Evasive Flight Research Articles

A trait‐based understanding of the vulnerability of a Paleotropical moth community to predation by a sympatric bat with flexible foraging strategies

Abstract Prey vulnerability across seasons can be predicted by measuring their morphological traits and availability. Although conventional prey–predator dynamics focus on pairs of prey and predator species, the trait‐based approach allows us to draw inferences at the scale of the entire assemblage. Here, we coupled measurable prey traits with their availability in the study area, to identify the vulnerability of a diverse moth assemblage to predation by the lesser false vampire bat (Megaderma spasma) Chiroptera: Megadermatidae, Linneaus 1758, a bat with flexible foraging strategies, in the Western Ghats biodiversity hotspot of India. We analysed the discarded prey remains from several roosts, collected over 3 years, for seasonal patterns in the diet and selective hunting. Through light‐trapping, we collected moth specimens in different seasons and measured the morphological traits likely to affect their vulnerability to predation, such as body size and evasive flight capability. Our results showed that consumed moth prey diversity varies seasonally, with moths belonging to the Hepialidae family being preferred in the wet season. We found that the larger moth species with lower evasive capabilities are more vulnerable to predation. Sphingid and Hepialid moths, among the most abundant in the diet, have the lowest manoeuvrability and the maximum body size, respectively. By assessing vulnerability at the prey assemblage level, our study sets the stage for future research on moth–bat interactions from the diverse and less‐explored Paleotropical communities. In addition, the study reiterates the usefulness of trait‐based approaches to understanding prey–predator dynamics.

A visuomotor circuit for evasive flight turns in Drosophila

Visual systems extract multiple features from a scene using parallel neural circuits. Ultimately, the separate neural signals must come together to coherently influence action. Here, we characterize a circuit in Drosophila that integrates multiple visual features related to imminent threats to drive evasive locomotor turns. We identified, using genetic perturbation methods, a pair of visual projection neurons (LPLC2) and descending neurons (DNp06) that underlie evasive flight turns in response to laterally moving or approaching visual objects. Using two-photon calcium imaging or whole-cell patch clamping, we show that these cells indeed respond to both translating and approaching visual patterns. Furthermore, by measuring visual responses of LPLC2 neurons after genetically silencing presynaptic motion-sensing neurons, we show that their visual properties emerge by integrating multiple visual features across two early visual structures: the lobula and the lobula plate. This study highlights a clear example of how distinct visual signals converge on a single class of visual neurons and then activate premotor neurons to drive action, revealing a concise visuomotor pathway for evasive flight maneuvers in Drosophila.

Maximally efficient prediction in the early fly visual system may support evasive flight maneuvers.

The visual system must make predictions to compensate for inherent delays in its processing. Yet little is known, mechanistically, about how prediction aids natural behaviors. Here, we show that despite a 20-30ms intrinsic processing delay, the vertical motion sensitive (VS) network of the blowfly achieves maximally efficient prediction. This prediction enables the fly to fine-tune its complex, yet brief, evasive flight maneuvers according to its initial ego-rotation at the time of detection of the visual threat. Combining a rich database of behavioral recordings with detailed compartmental modeling of the VS network, we further show that the VS network has axonal gap junctions that are critical for optimal prediction. During evasive maneuvers, a VS subpopulation that directly innervates the neck motor center can convey predictive information about the fly's future ego-rotation, potentially crucial for ongoing flight control. These results suggest a novel sensory-motor pathway that links sensory prediction to behavior.

Light might suppress both types of sound-evoked antipredator flight in moths.

Urbanization exposes wild animals to increased levels of light, affecting particularly nocturnal animals. Artificial light at night might shift the balance of predator–prey interactions, for example, of nocturnal echolocating bats and eared moths. Moths exposed to light show less last‐ditch maneuvers in response to attacking close‐by bats. In contrast, the extent to which negative phonotaxis, moths’ first line of defense against distant bats, is affected by light is unclear. Here, we aimed to quantify the overall effect of light on both types of sound‐evoked antipredator flight, last‐ditch maneuvers and negative phonotaxis. We caught moths at two light traps, which were alternately equipped with loudspeakers that presented ultrasonic playbacks to simulate hunting bats. The light field was omnidirectional to attract moths equally from all directions. In contrast, the sound field was directional and thus, depending on the moth's approach direction, elicited either only negative phonotaxis, or negative phonotaxis and last‐ditch maneuvers. We did not observe an effect of sound playback on the number of caught moths, suggesting that light might suppress both types of antipredator flight, as either type would have caused a decline in the number of caught moths. As control, we confirmed that our playback was able to elicit evasive flight in moths in a dark flight room. Showing no effect of a treatment, however, is difficult. We discuss potential alternative explanations for our results, and call for further studies to investigate how light interferes with animal behavior.

Nonchalant Flight in Tiger Moths (Erebidae: Arctiinae) Is Correlated With Unpalatability

Many aposematic animals are well-known to exhibit generally sluggish movements. However, less is known about their escape responses when under direct threat of predation. In this study, we characterize the anti-bat escape responses of 5 species of tiger moth (Erebidae: Arctiinae), a subfamily of Lepidoptera which possess ultrasound-sensitive ears. These ears act as an early-warning system which can detect the ultrasonic cries of nearby echolocating bats, allowing the moths to enact evasive flight behaviors in an effort to escape predation. We examine the role that unpalatability plays in predicting the likelihood that individuals of a given species will enact escape behaviors in response to predation. We hypothesized that more unpalatable species would be less likely to exhibit escape maneuvers (i.e., more nonchalant) than their less unpalatable counterparts. Our results demonstrate significant interspecific variation in the degree to which tiger moths utilize evasive flight behaviors to escape bat predators as well as in their degree of unpalatability. We provide evidence for the existence of a nonchalance continuum of anti-bat evasive flight response among tiger moths and show that species are arrayed along this continuum based on their relative unpalatability to bat predators. Relatively unpalatable prey more often exhibit nonchalant flight behaviors whereas palatable prey more often employ evasive dives. Our findings demonstrate that the degree to which certain animals are protected by potent chemical defenses can influence the likelihood that they will exhibit evasive escape behaviors. Further, we argue that the bat-moth predator-prey system is an ideal model for future studies of escape behaviors of prey which overcomes some of the limitations inherent to current model systems.

Neural representation of bat predation risk and evasive flight in moths: A modelling approach

Most animals are at risk from multiple predators and can vary anti-predator behaviour based on the level of threat posed by each predator. Animals use sensory systems to detect predator cues, but the relationship between the tuning of sensory systems and the sensory cues related to predator threat are not well-studied at the community level. Noctuid moths have ultrasound-sensitive ears to detect the echolocation calls of predatory bats. Here, combining empirical data and mathematical modelling, we show that moth hearing is adapted to provide information about the threat posed by different sympatric bat species. First, we found that multiple characteristics related to the threat posed by bats to moths correlate with bat echolocation call frequency. Second, the frequency tuning of the most sensitive auditory receptor in noctuid moth ears provides information allowing moths to escape detection by all sympatric bats with similar safety margin distances. Third, the least sensitive auditory receptor usually responds to bat echolocation calls at a similar distance across all moth species for a given bat species. If this neuron triggers last-ditch evasive flight, it suggests that there is an ideal reaction distance for each bat species, regardless of moth size. This study shows that even a very simple sensory system can adapt to deliver information suitable for triggering appropriate defensive reactions to each predator in a multiple predator community.

Species‐specific strategies increase unpredictability of escape flight in eared moths

Abstract Many prey species overlap in time and space and are hunted by the same predators. A common anti‐predator behaviour is using evasive manoeuvres to escape an attacking predator. The escape‐tactic diversity hypothesis postulates that species‐specific differences in evasive behaviour will increase the overall unpredictability experienced by predators within a predator–prey community. Evolutionary, escape‐tactic diversity would be driven by the enhanced predator protection for each prey individual in the community. However, escape‐tactic diversity could also be a functional consequence of morphological differences that correlate with evasive capabilities. Echolocating bats and eared moths are a textbook example of predator–prey interactions. Moths exhibit evasive flight with diverse tactics; however, the variability of their evasive flight within and between species and individuals has never been quantified systematically. In addition, moth species show variation in size, which correlates with their flight capability. We recorded flight strength during tethered flight of eight sympatric moth species in response to the same level of simulated bat predation. Our method allowed us to record kinematic parameters that are correlated with evasive flight in a controlled way to investigate species‐specific differences in escape tactics. We show species‐specific and size‐independent differences in both overall flight strength and change of flight strength over time, supporting the escape‐tactic diversity hypothesis for eared moths. Additionally, we show strong interindividual differences in evasive flight within some species. This diversity in escape tactic between eared moths increases the overall unpredictability of evasive flight experienced by bat predators, likely providing increased protection against predatory bats for the single individual.

Continued source level reduction during attack in the low‐amplitude bat Barbastella barbastellus prevents moth evasive flight

Abstract Ears evolved independently in many insect taxa due to the selection pressure of echolocating bats. Eared moths perform evasive flight manoeuvres upon hearing approaching bats, thereby substantially increasing survival probability. Accordingly, eared moths constitute only a minor portion of many bats’ diets. In contrast, the barbastelle bat Barbastella barbastellus almost exclusively feeds on eared moths by emitting low‐amplitude stealth echolocation calls that are undetectable by distant moths. While closing in on the prey, however, the calls might become audible. We thus hypothesised that barbastelle bats lower the source level of their calls even further while closing in, such that the level at the moth's ear remains below the moth's hearing threshold and the moth fails to elicit its evasive manoeuvre. We tested these hypotheses by offering tethered moths to barbastelle bats in the wild and in captivity. We reconstructed the bats’ three‐dimensional flight paths based on time‐of‐arrival differences of the echolocation calls at four microphones, measured the received sound levels at the moth's position with an additional miniature microphone, and calculated call source levels. We show that barbastelle bats continuously reduced source level upon detecting a moth, thereby delaying the time and shortening the distance when the moth might detect the bat. The received level at the targeted moth never exceeded the moth's neuronal hearing threshold by more than 10 dB, which is likely sufficiently low to prevent moth evasive flight. Barbastelle bats emit low‐amplitude calls to counter moth hearing. Continued amplitude reduction during an attack extends the time before the prey becomes aware of the predator, if at all. In combination, these two strategies allowed barbastelle bats to access a food resource which is largely unavailable to competing species, thereby probably altering competition between sympatric predators. A plain language summary is available for this article.

Ultrasound avoidance by flying antlions (Myrmeleontidae).

The acoustic arms race between insectivorous bats and their invertebrate prey has led to the convergent evolution of ultrasound hearing in seven orders of nocturnal insects. Upon hearing the echolocation calls of an approaching bat, such insects take defensive action. Here, we document a previously unknown sense of ultrasound hearing and phonotactic flight behaviour in the neuropteran family Myrmeleontidae (antlions). The antlion Myrmeleon hyalinus was presented with sound pulses at ultrasonic frequencies used by echolocating bats and its response thresholds in tethered flight determined. Behaviours included abdominal twitches, wing flicks, brief pauses in flight and flight cessation. Such behaviours create erratic evasive flight manoeuvres in other eared insects, particularly mantids and lacewings. Antlions responded best to ultrasound between 60 and 80 kHz (75 dB peSPL at 80 kHz), showing response thresholds similar to those of the related lacewings (Neuroptera, Chrysopidae). Yet, at lower ultrasonic frequencies (20-50 kHz), antlions were far less sensitive than lacewings. Based on calculated response distances, we conclude that antlions respond only after having been detected by bats rather than using early evasive flights. We argue that the high response threshold for low-frequency ultrasound is adaptive for an insect that is mainly active close to and within vegetation, because a behavioural response to the lower ultrasonic frequencies used by high-flying bats would result in evasive action in the absence of actual predation risk.

Evolutionary escalation: the bat-moth arms race.

Echolocation in bats and high-frequency hearing in their insect prey make bats and insects an ideal system for studying the sensory ecology and neuroethology of predator-prey interactions. Here, we review the evolutionary history of bats and eared insects, focusing on the insect order Lepidoptera, and consider the evidence for antipredator adaptations and predator counter-adaptations. Ears evolved in a remarkable number of body locations across insects, with the original selection pressure for ears differing between groups. Although cause and effect are difficult to determine, correlations between hearing and life history strategies in moths provide evidence for how these two variables influence each other. We consider life history variables such as size, sex, circadian and seasonal activity patterns, geographic range and the composition of sympatric bat communities. We also review hypotheses on the neural basis for anti-predator behaviours (such as evasive flight and sound production) in moths. It is assumed that these prey adaptations would select for counter-adaptations in predatory bats. We suggest two levels of support for classifying bat traits as counter-adaptations: traits that allow bats to eat more eared prey than expected based on their availability in the environment provide a low level of support for counter-adaptations, whereas traits that have no other plausible explanation for their origination and maintenance than capturing defended prey constitute a high level of support. Specific predator counter-adaptations include calling at frequencies outside the sensitivity range of most eared prey, changing the pattern and frequency of echolocation calls during prey pursuit, and quiet, or 'stealth', echolocation.

Acoustic Aposematism and Evasive Action in Select Chemically Defended Arctiine (Lepidoptera: Erebidae) Species: Nonchalant or Not?

Tiger moths (Erebidae: Arctiinae) have experienced intense selective pressure from echolocating, insectivorous bats for over 65 million years. One outcome has been the evolution of acoustic signals that advertise the presence of toxins sequestered from the moths’ larval host plants, i.e. acoustic aposematism. Little is known about the effectiveness of tiger moth anti-bat sounds in their natural environments. We used multiple infrared cameras to reconstruct bat-moth interactions in three-dimensional (3-D) space to examine how functional sound-producing organs called tymbals affect predation of two chemically defended tiger moth species: Pygarctia roseicapitis (Arctiini) and Cisthene martini (Lithosiini). P. roseicapitis and C. martini with intact tymbals were 1.8 and 1.6 times less likely to be captured by bats relative to those rendered silent. 3-D flight path and acoustic analyses indicated that bats actively avoided capturing sound-producing moths. Clicking behavior differed between the two tiger moth species, with P. roseicapitis responding in an earlier phase of bat attack. Evasive flight behavior in response to bat attacks was markedly different between the two tiger moth species. P. roseicapitis frequently paired evasive dives with aposematic sound production. C. martini were considerably more nonchalant and employed evasion in fewer interactions. Our results show that acoustic aposematism is effective at deterring bat predation in a natural context and that this strategy is likely to be the ancestral function of tymbal organs within the Arctiinae.

Light-emitting diode street lights reduce last-ditch evasive manoeuvres by moths to bat echolocation calls.

The light-emitting diode (LED) street light market is expanding globally, and it is important to understand how LED lights affect wildlife populations. We compared evasive flight responses of moths to bat echolocation calls experimentally under LED-lit and -unlit conditions. Significantly, fewer moths performed ‘powerdive’ flight manoeuvres in response to bat calls (feeding buzz sequences from Nyctalus spp.) under an LED street light than in the dark. LED street lights reduce the anti-predator behaviour of moths, shifting the balance in favour of their predators, aerial hawking bats.

Behavioral consequences of exotic host plant adoption and the differing roles of male harassment on female movement in two checkerspot butterflies

Herbivorous insects may evolve convergent behaviors when independent adoption of a shared novel host plant places populations in environmental conditions that diverge from the ancestral state. We investigated the behavioral consequences of adopting Plantago lanceolata, an exotic species to North America, in populations of Euphydryas p. phaeton and Euphydryas editha taylori, on the east and west coasts of North America. Activity budgets and short-term movements suggested that innate species tendencies exert a greater impact on behavior than adoption of the same exotic host plant. However, female E. phaeton from a Plantago-dependent population spent more time inspecting host plants than females from a population dependent on the native host plant, Chelone glabra. Both checkerspot species had similar diffusion coefficients (D) regardless of host plant association. But, E. e. taylori step-lengths appeared bimodal and power law distributed while E. phaeton step-lengths were unimodal and best fit by an exponential distribution. We attribute this bimodal step-length distribution to the persistent harassment of courting males which induces a “long-distance” evasive flight in otherwise sedentary E. e. taylori females. In contrast, the longer distance step-lengths of E. phaeton were associated with the inspection of oviposition plants. These two checkerspot species appear to move greater distances across the reproductive landscape with contrasting motivational states that could lead to either intimate mapping (E. phaeton) or coarse mapping (E. e. taylori) of host resources.

Fine-tuned echolocation and capture-flight ofMyotis capacciniiwhen facing different sized insects and fish prey

Formerly thought to be a strictly insectivorous trawling bat, recent studies have shown that Myotis capaccinii also preys on fish. To determine whether differences exist in bat flight behaviour, prey handling and echolocation characteristics when catching fish and insects of different size, we conducted a field experiment focused on the last stage of prey capture. We used synchronized video and ultrasound recordings to measure several flight and dip features as well as echolocation characteristics, focusing on terminal buzz phase I, characterized by a call rate exceeding 100 Hz, and buzz phase II, characterized by a drop in the fundamental well below 20 kHz and a repetition rate exceeding 150 Hz. When capturing insects, bats used both parts of the terminal phase to the same extent, and performed short and superficial drags on the water surface. In contrast, when preying on fish, buzz I was longer and buzz II shorter, and the bats made longer and deeper dips. These variations suggest that lengthening buzz I and shortening buzz II when fishing is beneficial, probably because buzz I gives better discrimination ability and the broader sonar beam provided by buzz II is useless when no evasive flight of the prey is expected. Additionally, bats continued emitting calls beyond the theoretical signal-overlap zone, suggesting that they might obtain information even when they have surpassed that threshold, at least initially. This study shows that M. capaccinii can regulate the temporal components of its feeding buzzes and modify prey capture technique according to the target.

Fear: A Blessing and Curse

F ear : a B lessing and C urse B S J Shruti Koti Imagine a lone adventurer standing at the edge of a cliff, miles away from civilization. He looks down at the unknown below and, taking a deep breath, jumps, attached to nothing but a single bungee cord. He feels the wind in his face, his clothes billowing up above him, and something else: a hollow pit in his stomach and the terrifying feeling that he may die at any moment. It sounds extreme, but what he is feeling is something we have all experienced, and it is completely natural: fear. To jump, the bungee jumper had to overcome his fear of heights, a fairly common fear as far as phobias go. However, grappling with fear is not always this easy. The reason we feel fear is not a mystery – evolutionarily, it puts you on guard and reduces your likelihood of getting attacked. Bats have evolved echolocation to detect and catch their prey; moths in turn have evolved echolocation and evasive flight maneuvers. Noctuid moths, which are eaten by bats, respond to bat echolocation in three ways: a startle response, sonar jamming, and acoustic aposematism (Yager, 2012).This is a prime example of how in a predator-prey relationship, there is an evolutionary arms race in which prey is usually better adapted for exaggerated caution. This basic fear response forms the biological foundation for human anxiety disorders. Early learning theory hypothesized that stimuli that became associated with fears were equipotent, i.e. every stimulus had an equal chance of becoming a feared stimulus (Carey, 1990). However, in practice, the limited range of common fears – heights, enclosed spaces, and certain types of animals (snakes, spiders) – led theorists to favor the concept of prepotency or preparedness, which states that we are biologically predisposed to certain fears, or “primed” to automatically select certain evolutionary stimuli. Fear is a complicated term because it can refer to both an emotion and a physical response to a stimulus. A stimulus is an object or event that promotes a fear response (increased heartbeat, freezing, etc.). Then fear conditioning is the behavioral process that leads organisms to predict and react to adverse events or stimuli – this refers to the natural fear acquisition process, too, not just processes occurring in laboratories. Conditioning occurs if the probability of the unconditioned stimulus (US) in the presence of the conditioned stimulus (CS) is different than it its absence. One of the most famous examples of classical (Pavlovian) conditioning was an experiment in which a little boy was conditioned to fear white rats. Initially, he showed no fear of a white rat, the neutral stimulus. Then the rat was continuously presented along with loud, unpleasant sounds – here the sounds were the unconditioned stimulus. By repeatedly pairing the rat with the unconditioned stimulus, the white rat (now the conditioned stimulus) came to evoke a fear response (the conditioned response) in the child (Jones, 1924). In general, a selective associative model shows four basic characteristics shaped by evolution: selectivity with regard to input, or threatening stimuli; automaticity, the triggering of a response in the absence of conscious awareness; encapsulation, the resistance to conscious cognitive influences; and specialized neural circuitry, the module controlled by a specific neural circuit that has been shaped by evolution (Hofmann, 2008). “...we are biologically predisposed to certain fears, or “primed” to automatically select certain evolutionary stimuli.” In expressing fear, exposure to acute stress triggers the “fight or flight” response, stimulating activity in the hypothalamic-pituitary-adrenal (HPA) axis, the locus coreruleus, noradrenergic systems, and the neurocircuitry of the fear system. The fear circuitry includes the amygdala and its subnuclei, the nucleus accumbens, the hippocampus, ventro- medial hypothalamus, periaqueductal gray, several brain stem nuclei, thalamic nuclei, insular cortex, and some prefrontal regions. Some regions, however, play a more prominent role in fear circuitry. The forebrain structures that have expanded the most in evolution are the prefrontal cortex and the amygdala. It has been shown that damage to the right and left amygdala disrupts fear conditioning: the right correlates with expression of learning, and the left hemisphere is involved in tasks that require cognitive interpretation of stimuli (Delgado et al, 2008). There are extensive connections between the amygdala and the visual system, consistent with behavioral, lesion, and neuroimaging data which show that the amygdala tunes visual brain areas for effective perception of fear-related stimuli (Ohman, 2009). Sensory information reaches the amygdala by two pathways. The first involves classical sensory 16 • B erkeley S cientific J ournal • E xtremes • F all 2014 • V olume 19 • I ssue 1

Optimal Predator Risk Assessment by the Sonar-Jamming Arctiine Moth Bertholdia trigona

Nearly all animals face a tradeoff between seeking food and mates and avoiding predation. Optimal escape theory holds that an animal confronted with a predator should only flee when benefits of flight (increased survival) outweigh the costs (energetic costs, lost foraging time, etc.). We propose a model for prey risk assessment based on the predator's stage of attack. Risk level should increase rapidly from when the predator detects the prey to when it commits to the attack. We tested this hypothesis using a predator – the echolocating bat – whose active biosonar reveals its stage of attack. We used a prey defense – clicking used for sonar jamming by the tiger moth Bertholdia trigona– that can be readily studied in the field and laboratory and is enacted simultaneously with evasive flight. We predicted that prey employ defenses soon after being detected and targeted, and that prey defensive thresholds discriminate between legitimate predatory threats and false threats where a nearby prey is attacked. Laboratory and field experiments using playbacks of ultrasound signals and naturally behaving bats, respectively, confirmed our predictions. Moths clicked soon after bats detected and targeted them. Also, B. trigona clicking thresholds closely matched predicted optimal thresholds for discriminating legitimate and false predator threats for bats using search and approach phase echolocation – the period when bats are searching for and assessing prey. To our knowledge, this is the first quantitative study to correlate the sensory stimuli that trigger defensive behaviors with measurements of signals provided by predators during natural attacks in the field. We propose theoretical models for explaining prey risk assessment depending on the availability of cues that reveal a predator's stage of attack.

How the bat got its buzz

Since the discovery of echolocation in bats, the final phase of an attack on a flying insect, the 'terminal buzz', has proved enigmatic. During the buzz, bats increase information update rates by producing vocalizations up to 220 times s(-1). The buzz's ubiquity in hawking and trawling bats implies its importance for hunting success. Superfast muscles, previously unknown in mammals, are responsible for the extreme vocalization rate. Some bats produce a second phase-buzz II-defined by a large drop in the fundamental frequency (F(0)) of their calls. By doing so, bats broaden their acoustic field of view and should thereby reduce the likelihood of insect escape. We make the case that the buzz was a critical adaptation for capturing night-flying insects, and suggest that the drop in F(0) during buzz II requires novel, unidentified laryngeal mechanisms in order to counteract increasing muscle tension. Furthermore, we propose that buzz II represents a countermeasure against the evasive flight of eared prey in the evolutionary arms-race that saw the independent evolution of bat-detecting ears in various groups of night-flying insects.

Adaptive beam-width control of echolocation sounds by CF–FM bats,Rhinolophus ferrumequinum nippon, during prey-capture flight

The echolocation sounds of Japanese CF-FM bats (Rhinolophus ferrumequinum nippon) were measured while the bats pursued a moth (Goniocraspidum pryeri) in a flight chamber. Using a 31-channel microphone array system, we investigated how CF-FM bats adjust pulse direction and beam width according to prey position. During the search and approach phases, the horizontal and vertical beam widths were ±22±5 and ±13±5 deg, respectively. When bats entered the terminal phase approximately 1 m from a moth, distinctive evasive flight by G. pryeri was sometimes observed. Simultaneously, the bats broadened the beam widths of some emissions in both the horizontal (44% of emitted echolocation pulses) and vertical planes (71%). The expanded beam widths were ±36±7 deg (horizontal) and ±30±9 deg (vertical). When moths began evasive flight, the tracking accuracy decreased compared with that during the approach phase. However, in 97% of emissions during the terminal phase, the beam width was wider than the misalignment (the angular difference between the pulse and target directions). These findings indicate that bats actively adjust their beam width to retain the moving target within a spatial echolocation window during the final capture stages.

Echolocation behavior of the Japanese horseshoe bat in pursuit of fluttering prey

Echolocation sounds of Rhinolophus ferrumequinum nippon as they approached a fluttering moth (Goniocraspidum pryeri) were investigated using an on-board telemetry microphone (Telemike). In 40% of the successful moth-capture flights, the moth exhibited distinctive evasive flight behavior, but the bat pursued the moth by following its flight path. When the distance to the moth was approximately 3-4 m, the bats increased the duration of the pulses to 65-95 ms, which is 2-3 times longer than those during landing flight (30-40 ms). The mean of 5.8 long pulses were emitted before the final buzz phase of moth capture, without strengthening the sound pressure level. The mean duration of long pulses (79.9 ± 7.9 ms) corresponded to three times the fluttering period of G. pryeri (26.5 × 3 = 79.5 ms). These findings indicate that the bats adjust the pulse duration to increase the number of temporal repetitions of fluttering information rather than to produce more intense sonar sounds to receive fine insect echoes. The bats exhibited Doppler-shift compensation for echoes returning from large static objects ahead, but not for echoes from target moths, even though the bats were focused on capturing the moths. Furthermore, the echoes of the Telemike recordings from target moths showed spectral glints of approximately 1-1.5 kHz caused by the fluttering of the moths but not amplitude glints because of the highly acoustical attenuation of ultrasound in the air, suggesting that spectral information may be more robust than amplitude information in echoes during moth capturing flight.

Beam-width control of echolocation pulses in Japanese CF-FM bats (Rhinolophus ferrumequinum nippon) during aerial prey hunting.

Beam-width control of echolocation pulses in Japanese CF-FM bats (Rhinolophus ferrumequinum nippon) during aerial prey hunting.