Mechanisms of cache retrieval in long-term hoarding birds

Food hoarding and memory have primarily been studied in two bird families, the Corvidae (crows, jays, nutcrackers, etc.) and the Paridae (tits, titmice and chickadees). In both families there are species that hoard large quantities of seeds and nuts in the autumn and depend on these stores during the winter. Caches are concealed or highly inconspicuous and the most efficient way to retrieve them is to remember the exact locations. However, a long-term memory for a large number of caches may be physiologically expensive, and especially after long retention intervals, an alternative strategy could be to retrieve caches by cheaper but less efficient methods. Very few studies have been designed to investigate the decay of the memory in birds, but both field observations and experiments point in the same direction: although long-term hoarding corvids seem to possess an accurate long-term memory, long-term hoarding parids do not appear to. I discuss possible reasons for this and suggest that differences between the families in their degree of dependence on stored food or/and size-related limitations of brain capacity may be important.     

Regulation of cache stores and body mass in Carolina chickadees (Panes carolinensis)

Here I report the results of laboratory experiments on cachingbehavior of Carolina chickadees (Parus carolinensis) designedto test the following predictions from a recent dynamic optimizationmodel: under limited resources, small birds, when fat, shouldcache food instead of eating it, but they should eat insteadof caching when lean; when resources are abundant, birds shouldcache less when fat and more when lean. In addition, when resourcesare abundant the amount of time spent in foraging-related activityshould decrease with an increase in body mass. Chickadees weretested for 2 weeks in either a poor-quality environment (wherethey were given four 5-min periods per day of access to a feederfilled with sunflower seeds) or a richer environment (wherethey were given four 10-min access periods); they were thenswitched to the alternative environment for an additional 2weeks. The entire experiment lasted from October through June.Within-individual comparisons showed that birds in both thepoor and rich environments exhibited the predicted correlationsbetween the probability that a seed was cached and body massmeasured at dawn. The number of seeds already stored had a weakand variable effect on caching decisions. Time budgets changedas predicted; birds spent less time with food-related behaviorswhen their energy stores were high compared to when they werelow, and overall spent a higher fraction of their time foragingin the poor-quality environment compared to the rich environment.Two other variables also affected caching behavior: experienceand season. Individuals were more likely to cache in the poorenvironment when they had been tested in the rich environmentthe previous 2 weeks, as compared with birds started in thepoor environment. However, this was true only for tests donein the winter. In late spring, all birds stopped caching orreduced caching rates when faced with limited food availability,irrespective of previous experience. The birds harvested seedsfaster when they cached instead of eating seeds; as a result,long-term weight regulation in the poor environment was affectedby caching decisions. Birds tested in late spring lost weightin the poor environment, whereas those tested in the wintermaintained a stable weight when switched from the rich to thepoor environment. Thus, annual endogenous cues directly affectcaching decisions and indirectly influence the long-term regulationof body mass     

啮齿动物的分散贮食行为

食物贮藏是许多动物重要的适应性行为,分散贮藏的食物以植物种子为主。每个贮藏点贮藏数量不等的食物项目。啮齿动物分散贮藏食物之后,可降低食物被其他个体获取的机率,提高对食物资源的控制能力,最终有利于自身的生存和繁殖成功。植物种子被贮藏之后,可减少非贮食鼠类对种子的取食。同时,合适的微生境和埋藏有利于种子萌发、幼苗建成和植物的更新;使植物的分布区得以扩展。探讨啮齿动物的分散贮食行为,能够更好地理解食物贮藏在啮齿动物生活史中的作用,进一步认识鼠类和植物的相互关系以及不同啮齿动物在群落形成中的潜在作用。本综述了啮齿动物分散贮食的研究进展,并提出今后工作中的几点建议。     

Climate change and perishable food hoards of an avian predator: Is the freezer still working?

Changing climate can modify predator–prey interactions and induce declines or local extinctions of species due to reductions in food availability. Species hoarding perishable food for overwinter survival, like predators, are predicted to be particularly susceptible to increasing temperatures. We analysed the influence of autumn and winter weather, and abundance of main prey (voles), on the food‐hoarding behaviour of a generalist predator, the Eurasian pygmy owl (Glaucidium passerinum), across 16 years in Finland. Fewer freeze–thaw events in early autumn delayed the initiation of food hoarding. Pygmy owls consumed more hoarded food with more frequent freeze–thaw events and deeper snow cover in autumn and in winter, and lower precipitation in winter. In autumn, the rotting of food hoards increased with precipitation. Hoards already present in early autumn were much more likely to rot than the ones initiated in late autumn. Rotten food hoards were used more in years of low food abundance than in years of high food abundance. Having rotten food hoards in autumn resulted in a lower future recapture probability of female owls. These results indicate that pygmy owls might be partly able to adapt to climate change by delaying food hoarding, but changes in the snow cover, precipitation and frequency of freeze–thaw events might impair their foraging and ultimately decrease local overwinter survival. Long‐term trends and future predictions, therefore, suggest that impacts of climate change on wintering food‐hoarding species could be substantial, because their ‘freezers’ may no longer work properly. Altered usability and poorer quality of hoarded food may further modify the foraging needs of food‐hoarding predators and thus their overall predation pressure on prey species. This raises concerns about the impacts of climate change on boreal food webs, in which ecological interactions have evolved under cold winter conditions.     

Why do hoarding birds gain fat in winter in the wrong way? Suggestions from a dynamic model

In winter, small birds should be fat to avoid starvation andlean and agile to escape predators. This means that they facea trade-off between the costs and benefits of carrying fat reserves.Every day they must gain enough fat to survive the coming night.Food-hoarding species can afford to carry less fat than nonhoardersbecause they can store energy outside the body. Furthermore, hoardersshould avoid carrying excessive fat during the day because theycan gain fat fast by retrieving food late in the afternoon.With no stored supplies, nonhoarders face more unpredictableaccess to food, and they should start gaining fat earlier inthe day. The predicted pattern is then that nonhoarders gainfat early and that hoarders gain fat late in the day. Recent fielddata show the opposite pattern: hoarders gain relatively morefat reserves in the morning than nonhoarders do. Using a dynamicmodel that mimics the conditions in a boreal winter forest,I investigated under which conditions this pattern will arise.The only assumption of those investigated that produced thispattern was to relax the effect of mass-dependent predation risk.I did this by introducing a limit under which fat reserves didnot affect predation risk. Hoarders then started the day bygaining fat in the morning. Later, when they had reached a safer(but still not risky) level, they switched to hoarding. Thepattern I searched would only occur if either not all food waspossible to store, or if retrieval gave less energy than foragingin good weather conditions. If I assumed that low levels ofbody fat also increased predation risk, hoarders would cachein the morning when they carried least fat. I discuss empiricalevidence for how body fat affects predation risk. In summary,the factors that produced the pattern I searched were a changein the predation-mortality function combined with restrictions onhoarding.     

FEEDING ECOLOGY OF THE BLACK-FACED DIOCH QUELEA QUELEA IN NIGERIA

The results of a three-year study of the diet of Quelea quelea in the Lake Chad region of Nigeria indicate why this bird periodically does extensive damage to crops of dry-season guinea-corn.
The normal food of the birds in the early dry-season consists of small grass seeds collected off the ground. As the supply of these diminishes there is a gradual change-over to larger seeds.
In years when this change begins early, it is liable to coincide with the ripening of the cereal crop and severe damage may be caused.
At the beginning of the rains the dry-season food supply is lost owing to the simultaneous germination of the seeds over large areas.
The birds lay down fat reserves in preparation for this lean period.
After a short time the birds migrate south to regions where rain has been falling for some weeks.
In the short period spent in these parts, Queleas feed on ripening grass seeds—including those of cultivated millet.
There is evidence for considerable mortality during this time of food scarcity and it is suggested that the numbers of Queleas are limited by the food supply.
The significance of communal roosting is discussed. It is proposed that the phenomenon is related to food finding, the roost being considered as an "information centre" for the large area prospected by the birds constituting the roosting community. A method is outlined by which information on food availability within the feeding area may feasibly be transmitted within the community.     

秦岭南北坡森林鼠类对板栗和锐齿栎种子扩散的影响

森林鼠类的种子贮藏行为对植物的扩散及更新会产生积极的影响。2012和2013年秋季,分别在秦岭北坡的周至国家级自然保护区和南坡的佛坪国家级自然保护区内,调查了森林鼠类对板栗(Castanea mollissima)和锐齿栎(Quercus aliena)种子的取食和扩散差异。结果显示:1)秦岭南北坡的环境因素,特别是植被因素,对鼠类扩散板栗和锐齿栎种子具有重要的影响。南坡较为丰富的壳斗科植被种类,导致2种种子在南坡存留时间均长于北坡,而北坡的扩散取食和丢失率均高于南坡。2)种子特征影响鼠类的取食或贮藏偏好。由于较高的蛋白、脂肪等营养含量,鼠类更喜好取食或搬运贮藏板栗种子。然而,低营养但高丹宁含量的锐齿栎种子仍然被鼠类大量贮藏。3)2种种子在南北坡的扩散历程在两个年份间有很大差异,在食物相对匮乏的年份(2012年),种子被扩散的速度更快且丢失的比率更高。这种差异反映了种子大小年现象对森林鼠类取食和贮藏策略的影响。4)无论在秦岭南坡还是北坡,营养价值含量(如蛋白和脂肪)较高的板栗种子的取食和贮藏距离都明显大于营养价值含量较低的锐齿栎种子,这与最优贮藏空间分布模型的预测一致。     

Time budgets of Nuthatches Sitta europaea with supplementary food

Individual time budgets during winter and spring were studied in a population of Nuthatches Sitta europaea in south-central Sweden. In late winter birds spent about 90% of daytime foraging, males feeding somewhat less than females, possibly due to male dominance. In early spring, foraging time decreased to about 65% of daytime activity, and sex-related differences became more pronounced. Males then increased time spent resting and singing. Females were nestbuilding, spent less time resting and also devoted more time to foraging than did males. Prior to the observation periods, food density for part of the population was experimentally increased by supplying sunflower seed. In spite of this, time budgets in the experimental group were similar to those of the control group. It is possible that the intensity of foraging, rather than actual time devoted to it, was influenced by food density and that, as a result, birds in the experimental group were able to maintain a higher level of vigilance. Also, an increase in food supply may be less important to a hoarding bird such as the Nuthatch. However, the result remains that Nuthatch time budgets in winter and spring are not readily influenced by an increase in food density.     

A prudent hoarder: effects of long-term hoarding in the European nuthatch, Sitta europaea

Although hoarding has been studied intensively for many decades,few studies have attempted to measure its actual fitness consequences.To fill this gap, we used ptilochronology, the growth of replacementfeathers as a measure of nutritional status, and thus a reflectionof starvation risk, of individual European nuthatches (Sittaeuropaea) during winter. We found that nuthatches are long-termhoarders, retrieving stored food up to at least 98 days afterstoring it. Long-term hoarding enhanced the nutritional statusof individual birds significantly because those individualsexperimentally given an opportunity to store seeds during autumnregrew plucked rectrices faster and larger than did controlbirds. Nuthatches used their stored seeds prudently by adjustingthe amounts they ate to meet their requirements, as determinedby ambient temperatures. Nuthatches refrained from using storedfood during periods of relatively benign conditions so theycould use the food during periods of more severe conditions.     

围栏条件下同域分布三种鼠对两种种子的贮藏行为差异

种子贮藏是啮齿动物利用食物资源的一种适应性行为。同域分布的啮齿动物可能进化出不同的贮藏方式和策略。为了解同域分布的啮齿动物的贮藏策略及种子特征在动物贮藏行为决策中的作用,于2014年10-12月,通过半自然围栏实验,在秦岭南坡的佛坪国家级自然保护区内调查了同域分布社鼠、中华姬鼠和甘肃仓鼠对板栗和锐齿槲栎种子的贮藏策略差异,并探讨了2种种子特征在鼠类贮藏行为决策中的作用。结果显示：1）社鼠主要集中贮藏板栗种子,未分散贮藏任何种子;中华姬鼠未贮藏板栗种子,对锐齿槲栎种子同时表现出集中和分散贮藏行为,以集中贮藏为主;甘肃仓鼠对2种种子均表现出集中贮藏行为,未表现分散贮藏行为。2）社鼠和甘肃仓鼠均倾向于集中贮藏有较高营养价值（高蛋白和脂肪）且单宁含量较低的板栗种子;中华姬鼠倾向于分散贮藏单宁含量高的锐齿槲栎种子。3）3种鼠均喜好取食有较高营养价值且单宁含量低的板栗种子,很少取食单宁含量高的锐齿槲栎种子。结果表明同域分布鼠类对不同种子的贮藏方式有所不同,种子特征影响鼠类的取食和贮藏策略。     

金秀大瑶山瑶民“鸟盆”狩猎区鸟类食物源植物及生态保育

2003年7月～2008年12月,对金秀大瑶山茶山瑶民"鸟盆"狩猎活动区域的鸟类食物源植物进行了调查,录得"鸟盆"狩猎区秋冬季鸟类取食果实、种子的植物有28科71种,当地称为"鸟果"树。此外,瑶民"鸟盆"狩猎活动所需的"鸟漆"(粘捕鸟类的粘胶)是用9种冬青科植物的树皮制作,其果实、种子亦是"鸟盆"狩猎活动区鸟类的主要食物。     

剥夺食物对雄性长爪沙鼠贮食行为的影响

禁食导致一些啮齿动物的贮食量增加,但禁食处理后雄性长爪沙鼠贮食行为的变化则不一致。每天禁食22 h,长爪沙鼠的一些个体表现出高水平的贮食行为(禁食贮食组),而另一些个体则没有表现出贮食行为(禁食无贮食组)。延长禁食(22 h)持续的时间(连续重复3 d 和20 d)和增加禁食时间(禁食48 h),都没有使禁食无贮食组的动物表现出贮食行为。同样在自由取食条件下,长爪沙鼠的贮食行为也表现为二型性。在自由取食和禁食条件下,贮食量与体重、体脂含量和瘦素的浓度之间无明显相关关系。研究结果表明,禁食是诱导雄性长爪沙鼠贮食行为发生的一个重要条件,但增加禁食的程度并不改变其贮食行为的表现。     

围栏条件下社鼠的食物贮藏行为

在北京东灵山地区, 用活捕笼从野外捕获社鼠, 并在野外建造围栏, 以山杏种子和辽东栎坚果为备选食物, 对围栏条件下社鼠的食物贮藏行为进行了研究。数据的统计分析采用SPSS for Windows (version 1010) 进行。结果表明: 1) 社鼠主要表现出食物的集中贮藏方式; 2) 贮藏食物被模拟盗窃使社鼠的食物贮藏活动加强; 3)社鼠倾向于选择山杏种子进行贮藏, 而对辽东栎坚果则取食较多。文中还讨论了食物类型、模拟盗窃等因素对社鼠食物贮藏行为的影响。     

鼠类对栓皮栎和锥栗种子的贮藏:验证高单宁假说

种子中的单宁影响鼠类的取食和贮藏策略。高单宁假说认为鼠类倾向于优先贮藏单宁含量高的种子、取食单宁含量低的种子。同域分布的鼠类对种子的取食和贮藏选择是否符合高单宁假说的预测尚缺乏足够的实验证据。本研究通过围栏实验研究了四川都江堰地区亚热带常绿阔叶林中的小泡巨鼠（Leopoldamys edwardsi）、针毛鼠（Niveventer fulvescens）、北社鼠（N.confucianus）、高山姬鼠（Apodemus chevrieri）、中华姬鼠（A.draco）对单宁含量高的栓皮栎（Quercus variabilis）种子和单宁含量低的锥栗（Castanea henryi）种子的取食和贮藏偏好,旨在进一步验证高单宁假说。结果表明：（1）5种鼠均偏好取食锥栗种子,很少取食或不取食栓皮栎种子;（2）仅具集中贮藏习性的针毛鼠和北社鼠偏好集中贮藏锥栗种子;兼具集中和分散贮藏习性的小泡巨鼠和高山姬鼠也倾向于贮藏锥栗种子;（3）兼具集中和分散贮藏习性的中华姬鼠偏好分散贮藏栓皮栎种子,集中贮藏锥栗种子。研究结果并不完全支持高单宁假说,表明同域分布的鼠类对种子取食和贮藏偏好表现出种间分化,高单宁假说在同域分布鼠类中可能不具有普遍性。     

Geographic variation of the storing behaviour in the Coal tit Parus ater: role of winter residency and environmental conditions

Foraging and hoarding behaviour of the Coal Tit Parus ater were studied in two widely separated populations, in the Pyrenees and in Norway. The two populations differed in their degree of winter residence and environmental pressures. Location of foraging and hoarding sites were described in the Pyrenees during winter, and during autumn in Norway where no hoarding takes place during winter. Significant differences in the hoarding behaviour of Coal Tits between these areas were observed. In the Pyrenees, birds hoarded on inner and lower parts of the trees, using trunks and thick branches as caching sites, which are the substrates most heavily used in conditions of winter environmental stress. In Norway, birds hoarded items on outer and higher parts of the trees, mainly among needled twigs, which were the substrates used in normal foraging. Animal food was hoarded more frequently by the Norwegian population. Our results show that hoarding behaviour varies among populations and suggest that the differences recorded may be related to differences in competitive pressures and the prevailing environmental conditions. Furthermore, the absence of a safe long-term hoarding niche in the Norwegian population, due to interspecific competition, would make a strong sedentary habit difficult, offering a functional explanation for the differences observed in the degree of winter residence between Norwegian and Pyrenean Coal Tits.     

Hoarding of individual nuthatches Sitta europaea and march tits Parus palustris

The hoarding behaviour of one pair of nuthatches Sitta europaea L. and of four individual marsh tits Parus palustris L. was studied during autumn and winter in a deciduous grove in central Sweden. Sunflower seeds were offered at a feeding table. AM individuals studied stored seeds intensively throughout the whole study period. The two species showed very different hoarding patterns. The nuthatch pair aggressively defended the area around the feeding table, which was within their territory, from other nuthatches and also seemed to affect the hoarding behaviour of the coexisting marsh tits. Some significant differences were found also between con-specifics in some aspects of hoarding behaviour, which could in some cases be related to sex or dominance. These differences may make hoarding profitable for the individual birds if they also differ in their foraging patterns individually, and so will have a greater probability of finding their own stored items than other individuals. However, the evidence for individual segregation of hoarding patterns is not conclusive.     

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.     

Daily patterns of body mass gain in four species of small wintering birds

Theoretically, the trajectories describing the daily accumulation of body reserves are expected to differ between bird species in relation to whether or not they hoard food. To carry reserves on the body may be costly and hoarding species can be expected to hoard food early in the day when light and retrieve it in the afternoon, with a concomitant rapid increase in body mass. Also, the increased food predictability resulting from being able to consume hoarded food late in the day should lead to a relatively faster gain in body reserves in the afternoon in hoarding species compared to non-hoarders. Non-hoarders may have to hedge against possible afternoon losses of foraging opportunities by accumulating more reserves early in the day.
In this study the daily patterns of body mass gain in four small bird species resident during winter in Scandinavia are described. Individually known birds were trained to come to a permanent feeder and their body masses were recorded every hour throughout the day with a remote-controlled balance. The hoarding willow tit Parus montanus , marsh tit P. palustris and European nuthatch Sitta europaea all displayed the most rapid gain in body mass in the early hours of the day. After the initial burst in the morning, reserves were accumulated at a roughly constant rate for the remainder of the day. In contrast, the non-hoarding great tit P. major apparently gained body reserves at a more even rate. The daily pattern of body mass gain found in the hoarding species differs from prevailing theoretical predictions, whereas the pattern in the non-hoarding great tit is in a better agreement with theory, from which this pattern has been predicted repeatedly.     

布氏田鼠合作贮食行为及其影响因素

合作贮食是社会性动物应对食物匮乏的重要对策,但其内在的生态学机制尚未阐明。本文以布氏田鼠为研究对象,根据亲缘关系划分为亲缘组和非亲缘组。在人工实验箱中录像统计不同组别合作贮食行为占用时间的差异,探究亲缘关系对合作贮食行为的影响,并利用相关性分析探究亲缘组个体对贮食的贡献—收益关系以及与贮食行为相关的个体特征因素。结果表明,在组间水平上,与非亲缘组相比,亲缘组的布氏田鼠表现更多的合作贮食。在亲缘组个体水平上,不同个体对贮食的参与度和贡献度存在很大差异。个体对合作贮食的付出与其取食的收益呈显著负相关关系,并且个体合作贮食贡献越大,其睾丸指数和睾酮含量降低越显著。研究结果说明,亲缘关系的存在有利于布氏田鼠的合作贮食,但合作贮食贡献大的个体,其繁殖受到了抑制。     

啮齿动物作用下退耕地山杏种子扩散与贮藏的季节变化

啮齿动物对植物种子的取食和扩散影响种子的时空分布,继而影响种子的萌发和幼苗建成,因而在森林更新中起着重要作用.在国有济源市愚公林场,选择退耕地生境,于春季、夏季、秋季分别释放人工标记的山杏种子,观察啮齿动物扩散与埋藏山杏种子的季节性差异.结果表明：1）退耕地中的啮齿动物主要包括大林姬鼠、社鼠、黑线姬鼠;2）山杏种子扩散速率在春季显著慢于夏季,夏季显著慢于秋季;3）种子搬运量受季节和种子状态交互作用影响,春季显著少于夏季,夏季显著少于秋季;4）不同季节种子平均搬运距离不同,秋季不同状态种子的搬运距离均大于春季和夏季;5）啮齿动物对山杏种子的贮藏点大小多为1粒种子,少量为2、3粒种子,且贮藏点大小与季节间存在显著的交互作用,春季单粒种子的贮藏点数量显著少于夏季和秋季,而夏季与秋季的贮藏点则倾向于多粒种子;6）在夏季和秋季各有5枚（共释放1800枚）被啮齿动物分散贮藏的山杏种子建成幼苗.