Neotropical Bat Species Research Articles

New records of hypopigmentation in two neotropical phyllostomid bat species with different roosting habits (Uroderma bilobatum, Glossophaga soricina)

AbstractHypopigmentation disorders were reported in several bat species roosting in dark and sheltered roosts, but comparable records from open foliage roosts are rare. Here, we present three observations of non-albinistic hypopigmentation in two neotropical bat species. One extensively hypopigmented individual of

Neotropical primary bat cell lines show restricted dengue virus replication.

Dengue is the most widespread arboviral disease affecting humans. Bats are recognized carriers of emerging viral zoonoses and have been proposed as dengue reservoirs, since RNA/NS1 and/or antiviral antibodies have been detected. Yet, experimental inoculation of Artibeus bats failed to show virus replication. This conflicting results prevent drawing further conclusions of whether bats sustain dengue infection. To test bat cellular permissivity to dengue infection, we established primary bat embryonic cells from diverse organs and tissues of Artibeus jamaicensis, Molossus sinaloae, and Desmodus rotundus. We observed a limited serotype-, organ-, and bat species- specific dengue susceptibility. Only some Molossus-derived primary cells sustained poorly initial Dengue serotype-1 replication, though it was latter absent. To elucidate if Molossus bats may play a role in dengue replication, ecological or in vivo experiments must be performed. Taken together our results show that Dengue did not replicate efficiently in cell lines derived from Neotropical bat species.

Reproductive pattern of the large fruit-eating bat, Artibeus amplus (Chiroptera: Phyllostomidae) in the Venezuelan Andes.

Bimodal polyestry is the most common reproductive pattern in tropical bats, and it consists in producing one offspring per female twice a year. Reproductive patterns are closely related to rainfall regimes, frequently occurring twice a year in tropical regions. The goal of our study was to determine the reproductive pattern of the large fruit-eating bat, Artibeus amplus Handley, 1987 in a cave in the Venezuelan Andes inhabited by a large, stable colony. Thus, in this study we describe for the first time this important biological aspect of this unknown Neotropical bat species through the examination of external reproductive characteristics of males (inguinal or scrotal testes) and females (pregnant, lactating, post-lactating), based on 211 individuals (120 males and 91 females) captured between September 2008 and August 2009, in Cueva del Parque Las Escaleras, Estado Táchira, Venezuela. During this period of monthly sampling for a full year, most males displayed large scrotal testes, averaging 10 mm maximum length. The examination of females indicated that although pregnancy was first observed in November 2008, it reached a maximum during January and February 2009. Although adult males with scrotal testes throughout the year could imply that females have more than one pregnancy, our results suggested a seasonally monoestrous reproductive pattern for A. amplus. This study represents the first report of reproductive pattern for this poorly-known Neotropical frugivorous species. The observed monoestrous reproductive pattern supports the existence of synchronization between precipitation and reproduction. This synchronization has been frequently observed in most species of fruit bats. In this study, Artibeus amplus presumably adjust the parturition to anticipate the rainy season, as a strategy that allows maintenance of offspring during high availability of fruits.

Multidimensionality of Chemical Information in Male Greater Sac-Winged Bats (Saccopteryx bilineata)

The complexity of social signals is thought to depend on the complexity of social systems, but evidence from wild animals is scarce. Here, we investigated the chemical information provided by individual male greater sac-winged bats (Saccopteryx bilineata), a small, long-lived neotropical bat species with a harem-polygynous mating system. We analysed the chemical fingerprints of wing-sac liquids that are displayed by males in front of females. Specifically, we tested if fingerprints of 45 males included information about age (adult, juvenile), year of sampling, and distance between colonies. We confirmed age-specific differences in male-specific substances, but show furthermore that chemical fingerprints correlate with year of collection and distance between colonies. Thus, the wing-sac chemistry of male S. bilineata conveys a multitude of information, which can potentially be used by conspecifics, especially by females to assess the status of potential mates. Our study provides evidence for a multidimensionality of chemical information in a free-ranging mammal with high social complexity.

Anthropogenic impacts on Costa Rican bat parasitism are sex specific.

While anthropogenic impacts on parasitism of wildlife are receiving growing attention, whether these impacts vary in a sex‐specific manner remains little explored. Differences between the sexes in the effect of parasites, linked to anthropogenic activity, could lead to uneven sex ratios and higher population endangerment. We sampled 1108 individual bats in 18 different sites across an agricultural mosaic landscape in southern Costa Rica to investigate the relationships between anthropogenic impacts (deforestation and reductions in host species richness) and bat fly ectoparasitism of 35 species of Neotropical bats. Although female and male bat assemblages were similar across the deforestation gradient, bat fly assemblages tracked their hosts closely only on female bats. We found that in female hosts, parasite abundance per bat decreased with increasing bat species richness, while in male hosts, parasite abundance increased. We hypothesize the differences in the parasite–disturbance relationship are due to differences in roosting behavior between the sexes. We report a sex‐specific parasite–disturbance relationship and argue that sex differences in anthropogenic impacts on wildlife parasitism could impact long‐term population health and survival.

Trophic similarity and coexistence of Carollia perspicillata and Sturnira lilium (Phyllostomidae), two sympatric fruit bats from the Brazilian Atlantic forest

AbstractThe objective of this study was to evaluate the relationship between availability and consumption of food for two species of Neotropical fruit bats

Cytogenetics and DNA barcoding of the Round-eared bats, Tonatia (Chiroptera: Phyllostomidae): a new karyotype for Tonatia bidens

There are two species of Neotropical Round-eared bats, Tonatia bidens Spix, 1823 and Tonatia saurophila Koopman & Williams, 1951, which present highly similar morphological characteristics that can lead to errors of identification. Specimens originally identified as T. bidens have recently been reclassified as T. saurophila, and the only karyotype documented previously for these species was 2n = 16, FN = 20. In the present study, specimens of Tonatia collected in the municipality of Barra do Garcas, in the Brazilian state of Mato Grosso, were analyzed morphologically, using conventional cytogenetic techniques (C-banding, Ag-NOR, and CMA3), and through sequences of the mitochondrial cytochrome c oxidase subunit I (COI) gene. In the specimens morphologically identified as T. bidens, the diploid number (2n) was 26, and the fundamental number (FN), 38, while in T. saurophila, 2n = 16 and FN = 20, which is the karyotype also described previously for T. bidens. The dendograms obtained with sequences of the COI marker resulted in the formation of two distinct groups between T. bidens and T. saurophila, consistent with the two species, with a high sequence divergence value (14.22%). Distinct clades were also observed between T. bidens and the other phyllostomines analyzed in this study, with T. bidens also close to Phyllostomus hastatus (14.18% of sequence divergence).

Unravelling the calls of discrete hunters: acoustic structure of echolocation calls of furipterid bats (Chiroptera, Furipteridae)

Detailed descriptions of echolocation calls for most of the Neotropical bat species have been published only recently. Yet, the available descriptions are from bats that emit high-intensity calls. The families of insectivorous bats that emit low-intensity calls, such as Furipteridae, are less frequently recorded by more traditional equipment; thus, there are no detailed descriptions of echolocation calls for these species. The family Furipteridae includes only two species of small insectivorous bats from Neotropics, the thumbless bat Furipterus horrens and the smoky bat Amorphochilus schnablii. The ecology, behaviour and even the natural history of both species are barely known. In order to contribute to the description of echolocation calls of Neotropical bat species and to the knowledge of these two poorly known species, here we describe in more detail the echolocation calls of furipterids. Thumbless bats were recorded from two colonies, one located in south-western Bahia, Brazil, and another located in the Amazon forest of Matoury, French Guyana, whereas the smoky bats were recorded in the Pacific coast of Arequipa, south-western Peru. Echolocation calls of both species were characterized by pulses of downward broadband frequency-modulated sweeps of short duration. Our results show that the ultrasound calls emitted by thumbless bats is one of the highest in frequency among Neotropical bats. This detailed characterization of furipterid calls and their distinct features, like very high frequencies and wide bandwidth, making it relatively easy to identify, aids in the inclusion of these species in acoustic surveys and monitoring.

Cambios recientes en la sistemática y taxonomía de murciélagos Neotropicales (Mammalia: Chiroptera)

Introduction: Conservation of biodiversity requires an accurate accounting of the entities (taxa) comprising that diversity, the species. In an ideal system, each entity would have a unique and unequivocal name that would integrate information from other disciplines within a universal concept to ease the communication. In spite of being a comparatively well-known group, the number of recognized species of Neotropical bats continues to increase each year, making the organization and management of this knowledge difficult for the non-taxonomist. Here, we review and detail the most recent proposals in regard to the taxonomy of Neotropical bats to make this information more easily accessible to the non-taxonomist. Methods: We used the list of species (and subspecies) recognized in the last edition of “Mammal Species of the World” (2005) as a starting point. From there, we gathered all relevant papers dealing with taxonomy of Neotropical bat species. We delimited the Neotropical region from the lowlands of tropical Mexico to Tierra del Fuego, including the Caribbean. We did not include fossil, extinct or unnamed species. Results: Since 2005, the number of taxonomic changes (Table 1) has resulted in a net increase of 75 species and eigth genera, with a regional diversity of 380 species in 98 genera (Table 2). This richness increase includes newly recognized taxa (split from previously valid genera or species, often listed as junior synonyms) as well as previously unknown species, discovered in the field or at museum collections (Figure 2). Whereas some genera have increased their species richness by almost 100%, the average increase is around two species per genus. Discussion: The use of molecular genetics in systematics research, with an emphasis on recognition of reciprocally monophyletic groups, has contributed the most to the increase in new names now recognized. Although these revisions may appear to the non-taxonomist as a sign of taxonomic instability, we emphasize that the goal of these studies is to facilitate the integration of genetic, morphological, and biogeographic data to improve our knowledge of these species. We anticipate that further advances will continue as we increase exploration and research, together with the use of multiple sources of taxonomic information. All these data should enhance confidence and support for these results, and hopefully a broader agreement among Neotropical bat researchers. Key words: taxonomic update, biodiversity, species, genera, nomenclature.

Frugivory is associated with low measures of plasma oxidative stress and high antioxidant concentration in free-ranging bats

Oxidative stress--an imbalance between reactive pro- and neutralising antioxidants--damages cell structures and impairs fitness-relevant traits such as longevity and reproduction. Theory predicts that feeding on diets with high antioxidant content such as fruits should reduce oxidative stress; however, there is no support of this idea in free-ranging mammals. Bats cover a large variety of ecological niches, and therefore, we asked if measures of oxidative stress are lower in species with fruit diets. We measured reactive oxygen metabolites (ROM) representing total pro-oxidants produced and antioxidants in the plasma of 33 Neotropical bat species. Species with a fruit diet showed the lowest level of ROM and the highest concentration of antioxidants, followed by omnivorous and animalivorous species. Potentially, frugivorous species ingest more antioxidants with food and thus are able to neutralise more pro-oxidants than species not feeding on fruits, resulting in an overall lower level of oxidative stress. We therefore showed for the first time that measures of oxidative stress vary according to diets in free-ranging mammals.

Wing morphology of Neotropical bats: a quantitative and qualitative analysis with implications for habitat use

Wing morphology has a direct influence on the flight manoeuvrability, agility, and speed of bats. Studies addressing the relationship between bat wing morphology and ecology are biased towards Old World species and few of them have addressed the ecologically rich Amazonian bat fauna. We quantitatively and qualitatively characterized the wing shape of 51 bat species found in the Brazilian Amazonia by measuring their aspect ratio (AR) and relative wing load (RWL). We found a high variability in wing shape: AR varied from 5.0862 (pygmy round-eared bat, Lophostoma brasiliense (Peters, 1866)) to 8.2774 (brown dog-faced bat, Molossus (Cynomops) paranus (Thomas, 1901)), while RWL varied from 20.0459 (spectral bat, Vampyrum spectrum (L., 1758)) to 55.3931 (Pallas’s mastiff, Molossus molossus (Pallas, 1766)). Insectivores had the largest variability, whereas frugivores and nectarivores had intermediate values with lower variability, indicating a higher flexibility in the use of space and resources. Our predictions on flight patterns are supported by capture and behavioural data from the literature, both of which point to the use of wing shape as a good proxy for habitat use and food partitioning among species. Our data are useful for integrative studies in ecology, physiology, behaviour, and evolution, and can contribute to a better understanding of the ecological interactions of Neotropical bat species.

Measures of the Constitutive Immune System Are Linked to Diet and Roosting Habits of Neotropical Bats

Ecological and social factors are central in the emergence and transmission of infectious diseases, thus bearing the potential for shaping a species’ immune functions. Although previous studies demonstrated a link between social factors and the cellular immune system for captive mammals, it is yet poorly understood how ecological factors are connected with the different branches of the immune system in wild populations. Here, we tested how variation in aspects of the constitutive cellular and humoral immune system of free ranging bats is associated with two ecological factors that likely influence the putative risk of species to become infected by parasites and pathogens: diet and shelter. We found that white blood cell counts of 24 syntopic Neotropical bat species varied with the species’ diet and body mass. Bats that included at least partially vertebrates in their diet exhibited the highest white blood cell counts, followed by phytophagous and insectivorous species, which is in agreement with the assumption that the immune system varies with the pathogen transmission risk of a trophic level. The soluble part of the constitutive immune response, assessed by an in vitro bacterial killing assay, decreased with increasing roost permanence. Our results suggest that the ecology is an important factor in the evolution of the immune system in bats and probably also other mammals.

Selective Eavesdropping Behaviour in Three Neotropical Bat Species

AbstractKnowledge of interspecies information transfer in mammals is scarce compared with other taxa. We investigated whether eavesdropping on echolocation calls of bats may be used by sympatric bats with similar feeding ecology. We performed playback experiments with three free‐ranging neotropical bat species, broadcasting search phase calls or feeding buzzes of conspecifics and heterospecifics belonging either to the same or to another bat family. Both the greater fishing batNoctilio leporinusand the lesser bulldog batNoctilio albiventris(Noctilionidae) reacted with repeated approaches in response to playbacks of search phase calls and feeding buzzes from conspecifics and also to congeneric feeding buzzes.Noctilio leporinusalso were attracted by search phase calls from its sister speciesN. albiventris. In contrast, the sac‐winged batSaccopteryx bilineata(Emballonuridae) did not react to any playback sequences presented. Our results support the existence of eavesdropping behaviour for both species ofNoctilio. We suggest that information transfer via eavesdropping may depend mainly on species‐specific traits, including foraging style and social behaviour (territoriality, group foraging), and on distribution and density of prey. Call design had only a minor influence on the reaction.

Sugar gustatory thresholds and sugar selection in two species of Neotropical nectar-eating bats

Nectar-feeding bats play an important role in natural communities acting as pollinators; however, the characteristics that affect their food selection are unclear. Here we explore the role that sugar gustatory thresholds and sugar concentration play on sugar selection of Glossophaga soricina and Leptonycteris yerbabuenae. We offered bats paired feeders containing sugar solutions of sucrose (S), glucose (G) or fructose (F) vs. pure water, and sucrose vs. 1:1 equicaloric solutions of glucose–fructose at 5, 15 and 35% (wt./vol.). To see the effect of sweetness on sugar selection, we habituated the bats with a diet containing either sucrose or hexoses and subsequently evaluated sugar preferences. Sugar thresholds were S<G,F for G. soricina and G<S<F for L. yerbabuenae. These thresholds did not match with sugar preferences when the bats fed on dilute nectars. L. yerbabuenae changed its sugar preferences with concentration while G. soricina did not. Finally, the bats consistently preferred the sugar they were habituated to. Our results suggest that bats become accustomed to the sugar found in the most abundant plants they use, and thus prefer the most common sugars included in their diet. This could confer an advantage by allowing them shifting sugar preferences on the most common food present in their environment.

Effects of anthropogenic disturbance and climate on patterns of bat fly parasitism.

Environmental conditions, including anthropogenic disturbance, can significantly alter host and parasite communities. Yet, our current knowledge is based mainly on endoparasites, while ectoparasites remain little studied. We studied the indirect effects of anthropogenic disturbance (human population density) and climate (temperature, precipitation and elevation) on abundance of highly host-specific bat flies in four Neotropical bat species across 43 localities in Venezuela. We formulated a set of 11 a priori hypotheses that included a combination of the two effectors and host species. Statistically, each of these hypotheses was represented by a zero-inflated negative binomial mixture model, allowing us to control for excess zeros in the data. The best model was selected using Akaike's information criteria. Fly abundance was affected by anthropogenic disturbance in Artibeus planirostris, Carollia perspicillata and Pteronotus parnellii, but not Desmodus rotundus. Climate affected fly abundance in all bat species, suggesting mediation of these effects via the host or by direct effects on flies. We conclude that human disturbance may play a role in shaping bat-bat fly interactions. Different processes could determine fly abundance in the different bat species.

Hematological Survey of Common Neotropical Bat Species from Costa Rica

Although bats are one of the largest groups within the class Mammalia and may carry several zoonotic diseases, basic information about their hematology is limited. In this study, hematocrit (Hct), total white blood cell counts (TWBC; leukocytes), and differential white blood cell counts (DWBC) of free-ranging Neotropical bats were quantified. Blood samples from 255 bats representing 26 species from the families of Emballonuridae (3 species; 33 individuals), Molossidae (2 species; 26 individuals), Mormoopidae (1 species; 1 individual), Phyllostomidae (18 species; 180 individuals), and Vespertilionidae (2 species; 15 individuals) were collected in a Caribbean lowland rainforest of Costa Rica. Hct was measured after centrifugation of microhematocrit capillaries, TWBCs were performed using the Unopette system and a hemocytometer, and DWBCs were performed on eosin methylene blue stained blood films. Hct of bats ranged between 51.8 +/- 0.7% for Phyllostomus discolor (n = 27) and 65.8 +/- 2.2% for Molossus sinaloae (n = 6). Bat species of the same taxonomic family had comparable TWBCs; these were lower for insectivorous emballonurid, molossid, and vespertilionid bat species than for mostly phytophagous phyllostomid bat species. However, Ectophylla alba (Phyllostomidae) exhibited exceptionally low TWBCs (836 +/- 166 /microl; n = 10); this was less than half of the TWBCs of all other bat species, which ranged from 1,714 +/- 297/microl for Molossus bondae (n = 20) to 7,339 +/- 1,503/microl for Trachops cirrhosus (n = 6). Species with higher TWBCs tended to have lower Hct values. Overall, blood cell morphology was similar to other mammalian species. A large number of polychromatophilic erythrocytes and differences in lymphocyte morphology were noted. This study provides important hematological values for Neotropical bat species and significantly expands the knowledge on basal physiological measurements of Chiroptera.

Neotropical bats: estimating species diversity with DNA barcodes.

DNA barcoding using the cytochrome c oxidase subunit 1 gene (COI) is frequently employed as an efficient method of species identification in animal life and may also be used to estimate species richness, particularly in understudied faunas. Despite numerous past demonstrations of the efficiency of this technique, few studies have attempted to employ DNA barcoding methodologies on a large geographic scale, particularly within tropical regions. In this study we survey current and potential species diversity using DNA barcodes with a collection of more than 9000 individuals from 163 species of Neotropical bats (order Chiroptera). This represents one of the largest surveys to employ this strategy on any animal group and is certainly the largest to date for land vertebrates. Our analysis documents the utility of this tool over great geographic distances and across extraordinarily diverse habitats. Among the 163 included species 98.8% possessed distinct sets of COI haplotypes making them easily recognizable at this locus. We detected only a single case of shared haplotypes. Intraspecific diversity in the region was high among currently recognized species (mean of 1.38%, range 0–11.79%) with respect to birds, though comparable to other bat assemblages. In 44 of 163 cases, well-supported, distinct intraspecific lineages were identified which may suggest the presence of cryptic species though mean and maximum intraspecific divergence were not good predictors of their presence. In all cases, intraspecific lineages require additional investigation using complementary molecular techniques and additional characters such as morphology and acoustic data. Our analysis provides strong support for the continued assembly of DNA barcoding libraries and ongoing taxonomic investigation of bats.

Cryptic Species? Patterns of Maternal and Paternal Gene Flow in Eight Neotropical Bats

Levels of sequence divergence at mitochondrial loci are frequently used in phylogeographic analysis and species delimitation though single marker systems cannot assess bi-parental gene flow. In this investigation I compare the phylogeographic patterns revealed through the maternally inherited mitochondrial COI region and the paternally inherited 7th intron region of the Dby gene on the Y-chromosome in eight common Neotropical bat species. These species are diverse and include members of two families from the feeding guilds of sanguivores, nectarivores, frugivores, carnivores and insectivores. In each case, the currently recognized taxon is comprised of distinct, substantially divergent intraspecific mitochondrial lineages suggesting cryptic species complexes. In Chrotopterus auritus, and Saccopteryx bilineata I observed congruent patterns of divergence in both genetic regions suggesting a cessation of gene flow between intraspecific groups. This evidence supports the existence of cryptic species complexes which meet the criteria of the genetic species concept. In Glossophaga soricina two intraspecific groups with largely sympatric South American ranges show evidence for incomplete lineage sorting or frequent hybridization while a third group with a Central American distribution appears to diverge congruently at both loci suggesting speciation. Within Desmodus rotundus and Trachops cirrhosus the paternally inherited region was monomorphic and thus does not support or refute the potential for cryptic speciation. In Uroderma bilobatum, Micronycteris megalotis and Platyrrhinus helleri the gene regions show conflicting patterns of divergence and I cannot exclude ongoing gene flow between intraspecific groups. This analysis provides a comprehensive comparison across taxa and employs both maternally and paternally inherited gene regions to validate patterns of gene flow. I present evidence for previously unrecognized species meeting the criteria of the genetic species concept but demonstrate that estimates of mitochondrial diversity alone do not accurately represent gene flow in these species and that contact/hybrid zones must be explored to evaluate reproductive isolation.

Folivory in the Giant Fruit-Eating BatArtibeus amplus(Phyllostomidae): A Non-Seasonal Phenomenon

Folivory has been reported in only five species of microbats, and described as a seasonal phenomenon. Bats feed on leaves by chewing a portion of leaf, extracting the liquid, and discarding the fibrous material. In the course of a study on the reproductive pattern of Artibeus amplus in the Venezuelan Andes, leaves were frequently observed in a cave used by this species as a roost. We took this opportunity to (1) identify the leaves consumed by this poorly known Neotropical bat species, and (2) test whether folivory is a temporal phenomenon, such as in other leaf-eating bat species. Artibeus amplus consumes the leaves of seven species of plants, and four of these were found in every month of the year during the study. We report for the first time: (1) folivory in A. amplus, (2) five plant species never reported before in the diet of a bat, and (3) folivory as a non-seasonal phenomenon.

Predictable timing of oestrus in the tropical bat Saccopteryx bilineata living in a Costa Rican rain forest

Abstract:Many tropical mammals reproduce seasonally, although the circum-equatorial climate is more stable and less seasonal than that of temperate zones. The mechanisms underlying seasonal reproduction in the tropics remain enigmatic. Female reproduction and its relation to environmental factors were investigated in the Neotropical bat species Saccopteryx bilineata. Colonies consist of year-round stable groups of several females that are defended each by an adult male. Females give birth to a single offspring each year and it is suggested that mating is restricted to November and December. In this study, it was asked whether females of a Costa Rican colony come into oestrus around the same time each year and whether oestrus times are synchronized. Oestrogen and progesterone metabolites were monitored from faeces between October and January in four years. Oestrus was identified in 32 females. In addition, climatic factors such as rainfall and temperature were monitored at the study site. Results indicate that (1) females exhibit monoestry, (2) oestrus dates cluster around the first half of December, (3) reproduction is strongly seasonal and highly predictable and (4) oestrus times are possibly influenced by long-term cues like photoperiod and short-term cues like sudden changes in rainfall and temperature.