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.     

Species richness matters for the quality of ecosystem services: a test using seed dispersal by frugivorous birds

The positive link between biodiversity and ecosystem functioning is a current paradigm in ecological science. However, little is known of how different attributes of species assemblages condition the quality of many services in real ecosystems affected by human impact. We explore the links between the attributes of a frugivore assemblage and the quantitative and qualitative components of its derived ecosystem service, seed dispersal, along a landscape-scale gradient of anthropogenic forest loss. Both the number and the richness of seeds being dispersed were positively related to frugivore abundance and richness. Seed dispersal quality, determined by the fine-scale spatial patterns of seed deposition, mostly depended on frugivore richness. In fact, richness was the only attribute of the frugivore assemblage affecting the probability of seed dispersal into deforested areas of the landscape. The positive relationships between frugivore richness per se (i.e. independent of frugivore abundance and composition) and all components of seed dispersal suggest the existence of functional complementarity and/or facilitation between frugivores. These links also point to the whole assemblage of frugivores as a conservation target, if we aim to preserve a complete seed dispersal service and, hence, the potential for vegetation regeneration and recovery, in human-impacted landscapes.     

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.     

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.     

Effects of frugivore impoverishment and seed predators on the recruitment of a keystone palm

Many plant species are threatened as a result of extinction of their large-bodied frugivores all over the world. Additionally, introduced herbivores and seed predators may cause severe pressure on early stages of plant recruitment. We studied the seed dispersal and seed predation of the keystone palm Euterpe edulis on a land-bridge island with a highly impoverished frugivore fauna and overabundant seed predators, and in a continuous Atlantic forest in Brazil. While the diversity of avian seed dispersers and predators was higher on the mainland, the abundance of seed dispersers was 4-fold higher on the island. Turdus flavipes was responsible for 72% and 96% of seeds removed in the island and mainland, respectively. However, the higher density of T. flaviceps on the island did not result in higher seed removal. In fact, seed removal rate was 1.7 times lower there than on the mainland, probably due to the aggressive behavior of the major seed disperser who defend palm fruits. Seed predation, on the other hand, was markedly higher on the island, where nearly 100% of seeds were preyed upon, but only 0.3% on the mainland. As a consequence of higher seed predation the population of E. edulis has few numbers of seedlings and saplings on the island. Therefore, management of the seed predator populations on the island is a key priority for recovering the natural population of this keystone palm and the frugivores that depend on its fruits.     

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.     

Unravelling seed dispersal through fragmented landscapes: Frugivore species operate unevenly as mobile links

Seed dispersal constitutes a pivotal process in an increasingly fragmented world, promoting population connectivity, colonization and range shifts in plants. Unveiling how multiple frugivore species disperse seeds through fragmented landscapes, operating as mobile links, has remained elusive owing to methodological constraints for monitoring seed dispersal events. We combine for the first time DNA barcoding and DNA microsatellites to identify, respectively, the frugivore species and the source trees of animal‐dispersed seeds in forest and matrix of a fragmented landscape. We found a high functional complementarity among frugivores in terms of seed deposition at different habitats (forest vs. matrix), perches (isolated trees vs. electricity pylons) and matrix sectors (close vs. far from the forest edge), cross‐habitat seed fluxes, dispersal distances and canopy‐cover dependency. Seed rain at the landscape‐scale, from forest to distant matrix sectors, was characterized by turnovers in the contribution of frugivores and source‐tree habitats: open‐habitat frugivores replaced forest‐dependent frugivores, whereas matrix trees replaced forest trees. As a result of such turnovers, the magnitude of seed rain was evenly distributed between habitats and landscape sectors. We thus uncover key mechanisms behind “biodiversity–ecosystem function” relationships, in this case, the relationship between frugivore diversity and landscape‐scale seed dispersal. Our results reveal the importance of open‐habitat frugivores, isolated fruiting trees and anthropogenic perching sites (infrastructures) in generating seed dispersal events far from the remnant forest, highlighting their potential to drive regeneration dynamics through the matrix. This study helps to broaden the “mobile‐link” concept in seed dispersal studies by providing a comprehensive and integrative view of the way in which multiple frugivore species disseminate seeds through real‐world landscapes.     

Effects of site and fruit size on the composition of avian frugivore assemblages in a fragmented Afrotropical forest

Factors influencing the interaction between fruiting trees and their frugivorous seed dispersers in fragmented Afrotropical landscapes are poorly known. With the use of Mantel statistics we analysed assemblages of frugivorous birds on 58 individual trees belonging to 11 species growing in seven Kenyan cloud forest fragments. Overall, frugivores showed little specialization on particular trees. Fruit size explained a substantial amount of the variation in frugivore assemblages among different tree species at the same site. In addition, frugivore assemblages on conspecific trees were significantly more similar when the trees occurred at the same site. This location effect was attributable to the different sites and forest fragments (of different sizes and disturbance levels) varying in the densities and composition of their avian frugivores, vegetation composition and tree fruiting phenologies. It was consolidated further by the low mobility of most of these avian frugivores, particularly their reluctance to cross between forest fragments. Habitat disturbance and fragmentation may therefore have affected fruit selection, with implications for both seed dispersal and regeneration.     

Differences among avian frugivores in seed dispersal to degraded habitats

Vertebrate frugivores enhance tropical forest regeneration by dispersing seeds into degraded areas. However, the importance of individual species as dispersers may vary within a community. Management and restoration would benefit from understanding which species are critical in moving native seeds into degraded habitats. We compared habitat composition of bird start and end locations for movement intervals based on mean gut passage times for the avian frugivore community on the island of Saipan. The proportion of movement intervals that began in intact, native forest varied among species, with Golden White‐eyes having the highest proportion. However, this species tended to remain in intact forest and only rarely crossed into degraded habitats. Bridled White‐eyes and Mariana Fruit Doves exhibited slightly higher rates of crossing from intact forest to degraded habitats, suggesting an ability to disperse native seeds to degraded areas. White‐throated Ground Doves were never recorded crossing from intact forest to degraded habitats. Despite having a low proportion of movement intervals beginning in intact forest, Micronesian Starlings showed a higher proportion and absolute number of movements from intact forest to degraded habitats, due to their propensity to move frequently, across long distances, and across habitat types. In this species‐poor frugivore network, seed dispersal into degraded habitats appears highly dependent on one species within the community. Regeneration of degraded lands may be severely hindered if this key disperser is lost.     

Survival and Scatterhoarding of Frugivores-Dispersed Seeds as a Function of Forest Disturbance

The effect of forest disturbance on survival and secondary dispersal of an artificial seed shadow (N= 800) was studied at Brownsberg Natural Park, Suriname, South America. We scattered single seeds of the frugivore‐dispersed tree Virola kwatae (Myristicaceae), simulating loose dispersal by frugivores, in undisturbed and disturbed secondary forest habitats. Seed survival rate aboveground was high (69%) within 2 wk and was negatively correlated with scatterhoarding rate by rodents, the latter being significantly lower in the undisturbed forest (9%) than in the disturbed forest (20%). Postdispersal seed predation by vertebrates was low (3%) and infestation of seeds by invertebrates was almost zero in all instances. Therefore, secondary seed dispersal by rodents in forest is not as critical for recruitment as observed among other bruchid‐infested large‐seeded species. Secondary seed dispersal by rodents may, however, facilitate seedling recruitment whether cached seeds experience greater survival than seeds remaining above ground surface.     

Seed dispersal effectiveness by a large‐bodied invasive species in defaunated landscapes

Animal‐dispersed plants are increasingly reliant on effective seed dispersal provided by small‐bodied frugivores in defaunated habitats. In the Neotropical region, the non‐native wild pig (Sus scrofa) is expanding its distribution and we hypothesized that they can be a surrogate for seed dispersal services lost by defaunation. We performed a thorough analysis of their interaction patterns, interaction frequencies, seed viability, and characteristics of the seed shadows they produce. We found 15,087 intact seeds in 56% of the stomachs and 5,186 intact seeds in 90% of the scats analyzed, 95% of which were smaller than 10 mm in diameter. Wild pigs were the third most effective disperser among 21 extant frugivore species in a feeding trail experiment in terms of quantity of seeds removed. Gut retention time was 70 ± 23 hr, indicating wild pigs can promote long‐distance seed dispersal. Seed survival after seed handling and gut passage by wild pigs was positively related with seed size, but large seeds were spat out and only smaller seeds were defecated intact, for which we observed a positive or neutral effect on germination relative to manually de‐pulped seeds. Finally, deposition of seeds was four times more frequent in unsuitable than suitable sites for seedling recruitment and establishment. Seed dispersal effectiveness by wild pigs is high in terms of the quantity of seeds dispersed but variable in terms of the quality of the service provided. Our study highlights that negative and positive effects delivered by non‐native species should be examined in a case by case scenario. Abstract in Portuguese is available with online material.     

Seed Dispersal Patterns by Large Frugivorous Mammals in a Degraded Mosaic Landscape

Seed dispersal by Red fox (Vulpes vulpes), Stone marten (Martes foina), and Wild boar (Sus scrofa) was analyzed in an extensively degraded mosaic landscape in Sierra Nevada (SE Spain). The main objective was to determine whether seed dispersal by mammals was related to habitat degradation within a mosaic of adjacent degraded patches mixed with native forest and thereby to determine the potential role of mammals as seed dispersers in degraded landscape units. For three consecutive years, mammal feces were collected in the fruit production period, extracting all seeds of woody species found therein and analyzing their viability. Feces were collected in three different plots for each of five different landscape units: shrubland, native forest, and dense, cleared, and fenced reforestation stands. Seeds from 16 woody species (which represent more than a half of the total fleshy‐fruited woody species available) were recorded, although some agrarian species are also introduced in a low percentage of the scats. Seeds showed a high viability rate for all dispersed species, irrespective of the mammal disperser. No differences in species composition appeared in the overall landscape units or in the seed density between degraded habitats. Due to the small patch size, the high viability of dispersed seeds, and the large home range of the large mammals, these three animal species act as efficient seed dispersers for a diverse assemblage of woody plant species regardless of the habitat type within this degradation framework. This fact has important consequences for the biodiversity recuperation in these degraded habitats, principally in pine plantations.     

Plant–frugivore networks are less specialized and more robust at forest–farmland edges than in the interior of a tropical forest

Forest fragmentation and local disturbance are prevailing threats to tropical forest ecosystems and affect frugivore communities and animal seed dispersal in different ways. However, very little is known about the effects of anthropogenic forest edges and of local disturbance on the structure and robustness of plant–frugivore networks. We carried out focal tree observations to record the frugivore species feeding on eight canopy tree species in the forest interior and at forest–farmland edges in a little and a highly disturbed part of a Kenyan rain forest. For each frugivore species, we recorded its body mass and its forest dependence. We examined how forest edge and local disturbance affected the abundance, the richness and the composition of the frugivore community and tested whether forest edge and local disturbance affected plant frugivore networks. Abundance and species richness of frugivores were higher at edges than in the forest interior. Forest visitors and small‐bodied frugivores increased, while forest specialists decreased in abundance at forest edges. The changes in frugivore community composition resulted in plant–frugivore networks that were more connected, more nested and more robust against species extinctions at forest–farmland edges than in the forest interior. Network specialization was lower at forest edges than in the forest interior because at the edges plant specialization on frugivores was very low in small‐fruited species. In contrast, small‐fruited plants were more specialized than large‐fruited plants in the forest interior. Our findings suggest that forest‐visiting birds may stabilize seed‐dispersal services for small‐fruited plant species at rain forest margins, while seed‐dispersal services for large‐fruited plant species may be disrupted at forest edges due to the decrease of large‐bodied frugviores. To assess the ultimate consequences of bird movements from farmland to forest edges for ecosystem functioning, future studies are required to investigate the seed‐dispersal qualities provided by forest‐visiting bird species in the tropics.     

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.     

Impact of habitat structure and fruit abundance on avian seed dispersal and fruit predation

So far, it is poorly understood how differential responses of avian seed dispersers and fruit predators to changes in habitat structure and fruit abundance along land-use gradients may translate into consequences for the seed dispersal of associated plants. We selected a gradient of habitat modification (forest, semi-natural, and rural habitat) characterized by decreasing tree cover and a high variation in local fruit availability. Along this gradient we quantified fruit removal by avian seed dispersers and fruit predators from 18 Sorbus aucuparia trees. We analyzed the relative importance of tree cover and fruit abundance in explaining species richness, abundance and fruit removal rates of both guilds from S. aucuparia trees. Species richness and abundance of seed dispersers decreased with decreasing tree cover, whereas fruit removal by seed dispersers decreased with decreasing fruit abundance independent of tree cover. Both variables had no effect on species richness, abundance and fruit removal by fruit predators. Consequently, seed dispersers dominated relative fruit removal in fruit-rich sites but the dispersal/predation ratio shifted in favor of predation in fruit-poor habitat patches. Our study demonstrates that variation in local habitat structure and fruit abundance can cause guild-specific responses. Such responses may result in a shift in fruit removal regimes and might affect the dispersal ability of dependent fruiting plants. Future studies should aim at possible consequences for plant recruitment and guild-specific responses of frugivores to disturbance gradients on the level of entire plant–frugivore associations.     

Dispersal of fig seeds in the Cook Islands: introduced frugivores are no substitutes for natives

Across the Pacific, island vegetation is altering in response to changes in seed disperser assemblages brought about by extinctions and introductions of birds and other animals. On the Cook Islands in the South Pacific, the Pacific Banyan (Ficus prolixa, Moraceae) is undergoing little if any recruitment, possibly linked to a lack of dispersal agents. On Rarotonga, where F. prolixa is found in semi-urban and agricultural environments, there is no recent recruitment in contrast to the situation on Atiu where the tree is common in native forest. We examined the quality and quantity of seed dispersal offered to F. prolixa by the available frugivores on these islands, comparing the effectiveness of extant native and introduced species. The native Cook Islands fauna, particularly birds and bats, appear to be the most effective seed dispersers of F. prolixa, both in terms of quantity and quality. Whilst these are relatively numerous on Atiu, they rarely visit F. prolixa on Rarotonga. The native Chocolate hermit crab Coenobita cavipes is a previously unreported additional native seed disperser, conferring low quantity, but high quality dispersal. Introduced birds and mammals are the most numerous F. prolixa frugivores on Rarotonga and in non-forest environments on Atiu, but they act mainly as seed predators. Consequently, the losses and rarity of remaining native frugivores have not been compensated for by introduced species on Rarotonga which may be contributing to the absence of recruitment there.     

Linking frugivore activity to early recruitment of a bird dispersed tree,Eugenia umbelliflora (Myrtaceae) in the Atlantic rainforest

Seed dispersal by animals is a complex process involving several distinct stages: fruit removal by frugivores, seed delivery in different microhabitats, seed germination, seedling establishment, and adult recruitment. Nevertheless, studies conducted until now have provided scarce information concerning the sequence of stages in a plant's life cycle in its entirety. The main objective of this study was to evaluate the immediate consequences of frugivore activity for Eugenia umbelliflora (Myrtaceae) early recruitment by measuring the relative importance of each fruit‐eating bird species on the establishment of new seedlings in scrub and low restinga vegetation in the Atlantic rainforest, Brazil. We conducted focal tree observations on E. umbelliflora trees recording birds' feeding behaviour and post‐feeding movements. We also recorded the fate of dispersed seeds in scrub and low restinga vegetation. We recorded 17 bird species interacting with fruits in 55 h of observation. Only 30% of the handled fruits were successfully removed. From 108 post flight movements of exit from the fruiting trees, 30.6% were to scrub and 69.4% to low restinga forest. Proportion of seed germination was higher in low restinga than in the scrub vegetation. Incorporating the probabilities of seeds' removal, deposition, and germination in both sites, we found that the relative importance of each frugivorous bird as seed dispersers varies largely among species. Turdus amaurochalinus and Turdus rufiventris were the best dispersers, together representing almost 12% probability of seed germination following removal. Our results show the importance of assessing the overall consequence of seed dispersal within the framework of disperser effectiveness, providing a more comprehensive and realistic evaluation of the relative importance of different seed dispersers on plant population dynamics.     

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.     

Observing frugivores or collecting scats: a method comparison to construct quantitative seed dispersal networks

Mutualistic interactions form the basis for many ecological processes and are often analyzed within the framework of ecological networks. These interactions can be sampled with a range of methods and first analyses of pollination networks sampled with different methods showed differences in common network metrics. However, it is yet unknown if metrics of seed dispersal networks are similarly affected by the sampling method and if different methods detect a complementary set of frugivores. This is necessary to better understand the (dis-)advantages of each method and to identify the role of each frugivore for the seed dispersal process. Here, we compare seed removal networks based on the observation of 2189 frugivore visits on ten focal plant species with seed deposition networks constructed by DNA barcoding of plant seeds in 3094 frugivore scats. We were interested in whether both methods identify the same disperser species and if species-level network metrics of plant species were correlated between network types. Both methods identified the same avian super-generalist frugivores, which accounted for the highest number of dispersed seeds. However, only with DNA barcoding, we detected elusive but frequent mammalian seed dispersers. The overall networks created by both methods were congruent but the plant species' degree, their interaction frequency and their specialization index (d′) differed. Our study suggests that DNA barcoding of defecated and regurgitated seeds can be used to construct quantitative seed deposition networks similar to those constructed by focal observations. To improve the overall completeness of seed dispersal networks it might be useful to combine both methods to detect interactions by both birds and mammals. Most importantly, the DNA barcoding method provides information on the post-dispersal stage and thus on the qualitative contribution of each frugivore for the plant community thereby linking species interactions to regeneration dynamics of fleshy-fruited plant species.     

Complementary seed dispersal by three avian frugivores in a fragmented Afromontane forest

Questions: To what extent does species‐specific variation in gut passage time (GPT), habitat use and mobility of three key avian frugivores synergistically affect the distribution of Xymalos monospora seeds within and among isolated forest fragments? Location: Three fragments of a severely fragmented cloud forest, Taita Hills, southeast Kenya. Methods: We experimentally determined GPTs of X. monospora seeds and recorded movements and habitat use by Turdus helleri, Andropadus milanjensis and Tauraco hartlaubi through radiotelemetry, and combined these data to generate species‐specific seed dispersal patterns. Results: Differences in mobility and habitat use among the three frugivores caused significant complementarity in seed dispersal, despite the fact that gut transit times were highly comparable. While the most sedentary and forest‐dependent species mainly led to short‐distance dispersal away from parent trees, two more mobile species dispersed seeds further away from the source trees, both within indigenous forest patches and towards exotic plantations and isolated fruiting trees in the landscape matrix. A. milanjensis inhabiting a very small forest fragment spent significantly more time in the landscape matrix than conspecifics residing in the two larger fragments. Conclusions: By varying distances over which seeds are carried away from parent trees and the habitat types in which they are ultimately deposited, avian frugivores affect the spatial distribution of seeds and early plant recruits in a distinct and complementary manner. Because landscape properties are expected to lead to different constraints on avian mobility for habitat specialists and for generalists, ecosystem processes such as avian seed dispersal are shaped by complex interactions between disperser behaviour and the environment.