Vertical stratification of figs and fig-eaters in a Bornean lowland rain forest: how is the canopy different?

Fig trees (Ficus spp; Moraceae) are a common constituent of many tropical forests, where they produce figs that are eaten by a wide range of bird and mammal species. In our Bornean field site six Ficus seed dispersal guilds can be recognised, differentially attracting subsets of the frugivore community. Guild membership appears to be determined by figs' size, colour, crop size and height above ground, and frugivores' size, sensory and locomotory physiology and foraging height. Vertical stratification therefore appears to be an important determinant of fig and frugivore partitioning. The guild structure observed is discussed with respect to implications for seed dispersal and the differences between the canopy and understorey. Regarding figs eaten primarily by birds, larger fruit and crops can be found in the canopy where they are exposed to larger assemblages of potential frugivores than those presented in the understorey.     

Resources determine frugivore assemblages and fruit removal along an elevational gradient

Geographic variation in the diversity, abundance or composition of plant and frugivore assemblages may have consequences for seed dispersal processes. Such variations may be related to climatic conditions as well as habitat characteristics such as fruit availability and forest complexity. Studying frugivore assemblages and seed dispersal processes along an elevational gradient can help to elucidate the interplay between the extent of dispersal services provided by frugivores and the geographic variability of the food resources. We studied frugivore assemblages on and fruit removal from 28 rowan trees (Sorbus aucuparia) along an elevational gradient in the Bavarian Forest, Germany. Both, the number of frugivore species and the number of frugivore individuals were significantly enhanced by high fruit availability. In both cases we found a slight interaction between elevation and fruit availability indicating a higher attractiveness of fruits for frugivores at lower than at higher elevations. A high number of frugivore individuals in turn significantly increased fruit removal from rowan trees. Here, we found a significant interaction between elevation and the number of frugivore individuals suggesting that the number of frugivores is of major importance for fruit removal particularly at lower elevations. Path analysis corroborated that the number of frugivore individuals indirectly mediated the effect of fruit availability on fruit removal. These findings suggest that fruit removal is rather influenced by changes in habitat characteristics than in climatic conditions across space.     

Food plant diversity as broad-scale determinant of avian frugivore richness

The causes of variation in animal species richness at large spatial scales are intensively debated. Here, we examine whether the diversity of food plants, contemporary climate and energy, or habitat heterogeneity determine species richness patterns of avian frugivores across sub-Saharan Africa. Path models indicate that species richness of Ficus (their fruits being one of the major food resources for frugivores in the tropics) has the strongest direct effect on richness of avian frugivores, whereas the influences of variables related to water-energy and habitat heterogeneity are mainly indirect. The importance of Ficus richness for richness of avian frugivores diminishes with decreasing specialization of birds on fruit eating, but is retained when accounting for spatial autocorrelation. We suggest that a positive relationship between food plant and frugivore species richness could result from niche assembly mechanisms (e.g. coevolutionary adaptations to fruit size, fruit colour or vertical stratification of fruit presentation) or, alternatively, from stochastic speciation-extinction processes. In any case, the close relationship between species richness of Ficus and avian frugivores suggests that figs are keystone resources for animal consumers, even at continental scales.     

Variation in seed dispersal effectiveness: the redundancy of consequences in diversified tropical frugivore assemblages

Plant–frugivore mutualistic assemblages frequently combine multiple, complementary or not (i.e. redundant), distinct effects of animal species. To a large extent, the outcomes of these interactions crucially depend on the delayed consequences of frugivore effectiveness on plant recruitment. We evaluated seed dispersal effectiveness for three plant species in a Brazilian Atlantic forest with a marked habitat heterogeneity defined by bamboo and non‐bamboo patches. Twenty one, 23 and 14 bird species ate fruits of Euterpe edulis, Sloanea guianensis and Virola bicuhyba trees, respectively. For both Euterpe and Virola, visitation rate was the variable contributing for most variance across frugivore species in the quantitative component of effectiveness (QC, which depends on the combined effects of interaction frequency and per‐interaction effect), while the number of fruits manipulated/visit had the greatest contribution in Sloanea. By combining observational data and experimental seed addition for Euterpe we tested for consistent functional patterns among species in the frugivore assemblage, extending beyond the fruit removal stage. Rankings of QC across Euterpe frugivores remained consistent with their relative contributions to fruit removal and, importantly, with their contributions to seedling establishment. Yet, QC of effectiveness across Euterpe frugivores were more homogeneous at the fruit removal and dispersal stages (contribution to seed dispersal) than for the delayed, dissemination and post‐dispersal effects on recruitment. High complementarity of diversified frugivore assemblages may increase through added variance in their delayed effects related to qualitative components of effectiveness. Our results underscore the importance of assessing how dispersal services provided by mutualistic frugivores play complementary, rather than redundant, roles in seed dispersal within heterogeneous landscapes. Such ecological outcomes highlight the value of combining observational and experimental field designs to assess functional diversity patterns of tropical frugivore assemblages and delayed effects of their interactions with plants.     

Reliability of macaques as seed dispersers

Seed dispersal is an ecological process crucial for forest regeneration and recruitment. To date, most studies on frugivore seed dispersal have used the seed dispersal effectiveness framework and have documented seed-handling mechanisms, dispersal distances and the effect of seed handling on germination. In contrast, there has been no exploration of “disperser reliability” which is essential to determine if a frugivore is an effective disperser only in particular regions/years/seasons or across a range of spatio-temporal scales. In this paper, we propose a practical framework to assess the spatial reliability of frugivores as seed dispersers. We suggest that a frugivore genus would be a reliable disperser of certain plant families/genera if: (a) fruits of these plant families/genera are represented in the diets of most of the species of that frugivore, (b) these are consumed by the frugivore genus across different kinds of habitats, and (c) these fruits feature among the yearly staples and preferred fruits in the diets of the frugivore genus. Using this framework, we reviewed frugivory by the genus Macaca across Asia to assess its spatial reliability as seed dispersers. We found that the macaques dispersed the seeds of 11 plant families and five plant genera including at least 82 species across habitats. Differences in fruit consumption/preference between different groups of macaques were driven by variation in plant community composition across habitats. We posit that it is essential to maintain viable populations of macaques across their range and keep human interventions at a minimum to ensure that they continue to reliably disperse the seeds of a broad range of plant species in the Anthropocene. We further suggest that this framework be used for assessing the spatial reliability of other taxonomic groups as seed dispersers.     

Fragmentation and local disturbance of forests reduce frugivore diversity and fruit removal in Ficus thonningii trees

Clearance, fragmentation, and degradation of tropical forests have resulted in declines of biodiversity. This loss of biodiversity is endangering important ecosystem processes such as seed dispersal. If anthropogenic disturbances affect seed dispersal of keystone plants, effects on tropical ecosystems might be especially pronounced. We studied frugivore assemblages and fruit removal from 25 Ficus thonningii trees in the heavily fragmented and disturbed Kakamega Forest, western Kenya. During 400 observation hours we recorded 36 frugivores visiting F. thonningii trees. We recorded significantly fewer frugivorous species in fragments compared to the main forest and in highly, compared to little, disturbed sites. Effects of fragmentation and local disturbance on the number of individuals were not significant but showed similar trends to those in the previous analyses. Furthermore, fruit removal from focal trees was slightly reduced in fragmented and significantly reduced in highly disturbed sites. These results suggest that mutualistic interactions of keystone species can be particularly sensitive to human forest disturbance with potential long-term effects on the biodiversity of tropical forests.     

Positive relationship between fruit removal by animals and seedling recruitment in a tropical forest

Fleshy-fruited plants rely on animal frugivores to disperse their seeds, and seed removal by frugivores may leave an imprint on seedling recruitment. However, to what extent plant–frugivore interactions are related to seedling recruitment has rarely been quantified at the community level, especially in species-rich tropical forests. In this study, we tested the effect of different plant traits on fruit removal by frugivores and tested the relative importance of fruit removal, plant traits and abiotic factors for seedling recruitment. We quantified plant–frugivore interactions of 22 fleshy-fruited plant species consumed by 56 diurnal frugivore species, and counted the number of seedlings that emerged along an elevational gradient in the Colombian Andes. We measured a set of plant traits (i.e., crop size; fruit size; seed load and mass; fruit nutritional contents), estimated the density of adult plants and recorded relevant abiotic factors (light, temperature and humidity). We found that fruit removal by frugivores was positively associated with crop size, but negatively associated with fruit length and unrelated to seed load and fruit nutritional content. Seedling densities were positively related to the density of adult plants, seed mass and fruit removal by animals. We found no relationship between abiotic factors and seedling recruitment. Our results indicate that fruit abundance and morphology are important determinants of fruit removal and that fruit removal is positively associated with seedling recruitment accounting for effects of species abundance and plant traits. We conclude that plant traits shape fruit removal and seedling recruitment at the community level, while these two crucial processes of forest regeneration are directly linked by seed dispersal of animals.     

Can Functional Traits Predict Ecological Interactions? A Case Study Using Rain forest Frugivores and Plants in Australia

In rain forest, the large numbers of species of fleshy-fruited plants and frugivorous animals result in a large number of potential fruit–frugivore interactions, which are challenging to survey in the field. Yet, knowledge of these relationships is needed to predict consequences of changes in the frugivore assemblage for seed dispersal. In the absence of comprehensive dietary information, it may be possible to delineate between frugivores that disperse different plants using ‘functional traits,’ or morphological and behavioral attributes of frugivores that interact with differences in salient characteristics of plant species. Here we use data on the consumption of 244 Australian rain forest plant species by 38 bird species to test for associations between patterns of frugivory and birds': (1) degree of frugivory, (2) gape width, and (3) seed treatment (seed crushing or seed dispersing). Degree of frugivory and gape width explain 74 percent of the variation in the sizes of fruits consumed by frugivorous birds. Among birds that consume a substantial dietary proportion of fruit, birds with wider gapes consume larger fruits. In contrast, this relationship was not shown by birds for which fruit is only a minor dietary component. Degree of frugivory and gape width, together with seed treatment, also strongly predict the overall taxonomic composition and diversity of plants consumed by bird species. Functional classifications of frugivore species may prove useful in developing a predictive understanding of fruit–frugivore interactions in other rain forest regions where detailed dietary information is not available for most frugivores.     

Enhanced seed dispersal of Prunus africana in fragmented and disturbed forests?

Forest destruction and disturbance can have long-term consequences for species diversity and ecosystem processes such as seed dispersal. Understanding these consequences is a crucial component of conserving vulnerable ecosystems. In the heavily fragmented and disturbed Kakamega Forest, western Kenya, we studied seed dispersal of Prunus africana (Rosaceae). In the main forest, five forest fragments, and differently disturbed sites, we quantified the overall frugivore community as an indicator for species diversity. Furthermore, we determined the frugivores on 28 fruiting P. africana trees, estimated seed dispersal, crop size and the general fruit availability of surrounding trees. During the overall frugivore census we recorded 49 frugivorous species; 36 of them were observed visiting P. africana trees and feeding on their fruits. Although overall frugivore species richness was 1.1 times lower in fragments than in main forest sites and 1.02 times higher in highly disturbed than in less disturbed sites, P. africana experienced 1.1 times higher numbers of frugivores in fragments than in main forest sites and 1.5 times higher numbers of frugivores in highly disturbed than in less disturbed sites. Correspondingly, seed dispersal was 1.5 times higher in fragments than in main forest sites and 1.5 times higher in more disturbed than less disturbed sites. Fruit availability of surrounding trees and crop size influenced the number of visitors to some degree. Thus, the number of dispersed seeds seemed to be slightly higher in fragmented and highly disturbed sites. This indicates that loss of single species does not necessarily lead to a decrease of ecosystem services. However, loss of diversity could be a problem in the long term, as a multitude of species might act as buffer against future environmental change.     

榕树在西双版纳热带雨林生态系统中的作用

榕树是西双版纳热带雨林中的关键植物类群之一,能够为多种生物提供栖息地和食物,从而维持该地区热带雨林生态系统的物种多样性。一些种类的榕树有绞杀特性,在森林更新演替中能够起到积极的作用;还有些种类的榕树是先锋物种,在植被恢复中起重要作用。但是,近些年对西双版纳的过度开发已经使热带雨林片断化,榕树种群数量大量减少,榕果内的寄生蜂、食榕果动物也受到了不同程度的影响。保护好西双版纳热带雨林中关键植物类群榕树,是保护和恢复热带雨林生态系统的重要措施之一。     

Nutritional Dimorphism in New Guinea Dioecious Figs

The life history of figs (Ficus, Moraceae) involves pollination by specialized insects and seed dispersal by vertebrate frugivores. This three-way interaction raises the possibility of conflict between pollinators and seed dispersers over fig resources. The conflict might be mediated in dioecious figs by the segregation of inflorescences with specialized male and female sexual functions, termed gall figs and seed figs, on separate trees. In dioecious figs, pollinators are intimately associated with gall figs, whereas vertebrate frugivores prefer seed figs and disperse the seeds they contain. Optimal foraging theory predicts that frugivore preference for ripe seed figs is associated with superior nutritional quality when compared to gall figs. We tested this prediction comparing nutrient and mineral properties of ripe figs in 12 functionally dioecious and two monoecious species from New Guinea. Analyses of variance indicated that gall figs contain more fiber and minerals, whereas seed figs contain significantly more carbohydrates and fat. Fruit bats, the primary dispersers of dioecious figs in New Guinea, prefer carbohydrate-rich diets, and from this perspective, seed figs offer a greater nutritional reward than gall figs. More nondigestible fiber in gall figs than seed figs would appear to discourage frugivory. Parallel differences between ripe gall figs and seed figs occur in each independent dioecious lineage whereas nutritional content in monoecious figs is more similar to seed figs. This suggests that sexual dimorphism in nutritional quality might be adaptive and associated with the maintenance of functional dioecy in figs.     

热带雨林片断化对榕小蜂和榕树物种的影响

榕树是热带雨林生态系统中的一类关键物种。榕树必须依靠榕小传数值和获得有性繁殖;而榕小蜂的幼虫又必须依靠榕树瘿花为食才能生长生长和繁衍后代,因此二者间有着密切的共生关系。研究表明：在西双版纳热带雨林榕小蜂科有３属１７种分布。热带十麻片断化使榕小蜂和榕树的种类呈明显下降趋势;片断热带雨林面积的大小二对二得的物种娄和个体数有明显的影响。     

Seed dispersal in an African fig tree: birds as high quantity,low quality dispersers?

Abstract. Ficus burtt-davyi is a shrub or small tree found in the south and east of South Africa. Based on studies carried out in an area where the plant grows mainly as a rock-splitter, we first describe the nature and timing of the fruit resources it offers to potential dispersal agents, and then the animals that feed on the fruits. The figs are eaten by a diverse avian disperser assemblage, although just two species comprised about half of the recorded visits to the trees. Germination trials with seeds defecated by the birds found that they germinated more quickly than control seeds. Small terrestrial mammals and ants were also found to have a role in fig seed dispersal which may be disproportionate to the number of seeds they transport.     

The role of frugivory in plant diversity maintenance – a simulation approach

Frugivores may play a key role in plant species coexistence by equalizing the species’ representation in the seed rain. Rare species may benefit from enhanced dispersal if frugivores prefer locally scarce fruits, or if rare plants are found in neighborhoods of high fruit density. Using a simulation model of frugivorous birds foraging on landscapes we tested if increased diversity in the seed rain could emerge from rare‐biased fruit selection, from the spatial configuration of plants, or both. In the absence of rare‐biased fruit selection, frugivores were not able to increase the diversity of the seed rain in any of our simulated landscapes. In contrast, when frugivores were attracted to locally scarce fruits, we found increased diversity in the seed rain whenever frugivore mobility across the landscape was high and plant species were well‐mixed in the fruiting neighborhoods. Irrespectively of the behavioral mechanism involved, landscape fragmentation lead to losses in diversity and species richness of simulated communities. In all simulations, density‐dependent mortality of dispersed seeds increased diversity in the community of seedlings. However, landscape homogenization at the scale of frugivores movements decreased the magnitude of this diversification effect. In summary, our study shows that frugivory has the potential to increase diversity in the seed rain when frugivores display rare‐biased fruit choices, provided that rare and common plants form heterogeneous neighborhoods. They also show that fragmentation is a major threat for diversity maintenance in the early‐regenerating community. Finally, they show that rarity confers advantages during regeneration only if it occurs at the scale of frugivores’ foraging decisions.     

Halting Regime Shifts in Floristically Intact Tropical Forests Deprived of Their Frugivores

Ecological restoration typically focuses on promoting vegetation recovery in degraded habitat or reintroducing endangered animals to enhance their regional or global persistence. Here, we argue that attention should also be devoted to vertebrate reintroductions in overhunted but floristically intact tropical forests in order to prevent insidious regime shifts in these systems. Growing evidence suggests that tropical forests deprived of seed‐dispersing animals exhibit replacement of fleshy fruiting trees by species with abiotic seed dispersal. Left unchecked, this process could eventually render the forest uninhabitable by frugivores through reduced density and diversity of their food plants. In tropical areas where hunting can be controlled, we contend that frugivore reintroduction, regulation of wild fruit harvest by humans, and outplanting of native fruiting trees should be deployed as management tools long before the systems are in need of traditional habitat restoration.     

Bird Assemblage and Visitation Pattern at Fruiting Elmerrillia tsiampaca (Magnoliaceae) Trees in Papua New Guinea

Most tropical trees produce fleshy fruits that attract frugivores that disperse their seeds. Early demography and distribution for these tree species depend on the effects of frugivores and their behavior. Anthropogenic changes that affect frugivore communities could ultimately result in changes in tree distribution and population demography. We studied the frugivore assemblage at 38 fruiting Elmerrillia tsiampaca, a rain forest canopy tree species in Papua New Guinea. Elmerrillia tsiampaca is an important resource for frugivorous birds at our study site because it produces abundant lipid-rich fruits at a time of low fruit availability. We classified avian frugivores into functional disperser groups and quantified visitation rates and behavior at trees during 56 canopy and 35 ground observation periods. We tested predictions derived from other studies of plant–frugivore interactions with this little-studied frugivore assemblage in an undisturbed rain forest. Elmerrillia tsiampaca fruits were consumed by 26 bird species, but most seeds were removed by eight species. The most important visitors (Columbidae, Paradisaeidae and Rhyticeros plicatus) were of a larger size than predicted based on diaspore size. Columbidae efficiently exploited the structurally protected fruit, which was inconsistent with other studies in New Guinea where structurally protected fruits were predominantly consumed by Paradisaeidae. Birds vulnerable to predation foraged for short time periods, consistent with the hypothesis that predator avoidance enhances seed dispersal. We identified seven functional disperser groups, indicating there is little redundancy in disperser groups among the regular and frequent visitors to this tropical rain forest tree species.     

Large frugivores matter more on an island: Insights from island‐mainland comparison of plant–frugivore communities

Endozoochory, a mutualistic interaction between plants and frugivores, is one of the key processes responsible for maintenance of tropical biodiversity. Islands, which have a smaller subset of plants and frugivores when compared with mainland communities, offer an interesting setting to understand the organization of plant–frugivore communities vis‐a‐vis the mainland sites. We examined the relative influence of functional traits and phylogenetic relationships on the plant–seed disperser interactions on an island and a mainland site. The island site allowed us to investigate the organization of the plant–seed disperser community in the natural absence of key frugivore groups (bulbuls and barbets) of Asian tropics. The endemic Narcondam Hornbill was the most abundant frugivore on the island and played a central role in the community. Species strength of frugivores (a measure of relevance of frugivores for plants) was positively associated with their abundance. Among plants, figs had the highest species strength and played a central role in the community. Island‐mainland comparison revealed that the island plant–seed disperser community was more asymmetric, connected, and nested as compared to the mainland community. Neither phylogenetic relationships nor functional traits (after controlling for phylogenetic relationships) were able to explain the patterns of interactions between plants and frugivores on the island or the mainland pointing toward the diffused nature of plant–frugivore interactions. The diffused nature is a likely consequence of plasticity in foraging behavior and trait convergence that contribute to governing the interactions between plants and frugivores. This is one of the few studies to compare the plant–seed disperser communities between a tropical island and mainland and demonstrates key role played by a point‐endemic frugivore in seed dispersal on island.     

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.     

A simple null model predicts fruit-frugivore interactions in a temperate rainforest

Studies of seed dispersal mutualisms typically test for adaptive relationships between fruits and frugivores. Here, I take the opposite approach, and ask what relationships would be expected based on chance encounters between mutualists. I derived a simple null model to predict pair-wise relationships between fruit and frugivore species. I assumed that all frugivores had identical fruit preferences, but allowed for interspecific variation in plant abundances, frugivore abundances and fruit phenologies. Under these conditions, the number of visits each frugivore species makes to each plant species results from the product of plant abundances and frugivore abundances when each plant species produces fruit. I then tested null model predictions with observations in a temperate rainforest in British Columbia, Canada. I measured the abundance and phenology of seven bird-dispersed plant species, seasonal changes in the abundances of six avian frugivore species and 212 interactions between them. Empirical results were generally consistent with predictions, suggesting that relationships between birds and fruits are structured randomly. However, some variation in relationships between observations and predictions was observed, suggesting deterministic processes may also be important. Overall results illustrate that predictable relationships between fruit and frugivore species can result from random encounters between mutualists.     

Fruit tracking,frugivore satiation,and their consequences for seed dispersal

Vertebrate frugivore communities are easily satiated by abundant fruit supplies and, contrary to abiotic dispersal agents, typically disperse only part of the available seed pool. This frugivore satiation is likely to be a widespread phenomenon and should be an influential predictor of plants’ ability to disperse their offspring to suitable establishment sites; yet it has never been systematically quantified. Here I investigate patterns of fruit abundance, frugivore activity and frugivore satiation, and their consequences for seed dispersal in the fleshy-fruited tree Frangula alnus. Based on constant-effort seed trapping conducted over 3 years, I assess densities of total and frugivore-consumed seedfall across two spatial (within/between populations) and two temporal (within/between ripening seasons) scales. Furthermore, I examine relationships between fruit abundance and the amount of seeds that are actually dispersed away from fruiting trees. Frugivore activity tightly matched fruit abundance, although some differences existed between scales. This marked fruit tracking did not prevent a significant frugivore satiation, however, and only 53% of the available fruit crops were actually consumed. The extent of satiation varied most at the within-population level, likely due to the territorial behaviour of important frugivore species. In contrast, levels of satiation remained remarkably invariable through time, suggesting that frugivores behave as opportunists and closely adjust the composition of their diet to the available food supply. Overall, greater fruit abundance resulted in a higher proportion of seeds falling beneath fruiting trees, but it also helped increase the (absolute) number of seeds dispersed. This study shows that frugivore satiation can be an important phenomenon even when frugivores tightly track fruit abundance. Its negative effects on recruitment may be attenuated, however, if greater fruit crops help increase population-wide frugivore activity and the amount of seeds being dispersed to suitable establishment sites.