Broad-scale gradients of resource utilization by phyllostomid bats in Atlantic Forest: patterns of dietary overlap, turnover and the efficacy of ecomorphological approaches.

Identifying mechanisms that promote coexistence at the local level is enigmatic for many organisms. Numerous studies have indirectly demonstrated that biotic interactions may not cause deterministic patterns reflective of the coexistence of interacting bat species. Nonetheless, demonstration of the partitioning of resources by phyllostomid bats by directly examining diet matrices may illuminate a mechanism of coexistence. I examined the dietary overlap of phyllostomid bats across 23 sites in the Atlantic Forest of South America. I also examined components of beta diversity (turnover and nestedness) of resources among species as well as the degree to which morphology can act as a surrogate for dietary similarity in each community. Bats exhibited high overlap. Nonetheless, dietary beta diversity was more related to turnover than nestedness of items suggesting substantive species-specific affinities. Niche breath and dietary overlap were positively related to the number of species and the number of resources consumed in communities. Accordingly, changes in richness across Atlantic Forest may be facilitated by increases in resources available at the community level. There were positive, yet weak relationships between morphological and dietary distance. The relationship between morphology and diet was invariant relative to geography, species richness, number of dietary resources, average diet breadth and average dietary overlap indicating that in the Atlantic Forest morphology is a consistent surrogate of dietary relationships of species. Atlantic Forest is one of the most anthropogenically modified tropical forests in the world. This in combination with distinct climatic seasonality likely causes higher dietary overlap, weaker ecomorphological relationships and persistence of only the most general bat species.

NeoBat Interactions: A data set of bat-plant interactions in the Neotropics.

Data papers and open databases have revolutionized contemporary science, as they provide the long-needed incentive to collaborate in large international teams and make natural history information widely available. Nevertheless, most data papers have focused on species occurrence or abundance, whereas interactions have received much less attention. To help fill this gap, we have compiled a georeferenced data set of interactions between 93 bat species of the family Phyllostomidae (Chiroptera) and 501 plant species of 68 families. Data came from 169 studies published between 1957 and 2007 covering the entire Neotropical Region, with most records from Brazil (34.5% of all study sites), Costa Rica (16%), and Mexico (14%). Our data set includes 2571 records of frugivory (75.1% of all records) and nectarivory (24.9%). The best represented bat genera are Artibeus (28% of all records), Carollia (24%), Sturnira (10.1%), and Glossophaga (8.8%). Carollia perspicillata (187), Artibeus lituratus (125), Artibeus jamaicensis (94), Glossophaga soricina (86), and Artibeus planirostris (74) were the bat species with the broadest diets recorded based on the number of plant species. Among the plants, the best represented families were Moraceae (17%), Piperaceae (15.4%), Urticaceae (9.2%), and Solanaceae (9%). Plants of the genera Cecropia (46), Ficus (42), Piper (40), Solanum (31), and Vismia (27) exhibited the largest number of interactions. These data are stored as arrays (records, sites, and studies) organized by logical keys and rich metadata, which helped to compile the information on different ecological and geographic scales, according to how they should be used. Our data set on bat-plant interactions is by far the most extensive, both in geographic and taxonomic terms, and includes abiotic information of study sites, as well as ecological information of plants and bats. It has already facilitated several studies and we hope it will stimulate novel analyses and syntheses, in addition to pointing out important gaps in knowledge. Data are provided under the Creative Commons Attribution 4.0 International License. Please cite this paper when the data are used in any kind of publication related to research, outreach, and teaching activities.

Relative contributions of ecological drift and selection on bat community structure in interior Atlantic Forest of Paraguay.

Despite extensive focus on numerous mechanisms that potentially structure Neotropical bat communities, understanding of the relative importance of any is still illusive. Recently, it has been demonstrated that all mechanisms used to explain community organization can be conceptualized as one or a combination of the few higher-level processes of dispersal, drift, selection and speciation. These four higher-level processes have not been addressed equally by Neotropical bat community ecologists. In particular, predictions formulated from a hypothesis of ecological drift have not been tested for any Neotropical bat community. Herein we contrast efficacy of predictions based on the higher-level processes of drift and selection in describing community structure of bats in the Atlantic Forest of eastern Paraguay. Predictions apply to species-environment interactions, patterns of trait variation and beta-diversity, predictability of dominant competitors and responses to seasonality. At best, there was inconsistent support for the operation of either drift or selection within this bat community. Selection, however, had more various forms of support including strong species-environment relationships, predictable patterns of dominant competitors and strong responses to seasonality. Despite stronger support for selection, a number of predictions of drift were supported as well. It is likely that a combination of both of these processes operates across the variable environments experienced in Atlantic Forest. Predictions of both processes are difficult to make operational. Support for drift often comes from failure to demonstrate a significant pattern and should not be considered strong support of a prediction. Similarly, many predictions of selection predict phenotypic patterns among species without specifying a particular trait. This is problematic because the phenotype is multifaceted and a lack of pattern in one measured trait might mask a strong pattern in some other unmeasured trait. Distilling mechanisms of community organization into four higher level processes is a substantial innovation in community ecology. Nonetheless, efforts need to be made to develop a suite of mutually exclusive and falsifiable predictions to facilitate future and more rapid understanding of community organization.

Insights into the assembly rules of a continent-wide multilayer network.

How are ecological systems assembled? Identifying common structural patterns within complex networks of interacting species has been a major challenge in ecology, but researchers have focused primarily on single interaction types aggregating in space or time. Here, we shed light on the assembly rules of a multilayer network formed by frugivory and nectarivory interactions between bats and plants in the Neotropics. By harnessing a conceptual framework known as the integrative hypothesis of specialization, our results suggest that phylogenetic constraints separate species into different layers and shape the network's modules. Then, the network shifts to a nested structure within its modules where interactions are mainly structured by geographic co-occurrence. Finally, organismal traits related to consuming fruits or nectar determine which bat species are central or peripheral to the network. Our results provide insights into how different processes contribute to the assemblage of ecological systems at different levels of organization, resulting in a compound network topology.

ATLANTIC BATS: a data set of bat communities from the Atlantic Forests of South America.

Bats are the second most diverse mammal order and they provide vital ecosystem functions (e.g., pollination, seed dispersal, and nutrient flux in caves) and services (e.g., crop pest suppression). Bats are also important vectors of infectious diseases, harboring more than 100 different virus types. In the present study, we compiled information on bat communities from the Atlantic Forests of South America, a species-rich biome that is highly threatened by habitat loss and fragmentation. The ATLANTIC BATS data set comprises 135 quantitative studies carried out in 205 sites, which cover most vegetation types of the tropical and subtropical Atlantic Forest: dense ombrophilous forest, mixed ombrophilous forest, semideciduous forest, deciduous forest, savanna, steppe, and open ombrophilous forest. The data set includes information on more than 90,000 captures of 98 bat species of eight families. Species richness averaged 12.1 per site, with a median value of 10 species (ranging from 1 to 53 species). Six species occurred in more than 50% of the communities: Artibeus lituratus, Carollia perspicillata, Sturnira lilium, Artibeus fimbriatus, Glossophaga soricina, and Platyrrhinus lineatus. The number of captures divided by sampling effort, a proxy for abundance, varied from 0.000001 to 0.77 individuals·h-1 ·m-2 (0.04 ± 0.007 individuals·h-1 ·m-2 ). Our data set reveals a hyper-dominance of eight species that together that comprise 80% of all captures: Platyrrhinus lineatus (2.3%), Molossus molossus (2.8%), Artibeus obscurus (3.4%), Artibeus planirostris (5.2%), Artibeus fimbriatus (7%), Sturnira lilium (14.5%), Carollia perspicillata (15.6%), and Artibeus lituratus (29.2%).

Threshold effect of habitat loss on bat richness in cerrado-forest landscapes.

Understanding how animal groups respond to contemporary habitat loss and fragmentation is essential for development of strategies for species conservation. Until now, there has been no consensus about how landscape degradation affects the diversity and distribution of Neotropical bats. Some studies demonstrate population declines and species loss in impacted areas, although the magnitude and generality of these effects on bat community structure are unclear. Empirical fragmentation thresholds predict an accentuated drop in biodiversity, and species richness in particular, when less than 30% of the original amount of habitat in the landscape remains. In this study, we tested whether bat species richness demonstrates this threshold response, based on 48 sites distributed across 12 landscapes with 9-88% remaining forest in Brazilian cerrado-forest formations. We also examined the degree to which abundance was similarly affected within four different feeding guilds. The threshold value for richness, below which bat diversity declines precipitously, was estimated at 47% of remaining forest. To verify if the response of bat abundance to habitat loss differed among feeding guilds, we used a model selection approach based on Akaike's information criterion. Models accounted for the amount of riparian forest, semideciduous forest, cerrado, tree plantations, secondary forest, and the total amount of forest in the landscape. We demonstrate a nonlinear effect of the contribution of tree plantations to frugivores, and a positive effect of the amount of cerrado to nectarivores and animalivores, the groups that responded most to decreases in amount of forest. We suggest that bat assemblages in interior Atlantic Forest and cerrado regions of southeastern Brazil are impoverished, since we found lower richness and abundance of different groups in landscapes with lower amounts of forest. The relatively higher threshold value of 47% suggests that bat communities have a relatively lower resistance to habitat degradation than other animal groups. Accordingly, conservation and restoration strategies should focus on increasing the amount of native vegetation of landscapes so as to enhance species richness of bats.

Taxonomic and Phylogenetic Determinants of Functional Composition of Bolivian Bat Assemblages.

Understanding diversity patterns and the potential mechanisms driving them is a fundamental goal in ecology. Examination of different dimensions of biodiversity can provide insights into the relative importance of different processes acting upon biotas to shape communities. Unfortunately, patterns of diversity are still poorly understood in hyper-diverse tropical countries. Here, we assess spatial variation of taxonomic, functional and phylogenetic diversity of bat assemblages in one of the least studied Neotropical countries, Bolivia, and determine whether changes in biodiversity are explained by the replacement of species or functional groups, or by differences in richness (i.e., gain or loss of species or functional groups). Further, we evaluate the contribution of phylogenetic and taxonomic changes in the resulting patterns of functional diversity of bats. Using well-sampled assemblages from published studies we examine noctilionoid bats at ten study sites across five ecoregions in Bolivia. Bat assemblages differed from each other in all dimensions of biodiversity considered; however, diversity patterns for each dimension were likely structured by different mechanisms. Within ecoregions, differences were largely explained by species richness, suggesting that the gain or loss of species or functional groups (as opposed to replacement) was driving dissimilarity patterns. Overall, our results suggest that whereas evolutionary processes (i.e., historical connection and dispersal routes across Bolivia) create a template of diversity patterns across the country, ecological mechanisms modify these templates, decoupling the observed patterns of functional, taxonomic and phylogenetic diversity in Bolivian bats. Our results suggests that elevation represents an important source of variability among diversity patterns for each dimension of diversity considered. Further, we found that neither phylogenetic nor taxonomic diversity can fully account for patterns of functional diversity, highlighting the need for examining different dimensions of biodiversity of bats in hyperdiverse ecosystems.

Phylogenetic community structure of North American desert bats: influence of environment at multiple spatial and taxonomic scales.

Numerous processes influence community structure. The relative importance of these processes is thought to vary with spatial, temporal and taxonomic scales: density-dependent interactions are thought to be most important at small scales; at intermediate scales, environmental conditions may be the most influential factor; and biogeographic processes are thought to be of greater importance at larger scales. Additionally, the stress-dominance hypothesis suggests that communities experiencing harsher environmental conditions will be predominantly structured by habitat filtering, whereas communities experiencing more favourable conditions will be structured predominantly by density-dependent interactions such as competition. The aim of this study was to investigate the influence of environmental factors on phylogenetic community structure (PCS) of North American desert bats at multiple spatial and taxonomic scales. We also examined whether the stress-dominance hypothesis is upheld in desert bats across an environmental gradient. Phylogenetic community structure metrics were calculated using species pools that differed in spatial (from all deserts to individual deserts) and taxonomic (all bat taxa, a single family and a single genus) scales. We calculated mean temperature, precipitation and seasonality for each site to determine whether environmental gradients were related to degree of community structure. At the largest spatial and taxonomic scales, communities were significantly phylogenetically clustered while degree of clustering decreased at the smallest spatial and taxonomic scales. Climatic data, particularly mean temperature and temperature seasonality, were important predictors of PCS at larger scales and under harsher conditions, but at smaller scales and in less stressful conditions there was a weaker relationship between PCS and climate. This suggests that North American deserts, while harsh, are not uniform in the challenges they present to the faunas residing in them. Overall, the relationship between PCS and climatic data at large spatial and taxonomic scales, and in harsher conditions, suggests the influence of habitat filtering has been important in North American desert bat community assembly and that other processes have been important at smaller scales.

Fragmentation of Atlantic forest has not affected gene flow of a widespread seed-dispersing bat.

Habitat loss and resultant fragmentation are major threats to biodiversity, particularly in tropical and subtropical ecosystems. It is increasingly urgent to understand fragmentation effects, which are often complex and vary across taxa, time and space. We determined whether recent fragmentation of Atlantic forest is causing population subdivision in a widespread and important Neotropical seed disperser: Artibeus lituratus (Chiroptera: Phyllostomidae). Genetic structure within highly fragmented forest in Paraguay was compared to that in mostly contiguous forest in neighbouring Misiones, Argentina. Further, observed genetic structure across the fragmented landscape was compared with expected levels of structure for similar time spans in realistic simulated landscapes under different degrees of reduction in gene flow. If fragmentation significantly reduced successful dispersal, greater population differentiation and stronger isolation by distance would be expected in the fragmented than in the continuous landscape, and genetic structure in the fragmented landscape should be similar to structure for simulated landscapes where dispersal had been substantially reduced. Instead, little genetic differentiation was observed, and no significant correlation was found between genetic and geographic distance in fragmented or continuous landscapes. Furthermore, comparison of empirical and simulated landscapes indicated empirical results were consistent with regular long-distance dispersal and high migration rates. Our results suggest maintenance of high gene flow for this relatively mobile and generalist species, which could be preventing or significantly delaying reduction in population connectivity in fragmented habitat. Our conclusions apply to A. lituratus in Interior Atlantic Forest, and do not contradict broad evidence that habitat fragmentation is contributing to extinction of populations and species, and poses a threat to biodiversity worldwide.

Rapid development and screening of microsatellite loci for Artibeus lituratus and their utility for six related species within Phyllostomidae.

Microsatellites are often the marker of choice for population genetic studies at intermediate spatial and temporal scales. Developing large numbers of markers has traditionally been technically difficult, and this has limited our ability to investigate evolutionary phenomena that emerge across short temporal scales. Moreover, few markers tend to successfully amplify across species boundaries. As rapid advancements in high-throughput sequencing make microsatellite development cost- and time-effective, new avenues for evolutionary, population genetic and chromosome linkage mapping research are emerging. We used a published PERL script and second-generation sequencing to rapidly and affordably develop microsatellite loci for a widespread phyllostomid bat, Artibeus lituratus, for which no markers were previously available. We used Roche FLX (Titanium) Genome Sequencing to randomly sequence ∼101 Mb (255,065 unique reads) of genomic DNA for A. lituratus, within which we discovered 30,100 microsatellite loci. We designed primers for 19,395 loci that contained suitable flanking regions. We ordered primers for 96 loci, 90 of which produced a single PCR product in A. lituratus. We genotyped 52 loci, and 45 were polymorphic in A. lituratus. We tested cross-species amplification for 96 loci in six additional phyllostomid species: A. planirostris, A. fimbriatus, A. phaeotis, Enchisthenes hartii, Sturnira lilium, and Carollia perspicillata. Cross-species amplification was successful for at least one species for 87 loci (A. fimbriatus), and in all species, at least 66 loci were amplified. These markers will not only facilitate future work on these seven species, but also illustrate the utility of this high-throughput method for development of primers across many species simultaneously.

Relative effects of time for speciation and tropical niche conservatism on the latitudinal diversity gradient of phyllostomid bats.

Determinants of contemporary patterns of diversity, particularly those spanning extensive latitudinal gradients, are some of the most intensely debated issues in ecology. Recently, focus has shifted from a contemporary environmental perspective to a historical one in an attempt to better understand the construction of latitudinal gradients. Although the vast majority of research on historical mechanisms has focused on tropical niche conservatism (TNC), other historical scenarios could produce similar latitudinal gradients. Herein, I formalize predictions to distinguish between two such historical processes--namely time for speciation (TFS) and TNC--and test relative support based on diversity gradients of New World bats. TFS and TNC are distinctly spatial and environmental mechanisms, respectively. Nonetheless, because of the way that environmental characteristics vary spatially, these two mechanisms are hard to distinguish. Evidence provided herein suggests that TNC has had a more important effect than TFS in determining diversity gradients of New World bats. Indeed, relative effects of different historical mechanisms, as well as relative effects of historical and contemporary environmental determinants, are probably context-dependent. Future research should move away from attempting to identify the mechanism with primacy and instead attempt to understand the particular contexts in which different mechanisms have greater influence on diversity gradients.

Elements of metacommunity structure of Paraguayan bats: multiple gradients require analysis of multiple ordination axes.

Techniques to evaluate elements of metacommunity structure (EMS; coherence, species turnover and range boundary clumping) have been available for several years. Such approaches are capable of determining which idealized pattern of species distribution best describes distributions in a metacommunity. Nonetheless, this approach rarely is employed and such aspects of metacommunity structure remain poorly understood. We expanded an extant method to better investigate metacommunity structure for systems that respond to multiple environmental gradients. We used data obtained from 26 sites throughout Paraguay as a model system to demonstrate application of this methodology. Using presence-absence data for bats, we evaluated coherence, species turnover and boundary clumping to distinguish among six idealized patterns of species distribution. Analyses were conducted for all bats as well as for each of three feeding ensembles (aerial insectivores, frugivores and molossid insectivores). For each group of bats, analyses were conducted separately for primary and secondary axes of ordination as defined by reciprocal averaging. The Paraguayan bat metacommunity evinced Clementsian distributions for primary and secondary ordination axes. Patterns of species distribution for aerial insectivores were dependent on ordination axis, showing Gleasonian distributions when ordinated according to the primary axis and Clementsian distributions when ordinated according to the secondary axis. Distribution patterns for frugivores and molossid insectivores were best described as random. Analysis of metacommunities using multiple ordination axes can provide a more complete picture of environmental variables that mold patterns of species distribution. Moreover, analysis of EMS along defined gradients (e.g., latitude, elevation and depth) or based on alternative ordination techniques may complement insights based on reciprocal averaging because the fundamental questions addressed in analyses are contingent on the ordination technique that is employed.

Geographical ecology of Paraguayan bats: spatial integration and metacommunity structure of interacting assemblages.

We examined the relative contributions of regional spatial characteristics and local environmental conditions in determining Paraguayan bat species composition. We used a suite of full and partial redundancy analyses to estimate four additive partitions of variance in bat species composition: (a) unexplained variation, (b) that explained purely by spatial characteristics, (c) that explained purely by local environmental conditions and (d) that explained jointly by space and environment. The spatial component to bat species composition was greater than the environmental component and both pure spatial and pure environmental characteristics accounted for significant amounts of variation in bat species composition. Results from variance decomposition suggest that the mass effects model describes metacommunity structure of Paraguayan bats better than species sorting or neutral models. Such mass effects may potentially be general for bats and could explain the inability of purely local factors to fully account for bat community organization. Mass effects also have substantial conservation implications because rescue effects may enhance the persistence of mobile species in fragmented landscapes with relatively few protected sites.