Long-tongued Bats Research Articles

Serial reversal learning in nectar-feeding bats

We explored the behavioral flexibility of Commissaris’s long-tongued bats through a spatial serial reversal foraging task. Bats kept in captivity for short periods were trained to obtain nectar rewards from two artificial flowers. At any given time, only one of the flowers provided rewards and these reward contingencies reversed in successive blocks of 50 flower visits. All bats detected and responded to reversals by making most of their visits to the currently active flower. As the bats experienced repeated reversals, their preference re-adjusted faster. Although the flower state reversals were theoretically predictable, we did not detect anticipatory behavior, that is, frequency of visits to the alternative flower did not increase within each block as the programmed reversal approached. The net balance of these changes was a progressive improvement in performance in terms of the total proportion of visits allocated to the active flower. The results are compatible with, but do not depend on, the bats displaying an ability to ‘learn to learn’ and show that the dynamics of allocation of effort between food sources can change flexibly according to circumstances.

Social information facilitates learning about novel food sources in adult flower-visiting bats.

Incorporating novel food sources into their diet is crucial for animals in changing environments. Although the utilization of novel food sources can be learned individually, learning socially from experienced conspecifics may facilitate this task and enable a transmission of foraging-related innovations across a population. In anthropogenically modified habitats, bats (Mammalia: Chiroptera) frequently adapt their feeding strategy to novel food sources, and corresponding social learning processes have been experimentally demonstrated in frugivorous and animalivorous species. However, comparable experiments are lacking for nectarivorous flower-visiting bats, even though their utilization of novel food sources in anthropogenically altered habitats is often observed and even discussed as the reason why bats are able to live in some areas. In the present study, we investigated whether adult flower-visiting bats may benefit from social information when learning about a novel food source. We conducted a demonstrator-observer dyad with wild Pallas' long-tongued bats (Glossophaga soricina; Phyllostomidae: Glossophaginae) and hypothesized that naïve individuals would learn to exploit a novel food source faster when accompanied by an experienced demonstrator bat. Our results support this hypothesis and demonstrate flower-visiting bats to be capable of using social information to expand their dietary repertoire.

Night on Earth

Night on Earth

Do Activity Patterns and the Degree of Foraging Specialization Enable Niche Partitioning in Nectarivorous Bats?

Niche partitioning is a strategy that favors the coexistence of sympatric species and prevents resource competition. Resource partitioning not only occurs along a temporal and spatial axis, but also within the niche breadth. The lesser long-nosed (Leptonycteris yerbabuenae) and the Pallas's long-tongued (Glossophaga soricina) bats are sympatric throughout much of their distribution range. Both species can be found in the Mexican tropical dry forest and co-occur during the winter in the pacific coast of Michoacan. These bats have similar requirements but differ in morphological characteristics associated with their particular methods for obtaining food. We evaluate whether these species exhibit niche partitioning in diet and activity patterns during their period of coexistence. Bats were sampled each month from April 2016 to March 2017, and mist-nets were set up at ground level from 19:00 to 03:00 h in Lazaro Cardenas, Michoacan. Diet was determined by taking pollen samples from bat fur and feces, and patterns of daily activity were analyzed. We found greater abundance of bats during November to January, which corresponds to the dry season. This abundance may be associated with a greater availability of floral resources in the study area. Bats fed on nectar from plants of the families Bombacaeae, Fabaceae, Convolvulaceae, Apocynaceae, Cactaceae and Rosaseae. We found no evidence that the diet of the species changes in relation to the presence of potential competitors. However, we found niche partitioning in daily activity patterns of G. soricina related to a high density of L. yerbabuenae.

A New Species of Anoura Gray, 1838 (Chiroptera: Phyllostomidae) from Peru, with Taxonomic and Biogeographic Comments on Species of the Anoura caudifer Complex

Anoura is a Neotropical genus of long-tongued bats containing at least 10 species, whose taxonomy has been revised substantially in recent years. Herein, we describe a new species of Anoura from the Cordillera Oriental of the Peruvian Andes, inhabiting montane forests (Yungas) at 1900–3450 m altitude, along the Rio Cosnipata valley in Manu Biosphere Reserve, Cuzco; where it is sympatric with A. peruana, A. cultrata, and A. caudifer. This new species is most similar to A. caudifer and A. aequatoris, but it is distinguished from them by a unique combination of morphological characters: pelage dark; uropatagium narrow with margins densely furred; foot claws whitish; skull with a long and narrow rostrum; zygomatic arches complete and straight (in lateral view); posterolateral margins of palate without processes; braincase smoothly rounded; first upper premolar (P2) peg-like and separated from the upper canine by a wide gap; second upper premolar (P3) without anterobasal cusp; mandible long, straight, thin and delicate with a large symphysis. Principal Component Analysis separated well the new species from A. aequatoris and A. caudifer. In MANOVA analyses, followed by Bonferroni post-hoc test, the new species differed significantly from A. aequatoris and A. caudifer in six and 11 characters, respectively. The new species and A. aequatoris have montane distributions, whereas A. caudifer occurs at lower elevations. In Peru, the new species and A. aequatoris show disjunct distributions: the former in the central and southern regions, and the latter in the north-central region of the country. This suggests a vicariant effect probably related to the deep Rio Apurimac. Finally, we comment on the taxonomy of the A. caudifer complex, discuss the biogeographical implications of the discovery of the new species, and suggest the recognition of a new region of endemism for small mammals in the southern Yungas, south of the Rio Apurimac to Bolivia.

Tracking host use by bat ectoparasites with stable isotope analysis

We used C and N stable isotopes of nectarivorous bats and their ectoparasites to determine the extent to which parasites depend on the host individual for food. The difference in stable isotope values between parasites and host tissues (Δ13C and Δ15N) was used as a proxy of host use. First, we tested the hypothesis that movement among individual Mexican long-tongued bats (Choeronycteris mexicana Tschudi, 1844) is more likely to occur in winged flies than in mites as indicated by higher host–parasite isotopic Euclidian distance (ED). Second, we tested the hypothesis that ectoparasite species in two coexisting bat species representing the C3 (Geoffroy’s tailless bat, Anoura geoffroyi Gray, 1838) and the CAM (lesser long-nosed bat, Leptonycteris yerbabuenae Martínez and Villa-R., 1940) food chains were monoxenous as indicated by their isotopic values. We also examined Δ13C and Δ15N of individual parasites in relation to 13C and 15N reference enrichment factors as an indication of host switching. In general, flies in C. mexicana had higher ED and wider ranges of individual Δ13C and Δ15N than mites, suggesting that host switching occurred to a larger extent. Most ectoparasites species collected in both coexisting bats were monoxenous, but one fly species appears to be oligoxenous. Individual Δ13C and Δ15N values varied widely in these parasite species, suggesting movements within species hosts.

Learning where to feed: the use of social information in flower-visiting Pallas' long-tongued bats (Glossophaga soricina).

Social learning is a widespread phenomenon among vertebrates that influences various patterns of behaviour and is often reported with respect to foraging behaviour. The use of social information by foraging bats was documented in insectivorous, carnivorous and frugivorous species, but there are little data whether flower-visiting nectarivorous bats (Phyllostomidae: Glossophaginae) can acquire information about food from other individuals. In this study, we conducted an experiment with a demonstrator-observer paradigm to investigate whether flower-visiting Pallas' long-tongued bats (Glossophaga soricina) are able to socially learn novel flower positions via observation of, or interaction with, knowledgeable conspecifics. The results demonstrate that flower-visiting G. soricina are able to use social information for the location of novel flower positions and can thereby reduce energy-costly search efforts. This social transmission is explainable as a result of local enhancement; learning bats might rely on both visual and echo-acoustical perception and are likely to eavesdrop on auditory cues that are emitted by feeding conspecifics. We additionally tested the spatial memory capacity of former demonstrator bats when retrieving a learned flower position, and the results indicate that flower-visiting bats remember a learned flower position after several weeks.

Resource landscape and spatio‐temporal activity patterns of a plant‐visiting bat in a Costa Rican lowland rainforest

We studied the home-range size and activity patterns of brown long-tongued bats Glossophaga commissarisi (Phyllostomidae) in the lowland rainforest of Costa Rica and related this to local nectar and fruit resource distribution. Home ranges were determined using radiotelemetry and food plants within were mapped. Within home ranges of 12.5 ± 6.7 ha, G. commissarisi used mainly small foraging areas of 3.0 ± 1.0 ha. Spatial use within foraging areas correlated for most bats with nectar and fruit resource density. Flight time and duration of flight phases were significantly lower for individuals feeding in a clearing with high abundance of nectar resources compared with those feeding in secondary rainforest with a lower nectar resource density. Our results indicate that G. commissarisi closely matches its flight activity to the available resource distribution.

A First Assessment of Home Range and Foraging Behaviour of the African Long-Tongued Bat Megaloglossus woermanni (Chiroptera: Pteropodidae) in a Heterogeneous Landscape within the Lama Forest Reserve, Benin

We investigated spatial use and foraging behaviour of the nectarivorous African long-tongued bat, Megaloglossus woermanni (Chiroptera: Pteropodidae), in the Lama Forest Reserve, southern Benin, West Africa. We monitored movement and activity patterns of two males and two females that were fitted with position-sensitive radio transmitters for five to nine nights within a three-month study period. The study site comprised the central patch of relatively undisturbed forest (‘Noyau Central’), and a mosaic of orchards, agroforestry plantations, and degraded forests surrounding the central patch. Spatial use of M. woermanni was characterized by small home ranges and high site-fidelity. Mean home range sizes (minimum convex polygon) were larger in females (139.0 and 146.8 ha) than in males (99.8 and 102.9 ha). Throughout the study period, long-tongued bats were frequently observed visiting flowers of cultivated bananas. The mean foraging areas (95% density kernel) of females (39.0 and 109.4 ha) were much larger than in males (12.3 and 14.1 ha). Difference in core areas (50% density kernel) between the sexes was less marked (both females: 6.8 ha, males: 2.7 and 2.9 hectares). Core areas constituted only a small part of home ranges (2.6–4.9%). Large segments of the home ranges were only used for commuting flights between discrete resource patches. Our study provides, for the first time, information on home ranges and foraging behaviour of the sole obligate nectar-drinking bat in Africa.

A nectar-feeding mammal avoids body fluid disturbances by varying renal function

To maintain water and electrolyte balance, nectar-feeding vertebrates oscillate between two extremes: avoiding overhydration when feeding and preventing dehydration during fasts. Several studies have examined how birds resolve this osmoregulatory dilemma, but no data are available for nectar-feeding mammals. In this article, we 1) estimated the ability of Pallas's long-tongued bats (Glossophaga soricina; Phyllostomidae) to dilute and concentrate urine and 2) examined how water intake affected the processes that these bats use to maintain water balance. Total urine osmolality in water- and salt-loaded bats ranged between 31 +/- 37 mosmol/kgH(2)O (n = 6) and 578 +/- 56 mosmol/kgH(2)O (n = 2), respectively. Fractional water absorption in the gastrointestinal tract was not affected by water intake rate. As a result, water flux, body water turnover, and renal water load all increased with increasing water intake. Despite these relationships, glomerular filtration rate (GFR) was not responsive to water loading. To eliminate excess water, Pallas's long-tongued bats increased water excretion rate by reducing fractional renal water reabsorption. We also found that rates of total evaporative water loss increased with increasing water intake. During their natural daytime fast, mean GFR in Pallas's long-tongued bats was 0.37 ml/h (n = 10). This is approximately 90% lower than the GFR we measured in fed bats. Our findings 1) suggest that Pallas's long-tongued bats do not have an exceptional urine-diluting or -concentrating ability and 2) demonstrate that the bats eliminate excess ingested water by reducing renal water reabsorption and limit urinary water loss during fasting periods by reducing GFR.

Ammonia Excretion Increased and Urea Excretion Decreased in Urine of a New World Nectarivorous Bat with Decreased Nitrogen Intake

We determined the effect of water and nitrogen intake on nitrogenous waste composition in the nectarivorous Pallas's long-tongued bat Glossophaga soricina (Phyllostomidae) to test the hypothesis that bats reduce excretion of urea nitrogen and increase the excretion of ammonia nitrogen as nitrogen intake decreases and water intake decreases. Because changes in urine nitrogen composition are expected only in animals whose natural diets are low in nitrogen and high in water content, we also measured maintenance nitrogen requirements (MNR). We hypothesized that, similar to other plant-eating vertebrates, nectarivorous bats have low MNR. Our nitrogen excretion hypothesis was partly proved correct. There was an increase in the proportion of N excreted as ammonia and a decrease in the proportion excreted as urea in low-nitrogen diets. The proportion of N excreted as ammonia and urea was independent of water intake. Most individuals were ureotelic (n = 28), and only a few were ureo-ammonotelic (n = 3) or ammonotelic (n = 2). According to our nitrogen requirement hypothesis, apparent MNR (60 mg kg(-0.75) d(-1)) and truly digestible MNR (54 mg N kg(-0.75) d(-1)) were low. A decrease in urea excretion in low-nitrogen diets may result from urea recycling from liver to the gut functioning as a nitrogen salvage system in nectarivorous bats. This mechanism probably contributes to the low MNR found in Pallas's long-tongued bats.

Effect of diet quality on carbon and nitrogen turnover and isotopic discrimination in blood of a New World nectarivorous bat

Diet composition of carbon and nitrogen (C:N) could affect diet-tissue isotopic discrimination and elemental turnover rate in consumers but studies that test the nature of these changes are scarce. We compared carbon and nitrogen isotopic discrimination and turnover rates in individuals of Pallas' long-tongued bats Glossophaga soricina fed diets with protein soya isolate or amaranth grains as their main source of protein. Diets were of similar protein biological value but the soya diet had higher nitrogen content (2.2%N) and lower C:N ratio (39.6) than the amaranth diet (1.3%N, C:N=40.5). Most bats on the soya diet gained body mass whereas most bats on the amaranth diet lost body mass. Half-lives of carbon (24.3+/-3.8 days) and nitrogen (25.6+/-4.4 days) in bats switched to the soya diet were very similar. In contrast, in the bats switched to the amaranth diet, carbon half-life (39.7+/-3.4 days) was longer than that of nitrogen (25.0+/-6.0 days). The enrichment in 15N between diet and blood was higher when bats were fed the amaranth diet (4.4+/-0.2 per thousand) than when they were fed the soya diet (3.3+/-0.2 per thousand). Similarly, bats on the amaranth diet had higher 13C enrichment (2.0+/-0.2 per thousand) than bats on the soya diet (0.1+/-0.1 per thousand). Our results support recent hypotheses of the effect of nutrition on diet-tissue isotopic discrimination and turnover rate, and further shows that blood stable isotope analysis is an adequate approach to track seasonal dietary shifts in wild bats.

Physiological Constraint to Food Ingestion in a New World Nectarivorous Bat

We investigated the intake response of the nectarivorous Pallas's long-tongued bat Glossophaga soricina to different nectar concentrations to test the hypothesis that bats show compensatory feeding. Bats were offered sucrose solutions between 146 and 1,168 mmol L(-1). Contrary to our expectations, long-tongued bats did not show compensatory feeding, suggesting that volumetric food intake is physiologically constrained. Energy intake was lower at the most dilute solutions (146-584 mmol L(-1)) and then remained relatively constant at more concentrated diets (876 and 1,168 mmol L(-1)). The shape of the observed intake response was very similar to the one predicted by a model dependent on intestinal morphology and in vitro sucrase activity. However, the model predicted higher volumetric food intake at the lower concentrations tested, which suggests that the intestines of the bats were not functioning to their full capacity. Rates of sucrose hydrolysis and water processing probably constrain food intake in long-tongued bats as diets get more dilute.

Differential transport of embryos and degenerating ova by the oviducts of the long-tongued bat, Glossophaga soricina

Female long-tongued bats which had been maintained in sexually segregated groups in captivity for more than 8 months were bred and killed at various intervals between Days 1 and 25 post coitum. Their reproductive tracts were then examined histologically. In 20 of the 28 bats carrying tubal embryos the remnants of 1-4 other ova were also observed in the oviductal ampullae. These remnants consisted of intact zonae pellucidae containing cellular debris, empty zonae, and/or zona fragments. Since long-tongued bats are monovular, the remnants had apparently been retained in the oviducts from previous, non-fertile reproductive cycles. In 27 of the 31 bats carrying implanting blastocysts, zonae pellucidae probably shed by the embryos had been retained in the oviducts. The remnants of 1-3 ova were also observed in the oviductal ampullae of 22 of the 31 bats carrying uterine blastocysts. In at least 14 of these bats the embryos had by-passed ovum remnants in the oviducts on their way to the uterus. No evidence of such remnants was found in the oviducts of 17 animals with tubal or uterine embryos, although old, as well as new, CL were present in the ovaries.

An outbreak of leptospirosis among U. S. army troops in the Canal Zone.

Summary Serological studies were conducted on 29 leptospiral isolates obtained during an epidemiological investigation of an outbreak of human leptospirosis. The isolates were derived from urine of 2 of 6 patients, from 1 of 15 samples of surface water obtained at the locus of infection and from 15 of 106 trapped mammals as follows: 11 of 27 spiny rats (Proechimys semispinosus), 2 of 14 spiny pocket mice (Liomys adspersus), 1 of 3 opossums (Didelphis marsupialis) and 1 of 3 four-eyed opossums (Philander opossum). No leptospiras were isolated from 49 short-tailed bats (Carollia perspicillata), 6 small-eared bats (Micronycteris megalotis), and 4 long-tongued bats (Glossophaga soricina). On the basis of cross-agglutination and agglutinin adsorption tests, seven different and hitherto unreported serologic types were classified and designated as follows: serotype bravo (hyos group) isolated from man, spiny rat and spiny pocket mouse; serotype weaveri (icterohaemorrhagiae group) isolated from man and spiny rat; serotypes canalzoni (cynopteri group) isolated from spiny rat, spiny pocket mouse and four-eyed opossum; kobbe (bataviae group) isolated from spiny rat; serotype pomona, subserotype tropica, isolated from spiny rat and spiny pocket mouse; maru (hebdomadis group) isolated from spiny rat and surface water; and panama (possible new group) isolated from opossum. Evidence of mixed infections was obtained in five animals. The bacteriological findings affirmed previous serological indications that Panama is an area of multiple leptospirosis.