The plainfin midshipman fish, Porichthys notatus, is a nocturnal marine teleost that uses social acoustic signals for communication during the breeding season. Nesting type I males produce ...multiharmonic advertisement calls by contracting their swim bladder sonic muscles to attract females for courtship and spawning while subsequently attracting cuckholding type II males. Here, we report intra- and intersexual dimorphisms of the swim bladder in a vocal teleost fish and detail the swim bladder dimorphisms in the three sexual phenotypes (females, type I and II males) of plainfin midshipman fish. Micro-computerized tomography revealed that females and type II males have prominent, horn-like rostral swim bladder extensions that project toward the inner ear end organs (saccule, lagena, and utricle). The rostral swim bladder extensions were longer, and the distance between these swim bladder extensions and each inner-ear end organ type was significantly shorter in both females and type II males compared to that in type I males. Our results revealed that the normalized swim bladder length of females and type II males was longer than that in type I males while there was no difference in normalized swim bladder width among the three sexual phenotypes. We predict that these intrasexual and intersexual differences in swim bladder morphology among midshipman sexual phenotypes will afford greater sound pressure sensitivity and higher frequency detection in females and type II males and facilitate the detection and localization of conspecifics in shallow water environments, like those in which midshipman breed and nest.
This study characterized the seasonal variation of the steroid hormones testosterone (T), 11-ketotestosterone (11-KT), 17β-estradiol (E
2), and cortisol (F) as they relate to the gonadal development ...and reproductive behavior of the plainfin midshipman fish,
Porichthys notatus. The plainfin midshipman is a deep-water teleost that seasonally migrates into the shallow intertidal zone where type I, or “singing,” males build nests, acoustically court and spawn with females. The gonadosomatic index and plasma steroid levels were measured from adult type I males and females collected over four time periods (non-reproductive, pre-nesting, nesting, and post-nesting) that corresponded to seasonal fluctuations in midshipman reproductive biology and behavior. Among type I males, plasma levels of T and 11-KT were low during the winter non-reproductive period, gradually increased during seasonal recrudescence of the testes in the spring pre-nesting period, and then peaked at the beginning of the summer nesting period. In the latter half of the nesting period and during the fall post-nesting period, plasma levels of T and 11-KT were low or non-detectable. Low, detectable levels of E
2 were also found in the plasma of 50% or more type I males during every seasonal period except the winter non-reproductive period. Among females, plasma levels of T and E
2 were low throughout the year but briefly peaked in April during the spring pre-nesting period when ovaries underwent seasonal recrudescence. Plasma F levels were correlated with collection depth and were lower in males than females when fish were collected deeper than 120
m. The sex-specific peaks of steroid hormone levels in male and female midshipman may serve differential functions related to the physiology, reproductive behavior, and vocal communication of this species.
This article describes a novel and interdisciplinary context for learning about real-world sound waves. The 'song' of the plainfin midshipman fish consists of an acoustical wave that is periodic but ...not sinusoidal. This acoustical signal is the focus of active research in sound source localization by fishes, the effects of hormones on hearing systems and the elucidation of neural mechanisms involved in social acoustic communication. In this paper, we introduce the reproductive biology and bioacoustics of the midshipman fish. We describe the use of the advertisement 'song' of the male fish to visualize and interpret the dramatically different displacement, velocity and acceleration waveforms, to explore the roles of pressure and particle motion in production and detection of acoustical waves and to apply Fourier analysis to understand the implications of the frequency spectrum in the production, transmission and reception of sound in an aquatic environment.
The auditory system of the plainfin midshipman fish, Porichthys notatus, is an important sensory receiver system used to encode intraspecific social communication signals in adults, but the response ...properties and function of this receiver system in pre-adult stages are less known. In this study we examined the response properties of auditory-evoked potentials from the midshipman saccule, the main organ of hearing in this species, to determine whether the frequency response and auditory threshold of saccular hair cells to behaviorally relevant single tone stimuli change during ontogeny. Saccular potentials were recorded from three relative sizes of midshipman fish: small juveniles 1.9-3.1 cm standard length (SL), large juveniles (6.8-8.0 cm SL) and non-reproductive adults (9.0-22.6 cm SL). The auditory evoked potentials were recorded from the rostral, middle and caudal regions of the saccule while single tone stimuli (75-1,025 Hz) were presented via an underwater speaker. We show that the frequency response and auditory threshold of the midshipman saccule is established early in development and retained throughout ontogeny. We also show that saccular sensitivity to frequencies greater than 385 Hz increases with age/size and that the midshipman saccule of small and large juveniles, like that of non-reproductive adults, is best suited to detect low frequency sounds (<105 Hz) in their natural acoustic environment.
Excessive noise exposure damages sensory hair cells, leading to permanent hearing loss. Zebrafish are a highly tractable model that have advanced our understanding of drug-induced hair cell death, ...yet no comparable model exists for noise exposure research. We demonstrate the utility of zebrafish as model to increase understanding of hair cell damage from acoustic trauma and develop protective therapies. We created an acoustic trauma system using underwater cavitation to stimulate lateral line hair cells. We found that acoustic stimulation resulted in exposure time- and intensity-dependent lateral line and saccular hair cell damage that is maximal at 48-72 h post-trauma. The number of TUNEL+ lateral line hair cells increased 72 h post-exposure, whereas no increase was observed in TUNEL+ supporting cells, demonstrating that acoustic stimulation causes hair cell-specific damage. Lateral line hair cells damaged by acoustic stimulation regenerate within 3 d, consistent with prior regeneration studies utilizing ototoxic drugs. Acoustic stimulation-induced hair cell damage is attenuated by pharmacological inhibition of protein synthesis or caspase activation, suggesting a requirement for translation and activation of apoptotic signaling cascades. Surviving hair cells exposed to acoustic stimulation showed signs of synaptopathy, consistent with mammalian studies. Finally, we demonstrate the feasibility of this platform to identify compounds that prevent acoustic trauma by screening a small redox library for protective compounds. Our data suggest that acoustic stimulation results in lateral line hair cell damage consistent with acoustic trauma research in mammals, providing a highly tractable model for high-throughput genetic and drug discovery studies.
► Aminoglycoside antibiotics do not completely ablate the lateral line in some fish species. ► Aminoglycosides may be less effective in marine fishes. ► Physical ablation with liquid nitrogen can be ...an effective alternative to chemical ablation.
The auditory system of adult midshipman fish Porichthys notatus Girard is an important sensory receiver system used during intraspecific social communication to encode conspecific vocalizations, but ...the response properties and function of this system in the pre-adult stages are unknown. Midshipman fish, like other teleosts, use the saccule as the main acoustic end organ of the inner ear. In this study, we examined the discharge properties and the frequency response dynamics of auditory saccular afferent neurons in pre-adult midshipman (approximately 4-12 months of age) to determine whether encoding of auditory information, inclusive of conspecific vocalizations, changes across life history stages. Extracellular single unit recordings were made from saccular afferents while sound was presented via an underwater speaker. Comparisons with adult data show that the resting discharge rate and auditory threshold sensitivity increased with age/size, while temporal encoding of frequency did not show any significant shifts. The results indicate that the saccular afferents of juveniles, like those of non-reproductive adults, are best adapted to temporally encode the low frequency components (<or=100 Hz) of midshipman vocalizations. This report represents the first in vivo investigation of age-related changes in the encoding properties of individual auditory neurons for any fish species.
A novel form of auditory plasticity for enhanced detection of social signals was described in a teleost fish, Porichthys notatus (Batrachoididae, Porichthyinae). The seasonal onset of male calling ...coincides with inshore migration from deep waters by both sexes and increased female sensitivity to dominant frequencies of male calls. The closely related Lusitanian toadfish, Halobatrachus didactylus, (Batrachoididae, Halophryninae) also breeds seasonally and relies on acoustic communication to find mates but, instead, both sexes stay in estuaries and show vocal activity throughout the year. We investigated whether the sensitivity of the inner ear saccule of H. didactylus is seasonally plastic and sexually dimorphic. We recorded evoked potentials from populations of saccular hair cells from non-reproductive and reproductive males and females in response to 15–945 Hz tones. Saccular hair cells were most sensitive at 15–205 Hz (thresholds between 111 and 118 dB re. 1 μPa). Both sexes showed identical hearing sensitivity and no differences were found across seasons. The saccule was well suited to detect conspecific vocalizations and low frequencies that overlapped with lateral line sensitivity. We showed that the saccule in H. didactylus has major importance in acoustic communication throughout the year and that significant sensory differences may exist between the two batrachoidid subfamilies.
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