Untargeted Metabolomics Reveals Fruit Secondary Metabolites Alter Bat Nutrient Absorption.

The ecological interaction between fleshy fruits and frugivores is influenced by diverse mixtures of secondary metabolites that naturally occur in the fruit pulp. Although some fruit secondary metabolites have a primary role in defending the pulp against antagonistic frugivores, these metabolites also potentially affect mutualistic interactions. The physiological impact of these secondary metabolites on mutualistic frugivores remains largely unexplored. Using a mutualistic fruit bat (Carollia perspicillata), we showed that ingesting four secondary metabolites commonly found in plant tissues affects bat foraging behavior and induces changes in the fecal metabolome. Our behavioral trials showed that the metabolites tested typically deter bats. Our metabolomic surveys suggest that secondary metabolites alter, either by increasing or decreasing, the absorption of essential macronutrients. These behavioral and physiological effects vary based on the specific identity and concentration of the metabolite tested. Our results also suggest that a portion of the secondary metabolites consumed is excreted by the bat intact or slightly modified. By identifying key shifts in the fecal metabolome of a mutualistic frugivore caused by secondary metabolite consumption, this study improves our understanding of the effects of fruit chemistry on frugivore physiology.

Differential distribution of inhibitory neuron types in subregions of claustrum and dorsal endopiriform nucleus of the short-tailed fruit bat.

Few brain regions have such wide-ranging inputs and outputs as the claustrum does, and fewer have posed equivalent challenges in defining their structural boundaries. We studied the distributions of three calcium-binding proteins-calretinin, parvalbumin, and calbindin-in the claustrum and dorsal endopiriform nucleus of the fruit bat, Carollia perspicillata. The proportionately large sizes of claustrum and dorsal endopiriform nucleus in Carollia brain afford unique access to these structures' intrinsic anatomy. Latexin immunoreactivity permits a separation of claustrum into core and shell subregions and an equivalent separation of dorsal endopiriform nucleus. Using latexin labeling, we found that the claustral shell in Carollia brain can be further subdivided into at least four distinct subregions. Calretinin and parvalbumin immunoreactivity reinforced the boundaries of the claustral core and its shell subregions with diametrically opposite distribution patterns. Calretinin, parvalbumin, and calbindin all colocalized with GAD67, indicating that these proteins label inhibitory neurons in both claustrum and dorsal endopiriform nucleus. Calretinin, however, also colocalized with latexin in a subset of neurons. Confocal microscopy revealed appositions that suggest synaptic contacts between cells labeled for each of the three calcium-binding proteins and latexin-immunoreactive somata in claustrum and dorsal endopiriform nucleus. Our results indicate significant subregional differences in the intrinsic inhibitory connectivity within and between claustrum and dorsal endopiriform nucleus. We conclude that the claustrum is structurally more complex than previously appreciated and that claustral and dorsal endopiriform nucleus subregions are differentially modulated by multiple inhibitory systems. These findings can also account for the excitability differences between claustrum and dorsal endopiriform nucleus described previously.

Cytoarchitecture of the medial nucleus of trapezoid body of three neotropical species of bats (Noctilio leporinus, Phyllostomus hastatus, and Carollia perspicillata) with different foraging behavior / Citoarquitetura do núcleo medial do corpo trapezoidal de três espécies neotropicais de morcegos (Noctilio leporinus, Phyllostomus hastatus e Carollia perspicillata) com diferentes comportamentos de forrageamento

Abstract The present study was taken to test the hypothesis that the medial nucleus of the trapezoid body (MNTB) of echolocating neotropical bats with different foraging behavior will exhibit morphological variations in relative size, degree of complexity and spatial distribution. The brains were collected from six male adult bats of each species: Noctilio leporinus (fish-eating), Phyllostomus hastatus (carnivorous/ omnivorous) and Carollia perspicillata (fruit-eating) and were double-embedded and transverse serial sections were cut and stained with cresyl fast violet. The results showed that the MNTB is well developed in all the bats in general and the mean length of the MNTB was 1160 ± 124 µm in N. leporinus, 400 ± 59 µm in P. hastatus and 320 ± 25µm in C. perspicillata. The body and brain weight do not reflect proportionately on the size of the MNTB in the present study. The hearing frequency spectrum did not covary with the size of the MNTB among the bats studied. The MNTB is clearly demarcated from the ventral nucleus of the trapezoid body (VNTB) only in P. hastatus. The MNTB comprised mainly three types of cells in all three bats: dense-staining multipolar cells (12.5 µm and 25.0 µm diameter); light-staining multipolar cells measuring (12.5 µm and 25.0 µm diameter) and light-staining round cells (5.0 µm diameter). The large sized MNTB was observed in N. leporinus, which suggests that it relies heavily on echolocation whereas P. hastatus and C. perspicillata use echolocation as well but also rely on hearing, smell and vision.

Resumo O presente estudo foi realizado para testar a hipótese de que o núcleo medial do corpo trapezoide (MNTB) de morcegos neotropicais ecolocativos com comportamento forrageiro diferente apresenta variações morfológicas no tamanho relativo, grau de complexidade e distribuição espacial. Os cérebros foram coletados de seis morcegos machos adultos de cada espécie, Noctilio leporinus (comedor de peixe), Phyllostomus hastatus (carnívoro/onívoro) e Carollia perspicillata (comedor de frutas), e foram seccionados em série e seções seriais transversais duplas e coradas com cresil violeta. Os resultados mostraram que o MNTB é bem desenvolvido em todos os morcegos em geral e que o comprimento médio do MNTB foi de 1.160 ± 124 µm em N. leporinus, 400 ± 59 µm em P. hastatus e 320 ± 25 µm em C. perspicillata. O peso corporal e cerebral não reflete proporcionalmente o tamanho do MNTB no presente estudo. O espectro da frequência auditiva não covaria com o tamanho do MNTB entre os morcegos estudados. O MNTB é claramente demarcado do núcleo ventral do corpo trapezoidal (VNTB) apenas em P. hastatus. O MNTB compreendia principalmente três tipos de células nos três morcegos: células multipolares de coloração densa (12,5 µm e 25,0 µm de diâmetro), células multipolares de coloração clara (12,5 µm e 25,0 µm de diâmetro) e células redondas manchadas de luz (5,0 µm de diâmetro). O MNTB de grande porte foi observado em N. leporinus, o que sugere que ele depende muito da ecolocalização, enquanto P. hastatus e C. perspicillata também usam a ecolocalização, mas dependem da audição, olfato e visão.

Mixed-species groups in bats: non-random roost associations and roost selection in neotropical understory bats.

BACKGROUND: Mixed-species groups in animals have been shown to confer antipredator, foraging and other benefits to their members that may provide selective advantages. In most cases, however, it is unclear whether functional benefits are a principal driver of heterospecific groups, or whether groups simply result from simultaneous exploitation of common resources. Mixed-species groups that form independently of environmental conditions may, however, evidence direct benefits of species associations. Bats are among the most gregarious mammals, with sometimes thousands of individuals of various species roosting communally. Despite numerous potential functional benefits of such mixed-species roosting groups, interspecific attraction has never been shown. To explore alternative explanations for mixed-species roosting, we studied roost selection in a speciose neotropical understory bat community in lowland rainforest in Costa Rica. Long term roost data were recorded over 10 years in a total of 133 roosts comprising both natural roosts and structurally uniform artificial roosts. We modelled bat roost occupancy and abundance in each roost type and in forest and pasture habitats to quantify the effects of roost- and environmental variability. RESULTS: We found that bat species presence in natural roosts is predictable from habitat and structural roost parameters, but that the presence and abundance of other bat species further modifies roost choice. One third of the 12 study species were found to actively associate with selected other bat species in roosts (e.g. Glossophaga commissarisi with Carollia sowelli). Other species did not engage in communal roosting, which in some cases indicates a role for negative interspecific interactions, such as roost competition. CONCLUSIONS: Mixed-species roosting may provide thermoregulatory benefits, reduce intraspecific competition and promote interspecific information transfer, and hence some heterospecific associations may be selected for in bats. Overall, our study contributes to an improved understanding of the array of factors that shape diverse tropical bat communities and drive the dynamics of heterospecific grouping in mammals more generally.

Diversity in olfactory receptor repertoires is associated with dietary specialization in a genus of frugivorous bat.

Mammalian olfactory receptor genes (ORs) are a diverse family of genes encoding proteins that directly interact with environmental chemical cues. ORs evolve via gene duplication in a birth-death fashion, neofunctionalizing and pseudogenizing over time. Olfaction is a primary sense used for food detection in plant-visiting bats, but the relationship between dietary specialization and OR repertoire diversity is unclear. Within neotropical Leaf-nosed bats (Phyllostomidae), many lineages are plant specialists, and some have a distinct OR repertoire compared to insectivorous species. Yet, whether specialization on particular plant genera is associated with the evolution of specialized, less diverse OR repertoires has never been tested. Using targeted sequence capture, we sequenced the OR repertoires of three sympatric species of short-tailed fruit bats (Carollia), which vary in their degree of specialization on the fruits of Piper plants. We characterized orthologous vs duplicated receptors among Carollia species, and explored the diversity and redundancy of the receptor gene repertoire. At the species level, the most dedicated Piper specialist, Carollia castanea, had lower OR diversity compared to the two generalists (C. sowelli and C. perspicillata), but we discovered a few unique sets of ORs within C. castanea with high redundancy of similar gene duplicates. These unique receptors potentially enable C. castanea to detect Piper fruit odorants better than its two congeners. Carollia perspicillata, the species with the most generalist diet, had a higher diversity of intact receptors, suggesting the ability to detect a wider range of odorant molecules. Variation among ORs may be a factor in the coexistence of these sympatric species, facilitating the exploitation of different plant resources. Our study sheds light on how gene duplication and changes in OR diversity may play a role in dietary adaptations and underlie ecological interactions between bats and plants.

Bats respond to simulated bacterial infection during the active phase by reducing food intake.

Sickness triggers a series of behavioral and physiological processes collectively known as acute phase response (APR). Bats are known as reservoirs of a broad variety of pathogens and the physiological changes resulting from APR activation have been tested predominantly during the resting phase (daytime) in several species exposed to lipopolysaccharide (LPS). In contrast, behavioral consequences of sickness for bats and other wild mammals have received less attention. We examined the physiological and behavioral consequences of APR activation in a fruit-eating bat (Carollia perspicillata) challenged with LPS during the active phase (nighttime). We measured changes in food intake, body mass, body temperature, total white blood cell counts, and the neutrophil/lymphocyte ratio (N/L). No fever and leukocytosis were observed in bats injected with LPS, but food intake decreased, bats lost body mass and their N/L ratio increased. The effect of LPS on daily energy balance is remarkable and, along with the increase in N/L ratio, it is assumed to be beneficial to fight disease. On the basis of our findings and those with other bats, it is probable that the physiological and behavioral components of the immune response to LPS follow circadian rhythms, but a formal test of this hypothesis is warranted.

Defensive fruit metabolites obstruct seed dispersal by altering bat behavior and physiology at multiple temporal scales.

The paradoxical presence of toxic chemical compounds in ripe fruits represents a balance between plant enemies and allies: chemical traits can defend seeds against antagonistic herbivores, seed predators, or fungal pathogens, but also can impose costs by repelling mutualistic seed dispersers, although the costs are often difficult to quantify. Seeds gain fitness benefits from traveling far from the parent plant, as they can escape from parental competition and elude specialized herbivores as well as pathogens that accumulate on adult plants. However, seeds are difficult to follow from their parent plant to their final destination. Thus, little is known about the factors that determine seed dispersal distance. We investigated this potential cost of fruit secondary compounds, reduced seed dispersal distance, by combining two data sets from previous work on a Neotropical bat-plant dispersal system (bats in the genus Carollia and plants in the genus Piper). We used data from captive behavioral experiments, which show how amides in ripe fruits of Piper decrease the retention time of seeds and alter food choices. With new analyses, we show that these defensive secondary compounds also delay the time of fruit removal. Next, with a behaviorally annotated bat telemetry data set, we quantified post-feeding movements (i.e., seed dispersal distances). Using generalized additive mixed models we found that seed dispersal distances varied nonlinearly with gut retention times as well as with the time of fruit removal. By interrogating the model predictions, we identified two novel mechanisms by which fruit secondary compounds can impose costs in terms of decreased seed dispersal distances: (1) small-scale reductions in gut retention time and (2) causing fruits to forgo advantageous bat activity peaks that confer high seed dispersal distances.

Experimental manipulation of reproductive tactics in Seba's short-tailed bats: consequences on sperm quality and oxidative status.

To reproduce, males have to fertilize the female's eggs, sometimes in competition with ejaculates of other males. In species where males display alternative reproductive tactics, whereby territorial males secure mating and non-territorial males have to sneak copulations, the latter might be expected to invest relatively more resources towards sperm quality compared with the territorial males. Sperm cells are especially vulnerable to oxidative stress, which reduces male fertility. Therefore, antioxidant resources are expected to modulate sperm quality, and might be allocated differently between reproductive tactics. To test the link between reproductive tactics, redox profile and sperm quality, we experimentally induced changes in the reproductive tactics of 39 captive males Seba's short-tailed bats Carollia perspicillata. We monitored the blood and ejaculate oxidative balance, and the sperm quality before, 7 days and 21 days after the manipulation of reproductive tactic. Although ejaculates' oxidative damage was negatively related to sperm velocity, males exhibited similar blood and ejaculates redox profiles and similar sperm quality, regardless of their reproductive tactic. Possibly, these results arise as a consequence of some constraints having been lifted during the experiment. Our results also suggest that, in Seba's short-tailed bats, the expression of alternative reproductive tactics is not subjected to strong oxidative constraints. Furthermore, our results could reflect an absence of trade-off between pre- and post-copulatory traits in harem males, as they could be selected to invest both in female attraction and sperm quality, as a consequence of their inability to fully monopolize females.

Can extreme MHC class I diversity be a feature of a wide geographic range? The example of Seba's short-tailed bat (Carollia perspicillata).

The major histocompatibility complex (MHC) is one of the most diverse genetic regions under pathogen-driven selection because of its central role in antigen binding and immunity. The highest MHC variability, both in terms of the number of individual alleles and gene copies, has so far been found in passerine birds; this is probably attributable to passerine adaptation to both a wide geographic range and a diverse array of habitats. If extraordinary high MHC variation and duplication rates are adaptive features under selection during the evolution of ecologically and taxonomically diverse species, then similarly diverse MHC architectures should be found in bats. Bats are an extremely species-rich mammalian group that is globally widely distributed. Many bat species roost in multitudinous groups and have high contact rates with pathogens, conspecifics, and allospecifics. We have characterized the MHC class I diversity in 116 Panamanian Seba's short-tailed bats (Carollia perspicillata), a widely distributed, generalist, neotropical species. We have detected a remarkable individual and population-level diversity of MHC class I genes, with between seven and 22 alleles and a unique genotype in each individual. This diversity is comparable with that reported in passerine birds and, in both taxonomic groups, further variability has evolved through length polymorphisms. Our findings support the hypothesis that, for species with a geographically broader range, high MHC class I variability is particularly adaptive. Investigation of the details of the underlying adaptive processes and the role of the high MHC diversity in pathogen resistance are important next steps for a better understanding of the role of bats in viral evolution and as carriers of several deadly zoonotic viruses.

Seasonal influence on testicular morphophysiological parameters of bat Carollia perspicillata in fragments of the Atlantic Forest, northeastern Brazil / Influência sazonal sobre os parâmetros morfofisiológicos testiculares de Carollia perspicillata (Chiroptera: Phyllostomidae) em fragmentos florestais de Mata Atlântica, Nordeste do Brasil

Bats belong to the order Chiroptera, family Phyllostomidae, and present a wide diversity of reproductive strategies. However, information on the reproductive biology of male bats is scarce, mainly in the Northeast Region of Brazil. Thus, this study evaluated the seasonal testicular histomorphometry of the bat Carollia perspicillata in fragments of the Atlantic Forest in Pernambuco state. To this end, adult males were collected, euthanized for removal of the testicles, and later submitted to a routine histological technique. Histomorphometric analysis included assessment of the areas of tubular and intertubular compartment occupation, as well as quantification of spermatocytes, rounded spermatids, elongated spermatids, and Sertoli and Leydig cells. Results indicated that this bat species presents reproductive seasonality, because significantly higher averages of the testicular parameters were observed in the rainy season, which is a period of greater availability of food resources. Such inferences indicate that there is a synchrony between peak spermatogenesis and hormonal inversion in the months of high precipitation; furthermore, a higher carrying capacity of the Sertoli cells is noted. C. perspicillata males possibly present greater sperm and androgenic activity in the rainy season, associated with increased tubular area and number of spermatogenic cells, as well as with the intertubular area and number of Leydig cells, respectively.(AU)

Os morcegos pertencem a ordem Chiroptera, família Phyllostomidae, e apresentam ampla diversidade de estratégias reprodutivas. Entretanto, as informações relacionadas à biologia reprodutiva dos machos são escassas, principalmente no Nordeste do Brasil. Dessa forma, o trabalho avaliou a histomorfometria sazonal testicular de Carollia perspicillata em fragmentos de Mata Atlântica de Pernambuco. Para tanto, os machos adultos foram coletados, eutanasiados para a remoção dos testículos, e posteriormente submetidos à técnica histológica de rotina. As análises histomorfométricas avaliaram as áreas de ocupação do compartimento tubular e intertubular, assim como a quantificação dos espermatócitos, espermátides arredondadas, espermátides alongadas, células de Sertoli e de Leydig. Os resultados indicaram que a espécie apresenta sazonalidade reprodutiva, visto que maiores médias significativas dos parâmetros testiculares foram encontradas na estação chuvosa, que é um período de maior disponibilidade de recursos alimentares. Tais inferências indicam que existe uma sincronia entre o pico de espermatogênese e investimento hormonal nos meses de alta precipitação, atrelado a isso, nota-se ainda, uma maior capacidade de suporte das células de Sertoli. Os machos de C. perspicillata possivelmente apresentam uma maior atividade espermática e androgênica na estação chuvosa, associadas ao aumento da área tubular e do número de células espermatogênicas, assim como da área intertubular e do número das células de Leydig, respectivamente.(AU)

Valuable carcasses: postmortem preservation of fatty acid composition in heart tissue.

In order to effectively conserve species, we must understand the structure and function of integral mechanisms at all levels of organismal organisation, from intracellular biochemistry to whole animal ecophysiology. The accuracy of biochemical analyses depend on the quality and integrity of the samples analysed. It is believed that tissue samples collected immediately postmortem provide the most reliable depiction of the living animal. Yet, euthanasia of threatened or protected species for the collection of tissue presents a number of ethical complications. Polyunsaturated fatty acids (PUFA) are essential to the cardiovascular system of all animals and the structure of PUFA can be degraded by peroxidation, potentially modifying the fatty acid composition of the tissue over postmortem time. Here, we assessed the composition of PUFA in cardiac tissue of bats (Carollia perspicillata) over the course of 12-h postmortem. We show that PUFA are resistant to naturally occurring postmortem degradation in heart tissue, with no difference in the overall composition of fatty acids across all time classes (0, 3, 6 or 12-h postmortem). Our results suggest that carcasses that would otherwise be discarded may actually be viable for the assessment of fatty acid composition in a number of tissues. We hope to spur further investigations into the viability of carcasses for other biochemical analyses as they may be an untapped resource available to biologists.

Processing of temporally patterned sounds in the auditory cortex of Seba's short-tailed bat,Carollia perspicillata.

This article presents a characterization of cortical responses to artificial and natural temporally patterned sounds in the bat species Carollia perspicillata, a species that produces vocalizations at rates above 50 Hz. Multi-unit activity was recorded in three different experiments. In the first experiment, amplitude-modulated (AM) pure tones were used as stimuli to drive auditory cortex (AC) units. AC units of both ketamine-anesthetized and awake bats could lock their spikes to every cycle of the stimulus modulation envelope, but only if the modulation frequency was below 22 Hz. In the second experiment, two identical communication syllables were presented at variable intervals. Suppressed responses to the lagging syllable were observed, unless the second syllable followed the first one with a delay of at least 80 ms (i.e., 12.5 Hz repetition rate). In the third experiment, natural distress vocalization sequences were used as stimuli to drive AC units. Distress sequences produced by C. perspicillata contain bouts of syllables repeated at intervals of ~60 ms (16 Hz). Within each bout, syllables are repeated at intervals as short as 14 ms (~71 Hz). Cortical units could follow the slow temporal modulation flow produced by the occurrence of multisyllabic bouts, but not the fast acoustic flow created by rapid syllable repetition within the bouts. Taken together, our results indicate that even in fast vocalizing animals, such as bats, cortical neurons can only track the temporal structure of acoustic streams modulated at frequencies lower than 22 Hz.

Cytoarchitecture of the medial nucleus of trapezoid body of three neotropical species of bats (Noctilio leporinus, Phyllostomus hastatus, and Carollia perspicillata) with different foraging behavior

Abstract The present study was taken to test the hypothesis that the medial nucleus of the trapezoid body (MNTB) of echolocating neotropical bats with different foraging behavior will exhibit morphological variations in relative size, degree of complexity and spatial distribution. The brains were collected from six male adult bats of each species: Noctilio leporinus (fish-eating), Phyllostomus hastatus (carnivorous/ omnivorous) and Carollia perspicillata (fruit-eating) and were double-embedded and transverse serial sections were cut and stained with cresyl fast violet. The results showed that the MNTB is well developed in all the bats in general and the mean length of the MNTB was 1160 ± 124 µm in N. leporinus, 400 ± 59 µm in P. hastatus and 320 ± 25µm in C. perspicillata. The body and brain weight do not reflect proportionately on the size of the MNTB in the present study. The hearing frequency spectrum did not covary with the size of the MNTB among the bats studied. The MNTB is clearly demarcated from the ventral nucleus of the trapezoid body (VNTB) only in P. hastatus. The MNTB comprised mainly three types of cells in all three bats: dense-staining multipolar cells (12.5 µm and 25.0 µm diameter); light-staining multipolar cells measuring (12.5 µm and 25.0 µm diameter) and light-staining round cells (5.0 µm diameter). The large sized MNTB was observed in N. leporinus, which suggests that it relies heavily on echolocation whereas P. hastatus and C. perspicillata use echolocation as well but also rely on hearing, smell and vision.

Resumo O presente estudo foi realizado para testar a hipótese de que o núcleo medial do corpo trapezoide (MNTB) de morcegos neotropicais ecolocativos com comportamento forrageiro diferente apresenta variações morfológicas no tamanho relativo, grau de complexidade e distribuição espacial. Os cérebros foram coletados de seis morcegos machos adultos de cada espécie, Noctilio leporinus (comedor de peixe), Phyllostomus hastatus (carnívoro/onívoro) e Carollia perspicillata (comedor de frutas), e foram seccionados em série e seções seriais transversais duplas e coradas com cresil violeta. Os resultados mostraram que o MNTB é bem desenvolvido em todos os morcegos em geral e que o comprimento médio do MNTB foi de 1.160 ± 124 µm em N. leporinus, 400 ± 59 µm em P. hastatus e 320 ± 25 µm em C. perspicillata. O peso corporal e cerebral não reflete proporcionalmente o tamanho do MNTB no presente estudo. O espectro da frequência auditiva não covaria com o tamanho do MNTB entre os morcegos estudados. O MNTB é claramente demarcado do núcleo ventral do corpo trapezoidal (VNTB) apenas em P. hastatus. O MNTB compreendia principalmente três tipos de células nos três morcegos: células multipolares de coloração densa (12,5 µm e 25,0 µm de diâmetro), células multipolares de coloração clara (12,5 µm e 25,0 µm de diâmetro) e células redondas manchadas de luz (5,0 µm de diâmetro). O MNTB de grande porte foi observado em N. leporinus, o que sugere que ele depende muito da ecolocalização, enquanto P. hastatus e C. perspicillata também usam a ecolocalização, mas dependem da audição, olfato e visão.

Development and characterization of fourteen novel microsatellite markers for the chestnut short-tailed fruit bat (Carollia castanea), and cross-amplification to related species.

Rapid anthropogenic land use change threatens the primary habitat of the Chestnut short-tailed bat (Carollia castanea) throughout much of its range. Information on population genetic structure can inform management strategies for this widespread frugivorous bat, and effective protection of C. castanea will also benefit the more than 20 mutualistic plant species of which this bat is the primary seed disperser. To facilitate understanding of population genetic structure in this species, fourteen novel microsatellite markers were developed using restriction-site-associated DNA libraries and Illumina sequencing and tested on 28 individuals from 13 locations in Costa Rica. These are the first microsatellite markers developed for C. castanea. All loci were polymorphic, with number of alleles ranging from 2-11 and average observed heterozygosity of 0.631. Markers were also cross-amplified in three additional frugivorous bat species threatened by habitat loss and fragmentation: Sowell's short-tailed bat (Carollia sowelli), Seba's short-tailed bat (Carollia perspicillata), and the Jamaican fruit bat (Artibeus jamaicensis), and 10, 11, and 8 were polymorphic, respectively.

Spatial pattern of genetic diversity and selection in the MHC class II DRB of three Neotropical bat species.

BACKGROUND: Although bats are natural reservoirs of many pathogens, few studies have been conducted on the genetic variation and detection of selection in major histocompatibility complex (MHC) genes. These genes are critical for resistance and susceptibility to diseases, and host-pathogen interactions are major determinants of their extensive polymorphism. Here we examined spatial patterns of diversity of the expressed MHC class II DRB gene of three sympatric Neotropical bats, Carollia perspicillata and Desmodus rotundus (Phyllostomidae), and Molossus molossus (Molossidae), all of which use the same environments (e.g., forests, edge habitats, urban areas). Comparison with neutral marker (mtDNA D-loop) diversity was performed at the same time. RESULTS: Twenty-three DRB alleles were identified in 19 C. perspicillata, 30 alleles in 35 D. rotundus and 20 alleles in 28 M. molossus. The occurrence of multiple DRB loci was found for the two Phyllostomidae species. The DRB polymorphism was high in all sampling sites and different signatures of positive selection were detected depending on the environment. The patterns of DRB diversity were similar to those of neutral markers for C. perspicillata and M. molossus. In contrast, these patterns were different for D. rotundus for which a geographical structure was highlighted. A heterozygote advantage was also identified for this species. No recombination or gene conversion event was found and phylogenetic relationships showed a trans-species mode of evolution in the Phyllostomids. CONCLUSIONS: This study of MHC diversity demonstrated the strength of the environment and contrasting pathogen pressures in shaping DRB diversity. Differences between positively selected sites identified in bat species highlighted the potential role of gut microbiota in shaping immune responses. Furthermore, multiple geographic origins and/or population admixtures observed in C. perspicillata and M. molossus populations acted as an additional force in shaping DRB diversity. In contrast, DRB diversity of D. rotundus was shaped by environment rather than demographic history.

Alternative reproductive tactics and reproductive success in male Carollia perspicillata (Seba's short-tailed bat).

The use of alternative reproductive tactics (ARTs) is widespread in animals. Males of some species may change tactics depending on age, body condition and social environment. Many bat species are polygynous where a fraction of males only have access to fertile females. For polygynous bats, knowledge of the reproductive success of males using different ARTs is scarce, and it remains unclear how age of males is related to switching decisions between social statuses. We studied a large captive population of Carollia perspicillata, where males are either harem holders, bachelors or peripheral males. Using a multistate procedure, we modelled the age-related switches in reproductive tactics and in survival probability. From the model, we calculated the reproductive success and the frequencies of males displaying different reproductive tactics. As in mammals, the switch between social statuses is often related to age, we predicted that the transition probability of bachelor and peripheral males to harem status would increase with age. We show, however, that social status transition towards a harem holding position was not related to age. Reproductive success changed with age and social status. Harem males had a significantly higher reproductive success than bachelor males except between a short period from 3.8 to 4.4 years of age where success was similar, and a significantly higher reproductive success than peripheral males between 2.6 and 4.4 years of age. Harem males showed a clear decrease in the probability of maintaining social status with age, which suggests that senescence reduces resource holding potential.

Interactions between frugivorous bats (Chiroptera: Phyllostomidae) and Piper tuberculatum (Piperaceae) in a tropical dry forest in Valle del Cauca, Colombia / Interacciones entre murciélagos frugívoros (Chiroptera: Phyllostomidae) y Piper tuberculatum (Piperaceae) en un bosque seco tropical en Valle del Cauca, Colombia

AbstractIn any ecosystem, fruits are resources that vary in time and space as well as in nutritional content. Coexistence of species from a trophic guild depends on the division and use of resources. Therefore, the organisms that depend on them as a food source, tend to show a certain degree of specialization. This way, understanding the factors that influence the dynamics of seed dispersal is important for the regeneration and conservation of tropical ecosystems. Our aim was to determine variation in consumption of Piper tuberculatum by fruit bat assemblages in the village of Robles (Jamundí, Valle del Cauca, Colombia). P. tuberculatum is a resource used not only by wildlife but also by people in the village of Robles. Bats were captured in mist nets between June and November 2014, their feces were collected, and the length of the forearm, wing area, leg length and mass were recorded. At the Universidad del Valle seed laboratory, fecal samples were washed, and their content determined. Of the 14 species captured, Sturnira lilium, Carollia brevicauda, Carollia perspicillata and Artibeus lituratus showed signs of having consumed P. tuberculatum.Sturnira lilium was the main consumer of P. tuberculatum fruits, with the greatest number of consumption events of fruit from this plant species, whereas the other bats showed more diversified consumption events. The greatest niche overlap was recorded between C. brevicauda and C. perspicillata, species that showed similar sizes (i.e., wing area and forearm length) followed by S. lilium and C. perspicillata. In contrast, A. lituratus showed the least niche overlap with the other three fruit bats captured. In conclusion, Sturnira lilium showed an interaction Sturnira-Piper, which is the result of low Solanum availability, and this bat species was the largest consumer of P. tuberculatum in the region. Rev. Biol. Trop. 64 (2): 701-713. Epub 2016 June 01.

ResumenLa coexistencia de las especies de un gremio trófico depende de la división y el uso de recursos. Los frutos en cualquier ecosistema son recursos alimenticios que varían en el tiempo y el espacio, así como en su contenido nutricional, por ende, los organismos que dependen de éstos como fuente alimenticia, tienden a presentar cierto grado de especialización. La comprensión de los factores que influyen en la dinámica de la dispersión de semillas es importante para la regeneración y conservación de los ecosistemas tropicales. Nuestro objetivo fue determinar cómo varía el consumo de Piper tuberculatum (Pipilongo) por parte del ensamblaje de murciélagos frugívoros en el corregimiento de Robles (Jamundí, Valle del Cauca, Colombia). P. tuberculatum es un recurso utilizado no solo por la fauna, sino también por los habitantes del corregimiento de Robles. Se capturaron murciélagos en redes de niebla entre junio y noviembre 2014, sus heces fueron recolectadas y medidas de la longitud del antebrazo, área alar, longitud de la pata y el peso fueron registradas. En el laboratorio de semillas de la Universidad del Valle, se lavaron las muestras y se determinó su contenido. Las especies Sturnira lilium, Carollia brevicauda, C. perspicillata, y Artibeus lituratus mostraron evidencia de consumo de frutos de P. tuberculatum, entre las 14 especies de murciélagos frugívoros capturadas. Entre ellas, S. lilium fue la principal consumidora de P. tuberculatum, con el mayor número de eventos de consumo de esta especie, mientras que las otras especies de murciélagos tuvieron eventos de consumo más diversos. El mayor traslape de nicho se registró entre las especies C. brevicauda y C. perspicillata, los cuales presentaron un tamaño similar (i.e., área alar, antebrazo), seguido de S. lilium y C. perspicillata. En contraste, el menor traslape de nicho se registró para A. lituratus con cada una de las otras tres especies de murciélagos frugívoras registradas. En conclusión, Sturnira lilium mostró una relación Sturnira-Piper, la cual es el resultado de la baja disponibilidad de Solanum, siendo ésta especie de murciélago el mayor consumidor de P. tuberculatum de la región.

Retinal projections in the short-tailed fruit bat, Carollia perspicillata, as studied using the axonal transport of cholera toxin B subunit: Comparison with mouse.

To provide a modern description of the Chiropteran visual system, the subcortical retinal projections were studied in the short-tailed fruit bat, Carollia perspicillata, using the anterograde transport of eye-injected cholera toxin B subunit, supplemented by the silver-impregnation of anterograde degeneration following eye removal, and compared with the retinal projections of the mouse. The retinal projections were heavily labeled by the transported toxin in both species. Almost all components of the murine retinal projection are present in Carollia in varying degrees of prominence and laterality. The projections: to the superior colliculus, accessory optic nuclei, and nucleus of the optic tract are predominantly or exclusively contralateral; to the dorsal lateral geniculate nucleus and posterior pretectal nucleus are predominantly contralateral; to the ventral lateral geniculate nucleus, intergeniculate leaflet, and olivary pretectal nucleus have a substantial ipsilateral component; and to the suprachiasmatic nucleus are symmetrically bilateral. The retinal projection in Carollia is surprisingly reduced at the anterior end of the dorsal lateral geniculate and superior colliculus, suggestive of a paucity of the relevant ganglion cells in the ventrotemporal retina. In the superior colliculus, in which the superficial gray layer is very thin, the projection is patchy in places where the layer is locally absent. Except for a posteriorly located lateral terminal nucleus, the other accessory optic nuclei are diminutive in Carollia, as is the nucleus of the optic tract. In both species the cholera toxin labeled sparse groups of apparently terminating axons in numerous regions not listed above. A question of their significance is discussed.

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.

ORGANIZACIÓN SOCIAL DE UNA COLONIA DEL MURCIÉLAGO Carollia brevicauda EN UN REFUGIO ARTIFICIAL, BOCHALEMA, NORTE DE SANTANDER, COLOMBIA / Social Organization of a Colony of Bats Carollia brevicauda in Artificial Shelter, Bochalema, Norte de Santander, Colombia

Se estudió la organización social de una colonia del murciélago frugívoro Carollia brevicauda en un refugio artificial en Bochalema, Norte de Santander, Colombia. Empleando un nuevo tipo de marcaje que consiste en decoloración capilar y mediante muestreos focales se observó la colonia desde septiembre de 2007 a septiembre de 2008. Se determinó que esta es definida por cuatro grupos los cuales no variaron en su conformación a lo largo del tiempo. Se estableció que las hembras fueron más fieles al refugio que los machos. Se evaluó el presupuesto de tiempo diurno y se registró que los individuos tienen un 73,9 % de tiempo en reposo, seguido del acicalamiento con un 26,6 % y las hembras presentaron mayor actividad que los machos sobre todo en época seca. Se determinaron diferencias en registros entre C. brevicauda y C. perspicillata, como por ejemplo la fidelidad de las hembras al refugio.

We studied the social organization of a colony of the fruit bat Carollia brevicauda in an artificial shelter in Bochalema, Norte de Santander, Colombia. Using a new type of marking and by focal sampling, one colony was observed from September 2007 to September 2008. It was determined that the social structure in the colony was integrated by four groups, which did not vary in structure over time. It was established that females were more faithful to the shelter than males. We assessed time budget dayly and there was that individuals hadx a 73.9 % time without any activity, followed by grooming with a 26.6 %, and females had higher activity than males, especially in dry season. We found that C. brevicauda has differences with records of C. perspicillata such as the fidelity of females and non-influence of lunar light over the hour of emergence from the refuge.