Fish Hearing Research Articles

The mechanism for directional hearing in fish

Locating sound sources such as prey or predators is critical for survival in many vertebrates. Terrestrial vertebrates locate sources by measuring the time delay and intensity difference of sound pressure at each ear1–5. Underwater, however, the physics of sound makes interaural cues very small, suggesting that directional hearing in fish should be nearly impossible6. Yet, directional hearing has been confirmed behaviourally, although the mechanisms have remained unknown for decades. Several hypotheses have been proposed to explain this remarkable ability, including the possibility that fish evolved an extreme sensitivity to minute interaural differences or that fish might compare sound pressure with particle motion signals7,8. However, experimental challenges have long hindered a definitive explanation. Here we empirically test these models in the transparent teleost Danionella cerebrum, one of the smallest vertebrates9,10. By selectively controlling pressure and particle motion, we dissect the sensory algorithm underlying directional acoustic startles. We find that both cues are indispensable for this behaviour and that their relative phase controls its direction. Using micro-computed tomography and optical vibrometry, we further show that D. cerebrum has the sensory structures to implement this mechanism. D. cerebrum shares these structures with more than 15% of living vertebrate species, suggesting a widespread mechanism for inferring sound direction.

Effects from particle motion and substrate-borne vibration on fishes and invertebrates: Recommendations on research questions and methodologies

There have been substantially increased interest in effects of particle motion and substrate-borne vibration on fishes and aquatic invertebrates over the past decade. This is because these signals, unlike sound pressure, are the basis of hearing in most fishes and in all aquatic invertebrates. However, studies to address these issues continue to face challenges due to the diversity of species, the broad range of hearing mechanism, and the complexity of the physical acoustic environment in conducting studies. Additionally, we do not yet have a good understanding of, and mechanisms for, source generation, calibration, and measurements to be able to examine effects properly. Related to this is the critical issue is how research questions are applicable to regulatory agencies. In October 2023, the US Bureau of Ocean Energy Management held a workshop to address different research methodologies and their pros and cons as the basis for study of the behavioral and physiological responses to particle motion and substrate-borne vibration. Subsequently, a review was conducted linking research priorities previously identified concerning anthropogenic noise effects on animals with appropriate research methodologies. The review also provides recommendations on experimental settings that are most appropriate to address specific research questions for regulatory concerns.

Fish responses to underwater sounds depend on auditory adaptations: An experimental test of the effect of motorboat sounds on the fish community of a large fluvial lake.

Freshwater fishes exhibit a wide range of auditory adaptations and capabilities, which are assumed to help them navigate their environment, avoid predators, and find potential mates. Yet, we know very little about how freshwater environments sound to fish, or how fish with different auditory adaptations respond to different soundscapes. We first compiled data on fish hearing acuity and adaptations and provided a portrait of how anthropogenic sounds compare to natural sounds in different freshwater soundscapes. We then conducted a sound-enrichment field experiment at Lake Saint Pierre, a large fluvial lake in Canada, to evaluate the effect of motorboat sound exposure on the fish community by looking at the extent to which changes in species abundances were linked to auditory adaptations. Data compilation showed that the hearing acuity of most species overlaps with a wide range of ambient and anthropogenic underwater sounds while the field experiment showed that species with more specialized auditory structures were captured less often in sound-enriched traps, indicating avoidance behavior. Our findings highlight the importance of considering species' sensorial adaptations when evaluating the community-scale effects of anthropogenic sounds on the fish community, especially at low levels of anthropogenic activity.

Diversity of sound production and hearing in fishes: Exploring the riddles of communication and sensory biology

My research in fish bioacoustics started in the mid-1980s and comprised the diversity in sound-generating mechanisms and sound production in various contexts such as dyadic contests. I worked on European freshwater and marine fish, but mainly on tropical fish from Southeast Asia (gouramis) and the Amazonian River system (pimelodid, doradid catfishes, piranhas). The diversity of sonic organs raised the question if general patterns of innervation of sonic muscles in vocal fishes exist. Different vocal (sonic) motor nuclei were identified in the brainstem and rostral spinal cord for pectoral and swim bladder vibration mechanisms. In addition, I wanted to find out if vocal fish differ from nonvocal species in hearing abilities. Measurements applying the auditory evoked potential technique revealed a large diversity of auditory sensitivities depending on the presence or lack of accessory hearing structures independently of sound production. Furthermore, I investigated the anatomy, ultrastructure of inner ears, and hearing enhancement by auxiliary hearing structures. Recently, we studied sound-induced motion of swim bladders, auditory ossicles, and otoliths using x-ray phase contrast imaging. A large part of my studies was carried out in cooperation with laboratories in the USA, Germany, Italy, Portugal, and Brasilia which made my research interesting.

Fish hearing revealed: Do we understand hearing in critical fishes and marine tetrapods.

Hearing evolved in lampreys with a frequency range of 50-200 Hz. This hearing range is comparable to that of elasmobranchs, most non-teleosts, and lungfish. Elasmobranchs most likely use the saccule and the papilla neglecta (PN) for hearing. In non-teleosts and teleosts, lungfish, and certain tetrapods the saccule is the likely sensor for sound reception while the lagena and the PN are important for gravistatic sensing. Coelacanth and most tetrapods have a basilar papilla (BP) for hearing. In coelacanth and tetrapods, the hair cells of the BP are in contact with a basilar and a tectorial membrane. These membranes transmit mechanical vibrations. A cochlear aqueduct (CA) provides a connection between the cerebrospinal fluid that has a sodium rich space in coelacanth and tetrapods while the potassium rich endolymph is known in vertebrates. A unique feature is known in basic sarcopterygians, the intracranial joint, that never developed in actinopterygians and has been lost in lungfish and tetrapods. The BP in coelacanths is thought to generate pressure with the intracranial joint that will be transmitted to the CA. Lungs or a swim bladder are not forming in Chondrichthyes, structures that have a major impact on hearing in teleosts and tetrapods.

Hearing diversity in 34 000 fish species: A personal perspective

I have been studying fish hearing since 1966. Over that time, my interests have evolved from basic mechanisms of hearing to “translational fish bioacoustics” where I help apply basic science to the protection of fishes from potential harm arising from anthropogenic sources. Yet, I am still most interested in basic science questions. Thus, this paper focuses on basic questions on fish hearing and shares my personal view of some of the interesting and important questions I think need to be asked about fish hearing by future investigators. Accordingly, I am not focusing on what has been learned, but, rather, I focus on the questions raised by what we have learned. Moreover, my focus is comparative—there are more than 34 000 extant fish species—and we know little about hearing in any one species. Indeed, most of our knowledge comes from about 100 species! Therefore, considering the immense importance of fishes, it is my contention that we need to know a great deal more about the sense that gives fishes rapid and highly directional information, often at a great distance, about the world around them.

Form function of sulcus acusticus of the sagittal otolith in seven Sciaenidae (Acanthuriformes) species using geometric morphometrics (southwestern Atlantic).

The morphology of otoliths determines the function they perform, and it is influenced by genetic and environmental factors. Knowing those relationships is necessary to understand the role of hearing in fish. The objectives of this work were: exploring the shape of the sulcus of the sagittal otolith in seven species of Sciaenidae, in relation to sound production, and analyzing whether the shape and size of the sulcus can be used as a phylogenetic character. For this purpose, geometric morphometry analysis was carried out using landmarks data. It was found that there is an influence of size on the shape of the sulcus, and significant differences were found between the shapes of the sulcus (permutational multivariate analysis of variance). Three general shapes of the sulcus were identified (using principal component analysis, canonical variate analysis, and clustering): (1) in species that produce sounds at dominant frequencies <350 Hz, the deformation of the sulcus showed a tendency towards circularity of the ostium; (2) in those species that produce sounds at frequencies >350 Hz, the ostium showed a flattened ovoid shape, and the cauda increased its length; (3) the species that do not produce sounds, did not show any modifications, relative to the form of consensus. Despite finding sister species that presented similar sulcus shapes in the phylogeny, the results did not confirm that this can be used as a phylogenetic character. This work discusses whether the combined effects of phylogenetic legacy and natural functional selection have led to convergent evolution for the sulcus form. The differences presented by the sulcus of species that occupy the same clade, could indicate that there is a displacement of characters. The sagittal otolith and the sensory macula associated with the sulcus acusticus are highly plastic structures that are subject to strong evolutionary pressure in relation to environmental and behavioral factors, resulting in great variability in shapes that can be associated with a specific character. The variation in the shape of the sulcus would allow the analysed species to coexist in the same coastal soundscapes, without losing their particular hearing needs, even in case of overlapping their spatial and temporal distribution areas.

The evolution of the various structures required for hearing in Latimeria and tetrapods

Sarcopterygians evolved around 415Ma and have developed a unique set of features, including the basilar papilla and the cochlear aqueduct of the inner ear. We provide an overview that shows the morphological integration of the various parts needed for hearing, e.g., basilar papilla, tectorial membrane, cochlear aqueduct, lungs, and tympanic membranes. The lagena of the inner ear evolved from a common macula of the saccule several times. It is near this lagena where the basilar papilla forms in Latimeria and tetrapods. The basilar papilla is lost in lungfish, certain caecilians and salamanders, but is transformed into the cochlea of mammals. Hearing in bony fish and tetrapods involves particle motion to improve sound pressure reception within the ear but also works without air. Lungs evolved after the chondrichthyans diverged and are present in sarcopterygians and actinopterygians. Lungs open to the outside in tetraposomorph sarcopterygians but are transformed from a lung into a swim bladder in ray-finned fishes. Elasmobranchs, polypterids, and many fossil fishes have open spiracles. In Latimeria, most frogs, and all amniotes, a tympanic membrane covering the spiracle evolved independently. The tympanic membrane is displaced by pressure changes and enabled tetrapods to perceive airborne sound pressure waves. The hyomandibular bone is associated with the spiracle/tympanic membrane in actinopterygians and piscine sarcopterygians. In tetrapods, it transforms into the stapes that connects the oval window of the inner ear with the tympanic membrane and allows hearing at higher frequencies by providing an impedance matching and amplification mechanism. The three characters-basilar papilla, cochlear aqueduct, and tympanic membrane-are fluid related elements in sarcopterygians, which interact with a set of unique features in Latimeria. Finally, we explore the possible interaction between the unique intracranial joint, basicranial muscle, and an enlarged notochord that allows fluid flow to the foramen magnum and the cochlear aqueduct which houses a comparatively small brain.

Fish bioacoustics: Navigating underwater sound.

Fish bioacoustics is about the sounds produced by fish, how fish hear, and what they hear. The focus of this article is on the hypothesis that some late pelagic stage reef fish larvae use the marine soundscape to locate reef settlement habitat. The hypothesis is evaluated by consideration of the nature of reef sound, hearing ability in late-stage larval fish, and direct behavioral evidence for orientation to reef sound.

A journey through the field of fish hearing

My interest in fish bioacoustics was ignited more than 50 years ago and resulted in a zigzag time travel between various interesting problems that were unsettled at the time. The present paper gives a brief overview of the main topics I have worked on in the field of fish hearing, i.e., auditory function of the swim bladder, directional hearing, function of the lateral line system, and infrasound sensitivity. Rather than being a comprehensive review of these issues, the paper is autobiographical and limited. The aim is to show young scientists that experimental science can be exciting, diverse, and rewarding-and open doors to a rich collegial network, collaboration, and friendships.

Ontogenetic changes in sagitta otoliths of whitemouth croaker Micropogonias furnieri (Acanthuriformes: Sciaenidae) and its implication in acoustic communication

Abstract The otoliths of teleosts are part of the inner ear. They are related to the balance system and are also mechanical components of sound transmission, responsible for hearing in fish. Their morphology is determined by the function they perform and is also influenced by environmental factors. In this context, our goal was to: analyse the possible morphological changes of sagitta otoliths of Micropogonias furnieri (Desmarest, 1823) during its ontogeny, based on six biometric indexes. We analysed 162 sagittae otoliths of Micropogonias furnieri collected in the Rio de la Plata estuary. The variation of the indexes was associated with the different size groups. Rectangularity and aspect ratio [otolith length/total fish length (OL/TL) and sulcus area/otolith area (SA/OA)] were the indexes that contributed the most to the discriminant function. Biometric index differences were related to diverse juvenile environments. The observed shift in the SA/OA relationship could be attributable to a need to respond to a change in the perception of sound (pulse and frequency) experienced by individuals larger than 20 cm that begin to frequent the same areas as spawning adults. In this sense, the ontogenetic morphological change of sagitta otoliths plays an important role in perception and acoustic communication for this species.

The career and research contributions of Richard R. Fay.

For over 50 years, Richard R. (Dick) Fay made major contributions to our understanding of vertebrate hearing. Much of Dick's work focused on hearing in fishes and, particularly, goldfish, as well as a few other species, in a substantial body of work on sound localization mechanisms. However, Dick's focus was always on using his studies to try and understand bigger issues of vertebrate hearing and its evolution. This article is slightly adapted from an article that Dick wrote in 2010 on the closure of the Parmly Hearing Institute at Loyola University Chicago. Except for small modifications and minor updates, the words and ideas herein are those of Dick.

Numerical modeling of the impacts of acoustic stimulus on fish otoliths from two directions.

Previous experiments have shown (1) evidence that exposure to high-intensity sounds (e.g., air-gun signals) may cause damage to the sensory hair cells of the fish ears and impair fish hearing and (2) evidence that in some circumstances such exposures cause minimal structural damage. The contradictory results regarding the damage accrued suggested that the angle of sound energy arrivals at the fish ears may play a part in the propensity of the sound to cause damage to sensory hair cells. To further study this and gain insight into specific details of the differential motion of the otolith relative to the sensory macula when incident sounds arrive from different directions, three-dimensional finite element models were constructed based on the micro-computed tomography imaging of the sagittal otoliths of the bight redfish (Centroberyx gerrardi). We used the models to study the response of fish sagittal otoliths to sounds arriving from horizontal and vertical directions. Sound pressure levels, relative displacement, acceleration, and shear stress of the otoliths and/or otolith-water boundary were calculated and compared. The results suggest that the angle of sound energy arrivals at the otoliths and the geometry of the otolith lead to different magnitudes of the differential motion between the macula and otoliths, with sound arriving in the vertical potentially creating more damage than the same sound arriving from the horizontal.

Noise-induced masking of hearing in a labyrinth fish: effects on sound detection in croaking gouramis.

An increasing level of anthropogenic underwater noise (shipping, drilling, sonar use, etc.) impairs acoustic orientation and communication in fish by hindering signal transmission or detection. Different noise regimes can reduce the ability to detect sounds of conspecifics due to an upward shift of the hearing threshold, a phenomenon termed masking. We therefore investigated the masking effect of white noise on the auditory thresholds in female croaking gouramis (Trichopsis vittata, Osphronemidae). We hypothesized that noise would influence the detection of conspecific vocalizations and thus acoustic communication. The auditory evoked potentials (AEP) thresholds were measured at six different frequencies between 0.1 and 4 kHz using the AEP recording technique. Sound pressure level audiograms were determined under quiet laboratory conditions (no noise) and continuous white noise of 110 dB RMS. Thresholds increased in the presence of white noise at all tested frequencies by 12-18 dB, in particular at 1.5 kHz. Moreover, hearing curves were compared to spectra of conspecific sounds to assess sound detection in the presence of noise in various contexts. We showed that masking hinders the detection of conspecific sounds, which have main energies between 1.0 and 1.5 kHz. We predict that this will particularly affect hearing of female's low-intensity purring sounds during mating. Accordingly, noise will negatively affect acoustic communication and most likely reproductive success.

An investigation of bubble resonance and its implications for sound production by deep-water fishes.

Although the continental slope and abyss comprise the largest habitat on earth, the absence of documented fish sounds from deep waters is striking. Fishes with sexually dimorphic muscles attached to their swim bladders suggests that sounds are likely used in male courtship on the upper, mid and lower continental slope. To investigate the effects of environmental extremes on fish sound production, the acoustic behavior of a driven bubble is examined. This study is also relevant to target strength of sonar returns from fish and hearing in auditory specialist fishes. A bubble is a classic, if imperfect, model for swim bladder behavior since the swim-bladder wall is an anisotropic viscoelastic structure responsible for rapid damping. Acoustic properties of bubbles-including far-field resonant frequency, damping factor, and quality factor-are calculated in warm and cold surface conditions and in cold deep-water (depths 1000 m, 2000 m, and 3500 m) conditions using parameters for oxygen and nitrogen, the dominant gases in swim bladders. The far-field resonant frequency and damping factor of a bubble increase with depth, and the scattering cross-section and quality factor decrease with depth. These acoustic properties scale with undamped oscillation frequency of the bubble and do not vary significantly due to gas type or temperature. Bubbles in the deep-water environments are much less efficient radiators of sound than bubbles near the surface because the far-field radiated power for the same excitation decreases with depth. A bubble at depth 3500 m has a 25 dB loss in radiated sound power compared to the same-radius bubble at the surface. This reduction of radiation efficiency in deep water likely contributes to the absence of fish sound recordings in those environments.

Multiscale analysis on otolith structural features reveals differences in ontogenesis and sex in Merluccius merluccius in the western Adriatic Sea.

Otolith biomineralization results from biochemical processes regulated by the interaction of internal (physiological) and external (environmental) factors which lead to morphological and ultrastructural variability at intra- and interspecific levels. The aim of this study was to conduct a multi-scale analysis of the sagittal otoliths of the Merlucius merlucius (European hake) from the western Adriatic Sea in order to correlate otolith features with fish ontogeny and sex. We show that otoliths of sexually undifferentiated (non-sexed) individuals having a fish body total length (TL) less than 15 cm had faster growth in length, width, area, perimeter, volume and weight and a higher amount of organic matrix compared with otoliths of sexually differentiated individuals (females and males) having a fish size range of 15–50 cm. Most importantly, with increasing fish TL, female saccular otoliths contained a higher number of protuberances and rougher surface compared with male specimens, which showed more uniform mean curvature density. The differences between females and males discovered in this study could be associated with fish hearing adaptation to reproductive behavioural strategies during the spawning season. The outcomes of this research provide insights on how size and sex-related variations in otolith features may be affected by fish ecological and behavioural patterns.

Natural cues for invertebrate and fish hearing: Particle motion measurements on coral reefs

Coral reef soundscapes are increasingly studied for their ecological uses by invertebrates and fishes, their applications for monitoring habitat quality, and to investigate effects of anthropogenic noise pollution. Few examinations of aquatic soundscapes have reported particle motion levels and variability, despite their relevance to invertebrates and fishes. We quantified ambient particle acceleration from orthogonal hydrophone arrays over several months at four coral reef sites in the U.S. Virgin Islands, which varied in benthic habitat and fish communities. Temporal trends of particle acceleration were similar to those of sound pressure, and the strength of diel trends in both metrics significantly correlated with percent coral cover. Low frequency (&amp;lt;100 Hz) and high magnitude empirical particle acceleration levels diverged from plane wave approximations. Particle acceleration levels were also determined for boat and example fish sounds. Comparisons with particle acceleration derived audiograms suggest greatest capacity of invertebrates and fishes to detect soundscape components below 100 Hz, and potentially poorer detectability of soundscape cues by some invertebrates compared to fishes. Based on our results, we discuss research questions in soundscape ecology for which reporting of particle motion is essential versus those for which sound pressure may suffice.

Revealing sound-induced motion patterns in fish hearing structures in 4D: a standing wave tube-like setup designed for high-resolution time-resolved tomography

ABSTRACTModern bony fishes possess a high morphological diversity in their auditory structures and auditory capabilities. Yet, how auditory structures such as the otoliths in the inner ears and the swim bladder work together remains elusive. Gathering experimental evidence on the in situ motion of fish auditory structures while avoiding artifacts caused by surgical exposure of the structures has been challenging for decades. Synchrotron radiation-based tomography with high spatio-temporal resolution allows the study of morphofunctional issues non-invasively in an unprecedented way. We therefore aimed to develop an approach that characterizes the moving structures in 4D (=three spatial dimensions+time). We designed a miniature standing wave tube-like setup to meet both the requirements of tomography and those of tank acoustics. With this new setup, we successfully visualized the motion of isolated otoliths and the auditory structures in zebrafish (Danio rerio) and glass catfish (Kryptopterus vitreolus).

Temperature (but not acclimation) affects hearing in fishes adapted to different temperature regimes

Temperature affects various metabolic and physiological processes in ectothermic animals, including auditory systems. The current study investigates the effect of temperature and thermal acclimation time on hearing sensitivities in a eurythermal and a stenothermal fish possessing accessory hearing structures. Using the auditory evoked potential (AEP) recording technique, we determined thresholds from 0.1 to 4 kHz and peak latencies of AEP-waveforms in response to a click stimulus. The goldfish Carassius auratus was chosen as a model for eurythermal and the Amazonian catfish Megalodoras uranoscopus as a model for stenothermal species. Both species were tested at two different temperatures (C. auratus: 15 °C and 25 °C, M. uranoscopus: 22 °C and 30 °C) and acclimation periods, within 22 h (unacclimated) or three to four weeks (acclimated) after reaching the target temperature. A frequency-dependent increase in auditory sensitivity and a decrease of peak latencies was recorded in both species at higher temperatures, independent of acclimation time. The change in hearing thresholds per degree Celsius was more pronounced in the stenothermal catfish. The data indicate that higher temperatures improved hearing (lower thresholds, shorter latencies), whereas acclimation had no effect on hearing in either species. The latter data contradict previous findings in the eurythermal channel catfish Ictalurus punctatus in which acclimation slightly improved hearing when raising the temperatures. A comparison of changes in hearing sensitivity per degree Celsius of all seven species tested so far revealed no differences between eurythermal and stenothermal species.

Fish hearing and how it is best determined

Abstract Hearing, as defined by numerous investigators of vertebrate hearing, involves not only detection of a sound, but the ability to respond to the sound behaviourally. Thus, in order to understand what a fish (or any animal) hears, it is important to use behavioural methods that allow an animal to “tell the investigator” which sounds are detected and which are not. However, since the 1980’s, most studies that suggest they are measuring fish hearing have used electrophysiological approaches to measure the response of the ear or lower levels of the central auditory system to sounds. In this paper, we argue that these electrophysiological measures do not represent hearing since they do not indicate what sounds a fish can potentially respond to behaviourally. Thus, while the electrophysiological measures provide some useful and interesting insights into fish sound detection mechanisms, the most valid measures of hearing sensitivity, and understanding which sounds (anthropogenic or otherwise) that fish are able to respond to, are obtained using behavioural studies. We also argue that these studies must be done in carefully designed acoustic setups so that the nature of the stimulus to which the fish responds is appropriate and well understood.