Seed Dispersal in the Dark: Shedding Light on the Role of Fruit Bats in Africa

In spite of their recognized importance as seed dispersers in other parts of the tropics, seed dispersal by fruit bats has received scant research attention in Africa. To evaluate the role of African fruit bats in seed dispersal, we studied fruits and seeds below 480 bat feeding roosts in the East Usambara Mountains of Tanzania. We compared these findings to those reported in other African localities to place our results in a broader context. We found 49 plant species dispersed by bats: 28 species, 18 genera, and one family are novel reports of bat dispersal in Africa. Approximately 20 percent of the submontane tree flora of the East Usambaras is bat‐dispersed, including both widespread and endemic trees. African fruit bats are important seed dispersers at our study site because they move seeds of dozens of species tens or hundreds of meters, even seeds that are too large to ingest (greater than 5 mm in length). Fruit bats are likely important seed dispersers in other Afrotropical forests, as bats elsewhere in Africa are known to consume 20 genera and 16 species of plants reported here. Insights from studying remains under bat feeding roosts offer a simple method to further document and substantially increase our understanding of the role of African fruit bats in seed dispersal.     

Seed Dispersal by Birds and Bats in Lowland Philippine Forest Successional Area

In the tropical forests of SE Asia, only a few studies have dealt with the role animal dispersal plays in early forest succession and rehabilitation, and a comparison of bird and bat dispersal is even rarer. We investigated seed dispersal by birds and bats in a successional area in the lowland dipterocarp forest of the Subic Watershed Forest Reserve (SWFR) in Luzon Island, Philippines. Using pairs of day and night traps, we collected seeds during 3 mo of wet season and 3 mo of dry season in a 1.2-ha study site. Bird-dispersed seeds predominated over those dispersed by bats in terms of both seed abundance and number of seed species. The most abundant endozoochorous seed species were significantly biased toward either bird or bat dispersal. Birds and bats appeared to compete more strongly for fruit resources during the dry season than during the wet season, and bats responded more to changes in the seasons than birds did. GLM analyses showed that the factor that had the strongest influence on overall seed distribution was the number of fleshy-fruited trees surrounding the traps, and that the distribution pattern of day-dispersed seeds was affected by more physical factors (number of trees, size of trees, presence of fleshy-fruited and conspecific trees) in the study site than the pattern of night-dispersed seeds were. Given that birds are the more important dispersers in the study site, restoration efforts in SWFR might benefit by focusing on attracting these dispersers into its degraded habitats.     

Seed Dispersal of Morus macroura (Moraceae) by Two Frugivorous Bats in Xishuangbanna, SW China

The dispersal of Morus macroura seeds by two species of frugivorous bats ( Rousettus leschenaulti and Cynopterus sphinx ) was studied in a forest at Xishuangbanna Tropical Botanical Garden in Southwest China from March to May 2005. Feeding roosts were identified within 500 m around parent trees and the types and number of seed loads under each roost were recorded. We found feeding roost density decreased with increasing distance from the parent, but found no correlation between distance and seed deposition. The effect of bat digestion on seed germination was investigated, and we found that germination percentage of all treatments involving ingestion by bats was significantly lower than control seeds and some germination parameters of seeds from different treatments changed.     

Old World fruit bats can be long-distance seed dispersers through extended retention of viable seeds in the gut

Seed dispersal and pollination by animals play a crucial role in the maintenance of forest ecosystems worldwide. Frugivorous bats are important pollen and seed dispersers in both the Palaeo- and Neotropics, and at least 300 plant species are known to rely on Old World fruit bats (Megachiroptera, Pteropodidae) for their propagation. However, rapid food transit times (generally less than 30 minutes) in frugivorous bats have been thought to limit their ability to disperse seeds to just a few tens of kilometres. Here we demonstrate regular daytime (greater than 12 hours) retention of food and viable fig seeds (Ficus, Moraceae) in the gut of the Old World fruit bat Cynopterus sphinx: a behaviour not previously reported for any frugivorous bat. Field observations indicate that this behaviour also occurs in other genera. Old World fruit bats are highly mobile and many species undertake considerable foraging and migration flights. Our findings indicate that Old World fruit bats have the potential to disperse small seeds hundreds of kilometres. This necessitates a reappraisal of their importance in transporting zoochorous seeds to remote areas and facilitating gene flow between isolated populations of plants, both within mainlands and across ocean barriers.     

Effect of Bat Exclusion on Patterns of Seed Rain in Tropical Rain Forest in French Guiana

To assess the impact of bats on seed dispersal in a tropical mature forest (Nouragues, French Guiana), we conducted a bat exclusion experiment and tested the hypotheses that an artificial reduction in the abundance of bats would result in: (1) a decrease in seed species diversity, at the community level; and (2) an increase in seed limitation (a failure of seeds to reach all suitable sites for germination) at the species level. Seed rain was sampled in two contiguous forest plots for a total of 120 d, using 49 seed traps (1 m²) arranged in 7 × 7 grids and spaced at 5-m intervals. Using mist nets, bat activity was reduced in one forest plot for a total of 60 nights. Thirty-nine plant species, or species groups, likely to be consumed and dispersed by bats, were collected within a total sample of 50,063 seeds. The overall seed rain was dominated by epiphytic Araceae and Cyclanthaceae (83.3%) and tree species within the genera Cecropia and Ficus (16.0%). Seeds from bat-dispersed shrubs and treelets ( Piper , Solanum , and Vismia ) were relatively rare (0.7%). The bat exclusion resulted in a 30.5 percent reduction in seed species richness and increased seed limitation for most of the species sampled. Seed limitation was caused mainly by a reduced seed rain (seed source limitation) rather than a decrease in seed dispersal uniformity (seed dispersal limitation). Therefore, bat-dispersed plants with low seed production are likely to be particularly affected by a decline in bat abundance, as a result of anthropogenic change.     

Roosting Requirements of Two Frugivorous Bats (Sturnira lilium and Arbiteus intermedius) in Fragmented Neotropical Forest1

As tropical forest fragmentation accelerates, scientists are concerned with the loss of species, particularly those that play important ecological roles. Because bats play a vital role as the primary seed dispersers in cleared areas, maintaining healthy bat populations is critical to natural forest regeneration. Observations of foraging bats suggest that many Neotropical fruit‐eating species have fairly general habitat requirements and can forage in many different kinds of disturbed vegetation; however, their roosting requirements may be quite different. To test whether or not general foraging requirements are matched by equally broad roosting requirements, we used radiotelemetry to locate roost sites of two common frugivorous bat species (Sturnira lilium and Artibeus intermedius) in a fragmented forest in southeastern Mexico. Sturnira lilium roosted inside tree cavities and selected large‐diameter roost trees in remnant patches of mature forest. Fewer than 2 percent of trees surveyed had a mean diameter equal to or greater than roost trees used by . S. lilium, Artibeus intermedius roosted externally on branches and vines and under palm leaves and selected roost trees of much smaller diameter. Compared to random trees, roost trees chosen by A. intermedius were closer to neighboring taller trees and also closer in height to these trees. Such trees likely provide cryptic roosts beneath multiple overlapping crowns, with sufficient shelter from predators and the elements. While males of A. intermedius generally roosted alone in small trees within secondary forest, females roosted in small groups in larger trees within mature forest and commuted more than three times farther than males to reach their roost sites. Loss of mature forest could impair the ability of frugivorous bats to locate suitable roost sites. This could have a negative impact on bat populations, which in turn could decrease forest regeneration in impacted areas.     

The effect of bat (Rousettus aegyptiacus) dispersal on seed germination in eastern Mediterranean habitats

The fruit-bat Rousettus aegyptiacus (Pteropodidae) in Israel consumes a variety of cultivated and wild fruits. The aim of this study was to explore some of its qualities as a dispersal agent for six fruit-bearing plant species. The feeding roosts of the fruit-bat are located an average of 30 m from its feeding trees and thus the bats disperse the seeds away from the shade of the parent canopy. The bat spits out large seeds but may pass some (2%) of the small seeds (<4 mg) through its digestive tract. However, neither the deposited seeds nor the ejected seeds (except in one case) had a significantly higher percentage germinating than intact seeds. Although the fruit-bat did not increase the percentage germinating, seeds of three plant species subject to different feeding behaviors (deposited in feces or spat out as ejecta) had a different temporal pattern of germination from the intact seeds. The combined seed germination distribution generated by these different treatments is more even over time than for each treatment alone. It is sugested that this increases asynchronous germination and therefore enhances plant fitness by spreading the risks encountered during germination, especially in eastern Mediterranean habitats where the pattern of rainfall is unpredictable.     

Can remnant frugivore species effectively disperse tree seeds in secondary tropical rain forests?

Seed dispersal by frugivores in tropical rain forests is important for maintaining viable tree populations. Over the years, vertebrate assemblages in tropical forests have been altered by anthropogenic disturbances, leading to concerns about the ability of remnant vertebrates to substitute for the lost or declining vertebrate populations. We compared vertebrate composition and frugivore visitation rates as an indirect measure of rate of seed dispersal in three tropical rain forests in Uganda, namely Mabira, Budongo and Kibale Forests. Mabira is highly disturbed, Kibale is little and Budongo is intermediate. The aim was to determine whether vertebrate assemblages in differentially disturbed forests had comparable abilities to disperse seeds and whether tree species were equally vulnerable to loss of seed dispersers. Assemblages of forest generalist species were similar in all forests, but specialists were less abundant in the heavily disturbed forest. Remnant frugivores in the heavily disturbed forest were mainly small-bodied species that spat seeds beneath fruiting trees compared to large-bodied species observed in the less disturbed forests that ingested and carried away the seeds. We postulate that the quantity of seeds dispersed in heavily disturbed forests is much reduced due to low visitation rates of frugivores and the absence of large frugivores that consume large quantities of fruit. The quality of seed dispersal is affected as well by the distance over which seeds are moved. Assessment of vulnerability of trees shows no evidence for disperser substitution for trees producing large fruits. Fruit trees with low nutritional contents and digestibility were least visited in frugivore-impoverished forests. The loss of large specialist frugivores is likely to affect recruitment of many trees, especially of species that cannot establish beneath adult conspecifics.     

Wahlberg’s epauletted fruit bat (<Emphasis Type="Italic">Epomophorus wahlbergi</Emphasis>) as a potential dispersal agent for fleshy-fruited invasive alien plants: effects of handling behaviour on seed germination

The spread of invasive alien plants into natural habitats is of growing global concern. Several studies have investigated the role that avian frugivores play in the dispersal of these seeds and their effects on germination success. Fruit bats have however received little attention as important dispersal agents of invasive alien plants, despite their recognized role as long distance dispersal agents of various native flora. We investigated whether Wahlberg’s epauletted fruit bats, Epomophorus wahlbergi, would positively influence the germination of seeds of invasive alien plants. These fruit bats were fed fruits of four invasive alien plant species—Psidium guajava, Melia azedarach, Eriobotrya japonica, and Morus alba. Epomophorus wahlbergi were able to process more fruit per gram body mass than birds have been observed to do. Spat and de-pulped control seeds had similar germination success and germinated at approximately the same time for most species. While seeds retained in whole fruit had significantly less germination success than spat seeds for all species, except M. azedarach, they mostly germinated at approximately the same time. Epomophorus wahlbergi can swallow small seeds (< 2 mm), while seeds larger than this are generally spat out. Large fruit are usually carried away to feeding roosts where seeds are dropped, thereby dispersing seeds and fruits which are too large for some bird species to ingest. Epomophorus wahlbergi should not be underestimated as dispersers of these invasive alien plants as they consume proportionally large amounts (0.62 ± 0.09 to 0.99 ± 0.11 g.g⁻¹ body mass) of fruit, except for M. azedarach, and positively affect their seed germination rates.     

On the density-dependence of seed predation in<Emphasis Type="Italic"> Dipteryx micrantha</Emphasis>, a bat-dispersed rain forest tree

We studied the effect of seed density on seed predation by following the fate of bat-dispersed Dipteryx micrantha (Leguminosae) seeds deposited under bat feeding roosts. The study was conducted in Cocha Cashu biological station, Amazonian Peru, during the fruiting period of Dipteryx. Predation of Dipteryx seeds in the area is mainly by large to medium-sized rodents. Seed deposits beneath bat feeding roosts were monitored for a 13-week period in an 18-ha study area. A total of 210 seed deposits were found, and on average, seed predators encountered 22% of them during any one week. About one-third of the seed deposits escaped predation, and those deposits that had relatively few seeds were more likely to go unnoticed by rodents than were deposits with many seeds. The mean seed destruction rate was 8% per week; deposits with many seeds tended to lose a smaller proportion of their seeds to seed predators than did deposits with few seeds. Regression tests for the weekly data showed that, at the beginning of the observation period, seed predation was not density-dependent. Later, when the total seed crop beneath roosts was high, the number of seeds predated per deposit was positively density-dependent, while the proportion of seeds predated was negatively density-dependent, indicating predator satiation. Seed deposits that had been visited by seed predators once had a higher probability of being revisited the week after, especially if they contained many seeds when first encountered. This indicates that the foraging behavior of rodents may be affected by their remembering the location of seed-rich patches.     

High-quality seed dispersal by fruit-eating fishes in Amazonian floodplain habitats

Seed dispersal is a critical stage in the life history of plants. It determines the initial pattern of juvenile distribution, and can influence community dynamics and the evolutionary trajectories of individual species. Vertebrate frugivores are the primary vector of seed dispersal in tropical forests; however, most studies of seed dispersal focus on birds, bats and monkeys. Nevertheless, South America harbors at least 200 species of frugivorous fishes, which move into temporarily flooded habitats during lengthy flood seasons and consume fruits that fall into the water; and yet, we know remarkably little about the quality of seed dispersal they effect. We investigated the seed dispersal activities of two species of large-bodied, commercially important fishes (Colossoma macropomum and Piaractus brachypomus, Characidae) over 3 years in Pacaya-Samiria National Reserve (Peru). We assessed the diet of these fishes during the flood season, conducted germination trials with seeds collected from digestive tracts, and quantified fruit availability. In the laboratory, we fed fruits to captive Colossoma, quantified the proportion of seeds defecated by adult and juvenile fish, and used these seeds in additional germination experiments. Our results indicate that Colossoma and Piaractus disperse large quantities of seeds from up to 35% of the trees and lianas that fruit during the flood season. Additionally, these seeds can germinate after floodwaters recede. Overexploitation has reduced the abundance of our focal fish species, as well as changed the age structure of populations. Moreover, older fish are more effective seed dispersers than smaller, juvenile fish. Overfishing, therefore, likely selects for the poorest seed dispersers, thus disrupting an ancient interaction between seeds and their dispersal agents. Electronic supplementary material  The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

Response of ants to human‐altered habitats with reference to seed dispersal of the myrmecochore Corydalis giraldii Fedde (Papaveraceae)

Anthropogenic habitat disturbance has potential consequences for ant communities. However, there is limited information on the effects of ant responses on associated ecological processes such as seed dispersal. We investigated the effect of disturbance on the abundance, richness, and composition of ant communities and the resulting seed‐dispersal services for a herbaceous myrmecochore, Corydalis giraldii (Papaveraceae), in an undisturbed habitat (forest understory), moderately disturbed habitat (abandoned arable field), and highly disturbed habitat (road verge) on Qinling Mountains, China. In total, we recorded 13 ant species, and five out of these were observed to transport seeds. The community composition of dispersers was significantly different amongst habitats. The richness of the dispersers did not differ among the habitats, but their total abundance varied significantly across habitats and was 21% lower in the road verge than in the abandoned arable fields. The major seed‐dispersing ant species in both the forest understory and the abandoned arable field were large‐bodied (Myrmica sp. and Formica fusca, respectively), whereas the major seed‐dispersing ants found in the road verge were the small‐bodied Lasius alienus. This difference resulted in lower seed removal rates and dispersal distances in the road verge than in the other two habitats. The different dispersal patterns were attributed primarily to differences in dispersing ant abundance and identity, most likely in response to habitats with different degree of anthropogenic disturbance. The possible influence of disturbance on the ecological specialization of ant‐seed dispersal interaction is also discussed.     

Diversity of seeds captured by interception exceeds diversity of seeds deposited in traps

Seed dispersal, a key process in terrestrial landscapes, is increasingly important in the face of habitat fragmentation and global climate change. Seed dispersal is also notoriously difficult to characterize, especially in species rich and spatially complex tropical forests. We contrasted assemblages of biotically dispersed seeds collected from four sites using two methods: deposition into seed traps and interception by the capture of frugivorous birds. We also compared seed deposition and interception with local fruit production. Species accumulation curves for seeds deposited in seed traps began to level off sooner than curves for seeds collected from birds captured in mist nets, and extrapolation showed significantly greater estimated species richness for seeds collected from birds than for those deposited in traps. Assemblages from birds and from traps at each site were quite different, with an abundance‐based similarity index of 0.64; this dissimilarity increases if bat‐dispersed seeds are included in the analysis. Common bird‐dispersed species were retrieved from both mist‐netted birds and from seed traps, but numerous locally fruiting understory species were recovered only from birds. We conclude that the sampling of seeds carried by birds provides a valuable complement to other methods of studying seed dispersal in species‐rich tropical forests by revealing relationships between specific dispersers and their seed plants and by creating a more complete account of species diversity of seeds being transported at a given site.     

Fishing‐down within populations harms seed dispersal mutualism

Large fish are often the most effective seed dispersers, but they are also the preferred target for fisheries. We recently started to comprehend the detrimental impacts of the extirpation of large frugivorous fish species on natural forest regeneration, but we lack a general understanding of how intraspecific size‐selective harvest affects fish–fruit mutualism. Our literature review demonstrated that large individuals within populations positively affect diverse aspects of seed dispersal, from consuming a higher diversity of seeds to enhancing germination. Furthermore, we filled a research gap by studying how individual size variations within two small frugivorous fish species (<16 cm) affect seed dispersal in flooded savannas. Even within small‐bodied species, large individuals swallow a higher number of intact seeds, but not necessarily a higher proportion. Overall, our results demonstrate the disproportional role of large‐bodied individuals as key seed dispersers in flooded habitats. Consequently, fishing‐down within both large‐ and small‐bodied species can negatively affect seed dispersal and natural regeneration in overfished wetlands.     

Does seed ingestion by bats enhance germination? A new meta‐analysis 15 years later

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The role of Orii’s flying-fox (Pteropus dasymallus inopinatus) as a pollinator and a seed disperser on Okinawa-jima Island, the Ryukyu Archipelago, Japan

The role of the Orii’s flying-fox (Pteropus dasymallus inopinatus) as a pollinator and a seed disperser on Okinawa-jima Island was investigated by direct observations and radio-tracking from October 2001 until January 2006. We found that Orii’s flying-fox potentially pollinated seven native plant species. Its feeding behavior and plant morphological traits suggested that this species is an important pollinator of Schima wallichii liukiuensis and Mucuna macrocarpa. The flying-fox also dispersed the seeds of 20 native plant species. The seeds of all plants eaten by the flying-fox were usually dropped beneath the parent tree, although large fruits of four plant species were occasionally brought to the feeding roosts in the mouth, with the maximum dispersal distance—for Terminalia catappa—estimated to be 126 m. Small seeds of 11 species (mostly Ficus species) were dispersed around other trees, during the subsequent feeding session, through the digestive tracts, with the mean dispersal distance for ingested seeds estimated at 150 ± 230.3 m (±SD); the maximum dispersal distance was 1833 m. A comparison of the seed dispersal of available fruits according to the size of flying-foxes and other frugivores suggested that the seed dispersal of eight plant species producing large fruits mostly depended on Orii’s flying-fox. On Okinawa-jima Island, the Orii’s flying-fox plays an important role as a pollinator of two native plants and as a long-distance seed disperser of Ficus species, and it functions as a limited agent of seed dispersal for plants producing large fruits on Okinawa-jima Island.     

Reduced Hornbill Abundance Associated with Low Seed Arrival and Altered Recruitment in a Hunted and Logged Tropical Forest

Logging and hunting are two key direct threats to the survival of wildlife in the tropics, and also disrupt important ecosystem processes. We investigated the impacts of these two factors on the different stages of the seed dispersal cycle, including abundance of plants and their dispersers and dispersal of seeds and recruitment, in a tropical forest in north-east India. We focused on hornbills, which are important seed dispersers in these forests, and their food tree species. We compared abundances of hornbill food tree species in a site with high logging and hunting pressures (heavily disturbed) with a site that had no logging and relatively low levels of hunting (less disturbed) to understand logging impacts on hornbill food tree abundance. We compared hornbill abundances across these two sites. We, then, compared the scatter-dispersed seed arrival of five large-seeded tree species and the recruitment of four of those species. Abundances of hornbill food trees that are preferentially targeted by logging were two times higher in the less disturbed site as compared to the heavily disturbed site while that of hornbills was 22 times higher. The arrival of scatter-dispersed seeds was seven times higher in the less disturbed site. Abundances of recruits of two tree species were significantly higher in the less disturbed site. For another species, abundances of younger recruits were significantly lower while that of older recruits were higher in the heavily disturbed site. Our findings suggest that logging reduces food plant abundance for an important frugivore-seed disperser group, while hunting diminishes disperser abundances, with an associated reduction in seed arrival and altered recruitment of animal-dispersed tree species in the disturbed site. Based on our results, we present a conceptual model depicting the relationships and pathways between vertebrate-dispersed trees, their dispersers, and the impacts of hunting and logging on these pathways.     

Feeding of the Bat,Sturnira lilium,on Fruits of Solanum riparium Influences Dispersal of this Pioneer Tree in Forests of Northwestern Argentina

The influence of fruit ingestion by the bat, Sturnira lilium, on germination of the seeds of the tree Solanum riparium was studied in a secondary rain forest in northwestern Argentina. Bat frequencies in disturbed areas were analyzed by mist net captures. Germination rates were determined for seeds collected from trees and bat feces. S. lilium was the most abundant fruit bat in the study area. Fruit digestion and the passage of seeds through the intestine did not significantly affect germination in S. riparium. In this case the fruit bats, therefore, probably provide only seed dispersal.     

Distribution and underground habitats of cave-dwelling bats in China

To understand the distribution and relative abundance of cave-dwelling bats and to identify those sites that would be important for conservation of bat species, 25 underground sites that had not been previously surveyed were investigated in this 3-year study (from December 2003 to April 2006) in Funiu Mountain of Henan province, China. Approximately 80 000 bats were recorded, representing 12 species. The most abundant species were Rhinolophus affini s, Miniopterus schreibersi and Hipposideros pratti . The roosts were evaluated for their conservation importance. The most important sites in the area are Yunhua and Nanzhao caves, which serve as hibernaculums and nursery roosts to c . 13 740 and 11 803 bats, respectively, representing seven species. By means of cluster and correspondence analysis, the distribution of bat species was different between the two sides of the mountain and was highly dependent on the size of the cave. The underground sites in the south region hosted c . 80% of the total bats, representing 11 species. The sites in the north region hosted 20% of the total bats, representing seven species. Presently, none of the caves in the region has adequate protection and some bat populations are under serious threat. Many large caves that contained large bat populations and several species of concern had been developed as tourist sites, and so some advice on protecting the most important local habitats was sought based on the assessment of the conservation status of underground sites. This paper presents basic data concerning the distribution of cave-dwelling bats and the patterns of cave use on Funiu Mountain. The data will help local governments and policy-makers develop suitable strategies to promote local tourisms while protecting important habitats of animal species.     

Scale‐dependent effects of forest restoration on Neotropical fruit bats

Neotropical fruit bats (family Phyllostomidae) facilitate forest regeneration on degraded lands by dispersing shrub and tree seeds. Accordingly, if fruit bats can be attracted to restoration sites, seed dispersal could be enhanced. We surveyed bat communities at 10 sites in southern Costa Rica to evaluate whether restoration treatments attracted more fruit bats if trees were planted on degraded farmlands in plantations or island configurations versus natural regeneration. We also compared the relative influence of tree cover at local and landscape spatial scales on bat abundances. We captured 68% more fruit bat individuals in tree plantations as in controls, whereas tree island plots were intermediate. Bat activity also responded to landscape tree cover within a 200‐m radius of restoration plots, with greater abundance but lower species richness in deforested landscapes. Fruit bat captures in controls and tree island plots declined with increasing landscape tree cover, but captures in plantations were relatively constant. Individual species responded differentially to tree cover measured at different spatial scales. We attribute restoration effects primarily to habitat structure rather than food resources because no planted trees produced fruits regularly eaten by bats. The magnitude of tree planting effects on fruit bats was less than previous studies have found for frugivorous birds, suggesting that bats may play a particularly important role in dispersing seeds in heavily deforested and naturally regenerating areas. Nonetheless, our results show that larger tree plantations in more intact landscapes are more likely to attract diverse fruit bats, potentially enhancing seed dispersal.