Björn M. Siemers

Echolocation signals reflect niche differentiation in five sympatric congeneric bat species

Echolocating bats can be divided into guilds according to their preferred habitat and foraging behaviour, which coincide with distinct adaptations in wing morphology and structure of echolocation signals. Although coarse structuring of niche space between different guilds is generally accepted, it is not clear how niches differ within guilds, or whether there is fine-grained niche differentiation reflected in echolocation signal structure. Using a standardized performance test, here we show clutter-dependent differences in prey-capture success for bats from five species of European Myotis. These species are morphologically similar, sympatric, and all belong to the guild labelled “edge space aerial/trawling foragers”. We further demonstrate a strong correlation between the prey-detection ability of the species and the respective search-call bandwidth. Our findings indicate that differences in echolocation signals contribute to within-guild niche differentiation. This is the first study relating sensory abilities of a set of potentially competing animal species to a direct measure of their respective foraging performance, suggesting an important role of sensory ecology in the structuring of animal communities.

Natterer's bat (Myotis nattereri Kuhl, 1818) hawks for prey close to vegetation using echolocation signals of very broad bandwidth

Abstract We present a hitherto unknown prey perception strategy in bats: Myotis nattereri (Vespertilionidae, Chiroptera) is able to perceive prey by echolocation within a few centimeters of echo-cluttering vegetation, by using frequency-modulated search signals of very large bandwidth (up to 135 kHz). We describe the species’ search behavior and echolocation repertoire from the field and from experiments in a flight tent. In the field, bats varied signal parameters in relation to their distance from vegetation and usually flew close to vegetation. In the flight tent, M. nattereri detected and localized prey by echolocation alone as close as 5 cm from vegetation. Apparently, the bats were able to tolerate some overlap between prey and clutter echoes. Passive prey cues (vision, olfaction, prey-generated sounds) were not used in prey perception. The bats selected prey by size. The animals performed aerial catches and produced approach sequences typical for aerial hawking bats, but were able to do so within a few centimeters of the substrate. M. nattereri thus has access to silent, suspended prey very close to vegetation (e.g., spiders, and caterpillars on threads).

Do echolocation calls of wild colony-living Bechstein's bats (Myotis bechsteinii) provide individual-specific signatures?

Social animals often use vocal communication signals that contain individual signatures. As bats emit echolocation calls several times per second to orient in space, these might seem ideal candidates for conveying the callers individual identity as a free by-product. From a proximate perspective, however, coding of caller identity is hampered by the simple acoustic structure of echolocation signals, by their task-specific design and by propagation loss. We investigated the occurrence of individual signatures in echolocation calls in individually marked, free-living Bechsteins bats (Myotis bechsteinii) in a situation with defined social context in the field. The bats belonged to two different colonies, for both of which genetic data on relatedness structure was available. While our data clearly demonstrate situation specificity of call structure, the evidence for individual-specific signatures was relatively weak. We could not identify a robust and simple parameter that would convey the callers identity despite the situation-specific call variability. Discriminant function analysis assigned calls to call sequences with good performance, but worsened drastically when tested with other sequences from the same bats. Therefore, we caution against concluding from a satisfactory discrimination performance with identical training and test sequences that individual bats can reliably be told apart by echolocation calls. At least the information contained in a single call sequence seems not to be sufficient for that purpose. Starting frequencies did give the best discrimination between individuals, and it was also this parameter that was correlated with genetic relatedness in one of our two study colonies. Echolocation calls could serve as an additional source of information for individual recognition in Bechsteins bats societies, while it is unlikely that a large number of individuals could be reliably identified in different situations based on echolocation alone.

Great tits search for, capture, kill and eat hibernating bats

Ecological pressure paired with opportunism can lead to surprising innovations in animal behaviour. Here, we report predation of great tits (Parus major) on hibernating pipistrelle bats (Pipistrellus pipistrellus) at a Hungarian cave. Over two winters, we directly observed 18 predation events. The tits specifically and systematically searched for and killed bats for food. A substantial decrease in predation on bats after experimental provisioning of food to the tits further supports the hypothesis that bat-killing serves a foraging purpose in times of food scarcity. We finally conducted a playback experiment to test whether tits would eavesdrop on calls of awakening bats to find them in rock crevices. The tits could clearly hear the calls and were attracted to the loudspeaker. Records for tit predation on bats at this cave now span more than ten years and thus raise the question of whether cultural transmission plays a role for the spread of this foraging innovation.

Stable carbon isotopes in exhaled breath as tracers for dietary information in birds and mammals

SUMMARY The stable carbon isotope ratio of exhaled CO2 (δ13Cbreath) reflects the isotopic signature of the combusted substrate and is, therefore, suitable for the non-invasive collection of dietary information from free-ranging animals. However,δ 13Cbreath is sensitive to changes in ingested food items and the mixed combustion of exogenous and endogenous substrates. Therefore, experiments under controlled conditions are pivotal for the correct interpretation of δ13Cbreath of free-ranging animals. We measured δ13Cbreath in fasted and recently fed insectivorous Myotis myotis (Chiroptera) to assess the residence time of carbon isotopes in the pool of metabolized substrate, and whether δ13Cbreath in satiated individuals levels off at values similar to the dietary isotope signature (δ13Cdiet) in insect-feeding mammals. Meanδ 13Cbreath of fasted individuals was depleted by– 5.8‰ (N=6) in relation toδ 13Cdiet. After feeding on insects, bats exchanged 50% of carbon atoms in the pool of metabolized substrates within 21.6±10.5 min, which was slower than bats ingesting simple carbohydrates. After 2 h, δ13Cbreath of satiated bats levelled off at –2.6‰ belowδ 13Cdiet, suggesting that bats combusted both exogenous and endogenous substrate at this time. A literature survey revealed that small birds and mammals metabolize complex macronutrients at slower rates than simple macronutrients. On average, δ13Cbreath of fasting birds and mammals was depleted in 13C by– 3.2±2.0‰ in relation toδ 13Cdiet. δ13Cbreath of satiated animals differed by –0.6±2.3‰ fromδ 13Cdiet when endogenous substrates were not in isotopic equilibrium with exogenous substrates and by +0.5±1.8‰ (N=6 species) after endogenous substrates were in isotopic equilibrium with exogenous substrates.

Wing Measurement Variations in the Five European Horseshoe Bat Species (Chiroptera : Rhinolophidae)

Abstract Wing morphology is crucial for flight performance and foraging ecology in bats. We describe variations in 5 wing parameters within the 5 species of European horseshoe bats (genus Rhinolophus) based on data taken from 3,081 adult individuals. All 5 species belong to a single ecological guild. Measurements were taken from live bats in the field in southeastern Europe (Bulgaria, Greece, and Turkey), where all 5 species occur in sympatry. Examination of our data shows that the species and accordingly their wings differ substantially in size. Albeit grossly similar in form, we additionally found several size-independent differences in wing shape. For example, the smallest species, Rhinolophus hipposideros, and to a lesser extent also R. blasii, have extremely short hand wings, enabling highly maneuverable search flight close to vegetation. The largest species, R. ferrumequinum, and the 2nd largest one, R. mehelyi, have rather long hand wings, allowing fast and economic commuting flight over longer distances. We argue that both size and shape are likely to play a role for niche separation between species. We found both sexual and geographic variation within species. There was sexual dimorphism for most parameters, with females being larger than males. Populations of R. mehelyi in southeastern Europe had significant variation in wing measurements. This was not so for R. ferrumequinum and R. euryale. We give a discriminant function based on only 2 parameters that correctly assigned 98% of the 3,081 individuals to species. This function may prove useful for identification of museum specimens.

Acoustic mirror effect increases prey detection distance in trawling bats

Many different and phylogenetically distant species of bats forage for insects above water bodies and take insects from and close to the surface; the so-called ‘trawling behaviour’. Detection of surface-based prey by echolocation is facilitated by acoustically smooth backgrounds such as water surfaces that reflect sound impinging at an acute angle away from the bat and thereby render a prey object acoustically conspicuous. Previous measurements had shown that the echo amplitude of a target on a smooth surface is higher than that of the same target in mid-air, due to an acoustic mirror effect. In behavioural experiments with three pond bats (Myotis dasycneme), we tested the hypothesis that the maximum distances at which bats can detect prey are larger for prey on smooth surfaces than for the same prey in an airborne situation. We determined the moment of prey detection from a change in echolocation behaviour and measured the detection distance in 3D space from IR-video recordings using stereo-photogrammetry. The bats showed the predicted increase in detection distance for prey on smooth surfaces. The acoustic mirror effect therefore increases search efficiency and contributes to the acoustic advantages encountered by echolocating bats when foraging at low heights above smooth water surfaces. These acoustic advantages may have favoured the repeated evolution of trawling behaviour.

Ground gleaning in horseshoe bats: comparative evidence from Rhinolophus blasii, R. euryale and R. mehelyi

The 71 species of horseshoe bat (genus Rhinolophus) use echolocation calls with long constant-frequency (CF) components to detect and localize fluttering insects which they seize in aerial captures or glean from foliage. Here we describe ground-gleaning as an additional prey-capture strategy for horseshoe bats. This study presents the first record and experimental evidence for ground-gleaning in the little-studied Blasius’ horseshoe bat (Rhinolophus blasii). The gleaning bouts in a flight tent included landing, quadrupedal walking and take-off from the ground. The bats emitted echolocation calls continuously during all phases of prey capture. Both spontaneously and in a choice experiment, all six individuals attacked only fluttering insects and never motionless prey. These data suggest that R. blasii performs ground-gleaning largely by relying on the same prey-detection strategy and echolocation behaviour that it and other horseshoe bats use for aerial hawking.We also studied the Mediterranean horseshoe bat (R. euryale) in the flight tent. All four individuals never gleaned prey from the ground, though they appeared to be well able to detect fluttering moths on the ground. It is not known yet whether ground-gleaning plays a role in Mehely’s horseshoe bat (R. mehelyi). In a performance test, we measured the ability of these three European species of “middle-sized” horseshoe bats (R. euryale, R. mehelyi and R. blasii) to take-off from the ground. All were able to take flight even in a confined space; i.e. the willingness to ground-glean in R. blasii is not related to a superior take-off performance. In contrast to ground-gleaning bats of other phylogenetic lineages, R. blasii appears not to be a specialist, but rather shows a remarkable behavioural flexibility in prey-capture strategies and abilities. We suggest that the key innovation of CF echolocation paired with behavioural flexibility in foraging strategies might explain the evolutionary success of Rhinolophus as the second largest genus of bat.

Divergent trophic levels in two cryptic sibling bat species

Changes in dietary preferences in animal species play a pivotal role in niche specialization. Here, we investigate how divergence of foraging behaviour affects the trophic position of animals and thereby their role for ecosystem processes. As a model, we used two closely related bat species, Myotis myotis and M. blythii oxygnathus, that are morphologically very similar and share the same roosts, but show clear behavioural divergence in habitat selection and foraging. Based on previous dietary studies on synanthropic populations in Central Europe, we hypothesised that M. myotis would mainly prey on predatory arthropods (i.e., secondary consumers) while M. blythii oxygnathus would eat herbivorous insects (i.e., primary consumers). We thus expected that the sibling bats would be at different trophic levels. We first conducted a validation experiment with captive bats in the laboratory and measured isotopic discrimination, i.e., the stepwise enrichment of heavy in relation to light isotopes between consumer and diet, in insectivorous bats for the first time. We then tested our trophic level hypothesis in the field at an ancient site of natural coexistence for the two species (Bulgaria, south-eastern Europe) using stable isotope analyses. As predicted, secondary consumer arthropods (carabid beetles; Coleoptera) were more enriched in 15N than primary consumer arthropods (tettigoniids; Orthoptera), and accordingly wing tissue of M. myotis was more enriched in 15N than tissue of M. blythii oxygnathus. According to a Bayesian mixing model, M. blythii oxygnathus indeed fed almost exclusively on primary consumers (98%), while M. myotis ate a mix of secondary (50%), but also, and to a considerable extent, primary consumers (50%). Our study highlights that morphologically almost identical, sympatric sibling species may forage at divergent trophic levels, and, thus may have different effects on ecosystem processes.

Behavioral evidence for eavesdropping on prey song in two Palearctic sibling bat species

Eavesdropping on prey communication signals has never before been reported for a Palearctic bat species. In this study, we investigated whether lesser and greater mouse-eared bats, Myotis blythii oxygnathus and Myotis myotis, find tettigoniid bushcrickets (Tettigoniidae) by eavesdropping on their mate-attraction song. Tettigoniids are known to be the most important prey item for M. blythii oxygnathus, while carabid beetles and other epigaeic arthropods are the most important prey for its sibling species, M. myotis, in many places in Europe. M. myotis locates walking beetles by listening for their rustling sounds. We compared these two species’ response to four acoustic prey cues: calling song of two tettigoniid species, the rustling sound made by walking carabid beetles, and a control tone. Individuals of both bat species attacked the speaker playing tettigoniid song, which clearly indicates that both species eavesdrop on prey-generated advertisement signals. There were, however, species differences in response. M. blythii oxygnathus exhibited stronger predatory responses to the calling song of two species of tettigoniid than to the beetle rustling sound or the control. M. myotis, in contrast, exhibited stronger predatory responses to the beetle rustling and to one tettigoniid species but not the other tettigoniid or the control. Our study (1) for the first time demonstrates eavesdropping on prey communication signals for Palearctic bats and (2) gives preliminary evidence for sensory niche partitioning between these two sympatric sibling bat species.