Eared Moths Research Articles

Tracing and 3-dimensional representation of the primary afferents from the moth ear

Heliothine moths perceive acoustic information via two auditory sensory neurons only. Previous cobalt staining experiments have described the projection pattern of the two auditory neurons, called the A1 and the A2 cell, plus one additional neuron, the so-called B cell, up to the prothorax. We have obtained new and improved data about the projection pattern of the three sensory afferents by means of fluorescent staining experiments combined with scanning confocal microscopy. The present data show the fine structure of each sensory axon that arises from the moth ear and its ascending pathway relative to that of the others. In accordance with the previous data, the A2 auditory cell was found to extend projections in the pterothorax only. A novel finding is that terminal branches of the A2 cell cross the midline. The staining pattern of the two remaining neurons, the A1 and B cell, which project tightly together in the thoracic ganglia, differ somewhat from that previously described. As demonstrated here, one of these two neurons, the A1 cell, terminates in the prothoracic ganglion whereas the other, the B cell, projects further on via the cervical connectives to the subesophageal ganglion. The current data, therefore, indicate that none of the auditory afferents in the heliothine moth projects to the brain.

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

Summary 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. 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. 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. 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. 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.

Mechanical tuning of the moth ear: distortion-product otoacoustic emissions and tympanal vibrations

The mechanical tuning of the ear in the moth Empyreuma pugione was investigated by distortion-product otoacoustic emissions (DPOAE) and laser Doppler vibrometry (LDV). DPOAE audiograms were assessed using a novel protocol that may be advantageous for non-invasive auditory studies in insects. To evoke DPOAE, two-tone stimuli within frequency and level ranges that generated a large matrix of values (960 frequency-level combinations) were used to examine the acoustic space in which the moth tympanum shows its best mechanical and acoustical responses. The DPOAE tuning curve derived from the response matrix resembles that obtained previously by electrophysiology, and is V-shaped and tuned to frequencies between 25 and 45 kHz with low Q10dB values of 1.21±0.26. In addition, while using a comparable stimulation regime, mechanical distortion in the displacement of the moth's tympanal membrane at the stigma was recorded with a laser Doppler vibrometer. The corresponding mechanical vibration audiograms were compared with DPOAE audiograms. Both types of audiograms have comparable shape, but most of the mechanical response fields are shifted towards lower frequencies. We showed for the first time in moths that DPOAE have a pronounced analogy in the vibration of the tympanic membrane where they may originate. Our work supports previous studies that point to the stigma (and the internally associated transduction machinery) as an important place of sound amplification in the moth ear, but also suggests a complex mechanical role for the rest of the transparent zone.

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

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.

Ultra high frequency hearing in a moth

Ultra high frequency hearing in a moth

Sound Strategies: The 65-Million-Year-Old Battle Between Bats and Insects

The intimate details regarding the coevolution of bats and moths have been elucidated over the past 50 years. The bat-moth story began with the evolution of bat sonar, an exquisite ultrasonic system for tracking prey through the night sky. Moths countered with ears tuned to the high frequencies of bat echolocation and with evasive action through directed turns, loops, spirals, drops, and power dives. Some bat species responded by moving the frequency and intensity of their echolocation cries away from the peak sensitivity of moth ears, and the arms race was on. Tiger moths countered by producing anti-bat sounds. Do the sounds advertise moth toxicity, similar to the bright coloration of butterflies; do they startle the bat, giving the moth a momentary advantage in their aerobatic battle; or do they jam the sonar of the bat? The answer is yes. They do all and more in different situations and in different species. Any insect that flies at night must deal with bat predation. Beetles, mantids, true crickets, mole crickets, katydids, green lacewings, and locusts have anti-bat strategies, and we have just scratched the surface. In an exciting new twist, researchers are taking the technologies developed in the laboratory back into the field, where they are poised to appreciate the full richness of this remarkable predator-prey interaction.

Life: ‘whispering’ gives bats advantage: Quieter echolocation allows closer approach to eared moths

Science NewsVolume 178, Issue 6 p. 12-12 In the News Life: ‘whispering’ gives bats advantage: Quieter echolocation allows closer approach to eared moths Susan Millus, Susan MillusSearch for more papers by this author Susan Millus, Susan MillusSearch for more papers by this author First published: 31 August 2010 https://doi.org/10.1002/scin.5591780614AboutPDF ToolsRequest permissionExport citationAdd to favoritesTrack citation ShareShare Give accessShare full text accessShare full-text accessPlease review our Terms and Conditions of Use and check box below to share full-text version of article.I have read and accept the Wiley Online Library Terms and Conditions of UseShareable LinkUse the link below to share a full-text version of this article with your friends and colleagues. Learn more.Copy URL Share a linkShare onFacebookTwitterLinked InRedditWechat No abstract is available for this article. Volume178, Issue611 September 2010Pages 12-12 RelatedInformation

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.

Auditory sensitivity and ecological relevance: the functional audiogram as modelled by the bat detecting moth ear

Auditory sensitivity has often been measured by identifying neural threshold in real-time (online) which can introduce bias in the audiograms that are produced. We tested this by recording auditory nerve activity of the notodontid moth Nadata gibbosa elicited by bat-like ultrasound and analysing the response offline. We compared this audiogram with a published online audiogram showing that the bias introduced can result in a difference in the audiogram shape. In the second part of our study we compared offline audiograms using spike number as threshold with others that used spike period and stimulus/spike latency, variables that have been suggested as providing behaviourally functional criteria. These comparisons reveal that functional audiograms are more flatly tuned than simple spike audiograms. The shapes of behavioural audiograms are discussed in the context of the selection pressure that maintains their shape, bat predation. Finally, we make predictions on the distance from bats at which notodontid moths use negative phonotaxis or the acoustic startle response.

Reanalyzing auditory sensitivity: The functional audiogram as modeled by the bat detecting moth ear.

Auditory sensitivity has often been measured by identifying neural threshold in real time (online) which can introduce bias in the audiograms that are produced. This was tested by recording auditory nerve activity of the Notodontid moth Nadata gibbosa elicited by bat-like ultrasound and analyzing the response offline. The offline audiogram was compared to a published online audiogram showing that the bias introduced can result in a difference in both the best frequency of this moth ear and the audiogram shape. The offline neural threshold audiogram was then compared to audiograms produced using behavioral threshold definitions based on (1) spike period and (2) the latency to first spike, showing that audiograms produced using these theoretical behavioral definitions to have a similar shape. Finally, predictions on the distance at which Notodontid moths may evade bats using negative phonotaxis or the acoustic startle response are made, using the number of spikes elicited as a proxy for distance.

Is food resource partitioning responsible for deviation of echolocation call frequencies from allometry in Rhinolophus macrotis?

There is an apparent allometric relationship between peak frequency of echolocation and body size in rhinophilids. However, some rhinolophids deviate from this rule. To date this variation has been explained as a result of partitioning of communication channels. An alternative hypothesis that food resource partitioning results in this divergence in expected frequencies was tested by comparing prey selection between Rhinolophus macrotis Blyth, 1844 and Rhinolophus lepidus Blyth, 1844 in Yunnan Province, China. These two sympatric species are morphologically similar but acoustically divergent: R. macrotis has an echolocation frequency significantly lower than that predicted by the allometric relationship, whereas that of R. lepidus agreed with expectations. Prey selection experiments, conducted in a flight tent, indicated that the dominant prey taxa of R. macrotis were Lasiocampidae, Arctiidae and Noctuidae, whilst that of R. lepidus were Arctiidae, Noctuidae and Ichneumonidae. R. macrotis ate more earless moths and fewer eared moths than R. lepidus, and R. macrotis fed on larger prey in general and captured a wider size range than that captured by R. lepidus. These results confirmed the existence of finely tuned trophic niche differentiation and suggested that food resource partitioning is one of the factors leading to lower peak frequency of calls in R. macrotis.

Tiger moths and the threat of bats: decision-making based on the activity of a single sensory neuron

Echolocating bats and eared moths are a model system of predator-prey interaction within an almost exclusively auditory world. Through selective pressures from aerial-hawking bats, noctuoid moths have evolved simple ears that contain one to two auditory neurons and function to detect bat echolocation calls and initiate defensive flight behaviours. Among these moths, some chemically defended and mimetic tiger moths also produce ultrasonic clicks in response to bat echolocation calls; these defensive signals are effective warning signals and may interfere with bats' ability to process echoic information. Here, we demonstrate that the activity of a single auditory neuron (the A1 cell) provides sufficient information for the toxic dogbane tiger moth, Cycnia tenera, to decide when to initiate defensive sound production in the face of bats. Thus, despite previous suggestions to the contrary, these moths' only other auditory neuron, the less sensitive A2 cell, is not necessary for initiating sound production. However, we found a positive linear relationship between combined A1 and A2 activity and the number of clicks the dogbane tiger moth produces.

Ultrasonic hearing in moths

Many moths possess ultrasound-sensitive ears, directly resulted from bat predation. Moth ears display an abundant diversity due to their body location, accessory structures, and number of auditory sensory cells. Anatomically, the moth ears are the simplest hearing organs in insects and most are tympanal organ with a tympanum. Eared moths have an optimal frequency range between 20 kHz and 50 kHz, which coincides with the peak frequency used by most insectivorous bats. The primary function of the moth ear is to detect and avoid the hunting of bats. Eared moths show a series of defensive behaviors, when they are exposed to the cries emitted by insectivorous bats. The presence of these tympanal organs also set the stage for the later evolution of ultrasonic courtship signals in the eared moth families. Over the years, entomologists worldwide have performed large numbers of studies on hearing of moths and their interactions with bats. This paper presents an overview of moth hearing, focusing on morphology, neurophysiology, and behavioral ecology.

Otoacoustic emissions from insect ears: evidence of active hearing?

Sensitive hearing organs often employ nonlinear mechanical sound processing which generates distortion-product otoacoustic emissions (DPOAE). Such emissions are also recordable from tympanal organs of insects. In vertebrates (including humans), otoacoustic emissions are considered by-products of active sound amplification through specialized sensory receptor cells in the inner ear. Force generated by these cells primarily augments the displacement amplitude of the basilar membrane and thus increases auditory sensitivity. As in vertebrates, the emissions from insect ears are based on nonlinear mechanical properties of the sense organ. Apparently, to achieve maximum sensitivity, convergent evolutionary principles have been realized in the micromechanics of these hearing organs-although vertebrates and insects possess quite different types of receptor cells in their ears. Just as in vertebrates, otoacoustic emissions from insects ears are vulnerable and depend on an intact metabolism, but so far in tympanal organs, it is not clear if auditory nonlinearity is achieved by active motility of the sensory neurons or if passive cellular characteristics cause the nonlinear behavior. In the antennal ears of flies and mosquitoes, however, active vibrations of the flagellum have been demonstrated. Our review concentrates on experiments studying the tympanal organs of grasshoppers and moths; we show that their otoacoustic emissions are produced in a frequency-specific way and can be modified by electrical stimulation of the sensory cells. Even the simple ears of notodontid moths produce distinct emissions, although they have just one auditory neuron. At present it is still uncertain, both in vertebrates and in insects, if the nonlinear amplification so essential for sensitive sound processing is primarily due to motility of the somata of specialized sensory cells or to active movement of their (stereo-)cilia. We anticipate that further experiments with the relatively simple ears of insects will help answer these questions.

Beware of bats, beware of birds: the auditory responses of eared moths to bat and bird predation

The allotonic frequency hypothesis (AFH) proposes that the preponderance of moths in the diets of some bats (e.g., Rhinolophidae) is the result of these bats echolocating at allotonic frequencies, that is, outside of the typical hearing range of most moths (ca., 20–60 kHz). The broader hearing range of African moths (5–110 kHz) suggests that their ears may function at frequencies usually considered allotonic. We investigated 1) whether moth ears were functionally audible to the Cape horseshoe bat, Rhinolophus capensis (Rhinolophidae), which forages in dense vegetation and echolocates at 84 kHz, and 2) whether moth auditory sensitivity below 10 kHz allows them to detect the rustling noises made by bird predators as they pursued moths through vegetation. The calls of R. capensis were audible to moths albeit over shorter distances relative to syntonic bats. Shorter detection distances combined with the constrained spaces in the cluttered habitat in which rhinolophids forage give moths both less time and less space within which to react to an attacking bat. Thus, the AFH in combination with habitat offers a better explanation for the preponderance of moths in the diets of rhinolophids than either of them on their own. Moths also responded both neurologically and behaviorally to the rustling sounds made by birds (Cape Bulbul, Pycnonotus capensis) as they pursued moths. We suggest that the high sensitivity of moths to frequencies from 5 to 10 kHz allows them to avoid these avian attacks by using responses that have traditionally been considered solely anti-bat behavior. Key words: allotonic frequency hypothesis, audition, bats, birds, moths, predation. [Behav Ecol]

Ignoring the irrelevant: auditory tolerance of audible but innocuous sounds in the bat-detecting ears of moths

Noctuid moths listen for the echolocation calls of hunting bats and respond to these predator cues with evasive flight. The African bollworm moth, Helicoverpa armigera, feeds at flowers near intensely singing cicadas, Platypleura capensis, yet does not avoid them. We determined that the moth can hear the cicada by observing that both of its auditory receptors (A1 and A2 cells) respond to the cicada's song. The firing response of the A1 cell rapidly adapts to the song and develops spike periods in less than a second that are in excess of those reported to elicit avoidance flight to bats in earlier studies. The possibility also exists that for at least part of the day, sensory input in the form of olfaction or vision overrides the moth's auditory responses. While auditory tolerance appears to allow H. armigera to exploit a food resource in close proximity to acoustic interference, it may render their hearing defence ineffective and make them vulnerable to predation by bats during the evening when cicadas continue to sing. Our study describes the first field observation of an eared insect ignoring audible but innocuous sounds.

Mechanics of a `simple' ear: tympanal vibrations in noctuid moths

Anatomically, the ears of moths are considered to be among the simplest ears found in animals. Microscanning laser vibrometry was used to examine the surface vibrations of the entire tympanal region of the ears of the noctuid moths Agrotis exclamationis, Noctua pronuba, Xestia c-nigrum and Xestia triangulum. During stimulation with ultrasound at intensities known to activate receptor neurones, the tympanum vibrates with maximum deflection amplitudes at the location where the receptor cells attach. In the reportedly heterogeneous tympana of noctuid moths, this attachment site is an opaque zone that is surrounded by a transparent, thinner cuticular region. In response to sound pressure, this region moves relatively little compared with the opaque zone. Thus, the deflections of the moth tympanic membrane are not those of a simple circular drum. The acoustic sensitivity of the ear of N. pronuba, as measured on the attachment site, is 100+/-14 nm Pa(-1) (N=10), corresponding to tympanal motion of a mere 200 pm at sound pressure levels near the neural threshold.

L1,L2 maps of distortion-product otoacoustic emissions from a moth ear with only two auditory receptor neurons

The tympanal organ of the moth Empyreuma affinis emits physiologically vulnerable distortion-product otoacoustic emissions. To assess the nature of underlying mechanical nonlinearities, we measured L1,L2 maps by varying both stimulus levels. Two types of maps were found: (1) Maps containing dominant islands centered at the L1=L2 diagonal as it is typical for saturating nonlinearities that can be described by Boltzmann functions. In contrast to maps published for mammals and frogs, the shape of such islands includes sharp ridges at L1 or L2 levels close to 70 dB sound pressure level. This could be produced by a strongly asymmetric operating point of the respective transfer functions, consistent with the fact that the auditory sensory cells are not hair cells but primary mechanoreceptors with a single cilium. The saturating map components could be selectively reduced by acoustic suppression. (2) Maps where separated islands were less conspicuous but in which the dominant feature consisted of contour lines which were orthogonal to the L1=2L2 diagonal and could be generated by an expansive nonlinearity. Maps showing strong islands were found for f2 frequencies between 26.7 and 45 kHz, maps without strong islands for f2 between 42 and 57.5 kHz. This suggests a frequency-dependent change regarding the involved mechanical nonlinearities.

Keeping up with Bats: Dynamic Auditory Tuning in a Moth

Many night-flying insects evolved ultrasound sensitive ears in response to acoustic predation by echolocating bats . Noctuid moths are most sensitive to frequencies at 20-40 kHz , the lower range of bat ultrasound . This may disadvantage the moth because noctuid-hunting bats in particular echolocate at higher frequencies shortly before prey capture and thus improve their echolocation and reduce their acoustic conspicuousness . Yet, moth hearing is not simple; the ear's nonlinear dynamic response shifts its mechanical sensitivity up to high frequencies. Dependent on incident sound intensity, the moth's ear mechanically tunes up and anticipates the high frequencies used by hunting bats. Surprisingly, this tuning is hysteretic, keeping the ear tuned up for the bat's possible return. A mathematical model is constructed for predicting a linear relationship between the ear's mechanical stiffness and sound intensity. This nonlinear mechanical response is a parametric amplitude dependence that may constitute a feature common to other sensory systems. Adding another twist to the coevolutionary arms race between moths and bats, these results reveal unexpected sophistication in one of the simplest ears known and a novel perspective for interpreting bat echolocation calls.

The relationship between echolocation-call frequency and moth predation of a tropical bat fauna

The allotonic frequency hypothesis proposes that the proportion of eared moths in the diet should be highest in bats whose echolocation calls are dominated by frequencies outside the optimum hearing range of moths i.e., <20 and >60 kHz. The hypothesis was tested on an ecologically diverse bat assemblage in northern tropical Australia that consisted of 23 species (5 families, 14 genera). Peak frequency of signals of bats within the echolocation assemblage ranged from 19.8 to 157 kHz but was greatest between 20 and 50 kHz. A strong positive relationship existed between peak call frequency and percentage of moths in the diet for a sample of 16 bats from the assemblage representing 13 genera (R2 = 0.54, p = 0.001). The relationship remained strong when the three species with low-intensity calls were excluded. When the two species with high duty cycle, constant-frequency signals were removed, the relationship was weaker but still significant. In contrast to previous research, eared moths constituted only 54% of moth captures in light traps at bat foraging grounds, and eared moths were significantly larger than non-eared individuals. These results show that the pattern of moth predation by tropical bats is similar to that already established for bat faunas in subtropical and temperate regions.