Swim bladder enhances lagenar sensitivity to sound pressure and higher frequencies in female plainfin midshipman (Porichthys notatus)

Abstract

The plainfin midshipman fish (Porichthys notatus) is an established model for investigating acoustic communication because the reproductive success of this species is dependent on the production and reception of social acoustic signals. Previous work showed that female midshipman have swim bladders with rostral horn-like extensions that project close to the saccule and lagena, while nesting (type I) males lack such rostral swim bladder extensions. The relative close proximity of the swim bladder to the lagena should increase auditory sensitivity to sound pressure and higher frequencies. Here, we test the hypothesis that the swim bladder of female midshipman enhances lagenar sensitivity to sound pressure and higher frequencies. Evoked potentials were recorded from auditory hair cell receptors in the lagena in reproductive females with intact (control condition) and removed (treated condition) swim bladders while pure tone stimuli (85-1005 Hz) were presented by an underwater speaker. Females with intact swim bladders had auditory thresholds 3-6 dB lower than females without swim bladders over a range of frequencies from 85 to 405 Hz. At frequencies from 545 to 1005 Hz, only females with intact swim bladders had measurable auditory thresholds (150-153 dB re. 1 µPa). The higher percentage of evoked lagenar potentials recorded in control females at frequencies >505 Hz indicates that the swim bladder extends the bandwidth of detectable frequencies. These findings reveal that the swim bladders in female midshipman can enhance lagenar sensitivity to sound pressure and higher frequencies, which may be important for the detection of behaviorally relevant social signals.

Keywords: Acoustic signal; Auditory threshold; Communication; Hearing; Inner ear.

Fig. 1.

Drawing of a female plainfin midshipman with a representative micro-computed tomography scan showing a lateral view of the swim bladder, saccule and lagena. SB, swim bladder; S, saccule; L, lagena. Inset: dotted lines indicate close proximity of rostral swim bladder extensions to the lagena. Drawing adapted from Robertson (2015) and micro-computed tomography scan modified from Mohr et al. (2017).

Fig. 2.

Representative examples of iso-intensity curves recorded from the lagena in response to pure tone frequencies at the highest sound pressure level tested (154 dB re. 1 µPa). A range of evoked potentials (low, middle and high) are shown for both control (intact swim bladder condition; bottom) and treated (removed swim bladder condition; top) females. The data are displayed as means±95% CI.

Fig. 3.

Representative examples of individual auditory threshold tuning curves based on evoked potentials recorded from the lagena of control and treated female midshipman. A range of characteristic frequencies (low, middle, high) are shown for both control (intact swim bladder condition; bottom) and treated (removed swim bladder condition; top) females. Thresholds were defined as the lowest sound pressure level (dB re. 1 µPa) to evoke a lagenar potential at least 2 s.d. above background noise.

Fig. 4.

Auditory threshold tuning curves based on sound pressure levels for lagenar potentials recorded in control and treated female midshipman. The auditory threshold was defined as the lowest sound pressure level (dB re. 1 µPa) needed to evoke a lagenar potential that was at least 2 s.d. above background noise. Data are represented as means±95% CI. For both control (intact swim bladder condition) and treated (removed swim bladder condition) fish, the number of individual animals (first N value) and records (second N value) is indicated in parentheses.

Fig. 5.

Auditory threshold tuning curves based on particle acceleration levels for lagenar potentials recorded in control and treated female midshipman. Particle acceleration measurements were made at each sound pressure level evaluated and thresholds for particle acceleration were constructed at the corresponding sound pressure levels. Data are represented as means±95% CI. The number of individual animals (first N value) and records (second N value) for both control (intact swim bladder condition) and treated (removed swim bladder condition) fish is indicated in parentheses.

Fig. 6.

Percentage of lagenar potentials evoked above threshold at each tested frequency for control and treated fish. Lagenar potentials were observed in all recordings at frequencies from 85 to 205 Hz in control (intact swim bladder condition; N=17) fish and at frequencies from 85 to 165 Hz in treated (removed swim bladder condition; N=30) fish. However, at frequencies >205 Hz in control fish or >165 Hz in treated fish, lagenar potentials were not always detected, even at the highest sound pressure evaluated. The number of individual animals (first N value) and records (second N value) for both treatment groups is indicated in parentheses.