Functional morphology of the sonic apparatus in Ophidion barbatum (Teleostei, Ophidiidae)

Most soniferous fishes producing sounds with their swimbladder utilize relatively simple mechanisms: contraction and relaxation of a unique pair of sonic muscles cause rapid movements of the swimbladder resulting in sound production. Here we describe the sonic mechanism for Ophidion barbatum, which includes three pairs of sonic muscles, highly transformed vertebral centra and ribs, a neural arch that pivots and a swimbladder whose anterior end is modified into a bony structure, the rocker bone. The ventral and intermediate muscles cause the rocker bone to swivel inward, compressing the swimbladder, and this action is antagonized by the dorsal muscle. Unlike other sonic systems in which the muscle contraction rate determines sound fundamental frequency, we hypothesize that slow contraction of these antagonistic muscles produces a series of cycles of swimbladder vibration.     

Modifications in call characteristics and sonic apparatus morphology during puberty in Ophidion rochei (actinopterygii: Ophidiidae)

Juveniles, females, and males of Ophidion rochei share similar external morphology, probably because they are mainly active in the dark, which reduces the role of visual cues. Their internal sonic apparatuses, however, are complex: three pairs of sonic muscles, and highly modified vertebrae and ribs are involved in sound production. The sonic apparatus of males differs from juveniles and females in having larger swimbladder plates (modified ribs associate with the swimbladder wall) and sonic muscles, a modified swimbladder shape and a mineralized structure called the “rocker bone” in front of the swimbladder. All of these male traits appear at the onset of sexual maturation. This article investigates the relationship between morphology and sounds in male O. rochei of different sizes. Despite their small size range total length (133–170 mm TL), the five specimens showed pronounced differences in sound‐production apparatus morphology, especially in terms of swimbladder shape and rocker bone development. This observation was reinforced by the positive allometry measured for the rocker bone and the internal tube of the swimbladder. The differences in morphology were related to marked differences in sound characteristics (especially frequency and pulse duration). These results suggest that male calls carry information about the degree of maturity. Deprived of most visual cues, ophidiids probably have invested in other mechanisms to recognize and distinguish among individual conspecifics and between ophidiid species. As a result, their phenotypes are externally similar but internally very different. In these taxa, the great variability of the sound production apparatus means this complex system is a main target of environmental constraints. J. Morphol. 275:650–660, 2014. © 2014 Wiley Periodicals, Inc.     

An Intermediate in the evolution of superfast sonic muscles

Background

Intermediate forms in the evolution of new adaptations such as transitions from water to land and the evolution of flight are often poorly understood. Similarly, the evolution of superfast sonic muscles in fishes, often considered the fastest muscles in vertebrates, has been a mystery because slow bladder movement does not generate sound. Slow muscles that stretch the swimbladder and then produce sound during recoil have recently been discovered in ophidiiform fishes. Here we describe the disturbance call (produced when fish are held) and sonic mechanism in an unrelated perciform pearl perch (Glaucosomatidae) that represents an intermediate condition in the evolution of super-fast sonic muscles.

Results

The pearl perch disturbance call is a two-part sound produced by a fast sonic muscle that rapidly stretches the bladder and an antagonistic tendon-smooth muscle combination (part 1) causing the tendon and bladder to snap back (part 2) generating a higher-frequency and greater-amplitude pulse. The smooth muscle is confirmed by electron microscopy and protein analysis. To our knowledge smooth muscle attachment to a tendon is unknown in animals.

Conclusion

The pearl perch, an advanced perciform teleost unrelated to ophidiiform fishes, uses a slow type mechanism to produce the major portion of the sound pulse during recoil, but the swimbladder is stretched by a fast muscle. Similarities between the two unrelated lineages, suggest independent and convergent evolution of sonic muscles and indicate intermediate forms in the evolution of superfast muscles.     

Movement and sound generation by the toadfish swimbladder

Although sound-producing (sonic) muscles attached to fish swimbladders are the fastest known vertebrate muscles, the functional requirement for such extreme speed has never been addressed. We measured movement of the swimbladder caused by sonic muscle stimulation in the oyster toadfish Opsanus tau and related it to major features of the sound waveform. The movement pattern is complex and produces sound inefficiently because the sides and bottom of the bladder move in opposite in and out directions, and both movement and sound decay rapidly. Sound amplitude is related to speed of swimbladder movement, and slow movements do not produce perceptible sound. Peak sound amplitude overlaps fundamental frequencies of the male's mating call because of muscle mechanics and not the natural frequency of the bladder. These findings suggest that rapid muscle speed evolved to generate sound from an inefficient highly damped system.     

Acoustic behaviour of Abudefduf luridus

Adult males Abudefduf luridus produced sounds during aggressive interactions, although not all aggressive interactions were associated with sounds. Such sounds were always related to characteristic swimming movements during an aggressive display or territorial defence. The sound was a combination of several sonic pulses, with most energy concentrated towards the low end of the spectrum (from <50 to 800 Hz), and was most frequently groups of two pulses. Analysis of the pulse structure suggested that these sounds are produced by muscles acting on the swimbladder. However, the mechanism of sound production has yet to be demonstrated. Sounds were emitted throughout the 24-h period with increased activity at sunrise and sunset.     

Seasonal variation in sonic muscles in the fawn cusk-eel Lepophidium profundorum

The fawn cusk-eel Lepophidium profundorum (Ophidiidae) has an unusual sound-producing system with sexually dimorphic sets of antagonistic muscles. Outside the mating season, the dorsal and ventral muscles are well developed and larger in males than in females, but the tiny intermediate muscles are smaller, suggesting a minor role, if any, in male advertisement call production. We examined summer individuals with more developed gonads and find a fourfold hypertrophy of the intermediate but not the other muscles. This result suggests androgen dependence and an important role in sound production for the intermediate muscle. Even though both sexes gain weight in the summer, the ventral and dorsal muscles in females lose weight, suggesting that sound production is less important in females and that muscle mass may be used to support egg growth.     

Sound production by a recoiling system in the pempheridae and terapontidae

Sound‐producing mechanisms in fishes are extraordinarily diversified. We report here original mechanisms of three species from two families: the pempherid Pempheris oualensis, and the terapontids Terapon jarbua and Pelates quadrilineatus. All sonic mechanisms are built on the same structures. The rostral part of the swimbladder is connected to a pair of large sonic muscles from the head whereas the posterior part is fused with bony widenings of vertebral bodies. Two bladder regions are separated by a stretchable fenestra that allows forward extension of the anterior bladder during muscle contraction. A recoiling apparatus runs between the inner face of the anterior swimbladder and a vertebral body expansion. The elastic nature of the recoiling apparatus supports its role in helping the swimbladder to recover its initial position during sonic muscle relaxation. This system should aid fast contraction (between 100 and 250Hz) of sonic muscles. There are many differences between species in terms of the swimbladder and its attachments to the vertebral column, muscle origins, and morphology of the recoiling apparatus. The recoiling apparatus found in the phylogenetically‐related families (Glaucosomatidae, Pempheridae, Terapontidae) could indicate a new character within the Percomorpharia. J. Morphol. 277:717–724, 2016. © 2016 Wiley Periodicals, Inc.     

COMPARATIVE ANALYSIS OF SWIMBLADDER (DRUMMING) AND PECTORAL (STRIDULATION) SOUNDS IN THREE FAMILIES OF CATFISHES

ABSTRACT

Among teleosts, only representatives of several tropical catfish families have evolved two sonic organs: pectoral spines for stridulation and swimbladder drumming muscles. Pectoral mechanisms differ in relative size between pimelodids, mochokids and doradids, whereas swimbladder mechanisms exhibit differences in origin and insertion of extrinsic muscles. Differences in vocalization among families were investigated by comparing distress calls in air and underwater. High frequency broad-band pulsed sounds of similar duration were emitted during abduction of pectoral spines in all three families. Adduction sounds were similar to abduction signals in doradids, shorter and of lower sound pressure in mochokids, and totally lacking in pimelodids. Simultaneously or successively with pectoral sounds, low frequency harmonic drumming sounds were produced by representatives of two families. Drumming sounds were of similar intensity as stridulatory sounds in pimelodids, fainter in doradids, and not present in mochokids. Swimbladder sounds were frequency modulated and the fundamental frequency was similar in pimelodids and doradids. The ratio of stridulatory to drumming sound amplitude was higher in air than underwater in both doradids and one of the pimelodids. Also, overall duration of pectoral sounds, compared to swimbladder sounds, was longer in air than underwater in one doradid and pimelodid species. This first comparison of vocalization within one major teleost order demonstrates a wide variation in occurrence, duration, intensity and spectral content of sounds and indicates family- and species-specific as well as context- (receiver-) dependent patterns of vocalization.     

Sound production evoked by electrical stimulation of the forebrain in the oyster toadfish

In mammals, birds and amphibians the neural pathways controlling sound production descend from higher centers in the forebrain, whereas in fishes only brainstem and spinal centers have been explicitly implicated in sound production. We now report that electrical stimulation of the forebrain of the oyster toadfish (Opsanus tau) readily evokes both the agonistic grunt and the courtship boatwhistle. Boatwhistles are more realistic than ones previously evoked from lower centers. Positive stimulation sites are localized in the preoptic area (nucleus preopticus parvocellularis anterior) and the supracommissural nucleus of the ventral telencephalon, a likely homologue of the amygdala. Both sites contain gonadal steroid-concentrating neurons and play a central role in fish courtship behavior. Evoked sounds form a continuum from knock grunts, burst grunts, transition boatwhistles to complete boatwhistles; sound pressure level (SPL), fundamental frequency and duration increase consistently within the continuum. For all sound types, SPLs exhibit the smallest variation (coefficients of variation of 2.7 to 5.7%), fundamental frequency is intermediate (5 to 13%) and durations vary most widely (18 to 60%). Boatwhistles, with the smallest variation and greatest amplitude, are likely generated by a maximal output of the CNS and sonic muscles. Grunt SPLs however, vary over a range of 26 dB for all fish and by as much as 18 dB in an individual, suggesting recruitment of variable numbers of motor units despite electrical coupling within the sonic motor nucleus.Abbreviations AC anterior commissure - CNS central nervous system - DHT dihydrotestosterone - Dm medial nucleus of dorsal telenecphalon - DTAM dorsal tegmental area of medulla - E estrogen - HRP horseradish peroxidase - PM nucleus praeopticus magnocellularis - POA preoptic area - PPa nucleus praeopticus parvocellularis anterior - SMA sonic motor area - SMN sonic motor nucleus - SPL sound pressure level - T testosterone - VS supracommissural nucleus of ventral telencephalon - Vv ventral nucleus of ventral telencephalon     

Sound-producing mechanisms and recordings in<Emphasis Type="Italic"> Carapini</Emphasis> species (Teleostei,Pisces)

Carapus boraborensis, C. homei and Encheliophis gracilis are three species of Carapidae that display the ability to penetrate and reside in the holothurian Bohadschia argus. This study describes both the particular morphology of the sound-producing structures and, for the first time, the sounds produced by each species. The study of the structures composing the sound-producing system seems to indicate that the action made by the primary sonic muscles (i.e. the pulling and releasing of the front of the swim bladder) might be responsible for the sound emissions of these three species by provoking a vibration of a thinner zone in front of the swim bladder (swimbladder fenestra). The sounds were only emitted and recorded when several individuals of the same species were inside the same sea cucumber. They were composed of serially repeated knocks and were heard as drum beats or drum rolls. Their specific differences were mainly defined as variations in the timing or grouping of the knocking sounds. The recordings of these sound productions demonstrate a vocal ability for the three species, linked with the presence of particular organs associated with sound production. Moreover, the ecological significance of the sounds and of the sound apparatus system is discussed.     

SOUND PRODUCTION BY THE LUSITANIAN TOAD FISH,HALOBATRACHUS DIDACTYLUS

ABSTRACT

Several batrachoidids have been known to produce sounds associated with courtship and agonistic interactions, and their repertoires have been studied acoustically and behaviourally. In contrast, sound production of the Lusitanian toadfish Halobatrachus didactylus, although often noted, has not been acoustically studied.

This sedentary predator of Northeastern Atlantic coastal waters is usually found in sandy and muddy substrates, under rocks or crevices. Sound recordings were made in Ria Formosa, a lagoon complex in southern Portugal. The sound producing apparatus was studied in adult individuals of both sexes captured by local fishermen.

It is shown that this species produces acoustic emissions similar to other batrachoidids. It produces a long, rhythmical, tonal sound, often in choruses, which is comparable to the boatwhistle or hum signals of Opsanus and Porichthys, and a complex of signals that were classified as grunts, croaks, double croaks and mixed calls (‘grunt-croak’). As in other toadfishes, H. didactylus presents sonic muscles connected to a bi-lobed swimbladder. Asynchronous contractions of the sonic muscles were detected when massaging the ventral surface of the fish.     

Sexual dimorphism of sonic apparatus and extreme intersexual variation of sounds in <Emphasis Type="Italic">Ophidion rochei</Emphasis> (Ophidiidae): first evidence of a tight relationship between morphology and sound characteristics in Ophidiidae

Background

Many Ophidiidae are active in dark environments and display complex sonic apparatus morphologies. However, sound recordings are scarce and little is known about acoustic communication in this family. This paper focuses on Ophidion rochei which is known to display an important sexual dimorphism in swimbladder and anterior skeleton. The aims of this study were to compare the sound producing morphology, and the resulting sounds in juveniles, females and males of O. rochei.

Results

Males, females, and juveniles possessed different morphotypes. Females and juveniles contrasted with males because they possessed dramatic differences in morphology of their sonic muscles, swimbladder, supraoccipital crest, and first vertebrae and associated ribs. Further, they lacked the ‘rocker bone’ typically found in males. Sounds from each morphotype were highly divergent. Males generally produced non harmonic, multiple-pulsed sounds that lasted for several seconds (3.5?±?1.3 s) with a pulse period of ca. 100 ms. Juvenile and female sounds were recorded for the first time in ophidiids. Female sounds were harmonic, had shorter pulse period (±3.7 ms), and never exceeded a few dozen milliseconds (18?±?11 ms). Moreover, unlike male sounds, female sounds did not have alternating long and short pulse periods. Juvenile sounds were weaker but appear to be similar to female sounds.

Conclusions

Although it is not possible to distinguish externally male from female in O. rochei, they show a sonic apparatus and sounds that are dramatically different. This difference is likely due to their nocturnal habits that may have favored the evolution of internal secondary sexual characters that help to distinguish males from females and that could facilitate mate choice by females. Moreover, the comparison of different morphotypes in this study shows that these morphological differences result from a peramorphosis that takes place during the development of the gonads.

     

Mutually exclusive muscle designs: the power output of the locomotory and sonic muscles of the oyster toadfish (Opsanus tau)

Animals perform a vast array of motor activities. Although it has generally been accepted that muscles are well suited to the function that they must perform, specialization for performing one function may compromise their ability for carrying out another. We examined this principle in the toadfish muscular system: slow-twitch red and fast-twitch white myotomal muscles are used for powering swimming at relatively low frequencies, while the superfast swimbladder muscle powers mating calls by contracting at 100 Hz. We measured muscle power output over a wide range of frequencies. The red and white locomotory muscles could not generate power over ca. 2.2 and 12 Hz, respectively and, hence, could not power sound production. In contrast, the swimbladder muscle has many specializations that permit it to generate power at frequencies in excess of 100 Hz. However, these specializations drastically reduce its power output at low frequencies: the swimbladder muscle generated only one-twentieth of the power of the red muscle and one-seventh of the power of the white muscle at the frequencies used during swimming. To generate the same total power needed for swimming would require unfeasibly large amounts of swimbladder muscle that could not fit into the fish. Hence, the designs of the swimbladder and locomotory muscles are mutually exclusive.     

Early events in myofibrillogenesis and innervation of skeletal,sound-generating muscle in a teleost fish

The plainfin midshipman, Porichthys notatus, generates acoustic communication signals through the rapid contraction of a pair of vocal (sonic) muscles attached to the walls of the swimbladder. Light and electron microscopic methods were used to study two aspects of sonic muscle ontogeny: (1) the development and transformation of myotubes into muscle fibers and (2) innervation, including the formation of sonic neuromuscular junctions and the myelination of sonic motor axons. Sonic motor axons are associated with sonic mesenchyme during its initial migration away from occipital somites. However, myofibrillogenesis, the formation of neuromuscular junctions, and axon myelination do not occur until sonic mesenchyme reaches its final destination (i.e., the swimbladder). A continuum of developing myotubes is present rather than two temporally distinct populations of primary and secondary myotubes as observed for skeletal muscles in mammalian and avian species. Potential reasons for the lack of primary and secondary myotubes are considered, including the functional homogeneity of the sonic motor system and the sonic muscle's unique architecture, namely its direct attachment to the wall of the swim-bladder. © 1993 Wiley-Liss, Inc.     

The rocker bone: a new kind of mineralised tissue?

In some Ophidiiform fishes, the anterior part of the swimbladder is thickened into a hard structure called the "rocker bone", which is thought to play a role in sound production. Although this structure has been described as cartilage or bone, its nature is still unknown. We have made a thorough analysis of the rocker bone in Ophidion barbatum and compared it with both classical bone and cartilage. The rocker bone appears to be a new example of mineralisation. It consists of (1) a ground substance mainly composed of proteoglycans (mucopolysaccharide acid) and fibres and (2) a matrix containing small mineralised spherules composed of a bioapatite and fibrils. These spherules are embedded in mineralised cement of a similar composition to the spherules themselves. The rocker bone grows via the apposition of new apatite spherules at its periphery. These spherules are first secreted by the innermost fibroblast layer of the capsule contained in the rocker bone and then grow extracellularly. Blood vessels, which represent the only means of transport for matrix and mineral material, are numerous. They enter the rocker bone via the hyle and ramify towards the capsule. We propose to call this new kind of mineralised tissue constituting the rocker bone "frigolite" (the Belgian name for styrofoam) in reference to the presence of spherules of different sizes and the peculiarity of the rocker bone in presenting a smooth surface when fractured.     

Sounds and sound production in fishes

The main information on the sounds and sound production in fishes is reviewed. The present systems of sound classification and specialized sound production in fishes with different taxonomic positions and ecology are described. The anatomy of sound generating organs is analyzed, and the mechanisms of production of different types of sounds (stridulation, drumming, cavitation, and percussion, as well as hydrodynamic, pneumatic, stringed, and respiratory sounds) are discussed. A brief characterization of the acoustic parameters of different sound types is given. Recent data on the anatomy and morphology of the sonic muscles (including their innervation, physiology, sexual dimorphism, and seasonal changes) are reviewed. The dynamics of the development of sound generating organs are described, and their capacity for sound production in the ontogeny of fishes is followed.     

Fast drum strokes: Novel and convergent features of sonic muscle ultrastructure,innervation, and motor neuron organization in the pyramid butterflyfish (hemitaurichthys polylepis)

Sound production that is mediated by intrinsic or extrinsic swim bladder musculature has evolved multiple times in teleost fishes. Sonic muscles must contract rapidly and synchronously to compress the gas‐filled bladder with sufficient velocity to produce sound. Muscle modifications that may promote rapid contraction include small fiber diameter, elaborate sarcoplasmic reticulum (SR), triads at the A–I boundary, and cores of sarcoplasm. The diversity of innervation patterns indicate that sonic muscles have independently evolved from different trunk muscle precursors. The analysis of sonic motor pathways in distantly related fishes is required to determine the relationships between sonic muscle evolution and function in acoustic signaling. We examined the ultrastructure of sonic and adjacent hypaxial muscle fibers and the distribution of sonic motor neurons in the coral reef Pyramid Butterflyfish (Chaetodontidae: Hemitaurichthys polylepis) that produces sound by contraction of extrinsic sonic muscles near the anterior swim bladder. Relative to adjacent hypaxial fibers, sonic muscle fibers were sparsely arranged among the endomysium, smaller in cross‐section, had longer sarcomeres, a more elaborate SR, wider t‐tubules, and more radially arranged myofibrils. Both sonic and non‐sonic muscle fibers possessed triads at the Z‐line, lacked sarcoplasmic cores, and had mitochondria among the myofibrils and concentrated within the peripheral sarcoplasm. Sonic muscles of this derived eutelost possess features convergent with other distant vocal taxa (other euteleosts and non‐euteleosts): small fiber diameter, a well‐developed SR, and radial myofibrils. In contrast with some sonic fishes, however, Pyramid Butterflyfish sonic muscles lack sarcoplasmic cores and A–I triads. Retrograde nerve label experiments show that sonic muscle is innervated by central and ventrolateral motor neurons associated with spinal nerves 1–3. This restricted distribution of sonic motor neurons in the spinal cord differs from many euteleosts and likely reflects the embryological origin of sonic muscles from hypaxial trunk precursors rather than occipital somites. J. Morphol., 2013. © 2012 Wiley Periodicals, Inc.     

The fastest contracting muscles of nonmammalian vertebrates express only one isoform of the ryanodine receptor.

The skeletal muscles of chickens, frogs, and fish have been reported to express two isoforms (alpha and beta) of the sarcoplasmic reticulum calcium release channel (ryanodine receptor or RYR), while mammals express only one. We have studied patterns of RYR isoform expression in skeletal muscles from a variety of fish, reptiles, and birds with immunological techniques. Immunoblot analysis with a monoclonal antibody that recognizes both nonmammalian RYR isoforms and a polyclonal antibody specific to the alpha isoform show two key results: (a) two reptilian orders share with mammals the pattern of expressing only the alpha (skeletal) RYR isoform in skeletal muscle; and (b) certain functionally specialized muscles of fish and birds express only the alpha RYR isoforms. While both isoforms are expressed in the body musculature of fish and birds, the alpha isoform is expressed alone in extraocular muscles and swimbladder muscles. The appearance of the alpha RYR isoform alone in the extraocular muscles and a fast-contracting sonic muscle in fish (toadfish swimbladder muscle) provides evidence that this isoform is selectively expressed when rapid contraction is required. The functional and phylogenetic implications of expression of the alpha isoform alone are discussed in the context of the mechanism and evolution of excitation-contraction coupling.     

Acoustic communication in two freshwater gobies: the relationship between ambient noise,hearing thresholds and sound spectrum

Two freshwater gobies Padogobius martensii and Gobius nigricans live in shallow (5-70 cm) stony streams, and males of both species produce courtship sounds. A previous study demonstrated high noise levels near waterfalls, a quiet window in the noise around 100 Hz at noisy locations, and extremely short-range propagation of noise and goby signals. To investigate the relationship of this acoustic environment to communication, we determined audiograms for both species and measured parameters of courtship sounds produced in the streams. We also deflated the swimbladder in P. martensii to determine its effect on frequency utilization in sound production and hearing. Both species are maximally sensitive at 100 Hz and produce low-frequency sounds with main energy from 70 to 100-150 Hz. Swimbladder deflation does not affect auditory threshold or dominant frequency of courtship sounds and has no or minor effects on sound amplitude. Therefore, both species utilize frequencies for hearing and sound production that fall within the low-frequency quiet region, and the equivalent relationship between auditory sensitivity and maximum ambient noise levels in both species further suggests that ambient noise shapes hearing sensitivity.     

Characterization of the primary sonic muscles in Carapus acus (Carapidae): a multidisciplinary approach

Sound production in carapid fishes results from the action of extrinsic muscles that insert into the swim bladder. Biochemical, histochemical and morphological techniques were used to examine the sonic muscles and compare them with epaxial muscles in Carapus acus. Sonic fibres are thicker than red and thinner than white epaxial fibres, and sonic fibres and myofibrils exhibit an unusual helicoidal organization: the myofibrils of the centre are in a straight line whereas they are more and more twisted towards the periphery. Sonic muscles have both features of red (numerous mitochondria, high glycogen content) and white (alkali-stable ATPase) fibres. They differ also in the isoforms of the light chain (LC3) and heavy chain (HC), in having T tubules at both the Z-line and the A-I junction and in a unique parvalbumin isoform (PAI) that may aid relaxation. All these features lead to the expression of two assumptions about sound generation: the sonic muscle should be able to perform fast and powerful contractions that provoke the forward movement of the forepart of the swim bladder and the stretching and "flapping" of the swim bladder fenestra; the helicoidal organization allows progressive drawing of the swim bladder fenestra which emits a sound when rapidly released in a spring-like manner.