Clark's Nutcracker (Aves: Corvidae) Spatial Memory: Interference Effects on Cache Recovery Performance?

Clark's nutcrackers, Nucifraga columbiana, accurately v recover thousands of caches per year in the field. Previous experiments have confirmed that these birds possess excellent, long-lasting spatial-memory capabilities. We tested whether resistance to interference is one of the features of nutcracker spatial memory. Experiment 1 tested retroactive interference. Nutcrackers showed no decrease in accuracy overall but performed relatively poorly in their final recovery session. Interference is unlikely to have caused these sites to be poorly remembered because they had fewer neighbouring cache sites than better-remembered sites. Experiment 2 tested for proactive interference. Interference would have caused the experimental birds to be less accurate than control birds. Instead then were slightly more accurate. In experiment 3, nutcrackers were allowed to repeatedly view their cache sites from a cage between caching and recovery. Nutcrackers were less accurate when recovering from cache sites they had viewed. This effect may be due to changes in motivation. Order of caching had no effect on accuracy but nutcrackers were more accurate when recovering caches from central than from peripheral areas of experimental rooms. In summary, these experiments provide further evidence of the remarkable spatial-memory abilities of Clark's nutcrackers and demonstrate that these birds are highly resistant to interference effects on spatial memory. Comparative tests will be needed to test if specialized food storers are exceptionally resistant to interference in spatial memory.     

Convenience Stores: Repeated Use of Some Cache Sites by Clark's Nutcrackers (Nucifraga columbiana)

Field studies reveal that Clark's nutcrackers (Nucifraga columbiana) cache thousands of seeds in subterranean caches during the autumn in some years, and laboratory studies have shown that these caches can be recovered with high levels of accuracy. Over the life of a bird, numerous cache recovery cycles may be experienced and many of these may be in the same area. Birds may thus develop strong individual preferences for certain sites. These sites may become more memorable and used preferentially. These sites might also be more vulnerable to theft because of continual reuse. In this study, birds were allowed to cache and recover four times from the same set of potential cache sites in a large experimental room. Three of five birds used some cache sites more often than would be expected by chance. However, these birds did not place more seeds per cache, have higher recovery accuracy, or make more revisits to cache sites previously used. Birds did not create caches earlier in previously used holes until cycle 4, when birds actually cached in used sites significantly sooner than in previously unused ones. Birds neither recovered caches earlier from previously used sites nor made error probes earlier at them. Sites that were repeatedly used for caching were holes that were significantly closer to a centrally located feeder than less frequently used sites. Thus, some birds may develop slight preferences for some locations but these sites are not treated preferentially. Birds appear not to gain the advantages, nor suffer the consequences associated with repeated use of the same sites.     

Revisits to emptied cache sites by Clark's nutcrackers (Nucifraga columbiana)

During cache recovery experiments, Clark's nutcrackers (Nucifraga columbiana) often revisit cache sites that were emptied during previous recovery sessions (Kamil & Balda 1985). In the current experiments, nutcrackers were allowed to cache pine seeds and recover them in several recovery sessions. The results of two experiments demonstrate that neither leaving signs of previous digging activity nor leaving many pine seeds in the caches affects the tendency to revisit.     

Ecosystem Services from Keystone Species: Diversionary Seeding and Seed‐Caching Desert Rodents Can Enhance Indian Ricegrass Seedling Establishment

Seeds of Indian ricegrass (Achnatherum hymenoides), a native bunchgrass common to sandy soils on arid western rangelands, are naturally dispersed by seed‐caching rodent species, particularly Dipodomys spp. (kangaroo rats). These animals cache large quantities of seeds when mature seeds are available on or beneath plants and recover most of their caches for consumption during the remainder of the year. Unrecovered seeds in caches account for the vast majority of Indian ricegrass seedling recruitment. We applied three different densities of white millet (Panicum miliaceum) seeds as “diversionary foods” to plots at three Great Basin study sites in an attempt to reduce rodents' over‐winter cache recovery so that more Indian ricegrass seeds would remain in soil seedbanks and potentially establish new seedlings. One year after diversionary seed application, a moderate level of Indian ricegrass seedling recruitment occurred at two of our study sites in western Nevada, although there was no recruitment at the third site in eastern California. At both Nevada sites, the number of Indian ricegrass seedlings sampled along transects was significantly greater on all plots treated with diversionary seeds than on non‐seeded control plots. However, the density of diversionary seeds applied to plots had a marginally non‐significant effect on seedling recruitment, and it was not correlated with recruitment patterns among plots. Results suggest that application of a diversionary seed type that is preferred by seed‐caching rodents provides a promising passive restoration strategy for target plant species that are dispersed by these rodents.     

贮藏点深度、大小及基质含水量对花鼠找寻红松种子的影响

2012年8-10月,在黑龙江省伊春市带岭林业局东方红林场,通过人工围栏控制实验,研究了贮藏点深度、大小及基质含水量对花鼠找寻红松种子的影响。发现：(1) 埋藏深度显著影响花鼠对贮藏点的找寻率,埋藏深度为 1 cm 和 2 cm 的找寻率显著高于 4 cm 和 6 cm。(2) 埋藏点大小对花鼠发现种子也有显著影响,埋藏点越大,花鼠发现贮藏点的比例越高。(3) 高的基质含水量利于花鼠找寻贮藏点。结果表明,围栏条件下食物贮藏点深度、大小及基质含水量的改变能显著影响花鼠对贮藏点的找寻。     

An experimental analysis of cache recovery in Clark's nutcracker

Five hypotheses of cache recovery behaviour in Clark's nutcracker (Nucifraga columbiana) were examined experimentally. Most caches were made in soil within 5 cm of conspicuous large objects. Both seed-caching and non-seed-caching nutcrackers were able to locate caches. Seed-caching nutcrackers relocated caches using large objects as remembered visual cues. Soil microtopography and small (<2 cm diameter) objects may be used as cues to facilitate cache recovery but are not essential. Non-seed-caching nutcrackers located caches by using soil disturbances at cache sites as visual cues and by searching preferentially near objects where caches were concentrated. Success rates of seed-caching nutcrackers ranged from 52 to 78% and those of non-seed-caching nutcrackers ranged from 8 to 12%. Nutcrackers do not use random search or olfactory cues to locate caches.     

Bolus recovery by gray jays: an experimental analysis

Gray jays (Perisoreus canadensis) typically store food boli in various sites on conifers. In a laboratory setting we determined whether gray jays recover stored boli by means of olfaction, trial-and-error search or spatial memory. Using an artificial tree with 52 possible caching sites, caching and/or recovery trials were performed with five captive gray jays for the following experiments: (1) no extra visual cues on tree; (2) extra visual cues (pine foliage) attached to tree; (3) pungent-smelling food hidden by observer; (4) one bird allowed to cache food but caches recovered by a second bird; (5) one bird allowed to observe another bird cache food and later permitted to recover those caches. Results supported the memory hypothesis, but cache site preferences were apparent for individual birds. To control for this, an additional experiment (6), in which cache site access was limited by the investigators, was conducted with two new birds. These results also indicated that gray jays use spatial memory to recover stored boli.     

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

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

Seasonal hippocampal plasticity in food-storing birds

Both food-storing behaviour and the hippocampus change annually in food-storing birds. Food storing increases substantially in autumn and winter in chickadees and tits, jays and nutcrackers and nuthatches. The total size of the chickadee hippocampus increases in autumn and winter as does the rate of hippocampal neurogenesis. The hippocampus is necessary for accurate cache retrieval in food-storing birds and is much larger in food-storing birds than in non-storing passerines. It therefore seems probable that seasonal change in caching and seasonal change in the hippocampus are causally related. The peak in recruitment of new neurons into the hippocampus occurs before birds have completed food storing and cache retrieval for the year and may therefore be associated with spacing caches, encoding the spatial locations of caches, or creating a neuronal architecture involved in the recollection of cache sites. The factors controlling hippocampal plasticity in food-storing birds are not well understood. Photoperiodic manipulations that produce change in food-storing behaviour have no effect on either hippocampal size or neuronal recruitment. Available evidence suggests that changes in hippocampal size and neurogenesis may be a consequence of the behavioural and cognitive involvement of the hippocampus in storing and retrieving food.     

Dispersal by rodent caching increases seed survival in multiple ways in canopy‐fire ecosystems

Seed‐caching rodents have long been seen as important actors in dispersal ecology. Here, we focus on the interactions with plants in a fire‐disturbance community, specifically Arctostaphylos species (Ericaceae) in California chaparral. Although mutualistic relationships between caching rodents and plants are well studied, little is known how this type of relationship functions in a disturbance‐driven system, and more specifically to systems shaped by fire disturbance. By burying seeds in the soil, rodents inadvertently improve the probability of seed surviving high temperatures produced by fire. We test two aspects of vertical dispersal, depth of seed and multiple seeds in caches as two important dimensions of rodent‐caching behavior. We used a laboratory experimental approach to test seed survival under different heating conditions and seed bank structures. Creating a synthetic soil seed bank and synthetic fire/heating in the laboratory allowed us to have control over surface heating, depth of seed in the soil, and seed cache size. We compared the viability of Arctostaphylos viscida seeds from different treatment groups determined by these factors and found that, as expected, seeds slightly deeper in the soil had substantial increased chances of survival during a heating event. A key result was that some seeds within a cache in shallow soil could survive fire even at a depth with a killing heat pulse compared to isolated seeds; temperature measurements indicated lower temperatures immediately below caches compared to the same depth in adjacent soil. These results suggest seed caching by rodents increases seed survival during fire events in two ways, that caches disrupt heat flow or that caches are buried below the heat pulse kill zone. The context of natural disturbance drives the significance of this mutualism and further expands theory regarding mutualisms into the domain of disturbance‐driven systems.     

Rapid effects of corticosterone on cache recovery in mountain chickadees (Parus gambeli)

Environmental perturbations increase adrenal activity in several vertebrates. Increases in corticosterone may serve as a proximate trigger whereby organisms can rapidly adapt their behavior to survive environmental fluctuations. In food-caching songbirds, inclement weather may present the need to alter caching and/or retrieval behaviors to ensure food supplies. We hypothesized that corticosterone may increase the rate of caching and/or retrieval behaviors in the mountain chickadee, a food-storing songbird, and tested if these potential effects were mediated by alterations in appetite, activity, or memory for cache sites. Corticosterone or vehicle was administered to subjects 5 min prior to either caching or recovery in a naturalistic laboratory paradigm during which we recorded the number of caching events, sites visited, and seeds eaten (caching) or caches recovered, total sites visited, cache-related visits, and non-cache-related visits (recovery). Data were analyzed using nested ANOVA for treatment within sequential trial. There was no effect on any caching behaviors following treatment. However, birds treated with corticosterone during retrieval recovered more seeds and tended to visit more cache-related sites than did controls. Since groups did not differ in the number of seeds eaten or the total number of sites visited, it seems unlikely that corticosterone affected appetite or activity. Rapid surges in corticosterone may increase the efficacy of an underlying memory process for cache sites which is reflected in higher cache recovery in corticosterone-treated birds than in controls. Thus, rapid alterations in plasma corticosterone following environmental change may alter memory-reliant behaviors which promote survival in the food-caching mountain chickadee.     

啮齿类对植物种子的传播作用

种子植物是固着生活的有机体 ,如果能成功地将种子扩散到适宜的生境 ,将会在生存竞争中获得优势。在长期的进化过程中 ,不同的植物依赖不同的媒介传播种子 ,如风传播 ,水传播 ,或自身的力量传播 (重力、弹爆力等 )。在很多情况下也依靠动物完成种子扩散 ,即所谓的动物传播。根据依赖的动物对象不同可以分为蚁传播 ,鸟传播 ,哺乳类传播 ,以及鱼传播 ,爬行类传播等。哺乳类中传播种子的类群主要包括翼手类 ,灵长类和啮齿类。由于能够飞行 ,热带食果实的蝙蝠(属翼手类 )对种子的传播作用最明显 ,研究得也最多 ,源于蝙蝠类的传播特称为ｃｈｉｒ…     

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.     

围栏条件下花鼠找寻种子的途径和方式

2009年8月和2010年8月,在黑龙江省带岭区东方红林场半天然围栏内研究了花鼠(Eutamias sibiricus)对地表放置和埋藏种子的发现过程,摸清围栏条件下花鼠找寻种子信号的途径和方式.实验步骤如下:第1天在花鼠巢区对角每释放点地表放置1粒标记种子,共30粒;第2天在巢区对角每释放点埋藏1粒标记种子,共30粒...     

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.     

The history of scatter hoarding studies

In this review, I will present an overview of the development of the field of scatter hoarding studies. Scatter hoarding is a conspicuous behaviour and it has been observed by humans for a long time. Apart from an exceptional experimental study already published in 1720, it started with observational field studies of scatter hoarding birds in the 1940s. Driven by a general interest in birds, several ornithologists made large-scale studies of hoarding behaviour in species such as nutcrackers and boreal titmice. Scatter hoarding birds seem to remember caching locations accurately, and it was shown in the 1960s that successful retrieval is dependent on a specific part of the brain, the hippocampus. The study of scatter hoarding, spatial memory and the hippocampus has since then developed into a study system for evolutionary studies of spatial memory. In 1978, a game theoretical paper started the era of modern studies by establishing that a recovery advantage is necessary for individual hoarders for the evolution of a hoarding strategy. The same year, a combined theoretical and empirical study on scatter hoarding squirrels investigated how caches should be spaced out in order to minimize cache loss, a phenomenon sometimes called optimal cache density theory. Since then, the scatter hoarding paradigm has branched into a number of different fields: (i) theoretical and empirical studies of the evolution of hoarding, (ii) field studies with modern sampling methods, (iii) studies of the precise nature of the caching memory, (iv) a variety of studies of caching memory and its relationship to the hippocampus. Scatter hoarding has also been the subject of studies of (v) coevolution between scatter hoarding animals and the plants that are dispersed by these.     

Effects of demanding foraging conditions on cache retrival accuracy in food-caching mountain chickadees (Poecile gambeli)

Birds rely, at least in part, on spatial memory for recovering previously hidden caches but accurate cache recovery may be more critical for birds that forage in harsh conditions where the food supply is limited and unpredictable. Failure to find caches in these conditions may potentially result in death from starvation. In order to test this hypothesis we compared the cache recovery behaviour of 24 wild-caught mountain chickadees (Poecile gambeli), half of which were maintained on a limited and unpredictable food supply while the rest were maintained on an ad libitum food supply for 60 days. We then tested their cache retrieval accuracy by allowing birds from both groups to cache seeds in the experimental room and recover them 5 hours later. Our results showed that birds maintained on a limited and unpredictable food supply made significantly fewer visits to non-cache sites when recovering their caches compared to birds maintained on ad libitum food. We found the same difference in performance in two versions of a one-trial associative learning task in which the birds had to rely on memory to find previously encountered hidden food. In a non-spatial memory version of the task, in which the baited feeder was clearly marked, there were no significant differences between the two groups. We therefore concluded that the two groups differed in their efficiency at cache retrieval. We suggest that this difference is more likely to be attributable to a difference in memory (encoding or recall) than to a difference in their motivation to search for hidden food, although the possibility of some motivational differences still exists. Overall, our results suggest that demanding foraging conditions favour more accurate cache retrieval in food-caching birds.     

A dynamic model of short-term energy management in small food-caching and non-caching birds

The survival of small birds in winter is critically dependenton the birds' ability to accumulate and maintain safe levelsof energy reserves. In some species, food caching facilitatesenergy regulation by providing an energy source complementaryto body fat. We present a dynamic optimization model of short-term,diurnal energy management for both food-caching and non-caching birds in which only short-day, winter conditions are considered.We assumed that birds can either rest, forage and eat, forageand cache, or retrieve existing caches (the two latter optionsare available only to caching birds). The model predicted thatwhen there is variability in foraging success (here modeledstrictly as within-day variability), both caching and non-caching birds should increase their fat reserves almost linearly inthe morning slowing down toward late afternoon, a result consistentwith field data but different than the result of a previousdynamic program. Non-cachers were predicted to carry higherfat levels than cachers especially when the variability inforaging success is high. Probability of death for non-caching birds was predicted to be higher than that for cachers, especiallyat higher levels of variability in foraging success. Amongcaching birds, an increase in number of caches and fat reserveswas also predicted if: (1) mean foraging success was decreased,(2) variability in foraging success was increased, and (3)energy expenditure at night was increased over our baselineconditions. Under the conditions simulated in our model, birdswere predicted to cache only if cache half-life (i.e., timeinterval over which 50% of the caches are forgotten or lostto pilferage) exceeded 2.5 days, indicating that low pilferagerate and long memory favor more caching. Finally, we showedthat such daily patterns of energy management do not necessarilyrequire relaxing assumptions about mass-dependent predationrisk.     

Two-phase seed dispersal: linking the effects of frugivorous birds and seed-caching rodents

Frugivorous birds disperse the seeds of many fruit-bearing plants, but the fate of seeds after defecation or regurgitation is often unknown. Some rodents gather and scatter hoard seeds, and some of these may be overlooked, germinate, and establish plants. We show that these two disparate modes of seed dispersal are linked in some plants. Rodents removed large (>25 mg) seeds from simulated bird feces (pseudofeces) at rates of 8–50%/day and scatter hoarded them in soil. Ants (Formica sibylla) also harvested some seeds and carried them to their nests. Rodents carried seeds 2.5±3.2 m to cache sites (maximum 12 m) and buried seeds at 8±7 mm depth. Enclosure studies suggest that yellow pine chipmunks (Tamias amoenus) and deer mice (Peromyscus maniculatus) made the caches. In spring, some seeds germinated from rodent caches and established seedlings, but no seedlings established directly from pseudofeces. This form of two-phase seed dispersal is important because each phase offers different benefits to plants. Frugivory by birds permits relatively long-range dispersal and potential colonization of new sites, whereas rodent caching moves seeds from exposed, low-quality sites (bird feces on the ground surface) to a soil environment that may help maintain seed viability and promote successful seedling establishment.     

Ravens, Corvus corax, differentiate between knowledgeable and ignorant competitors

Human social behaviour is influenced by attributing mental states to others. It is debated whether and to what extent such skills might occur in non-human animals. We here test for the possibility of ravens attributing knowledge about the location of food to potential competitors. In our experiments, we capitalize on the mutually antagonistic interactions that occur in these birds between those individuals that store food versus those that try to pilfer these caches. Since ravens' pilfer success depends on memory of observed caches, we manipulated the view of birds at caching, thereby designing competitors who were either knowledgeable or ignorant of cache location and then tested the responses of both storers and pilferers to those competitors at recovery. We show that ravens modify their cache protection and pilfer tactics not simply in response to the immediate behaviour of competitors, but also in relation to whether or not they previously had the opportunity of observing caching. Our results suggest that the birds not only recall whom they had seen during caching, but also know that obstacles can obstruct the view of others and that this affects pilfering.