Network and parasitological analyses reveal latitudinal gradient in bats-ectoparasitic fly interactions across the Neotropic.

Ecological interactions between parasites and their hosts play a fundamental role in evolutionary processes. Selection pressures are exerted on parasites and their hosts, usually resulting in high levels of specificity. Such is the case of ectoparasitic bat-flies, but how large-scale spatial gradients affect the dynamics of their interactions with their bat hosts is still unknown. In the present study, we investigated interaction patterns between bats and their ectoparasitic flies (Streblidae and Nycteribiidae), both presenting their peak of diversity in the Neotropical region, along a latitudinal gradient. Using network analyses and parasitic indices, grounded on the latitudinal diversity gradient pattern, we evaluated how spatial gradients affect species interactions and parasitic indices at the biogeopraphic scale, with increasing species richness in interaction networks closer to the tropics, leading to increases in network modularity, size, and specialization, and to a decrease in nesting and connectivity. We conducted a literature review, focusing on studies done in the Neotropical region, and own data. We obtained a bat richness of 97 species parasitized by 128 species of ectoparasitic flies, distributed into 57 interaction networks between latitudes 29° S and 19° N in the Neotropic. Network metrics and parasitic indices varied along the latitudinal gradient, with changes in the richness of bats and their ectoparasitic flies and in the structure of their interactions; network specialization, modularity, and connectance increase with latitude, while network size decreases with latitude. Regions closer to the equator had higher parasite loads. Our results show that interaction network metrics present a latitudinal gradient and that such interactions, when observed at a local scale, hide variations that only become perceptible at larger scales. In this way, ectoparasites such as bat flies are not only influenced by the ecology and biology of their hosts, but also by other environmental factors acting directly on their distribution and survival.

How aerial insectivore bats of different sizes respond to nightly temperature shifts.

Small, volant and nocturnal, bats face strong challenges to avoid heat loss. Among aerial insectivores, body mass varies by two orders of magnitude between the smallest and the largest species. At low temperatures, physiological constraints should be harsher for smaller bats, as they lose more heat through their body surface than larger species. So, temperature variations should lead to distinct behavioural responses by bats of different body masses. Also, because they feed on arthropods, dependent on ambient temperature, aerial insectivores should halt feeding at low temperatures. Using ultrasound detectors and temperature and humidity sensors, we investigated how aerial insectivores of the coldest region in austral Brazil respond to nightly temperature variations and compared those responses between guilds of distinct body masses. We predict that smaller bats reduce their activity faster than larger bats, but that foraging should reduce simultaneously in the two guilds, as they depend on ectothermic prey. Bat activity reduced significantly below 12 °C. Larger bats maintained their activity at temperatures where the activity of smaller bats had already halted. However, larger bats foraged mostly during the first half of the night, at higher temperatures than those chosen by smaller bats to forage. We associate these differential responses to the thermal convection process, which may increase prey availability at higher altitudes, where larger molossids are known to forage. Smaller species, mostly edge-space hunters, probably take advantage of less variable prey availability during the night, resulting in a more regular behavioural pattern of navigation and foraging.

Potential mammalian species for investigating the past connections between Amazonia and the Atlantic Forest.

Much evidence suggests that Amazonia and the Atlantic Forest were connected through at least three dispersion routes in the past: the Eastern route, the central route, and the Western route. However, few studies have assessed the use of these routes based on multiple species. Here we present a compilation of mammal species that potentially have dispersed between the two forest regions and which may serve to investigate these connections. We evaluate the present-day geographic distributions of mammals occurring in both Amazonia and the Atlantic Forest and the likely connective routes between these forests. We classified the species per habitat occupancy (strict forest specialists, species that prefer forest habitat, or generalists) and compiled the genetic data available for each species. We found 127 mammalian species presently occurring in both Amazonia and the Atlantic Forest for which, substantial genetic data was available. Hence, highlighting their potential for phylogeographic studies investigating the past connections between the two forests. Differently from what was previously proposed, the present-day geographic distribution of mammal species found in both Amazonia and the Atlantic Forest points to more species in the eastern portion of the dry diagonal (and adjoining forested habitats). The Central route was associated with the second most species. Although it remains to be seen how this present-day geography reflects the paleo dispersal routes, our results show the potential of using mammal species to investigate and bring new insights about the past connections between Amazonia and the Atlantic Forest.

Taxonomic and functional anuran beta diversity of a subtropical metacommunity respond differentially to environmental and spatial predictors.

Anurans exhibit limited dispersion ability and have physiological and behavioural characteristics that narrow their relationships with both environmental and spatial predictors. So, the relative contributions of environmental and spatial predictors in the patterns of taxonomic and functional anuran beta diversity were examined in a metacommunity of 33 ponds along the coast of south Brazil. We expected that neutral processes and, in particular, niche-based processes could have similar influence on the taxonomic and functional beta diversity patterns. Distance-based methods (db-RDA) with variation partitioning were conducted with abundance data to examine taxonomic and functional facets and components (total, turnover and nestedness) in relation to environmental and spatial predictors. Processes determining metacommunity structure differed between the components of beta diversity and among taxonomic and functional diversity. While taxonomic beta diversity was further accounted by both environmental and spatial predictors, functional beta diversity responded more strongly to spatial predictors. These two contrasting patterns were different to what we had predicted, suggesting that while there is a taxonomic turnover mediated by environmental filters, the spatial distance promotes the trait dissimilarity between sites. In addition, our data confirm that neutral and niche-based processes operate on anuran metacommunities even at short geographic scales. Our results reinforce the idea that studies aiming to evaluate the patterns of structure in metacommunities should include different facets of diversity so that better interpretations can be achieved.

Native and exotic seed dispersal by the stone marten (Martes foina): implications for the regeneration of a relict climactic forest in central Portugal.

The stone marten (Martes foina) is a carnivorous mammal that often consumes fleshy fruits, thus potentially promoting seed dispersion. The present study was developed in Bussaco National Forest, central Portugal, and aimed to assess the potential role of the stone marten in dispersing native and exotic plants in different forest landscape types. Seeds from stone marten scats and fleshy fruits were collected monthly and were thereafter identified and sowed in a nursery, following a randomized experimental setup. Plant emergence was monitored fortnightly. Generalized linear models were used to test for differences in time and success of emergence between seeds from scats and fruits of 3 native species (Rubus ulmifolius, Arbutus unedo and Celtis australis) and 1 exotic plant species with invasive behavior (Prunus laurocerasus). Fruit consumption by the stone martens significantly increased and accelerated the germination of the native R. ulmifolius but had no effect on the other 2 native species or on the invasive species. This suggested that stone martens contribute to gene flow and forest regeneration by dispersing native plant seeds. However, although the germination was not enhanced in the invasive species, the preference of stone martens for these fruits may potentially contribute to the proliferation of P. laurocerasus. Our study represents a contribution to better understanding the fauna and flora interactions, enabling for a more conscious and effective decision-making in forest management.

Updated distribution maps for neotropical bats in the superfamily Noctilionoidea.

The IUCN provides a spatial database for many species, including terrestrial mammals. This database includes shapefiles with taxonomic information and the extent of occurrence for each species, and has been used in hundreds of studies in ecology, biogeography and conservation. Here we provide updated distribution maps that comprise the extent of occurrence of the neotropical bat species in the superfamily Noctilionoidea (Mammalia: Chiroptera) after a thorough research of new records published between January 2008 and March 2018. The main motivation for this update was the inclusion of spatial and climatic variables in explaining the ecological and taxonomic diversity of noctilionoid bats. The core of the superfamily (246 species distributed in five families out of 250 species) occurs in the Neotropics and shows ecological diversity unparalleled among mammals. This clade also shows the only evolutionary shift towards higher speciation rates within the order Chiroptera. Updating the range maps for these bats resulted in the modification of maps of 94 species, and the creation of new maps for 37 species missing from the IUCN database. From the 94 modified maps, 55 species increased their latitudinal range and 38 increased their longitudinal range. These modifications did not change the overall extent of occurrence of the clade. Altogether, modified and new maps represent 53% of Noctilionoidea. No copyright or proprietary restrictions are associated with the use of this data set other than citation of this Data Paper.

Eating down the food chain: generalism is not an evolutionary dead end for herbivores.

The role of trophic specialisation in taxonomic diversification remains unclear. Plant specialists diversify faster than omnivores and animalivores, but at shorter macroevolutionary scales this pattern sometimes reverses. Here, we estimate the effect of diet diversification on speciation rates in noctilionoid bats, controlling for tree shape, rate heterogeneity and macroevolutionary regimes. We hypothesise that niche subdivision among herbivores positively relates to speciation rates, differing between macroevolutionary regimes. We found the rate at which new herbivorous lineages originate decreases as rates of diet evolution increase. Herbivores experience higher speciation rates, but generalist herbivores and predominantly herbivorous omnivores speciate faster than specialised herbivores, omnivores and animalivores. Generalised herbivory is not a dead end. We show that analysing ecological traits and diversification requires accounting for macroevolutionary regimes and within- and between-clade variation in evolutionary rates. Our approach overcomes the high false-positive rates of other methods and illuminates the roles of herbivory and specialisation in speciation.

Latitudinal diversity gradients in New World bats: are they a consequence of niche conservatism?

The increase in species diversity from the Poles to the Equator is a major biogeographic pattern, but the mechanisms underlying it remain obscure. Our aim is to contribute to their clarification by describing the latitudinal gradients in species richness and in evolutionary age of species of New World bats, and testing if those patterns may be explained by the niche conservatism hypothesis. Maps of species ranges were used to estimate species richness in a 100 x 100 km grid. Root distances in a molecular phylogeny were used as a proxy for the age of species, and the mean root distance of the species in each cell of the grid was estimated. Generalised additive models were used to relate latitude with both species richness and mean root distance. This was done for each of the three most specious bat families and for all Chiroptera combined. Species richness increases towards the Equator in the whole of the Chiroptera and in the Phyllostomidae and Molossidae, families that radiated in the tropics, but the opposite trend is observed in the Vespertilionidae, which has a presumed temperate origin. In the whole of the Chiroptera, and in the three main families, there were more basal species in the higher latitudes, and more derived species in tropical areas. In general, our results were not consistent with the predictions of niche conservatism. Tropical niche conservatism seems to keep bat clades of tropical origin from colonizing temperate zones, as they lack adaptations to survive cold winters, such as the capacity to hibernate. However, the lower diversity of Vespertilionidae in the Neotropics is better explained by competition with a diverse pre-existing community of bats than by niche conservatism.

Population structure of a cave-dwelling bat, Miniopterus schreibersii: does it reflect history and social organization?

Many colonial bat species make regional migrations, and the consequent gene flow may eliminate geographic genetic structure resulting from history of colonization. In this study, we verified that history and social organization have detectable impacts on the genetic structure of Miniopterus schreibersii, a cave-dwelling bat with high female philopatry. After studying all known nursing colonies in Portugal, we concluded that there is a significant geographic structure and that the overall pattern is similar for mitochondrial and nuclear DNA. Both pairwise Phi(ST) and F(ST) were significantly correlated with geographical distance, suggesting that isolation by distance is relevant for both mitochondrial and nuclear markers. However, structuring of mitochondrial DNA was much more marked than that of nuclear DNA, a consequence of the strong female philopatry and a bias for male-mediated gene flow. Wintering colonies were more genetically diverse than nursing colonies because the former receive individuals from distinct breeding populations. Haplotype diversity of the northern colonies, the more recent according to population expansion analyses, is only about half of that of the central and southern colonies. This is most likely a consequence of the colonization history of M. schreibersii, which presumably expanded northward from the south of the Iberian Peninsula or North Africa after the last glacial age.