Plainfin Midshipman Fish Research Articles

Seasonal plasticity of saccular sensitivity in the type II sneaker-male plainfin midshipman fish (Porichthys notatus).

Acoustic communication is essential to the reproductive success of the nocturnally breeding plainfin midshipman fish (Porichthys notatus). During the summer breeding season, type I singing-males excavate nests in the Pacific intertidal zone and vocalize a multiharmonic “advertisement hum” to attract potential mates. Summer reproductive females are more sensitive to the dominant frequencies that comprise the hum than winter nonreproductive females. Type II or “sneaker” males employ alternative mating strategies that do not require nest construction or hum production but instead involve satellite and/or sneak spawning strategies. These strategies require nocturnal nest selection and localization. Because sneaker-males must rely on their auditory system to find the nests of singing males just as females must, we hypothesized that the saccular sensitivity of the reproductive sneaker-males would be most like that of reproductive females. Here we measured the evoked saccular potentials of reproductive and nonreproductive sneaker-males to tones of various sound pressure levels, and determined saccular thresholds for frequencies from 65 to 505 Hz. As predicted, thresholds measured in reproductive sneaker-males very closely matched those reported for reproductive females. Future studies will investigate the effects of gonadal steroids on hearing in sneaker-male midshipman fish. [Work supported by NIH NIDCD Grant No. 2T32DC005361-06.]

Ontogeny of auditory saccular sensitivity in the plainfin midshipman fish, Porichthys notatus

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.

Sound source localization by the plainfin midshipman fish, Porichthys notatus

The aim of this study was to use plainfin midshipman fish (Porichthys notatus) as a general model to explore how fishes localize an underwater sound source in the relatively simple geometry of a monopole sound field. The robust phonotaxic responses displayed by gravid females toward a monopole sound projector (J-9) broadcasting a low-frequency (90 Hz) tone similar to the fundamental frequency of the male's advertisement call were examined. The projector's sound field was mapped at 5 cm resolution azimuth using an eight-hydrophone array. Acoustic pressure was measured with the array and acoustic particle motion was calculated from pressure gradients between hydrophones. The response pathways of the fish were analyzed from video recordings and compared to the sound field. Gravid females at initial release were directed toward the sound source, and the majority (73%) swam to the playback projector with straight to slightly curved tracks in the direction of the source and in line with local particle motion vectors. In contrast, the initial direction of the control (sound-off) group did not differ from random. This paper reports on a comparison of fish localization behavior with directional cues available in the form of local particle motion vectors.

Sound source localization of a dipole by the plainfin midshipman fish (Porichthys notatus).

Localization of a dipole sound source was studied in female plainfin midshipman fish (Porichthys notatus). Experiments were conducted and videotaped in a 3.65-m-diameter tank using a dipole underwater speaker system placed near the center of the tank. The sound was a 90-Hz tone, approximately the fundamental frequency of the male’s advertisement call. Pressure and particle motion components of the sound field were mapped with 9-cm resolution. Pressure was measured using an eight-hydrophone array, and particle motion vectors calculated from the pressure gradients. Mapping confirmed that the projector was operating as a dipole. Gravid fish were released 70 cm from the sound source at two different positions relative to the dipole axis: one near the dipole axis and one near the pressure null axis. Twenty-five positive responses were recorded from each release site. The phonotactic response pathways along the dipole axis consisted of slightly curved tracks to the sound source, whereas pathways from the null axis consisted of greatly curved tracks to the source that followed the particle motion vectors. Results confirm that fish can locate a dipole sound source and are sensitive to the direction of acoustic particle motion. [Work supported by NSF.]

Estradiol interacts with an opioidergic network to achieve rapid modulation of a vocal pattern generator

Estrogens rapidly regulate neuronal activity within seconds-to-minutes, yet it is unclear how estrogens interact with neural circuits to rapidly coordinate behavior. This study examines whether 17-beta-estradiol interacts with an opioidergic network to achieve rapid modulation of a vocal control circuit. Adult plainfin midshipman fish emit vocalizations that mainly differ in duration, and rhythmic activity of a hindbrain–spinal vocal pattern generator (VPG) directly establishes the temporal features of midshipman vocalizations. VPG activity is therefore predictive of natural calls, and ‘fictive calls’ can be elicited by electrical microstimulation of the VPG. Prior studies show that intramuscular estradiol injection rapidly (within 5 min) increases fictive call duration in midshipman. Here, we delivered opioid antagonists near the VPG prior to estradiol injection. Rapid estradiol actions on fictive calling were completely suppressed by the broad-spectrum opioid antagonist naloxone and the mu-opioid antagonist beta-funaltrexamine, but were unaffected by the kappa-opioid antagonist nor-binaltorphimine. Unexpectedly, prior to estradiol administration, all three opioid antagonists caused immediate, transient reductions in fictive call duration. Together, our results indicate that: (1) vocal activity is modulated by opioidergic networks, confirming hypotheses from birds and mammals, and (2) the rapid actions of estradiol on vocal patterning depend on interactions with a mu-opioid modulatory network.

Distribution of androgen receptor mRNA expression in vocal, auditory, and neuroendocrine circuits in a teleost fish

Across all major vertebrate groups, androgen receptors (ARs) have been identified in neural circuits that shape reproductive-related behaviors, including vocalization. The vocal control network of teleost fishes presents an archetypal example of how a vertebrate nervous system produces social, context-dependent sounds. We cloned a partial cDNA of AR that was used to generate specific probes to localize AR expression throughout the central nervous system of the vocal plainfin midshipman fish (Porichthys notatus). In the forebrain, AR mRNA is abundant in proposed homologs of the mammalian striatum and amygdala, and in anterior and posterior parvocellular and magnocellular nuclei of the preoptic area, nucleus preglomerulosus, and posterior, ventral and anterior tuberal nuclei of the hypothalamus. Many of these nuclei are part of the known vocal and auditory circuitry in midshipman. The midbrain periaqueductal gray, an essential link between forebrain and hindbrain vocal circuitry, and the lateral line recipient nucleus medialis in the rostral hindbrain also express abundant AR mRNA. In the caudal hindbrain-spinal vocal circuit, high AR mRNA is found in the vocal prepacemaker nucleus and along the dorsal periphery of the vocal motor nucleus congruent with the known pattern of expression of aromatase-containing glial cells. Additionally, abundant AR mRNA expression is shown for the first time in the inner ear of a vertebrate. The distribution of AR mRNA strongly supports the role of androgens as modulators of behaviorally defined vocal, auditory, and neuroendocrine circuits in teleost fish and vertebrates in general.

Isolation and characterization of polymorphic microsatellite loci in plainfin midshipman fish

Isolation and characterization of polymorphic microsatellite loci in plainfin midshipman fish

Seasonal Plasticity of Auditory Saccular Sensitivity in the Vocal Plainfin Midshipman Fish,Porichthys notatus

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.

Corticosteroid receptor expression in a teleost fish that displays alternative male reproductive tactics

Corticosteroid signaling mechanisms mediate a wide range of adaptive physiological responses, including those essential to reproduction. Here, we investigated the presence and relative abundance of corticosteroid receptors during the breeding season in the plainfin midshipman fish ( Porichthys notatus), a species that has two male reproductive morphs. Only type I “singing” males acoustically court females and aggressively defend a nest site, whereas type II “sneaker” males steal fertilizations from nesting type I males. Cloning and sequencing first identified glucocorticoid (GR) and mineralocorticoid (MR) receptors in midshipman that exhibited high sequence identity with other vertebrate GRs and MRs. Absolute-quantitative real-time PCR then revealed higher levels of GR in the central nervous system (CNS) of type II males than type I males and females, while GR levels in the sound-producing, vocal muscle and the liver were higher in type I males than type II males and females. MR expression was also greater in the CNS of type II males than type I males or females, but the differences were more modest in magnitude. Lastly, plasma levels of cortisol, the main glucocorticoid in teleosts, were 2- to 3-fold greater in type II males compared to type I males. Together, the results suggest a link between corticosteroid regulation and physiological and behavioral variation in a teleost fish that displays male alternative reproductive tactics.

Sound source localization by the plainfin midshipman fish, Porichthys notatus.

Sound source localization by the plainfin midshipman fish, <i>Porichthys notatus</i>.

Ontogeny of auditory saccular tuning in the plainfin midshipman fish, Porichthys notatus.

Sensory systems are important throughout an animal’s life history, allowing it to detect and respond to biologically relevant stimuli important for survival and reproduction. The auditory system of the plainfin midshipman fish (Porichthys notatus) plays an important sensory receiving role for encoding vocal‐acoustic communication signals produced by adults, but the response properties and function of this receiver system during ontogeny are less understood. Here, we examine the response properties of evoked saccular potentials in two size classes of juveniles [small = 1.9–3.0 cm standard length (SL) and large = 5.0–8.0 cm SL] and in nonreproductive adults (> 9.0 cm SL) to determine the auditory sensitivity of saccular hair cells during ontogeny. Saccular potentials, maximally evoked at twice the stimulus frequency, were recorded in vivo using a lock‐in amplifier while playing pure tone stimuli via an underwater speaker. Results indicate an ontogenetic retention of saccular tuning sensitivity with size/age with peak sensitivity ranging from 75 Hz (lowest frequency tested) to 185 Hz. In addition, maximum detectable frequency of the saccule also increased with size/age. These results suggest that the midshipman saccule is best suited to detect low frequency components (< 105 Hz) of conspecific vocalizations throughout ontogeny.

Adaptive hearing in the vocal plainfin midshipman fish: getting in tune for the breeding season and implications for acoustic communication

The plainfin midshipman fish (Porichthys notatus Girard, 1854) is a vocal species of batrachoidid fish that generates acoustic signals for intraspecific communication during social and reproductive activity and has become a good model for investigating the neural and endocrine mechanisms of vocal-acoustic communication. Reproductively active female plainfin midshipman fish use their auditory sense to detect and locate "singing" males, which produce a multiharmonic advertisement call to attract females for spawning. The seasonal onset of male advertisement calling in the midshipman fish coincides with an increase in the range of frequency sensitivity of the female's inner ear saccule, the main organ of hearing, thus leading to enhanced encoding of the dominant frequency components of male advertisement calls. Non-reproductive females treated with either testosterone or 17β-estradiol exhibit a dramatic increase in the inner ear's frequency sensitivity that mimics the reproductive female's auditory phenotype and leads to an increased detection of the male's advertisement call. This novel form of auditory plasticity provides an adaptable mechanism that enhances coupling between sender and receiver in vocal communication. This review focuses on recent evidence for seasonal reproductive-state and steroid-dependent plasticity of auditory frequency sensitivity in the peripheral auditory system of the midshipman fish. The potential steroid-dependent mechanism(s) that lead to this novel form of auditory and behavioral plasticity are also discussed.

Steroid-dependent auditory plasticity for the enhancement of acoustic communication: Recent insights from a vocal teleost fish

The vocal plainfin midshipman fish ( Porichthys notatus) has become an excellent model for identifying neural mechanisms of auditory perception that may be shared by all vertebrates. Recent neuroethological studies of the midshipman fish have yielded strong evidence for the steroid-dependent modulation of hearing sensitivity that leads to enhanced coupling of sender and receiver in this vocal-acoustic communication system. Previous work shows that non-reproductive females treated with either testosterone or 17β-estradiol exhibit an increase in the degree of temporal encoding by the auditory saccular afferents to the dominant frequency content of male vocalizations produced during social-reproductive behaviors. The expanded frequency sensitivity of steroid treated females mimics the reproductive female’s auditory phenotype and is proposed to improve the detection and localization of calling conspecific mates during the summer breeding season. This review focuses on the novel form of steroid-dependent auditory plasticity that is found in the adult midshipman fish and its association with the reproductive biology and behavior of this species. Evidence for midshipman reproductive-state and steroid-dependent auditory plasticity is reviewed and the potential mechanisms that lead to this novel form of adaptive plasticity are discussed.

Sound source localization by the plainfin midshipman fish (Porichthys notatus).

Sound source localization of the midshipman fish (Porichthys notatus) was studied using the phonotactic response of gravid females to synthetic advertisement calls. Playback experiments were conducted in a 12‐ft‐diameter outdoor concrete tank at the Bodega Marine Laboratory using a J‐9 transducer placed at the center of the tank. The sound field in the tank was measured at 5‐cm intervals using an eight‐hydrophone array to measure the pressure gradients from which particle motion vectors were calculated. The acoustic measurements confirmed that the J‐9 projector was operating as a monopole source. Animals were released 90 cm away from the sound source, and 60 positive phonotactic responses from naïve gravid females were video taped and analyzed. The phonotactic responses consisted primarily of straight to somewhat curved tracks to the sound source. Abrupt changes in trajectory to the sound source were rarely observed. The results confirm that fish can locate sound sources in the near field.

Saccular potentials of the vocal plainfin midshipman fish, Porichthys notatus

The plainfin midshipman fish, Porichthys notatus, is a vocal species of teleost fish that generates acoustic signals for intraspecific communication during social and reproductive behaviors. All adult morphs (females and males) produce single short duration grunts important for agonistic encounters, but only nesting males produce trains of grunts and growls in agonistic contexts and long duration multiharmonic advertisement calls to attract gravid females for spawning. The midshipman fish uses the saccule as the main acoustic endorgan for hearing to detect and locate vocalizing conspecifics. Here, I examined the response properties of evoked potentials from the midshipman saccule to determine the frequency response and auditory threshold sensitivity of saccular hair cells to behaviorally-relevant single tone stimuli. Saccular potentials were recorded from the rostral, medial and caudal regions of the saccule while sound was presented by an underwater speaker. Saccular potentials of the midshipman, like other teleosts, were evoked greatest at a frequency that was twice the stimulus frequency. Results indicate that midshipman saccular hair cells of non-reproductive adults had a peak frequency sensitivity that ranged from 75 (lowest frequency tested) to 145 Hz and were best suited to detect the low frequency components (<or=105 Hz) of midshipman vocalizations.

Seasonal variation in the frequency response of the ear: Implications for communication

Seasonal variation in vocal‐acoustic behavior is well known among nonmammalian vertebrates; however, studies of the neural mechanisms underlying such seasonal variation have focused mainly on the anatomical rather than the neurophysiological correlates of seasonal reproductive periodicity. In this talk, I present the neurophysiological evidence for seasonal variation in the frequency response of the ear in the plainfin midshipman fish (Porichthys notatus). Vocal communication is essential to the reproductive success of the seasonally breeding midshipman fish, which migrates during the late spring and summer from deep ocean sites into the shallow intertidal zone to breed. Female midshipman fish use the auditory sense to detect and locate males that are singing from their nests. The seasonal onset of male mate calling in the midshipman fish coincides with a dramatic increase in the range of frequency sensitivity of the female’s saccule, the midshipman’s main organ of hearing, thus leading to increased encoding of the male’s mate call. I will present evidence for a steroid‐dependent mechanism that leads to this form of auditory plasticity and discuss why this plasticity of peripheral auditory frequency sensitivity may represent an adaptation to enhance the acquisition of auditory information needed for mate identification and localization during the breeding season.

Dimorphic male midshipman fish: reduced sexual selection or sexual selection for reduced characters?

In most taxa with male dimorphisms, some males are large in body size with exaggerated secondary (exaggerated morph), whereas other males in the same population are small and have reduced secondary (reduced morph). What selective pressures cause male dimorphisms? Reduced morphologies may result when a) some males develop a morphology that, in the absence of selection pressures for an exaggerated morphology, reduces energetic and developmental costs and/or b) some males opt for an alternative morphology that does well at an alternative behavioral tactic such as cuckoldry. The 2 mechanisms could act together, but each alone is theoretically sufficient to drive dimorphisms. Here, we tested hypothesis b (sexual selection for reduced characters) in the plainfin midshipman fish, Porichthys notatus. Behavioral plasticity between territoriality and cuckoldry in an exaggerated male morph (type I) allows for a direct comparison of cuckoldry by exaggerated morph males to cuckoldry by reduced morph (type II) males. Compared with type I cuckolders, type II cuckolders were able to remain near the nest for longer periods before being chased by the territorial type I male, suggesting that the reduced type II morphology allows type II males to prolong the time before attack by territorial males. Combined with other studies showing a role of selection in maintaining the exaggerated morph, the data support the sexual selection for reduced characters hypothesis and elucidate how selection can act in different ways on different males to maintain 2 male morphologies within a single species. Copyright 2006.

Ontogenetic changes in the response properties of individual, primary auditory afferents in the vocal plainfin midshipman fish Porichthys notatus Girard

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.

Seasonal variation of steroid hormone levels in an intertidal-nesting fish, the vocal plainfin midshipman

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.

Filial cannibalism improves survival and development of beaugregory damselfish embryos

Cannibalism of small numbers of offspring by a parent has been proposed as an adaptive parental strategy, by providing energy to support parental care. However, there are few empirical studies to support this hypothesis. We conducted field and laboratory experiments to investigate partial filial cannibalism in Stegastes leucostictus, a coral reef fish with paternal care. Partial cannibalism was shown to be common, and males were found to remove developing embryos from throughout a clutch in a random pattern, rather than in the more aggregated pattern seen during embryo predation. Males that received a diet supplement grew faster than control males, but did not engage in less cannibalism. Also, males did not concentrate cannibalism on early embryonic stages with the highest energetic value. Experimental reduction of embryo densities was found to significantly increase embryo development rate and survival from egg deposition to hatching, and experimental reduction of oxygen levels significantly increased rates of partial filial cannibalism by males. Artificial spawning sites with low oxygen levels were avoided by spawning females, and cannibalism rates by males were higher. We propose that partial filial cannibalism serves as an adaptive parental strategy to low oxygen levels in S. leucostictus by increasing the hatching success of embryos.