Seed dispersal by ungulates as an ecological filter: a trait‐based meta‐analysis

Plant communities are often dispersal‐limited and zoochory can be an efficient mechanism for plants to colonize new patches of potentially suitable habitat. We predicted that seed dispersal by ungulates acts as an ecological filter – which differentially affects individuals according to their characteristics and shapes species assemblages – and that the filter varies according to the dispersal mechanism (endozoochory, fur‐epizoochory and hoof‐epizoochory). We conducted two‐step individual participant data meta‐analyses of 52 studies on plant dispersal by ungulates in fragmented landscapes, comparing eight plant traits and two habitat indicators between dispersed and non‐dispersed plants. We found that ungulates dispersed at least 44% of the available plant species. Moreover, some plant traits and habitat indicators increased the likelihood for plant of being dispersed. Persistent or nitrophilous plant species from open habitats or bearing dry or elongated diaspores were more likely to be dispersed by ungulates, whatever the dispersal mechanism. In addition, endozoochory was more likely for diaspores bearing elongated appendages whereas epizoochory was more likely for diaspores released relatively high in vegetation. Hoof‐epizoochory was more likely for light diaspores without hooked appendages. Fur‐epizoochory was more likely for diaspores with appendages, particularly elongated or hooked ones. We thus observed a gradient of filtering effect among the three dispersal mechanisms. Endozoochory had an effect of rather weak intensity (impacting six plant characteristics with variations between ungulate‐dispersed and non‐dispersed plant species mostly below 25%), whereas hoof‐epizoochory had a stronger effect (eight characteristics included five ones with above 75% variation), and fur‐epizoochory an even stronger one (nine characteristics included six ones with above 75% variation). Our results demonstrate that seed dispersal by ungulates is an ecological filter whose intensity varies according to the dispersal mechanism considered. Ungulates can thus play a key role in plant community dynamics and have implications for plant spatial distribution patterns at multiple scales. Synthesis Plant communities are often dispersal‐limited and zoochory can be an efficient mechanism for plants to colonize new patches of potentially suitable habitat. Our analysis is the first synthesis of ungulate seed dispersal that compares characteristics from both non‐dispersed and dispersed diaspores, distinguishing the three zoochory mechanisms ungulates are involved in: endozoochory, hoof‐epizoochory and fur‐epizoochory. We confirmed that seed dispersal by ungulates is an ecological filter whose intensity increases from endozoochory, then hoof‐epizoochory to finally fur‐epizoochory. By filtering seed traits through dispersal, ungulates can thus play a key role in plant community dynamics and have implications for plant spatial distribution patterns at multiple scales.     

Herbivore-induced expansion of <Emphasis Type="Italic">Helianthemum nummularium</Emphasis> in grassland–scrub mosaic vegetation: circumstantial evidence for zoochory and indirect grazing impact

Extensive grazing often has a strong influence on the structure and composition of herbaceous plant communities with increasing population sizes for some species and decreasing presence in others. Herbivores affect plant communities directly by selective grazing of plant species, and indirectly by either epizoochory or endozoochory. Helianthemum nummularium is considered an increasing species because its distribution increased after the introduction of large, free-ranging grazers in at least two coastal dune grassland areas in Belgium. However, its seeds lack any obvious adaptations for epizoochory, and direct observations of plant/seed consumption are scarce. Through field and lab experiments, we assessed the dispersal ability of H. nummularium via endozoochory and epizoochory. In a differentiated grazer exclusion experiment, evidence was found that plants are grazed by large domestic ungulates and small wild herbivores although these incidences were rare. Direct endozoochory evidence remained scarce. No seeds were found germinating in field-collected dung, and only few seedlings emerged following a seed feeding experiment. However, once deposited, we found higher growth rates when seeds were mixed with dung and decreased establishment success when seeds were sown in combination with competitively superior species. Epizoochory was plausible because both fur and hooves of cattle and horses were potentially capable of contributing to the transport of H. nummularium seeds. We conclude that herbivores play a role in seed dispersal, while their selective grazing behaviour most probably creates an appropriate environment for Helianthemum establishment and maintenance.     

Using basic plant traits to predict ungulate seed dispersal potential

Habitat fragmentation contributes to the decline of plant species by decreasing gene flow among populations. Restoring connectivity among habitat patches is therefore a major issue for plant conservation. However, deciding where to focus restoration efforts requires identifying suitable dispersers for each target plant species. We collected data from the literature on wild and domesticated ungulates, known to be effective seed dispersers, and on the plants they dispersed in Europe via epi‐ and/or endozoochory. We performed a systematic literature review to identify plant and animal traits relevant for seed dispersal. We first modeled the relationships between epi‐ or endozoochory and a priori selected plant traits (diaspore releasing height, length, shape and morphology, and habitat openness). The differences we underlined between the two dispersal mechanisms justified splitting our analyses accordingly. Then, for each dispersal mechanism, we asked whether basic plant traits could be used to predict specific traits of ungulates as endozoochorous or epizoochorous seed dispersers. We modeled the relationships between a priori selected ungulate traits for epizoochory (habitat openness, shoulder height, hair curliness, and hair length) and for endozoochory (habitat openness, body mass, feeding type and digestive system) and plant traits. Plant habitat openness and diaspore morphology were the predictors that most often explained differences among ungulates for epizoochory, whereas plant habitat openness and diaspore releasing height most often explained differences for endozoochory. Our trait‐based predictive models can help improve our ability to propose more precise management decisions for the conservation of plant populations worldwide by taking into account ungulate dispersers.     

The number and size of seeds in common versus restricted woodland herbaceous species in central Iowa, USA

Few plants have widespread distributions and occur wherever there is suitable habitat. Most species are absent from seemingly suitable sites because of limited colonizing ability. At a landscape scale colonization is limited by lack of seeds or suitable microsites, and this limit is likely to be exacerbated by current human alteration of the landscape. To test the hypothesis that species with restricted distributions have a more limited capacity for dispersal compared to common species, I compared seed number in a group of seven common woodland herbaceous species compared to seven species in the same genus or family with more restricted distributions. Restricted species had nearly an order of magnitude fewer seeds compared to closely related common species. They also produced over an order of magnitude larger seeds. These results support dispersal limitation. The ability to detect these differences was reduced when taxonomic information was not included. The data suggest that these species can not maximize both seed size and seed number. The results are interpreted in light of the human disturbance history that has had an overriding influence on the Iowa landscape and has likely favored species with an output advantage of abundant seeds over species with far many fewer seeds.     

Endozoochory varies with ecological scale and context

Several studies on endozoochory have established large herbivores as important for seed dispersal, yet no studies have evaluated how endozoochory is dependent on ecological scale and context. Here we address effects of reindeer density on endozoochory in a hierarchical, multi-scale study, encompassing several ecological contexts.
We found reindeer density effects on endozoochory to vary with spatial scale. Higher reindeer densities at the level of landscape areas, as indexed through faeces abundance, were related to both less species and lower abundance of emerging plants from faeces. In contrast, there was no effect of higher reindeer densities at the level of herding districts (i.e. large scale assemblages of landscapes). Lack of consistency between scales reflects ecological hierarchy, indicating that reindeer density effects on endozoochory best matches at the scale of landscapes.
Pasture seed plant composition was only partly an important ecological factor. That is, ericoid species, the dominating plants in the pastures, were also the most abundant seed plants found to emerge from the faeces. However, most herbaceous seed plant species in the pastures were not emerging from the faeces and the few that emerged were positively related to the site fertility and altitude of the pasture.
Studies addressing endozoochory of ruminants are typically concerned with seed plants, whereas in this study we also found indications of that diaspores of ferns are viable after passing the digestive tract of large herbivores. Vascular spore plants were even more abundant in the faeces than were vascular seed plants.
Results from this study demonstrate that reindeer may counteract a potentially negative impact on seed limitation from their grazing by returning viable seeds in their faeces. However, in Finnmark, northern Norway, this effect is only marginal, relates only to a very few species and individuals and shows ecological scale and context dependence.     

Implications of waterbird ecology for the dispersal of aquatic organisms

In this paper, we review some potential implications of waterbird ecology for their role as dispersers of aquatic plants and invertebrates. We focus particularly on internal transport (endozoochory) by the Anatidae (mainly ducks) and shorebirds, groups especially important for dispersal processes owing to their abundance, migratory habitats and diets. We conduct a literature review to assess the seasonal patterns shown by Anatidae in consumption of seeds and plankton, the interspecific patterns in such consumption (including the effects of body size, bill morphology, etc.), and differences in habitat use (e.g., shoreline vs. open water specialists) and migration patterns between species (e.g., true migrants vs. nomads). We show that many shorebirds are important consumers of seeds as well as plankton, and suggest that their role in plant dispersal has been underestimated. This review confirms that Anatidae, shorebirds and other waterbirds have great potential as dispersers of aquatic organisms, but illustrates how closely related, sympatric bird species can have very different roles in dispersal of specific aquatic organisms. Furthermore, great spatial and temporal variation is likely in dispersal patterns realized by a given bird population. We present evidence suggesting that northbound dispersal of aquatic propagules by endozoochory during spring migration is a frequent process in the northern hemisphere. Much more systematic fieldwork and reanalysis of the existing data sets (e.g., from diet studies) are needed before the relative roles of various waterbird species as dispersers can be fully assessed.     

SEED-SEEDLING CONFLICTS,HABITAT CHOICE,AND PATTERNS OF PLANT RECRUITMENT

The ecological forces determining where within a landscape plants recruit and grow has been termed proximal habitat choice. Habitat choice is imposed first by a heterogeneous pattern of seed dispersal across the patches that make up the landscape and second by environmental variation that favors plant survival in some patches more than in others. Seed-seedling conflicts can occur during both of these phases of habitat choice if conditions or traits that are favorable for seeds are unfavorable for seedlings. During the dispersal phase, smaller seeds may have a greater probability of dispersal than larger seeds, and thus a greater probability of escape from predation, but they contain fewer reserves for support of the establishing seedling. After dispersal, environmental characteristics of a given patch type that lead to disproportionately high seed survival may lead to disproportionately low seedling survival. Considering three hypothetical landscapes, each composed of five patch types, I demonstrate that seed-seedling conflicts can have a major impact on both the overall quantity of recruitment at the landscape level and on the distribution of recruitment among patches. Available empirical evidence suggests these conflicts may be widespread in natural systems. Given their potential importance and extent, seed-seedling conflicts may play a previously unrecognized role in habitat choice.     

Exploring the interaction of avian frugivory and plant spatial heterogeneity and its effect on seed dispersal kernels using a simulation model

Seed dispersal by avian frugivores is one of the key processes influencing plant spatial patterns, but may fail if there is disruption of plant–frugivore mutualisms, such as decline in abundance of dispersers, fragmentation of habitat, or isolation of individual trees. We used simulation model experiments to examine the interaction between frugivore density and behaviour and the spatial arrangement of fruiting plants and its effect on seed dispersal kernels. We focussed on two New Zealand canopy tree species that produce large fruits and are dispersed predominantly by one avian frugivore (Hemiphaga novaeseelandiae). Although the mean seed dispersal distance decreased when trees became more aggregated, there were more frugivore flights between tree clusters, consequently stretching the tails of the dispersal kernels. Conversely, when trees were less aggregated in the landscape, mean dispersal distances increased because seeds were deposited over larger areas, but the kernels had shorter tails. While there were no statistically meaningful changes in kernel parameters when frugivore density changed, decreases in density did cause a proportional reduction in the total number of dispersed seeds. However, birds were forced to move further when fruit availability and fruit ripening were low. Sensitivity analysis showed that dispersal kernels were primarily influenced by the model parameters relating to disperser behaviour, especially those determining attractiveness based on distance to candidate fruiting trees. Our results suggest that the spatial arrangement of plants plays an important role in seed dispersal processes – although tree aggregation curbed the mean seed dispersal distance, it was accompanied by occasional long distance events, and tree dispersion caused an increase in mean dispersal distance, both potentially increasing the probability of seeds finding suitable habitats for germination and growth. Even though low frugivore densities did not cause dispersal failure, there were negative effects on the quantity of seed dispersal because fewer seeds were dispersed.     

Linking landscape history and dispersal traits in grassland plant communities

Dispersal limitation and long-term persistence are known to delay plant species’ responses to habitat fragmentation, but it is still unclear to what extent landscape history may explain the distribution of dispersal traits in present-day plant communities. We used quantitative data on long-distance seed dispersal potential by wind and grazing cattle (epi- and endozoochory), and on persistence (adult plant longevity and seed bank persistence) to quantify the linkages between dispersal and persistence traits in grassland plant communities and current and past landscape configurations. The long-distance dispersal potential of present-day communities was positively associated with the amounts of grassland in the historical (1835, 1938) landscape, and with a long continuity of grazing management—but was not associated with the properties of the current landscape. The study emphasises the role of history as a determinant of the dispersal potential of present-day grassland plant communities. The importance of long-distance dispersal processes has declined in the increasingly fragmented modern landscape, and long-term persistent species are expected to play a more dominant role in grassland communities in the future. However, even within highly fragmented landscapes, long-distance dispersed species may persist locally—delaying the repayment of the extinction debt.     

Epianthropochory in Mexican weed communities

The diaspores of the 50 most important maize field weed species (agrestals) in a traditional maize-growing area of south-central Mexico (region of Puebla and Tlaxcala) were analyzed for morphological adaptations to long-distance dispersal. Adaptations to wind-dispersal were absent and to endozoochory were minimal. Most species had no visible adaptations and are presumably transported with mud. However, about one-quarter of the taxa, particularly the tall and dominant ones, relied at least partially on burrs with hooks or awns. The possible vectors for these exo- or epizoochorous species are discussed: the most likely regular dispersers are humans (epianthropochory). Interviews with farmers confirm this conclusion. Using humans as vectors allows the plant to transport relatively large seeds to favorable habitats (directed dispersal). The importance of this relatively rare dispersal adaptation in Mexican maize field weeds leads to questions on the origin and evolution of these agrestals.     

Long-distance endozoochorous dispersal of submerged macrophyte seeds by migratory waterbirds in northern Europe—a critical review of possibilities and limitations

We review whether migratory Anatidae, i.e., swans, geese and ducks, could be acting as vectors for dispersal of Zostera, Ruppia and Potamogeton propagules by endozoochory (carrying seeds in their guts). We list six prerequisites that must all be fulfilled, if successful dispersal should occur. Several Anatidae species feed on these macrophytes, and undertake rapid long-distance movements, making dispersal possible. We identify four problems, which in combination leads us to conclude that long-distance dispersal events are likely to be rare. (i) Most long-distance movements are out of phase with the reproductive efforts of the plants, and if birds arrive at sites when plants still bear seeds, they are likely to depart well after seed stocks have been depleted. (ii) Seed transport by birds will usually be uni-directional, from north to south on autumn migrations. (iii) Most of the gut contents of migratory birds are likely to have been discarded within 300 km of departure. (iv) In many cases, birds will arrive in habitats seriously different from those they departed, i.e., any seeds carried along will have low chances of surviving in their new site. We suggest that northbound dispersal by endozoochory can only occur during spring if waterbirds feed on seeds that have not been depleted and remained frozen down or buried in sediments, or during moult- or post-moult migrations. Moult migration takes place in summer in phase with the reproductive efforts of the plants. Also epizoochorous dispersal (external attachment) is subject to restrictions i, ii and iv.     

Frugivore Behavioural Details Matter for Seed Dispersal: A Multi-Species Model for Cantabrian Thrushes and Trees

Animal movement and behaviour is fundamental for ecosystem functioning. The process of seed dispersal by frugivorous animals is a showcase for this paradigm since their behaviour shapes the spatial patterns of the earliest stage of plant regeneration. However, we still lack a general understanding of how intrinsic (frugivore and plant species traits) and extrinsic (landscape features) factors interact to determine how seeds of a given species are more likely to be deposited in some places more than in others. We develop a multi-species mechanistic model of seed dispersal based on frugivore behavioural responses to landscape heterogeneity. The model was fitted to data from three-years of spatially-explicit field observations on the behaviour of six frugivorous thrushes and the fruiting patterns of three fleshy-fruited trees in a secondary forest of the Cantabrian range (N Spain). With such model we explore how seed rain patterns arise from the interaction between animal behaviour and landscape heterogeneity. We show that different species of thrushes respond differently to landscape heterogeneity even though they belong to the same genus, and that provide complementary seed dispersal functions. Simulated seed rain patterns are only realistic when at least some landscape heterogeneity (forest cover and fruit abundance) is taken into account. The common and simple approach of re-sampling movement data to quantify seed dispersal produces biases in both the distance and the habitat at which seeds arrive. Movement behaviour not only affects dispersal distance and seed rain patterns but also can affect frugivore diet composition even if there is no built-in preference for fruiting species. In summary, the fate of seeds produced by a given plant species is strongly affected by both the composition of the frugivore assemblage and the landscape-scale context of the plant location, including the presence of fruits from other plants (from the same or different species).     

Estimating plant migration rates under habitat loss and fragmentation

Changes in the global environment are modifying the geographical locations of habitats suitable for plant growth. The capacity of plants to migrate to sites of suitable environmental quality will strongly influence future distributions of plant diversity. However, it is not well understood how rates of plant migration are influenced by the habitat loss and habitat fragmentation that characterise contemporary landscapes. In this study we develop a model that can predict migration rates in both intact landscapes (potential migration rate) and in fragmented landscapes (realised migration rates). Migration rates in fragmented landscapes might be slower for many reasons. In this study we focus on two, non‐exclusive reasons. First, the processes that move seeds may break down in fragmented landscapes causing seeds to be dispersed shorter distances. Second, in fragmented landscapes some proportion of seeds will not be deposited in habitats suitable for recruitment. We describe the breakdown of dispersal processes as a competing risk between the factors influencing dispersal in intact landscapes and the factors that may disrupt dispersal processes in fragmented landscapes. We show how the parameters that influence dispersal in fragmented landscapes can be estimated, and how these estimates can be used to forecast migration rates using an integrodifference equation (IDE). The forecasts of the IDE described the effects of reduced dispersal distances adequately. However, the IDE produced biased estimates of the effects of a reduction in plant habitat on migration rates. Model analyses showed that, although we can expect realised migration rates to be lower than potential migration rates, we can also expect the sensitivity of migration rate to habitat loss to vary. In addition, simulations showed that the qualitative nature of the responses of migration rate to habitat loss were variable – some model species responded non‐linearly to habitat loss, others responded linearly. While our method provides guidelines for empirical data collection and model parameterisation, we recognise that obtaining these data will be challenging.     

Peduncles elicit large-mammal endozoochory in a dry-fruited plant

Background and Aims

Plants have evolved a variety of seed dispersal mechanisms to overcome lack of mobility. Many species embed seeds in fleshy pulp to elicit endozoochory, i.e. disseminating seed through the animal gut. In contrast to well-studied fleshy fruited plants, dry-fruited plants may exploit this dispersal mutualism by producing fleshy appendages as a nutritional reward to entice animals to swallow their diaspores, but this has been little studied. In this study, it is hypothesized that these accessory fruits represent co-adaptations facilitating the syndrome of mammalian endozoochorous dispersal.

Methods

Field observations (focal tree watches, faecal surveys and fruiting phenology) with experimental manipulations (examination of seed germination and feeding trials) were conducted over 2 years in a native population of the raisin tree, Hovenia dulcis, which produces enlarged, twisted brown peduncles with external black seeds, in central China.

Key Results

Birds were not observed to swallow seeds or carry infructescences away during 190 h of focal tree watches. However, H. dulcis seeds were detected in 247 faecal samples, representative of two herbivore and four carnivore mammalian species. Feeding trials revealed that peduncles attracted mammals to consume the entire infructescence, thereby facilitating effective seed dispersal. The germination rate of egested seeds proved higher than that of unconsumed seeds. It was also noted that this mutualism was most vulnerable in degraded forest.

Conclusions Hovenia dulcis

peduncle sets are confirmed to adapt primarily to mammalian endozoochory, a mutualistic association similar in function to fleshy pulp or foliage. This demonstrates that plant organ systems can be adapted to unique mutualisms that utilize animal dispersal agents. Such an ecological role has until now been attributed only to bird epizoochory. Future studies should consider more widely the putative role of peduncle sets and mammalian endozoochory as a dispersal mechanism, particularly for those plants that possess relatively large accessory fruits.     

Temporal dynamics of seed excretion by wild ungulates: implications for plant dispersal

Dispersal is a key process in metapopulation dynamics as it conditions species' spatial responses to gradients of abiotic and biotic conditions and triggers individual and gene flows. In the numerous plants that are dispersed through seed consumption by herbivores (endozoochory), the distance and effectiveness of dispersal is determined by the combined effects of seed retention time in the vector's digestive system, the spatial extent of its movements, and the ability of the seeds to germinate once released. Estimating these three parameters from experimental data is therefore crucial to calibrate mechanistic metacommunity models of plant–herbivore interactions. In this study, we jointly estimated the retention time and germination probability of six herbaceous plants transported by roe deer (Capreolus capreolus), red deer (Cervus elaphus), and wild boar (Sus scrofa) through feeding experiments and a Bayesian dynamic model. Retention time was longer in the nonruminant wild boar (>36 h) than in the two ruminant species (roe deer: 18–36 h, red deer: 3–36 h). In the two ruminants, but not in wild boar, small and round seeds were excreted faster than large ones. Low germination probabilities of the excreted seeds reflected the high cost imposed by endozoochory on plant survival. Trait‐mediated variations in retention time and germination probability among animal and plant species may impact plant dispersal distances and interact with biotic and abiotic conditions at the release site to shape the spatial patterns of dispersed plant species.     

动物传播者对植物更新的促进与限制

在动物 植物的关系网络中,传播者对植物更新具有促进与限制两方面作用.本文从种群尺度总结了传播者取食、空间利用等行为对植物更新的影响;从群落尺度分析了多种传播者传播有效性对植物更新的促进与限制.传播者对食物的处理方式决定了种子的命运,且具有明显的种间差异;植物在传播者食谱中的地位亦决定其更新的成败,成为动物偏好的食物可助其摆脱森林破碎化等不利事件的影响.动物的空间行为可导致种子命运发生改变.传播者移动距离能否逃逸同种成树对种子的距离限制,影响种子的更新命运;动物偏好的适宜生境与适于植物萌发生境的空间一致性程度影响传播者传播的成效.有效传播者的非冗余性促使种子传播网络更稳定,利于植物更新;无效传播直接限制植物更新,但为其他植物定殖提供了可用空间.今后应将传播者行为融入植物种群更新研究,而从生态系统服务角度揭示传播者在植被恢复的作用应是未来恢复生态学研究的重点.     

Seed dispersal by white-tailed deer: implications for long-distance dispersal,invasion, and migration of plants in eastern North America

For many plant species in eastern North America, short observed seed dispersal distances (ranging up to a few tens of meters) fail to explain rapid rates of invasion and migration. This discrepancy points to a substantial gap in our knowledge of the mechanisms by which seeds are dispersed long distances. We investigated the potential for white-tailed deer (Odocoileus virginianus Zimm.), the dominant large herbivore in much of eastern North America, to disperse seeds via endozoochory. This is the first comprehensive study of seed dispersal by white-tailed deer, despite a vast body of research on other aspects of their ecology. More than 70 plant species germinated from deer feces collected over a 1-year period in central New York State, USA. Viable seeds included native and alien herbs, shrubs, and trees, including several invasive introduced species, from the full range of habitat types in the local flora. A mean of >30 seeds germinated per fecal pellet group, and seeds were dispersed during all months of the year. A wide variety of presumed dispersal modes were represented (endo- and exozoochory, wind, ballistic, ant, and unassisted). The majority were species with small-seeded fruits having no obvious adaptations for dispersal, underscoring the difficulty of inferring dispersal ability from diaspore morphology. Due to their broad diet, wide-ranging movements, and relatively long gut retention times, white-tailed deer have tremendous potential for effecting long-distance seed dispersal via ingestion and defecation. We conclude that white-tailed deer represent a significant and previously unappreciated vector of seed dispersal across the North American landscape, probably contributing an important long-distance component to the seed shadows of hundreds of plant species, and providing a mechanism to help explain rapid rates of plant migration.Electronic Supplementary Material Supplementary material is available in the online version of this article at     

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。     

Plant recruitment bottlenecks in temperate forest fragments: seed limitation and insect herbivory

Numerous studies have documented declines in plant diversity in response to habitat loss in fragmented landscapes. However, determining the mechanisms that lead to species loss is challenging using solely a correlative approach. Here we link correlative assessments of plant community composition with seed additions for a focal species to test the hypothesis that distributions of forests plants within a fragmented landscape are limited by seed dispersal. Woody plant species richness of fragments declined as fragments (n=26) became more isolated by agricultural fields. We predicted that if these isolation effects were driven by poor dispersal rather than other effects associated with habitat loss, then plants should vary in their response to isolation in relation to their seed size (i.e., stronger effects for plants with larger seeds). As predicted under this dispersal limitation hypothesis, sensitivity of bird-dispersed shrubs to isolation was related to their seed mass, with species with heavy seeds (e.g., Lindera benzoin) exhibiting stronger declines in presence across isolation gradients than species with light seeds. Seed addition experiments were performed for Lindera benzoin in two high isolation forest fragments (nearest neighbor mean distance=803 m) where Lindera was naturally absent, and two low isolation fragments (nearest neighbor mean distance=218 m) with naturally occurring Lindera populations. Seed addition and control plots (n=50 1 m² plots per fragment) were monitored for 13 censuses over 3 years. Across all four fragments, seed additions resulted in significant increases in Lindera seedling recruitment with no differences in final seedling establishment among fragments. However, insect herbivory was higher on Lindera seedlings in high isolation compared to low isolation fragments and was negatively correlated with seedling survival over some years. Consistent with prior work, our results confirm that seed dispersal plays a significant role in affecting plant diversity in fragmented landscapes. However, results also suggest the need for a better understanding of how additional processes, such as herbivory, may be altered as habitat is lost and what effects such changes have for forest plants.     

Potential and realised contribution of endozoochory to seedling establishment

Many plant species have been shown to be dispersed by large herbivores through endozoochory, but there have been few studies that have demonstrated the ecological significance of this dispersal method. Known quantities of seeds were fed to sheep and the emergence of seeds germinating from dung in the field and glasshouse were compared with emergence in the field after direct sowing. All 12 species studied showed potential endozoochory as they germinated and grew from dung in the glasshouse. Six species showed no emergence in the field from either dung or direct sowing. Of the remaining, three did not emerge from dung in the field but did from direct sowing indicating a very high cost of dispersal (one other species showed this pattern but not significantly), one emerged in the field from dung but at comparatively low rates and one showed no cost to endozoochory as it emerged equally well from dung or after direct sowing. The results indicate that potential endozoochory, as measured by germination from dung in the glasshouse, over-estimates likely rates of establishment in the field. The results also indicate that there are potentially high costs to endozoochory that have to be balanced against the benefits of long-distance dispersal by large herbivores.