Acorn Pericarp Removal as a Cache Management Strategy of the Siberian Chipmunk,Tamias sibiricus

Numerous recent studies have revealed a variety of behavioral adaptations of rodents for maximizing returns from cached seeds. Herein we report on a novel behavior by the Siberian chipmunk (Tamias sibiricus) in northeastern China, by which they consistently remove the pericarp (shell) of Quercus mongolica acorns before dispersing and caching these nuts. We investigated the effects of pericarp removal on acorn germination, tannin concentrations, cache pilferage, and insect damage, to determine if and how pericarp removal facilitates cache management by Siberian chipmunks and whether or not such behavior influences seed fates. Chipmunks cached acorns only after the pericarps were removed. Chipmunks preferred pericarp‐removed acorns over intact acorns when removing them from seed stations for both consumption and caching. Pericarp removal did not affect germination or tannin concentration of cached Q. mongolica acorns, suggesting that the behavior is not an adaptation for long‐term storage and tannin decomposition. Acetone treatments of the pericarp and artificial pericarp removal failed to alter pilferage rates by Siberian chipmunks and wood mice (Apodemus peninsulae). Since damage of acorns by weevils often leads to cache losses, we also tested the effects of weevil infestation on cache decision following pericarp removal. Siberian chipmunks removed pericarps and then scatter hoarded significantly more sound than weevil‐infested acorns, strongly suggesting that pericarp removal is used to discriminate between the infested and non‐infested acorns. Thus, we argue that the primary function of this behavior is to ensure successful storage of sound acorns, at least for short‐term storage. Future studies should consider the potential impact of pericarp removal on weevil populations and long‐term patterns of seed survival and establishment from the Siberian chipmunk’s caches.     

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.     

Acorns containing deeper plumule survive better: how white oaks counter embryo excision by rodents

Several squirrel species excise the embryo of acorns of most white oak species to arrest germination for long‐term storage. However, it is not clear how these acorns counter embryo excision and survive in the arms race of coevolution. In this study, we simulated the embryo excision behavior of squirrels by removing 4 mm of cotyledon from the apical end of white oak acorns differing in embryo depths to investigate the effects of embryo excision on acorn germination and seedling performance of white oak species. The embryo depth in the cotyledons was significantly different among white oak acorns, with Quercus mongolica containing the embryo most deeply in the acorns. We found that artificial embryo excision significantly decreased acorn germination rates of Quercus variabilis, Quercus acutissima, Quercus aliena, Quercus aliena var. acutiserrata, Quercus serrata. var. brevipetiolata but not Q. mongolica. Artificial embryo excision exerted significant negative impacts on seedling performance of all oak species except Quercus aliena. Our study demonstrates the role of embryo depth of acorns in countering embryo excision by squirrels and may explain the fact that squirrels do not perform embryo excision in acorns of Q. mongolica with deeper embryos. This apparent adaptation of acorns sheds light on the coevolutionary dynamics between oaks and their seed predators.     

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.     

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.     

Epicotyl morphophysiological dormancy in seeds of Lilium polyphyllum (Liliaceae)

Dormancy-breaking and seed germination studies in genus Lilium reveal that the majority of Lilium spp. studied have an underdeveloped embryo at maturity, which grows inside the seed before the radicle emerges. Additionally, the embryo, radicle or cotyledon has a physiological component of dormancy; thus, Lilium seeds have morphophysiological dormancy (MPD). A previous study suggested that seeds of Lilium polyphyllum have MPD but the study did not investigate the development of the embryo, which is one of the main criteria to determine MPD in seeds. To test this hypothesis, we investigated embryo growth and emergence of radicles and epicotyls in seeds over a range of temperatures. At maturity, seeds had underdeveloped embryos which developed fully at warm temperature within 6 weeks. Immediately after embryo growth, radicles also emerged at warm temperatures. However, epicotyls failed to emerge soon after radicle emergence. Epicotyls emerged from >90% seeds with an emerged radicle only after they were subjected to 2 weeks of cold moist stratification. The overall temperature requirements for dormancy-breaking and seed germination indicate a non-deep simple epicotyl MPD in L. polyphyllum.     

Pregnancy coloration in macaques may act as a warning signal to reduce antagonism by conspecifics

Co-varying traits in acorns such as seed size and germination schedule are important to influence the behavioural decisions of hoarding rodents. Using acorn pairs from cork oak (Quercus variabilis) (large size and short germination schedules) serrate oak (Q. serrata) (small size and short germination schedule) and qinggang (Cyclobalanopsis glauca) (small size and long germination schedule) with contrasting seed size and germination schedule, we conducted a series of experiments to investigate hoarding preferences in response to seed size and germination schedule by Edward's long-tailed rats (Leopoldamys edwardsi) and South China field mice (Apodemus draco) in semi-natural enclosures. We found that the seed size hypothesis was consistently supported: both rodent species ate more small acorns but hoarded more large ones regardless of germination schedules. However, the germination schedule hypothesis was also supported when similar sized acorns were simultaneously provided, e.g. Q. serrata versus C. glauca or germinating versus non-germinating Q. variabilis. Our results, contrary to the studies from North America, indicate that seed size is more important than germination schedules in determining whether the tested animals eat or hoard a given seed.     

Radicle emergence with increased temperatures following summer dispersal in Trillium camschatcense: A species with deep simple double morphophysiological dormancy in seeds

Seeds with deep simple double morphophysiological dormancy (MPD) need cold stratification during the first winter after dispersal for radicle emergence, followed by the summer for root and bud development and finally a second winter for shoot emergence. In a previous study, we demonstrated that Trillium camschatcense seeds have this type of dormancy with radicles emerging from most seeds after the first winter. However, radicles also emerged from a few seeds in autumn during the same year as dispersal. We thought that temperatures after seed dispersal played a role in radicle emergence before the first winter. To confirm our idea, we investigated germination phenology outdoors, relationships between temperatures after seed dispersal and radicle emergence in the first year outdoors, radicle emergence in the first winter under varied temperatures using incubators, and shoot emergence from seeds with an emerged radicle in the first year outdoors. Our phenology study confirmed that T. camschatcense seeds have deep simple double MPD. Over 7 years, 0.2–7.5% of radicles emerged in the first year before winter and these percentages were moderately positively correlated with temperatures, especially minimum temperatures. Increasing August and September temperatures increased radicle emergence in the laboratory. Shoots emerged from seeds with an emerged radicle in the first year after the first winter. With increased autumn temperatures in warmer regions or with global warming, we predict that germination phenology may shift: increased radicle emergence in the first year and shoot emergence following the first (and not second) winter.     

Habitat and food utilization of the Siberian chipmunk,Tamias sibiricus,in Korea

Compared to European countries where the Siberian chipmunk (Tamias sibiricus) is an invasive species, there is a paucity of information on the ecology and natural history of Korean populations. T. sibiricus is a native species with large populations in Korea. We conducted field research during January to December 2012 in a forest habitat located in Hongcheon-gun, Gangwon-do (37° 45′ 50″ N, 127° 50′ 52″ E) in central Korea. We used both radio-tracking and capture-recapture techniques to determine home range size and nocturnal shelters. We also excavated and measured burrows and analyzed food items from caches. The mean 95 % of kernel home range size for males was 16,586 m² (100 % of MCP?=?14,129 m²) and 4,432 m² (100 % of MCP?=?4,512 m²) for females. Burrow systems typically had a nest, latrine, and food caches with tunnels. Nocturnal shelters were uncommon and co-habiting for summer sleeping and winter torpor were also rare. The primary food items in caches were chestnuts (77.0 %), Mongolian oak acorns (12.1 %), and bird’s-foot trefoil (2.1 %). The information on the ecology and natural history of the Korean subspecies of Siberian chipmunks reported in this research shows significant differences from the ecological information for the subspecies in Hokkaido Japan.     

Food hoarding behaviour of large field mouseApodemus peninsulae

An important behavioural adaptation for animal species with variable or unpredictable food availability is storing food. Food availability for large field mouseApodemus peninsulae (Thomas, 1907) is not reliable. We conducted a series of tests with the large field mouse to determine food hoarding behaviour, response when their hoarded food was removed, and whether perishable foods were treated different than non perishable foods. The study was conducted in four semi-natural enclosures (4 × 3 × 1 m), established on the Donglingshan Mountain near Beijing, China. Thirteen large field mice were placed in enclosures and offered wild apricotPrunus armeniaca seeds and Liaodong oakQuercus liaotungensis acorns. Our results indicated that although large field mice hoarded seeds in larder and scatter patterns, they more frequently exhibited larder hoarding. Liadong oak acorns were generally consumed near the feeder, whereas apricot seeds were more frequently transported to the nest box. Only apricot seeds were scattered among hoard sites. When seeds were removed from hoarding sites the mice responded by taking increased amounts of seeds to their nest for larder and scatter hoarding. Hoarding sites were not randomly distributed throughout the enclosure.     

锐齿槲栎橡子埋藏深度对发芽、幼苗出土和发育的影响

锐齿槲栎（Quercus aliena var.acuteserrata Maxim.)林内活动的许多型哺乳动物和鸟类不仅采食橡子,而且还常窖贮或在土壤大量的橡 子以便季后利用。这些埋藏的橡子构成了发育有效更新苗的主要种子来源。橡子被埋藏的深度和橡子的大小对幼苗的发育有潜在的影响。把橡子埋藏在6、12和18cm3个土层深度的实验结果显示：随着埋藏深度的增加,橡子的发芽率和发芽橡子的幼苗出土率都有明显下降,由深埋橡胶子发育的幼苗出土比较困难,所需时间较长,也更易腐烂,橡子的大小对发芽和幼苗出土没有明显的影响,早出土幼苗在第一个生长季内由于有较长的生长发育期,季末发育得较好,所以,由浅埋橡子发育的幼苗在更新成功方面有优势。     

Effect of Acorn Burying Depth on Germination,Seedling Emergence and Development of Quercus aliena var. acuteserrata

Acorns of Quercus aliena var. acuteserrata Maxim. are often predated by small mammals and birds in natural forests. These animals not only eat the acorns during the acorn ripening season, but also cache and hoard most of the remaining acorns on the forest floor in the soil for their future use. These buried acorns form the main seed resource for regeneration. Burying depth is potentially important for germination and for seedling development. The effects of burying depth on germination and seedling development in relation to acorn size were studied in an experiment, in which acorns were planted at 6 cm-, 12 cm- and 18 cm-depth. The experimental results showed that fewer acorns germinated as burying depth increased. From the deeply buried acorns fewer seedlings emerged at later time than from those acorns buried less deeply. They appeared to have more difficulties to emerge above-ground than the seedlings from shallowly buried acorns. The deeply buried acorns and their seedlings also appeared to be more susceptible to rot. Acorn size did not significantly affect germination and emergence of the seedlings. As early emerged seedlings had longer developmental periods in their first growing season, and therefore grew better than the late emerged seedlings, seedlings from the shallowly buried acorns took the advantage.     

STUDIES ON THE GERMINATION OF SEEDS OF THE ROOT PARASITES,ALECTRA VOGELII AND STRIGA GESNERIOIDES. I. ANATOMICAL CHANGES IN THE EMBRYOS

Anatomical changes in the radicle and shoot meristems of embryos of germinating seeds of the obligate root parasites, Alectra vogelii and Striga gesnerioides were studied. When germination of seeds was stimulated by cowpea (Vigna unguiculata) root exudate, growth occurred mainly in the radicular pole of embryos and minimally in the plumular pole, resulting in seedlings with elongated radicles. Maximum radicle elongations of about 3 mm in A. vogelii and 2 mm in S. gesnerioides were recorded during a period of 8 and 11 days, respectively. Analysis of the radicular tip during the course of seed germination revealed that the activity of the meristematic tissue progressively decreased until it completely disappeared. When germinated seeds were cultured on nutrient agar media, the radicle meristem of A. vogelii continued to grow producing a normal root with a root cap. On the other hand, the radicles of cultured S. gesnerioides seeds elongated only slightly before meristematic activity ceased. During continued growth of seedlings of both species on agar media, lateral roots whose tips had typical angiosperm root topography, were initiated from the radicle.     

Partial acorn consumption by small rodents: implication for regeneration of white oak, <Emphasis Type="Italic">Quercus mongolica</Emphasis>

Partial consumption of acorns by rodents, birds, and insects has been widely reported in various oak species. However, to what extent these partially eaten acorns contribute to the regeneration of oak trees is poorly understood. To date, there is limited knowledge of the effects of seed availability on partial consumption of acorns. Herein, we released tagged Quercus mongolica acorns in two consecutive years with different seed crops, to explore the probability of partial acorn consumption. We also placed simulated partially consumed acorns in the field to investigate their contribution to regeneration of white oak. Our results showed that more acorns were partially eaten in a good crop year than in poor crop year, reflecting an effect of predator satiation on acorn partial consumption by rodents at the population level. Partially eaten acorns were more likely to be damaged at the basal end, suggesting consistent consumption preferences of small rodents. Although, partially consumed acorns were less likely to be scatter-hoarded by small rodents, they germinated more rapidly than the intact acorns in the field, offsetting the negative effects of the non-buried deposition. Despite lower germination rates, lightly damaged acorns exhibited greater growth of roots and shoots, suggesting a compensatory response to partial acorn consumption. Partial consumption may spread predation pressure on acorns and thus appears to be much better for the plant than total consumption by seed-eating animals. Therefore, partially consumed acorns as dispersal leftovers may play a potential role in natural regeneration of Quercus mongolica, especially in mast years. However, this role and the underlying mechanisms of partial acorn consumption by rodents, birds, and herbivore insects need further investigation.     

Development of the quiescent center in maturing embryonic radicles of pea (Pisum sativum L. cv. Alaska)

Maturing embryos of pea (Pisum sativum L. cv. Alaska) were treated with an aqueous solution of tritiated thymidine for 1 h, sectioned, and processed for autoradiography. An analysis of the distribution of labelled nuclei and mitotic figures demonstrated the presence of a quiescent center (QC) in the radicles of developing embryos. The QC developed in the radicle during the growth of the embryo. Immature radicles that did not contain a well-formed zone of root-cap initials did not show a QC. In the latter stages of seed ripening, the pattern of arrest of DNA synthesis and mitosis was tissue-specific. Cells within the QC remained inactive. The region lacking labelled nuclei and mitotic figures progressively expanded to include the root cap initials and then the provascular cylinder. Mitosis was arrested before DNA synthesis in the embryonic cortex. Cells within the QC synthesized DNA during the first stages of seed germination.Abbreviations [³H]TdR tritiated thymidine - QC quiescent center     

Phenotypic plasticity in the holoparasitic mistletoe <Emphasis Type="Italic">Tristerix aphyllus</Emphasis> (Loranthaceae): consequences of trait variation for successful establishment

The ability of a genotype to respond to changes in the environment through modifications in the phenotype is adaptive when the plastic genotypes attain a higher fitness than non-plastic genotypes. In this study we examine whether parasite traits involved in host infection exhibit adaptive phenotypic plasticity to the heterogeneous host microenvironment. We focused on a host-parasite relationship characterized by the holoparasitic mistletoe Tristerix aphyllus and the cactus host Echinopsis chilensis. Unlike most mistletoes, whose seeds are deposited on the host branches, seeds of T. aphyllus are often deposited on the spines of the cactus. The extremely long radicles of T. aphyllus have been suggested to represent a parasite adaptation to overcome the barriers to infection imposed by the spines of cacti. However, plastic rather than canalized phenotypes may represent a better strategy in changing environments. We evaluated whether T. aphyllus exhibits adaptive plasticity in radicle length through a sire half-sib genetic design under field conditions in two contrasting microenvironments (seeds deposited on spines 4 and 28 mm from the host surface). We used phenotypic and genotypic selection analyses to evaluate the relationship between radicle length and seed establishment. Our results revealed significant phenotypic plasticity for radicle length and family level variation among maternal but not paternal families. Short radicles and large seeds were favored in the short-distance environment, and long radicles were favored in the long-distance environment, suggesting that no single optimal phenotype exists for T. aphyllus. The observation that the heritability of radicle length and seed mass did not differ from zero was consistent with this finding. Overall, our results indicate that plastic rather than long radicles seem to be a better parasite strategy to overcome the microenvironmental heterogeneity imposed by host defensive traits.     

栎属7种植物种子的发芽抑制物质研究

运用系统溶剂法和生物测定法,以栎属7种植物种子为材料,研究了其种皮、胚(胚及周围部分子叶)和子叶(远离胚端2/3子叶)1.0 g/mL和0.5 g/mL浓度甲醇等浸提液以及各有机相对白菜种子萌发的影响。结果表明:栓皮栎、锐齿栎、蒙古栎、沼生栎和麻栎甲醇浸提液均能显著降低白菜种子发芽率、根长和苗高,且对发芽率的抑制作用逐渐降低;夏栎和房山栎甲醇浸提液对白菜种子发芽率没有显著影响,但对根长和苗高有一定的抑制作用;种子不同部位甲醇浸提液的抑制作用表现为胚>子叶>种皮,且甲醇高浓度浸提液的抑制作用大于低浓度的抑制作用;甲醇相对白菜种子发芽率、苗高或根长的抑制作用最强,其次是乙酸乙酯相,其它溶剂相萃取液的抑制作用不明显。栎属种子甲醇浸提液及各有机相对白菜种子苗高和根长的抑制作用强于对发芽率的影响,说明栎属种子中所含抑制物质主要是限制自身根和芽的生长,可能是造成延迟萌发和出苗不整齐的原因。     

Activation of acid growth in germinating horse chestnut seeds

The validity of the acid-growth hypothesis is proved for the case of cell elongation initiation in germinating seeds of horse chestnut (Aesculus hippocastanum L.), the embryo axes of which are known to extend during the first stages of germination only by cell elongation. During seed imbibition, H⁺-ion excretion was firstly low; it increased several times prior to radicle emergence and was maintained at a high level during growth initiation and further cell elongation. Cell wall acidification and radicle emergence were enhanced in the presence of 0.02 mM fusicoccin, thus indicating the involvement of the plasma membrane H⁺-ATPase in the execution of acid growth. The presence of this enzyme and its activator (14-3-3 protein) in microsomal fractions obtained from radicles and hypocotyls of the embryo axes during and after initiation of cell elongation was demonstrated immunochemically. It is supposed that the initiation of cell elongation at early germination occurs via the activation of the plasma membrane H⁺-ATPase and results in the acidification of cell walls, leading to their higher extensibility, in accordance with the hypothesis of acid growth.     

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.     

Effect of plumule and radicle on somatic embryogenesis in the cultures of ginseng zygotic embryos

Immature zygotic embryos of ginseng produced somatic embryos on MS medium without growth regulators. However, in the culture of mature zygotic embryos, excision of the embryo was required for somatic embryo induction. Somatic embryos formed only on excised cotyledons without an embryo axis or on excised embryos without the plumule and radicle of the axis. This observation suggests that the axis tip of the embryo might suppress somatic embryo production although the cotyledon tissues have predetermined embryogenic competency. To clarify the role of the embryo axis on somatic embryo formation, excised plumules or radicles were placed in direct contact with the basal cut-ends of cotyledons. The adhesion of plumules or radicles highly suppressed somatic embryo formation from cotyledon explants. When an agar block containing exudate from excised plumules or radicles was placed in contact with the cut end of the cotyledon, a similar inhibition was observed. These results suggest that embryogenic competence is suppressed by endogenous inhibitors present in the axis tip of the zygotic embryo.