Holger R. Goerlitz

An Aerial-Hawking Bat Uses Stealth Echolocation to Counter Moth Hearing

Ears evolved in many nocturnal insects, including some moths, to detect bat echolocation calls and evade capture [1, 2]. Although there is evidence that some bats emit echolocation calls that are inconspicuous to eared moths, it is difficult to determine whether this was an adaptation to moth hearing or originally evolved for a different purpose [2, 3]. Aerial-hawking bats generally emit high-amplitude echolocation calls to maximize detection range [4, 5]. Here we present the first example of an echolocation counterstrategy to overcome prey hearing at the cost of reduced detection distance. We combined comparative bat flight-path tracking and moth neurophysiology with fecal DNA analysis to show that the barbastelle, Barbastella barbastellus, emits calls that are 10 to 100 times lower in amplitude than those of other aerial-hawking bats, remains undetected by moths until close, and captures mainly eared moths. Model calculations demonstrate that only bats emitting such low-amplitude calls hear moth echoes before their calls are conspicuous to moths. This stealth echolocation allows the barbastelle to exploit food resources that are difficult to catch for other aerial-hawking bats emitting calls of greater amplitude.

Sensory Basis of Food Detection in Wild Microcebus murinus

Very little is known about how nocturnal primates find their food. Here we studied the sensory basis of food perception in wild-caught gray mouse lemurs (Microcebus murinus) in Madagascar. Mouse lemurs feed primarily on fruit and arthropods. We established a set of behavioral experiments to assess food detection in wild-born, field-experienced mouse lemurs in short-term captivity. Specifically, we investigated whether they use visual, auditory, and motion cues to find and to localize prey arthropods and further whether olfactory cues are sufficient for finding fruit. Visual cues from motionless arthropod dummies were not sufficient to allow reliable detection of prey in choice experiments, nor did they trigger prey capture behavior when presented on the feeding platform. In contrast, visual motion cues from moving prey dummies attracted their attention. Behavioral observations and experiments with live and recorded insect rustling sounds indicated that the lemurs make use of prey-generated acoustic cues for foraging. Both visual motion cues and acoustic prey stimuli on their own were sufficient to trigger approach and capture behavior in the mouse lemurs. For the detection of fruit, choice experiments showed that olfactory information was sufficient for mouse lemurs to find a piece of banana. Our study provides the first experimental data on the sensory ecology of food detection in mouse lemurs. Further research is necessary to address the role of sensory ecology for food selection and possibly for niche differentiation between sympatric Microcebus species.

Cues for acoustic detection of prey: insect rustling sounds and the influence of walking substrate

SUMMARY When insects walk, they generally produce sounds. These can reveal the walkers presence and location to potential predators such as owls, bats and nocturnal primates. Additionally, predators might extract information on taxon, palatability, size or profitability from the rustling sounds. In contrast to ear morphology, hearing physiology and psychoacoustics of acoustically oriented predators, little attention has hitherto been paid to the acoustic structure and information content of prey sounds. An important element in the ecology of acoustic prey detection remained virtually unexplored: the influence of the substrate type on rustling sounds. In this study, we analysed amplitude and frequency parameters from insects walking on various natural substrates, in both Germany (Carabus beetles) and Madagascar (various beetles and cockroaches). The data show that rustling sound amplitude and frequency content depend on substrate type. On moist substrates arthropods produced less intense and less broadband rustling sounds than on dry substrates. Sound pressure level was reduced by about 6 dB, halving the detection range for the predator. For a given insect, rustling sound amplitude increased with walking speed. Finally, we found that the previously established correlation of arthropod size and rustling amplitude holds across multiple substrates. Based on these data, we provide for the first time estimates of realistic detection distances in the field. These distances range from below 1 m to over 13 m, depending on the substrate, insect mass, walking speed and background noise level. These estimates are crucial for an understanding of the foraging ecology, foraging efficiency and sensory ecology of acoustic predators.

Trophic niche flexibility in Glossophaga soricina: how a nectar seeker sneaks an insect snack

Summary 1. Omnivory enables animals to fill more than one trophic niche, providing access to a wider variety of food resources with potentially higher nutrient value, particularly when resources become scarce. Animals can achieve omnivory using different strategies, for example opportunistic foraging, or switching between multiple trophic niches. 2. The Neotropical bat Glossophaga soricina (Pallas, 1766) is a common and widespread species known for nectar feeding, but it also eats fruit and insects. Approaching stationary objects (flowers and fruits) or moving objects (insects) poses different sensory tasks and should require different echolocation behaviours. Here we tested the contrasting hypothesis that G. soricina can approach both stationary and moving objects using the same echolocation behaviour, thus feeding at different trophic levels by a single sensory mechanism. 3. Using DNA barcoding, we demonstrate that G. soricina eats beetles (Coleoptera), flies (Diptera) and noctuid moths with bat-detecting ears. Laboratory observations show that G. soricina actively hunts for prey so insect consumption does not appear to be opportunistic. After capture, individuals consumed prey while perched and manipulated them with jaw, thumb, wrist and wing movements, but food handling was longer and chewing rate slower than in obligate insectivores. 4. In contrast to most insectivorous bats, the echolocation calls of G. soricina are of high frequency and low intensity, and G. soricina did not produce feeding buzzes when approaching insects. An acoustic model of detection distances shows that its low-intensity calls fail to trigger the auditory neurons of eared moths, allowing G. soricina to overcome auditory prey defences. 5. Individuals achieved niche flexibility using a unique but generalist behavioural approach rather than employing two different specialist methods. Our findings provide a novel insight into the functional mechanisms of insect capture in G. soricina and highlight the importance of considering niche flexibility in classifying trophic links in ecological communities.

Global warming alters sound transmission: differential impact on the prey detection ability of echolocating bats

Climate change impacts the biogeography and phenology of plants and animals, yet the underlying mechanisms are little known. Here, we present a functional link between rising temperature and the prey detection ability of echolocating bats. The maximum distance for echo-based prey detection is physically determined by sound attenuation. Attenuation is more pronounced for high-frequency sound, such as echolocation, and is a nonlinear function of both call frequency and ambient temperature. Hence, the prey detection ability, and thus possibly the foraging efficiency, of echolocating bats and susceptible to rising temperatures through climate change. Using present-day climate data and projected temperature rises, we modelled this effect for the entire range of bat call frequencies and climate zones around the globe. We show that depending on call frequency, the prey detection volume of bats will either decrease or increase: species calling above a crossover frequency will lose and species emitting lower frequencies will gain prey detection volume, with crossover frequency and magnitude depending on the local climatic conditions. Within local species assemblages, this may cause a change in community composition. Global warming can thus directly affect the prey detection ability of individual bats and indirectly their interspecific interactions with competitors and prey.

The simple ears of noctuoid moths are tuned to the calls of their sympatric bat community

SUMMARY Insects with bat-detecting ears are ideal animals for investigating sensory system adaptations to predator cues. Noctuid moths have two auditory receptors (A1 and A2) sensitive to the ultrasonic echolocation calls of insectivorous bats. Larger moths are detected at greater distances by bats than smaller moths. Larger moths also have lower A1 best thresholds, allowing them to detect bats at greater distances and possibly compensating for their increased conspicuousness. Interestingly, the sound frequency at the lowest threshold is lower in larger than in smaller moths, suggesting that the relationship between threshold and size might vary across frequencies used by different bat species. Here, we demonstrate that the relationships between threshold and size in moths were only significant at some frequencies, and these frequencies differed between three locations (UK, Canada and Denmark). The relationships were more likely to be significant at call frequencies used by proportionately more bat species in the moths specific bat community, suggesting an association between the tuning of moth ears and the cues provided by sympatric predators. Additionally, we found that the best threshold and best frequency of the less sensitive A2 receptor are also related to size, and that these relationships hold when controlling for evolutionary relationships. The slopes of best threshold versus size differ, however, such that the difference in threshold between A1 and A2 is greater for larger than for smaller moths. The shorter time from A1 to A2 excitation in smaller than in larger moths could potentially compensate for shorter absolute detection distances in smaller moths.

Linking the sender to the receiver: vocal adjustments by bats to maintain signal detection in noise

Short-term adjustments of signal characteristics allow animals to maintain reliable communication in noise. Noise-dependent vocal plasticity often involves simultaneous changes in multiple parameters. Here, we quantified for the first time the relative contributions of signal amplitude, duration, and redundancy for improving signal detectability in noise. To this end, we used a combination of behavioural experiments on pale spear-nosed bats (Phyllostomus discolor) and signal detection models. In response to increasing noise levels, all bats raised the amplitude of their echolocation calls by 1.8–7.9u2009dB (the Lombard effect). Bats also increased signal duration by 13%–85%, corresponding to an increase in detectability of 1.0–5.3u2009dB. Finally, in some noise conditions, bats increased signal redundancy by producing more call groups. Assuming optimal cognitive integration, this could result in a further detectability improvement by up to 4u2009dB. Our data show that while the main improvement in signal detectability was due to the Lombard effect, increasing signal duration and redundancy can also contribute markedly to improving signal detectability. Overall, our findings demonstrate that the observed adjustments of signal parameters in noise are matched to how these parameters are processed in the receiver’s sensory system, thereby facilitating signal transmission in fluctuating environments.

Interspecific acoustic recognition in two European bat communities

Echolocating bats emit echolocation calls for spatial orientation and foraging. These calls are often species-specific and are emitted at high intensity and repetition rate. Therefore, these calls could potentially function in intra- and/or inter-specific bat communication. For example, bats in the field approach playbacks of conspecific feeding buzzes, probably because feeding buzzes indicate an available foraging patch. In captivity, some species of bats recognize and distinguish the echolocation calls of different sympatric species. However, it is still unknown if and how acoustic species-recognition mediates interspecific interactions in the field. Here we aim to understand eavesdropping on bat echolocation calls within and across species boundaries in wild bats. We presented playbacks of conspecific and heterospecific search calls and feeding buzzes to four bat species with different foraging ecologies. The bats were generally more attracted by feeding buzzes than search calls and more by the calls of conspecifics than their heterospecifics. Furthermore, bats showed differential reaction to the calls of the heterospecifics. In particular, Myotis capaccinii reacted equally to the feeding buzzes of conspecifics and to ecologically more similar heterospecifics. Our results confirm eavesdropping on feeding buzzes at the intraspecific level in wild bats and provide the first experimental quantification of potential eavesdropping in European bats at the interspecific level. Our data support the hypothesis that bat echolocation calls have a communicative potential that allows interspecific, and potentially intraspecific, eavesdropping in the wild.

Sonar detection of jittering real targets in a free-flying bat

The auditory system measures time with exceptional precision. Echolocating bats evaluate the time delay between call and echo to measure object range. An extreme and disputed result on ranging acuity was found in the virtual delay jitter experiments. In these studies, echoes with alternating delays were played back to bats, which detected a jitter down to 10 ns, corresponding to a ranging acuity of 1.7 microm. The current study was designed to measure the ranging acuity of the nectarivorous bat Glossophaga soricina under semi-natural conditions. Three free-flying bats were trained to discriminate between a stationary loudspeaker membrane and a membrane sinusoidally vibrating at 10 Hz. At detection threshold, the average peak-to-peak displacement of the vibrating membrane was 13 mm, corresponding to an echo delay jitter of 75 micros. The perceived jitter from call to call, which depends on the pulse interval and the call emission time relative to the membrane phase, was simulated for comparison with the virtual jitter experiments. This call-to-call jitter was between 20 to 25 micros (ca. 4 mm ranging acuity). These thresholds between 20 and 75 micros (4-13 mm) fall within both ecologically and physiologically plausible ranges, allowing for sufficiently precise navigation and foraging.

Tympanal mechanics and neural responses in the ears of a noctuid moth

Ears evolved in many groups of moths to detect the echolocation calls of predatory bats. Although the neurophysiology of bat detection has been intensively studied in moths for decades, the relationship between sound-induced movement of the noctuid tympanic membrane and action potentials in the auditory sensory cells (A1 and A2) has received little attention. Using laser Doppler vibrometry, we measured the velocity and displacement of the tympanum in response to pure tone pulses for moths that were intact or prepared for neural recording. When recording from the auditory nerve, the displacement of the tympanum at the neural threshold remained constant across frequencies, whereas velocity varied with frequency. This suggests that the key biophysical parameter for triggering action potentials in the sensory cells of noctuid moths is tympanum displacement, not velocity. The validity of studies on the neurophysiology of moth hearing rests on the assumption that the dissection and recording procedures do not affect the biomechanics of the ear. There were no consistent differences in tympanal velocity or displacement when moths were intact or prepared for neural recordings for sound levels close to neural threshold, indicating that this and other neurophysiological studies provide good estimates of what intact moths hear at threshold.