quality of seed dispersal are negatively affected by logging because of a change in the rodent scatter-hoarding dynamics. These changes suggest that plant-animal interactions are crucial to the understanding of the ecology and conservation of managed tropical forests.

Comparison of survey methods for monitoring Clark's Nutcrackers and predicting dispersal of whitebark pine seeds

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How plants manipulate the scatter-hoarding behaviour of seed-dispersing animals

Some plants that are dispersed by scatter-hoarding animals appear to have evolved the ability to manipulate the behaviour of those animals to increase the likelihood that seeds and nuts will be stored and that a portion of those items will not be recovered. Plants have achieved this in at least four ways. First, by producing large, nutritious seeds and nuts that are attractive to animals and that stimulate hoarding behaviour. Second, by imposing handling costs that cause animals to hoard rather than to eat items immediately. These handling costs can take one of two forms: physical barriers (e.g. hard seed coats) that take time to remove and secondary chemicals (e.g. tannins) that impose metabolic costs. Third, by masting, where a population of plants synchronizes reproductive effort, producing large nut crops at intervals of several years. Mast crops not only satiate seed predators, but also increase the amount of seed dispersal because scatter-hoarding animals are not easily satiated during caching (causing animals to store more food than they can consume) but are satiated during cache recovery. And fourth, by producing seeds that do not emit strong odours so that buried seeds are less likely to be discovered. These, and perhaps other, traits have increased the relative success of plant species with seeds dispersed by scatter-hoarding animals.

Can forest fragmentation disrupt a conditional mutualism? A case from central Amazon

This is the first study to investigate whether scatter-hoarding behavior, a conditional mutualism, can be disrupted by forest fragmentation. We examined whether acouchies (Myoprocta acouchy, Rodentia) and agoutis (Dasyprocta leporina, Rodentia) changed scatter-hoarding behavior toward seeds of Astrocaryum aculeatum (Arecaceae) as a consequence of a decrease in forest-patch area. Our study was conducted at the 30-year-old Biological Dynamics of Forest Fragments Project, in central Amazon, Brazil. We tested whether forest size affected the number of Astrocaryum seeds removed and scatter-hoarded (and likely dispersed) by acouchies and agoutis, as well as the distance that the seeds were hoarded. The study extended over three seasons: the peak of the rainy season (March-April), the transition between the rainy and the dry season (May-June), and the peak of the dry season (August-September). Our results revealed that the number of seeds removed was larger in smaller fragments, but that the percentage of seeds hoarded was much lower, and seeds eaten much higher, in 1-ha fragments. Moreover, fewer seeds were taken longer distances in fragments than in the continuous forest. Site affected the number of seeds removed and season affected the percentage of seeds hoarded: more seeds were removed from stations in one site than in two others, and hoarding was more important in April and September than in June. Our study reveals that scatter-hoarding behavior is affected by forest fragmentation, with the most important disruption in very small fragments. Fragmentation converts a largely mutualistic relationship between the rodents and this palm in large forest patches into seed predation in small fragments.

Inter‐Population Variation in Hoarding Behaviour in Degus,Octodon degus

AbstractAlthough foraging comprises a set of behaviours that typically vary with resource availability and/or climatic conditions, few studies have analysed how foraging, particularly food hoarding, varies across populations inhabiting different habitats. We carried out an inter‐population study on foraging behaviour with the caviomorph rodentOctodon deguscollected from two geographically separated populations in central Chile, with contrasting climates. One population was located in a mountainous zone (at 2600 m elevation) characterized by a high‐altitude climate. The other population was from a low‐altitude Mediterranean climate zone (450 m elevation). Under laboratory conditions, we measured population‐specific differences in food consumption and hoarding by recording food utilization. We also assessed whether acclimation played a role in behavioural differences, by using two different sets of animals that had been in captivity for (1) 2 wk or (2) 6 mo, under common conditions. The results showed variation in food hoarding between populations. Individuals from the low‐altitude population exclusively displayed scatter hoarding behaviour. In contrast, high‐altitude animals carried out larder hoarding combined with scatter hoarding (37.4% and 62.6% respectively). There was no intra‐population variation between degus with different acclimation periods under captivity, thus inter‐population differences in larder hoarding were maintained despite 6 mo of acclimation to a common environment. The geographic variation observed suggests that larder hoarding is favoured under harsher environmental conditions. We discuss some probable causes for this variation. The lack of effect of acclimation suggests that inter‐population differences in larder hoarding might be the result of local adaptation or, less likely, it corresponds to an ontogenetically acquired irreversible behaviour.

Reciprocal pilferage and the evolution of food-hoarding behavior

Current theories of food-hoarding behavior maintain that hoarding can be adaptive if a hoarder is more likely than any other animal to retrieve its own caches. A survey of the literature indicated that the hoarder often has a recovery advantage when searching for items it has stored, but levels of cache pilferage are often so high (2--30% per day) that at least for some long-term food hoarders, the caching animal is unlikely to recover a significant amount of its stored food. Except in a few cases (acorn woodpeckers and beavers), kin selection cannot explain the high levels of pilferage observed. We suggest that some small solitary animals with overlapping home ranges (e.g., most rodents, chickadees, and tits) are able to tolerate high levels of cache pilferage. Pilferage is not as damaging to these animals as it might otherwise be because many interspecific and all intraspecific cache pilferers also cache food. These or similar food caches can be pilfered later by the original food hoarder. In other words, pilfering in these species is often reciprocal, and because it is reciprocal, it can be tolerated. We argue that caching systems based on reciprocal pilfering can be stable and are not necessarily susceptible to cheaters, animals that pilfer food but do not scatter hoard food themselves, and we introduce a model of food hoarding to support this argument. These food-caching systems based on reciprocal pilfering resemble cooperative behavior, but the behavior is actually driven by the selfish interests of individuals. This theory of scatter-hoarding behavior based on reciprocity has important implications for the ways that food-hoarding animals interact with inter- and intraspecific competitors. Copyright 2003.

Intraspecific variation in seed size affects scatterhoarding behaviour of an Australian tropical rain-forest rodent

Vertebrate seed dispersers could impact the evolution of seed size or alter the pattern of seedling recruitment if they responded differently to seeds of varying size (Jordano 1995). For example, models of seed caching by birds and mammals predict that seeds of higher nutritive value should be placed farther from parent trees and in lower densities than lower quality seeds (Clarkson et al. 1986, Stapanian & Smith 1978, Tamura et al. 1999). Comparisons of seed removal rates among tropical tree species in South-East Asia (Blate et al. 1998) and Australia (Osunkoya 1994) failed to show a relationship between seed size and removal rate, although the probability that a seed was scatterhoarded by agoutis (Dasyprocta punctata) in a neotropical rain forest increased with interspecific seed size (Forget et al. 1998).

The Effects of Seed Value on the Caching Behavior of Yellow Pine Chipmunks

Yellow pine chipmunks scatter-hoard a variety of seed types, and these seeds vary considerably in their inherent value to the chipmunks. Models of optimal scatter hoarding behavior predict that animals should space items of greater value farther apart than items of lesser value to discourage theft from cache robbers. This prediction was tested by comparing how yellow pine chipmunks Tamias amoenus distribute Jeffrey pine Pinus jeffreyi and antelope bitterbrush Purshia tridentata seeds to cache sites. Chipmunks prefer Jeffrey pine seeds over bitterbrush seeds ; the pine seeds provide energy 3.8 times faster and contain a higher proportion of fat than bitterbrush seeds. The prediction of the model was upheld on several counts : chipmunks carry Jeffrey pine seeds farther from source plants to cache sites, they space Jeffrey pine seed caches farther apart, and they place fewer Jeffrey pine seeds than bitterbrush seeds in individual caches. Yellow pine chipmunks appear to be sensitive to the qualities of the food items they store and modify their caching behavior to reduce loss of more valuable food items.

What currency do scatter-hoarding gray jays maximize?

Gray jays (Perisoreus canadensis) cache thousands of food items during each summer for use during the subsequent winter. Previous work on the economics of gray jay scatter-hoarding behavior was based on the assumption that the jays maximize the rate at which they store food energy; alternative currencies were not considered. Here we develop and test models based on two currencies, net rate (net recoverable energy stored per unit time) and efficiency (recoverable energy stored per unit energy expended). Our experiment involved providing gray jays with two options. After collecting a single food item upon arrival at a feeding apparatus, a jay could wait for two additional food items to become (simultaneously) available and then transport all three items for storage in scattered arboreal sites. Alternatively, the jay could immediately transport the single item to a storage site and return to the source repeatedly for additional single-item loads. By incrementally increasing the amount of time jays were required to wait for multipleitem loads, we were able to determine how long jays would wait before switching from multiple- to single-item caching trips. In contrast with the finding in a variety of species that efficiency-maximization models provide a better account of foraging behavior, the net rate-maximization model was a better predictor of the jays' switching point than was the efficiency-maximization model (Figs. 2 and 3). We discuss these conflicting results in the context of recent theory that describes the conditions favoring rate- versus efficiency-maximizing behavior (Ydenberg et al. 1994).

Gray Jay Scatterhoarding Behavior, Rate Maximization, and the Effect of Local Cache Density

A model is presented that concerns how a scatterhoarder should distribute food items taken from an ephemeral, locally abundant source among cache sites scattered throughout its territory, and how such an animal should adjust the way it distributes its caches in response to the presence of previously made caches. The model assumes that such an animal behaves in a manner that maximizes the rate at which recoverable (surviving) food energy is stored. One application of this model concerns how a scatterhoarder should respond when it encounters a food source in the same location as a previously exploited one. Such spatial overlap of food sources through time may be a common occurrence for animals such as Gray Jays Perisoreus canadensis which store thousands of food items throughout their territory during the summer months for use during winter. Under the conditions of the experiment, but not under all theoretical conditions, the model predicts that Gray Jays should space their caches more widely during subsequent encounters with a source at a given location. Consequently, they should take longer to cache a given number of food items, and, because fewer of these caches will survive, the number of recoverable caches made per unit of time spent caching should be reduced. A field experiment using Gray Jays is described. As predicted, jays compensated for the local density of extant caches by transporting food items farther from the source during second encounters with a source in a given location. These results indicate that the jays, at least for the conditions of this experiment, are not forced by a memory constraint to behave in some standard fashion when they encounter a point food source. The theoretical and empirical results begin to show how scatterhoarders, by flexibly adjusting their behavior in response to previously made caches, may approach the maximal rate of storage of recoverable food throughout their territory over the long term.

Caching Behaviour in the Gray Jay and the Source-Departure Decision for Rate-Maximizing Scatterhoarders

AbstractWe developed a model that concerns, in part, how long a scatterhoarder should persist in caching food from an ephemeral, locally abundant source ('bonanza') before moving on in search of other sources. The model assumes that an animal scattering food caches for later use behaves in a manner that maximizes the rate at which it stores recoverable (surviving) food in its habitat. It is shown theoretically that under some conditions it is better not to cache all available food but instead to move on in search of other food sources. This 'source-departure decision' for scatterhoarders is analogous to the patch-departure decision for animals that forage among food patches. It is shown that whether, and at what point, a 'moving-on threshold' is reached should depend on the size of the source, the strength of density-dependent cache theft, and the abundance of sources in the habitat. A field experiment was performed to test the qualitative prediction that gray jays, Perisoreus canadensis, should not persist as long in caching food when a day-long opportunity for caching is restricted to a single source (single-source treatment) as when such an opportunity is divided among a series of disjunct sources (multiple-source treatment). In the single-source treatment, jays tended to cache at lower overall rates, transport food items to more distant cache sites, and spend less time caching. These tendencies became more pronounced later in the day. However, although the rate of caching approached zero in the single-source treatment, the jays did not completely cease caching. This apparent violation of the model is attributed to the behaviour of recaching, a facet of gray jay scatterhoarding behaviour that was not built into the model. This retrieval and redistribution of previous caches resulted in the stabilization of the density of caches near the source. In addition, this switch from single- to multiple-load caching trips arguably would make it economical for gray jays to continue to make caching trips from a source beyond the source-departure point predicted by the model. Our theoretical and empirical results begin to show how scatterhoarders may behave in a manner that maximizes the long-term average rate of storage of recoverable food energy throughout their habitat.

Spatial patterns of food storage by Merriam's kangaroo rats

We investigated scatter-hoarding behavior by Merriam's kangaroo rats (Dipodomys merriami) in a complex arena in the laboratory. Animals cached seeds in four sand-filled boxes connected by runways, with an artificial burrow at one end of the system and a food source at the other. Animals initially cached more seeds in boxes close to the food source, but amounts cached became more evenly distributed among boxes as sessions progressed. The results were consistent with the hypothesis that scatter hoarding by kangaroo rats may represent a compromise between rapidly sequestering seeds, hence making them unavailable to nondigging competitors, and spacing-out caches, making them less vulnerable to pilferage by other rodents.