The missing part of seed dispersal networks: structure and robustness of bat-fruit interactions

Mutualistic networks are crucial to the maintenance of ecosystem services. Unfortunately, what we know about seed dispersal networks is based only on bird-fruit interactions. Therefore, we aimed at filling part of this gap by investigating bat-fruit networks. It is known from population studies that: (i) some bat species depend more on fruits than others, and (ii) that some specialized frugivorous bats prefer particular plant genera. We tested whether those preferences affected the structure and robustness of the whole network and the functional roles of species. Nine bat-fruit datasets from the literature were analyzed and all networks showed lower complementary specialization (H₂'' = 0.37±0.10, mean ± SD) and similar nestedness (NODF = 0.56±0.12) than pollination networks. All networks were modular (M = 0.32±0.07), and had on average four cohesive subgroups (modules) of tightly connected bats and plants. The composition of those modules followed the genus-genus associations observed at population level (Artibeus-Ficus, Carollia-Piper, and Sturnira-Solanum), although a few of those plant genera were dispersed also by other bats. Bat-fruit networks showed high robustness to simulated cumulative removals of both bats (R = 0.55±0.10) and plants (R = 0.68±0.09). Primary frugivores interacted with a larger proportion of the plants available and also occupied more central positions; furthermore, their extinction caused larger changes in network structure. We conclude that bat-fruit networks are highly cohesive and robust mutualistic systems, in which redundancy is high within modules, although modules are complementary to each other. Dietary specialization seems to be an important structuring factor that affects the topology, the guild structure and functional roles in bat-fruit networks.     

Bat-Fruit Interactions Are More Specialized in Shaded-Coffee Plantations than in Tropical Mountain Cloud Forest Fragments

Forest disturbance causes specialization of plant-frugivore networks and jeopardizes mutualistic interactions through reduction of ecological redundancy. To evaluate how simplification of a forest into an agroecosystem affects plant-disperser mutualistic interactions, we compared bat-fruit interaction indexes of specialization in tropical montane cloud forest fragments (TMCF) and shaded-coffee plantations (SCP). Bat-fruit interactions were surveyed by collection of bat fecal samples. Bat-fruit interactions were more specialized in SCP (mean H₂ '' = 0.55) compared to TMCF fragments (mean H₂ '' = 0.27), and were negatively correlated to bat abundance in SCP (R = -0.35). The number of shared plant species was higher in the TMCF fragments (mean = 1) compared to the SCP (mean = 0.51) and this was positively correlated to the abundance of frugivorous bats (R= 0.79). The higher specialization in SCP could be explained by lower bat abundance and lower diet overlap among bats. Coffee farmers and conservation policy makers must increase the proportion of land assigned to TMCF within agroecosystem landscapes in order to conserve frugivorous bats and their invaluable seed dispersal service.     

The restoration of tropical seed dispersal networks

Human activities have led to the loss of habitats and biodiversity in the Atlantic Rain Forest in Brazil. Ecological restoration aims to rebuild this biome and should include not only the reinstatement of species but also the reestablishment of complex ecological interactions and the ecological functions that they provide. One such function is seed dispersal, which is provided by the interactions between animal frugivores and plants. We studied seed dispersal networks in 3 different tropical forest sites restored 15, 25, and 57 years ago; temporal scales rarely observed in restoration studies. We investigated changes in network structure (nestedness, modularity, and network specialization) in these communities over restoration time. Although network size and the number of interactions increased with time since restoration, the networks were composed of generalist birds, and the large frugivores remained absent. Contrary to our expectations though, species richness was highest in the 25‐year‐old site, maybe due to the higher number of species used in the planting. Nestedness values were low in all 3 networks, but the highest nestedness was observed in the intermediate‐aged site. However, the oldest network was significantly modular and showed higher complementary specialization. These results suggest that 57 years after restoration, the complexity of mutualistic interactions in seed dispersal networks has increased, this enhancing ecosystem function in the Atlantic forest.     

Increasing modularity when downscaling networks from species to individuals

Downscaling networks from species to individuals is a useful approach to incorporate inter‐individual variation and to investigate whether topology of species‐based networks results from processes acting at the scale of individuals, such as foraging behaviour. Here, we analyzed pollen‐transport networks at two scales, i.e. pollinator species–plant species (sp–sp) and pollinator individuals–plant species (i–sp), and assessed whether modularity – a prevalent pattern in most pollination networks – is consistent across both scales. To test this we use three different algorithms developed for the calculation of modularity (unipartite, bipartite and weighted bipartite modularity) and compare the results obtained. Downscaling networks revealed a higher modular structure in i–sp networks than in sp–sp networks, regardless of the modular metric used. Using a null model approach, we show that modularity at the individual scale is originated by the existence of a high heterogeneity and specialization in the partition of pollen resources among conspecific individuals, a pattern which obviously cannot be observed at the species level. Modules in i–sp networks consisted of individuals sometimes neither taxonomically nor functionally related, but sharing common pollen resources at different moments of the flowering season. Interestingly, conspecific individuals may belong to different modules. Both plant and insect phenologies were important drivers of the modularity detected in individual‐based networks, even determining the topological roles of nodes in the networks. A temporal turnover of modules was identified, i.e. modules of individuals assembled and disassembled over time as species modify their foraging choices throughout the flowering season adjusting to ecological conditions. Downscaling from species to individual‐based networks is a promising approach to study the interplay among structural patterns and processes at different, but interdependent organizational levels.     

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.     

Availability of food resources and habitat structure shape the individual‐resource network of a Neotropical marsupial

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Seasonal dietary niche contraction in coexisting Neotropical frugivorous bats (Stenodermatinae)

Tropical dry forests are characterized by punctuated seasonal precipitation patterns that drive primary production and the availability of fruits, seeds, flowers, and insects throughout the year. In environments in which the quantity and quality of food resources varies seasonally, consumers should adjust their foraging behavior to maximize energy intake while minimizing overlap with competitors during periods of low food availability. Here, we investigated how the diets of frugivorous bats in tropical dry forests of NW Mexico varied in response to seasonal availability and how this affected dietary overlap of morphologically similar species. We performed stable isotope analyses to understand temporal and interspecific patterns of overall isotopic niche breadth, trophic position, and niche overlap in the diet of six frugivorous species of closely related New World leaf-nosed bats (family Phyllostomidae, subfamily Stenodermatinae). We estimated seasonal changes in resource abundance in two complementary ways: (a) vegetative phenology based on long-term remote sensing data and (b) observational data on food availability from previously published insect and plant fruiting surveys. In all species, there was a consistent pattern of reduced isotopic niche breadth during periods of low food availability. However, patterns of niche overlap varied between morphologically similar species. Overall, results from our study and others suggest that seasonal food availability likely determines overall dietary niche breadth in Phyllostomidae and that despite morphological specialization, it is likely that other mechanisms, such as opportunistic foraging and spatiotemporal niche segregation, may play a role in maintaining coexistence rather than simply dietary displacement.     

Keystone species in seed dispersal networks are mainly determined by dietary specialization

A central issue in ecology is the definition and identification of keystone species, i.e. species that are relatively more important than others for maintaining community structure and ecosystem functioning. Network theory has been pointed out as a robust theoretical framework to enhance the operationality of the keystone species concept. We used the concept of centrality as a proxy for a species’ relative importance for the structure of seed dispersal networks composed of either frugivorous bats or birds and their food‐plants. Centrality was expected to be determined mainly by dietary specialization, but also by body mass and geographic range size. Across 15 Neotropical datasets, only specialized frugivore species reached the highest values of centrality. Furthermore, the centrality of specialized frugivores varied widely within and among networks, whereas that of secondary and opportunistic frugivores was consistently low. A mixed‐effects model showed that centrality was best explained by dietary specialization, but not by body mass or range size. Furthermore, the relationship between centrality and those three ecological correlates differed between bat– and bird–fruit networks. Our findings suggest that dietary specialization is key to understand what makes a frugivore species a keystone in seed dispersal networks, and that taxonomic identity also plays a significant role. Specialized frugivores may play a central role in network structuring and ecosystem functioning, which has important implications for conservation and restoration.     

Evaluating the Spatio-Temporal Factors that Structure Network Parameters of Plant-Herbivore Interactions

Despite the dynamic nature of ecological interactions, most studies on species networks offer static representations of their structure, constraining our understanding of the ecological mechanisms involved in their spatio-temporal stability. This is the first study to evaluate plant-herbivore interaction networks on a small spatio-temporal scale. Specifically, we simultaneously assessed the effect of host plant availability, habitat complexity and seasonality on the structure of plant-herbivore networks in a coastal tropical ecosystem. Our results revealed that changes in the host plant community resulting from seasonality and habitat structure are reflected not only in the herbivore community, but also in the emergent properties (network parameters) of the plant-herbivore interaction network such as connectance, selectiveness and modularity. Habitat conditions and periods that are most stressful favored the presence of less selective and susceptible herbivore species, resulting in increased connectance within networks. In contrast, the high degree of selectivennes (i.e. interaction specialization) and modularity of the networks under less stressful conditions was promoted by the diversification in resource use by herbivores. By analyzing networks at a small spatio-temporal scale we identified the ecological factors structuring this network such as habitat complexity and seasonality. Our research offers new evidence on the role of abiotic and biotic factors in the variation of the properties of species interaction networks.     

Modularity and specialization in bat–fly interaction networks are remarkably consistent across patches within urbanized landscapes and spatial scales

Patterns of specialization and the structure of interactions between bats and ectoparasitic flies have been studied mostly on non-urban environments and at local scales. Thus, how anthropogenic disturbances influence species interactions and network structure in this system remain poorly understood. Here, we investigated patterns of interaction between Phyllostomidae bats and ectoparasitic Streblidae flies, and variations in network specialization and structure across Cerrado patches within urbanized landscapes in Brazil and between local and regional scales. We found high similarity in the richness and composition of bat and fly species across communities, associated with low turnover of interactions between networks. The high specialization of bat–streblid interactions resulted in little connected and modular networks, with the emergence of modules containing subsets of species that interact exclusively or primarily with each other. Such similarities in species and interaction composition and network structure across communities and scales suggest that bat–fly interactions within Cerrado patches are little affected by the degree of human modification in the surrounding matrix. This remarkable consistency is likely promoted by specific behaviors, the tolerance of Phyllostomidae bats to surrounding urbanized landscapes as well as by the specificity of the streblid–bat interactions shaped over evolutionary time.     

Specialization Can Drive the Evolution of Modularity

Organismal development and many cell biological processes are organized in a modular fashion, where regulatory molecules form groups with many interactions within a group and few interactions between groups. Thus, the activity of elements within a module depends little on elements outside of it. Modularity facilitates the production of heritable variation and of evolutionary innovations. There is no consensus on how modularity might evolve, especially for modules in development. We show that modularity can increase in gene regulatory networks as a byproduct of specialization in gene activity. Such specialization occurs after gene regulatory networks are selected to produce new gene activity patterns that appear in a specific body structure or under a specific environmental condition. Modules that arise after specialization in gene activity comprise genes that show concerted changes in gene activities. This and other observations suggest that modularity evolves because it decreases interference between different groups of genes. Our work can explain the appearance and maintenance of modularity through a mechanism that is not contingent on environmental change. We also show how modularity can facilitate co-option, the utilization of existing gene activity to build new gene activity patterns, a frequent feature of evolutionary innovations.     

Opposed latitudinal patterns of network‐derived and dietary specialization in avian plant–frugivore interaction systems

Latitudinal patterns of biodiversity have been studied for centuries, but it is only during the last decades that species interaction networks have been used to examine the proposed latitudinal gradient of biotic specialization. These studies have given idiosyncratic results, which may either be because of genuine biological differences between systems, different concepts and scales used to quantify biotic specialization or because the methodological approaches used to compare interaction networks were inappropriate. Here we carefully examine the latitudinal specialization gradient using a global dataset of avian plant–frugivore assemblages and interaction networks. In particular, we test whether network‐derived specialization patterns differ from patterns based on assemblage‐level information on avian dietary preferences on specific food types. We found that network‐derived measures of specialization (complementary specialization H₂′ and < d’>, modularity Q) increased with latitude, i.e. frugivorous birds divide the niche of fruiting plants most finely at high latitudes where they also formed more modular interaction networks than at tropical latitudes. However, the strength and significance of the relationship between specialization metrics and latitude was influenced by the methodological approach. On the other hand, assemblage‐level information on avian specialization on fruit diet (i.e. the proportion of obligate frugivorous bird species feeding primarily on fruit) revealed an opposed latitudinal pattern as more bird species were specialized on fruit diet in tropical than in temperate assemblages. This difference in the latitudinal specialization gradient reflects that obligate frugivores require a high diversity of fruit plants, as observed in tropical systems, and fulfil more generalized roles in plant–frugivore networks than bird species feeding on different food types. Future research should focus on revealing the underlying ecological, historical and evolutionary mechanisms shaping these patterns. Our results highlight the necessity of comparing different scales of biotic specialization for a better understanding of geographical patterns of specialization in resource–consumer interactions.     

Individual variation in resource use by opossums leading to nested fruit consumption

Despite recent findings on the ecological relevance of within population diet variation far less attention has been devoted to the role diet variation for ecological services. Seed dispersal is a key ecological service, affecting plant fitness and regeneration based on foraging by fruit‐eating vertebrates. Here we used a network approach, widely used to understand how seed‐dispersal is organized at the species level, to gain insights into the patterns that emerge at the individual‐level. We studied the individual fruit consumption behavior of a South American didelphid Didelphis albiventris, during the cool–dry and warm–wet seasons. In species–species networks the heterogeneity in specialization levels generates patterns such as nestedness and asymmetry. Because generalist populations may be comprised of specialized individuals, we hypo thesized that network structural properties, such as nestedness, should also emerge at the individual level. We detected variation in fruit consumption that was not related to resource availability, ontogenetic or sexual factors or sampling biases. Such variation resulted in the structural patterns often found in species–species seed‐dispersal networks: low connectance, a high degree of nestedness and the absence of modules. Moreover structure varied between the warm–wet and cool–dry seasons, presumably as a consequence of seasonal fluctuation in fruit availability. Our findings suggest individuals may differ in selectivity causing asymmetries in seed dispersal efficiency within the population. In this sense the realized dispersal would differ from the expected dispersal estimated from their average dispersal potential. Additionally the results suggest possible frequency‐dependent effects on seed dispersal that might affect individual plant performance and plant community composition.     

Abiotic factors shape temporal variation in the structure of an ant–plant network

Despite recognition of key biotic processes in shaping the structure of biological communities, few empirical studies have explored the influences of abiotic factors on the structural properties of mutualistic networks. We tested whether temperature and precipitation contribute to temporal variation in the nestedness of mutualistic ant–plant networks. While maintaining their nested structure, nestedness increased with mean monthly precipitation and, particularly, with monthly temperature. Moreover, some species changed their role in network structure, shifting from peripheral to core species within the nested network. We could summarize that abiotic factors affect plant species in the vegetation (e.g., phenology), meaning presence/absence of food sources, consequently an increase/decrease of associations with ants, and finally, these variations to fluctuations in nestedness. While biotic factors are certainly important, greater attention needs to be given to abiotic factors as underlying determinants of the structures of ecological networks.     

Temporal variation in structural properties of tropical plant-herbivore networks: The role of climatic factors

Plant herbivore interactions can be influenced by abiotic factors such as climate or resource availability. Nevertheless, the influence of climatic variation on the temporal dynamics of plant-herbivore networks has been scarcely studied. In this study we evaluated the influence of temperature and precipitation on the structure and selectiveness of plant-herbivore networks associated to a seasonal tropical ecosystem in the Gulf of Mexico. Although a significant turnover was observed in plant and herbivore species across seasons, high modularity and selectivity of the networks remained relatively constant despite the temporal variation in climatic variables. However, precipitation and temperature was negatively associated with niche overlap for herbivores and positively related to evenness of network interactions. In other words, less stressful conditions are likely to promote the diversification in the use of resources by herbivores, and increase evenness of interactions in the network. An increase in niche overlap and a decrease in the evenness of interactions during the driest and coldest months could be promoted by the presence of less specialized herbivores when availability and quality of host resources is lower.We suggest that the constancy in network selectiveness and modularity facilitates the coexistence of species through the fine distribution of niches and the equitable distribution of food resources in periods of greater precipitation and temperature, when the availability of host plants is greater. Overall, we show for the first time how abiotic factors can influence the emergent structural properties of an antagonistic tropical plant-herbivore network.     

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.     

Bayesian hierarchical models suggest oldest known plant-visiting bat was omnivorous

The earliest record of plant visiting in bats dates to the Middle Miocene of La Venta, the world''s most diverse tropical palaeocommunity. Palynephyllum antimaster is known from molars that indicate nectarivory. Skull length, an important indicator of key traits such as body size, bite force and trophic specialization, remains unknown. We developed Bayesian models to infer skull length based on dental measurements. These models account for variation within and between species, variation between clades, and phylogenetic error structure. Models relating skull length to trophic level for nectarivorous bats were then used to infer the diet of the fossil. The skull length estimate for Palynephyllum places it among the larger lonchophylline bats. The inferred diet suggests Palynephyllum fed on nectar and insects, similar to its living relatives. Omnivory has persisted since the mid-Miocene. This is the first study to corroborate with fossil data that highly specialized nectarivory in bats requires an omnivorous transition.     

Seasonal differences in population‐, ensemble‐ and community‐level responses of bats to landscape structure in Amazonia

The amount (composition) and spatial arrangement (configuration) of forest patches in fragmented landscapes influence the accessibility, as well as the abundance and diversity of resources available to bats. Moreover, tropical fruit and insect abundance differ seasonally in response to changes in precipitation, and many bats in the family Phyllostomidae employ seasonal reproductive strategies. Because reproductive activities involve constraints on time and energy as well as increased nutritional demands, foraging behavior and home range size may differ between wet and dry seasons. Nonetheless, seasonal variation in response to landscape structure by bats has not been examined previously. Consequently, population‐, ensemble‐ and assemblage‐level responses of phyllostomids to landscape composition and configuration were quantified separately during the wet and dry season at three circular focal scales (1, 3 and 5 km radii) for 14 sites in fragmented lowland Amazon forest. Responses to landscape characteristics were scale‐dependent, species‐specific, and seasonal. Abundances of frugivores responded to landscape composition in the dry season and to landscape configuration in the wet season. Conversely, abundances of animalivores responded to landscape configuration in the dry season and to landscape composition in the wet season. Divergent responses to landscape structure between seasons suggest that variation in resource abundance and diversity play a significant role in structuring population‐, ensemble‐ and assemblage‐level patterns. As such, considerations of the effects of dietary flexibility and reproductive constraints on foraging strategies and habitat use may be important when designing management plans that successfully promote long‐term persistence of biodiversity in fragmented landscapes.     

Bat frugivory in two subtropical rain forests of Northern Argentina: Testing hypotheses of fruit selection in the Neotropics

Phyllostomid bats are prominent components of mammalian assemblages in the Neotropics. With many species specialized in frugivory, phyllostomids represent major partners of fleshy-fruited plants in the mutualism of seed dispersal. Here we present dietary data from two subtropical rainforests of Argentina, where fruit diversity is low and thus offer unique opportunities to test hypotheses of diet selection originally proposed for species-rich tropical assemblages. Particularly, we tested whether frugivorous phyllostomids exhibit pronounced dietary specialization in core plant taxa where fruit offer is greatly reduced as compared to tropical rainforests. We analyzed dietary overlap and niche breadth of subtropical frugivorous bats on the basis of >1000 dietary records plus >500 samples from a previous study in the region. We show that in the subtropics, frugivores from different genera remain faithful to their respective core plant taxa with few exceptions, rather than shifting toward alternative fruit resources available in the study sites. This supports predictions of specialization, which is confirmed to have a deep historical origin. The response of phyllostomid ensembles to restricted fruit diversity is at the level of species composition: absence of species for which preferred fruits do not occur in the sites. Taken together, these data lend strong support to hypotheses that explain coexistence of frugivorous phyllostomids on the basis of dietary specialization on core plant taxa with chiropterochorous fruits.