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.     

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.     

Substrate type affects caching and pilferage of pine seeds by chipmunks

The abiotic environment often influences the ways in which animalsinteract. By affecting the cues associated with buried seeds,the type of substrate used by seed-caching rodents may alterthe relative probabilities of cache pilferage and cache retrieval.We predicted that, after a wildfire, the presence of ash wouldimpair rodents' ability to smell pine seeds on the forest floor.In a laboratory experiment, we compared the foraging success,caching frequency, and cache recovery of chipmunks (six Tamiasamoenus and six T. quadrimaculatus) in ash versus sand substrates.Initial results supported our hypothesis: chipmunks found only2.3% of 108 caches of Jeffrey pine (Pinus jeffreyi) seeds thatwe buried in ash but found 98% of caches in sand. However, chipmunksmade as many or more of their own caches in ash compared withsand (48% for T. amoenus, 73% for T. quadrimaculatus.) Whenforaging for seeds cached in ash by themselves and by otherindividuals, they found significantly higher proportions oftheir own caches (62%) than of caches made by others (25%).However, when foraging in sand, they found high proportionsboth of their own caches and those of others (86 versus 81%).These results suggest that olfaction is less effective in ashthan in sand, that spatial memory enables chipmunks to recovertheir own caches in ash, and that caching in ash may allow animalsto avoid pilferage of stored food. As chipmunks are importantdispersers of seeds, changes in their foraging patterns or competitiveinteractions after fire could significantly affect pine regeneration.     

同种或异种干扰对花鼠分散贮藏点选择的影响

同种和异种干扰竞争可以增强花鼠(Tamias sibiricus)分散贮食强度,但对其贮藏点选择的影响还不清楚.在半自然围栏内,研究了同种(干扰源为不同性别花鼠)或异种(干扰源为大林姬鼠,Apodemus peninsulae)干扰竞争对花鼠贮藏点选择的影响.结果发现:(1)同种和异种干扰竞争均显著降低了花鼠在高竞争区内的贮藏比例;(2)同种个体存在时,雌性花鼠显著降低了在高竞争区内的贮藏比例,雄性花鼠则显著增加了在中竞争区的埋藏比例.结果表明,花鼠贮藏食物时会避开高竞争区域以降低同种或异种的盗食损失,同时雌雄个体对同种竞争干扰的响应有所差异.     

Seasonal variation in the effect of cache pilferage on cache and body mass regulation in Carolina chickadees: what are the trade-offs?

Current dynamic optimization models predict that animals shouldrespond to cache pilferage by decreasing the probability ofcaching food and by increasing internal fat storage to compensatefor a reduction in cache size. We tested these predictions underlaboratory conditions with variable food access (four 15-minintervals/day). Carolina chickadees (Poecile carolinensis) weresubjected to two environments: under pilferage conditions, one-quarterof their cached seeds were stolen every 0.5 h, and under no-pilferageconditions, seeds were left in place. Half the birds startedwith pilferage conditions and were then switched to the no-pilferagecondition; the other half started with no pilferage and werethen switched to pilferage conditions. The experiment was conductedover the course of a year to test for seasonal variation inthe response to seed pilferage. The birds responded to seedpilferage by taking more seeds from a feeder, suggesting thatthey monitored cache availability. Alternatively, the birdsmay have taken additional seeds from the feeder in responseto increased hunger caused by a loss of cached food. Contraryto our prediction, birds cached a higher percentage of seedsfrom the feeder when cached seeds were pilfered than when cacheswere left in place. Treatment order also affected caching behaviorfor all but the summer birds: chickadees initially subjectedto pilferage stored a higher proportion of seeds than thoseinitially subjected to no pilferage. Caching percentages inthe summer were unaffected by cache pilferage. Caching rates(number cached/day) also followed the same trends: rates werehigher when seeds were pilfered than when seeds were not pilfered,and there was a treatment-order effect for all but the summerbirds. Variation in body mass also failed to match predictedtrends. All birds exhibited a monotonic increase in mass asthe experiments proceeded, irrespective of treatment order.Controlling for this monotonic increase in mass, an analysisof residual variation in body mass indicated that birds gainedless weight when seeds were pilfered than when seeds were leftin place. Finally, birds tested in the fall and spring wereheavier than those tested in the summer. These results failto support the relationship between cache maintenance and bodymass regulation predicted by current models of energy regulation.We discuss the applicability of three hypotheses for the observedtrends.     

Dietary circumvention of acorn tannins by blue jays

Blue jays consume large quantities of acorns to fuel energy-demanding caching flights in the fall. Yet blue jays possess no known physiological adaptation to counter the negative effects of a high tannin diet on protein digestion. Dietary experiments were conducted to determine if blue jays could subsist on an acorn-only diet, and if they could not, to determine whether supplements of acorn weevil larvae (Curculio), present inside acorns, enabled them to maintain their mass. Comparative tannin assays also were conducted on Lepidobalanus (low tannin; white oak) and Erythrobalanus (high tannin; pin oak) acorns using radial diffusion assay. Captive jays consumed considerable acorn material, yet were unable to maintain mass on ad lib. acorn-only diets or on an acorn +1.5 g larvae/day supplement. There were no significant differences in mass loss between high and low tannin diets. In contrast, blue jays were able to stabilize mass on a diet of acorns +5.0 g larvae supplement/day. These results suggest that acorn weevil larvae, or perhaps other insects, counteract the effects of acorn tannins in the jay diet allowing jays to subsist largely on acorns during the fall caching season. Oak demographic processes may be partly regulated by a tri-trophic relationship among plant, insect and bird. Acorn weevil larvae, considered damaging to oak populations, may actually facilitate oak recruitment and population vagility in the long-term.     

The Proximate Basis of the Oak Dispersal Syndrome: Detection of Seed Dormancy by Rodents

Previously we have shown how a range of physical and chemicalcharacteristics of acorns influences the behavioral decisionsof food-hoarding rodents which in turn affects the dispersal,establishment and spatial arrangement of oaks. One such behaviorinvolves the selective caching of acorns of red oaks (subgenus:Erythrobalanus) over those of white oaks (Quercus) because ofreduced perishability that results from delayed germinationof acorns in the red oak group. In this study, we sought toidentify the specific proximate cues (visual and olfactory)that eastern gray squirrels (Sciurus carolinensis) use whenmaking these decisions. In two series of field experiments,we presented individual, free-ranging animals with pairs ofexperimentally altered acorns (that differed with respect toa single chemical or visual characteristic) and recorded theirfeeding and caching responses. Squirrels cached artificial acornswith pericarps (shells) of red oak acorns and ate those withshells of white oak regardless of the internal chemical compositionof either type of acorn. Only when the shells of artificialacorns were first soaked in acetone (to remove potential chemicalodors) did animals eat artificial acorns made with the shellsof red oak acorns. Squirrels also ate one-year old red oak acornsthat had broken dormancy, even when they exhibited no signsof germination. We argue that a chemical cue in the shell ofacorns is important in the detection of seed dormancy and thedecision to cache acorns, and that such a cue might ultimatelycontribute to the differential dispersal of red and white oaksby rodents.     

Rodents change acorn dispersal behaviour in response to ungulate presence

Small rodents are prominent seed predators, but they also favour plant recruitment as seed dispersers. The direct interactions of ungulates on plants are more one‐sided and negative, as they mainly reduce plant recruitment through predation on seeds and seedlings. The effects of small rodents and ungulates on plant recruitment have been considered and studied as independent episodes within plant regeneration cycles. However, ungulate–rodent interactions and their potential effects on plant regeneration have not been considered so far. A number of studies have recently documented ungulate effects on the abundance, diversity and spatial distribution of small rodents. Here, we hypothesize that ungulates may also affect rodent seed dispersal behaviour. We monitored acorn dispersal by small rodents (Mus spretus and Apodemus sylvaticus) in oak woodlands with and without exclosures for large ungulates, mainly red deer, Cervus elaphus, and wild boar, Sus scrofa. The study was carried out in a typical Mediterranean Holm oak, Quercus ilex, forest throughout the acorn fall season in 2003 and 2004. We found that, in both years, the proportion of acorns cached and not recovered in the short‐term was, on average, lower in the presence (1.4%) than in the absence (19.9%) of ungulates. Acorn dispersal distances were not affected by ungulate presence in either year. However, ungulates had an effect on the spatial distribution of dispersed seeds; rodents apparently avoided shrubs as caching sites in both years. This result was interpreted as a behavioural response to reduce the risk of cache pilferage by conspecifics, which are closely associated with shrubs in presence, but not in absence, of ungulates. Potential effects of different densities of rodents or predators were discarded, as none of them differed between the areas with and without ungulates. The present study found significant interactions between heterospecific seed and seedling consumers that had been considered as independent episodes within tree regeneration cycles. As a result of such interactions, ungulates may have negative indirect effects on oak recruitment by reducing (1) acorn caching frequency, and (2) the proportion of acorns cached under shrubs, key nurse‐plants for the establishment of Holm oak seedlings in Mediterranean areas.     

外果皮厚度和种子大小对五种栎属橡子扩散的影响

动物对种子的扩散和贮藏是一个复杂的生态学过程,常常受到种子特征的影响。有关种子特征如何影响动物对种子扩散,许多研究结果并非完全一致。我们于2009 年9 月在黑龙江东方红林场野外和围栏内释放五种栎属橡子(Quercus mongolica,Q.serrata var. brevipetiolata,Q. aliena,Q.variabilis 和Q. liaotungensis),研究种子特征对鼠类(Apodemus peninsulae, Clethrionomys rufocanus 和Tamias sibiricus)扩散和埋藏橡子的影响。野外释放结果表明:橡子大小和外果皮厚度显著影响鼠类对橡子的扩散和埋藏。鼠类偏向扩散和埋藏种皮厚的大橡子,种皮薄的小橡子则多被原地取食。种皮厚的大橡子扩散距离显著高于种皮薄的小橡子。然而,只有外果皮的厚度显著影响围栏内花鼠对橡子的扩散和埋藏,橡子大小并非主要的影响因素。种子特征影响种子扩散的效应可能在种群和群落水平上存在差异。     

Re-caching of acorns by rodents: Cache management in eastern deciduous forests of North America

Scatter-hoarding rodents such as tree squirrels selectively cache seeds for subsequent use in widely-spaced caches placed below the ground surface. This behavior has important implications for seed dispersal, seedling establishment, and tree regeneration. Hoarders manage these caches by recovering and eating some seeds, and moving and re-caching others. This process of re-caching, however, is poorly understood. Here, we use radio-telemetry to evaluate re-caching behavior for the management of acorn caches by rodents in eastern deciduous forests. We also test the hypothesis that as seeds are re-cached, the distance from the source increases. Radio transmitters were implanted in Northern red oak (Quercus rubra) acorns and presented to rodents in a natural setting over 3 seasons. We used radio-telemetry to track and document evidence of recovery and re-caching. We tracked a total of 102 acorns. Of the 39 radio-tagged acorns initially cached, 19 (49%) were cached on two or more occasions; one acorn was cached four times. The hypothesis that rodents move seeds to progressively greater distances from the source is not well-supported, suggesting that acorns are being moved within an individual's home range. Given the species of rodents in the study area, gray squirrels (Sciurus carolinensis) are the most likely to be responsible for the caching and re-caching events. Gray squirrels appear to engage in extensive re-caching during periods of long-term food storage, which has important implications for understanding how caching behavior influences acorn dispersal and oak regeneration.     

Cache site selection by chipmunks (Tamias spp.) and its influence on the effectiveness of seed dispersal in Jeffrey pine (Pinus jeffreyi)

The effectiveness of Jeffrey pine (Pinus jeffreyi) seed dispersal performed by seed-caching yellow pine chipmunks (Tamias amoenus) and lodgepole chipmunks (Tamias speciosus) was compared to that of wind dispersal in the Sierra Nevada of western Nevada. Wind-dispersed seeds typically fall under or near the parent tree. Chipmunks removed 90 and 97% of 1064 radioactive seeds from each of two simulated wind-dispersed seed shadows in less than 24 h. Wind-dispersed seeds were deployed within 12 m of the two source trees, but chipmunk caches were found from 2–69 m from the trees. Chipmunks carried nearly all seeds away from source trees, greatly reducing the density of seeds under and near source trees. Caches contained from 1–35 seeds and most were buried 7–21 mm deep. Chipmunks cached in open bitterbrush shrubland with mineral soils much more than expected and cached in closed-canopy Jeffrey pine and lodgepole pine forests with thick needle litter much less than expected. Many Jeffrey pine seedlings and saplings grow in the bitterbrush habitat and few grow in the pine forests. Ten and 20% of the original caches survived until April, the time of seed germination, at the two sites. The movement of wind-dispersed seeds is random relative to environmental variables important in seedling survival, and the wind in coniferous forests cannot quickly bury seeds. The quality of seed dispersal rendered by chipmunks was superior to that provided by the wind because the chipmunks quickly harvested seeds on the ground, moved them away from source trees, and buried them in the ground in habitats and microhabitats where they were more likely to establish new seedlings. The increased quality of seed dispersal provided by animals relative to the wind may help explain why over twenty species of pines have evolved seeds and cones that are adapted for dispersal by seed-caching animals.     

The role of birds and mammals in Korean pine (Pinus koraiensis) regeneration dynamics

This study examined the interrelationships of the fall seed-foraging guild with Korean pine (Pinus koraiensis) and its regeneration. The study took place in old-growth and secondary-growth forests in Northeastern China. Foraging behavior, seed transportation distance, and cache location of various birds and mammals were observed. Regeneration characteristics of Korean pine were also analyzed using plots in various vegetation cover types, successional stages, and topographical situations. Ten species of vertebrates were able to harvest seed from the closed-cone Korean pine. Of these, the Eurasian nutcracker, Eurasian nuthatch, red squirrel, and Siberian chipmunk were found to be potential seed dispersal agents. The nutcracker was the most important dispersal agent, easily acquiring seed with its large pointed bill, carrying up to 62 seeds in one trip, carrying seed at least 4 km, and placing seed in a variety of sites 2.5–3 cm deep in the soil. The Eurasian nuthatch carried a single seed per trip at distances less than 50 m, needed nutcrackers to open the cones and expose seed before they could acquire seed, and occasionally cached seed in the soil. Red squirrels were uncommon visitors to the tree tops of Korean pine, carried cones shorter distances than nutcrackers, and were only found under forest canopies. Human harvest of cones by knocking off branches also affected squirrel behavior and reduced future cone crops. Siberian chipmunks also collected seed from cones in trees and appeared to transport seed less than 50 m. Six other species were observed in this study successfully harvesting seed from cones but were not potential seed dispersers. Natural seedling establishment was found to be over 1000 seedlings/ha except on old-growth pine-hardwood sites. Squirrels were commonest here, but few seedlings survived past the 2nd year due to the intense shading. Second-growth forest types, including aPicea plantation where nutcrackers cached seed daily, and an old-growth pine-hardwood selective-harvest site, had the greatest regeneration. In conclusion, most natural regeneration of Korean pine in this part of its range is due primarily to the Eurasian nutcracker. Nutcrackers can aid forest managers in reaching desired stocking levels after disturbance, as well as a more natural-appearing forest. Squirrels, chipmunks, and nuthatches are minor seedling establishment agents. Korean pine seed is an important food source used by at least 22 species of forest wildlife.     

啮齿动物对不同林木种子的搬运和取食微生境选择机制

不同植物种子依靠不同的方式实现扩散,啮齿动物对林木种子搬运后在取食点微生境和贮藏方式的选择存在偏好,研究其贮藏行为与微生境的关系是探究幼苗建成的关键。在秦岭中段火地塘林区,采用标签标记法,以锐齿槲栎、华山松和油松种子为材料,探究了小型啮齿动物对松栎混交林建群种种子扩散过程的影响。结果表明:1)油松种子原地取食率显著高于锐齿槲栎和华山松种子,且啮齿动物更倾向于搬运后取食(60%)和埋藏(4.33%)华山松种子,搬运后取食距离也为华山松最大(2.49 m);锐齿槲栎小种子被搬运后埋藏的距离最大(4.92 m)。2)除华山松种子外,其他类型种子被搬运后单个取食的比例均在85%以上;油松种子不存在埋藏点,而其他类型种子90%以上均以单个形式被埋藏。3)大部分种子被啮齿动物搬运后选择在裸地丢弃;锐齿槲栎大种子(87.5%)、小种子(78.57%)和华山松种子(53.33%)较大比例被啮齿动物埋藏在灌丛下方,埋藏在裸地的种子较少。4)大部分种子在灌丛下方被取食,仅华山松种子被啮齿动物搬运到洞穴取食;除油松种子被大量原地取食外,其他类型种子被搬运到取食点的种子比例基本呈现由微生境植被复杂到简单(灌丛—草丛—灌丛边缘—裸地)而逐渐减小的趋势。种子的营养价值及取食和搬运过程中啮齿动物付出的成本是影响种子命运的关键性因子,且啮齿动物对种子埋藏和取食地点的微生境存在较明显的选择性。     

The Ultimate Basis of the Caching Preferences of Rodents, and the Oak-Dispersal Syndrome: Tannins, Insects, and Seed Germination

We have shown that eastern gray squirrels and other animalsconsistently prefer to store intact acorns from the red oakgroup rather than those from the white oak group. We hypothesizedthat the ultimate advantage to this behavior comes from thedormancy of red oak acorns. Acorns of the white oak group germinateearly in the autumn; thus, we hypothesize that avoiding germinationis the primary selective advantage to the preference for cachingred oak acorns. Here, we test two alternative hypotheses toexplain the benefits of this caching preference: 1) storingred oak acorns allows the high tannin concentrations in redoak acorns to decline (making them more palatable), and 2) storingred oak acorns minimizes losses to insects, presuming they areless infested with insects. We also test the effect of germinationschedule on squirrel caching preferences directly, by presentingthem with dormant red oak acorns, and red oak acorns about togerminate. We find no evidence that tannin concentrations inred oak acorns decline, although tannin levels did decline inour white oak acorns. We found high losses to insect infestationsin one white oak species, but a second white oak species lostvery little mass to insects. Finally, we found that germinationschedule directly affects squirrel caching preferences: redoak acorns that are near germination are treated like whiteoak acorns. We conclude that the primary advantage to the preferencefor caching red oak acorns is that they are less perishable,due to their dormancy. We discuss the effects of this preferenceon the dispersal of red and white oak acorns, and the subsequenteffects of differential dispersal on the ecology and evolutionof oaks.     

Weak olfaction increases seed scatter‐hoarding by Siberian chipmunks: implication in shaping plant–animal interactions

Scatter‐hoarding of seeds by animals plays an essential role in seed dispersal of plants and in shaping plant–animal interactions in forest ecosystems, but the function of scatter‐hoarding behavior is still unclear. We hypothesize that weak olfactory cues between seeds and scatter‐hoarding animals would increase scatter‐hoarding. Using a rodent–plant system of Siberian chipmunks Tamias sibiricus and Korean pines Pinus koraiensis, we tested the effects on seed scatter‐hoarding intensity by measuring and modifying the seed odor intensities and the abilities of the animals to detect seed odor. Siberian chipmunks seemed to scatter‐hoard more seeds with weaker odor signals, and Siberian chipmunks with reduced olfactory ability scatter‐hoarded more seeds, supporting our hypothesis. Our studies suggest that olfaction may have played an important role in the evolution of the strength of seed odor and scatter‐hoarding behavior of animals, and in shaping plant–animal interactions.     

槲栎超寄生橡子内象甲幼虫的适应对策

栎属植物的橡子常常受到象甲的侵害, 对橡子存活产生影响, 但有关橡子对象甲幼虫适合度影响的研究尚未见报道。本研究旨在通过对槲栎Quercus aliena种子雨进程以及象甲幼虫逃逸过程的调查, 研究二者之间的进化适应关系。结果表明： 当年槲栎的种子产量为51.92±29.26粒/m², 虫蛀率达到42.4%。虫蛀的橡子中65%以上被象甲超寄生, 且显著大于完好的橡子。在种子下落过程中, 早期从橡子中逃逸的象甲幼虫要比后期逃逸的大。对某一超寄生的橡子而言, 首先逃逸出的象甲幼虫要比随后逃逸的幼虫大。另外, 从早期脱落的橡子中逃逸的幼虫明显小于后期脱落的橡子。象甲幼虫的干重随着橡子内象甲幼虫数量的增加而显著下降。象甲幼虫寄生数量与橡子的长径和短径呈现明显的正相关关系。尽管超寄生降低了象甲虫的适合度, 但雌性成体象甲产卵过程中偏好选择大橡子在一定程度上可以减少这种不利影响。因此, 小橡子可能更容易逃脱象甲的超寄生而获得较大的存活机会。     

Impact of site‐induced mouse caching and transport behaviour on regeneration in Castanea crenata

Abstract. Dispersal and retrieval site selection by mice, transport distance, cache depth, and emergence and survival of seedlings of Castanea crenata (Japanese chestnut) were investigated by a magnet‐locating experiment in two habitat conditions (gap vs. forest understorey). Magnets were inserted into nuts (n= 450) and the nuts placed in the edge of forest gaps. Although wood mice (Apodemus speciosus and A. argenteus) initially buried nuts singly in shallow surface caches near the nut source, by the following spring these cached nuts were retrieved and re‐cached in larger, deeper caches farther from the source, particularly in forest understories, probably to reduce the threat of pilferage. All the nuts cached in the forest understories were consumed, but 4 seedlings emerged in gaps, apparently because of lower foraging activity in the gaps by the mice. Seed size was not correlated with cache depth or cache site selection. With increasing seed size, transport distance increased, particularly in gaps, possibly due to a greater potential energy gain (relative to handling cost to the cacher), or to attempts to prevent density‐ or mass‐dependent loss of caches by other foragers. Variable seed dispersal behaviour based on variation in seed size may influence the chances of colonization and distribution of the light‐demanding Castanea trees in mosaic landscapes and may play an important role in community organization and dynamics.     

A reevaluation of the logic of pilferage effects, predation risk, and environmental variability on avian energy regulation: the critical role of time budgets

We studied the effect of pilferage rates, variation in foodencounter rate, and predation risk on cache and fat-storageregulation using dynamic programming. Previous predictionsthat small birds facing increased pilferage rates should cacheless and store more body fat are not generally supported. Instead,cache investment (caching rate or percent of food cached) is predicted to be unimodal, peaking at intermediate pilferagerates. This pattern is determined, in part, by pilferage-inducedchanges in time budgets: at low pilferage rates, a marginalincrease in pilferage rates can be offset by an increase incache investment. However, increased caching increases time allocated to both caching and foraging. The increased foragingis caused by the energetic costs of caching and by the lossof energy from the cache. Increased time spent caching andforaging in turn decreases time spent resting under low predationrisk. Above some threshold pilferage rate, the marginal valueof resting exceeds the marginal value of caching, and cacheinvestment declines with further increasing pilferage rates.These patterns hold for three levels of variation in food encounterrate: time-invariant, between-day, and within-day variation;they also hold across different mean rates of food encounter.We show that previous predictions concerning decreased energy-storagelevels with increased food abundance are not supported when there is between-day variation in mean food encounter ratesand food abundance increases only on "good" days. Finally,predation risk affects the predictions described above in twoways. First, these trends assume that the birds can rest ina predator-free refuge. If the refuge is not available, birdsare predicted to cache less at higher pilferage rates irrespectiveof the absolute level of pilferage. With the refuge in place,levels of predation risk affect the skew in the pilferage-rate/cachingfunction. As a result, the relative effect of predation riskon caching intensity varies with pilfer rate. At very low pilferrates, lowered predation risk causes more caching, but loweredpredation risk under high pilferage rates can lower caching intensity, contrary to previous predictions. Surprisingly, predationrisk has an appreciable effect on body mass only when the birdis predicted to cease caching (i.e., at the highest pilferrates); otherwise a change of two orders of magnitude in theprobability of encountering predators has little effect on body mass. Our results suggest that the tradeoffs associatedwith the joint regulation of internal energy stores and externallycached stores are more complicated than previous literaturewould indicate. Our results also show that we have underestimatedthe role that time budgets play in patterns of energy regulation.     

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.     

昆虫蛀蚀对鼠类介导下的锐齿槲栎种子扩散的影响

森林鼠类的种子贮藏行为对植物的扩散和自然更新有着非常重要的影响。然而,鼠类是否具有鉴别虫蛀种子的能力还存在一定的争议。此外,鼠类的鉴别能力是否受到食物丰富度变化的影响也未见相关报道。采用标签标记法,2011年秋季(9—11月,食物丰富季节)和2012年春季(4—6月,食物匮乏季节)分别在秦岭南坡的佛坪国家级自然保护区内,调查了森林鼠类对完好和虫蛀锐齿槲栎(Quercus aliena)种子的选择差异。结果显示:1)在秋季,尽管2种类型种子的存留动态没有显著差异,但是在后期虫蛀种子的存留时间相对更长;而在春季2种类型种子的存留动态则极为显著,几乎所有的完好种子(99%)在释放后的第3天就被鼠类全部扩散,虫蛀种子的存留时间则相对较长。2)在秋季,鼠类更喜好扩散后取食完好种子;而在春季,鼠类则喜好在原地取食绝大部分的种子,并且优先取食完好种子。3)在秋季,鼠类贮藏了更多的完好种子;而在春季,尽管完好种子在释放后第1天便达到贮藏高峰,然而由于后期的大量被捕食,2种类型种子在贮藏动态上没有显示出显著差异。研究结果表明秦岭地区森林鼠类可以准确区分完好与虫蛀种子,但是食物丰富度会影响鼠类对种子的选择策略。在食物丰富的秋季,鼠类更多地选择贮藏完好种子;而在食物相对匮乏的春季,鼠类更倾向于同时取食2种类型种子。森林鼠类通过对2种类型种子的鉴别和选择,影响不同种子的命运,从而可能对种子的扩散和自然更新产生重要影响。