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.

Wall structure and material properties cause viscous damping of swimbladder sounds in the oyster toadfish Opsanus tau.

Despite rapid damping, fish swimbladders have been modelled as underwater resonant bubbles. Recent data suggest that swimbladders of sound-producing fishes use a forced rather than a resonant response to produce sound. The reason for this discrepancy has not been formally addressed, and we demonstrate, for the first time, that the structure of the swimbladder wall will affect vibratory behaviour. Using the oyster toadfish Opsanus tau, we find regional differences in bladder thickness, directionality of collagen layers (anisotropic bladder wall structure), material properties that differ between circular and longitudinal directions (stress, strain and Young's modulus), high water content (80%) of the bladder wall and a 300-fold increase in the modulus of dried tissue. Therefore, the swimbladder wall is a viscoelastic structure that serves to damp vibrations and impart directionality, preventing the expression of resonance.

Characterization and generation of male courtship song in Cotesia congregata (Hymenoptera: Braconidae).

BACKGROUND: Male parasitic wasps attract females with a courtship song produced by rapid wing fanning. Songs have been described for several parasitic wasp species; however, beyond association with wing fanning, the mechanism of sound generation has not been examined. We characterized the male courtship song of Cotesia congregata (Hymenoptera: Braconidae) and investigated the biomechanics of sound production. METHODS AND PRINCIPAL FINDINGS: Courtship songs were recorded using high-speed videography (2,000 fps) and audio recordings. The song consists of a long duration amplitude-modulated "buzz" followed by a series of pulsatile higher amplitude "boings," each decaying into a terminal buzz followed by a short inter-boing pause while wings are stationary. Boings have higher amplitude and lower frequency than buzz components. The lower frequency of the boing sound is due to greater wing displacement. The power spectrum is a harmonic series dominated by wing repetition rate ∼220 Hz, but the sound waveform indicates a higher frequency resonance ∼5 kHz. Sound is not generated by the wings contacting each other, the substrate, or the abdomen. The abdomen is elevated during the first several wing cycles of the boing, but its position is unrelated to sound amplitude. Unlike most sounds generated by volume velocity, the boing is generated at the termination of the wing down stroke when displacement is maximal and wing velocity is zero. Calculation indicates a low Reynolds number of ∼1000. CONCLUSIONS AND SIGNIFICANCE: Acoustic pressure is proportional to velocity for typical sound sources. Our finding that the boing sound was generated at maximal wing displacement coincident with cessation of wing motion indicates that it is caused by acceleration of the wing tips, consistent with a dipole source. The low Reynolds number requires a high wing flap rate for flight and predisposes wings of small insects for sound production.

Acoustical properties of the swimbladder in the oyster toadfish Opsanus tau.

Both the swimbladder and sonic muscles of the oyster toadfish Opsanus tau (Linnaeus) increase in size with fish growth making it difficult to distinguish their relative contributions to sound production. We examined acoustics of the swimbladder independent of the sonic muscles by striking it with a piezoelectric impact hammer. Amplitude and timing characteristics of bladder sound and displacement were compared for strikes of different amplitudes. Most of the first cycle of sound occurred during swimbladder compression, indicating that the bladder rapidly contracted and expanded as force increased during the strike. Harder hits were shorter in duration and generated a 30 dB increase in amplitude for a 5-fold or 14 dB range in displacement. For an equivalent strike dominant frequency, damping, bladder displacement and sound amplitude did not change with fish size, i.e. equal input generated equal output. The frequency spectrum was broad, and dominant frequency was driven by the strike and not the natural frequency of the bladder. Bladder displacement decayed rapidly (zeta averaged 0.33, equivalent to an automobile shock absorber), and the bladder had a low Q (sharpness of tuning), averaging 1.8. Sound output of an acoustic source is determined by volume velocity (surface area x velocity), and bladder surface area, muscle dimensions and contraction amplitude increase with fish size. Therefore, larger fish will be capable of producing more intense sound. Because the bladder is a low Q resonator, its output will follow muscle contraction rates independent of its size and natural frequency.

Functional morphology of the sonic apparatus in the fawn cusk-eel Lepophidium profundorum (Gill, 1863).

Recent reports of high frequency sound production by cusk-eels cannot be explained adequately by known mechanisms, i.e., a forced response driven by fast sonic muscles on the swimbladder. Time to complete a contraction-relaxation cycle places a ceiling on frequency and is unlikely to explain sounds with dominant frequencies above 1 kHz. We investigated sonic morphology in the fawn cusk-eel Lepophidium profundorum to determine morphology potentially associated with high frequency sound production and quantified development and sexual dimorphism of sonic structures. Unlike other sonic systems in fishes in which muscle relaxation is caused by internal pressure or swimbladder elasticity, this system utilizes antagonistic pairs of muscles: ventral and intermediate muscles pull the winglike process and swimbladder forward and pivot the neural arch (neural rocker) above the first vertebra backward. This action stretches a fenestra in the swimbladder wall and imparts strain energy to epineural ribs, tendons and ligaments connected to the anterior swimbladder. Relatively short antagonistic dorsal and dorsomedial muscles pull on the neural rocker, releasing strain energy, and use a lever advantage to restore the winglike process and swimbladder to their resting position. Sonic components grow isometrically and are typically larger in males although the tiny intermediate muscles are larger in females. Although external morphology is relatively conservative in ophidiids, sonic morphology is extremely variable within the family.

The effect of loading on disturbance sounds of the Atlantic croaker Micropogonius undulatus: air versus water.

Physiological work on fish sound production may require exposure of the swimbladder to air, which will change its loading (radiation mass and resistance) and could affect parameters of emitted sounds. This issue was examined in Atlantic croaker Micropogonius chromis by recording sounds from the same individuals in air and water. Although sonograms appear relatively similar in both cases, pulse duration is longer because of decreased damping, and sharpness of tuning (Q factor) is higher in water. However, pulse repetition rate and dominant frequency are unaffected. With appropriate caution it is suggested that sounds recorded in air can provide a useful tool in understanding the function of various swimbladder adaptations and provide reasonable approximation of natural sounds. Further, they provide an avenue for experimentally manipulating the sonic system, which can reveal details of its function not available from intact fish underwater.