Functional plasticity of the swim bladder as an acoustic organ for communication in a vocal fish.

Teleost fishes have evolved a number of sound-producing mechanisms, including vibrations of the swim bladder. In addition to sound production, the swim bladder also aids in sound reception. While the production and reception of sound by the swim bladder has been described separately in fishes, the extent to which it operates for both in a single species is unknown. Here, using morphological, electrophysiological and modelling approaches, we show that the swim bladder of male plainfin midshipman fish (Porichthys notatus) exhibits reproductive state-dependent changes in morphology and function for sound production and reception. Non-reproductive males possess rostral 'horn-like' swim bladder extensions that enhance low-frequency (less than 800 Hz) sound pressure sensitivity by decreasing the distance between the swim bladder and inner ear, thus enabling pressure-induced swim bladder vibrations to be transduced to the inner ear. By contrast, reproductive males display enlarged swim bladder sonic muscles that enable the production of advertisement calls but also alter swim bladder morphology and increase the swim bladder to inner ear distance, effectively reducing sound pressure sensitivity. Taken together, we show that the swim bladder exhibits a seasonal functional plasticity that allows it to effectively mediate both the production and reception of sound in a vocal teleost fish.

Response of toadfish (Opsanus tau) utricular afferents to multimodal inputs.

The inner ear of teleost fishes is composed of three paired multimodal otolithic end organs (saccule, utricle, and lagena), which encode auditory and vestibular inputs via the deflection of hair cells contained within the sensory epithelia of each organ. However, it remains unclear how the multimodal otolithic end organs of the teleost inner ear simultaneously integrate vestibular and auditory inputs. Therefore, microwire electrodes were chronically implanted using a 3-D printed micromanipulator into the utricular nerve of oyster toadfish (Opsanus tau) to determine how utricular afferents respond to conspecific mate vocalizations termed boatwhistles (180 Hz fundamental frequency) during movement. Utricular afferents were recorded while fish were passively moved using a sled system along an underwater track at variable speeds (velocity: 4.0-12.5 cm/s; acceleration: 0.2-2.6 cm/s2) and while fish freely swam (velocity: 3.5-18.6 cm/s; acceleration: 0.8-29.8 cm/s2). Afferent fiber activities (spikes/s) increased in response to the onset of passive and active movements; however, afferent fibers differentially adapted to sustained movements. In addition, utricular afferent fibers remained sensitive to playbacks of conspecific male boatwhistle vocalizations during both passive and active movements. Here, we demonstrate in alert toadfish that utricular afferents exhibit enhanced activity levels (spikes/s) in response to behaviorally relevant acoustic stimuli during swimming.NEW & NOTEWORTHY The inner ear of teleost fishes is composed of three paired multimodal otolithic end organs, which are sensitive to vestibular and auditory inputs. Previous studies investigating inner ear functions have primarily focused on the effects of unimodal stimuli; therefore, it remains unclear how otolithic end organs simultaneously encode multiple stimuli. Here, we show that utricular afferents remain sensitive to behaviorally relevant acoustic stimuli during swimming.

Auditory evoked potentials of utricular hair cells in the plainfin midshipman, Porichthys notatus.

The plainfin midshipman, Porichthys notatus, is a soniferous marine teleost fish that generates acoustic signals for intraspecific social communication. Nocturnally active males and females rely on their auditory sense to detect and locate vocally active conspecifics during social behaviors. Previous work showed that the midshipman inner ear saccule and lagena are highly adapted to detect and encode socially relevant acoustic stimuli, but the auditory sensitivity and function of the midshipman utricle remain largely unknown. Here, we characterized the auditory evoked potentials from hair cells in the utricle of non-reproductive type I males and tested the hypothesis that the midshipman utricle is sensitive to behaviorally relevant acoustic stimuli. Hair cell potentials were recorded from the rostral, medial and caudal regions of the utricle in response to pure tone stimuli presented by an underwater speaker. We show that the utricle is highly sensitive to particle motion stimuli produced by an underwater speaker positioned in the horizontal plane. Utricular potentials were recorded across a broad range of frequencies with lowest particle acceleration (dB re. 1 m s-2) thresholds occurring at 105 Hz (lowest frequency tested; mean threshold -32 dB re. 1 m s-2) and highest thresholds at 605-1005 Hz (mean threshold range -5 to -4 dB re. 1 m s-2). The high gain and broadband frequency sensitivity of the utricle suggest that it likely serves a primary auditory function and is well suited to detect conspecific vocalizations including broadband agonistic signals and the multiharmonic advertisement calls produced by reproductive type I males.

Ontogenetic variation in the auditory sensitivity of black sea bass (Centropristis striata) and the implications of anthropogenic sound on behavior and communication.

Black sea bass (Centropristis striata) is an important fish species in both commercial and recreational fisheries of southern New England and the mid-Atlantic Bight. Due to the intense urbanization of these waters, this species is subject to a wide range of anthropogenic noise pollution. Concerns that C. striata are negatively affected by pile driving and construction noise predominate in areas earmarked for energy development. However, as yet, the hearing range of C. striata is unknown, making it hard to evaluate potential risks. This study is a first step in understanding the effects of anthropogenic noise on C. striata by determining the auditory detection bandwidth and thresholds of this species using auditory evoked potentials, creating pressure and acceleration audiograms. These physiological tests were conducted on wild-caught C. striata in three size/age categories. Results showed that juvenile C. striata had the significantly lowest thresholds, with auditory sensitivity decreasing in the larger size classes. Furthermore, C.striata has fairly sensitive sound detection relative to other related species. Preliminary investigations into the mechanisms of their sound detection ability were undertaken with gross dissections and an opportunistic micro-computed tomography image to address the auditory structures including otoliths and swim bladder morphology. Crucially, the auditory detection bandwidth of C. striata, and their most sensitive frequencies, directly overlap with high-amplitude anthropogenic noise pollution such as shipping and underwater construction.

Auditory evoked potentials of the plainfin midshipman fish (Porichthys notatus): implications for directional hearing.

The plainfin midshipman (Porichthys notatus) is an acoustically communicative teleost fish. Here, we evaluated auditory evoked potentials (AEPs) in reproductive female midshipman exposed to tones at or near dominant frequencies of the male midshipman advertisement call. An initial series of experiments characterized AEPs at behaviorally relevant suprathreshold sound levels (130-140 dB SPL re. 1 µPa). AEPs decreased in magnitude with increasing stimulus frequency and featured a stereotyped component at twice the stimulus frequency. Recording electrode position was varied systematically and found to affect AEP magnitude and phase characteristics. Later experiments employed stimuli of a single frequency to evaluate contributions of the saccule to the AEP, with particular attention to the effects of sound source azimuth on AEP amplitude. Unilateral excision of saccular otoliths (sagittae) decreased AEP amplitude; unexpectedly, decreases differed for right versus left otolith excision. A final set of experiments manipulated the sound pressure-responsive swim bladder. Swim bladder excision further reduced the magnitude of AEP responses, effectively eliminating responses at the standard test intensity (130 dB SPL) in some animals. Higher-intensity stimulation yielded response minima at forward azimuths ipsilateral to the excised sagitta, but average cross-azimuth modulation generally remained slight. Collectively, the data underscore that electrode position is an essential variable to control in fish AEP studies and suggest that in female midshipman: (1) the saccule contributes to the AEP, but its directionality as indexed by the AEP is limited, (2) a left-right auditory asymmetry may exist and (3) the swim bladder provides gain in auditory sensitivity that may be important for advertisement call detection and phonotaxis.

Ecology of fish hearing.

Underwater sound is directional and can convey important information about the surrounding environment or the animal emitting the sound. Therefore, sound is a major sensory channel for fishes and plays a key role in many life-history strategies. The effect of anthropogenic noise on aquatic life, which may be causing homogenisation or fragmentation of biologically important signals underwater is of growing concern. In this review we discuss the role sound plays in the ecology of fishes, basic anatomical and physiological adaptations for sound reception and production, the effects of anthropogenic noise and how fishes may be coping to changes in their environment, to put the ecology of fish hearing into the context of the modern underwater soundscape.

The effects of stimulus parameters on auditory evoked potentials of Carassius auratus.

Whole-brain responses to sound are easily measured through auditory evoked potentials (AEP), but it is unclear how differences in experimental parameters affect these responses. The effect of varying parameters is especially unclear in fish studies, the majority of which use simple sound types and then extrapolate to natural conditions. The current study investigated AEPs in goldfish (Carassius auratus) using sounds of different durations (5, 10, and 20 ms) and frequencies (200, 500, 600 and 700 Hz) to test stimulus effects on latency and thresholds. We quantified differences in latency and threshold in comparison to a 10-ms test tone, a duration often used in AEP fish studies. Both response latency and threshold were significantly affected by stimulus duration, with latency patterning suggesting that AEP fires coincident with a decrease in stimulus strength. Response latency was also significantly affected by presentation frequency. These results show that stimulus type has important effects on AEP measures of hearing and call for clearer standards across different measures of AEP. Duration effects also suggest that AEP measures represent summed responses of duration-detecting neural circuit, but more effort is needed to understand the neural drivers of this commonly used technique.

Evaluation of Three Sensor Types for Particle Motion Measurement.

All fish sense acoustic particle motion; some species also sense pressure. Concern over the effects of anthropogenic sounds is increasing the need to monitor acoustic particle motion. Particle motion can be measured directly using vector sensors or calculated from pressure gradients. This article compares three devices that measure particle motion: a three-axis accelerometer, a three-axis velocity sensor, and two 4-element hydrophone arrays. A series of sounds (constant-wave tones, white noise, and Ricker wavelets) were played from a fixed-position projector. The particle motion of sounds from imploding light bulbs was also measured.

Convergent Aspects of Acoustic Communication in Darters, Sculpins, and Gobies.

Darters (Perciformes, Percidae), sculpins (Perciformes, Cottidae), and gobioids (Gobiiformes, Gobioidei) exhibit convergent life history traits, including a benthic lifestyle and a cavity nesting spawning mode. Soniferous species within these taxa produce pulsed and/or tonal sounds with peak frequencies below 200 Hz (with some exceptions), primarily in agonistic and/or reproductive contexts. The reduced or absent swim bladders found in these taxa limit or prevent both hearing enhancement via pressure sensitivity and acoustic amplification of the contracting sonic muscles, which are associated with the skull and pectoral girdle. While such anatomies constrain communication to low frequency channels, optimization of the S/N (signal-to-noise) ratio in low frequency channels is evident for some gobies, as measured by habitat soundscape frequency windows, nest cavity sound amplification, and audiograms. Similar S/N considerations are applicable to many darter and sculpin systems. This chapter reviews the currently documented diversity of sound production in darters, sculpins, and gobioids within a phylogenetic context, examines the efficacy of signal transmission from senders to receivers (sound production mechanisms, audiograms, and masking challenges), and evaluates the potential functional significance of sound attributes in relation to territorial and reproductive behaviours.

The Potential Overlapping Roles of the Ear and Lateral Line in Driving "Acoustic" Responses.

Examination of fish responses to sound stimuli has a rich and varied history but it is not always clear when responses are true measures of hearing or the lateral-line. The central innervation of auditory and lateral-line sensory afferents lie in close proximity in the brainstem and both sets of receptors are, at heart, hair cell-based particle motion detectors. While it is possible to separately measure physiological activity of these two receptor subtypes, many studies of fish "hearing" use whole brain potentials or behavioural assays in complex sound fields where it is not possible to distinguish inputs. We argue here that, as often measured, what is thought of as fish "hearing" is often a multisensory response of both auditory and lateral line receptors. We also argue that in many situations where fish use sound stimuli, the behaviour is also an integrative response of both systems, due to the often close proximity of fish during sound communication. We end with a set of recommendations for better understanding the separate and combined roles of ear and lateral-line hair cells as well as an acknowledgment of the seminal and continuing contributions of Arthur N. Popper and Richard R. Fay to this field.

A novel hearing specialization in the New Zealand bigeye, Pempheris adspersa.

The New Zealand bigeye, Pempheris adspersa, is a nocturnal planktivore and has recently been found to be an active sound producer. The rostral end of the swim bladder lies adjacent to Baudelot's ligament which spans between the bulla and the cleithrum bone of the pectoral girdle. The aim of this study was to use the auditory evoked potential technique to physiologically test the possibility that this structure provides an enhanced sensitivity to sound pressure in the bigeye. At 100 Hz, bigeye had hearing sensitivity similar to that of goldfish (species with a mechanical connection between the swim bladder and the inner ear mediated by the Weberian ossicles) and were much more sensitive than other teleosts without ancillary hearing structures. Severing Baudelot's ligament bilaterally resulted in a marked decrease in hearing sensitivity, as did swim bladder puncture or lateral line blockage. These results show that bigeye have an enhanced sensitivity to sound pressure and provide experimental evidence that the functional basis of this sensitivity represents a novel hearing specialization in fish involving the swim bladder, Baudelot's ligament and the lateral line.