No fever and leucocytosis in response to a lipopolysaccharide challenge in an insectivorous bat

Bat immune systems may allow them to respond to zoonotic agents more efficiently than other mammals. As the first line of defence, the taxonomically conserved acute phase immune reaction of leucocytosis and fever is crucial for coping with infections, but it is unknown if this response is a key constituent to bat immunological success. We investigated the acute phase reaction to a standard lipopolysaccharide (LPS) challenge in Pallas''s mastiff bats (Molossus molossus). Challenged bats lost mass, but in contrast to other mammals showed no leucocytosis or fever. There also was no influence on body temperature reduction during torpor. When compared to recent genome-wide assays for constituent immune genes, this lack of a conserved fever response to LPS contributes to a clearer understanding of the innate immune system in bat species and of the coevolution of bats with a wide diversity of pathogens.     

Allometric patterning in the limb skeleton of bats: Implications for the mechanics and energetics of powered flight

Allometric analysis was employed to compare linear dimensions of forelimb and hindlimb bones (humeri, radii, third and fifth metacarpals, third and fifth manual phalanges, femora, and tibiae) of 227 species of bats and 105 species of nonvolant mammals of varying degrees of phylogenetic affinity to bats. After accounting for body size, all forelimb bones are longer in bats than in nonvolant species, with the exception of humeri and radii of a few highly arboreal primates. Hindlimb bones are generally, but not uniformly, shorter in bats than in other mammals. For the humerus, radius, and metacarpals, midshaft diameters are greater in bats than in their comparably sized relatives. Proximal phalangeal midshaft diameters are statistically indistinguishable from those of other mammals, and distal phalanges show significantly reduced outer diameters. The pattern of relative reduction in wing bone diameters along the wing's proximodistal axis parallels the reduction in bone mineralization along the same axis, and a similar pattern of change in cortical thickness from the smallest wall thicknesses among mammals in the humerus and radius to the greatest wall thicknesses among mammals in the phalanges. The combination of altered cross-sectional geometry and mineralization appears significantly to reduce the mass moment of inertia of the bat wing relative to a theoretical condition in which elongated bones preserve primitive mammalian mineralization levels and patterns of scaling of long bone diameters. This intercorrelated suite of skeletal specializations may significantly reduce the inertial power of flight, contributing significant energetic savings to the total energy budgets of the only flying mammals. J. Morphol. 234: 277–294, 1997. © 1997 Wiley-Liss, Inc.     

Bat fly species richness in Neotropical bats: correlations with host ecology and host brain

Patterns of ectoparasite species richness in mammals have been investigated in various terrestrial mammalian taxa such as primates, ungulates and carnivores. Several ecological or life traits of hosts are expected to explain much of the variability in species richness of parasites. In the present comparative analysis we investigate some determinants of parasite richness in bats, a large and understudied group of flying mammals, and their obligate blood-sucking ectoparasite, streblid bat flies (Diptera). We investigate the effects of host body size, geographical range, group size and roosting ecology on the species richness of bat flies in tropical areas of Venezuela and Peru, where both host and parasite diversities are high. We use the data from a major sampling effort on 138 bat species from nine families. We also investigate potential correlation between bat fly species richness and brain size (corrected for body size) in these tropical bats. We expect a relationship if there is a potential energetic trade-off between costly large brains and parasite-mediated impacts. We show that body size and roosting in cavities are positively correlated with bat fly species richness. No effects of bat range size and group size were observed. Our results also suggest an association between body mass-independent brain size and bat fly species richness. Electronic supplementary material  The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

Three‐dimensional stratification pattern in an old‐growth lowland forest: How does height in canopy and season influence temperate bat activity?

The study of animal–habitat interactions is of primary importance for the formulation of conservation recommendations. Flying, gliding, and climbing animals have the ability to exploit their habitat in a three‐dimensional way, and the vertical canopy structure in forests plays an essential role for habitat suitability. Forest bats as flying mammals may seasonally shift their microhabitat use due to differing energy demands or changing prey availability, but the patterns are not well understood. We investigated three‐dimensional and seasonal habitat use by insectivorous bats in a temperate lowland old‐growth forest, the Belovezhskaya Pushcha in Belarus. We acoustically sampled broadleaved and mixed coniferous plots in the forest interior and in gaps in three heights during two reproductive periods (pregnancy/lactation vs. postlactation). In canopy gaps, vertical stratification in bat activity was less pronounced than in the forest interior. Vertical activity patterns differed among species. The upper canopy levels were important foraging habitats for the open‐space forager guild and for some edge‐space foragers like the Barbastelle bat Barbastella barbastellus and the soprano pipistrelle Pipistrellus pygmaeus. Myotis species had highest activity levels near the ground in forest gaps. Moreover, we found species‐dependent seasonal microhabitat shifts. Generally, all species and species groups considered except Myotis species showed higher activity levels during postlactation. Myotis species tended toward higher activity in the forest interior during postlactation. P. pygmaeus switched from high activity levels in the upper canopy during pregnancy and lactation to high activity levels near the ground during postlactation. We conclude that a full comprehension of forest bat habitat use is only possible when height in canopy and seasonal patterns are considered.     

An exception to the rule: common vampire bats do not learn taste aversions

Conditioned taste aversions function by preventing an organism from ingesting a food previously associated with gastrointestinal malaise. Taste-aversion learning has been observed in many animals: molluscs to mammals, insects to birds. However, among mammals, neither bats nor monophagous species have been investigated adequately. Here we show that although three dietary generalists (one insectivorous and two frugivorous bats) readily acquired taste aversions, the common vampire bat, Desmodus rotundus, a monophageous feeder on vertebrate blood, did not learn to associate a novel flavour with aversive gastrointestinal events. We interpret these data as consistent with the hypothesis that taste aversions are an adaptive specialization of learning. Copyright 2003 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.      

Ear morphology of the frog-eating bat (Trachops cirrhosus,family: Phyllostomidae): Apparent specializations for low-freqency hearing

The frog-eating bat (Trachops cirrhosus) is unusual among bats studied because of its reliance on low-frequency (<5 kHz) sounds emitted by frogs for prey localization. We investigated the ear of this bat in order to identify anatomical features that might serve as adaptations for low-frequency hearing. Trachops cirrhosus has a variety of anatomical features that might enhance low-frequency hearing, either by increasing sensitivity to low-frequency sounds or expanding the total frequency range to include lower frequencies. These bats have long pinnae, and a long and wide basilar membrane. The basal portion of the basilar membrane is much stiffer than the apical portion, and the basal portion of the tectorial membrane is more massive than the apical portion. There is also a concentration of mass in the apical portion of the cochlea. T. cirrhosus possesses the largest number of cochlear neurons reported for any mammal, the second highest density of cochlear neurons innervation known among mammals, and three peaks of cochlear neuron density. Other bats have two peaks of cochlear neuron density, lacking the apical concentration, while other mammals usually have only one. T. cirrhosus differs from most other small mammals and bats in characteristics of the apical portion of the cochlea, i.e., that area where the place theory of hearing predicts that low frequencies are detected.     

Social Grooming in Bats: Are Vampire Bats Exceptional?

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

Seasonal reliance on nectar by an insectivorous bat revealed by stable isotopes

Many animals have seasonally plastic diets to take advantage of seasonally abundant plant resources, such as fruit or nectar. Switches from insectivorous diets that are protein rich to fruits or nectar that are carbohydrate rich present physiological challenges, but are routinely done by insectivorous songbirds during migration. In contrast, insectivorous bat species are not known to switch diets to consume fruit or nectar. Here, we use carbon stable isotope ratios to establish the first known case of a temperate bat species consuming substantial quantities of nectar during spring. We show that pallid bats (Antrozous pallidus) switch from a diet indistinguishable from that of sympatric insectivorous bat species in winter (when no cactus nectar is present) to a diet intermediate between those of insectivorous bats and nectarivorous bats during the spring bloom of a bat-adapted cactus species. Combined with previous results that established that pallid bats are effective pollinators of the cardon cactus (Pachycereus pringlei), our results suggest that the interaction between pallid bats and cardon cacti represents the first-known plant-pollinator mutualism between a plant and a temperate bat. Diet plasticity in pallid bats raises questions about the degree of physiological adaptations of insectivorous bats for incorporation of carbohydrate-rich foods, such as nectar or fruit, into the diet.     

Adaptive Evolution of the Hox Gene Family for Development in Bats and Dolphins

Bats and cetaceans (i.e., whales, dolphins, porpoises) are two kinds of mammals with unique locomotive styles and occupy novel niches. Bats are the only mammals capable of sustained flight in the sky, while cetaceans have returned to the aquatic environment and are specialized for swimming. Associated with these novel adaptations to their environment, various development changes have occurred to their body plans and associated structures. Given the importance of Hox genes in many aspects of embryonic development, we conducted an analysis of the coding regions of all Hox gene family members from bats (represented by Pteropus vampyrus, Pteropus alecto, Myotis lucifugus and Myotis davidii) and cetaceans (represented by Tursiops truncatus) for adaptive evolution using the available draft genome sequences. Differences in the selective pressures acting on many Hox genes in bats and cetaceans were found compared to other mammals. Positive selection, however, was not found to act on any of the Hox genes in the common ancestor of bats and only upon Hoxb9 in cetaceans. PCR amplification data from additional bat and cetacean species, and application of the branch-site test 2, showed that the Hoxb2 gene within bats had significant evidence of positive selection. Thus, our study, with genomic and newly sequenced Hox genes, identifies two candidate Hox genes that may be closely linked with developmental changes in bats and cetaceans, such as those associated with the pancreatic, neuronal, thymus shape and forelimb. In addition, the difference in our results from the genome-wide scan and newly sequenced data reveals that great care must be taken in interpreting results from draft genome data from a limited number of species, and deep genetic sampling of a particular clade is a powerful tool for generating complementary data to address this limitation.     

Characterizing Pneumocystis in the Lungs of Bats: Understanding Pneumocystis Evolution and the Spread of Pneumocystis Organisms in Mammal Populations

Bats belong to a wide variety of species and occupy diversified habitats, from cities to the countryside. Their different diets (i.e., nectarivore, frugivore, insectivore, hematophage) lead Chiroptera to colonize a range of ecological niches. These flying mammals exert an undisputable impact on both ecosystems and circulation of pathogens that they harbor. Pneumocystis species are recognized as major opportunistic fungal pathogens which cause life-threatening pneumonia in severely immunocompromised or weakened mammals. Pneumocystis consists of a heterogeneous group of highly adapted host-specific fungal parasites that colonize a wide range of mammalian hosts. In the present study, 216 lungs of 19 bat species, sampled from diverse biotopes in the New and Old Worlds, were examined. Each bat species may be harboring a specific Pneumocystis species. We report 32.9% of Pneumocystis carriage in wild bats (41.9% in Microchiroptera). Ecological and behavioral factors (elevation, crowding, migration) seemed to influence the Pneumocystis carriage. This study suggests that Pneumocystis-host association may yield much information on Pneumocystis transmission, phylogeny, and biology in mammals. Moreover, the link between genetic variability of Pneumocystis isolated from populations of the same bat species and their geographic area could be exploited in terms of phylogeography.     

The capacity for paracellular absorption in the insectivorous bat Tadarida brasiliensis

Water-soluble nutrients are absorbed by the small intestine via transcellular and paracellular processes. The capacity for paracellular absorption seems greater in fliers than in nonfliers, although that conclusion rests mainly on a comparison of flying birds and nonflying mammals because only two frugivorous bat species have been studied. Furthermore, the bats studied so far were relatively large (>85 g, compared with most bat species which are <20 g) and were not insectivores (like about 70 % of bat species). We studied the small (11 g) insectivorous bat Tadarida brasiliensis and tested the prediction that the capacity for paracellular absorption would be as high as in the other bat and avian species studied so far, well above that in terrestrial, nonflying mammals. Using standard pharmacokinetic technique, we measured the extent of absorption (fractional absorption = f) of inert carbohydrate probes: L-arabinose (MM = 150.13) absorbed exclusively by paracellular route and 3OMD-glucose (MM = 194) absorbed both paracellularly and transcellularly. As predicted, the capacity of paracellular absorption in this insectivorous bat was high (L-arabinose f = 1.03 ± 0.14) as in other frugivorous bats and small birds. Absorption of 3OMD-glucose was also complete (f = 1.09 ± 0.17), but >80 % was accounted for by paracellular absorption. We conclude that passive paracellular absorption of molecules of the size of amino acids and glucose is extensive in this bat and, generally in bats, significantly higher than that in nonflying mammals, although the exact extent can be somewhat lower or higher depending on molecule size, polarity and charge.     

Handedness of a Motor Program in C. elegans Is Independent of Left-Right Body Asymmetry

Complex animals display bilaterally asymmetric motor behavior, or “motor handedness,” often revealed by preferential use of limbs on one side. For example, use of right limbs is dominant in a strong majority of humans. While the mechanisms that establish bilateral asymmetry in motor function are unknown in humans, they appear to be distinct from those for other handedness asymmetries, including bilateral visceral organ asymmetry, brain laterality, and ocular dominance. We report here that a simple, genetically homogeneous animal comprised of only ∼1000 somatic cells, the nematode C. elegans, also shows a distinct motor handedness preference: on a population basis, males show a pronounced right-hand turning bias during mating. The handedness bias persists through much of adult lifespan, suggesting that, as in more complex animals, it is an intrinsic trait of each individual, which can differ from the population mean. Our observations imply that the laterality of motor handedness preference in C. elegans is driven by epigenetic factors rather than by genetic variation. The preference for right-hand turns is also seen in animals with mirror-reversed anatomical handedness and is not attributable to stochastic asymmetric loss of male sensory rays that occurs by programmed cell death. As with C. elegans, we also observed a substantial handedness bias, though not necessarily the same preference in direction, in several gonochoristic Caenorhabditis species. These findings indicate that the independence of bilaterally asymmetric motor dominance from overall anatomical asymmetry, and a population-level tendency away from ambidexterity, occur even in simple invertebrates, suggesting that these may be common features of bilaterian metazoans.     

Barriers and benefits: implications of artificial night-lighting for the distribution of common bats in Britain and Ireland

Artificial lighting is a particular problem for animals active at night. Approximately 69% of mammal species are nocturnal, and one-third of these are bats. Due to their extensive movements—both on a nightly basis to exploit ephemeral food supplies, and during migration between roosts—bats have an unusually high probability of encountering artificial light in the landscape. This paper reviews the impacts of lighting on bats and their prey, exploring the direct and indirect consequences of lighting intensity and spectral composition. In addition, new data from large-scale surveys involving more than 265 000 bat calls at more than 600 locations in two countries are presented, showing that prevalent street-lighting types are not generally linked with increased activity of common and widespread bat species. Such bats, which are important to ecosystem function, are generally considered ‘light-attracted’ and likely to benefit from the insect congregations that form at lights. Leisler''s bat (Nyctalus leisleri) may be an exception, being more frequent in lit than dark transects. For common pipistrelle bats (Pipistrellus pipistrellus), lighting is negatively associated with their distribution on a landscape scale, but there may be local increases in habitats with good tree cover. Research is now needed on the impacts of sky glow and glare for bat navigation, and to explore the implications of lighting for habitat matrix permeability.     

Group Hunting—A Reason for Sociality in Molossid Bats?

Many bat species live in groups, some of them in highly complex social systems, but the reasons for sociality in bats remain largely unresolved. Increased foraging efficiency through passive information transfer in species foraging for ephemeral insects has been postulated as a reason for group formation of male bats in the temperate zones. We hypothesized that benefits from group hunting might also entice tropical bats of both sexes to live in groups. Here we investigate whether Molossus molossus, a small insectivorous bat in Panama, hunts in groups. We use a phased antenna array setup to reduce error in telemetry bearings. Our results confirmed that simultaneously radiotracked individuals from the same colony foraged together significantly more than expected by chance. Our data are consistent with the hypothesis that many bats are social because of information transfer between foraging group members. We suggest this reason for sociality to be more widespread than currently assumed. Furthermore, benefits from group hunting may also have contributed to the evolution of group living in other animals specialized on ephemeral food sources.     

Molecular Cloning and Evolutionary Analysis of Hemoglobin α-Chain Genes in Bats

Bats are the only mammals with the capacity for powered flight. When flying, they need abundant energy and oxygen. According to previous works, the hemoglobin (Hb) oxygen loading function of bats is insensitive to variations in body temperature, although different bat species have different heat sensitivity. We cloned Hb α-chain sequences from eight bat species to investigate whether they have different characteristics. We found that Hb in the bat lineages is under purifying selection, which accords with the importance of its function in bats. Three turn regions in bat Hb, however, have distinct evolutionary rates compared with those of other mammals, and the codons in these regions have an accelerated rate of evolution. These codons are under divergent selection in bats. These changes in Hb may have occurred in response to the physiological requirements of the species concerned, as adaptations to different lifestyles.     

Winter diet analysis in Rhinolophus euryale (Chiroptera)

We investigated the winter food of Mediterranean horseshoe bats (Rhinolophus euryale) in four winter cave roosts in southern Slovakia and northern Hungary and investigated the relationship between food and ambient temperature. The bats were active during the whole winter period and they produced excrement throughout the entire hibernation period, even when outside temperatures dropped below zero. The guano was in two forms, containing (1) prey items and (2) non-prey items. The identifiable items belonged to lepidopteran species, but only one was identified, on the basis of the genital fragments, the moth Colotois pennaria, which was the main prey species in autumn and early winter. Our results shed light on the extraordinarily high level of activity in this bat species during winter hibernation, which in temperate regions is a strategy that enables bats to survive when prey is reduced or absent. In R. euryale, the torpor in the course of hibernation is not continuous and our results help to explain how energy losses caused by bat movements are covered.