DPOAEs and tympanal membrane vibrations reveal adaptations of the sexually dimorphic ear of the concave-eared torrent frog, Odorrana tormota.

While most anuran species are highly vocal, few of them seem to be endowed with a complex call repertoire. Odorrana tormota, combines a remarkable vocalization complexity with auditory sensitivity over an extended spectral range spanning from audible to ultrasonic frequencies. This species is also exceptional for its ability to modify its middle ear tuning by closing the Eustachian tubes (ET). Using scanning laser Doppler vibrometry, the tympanal vibrations were measured to investigate if the tuning shift caused by the ET closure contributes to intraspecific acoustic communication. To gain insight into the inner ear frequency selectivity and sensitivity of this species, distortion product otoacoustic emissions were recorded at multiple frequency-level combinations. Our measurements of inner ear responses indicated that in O. tormota each sex is more sensitive to the frequencies of the other sex's vocalizations, female ears are more sensitive to 2-7 kHz, while male ears are more sensitive to 3-15 kHz. We also found that in both sexes the ET closure impacts the sensitivity of the middle and inner ear at frequencies used for communication with conspecifics. This study broadens our understanding of peripheral auditory mechanisms contributing to intraspecific acoustic communication in anurans.

Beyond the limits: identifying the high-frequency detectors in the anuran ear.

Despite the predominance of low-frequency hearing in anuran amphibians, a few frog species have evolved high-frequency communication within certain environmental contexts. Huia cavitympanum is the most remarkable anuran with regard to upper frequency limits; it is the first frog species known to emit exclusively ultrasonic signals. Characteristics of the Distortion Product Otoacoustic Emissions from the amphibian papilla and the basilar papilla were analysed to gain insight into the structures responsible for high-frequency/ultrasound sensitivity. Our results confirm the matching of vocalization spectra and inner ear tuning in this species. Compared to most anurans, H. cavitympanum has a hyperextended hearing range spanning from audible to ultrasonic frequencies, far above the previously established 'spectral limits' for the amphibian ear. The exceptional high-frequency sensitivity in the inner ear of H. cavitympanum illustrates the remarkable plasticity of the auditory system and the extent to which evolution can modify a sensory system to adapt it to its environment.

Reciprocal Matched Filtering in the Inner Ear of the African Clawed Frog (Xenopus laevis).

Anurans (frogs and toads) are the most vocal amphibians. In most species, only males produce advertisement calls for defending territories and attracting mates. Female vocalizations are the exceptions among frogs, however in the African clawed frog (Xenopus laevis) both males and females produce distinct vocalizations. The matched filter hypothesis predicts a correspondence between peripheral auditory tuning of receivers and properties of species-specific acoustic signals, but few studies have assessed this relationship between the sexes. Measuring hearing sensitivity with a binaural recording of distortion product otoacoustic emissions, we have found that the ears of the males of this species are tuned to the dominant frequency of the female's calls, whereas the ears of the females are tuned close to the dominant frequency of the male's calls. Our findings provide support for the matched filter hypothesis extended to include male-female calling. This unique example of reciprocal matched filtering ensures that males and females communicate effectively in high levels of background noise, each sex being most sensitive to the frequencies of the other sex's calls.

MEMRI for visualizing brain activity after auditory stimulation in frogs.

Anuran amphibians are common model organisms in bioacoustics and neurobiology. To date, however, most available methods for studying auditory processing in frogs are highly invasive and thus do not allow for longitudinal study designs, nor do they provide a global view of the brain, which substantially limits the questions that can be addressed. The goal of this study was to identify areas in the frog brain that are responsible for auditory processing using in vivo manganese-enhanced MRI (MEMRI). We were interested in determining if the neural processing of socially relevant acoustic stimuli (e.g., species-specific calls) engages a specific pattern of brain activation that differs from patterns elicited by less- or nonrelevant acoustic signals. We thus designed an experiment, in which we presented three different types of acoustic stimuli (species-specific calls, band-limited noise, or silence) to fully awake northern leopard frogs (Rana pipiens) and then conducted MEMRI T1-weighted imaging to investigate differences in signal intensity due to manganese uptake as an indication of brain activity across all three conditions. We found the greatest change in signal intensity within the torus semicircularis (the principal central auditory region), the habenula, and the paraphysis of frogs that had been exposed to conspecific calls compared with noise or silence conditions. Stimulation with noise did not result in the same activation patterns, indicating that signals with contrasting social relevance are differentially processed in these areas of the amphibian brain. MEMRI provides a powerful approach to studying brain activity with high spatial resolution in frogs. (PsycINFO Database Record (c) 2019 APA, all rights reserved).

Plant-borne vibrations modulate calling behaviour in a tropical amphibian.

Terrestrial frogs and toads produce conspicuous vocalizations that may be accompanied by substrate-borne vibrations [1]. Unlike airborne sound, these substrate-borne components are relatively understudied in animal communication. Some anurans exploit the forest floor as a relatively noiseless communication channel in which to propagate call-derived vibrations [2]. Insects on vegetation often use leaves and stems as substrates through which they transmit and receive seismic signals [3]. Here we report that golden rocket frogs calling from their natural substrate generate plant-borne vibrations, and we show that these vibrations can change the frog's behavior. This suggests that plant-borne vibrations can play a role in both modifying the call structure of a vertebrate and directing its movements on the substrate.

Hearing diversity in moths confronting a neotropical bat assemblage.

The tympanal ear is an evolutionary acquisition which helps moths survive predation from bats. The greater diversity of bats and echolocation strategies in the Neotropics compared with temperate zones would be expected to impose different sensory requirements on the neotropical moths. However, even given some variability among moth assemblages, the frequencies of best hearing of moths from different climate zones studied to date have been roughly the same: between 20 and 60 kHz. We have analyzed the auditory characteristics of tympanate moths from Cuba, a neotropical island with high levels of bat diversity and a high incidence of echolocation frequencies above those commonly at the upper limit of moths' hearing sensitivity. Moths of the superfamilies Noctuoidea, Geometroidea and Pyraloidea were examined. Audiograms were determined by non-invasively measuring distortion-product otoacoustic emissions. We also quantified the frequency spectrum of the echolocation sounds to which this moth community is exposed. The hearing ranges of moths in our study showed best frequencies between 36 and 94 kHz. High sensitivity to frequencies above 50 kHz suggests that the auditory sensitivity of moths is suited to the sounds used by sympatric echolocating bat fauna. Biodiversity characterizes predators and prey in the Neotropics, but the bat-moth acoustic interaction keeps spectrally matched.

Unexpected dynamic up-tuning of auditory organs in day-flying moths.

In certain nocturnal moth species the frequency range of best hearing shifts to higher frequencies during repeated sound stimulation. This could provide the moths with a mechanism to better detect approaching echolocating bats. However, such a dynamic up-tuning would be of little value for day-flying moths that use intra-specific acoustic communication. Here we examined if the ears of day-flying moths provide stable tuning during longer sound stimulation. Contrary to our expectations, dynamic up-tuning was found in the ear of the day-flying species Urania boisduvalii and Empyreuma pugione. Audiograms were measured with distortion-product otoacoustic emissions (DPOAEs). The level of the dominant distortion product (i.e. 2f1-f2) varied as a function of time by as much as 45 dB during ongoing acoustic stimulation, showing a systematic decrease at low frequencies and an increase at high frequencies. As a consequence, within about 2 s of acoustic stimulation, the DPOAEs audiogram shifted from low to high frequencies. Despite the up-tuning, the range of best audition still fell within the frequency band of the species-specific communication signals, suggesting that intra-specific communication should not be affected adversely. Up-tuning could be an ancestral condition in moth ears that in day-flying moths does not underlie larger selection pressure.

The frog inner ear: picture perfect?

Many recent accounts of the frog peripheral auditory system have reproduced Wever's (1973) schematic cross-section of the ear of a leopard frog. We sought to investigate to what extent this diagram is an accurate and representative depiction of the anuran inner ear, using three-dimensional reconstructions made from serial sections of Rana pipiens, Eleutherodactylus limbatus and Xenopus laevis. In Rana, three discrete contact membranes were found to separate the posterior otic (=endolymphatic) labyrinth from the periotic (=perilymphatic) system: those of the amphibian and basilar recesses and the contact membrane of the saccule. The amphibian 'tegmentum vasculosum' was distinguishable as a thickened epithelial lining within a posterior recess of the superior saccular chamber. These features were also identified in Eleutherodactylus, but in this tiny frog the relative proportions of the semicircular canals and saccule resemble those of ranid tadpoles. There appeared to be a complete fluid pathway between the right and left periotic labyrinths in this species, crossing the cranial cavity. Xenopus lacks a tegmentum vasculosum and a contact membrane of the saccule; the Xenopus ear is further distinguished by a lateral passage separating stapes from periotic cistern and a more direct connection between periotic cistern and basilar recess. The basilar and lagenar recesses are conjoined in this species. Wever's diagram of the inner ear of Rana retains its value for diagrammatic purposes, but it is not anatomically accurate or representative of all frogs. Although Wever identified the contact membrane of the saccule, most recent studies of frog inner ear anatomy have overlooked both this and the amphibian tegmentum vasculosum. These structures deserve further attention.

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.