Role of small rodents in the seed dispersal process: Microcavia australis consuming Prosopis flexuosa fruits

Understanding the functional role of animal species in seed dispersal is central to determining how biotic interactions could be affected by anthropogenic drivers. In the Monte Desert, mammals play different functional roles in Prosopis flexuosa seed dispersal, acting as opportunistic frugivores (endozoochorous medium‐sized and large mammals) or seed hoarders (some small sigmodontine rodents). Our objective was assessing the functional role of Microcavia australis, a small hystricognathi rodent, in the fruit removal and seed deposition stages of P. flexuosa seed dispersal, compared to sympatric sigmodontine rodents. In situ, we quantified fruit removal by small rodents during non‐fruiting and fruiting periods, and determined the distance seeds were transported, particularly by M. australis. In laboratory experiments, we analysed how M. australis stores seeds (through scatter‐ or larder‐hoarding) and how many seeds are left in caches as living seeds, relative to previous data on sigmodontine rodents. To conduct field studies, we established sampling stations under randomly chosen P. flexuosa trees at the Ñacuñán Man and Biosphere Reserve. We analysed fruit removal by small rodents and seed dispersal distance by M. australis using camera traps focused on P. flexuosa fruits covered with wire screen, which only allowed entry of small animals. In laboratory trials, we provided animals with a known number of fruits and assessed seed conditions after removal. Small rodents removed 75.7% of fruit supplied during the non‐fruiting period and 53.2% during the fruiting period. Microcavia australis and Graomys griseoflavus were the main fruit removers. Microcavia australis transported seeds to a mean distance of 462 cm and cached seeds mainly in scatter‐hoards, similarly as Eligmodontia typus. All transported seeds were left in fruit segments or covered only by the endocarp, never as predated seeds. Microcavia australis disperses P. flexuosa seeds by carrying fruits away from a source to consume them and then by scatter‐hoarding fruits and seeds.     

种子特征和结实量对啮齿动物取食和扩散种子行为的影响

为了深入了解啮齿动物在不同种子丰富度条件下对不同大小和单宁含量种子的觅食行为策略及其与植物种群更新的关系,在宁夏六盘山区的华北落叶松人工林,研究了不同大小和单宁含量[0%Tannin(T)、2%T、8%T和15%T]的人工种子在模拟结实小年和结实大年对啮齿动物取食和扩散行为的影响.结果表明: 啮齿动物消耗种子速度在结实小年更快,结实大年的种子消耗速度相对缓慢. 种子就地取食率(ISPR)在不同结实年份间无显著差异,扩散后取食率(PRAD)在结实小年显著高于结实大年,但前者的扩散后贮藏率(HRAD)显著低于后者;种子扩散后的取食距离(PDAD)和贮藏距离(HDAD)在结实小年均显著大于结实大年.在结实小年,大种子的PDAD和HDAD均大于小种子,前者在不同大小种子间均差异显著,而后者仅在2%T和15%T的不同大小种子间差异显著;在结实大年,除0%T外的其他单宁含量种子的PDAD和HDAD在不同大小种子间均差异显著.ISPR在中等单宁含量种子最大,高单宁含量种子最小;PRAD分别在结实小年的高单宁含量种子和结实大年的无单宁种子最大;不论在结实大年还是结实小年,HRAD均在高单宁含量种子最大,中等单宁含量种子最小.这说明结实大年可延缓啮齿动物对种子的消耗速率,提高种子的HRAD,但种子扩散距离减小;啮齿动物在结实大年和小年均表现出对大种子的扩散偏好,且大种子被扩散的距离更远;啮齿动物在不同结实年份均偏好于就地取食中等单宁含量种子,而扩散高单宁含量种子.     

The role of Rhytidoponera metallica (Hymenoptera,Formicidae) in facilitating post‐fire seed germination of three ant‐dispersed legume species

The fire avoidance hypothesis proposes that a benefit of seed dispersal by ants (myrmecochory) is to protect seeds from being killed during fire and to facilitate post‐fire germination of seeds that require heat shock to break their physical dormancy. The aim of this study was to quantify the effect of fire and seed burial by a predominant seed‐dispersing ant, Rhytidoponera metallica (subfamily: Ectatomminae) on germination levels of three ant‐dispersed legume species (Pultenaea daphnoides, Acacia myrtifolia and Acacia pycnantha). Experimental burial of seeds within aluminium cans at a site prior to being burnt and at an adjacent unburnt site showed that fire increased germination levels, particularly for seeds buried at 1‐ and 2‐cm deep and that overall, germination levels differed among the three plant species. To quantify seed burial depths and post‐fire germination levels facilitated by R. metallica ants, seeds were fed to colonies prior to fire at the burnt and unburnt sites. Of the seeds buried within nests that were recovered, between 45% and 75% occurred within the upper 6 cm of the soil profile, although unexpectedly, greater percentages of seeds were recovered from the upper 0–2 cm of nests in the unburnt site compared with nests in the burnt site. Germination levels of buried seeds associated with R. metallica nests ranged from 21.2% to 29.5% in the burnt site compared with 3.1–14.8% in the unburnt site. While increased seed germination levels were associated with R. metallica nests following fire, most seeds were buried at depths below those where optimal temperatures for breaking seed dormancy occurred during the fire. We suggest that R. metallica ants may provide fire avoidance benefits to myrmecochorous seeds by burying them at a range of depths within a potential germination zone defined by intra‐ and inter‐fire variation in levels of soil heating.     

Interspecific synchrony of seed rain shapes rodent‐mediated indirect seed–seed interactions of sympatric tree species in a subtropical forest

Animal‐mediated indirect interactions play a significant role in maintaining the biodiversity of plant communities. Less known is whether interspecific synchrony of seed rain can alter the indirect interactions of sympatric tree species. We assessed the seed dispersal success by tracking the fates of 21 600 tagged seeds from six paired sympatric tree species in both monospecific and mixed plots across 4 successive years in a subtropical forest. We found that apparent mutualism was associated with the interspecific synchrony of seed rain both seasonally and yearly, whereas apparent competition or apparent predation was associated with interspecific asynchrony of seed rain either seasonally or yearly. We did not find consistent associations of indirect interactions with seed traits. Our study suggests that the interspecific synchrony of seed rain plays a key role in the formation of animal‐mediated indirect interactions, which, in turn, may alter the seasonal or yearly seed rain schedules of sympatric tree species.     

鼠类扩散种子的几种标签标记法的比较

以四川省都江堰市亚热带常绿阔叶林内的优势鼠种——小泡巨鼠为实验动物,通过半自然状态围栏控制实验,检验了几种种子标签法对鼠类扩散植物种子的影响。结果表明:鱼线和细钢丝两种标记线在跟踪扩散种子命运上都是很有效的,但考虑到鱼线有时会被实验鼠咬断,细钢丝是更值得推广应用的一种标记线。3种标记牌(大塑料牌、小塑料牌和金属牌)在跟踪扩散种子命运上没有显著差异,但由于较大的尺寸和较强的可见度,大塑料牌更适合作为标签应用于野外种子扩散标记。     

Seed caching by woylies Bettongia penicillata can increase sandalwood Santalum spicatum regeneration in Western Australia

Abstract The role a small marsupial, the woylie Bettongia penicillata, might play in the recruitment and regeneration of Western Australian sandalwood Santalum spicatum through its seed caching behaviour was investigated in this study. To determine the fate of the seeds, cotton thread was attached to the seeds and the trail followed. A total of 25 seed caches were located. All of the seeds were found in separate caches, which was consistent with scatter‐hoarding behaviour. The average distance from the source of the seeds to the cache was 43.1 m ± 5.8 m at Dryandra woodland and 29.1 m ± 3.8 m at Karakamia sanctuary. The mean cache depth was 4.3 cm ± 0.2 cm at Dryandra woodland compared with 4.6 cm ± 0.3 cm at Karakamia sanctuary. Significantly more seedlings and saplings grew away from sandalwood trees at sites where woylies were present than at sites with no woylies. In contrast, significantly more seedlings and saplings grew under adult sandalwood trees at the site without woylies than where they were present, although there were significantly lower rates of recruitment and sandalwood regeneration at these sites. In addition, significantly more whole, undisturbed sandalwood seeds were found under the parent trees at the woylie‐free site than at the site with woylies. These findings strongly suggest that little seed dispersal or regeneration of sandalwood occurs in the absence of woylies. Through scatter‐hoarding, woylies have the potential to disperse and cache sandalwood seeds away from the source and significantly alter the subsequent regeneration of sandalwood. Furthermore, by caching seeds large distances away from a source, woylies could modify the distribution of sandalwood in an area.     

Directed seed dispersal towards areas with low conspecific tree density by a scatter‐hoarding rodent

Scatter‐hoarding animals spread out cached seeds to reduce density‐dependent theft of their food reserves. This behaviour could lead to directed dispersal into areas with lower densities of conspecific trees, where seed and seedling survival are higher, and could profoundly affect the spatial structure of plant communities. We tested this hypothesis with Central American agoutis and Astrocaryum standleyanum palm seeds on Barro Colorado Island, Panama. We radio‐tracked seeds as they were cached and re‐cached by agoutis, calculated the density of adult Astrocaryum trees surrounding each cache, and tested whether the observed number of trees around seed caches declined more than expected under random dispersal. Seedling establishment success was negatively dependent on seed density, and agoutis carried seeds towards locations with lower conspecific tree densities, thus facilitating the escape of seeds from natural enemies. This behaviour may be a widespread mechanism leading to highly effective seed dispersal by scatter‐hoarding animals.     

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。     

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.     

Fruit Removal and Natural Seed Dispersal of the Brazil Nut Tree (Bertholletia excelsa) in Central Amazonia,Brazil

Experimental approaches to study seed dispersal of the Brazil nut tree have hitherto relied on exposed seeds deposited on the forest floor. Here we use a new method to study the natural dispersal by large rodents such as agoutis; tracking experimentally manipulated and tagged fruits containing individually marked seeds. Fruit manipulation did not deter agoutis from handling fruits. We found that agoutis usually moved intact fruits away from their original location below the parent tree before either hiding them or gnawing through the pericarp to access the seeds inside. Most fruits were moved to distances of 15–30 m from their original position, but some fruits could be taken as far as 60 m. A large number of seeds extracted from manipulated fruits appeared to be eaten immediately. Only 27 out of 1740 experimental seeds were found buried in shallow caches, generally within 5 m of the opened fruit. Fruit removal distance accounted for a disproportionate amount of total seed movement and seeds in the current study were dispersed significantly farther than in a previous experiment using exposed seeds, suggesting that classic dispersal experiments of this character may severely underestimate seed dispersal distances. We therefore conclude that the new method provides a more realistic and accurate approach to investigate natural seed dispersal of Brazil nuts and that the removal of fruits from underneath parent trees before being opened is the key to the significantly increased distances at which seeds are dispersed. Abstract in Portuguese is available at http://www.blackwell‐synergy.com/loi/btp .     

凋落物和土壤覆盖对动物取食和搬运辽东栎种子的影响

在六盘山区的华北落叶松人工林,研究了清除凋落物、凋落物覆盖和土壤覆盖(以不清除凋落物直接将种子投放于森林地表为对照)等处理对动物取食和搬运辽东栎种子的影响.结果表明:种子释放3d后,凋落物和土壤覆盖处理种子均具有较高的留存率(分别为10.7％和7.0％);释放14 d后,土壤覆盖处理种子的留存率仍最高(0.7％),但凋落物覆盖处理种子的留存率为0.凋落物和土壤覆盖处理种子的就地取食率很高(分别为45.9％和41.5％);清除凋落物处理种子的就地取食率最低(27.0％),但其被搬运后的取食率最高(49.8％);凋落物覆盖、清除凋落物和土壤覆盖处理种子被动物搬运后的埋藏率均显著高于对照(P＜0.01).种子被动物搬运后集中分布于5 m以内,尤其在＜1 m和l～2m两个距离组的分布频率更高;种子被搬运后取食的平均距离大干埋藏的平均距离,以土壤覆盖和凋落物覆盖处理最大,分别为2.38 m±0.55 m和1.44m±0.26 m.     

Interactive influences of fire intensity and vertical distribution of seed banks on post‐fire recolonization of a tall‐tussock grassland in Argentina

Abstract Recolonization patterns of a tall‐tussock grassland differ between low‐frequency and high‐intensity fires. A series of laboratory and field experiments were performed on the seed bank and on seeds of the main colonizing species (Carduus acanthoides, Cirsium vulgare, Lotus glaber) to determine and compare the effects of fire frequency and fire intensity on their recolonization potential. Seed‐bank size of colonizing species did not show a significant variation with contrasting fire frequencies, so overall interval‐dependent effects do not seem to affect their propagule pool at the time of fire. However, frequency of fire modified the proportion of viable seeds and their dormancy state according to species. Accumulated emergence from experimentally buried soft‐seeds of Lotus was lower after high‐intensity fires (following wind direction) than after back‐fires (against wind direction), but no significant effects of fire‐front direction on seedling emergence were observed for hard‐seeds of Lotus nor Carduus and Cirsium. Seedling emergence from buried seeds of Cirsium was increased with doubling fuel loads, particularly from deepen soil layers, where Cirsium had most of their viable seeds after a low frequency of fire. Emergence from hard‐seeds of Lotus was less promoted than Cirsium by doubling fuel loads, and according to analysis of excavated seedlings, it was completely inhibited from upper soil layers of the seed bank. Integration of species‐specific and burial depth‐specific responses of Cirsium and Lotus seeds according to fuel load, vertical distribution of the seed banks, seed dormant states and mean emergence depths, resulted in expected emergence values which agree with their previously observed patterns of recolonization. Thus, event‐dependent mechanisms had a better predictive value on recolonization success of the studied species than the observed cumulative effects of fire history on their seed‐bank size.     

Seed dynamics of resprouting shrubs in grassy woodlands: Seed rain,predators and seed loss constrain recruitment potential

Abstract Measuring the fate of seeds between seed production and seedling establishment is critical in understanding mechanisms of recruitment limitation of plants. We examined seed fates to better understand the recruitment dynamics of four resprouting shrubs from two families (Fabaceae and Epacridaceae) in temperate grassy woodlands. We tested whether: (i) pre‐dispersal seed predation affected seed rain; (ii) post‐dispersal seed predation limited seed bank accumulation; (iii) the size of the seed bank was related to seed size; and (iv) viable seeds accumulated in the soil after seed rain. There was a distinct difference in seed production per plant between plant families with the legumes producing significantly more seeds per individual than the epacrids. Seed viability ranged from 43% to 81% and all viable had seed or fruit coat dormancy broken by heat or scarification. Pre‐dispersal predation by Lepidopteran larvae removed a large proportion of seed from the legume seed rain but not the epacrids. Four species of ants (Notoncus ectatomoides, Pheidole sp., Rhytidoponera tasmaniensis and Iridomyrmex purpureus) were major post‐dispersal seed removers. Overall, a greater percentage of Hardenbergia (38%) and Pultenaea (59%) seeds were removed than the fleshy fruits of Lissanthe (14%) or Melichrus (0%). Seed bank sizes were small (<15 seeds m^?2) relative to the seed rain and no significant accumulation of seed in the soil was detected. Lack of accumulation was attributed to seed predation as seed decay was considered unlikely and no seed germination was observed in our study sites. Our study suggests that seed predation is a key factor contributing to seed‐limited recruitment in grassy woodland shrubs by reducing the number of seeds stored in the soil.     

The Interplay of Habitat and Seed Type on Scatterhoarding Behavior in a Fragmented Afromontane Forest Landscape

Scatterhoarding by rodents, whereby seeds are collected and stored for later consumption, can result in seed dispersal. Seeds may be covered in litter on the forest floor (cached) or buried. This is particularly so in the Neotropics for large, nutritious seeds, and where primary dispersers are rare or missing. In African forests, contemporary anthropogenic pressures such as hunting, forest degradation, and fragmentation are contributing toward major declines in large frugivores, yet the potential for scatterhoarding to mitigate this loss is largely unknown. In this study, we used thread‐marked seed to explore the balance between seed predation and dispersal by rodents in Afromontane forest. We studied two tree species in three habitats: (1) continuous forest; (2) continuous forest edge, and (3) small, degraded riparian forest patches. We found that seed removal rates were high and almost the same in all three habitats for both tree species, but that the predation/dispersal balance differed among habitats. In continuous forest, more seeds of each species were scatterhoarded than depredated, and rates of scatterhoarding differed between the two species. In all habitats, burying seeds up to 2 cm belowground was more common than caching. Distances seeds were moved was approximately five times greater in continuous forest than in forest edge or riparian patches. We found strong evidence to suggest that the African pouched rat, Cricetomys sp. nov was responsible for the scatterhoarding.     

Extrafloral nectar increases seed removal by ants in Turnera ulmifolia

To investigate whether extrafloral nectar (EFN) increases seed dispersal in Turnera ulmifolia, we measured seed removal on plants with and without EFN. Plants producing EFN had more seeds removed than control plants, suggesting that EFN does play a role in seed dispersal. This is a novel function of EFN.     

Seed Dispersal by Salvin's Curassow,Mitu salvini (Cracidae), in a Tropical Forest of Colombia: Direct Measurements of Dispersal Distance1

Seed dispersal by Salvin's curassows (Mitu salvini) was studied in a lowland tropical forest at La Macarena on the border of the Macarena and Tinigua National Parks, the Department of Meta, Colombia. Continuous observations were made on the feeding and ranging behavior of a well-habituated pair of birds from 0600 to 1800 h for 19 days. Ibtal observation time was 222 h. The daily distance traveled by the birds ranged from 630 to 3750 m, with a mean of 1959 m (± 776 m). The total home range was ca 34.4 ha. Although curassows were observed consuming fruits of 13 species belonging to the families Rubiaceae, Meliaceae, Moraceae, Burseraceae, Leguminosae, and Lecythidaceae, only seeds of Geophila re fens (Rubiaceae) and Picas spbenophylla (Moraceae) were found in their feces. For G. repens, the mean and maximum retention times were 1 h 52 min (± 1 h 20 min) and 6 h 08 min, and the mean and maximum direct dispersal distances were 245 m (± 164 m) and 633 m. More than half the seeds were dispersed in canopy gaps. For F. sphenophylla, the mean and maximum retention times were 3 h 1 5 mm (± .37 min) and 7 h 08 min, and the mean and maximum direct dispersal distances were 329 m (± 46 m) and 451 m. Nearly 60 percent of the estimated seed intake of G. repens and 92-94 percent of F. sphenophylla were digested or damaged. The retention times and the dispersal distances for Streptogyna americana, which has adhesive burrs, were also measured. The mean and maximum retention times were 1 h 55 min (± 1 h 56 min) and 9 h 11 min, and the mean and maximum direct dispersal distances were 128 m (± 68 m) and 280 m. This is the first study in which direct measurements were made for retention times and dispersal distances of the epizoochory and endozoochory for birds in the field.     

淡水湿地种子库的小尺度空间格局

以长江中下游淡水湿地湖里沼泽为对象,研究了种子库在小尺度空间范围的水平分布格局。在沼泽中选择地表植被分布比较均一的16m×4m大小的方形区域,按1m间隔获取64个内径7·8cm、深5cm的圆柱状土样,通过幼苗萌发法鉴定每个土样的种子库组成。采用2个格局指数(离散系数和Lloyd平均拥挤指数)以及Moran空间自相关系数分析了种子库中优势种的空间分布格局。结果显示种子库由17个物种组成,多年生的锐棱荸荠(Eleocharisacutangula)和龙师草(E·tetraqueter)是种子库中密度最大的物种。两个格局指数显示7个分布频率大于10%的物种的种子全部为聚集分布。MoransI统计分析显示其中只有3个物种为显著的正的空间自相关,表明这3个物种的种子斑块大小超过了目前的两个取样单位之间的距离(1m),而其它4个物种的种子斑块则小于这个尺度。