Aerial Hearing Research Articles

Aerial hearing thresholds and ecoacoustics of a threatened pursuit-diving seabird, the marbled murrelet Brachyramphus marmoratus

As humans increasingly utilize sensitive coastal areas, diving seabirds like the marbled murrelet Brachyramphus marmoratus face a unique combination of exposure to pervasive anthropogenic sound and acoustically mediated disturbances in terrestrial and marine environments. Despite its threatened status, the sound sensitivities and sensory ecology of this species are unknown, limiting any predictions of the frequencies or sound levels that may induce acoustic impacts. In this study, we measured electrophysiological aerial hearing thresholds for 10 wild individuals captured, sedated, examined inside a field-deployed anechoic chamber and subsequently released. Auditory responses were detected across a 0.5 to 6 kHz frequency range. The median auditory threshold was lowest at 2 kHz (33 dB), while hearing was generally sensitive between 0.75 and 3.8 kHz. B. marmoratus thresholds were elevated compared to other studied alcid species. In-air sensitivities were used to provide an initial prediction of underwater hearing thresholds. To further explore the auditory sensory ecology of this solitary-nesting species, hearing data were also compared to short-term recordings (5 d) of the aerial soundscape of a marbled murrelet nesting habitat. The soundscape contained both abiotic and biotic sounds that contributed to broadband sound levels of 46-55 dB re: 20 µPa rms (0.2-10 kHz). This comparatively quiet habitat enabled relatively frequent detection of anthropogenic sounds within the soundscape. Energy from this acoustic pollution consistently overlapped marbled murrelet sound sensitivities, indicating that the species is susceptible to disturbance from a range of noise types.

Sensitive aerial hearing within a noisy nesting soundscape in a deep-diving seabird, the common murre Uria aalge

Diving seabirds face a combination of sound exposure in marine and terrestrial environments due to increasing human encroachment on coastal ecosystems. Yet the sound-sensitivity and sensory ecology of this threatened group of animals is largely unknown, complicating effective management and conservation. Here, we characterize aspects of the acoustic ecology of the common murre Uria aalge, one of the deepest diving alcid seabirds. Electrophysiological aerial hearing thresholds were measured for 12 wild, nesting individuals and compared to conspecific vocalizations and short-term aerial soundscape dynamics of their cliff nesting habitat. Auditory responses were measured from 0.5 to 6 kHz, with a lowest mean threshold of 30 dB at 2 kHz and generally sensitive hearing from 1 to 3.5 kHz. The short-term murre nesting soundscape contained biotic sounds from con- and heterospecific avifauna; broadband sounds levels of 56-69 dB re: 20 µPa rms (0.1-10 kHz) were associated with both diel and tidal-cycle factors. Five murre vocalization types showed dominant spectral emphasis at or below the region of best hearing. Common murre hearing appears to be less sensitive than a related alcid, the Atlantic puffin Fratercula arctica, but more sensitive than other non-alcid diving birds described to date, suggesting that adaptations for deep diving have not caused a loss of the species’ hearing ability above water. Overall, frequencies of common murre hearing and vocalization overlap with many anthropogenic noise sources, indicating that the species is susceptible to disturbance from a range of noise types.

Aquatic birds have middle ears adapted to amphibious lifestyles

Birds exhibit wide variation in their use of aquatic environments, on a spectrum from entirely terrestrial, through amphibious, to highly aquatic. Although there are limited empirical data on hearing sensitivity of birds underwater, mounting evidence indicates that diving birds detect and respond to sound underwater, suggesting that some modifications of the ear may assist foraging or other behaviors below the surface. In air, the tympanic middle ear acts as an impedance matcher that increases sound pressure and decreases sound vibration velocity between the outside air and the inner ear. Underwater, the impedance-matching task is reversed and the ear is exposed to high hydrostatic pressures. Using micro- and nano-CT (computerized tomography) scans of bird ears in 127 species across 26 taxonomic orders, we measured a suite of morphological traits of importance to aerial and aquatic hearing to test predictions relating to impedance-matching in birds with distinct aquatic lifestyles, while accounting for allometry and phylogeny. Birds that engage in underwater pursuit and deep diving showed the greatest differences in ear structure relative to terrestrial species. In these heavily modified ears, the size of the input areas of both the tympanic membrane and the columella footplate of the middle ear were reduced. Underwater pursuit and diving birds also typically had a shorter extrastapedius, a reduced cranial air volume and connectivity and several modifications in line with reversals of low-to-high impedance-matching. The results confirm adaptations of the middle ear to aquatic lifestyles in multiple independent bird lineages, likely facilitating hearing underwater and baroprotection, while potentially constraining the sensitivity of aerial hearing.

Exposição a agrotóxicos e associação com sintomas físicos e auditivos de trabalhadores rurais

hearing. The purpose of the study was to characterize rural workers in terms of sociodemographic aspects andexposure to pesticides, as well as to analyze the relationship between this exposure and the occurrence of physical andauditory symptoms. This was a quantitative study, with a descriptive and explanatory scope, using a cross-sectionaldesign, carried out with 71 rural workers, males, exposed to pesticides. Data collection was performed in two ways:(i) a collection instrument for characterizing contact with pesticides, physical and auditory symptoms (ii) auditoryscreening for the investigation of aerial hearing thresholds. Data analysis was performed through descriptive statisticsand through the Wilcoxon test and Spearman’s correlation. The level of significance was set at 5% for statistical tests.Among the physical symptoms associated with the use of pesticides, headaches prevailed (31.0%). As for the resultof auditory screenings, 31 (43.7%) rural workers failed in both ears, 28 (39.4%) obtained the results of “passing” and12 (16.9%) failed in only one ear. When analyzing the association between the results of auditory screenings andvariables regarding exposure to pesticides, exposure time was the only variable that showed a significant association.The findings clarify that the professional activity of farmers poses a risk to hearing, however, it is necessary to considerthat other factors, such as noise and vibration, can aggravate hearing loss in this population.

A field study of auditory sensitivity of the Atlantic puffin, Fratercula arctica.

Hearing is vital for birds as they rely on acoustic communication with parents, mates, chicks and conspecifics. Amphibious seabirds face many ecological pressures, having to sense cues in air and underwater. Natural noise conditions have helped shape this sensory modality but anthropogenic noise is increasingly impacting seabirds. Surprisingly little is known about their hearing, despite their imperiled status. Understanding sound sensitivity is vital when we seek to manage the impacts of man-made noise. We measured the auditory sensitivity of nine wild Atlantic puffins, Fratercula arctica, in a capture-and-release setting in an effort to define their audiogram and compare these data with the hearing of other birds and natural rookery noise. Auditory sensitivity was tested using auditory evoked potential (AEP) methods. Responses were detected from 0.5 to 6 kHz. Mean thresholds were below 40 dB re.20 µPa from 0.75 to 3 kHz, indicating that these were the most sensitive auditory frequencies, similar to other seabirds. Thresholds in the 'middle' frequency range 1-2.5 kHz were often down to 10-20 dBre.20 µPa. The lowest thresholds were typically at 2.5 kHz. These are the first in-air auditory sensitivity data from multiple wild-caught individuals of a deep-diving alcid seabird. The audiogram was comparable to that of other birds of similar size, thereby indicating that puffins have fully functioning aerial hearing despite the constraints of their deep-diving, amphibious lifestyles. There was some variation in thresholds, yet animals generally had sensitive ears, suggesting aerial hearing is an important sensory modality for this taxon.

Do Body Wall Vibrations Over the Lungs Aid Aerial Hearing in Salamanders? An Investigation into Extratympanic Hearing Mechanisms

Abstract Tympanic middle ears are key innovations in the evolution of terrestrial hearing. These structures facilitate sound transmission between air and the inner ear, across an impedance mismatch boundary. Nontympanic taxa present an opportunity to explore extratympanic hearing mechanisms, which could inform our understanding of terrestrial hearing evolution. Salamanders are useful models in this regard because they lack tympanic middle ears. Lung-based extratympanic auditory mechanisms have been demonstrated in earless anurans and are hypothesized to apply to salamanders, based on observations that the body walls overlying the lungs vibrate in response to airborne sound. We tested the hypothesis that body wall vibrations over the lungs aid aerial hearing in salamanders. We immersed the body walls and pectoral girdle below a water surface in two lunged species, Notophthalmus viridescens and Ambystoma talpoideum, predicting that this would elevate auditory thresholds (measured using evoked potentials) by...

Aerial low-frequency hearing in captive and free-ranging harbour seals (Phoca vitulina) measured using auditory brainstem responses

The hearing sensitivity of 18 free-ranging and 10 captive harbour seals (Phoca vitulina) to aerial sounds was measured in the presence of typical environmental noise through auditory brainstem response measurements. A focus was put on the comparative hearing sensitivity at low frequencies. Low- and mid-frequency thresholds appeared to be elevated in both captive and free-ranging seals, but this is likely due to masking effects and limitations of the methodology used. The data also showed individual variability in hearing sensitivity with probable age-related hearing loss found in two old harbour seals. These results suggest that the acoustic sensitivity of free-ranging animals was not negatively affected by the soundscape they experienced in the wild.

Hearing in the Juvenile Green Sea Turtle (Chelonia mydas): A Comparison of Underwater and Aerial Hearing Using Auditory Evoked Potentials.

Sea turtles spend much of their life in aquatic environments, but critical portions of their life cycle, such as nesting and hatching, occur in terrestrial environments, suggesting that it may be important for them to detect sounds in both air and water. In this study we compared underwater and aerial hearing sensitivities in five juvenile green sea turtles (Chelonia mydas) by measuring auditory evoked potential responses to tone pip stimuli. Green sea turtles detected acoustic stimuli in both media, responding to underwater stimuli between 50 and 1600 Hz and aerial stimuli between 50 and 800 Hz, with maximum sensitivity between 200 and 400 Hz underwater and 300 and 400 Hz in air. When underwater and aerial hearing sensitivities were compared in terms of pressure, green sea turtle aerial sound pressure thresholds were lower than underwater thresholds, however they detected a wider range of frequencies underwater. When thresholds were compared in terms of sound intensity, green sea turtle sound intensity level thresholds were 2–39 dB lower underwater particularly at frequencies below 400 Hz. Acoustic stimuli may provide important environmental cues for sea turtles. Further research is needed to determine how sea turtles behaviorally and physiologically respond to sounds in their environment.

Auditory Discrimination of Natural and High-Pass Filtered Bark Vocalizations in a California Sea Lion (Zalophus californianus).

A California sea lion performed a psychophysical auditory discrimination task with a set of six stimuli: three barks recorded from conspecific males and high-pass filtered versions of the barks that removed the majority of energy at fundamental frequencies. Discrimination performance and subject reaction times (RTs) suggested that the vocalizations were all perceived as fairly dissimilar. This preliminary study hints that low-frequency components are a salient part of the California sea lion bark despite elevation of this species' aerial hearing thresholds and the potential for elevated environmental noise levels at frequencies below 1 kHz.

Amphibious auditory evoked potentials in four North American Testudines genera spanning the aquatic-terrestrial spectrum.

Animals exhibit unique hearing adaptations in relation to the habitat media in which they reside. This study was a comparative analysis of auditory specialization in relation to habitat medium in Testudines, a taxon that includes both highly aquatic and fully terrestrial members. Evoked potential audiograms were collected in four species groups representing diversity along the aquatic-terrestrial spectrum: terrestrial and fossorial Gopherus polyphemus, terrestrial Terrapene carolina carolina, and aquatic Trachemys scripta and Sternotherus (S. odoratus and S. minor). Additionally, underwater sensitivity was tested in T. c. carolina, T. scripta, and Sternotherus with tympana submerged just below the water surface. In aerial audiograms, T. c. carolina were most sensitive, with thresholds 18 dB lower than Sternotherus. At 100-300 Hz, thresholds in T. c. carolina, G. polyphemus, and T. scripta were similar to each other. At 400-800 Hz, G. polyphemus thresholds were elevated to 11 dB above T. c. carolina. The underwater audiograms of T. c. carolina, T. scripta, and Sternotherus were similar. The results suggest aerial hearing adaptations in emydids and high-frequency hearing loss associated with seismic vibration detection in G. polyphemus. The underwater audiogram of T. c. carolina could reflect retention of ancestral aquatic auditory function.

Better than fish on land? Hearing across metamorphosis in salamanders.

Early tetrapods faced an auditory challenge from the impedance mismatch between air and tissue in the transition from aquatic to terrestrial lifestyles during the Early Carboniferous (350 Ma). Consequently, tetrapods may have been deaf to airborne sounds for up to 100 Myr until tympanic middle ears evolved during the Triassic. The middle ear morphology of recent urodeles is similar to that of early 'lepospondyl' microsaur tetrapods, and experimental studies on their hearing capabilities are therefore useful to understand the evolutionary and functional drivers behind the shift from aquatic to aerial hearing in early tetrapods. Here, we combine imaging techniques with neurophysiological measurements to resolve how the change from aquatic larvae to terrestrial adult affects the ear morphology and sensory capabilities of salamanders. We show that air-induced pressure detection enhances underwater hearing sensitivity of salamanders at frequencies above 120 Hz, and that both terrestrial adults and fully aquatic juvenile salamanders can detect airborne sound. Collectively, these findings suggest that early atympanic tetrapods may have been pre-equipped to aerial hearing and are able to hear airborne sound better than fish on land. When selected for, this rudimentary hearing could have led to the evolution of tympanic middle ears.

Hearing of the African lungfish (Protopterus annectens) suggests underwater pressure detection and rudimentary aerial hearing in early tetrapods.

In the transition from an aquatic to a terrestrial lifestyle, vertebrate auditory systems have undergone major changes while adapting to aerial hearing. Lungfish are the closest living relatives of tetrapods and their auditory system may therefore be a suitable model of the auditory systems of early tetrapods such as Acanthostega. Therefore, experimental studies on the hearing capabilities of lungfish may shed light on the possible hearing capabilities of early tetrapods and broaden our understanding of hearing across the water-to-land transition. Here, we tested the hypotheses that (i) lungfish are sensitive to underwater pressure using their lungs as pressure-to-particle motion transducers and (ii) lungfish can detect airborne sound. To do so, we used neurophysiological recordings to estimate the vibration and pressure sensitivity of African lungfish (Protopterus annectens) in both water and air. We show that lungfish detect underwater sound pressure via pressure-to-particle motion transduction by air volumes in their lungs. The morphology of lungfish shows no specialized connection between these air volumes and the inner ears, and so our results imply that air breathing may have enabled rudimentary pressure detection as early as the Devonian era. Additionally, we demonstrate that lungfish in spite of their atympanic middle ear can detect airborne sound through detection of sound-induced head vibrations. This strongly suggests that even vertebrates with no middle ear adaptations for aerial hearing, such as the first tetrapods, had rudimentary aerial hearing that may have led to the evolution of tympanic middle ears in recent tetrapods.

Hearing in the sea otter (Enhydra lutris): auditory profiles for an amphibious marine carnivore.

In this study we examine the auditory capabilities of the sea otter (Enhydra lutris), an amphibious marine mammal that remains virtually unstudied with respect to its sensory biology. We trained an adult male sea otter to perform a psychophysical task in an acoustic chamber and at an underwater apparatus. Aerial and underwater audiograms were constructed from detection thresholds for narrowband signals measured in quiet conditions at frequencies from 0.125-40 kHz. Aerial hearing thresholds were also measured in the presence of octave-band masking noise centered at eight signal frequencies (0.25-22.6 kHz) so that critical ratios could be determined. The aerial audiogram of the sea otter resembled that of sea lions and showed a reduction in low-frequency sensitivity relative to terrestrial mustelids. Best sensitivity was -1 dB re 20 µPa at 8 kHz. Under water, hearing sensitivity was significantly reduced when compared to sea lions and other pinniped species, demonstrating that sea otter hearing is primarily adapted to receive airborne sounds. Critical ratios were more than 10 dB higher than those measured for pinnipeds, suggesting that sea otters are less efficient than other marine carnivores at extracting acoustic signals from background noise, especially at frequencies below 2 kHz.

Selection on aerial hearing in turtles: Auditory evoked potentials in the box turtle, Terrapene carolina relative to the stinkpot, Sternotherus odoratus

Mechanisms of auditory stimulation differ underwater versus in air due to differences in each medium's acoustic impedance, which has resulted in unique hearing adaptations in aquatic relative to terrestrial organisms. Testudines are a useful taxon for studying the evolution of hearing specializations in relation to the air-water interface because this group includes members at various points on the aquatic-terrestrial lifestyle continuum. Here we tested for differences in auditory function between the terrestrial box turtle, Terrapene carolina (Emydidae) and the fully aquatic stinkpot, Sternotherus odoratus (Kinosternidae). Auditory evoked potentials were collected in response to tone pips to generate threshold audiograms in air as well as with tympana submerged underwater. Sensitivities and bandwidths of both species were similar underwater and in air, but the thresholds of box turtles were 9–20 dB more sensitive than stinkpots in air across the entire frequency range. The results indicate selective pressures to enhance aerial hearing in box turtles.

Aerial hearing thresholds and detection of hearing loss in male California sea lions (Zalophus californianus) using auditory evoked potentials

AbstractAuditory evoked potential (AEP) measurements are useful for describing the variability of hearing among individuals in marine mammal populations, an important consideration in terms of basic biology and the design of noise mitigation criteria. In this study, hearing thresholds were measured for 16 male California sea lions at frequencies ranging from 0.5 to 32 kHz using the auditory steady state‐response (ASSR), a frequency‐specific AEP. Audiograms for most sea lions were grossly similar to previously reported psychophysical data in that hearing sensitivity increased with increasing frequency up to a steep reduction in sensitivity between 16 and 32 kHz. Average thresholds were not different from AEP thresholds previously reported for male and female California sea lions. Two sea lions from the current study exhibited abnormal audiograms: a 26‐yr‐old sea lion had impaired hearing with a high‐frequency hearing limit (HFHL) between 8 and 16 kHz, and an 8‐yr‐old sea lion displayed elevated thresholds across most tested frequencies. The auditory brainstem responses (ABRs) for these two individuals and an additional 26‐yr‐old sea lion were aberrant compared to those of other sea lions. Hearing loss may have fitness implications for sea lions that rely on sound during foraging and reproductive activities.

Psychophysical studies of hearing in sea otters (Enhydra lutris)

The sensory biology of sea otters is of special interest, given their amphibious nature and their recent evolutionary transition from land to sea. However, little is known about the acoustic sense of sea otters, including sensitivity to airborne and underwater sound. In this study, we sought to obtain direct measures of auditory function. We trained an adult-male southern sea otter to participate in audiometric testing in an acoustic chamber and an acoustically mapped pool. We used a psychoacoustic method of limits to determine absolute auditory thresholds in air and under water across the hearing range. In addition to obtaining aerial and underwater audiograms, we also evaluated hearing in the presence of noise. The otter’s aerial hearing closely resembled that of a sea lion, and showed reduced sensitivity to high-frequency (>22 kHz) and low-frequency (<2 kHz) sounds relative to terrestrial mustelids. Under water, hearing was less sensitive than sea lions and other pinnipeds, especially at frequencies below 1 kHz. Critical ratios were >10 dB above those measured in pinnipeds, indicating that sea otters are not especially well-adapted for extracting acoustic signals from noise. These data suggest that evolutionary changes in hearing are secondary to other adaptations for semi-aquatic living.

Comparative assessment of amphibious hearing in pinnipeds

Auditory sensitivity in pinnipeds is influenced by the need to balance efficient sound detection in two vastly different physical environments. Previous comparisons between aerial and underwater hearing capabilities have considered media-dependent differences relative to auditory anatomy, acoustic communication, ecology, and amphibious life history. New data for several species, including recently published audiograms and previously unreported measurements obtained in quiet conditions, necessitate a re-evaluation of amphibious hearing in pinnipeds. Several findings related to underwater hearing are consistent with earlier assessments, including an expanded frequency range of best hearing in true seals that spans at least six octaves. The most notable new results indicate markedly better aerial sensitivity in two seals (Phoca vitulina and Mirounga angustirostris) and one sea lion (Zalophus californianus), likely attributable to improved ambient noise control in test enclosures. An updated comparative analysis alters conventional views and demonstrates that these amphibious pinnipeds have not necessarily sacrificed aerial hearing capabilities in favor of enhanced underwater sound reception. Despite possessing underwater hearing that is nearly as sensitive as fully aquatic cetaceans and sirenians, many seals and sea lions have retained acute aerial hearing capabilities rivaling those of terrestrial carnivores.

Preliminary investigation of sound reception in southern sea otters (Enhydra lutris nereis).

Due to their dependence upon a highly restricted coastal habitat, sea otters are vulnerable to a variety of environmental and anthropogenic threats. Among these is the potential disturbance from human‐generated sources of noise. Presently, there are no data on the auditory sensitivity of sea otters, and little evidence to suggest what sounds may be most relevant to these animals. As an initial step toward describing the acoustic sense of sea otters, we conducted a controlled exposure experiment, adapted from sound exposure studies used in behavioral field research, to efficiently measure the aerial frequency range of hearing in four captive sea otters. This approach was designed to determine which frequencies were audible to each animal, rather than to provide direct measures of auditory sensitivity. The maximum range of aerial hearing determined using this method was 0.125 to 32 kHz. These are the first direct measurements of hearing obtained for sea otters, and the results are relevant to improving understanding of their acoustic communication, evolutionary biology, and behavioral ecology, as well as in supporting ongoing conservation efforts. This research effort draws from the work of Kastak and Schusterman, especially with respect to the value of behavioral baselines in captive studies of marine mammals.

California sea lion (Zalophus californianus) aerial hearing sensitivity measured using auditory steady-state response and psychophysical methods

Although electrophysiological methods of measuring the hearing sensitivity of pinnipeds are not yet as refined as those for dolphins and porpoises, they appear to be a promising supplement to traditional psychophysical procedures. In order to further standardize electrophysiological methods with pinnipeds, a within-subject comparison of psychophysical and auditory steady-state response (ASSR) measures of aerial hearing sensitivity was conducted with a 1.5-yr-old California sea lion. The psychophysical audiogram was similar to those previously reported for otariids, with a U-shape, and thresholds near 10 dB re 20 μPa at 8 and 16 kHz. ASSR thresholds measured using both single and multiple simultaneous amplitude-modulated tones closely reproduced the psychophysical audiogram, although the mean ASSR thresholds were elevated relative to psychophysical thresholds. Differences between psychophysical and ASSR thresholds were greatest at the low- and high-frequency ends of the audiogram. Thresholds measured using the multiple ASSR method were not different from those measured using the single ASSR method. The multiple ASSR method was more rapid than the single ASSR method, and allowed for threshold measurements at seven frequencies in less than 20 min. The multiple ASSR method may be especially advantageous for hearing sensitivity measurements with otariid subjects that are untrained for psychophysical procedures.

New approaches for studying the perception of vocal signals in otariid pinnipeds.

The pioneering work of Ronald Schusterman and David Kastak considered the acoustic signaling of pinnipeds from the perspectives of both sender and receiver. Their work often highlighted the otariid pinnipeds (sea lions and fur seals), which are known for their frequent, loud aerial vocalizations. Numerous aerial vocalizations have been described for otariids, and research has demonstrated that a number of call characteristics are sufficient for individual and species recognition. In contrast to the marked interspecific variability found in these vocalizations, laboratory studies with pure-tone stimuli suggest that the aerial hearing capabilities of otariids are nearly identical among species. This is a surprising result, as many components in the calls of otariids exist at frequencies well below the range of best hearing sensitivity. Future studies can potentially examine the relevance of frequency composition and other vocalization parameters using psychophysical methods that include complex acoustic stimuli and an analysis of subject response latencies. Such methods have proven useful for studying the manner in which birds perceptually categorize vocalizations [Dooling et al., J. Comp. Psychol. 101, 367–381 (1987)] and they may provide novel tools for investigating the link between vocalization structure and auditory perception in otariids. [Work supported by ONR.]