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.     

动物分散贮食行为对植物种群更新的影响

分散贮食是许多动物取食行为策略的重要组成部分。对以植物种子为主要贮食对象的动物来说,种子内营养物质含量、种子大小以及种子内次生化合物的含量等因素都直接影响动物的贮食行为。动物偏爱贮藏个体较大的种子,大种子多被搬运并分散贮藏在远离种源的地方,而小种子则多被就地取食,以补充动物贮食过程中的能量消耗。贮食动物主要通过空间记忆、特殊路线以及贮藏点周围的直接线索等途径重新获取贮藏点内食物。在重取过程中,一些贮藏点被遗忘,其中的种子成为植物种群更新的潜在种子库。因此,分散贮食动物不仅是种子捕食者,还是种子传播者,它们对植物种子的捕食、搬运和贮藏,影响了植物种子的存活和幼苗的建成,从而在一定程度上影响植物种群的更新、分布。植物种群为了促进种子的传播,在进化过程中逐渐形成了形式多样的适应性策略,降低种子的直接被捕食率,提高种子的被贮藏率。研究动物分散贮食行为对植物种群更新的影响,将有助于理解贮食动物与植物之间的互惠关系,从而认识贮食动物种群在生态系统中的作用,为生物多样性的保护提供科学依据。     

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.     

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。     

Burrow fractal dimension and foraging success in subterranean rodents: a simulation

For animals that forage underground, the success with whichfood items are located may be closely related to burrow architecture.Fractal dimension, which describes how a burrow explores thesurrounding area in a way that is independent of burrow length,is an obvious choice for a single metric describing burrow shape.Although it is often assumed that burrows of high fractal dimensionwill be associated with greater foraging success, this has notpreviously been demonstrated. In this study, we use computersimulations to study the success with which burrows of differentfractal dimensions locate randomly distributed food items. Inaddition, we examine the effect of different patterns of fooddistribution (in particular the patchiness with which food itemsare distributed) and consider how using different criteria forlocating food items affects the relationship between fractaldimension and foraging success. We conclude that, under a widerange of plausible assumptions about the ways in which subterraneanrodents forage, burrows of high fractal dimension are more successfulat locating food items than burrows of lower fractal dimension.     

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。     

岩松鼠的食物贮藏行为

食物贮藏是许多动物对不可预见的食物供应变化的一种重要适应.岩松鼠(Sciurotamias davidianus)为中国特有物种,广泛分布于华北地区的山地和丘陵地带.作者在北京市东灵山地区建造半自然围栏(4 m×3 m× 1 m),以核桃(Juglans regia)和山杏(Prunus armeniaca)种子为备选食物,对岩松鼠(12只)的食物贮藏行为进行了研究.数据的统计分析采用SPSS for Windows进行.研究结果表明1)岩松鼠表现出集中和分散两种食物贮藏方式,而分散贮藏是其偏好的贮藏方式;2) 当遇到贮藏食物被盗窃时,岩松鼠倾向于搬运更多的食物进行集中和分散贮藏;3)岩松鼠没有在食盘就地取食任何一种食物;把食物搬离后,岩松鼠所取食的山杏种子数量明显多于所取食的核桃数量;4)岩松鼠只选择核桃进行分散贮藏;5)岩松鼠对核桃的搬运距离大于山杏种子.本研究结果提示,在自然条件下,岩松鼠对核桃和山杏的天然更新起着不同的作用[动物学报 51(3)376-382,2005].     

Activity patterns, feeding and burrowing behaviour of the crab Ucides cordatus (Ucididae) in a high intertidal mangrove forest in North Brazil

Activity patterns, feeding and burrowing behaviour of the economically important semi-terrestrial mangrove crab Ucides cordatus (Ucididae, L. 1763) was studied in a high intertidal Rhizophora mangle forest stand in Bragança, North Brazil. Video observations in the rainy and dry season were conducted over 24 h cycles at different lunar phases to investigate the behaviour of these litter-feeding crabs outside their burrows. During the rainy season, crabs stayed inside their burrows for 79% and 92% of the time during day and night, respectively. Time spent for feeding, burrowing and other activities outside their burrows was significantly longer during the day with 9.9% (night: 1.7%) and at waning and waxing moon with 9% (full and new moon: 0.9%). At neap tides (no tidal inundation) foraging and feeding activities outside burrows were clearly light-dependent, increasing at dawn and decreasing at dusk. Highest activities during daytime relate to the visual localisation of food. During the dry season, crabs spent less time inside burrows at neap tides than during the rainy season (80% and 91%, respectively). However, time spent for feeding activities was similar during both seasons. During almost all observation periods crabs collected leaf litter, but rarely fed on it outside burrows. At neap tides nearly all available litter was collected, suggesting that the U. cordatus population is litter-limited during these times. At spring tides (regular tidal inundation) the surface activity of U. cordatus was tide-dependent. Crabs closed their burrow entrances 2-3 h before flooding and re-emerged as soon as the tide retreated. During the day, burrow maintenance was the second most frequent behaviour after feeding. Agonistic interactions were regularly observed and were mainly related to burrow defence. The mean foraging radius of the crabs was only 19 cm (max: 1 m) underneath high Rhizophora mangle trees where crab densities were high. The results point to a high competition for burrows and show that U. cordatus is territorial. It is concluded that several exogenous factors, in particular light, leaf litter availability, flooding of burrows and the presence of conspecifics are important in controlling the crabs' activity patterns.     

Seed caching and cache pilferage by three rodent species in a temperate forest in the Xiaoxinganling Mountains

Although differences in food-hoarding tactics both reflect a behavioral response to cache pilferage among rodent species and may help explain their coexistence, differentiation in cache pilfering abilities among sympatric rodents with different hoarding strategies is seldom addressed. We carried out semi-natural enclosure experiments to investigate seed hoarding tactics among three sympatric rodent species (Tamias sibiricus, Apodemus peninsulae and Clethrionomys rufocanus) and the relationship of their pilfering abilities at the inter- and intraspecific levels. Our results showed that T. sibiricus exhibited a relatively stronger pilfering ability than A. peninsulae and C. rufocanus, as indicated by its higher recovery rate of artificial caches. Meanwhile A. peninsulae showed a medium pilfering ability and C. rufocanus displayed the lowest ability. We also noted that both cache size and cache depth significantly affected cache recovery in all three species. T. sibiricus scatter-hoarded more seeds than it larder-hoarded, A. peninsulae larder-hoarded more than scatter-hoarded, and C. rufocanus acted as a pure larder-hoarder. In T. sibiricus, individuals with lower pilfering abilities tended to scatter hoard seeds, indicating an intraspecific variation in hoarding propensity. Collectively, these results indicated that sympatric rodent species seem to deploy different food hoarding tactics that allow their coexistence in the temperate forests, suggesting a strong connection between hoarding strategy and pilfering ability.     

Rodent handling of Araucaria araucana seeds

In an intermast year of very low seed production, we studied seed handling in an Araucaria araucana (Araucariaceae) forest in Neuquén Province, Argentina. Rodents identified in 844 photographs from automatic cameras removed 589 seeds marked with small embedded magnets. Within 12 days of removal, 460 were recovered using a magnetic field locator; 79% of recoveries were from burrows and caches in litter or soil. Rodents exhibited a diversity of seed‐handling strategies and differed in their potential as dispersal agents. Seed removal was most likely between 15.00 hours and 21.00 hours, but diurnal and nocturnal visits were recorded for all species. Oligoryzomys longicaudatus (Cricetidae) was a seed predator that took 8% of marked seeds and left none whole. Chelemys macronyx (Cricetidae) and Rattus norvegicus (Muridae) removed 25% and 19% of marked seeds respectively. These two species deposited the majority of seeds in groups of 10 or more in burrow larders that were unfavourable seedling establishment sites far from daylight. Abrothrix longipilis (Cricetidae) removed 43% of seeds, scatter‐hoarded the largest percentage of whole seeds (37%), moved some seeds farther than 40 m, and left them in favourable seedling establishment sites near daylight. For all species, the number and proportion of seeds cached whole increased as more seeds were removed. Rodents, especially A. longipilis, may play an important role in regeneration of A. araucana. Seed‐handling strategies and potentially effective dispersal are discussed in terms of masting seed production.     

A telemetric thread tag for tracking seed dispersal by scatter-hoarding rodents

The seeds of many tree species are dispersed more than once, and this secondary seed dispersal is believed to enhance seedling recruitment. However, the effectiveness of secondary seed dispersal has rarely been assessed because it is difficult to track seeds until they die or germinate. We describe a new technique that uses thread tags attached to radio transmitters (telemetric thread tags) to track long-distance multistep seed dispersal by scatter-hoarding rodents. These telemetric thread tags can be turned off with a magnet and are reactivated when the seed moves. This method allows for seed tracking with minimal cache disturbance or distance bias, over long time spans, multiple seed movements, and with few effects on animal behavior. We used telemetric thread tags to track seed dispersal of the palm tree Astrocaryum standleyanum in a Neotropical forest, and achieved near-complete recovery of dispersed seeds tracked over distances as far as 241?m. We were also able to record the recovery time and fate of cached seeds without disturbing caches. Neither the removal rate nor the dispersal distance differed between seeds with telemetric thread tags and thread-tagged seeds. We conclude that telemetric thread tags can be used to document secondary seed dispersal by scatter-hoarding animals with unprecedented efficacy and precision. Given the size of these tags relative to the size of seeds and their dispersers, this method is applicable to the majority of tree species that are secondarily dispersed by scatter-hoarding mammals.     

Effects of habitat and season on removal and hoarding of seeds of wild apricot (Prunus armeniaca) by small rodents

The wild apricot (Prunus armeniaca) is widely distributed in the Donglingshan Mountains of Mentougou District of Beijing, China, where its seeds may be an important food resource for rodents. Predation, removal and hoarding of seeds by rodents will inevitably affect the spatio-temporal pattern of seed fate of wild apricot in this area. By marking and releasing tagged seeds of wild apricot, we investigated seeds survival, scatter-hoarding, cache size and seedling establishment, and the preference of micro-habitats used by rodents to store seeds. The results showed that: (1) rodents in this area hoarded food intensively in autumn, as well as in spring and summer. (2) There were significant effects of habitat and season on removal rate of tagged seeds at releasing plots. In both two types of habitats, Low and High shrub, tagged seeds were removed most rapidly by rodents in autumn, at intermediate rates in spring and least rapidly in summer. (3) During three seasons, mean dispersal distance of scatter-hoarded seeds in Low shrub habitat was greater than that in High shrub. Most removed seeds were buried within 21.0 m of the releasing plots. (4) In both two types of habitats, Low and High shrub, rodents tended to carry seeds to US (Under shrub) and SE (Shrub edge) microhabitats for scatter-hoarding or predation. (5) Among the caches made by rodents, most caches contained only one seed, but up to three seeds were observed; caches of 2–3 seeds were common in autumn. (6) By comparing dental marks, we determined that large field mice (Apodemus peninsulae) and David’s rock squirrels (Sciurotamias davidianus) contributed to removal and predation of released tagged seeds. However, only the large field mice exerted a pivotal and positive role on the burial of dispersed seeds. (7) Establishment of three seedlings originated from seeds buried by rodents was documented in High shrub habitat.     

食物源距离对中华姬鼠贮藏策略的影响

在围栏条件下, 检验食物源距离对中华姬鼠贮藏策略的影响,并检验根据快速隔离假说和最优贮藏空间分布模型做出的两个预测：（1）3个释放点无论距离远近,种子均先被大量分散贮藏在各个释放点周围;（2）随着释放点远离巢穴,种子被集中贮藏的比例下降。结果发现: 分散贮藏是中华姬鼠的主要贮藏方式,3个释放点种子被分散贮藏的数量无显著差异,这个结果支持预测（1）;3个种子释放点（1m,5m,13m）被集中贮藏的比例分别为(1m: 6.25%; 5m: 1.88%; 13m: 1.25%),说明被集中贮藏的种子数量随种子释放点与巢穴距离的增大而逐渐减少,这个结果支持预测（2）。本研究表明中华姬鼠应对捕食风险升高的策略是降低取食量和贮藏量。     

Diet of the killifish Rivulus marmoratus collected from land crab burrows,with further ecological notes

Synopsis One-hundred eleven specimens of the cyprinodont fish Rivulus marmoratus were trapped from burrows of the great land crab Cardisoma guanhumi in east central Florida and the entire alimentary tract removed for analysis of food items. Three categories of burrows (inactive, active and sealed) were sampled to examine possible relationships between burrow type and presence of R. marmoratus. Forty percent of the guts examined contained no food items, while the remaining 60% contained items of both terrestrial and aquatic origin. Capture rates among burrow categories did not vary significantly, and most collections consisted of 1 or 2 individuals per burrow. Mean standard length of fish within a burrow declined when more than 3 specimens were captured from a burrow. Supplemental observations on reproductive status and burrow water temperature are noted.     

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。     

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。     

Home Range,Population Density,and Food Resources of Agouti paca (Rodentia: Agoutidae) in Costa Rica: A Study Using Alternative Methods1

Field studies of elusive mammals such as Agouti paca are difficult, and results are often biased and incomplete because the animals are nocturnal and avoid traps. By studying an A. paca population in a Pacific lowland forest of Costa Rica, we developed indirect observational methods to estimate population density and food resource utilization. To estimate population density, we divided the number of A. paca burrows found in a 12-ha census area by the average number of burrows utilized per individual from radiotelemetry data. We compared this estimate to independent population estimates obtained using two transect methods. Agouti paca density was estimated at 93 individuals/km² based on burrow number, and between 67 to 70 individuals/km² using transect methods. This discrepancy corroborates previous studies suggesting that transect methods underestimate population density. To identify food resources consumed by the species, we collected fruits and seeds with unambiguous A. paca teeth marks. The only animal in Central America with an incisor width similar to A. paca. is Dasyprocta variegata; in a comparison of both species, however, we found that A. paca had a significantly larger incisor width and that teeth marks of 4 mm or wider unambiguously indicated handling by this species. By applying this technique, food resources utilized by A. paca can be identified more easily than by direct observation. At our study site, we identified 33 plant species consumed by A. paca; 61 percent are new records for this animal. Our results suggest that A. paca plays a major, although not fully understood, ecological role in seed predation and dispersal.     

The underground life of the oriental mole cricket: an analysis of burrow morphology

The underground life of the oriental mole cricket Gryllotalpa orientalis has been investigated by studying the structure of its burrows under different environmental situations and in different seasons. The different uses of different burrow types and their advantages and disadvantages have been examined. The total length, number of tunnels and combination of burrow types varied from a simple tunnel to a more complex one with branches at various angles to the surface, burrow types being divided roughly into shallow horizontal or deep vertical ones. In horizontal burrows, the branching structure was well developed in various directions. It is notable that the vertical burrows of G. orientalis were occupied by only one individual. Both vertical and horizontal burrows were used for foraging: vertical burrows for plants with subterranean stems and horizontal burrows for creeping plants. Vertical burrows were also used for hiding from predators, resting, moulting and overwintering, whereas horizontal burrows were used for escaping from predators and as mating routes. Egg chambers were constructed beside horizontal burrows, and calling burrows were constructed as part of horizontal burrows. Based on their current requirements, mole crickets continuously modify their burrow structures or change burrowing sites.     

The burrow system of the African ice rat Otomys sloggetti robertsi

We studied the architecture of the burrow system of the African ice rat Otomys sloggetti robertsi, a non–hibernating, diurnal murid rodent endemic to the sub–alpine and alpine regions of the southern African Drakensberg and Maluti mountains. In our study site we found ice rat burrows in two substrates (organic and mineral soils). The structure of the burrow system was similar in both soil types, comprising several interlinking tunnels, numerous burrow entrances and 1–2 nest chambers. However, the surface area of the burrow systems in organic soils was larger, the tunnels were deeper, and some of the systems contained two levels, all of which was contrary to our assumption that digging would be more difficult in the compact organic soils. Ice rats occur in colonies of up to 17 individuals, and the collected efforts of several individuals are required for constructing complex burrow systems. The burrow structure is similar to those of two arid–adapted relatives, Parotomys brantsii and Parotomys littledalei, suggesting that the burrow architecture among these three taxa may reflect the similar functions of burrows in extreme environments. For ice rats, burrows could provide a suitable microhabitat in which to escape adverse environmental conditions, particularly during winter. Moreover, ice rat burrows contained far fewer nest chambers than those of both Parotomys species, indicating that members in a colony share nest chambers, thereby facilitating huddling. Finally, the extensive interlinking tunnels may provide underground routes to aboveground feeding sites, thereby reducing exposure to adverse conditions.     

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。