Hormonal basis for sexual dimorphism of the sound-producing apparatus of the oyster toadfish

doi:10.1016/0014-4886(86)90081-6

Experimental Neurology

Volume 92, Issue 2, May 1986, Pages 289-298

https://doi.org/10.1016/0014-4886(86)90081-6 Get rights and content

Abstract

We investigated the endocrine basis for sexual dimorphism of the sound-producing apparatus (swimbladder and attached sonic muscles) in the oyster toadfish Opsanus tau by implanting steroid pellets in gonadectomized females and males. In females, testosterone and dihydrotestosterone caused, respectively, 32.3 and 31.5% increase (P < 0.0001), and estradiol 17 β caused 11.3% increase (P < 0.0104) in swimbladder weight compared with controls. In males, testosterone caused 17.7% (P < 0.028), dihydrotestosterone 24.0% (P < 0.0008), and estradiol 10.8% (N.S.) increase from controls. Swimbladder weight gains occurred despite the fact that these fish refused food and did not gain weight. In a final experiment on fed females, testosterone and 11-ketotestosterone caused a similar increase (16.6 and 18.9%, respectively) compared with controls. These results indicate that swimbladders in adults of both sexes retain the ability to respond to steroid treatments and suggest that sexual differences in bladder size are controlled without a critical period by hormonal concentrations within the fish.

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Cited by (33)

Ontogeny of the swim bladder of the Plainfin Midshipman, Porichthys notatus (Percomorphacea: Batrachoidiformes)
2023, Zoology
The batracoidid Plainfin Midshipmen Porichthys notatus Girard has been extensively studied due to the sound production abilities and specializations of its swim bladder. The present study describes three-dimensional variations of the morphology of the swim bladder and sonic muscles of P. notatus during its post-hatch larval development, with the use of three-dimensional computed tomography. This study also includes descriptions of the relative position of the swim bladder to other visceral organs. The swim bladder, digestive tract, and liver were already present in the smallest examined specimens (5.9 mm; newly hatched larvae) along with the yolk sac. In the smallest specimens, the digestive tract is straight, but from 7.1 mm TL, the digestive tract forms the first intestinal loops, and at 25.5 mm TL, a second intestinal loop. In smallest specimens, the swim bladder is oval, but at 7.1 mm TL, the anterior margin starts invaginating, forming a pair of anterior lobes. The first appearance of the intrinsic sonic muscles in swim bladder occurs at 13.1 mm TL. Additionally, we provide comparisons between the shape of the swim bladder of P. notatus and other species. The shape of the swim bladder of P. notatus and other members of Porichthyinae have an ovoid posterior region with two anterior lobes and differs from the cordiform or semiconected/bilobed the swim bladders observed in the other Batrachoididae.
Acoustic modulation of reproductive hormones in the blacktail shiner, Cyprinella venusta, a soniferous cyprinid
2022, Animal Behaviour
Animal communication networks consist of multisensory signals and often include an acoustic element. Many freshwater fishes, including the blacktail shiner, Cyprinella venusta, produce specific vocalizations during courtship and agonistic behaviours. Similar to other vocal taxa, fish communication networks are vulnerable to noise pollution. The dominant frequencies of anthropogenic noise often overlap spectrally with animal acoustic signals. To investigate the role of acoustic signalling in breeding soniferous fishes in a physiological context, we conducted a series of acoustic playback trials. We measured waterborne levels of oestradiol (E2) and prostaglandin F2_α (PGF2_α) in gravid females exposed to courtship calls, and levels of 11-ketotestosterone (11KT) in males exposed to agonistic calls. In a separate series of trials, we exposed individuals to calls masked with bridge traffic noise. Hormone levels were quantified using enzyme-linked immunosorbent assays (ELISA) and analysed using repeated measures ANOVAs. Gravid females exhibited a significant drop in E2 (P = 0.023) and an increase in PGF2_α during courtship calls (P = 0.01). Our research suggests that growl signals contribute to the onset of spawning behaviours in female C. venusta and this response may be dampened by anthropogenic noise pollution.
Calling activity and calls' temporal features inform about fish reproductive condition and spawning in three cultured Sciaenidae species
2020, Aquaculture
Citation Excerpt :
Variations in component proportions can provide to the muscle different kinds of performances that are mutually exclusive (Rome and Lindstedt, 1998). Androgens are known to stimulate sonic muscle hypertrophy in various fish species sharing the forced response model sound production mechanism (Fine and Pennypacker, 1986; Brantley et al., 1993; Connaughton and Taylor, 1995; Connaughton et al., 1997; Rowe and Hutchings, 2004; Rowe et al., 2004; Parmentier and Fine, 2016). Treatment of spermiating males of various fishes with GnRHa resulted in rapid increases in the major fish androgens (testosterone and 11-ketotestosterone), concomitantly to increases in sperm production (Mylonas et al., 1997; Mañanos et al., 2002; Mylonas et al., 2017).
Although many fish species are vocal, the use of fish sounds for aquaculture management and wild population protection has not received much attention. In this study, sound production of three members of the Sciaenidae family was monitored before and during spawning in aquaculture facilities. The species examined include the meagre Argyrosomus regius, the shi dum Umbrina cirrosa and red drum Sciaenops ocellatus. Red drum reproduces spontaneously in captivity, whereas shi drum and meagre often require hormonal stimulation using gonadotropin releasing hormone agonist (GnRHa) for the induction of oocyte maturation, ovulation and spawning. In all three species, a clear increase in calling activity was detected during spawning nights, when longer sounds with a higher number of faster repeated pulses were emitted. Changes of call temporal features could be related to histological changes in the sonic muscles. After GnRHa treatment and during spawning, meagre sonic fibres were wider and the ratio of sarcoplasmic reticulum to myofibril cross-sectional area was higher. The correlation of calling activity with spawning events opens up the possibility of using the monitoring of calling activity and of call temporal features as tools for evaluating the reproductive state of different sciaenid species, both in the wild and captivity.
Agonistic sounds signal male quality in the Lusitanian toadfish
2015, Physiology and Behavior
Citation Excerpt :
Sonic muscle features are androgen dependent. Sonic muscle mass, morphological and physiological traits adapted for rapid contraction are driven seasonally by androgens in batrachoidids and other vocal fish, paralleling the increased vocal activity in the breeding season (e.g. [39–42]). For example, androgens drive an increase of mitochondria-filled sarcoplasm in sonic muscles necessary for sustained aerobic activity of muscle contraction [39] that is key to reproductive success [17].
Acoustic communication during agonistic behaviour is widespread in fishes. Yet, compared to other taxa, little is known on the information content of fish agonistic calls and their effect on territorial defence. Lusitanian toadfish males (Halobatrachus didactylus) are highly territorial during the breeding season and use sounds (boatwhistles, BW) to defend nests from intruders. BW present most energy in either the fundamental frequency, set by the contraction rate of the sonic muscles attached to the swimbladder, or in the harmonics, which are multiples of the fundamental frequency. Here we investigated if temporal and spectral features of BW produced during territorial defence reflect aspects of male quality that may be important in resolving disputes. We found that higher mean pulse period (i.e. lower fundamental frequency) reflected higher levels of 11-ketotestosterone (11KT), the main teleost androgen which, in turn, was significantly related with male condition (relative body mass and glycogen content). BW dominant harmonic mean and variability decreased with sonic muscle lipid content. We found no association between BW duration and male quality. Taken together, these results suggest that the spectral content of fish agonistic sounds may signal male features that are key in fight outcome.
Neuroendocrine control of seasonal plasticity in the auditory and vocal systems of fish
2015, Frontiers in Neuroendocrinology
Citation Excerpt :
Following playbacks of dolphin calls known as pops that have a frequency content overlapping the hearing range of toadfish, there was a significant reduction in the number, but not the duration, of boatwhistle calls by males that was paralleled by significantly elevated plasma cortisol levels. Several studies have documented the effects of androgens on vocal muscle mass (e.g., Brantley et al., 1993; Connaughton and Taylor, 1995; Fine and Pennypacker, 1986; Lee and Bass, 2005 consistent with seasonal shifts in circulating androgen levels and sonic muscle mass (e.g., Sisneros et al., 2009; Nguyen et al., 2008; Walsh et al., 1995). Most recently, Genova et al. (2013) investigated molecular mechanisms that might be mediating the effects of steroids on vocal muscle function by comparing the abundance of mRNA transcripts coding for different receptors and enzymes involved in steroid signaling pathways between advertisement calling (“humming”) and non-calling type I male midshipman.
Seasonal changes in reproductive-related vocal behavior are widespread among fishes. This review highlights recent studies of the vocal plainfin midshipman fish, Porichthys notatus, a neuroethological model system used for the past two decades to explore neural and endocrine mechanisms of vocal-acoustic social behaviors shared with tetrapods. Integrative approaches combining behavior, neurophysiology, neuropharmacology, neuroanatomy, and gene expression methodologies have taken advantage of simple, stereotyped and easily quantifiable behaviors controlled by discrete neural networks in this model system to enable discoveries such as the first demonstration of adaptive seasonal plasticity in the auditory periphery of a vertebrate as well as rapid steroid and neuropeptide effects on vocal physiology and behavior. This simple model system has now revealed cellular and molecular mechanisms underlying seasonal and steroid-driven auditory and vocal plasticity in the vertebrate brain.
Individual, temporal, and population-level variations in circulating 11-ketotestosterone and 17β-estradiol concentrations in the oyster toadfish Opsanus tau
2009, Comparative Biochemistry and Physiology - A Molecular and Integrative Physiology
Sex steroid hormones are important for reproduction in all vertebrates, but few studies examine inter-individual, temporal, and population-level variations, as well as environmental influences on circulating steroid levels within the same species. In this study we analyzed plasma 11-ketotoestosterone (11-KT) and 17β-estradiol (E₂) levels in the oyster toadfish to test for 1) individual and temporal variations by serially sampling the same individuals during the reproductive and post-reproductive period, 2) variations in steroid levels among toadfish obtained from different sources or maintained under different holding conditions, and 3) correlations with environmental parameters. Results from serial sampling showed marked inter-individual variations in male 11-KT levels in two separate groups of toadfish, but no temporal differences from June to September. Females also showed inter-individual variations in E₂ concentrations, but most had elevated levels late in the reproductive season coincident with oocyte growth prior to winter quiescence. E₂ concentration, but not 11-KT, was positively correlated with water temperature, and negatively correlated with daylength and lunar phase. Maricultured toadfish held under constant conditions had elevated levels of E₂ and 11-KT that should be considered when using these fish for experimentation. This study provides important comparative information on the relationship between individual variations in steroid levels, and how they relate to physiological and environmental correlates in a model marine teleost.

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¹: We thank Dr. Jennifer Stewart for reviewing the manuscript, Gary Hill for procuring toadfish, and Kathleen A. Drummond for technical assistance. Supported by Virginia Commonwealth University Biomedical Grant-in-Aid and National Institutes of Health grant MH38921. Contribution 1292 from the Virginia Institute of Marine Science, The College of William and Mary.

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Hormonal basis for sexual dimorphism of the sound-producing apparatus of the oyster toadfish

Abstract

Brain Res.

Horm. Behav.

J. Exp. Mar. Biol. Ecol.

Dev. Biol.

Gen. Comp. Endocrinol.

Testosterone increases acetylcholine receptor number in the levator ani muscle of the rat

J. Neurobiol.

Hormonal control of a developing neuromuscular system. I. Complete demasculinization of the male rat spinal nucleus of the bulbocavernosus using the anti-androgen flutamide

J. Neurosci.

Central and peripheral mechanisms of teleost sound production

Am. Zool.

The sarcoplasmic reticulum of a fast-acting fish muscle

J. Biophys. Biochem. Cytol.

Sexual dimorphism of the growth rate of the swimbladder of the oyster toadfish Opsanus tau

Copeia

Seasonal and geographical variation of the mating call of the oyster toadfish Opsanus tau L

Oecologia

Sounds evoked by brain stimulation in the oyster toadfish Opsanus tau

Exp. Brain Res.

Ontogeny and sexual dimorphism of the sonic motor nucleus in the oyster toadfish

J. Comp. Neurol.

Testosterone uptake in the brainstem of a sound producing fish

Science

Communication in fishes