Carollia Perspicillata Research Articles

Footprints of inhibition in the response of cortical delay-tuned neurons of bats

Responses of echo-delay-tuned neurons that encode target distance were investigated in the dorsal auditory cortex of anesthetized short-tailed fruit bats (Carollia perspicillata). This species echolocates using short downward frequency-modulated (FM) biosonar signals. In response to FM sweeps of increasing level, 60 out of 131 studied neurons (47%) displayed a "paradoxical latency shift," i.e., longer response latency to loud sounds and shorter latency to faint sounds. In addition, a disproportionately large number of neurons (80%) displayed nonmonotonic responses, i.e., weaker responses to loud sounds and stronger responses to faint sounds. We speculate that the observed paradoxical latency shift and nonmonotonic responses are extracellular footprints of inhibitory processes evoked by loud sounds and that they could represent a specialization for the processing of the emitted loud biosonar pulse. Supporting this idea is the fact that all studied neurons displayed strong response suppression when an artificial loud pulse and a faint echo were presented together at a nonoptimal delay. In 24 neurons, iontophoresis of bicuculline (an antagonist of A-type γ-aminobutyric acid receptors) did not remove inhibitory footprints but did increase the overall spike output, and in some cases it also modified the response bandwidth and shifted the neuron's "best delay." We suggest that inhibition could play a dual role in shaping delay tuning in different auditory stations. Below the cortex it participates in delay-tuning implementation and leaves a footprint that is measurable in cortical responses, while in the cortex it provides a substrate for an in situ control of neuronal selectivity.

Bat airway epithelial cells: a novel tool for the study of zoonotic viruses.

Bats have been increasingly recognized as reservoir of important zoonotic viruses. However, until now many attempts to isolate bat-borne viruses in cell culture have been unsuccessful. Further, experimental studies on reservoir host species have been limited by the difficulty of rearing these species. The epithelium of the respiratory tract plays a central role during airborne transmission, as it is the first tissue encountered by viral particles. Although several cell lines from bats were established recently, no well-characterized, selectively cultured airway epithelial cells were available so far. Here, primary cells and immortalized cell lines from bats of the two important suborders Yangochiroptera and Yinpterochiroptera, Carollia perspicillata (Seba's short-tailed bat) and Eidolon helvum (Straw-colored fruit bat), were successfully cultured under standardized conditions from both fresh and frozen organ specimens by cell outgrowth of organ explants and by the use of serum-free primary cell culture medium. Cells were immortalized to generate permanent cell lines. Cells were characterized for their epithelial properties such as expression of cytokeratin and tight junctions proteins and permissiveness for viral infection with Rift-Valley fever virus and vesicular stomatitis virus Indiana. These cells can serve as suitable models for the study of bat-borne viruses and complement cell culture models for virus infection in human airway epithelial cells.

Distance from the mainland is a selective pressure for Phyllostomidae bats: the case of Maracá-Jipioca Island in the northern coast of Brazil

Large islands near the mainland tend to have greater species richness than smaller or remote oceanic islands. This study aimed to compare the community of Phyllostomidae bats on the island of Maracá-Jipioca, in Amapá, northern Brazil, and on the adjacent mainland. We also compared the community in four vegetation types present in both areas. Sampling occurred during the wet and dry seasons of 2010 at 24 independent sampling points. We recorded 333 Phyllostomidae bats belonging to 19 species. Species richness did not differ between the island and mainland but was different among the vegetation types, with grassland being the poorest. Species composition and abundance were different between the island and mainland. This difference was significant for Carollia perspicillata and Phyllostomus elongatus, which were more abundant on the island and mainland, respectively. Artibeus concolor did not exhibit differences between the two areas but differed among the vegetation types, being more abundant in flooded forest. Our findings did reveal that isolation and distance act as selective pressures for Phyllostomidae bats.

High paracellular nutrient absorption in intact bats is associated with high paracellular permeability in perfused intestinal segments.

Water-soluble nutrients are absorbed by the small intestine via transcellular and paracellular mechanisms. Based on a few previous studies, the capacity for paracellular nutrient absorption seems greater in flying mammals than in nonflying mammals, but there has been little investigation of the mechanisms driving this difference. Therefore, we studied three species each of bats (Artibeus lituratus, Sturnira lilium and Carollia perspicillata) and nonflying mammals (Akodon montensis, Mus musculus and Rattus norvegicus). Using standard pharmacokinetic techniques in intact animals, we confirmed the greater paracellular nutrient absorption in the fliers, comparing one species in each group. Then we conducted in situ intestinal perfusions on individuals of all species. In both approaches, we measured the absorption of 3OMD-glucose, a nonmetabolizable glucose analog absorbed both paracellularly and transcellularly, as well as L-arabinose, which has no mediated transport. Fractional absorption of L-arabinose was three times higher in the bat (S. lilium: 1.2±0.24) than in the rodent (A. montensis: 0.35±0.04), whereas fractional absorption of 3OMD-glucose was complete in both species (1.46±0.4 and 0.97±0.12, respectively). In agreement, bats exhibited two to 12 times higher l-arabinose clearance per square centimeter nominal surface area than rodents in intestinal perfusions. Using L-arabinose, we estimated that the contribution of the paracellular pathway to total glucose absorption was higher in all three bats (109-137%) than in the rodents (13-39%). These findings contribute to an emerging picture that reliance on the paracellular pathway for nutrient absorption is much greater in bats relative to nonflying mammals and that this difference is driven by differences in intestinal permeability to nutrient-sized molecules.

Male courtship displays and vocal communication in the polygynous bat Carollia perspicillata

Male courtship behaviour towards choosy females often comprises elaborate displays that address multiple sensory channels. In bats, detailed quantitative descriptions of multimodal courtship displays are still fairly scarce, despite the taxon’s speciose nature. We studied male courtship behaviour in a polygynous Neotropical bat, Seba’s short-tailed fruit bat Carollia perspicillata, by monitoring harem males in a captive colony. Courting male C. perspicillata performed stereotypic tactile, visual and acoustic displays. A courtship sequence, directed at one female at a time, lasted up to 120 s. During courtship, males approached females by brachiating or flying, hovered in front of them, pursued them on the wing, sniffed them and repeatedly poked the females with one or both folded wings; the latter behaviour was the most conspicuous male courtship display. Immediately before copulation, males wrapped their wings around the females and bit their necks. As acoustic display, courting male C. perspicillata produced highly variable, monosyllabic courtship trills. The species’ vocal repertoire consisted of ten different social vocalisation types, three for benign interactions (courtship trills, wobbles, isolation calls), four for aggressive encounters (aggressive trills, down-sweeps, warbles, distress calls) and the remaining three for unknown behavioural contexts (V-shaped calls, flat down-sweeps, hooks). Courtship trills and aggressive trills were exclusively produced by males. We measured 245 courtship trills of five males and found statistical evidence for a strong individual signature which has the potential to facilitate female choice, mate recognition or neighbour–stranger recognition among male competitors.

Patterns of rDNA and telomeric sequences diversification: contribution to repetitive DNA organization in Phyllostomidae bats

Chromosomal organization and the evolution of genome architecture can be investigated by physical mapping of the genes for 45S and 5S ribosomal DNAs (rDNAs) and by the analysis of telomeric sequences. We studied 12 species of bats belonging to four subfamilies of the family Phyllostomidae in order to correlate patterns of distribution of heterochromatin and the multigene families for rDNA. The number of clusters for 45S gene ranged from one to three pairs, with exclusively location in autosomes, except for Carollia perspicillata that had in X chromosome. The 5S gene all the species studied had only one site located on an autosomal pair. In no species the 45S and 5S genes collocated. The fluorescence in situ hybridization (FISH) probe for telomeric sequences revealed fluorescence on all telomeres in all species, except in Carollia perspicillata. Non-telomeric sites in the pericentromeric region of the chromosomes were observed in most species, ranged from one to 12 pairs. Most interstitial telomeric sequences were coincident with heterochromatic regions. The results obtained in the present work indicate that different evolutionary mechanisms are acting in Phyllostomidae genome architecture, as well as the occurrence of Robertsonian fusion during the chromosomal evolution of bats without a loss of telomeric sequences. These data contribute to understanding the organization of multigene families and telomeric sequences on bat genome as well as the chromosomal evolutionary history of Phyllostomidae bats.

Directed seed dispersal of Piper by Carollia perspicillata and its effect on understory plant diversity and folivory

Directed dispersal occurs when seeds are differentially deposited to sites where offspring survivorship is higher than at randomly chosen sites. Traditionally, characteristics of the dispersal target sites that could increase survivorship of the dispersed plants are thought to be intrinsic to the sites. If directed dispersal is constant over extended periods of time, however, it is likely that nonrandom patterns of dispersal could modify the ecological characteristics of the target site in ways that could increase survivorship and fitness of the dispersed plants. Here we report patterns of Piper diversity (richness, equitability, and similarity) and Piper folivory within plots near natural or artificial roosts of Carollia perspicillata vs. similar plots without bat roosts. Plots with bat roosts, both natural and artificial, had significantly higher Piper species diversity. Additionally, we found that plots with a higher Piper species diversity showed less specialist folivory, higher generalist folivory, and lower total herbivore leaf damage than plots with low Piper diversity. Finally, plots with bat roosts also showed less specialist folivory, lower generalist folivory, and lower total folivory when compared to plots without roosts. We propose that long-lasting nonrandom patterns of seed dispersal can change the local ecological characteristics of target sites via changes in plant diversity, and that these changes are likely to reduce the local rates of folivory and, therefore, increase seed and adult plant survivorship.

Blurry topography for precise target-distance computations in the auditory cortex of echolocating bats

Echolocating bats use the time from biosonar pulse emission to the arrival of echo (defined as echo delay) to calculate the space depth of targets. In the dorsal auditory cortex of several species, neurons that encode increasing echo delays are organized rostrocaudally in a topographic arrangement defined as chronotopy. Precise chronotopy could be important for precise target-distance computations. Here we show that in the cortex of three echolocating bat species (Pteronotus quadridens, Pteronotus parnellii and Carollia perspicillata), chronotopy is not precise but blurry. In all three species, neurons throughout the chronotopic map are driven by short echo delays that indicate the presence of close targets and the robustness of map organization depends on the parameter of the receptive field used to characterize neuronal tuning. The timing of cortical responses (latency and duration) provides a binding code that could be important for assembling acoustic scenes using echo delay information from objects with different space depths.

Mother–offspring recognition in the bat Carollia perspicillata

Parental care is crucial for offspring survival in many taxa but its burden and costs are often not equally distributed between the sexes. In bats, the majority of parental care is provided by females, making examples of paternal support towards pups exceedingly rare. One exception to this general pattern seemed to be the polygynous Seba's short-tailed fruit bat Carollia perspicillata; two earlier studies suggested that paternal care occurs, i.e. that harem males prompt females to retrieve vocalizing pups. To corroborate this suggestion, we investigated the occurrence of maternal and paternal care in reaction to pup isolation calls in C. perspicillata. Acoustic measurements of 905 isolation calls from 17 pups revealed sufficient interindividual variation to encode an individual vocal signature. Correspondingly, mothers were capable of using this individual signature to discriminate between their own pups and age-matched pups from other females belonging to their colony. Maternal experience was positively correlated with the strength of response behaviour during playbacks. Thus, our results indicate that pup isolation calls were used to elicit maternal care and that mothers recognize their pups based on an individual signature in isolation calls. However, in contrast to the previous studies mentioned above, we found no evidence that harem males reacted to pup isolation calls by prompting the respective mothers to retrieve their vocalizing pups. Instead, our results demonstrate that harem males engaged in courtship activities that were unaffected by pup isolation calls.

New record, host and localities of bat mite of genusChirnyssoides (Acari, Sarcoptiformes, Sarcoptidae)

Chirnyssoides parasitizes the anterior and posterior edges of bat wing membranes. Possibly due to a lack of studies, its distribution is believed to be restricted to a few countries of Central and South America, but its actual range is probably wider. The purpose of this paper is to report the presence of Chirnyssoides amazonae on the bat Carollia perspicillata in the state of Rio de Janeiro, Brazil, and to present a checklist of hosts and localities for Chirnyssoides. Eleven females and 22 egg clusters of C. amazonae were collected from 11 individuals of C. perspicillata captured in Tinguá Biological Reserve using mist nets. Our search of the literature came up with 69 records of Chirnyssoides. There are reports of Chirnyssoides caparti, Chirnyssoides amazonae, Chirnyssoides brasiliensis and Chirnyssoides phyllostomus in Brazil. This paper reports the first record of Chirnyssoides amazonae in the state of Rio de Janeiro and the second in Brazil, indicating that their known distribution extends to the south. There are records of C. amazonae and C. surinamensis parasitizing C. perspicillata, but this is the first record of C. amazonae on C. perspicillata in Brazil.

Flight metabolism in relation to speed in Chiroptera: Testing the U-shape paradigm in the short-tailed fruit batCarollia perspicillata

Aerodynamic theory predicts that flight for fixed-wing aircraft requires more energy at low and high speeds compared with intermediate speeds, and this theory has often been extended to predict speed-dependent metabolic rates and optimal flight speeds for flying animals. However, the theoretical U-shaped flight power curve has not been robustly tested for Chiroptera, the only mammals capable of flapping flight. We examined the metabolic rate of seven Seba's short-tailed fruit bats (Carollia perspicillata) during unrestrained flight in a wind tunnel at air speeds from 1 to 7 m s(-1). Following intra-peritoneal administration of (13)C-labeled Na-bicarbonate, we measured the enrichment in (13)C of exhaled breath before and after flight. We converted fractional turnover of (13)C into metabolic rate and power, based on the assumption that bats oxidized glycogen during short flights. Power requirements of flight varied with air speed in a U-shaped manner in five out of seven individuals, whereas energy turnover was not related to air speed in two individuals. Power requirements of flight were close to values predicted by Pennycuick's aerodynamic model for minimum power speed, but differed for maximum range speed. The results of our experiment support the theoretical expectation of a U-shaped power curve for flight metabolism in a bat.

Inflammatory challenge increases measures of oxidative stress in a free-ranging, long-lived mammal

Oxidative stress - the imbalance between reactive oxygen species (ROS) and neutralising antioxidants - has been under debate as the main cause of ageing in aerobial organisms. The level of ROS should increase during infection as part of the activation of an immune response, leading to oxidative damage to proteins, lipids and DNA. Yet, it is unknown how long-lived organisms, especially mammals, cope with oxidative stress. Bats are known to carry a variety of zoonotic pathogens and at the same time are, despite their high mass-specific basal metabolic rate, unusually long lived, which may be partly the result of low oxidative damage of organs. Here, we asked whether an immune challenge causes oxidative stress in free-ranging bats, measuring two oxidative stress markers. We injected 20 short-tailed fruit bats (Carollia perspicillata) with bacterially derived lipopolysaccharide (LPS) and 20 individuals with phosphate-buffered saline solution (PBS) as a control. Individuals injected with LPS showed an immune reaction by increased white blood cell count after 24 h, whereas there was no significant change in leukocyte count in control animals. The biological antioxidant potential (BAP) remained the same in both groups, but reactive oxygen metabolites (ROMs) increased after treatment with LPS, indicating a significant increase in oxidative stress in animals when mounting an immune reaction toward the inflammatory challenge. Control individuals did not show a change in oxidative stress markers. We conclude that in a long-lived mammal, even high concentrations of antioxidants do not immediately neutralise free radicals produced during a cellular immune response. Thus, fighting an infection may lead to oxidative stress in bats.

Bat flies (Diptera: Streblidae, Nycteribiidae) and mites (Acari) associated with bats (Mammalia: Chiroptera) in a high-altitude region in southern Minas Gerais, Brazil

A total of 71 bat flies belonging to families Nycteribiidae and Streblidae, and 37 mites were collected on 12 species of bats (Phyllostomidae and Vespertilionidae) from the Chapada do Abanador (Minas Gerais, Brazil), between July 2009 and April 2010. Two new occurrences of ectoparasites were recorded on Histiotus velatus (bat fly Basilia producta) and on Carollia perspicillata (mite Parichoronyssus bakeri). Five new occurrences were recorded for the state of Minas Gerais, increasing the range for bat flies Anatrichobius passosi, Paraeuctenodes similis, Basilia juquiensis, Basilia producta and for mite Periglischrus vargasi. Moreover, two new species of mites were recorded for Brazil (P. bakeri and Macronyssus aff. leislerianus). With regard to infracommunities, the most frequent association was between Anastrebla modestini and Exastinion clovisi on bat Anoura geoffroyi. This study contributed to characterize the fauna of bat ectoparasites in representative but poorly-sampled environments of the Atlantic Forest, the campos de altitude (high altitude grasslands) and cloud forests of southern Minas Gerais.

First record of predation on the bat Carollia perspicillata by the false coral snake Oxyrhopus petolarius in the Atlantic Rainforest

Records of bats as prey of snakes are very few in the literature, but recent studies have shown that this predation doesn’t seem to be an unusual phenomenon. We present here the first record of predation on the bat Carollia perspicillata by the false coral snake Oxyrhopus petolarius in an Atlantic Rainforest area in the Northeastern Brazil.

Comunidade de morcegos (Mammalia, Chiroptera) no Refúgio de Vida Silvestre Mata do Junco, Sergipe, nordeste do Brasil

A ordem Chiroptera é a segunda maior em riqueza de mamíferos no Brasil e a Mata Atlântica é o bioma com o melhor estado de conhecimento para esse grupo. Em Sergipe, estudos sobre quirópteros ainda são escassos, sendo necessário ampliar as pesquisas com esses animais. O presente trabalho teve como objetivo realizar o inventário de morcegos do Refúgio de Vida Silvestre Mata do Junco (RVSMJ), segunda maior reserva de Mata Atlântica do estado de Sergipe. As coletas foram realizadas durante duas noites por mês, entre fevereiro de 2011 a fevereiro de 2012, exceto junho. Com um esforço de captura de 21.168 m².h foram registrados 189 indivíduos de duas famílias e 14 espécies. Destas, Artibeus planirostris, Chiroderma doriae, Myotis nigricans, Phyllostomus discolor, Trachops cirrhosus e Trinycteris nicefori correspondem a novas ocorrências para a localidade, sendo T. nicefori novo registro para o estado. Phyllostomidae foi a família com maior riqueza e abundância e A. lituratus (N = 67), Carollia perspicillata (N = 45) e Dermanura cinerea (N = 45) foram as espécies mais abundantes. Essas três espécies juntas representam 83,0% dos indivíduos capturados; sendo caracterizadas como generalistas no uso do habitat e dieta. Com relação às guildas alimentares, a maioria das espécies é frugívora (57,1%), devido a metodologia e existência de áreas agrícolas presentes no RVSMJ. O registro de novas espécies para a localidade, juntamente com os parâmetros obtidos de riqueza, abundância e guilda alimentar, contribuem para o aumento do conhecimento dos quirópteros em Sergipe e podem servir de base para estratégias de conservação e manejo dessa área.

Metapopulation in bats of Southern Brazil

The purpose was to show that displacements, promoters of genetic diversity in metapopulations, increase the probability of survival of bat species adapted to medium and long-distance flights. Samples were taken in four forest fragments, distributed in three municipalities in northern Paraná, and the maximum distance between the studied areas is 20 km. A monthly sampling was performed for each fragment, for the period of July 2008 to June 2009. We used eight nets for collection which remained open during the first four hours of the night, totalling 192 hours during a year of study. The marking occurred from October 2008 to March 2009 and was accomplished through the use of anodised metal rings of four different colours. One hundred and fifty individuals were banded and since the first capture, four displacements were recorded. After five months of collecting and marking, one Carollia perspicillata was found three km away. Two Artibeus lituratus were recorded about 20 km from the marking place: the first one after 22 months and the second one after 24 months. Additionally, one Platyrrhinus lineatus was captured at about 20 km, after 26 months. As they moved around over considerable distances and are not monogamous, they mate with females of other fragments, exchanging genes and reducing or even avoiding inbreeding. Thus, populations of bats have the ability to increase genetic diversity in metapopulations, provided by displacements between the forest fragments. Species that behave like this are not vulnerable to isolation.

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.

Effects of aversive experience on the behavior within a custom-made plus maze in the short-tailed fruit bat, Carollia perspicillata

Stress exposure evokes a variety of physiological and behavioral responses in an organism, enabling it to cope with stressful situations and changes in the environment. In a previous study, we found that subjecting individuals of Carollia perspicillata to a chronic immobilization stress paradigm resulted in a significant increase of fecal cortisol concentrations. In the present study, we investigated the influence of stress on the behavior of C. perspicillata, by adapting a commonly used behavioral paradigm for characterizing coping styles of animals (i.e., the elevated-plus maze) to bats. Adult bats were subjected 1 h/day to immobilization over a period of 10 days. On the subsequent day, the behavior of each animal was analyzed in a custom-made plus maze, consisting of four arms (two open and two enclosed ones) and designed 3D because of the bats' ability to fly. In this newly invented design, we compared the behaviors of stressed animals and controls. Changes in locomotor and exploratory behavior suggest two divergent adaptive behaviors in C. perspicillata following the chronic stress paradigm, possibly indicating different stress coping styles.

Bats (Chiroptera, Phyllostomidae) in the urbanized area in South of Brazil

The present study aimed to inventory of bats species present in an urban area, located within the main campus of the State University of Maringá, northwestern Paraná State, and to present data on the diet, reproduction, and activity times of the captured species. Collections were performed monthly, between September 2007 and August 2008, and 377 individuals were captured, belonging to four species from the Phyllostomidae family: Artibeus lituratus (90%), Platyrrhinus lineatus (6.4%), Sturnira lilium (2.4%), and Carollia perspicillata (1.3%). The types of fruit ingested consisted especially of Cecropiaceae, Moraceae, Myrtaceae, Piperaceae and Solanaceae. Among the captured exemplars, 51% were female and 49% male. No pregnant females of A. lituratus or males with descended testicles were captured in autumn, and the largest recorded numbers of these groups were verified in winter. With regard to lactating females, A. lituratus was sampled year-round, with predominance during the warmer season. In spite of the low species diversity, the campus area is used by frugivore species that are generalists and are able to feed and reproduce in urbanized areas. In order to increase that diversity, management programs should be implemented so that urbanization and Chiroptera diversity can coexist with lower risks and losses to ecosystems.

Independent evolution of functional MHC class II DRB genes in New World bat species

Genes of the major histocompatibility complex (MHC) play a pivotal role in the vertebrate immune system and are attractive markers for functional, fitness-related, genetic variation. Although bats (Chiroptera) represent the second largest mammalian order and are prone to various emerging infectious diseases, little is known about MHC evolution in bats. In the present study, we examined expressed MHC class II DRB sequences (exons 1 to 4) of New World bat species, Saccopteryx bilineata, Carollia perspicillata, Noctilio albiventris and Noctilio leporinus (only exon 2). We found a wide range of copy number variation of DRB loci with one locus detected in the genus Noctilio and up to ten functional loci observed in S. bilineata. Sequence variation between alleles of the same taxa was high with evidence for positive selection. We found statistical support for recombination or gene conversion events among sequences within the same but not between bat species. Phylogenetic relationships among DRB alleles provided strong evidence for independent evolution of the functional MHC class II DRB genes in the three investigated species, either by recent gene duplication, or homogenization of duplicated loci by frequent gene conversion events. Phylogenetic analysis of all available chiropteran DRB exon 2 sequences confirmed their monophyletic origin within families, but revealed a possible trans-species mode of evolution pattern in congeneric bat species, e.g. within the genera Noctilio and Myotis. This is the first study investigating phylogenetic relationships of MHC genes within bats and therefore contributes to a better understanding of MHC evolution in one of the most dominant mammalian order.