Buckling-induced sound production in the aeroelastic tymbals of Yponomeuta.

The loss of elastic stability (buckling) can lead to catastrophic failure in the context of traditional engineering structures. Conversely, in nature, buckling often serves a desirable function, such as in the prey-trapping mechanism of the Venus fly trap (Dionaea muscipula). This paper investigates the buckling-enabled sound production in the wingbeat-powered (aeroelastic) tymbals of Yponomeuta moths. The hindwings of Yponomeuta possess a striated band of ridges that snap through sequentially during the up- and downstroke of the wingbeat cycle-a process reminiscent of cellular buckling in compressed slender shells. As a result, bursts of ultrasonic clicks are produced that deter predators (i.e. bats). Using various biological and mechanical characterization techniques, we show that wing camber changes during the wingbeat cycle act as the single actuation mechanism that causes buckling to propagate sequentially through each stria on the tymbal. The snap-through of each stria excites a bald patch of the wing's membrane, thereby amplifying sound pressure levels and radiating sound at the resonant frequencies of the patch. In addition, the interaction of phased tymbal clicks from the two wings enhances the directivity of the acoustic signal strength, suggesting an improvement in acoustic protection. These findings unveil the acousto-mechanics of Yponomeuta tymbals and uncover their buckling-driven evolutionary origin. We anticipate that through bioinspiration, aeroelastic tymbals will encourage novel developments in the context of multi-stable morphing structures, acoustic structural monitoring, and soft robotics.

Models for resonant acoustic metasurfaces with application to moth wing ultrasound absorption.

Taking as bioinspiration the remarkable acoustic absorption properties of moth wings, we develop a simple analytical model that describes the interaction between acoustic pressure fields, and thin elastic plates incorporating resonant sub-structures. The moth wing is an exemplar of a natural acoustic metamaterial; the wings are deeply subwavelength in thickness at the frequencies of interest, the absorption is broadband and the tiny scales resonate on the moth wing acting in concert. The simplified model incorporates only the essential physics and the scales are idealized to flat rigid rectangular plates coupled via a spring to an elastic plate that forms the wing; all the components are deep-subwavelength at desired frequencies. Based on Fourier analysis, complemented by phenomenological modelling, our theory shows excellent agreement with simulation mimicking the moth-wing structure. Moth wings operate as broadband sound absorbers employing a range of scale sizes. We demonstrate that a random distribution of scale sizes generates a broadband absorption spectrum. To further illustrate the potential of the model, we design a deeply sub-wavelength acoustic counterpart of electromagnetically induced reflectance. This article is part of the theme issue 'Wave generation and transmission in multi-scale complex media and structured metamaterials (part 2)'.

Moth wings as sound absorber metasurface.

In noise control applications, a perfect metasurface absorber would have the desirable traits of not only mitigating unwanted sound, but also being much thinner than the wavelengths of interest. Such deep-subwavelength performance is difficult to achieve technologically, yet moth wings, as natural metamaterials, offer functionality as efficient sound absorbers through the action of the numerous resonant scales that decorate their wing membrane. Here, we quantify the potential for moth wings to act as a sound-absorbing metasurface coating for acoustically reflective substrates. Moth wings were found to be efficient sound absorbers, reducing reflection from an acoustically hard surface by up to 87% at the lowest frequency tested (20 kHz), despite a thickness to wavelength ratio of up to 1/50. Remarkably, after the removal of the scales from the dorsal surface the wing's orientation on the surface changed its absorptive performance: absorption remains high when the bald wing membrane faces the sound but breaks down almost completely in the reverse orientation. Numerical simulations confirm the strong influence of the air gap below the wing membrane but only when it is adorned with scales. The finding that moth wings act as deep-subwavelength sound-absorbing metasurfaces opens the door to bioinspired, high-performance sound mitigation solutions.

Acoustic deterrents influence foraging activity, flight and echolocation behaviour of free-flying bats.

Acoustic deterrents have shown potential as a viable mitigation measure to reduce human impacts on bats; however, the mechanisms underpinning acoustic deterrence of bats have yet to be explored. Bats avoid ambient ultrasound in their environment and alter their echolocation calls in response to masking noise. Using stereo thermal videogrammetry and acoustic methods, we tested predictions that: (i) bats would avoid acoustic deterrents and forage and social call less in a 'treated airspace'; (ii) deterrents would cause bats to fly with more direct flight paths akin to commuting behaviour and in line with a reduction in foraging activity, resulting in increased flight speed and decreased flight tortuosity; and (iii) bats would alter their echolocation call structure in response to the masking deterrent sound. As predicted, overall bat activity was reduced by 30% and we recorded a significant reduction in counts of Pipistrellus pygmaeus (27%), Myotis spp. (probably M. daubentonii) (26%), and Nyctalus spp. and Eptesicus spp. (68%) passes. Pipistrellus pygmaeus feeding buzzes were also reduced by the deterrent in relation to general activity (by 38%); however, social calls were not (only 23% reduction). Bats also increased their flight speed and reduced the tortuosity of their flight paths, and P. pygmaeus reduced echolocation call bandwidth and start frequency of calls in response to deterrent playback, probably owing to the masking effect of the sound. Deterrence could therefore be used to remove bats from areas where they forage, for example wind turbines and roads, where they may be under threat from direct mortality.

Wingtip folds and ripples on saturniid moths create decoy echoes against bat biosonar.

Sensory coevolution has equipped certain moth species with passive acoustic defenses to counter predation by echolocating bats.1,2 Some large silkmoths (Saturniidae) possess curved and twisted biosonar decoys at the tip of elongated hindwing tails.3,4 These are thought to create strong echoes that deflect biosonar-guided bat attacks away from the moth's body to less essential parts of their anatomy. We found that closely related silkmoths lacking such hindwing decoys instead often possess intriguing ripples and folds on the conspicuously lobed tips of their forewings. The striking analogy of twisted shapes displayed far from the body suggests these forewing structures might function as alternative acoustic decoys. Here we reveal that acoustic reflectivity and hence detectability of such wingtips is higher than that of the body at ultrasonic frequencies used by hunting bats. Wingtip reflectivity is higher the more elaborate the structure and the further from the body. Importantly, wingtip reflectivity is often considerably higher than in a well-studied functional hindwing decoy. Such increased reflectivity would misdirect the bat's sonar-guided attack toward the wingtip, resulting in similar fitness benefits to hindwing acoustic decoys. Structurally, folded wingtips present echo-generating surfaces to many directions, and folds and ripples can act as retroreflectors that together create conspicuous targets. Phylogenetically, folds and ripples at wingtips have evolved multiple times independently within silkmoths and always as alternatives to hindwing decoys. We conclude that they function as acoustic wingtip decoys against bat biosonar. VIDEO ABSTRACT.

Moth wings are acoustic metamaterials.

Metamaterials assemble multiple subwavelength elements to create structures with extraordinary physical properties (1-4). Optical metamaterials are rare in nature and no natural acoustic metamaterials are known. Here, we reveal that the intricate scale layer on moth wings forms a metamaterial ultrasound absorber (peak absorption = 72% of sound intensity at 78 kHz) that is 111 times thinner than the longest absorbed wavelength. Individual scales act as resonant (5) unit cells that are linked via a shared wing membrane to form this metamaterial, and collectively they generate hard-to-attain broadband deep-subwavelength absorption. Their collective absorption exceeds the sum of their individual contributions. This sound absorber provides moth wings with acoustic camouflage (6) against echolocating bats. It combines broadband absorption of all frequencies used by bats with light and ultrathin structures that meet aerodynamic constraints on wing weight and thickness. The morphological implementation seen in this evolved acoustic metamaterial reveals enticing ways to design high-performance noise mitigation devices.

A new stump-toed frog from the transitional forests of NW Madagascar (Anura, Microhylidae, Cophylinae, Stumpffia).

A new species of the miniaturised microhylid frog genus Stumpffia, from north-western Madagascar, is described. Stumpffia froschaueri sp. nov. differs from all other described Stumpffia species in colouration and morphology and is genetically divergent (≥ 7% uncorrected p-distance to all other nominal species of the genus) in a fragment of the mitochondrial 16S rRNA gene and in a segment of the nuclear Rag-1 gene. The new species is reliably known only from a few specimens collected in the Sahamalaza (and surroundings) region. Its known distribution is limited to three forest patches severely threatened by fire, drought and high levels of forest clearance, thus suggesting a classification of "Critically Endangered" according to IUCN Red List criteria.

Thoracic scales of moths as a stealth coating against bat biosonar.

Many moths are endowed with ultrasound-sensitive ears that serve the detection and evasion of echolocating bats. Moths lacking such ears could still gain protection from bat biosonar by using stealth acoustic camouflage, absorbing sound waves rather than reflecting them back as echoes. The thorax of a moth is bulky and hence acoustically highly reflective. This renders it an obvious target for any bat. Much of the thorax of moths is covered in hair-like scales, the layout of which is remarkably similar in structure and arrangement to natural fibrous materials commonly used in sound insulation. Despite this structural similarity, the effect of thorax scales on moth echoes has never been characterized. Here, we test whether and how moth thorax scales function as an acoustic absorber. From tomographic echo images, we find that the thin layer of thoracic scales of diurnal butterflies affects the strength of ultrasound echoes from the thorax very little, while the thorax scales of earless moths absorbs an average of 67 ± 9% of impinging ultrasonic sound energy. We show that the thorax scales of moths provide acoustic camouflage by acting as broadband (20-160 kHz) stealth coating. Modelling results suggest the scales are acting as a porous sound absorber; however, the thorax scales of moths achieve a considerably higher absorption than technical fibrous porous absorbers with the same structural parameters. Such scales, despite being thin and lightweight, constitute a broadband, multidirectional and efficient ultrasound absorber that reduces the moths' detectability to hunting bats and gives them a survival advantage.

Comparing acoustic and radar deterrence methods as mitigation measures to reduce human-bat impacts and conservation conflicts.

Where humans and wildlife co-exist, mitigation is often needed to alleviate potential conflicts and impacts. Deterrence methods can be used to reduce impacts of human structures or activities on wildlife, or to resolve conservation conflicts in areas where animals may be regarded as a nuisance or pose a health hazard. Here we test two methods (acoustic and radar) that have shown potential for deterring bats away from areas where they forage and/or roost. Using both infrared video and acoustic methods for counting bat passes, we show that ultrasonic speakers were effective as bat deterrents at foraging sites, but radar was not. Ultrasonic deterrents decreased overall bat activity (filmed on infrared cameras) by ~80% when deployed alone and in combination with radar. However, radar alone had no effect on bat activity when video or acoustic data were analysed using generalised linear mixed effect models. Feeding buzzes of all species were reduced by 79% and 69% in the ultrasound only treatment when compared to the control and radar treatments, but only the ultrasound treatment was significant in post-hoc tests. Species responded differently to the ultrasound treatments and we recorded a deterrent effect on both Pipistrellus pipistrellus (~40-80% reduction in activity) and P. pygmaeus (~30-60% reduction), but not on Myotis species. However, only the ultrasound and radar treatment was significant (when compared to control and radar) in post-hoc tests for P. pipistrellus. Deterrent treatment was marginally non-significant for P. pygmaeus, but the ultrasound only treatment was significant when compared to radar in post-hoc tests. We therefore suggest that acoustic, but not radar methods are explored further as deterrents for bats. The use of acoustic deterrence should always be assessed on a case-by-case basis, with a focus on bat conservation.

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.

Nathusius' bats optimize long-distance migration by flying at maximum range speed.

Aerial migration is the fastest, yet most energetically demanding way of seasonal movement between habitats. However, for many taxa, and bats in particular, we lack a clear understanding of the energy requirements for migration. Here, we examined the energetic cost and flight speed of the long-distance migratory Nathusius' bat (Pipistrellus nathusii). We measured flight metabolism in relation to airspeed in a wind tunnel, inferred the optimal traveling speed over long distances, i.e. maximum range speed, and compared this value with flight speed measured in wild conspecifics. Body mass and wing morphologies were similar in captive and wild bats, indicating that the body condition of captive bats was similar to that of migratory bats. Nine out of the 12 captive bats exhibited a U-shaped relationship between flight metabolic power and airspeed when flying in the wind tunnel. The flight metabolic rate across all airspeeds averaged 0.98±0.28 W, which corresponds well to established allometric relationships between flight metabolic rate and body mass for bats. During summer migration, P. nathusii traveled at an average speed of 6.9±0.7 m s-1, which was significantly higher than the minimum power speed (5.8±1.0 m s-1), yet within the range of expected maximum range speed inferred from wind tunnel experiments. This suggests that P. nathusii may migrate at an energetically optimal speed and that aerial refueling does not substantially lower migratory speed in P. nathusii.

Deaf moths employ acoustic Müllerian mimicry against bats using wingbeat-powered tymbals.

Emitting ultrasound upon hearing an attacking bat is an effective defence strategy used by several moth taxa. Here we reveal how Yponomeuta moths acquire sophisticated acoustic protection despite being deaf themselves and hence unable to respond to bat attacks. Instead, flying Yponomeuta produce bursts of ultrasonic clicks perpetually; a striated patch in their hind wing clicks as the beating wing rotates and bends. This wing structure is strikingly similar to the thorax tymbals with which arctiine moths produce their anti-bat sounds. And indeed, Yponomeuta sounds closely mimic such arctiine signals, revealing convergence in form and function. Because both moth taxa contain noxious compounds, we conclude they are mutual Müllerian acoustic mimics. Yponomeuta's perpetual clicking would however also attract bat predators. In response, their click amplitude is reduced and affords acoustic protection just as far as required, matching the distance over which bat biosonar would pick up Yponomeuta echoes anyway - advanced acoustic defences for a deaf moth.

Biomechanics of a moth scale at ultrasonic frequencies.

The wings of moths and butterflies are densely covered in scales that exhibit intricate shapes and sculptured nanostructures. While certain butterfly scales create nanoscale photonic effects, moth scales show different nanostructures suggesting different functionality. Here we investigate moth-scale vibrodynamics to understand their role in creating acoustic camouflage against bat echolocation, where scales on wings provide ultrasound absorber functionality. For this, individual scales can be considered as building blocks with adapted biomechanical properties at ultrasonic frequencies. The 3D nanostructure of a full Bunaea alcinoe moth forewing scale was characterized using confocal microscopy. Structurally, this scale is double layered and endowed with different perforation rates on the upper and lower laminae, which are interconnected by trabeculae pillars. From these observations a parameterized model of the scale's nanostructure was formed and its effective elastic stiffness matrix extracted. Macroscale numerical modeling of scale vibrodynamics showed close qualitative and quantitative agreement with scanning laser Doppler vibrometry measurement of this scale's oscillations, suggesting that the governing biomechanics have been captured accurately. Importantly, this scale of B. alcinoe exhibits its first three resonances in the typical echolocation frequency range of bats, suggesting it has evolved as a resonant absorber. Damping coefficients of the moth-scale resonator and ultrasonic absorption of a scaled wing were estimated using numerical modeling. The calculated absorption coefficient of 0.50 agrees with the published maximum acoustic effect of wing scaling. Understanding scale vibroacoustic behavior helps create macroscopic structures with the capacity for broadband acoustic camouflage.

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.

PRINCIPLES AND PATTERNS OF BAT MOVEMENTS: FROM AERODYNAMICS TO ECOLOGY.

Movement ecology as an integrative discipline has advanced associated fields because it presents not only a conceptual framework for understanding movement principles but also helps formulate predictions about the consequences of movements for animals and their environments. Here, we synthesize recent studies on principles and patterns of bat movements in context of the movement ecology paradigm. The motion capacity of bats is defined by their highly articulated, flexible wings. Power production during flight follows a U-shaped curve in relation to speed in bats yet, in contrast to birds, bats use mostly exogenous nutrients for sustained flight. The navigation capacity of most bats is dominated by the echolocation system, yet other sensory modalities, including an iron-based magnetic sense, may contribute to navigation depending on a bat's familiarity with the terrain. Patterns derived from these capacities relate to antagonistic and mutualistic interactions with food items. The navigation capacity of bats may influence their sociality, in particular, the extent of group foraging based on eavesdropping on conspecifics' echolocation calls. We infer that understanding the movement ecology of bats within the framework of the movement ecology paradigm provides new insights into ecological processes mediated by bats, from ecosystem services to diseases.

Place recognition using batlike sonar.

Echolocating bats have excellent spatial memory and are able to navigate to salient locations using bio-sonar. Navigating and route-following require animals to recognize places. Currently, it is mostly unknown how bats recognize places using echolocation. In this paper, we propose template based place recognition might underlie sonar-based navigation in bats. Under this hypothesis, bats recognize places by remembering their echo signature - rather than their 3D layout. Using a large body of ensonification data collected in three different habitats, we test the viability of this hypothesis assessing two critical properties of the proposed echo signatures: (1) they can be uniquely classified and (2) they vary continuously across space. Based on the results presented, we conclude that the proposed echo signatures satisfy both criteria. We discuss how these two properties of the echo signatures can support navigation and building a cognitive map.

Sensorimotor Model of Obstacle Avoidance in Echolocating Bats.

Bat echolocation is an ability consisting of many subtasks such as navigation, prey detection and object recognition. Understanding the echolocation capabilities of bats comes down to isolating the minimal set of acoustic cues needed to complete each task. For some tasks, the minimal cues have already been identified. However, while a number of possible cues have been suggested, little is known about the minimal cues supporting obstacle avoidance in echolocating bats. In this paper, we propose that the Interaural Intensity Difference (IID) and travel time of the first millisecond of the echo train are sufficient cues for obstacle avoidance. We describe a simple control algorithm based on the use of these cues in combination with alternating ear positions modeled after the constant frequency bat Rhinolophus rouxii. Using spatial simulations (2D and 3D), we show that simple phonotaxis can steer a bat clear from obstacles without performing a reconstruction of the 3D layout of the scene. As such, this paper presents the first computationally explicit explanation for obstacle avoidance validated in complex simulated environments. Based on additional simulations modelling the FM bat Phyllostomus discolor, we conjecture that the proposed cues can be exploited by constant frequency (CF) bats and frequency modulated (FM) bats alike. We hypothesize that using a low level yet robust cue for obstacle avoidance allows bats to comply with the hard real-time constraints of this basic behaviour.

Acoustic shadows help gleaning bats find prey, but may be defeated by prey acoustic camouflage on rough surfaces.

Perceptual abilities of animals, like echolocating bats, are difficult to study because they challenge our understanding of non-visual senses. We used novel acoustic tomography to convert echoes into visual representations and compare these cues to traditional echo measurements. We provide a new hypothesis for the echo-acoustic basis of prey detection on surfaces. We propose that bats perceive a change in depth profile and an 'acoustic shadow' cast by prey. The shadow is more salient than prey echoes and particularly strong on smooth surfaces. This may explain why bats look for prey on flat surfaces like leaves using scanning behaviour. We propose that rather than forming search images for prey, whose characteristics are unpredictable, predators may look for disruptions to the resting surface (acoustic shadows). The fact that the acoustic shadow is much fainter on rougher resting surfaces provides the first empirical evidence for 'acoustic camouflage' as an anti-predator defence mechanism.

A new species of the Boophis rappiodes group (Anura, Mantellidae) from the Sahamalaza Peninsula, northwest Madagascar, with acoustic monitoring of its nocturnal calling activity.

A new species of treefrog of the Boophis rappiodes group (Anura, Mantellidae) is described from the Sahamalaza - Iles Radama National Park in northwest Madagascar. This new species is green in colour with bright red speckling across its head and dorsum; similar in morphology to other species of this group including: B. bottae, B. rappiodes, B. erythrodactylus and B. tasymena. The new species can be distinguished by its advertisement call and by a genetic divergence of more than 4.9% in the analysed mitochondrial 16S rRNA gene fragment. Its call consists of two note types: a trill and a click; although similar sounding to B. bottae, the trill note of the new species has a faster pulse rate while the click note is predominantly two-pulsed rather than three. All individuals were detected from the banks of two streams in Ankarafa Forest. The new species represents the only member of the B. rappiodes group endemic to Madagascar's western coast, with the majority of other members known from the eastern rainforest belt. Despite its conspicuous call, it has not been detected from other surveys of northwest Madagascar and it is likely to be a local endemic to the peninsula. The ranges of two other amphibian species also appear restricted to Sahamalaza, and so the area seems to support a high level of endemicity. Although occurring inside a National Park, this species is highly threatened by the continuing decline in the quality and extent of its habitat. Due to these threats it is proposed that this species should be classified as Critically Endangered according to the IUCN Red List criteria.

A whispering bat that screams: bimodal switch of foraging guild from gleaning to aerial hawking in the desert long-eared bat.

Echolocating bats have historically been classified as either loud aerial hawkers or whispering gleaners. Some bat species can forage in multiple ways and others have demonstrated limited flexibility in the amplitude of their echolocation calls. The desert long-eared bat, Otonycteris hemprichii, has been said to be a passive gleaning whispering bat preying on terrestrial arthropods such as scorpions. Using an acoustic tracking system, we recorded individuals flying at foraging and drinking sites and compared their flight height, flight speed, call duration, pulse interval and source levels with those of gleaning individuals previously recorded using the same setup. We found differences in all variables with the strongest difference in source levels, where bats called at a mean of 119 dB peSPL (compared with 75 dB peSPL when gleaning). Bat faecal analysis indicated that their diet differed from previous studies and that prey species were capable of flight. We conclude that the bats switched from passive gleaning to capturing airborne insects (aerial hawking). Although whispering bats have been known to opportunistically catch insects on the wing, in the present study we show a full bimodal switch between foraging guilds with the respective changes in source level to those typical of a true aerial hawker.