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.     

Intrinsic and extrinsic factors affecting dietary specialization in Neotropical frugivorous bats

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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.     

Seasonal variation in food availability and relative importance of dietary items in the Gambian epauletted fruit bat (Epomophorus gambianus)

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Phyllostomid Bat Assemblage Structure in Amazonian Flooded and Unflooded Forests

In Amazonia, the assemblages of several taxa differ significantly between upland terra firme and white‐water flooded várzea forests, but little is known about the diversity and distribution of bats in these two forest types. We compare the spatio‐temporal patterns of bat assemblage composition and structure in adjacent terra firme and várzea forests in the lower Purus River region of central Brazilian Amazonia. Bats were sampled using mist nets at five sites in each forest type during 40 nights (2400 net‐hours). We captured 1069 bats representing 42 species and Phyllostomidae bats comprised 99.3 percent of all captures. The bat assemblages in várzea and terra firme forests were significantly different, mainly due to a marked dissimilarity in species composition and in the number of captures during high‐water season. In addition, bat assemblages within forest types differed significantly between seasons for both terra firme and várzea. Frugivores dominated the bat assemblages in both forest types. Overall guild structure did not change between várzea and terra firme or between seasons, but frugivore and animalivore abundance increased significantly in várzea forest during the inundation. The difference in assemblage structure observed in the high‐water season is probably caused by the annual várzea flooding, which provides an effective barrier to the persistence of many understory bats. We also hypothesize that some bat species may undertake seasonal movements between forest types in response to fruit abundance, and our results further underline the importance of floodplain habitats for the conservation of species in the Amazon.     

Trophic structure of a neotropical frugivore community: is there competition between birds and bats?

Summary Dietary overlap and competition between frugivorous birds and bats in the Neotropics have been presumed to be low, but comparative data have been lacking. We determined the diets of volant frugivores in an early successional patch of Costa Rican wet forest over a one month period. Ordination of the diet matrix by Reciprocal Averaging revealed that birds and bats tend to feed on different sets of fruits and that diets differed more among bat species than among bird species. However, there was overlap between Scarlet-rumped Tanagers and three Carollia bat species on fruits of several Piper species which comprised most of the diet of these bats. Day/night exclosure experiments on P. friedrichsthalli treetlets provided evidence that birds deplete the amount of ripe fruit available to bats. These results indicate that distantly related taxa may overlap in diet and compete for fruit, despite the apparent adaptation of animal-dispersed plant species for dispersal by particular animal taxa.     

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.     

Abundance responses of frugivorous bats (Stenodermatinae) to coffee cultivation and selective logging practices in mountainous central Veracruz,Mexico

Shifting and permanent cultivation, selective logging, cattle production and coffee plantations are among the most important factors in montane cloud forest conversion and disturbance. Although shaded-coffee plantations can contribute to the preservation of local species richness, abundance of organisms could be determined by habitat resource availability in agricultural landscapes. We compared abundance of Sturnira and Artibeus bats (Phyllostomidae, Stenodermatinae), in shade coffee plantations and disturbed cloud forest fragments, which represent habitats with different chiropterochorous plant density. We also investigated the relationship between bat species abundance and food plant richness, abundance and diversity. We captured 956 bats, 76% in cloud forest fragments and 24% in shaded coffee plantations. Abundance of Sturnira spp. (small bats) was greater in cloud forest than in coffee plantations, but Artibeus spp. (large bats) abundance was similar in both habitats. Chiropterochorous plant abundance was positively related with bat abundance for Sturnira spp., while chiropterochorous plant richness and diversity were negatively related for Artibeus spp. This suggests that frugivorous bats with different morphological and ecological characteristics respond differentially to anthropogenic activities. For landscape management purposes, the maintenance and augmentation of diverse food resources, for frugivorous bats with different foraging requirements in coffee plantations, will benefit the resilience of bats to modification of their natural habitat.     

Niche Differentiation and its Relationship with Food Abundance and Vegetation Complexity in Four Frugivorous Bat Species in Southern Mexico

Species can co‐exist within a community when their use of limiting resources is differentiated. To test whether differentiation facilitates coexistence, we quantified differences and overlap in habitat use, fruit consumption, morphological characteristics, and the relationship with vegetation structure for two pairs of ecologically similar frugivorous bat species, Carollia sowelli and C. perspicillata, and Artibeus jamaicensis and A. lituratus. In Carollia sowelli and C. perspicillata, differences in body mass and wing aspect ratio were not reflected in differences in fruit or habitat use (diet overlap, 96 percent; habitat overlap, 98 percent). However, the capture rate of Carollia sowelli positively correlated with canopy openness, and that of C. perspicillata positively correlated with tree height. Body mass and wing characteristics of Artibeus species suggested a greater maneuverability for A. jamaicensis. Also, more A. jamaicensis individuals were captured feeding on Ficus spp., while Artibeus lituratus preferred fruits of the early successional tree Cecropia. However, both habitat overlap and diet overlap were higher than by chance (diet overlap, 75 percent; habitat overlap, 92 percent). The co‐existence of the four bat species in the study area may be facilitated by the abundance of the food resources forming part of the diets of both Carollia species, by the morphological differences between the Artibeus species, which allow the differentiation of foraging behavior in relation to fruit consumption, and by the structural characteristics of the vegetation.     

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.     

Sources of assimilated protein in five species of New World frugivorous bats

Fruits are N-poor items and their availability in the tropics varies throughout the year. Field and experimental studies debate whether frugivorous bats have to switch to N-rich sources of food during part of the year or if they are able to subsist on a fruit-only diet. Different strategies to meet their N requirements may influence the way in which frugivorous bats partition food resources allowing the coexistence of numerous species in tropical communities. We examined the extent to which five species of frugivorous bats relied on plant and insect sources of assimilated protein using stable-N isotope analysis. We assumed that bats only had access to fruits and insects in our analysis but we also collected fecal samples to examine the presence of other food items. We conducted the study during at least 1 full year depending on the species of bat in a tropical rain forest in southern Mexico. In the five species of bats examined, plant sources (i.e. fruits) provided most of the protein assimilated during the year, although there was a general trend for all species to show a decrease in relative plant contribution at the end of the rainy season and beginning of the dry season. In Artibeus jamaicensis, Uroderma bilobatum and Dermanura phaeotis, plants were still a major source of protein during this period, but in some individuals of Sturnira lilium and Carollia brevicauda insects represented an important contribution to their diet. Fecal samples of most bats presented fruit remains, and insects and pollen were found in small proportions. Bat reproductive activity was detected at the end of the dry season and in the middle of the rainy season, and plants were the major source of protein during this period with the exception of pregnant S. lilum and one pregnant D. phaeotis during the dry season. Our findings showed that frugivorous bats might differ in their strategies to satisfy their N demands with some species relying almost completely on fruits during most of the year and some species switching to insects when fruits were less abundant.     

Frugivory and the effects of ingestion by bats on the seed germination of three pioneering plants

The dispersion and seedling establishment of pioneering plants can be favoured by the presence of frugivorous bats because the bats usually improve seed germination after ingestion. Although seed germinability is known to vary greatly after ingestion by different bats, the relative contribution of each bat species to seed germination within plant communities is poorly understood. In this study, we first determined the fauna of frugivorous bats in a semideciduous seasonal forest remnant in southern Brazil and subsequently identified the plant species of the seeds passed through their guts. Second, the germination performance (i.e., germination percentage and speed) of the seeds of three pioneering plants (Piper aduncum, Piper hispidinervum and Solanum granuloso-leprosum) ingested by the most abundant bats was compared with that of the non-ingested seeds (seeds collected from fruits). Additionally, the effects on seed germination of different bat species were compared. During one year, five species of frugivorous bats were caught, and the seeds of eleven identifiable plant species (not counting those of undetermined species) were found in their faeces. We found that the germination performance of the seeds of Piper species was significantly enhanced after ingestion by bats, whereas S. granuloso-leprosum seeds had neutral or reduced germinability when seeds in faeces were compared with pulp-removed seeds. Our results revealed that the bat species that were captured exerted different effects upon seed germination; such a disparity is expected to result in different rates of early establishment of these pioneer plants in tropical forests, most likely affecting forest composition and structure, particularly during the initial stages of succession.     

Enriching agroecosystems with fruit-producing tree species favors the abundance and richness of frugivorous and nectarivorous bats in Veracruz, Mexico

We evaluated how the abundance and richness of frugivorous and nectarivorous bat species differs among three types of common agroecosystems (diversified coffee plantations, simple coffee plantations and pastures) in Veracruz, Mexico, that represent a gradient of structural and floristic complexity. Using mixed effects models we demonstrated that both the richness and the total abundance of bats was higher in the diversified coffee plantations. We detected similar patterns on comparing the abundance of the four most abundant bat species. Neither season nor the season-agroecosystem interaction had any effect on the comparisons made. Using multiple regressions we found that the richness of plants that are useful to both people and bats had the most explanatory power for the richness and total abundance of frugivorous and nectarivorous bats, as well as for the abundance of Carollia sowelli, Glossophaga soricina and Sturnira spp. Our results indicate that agroecosystems value for conservation of fruit and nectar-eating bats increases as the fruit-bearing trees increases. For the effective conservation of these guilds of bats in tropical agroecosystems, a strategy of diversification with fruit-bearing species is highly recommended; such a strategy would benefit both agricultural producers and wildlife.     

Fecundity,fruiting pattern,and seed dispersal in Piper amalago (Piperaceae), a bat-dispersed tropical shrub

Summary This paper describes the nightly and seasonal production of ripe fruit by Piper amalago (Piperaceae), a patchily distributed, bat-dispersed forest shrub, at Parque Nacional Santa Rosa, Costa Rica. Phenological observations over several years indicate that individuals produce a low (usually 1–3) and variable number of ripe fruit each night for 3–4 wks in the early wet season (June and July). Observations of the disappearance rates of marked fruits and fruit manipulation experiments indicate that fruit removal probabilities are high (often nearly 1.0) and independent of nightly and seasonal ripe fruit crop size. Data from previous feeding and foraging studies of the bat Carollia perspicillata (Phyllostomidae) are used to estimate the mobility of P. amalago's seeds. Most seeds (>90%) are deposited 50 m from parent plants under night feeding roosts. Relatively few seeds move >300 m, and movements this long are more likely to occur early and late in the fruiting season when bats change feeding sites more frequently. Seed experiments indicate that P. amalago seedling establishment probabilities are higher in light gaps than under forest canopy. The dispersal quality (sensu McKey 1975) of P. amalago's chiropteran seed dispersers is directly proportional to the number of seeds they excrete in actual or incipient light gaps.     

Do Bats Roost and Forage in Shade Coffee Plantations? A Perspective from the Frugivorous Bat Sturnira hondurensis

Shade coffee plantations are considered important habitats for frugivorous bats. However, it is not known if bats use this agricultural habitat for shelter, food resources, or both. This study addresses these questions using the highland yellow‐shouldered bat (Sturnira hondurensis) as an example. Twenty‐six adult individuals of S. hondurensis were captured, 50 percent in tropical montane cloud forest (TMCF) and 50 percent in shade coffee plantations (SCP) in Veracruz, Mexico, and each was fitted with a radio transmitter for locating roosts and feeding areas. Data were obtained from 24 of them. The fieldwork was conducted between October 2010 and October 2011 covering all seasons. Twenty‐two day roosts were located in the cavities of twelve different species of tree. Roosts located in TMCF differed significantly from those in SCP, having a smaller crown area and a greater species richness and density of plants around the roost. In SCP, both the average home range and the average core use area were smaller than in TMCF, but the differences were not statistically significant. Distances travelled by bats were generally longer and more variable in the SCP; the distance between capture site and foraging site was significantly greater in SCP than in TMCF. In SCP, there were fewer understory chiropterochorous plants, which are the main item in the diet of this bat and many other sympatric species of frugivorous bats. Although S. hondurensis does use roosts and foraging sites in the SCP, it is important to note that this species and others with similar requirements primarily depend on the preservation of intact forest adjacent to modified landscapes, where roosts and fruit are constantly available in abundance. Management practices should guarantee a greater density and diverse of trees and the preservation of understory plants with fruits in the coffee plantations that allow a long‐term survival of frugivorous bats populations.     

Numerical and Functional Responses of Forest Bats to a Major Insect Pest in Pine Plantations

Global change is expected to modify the frequency and magnitude of defoliating insect outbreaks in forest ecosystems. Bats are increasingly acknowledged as effective biocontrol agents for pest insect populations. However, a better understanding is required of whether and how bat communities contribute to the resilience of forests to man- and climate-driven biotic disturbances. We studied the responses of forest insectivorous bats to a major pine defoliator, the pine processionary moth pityocampa, which is currently expanding its range in response to global warming. We used pheromone traps and ultrasound bat recorders to estimate the abundance and activity of moths and predatory bats along the edge of infested pine stands. We used synthetic pheromone to evaluate the effects of experimentally increased moth availability on bat foraging activity. We also evaluated the top-down regulation of moth population by estimating T. pityocampa larval colonies abundance on the same edges the following winter. We observed a close spatio-temporal matching between emergent moths and foraging bats, with bat activity significantly increasing with moth abundance. The foraging activity of some bat species was significantly higher near pheromone lures, i.e. in areas of expected increased prey availability. Furthermore moth reproductive success significantly decreased with increasing bat activity during the flight period of adult moths. These findings suggest that bats, at least in condition of low prey density, exhibit numerical and functional responses to a specific and abundant prey, which may ultimately result in an effective top-down regulation of the population of the prey. These observations are consistent with bats being useful agents for the biocontrol of insect pest populations in plantation forests.     

Seasonal dietary niche contraction in coexisting Neotropical frugivorous bats (Stenodermatinae)

Tropical dry forests are characterized by punctuated seasonal precipitation patterns that drive primary production and the availability of fruits, seeds, flowers, and insects throughout the year. In environments in which the quantity and quality of food resources varies seasonally, consumers should adjust their foraging behavior to maximize energy intake while minimizing overlap with competitors during periods of low food availability. Here, we investigated how the diets of frugivorous bats in tropical dry forests of NW Mexico varied in response to seasonal availability and how this affected dietary overlap of morphologically similar species. We performed stable isotope analyses to understand temporal and interspecific patterns of overall isotopic niche breadth, trophic position, and niche overlap in the diet of six frugivorous species of closely related New World leaf-nosed bats (family Phyllostomidae, subfamily Stenodermatinae). We estimated seasonal changes in resource abundance in two complementary ways: (a) vegetative phenology based on long-term remote sensing data and (b) observational data on food availability from previously published insect and plant fruiting surveys. In all species, there was a consistent pattern of reduced isotopic niche breadth during periods of low food availability. However, patterns of niche overlap varied between morphologically similar species. Overall, results from our study and others suggest that seasonal food availability likely determines overall dietary niche breadth in Phyllostomidae and that despite morphological specialization, it is likely that other mechanisms, such as opportunistic foraging and spatiotemporal niche segregation, may play a role in maintaining coexistence rather than simply dietary displacement.     

Seasonality in fruit availability affects frugivorous primate biomass and species richness

We examine the effect of total annual food abundance and seasonal availability on the biomass and species richness for frugivorous primates on three continents (n=16 sites) by data on fruit fall. We reveal that the best‐fit models for predicting primate biomass include total annual fruit fall (positive), seasonality (negative) and biogeography (Old World>New World and mainland>island) and that these factors explain 56–67% of the variation. For the number of species, the best‐fit models include seasonality (negative) and biogeography (Old World>New World and mainland>island) but not total annual fruit fall. Annual temperature has additional effects on primate biomass when the effects of fruits and biogeography are controlled, but there is no such effect on species richness. The present results indicate that, measured on local scales, primate biomass and number of species is affected by the seasonal variation in food availability.     

Cloning and Molecular Evolution of the Aldehyde Dehydrogenase 2 Gene (Aldh2) in Bats (Chiroptera)

Old World fruit bats (Pteropodidae) and New World fruit bats (Phyllostomidae) ingest significant quantities of ethanol while foraging. Mitochondrial aldehyde dehydrogenase (ALDH2, encoded by the Aldh2 gene) plays an important role in ethanol metabolism. To test whether the Aldh2 gene has undergone adaptive evolution in frugivorous and nectarivorous bats in relation to ethanol elimination, we sequenced part of the coding region of the gene (1,143 bp, ~73 % coverage) in 14 bat species, including three Old World fruit bats and two New World fruit bats. Our results showed that the Aldh2 coding sequences are highly conserved across all bat species we examined, and no evidence of positive selection was detected in the ancestral branches leading to Old World fruit bats and New World fruit bats. Further research is needed to determine whether other genes involved in ethanol metabolism have been the targets of positive selection in frugivorous and nectarivorous bats.     

Ovarian morphology and folliculogenesis and ovulation process in the flat-faced fruit-eating bat Artibeus planirostris and the Argentine brown bat Eptesicus furinalis: A comparative analysis

The Neotropical bat species Artibeus planirostris and Eptesicus furinalis present a different morphology of the female reproductive organs: the first presents a simplex uterus, while the second presents a bicornuate uterus, but there is no information about their ovaries. Our aim was to compare the general ovary morphology and the folliculogenesis process in these species to increase the knowledge about the reproductive diversity of tropical bats. We observed a morphological distinction between the ovaries of both species: A. planirostris presents the primordial follicles located in a cranial portion of the ovary and the interstitial gland cells are not distinctive, while in E. furinalis, the primordial follicles are located throughout the cortex, and there is an abundance of interstitial gland cells. Both species present binovular or triovular follicles. Artibeus planirostris is a monovular species, with a preferential ovulation in the left side. Some females of E. furinalis exhibited two corpora lutea in the same ovary, and others presented a corpus luteum in both right and left ovaries at the same time; thus, E. furinalis is a polyovular species. Our results express the variation between two Neotropical species, reflecting the great variation in the reproductive aspects in Chiroptera.