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Bats: important reservoir hosts of emerging viruses.

Bats (order Chiroptera, suborders Megachiroptera ["flying foxes"] and Microchiroptera) are abundant, diverse, and geographically widespread. These mammals provide us with resources, but their importance is minimized and many of their populations and species are at risk, even threatened or endangered. Some of their characteristics (food choices, colonial or solitary nature, population structure, ability to fly, seasonal migration and daily movement patterns, torpor and hibernation, life span, roosting behaviors, ability to echolocate, virus susceptibility) make them exquisitely suitable hosts of viruses and other disease agents. Bats of certain species are well recognized as being capable of transmitting rabies virus, but recent observations of outbreaks and epidemics of newly recognized human and livestock diseases caused by viruses transmitted by various megachiropteran and microchiropteran bats have drawn attention anew to these remarkable mammals. This paper summarizes information regarding chiropteran characteristics and information regarding 66 viruses that have been isolated from bats. From these summaries, it is clear that we do not know enough about bat biology; we are doing too little in terms of bat conservation; and there remain a multitude of questions regarding the role of bats in disease emergence.

Animals↗

Contribution of BAT and skeletal muscle to thermogenesis induced by ephedrine in man.

This investigation was performed to examine the role of brown adipose tissue (BAT) in thermogenesis induced by ephedrine in man. Light microscopy of biopsies from necropsy cases showed BAT to occur most frequently in the perirenal fat. Perirenal BAT thermogenesis was investigated in five lean men before and during stimulation with 1 mg ephedrine orally X kg body wt-1. Perirenal BAT thermogenesis was assessed by continuous measurements of local temperature and blood flow with the 133xenon clearance method. In the same study the effect of ephedrine on skeletal muscle oxygen consumption was estimated by measurements of leg blood flow and arteriovenous oxygen difference. The perirenal adipose tissue blood flow increased approximately twofold, whereas the local temperature increased approximately 0.1 degrees C on an average. Assuming that man possesses 700 g of BAT with a similar thermogenic capacity, this tissue contributed only 10 ml X min-1 to the 40 ml X min-1 increase in oxygen consumption in the subject whose perirenal BAT showed the most pronounced response to ephedrine. The leg oxygen consumption increased on an average 60% after ephedrine. By extrapolation of this value to whole body skeletal muscle, approximately 50% of the increase in oxygen consumption induced by ephedrine may take place in skeletal muscle. It is concluded that skeletal muscle is a tissue of importance with respect to the thermogenic effect of sympathomimetics in man, whereas the results do not support a major role for perirenal BAT.

Adipose Tissue, Brown↗

Insulin and metabolic efficiency in rats. I. Effects of sucrose feeding and BAT axotomy.

The role of insulin and brown adipose tissue (BAT) thermogenesis in metabolic efficiency (ME, the efficiency of body wt gain) was examined in rats with varied basal insulin status. Long-lasting insulin was administered using a protocol that did not alter food intake, yet increased ME in both groups. Half the rats were fed sucrose to stimulate BAT growth and thermogenesis. Insulin overrode the exaggerated decrease in ME in sucrose-fed diabetics, with only partial attenuation in controls. Interscapular BAT (IBAT) lipoprotein lipase activity was decreased in diabetic rats, restored by insulin treatment, and not affected in controls. Sucrose-fed diabetics and controls had their IBAT sham or bilaterally surgically denervated. Insulin decreased the thermogenic potential of BAT [cytochrome oxidase activity (COA)] in intact controls and diabetics; in the latter, insulin restored COA independent of BAT innervation. We conclude that insulin can increase ME without an associated increase in energy intake, regardless of basal insulin status, both insulin deficiency and excess decrease BAT thermogenic potential (COA), and hyperinsulinemia-induced increases in ME may result from decreased BAT mitochondrial proliferation.

Adipose Tissue, Brown↗

Subcellular localization of prolactin in the anterior pituitary cells of the female Japanese house bat, Pipistrellus abramus.

We investigated the subcellular localization of PRL and GH in the pituitary gland of the female Japanese house bat by the double immunolabeling procedure using the protein A-gold method combined with electron microscopy and demonstrated a seasonal alteration in the distribution of PRL within the cells. The seasonal changes were related to the different phases of the bats' reproductive cycles. Mammosomatotrophs (MS cells) containing both PRL and GH were constantly present throughout the reproductive cycles of the female bats and they were remarkably hypertrophied during pregnancy. The distribution pattern of PRL and GH within the MS cells was extremely variable owing to the different phases of reproductive cycles of the bats. We divided MS cells into the following four types: the cell containing 1) only mixed granules containing both PRL and GH, 2) both mixed and PRL granules, 3) mixed, PRL and GH granules, 4) both mixed and GH granules. While pure PRL-containing cells were observed in pregnant and lactating bats, they were not observed in bats obtained during prehibernation, midhibernation, and arousal periods. These results suggest that MS cells in the female bats hypertrophy during pregnancy and that some of them may be transformed into PRL-producing cells.

Animals↗

Low turnover rates of carbon isotopes in tissues of two nectar-feeding bat species.

Stable isotopes of carbon are commonly used to characterize dietary preferences in animals. Because turnover rates of carbon isotopes are related to metabolic rate, we wanted to determine the rates at which carbon isotopes are exchanged in tissues of two species of nectar-feeding bats (Leptonycteris curasoae and Glossophaga soricina), both of which have relatively high mass-specific metabolic rates. To test the hypothesis that isotope turnover is higher in nectar-feeding bats, because of their high mass-specific metabolic rates, than in other eutherian mammals, we conducted diet-switching experiments and chose three target tissues (hair, wing membrane and blood) to evaluate the isotopic turnover rates. We made the following predictions: (1) isotopic composition should change towards higher delta(13)C-values due to the turnover of carbon isotopes of C(3) origin with those of C(4)/CAM origin; (2) the turnover rates of carbon isotopes would differ between the three types of tissues in the following order of decreasing turnover rates: blood>wing membrane>hair; and (3) turnover rates of nectar-feeding bats should exceed those reported for other small mammals because of the high mass-specific metabolic rate of nectar-feeding bats. Compared to the initial diet, target tissues were enriched in heavy carbon isotopes by 2.8 per thousand in L. curasoae and by 2.6 per thousand in G. soricina. After changing the diet from C(3) to C(4)/CAM origin we found an increase in abundance of (13)C in blood and wing membrane in all experimental subjects. The estimated half life of carbon isotope turnover ranged from 100 to 134 days and did not differ significantly between blood and wing membrane, nor did it differ between the two species. The low turnover rate in wing membrane may reflect its specific composition and the relatively low temperature of this tissue, and long-lived erythrocytes in bat blood may be responsible for the low turnover rate of carbon isotopes in blood. The turnover rate of stable carbon isotopes in hair was low in L. curasoae and undetectable in G. soricina, which may be explained by the seasonal growth of the hair in these two species. Because both species are small (10 and 25 g, respectively) and nectar-feeding bats have higher mass-specific metabolic rates than bats in temperate regions or similar sized terrestrial mammals, our findings of low turnover rates were unexpected.

Analysis of Variance↗

'Binaural echo disparity' as a potential indicator of object orientation and cue for object recognition in echolocating nectar-feeding bats.

Echolocating bats emit ultrasonic calls through their mouth or their nostrils and receive echoes from objects with both their ears. Information conveyed in the echoes is the basis for their three-dimensional acoustic perception of the surroundings. The direction of an object is encoded in binaural echo differences, i.e. on the one hand in the different arrival times of its echo at the two ears, and on the other hand in spectral differences through direction-dependent frequency filtering of head and pinnae. Insufficient attention has been paid, however, to the fact that three-dimensional objects produce structured spatial echo fields, and that the position of the ear in this field determines the echo it receives. We were interested to determine whether the two ears, in addition to direction-specific echo differences, receive object-specific echo disparities that might be useful for the bat. Our measurements with an artificial bat head, which consisted of two microphones and a small ultrasound loudspeaker arranged to resemble a bat's ears and mouth, revealed that echoes at the two ears differed largely depending on the shape and orientation of the echo-giving object. Binaural echo disparities of a bat-pollinated flower did indeed carry information about the orientation and, to a lesser extent, the shape of the flower. During flower approach such object-specific binaural echo disparities even exceed the binaural differences encoding direction of echo incidence, because the echo from the flower in front undergoes the same directional filtering by the two symmetrical ears. Nectar-feeding bats could use these object-specific binaural echo disparities not only to determine the object's orientation relative to the approaching bat, facilitating flight planning, but also to improve object recognition through spatial reconstruction of details of the object creating the echo. Our results suggest that the evaluation of binaural echo disparity has a greater importance for these tasks than has previously been assumed.

Animals↗

Lack of generalization of object discrimination between spatial contexts by a bat.

Discrimination and generalization are important elements of cognition in the daily lives of animals. Nectar-feeding bats detect flowers by olfaction and probably vision, but also use echolocation and echo-perception of flowers in immediate target surroundings. The echo received from an interference-rich flower corolla is a function of a bat's own relative position in space. This raises the question how easily a free-flying bat will generalize an echo stimulus from a learning situation to a new spatial context where differences in relative flight approach trajectories may lead to an unfamiliar spectral composition of the self-generated echoes. We trained free-flying Glossophaga soricina in echoacoustic discrimination in a two-alternative forced-choice (2-AFC) paradigm at location A. We then tested at location B for spontaneous transfer of discrimination ability. Bats did not spontaneously transfer the discrimination ability acquired at A to location B. This lack of spontaneous generalization may have been caused by factors of the underlying learning mechanisms. 2-AFC tasks may not be representative of the natural foraging behaviour of flower-visiting bats. In contrast to insect-eating bats that constantly evaluate the environment to detect unpredictable prey, the spatial stability of flowers may allow flower visitors to rely on spatial memory to guide foraging. The 2-AFC task requires the disregard (learned irrelevance) of salient spatial location cues that are different at each new location. In Glossophaga, a conjunction between spatial context and 2-AFC discrimination learning may have inhibited the transfer of learned irrelevance of spatial location in the 2-AFC task to new spatial locations. Alternatively, the bats may have learnt the second discrimination task completely anew, and were faster only because of an acquired learning set. We suggest a dissociation between 2-AFC task acquisition and novel object discrimination learning to resolve the issue.

Animals↗

Echolocation and passive listening by foraging mouse-eared bats Myotis myotis and M. blythii.

The two sibling mouse-eared bats, Myotis myotis and M. blythii, cope with similar orientation tasks, but separate their trophic niche by hunting in species-specific foraging microhabitats. Previous work has shown that both species rely largely on passive listening to detect and glean prey from substrates, and studies on other bat species have suggested that echolocation is ;switched off' during passive listening. We tested the hypothesis that mouse-eared bats continuously emit echolocation calls while approaching prey. Echolocation may be needed for orientation while simultaneously listening for prey. Because these sibling species forage in different microhabitats and eat different prey, we also compared their echolocation behaviour and related it to their ecology. Both species used echolocation throughout prey approach, corroborating a functional role for echolocation during gleaning. Captive bats of both species emitted similar orientation calls, and pulse rate increased during prey approach. Between the search to approach phases, call amplitude showed a sudden, dramatic drop and bats adopted ;whispering echolocation' by emitting weak calls. Whispering echolocation may reduce the risks of masking prey-generated sounds during passive listening, the mouse-eared bats' main detection tactic; it may also avoid alerting ultrasound-sensitive prey. In several cases M. myotis emitted a loud buzz made of 2-18 components when landing. We hypothesise that the buzz, absent in M. blythii at least when gleaning from the same substrate, is used to assess the distance from ground and refine the landing manoeuvre. Our findings have implications for niche separation between sibling species of echolocating bats, support a role for echolocation during passive listening and suggest a functional role for buzzes in landing control.

Animals↗

The gleaning attacks of the northern long-eared bat, Myotis septentrionalis, are relatively inaudible to moths.

This study empirically tests the prediction that the echolocation calls of gleaning insectivorous bats (short duration, high frequency, low intensity) are acoustically mismatched to the ears of noctuid moths and are less detectable than those of aerially hawking bats. We recorded auditory receptor cell action potentials elicited in underwing moths (Catocala spp.) by echolocation calls emitted during gleaning attacks by Myotis septentrionalis (the northern long-eared bat) and during flights by the aerial hawker Myotis lucifugus (the little brown bat). The moth ear responds inconsistently and with fewer action potentials to the echolocation calls emitted by the gleaner, a situation that worsened when the moth's ear was covered by its wing (mimicking a moth resting on a surface). Calls emitted by the aerial-hawking bat elicited a significantly stronger spiking response from the moth ear. Moths with their ears covered by their wings maintained their relative hearing sensitivity at their best frequency range, the range used by most aerial insectivorous bats, but showed a pronounced deafness in the frequency range typically employed by gleaning bats. Our results (1) support the prediction that the echolocation calls of gleaners are acoustically inconspicuous to the ears of moths (and presumably other nocturnal tympanate insects), leaving the moths particularly vulnerable to predation, and (2) suggest that gleaners gain a foraging advantage against eared prey.

Acoustics↗

Heterothermy, torpor, respiratory gas exchange, water balance and the effect of feeding in Gould's long-eared bat Nyctophilus gouldi.

The effects of temperature and nutritional status on the metabolic rate of Nyctophilus gouldi were examined. Bats fed marked meals first defecated approximately 1.34 h after feeding and were calculated to have a mean retention time of 5.38 +/- 0.57 h but to be truly post-absorptive after 9 h. Over the temperature range 1-35 degrees C, the metabolic rate (Vo2) and body temperature (Tb) of fasted bats were extremely labile. Below 30 degrees C, the bats all entered torpor and between 10 and 15 degrees C showed a mean 84% reduction over the maximal Vo2. Body temperature was also minimal over this range (Tb = 12.5 degrees C, Ta = 10-15 degrees C). Both total and dry thermal conductance increased in a curvilinear manner with temperature, total conductance from 3.38 +/- 0.65 J g-1 h-1 degree C-1 at 1 degree C to 24.25 +/- 1.99 J g-1 h-1 degree C-1 at 35 degrees C (mean +/- S.E.M.), while the rate of evaporative water loss increased with Ta by a maximum of 10-fold from 0.21 mg g-1 h-1 at 5 degrees C to 2.69 mg g-1h-1 at 35 degrees C. Between 10 and 25 degrees C, intermittent respiration characterised by episodic bouts of breathing/gas exchange and periods of apnoea with no measurable Vo2 occurred. Although the duration of apnoea decreased when temperature was increased, the volume of oxygen taken up in each episode did not change. Mean respiratory exchange ratio (RER) was low (0.64-0.77) in post-absorptive bats, typical of fat utilisation, but during torpor ranged from near 0 to near 2, indicating discontinuous and disproportional gas exchange. Feeding produced a condition of relatively sustained homeothermy and high RER in the bats which persisted for 9 h, after which the N. gouldi became torpid. Immediately after feeding, the Vo2 of the bats increased fivefold above the post-absorptive level, while the Vco2 increased by more than eightfold. Similarly, body temperature also increased, declining to torpid values after 9. The RER in immediately post-feeding bats was near 1.0 but subsequently declined to near 0.7, indicating a switch from carbohydrate to fat utilisation. Therefore, the N. gouldi were heterothermic, exhibited a highly labile metabolic rate, and rates of heat and water loss, and Tb which were influenced both by ambient temperature and by nutritional status.

Animal Feed↗

The peripheral auditory characteristics of noctuid moths: responses to the search-phase echolocation calls of bats

The noctuid moths Agrotis segetum and Noctua pronuba show peak auditory sensitivity between 15 and 25 kHz, and a maximum sensitivity of 35 dB SPL. A. segetum shows a temporal integration time of 69 ms. It is predicted that bats using high-frequency and short-duration calls will be acoustically less apparent to these moths. Short-duration frequency-modulated (FM) calls of Plecotus auritus are not significantly less acoustically apparent than those of other FM bats with slightly longer call durations, based on their combined frequency and temporal structure alone. Long-duration, high-frequency, constant-frequency (CF) calls of Rhinolophus hipposideros at 113 kHz are significantly less apparent than those of the FM bats tested. The predicted low call apparency of the 83 kHz CF calls of R. ferrumequinum appears to be counteracted by their long duration. It is proposed that two separate mechanisms are exploited by bats to reduce their call apparency, low intensity in FM bats and high frequency in CF bats. Within the FM bats tested, shorter-duration calls do not significantly reduce the apparency of the call at the peripheral level, though they may limit the amount of information available to the central nervous system.

Journal Article↗

Variations in respiratory muscle activity during echolocation when stationary in three species of bat (Microchiroptera: Vespertilionidae).

Echolocating bats use respiratory muscles to power the production of biosonar vocalisations. The physical characteristics of these calls vary among species of bat, and variations also exist in the timing and patterns of respiratory muscle recruitment during echolocation. We recorded electromyograms from the respiratory muscles of three species of bat (Family Vespertilionidae) while the animals vocalised from stationary positions. Activity was recorded consistently from the lateral abdominal muscles (internal abdominal oblique and transversus abdominis) from all calling bats, but we found much variation within and among species. Bats in the family Vespertilionidae devoted longer periods of expiratory muscle activity to each call than did the mormoopid bat Pteronotus parnellii. These differences correlate negatively with the duration of calls. We suggest that morphological adaptations in some bats may facilitate the economic production of echolocation calls at rest.

Abdominal Muscles↗

Molecular epidemiological analysis of bat rabies viruses in Brazil.

A molecular epidemiological analysis was performed in 19 rabies viruses (RVs) isolated from haematophagous, frugivorous and insectivorous bats, in Sao Paulo, Brazil. The authors carried out RT-PCR for amplification of the RV nucleoprotein (N) gene, and determined 1,335 nucleotide sequences of N gene by direct sequencing method. Phylogenetic analysis, which was based on the N gene of Brazilian RV isolates identified presently and previously, revealed that RVs isolated from bats were genetically divided into four lineages had a tendency to depend on the host bat species. The first lineage consisted mainly of haematophagous bat (Desmodus rotundus) isolates, including frugivorous bat (Artibeus spp.) isolates. Other three lineages consisted of insectivorous bat isolates; mainly Eptesicus spp., Molossus spp. and Nyctinomops spp. isolates, respectively. These results indicate a possibility of that there are bat species-specific RV variants in Brazil.

Animals↗

Delayed development in Fischer's pygmy fruit bat, Haplonycteris fischeri, in the Philippines.

A long delay in post-implantation embryonic development was detected in Fischer's pygmy fruit bats (palaeotropical fruit bats of the suborder Megachiroptera), the first time such a delay has been demonstrated outside the bat suborder Microchiroptera. Samples of bats were obtained from the Philippines over 5 years, and reproductive tracts were preserved and examined using standard histological techniques. Most parous female pygmy bats were impregnated in June, within a few weeks of parturition, and the embryos underwent superficial implantation at the anterior end of the uterus contralateral to the previously gravid uterus. Shortly thereafter, the rate of embryonic growth slowed tremendously for up to 8 months. During the period of delay, the mean length of the embryoblast increased only from 280 microns to 520 microns. In March of the following year, the developmental rate increased, and the embryos completed development in the next 3 months. The 8-month delay gives these bats a gestation period of 11.5 months, the longest known in bats. Most nulliparous females become pregnant at an age of 3-5 months, and their embryos entered a similar delay that terminated in March or April, after 2-6 months of delay. Males showed signs of fertility throughout the entire year, but testis volume was highest during May, June and July, at about the time when most females become receptive.

Animals↗

Bat rabies in the north-northwestern regions of the state of São Paulo, Brazil: 1997-2002.

OBJECTIVE: Reports on bat rabies in Brazil are sporadic and isolated. This study aimed at describing the detection of rabies virus in bats in the state of São Paulo. METHODS: A total of 7,393 bats from 235 municipalities of the north and northwestern areas of the state of São Paulo, Southeastern Brazil, were assessed according to their morphological and morphometric characteristics from 1997 to 2002. Fluorescent antibody test and mice inoculation were used for viral identification. RESULTS: Of all samples examined, 1.3% was rabies virus positive, ranging from 0.2% in 1997 to 1.6% in 2001. There were found 98 bats infected, 87 in the urban area. Fluorescent antibody test was detected in 77 positive samples, whereas 92 produced rabies signs in mice; incubation period ranging from 4 to 23 days. In 43 cities at least one rabid bat was observed. The highest proportion (33.7%) of rabies virus was found in Artibeus lituratus. Eptesicus and Myotis were the most frequent positive species (24.5%) of the Vespertilionidae family. The species Molossus molossus and Molossus rufus showed 14.3% positive bats. There were no differences in the distribution of positive rabies between females (33; 48.5%) and males (35; 51.5%). CONCLUSIONS: Rabies-infected bats were found in environments that pose a risk to both human and domestic animal population and there is a need for actions aiming at the control of these species and public education.

Animals↗

Common vampire bat attacks on humans in a village of the Amazon region of Brazil.

Many people in Amazonian communities have reported bat bites in the last decade. Bites by vampire bats can potentially transmit rabies to humans. The objective of this study was to analyze factors associated with bat biting in one of these communities. A cross-sectional survey was conducted in a village of gold miners in the Amazonian region of Brazil (160 inhabitants). Bats were captured near people's houses and sent to a lab. Of 129 people interviewed, 41% had been attacked by a bat at least once, with 92% of the bites located on the lower limbs. A logistic regression found that adults were bitten around four times more often than children (OR = 3.75, CI 95%: 1.46-9.62, p = 0.036). Males were bitten more frequently than females (OR = 2.08, CI 95%: 0.90-4.76, p = 0.067). Nine Desmodus rotundus and three frugivorous bats were captured and tested negative for rabies. The study suggests that, in an area of gold miners, common vampire bats are more likely to attack adults and males. The control strategy for human rabies developed in this region should therefore place special emphasis on adult males. There should also be more research on how the search for gold in the Amazonian region places people and the environment at risk.

Adult↗

Control of sex steroid-binding protein (SBP) in the male little brown bat: relationship of plasma thyroxine levels to the induction of plasma SBP in immature males.

The seasonally reproductive male little brown bat (Myotis lucifugus lucifugus) exhibits marked increases in plasma concentrations of sex steroid-binding protein (SBP) in the spring following arousal from hibernation. In this species an increase in SBP levels is induced prematurely in male bats aroused during the first half of hibernation and housed under long photoperiods; however, this rise is inhibited in bats housed under short photoperiods. In order to investigate the physiological role of the thyroid gland in the regulation of plasma SBP activity, plasma total thyroxine (T4) and SBP concentrations were determined in immature male little brown bats prematurely aroused from the first half of hibernation and maintained on either a short or long photoperiod. For this purpose a radioimmunoassay for the measurement of total T4 in bat plasma was established and validated. The results showed that immature male little brown bats aroused prematurely from hibernation and housed under a long spring-like photoperiod exhibited marked increases in plasma T4 and SBP concentrations, while animals housed under a short photoperiod showed only marginal increases in SBP, and plasma T4 remained undetectable. These results suggest that the thyroid gland, through the action of T4, may normally play an important role in the control of the post-arousal rise in plasma SBP concentrations in the little brown bat.

Animals↗

Noradrenergic and cholinergic nerves in the uterus of the Japanese long-fingered bat, Miniopterus schreibersii fuliginosus, change with reproductive cycle.

The pattern of uterine innervation by noradrenergic (NA) and acetylcholinesterase-positive (AChE) nerves in different reproductive stages of the adult Japanese long-fingered bats were investigated histochemically and immunohistochemically. In the non-pregnant bat, the uterine horn was supplied with abundant NA and AChE nerves. These two types of nerves were closely associated with the uterine arteries and myometrial smooth muscles. In the pregnant bat, NA and AChE nerves supplying the uterus did not degenerate much during hibernating period, but reduced markedly after arousal. In the postpartum bat, the density of nerves recovered progressively. The significant change in the innervation pattern of uterine NA and AChE nerves in the pregnant bats under and after hibernation, and in the postpartum bat must be considered in relation to the adrenergic and cholinergic controlling mechanisms on the uterine function that is matched for the unique reproductive cycle of this bat.

Acetylcholinesterase↗