My research has been devoted to neuromuscular control of sound production in toadfish, catfish, and other species along with an occasional foray into hearing. Toadfish utilize a heart shaped swim bladder and superfast muscles with small fibers and an unusual ultrastructure. Both sonic motor neurons and muscle fibers increase in size and number for multiple years, and large muscle fibers fragment and likely divide, maintaining energetic efficiency. Toadfish sonic muscles drive the swim bladder directly (a forced response), and the sound waveform parallels bladder movement. The forced response differs from traditional interpretations of swim bladders as underwater resonant bubbles. High water content in the swim bladder wall inhibits resonance by viscous damping at shallow but likely less effectively at deeper depths, suggesting both notions might apply. Catfish produce sounds with their pectoral spines by rubbing a ridged surface on the dorsal process against a rough surface on the cleithrum: a series of quick jerks produce sounds via a slip-stick mechanism. Recent discoveries on other species reveal novel adaptations for sound production and suggestions are made for future work.

I was an undergraduate zoology major at the University of Maryland and worked for Howard Winn, a pioneer in fish bioacoustics, on his oyster toadfish (Opsanus tau) playback project. George Offutt, one of Winn's graduate students, was teaching temporarily at the middle school where my mom taught English, and George told her that Winn needed an undergraduate assistant. This chance conversation affected my future.

Unsure of a narrow field, I decided to go on in marine biology and got my Master's Degree at the Virginia Institute of Marine Science (VIMS) working on pelagic Sargassum communities (Fine, 1970). At that time most biologists at VIMS were identifying and counting things, which was fine but not where my heart was. I applied to other schools, and Dr. Winn, now at the Graduate School of Oceanography of the University of Rhode Island (URI), called and said he had an NIH traineeship to work on toadfish. I signed on.

The summer before heading up to Rhode Island, I was still at VIMS. To get a head start, I examined swim bladder growth in the oyster toadfish and found that the swim bladder and sonic muscles grow larger in males, who produce courtship boatwhistle calls, rather than in females (Fine, 1975). At URI, Dr. Winn decided I should try to induce calls in the toadfish by brain stimulation although Leo Demski and Gerry Gerald had just published a paper doing that in the gulf toadfish Opsanus beta (Demski and Gerald, 1972). An oceanography school was not the best place to try this on my own, and I had troubles. Winn could not help me, but he did corner me from time to time and go over my progress (or lack thereof) in excruciating detail.

The Winn lab went on a whale cruise in the Caribbean and then flew back to New York. By chance there was a behavior conference at the American Museum of Natural History, and Leo Demski was present. Leo said he would be up north in the spring and promised to help. He watched what I was doing and made several recommendations. After that things started working. I am not sure what would have happened without Leo's visit.

Marie Fish and Bill Mowbray had an Office of Naval Research (ONR) grant that funded weekly sound recordings at multiple locations along the US East Coast (Fish and Mowbray, 1970). The tapes had been sitting on shelves in Winn's lab. I analyzed toadfish boatwhistles from a year's recordings for stations at Delaware, Virginia and South Carolina and also made multiple recordings in Narrow River, Rhode Island to factor out acute temperature effects on the calls.

The short-term recordings indicate that boatwhistle fundamental frequency increases with temperature, but the duration is unaffected. Seasonal changes are greater than short-term ones: fundamental frequency increases more rapidly than in short-term recordings during the main part of the mating season, and then fundamental frequency and duration decrease when the temperature is still warm after July (the end of the active mating season), suggesting hormonal effects on the sonic pathway (Fine, 1978b).

Additionally, there were geographical differences. Virginia calls were shorter than ones from South Carolina and Delaware. There were also geographical differences in the patterning of “following grunts” (grunts released following the termination of an electric stimulus to the brain) between Rhode Island and St Augustine, Florida toadfish (Fine, 1978a). Differences in boatwhistles north and south of the Chesapeake Bay suggested genetic drift in the origins of the different populations (Fine, 1978b). One interesting note is that initially, I heard no boatwhistles in the South Carolina recordings. Winn's sound technician Paul Perkins, a former US Navy sonar man, suggested low-pass filtering the recordings, which decreased amplitude of snapping shrimp sounds, and the previously masked boatwhistles became audible.

Brain stimulation was working routinely (Fine, 1979) when ONR had a site visit at the URI Bay Campus; they were funding Winn's humpback whale work. I saw Bernie Zahuranec in the hall, a friend from an undergraduate summer job at the US Naval Oceanographic Office, and one of the site visitors. I pulled him into the room where I had a toadfish with an electrode ready to go, pushed the trigger on the stimulators, and the fish started grunting. Bernie told Dr. Winn that I was doing great. From then on our relationship improved. Dr. Winn was asked to write the chapter on fishes for Thomas Sebeok's book Animal Communication. After some thought, he asked me if I wanted to write it with him. A couple of weeks later he said, “start writing” (Fine , 1977b).

Successful stimulation sites in both Opsanus beta and O. tau (Demski and Gerald, 1972; Fine, 1979) were restricted to the brainstem and produced grunts. Years later with Michael Perini at VCU, we sought sites in the forebrain and evoked boatwhistle-like sounds from an amygdala homolog (Vs) and the anterior preoptic area (PPa) (Fine and Perini, 1994).

Paul Yevich at the Environmental Protection Administration lab taught me basic tissue processing and let me use his lab in order to localize electrical stimulation sites. Also, thanks to Tom Finger, then a graduate student of Harvey Karten at MIT, who helped me identify structures in my first naive exposure to fish-brain anatomy. By this time I was interested in neuroscience and wrote an NIH postdoctoral proposal to work with Robert Capranica, a frog auditory neurophysiologist in the Section of Neurobiology and Behavior at Cornell, recording from the toadfish auditory nerve (Fine, 1981).

In 1979, I accepted a tenure-track position in Biology at Virginia Commonwealth University (VCU), which had a Master's program and was newly interested in research. The four original members of the Department were still there and reminded us they each used to teach classes that required 24 h every semester. Shudder! My funds to set up a lab were just enough to purchase a Zeiss surgical microscope on a copy stand, far different from what would happen today. With minimal startup funds, I decided to work on toadfish sound production, which required less equipment than auditory work. There had been a flurry of work in fish hearing and sound production in the 1960s and 1970s, and Arthur Myrberg was the major active US scientist still working on fish sound production, but in damselfish (Pomacentridae). This left the toadfish sound world neglected for a short time and allowed me to pursue questions in several areas for the first time.

An early project at VCU, with Marty Lenhardt in Otolaryngology at the medical school, was to investigate boatwhistle transmission in shallow water where toadfish commonly nest (Fine and Lenhardt, 1983). Boatwhistle recordings and low-frequency tone bursts played through a J9 sound projector in the York River, VA, attenuated rapidly in depths of about a meter, and only the fundamental frequency of a boatwhistle was barely visible on a sonogram at a distance of 5 m (Fig. 1).

FIG. 1.

A toadfish boatwhistle played through a J9 sound projector recorded at 1 m intervals in water of about 1 m in depth in the York River, VA. Reprinted from Comparative Biochemistry and Physiology Part A: Physiology, 76, Fine, M. L., and Lenhardt, M. L., “Shallow-water propagation of the toadfish mating call,” 225-231, Copyright 1983, with permission from Elsevier.

FIG. 1.

A toadfish boatwhistle played through a J9 sound projector recorded at 1 m intervals in water of about 1 m in depth in the York River, VA. Reprinted from Comparative Biochemistry and Physiology Part A: Physiology, 76, Fine, M. L., and Lenhardt, M. L., “Shallow-water propagation of the toadfish mating call,” 225-231, Copyright 1983, with permission from Elsevier.

Close modal

Assuming cylindrical spreading (transmission loss of 10 log r or 3 dB/distance doubled), absorption loss was calculated as 3–9 dB/m in various transects. Sound propagates over long distances in deep water, and fish sounds were assumed to be audible over long distances as well. However, owing to the long wavelength of low frequency sound (a 100 Hz tone underwater would have a 15 m wavelength), low frequencies attenuate rapidly in extremely shallow water (Urick, 1975; Rogers and Cox, 1988). Later, working with Marco Lugli from Italy, we found that in shallow rock-lined streams, transmission of goby sounds was restricted even further, attenuating about 30 dB in half a meter (Lugli , 2003; Lugli and Fine, 2003; Lugli and Fine, 2007). Therefore, the Umwelt (perceptual world) of shallow water bottom fish is likely restricted to short distances.

1. Neuroanatomy

Highlights of early work at VCU included the first demonstration of the toadfish sonic motor nucleus via retrograde transport of horseradish peroxidase (HRP) (Fine , 1982). We also used HRP to describe lateral line nuclei in the toadfish (DeRosa and Fine, 1988). George Leichnetz in the Anatomy Department of the medical school provided the HRP and helped us set up.

We collaborated with Don Keefer at the University of Virginia on steroid autoradiography and were the first to demonstrate steroid-concentrating neurons in the brainstem of a fish (Fine , 1982). Brainstem target neurons had not been found in several studies of non-sonic teleosts. Based on work with bird song (Arnold and Saltiel, 1979), we hypothesized and then found overlap of steroid target neurons with the brainstem sonic pathway, at that time known only grossly in toadfish from brain stimulation. The collaborations resulted in a paper in Science, unique because the toadfish had been kept in trash cans in the basement of the biology building. More complete autoradiographic studies using [3H]estrogen, testosterone, and dihydrotestosterone were published later (Fine , 1990b; Fine , 1996a).

2. Sexual dimorphism of the brain

Another highlight with Ross McClung, Department of Anatomy and Neurobiology, was the first demonstration of sexual dimorphism in a fish brain (Fine , 1984). Neurons in the toadfish sonic motor nucleus increase in number and size for 7–8 years based on aging using annual rings on saccular otoliths (Radtke , 1985). Furthermore, males have two forms, one with large neurons and another with small neurons (now known as type I and II males). The small neurons in males are the same size as in females. This was a startling discovery since male oyster toadfish have one external form. We hypothesized that large-celled males are territorial, and ones with small cells are satellite males who attempt sneak fertilizations as later demonstrated in the midshipman Porichthys notatus, a toadfish in another subfamily (Bass and Marchaterre, 1989; Bass and Anderson, 1991).

We also described the origin of embryonic sonic motor neurons from ependymal cells lining the central canal (Galeo , 1987), and implanted steroid pellets in gonadectomized male and female toadfish to investigate the basis for sexual dimorphism in toadfish sonic muscles. Estradiol stimulated a small and androgens (testosterone and dihydrotestosterone and 11 ketotestosterone) in females and a larger increase in the combined swim bladder and sonic muscles in males (Fine and Pennypacker, 1986).

Friedrich Ladich visited from Vienna twice and used HRP to identify sonic motor neurons, first in croaking gouramis Trichopsis (Ladich and Fine, 1992) and then in pimelodid catfish (Ladich and Fine, 1994). Position and morphology of the pectoral motor neurons in Trichopsis were similar to those of a Betta, a related but silent species, suggesting that the central nervous system of the croaking gourami was able to adapt to a new function (sound production) without major reorganization of the pectoral motor-neuron pool. Catfish sonic organs are innervated by occipital and true spinal nerves with nuclei in three separate motor columns for pectoral, swimbladder sonic muscles and the tensor tripodus muscle that inserts on the swimbladder.

3. Sonic muscle synchronization

Toadfish sonic muscles line the sides and back of a heart-shaped swim bladder (Fig. 2) and contract rapidly in order to generate sounds. Yet the sonic nerves enter the front of the muscles and could potentially delay contractions of muscle fibers further back. In order to be effective at generating sound, muscle fibers must contract synchronously. Much of the answer to this problem was the earlier discovery of electric synapses in the sonic motor nucleus (SMN) (Pappas and Bennett, 1966), which synchronize efferent output to the muscles. We further examined the problem by implanting HRP in the anterior, mid, and posterior sonic muscle to detail connectivity between the SMN and sonic muscles, measured diameter of myelinated nerve fibers within the muscle, and cleared and stained whole mounts with Sudan black to illustrate nerve branching within the sonic muscle (Fine and Mosca, 1989).

FIG. 2.

(Color online) Swimbladder of the oyster toadfish Opsanus tau showing intrinsic sonic muscles on the sides and back of the swim bladder in (A) Dorsal view, (B) ventral view, and (C) ventral view with the bottom removed. Dual arrow heads point to a heavy column at the confluence of the two anterior halves of the anterior bladder that appear to decrease anterior vibrations. Scale bar = 1 cm. Reproduced from Barimo, J. F., and Fine, M. L. (1998). Relationship of swim-bladder shape to the directionality pattern of underwater sound in the oyster toadfish. Can. J. Zool. 76, 134–143.

FIG. 2.

(Color online) Swimbladder of the oyster toadfish Opsanus tau showing intrinsic sonic muscles on the sides and back of the swim bladder in (A) Dorsal view, (B) ventral view, and (C) ventral view with the bottom removed. Dual arrow heads point to a heavy column at the confluence of the two anterior halves of the anterior bladder that appear to decrease anterior vibrations. Scale bar = 1 cm. Reproduced from Barimo, J. F., and Fine, M. L. (1998). Relationship of swim-bladder shape to the directionality pattern of underwater sound in the oyster toadfish. Can. J. Zool. 76, 134–143.

Close modal

Despite a restricted injection site, neurons were labeled throughout the ipsilateral SMN, indicating the absence of any systematic, or somatotopic, order in projection to muscle fibers, which would work against synchronization. Staining indicates the main nerve trunk is unbranched until about a third of the way through the muscle where it sends branches forward to the anterior regions of the muscle. The branching pattern indicates a delay line ensuring that fibers in the front of the sonic muscle are not stimulated before those much further back.

We also quantified differences in neuron morphology with Golgi stains (Fine and Mosca, 1995) that were consistent with synchronization by electrical synapses between neurons (Fig. 3). Neurons at the base of the nucleus send out large dendrites bilaterally to bring efferent input to the nucleus from the left and right pacemaker nucleus. Caudal neurons also have caudally-directed dendrites that leave the nucleus. Neurons in the middle branch in various directions, and ones lining the top of the SMN form a network of anterior and posteriorly-directed dendrites connecting this region from front to back. Additionally, dorsal neurons have a large dendrite directed ventrally. Thus input to the SMN would be spread throughout the nucleus from the bottom and caudal region via synchronizing electric synapses.

FIG. 3.

(A) Sagittal section of a Golgi stained sonic motor nucleus of the oyster toadfish Opsanus tau showing that motor neurons in different regions of the nucleus have different dendritic patterns that will help synchronize motor output to sonic muscles. Anterior is to the right. (B)–(F). Neurons in (A), shown individually at a higher magnification in separate panels, respectively, dorsal neurons in (B), rostral neurons in (C), vental neurons in (D), stellate neurons in (E), and caudal neurons in (F). Scale bar = 400 μm in (A) and 50 μm in other panels. Reproduced from Fine, M. L., and Mosca, P. J. (1995). ”A golgi and horseradish peroxidase study of the sonic motor nucleus of the oyster toadfish,“ Brain Behav. Evol. 45, 123–137, with permission of Karger Publishers. ©1995 S. Karger AG, Basel.

FIG. 3.

(A) Sagittal section of a Golgi stained sonic motor nucleus of the oyster toadfish Opsanus tau showing that motor neurons in different regions of the nucleus have different dendritic patterns that will help synchronize motor output to sonic muscles. Anterior is to the right. (B)–(F). Neurons in (A), shown individually at a higher magnification in separate panels, respectively, dorsal neurons in (B), rostral neurons in (C), vental neurons in (D), stellate neurons in (E), and caudal neurons in (F). Scale bar = 400 μm in (A) and 50 μm in other panels. Reproduced from Fine, M. L., and Mosca, P. J. (1995). ”A golgi and horseradish peroxidase study of the sonic motor nucleus of the oyster toadfish,“ Brain Behav. Evol. 45, 123–137, with permission of Karger Publishers. ©1995 S. Karger AG, Basel.

Close modal

Building on earlier work using cholinesterase histochemistry (Gainer and Klancher, 1965), we found that the number of neuromuscular junctions, but not their spacing, increases with fish size as muscle fibers grow longer (Hirsch , 1998), indicating that new junctions are forming in growing muscle fibers. Sonic muscle fibers have a slow conduction velocity (Gainer, 1969). Therefore, adding junctions at regular intervals would minimize delay and facilitate rapid contraction within individual fibers.

Although somewhat successful in working on CNS control of sound production, I was the odd guy working on fish sound production in a department with a high-teaching load and a premed orientation, which at the time granted only Master's degrees. At my poster at a Society for Neuroscience meeting, Tom Finger, who had helped me as a fellow graduate student, planted a seed when he asked me about the implications of the work on sexual dimorphism of the sonic motor nucleus for sonic muscle. His question got me thinking, and I gradually changed my focus away from the nervous system to sonic muscle and mechanisms of fish sound production, first in toadfish and then in other species.

Toadfish have been a classic subject for fish sound production. Nesting males remain stationary for long periods and produce long duration tonal courtship boatwhistle calls as well as shorter and lower frequency agonistic grunts (Tavolga, 1958; Gray and Winn, 1961). Since individuals readily enter shelters placed in shallow water, they can be recorded and manipulated in the field without inherent problems of small-tank acoustics. Toadfish in shelters allowed Winn (Winn, 1967, 1972) and his student James Fish (Fish, 1972) to use playbacks to demonstrate that boatwhistles or tone bursts, played back at a rapid rate, increase calling in subject fish. Finally, toadfish have one of the fastest-contracting muscles in vertebrates (Skoglund, 1961; Rome , 1996), and muscle fibers have an unusual ultrastructure (Fawcett and Revel, 1961), a single IIa fiber type [fast type ATPase (the enzyme that provides energy by removing a phosphate from adenosine triphosphate) and oxidative] and higher levels of glycogen and lipids (metabolic fuels) than white body muscle (Fine , 1986; Fine and Pennypacker, 1988).

As originally described (Fawcett and Revel, 1961), toadfish sonic muscle fibers have a central core of sarcoplasm (muscle cytoplasm) surrounded by a contractile cylinder of radially alternating myofibrils and sarcoplasmic reticulum (SR) and an area of sarcoplasm at the fiber periphery (Fig. 4). Unlike most muscles, glycogen granules and mitochondria are absent in the contractile cylinder and occur in the central core and at the fiber periphery under the sarcolemma (muscle cell membrane): thus a separation of the energy generating and energy utilizing parts of the fiber. Sonic muscle fibers are generally smaller than fibers in other body muscles (Fine and Parmentier, 2015), and small size, with a high surface-to-volume ratio, appears to be an important adaptation for rapid contraction since it facilitates movement of oxygen in and carbon dioxide out of the fibers and movement of ATP within fibers. Female toadfish actually have larger fibers than more vocally-active males (Fine , 1990a).

FIG. 4.

(A) Ultrastructure of a typical sonic muscle fiber. The central core with mitochondria and glycogen granules is surrounded by a contractile cylinder of alternating SR and myofibrils, and the fiber periphery also has glycogen granules, mitochondria and nuclei. (B) A large fiber that is fragmenting. Note a small fiber in both panels (asterisks) has yet to differentiate a core, and their outline is similar to fragments still contained in the mature fiber. The myofibrils and SR in the separated fibers have assumed a radial orientation. Scale bar = 3 μm. Reproduced from Fine, M. L., Bernard, B., and Harris, T. M. (1993). “Functional morphology of toadfish sonic muscle fibers: relationship to possible fiber division,” Can. J. Zool. 71, 2262–2274.

FIG. 4.

(A) Ultrastructure of a typical sonic muscle fiber. The central core with mitochondria and glycogen granules is surrounded by a contractile cylinder of alternating SR and myofibrils, and the fiber periphery also has glycogen granules, mitochondria and nuclei. (B) A large fiber that is fragmenting. Note a small fiber in both panels (asterisks) has yet to differentiate a core, and their outline is similar to fragments still contained in the mature fiber. The myofibrils and SR in the separated fibers have assumed a radial orientation. Scale bar = 3 μm. Reproduced from Fine, M. L., Bernard, B., and Harris, T. M. (1993). “Functional morphology of toadfish sonic muscle fibers: relationship to possible fiber division,” Can. J. Zool. 71, 2262–2274.

Close modal

There appear to be tradeoffs in sonic fiber morphology. The SR constitutes about a third of the fiber volume (Franzini-Armstrong and Nunzi, 1983), and its intimate association with myofibrils ensures that calcium ions released from the SR are therefore close to binding sites on myofibrils. However, the cost is the exclusion of mitochondria and glycogen granules from proximity to sites that require energy. Mitochondria comprise only about 4% of fiber volume in males and 1% in females, and a large SR is typically associated with fast muscles (Franzini-Armstrong and Nunzi, 1983; Appelt , 1991). We showed with Thomas Harris in the Department of Anatomy and Neurobiology that, as sonic fibers grow in size, they change from having no core in the smallest fibers to a single one (the common condition), and the largest fibers differentiate several cores (Fine , 1990a; Fine , 1993). The distance between mitochondria and the far side of contractile cylinder likely becomes limiting with fiber growth. The muscle solves this problem by differentiating new cores allowing the maximal distance between contractile tissue and mitochondria to remain relatively constant. Eventually, this distance becomes difficult to maintain in increasingly larger fibers, and they fragment [Fig. 4(B)] before presumably dividing.

Intrinsic toadfish muscle fibers do not have a standard origin or insertion; rather each muscle fiber attaches to the swim bladder at its dorsal and ventral ends. The muscle grows like an onion adding most new fibers, which have small diameters, at the muscle periphery (Fine , 1990a) Both the swim bladder and sonic muscles increase in size with fish growth (Fine , 1990a) although males grow larger and live longer than females (Radtke , 1985). Regression data indicate that the swim bladder and sonic muscles are, respectively, 20% and 44% heavier in males than in females. There could be several reasons for a larger swim bladder including increased buoyancy, effects on sound radiation or simply a larger base to house the sonic muscles in males. Toadfish buoyancy measurements discount the first hypothesis since there is considerable overlap between males and females except in the largest individuals who are all male (Fine , 1995), therefore supporting the other two hypotheses. Although the toadfish is negatively buoyant, the swim bladder still decreases specific gravity over that of a fish with the bladder removed (1.049 and 1.083, respectively).

Fibers are added to the sonic muscle continuously although at a declining rate in older individuals. The number increases at least 16 fold (from 30 800 in a 6.4 g juvenile to 488 500 in a large male), and mean fiber diameter increases almost threefold (11.5 to 28.6 μm) with toadfish size (Fine , 1990a). Interestingly, fiber diameter in females is ca. 15% larger than in males, but males have almost 50% more fibers than females. Fiber size increases are a potential problem owing to the difficulty in maintaining contraction speed in energetically less efficient large fibers.

These findings bring up the question of how new fibers are recruited since mammals are typically born with an adult number of muscle fibers and grow primarily by fiber hypertrophy. It was once commonly believed that muscle fibers could divide, albeit non-mitotically. Then Mauro (1961) discovered satellite cells that are similar to embryonic myoblasts and can be incorporated into muscles as new nuclei. His discovery resulted in a paradigm shift and observations that had been interpreted as muscle fiber splitting were reinterpreted as the accretion of satellite cells onto damaged fibers. However, wild toadfish are unlikely to have large numbers of damaged fibers. In later work with Cathy Loesser Casey, we found satellite cells, which were common in young fish but rare in older ones and thus are unlikely to account for the large increase in fiber number (Loesser , 1997).

We found a number of lines of strong circumstantial evidence that toadfish sonic fibers divide (Fine , 1993). As mentioned before, the first Fawcett and Revel (1961) description of toadfish sonic fibers described fibers as basically identical with a single sarcoplasmic core. Our reexamination (Fine , 1993) indicated the largest fibers develop additional cores containing mitochondria and are often fragmented [Fig 4(B)], some looking like pie slices still within a single fiber. There are also small fibers adjacent to large ones, and the shape and ultrastructural details of small fibers line up with their larger presumably mother fibers. Occasionally, the cytoplasm between fragments assumes a similar appearance to the fiber periphery with glycogen granules and mitochondria, not normally present in the contractile cylinder. Additionally, fibers in small juveniles and separate but small cells in mature fish had yet to differentiate a central core. A small fiber without a core is likely newly formed.

In a separate study on growth of blue catfish Ictalurus furcatus, we examined pectoral muscles involved in stridulation sounds (Lahiri and Fine, 2015). There was a window in 26–27 cm total length catfish when the number of fibers in all eight pectoral muscles doubled as their fiber diameter dropped by half. A fish with indeterminate growth that can increase in mass to over 45 kg (100 pounds) appears unable to pack all the muscle fibers it will need into an embryo, and process akin to a metamorphosis occurs to double the number of fibers. Although evidence is circumstantial, parsimony suggests that fibers are dividing in both toadfish sonic muscle and blue catfish pectoral muscle fibers.

The chief ability of toadfish sonic muscles is rapid contraction rather than fatigue resistance or power (Rome and Linstedt, 1998). Muscles can complete a twitch in 10 ms (Skoglund, 1961; Fine , 2001), and each contraction generates a sound cycle: a boatwhistle with a 200 Hz fundamental frequency is caused by a train of 200 Hz contractions (Fine , 2001). The highest fundamental frequencies recorded from oyster and gulf toadfish in the field are about 278 Hz (Fine, 1978b; Thorson and Fine, 2002b). However, isolated muscle fibers in an in vitro preparation (Rome 1996) only contract to about 100 Hz when electrically stimulated, compared to at least 400 Hz in an intact fish (Fine , 2001). At 500 Hz the intact muscle still fails to tetanize and contracts to every other cycle (250 Hz). Compared to in vitro fibers, higher speeds in intact muscle will be aided by increased pressure in the swim bladder from muscle contraction that will support muscle relaxation and return the swim bladder to its resting shape.

1. Sarcoplasmic reticulum and calcium uptake

The high speed of muscle contraction caused us (led by Joseph Feher in the Physiology Department and Tyler Waybright) to examine the ability of the sarcoplasmic reticulum to sequester calcium, necessary for muscle relaxation (Feher , 1998). We hypothesized that it would be considerably faster than a mammalian fast muscle (rat extensor digitorum longus or EDL). Surprisingly, calcium uptake rate is similar between the two muscles. However, the calcium capacity in the toadfish is five times higher indicating that large calcium stores in the SR will allow the muscle to keep contracting during a long duration boatwhistle. It is likely that another calcium binding protein, parvalbumin, assists with restoring calcium to the SR in the multiple seconds between boatwhistles.

2. Calling energetics

We explored the energetic costs of calling with Clara Amorim from Portugal by measuring toadfish oxygen consumption in a respirometer while stimulating the sonic nerve electrically (Amorim , 2002). Because of rapid contraction, we hypothesized that stimulated fish would consume large amounts of oxygen when calling at a rapid rate but again found the opposite. First trials on individuals caused a 40%–60% increase in oxygen consumption, which resulted from a freaked out fish attempting to escape from the enclosed respirometer. Successive trials with the same individuals resulted in calmer fish and no measurable increase in oxygen consumption. Low oxygen consumption was ascribed to the relatively small weight of the sonic muscle and minimal contraction time, even when contracting at a rapid rate (see next paragraph).

3. Muscle fatigue

Later with Steve Mitchell and James Poland in the Physiology Department (Mitchell , 2008), we tested fatigue resistance explicitly, employing Burke's fatigue index (Burke , 1973): stimulating the muscle electrically with 100 ms trains of 200 Hz every 4 s or 15 times per min for 5 min (Fig. 5). Although the stimulus duration was shorter than a typical boatwhistle, the other parameters were equivalent to a fish calling at a rapid rate. By 5 min there was only a brief contraction and weak sound at stimulus onset, after which there was no recordable motion despite continued stimulation (Fig. 5). Therefore, the sonic muscle was almost completely fatigued. Although attenuated, muscle action potentials (EMGs) were still robust. Additionally, males used 11% and females 23% of their muscle glycogen compared to the opposite unstimulated muscle, thus indicating that metabolic substrates are not the primary cause of fatigue although they decrease at a high rate.

FIG. 5.

Responses of sonic muscle of the oyster toadfish Opsanus tau to repeated stimulation. Sonic muscles were stimulated with 100 ms trains of electrical stimuli at 200 Hz every 4 s shown for the first stimulus (0 min) and at 5 min. Recordings indicate muscle action potentials (EMG), swimbladder displacement (SD) measured with a laser vibrometer, and sound recorded with a hydrophone. Reprinted from Animal Behavior, 76, Mitchell, S., Poland, J., and Fine, M. L, “Does muscle fatigue limit advertisement calling in the oyster toadfish Opsanus tau?,” 1011–1016, Copyright 2008, with permission from The Association for the Study of Animal Behaviour.

FIG. 5.

Responses of sonic muscle of the oyster toadfish Opsanus tau to repeated stimulation. Sonic muscles were stimulated with 100 ms trains of electrical stimuli at 200 Hz every 4 s shown for the first stimulus (0 min) and at 5 min. Recordings indicate muscle action potentials (EMG), swimbladder displacement (SD) measured with a laser vibrometer, and sound recorded with a hydrophone. Reprinted from Animal Behavior, 76, Mitchell, S., Poland, J., and Fine, M. L, “Does muscle fatigue limit advertisement calling in the oyster toadfish Opsanus tau?,” 1011–1016, Copyright 2008, with permission from The Association for the Study of Animal Behaviour.

Close modal

Therefore, a low rate of spontaneous calling can be elevated for bursts of activity. Our stimulation paradigm would excite the sonic muscle for only 1.5 s per min (100 ms × 15 per min) or 7.5 s for the 5 min of stimulation, yet caused almost complete muscle fatigue. Owing to the small weight of sonic muscles (1% of body weight in males and 0.7% in females) (Johnson , 2000), the energetic cost of calling is extremely low. However, the toadfish faces the problem of shuttling energy to the contractile machinery necessitated by extreme contraction speed, which is made more difficult by the small number of mitochondria and their separation from the contractile cylinder.

Oyster toadfish are often silent or produce their boatwhistle advertisement calls at a low rate (one or two times a minute) during day and night (Fine , 1977a). The same is true for the gulf toadfish although it exhibits a pronounced peak in calling at afternoon twilight (Thorson and Fine, 2002b). Gulf toadfish produce a more complex call consisting of a long note followed by zero to several shorter ones, and their calls can exceed a second in duration. Both species increase their call rate when stimulated by other callers or playbacks in O. tau (Winn, 1967, 1972; Fish, 1972). James Fish witnessed a male oyster toadfish calling over 20 times a minute when encountering a ripe female who entered his nest (Fish, 1972), and a similar sprint has been heard in a gulf toadfish (Thorson and Fine, 2002b). In the gulf toadfish notes per boatwhistle decrease as males call faster, indicating a behavioral flexibility and supporting a limit on muscle contraction (Thorson and Fine, 2002b).

In addition to boatwhistling at a more rapid rate, toadfish of both species have a behavior we term acoustic tagging in which a male grunts during or shortly after the boatwhistle or grunt of a nearby toadfish (Thorson and Fine, 2002a; Fine and Thorson, 2008; Mensinger, 2014). We identified calls of four nearby individuals in a Florida canal and were able to track them by variation in the frequency spectra and amplitude of their calls. There were parallels to a dominance hierarchy: one toadfish tagged others, but in turn, was rarely tagged. Tagging with a grunt rather than a boatwhistle saves energy since grunts are shorter with fewer muscle contractions. Hierarchical tagging likely influences female choice in mate selection and demonstrates eavesdropping—males are clearly listening to the calls of neighbors. Surprisingly, toadfish frequently tagged intense snaps from nearby snapping shrimp with latencies as short as 41 ms, which can lead to multiple tags (Fig. 6).

FIG. 6.

Top panel: A shrimp snap that was tagged by a toadfish, and the same selection expanded (middle panel). Bottom panel: A shrimp snap S that was tagged by fish 3 who was tagged by fish 2 who in turn was tagged by fish 1. Amplitude of grunt tags reflects proximity to the hydrophone. Reproduced from Thorson, R. F., and Fine, M. L. (2002). “Acoustic competition in the gulf toadfish Opsanus beta: acoustic tagging,” J. Acoust. Soc. Am. 111, 2302–2307, with permission of Acoustical Society of America. Copyright 2002, Acoustical Society of America.

FIG. 6.

Top panel: A shrimp snap that was tagged by a toadfish, and the same selection expanded (middle panel). Bottom panel: A shrimp snap S that was tagged by fish 3 who was tagged by fish 2 who in turn was tagged by fish 1. Amplitude of grunt tags reflects proximity to the hydrophone. Reproduced from Thorson, R. F., and Fine, M. L. (2002). “Acoustic competition in the gulf toadfish Opsanus beta: acoustic tagging,” J. Acoust. Soc. Am. 111, 2302–2307, with permission of Acoustical Society of America. Copyright 2002, Acoustical Society of America.

Close modal

In summary, the small number of mitochondria, hours in silence or producing a small number of boatwhistles, calling increases during playbacks, and acoustic tagging all suggest limitations on calling because of high-speed contraction. Therefore, muscle morphology and physiology agree with behavioral findings of a low rate of spontaneous calling that is elevated for bursts of activity to compete with other males and to attract females (Winn, 1967, 1972, Fish, 1972; Fine , 1977a; Thorson and Fine, 2002a,b; Fine and Thorson, 2008).

Classically, the swim bladder has been modeled as an underwater resonant bubble (Minnaert, 1933; Bergeijk, 1964; Harris, 1964; Weston, 1967). Resonant frequency will increase with depth due to increased hydrostatic pressure and decrease with swim bladder size since it is proportional to the square root of stiffness divided by mass (Kinsler , 2000). A recent mathematical treatment of bubbles in warm and cold surface water and cold deep water at 3500 m examined bubble resonance, considering the effect of the two dominant swim bladder gases (N2 and O2), damping and quality factor, a measure of sharpness of tuning (Sprague , 2022).

As shown by Sprague , (2022) a bubble with a 1 cm radius at 3500 m would have a resonant frequency of about 7 kHz, considerably above the upper hearing range of most fishes (Popper , 2019). Temperature does not influence bubble resonance, and there are minor differences in the effect of N2 and O2. However, the damping factor increases by 300 fold with depth, and therefore amplitude would be 25 dB less at 3500 m than at the surface. Further, decreases in quality factor expand the width and lower the peak amplitude of a resonance curve.

Low concentrations of deep-water fishes and high damping likely explain the absence of fish sound recordings from deep water despite species with swim bladder muscles (Marshall, 1967). Likely fish sounds have been recorded at depths around 600 m (Mann and Jarvis, 2004; Rountree , 2012), and two species of Genypterus, a cusk-eel, found from 200–800 m on the continental shelf and slope, have been recorded in aquaculture tanks (Parmentier , 2018).

Experimental work with sonar and echo sounders has indicated that swim bladders are resonant and responsible for most of the target strength of echo returns (McCartney and Stubbs, 1970; Love, 1978). Further, playing sounds to captive codfish and other species in ocean water before and after altering water depth, changes return frequencies and supports resonance (Sand and Hawkins, 1973; Lovik and Hovem, 1979). Given mathematical and experimental evidence primarily from the scattering community, the resonant bubble model of the swim bladder became fixed in the fields of fish sound production and hearing. As if dictated by a medieval monarch, contrary evidence was considered a heresy or ignored.

Our work on the toadfish indicated that generalizations and predictions of resonance failed to apply; see Fine and Parmentier (2022) for a detailed review. First, deflation of the heart-shaped swim bladder (Fig. 2) that points toward the nearby ears does not change auditory thresholds (Yan , 2000), indicating that reradiated swim bladder sounds are not effectively transferred to the ears in the oyster toadfish. Goldfish thresholds, tested as a control, decrease by 35–50 dB after deflation using the same procedure.

Most swim bladders are more or less ovular in cross section and extend longitudinally in the rostrocaudal dimension, a prolate spheroid (Weston, 1967). Therefore, modification of the bladder to a cardioid, or heart shape, in toadfish and other species (Ladich and Fine, 2006) suggests a functional adaptation. We tested a directional radiation hypothesis in the field by recording boatwhistles with a hydrophone fixed 1 m in front of a fish and one roved at various positions around the fish (from 0° to 360°). The directional sound field mirrored the shape of the swim bladder and attached sonic muscles (Barimo and Fine, 1998). In fact, boatwhistle amplitude was several dB greater behind than in front of the fish whereas the resonant bubble would predict an omnidirectional sound field.

We stimulated the sonic nerve to make muscle twitch and tonal boatwhistle-like sounds (Fine , 2001) and recorded evoked sounds and swim bladder movement with a noncontact laser vibrometer. Stimulating at different frequencies from 50 to 400 Hz produced movement and sound at the stimulus frequency indicating a forced response rather than a resonant one. Additionally, the fundamental frequency of boatwhistle choruses from the York River, VA, often varies by as little as 10 Hz in individual recordings despite coming from a natural population that would contain different-sized fish (Fine, 1978b). Nerve stimulation causes the curved muscle lining the sides and back of the bladder to push the bladder inward (like a human diaphragm), and the inward pressure then pushes the bottom outward, a quadrupole motion rather than the simple monopole oscillation of an underwater bubble. The top of the bladder is pinned against the backbone and relatively stationary. Compared to a monopole, a quadrupole is an inefficient radiator, explaining why the sonic muscle must contract rapidly to generate sound.

In order to avoid forcing by the sonic muscles and observe the swim bladder independently, we struck different sized swim bladders with a modal analysis hammer, which is used to excite artificial structures (car, bridge, etc) and records strike force in Newtons over time (Fine , 2009). Evoked peak frequencies were not proportional to bladder size. Additionally, harder (faster) hits generated higher frequencies, and sound and motion damped rapidly, equivalent to an automobile shock absorber rather than continuing to ring as would be expected for a resonant structure.

Thus a number of lines of evidence indicate that the swim bladder produces sound as a forced response dependent on muscle movement and not the resonant behavior of the internal gas bubble. Why might this be so? We examined material properties of the swim bladder wall (stress, strain, and Young's modulus), stained for collagen and elastin fibers, and dried bladders to measure percent water (Fine , 2016). The bladder wall is an anisotropic structure; fiber directions vary in a complex manner as do material properties, which should contribute to regional differences in vibration. Finally, the viscoelastic bladder wall is composed of 80% water and is therefore responsible for viscous damping that would suppress vibrations of the internal bubble.

Although both fields share an interest in swim bladders, workers in the fish acoustic communication (hearing and sound production) and sonar communities are largely distinct with different tools and interests. It is also premature to assume all auditory and sound investigators have accepted the forced response model since swim bladder resonance has been the reigning paradigm for more than 50 years.

Three conclusions from the Sprague (2022) treatment of underwater bubbles provide a logical basis to potentially (start to) reconcile the two fields: (1) Due to high water content, the characteristic impedance of the swim bladder wall is similar to the surrounding water and will have negligible effects on mass loading. (2) With depth the stiffness of the internal gas becomes dominant and the swim bladder wall will contribute less to overall stiffness. (3) The wall tissue will not be affected by depth and its contribution to damping will remain constant, e.g., it will reduce the resonant amplitude and quality factor at all depths. However, with increasing depth, the swim bladder gas stiffness will add to resonant behavior as the damping effect of the bladder wall has a relatively smaller effect. Most fish sound and hearing work is conducted in tanks or shallow water, whereas sonar and scattering studies tend to occur in deeper water, albeit mostly less than 3500 m. Thus, apparent opposites (the resonant and forced response) may be reconciled by realizing that they apply to different environmental conditions although experimentation is required to support this idea.

During Friedrich Ladich's visit from Vienna, we tried to get channel catfish Ictalurus punctatus to make sound by netting and holding them without success, and Fritz returned to Vienna believing channel catfish were silent, unlike many South American catfishes. We tried again later and found some but not all channel catfish would make sounds when held. They produce stridulation sounds using ridges on the dorsal process on the base of the pectoral spines that rub against a rough surface on the cleithrum of the pectoral girdle (Fine , 1997) (Fig. 7). Interestingly, most channel catfish are right-handed, a clear example of lateralization in fishes (Fine , 1996b). We demonstrated that spines can be locked when maximally abducted to a right angle due to specialized matching processes on the spine base and girdle and bound in various positions by torqueing the spine ventrolaterally, thereby engaging friction-locking surfaces (Fine , 1997). Previously, both binding and locking had been termed locking, and we separated the two actions and their morphological bases. A locked spine can turn eating a catfish into a risky and occasionally lethal enterprise for a largemouth bass (Bosher , 2006; Fine , 2011; Sismour , 2013).

FIG. 7.

Scanning electron micrograph of the left pectoral spine of a channel catfish Ictalurus punctatus and rubbing surface on the cleithrum. (A) Spine. Medial is to the right showing the dorsal process pointing upward and anterior process protruding to the right on the spine base. (B) Undersurface of the ridged dorsal process that rubs against a rough but featureless surface on the cleithrum in (C) when depressed during spine abduction. Inset is a higher magnification picture of the rubbing surface. Scale bar = 1 mm in (A) and 0.5 mm in (B) and (C). Reproduced from Mohajer, Y., Ghahramani, Z. N., and Fine, M. L. (2015). “Pectoral sound generation in the blue catfish Ictalurus furcatus,” J. Comp. Physiol. A 201, 305–315, with permission from SNCSC.

FIG. 7.

Scanning electron micrograph of the left pectoral spine of a channel catfish Ictalurus punctatus and rubbing surface on the cleithrum. (A) Spine. Medial is to the right showing the dorsal process pointing upward and anterior process protruding to the right on the spine base. (B) Undersurface of the ridged dorsal process that rubs against a rough but featureless surface on the cleithrum in (C) when depressed during spine abduction. Inset is a higher magnification picture of the rubbing surface. Scale bar = 1 mm in (A) and 0.5 mm in (B) and (C). Reproduced from Mohajer, Y., Ghahramani, Z. N., and Fine, M. L. (2015). “Pectoral sound generation in the blue catfish Ictalurus furcatus,” J. Comp. Physiol. A 201, 305–315, with permission from SNCSC.

Close modal

Catfish are aware of nearby predators and change their feeding, growth, and behavior in the presence of a big largemouth bass separated by a rubber-mesh barrier (Fine , 2011). Catfishes have both aerial and aquatic predators, and it was unclear if sounds were directed to either medium. We demonstrated that sounds have greater amplitudes and propagate further in water and are therefore unlikely directed at common aerial predators such as osprey and bald eagles (Ghahramani , 2014). We also found that the pectoral spine was reduced in size in domesticated (aquaculture) catfish that are less likely to suffer predation than wild fish (Fine , 2014)

Generally, fish sound production mechanisms are exaptations (Gould and Vrba, 1982), structures that exhibit an evolutionary modification in structure, which allows changes from their ancestral function (Parmentier , 2007; Parmentier , 2017). In the case of catfish pectoral spines, there were likely multiple steps in the modification of a typical fish slender pectoral spine into a defensive and later sound-producing structure. Catfish spines are heavily modified and robust structures that look like a medieval weapon (Fig. 7). It is likely that spines evolved as an antipredator adaptation by becoming thicker and stronger (Schaefer, 1984), developing processes that enable binding and locking, and finally adding ridges to the dorsal process that would excite the fused pectoral girdle into sound production. Likely the ridges would have enabled the primitive but already modified locking system to produce sounds that might have warned predators and later were used for communication in many catfish families (Fine and Ladich, 2003). In some groups ridges have been lost rendering them silent (Kaatz 2010). Due to multiple functions (swimming and steering, locking, binding and sound production), catfish pectoral muscles exhibit size differences and minor modifications across species in ictalurid catfishes (Miano , 2013); ictalurids vary in size from several centimeter madtoms to blue catfish that occasionally exceed 45 kg (100 pounds).

We knew from our work and the work of others (Heyd and Pfeiffer, 2000; Ladich, 2001; Kaatz and Stewart, 2012) that sounds were produced as a rapid series of pulses when ridges on the dorsal process were rubbed across the cleithrum during abduction (forward movement of the fin) and in some families during both abduction and adduction (Fine and Ladich, 2003). Parmentier (2010b) determined that sound pulses were caused by a series of pectoral jerk motions. Patek (2001) demonstrated that the spiny lobster buzz was produced by a slip-stick mechanism (starts and stops) as a bow over a violin string: the motion is too fast for the human eye to resolve but is not continuous. We borrowed a high-speed camera from our Mechanical Engineering Department (thanks to Gary Tepper) and took pictures of sonic abductions at 500 frames a second. A short segment of low amplitude sound was produced while the spine made a quick 1–2 ms movement (Parmentier et al. jerks), but the sound continued with higher amplitude after movement ceased due to energy stored in the pectoral girdle, the sound radiator (Mohajer , 2015), thus supporting the slip-stick mechanism for the first time in a vertebrate (Fig. 8).

FIG. 8.

Oscillograph of a pectoral stridulation sound of a blue catfish Ictalurus furcatus. Bar in (A) indicates three expanded sound pulses in (B) photographed at 500 frames per s. Up and down arrows indicate when abduction started and stopped. Note that sound amplitude increases after movement stopped. Reproduced from Mohajer, Y., Ghahramani, Z. N., and Fine, M. L. (2015). “Pectoral sound generation in the blue catfish Ictalurus furcatus,” J. Comp. Physiol. A 201, 305–315, with permission from SNCSC.

FIG. 8.

Oscillograph of a pectoral stridulation sound of a blue catfish Ictalurus furcatus. Bar in (A) indicates three expanded sound pulses in (B) photographed at 500 frames per s. Up and down arrows indicate when abduction started and stopped. Note that sound amplitude increases after movement stopped. Reproduced from Mohajer, Y., Ghahramani, Z. N., and Fine, M. L. (2015). “Pectoral sound generation in the blue catfish Ictalurus furcatus,” J. Comp. Physiol. A 201, 305–315, with permission from SNCSC.

Close modal

Eric Parmentier, a classically trained morphologist, visited from Belgium. He had started working on sonic morphology and had recorded fish sounds but was new to sound analysis. It was amazing to watch him in action. Whereas I get up and pace frequently, Eric, armed with a 2 L Diet Coke, worked continuously for hours. We collaborated on a number of projects, often detailing novel mechanisms of fish sound production in various families, and some of these and other studies will be detailed briefly. They add considerable variation to what had been known about sound generation in fishes.

Characiforms are abundant in the Amazon and produce numerous sounds in the mating season with modified intercostal (rib) muscles that excite the anterior swim bladder (Smith , 2018; Borie , 2019). In the families Curimatidae and Prochilodontidae, these muscles have maintained their ancestral horizontal fiber direction and attach to one or several ribs. They form an aponeurosis that sits in front of the swim bladder and connects ribs bilaterally. Contraction compresses the front of the anterior chamber of the swim bladder. In piranhas, the muscle fibers have been modified to assume a vertical orientation and compress the anterior chamber of the swim bladder in the vertical plane (Ladich and Bass, 2005; Millot , 2011).

Cusk-eels are largely deep-sea species although there are nocturnal shallow water representatives not often seen since they bury in the bottom during the day. We had obtained a number of fawn cusk-eels (Lepophidium profundorum) from about 100 m courtesy of the National Marine Fishery Service (Fine , 2007; Nguyen , 2008), Eric and his students were working on two shallow European species (Ophidion barbatum and O. rochei) (Parmentier , 2006a; Parmentier , 2010a), and he later recorded Genypterus chilensis and G. maculatus in aquaculture tanks in Chile (Parmentier , 2018). Mike (Hin-Kiu) Mok obtained the neobythitine cusk-eels Hoplobrotula armata, Neobythites armata and N. longipes from the upper continental slope in Taiwan (Ali , 2016). Finally, Jack Musick at VIMS provided Dicrolene intronigra, Bathyonus pectoralis and Porogadus miles from his deep-sea trawling program. Therefore, we were able to compare the sonic system in neobythitine cusk-eels from the upper, mid, and deep continental slopes from 100 m to 5 km (Fine , 2018).

Although the external anatomy is relatively conservative in the family, internal anatomy related to sound production is strikingly diverse. There is sexual dimorphism in bones, tendons, muscles, and swim bladders, which tend to be larger in males. In shallow species and even down to over a kilometer deep, there are several sets of sonic muscles arranged in antagonistic pairs that move the swim bladder in opposite directions. In the fawn cusk-eel, the neural arch over the first vertebra pivots in the rostrocaudal plane courtesy of two prongs that permit rotation within depressions in the vertebral body (an inverse toilet paper roll joint). Dorsal muscles attach to the first neural arch and pull it forward. The rib of the first vertebra is expanded to a winglike process that connects to the bladder and has a large surface for attachments of ventral and intermediate sonic muscles that pull it forward causing the neural arch to rotate backward, as in a seesaw. Other species actually form a lima-bean shaped rocker bone from the anterior bladder (Parmentier , 2008). It pivots in opposite directions when antagonistic muscles contract, deforming the bladder. Antagonistic muscles are uncommon in swim-bladder sound production since they would likely impede rapid changes in bladder oscillation, which would work against sound production. We hypothesized that the dorsal muscle remains contracted, increasing bladder stiffness, and the antagonist ventral and intermediate muscles are responsible for bladder oscillation.

Cusk-eel swim bladders can have a thin pliable fenestra that facilitates movement of the anterior swim bladder, but the posterior bladder is held in place. In some species, the bladder ends in a slender ducktail, as in many unrelated sciaenids (drums and croaker). In others, the posterior bladder is rounded and sometimes has a protruding collar surrounding a slender thin round membrane (posterior tube) that may function as a pressure release adaptation to facilitate movement of the anterior bladder. In Dicrolene intronigra, which can be found below 1 km in depth, the tube membrane is only present in males, suggesting its importance in sound production. Length-weight regressions indicate that species decrease in body mass with depth reflecting food limitation and therefore the importance of maintaining a robust sonic system.

In two deep slope species (Bathyonus and Porogadus) sonic muscles are reduced to a single pair and are larger in males, the swim bladder wall is thin, and the swim bladder fenestra and posterior tube are absent. The single pair of muscles is also reduced in length and connects to the swim bladder with a tendon that in Bathyonus is threefold longer than the muscle! Since tendons utilize less energy than muscle (Alexander, 2002), long tendons with reduced muscles are interpreted as an adaptation to low food availability and may allow sound production with slower fibers. Another deep species (Acanthonus armatus) with the lowest brain-body weight ratio of any known vertebrate (Horn , 1978; Fine , 1987) has lost its swim bladder and is presumably mute.

Carapus boraborensis, in another family of ophidiiform fishes, produces sounds with a pair of slow muscles that require 490 ms for a twitch and exhibit an unfused tetanus at 13 Hz (Parmentier , 2006b). For comparison, the oyster toadfish requires ca. 10 ms for a twitch and fails to tetanize at 500 Hz (Skoglund, 1961; Fine , 2001). In the carapid, the muscles attach to small protrusions on the swim bladder with hooks that act like a latch. Muscle contraction pulls the anterior bladder forward stretching the fenestra until the hooks release causing the bladder to snap back to its resting position. The fenestra, overlain by a bony swim bladder plate, will be excited, and it appears to drive swim bladder vibrations. Peak frequency of sounds decreases with fish size, but calculated resonant frequency of the swimbladder is approximately double the recorded frequency. Therefore, we suggested that peak frequency is determined by acoustic properties of the bony swim-bladder plate rather than the swim bladder.

Sciaenids are important commercial and aquaculture fishes found on multiple continents and known for sound production and large saccular otoliths. In most species, sonic muscles occur in males exclusively although some species have muscles in both sexes. For instance, sonic muscles in the Atlantic croaker Micropogonias undulates, present in males and females, are larger in males (Hill , 1987). Muscles are generally extrinsic, attaching to the dorsal swim bladder via an aponeurosis (sheet-like tendon), travel around the sides of the swim bladder and insert at least in some cases on a midline ventral tendon (Fine and Parmentier, 2015; Mok , 2020). Hill (1987) found that the muscles first form during puberty, which can occur in year-old weakfish Cynoscion regalis, when muscle fibers grow out from the aponeurosis. Thus the affinity of these muscles is unclear even though they have a similar contour and lie internally adjacent to hypaxial body muscle. In several species including the black drum (Chao, 1986; Tellechea , 2011), the muscles are intrinsic and completely attach to the sides of the swim bladder.

During the mating season the weakfish sonic muscles hypertrophy (Connaughton , 1997; Connaughton , 2002): they increase in mass, muscle fiber size, and concentration of glycogen, protein, and lipid. Additionally, amplitude of sound pulses increases and duration decreases indicating more rapid contraction of the sonic muscles. Similarly, the Brazilian sciaenid Plagioscion squamissimus has darker and thicker muscles that produce higher amplitude and higher pitched calls with a more rapid pulse rate during the mating season (Borie , 2014). Toadfish and sciaenid sonic muscles are clearly not homologous since they are innervated by occipital spinal nerves in toadfish and segmentally by true spinal nerves segmentally in sciaenids. Yet both species have superfast contracting sonic muscles with a similar ultrastructure of radially arranged SR and myofibrils surrounding a central core (Ono and Poss, 1982). Unlike sciaenids, oyster toadfish sonic muscles do not exhibit a seasonal hypertrophy-atrophy cycle (Johnson , 2000) Thus, despite exhibiting differences, convergent evolution has selected for similar morphology of superfast muscle fibers necessary to produce sounds from a swim bladder in these two families.

Sciaenids tend to have typical carrot-shaped swim bladders that can taper to a slender caudal ducktail. There are paired diverticula (skinny tubes) that extend rostrally (Chao, 1986). In some species like silver perch Bairdiella chrysura and weakfish Cynoscion regalis, the diverticula terminate in close proximity to the ears, but in Atlantic croaker Micropogonias undulates and spot Leiostomus xanthurus the diverticula are short. Silver perch and weakfish have lower auditory thresholds and hear higher frequencies than spot and croaker (Ramcharitar , 2004; Horodysky , 2008), indicating that the longer diverticula conduct sound to the ears. Additionally, there are several Asian species with long diverticula that extend posteriorly (Chao, 1986), and these would not affect hearing. The freshwater sciaenid Boesemania microlepis swim bladder has six long diverticula on either side of the bladder, and they extend caudally parallel to the bladder. It produces sounds with a peak frequency of 1–2 kHz (higher than typical sciaenids), and lower harmonics are attenuated or missing (Mok , 2020), suggesting that the diverticula act as Helmholz absorbers turning the swim bladder into a high-pass filter

1. Damselfish (pomacentridae)

Damselfish have paired tendons that cause rapid mouth closure (jaw slams) and facilitate feeding. These slams have been turned into communication calls, a classic exaptation (Parmentier , 2007). Ablation experiments indicate that teeth in the front of the jaw collide, stimulating sound. Energy is then transferred to the swim bladder, which is involved with sound radiation (Colleye , 2012). It was once commonly assumed that sounds generated elsewhere in the body would be radiated by the swim bladder. However, swim bladder deflation in channel catfish has no effect on frequency spectrum or amplitude of pectoral stridulation sounds (Fine , 1997), and therefore one should not assume larger swim bladders produce lower frequency sounds without testing.

The glaucosomatid Glaucosoma buergeri produces a two-part sound: a quieter part produced by fast sonic muscles that extend the anterior part of the rostral chamber forward by stretching the swim bladder fenestra. The second part is a more intense snap back sound caused by a stretched tendon attached to a smooth muscle (potentially a damper) that in turn attaches to the inner wall of the anterior bladder chamber (Mok , 2011). Unlike antagonistic muscles, a snap-back tendon will not interfere with sound production by adding inertia to swim bladder movement. Members of related families, Pempheridae and Teraponidae, have a similar system but without the smooth muscle and produce longer duration continuous sounds (Parmentier , 2016).

Owing to passive acoustic monitoring (PAM), the field of fish sound production has blossomed from a small discipline with a few workers to one with a budding worldwide interest that will provide opportunities for ecologists and fishery biologists. At this point however, it is not unusual to see PAM papers with unidentified sounds, and sound libraries will become increasingly important (Parsons , 2022; Looby , 2023). However, it is easier to record unseen fish than to identify callers or to demonstrate sound functions, and there is much to learn. For example, the well-known cardinalfishes (Apogonidae), have only recently been discovered to produce agonistic and courtship sounds (Chang , 2022).

Numerous fish families have sonic representatives, many with strikingly unique characters (Fine and Parmentier, 2015; Parmentier , 2021; Looby , 2022; Rice , 2022). Swim bladders and associated structures are certainly one of the most variable internal structures in fishes and likely in all vertebrates. Here are some generalizations and examples that highlight this variability and the need for further work:

  • Sonic structures are evolutionary exaptations (Parmentier and Fine, 2016; Parmentier , 2017) that assumed new functions for sound production (swim bladders, pectoral spines and pharyngeal teeth, bones, and tendons) and hearing (Weberian ossicles, diverticula that travel from the swim bladder to the ears, suprabranchial chambers; Yan, 1998) although the swim bladder maintains its ancestral buoyancy role (Fine , 1995).

  • Swim bladders can be lost or consist of one, or more, chambers, have variable shapes (prolate spheroid to cardioid to T shaped) with a rounded or narrow ducktail caudal termination. The anterior chamber in some otophysans and other groups is likely specialized for hearing and/or sound production. More functional work is needed on these interesting specializations.

  • Swim bladders vary from having no external surface features to ones that contain a thin pliable region (fenestra), a caudal tube (thin membrane) surrounded by a collar and various diverticula. There may be functional parallels between a fenestra and a smaller separate anterior chamber, and this possibility is unexplored.

  • Sonic muscles can be extrinsic (origins on the skull or other places and insertions on the bladder or structures attached to the bladder) or intrinsic (completely attached to the bladder), and there are scorpaenid and tetradontiform fishes with both intrinsic and extrinsic muscles (Yabe, 1985; Parmentier , 2019).

  • Toadfish, and likely most sonic species, have paired sonic muscles that contract in unison, but sea robin muscles contract alternately thus doubling call fundamental frequency with half the contraction speed (Connaughton, 2004).

  • Sonic muscles innervated by occipital spinal nerves or serially by true spinal nerves are not homologous even if they share a similar structure. Molecular and developmental work comparing the genetic basis for these two innervation patterns should be fruitful.

  • Sonic muscles can form embryonically (toadfish) or during puberty (sciaenids). Work is needed on their development in additional species.

  • Antagonistic muscle pairs are rare in swimbladder sound production since they would likely interfere with rapid changes in swim-bladder directional movement necessary to produce sounds. Sonic muscle contraction in a swim bladder will increase internal pressure causing the bladder to return to its resting position without a muscle antagonist and therefore less inertia. Snap-back tendons, only recently found in carapids, can restore swim bladder position rapidly. Muscle antagonists will be present in sound-production systems utilizing pectoral muscles.

  • Physiological work on sound production has been confined to a small suite of species. Future work is likely to uncover new anatomical and physiological adaptations.

  • No identified deep sea fish sound has been recorded from the continental slope despite the presence of numerous species (mostly macrourids and ophidiids) with swim-bladder muscles.

In general, stridulation sounds have received less attention than swim bladder sounds. Grunts (Haemulidae) produce sounds using contact between pharyngeal teeth during feeding although behavioral functions remain unclear (Bertucci , 2014), and pomacentrids produce sounds by jaw slams that cause contact between front teeth. Catfish pectoral stridulation sounds utilize a slip-stick mechanism, and croaking gouramis employ a plucking mechanism (hypertrophied tendons against fin rays) in pectoral sound production (Ladich and Fine, 2006).

Little is known about the evolution of fish sonic structures, which may be homologous within and sometimes between related families. In other cases of convergent evolution, adaptations such as a swim bladder fenestra have arisen independently in ophidiiform fishes, tetradontiforms (Ostracion meleagris and O. cubicus) (Parmentier , 2019), and in the related families (Teraponidae, Glaucosomatidae, and Pempheridae) (Mok , 2011; Parmentier , 2016), and are likely homologous in these three families. Mok (2011) suggested that extrinsic muscles may be a precursor of intrinsic ones. For instance, the toadfish sonic nerve and muscle form embryonically in the occipital (neck) region, migrate, and then attach to the swim bladder where they form an intrinsic muscle (Tracy, 1961). Unfortunately, Tracy's finding leaves no suggestions as to what would select for an intermediate condition, and intermediates are generally unknown. An incipient sonic muscle, which does not reach the swim bladder, or swim bladder diverticula that do not extend sufficiently close to the ears, have no demonstrated function. Might shorter diverticula in Atlantic croaker and spot represent a loss of function? The myriad adaptations utilized in fish sound production suggest difficult but important unanswered physiological, evolutionary, and molecular questions. The realization of swim bladder variability has been underappreciated, and hopefully, others will take a fresh look and likely uncover additional adaptations, particularly since developmental and physiological investigations of sound production have been conducted in a relatively small number of species. Molecular biology, now a gaping hole in the field, should be recruited to help with unanswered questions.

Thanks to Arthur Popper for suggestions on the manuscript and to all the people I have worked with over the years. I would particularly like to thank Tim Cameron, a mechanical engineer, who has collaborated on a number of papers and allowed me to approach sound production in a more sophisticated way, and to Jennifer Stewart who helped convert old figures into JPEG files.

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