Elisabeth K. V. Kalko

Bats host major mammalian paramyxoviruses

The large virus family Paramyxoviridae includes some of the most significant human and livestock viruses, such as measles-, distemper-, mumps-, parainfluenza-, Newcastle disease-, respiratory syncytial virus and metapneumoviruses. Here we identify an estimated 66 new paramyxoviruses in a worldwide sample of 119 bat and rodent species (9,278 individuals). Major discoveries include evidence of an origin of Hendra- and Nipah virus in Africa, identification of a bat virus conspecific with the human mumps virus, detection of close relatives of respiratory syncytial virus, mouse pneumonia- and canine distemper virus in bats, as well as direct evidence of Sendai virus in rodents. Phylogenetic reconstruction of host associations suggests a predominance of host switches from bats to other mammals and birds. Hypothesis tests in a maximum likelihood framework permit the phylogenetic placement of bats as tentative hosts at ancestral nodes to both the major Paramyxoviridae subfamilies (Paramyxovirinae and Pneumovirinae). Future attempts to predict the emergence of novel paramyxoviruses in humans and livestock will have to rely fundamentally on these data. Supplementary information The online version of this article (doi:10.1038/ncomms1796) contains supplementary material, which is available to authorized users.

Plasticity in echolocation signals of European pipistrelle bats in search flight: implications for habitat use and prey detection

We studied the echolocation and hunting behavior of three aerial insectivorous species of bats (Vespertilionidae: Pipistrellus) in the field in order to characterize the signals used by the bats and to determine how call structure varies in relation to habitat structure (“uncluttered” versus “cluttered” space). We documented free-flying, naturally foraging wild pipistrelles in various habitats using multiflash stereophotography combined with simultaneous sound recordings. Then we reconstructed the bats flight position in three-dimensional space and correlated it with the corresponding echolocation sequences. In all three species of pipistrelles, signal structure varied substantially. In echolocation sequences of the search phase we found a consistent association of signal types with habitat types. In uncluttered habitats (obstacles more than 5 m from the bat) pipistrelles emitted almost exclusively narrowband signals with bandwidths less than 15 kHz. In cluttered habitats (obstacles less than 5 m from the bat) they switched to signals with bandwidths of more than 15 kHz. Wideband signals were also used when the bats were turning in cluttered and uncluttered spaces and for an instant after turning away from obstacles. Prey detection occured only when the outgoing signal did not overlap with the returning echo from potential prey. The bats also avoided overlap of echoes from potential prey and obstacles. Based on the results of this study, we propose an overlap-free “window” within which pipistrelles may detect potential prey and which allows predictions of minimum distances to prey and clutter-producing objects.

Human Betacoronavirus 2c EMC/2012–related Viruses in Bats, Ghana and Europe

We screened fecal specimens of 4,758 bats from Ghana and 272 bats from 4 European countries for betacoronaviruses. Viruses related to the novel human betacoronavirus EMC/2012 were detected in 46 (24.9%) of 185 Nycteris bats and 40 (14.7%) of 272 Pipistrellus bats. Their genetic relatedness indicated EMC/2012 originated from bats.

The echolocation and hunting behavior of Daubenton's bat, Myotis daubentoni

SummaryThe echolocation and hunting behavior of Daubentons bat (Myotis daubentoni) were studied in the field under completely natural conditions using a multiflash photographic system synchronized with high-speed tape recordings. The hunting behavior of M. daubentoni is separated into four stages. In the search flight stage Daubentons bat flies with an average speed of 3.4±0.6 m/s SD usually within 30 cm over water surfaces searching for insects. After the detection of potential prey, the approach flight stage occurs, during which the bat approaches the target in a goal-directed flight. The stage tail down indicates that M. daubentoni is close to the potential prey (approximately 10–22 cm) and is preparing for the catch. The insects are caught with the interfemoral membrane, the feet, and sometimes with the additional aid of a wing. In the stage head down, the bat seizes the prey during flight. Immediately afterwards, Daubentons bat returns to search flight. M. daubentoni shows the typical echolocation behavior of a vespertilionid bat, emitting frequency-modulated (FM) echolocation signals. The three behavioral stages search, approach, and terminal phase (Griffin et al. 1960) are used to describe the pulse pattern of foraging M. daubentoni in the field. The terminal phase (or buzz) of Daubentons bat is separated into two parts: buzz I and buzz II. Buzz II is distinguished from buzz I by the following characteristics: a sharp drop in terminal frequency, a distinct reduction in the bandwidth of the first harmonic, a continuous high repetition rate throughout the phase in the range 155–210 Hz, very short pulses (0,25–0.3 ms) and interpulse intervals (4.5–5.0 ms) at the end of the phase, and a distinct decrease in duty cycle. A pause in echolocation separates the end of the terminal phase from the ongoing search phase. The reduction in sound duration after the detection of a target and during pursuits with successfull or attempted catches is discussed in relation to the actual distance of the bat to the target at each stage. It is likely that Daubentons bat reduces sound duration during approach and terminal phase in order to prevent an overlap of an outgoing pulse with the returning echo from the target. It is argued that the minimum detection distance can be estimated from the sound duration during search flight. Estimates of detection and reaction distances of M. daubentoni based upon synchronized photos and echolocation sequences are given to corroborate this hypothesis. An average detection distance of 128 cm and an average reaction distance of 112 cm were determined. Each behavioral stage of foraging M. daubentoni is characterized by a distinct pattern of echolocation signals and a distinct stage in hunting behavior. The approach flight in hunting behavior coincides with the approach phase and with buzz I in echolocation behavior. The stage tail down corresponds to buzz II. The stage head down is correlated with a pause in echolocation. Immediately afterwards, the bat returns into search flight and into the search phase, emitting search signals.

CHAPTER 16 – Organization, Diversity, and Long-Term Dynamics of a Neotropical Bat Community

The study of processes that influence the distribution, diversity, and abundance of species is one of the most challenging and complex fields in biology. Many basic questions are still controversial. As the results of an increasing number of studies clearly demonstrate, good data on temporal and spatial variability in community composition and species abundance are essential for formulating and evaluating hypotheses about the processes determining organization of communities and diversity of species. However, recent studies indicate that ecomorphologically similar species may be clearly differentiated by behavioral traits such as spatial segregation in habitat use, roost site selection, foraging strategies, and diet. Ecomorphological predictions alone would have placed these species closer together in the community than they actually are. Furthermore, relative abundance of well-sampled species showed individual year-to-year variation. Some frugivorous species with large seasonal variation in numbers may be migratory, but except for one species that declined, long-term population trends remained rather constant. Long-term monitoring of bats at many localities is urgently needed to build databases for intercommunity comparisons.

Bats Limit Arthropods and Herbivory in a Tropical Forest

Previous exclosure studies measuring the top-down control of arthropod abundance and herbivory combined the effects of birds and bats. We experimentally partitioned bird predation from bat predation in a lowland tropical forest in Panama and measured the direct effects (arthropod abundance) and indirect effects (herbivory). The exclusion of birds and bats each directly increased arthropod abundance on plants: Bird-exclosed plants contained 65% more, and bat-exclosed plants 153% more, arthropods than controls. Birds and bats also indirectly increased herbivory: Bird-exclosed plants suffered 67% more, and bat-exclosed plants 209% more, herbivory than controls. We conclude that bats have dramatic ecological effects that were previously overlooked.

Neotropical bats in the canopy: diversity, community structure, and implications for conservation

We compare results of parallel ground and canopy netting of bats (Microchiroptera) in three adjacent forest sites near Belém, Brazil, to document possible differences in vertical distribution of species. We caught 1871 individuals representing 49 species of three families (Emballonuridae, Phyllostomidae, Vespertilionidae). Capture effort, totaling 1955.5 mistnet hours in several cycles over a two-year period, was similar for ground and canopy nets. The canopy rigs yielded more species (n = 41) than the ground nets (n = 35), but both samples were characterized by rank abundance curves with similar shape and with a dominance of frugivores (Phyllostomidae). Nearly half (n = 24) of the species were captured in numbers too small (n < 6) to allow firm classification, but differences in capture frequencies of some of the better-sampled species in high and low nets reveal vertical stratification. Species-specific differences in diet, foraging strategies, roost sites, and sampling bias contribute to this pattern. As a result of the differential use of space among bats, alterations of forest structure are likely to result in changes in structure and function of local bat communities, but our limited knowledge of natural history and ecology of many species limits definition of changes. We see a critical need for further research into the extent to which habitat complexity influences species richness and abundance of bats. This information is especially important in view of the need to develop and apply conservation-oriented programs to maintain biodiversity. A review of recent improvements in techniques for inventorying bats shows that a combination of methods, including mistnetting and acoustic monitoring, is mandatory for such studies.

Insect pursuit, prey capture and echolocation in pipestirelle bats (Microchiroptera)

Abstract The foraging and echolocation behaviour of three European pipistrelles ( Pipistrellus pipistrellus, P. nithusii and P. kuhlii ) was studied under natural conitions. The pipistrelles were photographed with two 35 mm cameras under stroboscopic illumination, and their echolocation signals were recorded simultaneously. This permits a three-dimensional reconstruction of the flight paths of bat and prey, and allows the details of echolocation behaviour to be studied in the context of natureal foraging behaviour. The general relationships between foraging and echolocation behaviour were consistent among the three species. Foraging behaviour consisted of four stages: search flight (before detection of prey), approach flight (pursuit after detection of prey), capture and retrieval of prey. These stages correlated with phases in echolocation behaviour: search, approach, and terminal phase followed by a pause. Detection of prey occurred at distances of 1·14−2·20 m. The search cone extending from the bats mouth was up to 150° wide. The pipistrelles caught prey in mid-air, either with the tail membrane alone or by funnelling it with a wing onto the tail membrane. Except for some intra- and interspecific differences in sound duration, pulse interval, bandwidth and terminal frequency in search phase, the structure and pattern of the echolocation signals were similar in the three pipistrelles. In the approach and terminal phases, pulse duration and pulse interval decreased with the approach to the target, while bandwidth and sweeprate increased. While pursuing insects, the pipistrelles precisely avoided an overlap between outgoing signal and the echo returning from the prey. Furthermore, the bats stopped emitting signals several centimeters before they reached the insect.

Bats Worldwide Carry Hepatitis E Virus-Related Viruses That Form a Putative Novel Genus within the Family Hepeviridae

ABSTRACT Hepatitis E virus (HEV) is one of the most common causes of acute hepatitis in tropical and temperate climates. Tropical genotypes 1 and 2 are associated with food-borne and waterborne transmission. Zoonotic reservoirs (mainly pigs, wild boar, and deer) are considered for genotypes 3 and 4, which exist in temperate climates. In view of the association of several zoonotic viruses with bats, we analyzed 3,869 bat specimens from 85 different species and from five continents for hepevirus RNA. HEVs were detected in African, Central American, and European bats, forming a novel phylogenetic clade in the family Hepeviridae. Bat hepeviruses were highly diversified and comparable to human HEV in sequence variation. No evidence for the transmission of bat hepeviruses to humans was found in over 90,000 human blood donations and individual patient sera. Full-genome analysis of one representative virus confirmed formal classification within the family Hepeviridae. Sequence- and distance-based taxonomic evaluations suggested that bat hepeviruses constitute a distinct genus within the family Hepeviridae and that at least three other genera comprising human, rodent, and avian hepeviruses can be designated. This may imply that hepeviruses invaded mammalian hosts nonrecently and underwent speciation according to their host restrictions. Human HEV-related viruses in farmed and peridomestic animals might represent secondary acquisitions of human viruses, rather than animal precursors causally involved in the evolution of human HEV.

Henipavirus RNA in African bats.

Background Henipaviruses (Hendra and Nipah virus) are highly pathogenic members of the family Paramyxoviridae. Fruit-eating bats of the Pteropus genus have been suggested as their natural reservoir. Human Henipavirus infections have been reported in a region extending from Australia via Malaysia into Bangladesh, compatible with the geographic range of Pteropus. These bats do not occur in continental Africa, but a whole range of other fruit bats is encountered. One of the most abundant is Eidolon helvum, the African Straw-coloured fruit bat. Methodology/Principal Findings Feces from E. helvum roosting in an urban setting in Kumasi/Ghana were tested for Henipavirus RNA. Sequences of three novel viruses in phylogenetic relationship to known Henipaviruses were detected. Virus RNA concentrations in feces were low. Conclusions/Significance The finding of novel putative Henipaviruses outside Australia and Asia contributes a significant extension of the region of potential endemicity of one of the most pathogenic virus genera known in humans.