Peter W. Alderks

Sound source localization by the plainfin midshipman fish (Porichthys notatus).

The aim of this study was to use plainfin midshipman fish (Porichthys notatus) as a general model to explore how fishes localize an underwater sound source in the relatively simple geometry of a monopole sound field. The robust phonotaxic responses displayed by gravid females toward a monopole sound projector (J-9) broadcasting a low-frequency (90 Hz) tone similar to the fundamental frequency of the males advertisement call were examined. The projectors sound field was mapped at 5 cm resolution azimuth using an eight-hydrophone array. Acoustic pressure was measured with the array and acoustic particle motion was calculated from pressure gradients between hydrophones. The response pathways of the fish were analyzed from video recordings and compared to the sound field. Gravid females at initial release were directed toward the sound source, and the majority (73%) swam to the playback projector with straight to slightly curved tracks in the direction of the source and in line with local particle motion vectors. In contrast, the initial direction of the control (sound-off) group did not differ from random. This paper reports on a comparison of fish localization behavior with directional cues available in the form of local particle motion vectors.

Local acoustic particle motion guides sound-source localization behavior in the plainfin midshipman fish, Porichthys notatus

SUMMARY Sound-source localization behavior was studied in the plainfin midshipman fish (Porichthys notatus) by making use of the naturally occurring phonotaxis response of gravid females to playback of the males advertisement call. The observations took place outdoors in a circular concrete tank. A dipole sound projector was placed at the center of the tank and an 80–90 Hz tone (the approximate fundamental frequency to the males advertisement call) was broadcast to gravid females that were released from alternative sites approximately 100 cm from the source. The phonotaxic responses of females to the source were recorded, analyzed and compared with the sound field. One release site was approximately along the vibratory axis of the dipole source, and the other was approximately orthogonal to the vibratory axis. The sound field in the tank was fully characterized through measurements of the sound pressure field using hydrophones and acoustic particle motion using an accelerometer. These measurements confirmed that the sound field was a nearly ideal dipole. When released along the dipole vibratory axis, the responding female fish took essentially straight paths to the source. However, when released approximately 90 deg to the sources vibratory axis, the responding females took highly curved paths to the source that were approximately in line with the local particle motion axes. These results indicate that the acoustic cues used by fish during sound-source localization include the axes of particle motion of the local sound field.

Use of the swim bladder and lateral line in near-field sound source localization by fish

We investigated the roles of the swim bladder and the lateral line system in sound localization behavior by the plainfin midshipman fish (Porichthys notatus). Reproductive female midshipman underwent either surgical deflation of the swim bladder or cryoablation of the lateral line and were then tested in a monopolar sound source localization task. Fish with nominally ‘deflated’ swim bladders performed similar to sham-deflated controls; however, post-experiment evaluation of swim bladder deflation revealed that a majority of ‘deflated’ fish (88%, seven of the eight fish) that exhibited positive phonotaxis had partially inflated swim bladders. In total, 95% (21/22) of fish that localized the source had at least partially inflated swim bladders, indicating that pressure reception is likely required for sound source localization. In lateral line experiments, no difference was observed in the proportion of females exhibiting positive phonotaxis with ablated (37%) versus sham-ablated (47%) lateral line systems. These data suggest that the lateral line system is likely not required for sound source localization, although this system may be important for fine-tuning the approach to the sound source. We found that midshipman can solve the 180 deg ambiguity of source direction in the shallow water of our test tank, which is similar to their nesting environment. We also found that the potential directional cues (phase relationship between pressure and particle motion) in shallow water differs from a theoretical free-field. Therefore, the general question of how fish use acoustic pressure cues to solve the 180 deg ambiguity of source direction from the particle motion vector remains unresolved.

Vocal differentiation parallels development of auditory saccular sensitivity in a highly soniferous fish

ABSTRACT Vocal differentiation is widely documented in birds and mammals but has been poorly investigated in other vertebrates, including fish, which represent the oldest extant vertebrate group. Neural circuitry controlling vocal behaviour is thought to have evolved from conserved brain areas that originated in fish, making this taxon key to understanding the evolution and development of the vertebrate vocal-auditory systems. This study examines ontogenetic changes in the vocal repertoire and whether vocal differentiation parallels auditory development in the Lusitanian toadfish Halobatrachus didactylus (Batrachoididae). This species exhibits a complex acoustic repertoire and is vocally active during early development. Vocalisations were recorded during social interactions for four size groups (fry: <2 cm; small juveniles: 2–4 cm; large juveniles: 5–7 cm; adults >25 cm, standard length). Auditory sensitivity of juveniles and adults was determined based on evoked potentials recorded from the inner ear saccule in response to pure tones of 75–945 Hz. We show an ontogenetic increment in the vocal repertoire from simple broadband-pulsed ‘grunts’ that later differentiate into four distinct vocalisations, including low-frequency amplitude-modulated ‘boatwhistles’. Whereas fry emitted mostly single grunts, large juveniles exhibited vocalisations similar to the adult vocal repertoire. Saccular sensitivity revealed a three-fold enhancement at most frequencies tested from small to large juveniles; however, large juveniles were similar in sensitivity to adults. We provide the first clear evidence of ontogenetic vocal differentiation in fish, as previously described for higher vertebrates. Our results suggest a parallel development between the vocal motor pathway and the peripheral auditory system for acoustic social communication in fish. Highlighted Article: Vocal differentiation and parallel development between vocal–motor control and saccular sensitivity in toadfish.

Development of Structure and Sensitivity of the Fish Inner Ear

Fish represent the largest group of vertebrates and display the greatest diversity of auditory structures. However, studies addressing how the form and function of the auditory system change during development to enhance perception of the acoustic environment are rather sparse in this taxon compared to other vertebrate groups. An ontogenetic perspective of the auditory system in fishes provides a readily testable framework for understanding structure-function relationships. Additionally, studying ancestral models such as fish can convey valuable comparable information across vertebrates, as early developmental events are often evolutionary conserved. This chapter reviews the literature on the morphological development of the fish auditory system, with particular focus on the inner ear structures that evolve from an otic placode during early embryonic development and then continue to undergo differentiation and maturation in the postembryonic phase. Moreover, the chapter provides a systematic overview of how auditory sensitivity develops during ontogeny. Although most studies indicate a developmental improvement in auditory sensitivity, there is considerably species-specific variation. Lastly, the paucity of information and literature concerning the development of auditory capabilities for social communication in fishes is also discussed. Further investigation on the development of structure and function of the fish auditory system is recommended in order to obtain a deeper understanding of how ontogenetic morphological changes in the auditory pathway relate to modifications in acoustic reception, auditory processing, and the capacity to communicate acoustically.

Sound source localization of a dipole by the plainfin midshipman fish (Porichthys notatus).

Localization of a dipole sound source was studied in female plainfin midshipman fish (Porichthys notatus). Experiments were conducted and videotaped in a 3.65‐m‐diameter tank using a dipole underwater speaker system placed near the center of the tank. The sound was a 90‐Hz tone, approximately the fundamental frequency of the male’s advertisement call. Pressure and particle motion components of the sound field were mapped with 9‐cm resolution. Pressure was measured using an eight‐hydrophone array, and particle motion vectors calculated from the pressure gradients. Mapping confirmed that the projector was operating as a dipole. Gravid fish were released 70 cm from the sound source at two different positions relative to the dipole axis: one near the dipole axis and one near the pressure null axis. Twenty‐five positive responses were recorded from each release site. The phonotactic response pathways along the dipole axis consisted of slightly curved tracks to the sound source, whereas pathways from the null axis consisted of greatly curved tracks to the source that followed the particle motion vectors. Results confirm that fish can locate a dipole sound source and are sensitive to the direction of acoustic particle motion. [Work supported by NSF.]

Ontogeny of early audition in the plainfin midshipman, Porichthys notatus.

Early development is a time of great organizational activity. As sensory systems become functionally active, they often undergo a period of ontogenetic plasticity. The early ontogeny of the auditory system of the plainfin midshipman is of particular interest. During early ontogeny, the fertilized eggs of the midshipman are attached to the underside of rocks guarded by nesting (type I) males. These nesting males often guard multiple clutches of eggs while actively calling to attract additional mates. The males’ advertisement call is high intensity (approximately 145 dB re 1 μPa at the source) and long duration (minutes to hours). During nest incubation, the auditory system of the developing embryos becomes active. We previously showed that when juveniles leave the nest, the auditory sensitivity of their saccule closely resembles that of nonreproductive adults. Here, we investigate auditory sensitivity from the time the auditory system becomes functional until the juvenile midshipman is free swimming using ...

Localization of monopole and dipole sound sources by midshipman fish (Porichthys notatus).

A series of experiments was undertaken to investigate methods of sound source localization by fish. In these experiments, positive phonotaxic responses of gravid female plainfin midshipman fish (Porichthys notatus) to low‐frequency, playback tones (80–90 Hz) were studied as they approached sound sources. The sound fields for simple (monopole) and relatively complex (dipole) sources within the behavioral arena were measured and characterized in terms of pressure and particle motion. Results indicate that female midshipman fish are able to locate sound sources in the near field using acoustic cues alone, and that they used the particle motion vectors to locate the source in both the monopole and dipole sound fields. It was also found that neither the lateral line nor the swim bladder was necessary for localization behavior, and that the fish were able to solve the 180 deg ambiguity inherent in the particle motion vectors. [Work was supported by the National Science Foundation.]

Ontogeny of auditory saccular tuning in the plainfin midshipman fish, Porichthys notatus.

Sensory systems are important throughout an animal’s life history, allowing it to detect and respond to biologically relevant stimuli important for survival and reproduction. The auditory system of the plainfin midshipman fish (Porichthys notatus) plays an important sensory receiving role for encoding vocal‐acoustic communication signals produced by adults, but the response properties and function of this receiver system during ontogeny are less understood. Here, we examine the response properties of evoked saccular potentials in two size classes of juveniles [small = 1.9–3.0 cm standard length (SL) and large = 5.0–8.0 cm SL] and in nonreproductive adults (> 9.0 cm SL) to determine the auditory sensitivity of saccular hair cells during ontogeny. Saccular potentials, maximally evoked at twice the stimulus frequency, were recorded in vivo using a lock‐in amplifier while playing pure tone stimuli via an underwater speaker. Results indicate an ontogenetic retention of saccular tuning sensitivity with size/age with peak sensitivity ranging from 75 Hz (lowest frequency tested) to 185 Hz. In addition, maximum detectable frequency of the saccule also increased with size/age. These results suggest that the midshipman saccule is best suited to detect low frequency components (< 105 Hz) of conspecific vocalizations throughout ontogeny.