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。     

啮齿动物的贮藏行为与植物种子的扩散

绝大多数啮齿动物一方面取食大量的植物种子和果实,另一方面通过其贮食行为将植物种子和果实搬运到远离母树的地点,即扩散,并将它们分散埋藏在落叶下或浅表的土层中,从而影响种子和果实的时空分布,最后导致幼苗在有利的条件下发生和建成,实现植物更新。啮齿动物与植物种子和果实之间已广泛形成了互惠或协同进化的关系。啮齿动物的贮食行为主要通过以下几个过程对植物种子和果实的扩散产生影响：选择、搬运和埋藏以及随后对种子和幼苗存活和死亡的影响等。本综述了啮齿动物对植物种子和果实贮藏的研究结果,以期为进一步开展啮齿动物的贮食行为在植物种子和果实的扩散中的作用的研究提供参考。     

动物与红松天然更新关系的研究综述

红松球果成熟后,种子自身不能脱落到达适宜的萌发地,因而无法自身完成天然更新而要依赖动物帮助传播种子。捕食红松种子的动物包括啮齿类、鸟类和一些大型兽类。其中,松鼠、星雅和普通币鸟具有分散贮藏的行为,以前两者为重要。这些动物从球果中取出种子,吃掉一部分后,靠颊囊或舌下囊搬运至贮藏地,将种子埋藏在地被物下准备冬、春食物缺乏时再重新捕食。搬运的距离远达数百米至几公里。分散贮藏的贮点数量很大。每个贮点有一至数粒种子。贮点小生境比较适合红松种子的萌发,因此大量的未被重新发现和捕食的贮点的种子在20个月后可能萌发。虽然动物贮藏的生境适合幼苗的萌发,但是不一定适合幼苗的继续生长。由于动物的捕食和贮藏行为,阔叶红松林内红松种子运转途径在4个层次（树上、地面、地被物下和洞穴）进行,最后只有少数种子萌发为幼苗。幼苗的生长过程同样受到动物的捕食和破坏。由于红松结实的丰欠年度变化,动物种群也随之变动。     

动物与植物种子更新的关系Ⅱ．动物对种子的捕食、扩散、贮藏及与幼苗建成的关系

植物的繁殖体总是面临来自各类生物（如昆虫、脊椎动物、真菌）的捕食风险。因动物捕食引起的种子死亡率影响植物的适合度、种群动态、群落结构和物种多样性的保持。种子被捕食的时间和强度成为植物生活史中发芽速度、地下种子库等特征的主要选择压力,而种子大小、生境类型等因素也影响动物对植物种子的捕食。捕食者饱和现象被认为是植物和种子捕食者之间的高度协同进化作用的结果,是限制动物破坏种子、提高被扩散种子存活率的一种选择压力。大部分群落中的大多数植物种子被动物扩散。种子扩散影响种子密度、种子被捕食率、病原体攻击率、种子与母树的距离、种子到达的生境类型以及建成的植株将与何种植物竞争,从而影响种子和幼苗的存活,最终影响母树及后代植物的适合度。种子被动物扩散后的分布一般遵循负指数分布曲线,大多数种子并没有扩散到离母树很远的地方。捕食风险、生境类型、植被盖度均影响动物对种子的扩散。植物结实的季节和果实损耗的过程也体现了其对扩散机会的适应。许多动物有贮藏植物种子的行为。动物贮藏植物繁殖体的行为,一方面调节食物的时空分布,提高了贮食动物在食物缺乏期的生存概率;另一方面也为种子萌发提供了适宜条件,促进了植物的扩散。于是,植物与贮食动物形成了一种协同进化关系,这种关系可能是自然界互惠关系（mutualism)的一种。影响幼苗存活和建成的因子包括种子贮蒇点的微生境、湿度、坡向、坡度、林冠盖度等。许多果食性动物吃掉果肉后,再将完好的种子反刍或排泄出来。种子经动物消化道处理后,发芽率常有所提高。     

种子捕食者对针叶树种子的捕食模式及二者的防御适应

在寒温带地区,针叶树种子因其油脂和蛋白含量高,成为许多动物的重要食物来源。在针叶林中,针叶树种子捕食者主要存在2种捕食方式,即传播前捕食和传播后捕食。通常,动物捕食种子的过程被认为是树种实现更新的重要途径。种子为躲避捕食者会形成相应的防御策略,种子的大小、营养、纤维含量、次级代谢产物等特征,通常也是植物种子防御捕食者捕食的策略。同样,这些防御策略一方面会影响种子捕食者的种群动态和取食行为,另一方面也可促使种子捕食者形成反对种子防御的适应对策。因此,研究种子捕食者捕食针叶树种子模式对于进一步认识针叶林中动物取食行为具有重要意义,同时,研究针叶树种子的防御及种子捕食者对其防御的适应策略,将有助于了解动植物之间相互作用。     

片段化景观中壳斗科植物种子捕食和扩散模式

生境片段化伴随的面积效应和边缘效应, 可改变分散贮食动物的竞争强度、觅食行为以及隐蔽条件, 影响种子捕食和扩散模式。阐明生境片段化对多物种种子捕食和扩散的影响, 对理解片段化生境中的植物更新和生物多样性维持十分重要。该研究在浙江省千岛湖地区的岛屿和大陆上开展了针对6种壳斗科植物的种子捕食和扩散实验, 分析了物种、分散贮食动物相对多度、种子产量、岛屿大小和边缘效应如何共同影响种子命运和种子扩散距离。主要结果: (1)种子命运和扩散距离在物种间存在显著差异; (2)大陆比岛屿有更长的种子留存时间, 小岛种子留存时间最短, 岛屿内部比岛屿边缘有更长的种子留存时间; (3)物种和岛屿大小对种子原地取食率存在交互作用, 白栎(Quercus fabri)种子在大岛上有更高的原地取食率; (4)种子在小岛上有最高的扩散率, 分散贮食动物相对多度对种子扩散后贮藏率有负效应。表明在千岛湖地区, 生境片段化改变了种子捕食和扩散模式, 且面积效应对不同物种的种子捕食和扩散模式产生了不同作用, 从而影响森林群落更新和生物多样性维持。     

动物在大别山五针松种群天然更新中的作用

大别山五针松(Pinus dabeshanensis)为我国特有树种,其天然植株较少且分布范围狭窄,种群更新困难,已被列为国家二级重点保护野生植物。分别于2015年和2016年的10—12月,在目前已知最大天然种群所在地安徽岳西县河图镇大王沟,研究了大别山五针松球果与种子特征、种子雨与土壤种子库、动物对种子的取食和搬运,幼苗分布格局及其与鼠穴分布的关系,以期探明动物在其天然更新中的作用,分析其天然更新不力的原因。结果显示:大别山五针松种子败育率较高,阳坡个体球果发育情况好于阴坡;种子成熟期间没有明显的种子雨,土壤种子库也未调查到完整种子。共记录到母树与球果的访问动物6目11科16种,其中7种动物确定取食种子;地面种子摆放实验显示超过95%以上的种子被啮齿动物捕食或搬运至他处取食或贮藏,不同的摆放处理对啮齿动物的捕食、搬运没有显著影响;小林姬鼠(Apodemus sylvaticus)盗食现象严重,埋藏实验中人工贮点当夜被发现的概率在90%左右,岩松鼠(Sciurotamias davidianus)和小林姬鼠是其种子主要捕食者。研究地的大别山五针松种群于2015年和2016年分别新增一年生幼苗5株和7株,这表明大别山五针松在当地存在天然更新。幼苗多单独生长在母树周围,点格局分析显示在0—0.6 m的尺度范围内呈随机分布;在0.6 m尺度呈聚集分布。大别山五针松幼苗在小林姬鼠巢穴周边分布,其更新格局受到小林姬鼠贮点位置分布情况影响,小林姬鼠极有很可能为大别山五针松的传播者,啮齿动物对大别山五针松种子的捕食与搬运影响了大别山五针松的天然种群更新。     

啮齿动物对植物种子的多次贮藏

啮齿动物对种子的多次搬运和贮藏是极为复杂的行为过程,既是对自己贮藏物进行管理、防御竞争者盗食的一种策略,也是盗食其它个体贮藏物的一种食物利用方式。此外,啮齿动物多次贮藏种子的过程实际上也是植物种子的多阶段扩散过程,因而对植物更新产生重要影响。本文综述了啮齿动物对植物种子多次贮藏的研究进展,分析了多次贮藏种子的原因,并从啮齿动物与植物的相互关系上探讨其生态学意义。     

啮齿动物对六盘山区辽东栎、野李和华山松种子的取食和搬运

为了阐明不同种子投放方式和覆盖处理对啮齿动物取食和搬运/贮藏种子行为的影响,2010年春季,我们在宁夏六盘山区的辽东栎幼林,用塑料标签标记法研究了不同种子投放方式(单独投放、两两组合投放和混合投放)和覆盖处理(对照、凋落物覆盖和土壤覆盖)下啮齿动物对辽东栎、野李和华山松种子的取食和搬运特点。结果表明:(1)不同物种、不同种子投放方式和覆盖处理对种子的就地取食率、搬运后的取食率和贮藏率均具有显著影响,种子较大或具有厚而坚硬的种皮(内果皮)、组合和混合投放及覆盖处理均不同程度地促进啮齿动物对种子的搬运;(2)3种植物的种子被搬运后取食和贮藏的平均距离范围均在5.5m以内,而且种子被搬运后贮藏的距离均大于搬运后取食的距离,其中华山松种子被搬运后取食的距离显著大于辽东栎和野李种子,但搬运后的贮藏距离显著小于后两者。(3)种子被搬运后单个种子的取食点和贮藏点占多数,其他大小的取食点和贮藏点较少,种子被搬运后以土壤埋藏为主要的贮藏方式。结果表明,种子的种皮特征以及种子在群落中的分布方式和存在状态,可能通过延长啮齿动物处理的时间而增大啮齿动物的被捕食风险,使动物改变对种子的取食和搬运行为,进而决定了种子的命运。     

围栏条件下捕食风险对岩松鼠贮藏核桃种子行为的影响

面对捕食风险,贮藏植物种子的啮齿动物如何通过调整其贮藏行为,权衡捕食风险和贮食效益,需要深入研究。2006 年9 月,在北京东灵山地区,以黄鼬作为捕食风险源,在半自然围栏内比较了有无捕食风险源时,岩松鼠贮藏的核桃种子的状态,以及埋藏种子在实验围栏内的分布、微生境和搬运距离,以探讨捕食风险对岩松鼠贮藏种子行为的影响。结果表明,捕食风险源存在时,搬运和埋藏种子的比例都显著减少,弃置地表种子的比例无显著差异;埋藏于高风险区的种子比例减少,中风险区和低风险区的埋藏种子比例增加,但差异都不显著;位于裸地和草下的埋藏种子比例减少,位于墙基的埋藏种子比例增加,但差异都不显著;此外,埋藏种子的搬运距离也没有显著差异。可见,捕食风险源存在时,岩松鼠显著减少了搬运和埋藏种子的比例,但对埋藏种子时的埋藏区域和微生境选择,以及搬运距离无显著影响。差异不显著可能与围栏效应有关。     

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.     

Effects of burrow condition and seed handling time on hoarding strategies of Edward's long-tailed rat (Leopoldamys edwardsi)

Many hoarding rodents use burrows not only for dwelling and protection from natural enemies, but also for food storage. However, little is known how burrows used by scatter-hoarding animals influence their foraging behaviors. In addition, handling time for a given food item has a fundamental impact on hoarding strategies of these hoarding animals: food items with longer handling time are more likely to be hoarded due to increasing predation risk because the animals spend more time outside their burrows if they consumed such food. By providing with two types of artificial burrows (aboveground vs. underground) and two types of food items (i.e. seeds) with contrasting handling times, we investigated how burrow condition and handling time co-influence hoarding strategies of a key scatter-hoarding rodent, Edward's long-tailed rat (Leopoldamys edwardsi) in large enclosures in southwest China. We found that only a few animals larder-hoarded fewer seeds when only aboveground burrows were available, while over 80% of the animals preferred to use the underground burrows and hoard significantly more seeds in the burrows when both aboveground and underground burrows were provided simultaneously. We also found that seed handling time significantly affected hoarding strategies of the animals: they consumed and/or scatter-hoarded more Camellia oleifera seeds with shorter handling time outside the burrow, but consumed and larder-hoarded more Lithocarpus harlandii seeds with longer handling time in underground burrows. Our study indicates that both burrow types and seed handling time have important impacts on hoarding strategies of scatter-hoarding animals.     

Effects of seed abundance on seed scatter-hoarding of Edward’s rat (<Emphasis Type="Italic">Leopoldamys edwardsi</Emphasis> Muridae) at the individual level

Mast seeding is a common phenomenon, and has important effects on seed dispersal and hoarding by animals. At population level, the predator satiation hypothesis proposes that the satiating effect of a large amount of seeds on a relatively small number of predators benefits seed survival in mast-seeding years. However, the effect of mast seeding on the scatter-hoarding of rodents at the individual level is largely unknown. In this study, we investigated the effects of seed abundance (by simulating mast seeding and non-mast seeding) on the removal, consumption and scatter-hoarding of seeds of Camellia oleifera (Theaceae) by Edward’s rat Leopoldamys edwardsi (Muridae) in seminatural enclosures in southwest China. We wanted to test the masting-enhanced hoarding hypothesis, which suggests that rodents tend to scatter-hoard more seeds in mast-seeding years in order to occupy more food resources. Our results indicate that L. edwardsi tended to disperse and scatter-hoard more seeds of C. oleifera per night with increasing seed abundance, and to eat less seeds per night when there was a high level of seed abundance in the enclosure experiments. These results support the masting-enhanced hoarding hypothesis. This capacity of rodents may be an evolutionary adaptation to the mast-seeding phenomenon. Our results suggest that mast seeding benefits forest regeneration not only through the predator satiation effect at the population level, but also through increased hoarding by animals at the individual level. Hongmao Zhang and Jinrui Cheng have contributed equally to this work.     

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.     

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。     

Using ecology to guide the study of cognitive and neural mechanisms of different aspects of spatial memory in food-hoarding animals

Understanding the survival value of behaviour does not tell us how the mechanisms that control this behaviour work. Nevertheless, understanding survival value can guide the study of these mechanisms. In this paper, we apply this principle to understanding the cognitive mechanisms that support cache retrieval in scatter-hoarding animals. We believe it is too simplistic to predict that all scatter-hoarding animals will outperform non-hoarding animals on all tests of spatial memory. Instead, we argue that we should look at the detailed ecology and natural history of each species. This understanding of natural history then allows us to make predictions about which aspects of spatial memory should be better in which species. We use the natural hoarding behaviour of the three best-studied groups of scatter-hoarding animals to make predictions about three aspects of their spatial memory: duration, capacity and spatial resolution, and we test these predictions against the existing literature. Having laid out how ecology and natural history can be used to predict detailed cognitive abilities, we then suggest using this approach to guide the study of the neural basis of these abilities. We believe that this complementary approach will reveal aspects of memory processing that would otherwise be difficult to discover.     

Reciprocal pilferage and the evolution of food-hoarding behavior

Current theories of food-hoarding behavior maintain that hoardingcan be adaptive if a hoarder is more likely than any other animalto retrieve its own caches. A survey of the literature indicatedthat the hoarder often has a recovery advantage when searchingfor items it has stored, but levels of cache pilferage are oftenso high (2–30% per day) that at least for some long-termfood hoarders, the caching animal is unlikely to recover a significantamount of its stored food. Except in a few cases (acorn woodpeckersand beavers), kin selection cannot explain the high levels ofpilferage observed. We suggest that some small solitary animalswith 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 otherwisebe because many interspecific and all intraspecific cache pilferersalso cache food. These or similar food caches can be pilferedlater by the original food hoarder. In other words, pilferingin these species is often reciprocal, and because it is reciprocal,it can be tolerated. We argue that caching systems based onreciprocal pilfering can be stable and are not necessarily susceptibleto "cheaters," animals that pilfer food but do not scatter hoardfood themselves, and we introduce a model of food hoarding tosupport this argument. These food-caching systems based on reciprocalpilfering resemble cooperative behavior, but the behavior isactually driven by the selfish interests of individuals. Thistheory of scatter-hoarding behavior based on reciprocity hasimportant implications for the ways that food-hoarding animalsinteract with inter- and intraspecific competitors.