The plainfin midshipman fish (Porichthys notatus) has long served as a model organism for neuroethology research on acoustic communication and related social behaviors. Type I or 'singing' males ...produce highly stereotyped, periodic advertisement calls that are the longest known uninterrupted vertebrate vocalizations. Despite the extensive literature on the acoustic behaviour of this species, it remains unclear whether reproductive males signal their quality via their highly energetic, multiharmonic advertisement calls. Here, we recorded the advertisement calls of 22 reproductive type I males at night in a controlled laboratory setting in which males were housed in aquaria maintained at a constant temperature (13.9±0.3°C). The duration of the advertisement calls from type I males was observed to increase from the first call of the night to the middle call after which call duration remained steady until the early morning hours and first light. A strong positive correlation was observed between loudness (sound pressure level and maximum sound pressure level) of the advertisement call and body size (mass and standard length; rs>0.8). In addition, an asymptotic relationship was observed between the harmonic frequencies (f0-f10) of the advertisement calls and male body condition, with harmonic frequencies initially increasing with body condition indices, but then plateauing when body condition measures were high. Taken together, our results suggest that type I male advertisement calls provide reliable honest information about male quality regarding size and body condition. Such condition-dependent information of calling males could potentially be used by receptive females to help facilitate mate choice decisions.
The plainfin midshipman fish, Porichthys notatus, is a seasonally breeding species of marine teleost fish that generates acoustic signals for intraspecific social and reproductive-related ...communication. Female midshipman use the inner ear saccule as the main acoustic endorgan for hearing to detect and locate vocalizing males that produce multiharmonic advertisement calls during the breeding season. Previous work showed that the frequency sensitivity of midshipman auditory saccular afferents changed seasonally with female reproductive state such that summer reproductive females became better suited than winter nonreproductive females to encode the dominant higher harmonics of the male advertisement calls. The focus of this study was to test the hypothesis that seasonal reproductive-dependent changes in saccular afferent tuning is paralleled by similar changes in saccular sensitivity at the level of the hair-cell receptor. Here, I examined the evoked response properties of midshipman saccular hair cells from winter nonreproductive and summer reproductive females to determine if reproductive state affects the frequency response and threshold of the saccule to behaviorally relevant single tone stimuli. Saccular potentials were recorded from populations of hair cells in vivo while sound was presented by an underwater speaker. Results indicate that saccular hair cells from reproductive females had thresholds that were approximately 8 to 13 dB lower than nonreproductive females across a broad range of frequencies that included the dominant higher harmonic components and the fundamental frequency of the male's advertisement call. These seasonal-reproductive-dependent changes in thresholds varied differentially across the three (rostral, middle, and caudal) regions of the saccule. Such reproductive-dependent changes in saccule sensitivity may represent an adaptive plasticity of the midshipman auditory sense to enhance mate detection, recognition, and localization during the breeding season.
Despite identification of multiple factors mediating salmon survival, significant disparities in survival-to-adulthood among hatchery- versus wild-origin juveniles persist. In the present report, we ...explore the hypothesis that hatchery-reared juveniles might exhibit morphological defects in vulnerable mechanosensory systems prior to release from the hatchery, potentiating reduced survival after release. Juvenile steelhead (Oncorhynchus mykiss) from two different hatcheries were compared to wild-origin juveniles on several morphological traits including lateral line structure, otolith composition (a proxy for auditory function), and brain weight. Wild juveniles were found to possess significantly more superficial lateral line neuromasts than hatchery-reared juveniles, although the number of hair cells within individual neuromasts was not significantly different across groups. Wild juveniles were also found to possess primarily normal, aragonite-containing otoliths, while hatchery-reared juveniles possessed a high proportion of crystallized (vaterite) otoliths. Finally, wild juveniles were found to have significantly larger brains than hatchery-reared juveniles. These differences together predict reduced sensitivity to biologically important hydrodynamic and acoustic signals from natural biotic (predator, prey, conspecific) and abiotic (turbulent flow, current) sources among hatchery-reared steelhead, in turn predicting reduced survival fitness after release. Physiological and behavioral studies are required to establish the functional significance of these morphological differences.
The plainfin midshipman fish (
) 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.
The plainfin midshipman,
, is a seasonally breeding vocal fish that relies on acoustic communication to mediate nocturnal reproductive behaviors. Reproductive females use their auditory senses to ...detect and localize "singing" males that produce multiharmonic advertisement (mate) calls during the breeding season. Previous work showed that the midshipman saccule, which is considered the primary end organ used for hearing in midshipman and most other fishes, exhibits reproductive state and hormone-dependent changes that enhance saccular auditory sensitivity. In contrast, the utricle was previously posited to serve primarily a vestibular function, but recent evidence in midshipman and related toadfish suggests that it may also serve an auditory function and aid in the detection of behaviorally relevant acoustic stimuli. Here, we characterized the auditory-evoked potentials recorded from utricular hair cells in reproductive and nonreproductive female midshipman in response to underwater sound to test the hypothesis that variation in reproductive state affects utricular auditory sensitivity. We show that utricular hair cells in reproductive females exhibit up to a sixfold increase in the utricular potential magnitude and have thresholds based on measures of particle acceleration (re: 1 ms
) that are 7-10 dB lower than nonreproductive females across a broad range of frequencies, which include the dominant harmonics of male advertisement calls. This enhanced auditory sensitivity of the utricle likely plays an essential role in facilitating midshipman social and reproductive acoustic communication.
In many animals, vocal-acoustic communication is fundamental for facilitating social behaviors. For the vocal plainfin midshipman fish, the detection and localization of social acoustic signals are critical to the species' reproductive success. Here, we show that the utricle, an inner ear end organ often thought to primarily serve a vestibular function, serves an auditory function that is seasonally plastic and modulated by the animal's reproductive state effectively enhancing auditory sensitivity to courting male advertisement calls.
Dopamine is integral to attentional and motivational processes, but studies are largely restricted to the central nervous system. In mammals 1, 2 and fishes 3, 4, central dopaminergic neurons project ...to the inner ear and could modulate acoustic signals at the earliest stages of processing. Studies in rodents show dopamine inhibits cochlear afferent neurons and protects against noise-induced acoustic injury 5–10. However, other functions for inner ear dopamine have not been investigated, and the effect of dopamine on peripheral auditory processing in non-mammalians remains unknown 11, 12. Insights could be gained by studies conducted in the context of intraspecific acoustic communication. We present evidence from a vocal fish linking reproductive-state-dependent changes in auditory sensitivity with seasonal changes in the dopaminergic efferent system in the saccule, their primary organ of hearing. Plainfin midshipman (Porichthys notatus) migrate from deep-water winter habitats to the intertidal zone in the summer to breed. Nesting males produce nocturnal vocalizations to attract females 13. Both sexes undergo seasonal enhancement of hearing sensitivity at the level of the hair cell 14–16, increasing the likelihood of detecting conspecific signals 17, 18. Importantly, reproductive females concurrently have reduced dopaminergic input to the saccule 19. Here, we show that dopamine decreases saccule auditory sensitivity via a D2-like receptor. Saccule D2a receptor expression is reduced in the summer and correlates with sensitivity within and across seasons. We propose that reproductive-state-dependent changes to the dopaminergic efferent system provide a release of inhibition in the saccule, enhancing peripheral encoding of social-acoustic signals.
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•Dopamine reduces inner ear sensitivity in a vocal fish, matching seasonal changes•Reduced sensitivity is mediated by D2 receptors (D2Rs) expressed in hair cells•D2 receptors vary with reproductive state and inversely correlate with sensitivity•Results suggest a role for inner ear dopamine in social-acoustic communication
In mammals and fishes, central dopamine neurons project to the inner ear and could affect the encoding of acoustic signals at the earliest stage of processing. Perelmuter et al. provide evidence from a vocal fish that dopamine contributes to a reproductive-state-dependent shift in inner ear sensitivity, enhancing a female’s ability to detect mates.
While the neural circuitry and physiology of the auditory system is well studied among vertebrates, far less is known about how the auditory system interacts with other neural substrates to mediate ...behavioral responses to social acoustic signals. One species that has been the subject of intensive neuroethological investigation with regard to the production and perception of social acoustic signals is the plainfin midshipman fish, Porichthys notatus, in part because acoustic communication is essential to their reproductive behavior. Nesting male midshipman vocally court females by producing a long duration advertisement call. Females localize males by their advertisement call, spawn and deposit all their eggs in their mate's nest. As multiple courting males establish nests in close proximity to one another, the perception of another male's call may modulate individual calling behavior in competition for females. We tested the hypothesis that nesting males exposed to advertisement calls of other males would show elevated neural activity in auditory and vocal-acoustic brain centers as well as differential activation of catecholaminergic neurons compared to males exposed only to ambient noise. Experimental brains were then double labeled by immunofluorescence (-ir) for tyrosine hydroxylase (TH), an enzyme necessary for catecholamine synthesis, and cFos, an immediate-early gene product used as a marker for neural activation. Males exposed to other advertisement calls showed a significantly greater percentage of TH-ir cells colocalized with cFos-ir in the noradrenergic locus coeruleus and the dopaminergic periventricular posterior tuberculum, as well as increased numbers of cFos-ir neurons in several levels of the auditory and vocal-acoustic pathway. Increased activation of catecholaminergic neurons may serve to coordinate appropriate behavioral responses to male competitors. Additionally, these results implicate a role for specific catecholaminergic neuronal groups in auditory-driven social behavior in fishes, consistent with a conserved function in social acoustic behavior across vertebrates.
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