Echolocation by free-tailed bats (Tadarida)

Summary The echolocation of bats in the genusTadarida is highly adaptive to different acoustic conditions. These bats use different types of sonar signals with a diversity usually observed in comparisons across families of bats.Tadarida brasiliensis andT. macrotis search for airborne prey in open, uncluttered spaces using narrow-band, short CF signals with no FM components. They add broadband FM components while dropping the CF components when approaching or capturing prey. Only one harmonic is present in these insect-pursuit signals. When flying in cluttered situations or echolocating in a laboratory room,T. brasiliensis uses multiple-harmonic FM signals. Stationary bats tend to use linear frequency sweeps and moving bats tend to use curvilinear frequency sweeps or linear period sweeps. When emerging from a roost they initially use a short-CF/FM signal, changing to an FM signal as they fly away. The acuity of perception of target range inT. brasiliensis is about 1.0 to 1.5 cm and is determined by the bandwidth of the target-ranging sonar signals as represented by their autocorrelation functions. Many less adaptable species of bats use signals corresponding to part of the sonar repertoire ofTadarida. The functions of short CF or narrowband signals for detection and FM or broadband signals for resolution and acoustic imaging identified from comparisons among such species are confirmed by observations of echolocation byTadarida. The differences observed in echolocation among many species and families of bats appear to be evolutionary adaptations to some of the same features of the acoustic environment to whichTadarida responds behaviorally.Abbreviations CF frequency modulated - FM constant frequency - LPM linear period modulation - LFM linear-frequency modulation We thank Prof. T.T. Sandel, Prof. D.R. Griffin, Dr. George Pollak, and P.H. Dolkart for their advice and assistance. This research was supported by Grant No. BMS 72-02351-A01 from the National Science Foundation and by Biomedical Research Support Grant No. RR-07054 from the Division of Research Resources, National Institutes of Health.     

Pollination by the locally endangered island flying fox (Pteropus hypomelanus) enhances fruit production of the economically important durian (Durio zibethinus)

Fruit bats provide valuable pollination services to humans through a unique coevolutionary relationship with chiropterophilous plants. However, chiropterophily in the Old World and the pollination roles of large bats, such as flying foxes (Pteropus spp., Acerodon spp., Desmalopex spp.), are still poorly understood and require further elucidation. Efforts to protect these bats have been hampered by a lack of basic quantitative information on their role as ecosystem service providers. Here, we investigate the role of the locally endangered island flying fox Pteropus hypomelanus in the pollination ecology of durian (Durio zibethinus), an economically important crop in Southeast Asia. On Tioman Island, Peninsular Malaysia, we deployed 19 stations of paired infrared camera and video traps across varying heights at four individual flowering trees in a durian orchard. We detected at least nine species of animal visitors, but only bats had mutualistic interactions with durian flowers. There was a clear vertical stratification in the feeding niches of flying foxes and nectar bats, with flying foxes feeding at greater heights in the trees. Flying foxes had a positive effect on mature fruit set and therefore serve as important pollinators for durian trees. As such, semi‐wild durian trees—particularly tall ones—may be dependent on flying foxes for enhancing reproductive success. Our study is the first to quantify the role of flying foxes in durian pollination, demonstrating that these giant fruit bats may have far more important ecological, evolutionary, and economic roles than previously thought. This has important implications and can aid efforts to promote flying fox conservation, especially in Southeast Asian countries.     

Roosting ecology and variation in adaptive and innate immune system function in the Brazilian free-tailed bat (<Emphasis Type="Italic">Tadarida brasiliensis</Emphasis>)

Bats have recently been implicated as reservoirs of important emerging diseases. However, few studies have examined immune responses in bats, and even fewer have evaluated these responses in an ecological context. We examined aspects of both innate and adaptive immune response in adult female Brazilian free-tailed bats (Tadarida brasiliensis) at four maternity roosts (two natural caves and two human-made bridges) in south-central Texas. Immune measurements included in vitro bactericidal ability of whole blood and in vivo T cell mediated response to mitogenic challenge. Bactericidal activity in T. brasiliensis varied with roosting ecology, but appears to be sensitive to colony-level effects. Blood from females living at one cave had significantly lower bactericidal ability than blood from females at three other sites. T cell mediated response in this species was associated with variation in roost ecology, with females from two caves having greater responses than females from two bridges. T cell mediated response and bactericidal activity were negatively correlated with one another within individuals that were tested for both. Variation in immunological response of T. brasiliensis is important for understanding the influence of the environment on the frequency and distribution of immunologically competent individuals and for understanding disease-host dynamics in this and other colonial species.     

Echolocation Performance of the Vampire Bat (Desmodus rotundus)

The neotropical vampire bats (Desmodus rotundus) echolocate using ultrasonic pulses like those of the Latin American phyllostomatid bats. In this paper the orally produced echolocation sounds of Desmodus are analysed and the performance of the echolocation system is studied in two-choice training experiments on two vampire bats. Ability to detect objects is relatively limited; both animals were capable of discerning the presence of a 1 cm wide metal strip at a distance of 50 cm, but they failed with 0.5 cm wide strips. The ultrasonic pulses produced at a distance of 50 cm appear to sample an area with a diameter of 2.5 to 3.0 cm (i. e., the solid angle tested with each pulse is 3° to 3° 40′ in extent).     

Comparison of frugivory by howling monkeys (Alouatta palliata) and bats (Artibeus jamaicensis) in the tropical rain forest of Los Tuxtlas,Mexico

Information on the fruit diets of howling monkeys and fruit-eating bats in the tropical rain forest of Los Tuxtlas, Mexico was collected for a year to compare the plant species used. Howling monkeys used 19 plant species whereas bats used 32 plant species as fruit sources. Eleven species were common in the diet of both mammals. A rank analysis at the plant species level showed that the fruit diets of Alouatta and Artibeus were very different. In contrast to bats, howling monkeys displayed a seasonal pattern in fruit consumption. Diet overlap between the two mammals was highest during the monkeys' fruit-eating season. Measures of fruit production in eight trees (four species) indicated marked variations in fruit biomass produced and in length of fruiting from tree to tree and species to species. Peaks in fruit production were typical both at the species and the individual tree levels, demonstrating the very patchy nature of the fruit available to the monkeys and the bats.     

Emergence,Echolocation, Diet and Foraging Behavior of Molossus ater (Chiroptera: Molossidae)1

Between 4 and 16 January 1996, during a period of cool weather, we studied the emergence and foraging behavior of Molossus ater at a site near Akumal, in the Yucatan Peninsula in Mexico. The bats, a colony of at least 32 individuals, roosted in a north-facing cinder block wall, and emerged about sunset. Emerging bats were usually clustered in time, while those returning usually were not. Radio-tracking revealed that the bats foraged for short periods (mean 26.8 min) and captures of returning individuals indicated that 27 of 28 had fed, taking, on average, 4.4 g of insects, mainly hydrophilid beetles. On some nights, few or none of the radio-tagged bats emerged from the roost. Calculations concerning the costs of flight and roosting show that they were more than covered by the energy intake the bats achieved. Molossus ater have high aspect ratio (8.3–9.1) wings and high wing-loadings of 17.55–24.15 N/m². When searching for prey, these bats produce long (12.3 ms), narrowband(3.8 kHz), echolocation calls that sweep from 27.6–23.8 kHz. Energy was not limiting for these bats at the time of our study.     

Histological assessment of cellular immune response to the phytohemagglutinin skin test in Brazilian free-tailed bats (Tadarida brasiliensis)

Bats are known reservoirs for numerous emerging infectious diseases, occupy unique ecological niches, and occur globally except for Antarctica. Given their impact on human and agricultural health, it is critical to understand the mechanisms underlying immunocompetence in this reservoir host. To date, few studies have examined immune function in the Order Chiroptera, particularly among natural colonies of bats. The phytohemagglutinin (PHA) skin test has been widely used to measure delayed-type cellular immune response in a wide variety of vertebrates, and has been routinely employed in immunoecological studies. Although this test is frequently described as a measure of T cell proliferation, recent studies indicate it may represent a combination of immune responses. In mammals, the immune response is differentially, temporally and spatially regulated, therefore, we characterized the infiltrating leukocyte response to the PHA skin test in bats by examining a time-series of histological sections from PHA and saline injection areas in 41 Brazilian free-tailed bats (Tadarida brasiliensis). Results suggest that bats exhibit diverse leukocyte traffic within 6 h, and up to 24 h following subcutaneous PHA injection. There was a significant presence of lymphocytes and neutrophils, as well as eosinophils, basophils, and macrophages observed in the PHA-injected tissues, compared with saline-injected control tissues. We observed a highly significant negative correlation between the number of lymphocytes and neutrophils in PHA-injected tissue, with peak lymphocyte response at 12 h, and peak neutrophil response at 24 h post-injection. These results indicate substantial variation in the immune response of individuals, and may aid our understanding of disease emergence in natural populations of bats.     

Auditory-based defence against gleaning bats in neotropical katydids (Orthoptera: Tettigoniidae)

Neotropical katydids (Orthoptera: Tettigoniidae) are preyed on by gleaning bats, which are known to use male calling songs to locate them. At least one katydid species has been reported to stop singing in response to bat echolocation calls. To investigate the relationship between this behavioural defence and ecological and sensory factors, we surveyed calling song characteristics, song cessation in response to the echolocation calls of a sympatric gleaning bat (Trachops cirrhosus), and T-cell responses (an auditory interneuron sensitive to ultrasound) in five katydid species from Panamá. The two katydid species that stopped singing in response to bat calls (Balboa tibialis and Ischnomela gracilis, Pseudophyllinae) also had the highest T-cell spike number and rate in response to these stimuli. The third pseudophylline species (Docidocercus gigliotosi) did not reliably cease singing and had low T-cell spiking activity. Neoconocephalus affinis (Copiphorinae) produced continuous calling song, possibly preventing males from hearing the bat during singing, and did not show a behavioural response despite high T-cell activity in response to bat calls. Steirodon rufolineatum (Phaneropterinae) did not cease singing and differed in T-cell activity compared to the other species. T-cell function might not be conserved in katydids, and evidence for this idea is discussed.     

Evidence of homing following translocation of long‐tailed bats (Chalinolobus tuberculatus) at Grand Canyon Cave,New Zealand

Abstract

Homing behaviour in the New Zealand long‐tailed bat (Chalinolobus tuberculatus), a temperate insectivorous species, was investigated at Grand Canyon Cave, central North Island. A pilot study of nine adult male bats was conducted to determine whether use of the cave was regular enough for a homing study. Eight bats returned to the cave over the 3‐week monitoring period, six on the night following release. Nine additional bats carrying radio transmitters were then released at three sites (three at each site) c. 5, 10 and 20 km due east of the cave; sites estimated to be located within, on the border of, and outside the population's known familiar area respectively. All but one of these nine bats were subsequently detected at the cave. Results suggest that adult long‐tailed bats are able to return home following displacement both inside and outside their familiar area. Implications of these findings for translocations of bats and the possession of a potential long‐distance navigation system by this species are discussed.     

Torpor, thermal biology, and energetics in Australian long-eared bats (Nyctophilus)

Previous studies have suggested that Australian long-eared bats (Nyctophilus) differ from northern-hemisphere bats with respect to their thermal physiology and patterns of torpor. To determine whether this is a general trait of Australian bats, we characterised the temporal organisation of torpor and quantified metabolic rates and body temperatures of normothermic and torpid Australian bats (Nyctophilus geoffroyi, 7 g and N. gouldi, 10 g) over a range of air temperatures and in different seasons. The basal metabolic rate of normothermic bats was 1.36 ± 0.17 ml g⁻¹ h⁻¹ (N. geoffroyi) and 1.22 ± 0.13 ml g⁻¹ h⁻¹ (N. gouldi), about 65% of that predicted by allometric equations, and the corresponding body temperature was about 36 °C. Below an air temperature of about 25 °C bats usually remained normothermic for only brief periods and typically entered torpor. Arousal from torpor usually occurred shortly after the beginning of the dark phase and torpor re-entry occurred almost always during the dark phase after normothermic periods of only 111 ± 48 min (N. geoffroyi) and 115 ± 66 min (N. gouldi). At air temperatures below 10 °C, bats remained torpid for more than 1 day. Bats that were measured overnight had steady-state torpor metabolic rates representing only 2.7% (N. geoffroyi) and 4.2% (N. gouldi) of the basal metabolic rate, and their body temperatures fell to minima of 1.4 and 2.3 °C, respectively. In contrast, bats measured entirely during the day, as in previous studies, had torpor metabolic rates that were up to ten times higher than those measured overnight. The steady-state torpor metabolic rate of thermoconforming torpid bats showed an exponential relationship with body temperature (r ² = 0.94), suggesting that temperature effects are important for reduction of metabolic rate below basal levels. However, the 75% reduction of metabolic rate between basal metabolic rate and torpor metabolic rate at a body temperature of 29.3 °C suggests that metabolic inhibition also plays an important role. Torpor metabolic rate showed little or no seasonal change. Our study suggests that Australian Nyctophilus bats have a low basal metabolic rate and that their patterns of torpor are similar to those measured in bats from the northern hemisphere. The low basal metabolic rate and the high proclivity of these bats for using torpor suggest that they are constrained by limited energy availability and that heterothermy plays a key role in their natural biology. Accepted: 22 November 1999     

The potential availability of roosting sites for lesser short‐tailed bats (Mystacina tuberculata) on Kapiti Island,New Zealand: Implications for a translocation

Abstract

Lesser short‐tailed bats (Mystacina tuberculata) have recently been translocated to Kapiti Island in an attempt to form a new population of this threatened species. However, the island's vegetation is regenerating, and there was doubt that the forests provided enough large trees with cavities for bats to roost in. This study measured the availability of tree‐trunk cavities of the right size for potential roost sites on Kapiti Island, and assessed if habitat restoration would be required to increase the translocation's chance of success. first, trees with cavities accessible to us were sampled in six of Kapiti Island's forest types. Size variables known to affect roost site selection by lesser short‐tailed bats at the tree and cavity level were measured. Trees were classified as containing cavities that could potentially provide suitable roosts if their values for all variables measured fell within the range of roosts used by lesser short‐tailed bats in natural populations. Roosts were classified as suitably sized for solitary bats or for colonies, using measurements from both types of roosts in natural populations. Second, the density of these potential roost cavities was calculated. Cavities of a size potentially suitable for colonies were found in four of the six forest types at densities ranging from 3.2 ± 3.2 Se to 52.4 ± 14.0 trees per ha. density of potential solitary roosts was much higher. Not all potential cavities will be suitable because they may be damp, poorly insulated, or have an unsuitable microclimate. Nevertheless, our estimates indicated that the two most extensive forest types each contained thousands of potential cavities of a size suitable for colonies of lesser short‐tailed bats. In addition, there were tens of thousands of cavities large enough to shelter solitary bats. Roost habitat restoration appears unnecessary to assist translocated Mystacina tuberculata on Kapiti Island.     

Hibernation by a free-ranging subtropical bat (Nyctophilus bifax)

Knowledge about torpor in free-ranging subtropical bats is scarce and it is widely believed that low and stable ambient temperatures are necessary for prolonged torpor. We present temperature-telemetry data from free-ranging male (n = 4) and female (n = 4) subtropical vespertilionid bats, Nyctophilus bifax (~10 g), exposed to pronounced daily fluctuations of ambient temperature. All bats used torpor on every day in winter and both males and females exhibited multi-day torpor bouts of up to 5.4 days. Although females were larger than males, patterns of torpor were similar in both sexes. Torpor use was correlated with prevailing weather conditions and, on days when bats remained torpid, maximum ambient temperature was significantly lower than on days when bats aroused. Moreover, the duration of interbout normothermic periods at night increased with increasing average nightly ambient temperature. Skin temperature of torpid bats varied by 10.2 ± 3.6°C day⁻¹ (n = 8, N = 47) and daily minimum skin temperature was positively correlated with the daily minimum ambient temperature. Our study shows that prolonged torpor is an important component of the winter ecology of a subtropical bat and that torpor and activity patterns of N. bifax predominantly reflect prevailing weather conditions.     

Behavioral analyses of auditory sensitivity inCycnia tenera Hübner (Lepidoptera: Arctiidae)

Summary The auditory characteristics of the arctiid moth,Cycnia tenera were examined using two behavioral criteria, sound production and flight cessation. The majority of the individuals tested indicated a maximum sensitivity to frequencies between 30 and 50 kHz although there is a substantial degree of interindividual variation.Spectral analyses of the echolocation/hunting cries of two species of sympatric, insectivorous bats,Eptesicus fuscus andMyotis lucifugus reveal maximally intense spectral peaks at 29.3 and 41.9 kHz, respectively.The audiograms offer a behavioral correlation to neural studies done with other species of moths and illustrate the existence of behaviorally expressed intensity discrimination in these insects. The variation evident between individuals may represent the differential response characteristics reported for free-flying tympanate moths in field conditions.I am indebted to Ms K. Van Every for her invaluable and patient assistance during the field portion of this study and to Dr. R. Robertson for his permission to use the facilities at the Queen's University Biology Station. Dr. M.B. Fenton provided me with financial support and much appreciated advice for the project. I also thank Dr. Fenton for the tapes ofE. fuscus that he made. The helpful criticisms of Drs. G.K. Morris, G.E. Kerr, A. Michelsen and an anonymous reviewer were gratefully appreciated. I thank Dr. J.A. Simmons for Fig. 1.     

Isolation of Salmonella Virchow from a Fruit Bat (Pteropus giganteus)

Detection of zoonotic pathogens carried by bats is important both for understanding disease ecology and for developing preventive measures. Pteropus fruit bats have been identified as potential carriers of Salmonella enterica serotype Typhi. A cross-sectional study was conducted to determine the prevalence of Salmonella Typhi and other Salmonella serotypes in Pteropus giganteus fruit bats in Bangladesh. Rectal swabs were collected from 302 bats and cultured for Salmonella species. The bats were trapped in three districts (Faridpur, Rajbari, and Cox’s Bazar). Salmonella Typhi was not found but one juvenile female bat from Faridpur district was positive for Salmonella Virchow. Close associations between frugivorous bats, humans, and livestock in rural Bangladesh make it likely that the bat was infected by consuming contaminated water.     

Diversity and community structure of bats (Chiroptera) in the Centre Region of Cameroon

In this survey, we investigated the diversity and community structure of bats in the Centre Region of Cameroon with respect to their distribution in the different vegetation zones of the region. We mist-netted bats monthly from January 2016 to June 2017 for five nonconsecutive nights per month. Thirty-nine sites were surveyed: 24 in traditional farms, nine in the savannah and six in the forests. A total of 668 bats were captured during 81 nights of capture, covering seven families, 21 genera and 36 species. This included 26 species in traditional farms, 13 species in savannah and 11 species in the forest. Micropteropus pusillus was the most abundant species (30.7%) recorded, followed by Hipposideros ruber (24.9%). The sample efficiency was estimated at 72.1% with fitted species accumulation curves not reaching asymptotes for the three habitat types, suggesting that the survey did not record all the bats present. There was an indication of general increased in abundance of bats during the dry and rainy seasons but it is not significant (Mann–Whitney U: 783.5, p = .195). The rarity index was highest in traditional farms (0.44), followed by savannah (0.38) and then forest (0.33). This preliminary survey provides baseline data on the distribution of bats in the different vegetation types in the Centre Region of Cameroon.     

Expression of enzymatically active and correctly targeted strictosidine synthase in transgenic tobacco plants

Strictosidine, a precursor to over 1000 indole alkaloids including the anti-tumor drugs vinblastine, vincristine, and camptothecin, is produced by the condensation of tryptamine and secologanin. Strictosidine synthase, the enzyme responsible for this condensation, is the first committed step in the indole-alkaloid pathway. We have introduced a modified cDNA encoding Strictosidine synthase from Catharanthus roseus (L.) Don. (McKnight et al. 1990, Nucl. Acids Res. 18, 4939) driven by the CaMV 35S promoter into tobacco (Nicotiana tabacum L.). Transgenic tobacco plants expressing this construct had from 3 to 22 times greater strictosidinesynthase activity than C. roseus plants. Ultrastructural immunolocalization demonstrated that strictosidine synthase is a vacuolar protein in C. roseus and is correctly targeted to the vacuole in transgenic tobacco. Immunoblot analysis of strictosidine synthase showed that two distinct forms of the enzyme were produced in transgenic tobacco plants but that only a single form was made in C. roseus. This observation indicates that the second form of the protein is not simply a result of overexpression in tobacco, but may reflect differences in protein processing between tobacco and C. roseus.Abbreviations cDNA complementary DNA - TLC thin-layer chromatography We thank Dr. C.A. Roessner for providing the E. coli strain expressing strictosidine synthase, Dr. J. Balsevich for providing alkaloid standards, and Dr. L. Cloney for assisting with antibody preparation. This work was supported by a National Institutes of Health Biomedical Research Support Grant to T.D.M and by a grant from the US Department of Agriculture, Competitive Research Grants Office (90-37262-5375) to C.L.N.     

Habitat fragmentation and the prevalence of parasites (Diptera,Streblidae) on three Phyllostomid bat species

Ectoparasitism in bats seems to be influenced strongly by the type of roost preferred by the hosts, and group size; however, the effect of habitat loss and fragmentation on the prevalence of ectoparasites in bats has scarcely been studied. In northeastern Yucatan, Mexico, we estimated the prevalence of infestation by Streblidae flies in three phyllostomid bat species with different roost preferences (caves, trees, or both) in two types of landscape matrices (tropical semi‐deciduous forest and man‐made pastures) that differed in area of forest cover and the number of forest fragments. Habitat fragmentation and the presence of a contrasting matrix may limit the availability of roosts (trees) and the movement of bats across the landscape. Accordingly, we hypothesized higher prevalence of Streblidae infestation in the pasture matrix and in the group of bats that roost in trees. Bat abundance was higher in the pasture matrix; however, the prevalence of infestation was significantly higher in the continuous forest matrix and in bats that roosted in caves. The prevalence of some species of Streblidae was affected by habitat fragmentation in species that roost in caves, such as Desmodus rotundus, as well as those using foliage and caves, such as Artibeus jamaicensis. Our results provide evidence that some species of Streblidae may respond differently to habitat fragmentation than their hosts, generating changes to bat‐ectoparasite interactions in fragmented areas. Environmental variations involving roosts, not evaluated in this study, may influence our results, since these factors affect ectoparasite abundance and reproduction.     

Winter mortality rates of bats inhabiting man-made shelters (northern Poland)

Non-predator and non-accidental mortality rates of bats inside the city of Toruń's fortification system (northern Poland) were studied over winter periods from 1995 to 2000. The bats were counted and dead bats collected at 1-month intervals from October to April. In total, thirty four dead bats were found. The percentage of dead individuals of the surveyed bats was low:Myotis daubentonii (0.6%),M. nattereri (0.4%),Plecotus auritus (0.4%),M. myotis (0.1%), and zero forBarbastella barbastellus. There was no clear difference in the species ratio of the observed and dead bats. The percentage of the dead to surveyed bats was lower in November (0.07%) and December (0.07%), and higher in September (3.3%) and April (1.3%). Temperature explained 84% of variation of the differences in mortality rates. Observations suggest that non-predator and non-accidental mortality inside the fortifications was extremely low and non-linearly correlated with the ambient temperature measured outside the fortifications.