Genetic Diversity of Bartonella spp. in Cave-Dwelling Bats and Bat Flies, Costa Rica, 2018.

To determine Bartonella spp. dynamics, we sampled bats and bat flies across 15 roosts in Costa Rica. PCR indicated prevalence of 10.7% in bats and 29.0% in ectoparasite pools. Phylogenetic analysis of 8 sequences from bats and 5 from bat fly pools revealed 11 distinct genetic variants, including 2 potentially new genotypes.

The structure of tropical bat-plant interaction networks during an extreme El Niño-Southern Oscillation event.

Interaction network structure reflects the ecological mechanisms acting within biological communities, which are affected by environmental conditions. In tropical forests, higher precipitation usually increases fruit production, which may lead frugivores to increase specialization, resulting in more modular and less nested animal-plant networks. In these ecosystems, El Niño is a major driver of precipitation, but we still lack knowledge of how species interactions change under this influence. To understand bat-plant network structure during an extreme El Niño-Southern Oscillation event, we determined the links between plantivorous bat species and the plants they consume by DNA barcoding seeds and pulp in bat faeces. These interactions were recorded in the dry forest and rainforest of Costa Rica, during the dry and the wet seasons of an extreme El Niño year. From these we constructed seasonal and whole-year bat-plant networks and analysed their structures and dissimilarities. In general, networks had low nestedness, had high modularity, and were dominated by one large compartment which included most species and interactions. Contrary to our expectations, networks were less nested and more modular in drier conditions, both in the comparison between forest types and between seasons. We suggest that increased competition, when resources are scarce during drier seasons and habitats, lead to higher resource partitioning among bats and thus higher modularity. Moreover, we have found similar network structures between dry and rainforests during El Niño and non-El Niño years. Finally, most interaction dissimilarity among networks occurred due to interaction rewiring among species, potentially driven by seasonal changes in resource availability.

Tropical bat as mammalian model for skin carotenoid metabolism.

Animals cannot synthesize carotenoid pigments de novo, and must consume them in their diet. Most mammals, including humans, are indiscriminate accumulators of carotenoids but inefficiently distribute them to some tissues and organs, such as skin. This limits the potential capacity of these organisms to benefit from the antioxidant and immunostimulatory functions that carotenoids fulfill. Indeed, to date, no mammal has been known to have evolved physiological mechanisms to incorporate and deposit carotenoids in the skin or hair, and mammals have therefore been assumed to rely entirely on other pigments such as melanins to color their integument. Here we use high-performance liquid chromatography (HPLC) in combination with time-of-flight mass spectrometry (HPLC-TOF/MS) to show that the frugivorous Honduran white bat Ectophylla alba colors its skin bright yellow with the deposition of the xanthophyll lutein. The Honduran white bat is thus a mammalian model that may help developing strategies to improve the assimilation of lutein in humans to avoid macular degeneration. This represents a change of paradigm in animal physiology showing that some mammals actually have the capacity to accumulate dietary carotenoids in the integument. In addition, we have also discovered that the majority of the lutein in the skin of Honduran white bats is present in esterified form with fatty acids, thereby permitting longer-lasting coloration and suggesting bright color traits may have an overlooked role in the visual communication of bats.

Understory bat roosts, availability and occupation patterns in a Neotropical rainforest of Costa Rica.

The strong link between bats and their roosts is widely recognized as being particularly significant. Despite this, roosting ecology of bats is poorly understood and much of the basic information is still unknown. In this study, we investigated the availability and occupation patterns of four roost types (trees, caves, termite nests and tents) used by bats at Tirimbina Biological Reserve (TBR), Costa Rica. To accomplish our aim, we systematically surveyed both sides of established trails and transects, looking for understory roosts. Potential roosts were examined for bat presence in order to establish occupation. Roost availability and density were estimated using traveled distances (km) and inspected area (10 m for trees/caves and 15 m for tents/termite nests) of each trail or transect sampled. For the tent roosts, data on taxonomic information of plant modified, type of architecture, condition and construction achievement were also recorded. The area surveyed represented 45.4 % of the total area of the TBR (345 ha). Tents were the most common roost (56.6 % of all roosts, N = 223), followed by trees (24.4 %, N = 96), termite nests (18.8 %, N = 74) and caves (0.2 %, N = 1). We detected only 27 roosts occupied by bats (6.8 % of all roosts, 0.17 occupied roosts/ha). Caves showed the highest occupation rate (100 %, N = 1), followed by trees (17.7 %, N = 17), tents (3.6 %, N = 8) and termite nests (1.3 %, N = 1). We found the roosts for 10 species, representing 33.9 % of the bat fauna documented at the reserve (62 species). Density of roosts per bat species varied between 0.017-0.138 roosts/ha. Phyllostomidae was the best-represented family with Micronycteris microtis representing the most common species encountered. Four distinct tent architectures were documented. Bifid architecture was the most common (133 tents), followed by Conical (47 tents), Apical (27 tents) and Inverted Boat (16 tents). Most of the tents found were healthy (76.7 %, N = 171) and totally constructed (88.8 %, N = 198). Our study demonstrated that occupied bat roosts are difficult to find in the forest. When compared to the roost availability, the low occupation rates suggested that, at least in our study area, roosts might not be a limiting resource. Nevertheless, to confirm this hypothesis, information about fidelity and selection process of the species is fundamental for understanding to what extent these roosts meet the requirements to be inhabited or modified. Worldwide conservation efforts on bats should focus on understanding roosting ecology, especially due to anthropogenic pressures that are continuously reducing the availability of roosts, which undoubtedly contributes to the risk of extinction for specialized and sensitive species.

First evidence for multimodal animal seed dispersal in orchids.

Identifying the mechanisms for seed dispersal and persistence of species is a central aim of ecology. Seed dispersal by animals is an essential form of dissemination in many plant communities, including seeds of over 66% of neotropical canopy tree species.1,2 Besides physical dispersal, animals influence seed germination probabilities through scarification, breaking dormancy, and preventing rotting, so plants often invest important resources in attracting them. Orchids are predominantly adapted to wind dispersal, having dust-like seeds that are easily uplifted. Exceptions include bird-,3,4 cricket-,5,6 and mammal-dispersed7 species, featuring fleshy fruits with hard seeds that germinate after passing the animal's digestive system. Given the similarity in fruit and seed morphology, zoochory has also been suggested in Vanilla,8,9,10,11,12,13,14,15 a pantropical genus of 118 species with vine-like growth.16,17,18 We test this prediction through in situ and ex situ experimentation using fruits of Vanilla planifolia, and wild relatives, from which vanillin-a widely used natural aroma and flavoring-is obtained. Seeds from dehiscent fruits are removed by male Euglossini collecting fragrances, a unique case in plants, and female Meliponini bees gathering nest-building materials, a first among monocots. By contrast, mammals, mostly rodents, consume the nutritious indehiscent fruits, passing the seeds up to 18 h after consumption. Protocorm formation in digested and undigested seeds proves that scarification in the gut is not strictly required for germination. Multimodal seed dispersal mechanisms are proven for the first time in Orchidaceae, with ectozoochory and endozoochory playing crucial roles in the unusually broad distribution of Vanilla.

Systematics and diversification of the Ichthyomyini (Cricetidae, Sigmodontinae) revisited: evidence from molecular, morphological, and combined approaches.

Ichthyomyini, a morphologically distinctive group of Neotropical cricetid rodents, lacks an integrative study of its systematics and biogeography. Since this tribe is a crucial element of the Sigmodontinae, the most speciose subfamily of the Cricetidae, we conducted a study that includes most of its recognized diversity (five genera and 19 species distributed from southern Mexico to northern Bolivia). For this report we analyzed a combined matrix composed of four molecular markers (RBP3, GHR, RAG1, Cytb) and 56 morphological traits, the latter including 15 external, 14 cranial, 19 dental, five soft-anatomical and three postcranial features. A variety of results were obtained, some of which are inconsistent with the currently accepted classification and understanding of the tribe. Ichthyomyini is retrieved as monophyletic, and it is divided into two main clades that are here recognized as subtribes: one to contain the genus Anotomys and the other composed by the remaining genera. Neusticomys (as currently recognized) was found to consist of two well supported clades, one of which corresponds to the original concept of Daptomys. Accordingly, we propose the resurrection of the latter as a valid genus to include several species from low to middle elevations and restrict Neusticomys to several highland forms. Numerous other revisions are necessary to reconcile the alpha taxonomy of ichthyomyines with our phylogenetic results, including placement of the Cajas Plateau water rat (formerly Chibchanomys orcesi) in the genus Neusticomys (sensu stricto), and the recognition of at least two new species (one in Neusticomys, one in Daptomys). Additional work is necessary to confirm other unanticipated results, such as the non-monophyletic nature of Rheomys and the presence of a possible new genus and species from Peru. Our results also suggest that ichthyomyines are one of the main Andean radiations of sigmodontine cricetids, with an evolutionary history dating to the Late Miocene and subsequent cladogenesis during the Pleistocene.

Morphological Variation in the Wing Mite Periglischrus paracaligus (Acari: Spinturnicidae) Associated With Different Moving Strategies of the Host Leptonycteris yerbabuenae (Chiroptera: Phyllostomidae).

We evaluated the morphometric variation of wing mite Periglischrus paracaligus Herrin and Tipton, along with the distribution of their host Leptonycteris yerbabuenae Martinez and Villa, in Mexico. A total of 115 female and 96 male specimens of P. paracaligus were used to conduct linear and geometric morphometric analyses. We assessed the influence of the geographic distribution of the migratory and nonmigratory populations of its bat host species on changes in size and shape on these parasites. Both analyses revealed high intraspecific variation in P. paracaligus, but subtle geographic differentiation. None of the approaches used identified a consistent pattern that separates unambiguously migratory from nonmigratory populations. Females presented more phenotypic variation than males and UPGMA analyses showed southern and northern colonies grouped in two distinct clades. Males on the other hand showed randomly grouped colonies with no geographic concordance. Interestingly, the most differentiated colony was the north Pacific colony of Jalisco. For both, males and females, isolation by distance (IBD) was not observed. We discuss these results as a possible scenario of contact between migratory populations located in northern Mexico with nonmigratory populations in other localities in central and southern Mexico conforming to a panmictic population along with their distribution range.

Traveler Mites: Population Genetic Structure of the Wing Mites Periglischrus paracaligus (Acari: Mesostigmata: Spinturnicidae).

Wing mites of the genus Periglischrus are ectoparasites exclusively associated with phyllostomid bats. These mites show high host specificity and have been studied to understand the evolutionary history of their bat hosts mainly by using a morphological variation. Through a phylogeographic approach, we analyzed the genetic diversity and population genetic structure of the ectoparasite Periglischrus paracaligus Herrin and Tipton which parasitizes Leptonycteris yerbabuenae Martínez and Villa (lesser long-nosed bat) in Mexico. By the implementation of a multilocus approach, we found that P. paracaligus populations were diverse for haplotype diversity, and had values ranging from 0.5 to 1. No genetic structuring in the P. paracaligus parasites was observed along with the distribution of the host, L. yerbabuenae, in Mexico, nor when populations or regions were compared, but our results revealed a process of historical demographic expansion in all the analyzed markers. We discuss possible scenarios that could explain the lack of population structure in the light of the data analyzed for the parasites and the biology of L. yerbabuenae, such as the interplay between parasite and host traits being responsible for the genetic make-up of parasite populations. We also inferred its phylogenetic position among wing mites parasitizing the two other species of Leptonycteris bats. Long-nosed bats' monophyly helps to explain the observed presence of distinctive clades in the wing mite's phylogeny in specific association with each long-nosed bat host species.

Social behaviour and vocalizations of the tent-roosting Honduran white bat.

Bats are highly gregarious animals, displaying a large spectrum of social systems with different organizational structures. One important factor shaping sociality is group stability. To maintain group cohesion and stability, bats often rely on vocal communication. The Honduran white bat, Ectophylla alba, exhibits an unusual social structure compared to other tent-roosting species. This small white-furred bat lives in perennial stable mixed-sex groups. Tent construction requires several individuals and, as the only tent roosting species so far, involves both sexes. The bats´ social system and ecology render this species an interesting candidate to study social behaviour and vocal communication. In our study, we investigated the social behaviour and vocalizations of E. alba in the tent by observing two stable groups, including pups, in the wild. We documented 16 different behaviours, among others play and fur chewing, a behaviour presumably used for scent-marking. Moreover, we found 10 distinct social call types in addition to echolocation calls, and for seven call types we were able to identify the corresponding broad behavioural context. Most of the social call types were affiliative, including two types of contact calls, maternal directive calls, pup isolation calls and a call type related to the fur-chewing behaviour. In sum, this study entails an ethogram and describes the social vocalizations of a tent-roosting phyllostomid bat, providing the basis for further in-depth studies about the sociality and vocal communication in E. alba.

Socio-spatial organization reveals paternity and low kinship in the Honduran white bat (Ectophylla alba) in Costa Rica.

Ectophylla alba is a tent-making bat that roosts in mixed-sex clusters comprising adults and offspring. Our goal was to determine the genetic identity of individuals belonging to different roosting groups. We tested the hypothesis of kin selection as a major force structuring group composition. We used 9 microsatellites designed for E. alba to determine the genetic identity and probability of parentage of individuals. We analyzed parentage and kinship using the software ML-Relate, GenAIEx, and Cervus. The obtained relationship probabilities (0.5) revealed a clear maternal relationship between female adults and offspring with allele compatibility, and at least 5 relationships between male adults and pups. We found a low degree of relatedness within roosting groups. Between roosting groups at different sites, the mean probability of a half-sibling relationship ranged from 0.214 to 0.244 and, for full-sibling relationship, from 0.383 to 0.553. Genetically, adult individuals were poorly related within clusters, and kinship as an evolutionary force could not explain group membership.

Wing morphology predicts individual niche specialization in Pteronotus mesoamericanus (Mammalia: Chiroptera).

Morphological variation between individuals can increase niche segregation and decrease intraspecific competition when heterogeneous individuals explore their environment in different ways. Among bat species, wing shape correlates with flight maneuverability and habitat use, with species that possess broader wings typically foraging in more cluttered habitats. However, few studies have investigated the role of morphological variation in bats for niche partitioning at the individual level. To determine the relationship between wing shape and diet, we studied a population of the insectivorous bat species Pteronotus mesoamericanus in the dry forest of Costa Rica. Individual diet was resolved using DNA metabarcoding, and bat wing shape was assessed using geometric morphometric analysis. Inter-individual variation in wing shape showed a significant relationship with both dietary dissimilarity based on Bray-Curtis estimates, and nestedness derived from an ecological network. Individual bats with broader and more rounded wings were found to feed on a greater diversity of arthropods (less nested) in comparison to individuals with triangular and pointed wings (more nested). We conclude that individual variation in bat wing morphology can impact foraging efficiency leading to the observed overall patterns of diet specialization and differentiation within the population.

The masked seducers: Lek courtship behavior in the wrinkle-faced bat Centurio senex (Phyllostomidae).

Centurio senex is an iconic bat characterized by a facial morphology deviating far from all other New World Leaf Nosed Bats (Phyllostomidae). The species has a bizarrely wrinkled face and lacks the characteristic nose leaf. Throughout its distribution from Mexico to Northern South America the species is most of the time rarely captured and only scarce information on its behavior and natural history is available. Centurio senex is frugivorous and one of the few bats documented to consume also hard seeds. Interestingly, the species shows a distinct sexual dimorphism: Adult males have more pronounced facial wrinkles than females and a fold of skin under the chin that can be raised in style of a face mask. We report the first observations on echolocation and mating behavior of Centurio senex, including synchronized audio and video recordings from an aggregation of males in Costa Rica. Over a period of 6 weeks we located a total of 53 perches, where during the first half of the night males were hanging with raised facial masks at a mean height of 2.35 m. Most of the time, the males moved just their wing tips, and spontaneously vocalized in the ultrasound range. Approaches of other individuals resulted in the perching male beating its wings and emitting a very loud, low frequency whistling call. Following such an encounter we recorded a copulation event. The observed aggregation of adult C. senex males is consistent with lek courtship, a behavior described from only few other bat species.

The effect of local land use on aerial insectivorous bats (Chiroptera) within the two dominating crop types in the Northern-Caribbean lowlands of Costa Rica.

Land transformation into agricultural areas and the intensification of management practices represent two of the most devastating threats to biodiversity worldwide. Within this study, we investigated the effect of intensively managed agroecosystems on bat activity and species composition within two focal areas differing in landscape structure. We sampled bats via acoustic monitoring and insects with flight interception traps in banana and pineapple monoculture plantations and two nearby protected forested areas within the area of Sarapiquí, Costa Rica. Our results revealed that general occurrence and feeding activity of bats was higher above plantations compared to forested areas. We also recorded higher species richness at recording sites in plantations. This trend was especially strong within a fragmented landscape, with only four species recorded in forests, but 12 above pineapple plantations. Several bat species, however, occurred only once or twice above plantations, and forest specialist species such as Centronycteris centralis, Myotis riparius and Pteronotus mesoamericanus were only recorded at forest sites. Our results indicated, that mostly mobile open space and edge foraging bat species can use plantations as potential foraging habitat and might even take advantage of temporal insect outbreaks. However, forests are vital refugia for several species, including slower flying forest specialists, and thus a prerequisite to safeguard bat diversity within agricultural dominated landscapes.

Nocturnal scent in a 'bird-fig': A cue to attract bats as additional dispersers?

The plant genus Ficus is a keystone resource in tropical ecoystems. One of the unique features of figs is the diversity of fruit traits, which in many cases match their various dispersers, the so-called fruit syndromes. The classic example of this is the strong phenotypic differences found between figs with bat and bird dispersers (color, size, presentation, and scent). The 'bird-fig' Ficus colubrinae represents an exception to this trend since it attracts the small frugivorous bat species Ectophylla alba at night, but during the day it attracts bird visitors. Here we investigate day to night changes in fruit scent as a possible mechanism by which this 'bird-fig' could attract bats despite its fruit traits, which should appeal solely to birds. Analyses of odor bouquets from the bat- and bird-dispersal phases (i.e. day and night) differed significantly in their composition of volatiles. We observed a significant increase in relative amounts of sesquiterpene and aromatic compounds at night while relative amounts of two compounds of the fatty acid pathway were significantly higher during day. This finding raises the question whether Ficus colubrinae, a phenotypically classic 'bird-fig', might be able to attract bat dispersers by an olfactory signal at night. Preliminary observations from feeding experiments which indicate that Ectophylla alba is capable of finding ripe figs by scent alone point in this direction. However, additional behavioral experiments on whether bats prefer the 'night-bouquet' over the 'day-bouquet' will be needed to unequivocally answer this question.

Neotropical bats that co-habit with humans function as dead-end hosts for dengue virus.

Several studies have shown Dengue Virus (DENV) nucleic acids and/or antibodies present in Neotropical wildlife including bats, suggesting that some bat species may be susceptible to DENV infection. Here we aim to elucidate the role of house-roosting bats in the DENV transmission cycle. Bats were sampled in households located in high and low dengue incidence regions during rainy and dry seasons in Costa Rica. We captured 318 bats from 12 different species in 29 households. Necropsies were performed in 205 bats to analyze virus presence in heart, lung, spleen, liver, intestine, kidney, and brain tissue. Histopathology studies from all organs showed no significant findings of disease or infection. Sera were analyzed by PRNT90 for a seroprevalence of 21.2% (51/241), and by PCR for 8.8% (28/318) positive bats for DENV RNA. From these 28 bats, 11 intestine samples were analyzed by RT-PCR. Two intestines were DENV RNA positive for the same dengue serotype detected in blood. Viral isolation from all positive organs or blood was unsuccessful. Additionally, viral load analyses in positive blood samples by qRT-PCR showed virus concentrations under the minimal dose required for mosquito infection. Simultaneously, 651 mosquitoes were collected using EVS-CO2 traps and analyzed for DENV and feeding preferences (bat cytochrome b). Only three mosquitoes were found DENV positive and none was positive for bat cytochrome b. Our results suggest an accidental presence of DENV in bats probably caused from oral ingestion of infected mosquitoes. Phylogenetic analyses suggest also a spillover event from humans to bats. Therefore, we conclude that bats in these urban environments do not sustain DENV amplification, they do not have a role as reservoirs, but function as epidemiological dead end hosts for this virus.

[Diversity, natural history and conservation of mammals from San Vito de Coto Brus, Costa Rica]. / Diversidad, historia natural y conservación de los mamiferos de San Vito de Coto Brus, Costa Rica.

Although Costa Rica has been biologically well studied, few areas have complete mammal inventories, which are essential for ecological studies and conservation. The San Vito region is considered among the most important for scientific research in the country because of the presence of the Wilson Botanical Garden and Las Cruces. However, the knowledge of its mammalian fauna is incomplete. We extensively studied the mammals of San Vito, compiled a checklist, and evaluated its composition, relative abundance, habitat distribution, and conservation status. We recorded 105 species, representing 85 genera, 29 families, and 10 orders. Non-volant mammals represented 62 species, 59 genera, 23 families, and 9 orders. Bats belonged to 6 families, 26 genera and 43 species. The extensive deforestation and hunting have caused the extinction of seven species, but the region still supports, surprisingly, a relatively high number of species, most of which are rare. Few species are common and abundant. Species richness was higher in forest, and forest fragments; fewer species were found in coffee plantations, induced grasslands, and secondary vegetation. Around 21% (13 species) are included in the IUCN red book. Three species are considered endangered (Saimiri oerstedii, Tapirus bairdii, and Sylvilagus dicei), and two threatened (Myrmecophaga trydactila and Caluromys derbianus), of which two (T. bairdii and M. trydactila) are locally extinct. The other species in IUCN are either of low risk (i.e. Chironectes minimus) or data deficient (Lontra longicaudis). Additionally, 24 species (39%) are included in CITES.

Frugivorous bats maintain functional habitat connectivity in agricultural landscapes but rely strongly on natural forest fragments.

Anthropogenic changes in land use threaten biodiversity and ecosystem functioning by the conversion of natural habitat into agricultural mosaic landscapes, often with drastic consequences for the associated fauna. The first step in the development of efficient conservation plans is to understand movement of animals through complex habitat mosaics. Therefore, we studied ranging behavior and habitat use in Dermanura watsoni (Phyllostomidae), a frugivorous bat species that is a valuable seed disperser in degraded ecosystems. Radio-tracking of sixteen bats showed that the animals strongly rely on natural forest. Day roosts were exclusively located within mature forest fragments. Selection ratios showed that the bats foraged selectively within the available habitat and positively selected natural forest. However, larger daily ranges were associated with higher use of degraded habitats. Home range geometry and composition of focal foraging areas indicated that wider ranging bats performed directional foraging bouts from natural to degraded forest sites traversing the matrix over distances of up to three hundred meters. This behavior demonstrates the potential of frugivorous bats to functionally connect fragmented areas by providing ecosystem services between natural and degraded sites, and highlights the need for conservation of natural habitat patches within agricultural landscapes that meet the roosting requirements of bats.

Survey of wild mammal hosts of cutaneous leishmaniasis parasites in panamá and costa rica.

The eco-epidemiology of American cutaneous leishmaniasis (ACL) is driven by animal reservoir species that are a source of infection for sand flies that serve as vectors infecting humans with Leishmania spp parasites. The emergence and re-emergence of this disease across Latin America calls for further studies to identify reservoir species associated with enzootic transmission. Here, we present results from a survey of 52 individuals from 13 wild mammal species at endemic sites in Costa Rica and Panama where ACL mammal hosts have not been previously studied. For Leishmania spp. diagnostics we employed a novel PCR technique using blood samples collected on filter paper. We only found Leishmania spp parasites in one host, the two-toed sloth, Choloepus hoffmanni. Our findings add further support to the role of two-toed sloths as an important ACL reservoir in Central America.

The bats of Rio Grande do Norte state, northeastern Brazil / Morcegos do estado do Rio Grande do Norte, nordeste do Brasil

Abstract Rio Grande do Norte is one of the smallest states in Brazil but has a rich diversity of ecosystems, including Caatinga vegetation, remnants of Atlantic Forest, coastal habitats, mangroves and large karstic areas with caves. However, its chiropteran fauna is little known, and the state contains conspicuous gaps of information on the occurrence and distribution of bats in Brazil. In order to reduce this information gap, based on a review of scientific literature and regional mammal collections, we list 42 species of bats, including new occurrences for 13 species and discussion on their conservation status. Results show that more than half (54%) of the recorded species are phyllostomid bats, and about one third of the bats in the state roosts in underground cavities. The Caatinga harbored the highest bat richness in the state, including the occurrence of four vulnerable species (Furipterus horrens, Lonchorhina aurita, Natalus macrourus and Xeronycteris vieirai). The Atlantic Forest needs to be more sampled, including mangroves, coastal habitats and areas of Caatinga in the central region of the state (Borborema highlands), which are virtually unsurveyed. Although the recent increase of studies on bats in the state, future studies should complement conventional mistnetting with active roost search and bioacoustical records in order to obtain better data for unraveling the bat fauna of Rio Grande do Norte.

Resumo O Rio Grande do Norte é um dos menores estados do Brasil, mas possui grande diversidade de ecossistemas, incluindo vegetação de Caatinga, Mata Atlântica, habitats costeiros, manguezais e grandes áreas cársticas com cavernas. No entanto, a fauna de quirópteros é pouco conhecida, e o estado contém lacunas importantes sobre a ocorrência e distribuição de morcegos no Brasil. Para reduzir essa lacuna de informação, com base em uma revisão da literatura científica e coleções regionais de mamíferos, listamos 42 espécies de morcegos, incluindo novas ocorrências para 13 espécies e discusões sobre seu estado de conservação. Os resultados mostram que mais de metade (54%) das espécies registradas são morcegos filostomídeos e cerca de um terço dos morcegos no estado se abrigam em cavidades subterrâneas. A Caatinga abrigou a maior riqueza de morcegos no estado, incluindo a ocorrência de quatro espécies vulneráveis (Furipterus horrens, Lonchorhina aurita, Natalus macrourus e Xeronycteris vieirai). A Mata Atlântica precisa ser mais amostradas, incluindo manguezais, habitats costeiros e áreas de Caatinga principalmente na região central do estado (planalto da Borborema), que são virtualmente inexplorados. Embora o recente aumento das investigações no estado em relação aos morcegos, estudos futuros devem complementar os métodos convencionais de captura com procura ativa de abrigos e monitoramento bioacústico para obter melhores dados na tarefa de desvendar a diversidade de morcegos do Rio Grande do Norte.

Understory bat roosts, availability and occupation patterns in a Neotropical rainforest of Costa Rica / Refugios de murciélagos en el sotobosque, disponibilidad y patrones de ocupación en un bosque Neotropical lluvioso de Costa Rica

Abstract:The strong link between bats and their roosts is widely recognized as being particularly significant. Despite this, roosting ecology of bats is poorly understood and much of the basic information is still unknown. In this study, we investigated the availability and occupation patterns of four roost types (trees, caves, termite nests and tents) used by bats at Tirimbina Biological Reserve (TBR), Costa Rica. To accomplish our aim, we systematically surveyed both sides of established trails and transects, looking for understory roosts. Potential roosts were examined for bat presence in order to establish occupation. Roost availability and density were estimated using traveled distances (km) and inspected area (10 m for trees/caves and 15 m for tents/termite nests) of each trail or transect sampled. For the tent roosts, data on taxonomic information of plant modified, type of architecture, condition and construction achievement were also recorded. The area surveyed represented 45.4 % of the total area of the TBR (345 ha). Tents were the most common roost (56.6 % of all roosts, N = 223), followed by trees (24.4 %, N = 96), termite nests (18.8 %, N = 74) and caves (0.2 %, N = 1). We detected only 27 roosts occupied by bats (6.8 % of all roosts, 0.17 occupied roosts/ha). Caves showed the highest occupation rate (100 %, N = 1), followed by trees (17.7 %, N = 17), tents (3.6 %, N = 8) and termite nests (1.3 %, N = 1). We found the roosts for 10 species, representing 33.9 % of the bat fauna documented at the reserve (62 species). Density of roosts per bat species varied between 0.017-0.138 roosts/ha. Phyllostomidae was the best-represented family with Micronycteris microtis representing the most common species encountered. Four distinct tent architectures were documented. Bifid architecture was the most common (133 tents), followed by Conical (47 tents), Apical (27 tents) and Inverted Boat (16 tents). Most of the tents found were healthy (76.7 %, N = 171) and totally constructed (88.8 %, N = 198). Our study demonstrated that occupied bat roosts are difficult to find in the forest. When compared to the roost availability, the low occupation rates suggested that, at least in our study area, roosts might not be a limiting resource. Nevertheless, to confirm this hypothesis, information about fidelity and selection process of the species is fundamental for understanding to what extent these roosts meet the requirements to be inhabited or modified. Worldwide conservation efforts on bats should focus on understanding roosting ecology, especially due to anthropogenic pressures that are continuously reducing the availability of roosts, which undoubtedly contributes to the risk of extinction for specialized and sensitive species. Rev. Biol. Trop. 64 (3): 1333-1343. Epub 2016 September 01.

ResumenLa estrecha relación entre los murciélagos y sus refugios es ampliamente reconocida por ser de particular importancia. A pesar de esto, la ecología de los refugios en murciélagos es pobremente comprendida y gran parte de la información básica aún es desconocida. En este estudio, investigamos la disponibilidad y los patrones de ocupación de cuatro tipos de refugios (árboles, cuevas, termiteros y tiendas) utilizados por los murciélagos en la Reserva Biológica Tirimbina (RBT), Costa Rica. Para lograr nuestro objetivo, nosotros inspeccionamos sistemáticamente ambos lados de senderos establecidos y transectos, en busca de refugios a nivel del sotobosque. Los refugios potenciales fueron examinados en busca de murciélagos con el fin de establecer la ocupación de los mismos. La disponibilidad y densidad de los refugios fue estimada utilizando la distancia recorrida (km) y el área inspeccionada (10 m para árboles/cuevas y 15 m para tiendas/termiteros) de cada sendero o transecto muestreado. Para los refugios en tiendas, también se registraron datos sobre información taxonómica de la planta modificada, el tipo de arquitectura, la condición y la consecución de la construcción. El área inspeccionada representa el 45.4 % del área total de la RBT (345 ha). Las tiendas fueron el refugio más común (56.6 % de todos los refugios, N = 223), seguido por los árboles (24.4 %, N = 96), los termiteros (18.8 %, N = 74) y las cuevas (0.2 %, N = 1). Detectamos únicamente 27 refugios ocupados por murciélagos (6.8 % de todos los refugios, 0.17 refugios ocupados/ha). Las cuevas mostraron la tasa más alta de ocupación (100 %, N = 1), seguido por los árboles (17.7 %, N = 17), las tiendas (3.6 %, N = 8) y los termiteros (1.3 %, N = 1). Encontramos los refugios de 10 especies, lo que representa un 33.9 % de la fauna de murciélagos documentada en la reserva (62 especies). La densidad de refugios por especie de murciélago varió entre 0.017-0.138 refugios/ha. Phyllostomidae fue la familia mejor representada, con Micronycteris microtis como la especie más común encontrada en los refugios. Cuatro tipos de arquitectura fueron documentadas en las tiendas. La arquitectura Bífida fue la más común (133 tiendas), seguida por la Cónica (47 tiendas), la Apical (27 tiendas) y la Bote Invertido (16 tiendas). La mayoría de las tiendas encontradas se encontraban en buen estado (76.7 %, N = 171) y totalmente construidas (88.8 %, N = 198). Nuestro estudio demostró que encontrar refugios ocupados por murciélagos en el bosque es difícil. Cuando es comparada con la disponibilidad de refugios, la baja tasa de ocupación sugiere que, al menos en nuestra área de estudio, los refugios podrían no ser un recurso limitante. No obstante, para confirmar esta hipótesis, información acerca de la fidelidad y el proceso de selección de las especies es fundamental para comprender en que medida estos refugios cumplen con los requerimientos para ser habitados o modificados. A nivel mundial, los esfuerzos de conservación de los murciélagos deberían priorizar en comprender la ecología de los refugios, especialmente debido a que las presiones antropogénicas están continuamente reduciendo la disponibilidad de este recurso, lo cual sin duda alguna contribuye al riesgo de extinción para las especies más sensibles y especializadas.