Frugivory and seed dispersal by vertebrates in the Oriental (Indomalayan) Region

Current knowledge of frugivory and seed dispersal by vertebrates in the Oriental Region is summarized. Some degree of frugivory has been reported for many fish and reptile species, almost half the genera of non-marine mammals and more than 40% of bird genera in the region. Highly frugivorous species, for which fruit dominates the diet for at least part of the year, occur in at least two families of reptiles, 12 families of mammals and 17 families of birds. Predation on seeds in fleshy fruits is much less widespread taxonomically: the major seed predators are colobine monkeys and rodents among the mammals, and parrots, some pigeons, and finches among the birds. Most seeds in the Oriental Region, except near its northern margins, are dispersed by vertebrate families which are endemic to the region or to the Old World. Small fruits and large, soft fruits with many small seeds are consumed by a wide range of potential seed dispersal agents, including species which thrive in small forest fragments and degraded landscapes. Larger, bigger-seeded fruits are consumed by progressively fewer dispersers, and the largest depend on a few species of mammals and birds which are highly vulnerable to hunting, fragmentation and habitat loss.     

Ecological,historical and evolutionary determinants of modularity in weighted seed‐dispersal networks

Modularity is a recurrent and important property of bipartite ecological networks. Although well‐resolved ecological networks describe interaction frequencies between species pairs, modularity of bipartite networks has been analysed only on the basis of binary presence–absence data. We employ a new algorithm to detect modularity in weighted bipartite networks in a global analysis of avian seed‐dispersal networks. We define roles of species, such as connector values, for weighted and binary networks and associate them with avian species traits and phylogeny. The weighted, but not binary, analysis identified a positive relationship between climatic seasonality and modularity, whereas past climate stability and phylogenetic signal were only weakly related to modularity. Connector values were associated with foraging behaviour and were phylogenetically conserved. The weighted modularity analysis demonstrates the dominating impact of ecological factors on the structure of seed‐dispersal networks, but also underscores the relevance of evolutionary history in shaping species roles in ecological communities.     

Scale and macroecological patterns in seed dispersal mutualisms

Although some studies of seed dispersal mutualisms have documented adaptive relationships between fruits and frugivores, others have shown that adaptive patterns are constrained by phylogenetic, historical or climatic effects. Variable results among studies have thwarted attempts to find a paradigm to unite the field and direct research. Two recent studies in Global Ecology and Biogeography exemplify this dichotomy. One paper reported adaptive relationships between abundances of birds and fruits, while the other study found that bird‐fruit abundance patterns were constrained by climatic effects. Almost paradoxically, both studies were conducted at the same locale. However, they focused on different spatio‐temporal scales. These results are surprisingly consistent with several other recent studies that have taken a macroecological approach. They also indicate that mutualistic relationships between fruits and frugivores are scale dependent. When viewed together, recent work suggests that the conflicting results of previous studies may result from spatio‐temporal variability of mutualistic relationships. This paper briefly reviews the emerging field of seed dispersal macroecology. A growing appreciation for scale appears to be leading the field in a new direction.     

Seed‐dispersal interactions in fragmented landscapes – a metanetwork approach

Mutualistic interactions repeatedly preserved across fragmented landscapes can scale‐up to form a spatial metanetwork describing the distribution of interactions across patches. We explored the structure of a bird seed‐dispersal (BSD) metanetwork in 16 Neotropical forest fragments to test whether a distinct subset of BSD‐interactions may mediate landscape functional connectivity. The metanetwork is interaction‐rich, modular and poorly connected, showing high beta‐diversity and turnover of species and interactions. Interactions involving large‐sized species were lost in fragments < 10 000 ha, indicating a strong filtering by habitat fragmentation on the functional diversity of BSD‐interactions. Persistent interactions were performed by small‐seeded, fast growing plant species and by generalist, small‐bodied bird species able to cross the fragmented landscape. This reduced subset of interactions forms the metanetwork components persisting to defaunation and fragmentation, and may generate long‐term deficits of carbon storage while delaying forest regeneration at the landscape level.     

Seed‐dispersal networks respond differently to resource effects in open and forest habitats

While patterns in species diversity have been well studied across large‐scale environmental gradients, little is known about how species’ interaction networks change in response to abiotic and biotic factors across such gradients. Here we studied seed‐dispersal networks on 50 study plots distributed over ten different habitat types on the southern slopes of Mt Kilimanjaro, Tanzania, to disentangle the effects of climate, habitat structure, fruit diversity and fruit availability on different measures of interaction diversity. We used direct observations to record the interactions of frugivorous birds and mammals with fleshy‐fruited plants and recorded climatic conditions, habitat structure, fruit diversity and availability. We found that Shannon interaction diversity (H) increased with fruit diversity and availability, whereas interaction evenness (E_H) and network specialization (H₂) responded differently to changes in fruit availability depending on habitat structure. The direction of the effects of fruit availability on E_H and H₂ differed between open habitats at the mountain base and structurally complex habitats in the forest belt. Our findings illustrate that interaction networks react differently to changes in environmental conditions in different ecosystems. Hence, our findings demonstrate that future projections of network structure and associated ecosystem functions need to account for habitat differences among ecosystems.     

An invasive tree alters the structure of seed dispersal networks between birds and plants in French Polynesia

Aim We studied how the abundance of the highly invasive fruit‐bearing tree Miconia calvescens DC. influences seed dispersal networks and the foraging patterns of three avian frugivores. Location Tahiti and Moorea, French Polynesia. Methods Our study was conducted at six sites which vary in the abundance of M. calvescens. We used dietary data from three frugivores (two introduced, one endemic) to determine whether patterns of fruit consumption are related to invasive tree abundance. We constructed seed dispersal networks for each island to evaluate how patterns of interaction between frugivores and plants shift at highly invaded sites. Results Two frugivores increased consumption of M. calvescens fruit at highly invaded sites and decreased consumption of other dietary items. The endemic fruit dove, Ptilinopus purpuratus, consumed more native fruit than either of the two introduced frugivores (the red‐vented bulbul, Pycnonotus cafer, and the silvereye, Zosterops lateralis), and introduced frugivores showed a low potential to act as dispersers of native plants. Network patterns on the highly invaded island of Tahiti were dominated by introduced plants and birds, which were responsible for the majority of plant–frugivore interactions. Main conclusions Shifts in the diet of introduced birds, coupled with reduced populations of endemic frugivores, caused differences in properties of the seed dispersal network on the island of Tahiti compared to the less invaded island of Moorea. These results demonstrate that the presence of invasive fruit‐bearing plants and introduced frugivores can alter seed dispersal networks, and that the patterns of alteration depend both on the frugivore community and on the relative abundance of available fruit.     

Defaunation leads to interaction deficits,not interaction compensation,in an island seed dispersal network

Following defaunation, the loss of interactions with mutualists such as pollinators or seed dispersers may be compensated through increased interactions with remaining mutualists, ameliorating the negative cascading impacts on biodiversity. Alternatively, remaining mutualists may respond to altered competition by reducing the breadth or intensity of their interactions, exacerbating negative impacts on biodiversity. Despite the importance of these responses for our understanding of the dynamics of mutualistic networks and their response to global change, the mechanism and magnitude of interaction compensation within real mutualistic networks remains largely unknown. We examined differences in mutualistic interactions between frugivores and fruiting plants in two island ecosystems possessing an intact or disrupted seed dispersal network. We determined how changes in the abundance and behavior of remaining seed dispersers either increased mutualistic interactions (contributing to “interaction compensation”) or decreased interactions (causing an “interaction deficit”) in the disrupted network. We found a “rich‐get‐richer” response in the disrupted network, where remaining frugivores favored the plant species with highest interaction frequency, a dynamic that worsened the interaction deficit among plant species with low interaction frequency. Only one of five plant species experienced compensation and the other four had significant interaction deficits, with interaction frequencies 56–95% lower in the disrupted network. These results do not provide support for the strong compensating mechanisms assumed in theoretical network models, suggesting that existing network models underestimate the prevalence of cascading mutualism disruption after defaunation. This work supports a mutualist biodiversity‐ecosystem functioning relationship, highlighting the importance of mutualist diversity for sustaining diverse and resilient ecosystems.     

Scale‐Dependent Spatial Match between Fruits and Fruit‐eating Birds during the Breeding Season in Yungas Andean Forests

The multi‐scale spatial match between bird and food abundances is a main driver of the structure of fruit‐eating bird assemblages. We explored how the activity of fruit‐eating birds was influenced by the abundance of fruits at the local and landscape scales in Andean mountain forests during the breeding season, when most birds forage close to their nest. We measured: (1) the spatial scale of variation in the abundance of fruits, (2) the spatial scale of variation in the activity of fruit‐eating birds, and (3) the spatial match between both variables. The sampling design consisted of eleven 1.2‐ha sites, each subdivided into 30 cells of 20 × 20 m, where we sampled fruits and fruit‐eating birds. We found that fruit consumption, and to a lesser extent bird abundance, were associated with local spatial variation in abundance of selected fruit species. However, fruit‐eating birds did not modify their spatial distribution in the landscape following changes in availability of these fruits. Our study shows that fruit‐eating birds detect local spatial variation in fruit availability in their home breeding ranges, and exploit patches with large clusters of selected fruits. However, it may be unprofitable for breeding birds to stray too far from their nests to exploit fruit‐rich patches, accounting for the absence of fruit tracking at larger spatial scales.     

When the company does not matter: High‐quality ant seed‐disperser does not drive the spatial distribution of large‐seeded myrmecochorous plants

Mutualisms are one of the main forces shaping species spatial patterns at all geographic scales. In generalised mutualisms, however, the dependence among partners is highly variable in time and space, and therefore, the effect of diffuse mutualisms on species geographic distributions is unclear. Myrmecochorous seeds in Brazilian semi‐arid vegetation are dispersed by several ant species. However, large‐seeded species are especially dependent on dispersal by the giant ant Dinoponera quadriceps, which is the main disperser of such diaspores and the species that provide the longest dispersal distance among ant species in this system. Hence, we hypothesise that the presence of D. quadriceps shapes the distribution of large‐seeded, but not the distribution of small‐seeded myrmecochorous plant species. To evaluate this hypothesis, we modelled the potential distribution of two large‐seeded (which are predominantly dispersed by D. quadriceps) and two small‐seeded (which are barely dispersed by D. quadriceps) Euphorbiaceae species and the potential distribution of D. quadriceps. We analysed the relationship between the occurrence suitability of D. quadriceps and the occurrence suitability of plant species. We found that the potential distribution of both large‐seeded and small‐seeded myrmecochorous plants was unrelated to D. quadriceps occurrence suitability. It means that the disproportional benefits provided by high‐quality disperser at local scales may not emerge at broader geographical scales. In Caatinga vegetation, diaspores are submitted to strong abiotic filters that constraint seed germination and establishment after the dispersal phase. Such abiotic filters may dilute the initial benefit provided by long‐distance dispersers. Therefore, we suggest that in dry environments like the Caatinga, the benefits of long‐distance removals should be outweighed by the risk of reach new habitats with unfavourable conditions for germination and establishment.     

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

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

Global patterns in anuran–prey networks: structure mediated by latitude

Life on Earth is supported by an infinite number of interactions among organisms. Species interactions in these networks are influenced by latitude, evolutionary history and species traits. We performed a global‐scale literature analysis to build up a database of interactions between anuran communities and their preys, from a wide range of geographical areas, using a network approach. For this purpose, we compiled a total of 55 weighted anuran–prey interaction networks, 39 located in the tropics and 16 in temperate areas. We tested the influence of latitude, as well as anuran taxonomic, functional and phylogenetic richness on network metrics. We found that anuran–prey networks are not nested, exhibit low complementary specialization and modularity and high connectance when compared to other types of networks. The main effects on network metrics were related to latitude, followed by anuran taxonomic, functional and phylogenetic richness, a pattern similar to the emerging in mutualistic networks. Our study is the first integrated analysis of the structural patterns in anuran–prey antagonistic interaction networks in different parts of the world. We suggest that different processes, mediated mainly by latitude, are modeling the architecture of anuran–prey networks across the globe.     

Seed‐swallowing Toucans are Less Effective Dispersers of Guettarda viburnoides (Rubiaceae) than Pulp‐feeding Jays

For many tropical plants, birds are the most important seed dispersers. Not all birds, however, will provide equally effective dispersal services. Behavioral differences, during and after feeding, can result in different establishment probabilities of new individuals. During 3 yr, we examined species‐specific quantitative and qualitative aspects of Guettarda viburnoides seed dispersal by avian frugivores, focusing on how these aspects modify seed dispersal effectiveness. Fruits of G. viburnoides were consumed by ten species of birds, two of which, Cyanocorax cyanomelas and Pteroglossus castanotis, removed 80 percent of the fruits. These two species differ in qualitative aspects of seed dispersal. First, they select for fruits of different sizes; C. cyanomelas feeds on larger fruits than P. castanotis, which results in the former dispersing larger endocarps than the latter. Second, they differ in their fruit handling treatment; C. cyanomelas are pulp consumers, whereas P. castanotis swallow the fruit whole, and are thus traditionally considered ‘legitimate’ dispersers. The probability of seedling emergence, the temporal pattern of emergence, the number of emerged seedlings per endocarp, and the probability of post‐dispersal seed predation differs between endocarps dispersed by C. cyanomelas and P. castanotis; endocarps dispersed by the former have higher emergence probabilities, higher number of seedlings, faster emergence times, and lower predation probabilities than those dispersed by the latter. Finally, these birds differ in their landscape patterns of endocarp deposition; C. cyanomelas disperses endocarps to habitats with higher recruitment probabilities. Ultimately, the pulp consumer C. cyanomelas is a more effective disperser of G. viburnoides than P. castanotis.     

Vertebrate‐mediated seed rain and artificial perches contribute to overcome seed dispersal limitation in a Mediterranean old field

Natural regeneration of vegetation is a frequent outcome of land abandonment, although the rate and diversity of such regeneration may be severely restricted by seed dispersal limitation, among other factors. In spite of this, studies aiming to quantify seed rain and test methods to enhance it, such as artificial perches, are still underrepresented in the Mediterranean. In our study, we quantified seed rain density and richness and tested the effects of artificial perches on such rain over a distance gradient on seven Mediterranean island old fields. In each of the seven sites, we positioned three sampling stations, each consisting of 1 seed trap under an artificial perch and 1 as a control on the ground, distributed at 30, 60, and 90 m from natural vegetation remnant. All traps received seeds, suggesting no overall dispersal limitation. Of the 11 seed species found, 10 were fleshy‐fruited and dispersed by vertebrates. Seed traps under perches received significantly higher seed rain of fleshy‐fruited species dispersed by birds, while ground traps received significantly more seeds of the species also dispersed by mammals, especially Rubus ulmifolius. The distance from the seed source was nonsignificant in all cases. Our study demonstrates the key role of vertebrate‐mediated seed dispersal services to overcome dispersal limitation in old fields, as well as the effective contribution of even small artificial perches in contrasting such limitation. The lack of differences over the distance gradient reveal that the upper spatial limit of dispersal limitation was not achieved.