Sexually dimorphic swim bladder extensions enhance the auditory sensitivity of female plainfin midshipman fish,Porichthys notatus

Abstract

The plainfin midshipman fish, Porichthys notatus, is a seasonally breeding, nocturnal marine teleost fish that produces acoustic signals for intraspecific social communication. Females rely on audition to detect and locate 'singing' males that produce multiharmonic advertisement calls in the shallow-water, intertidal breeding environments. Previous work showed that females possess sexually dimorphic, horn-like rostral swim bladder extensions that extend toward the primary auditory end organs, the saccule and lagena. Here, we tested the hypothesis that the rostral swim bladder extensions in females increase auditory sensitivity to sound pressure and higher frequencies, which potentially could enhance mate detection and localization in shallow-water habitats. We recorded the auditory evoked potentials that originated from hair cell receptors in the saccule of control females with intact swim bladders and compared them with those from treated females (swim bladders removed) and type I males (intact swim bladders lacking rostral extensions). Saccular potentials were recorded from hair cell populations in vivo while behaviorally relevant pure-tone stimuli (75-1005 Hz) were presented by an underwater speaker. The results indicate that control females were approximately 5-11 dB re. 1 µPa more sensitive to sound pressure than treated females and type I males at the frequencies tested. A higher percentage of the evoked saccular potentials were recorded from control females at frequencies >305 Hz than from treated females and type I males. This enhanced sensitivity in females to sound pressure and higher frequencies may facilitate the acquisition of auditory information needed for conspecific localization and mate choice decisions during the breeding season.

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

“…Such extensions, also present in certain other teleost species, are hypothesized to impart sound pressure sensitivity via mechanical coupling of the swim bladder and inner ear, akin to that provided by Weberian ossicles in otophysan species (e.g. Coombs and Popper, 1979;Ramcharitar et al, 2006), which is supported by recent saccular potential measurements (Colleye et al 2019). We note that 'type II' male midshipman, an alternative male morph not considered further in the present report, also possess rostral swim bladder extensions and exhibit seasonally enhanced auditory sensitivity (see Mohr et al, 2017;Bhandiwad et al, 2017).…”

“…This preparation (see Materials and Methods) points to interesting possibilities for future studies of swim bladder acoustic/auditory functionality, but in the present study served chiefly to demonstrate that contributions of the swim bladder could be measured in female midshipman via the AEP paradigm we employed (cf. Colleye et al 2019, describing saccular potential measurements after swim bladder excision).…”

Ontogeny of Inner Ear Saccular Development in the Plainfin Midshipman (Porichthys notatus)

“…These end organ differences in HC number are likely related to the end organ size of the macular area with the saccule having the largest macular area in general (note, we did not compare the macular areas of the utricle, lagena, and saccule, but the differences in end organ size visually are obvious). Not sur-prisingly, the lagena, which is the smallest end organ, is significantly less sensitive than the saccule and utricle based on HC auditory evoked potentials [Colleye et al, 2019;Vetter et al, 2019;Rogers and Sisneros, 2020]. In addition to having fewer total HCs as we report here, the lagena also has the lowest otolith mass (smallest of the three end organs) and contains an otolith (asteriscus) that is predominantly composed of lighter vaterite [Campana, 1999;Reimer et al, 2016].…”

“…3) that changed from vertically oriented HCs to horizontally oriented HCs that followed the macula margin in juveniles and adults. Recently Colleye et al [2019] have shown that female midshipman fish which possess sexually dimorphic rostral swim bladder extensions have enhanced auditory sensitivity to sound pressure and fre- quencies >305 Hz. The swim bladder horn-like extensions decrease the distance between the swim bladder and saccule to effectively enhance the detection of local particle motion generated by pressure-induced vibrations of the swim bladder when exposed to sound.…”

“…In addition to having fewer total HCs as we report here, the lagena also has the lowest otolith mass (smallest of the three end organs) and contains an otolith (asteriscus) that is predominantly composed of lighter vaterite [Campana, 1999;Reimer et al, 2016]. Although the adult utricle has a significantly lower number of HCs than the saccule, a recent study by Rogers and Sisneros [2020] showed that the auditory sensitivity of the utricle based on HC auditory evoked potentials was very similar to the saccular sensitivity of type I males at frequencies <305 Hz; however, at frequencies >305 Hz the utricle was even more sensitive than the saccule [Colleye et al, 2019]. Given that the otoliths of the saccule (sagitta) and utricle (lapillus) are both primarily composed of calcium carbonate in the form of aragonite [Thorrold and Hare, 2002] and would share similar densities but different overall otolith masses, it remains unclear how differences in otolith mass and end organ HC numbers and densities would affect auditory sensitivity based on HC auditory evoked potentials.…”