Auditory evoked potential audiometry in fish

© The Author(s), 2013. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Reviews in Fish Biology and Fisheries 23 (2013): 317-364, doi:10.1007/s11160-012-9297-z.A recent survey lists more than 100 papers utilizing the auditory evoked potential (AEP) recording technique for studying hearing in fishes. More than 95 % of these AEP-studies were published after Kenyon et al. introduced a non-invasive electrophysiological approach in 1998 allowing rapid evaluation of hearing and repeated testing of animals. First, our review compares AEP hearing thresholds to behaviorally gained thresholds. Second, baseline hearing abilities are described and compared in 111 fish species out of 51 families. Following this, studies investigating the functional significance of various accessory hearing structures (Weberian ossicles, swim bladder, otic bladders) by eliminating these morphological structures in various ways are dealt with. Furthermore, studies on the ontogenetic development of hearing are summarized. The AEP-technique was frequently used to study the effects of high sound/noise levels on hearing in particular by measuring the temporary threshold shifts after exposure to various noise types (white noise, pure tones and anthropogenic noises). In addition, the hearing thresholds were determined in the presence of noise (white, ambient, ship noise) in several studies, a phenomenon termed masking. Various ecological (e.g., temperature, cave dwelling), genetic (e.g., albinism), methodical (e.g., ototoxic drugs, threshold criteria, speaker choice) and behavioral (e.g., dominance, reproductive status) factors potentially influencing hearing were investigated. Finally, the technique was successfully utilized to study acoustic communication by comparing hearing curves with sound spectra either under quiet conditions or in the presence of noise, by analyzing the temporal resolution ability of the auditory system and the detection of temporal, spectral and amplitude characteristics of conspecific vocalizations.Support from the Austrian Science Fund (FWF grant 22319 to F.L.)

Effects of Temperature on Sound Production and Auditory Abilities in the Striped Raphael Catfish Platydoras armatulus (Family Doradidae)

Background: Sound production and hearing sensitivity of ectothermic animals are affected by the ambient temperature. This is the first study investigating the influence of temperature on both sound production and on hearing abilities in a fish species, namely the neotropical Striped Raphael catfish Platydoras armatulus. Methodology/Principal Findings: Doradid catfishes produce stridulation sounds by rubbing the pectoral spines in the shoulder girdle and drumming sounds by an elastic spring mechanism which vibrates the swimbladder. Eight fish were acclimated for at least three weeks to 22 degrees, then to 30 degrees and again to 22 degrees C. Sounds were recorded in distress situations when fish were hand-held. The stridulation sounds became shorter at the higher temperature, whereas pulse number, maximum pulse period and sound pressure level did not change with temperature. The dominant frequency increased when the temperature was raised to 30 degrees C and the minimum pulse period became longer when the temperature decreased again. The fundamental frequency of drumming sounds increased at the higher temperature. Using the auditory evoked potential (AEP) recording technique, the hearing thresholds were tested at six different frequencies from 0.1 to 4 kHz. The temporal resolution was determined by analyzing the minimum resolvable click period (0.3-5 ms). The hearing sensitivity was higher at the higher temperature and differences were more pronounced at higher frequencies. In general, latencies of AEPs in response to single clicks became shorter at the higher temperature, whereas temporal resolution in response to double-clicks did not change

Development of vocalization, auditory sensitivity and acoustic communication in the Lusitanian toadfish Halobatrachus didactylus

The ontogenetic development of acoustic communication has so far only been investigated in one fish species. In order to determine whether detectability of conspecific sounds changes during growth in a species with limited hearing abilities (generalist), we investigated the development of auditory sensitivity and agonistic vocalizations in the Lusitanian toadfish Halobatrachus didactylus. Agonistic grunts were recorded, their sound pressure levels determined, and auditory sensitivities measured in five different size groups ranging from 3 to 32·cm standard length. Hearing thresholds were obtained using the auditory evoked potentials (AEP) recording technique. Dominant frequency, sound duration and number of pulses decreased, whereas pulse period and sound level increased with increasing fish size. The best hearing was below 300·Hz in all groups. Lower hearing sensitivity was found in the smallest juveniles at 100·Hz as well as at higher frequencies (800 and 1000·Hz). Comparisons between audiograms and sound spectra within the same-sized fish revealed that smaller juveniles would be barely able to detect agonistic grunts, while these vocalizations were clearly perceived by larger fish. In the latter, the main energy of sounds was found at the most sensitive frequencies. This study demonstrates that acoustic communication in the Lusitanian toadfish might be absent in early developmental stages and seems to start when juveniles are able to generate grunts of higher sound level and lower dominant frequency

A unique swim bladder-inner ear connection in a teleost fish revealed by a combined high-resolution microtomographic and three-dimensional histological study

Background: In most modern bony fishes (teleosts) hearing improvement is often correlated with a close morphological relationship between the swim bladder or other gas-filled cavities and the saccule or more rarely with the utricle. A connection of an accessory hearing structure to the third end organ, the lagena, has not yet been reported. A recent study in the Asian cichlid Etroplus maculatus provided the first evidence that a swim bladder may come close to the lagena. Our study was designed to uncover the swim bladder-inner ear relationship in this species. We used a new approach by applying a combination of two high-resolution techniques, namely microtomographic (microCT) imaging and histological serial semithin sectioning, providing the basis for subsequent three-dimensional reconstructions. Prior to the morphological study, we additionally measured auditory evoked potentials at four frequencies (0.5, 1, 2, 3 kHz) to test the hearing abilities of the fish. Results: E. maculatus revealed a complex swim bladder-inner ear connection in which a bipartite swim bladder extension contacts the upper as well as the lower parts of each inner ear, a condition not observed in any other teleost species studied so far. The gas-filled part of the extension is connected to the lagena via a thin bony lamella and is firmly attached to this bony lamella with connective material. The second part of the extension, a pad-like structure, approaches the posterior and horizontal semicircular canals and a recessus located posterior to the utricle. Conclusions: Our study is the first detailed report of a link between the swim bladder and the lagena in a teleost species. We suggest that the lagena has an auditory function in this species because the most intimate contact exists between the swim bladder and this end organ. The specialized attachment of the saccule to the cranial bone and the close proximity of the swim bladder extension to the recessus located posterior to the utricle indicate that the saccule and the utricle also receive parallel inputs from the swim bladder extension. We further showed that a combination of non-destructive microCT imaging with histological analyses on the same specimen provides a powerful tool to decipher and interpret fine structures and to compensate for methodological artifacts

Effects of ship noise on the detectability of communication signals in the Lusitanian toadfish

Underwater noise pollution is an increasing environmental problem which might affect communication, behaviour, fitness and consequently species’ survival. The most common anthropogenic noises in aquatic habitats derive from shipping. In the present study we investigated the implications of noise pollution from a ship on the sound detectability, namely of conspecific vocalizations in the Lusitanian toadfish, Halobatrachus didactylus. Ambient and ferry-boat noises were recorded in the Tagus River estuary (Portugal), as well as toadfish sounds, and their sound pressure levels determined. Hearing sensitivities were measured under quiet lab conditions and in the presence of these masking noises at levels encountered in the field, using the auditory evoked potentials (AEP) recording technique. The Lusitanian toadfish is a hearing generalist, with best hearing sensitivity at low frequencies between 50 and 200·Hz (below 100·dB re. 1· Pa). Under ambient noise conditions, hearing was only slightly masked at lower frequencies. In the presence of ship noise, auditory thresholds increased considerably, by up to 36·dB, at most frequencies tested. This is mainly because the main energies of ferry-boat noise were within the most sensitive hearing range of this species. Comparisons between masked audiograms and sound spectra of the toadfish’s mating and agonistic vocalizations revealed that ship noise decreased the ability to detect conspecific acoustic signals. This study provides the first evidence that fishes’ auditory sensitivity can be impaired by ship noise and that acoustic communication, which is essential during agonistic encounters and mate attraction, might be restricted in coastal environments altered by human activity

Auditory chain reaction: Effects of sound pressure and particle motion on auditory structures in fishes

Despite the diversity in fish auditory structures, it remains elusive how otolith morphology and swim bladder-inner ear (= otophysic) connections affect otolith motion and inner ear stimulation. A recent study visualized sound-induced otolith motion;but tank acoustics revealed a complex mixture of sound pressure and particle motion. To separate sound pressure and sound-induced particle motion, we constructed a transparent standing wave tubelike tank equipped with an inertial shaker at each end while using X-ray phase contrast imaging. Driving the shakers in phase resulted in maximised sound pressure at the tank centre, whereas particle motion was maximised when shakers were driven out of phase (180 degrees). We studied the effects of two types of otophysic connections-i.e. the Weberian apparatus (Carassius auratus) and anterior swim bladder extensions contacting the inner ears (Etroplus canarensis)-on otolith motion when fish were subjected to a 200 Hz stimulus. Saccular otolith motion was more pronounced when the swim bladder walls oscillated under the maximised sound pressure condition. The otolith motion patterns mainly matched the orientation patterns of ciliary bundles on the sensory epithelia. Our setup enabled the characterization of the interplay between the auditory structures and provided first experimental evidence of how different types of otophysic connections affect otolith motion

Ontogenetic Development of Weberian Ossicles and Hearing Abilities in the African Bullhead Catfish

BACKGROUND: The weberian apparatus of otophysine fishes facilitates sound transmission from the swimbladder to the inner ear to increase hearing sensitivity. It has been of great interest to biologists since the 19(th) century. No studies, however, are available on the development of the weberian ossicles and its effect on the development of hearing in catfishes. METHODOLOGY/PRINCIPAL FINDINGS: We investigated the development of the weberian apparatus and auditory sensitivity in the catfish Lophiobagrus cyclurus. Specimens from 11.3 mm to 85.5 mm in standard length were studied. Morphology was assessed using sectioning, histology, and X-ray computed tomography, along with 3D reconstruction. Hearing thresholds were measured utilizing the auditory evoked potentials recording technique. Weberian ossicles and interossicular ligaments were fully developed in all stages investigated except in the smallest size group. In the smallest catfish, the intercalarium and the interossicular ligaments were still missing and the tripus was not yet fully developed. Smallest juveniles revealed lowest auditory sensitivity and were unable to detect frequencies higher than 2 or 3 kHz; sensitivity increased in larger specimens by up to 40 dB, and frequency detection up to 6 kHz. In the size groups capable of perceiving frequencies up to 6 kHz, larger individuals had better hearing abilities at low frequencies (0.05-2 kHz), whereas smaller individuals showed better hearing at the highest frequencies (4-6 kHz). CONCLUSIONS/SIGNIFICANCE: Our data indicate that the ability of otophysine fish to detect sounds at low levels and high frequencies largely depends on the development of the weberian apparatus. A significant increase in auditory sensitivity was observed as soon as all weberian ossicles and interossicular ligaments are present and the chain for transmitting sounds from the swimbladder to the inner ear is complete. This contrasts with findings in another otophysine, the zebrafish, where no threshold changes have been observed