Limiting similarity and species assemblages in the short-tailed fruit bats

We analyzed the morphometrics of seven taxa of short-tailed fruit bats Chiroptera : Phyllostomidae : Carollia , ( Carollia benkeithi , Carollia brevicauda , Carollia castanea , Carollia perspicillata azteca , Carollia perspicillata perspicillata , Carollia sowelli and Carollia subrufa ) to assess within-taxon variation and to address the possibility that morphological distinctions facilitate sympatry within this genus of ecologically similar bats. Whereas morphological similarities were found among species in certain combinations of allopatric taxa, members of sympatric assemblages differ significantly, indicating that there is a consistent representation of morphotypes within various assemblages of Carollia despite changes in species composition across the range of the genus. Furthermore, the differences in the skull size and shape among taxa correspond to potential differences in food-handling abilities and point to dietary differentiation among species as a factor in the facilitation of coexistence.     

Comparative phylogeography of short-tailed bats (Carollia: Phyllostomidae)

This is the first study of comparative phylogeography involving closely related species of Neotropical bats of the family Phyllostomidae. We compared patterns of geographical variation within the five species of fruit-eating bats currently recognized in the genus Carollia using the complete mitochondrial cytochrome-b gene. Our results suggest that the combined effect of the uplift of the Andes and the Panamanian land bridge has been as important for bats as for terrestrial mammals in shaping present-day biodiversity in the New World tropics. Species in this genus can be arranged in two highly supported clades, with a deep subdivision within each that corresponds well to differences across the Andes. We found three congruent phylogeographical patterns across species in this genus. First, the closer relationship between samples from western Ecuador and those from Central America, compared with populations east of the Andes in C. brevicauda, C. castanea and C. perspicillata. Second, the likelihood of a similar timing in South America for the arrival and diversification of C. brevicauda and C. perspicillata from their Central America ancestors. Third, the expansion of C. perspicillata and C. sowelli into northwestern Central America in the relatively recent past. Using a molecular clock, with rates ranging from 2.3 to 5% per 10(6) years, diversification within Carollia would have occurred over the last 1-4.5 Myr. These estimates agree well with the last rise of the Northern Andes and the Panama isthmus.     

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.     

Nutrition or detoxification: why bats visit mineral licks of the Amazonian rainforest

Many animals in the tropics of Africa, Asia and South America regularly visit so-called salt or mineral licks to consume clay or drink clay-saturated water. Whether this behavior is used to supplement diets with locally limited nutrients or to buffer the effects of toxic secondary plant compounds remains unclear. In the Amazonian rainforest, pregnant and lactating bats are frequently observed and captured at mineral licks. We measured the nitrogen isotope ratio in wing tissue of omnivorous short-tailed fruit bats, Carollia perspicillata, and in an obligate fruit-eating bat, Artibeus obscurus, captured at mineral licks and at control sites in the rainforest. Carollia perspicillata with a plant-dominated diet were more often captured at mineral licks than individuals with an insect-dominated diet, although insects were more mineral depleted than fruits. In contrast, nitrogen isotope ratios of A. obscurus did not differ between individuals captured at mineral lick versus control sites. We conclude that pregnant and lactating fruit-eating bats do not visit mineral licks principally for minerals, but instead to buffer the effects of secondary plant compounds that they ingest in large quantities during periods of high energy demand. These findings have potential implications for the role of mineral licks for mammals in general, including humans.     

Dyssochroma viridiflorum (Solanaceae): a reproductively bat-dependent epiphyte from the Atlantic rainforest in Brazil

Few Neotropical plant species seem to depend on the same animal type both for pollination and seed dispersal, and the known instances refer mostly to birds as the agents in these two phases of a plant reproductive cycle. Dyssochroma viridiflorum (Solanaceae), an epiphyte endemic to the Atlantic rainforest in south-eastern Brazil, was found to be visited by phyllostomid bats for nectar as well as for fruits, with the pollination and seed dispersal of the plant ensured by these flying mammals. The greenish flowers open at night and are visited by the nectar-feeding bat Glossophaga soricina, whereas the yellowish-white fruits are consumed by two species of fruit-eating bats, Carollia perspicillata and Sturnira lilium. Only clinging visits, an uncommon behavioural pattern for glossophagine bats while feeding on flowers, were recorded. The small seeds of D. viridiflorum are swallowed along with the fruit pulp and later defecated on the bats' flying pathways. It is suggested that species of Dyssochroma and two other solanaceous bat-pollinated genera, Merinthopodium and Trianaea, form a derived and bat-dependent clade within the Juanulloeae.     

Preliminary Information on the Home Range and Movement Patterns of Sturnira lilium (Phyllostomidae) in a Naturally Fragmented Landscape in Bolivia

Here, we used radiotelemetry to determine home range and movement patterns of the frugivorous bat Sturnira lilium in a naturally fragmented landscape in Beni, Bolivia. Four females were monitored for up to 7 d. Based on 575 radiotelemetry positions, kernel home ranges were between 36.5 and 90.7 ha. During each night, bats visited most of their home range, which included forest islands and continuous forest; however activity was concentrated in core-use areas representing 6–12 percent of the home ranges. There was moderate overlap in home range and core-use areas among the four females. The mean long axis across the kernel home ranges was 1324 m. The results reported here show that S. lilium is able to move freely among forest elements in the landscape while crossing a savanna matrix. Hence, S. lilium may contribute to maintain connectivity and ecological processes in a fragmented landscape.     

Home Range of Dobsonia minor (Pteropodidae): A Solitary, Foliage–roosting Fruit Bat in Papua New Guinea

Lesser bare–backed bats (Dobsonia minor [Pteropodidae]) are solitary and roost in foliage of understory and subcanopy trees in lowland rain forest. These 70–90 gram frugivorous bats forage in primary and secondary forest and in abandoned gardens. At the Kau Wildlife Area in Papua New Guinea, movements (N = 1041) of four males and four females fitted with radio transmitters were monitored for 1 to 18 months. Mean home range within 30–day sampling periods was 5.1 ha (N = 12). There were no significant differences in home ranges by sex or by dry–wet season. Females, however, had significandy larger mean core–use areas than males (1.43 ± 0.61 and 0.65 ±0.16 ha, respectively). There was moderate overlap in home range and core–use areas among some simultaneously tracked animals. The long axes of home ranges varied from 150 to 1150 m and the mean was significantly larger in females. Individuals commuted from day roosts to multiple feeding areas, sometimes resulting in disjunct core–use areas and home ranges. Fruits of native Fiats species and the exotic shrub Piper attuncum were staple food items. Piper aduncum grew as dense clusters within early successional habitats, and individual plants ripened 5–20 fruits per night throughout the year. Ficus spp. grew in primary and secondary forest and fruited asynchronously, but individual trees produced tens to thousands of ripe fruits over 7 to 10 days. Three adult female D. minor were tracked over multiple periods spanning 2.5–18 months. Although each female continued to visit a core–use area containing P. aduncum throughout the study, turnover of other core–use areas reflected the ephemeral locations of fruiting fig trees.     

The effect of unripe fruits on ripe fruit removal by birds in Pistacia terebinthus: flag or handicap?

The shrub Pistacia terebinthus produces crowded infructescences with up to several hundred fruits, which are bright red when unripe and turn green when ripe. Most fruits contain an empty seed and never reach maturity. More ripe fruits were removed by birds from experimental bicolored fruit displays (consisting of infructescences with ten ripe fruits and stripped of unripe fruits, paired with infructescences with only unripe fruits) than from monocolored ones (single infructescences with ten ripe fruits and stripped of unripe fruits). Thus, the presence of unripe fruits seems to increase the conspicuousness or attractiveness of fruit displays to fruit-eating birds. A second experiment compared ripe fruit removal from experimental infructescences having only ripe fruits, with that from control infructescences containing both ripe fruits and natural numbers of unripe fruits, all on P. terebinthus plants. Unlike the first experiment, each bicolored display in this case consisted of a single infructescence with both unripe and ripe fruits. A higher proportion of ripe fruits was removed by birds from infructescences free of unripe fruits. This result suggests that the presence of unripe fruits reduces the accessibility of ripe fruits for fruit-eating birds. This is further supported by field observations of bird foraging behavior.     

Trapped in the darkness of the night: thermal and energetic constraints of daylight flight in bats

Bats are one of the most successful mammalian groups, even though their foraging activities are restricted to the hours of twilight and night-time. Some studies suggested that bats became nocturnal because of overheating when flying in daylight. This is because--in contrast to feathered wings of birds--dark and naked wing membranes of bats efficiently absorb short-wave solar radiation. We hypothesized that bats face elevated flight costs during daylight flights, since we expected them to alter wing-beat kinematics to reduce heat load by solar radiation. To test this assumption, we measured metabolic rate and body temperature during short flights in the tropical short-tailed fruit bat Carollia perspicillata at night and during the day. Core body temperature of flying bats differed by no more than 2°C between night and daytime flights, whereas mass-specific CO(2) production rates were higher by 15 per cent during daytime. We conclude that increased flight costs only render diurnal bat flights profitable when the relative energy gain during daytime is high and risk of predation is low. Ancestral bats possibly have evolved dark-skinned wing membranes to reduce nocturnal predation, but a low degree of reflectance of wing membranes made them also prone to overheating and elevated energy costs during daylight flights. In consequence, bats may have become trapped in the darkness of the night once dark-skinned wing membranes had evolved.     

Menstruation in short-tailed fruit bats (Carollia spp.).

Uterine function was assessed histologically in Carollia spp. removed from a laboratory breeding colony. The uteri of periovulatory bats examined on days 1-3 post coitum varied considerably depending upon whether regressing corpora lutea were present. In females lacking such corpora lutea, the endometrium was shallow and proliferative. In most of the bats having regressing corpora lutea, the endometrium was thicker and necrotic portions of the superficial lamina functionalis were being sloughed off with associated bleeding (i.e. in the form of a true menstrual process). The presence of regressing corpora lutea and well-developed endometria in these animals indicated that short-tailed fruit bats are spontaneous ovulators with a functional luteal phase to their cycles. Menstruation was also observed in some females that were not periovulatory, or that lacked regressing corpora lutea. The endometrium was not vascularized by spiral arterioles, but it did contain distinctive granulocytes similar to those observed in catarrhine primates and other menstruating bats. Most endometrial growth occurred after ovulation and, in pregnant animals, was associated with retention of the embryos in the oviducts for approximately 13-16 days. Carollia perspicillata normally produces one young at a time, after a gestation period of about 4 months, and is a seasonal breeder in the wild. Menstruation probably provides this bat with an efficient mechanism for eliminating a well-developed endometrium from its simplex uterus in the event of fertilization failure or early embryonic loss. This may give the female another chance to establish a pregnancy and produce an infant at a reasonably opportune time during the same breeding season.     

Attraction of Fruit-Eating Bats with Essential Oils of Fruits: A Potential Tool for Forest Restoration

Previous tests with essential oils from ripe chiropterochoric fruits suggested they can be used to attract and capture fruit-eating bats inside forest remnants. Here we evaluated the efficiency of these oils to attract frugivorous bats to open areas. We performed field tests with artificial fruits impregnated with essential oils of the genera Piper or Ficus that were attached to two groups of mist-nets set 50 m outside the border of a forest remnant. One group of artificial fruits received the corresponding oil isolated through hydrodistillation and the other received water only. Fruits with oils attracted significantly more fruit-eating bats, especially Artibeus lituratus that regularly crosses open habitats to reach other forest remnants. The highly significant attraction of A. lituratus by the oil of Piper was unexpected, since this bat is a specialist on Ficus fruits. We hypothesize that in habitats with no fruit available it is possible to attract frugivorous bats with the odor of several ripe fruit species. Furthermore, we verified that almost half of the individuals captured defecated seeds, indicating that the oils also attract recently fed bats, even when their preferred food is available nearby. This technique potentially may increase seed rain at specific locations, being particularly promising to restoration projects.     

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

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

Normal embryonic development of the Japanese pipistrelle, Pipistrellus abramus

The normal embryonic development of the Japanese pipistrelle, Pipistrellus abramus was described. A total of 13 stages between the early pharyngula and the embryo just before birth were established, based on external morphological features of 33 embryonic specimens. To aid embryological comparison between chiropteran lineages, the stage numbers used in the Carollia perspicillata embryonic staging system (Cretekos et al., 2005) were applied to each embryonic stage of P. abramus. The size (crown-rump length, CRL) of P. abramus embryos became larger throughout ontogeny at a relatively constant rate. When the CRL of embryos was compared in each morphologically corresponding embryonic stage, the CRL of P. abramus was always smaller than that of C. perspicillata. The overall nature of organogenesis was almost similar in both P. abramus and C. perspicillata. Species-specific differences in bats were observed at later stages of embryogenesis, notably in the craniofacial and tail regions.     

Efficiency of facultative frugivory in the nectar-feeding bat Glossophaga commissarisi: the quality of fruits as an alternative food source

The efficiency of food exploitation correlates positively with the extent of dietary specialization. Neotropical nectar-feeding bats (Glossophaginae) have one of the most specialized diets among mammals, as floral nectar constitutes a sugar-rich and highly digestible but protein and fiber depleted food source. However, dietary constraints, such as a temporary scarcity of nectar, or protein demands may sometimes require the uptake of alternative food items. We investigated the influence of a diet switch from nectar to fruit on intestinal morphology, body mass, and energy budget in the nectar-feeding bat Glossophaga commissarisi and quantified feeding efficiency. We hypothesized that these nectar specialists depend on a constant supply of nectar, if they were lacking the ability for morphological and physiological plasticity in response to a fiber-rich diet. Although capable of harvesting infructescences of Piper hispidum, G. commissarisi was less efficient in extracting energy from fruits (48% digestive efficiency of total fruit energy content) than from nectar (c. 99% digestive efficiency). The intestinal morphology and organ masses did not change after bats were switched from nectar to fruits. Captive bats exhibited lower daily energy expenditures and flight activity when feeding on fruits than during nectarivory. Possibly, this may have been a deliberate regulation to balance reduced feeding efficiency, or simply the consequence of extended digestive pauses. The low digestibility of Piper, in combination with slow digestion and the bats’ inability for morphological and physiological plasticity may cause nectar-feeders to reduce their maximum energy expenditure when feeding on fruits. We argue that although fruits may substitute for nectar, they may cause restricted maximum energy assimilation compared with nectar.     

Small-Scale Fragmentation Effects on Local Genetic Diversity in Two Phyllostomid Bats with Different Dispersal Abilities in Panama

Habitat fragmentation is one of the greatest threats to biodiversity. Despite their importance for conservation, the genetic consequences of small-scale habitat fragmentation for bat populations are largely unknown. In this study, we linked genetic with ecological and demographic data to assess the effects of habitat fragmentation on two species of phyllostomid bats ( Uroderma bilobatum and Carollia perspicillata ) that differ in their dispersal abilities and demographic response to fragmentation. We hypothesized that population differentiation and the effect of habitat fragmentation on levels of genetic diversity will be a function of the species' mobility. We sequenced mtDNA from 232 bats caught on 11 islands in Gatún Lake, Panamá, isolated from the mainland for ca 90 yr, and in adjacent, continuous forest on the mainland. Populations of both species showed significant genetic differentiation ( F _ST). Consistent with our prediction, population subdivision was lower in the highly mobile U. bilobatum ( F _ST= 0.01) compared to the less vagile C. perspicillata ( F _ST= 0.06), and only the latter species showed a pattern indicative of isolation by distance and, in addition, an effect of fragmentation. Genetic erosion as a result of fragmentation was also only detectable in the less mobile species, C. perspicillata , where haplotype diversity was lower in island compared to mainland populations. Our results suggest that some Neotropical bat species are prone to loss of genetic variation in response to anthropogenic small-scale habitat fragmentation. In this context, our findings point toward mobility as a good predictor of a species' vulnerability to fragmentation and altered population genetic structure.     

Bat flies on phyllostomid hosts in the Cerrado region: component community, prevalence and intensity of parasitism

Streblidae flies are specialised parasites of bat hosts, mainly phyllostomids. There is a high richness of streblids in the savannah-like Cerrado region; however, there is little quantitative data available in parasitological indices. Here, we describe the component community, prevalence and intensity of a streblid infestation on a phyllostomid bat assemblage in Serra da Bodoquena, a Cerrado region in Southwest Brazil. We conducted surveys by capturing and inspecting bat hosts during the seven-month period between October 2004-December 2005. All the ectoparasites found on the bats were collected in the field and then counted and identified in the laboratory. We captured 327 bats belonging to 13 species, of which eight species were parasitized by 17 species of streblids. Carollia perspicillata and Glossophaga soricina were infested with seven streblid species, whereas the other bat species were infested with four or fewer streblid species. Megistopoda proxima and Aspidoptera falcata flies were found on Sturnira lilium, and Trichobius joblingi was the most prevalent fly on C. perspicillata. Megistopoda aranea and Aspidoptera phyllostomatis were highly prevalent and had a high intensity of infestation on Artibeus planirostris. Overall comparisons of the available data suggest that the component communities of streblids vary more between the Cerrado and Atlantic Forest phytogeographical regions than between localities within the same phytogeographical region.     

Ultrastructure of spermatogenesis in the short‐tailed fruit bat,Carollia perspicillata (Chiroptera: Phyllostomidae: Carollinae)

Among species of the Chiroptera, spermatogenesis and the fully differentiated spermatozoa differ in morphological and ultrastructural detail. This study therefore aimed to ultrastructurally characterize the spermatogenesis and the spermatozoa of Carollia perspicillata (Phyllostomidae) and compare the process with other species of bats and mammals. The differentiation of spermatogonia is similar to other bats and to Primates, with three main spermatogonia types: A_d, A_p, and B. Meiotic divisions proceed similarly to those of most mammals and spermiogenesis is clearly divided into 12 steps, in the middle of the range of developmental steps for bats (9–16 steps). The process of acrosome formation is similar to that found in Platyrrhinus lineatus, with the acrosome formed by two different types of proacrosomal vesicles. The ultrastructure of the spermatozoon is similar to other bats already described and resembles the typical mammalian sperm model; however, its morphology differs from other mammals such as marsupials and rodents, on account of a simpler spermatozoon head morphology, which indicates a pattern that is more closely related to the sperm cells of humans and other primates. Our data demonstrated that spermatogenesis in C. perspicillata presents great ultrastructural similarities to P. lineatus. This pattern is not surprising, because both species belong to the same family (Phyllostomidae); however, it is observed that C. perspicillata presents some characteristics that are more closely related to phylogenetically distant species, such as Myotis nigricans (Vespertilionidae), which is a fact that deserves attention. J. Morphol. 275:111–123, 2014. © 2013 Wiley Periodicals, Inc.     

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.     

Bat Community in a Cave From Eastern Brazil,Including a New Record of Lionycteris (Phyllostomidae,Glossophaginae)

A cave bat community from a semiarid region in eastern Brazil was studied during the dry season. A high diversity was observed, with thirteen species recorded. Except for Micronycteris minuta and Lionycteris spurrelli, these bats were also found in other Brazilian karstic areas. The commonest species were the hematophague Desmodus rotundus, the omnivore Carollia perspicillata, and the insectivore Natalus stramineus. The bats formed itinerant colonies, moving frequently inside the cave. L. spurrelli was previously known from Amazonia, usually associated with evergreen forests. The present record extends its range 1600 km to the south. A disjunct distribution explains some morphological differentiation between Amazonia and Olhos d'Água cave populations. The latter may be a relict of former continuous forest vegetation, which has been fragmented after the climatic optimum. Dispersion through the Cerrado forest gallery is also possible.     

Cecropia as a food resource for bats in French Guiana and the significance of fruit structure in seed dispersal and longevity

Cecropia (Cecropiaceae) is a Neotropical genus of pioneer plants. A review of bat/plant dispersal interactions revealed that 15 species of Cecropia are consumed by 32 species of bats. In French Guiana, bats were captured in primary and secondary forests, yielding 936 fecal samples with diaspores, among which 162 contained fruits of C. obtusa, C. palmata, and C. sciadophylla. A comparative morphological and anatomical study of fruits and seeds taken directly from herbarium specimens, bat feces, and an experimental soil seed bank was made. Contrary to previous reports, the dispersal unit of Cecropia is the fruit not the seed. Bats consume the infructescence, digest pulp derived from the enlarged, fleshy perianth, and defecate the fruits. The mucilaginous pericarp of Cecropia is described. The external mucilage production of Cecropia may facilitate endozoochory. The exocarp and part of the mesocarp may be lost after passage through the digestive tract of bats, but fruits buried for a year in the soil seed bank remain structurally unchanged. Fruit characters were found to be useful for identifying species of bat-dispersed Cecropia. Bat dispersal is not necessary for seed germination but it increases seed survival and subsequent germination. Fruit structure plays a significant role in seed longevity.