Identification of sympatric bat species by the echolocation calls

One hundred and thirty-eight echolocation calls of 63 free-flying individuals of five bat species (Rhinolophus ferrumequinum,Myotis formosus,Myotis ikonnikovi,Myotis daubentoni and Murina leucogaster)were recorded (by ultrasonic bat detector (D980)) in Zhi'an village of Jilin Province,China.According to the frequency-time spectra,these calls were categorized into two types:FM/CF (constant frequency) / FM (R.ferrumequinum) and FM (frequency modulated)(M.formosus,M.ikonnikovi,M.daubentoni and M.leucogaster).Sonograms of the calls of R.ferrumequinum could easily be distinguished from those of the other four species.For the calls of the remaining four species,six echolocation call parameters,including starting frequency,ending frequency,peak frequency duration,longest inter-pulse interval and shortest inter-pulse interval,were examined by stepwise discriminant analysis.The results show that 84.1% of calls were correctly classified,which indicates that these parameters of echolocation calls play an important role in identifying bat species.These parameters can be used to test the accuracy of general predictions based on bats' morphology in the same forest and can provide essential information for assessing patterns of bat habitat use.     

Variations in the echolocation calls of the European free-tailed bat

The echolocation calls of Tadarida teniotis were studied in an outdoor flight enclosure (captive individuals) and in the wild using single microphones or an array of four microphones. Calls were characterized by measures of 10 call variables. Comparison of individual calls recorded on four microphones arrayed in a tetrahedron with 1 m between each microphone revealed that all calls were not equally detectable by all microphones but that there were no significant differences in call features obtained from calls recorded on all four microphones. A comparison of 47 calls recorded by all four microphones showed no significant differences in the features of the four recordings of each call. Analysis of calls of five individuals flying individually in an outdoor flight cage revealed significant individual differences in call features. In the field, T. teniotis used long, narrowband search-phase calls, usually without harmonics. Analysis of 1876 search-phase echolocation calls of T. teniotis recorded in the field in Israel and Greece in 2002, 2005 and 2006 showed significant year-to-year and site-to-site differences in some call features. When flying in the presence of conspecifics, T. teniotis changed their echolocation calls. We found a range of different buzzes in the wild, and based on their structure we attempted to classify them as feeding and social buzzes. The features of individual calls comprising buzzes differed significantly among buzzes, and yet there were no consistent differences between what we classified as feeding and social buzzes.     

六种共栖蝙蝠的回声定位信号及翼型特征的比较

本研究于2006 年5 ～ 8 月在桂林市七星公园七星岩洞进行,比较分析了共栖2 科(蹄蝠科和蝙蝠科)6 种共75 只蝙蝠的回声定位信号和翼型特征。普氏蹄蝠的回声定位叫声为短而多谐波的CF/ FM 型,主频率为61.2±0.8 kHz, 具有高翼载、低翼展比和中等翼尖指数; 大蹄蝠的回声定位叫声为单CF/ FM 型,主频率为68. 6 ±0.7 kHz,具有高翼载、低翼展比和中等翼尖指数;中蹄蝠的回声定位叫声为单CF / FM 型,主频率为85.2 ±0.5 kHz,具有中等翼载、低翼展比和中等翼尖指数;高颅鼠耳蝠的回声定位叫声为长带宽的FM 型,主频率为50.7 ±3.8 kHz,具有低翼载、中等翼展比和低翼尖指数;大足鼠耳蝠回声定位叫声为FM 型,主频率为39.9 ±3.2 kHz,具有中等翼载、低翼展比和高翼尖指数;绒山蝠回声定位叫声为短而多谐波的FM 型,主频率为49.0± 0. 4 kHz,具有高翼载、中等翼展比和低翼尖指数。经单因素方差分析表明,6 种蝙蝠之间绝大部分的形态和声音参数差异显著(One-way ANOVA,P < 0. 05)。以上结果说明,6 种同地共栖蝙蝠种属特异的回声定位叫声
和形态结构体现出了相互之间的生态位分离,从而降低了种间竞争压力,使得6 种蝙蝠能够同地共存。     

形态和声波相似的中华菊头蝠与中菊头蝠的共存机制

研究了同域分布的中华菊头蝠(Rhinolophus sinicus)与中菊头蝠(Rhinolophus affinis)的食性、形态、回声定位声波及捕食时间.中华菊头蝠与中菊头蝠均属于中等体型的菊头蝠,前臂长分别为(51.25±0.22) mm和(52.40±0.37) mm;悬挂状态下的回声定位声波均为典型的调频-恒频-调频(FM-CM-FM)型叫声,峰频分别为(82.07±0.17) kHz和(84.41±0.48) kHz.粪便分析显示中华菊头蝠与中菊头蝠分别捕食9目和7目昆虫,均以鳞翅目(Lepidiptera)和鞘翅目(Coleoptera)昆虫为主要食物(体积百分比总和> 90%),捕食鳞翅目昆虫的体积百分比差异显著,对猎物大小(以鞘翅目昆虫体长衡量)的选择无显著差异.中华菊头蝠与中菊头蝠的营养生态位宽度分别为2.38和2.28,重叠度达0.91,营养生态位未发生明显分化,但充足的食物资源促进了二者的共存.另外,2种菊头蝠的感官生态位和时间生态位未发生明显分化.由2种菊头蝠的翼载和峰频的差异推测二者发生了空间生态位和捕食微生境的分化,这也可能促进了二者的共存.     

马铁菊头蝠(Rhinolophus ferrumequinum)回声定位声波与生境类型和环境因子的关系

2007年在吉林省罗通山自然保护区,利用超声波探测仪（Avisoft-SASLAB PRO）录制并分析不同生境中马铁菊头蝠的回声定位声波。结果显示马铁菊头蝠在不同类型生境中活动;各生境中回声定位声波参数存在显著差异（one-way ANOVA,P〈0.05）。从环境因子中通过主成分分析筛选出与其回声定位声波相关的植被、气候和地形因子,探讨回声定位声波与这些因子的相关性。结果显示FM1和FM2带宽与乔木高（r=-0.948,-0.825;P〈0.05）、FM1起始频率和FM2终止频率与林冠面积（r=-0.967,-0.958;P〈0.05）、FM1起始频率、FM2终止频率和峰频与湿度（r=-0.776、-0.875和-0.794,P〈0.05）、脉冲持续时间和脉冲间隔与平均灌木高均呈显著负相关（r=-0.911,-0.990;P〈0.05）,峰频与植被株数（r=0.756,P〈0.05）、脉冲持续时间与冠下高呈显著正相关（r=0.870,P〈0.05）。表明各种环境因子（植被因子、气候因子和地形因子）都在一定程度上影响回声定位声波,回声定位声波具有表型可塑性和生境适应性,这些特性决定了马铁菊头蝠生境利用的程度和可利用的资源。     

同地共栖四种蝙蝠食性和回声定位信号的差异及其生态位分化

本研究于 2 0 0 2年 5月初至 2 0 0 3年 9月中旬在北京房山区霞云岭四合村蝙蝠洞进行 ,分析了共栖同一山洞四种蝙蝠的形态特征、食性和回声定位信号。大足鼠耳蝠食谱中以宽鳍等三种鱼为主 (体积百分比为5 3% ) ,回声定位主频 4 1 87± 1 0 7kHz;马铁菊头蝠主要掠捕鳞翅目昆虫 (73% ) ,恒频叫声主频 74 70± 0 13kHz ;中华鼠耳蝠以近地面或在地表活动的鞘翅目昆虫步甲类和埋葬甲类为主要食物 (6 5 4 % ) ,声脉冲主频较低 35 73± 0 92kHz;白腹管鼻蝠捕食花萤总科和瓢虫科等鞘翅目昆虫 (90 % ) ,回声定位信号主频为 5 9 4 7±1 5 0kHz。结果证实同地共栖四种蝙蝠种属特异的回声定位叫声和形态结构的差异 ,以及不同的捕食生境和捕食策略 ,导致取食生态位分离是四种蝙蝠同地共栖的原因     

Weather conditions determine attenuation and speed of sound: Environmental limitations for monitoring and analyzing bat echolocation

Echolocating bats are regularly studied to investigate auditory‐guided behaviors and as important bioindicators. Bioacoustic monitoring methods based on echolocation calls are increasingly used for risk assessment and to ultimately inform conservation strategies for bats. As echolocation calls transmit through the air at the speed of sound, they undergo changes due to atmospheric and geometric attenuation. Both the speed of sound and atmospheric attenuation, however, are variable and determined by weather conditions, particularly temperature and relative humidity. Changing weather conditions thus cause variation in analyzed call parameters, limiting our ability to detect, and correctly analyze bat calls. Here, I use real‐world weather data to exemplify the effect of varying weather conditions on the acoustic properties of air. I then present atmospheric attenuation and speed of sound for the global range of weather conditions and bat call frequencies to show their relative effects. Atmospheric attenuation is a nonlinear function of call frequency, temperature, relative humidity, and atmospheric pressure. While atmospheric attenuation is strongly positively correlated with call frequency, it is also significantly influenced by temperature and relative humidity in a complex nonlinear fashion. Variable weather conditions thus result in variable and unknown effects on the recorded call, affecting estimates of call frequency and intensity, particularly for high frequencies. Weather‐induced variation in speed of sound reaches up to about ±3%, but is generally much smaller and only relevant for acoustic localization methods of bats. The frequency‐ and weather‐dependent variation in atmospheric attenuation has a threefold effect on bioacoustic monitoring of bats: It limits our capability (1) to monitor bats equally across time, space, and species, (2) to correctly measure frequency parameters of bat echolocation calls, particularly for high frequencies, and (3) to correctly identify bat species in species‐rich assemblies or for sympatric species with similar call designs.     

五种蝙蝠形态与回声定位叫声的性别差异

为研究角菊头蝠(Rhinolophus cornutus)、三叶蹄蝠(Aselliscus uheeleri)、大蹄蝠(Hipposideros armiger)、大鼠耳蝠(Myotis myotis)和大足鼠耳蝠(M．riketti)的形态和回声定位叫声的性别差异性,明确同种蝙蝠雌雄个体对食物、栖息地等资源利用的细微差异,我们利用超声波探测仪、Batsound分析软件及SPSS11．0统计软件对5种95只蝙蝠进行了录音、声波分析和统计分析。5种蝙蝠形态性别差异性不显著,角菊头蝠、三叶蹄蝠、大蹄蝠和大足鼠耳蝠叫声频率性别差异性显著,大鼠耳蝠叫声频率性别差异性不显著。角菊头蝠雌性叫声的基频、分音、主频率高于雄性,声脉冲时间、间隔时间大于雄性,调频(FM)带宽小于雄性;三叶蹄蝠、大蹄蝠叫声的基频、主频率雄性高于雌性,调频带宽雌性小于雄性;大足鼠耳蝠叫声的主频率雄性高于雌性,FM带宽雌性大于雄性[动物学报49(6)：742～747,2003]。     

蝙蝠回声定位声波的可塑性及其生态适应

蝙蝠通过调节回声定位声波特征来满足自身的感官需求,表现出回声定位声波的可塑性及其对生态环境与需求的适应。声波频率、强度、脉冲持续时间和间隔时间等特征与蝙蝠所处的生态位密切相关,声波可塑性在蝙蝠进化过程中起着至关重要的作用。本文结合马铁菊头蝠(Rhinolophus ferrumequinum)和大趾鼠耳蝠(Myotis macrodactylus)回声定位声波可塑性的研究,从回声定位声波的方向性、目标距离、环境复杂度和应对干扰4个方面总结了蝙蝠如何通过改变回声定位声波特征来满足自身在导航和捕捉猎物过程中的感官需求与生态适应,并阐述了回声定位声波可塑性的研究现状,为开展蝙蝠声学和行为学研究提供参考。     

Geographical variation in the high-duty cycle echolocation of the cryptic common mustached bat Pteronotus cf. rubiginosus (Mormoopidae)

The use of bioacoustics as a tool for bat research is rapidly increasing worldwide. There is substantial evidence that environmental factors such as weather conditions or habitat structure can affect echolocation call structure in bats and thus compromise proper species identification. However, intraspecific differences in echolocation due to geographical variation are poorly understood, which poses a number of issues in terms of method standardization. We examined acoustic data for Pteronotus cf. rubiginosus from the Central Amazon and the Guiana Shield. We provide the first evidence of intraspecific geographic variation in bat echolocation in the Neotropics, with calls significantly differing in almost all standard acoustic parameters for the two lineages of this clade. We complement our bioacoustic data with molecular and morphological data for both species. Considerable overlap in trait values prevents reliable discrimination between the two sympatric Pteronotus based on morphological characters. On the other hand, significant divergence in the frequency of maximum energy suggests that bioacoustics can be used to readily separate both taxa despite extensive intraspecific variability in their echolocation across the Amazon. Given the relative lack of barriers preventing contact between bat populations from the Central Amazon and French Guiana, the documented acoustic variation needs to be further studied in geographically intermediate locations to understand the potential isolation processes that could be causing the described divergence in echolocation and to determine whether this variation is either discrete or continuous.     

Testing the performances of automated identification of bat echolocation calls: A request for prudence

Echolocating bats are surveyed and studied acoustically with bat detectors routinely and worldwide, yet identification of species from calls often remains ambiguous or impossible due to intraspecific call variation and/or interspecific overlap in call design. To overcome such difficulties and to reduce workload, automated classifiers of echolocation calls have become popular, but their performance has not been tested sufficiently in the field. We examined the absolute performance of two commercially available programs (SonoChiro and Kaleidoscope) and one freeware package (BatClassify). We recorded noise from rain and calls of seven common bat species with Pettersson real-time full spectrum detectors in Sweden. The programs could always (100%) distinguish rain from bat calls, usually (68–100%) identify bats to group (Nyctalus/Vespertilio/Eptesicus, Pipistrellus, Myotis, Plecotus, Barbastella) and usually (83–99%) recognize typical calls of some species whose echolocation pulses are structurally distinct (Pipistrellus pygmaeus, Barbastella barbastellus). Species with less characteristic echolocation calls were not identified reliably, including Vespertilio murinus (16–26%), Myotis spp. (4–93%) and Plecotus auritus (0–89%). All programs showed major although different shortcomings and the often poor performance raising serious concerns about the use of automated classifiers for identification to species level in research and surveys. We highlight the importance of validating output from automated classifiers, and restricting their use to specific situations where identification can be made with high confidence. For comparison we also present the result of a manual identification test on a random subset of the files used to test the programs. It showed a higher classification success but performances were still low for more problematic taxa.     

Morphology, echolocation and foraging behaviour in two sympatric sibling species of bat (Tylonycteris pachypus and Tylonycteris robustula) (Chiroptera: Vespertilionidae)

We studied the wing morphology, echolocation calls, foraging behaviour and flight speed of Tylonycteris pachypus and Tylonycteris robustula in Longzhou County, South China during the summer (June–August) of 2005. The wingspan, wing loading and aspect ratio of the two species were relatively low, and those of T. pachypus were lower compared with T. robustula . The echolocation calls of T. pachypus and T. robustula consist of a broadband frequency modulated (FM) sweep followed by a short narrowband FM sweep. The dominant frequency of calls of T. pachypus was 65.1 kHz, whereas that of T. robustula was 57.7 kHz. The call frequencies (including highest frequency of the call, lowest frequency of the call and frequency of the call that contained most energy) of T. pachypus were higher than those of T. robustula , and the pulse duration of the former was longer than that of the latter. The inter-pulse interval and bandwidth of the calls were not significantly different between the two species. Tylonycteris pachypus foraged in more complex environments than T. robustula , although the two species were both netted in edge habitats (around trees or houses), along pathways and in the tops of trees. Tylonycteris pachypus flew slower (straight level flight speed, 4.3 m s⁻¹) than T. robustula (straight level flight speed, 4.8 m s⁻¹). We discuss the relationship between wing morphology, echolocation calls, foraging behaviour and flight speed, and demonstrate resource partitioning between these two species in terms of morphological and behavioural factors.     

Assessing niche partitioning of co‐occurring sibling bat species by DNA metabarcoding

Niche partitioning through foraging is a mechanism likely involved in facilitating the coexistence of ecologically similar and co‐occurring animal species by separating their use of resources. Yet, this mechanism is not well understood in flying insectivorous animals. This is particularly true of bats, where many ecologically similar or cryptic species coexist. The detailed analysis of the foraging niche in sympatric, cryptic sibling species provides an excellent framework to disentangle the role of specific niche factors likely involved in facilitating coexistence. We used DNA metabarcoding to determine the prey species consumed by a population of sympatric sibling Rhinolophus euryale and Rhinolophus mehelyi whose use of habitat in both sympatric and allopatric ranges has been well established through radio tracking. Although some subtle dietary differences exist in prey species composition, the diet of both bats greatly overlapped (O_jk = 0.83) due to the consumption of the same common and widespread moths. Those dietary differences we did detect might be related to divergences in prey availabilities among foraging habitats, which prior radio tracking on the same population showed are differentially used and selected when both species co‐occur. This minor dietary segregation in sympatry may be the result of foraging on the same prey‐types and could contribute to reduce potential competitive interactions (e.g., for prey, acoustic space). Our results highlight the need to evaluate the spatial niche dimension in mediating the co‐occurrence of similar insectivorous bat species, a niche factor likely involved in processes of bat species coexistence.     

Dietary composition and echolocation call design of three sympatric insectivorous bat species from China

Studying the diet of echolocating, insectivorous bats can provide important insights into their foraging behaviors and ecological constraints they are facing. By examining an extensive data set covering a period of 2 years, the present study identifies the dietary composition of three sympatric insectivorous bat species in rural areas of Beijing municipality. Each species clearly has different preferences for particular food items. Greater horseshoe bats, Rhinolophus ferrumequinum, preferred to catch nocturnal, actively flying insects, mostly moths (Lepidoptera), and to a lesser percentage flies (Diptera), beetles (Coleoptera), and flying ants and termites (Hymenoptera). Other nocturnal insects which do not exhibit any perceptible wing movements, such as true bugs (Homoptera), or strictly diurnal insects that hardly ever fly in the dark, such as grasshoppers (Orthoptera) and dragon- and damselflies (Odonata), were never found in droppings of horseshoe bats. Large mouse-eared bats, Myotis chinensis, preferentially glean relatively large terrestrial prey of the order Coleoptera (mostly carabid beetles) and Orthoptera, whereas greater tube-nosed bats, Murina leucogaster, consume predominantly smaller, diurnal Coleoptera (mostly soldier beetles, Cantharidae, and ladybugs, Coccinellidae). Our findings also indicate previously not described, significant spectro-temporal differences in the echolocation signals of M. chinensis and M. leucogaster. The results suggest that in our study area the dramatic differences in the dietary composition of these three bat species are mainly based upon differences in their foraging behaviors, including differences in their echolocation signal structure. The dietary data provide important background information for conservational efforts, such as habitat protection.     

Moth wing scales slightly increase the absorbance of bat echolocation calls

Coevolutionary arms races between predators and prey can lead to a diverse range of foraging and defense strategies, such as countermeasures between nocturnal insects and echolocating bats. Here, we show how the fine structure of wing scales may help moths by slightly increasing sound absorbance at frequencies typically used in bat echolocation. Using four widespread species of moths and butterflies, we found that moth scales are composed of honeycomb-like hollows similar to sound-absorbing material, but these were absent from butterfly scales. Micro-reverberation chamber experiments revealed that moth wings were more absorbent at the frequencies emitted by many echolocating bats (40-60 kHz) than butterfly wings. Furthermore, moth wings lost absorbance at these frequencies when scales were removed, which suggests that some moths have evolved stealth tactics to reduce their conspicuousness to echolocating bats. Although the benefits to moths are relatively small in terms of reducing their target strengths, scales may nonetheless confer survival advantages by reducing the detection distances of moths by bats by 5-6%.