Bat assemblage structure in two dry forests of Colombia: Composition, species richness, and relative abundance

We studied the composition, species richness, and relative abundance of bat assemblages in the Colombian dry forests of Chicamocha and Patía. In Chicamocha, 11 bats of the family Phyllostomidae were captured with mist-nets, corresponding to 85–100% of the potential phyllostomids species in the area. Two bats of the family Vespertilionidae were also captured in Chicamocha. In Patía, 12 species were captured with mist-nets, all Phyllostomidae, representing 72–100% of the estimated total number of species in the zone. Minor differences in number of species and composition were detected among sampling periods in Chicamocha. The most common species in this dry forest were Glossophaga longirostris and Sturnira lilium. In Patía, notable differences in the number of species and composition were observed among sampling periods, and the most common species were Artibeus jamaicensis, Carollia perspicillata and Phyllostomus discolor. Arid-zone dwelling bats were absent in Patía and we suggest that this absence may be associated with the isolation of Patía from other northern dry zones of Colombia since Quaternary times. There was also low abundance of bats in Patía, which appears to be related to human disturbance. The most abundant phyllostomid bat species in the two dry forests studied are those that include fruit and/or nectar-pollen from columnar cacti as an important proportion of their diets.     

Phyllostomid bat assemblages in different successional stages of tropical rain forest in Chiapas,Mexico

Due to their role in seed dispersal, changes in the community of phyllostomid bats have direct consequences on ecological succession. The objective of this work was to document changes in the structure of bat assemblages among secondary successional stages of tropical rain forest in Chiapas, Mexico. Bats were mist-netted at ground level during 18 months in 10 sites belonging to 3 successional stages: four sites represented early succession (2–8 years of abandonment), four intermediate succession (10–20 years of abandonment), and two late succession (mature old-growth forest).We captured 1,179 phyllostomids comprising 29 species. Phyllostomid species richness was 17 (58% of all species) in the early stage, 18 (62%) in the intermediate stage and 24 (83%) in the late stage. The late successional mature forest possessed nine species that were exclusively found there, whereas early and intermediate successional stages contained only one exclusive species. Sturnira lilium, Artibeus lituratus, Carollia perpicillata, Artibeus jamaicensis and Glossophaga soricina represented 88% of all captured phyllostomid bats. Frugivores made up more than 90% of the species captured in early and intermediate successional stages and 84% in late successional forest. The Bray–Curtis index of dissimilarity showed a replacement of species through successional stages with the largest dissimilarity between early and late stages, followed by intermediate and late, and the lowest dissimilarity between early and intermediate stages. The number of gleaning insectivore species increased during succession. The carnivorous guild was exclusively found in the late stage (three species). We conclude that the late successional mature forest was the main reservoir for the gleaning insectivore and carnivore guilds; however, early and intermediate successional stages possessed a great diversity of species including many frugivores.     

Ecological Responses of Frugivorous Bats to Seasonal Fluctuation in Fruit Availability in Amazonian Forests

Lowland Amazon is climatically one of the least seasonal regions on the planet, but little is known about how this is reflected in ecological seasonality. The central objective of this study was to determine whether seasonal fluctuations in the availability of fruit resources in Neotropical forests are sufficiently marked to affect the ecology and physiology of frugivorous bats. Seasonal variations in the overall bat abundance and in the captures, body condition, and reproductive activity of the two most abundant species, Carollia perspicillata and Artibeus planirostris, were studied within a region of central Brazilian Amazonia dominated by a mosaic of nonflooded (terra firme) and seasonally flooded forests (várzea and igapó). Concurrent seasonal changes in fruit availability were measured. The abundance of fruits was markedly seasonal, with far fewer resources available during the low-water season. There was a positive correlation between fruit and bat abundance. Overall, bats did not increase the consumption of arthropods during the period of fruit shortage. In A. planirostris, the body condition declined when fruits were scarcer. In both C. perspicillata and A. planirostris, foraging and reproductive activity were positively correlated with fruit availability. Consequently, the results suggest that resource seasonality is sufficiently marked to affect frugivorous bats and force them to make important eco-physiological adjustments.     

Trophic niche changes associated with habitat fragmentation in a Neotropical bat species

Habitat fragmentation could alter ecological traits including species trophic habits. Here, we used carbon and nitrogen stable isotope ratios to establish differences in isotopic niche width and food resource use between forest fragments and the continuous forest for the phyllostomid frugivorous bat Artibeus lituratus. Using mist nests, we captured bats from two forest fragments and two sites in continuous forest, and sampled from each individual captured three body tissues with contrasting turnover rates (skin, muscle, and liver). Samples were collected between February and March (austral summer) and between August and September (austral winter). In addition, in each sampling site and season we collected potential food resources (fruits and insects) consumed by our A. lituratus. Our findings indicate that A. lituratus had a predominantly omnivorous diet, with high consumption of insects during summer in forest fragments. The increasing consumption of insects in these fragments seems to have led to a wider isotopic niche, in relation to the continuous forest. Because A. lituratus is typically a seed disperser, changes in trophic habits in the forest fragments from frugivory to insectivory may diminish their role in forest regeneration. Abstract in Portuguese is available with online material.     

Community of bat flies (Streblidae and Nycteribiidae) on bats in the Cerrado of Central-West Brazil: hosts,aggregation, prevalence,infestation intensity,and infracommunities

Streblidae and Nycteribiidae are families of bloodsucking flies that parasitize bats exclusively. We studied the community of these flies in a Cerrado area in the Central-West Brazil. We captured 708 bats over 17 nights from October 2012 to March 2013. Forty-five per cent of the hosts were parasitized by 836 specimens of bat flies of 22 species. The most abundant flies were Trichobius joblingi on Carollia perspicillata, followed by Megistopoda aranea on Artibeus planirostris, and Strebla guajiro on C. perspicillata. All bat flies showed a high level of specificity for their hosts. Trichobius joblingi was the bat fly with the highest prevalence (80%) and mean intensity of infestation (3.5) on hosts with a representative sample size (n > 20). This result is likely related to the type of roosting (cavity) used by C. perspicillata, primary host of this fly species. Anoura caudifer hosted the largest infracommunities (n = 7). However, most bats were parasitized by a single fly species, suggesting a pattern in infestations. The aggregation index was high, indicating an unequal occurrence in parasite infestations. The majority of hosts were infested by few or no flies and few hosts were highly infested, showing a negative binomial distribution.     

Morphology,Diet and Flower‐visiting by Phyllostomid Bats in Cuba

Pollinator morphology can play an important role in structuring plant–pollinator relationships and a pollinator's morphology may be associated with aspects of its diet. We examined the relationship between morphology and the partitioning of flower‐based food resources for five species of flower‐visiting Cuban bats: Artibeus jamaicensis, Brachyphylla nana, Erophylla sezekorni, Monophyllus redmani and Phyllonycteris poeyi. We analyzed cranial traits and body size to assess differences among species with respect to morphological specializations. We also collected dietary data from guano and used acoustic monitoring to assess bat activity at flowers. We found evidence that bats partition floral resources, but we found no direct evidence that plants were limiting resources for the bats. Morphological similarity among bat species did not predict dietary overlap. Rather it was associated with phylogenic relationships among some species. Species with different morphological specialization for flower‐visiting consumed resources and visited food plants at different frequencies.     

Scale‐dependent responses to forest cover displayed by frugivore bats

Despite vast evidence of species turnover displayed by Neotropical bat communities in response to forest fragmentation, the exact shape of the relationship between fragment area and abundance for individual bat species is still unclear. Bats’ ample variation in diet, morphology, and movement behaviour can potentially influence species’ perception of the landscape. Thus, studies describing fragment area at a single spatial scale may fail to capture the amount of forest available from the perspective of individual bat species. In the present paper, we study the influence of forest cover on bats inhabiting a fragmented forest in Mexico, focusing on some of the most common frugivore species: Artibeus jamaicensis, Carollia spp. (C. brevicauda/C. perspicillata) and Sturnira spp. (S. lilium/S. ludovici). We quantified forest cover at scales ranging from 50 to 2000 m, and measured the influence of forest cover on bat capture success, a surrogate for abundance. The three species displayed positive and significant scale‐dependent associations with forest cover. Abundance of A. jamaicensis increased with forest cover measured at scales ranging between 500 and 2000 m, while Carollia spp. responded more strongly to variation in forest cover measured at scales 100–500 m. For Sturnira spp., abundance was a function of presence of creeks near mist‐netting sites, and amount of secondary forest present at a 200 m scale. The observed variation in responses to forest cover can be explained in light of interspecific differences in diet, home range, and body size. Our results illustrate a method for measuring the effect of forest fragmentation on mobile species and suggest that changes in abundance in fragmented landscapes emerge from the interaction between species’ traits and landscape structure.     

A Comparison of the Phyllostomid Bat Assemblages in Undisturbed Neotropical Forest and in Forest Fragments of a Slash‐and‐Burn Farming Mosaic in Petén,Guatemala1

Using mist nets, we compared phyllostomid bat ensembles of continuous mature forest in Tikal National Park, Guatemala, and of forest fragments in the nearby farming landscape. Of 20 species captured, 13 were shared between treatments, 4 were unique to continuous forest, and 3 were unique to forest fragments. Dominance–diversity curves were similar for the two treatments except that Sturnira lilium comprised 43 percent of captures in the forest fragments, resulting in greater dominance there. Capture rates (and presumably relative abundance) differed significantly between continuous forest and forest fragments, both in terms of species and feeding guilds. Sturnia lilium and Dermanura sp. were captured significantly more often in forest fragments than in continuous forest, whereas Artibeus jamaicensis, A. lituratus, and Centurio senex were taken significantly more often in continuous forest. Large frugivores accounted for a higher proportion of total captures in continuous forest than in forest fragments, whereas small frugivores showed the opposite pattern. By their abundances, Carollia perspicillata and S. lilium are indicators of forest disturbance. The relative abundances of large frugivores, which feed on large fruits of mature forest trees, and small frugivores, which feed on small‐fruited plants occurring in early succession, are an indicator of forest disturbance. Other groups, such as large insect‐ and vertebrate‐eating bats, because of their low capture rates, are impractical as indicators for rapid assessment of forest disturbance based on mist netting, but may prove especially vulnerable to forest fragmentation.     

Trypanosoma pifanoi n. sp. from Colombian Bats*

SYNOPSIS. A new large trypanosome was found in the blood of 19 Artibeus lituratus and 2 Phyllostomus hastatus bats. The monomorphic trypanosome resembles Trypanosoma megadermae in some respects, but differs from it in that it is larger and has a short flagellum, both extremities are very tapered, the kinetoplast is very close to a small nucleus and there is a greater distance between the kinetoplast and the posterior extremity of the body. In diphasic blood-agar cultures there is a great variety of odd multiplication forms not described from other trypanosome cultures, but some simulate T. cruzi. This trypanosome is not capable of infecting mice, tissue culture cells, Carollia perspicillata bats, or triatomids, but is able to infect A. lituratus bats. Culture forms of the trypanosome inoculated intra-coelomically are pathogenic for several species of triatomids, and multiply in the hemolymph of Rhodnius prolizus, often producing forms similar to crithidiae of T. rangeli. Culture forms of the trypanosome seem to have common antigens with T. cruzi. This new species is described as Trypanosoma pifanoi.     

Long-term bat study on an island in the southeastern Brazilian coast with comparison of richness and composition of species among sites

Although Rio de Janeiro is one of the best sampled states of Brazil for bats, there are still some poorly studied islands on its coast. Hence, we inventoried the bat species of an island on the southwestern coast of Rio de Janeiro, compared five sites sampled within this island, and compared its bat community with seven other sites in the same region. We carried out sampling in July 1995 and from September 2006 to August 2010, comprising 58 samplings. We captured a total of 1502 individuals of 25 bat species with mist nets set far from roosts, or close to or inside roosts. The most abundant species were Artibeus lituratus, Molossus molossus, and Carollia perspicillata. Total sampling effort was 89,400 m² h. The present study was one out of five inventories carried out in the southwestern coast of Rio de Janeiro that registered more than 1000 bat individuals from more than 24 bat species. Long-term inventories on islands are still needed, because they can result in a large number of species and captures as observed in the present study.     

Social Grooming in Bats: Are Vampire Bats Exceptional?

Evidence for long-term cooperative relationships comes from several social birds and mammals. Vampire bats demonstrate cooperative social bonds, and like primates, they maintain these bonds through social grooming. It is unclear, however, to what extent vampires are special among bats in this regard. We compared social grooming rates of common vampire bats Desmodus rotundus and four other group-living bats, Artibeus jamaicensis, Carollia perspicillata, Eidolon helvum and Rousettus aegyptiacus, under the same captive conditions of fixed association and no ectoparasites. We conducted 13 focal sampling sessions for each combination of sex and species, for a total of 1560 presence/absence observations per species. We observed evidence for social grooming in all species, but social grooming rates were on average 14 times higher in vampire bats than in other species. Self-grooming rates did not differ. Vampire bats spent 3.7% of their awake time social grooming (95% CI = 1.5–6.3%), whereas bats of the other species spent 0.1–0.5% of their awake time social grooming. Together with past data, this result supports the hypothesis that the elevated social grooming rate in the vampire bat is an adaptive trait, linked to their social bonding and unique regurgitated food sharing behavior.     

Food niche overlap among neotropical frugivorous bats in Costa Rica

Food habits of 15 species of frugivorous bats were studied at La Selva Biological Station, Costa Rica. Eight hundred and fifty-four (854) fecal samples and 169 samples from fruit parts and seeds discarded by bats beneath feeding roosts were analyzed. During eight months of study, 47 fruit species consumed by bats were identified. Five plant genera (Cecropia, Ficus, Piper Solanum, and Vismia) constituted 85% of all plants found in fecal samples. Feeding niche breadth differed significantly among the six most common species of frugivorous bats (Artibeus jamaicensis, Carollia sowelli, C. castanea, C. perspicillata, Dermanura sp., and Glossophaga commissarisi). All species, except for Dermanura sp., showed a diet dominated by one or two plant species. This suggests a pattern of resource partitioning at a generic level, in which Carollia consumed mainly Piper, Artibeus consumed Ficus and Cecropia, and Glossophaga consumed Vismia. Cluster analysis revealed higher values of food niche overlap in congeneric species than among species of different genera. Results show that if food is a limiting factor, mechanisms other than trophic selection must reduce interspecific interference or competition for food in this frugivorous bat guild.     

Columnar cacti as sources of energy and protein for frugivorous bats in a semi‐arid ecosystem

Columnar cacti constitute the dominant elements in the vegetation structure of arid and semi‐arid New World ecosystems representing a plethora of food resources for vertebrate consumers. Previous stable isotope analysis in Central Mexico showed that columnar cacti are of low importance to build tissue for frugivorous bats. We used carbon stable isotope analysis of whole blood and breath samples collected from four species of frugivorous bats (Sturnira parvidens, Sturnira ludovici, Artibeus jamaicensis, and Artibeus intermedius) to reconstruct the importance of cactus plants in their diet. Breath samples were collected within 10 min (B₁₀) of bat capture and ~12 h after capture (B₇₂₀), representing the oxidation of recently ingested food and of body reserves, respectively. We expected that bats relied primarily on non‐cactus food to construct tissues and fuel oxidative metabolism. Non‐cactus food strongly predominated for tissue building, whereas oxidative metabolism was supported by a moderate preponderance of non‐cactus food for B₁₀ samples, and a moderate preponderance of cactus food or an equal contribution of both sources for B₇₂₀ samples. Artibeus and Surnira species appear to cover a narrow part of the diet with cactus food, confirming that the incorporation of nutrients derived from these plants is not generalized among vertebrate consumers.     

Tropical Secondary Forest Management Influences Frugivorous Bat Composition,Abundance and Fruit Consumption in Chiapas,Mexico

Most studies on frugivorous bat assemblages in secondary forests have concentrated on differences among successional stages, and have disregarded the effect of forest management. Secondary forest management practices alter the vegetation structure and fruit availability, important factors associated with differences in frugivorous bat assemblage structure, and fruit consumption and can therefore modify forest succession. Our objective was to elucidate factors (forest structural variables and fruit availability) determining bat diversity, abundance, composition and species-specific abundance of bats in (i) secondary forests managed by Lacandon farmers dominated by Ochroma pyramidale, in (ii) secondary forests without management, and in (iii) mature rain forests in Chiapas, Southern Mexico. Frugivorous bat species diversity (Shannon H’) was similar between forest types. However, bat abundance was highest in rain forest and O. pyramidale forests. Bat species composition was different among forest types with more Carollia sowelli and Sturnira lilium captures in O. pyramidale forests. Overall, bat fruit consumption was dominated by early-successional shrubs, highest late-successional fruit consumption was found in rain forests and more bats consumed early-successional shrub fruits in O. pyramidale forests. Ochroma pyramidale forests presented a higher canopy openness, tree height, lower tree density and diversity of fruit than secondary forests. Tree density and canopy openness were negatively correlated with bat species diversity and bat abundance, but bat abundance increased with fruit abundance and tree height. Hence, secondary forest management alters forests’ structural characteristics and resource availability, and shapes the frugivorous bat community structure, and thereby the fruit consumption by bats.     

The Role of Fruits and Insects in the Nutrition of Frugivorous Bats: Evaluating the Use of Stable Isotope Models1

We estimated the relative contribution of fruits and insects as sources of dietary protein in two species of Neotropical frugivorous bats (Artibeus jamaicensis and Sturnira lilium) using stable carbon and nitrogen isotope analyses. An insectivorous species (Pteronotus parnellii) was also included for comparison. We found constant patterns in stable carbon and nitrogen isotope composition in blood that separated the two species of frugivorous bats from the insectivorous bat. When we used these isotopic values (combined with those of dietary fruits and insects) to estimate the percent contribution of fruits and insects to the diet of the bats, we obtained different results, depending on assumptions and model adopted. We tested models using both 8“N and 8′³C results simultaneously and separately and further used diet‐tissue fractionation factors of 3%o for nitrogen and 1 and 3.5%o for carbon. We found that a carbon‐based model with a diet‐blood enrichment factor of 3.5%o produced the most parsimonious results. The model estimated that A. jamaicensis and S. lilium obtained most of their protein requirements from fruits, whereas P. parnellii fed mostly on insects. No sexual or seasonal variations in the diet of the two frugivorous species were detected. We found no evidence that the diet of sexually active females differed from that of nonsexually active females in the two species of frugivorous bats. We suggest that future studies better define isotopic fractionation between diet and tissues of bats using captive rearing and controlled diets.     

Comparative hindlimb bone morphology in noctilionid fisher bats (Chiroptera: Noctilionidae), with emphasis on Noctilio leporinus postnatal development

The hindlimbs allow bats to attach to the mother from birth, and roost during independent life. Despite the great morphological diversity in Chiroptera, the hindlimbs morphology and its postnatal development have been poorly studied. Postnatal development of hindlimbs in Noctilio leporinus is described, further comparing the morphology of adults with that of Noctilio albiventris and previously reported species (Desmodus rotundus, Artibeus lituratus, Molossus molossus). The ossification ending sequence at autopodium elements of N. leporinus does not follow the distal to proximal directional sequence described for D. rotundus, exhibiting a heterochronic delayed ossification ending for the digits of N. leporinus regarding other hindlimb elements, associated with the bigger relative autopodium size of this fisher bat regarding other bat species. Noctilionid bats share the same adult hindlimb bone morphology, except for differences at hindlimb proportions and calcar ossification degree. There are differences in the number and position of bony processes, slots and sesamoids of adult noctilionid fisher bats regarding previously reported species; most differences are concentrated at the autopodium and are related to an increased surface for muscular insertion and the structural support of claws. These facts seem to be closely associated with functional demands of the feeding strategy of noctilionid fisher bats.     

Isolation of polymorphic tetranucleotide microsatellite markers for the silky short‐tailed bat Carollia brevicauda

We isolated 10 polymorphic microsatellite markers for the silky short‐tailed bat, Carollia brevicauda, from genomic libraries enriched for (AAGG)_n repetitive elements. The number of alleles ranged from six to 25 per locus with the observed heterozygosity ranging from 0.29 to 0.95. These markers will be useful for analysis of questions concerning population genetic structure and models of speciation. Results of cross‐species amplification in Carollia castanea and Carollia perspicillata are also reported.     

Histochemical and myosin composition of vampire bat (Desmodus rotundus) pectoralis muscle targets a unique locomotory niche

The vampire bat pectoralis muscle contains at least four fiber types distributed in a nonhomogeneous pattern. One of these fiber types, here termed IIe, can be elucidated only by adenosine triphosphatase (ATPase) histochemistry combined with reactions against antifast and antislow myosin antibodies. The histochemical and immunohistochemical observations indicate a well-developed specialization of function within specific regions of the muscle. In parallel, analyses of native myosin isoforms and myosin heavy chain isoforms indicate two points. First, the histochemical “type IIe” fiber is predominant in cranial portions of the muscle, and myosin extracted from these regions exhibits a unique electrophoretic mobility not observed in the myosin isoforms of more traditional laboratory mammals. Second, the type I fibers are confined to the pectoralis abdominalis muscle and a small adjacent region of the caudal part of the pectoralis. This pattern of type I fiber distribution is considered a derived character state compared to muscle histochemical phenotype and isoform composition in the pectoralis muscles of other phyllostomids we have studied (Artibeus jamaicensis, Artibeus lituratus, Carollia perspicillata). We relate this to the unique locomotory needs of the common vampire bat, Desmodus rotundus. © 1993 Wiley-Liss, Inc.     

Thermogenic capacity of three species of fruit-eating phyllostomid bats

This study evaluated the thermogenic capacity of three species of fruit-eating phyllostomid bats (Carollia perspicillata, Sturnira lilium and Artibeus lituratus) during the dry-cool and wet-warm seasons, by measuring changes in body mass, basal metabolic rate (BMR), maximal metabolic rate (MMR), nonshivering thermogenesis and shivering thermogenesis. Body mass was lower, on average, during the dry-cool season and all species of fruit-eating bats showed an increase in oxygen consumption after noradrenaline injection and after exposure to a He-O₂ atmosphere. However, the magnitude of this increase was similar in both seasons. BMR also did not vary between seasons. Although, our results showed for the first time that all three species studied were able to increase thermogenesis by both nonshivering and shivering thermogenesis, we did not find significant differences in any thermoregulatory variable measured when comparing data from the two different seasons. Probably the difference in the mean and variance of the temperature profile between seasons were not strong enough to alter the thermogenic capacity of these species. Furthermore, the use of alternative physiological (torpor) or behavioral (huddling) strategies might have alleviated the need to trigger energetic-costly thermogenic responses.     

Patterns of diversification in two species of short‐tailed bats (Carollia Gray, 1838): the effects of historical fragmentation of Brazilian rainforests

The small‐sized frugivorous bat Carollia perspicillata is an understory specialist and occurs in a wide range of lowland habitats, tending to be more common in tropical dry or moist forests of South and Central America. Its sister species, Carollia brevicauda, occurs almost exclusively in the Amazon rainforest. A recent phylogeographic study proposed a hypothesis of origin and subsequent diversification for C. perspicillata along the Atlantic coastal forest of Brazil. Additionally, it also found two allopatric clades for C. brevicauda separated by the Amazon Basin. We used cytochrome b gene sequences and a more extensive sampling to test hypotheses related to the origin and diversification of C. perspicillata plus C. brevicauda clade in South America. The results obtained indicate that there are two sympatric evolutionary lineages within each species. In C. perspicillata, one lineage is limited to the Southern Atlantic Forest, whereas the other is widely distributed. Coalescent analysis points to a simultaneous origin for C. perspicillata and C. brevicauda, although no place for the diversification of each species can be firmly suggested. The phylogeographic pattern shown by C. perspicillata is also congruent with the Pleistocene refugia hypothesis as a likely vicariant phenomenon shaping the present distribution of its intraspecific lineages. © 2011 The Linnean Society of London, Biological Journal of the Linnean Society, 2011, 102 , 527–539.