Introduction to the special issue on fish bioacoustics: Hearing and sound communicationa).

Fish bioacoustics, or the study of fish hearing, sound production, and acoustic communication, was discussed as early as Aristotle. However, questions about how fishes hear were not really addressed until the early 20th century. Work on fish bioacoustics grew after World War II and considerably in the 21st century since investigators, regulators, and others realized that anthropogenic (human-generated sounds), which had primarily been of interest to workers on marine mammals, was likely to have a major impact on fishes (as well as on aquatic invertebrates). Moreover, passive acoustic monitoring of fishes, recording fish sounds in the field, has blossomed as a noninvasive technique for sampling abundance, distribution, and reproduction of various sonic fishes. The field is vital since fishes and aquatic invertebrates make up a major portion of the protein eaten by a signification portion of humans. To help better understand fish bioacoustics and engage it with issues of anthropogenic sound, this special issue of The Journal of the Acoustical Society of America (JASA) brings together papers that explore the breadth of the topic, from a historical perspective to the latest findings on the impact of anthropogenic sounds on fishes.

Vocal repertoire and sound characteristics in the variegated cardinalfish, Fowleria variegata (Pisces: Apogonidae).

The variegated cardinalfish Fowleria variegata produces grunt and hoot calls during agonistic and courtship interactions. Both sounds are tonal and occur as single and multiunit calls. Grunts are of short duration with variable frequency spectra. Hoots are longer, have a higher fundamental frequency, and a more developed harmonic structure. Agonistic grunt calls and short hoot calls (1-2 hoots) are produced during chases and when striking an individual or a mirror. Grunts are produced primarily in male-female and mirror-image encounters, and short hoot calls are produced primarily in male-male interactions. During the reproductive period, long hoot calls (three and four hoots) are the main sound type in a mix-sexed tank and at Dongsha Atoll. These are likely produced by males because isolated females are silent, and isolated males emit long hoot calls. Courtship interactions are mostly silent, and males are silent after capturing eggs for oral brooding. Tank sounds peak at dusk to early evening with a smaller peak at noon, although there are dusk and dawn peaks at Dongsha Atoll. Tank sounds exhibit a semilunar rhythm with peaks at the new and full moon. Other cardinalfish species from the atoll produce grunts but not hoot calls.

An investigation of bubble resonance and its implications for sound production by deep-water fishes.

Although the continental slope and abyss comprise the largest habitat on earth, the absence of documented fish sounds from deep waters is striking. Fishes with sexually dimorphic muscles attached to their swim bladders suggests that sounds are likely used in male courtship on the upper, mid and lower continental slope. To investigate the effects of environmental extremes on fish sound production, the acoustic behavior of a driven bubble is examined. This study is also relevant to target strength of sonar returns from fish and hearing in auditory specialist fishes. A bubble is a classic, if imperfect, model for swim bladder behavior since the swim-bladder wall is an anisotropic viscoelastic structure responsible for rapid damping. Acoustic properties of bubbles-including far-field resonant frequency, damping factor, and quality factor-are calculated in warm and cold surface conditions and in cold deep-water (depths 1000 m, 2000 m, and 3500 m) conditions using parameters for oxygen and nitrogen, the dominant gases in swim bladders. The far-field resonant frequency and damping factor of a bubble increase with depth, and the scattering cross-section and quality factor decrease with depth. These acoustic properties scale with undamped oscillation frequency of the bubble and do not vary significantly due to gas type or temperature. Bubbles in the deep-water environments are much less efficient radiators of sound than bubbles near the surface because the far-field radiated power for the same excitation decreases with depth. A bubble at depth 3500 m has a 25 dB loss in radiated sound power compared to the same-radius bubble at the surface. This reduction of radiation efficiency in deep water likely contributes to the absence of fish sound recordings in those environments.

Sound production and mechanism in the cryptic cusk-eel Parophidion vassali.

This study investigates the sounds and the anatomy of the sound-producing organ in the male and female sand-dwelling cusk-eel Parophidion vassali. Although both sexes have similar external phenotype, they can be distinguished by their sonic apparatus and sounds. As in many Ophioidei, Parophidion vassali presents a panel of highly derived characters. Fish possess three pairs of sonic muscles, and males have mineralized swimbladder caps on which inserts the ventral sonic muscle, a neural arch that pivots, a stretchable swimbladder fenestra, an osseous swimbladder plate and a rounded pressure-release membrane in the caudal swimbladder. Females, however, do not possess anterior swimbladder caps, a swimbladder fenestra and the caudal rounded membrane. Males possess the unusual ability to produce sounds starting with a set of low amplitude pulses followed by a second set with higher amplitudes clearly dividing each sound unit into two parts. Females do not vary their sound amplitude in this way: they produce shorter sounds and pulse periods but with a higher peak frequency. Morphology and sound features support the sound-producing mechanism is based on a rebound system (i.e. quick backward snap of the anterior swimbladder). Based on features of the sounds from tank recordings, we have putatively identified the sound of male Parophidion vassali at sea. As these species are ecologically cryptic, we hope this work will allow assessment and clarify the distribution of their populations.

A sciaenid swim bladder with long skinny fingers produces sound with an unusual frequency spectrum.

Swim bladders in sciaenid fishes function in hearing in some and sound production in almost all species. Sciaenid swim bladders vary from simple carrot-shaped to two-chambered to possessing various diverticula. Diverticula that terminate close to the ears improve hearing. Other unusual diverticula heading in a caudal direction have not been studied. The fresh-water Asian species Boesemania microlepis has an unusual swim bladder with a slightly restricted anterior region and 6 long-slender caudally-directed diverticula bilaterally. We hypothesized that these diverticula modify sound spectra. Evening advertisement calls consist of a series of multicycle tonal pulses, but the fundamental frequency and first several harmonics are missing or attenuated, and peak frequencies are high, varying between < 1-2 kHz. The fundamental frequency is reflected in the pulse repetition rate and in ripples on the frequency spectrum but not in the number of cycles within a pulse. We suggest that diverticula function as Helmholz absorbers turning the swim bladder into a high-pass filter responsible for the absence of low frequencies typically present in sciaenid calls. Further, we hypothesize that the multicycle pulses are driven by the stretched aponeuroses (flat tendons that connect the sonic muscles to the swim bladder) in this and other sciaenids.

Disturbance calls of five migratory Characiformes species and advertisement choruses in Amazon spawning sites.

Species-specific disturbance calls of five commercially-important characiform species are described, the Curimatidae commonly called branquinhas: Potamorhina latior, Potamorhina altamazonica and Psectrogaster amazonica; Prochilodontidae: jaraquí Semaprochilodus insignis and curimatã Prochilodus nigricans. All species have a two-chambered swimbladder and the sonic mechanism, present exclusively in males, utilises hypertrophied red muscles between ribs that adhere to the anterior chamber. The number of muscles is unusually plastic across species and varies from 1 to 4 pairs suggesting considerable evolution in an otherwise conservative system. Advertisement calls are produced in river confluences in the Madeira Basin during the high-water mating season (January-February). Disturbance calls and sampling allowed recognition of underwater advertisement choruses from P. latior, S. insignis and P. nigricans. The advertisement calls of the first two species have largely similar characteristics and they mate in partially overlapping areas in the Guaporé River. However, P. latior sounds have a lower dominant frequency and it prefers to call from river confluences whereas S. insignis shoals occur mostly in the main river channel adjacent to the confluence. These results help identify and differentiate underwater sounds and evaluate breeding areas during the courtship of commercially important characids likely to be affected by two hydroelectric dams.

Simultaneous production of two kinds of sounds in relation with sonic mechanism in the boxfish Ostracion meleagris and O. cubicus.

In fishes, sonic abilities for communication purpose usually involve a single mechanism. We describe here the sonic mechanism and sounds in two species of boxfish, the spotted trunkfish Ostracion meleagris and the yellow boxfish Ostracion cubicus. The sonic mechanism utilizes a T-shaped swimbladder with a swimbladder fenestra and two separate sonic muscle pairs. Extrinsic vertical muscles attach to the vertebral column and the swimbladder. Perpendicularly and below these muscles, longitudinal intrinsic muscles cover the swimbladder fenestra. Sounds are exceptional since they are made of two distinct types produced in a sequence. In both species, humming sounds consist of long series (up to 45 s) of hundreds of regular low-amplitude pulses. Hums are often interspersed with irregular click sounds with an amplitude that is ten times greater in O. meleagris and forty times greater in O. cubicus. There is no relationship between fish size and many acoustic characteristics because muscle contraction rate dictates the fundamental frequency. We suggest that hums and clicks are produced by either separate muscles or by a combination of the two. The mechanism complexity supports an investment of boxfish in this communication channel and underline sounds as having important functions in their way of life.

Taxonomic validation of Encheliophis chardewalli with description of calling abilities.

Encheliophis chardewalli was described from a single cleared and stained specimen. Twelve years later, additional specimens were found in the lagoon of Moorea (French Polynesia) in association with their host, the sea cucumber Actinopyga mauritiana. These fish were used to consolidate the species diagnosis, to validate species status and to record sound production. This species is remarkable because of its ability to penetrate inside the cloaca of sea cucumbers having anal teeth and the fact this species is largely unknown despite it lives in lagoons in 1m depth. Encheliophis chardewalli produced three sound types: long regular calls made of trains of numerous pulses, short irregular calls characterized by a constant lowering of its pulse period and short regular call (or knock) made of 3 to 6 pulses. Comparison with other sympatric Carapini supports a large and distinct repertoire. Morphological characteristics could be the result of reduced body size allowing to penetrate inside a new host, thus avoiding competition and conflict with other larger sympatric Carapini species.

Wall structure and material properties cause viscous damping of swimbladder sounds in the oyster toadfish Opsanus tau.

Despite rapid damping, fish swimbladders have been modelled as underwater resonant bubbles. Recent data suggest that swimbladders of sound-producing fishes use a forced rather than a resonant response to produce sound. The reason for this discrepancy has not been formally addressed, and we demonstrate, for the first time, that the structure of the swimbladder wall will affect vibratory behaviour. Using the oyster toadfish Opsanus tau, we find regional differences in bladder thickness, directionality of collagen layers (anisotropic bladder wall structure), material properties that differ between circular and longitudinal directions (stress, strain and Young's modulus), high water content (80%) of the bladder wall and a 300-fold increase in the modulus of dried tissue. Therefore, the swimbladder wall is a viscoelastic structure that serves to damp vibrations and impart directionality, preventing the expression of resonance.

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.

Grunt variation in the oyster toadfish Opsanus tau: effect of size and sex.

As in insects, frogs and birds, vocal activity in fishes tends to be more developed in males than in females, and sonic swimbladder muscles may be sexually dimorphic, i.e., either larger in males or present only in males. Male oyster toadfish Opsanus tau L produce a long duration, tonal boatwhistle advertisement call, and both sexes grunt, a short duration more pulsatile agonistic call. Sonic muscles are present in both sexes but larger in males. We tested the hypothesis that males would call more than females by inducing grunts in toadfish of various sizes held in a net and determined incidence of calling and developmental changes in grunt parameters. A small number of fish were recorded twice to examine call repeatability. Both sexes were equally likely to grunt, and grunt parameters (sound pressure level (SPL), individual range in SPL, number of grunts, and fundamental frequency) were similar in both sexes. SPL increased with fish size before leveling off in fish >200 g, and fundamental frequency and other parameters did not change with fish size. Number of grunts in a train, grunt duration and inter-grunt interval were highly variable in fish recorded twice suggesting that grunt parameters reflect internal motivation rather than different messages. Grunt production may explain the presence of well-developed sonic muscles in females and suggests that females have an active but unexplored vocal life.

Pectoral sound generation in the blue catfish Ictalurus furcatus.

Catfishes produce pectoral stridulatory sounds by "jerk" movements that rub ridges on the dorsal process against the cleithrum. We recorded sound synchronized with high-speed video to investigate the hypothesis that blue catfish Ictalurus furcatus produce sounds by a slip-stick mechanism, previously described only in invertebrates. Blue catfish produce a variably paced series of sound pulses during abduction sweeps (pulsers) although some individuals (sliders) form longer duration sound units (slides) interspersed with pulses. Typical pulser sounds are evoked by short 1-2 ms movements with a rotation of 2°-3°. Jerks excite sounds that increase in amplitude after motion stops, suggesting constructive interference, which decays before the next jerk. Longer contact of the ridges produces a more steady-state sound in slides. Pulse pattern during stridulation is determined by pauses without movement: the spine moves during about 14 % of the abduction sweep in pulsers (~45 % in sliders) although movement appears continuous to the human eye. Spine rotation parameters do not predict pulse amplitude, but amplitude correlates with pause duration suggesting that force between the dorsal process and cleithrum increases with longer pauses. Sound production, stimulated by a series of rapid movements that set the pectoral girdle into resonance, is caused by a slip-stick mechanism.

Developmental variation in sound production in water and air in the blue catfish Ictalurus furcatus.

Blue catfish, Ictalurus furcatus, the largest catfish in North America, produce pectoral stridulation sounds (distress calls) when attacked and held. They have both fish and bird predators, and the frequency spectrum of their sounds is better matched to the hearing of birds than to that of unspecialized fish predators with low frequency hearing. It is unclear whether their sounds evolved to function in air or water. We categorized the calls and how they change with fish size in air and water and compared developmental changes in call parameters with stridulation motions captured with a high-speed camera. Stridulation sounds consist of a variable series of pulses produced during abduction of the pectoral spine. Pulses are caused by quick rapid spine rotations (jerks) of the pectoral spine that do not change with fish size although larger individuals generate longer, higher amplitude pulses with lower peak frequencies. There are longer pauses between jerks, and therefore fewer jerks and fewer pulses, in larger fish, which take longer to abduct their spines and therefore produce a longer series of pulses per abduction sweep. Sounds couple more effectively to water (1400 times greater pressure in Pascals at 1 m), are more sharply tuned and have lower peak frequencies than in air. Blue catfish stridulation sounds appear to be specialized to produce underwater signals although most of the sound spectrum includes frequencies matched to catfish hearing but largely above the hearing range of unspecialized fishes.

Spatiotemporal variability and sound characterization in silver croaker Plagioscion squamosissimus (Sciaenidae) in the Central Amazon.

BACKGROUND: The fish family Sciaenidae has numerous species that produce sounds with superfast muscles that vibrate the swimbladder. These muscles form post embryonically and undergo seasonal hypertrophy-atrophy cycles. The family has been the focus of numerous passive acoustic studies to localize spatial and temporal occurrence of spawning aggregations. Fishes produce disturbance calls when hand-held, and males form aggregations in late afternoon and produce advertisement calls to attract females for mating. Previous studies on five continents have been confined to temperate species. Here we examine the calls of the silver croaker Plagioscion squamosissimus, a freshwater equatorial species, which experiences constant photoperiod, minimal temperature variation but seasonal changes in water depth and color, pH and conductivity. METHODS AND PRINCIPAL FINDINGS: Dissections indicate that sonic muscles are present exclusively in males and that muscles are thicker and redder during the mating season. Disturbance calls were recorded in hand-held fish during the low-water mating season and high-water period outside of the mating season. Advertisement calls were recorded from wild fish that formed aggregations in both periods but only during the mating season from fish in large cages. Disturbance calls consist of a series of short individual pulses in mature males. Advertisement calls start with single and paired pulses followed by greater amplitude multi-pulse bursts with higher peak frequencies than in disturbance calls. Advertisement-like calls also occur in aggregations during the off season, but bursts are shorter with fewer pulses. CONCLUSIONS AND SIGNIFICANCE: Silver croaker produce complex advertisement calls that vary in amplitude, number of cycles per burst and burst duration of their calls. Unlike temperate sciaenids, which only call during the spawning season, silver croaker produce advertisement calls in both seasons. Sonic muscles are thinner, and bursts are shorter than at the spawning peak, but males still produce complex calls outside of the mating season.

Reduction of the pectoral spine and girdle in domesticated Channel catfish is likely caused by changes in selection pressure.

Locked pectoral spines of the Channel Catfish Ictalurus punctatus more than double the fish's width and complicate ingestion by gape-limited predators. The spine mates with the pectoral girdle, a robust structure that anchors the spine. This study demonstrates that both spine and girdle exhibit negative allometric growth and that pectoral spines and girdles are lighter in domesticated than in wild Channel Catfish. This finding could be explained by changes in selection pressure for spine growth during domestication or by an epigenetic effect in which exposure to predators in wild fish stimulates pectoral growth. We tested the epigenetic hypothesis by exposing domesticated Channel Catfish fingerlings to Largemouth Bass Micropterus salmoides predators for 13 weeks. Spines and girdles grow isometrically in the fingerlings, and regression analysis indicates no difference in proportional pectoral growth between control and predator-exposed fish. Therefore a change in selection pressure likely accounts for smaller pectoral growth in domesticated Channel Catfish. Decreasing spine growth in older fish suggests anti-predator functions are most important in smaller fish. Additionally, growth of the appendicular and axial skeleton is controlled differentially, and mechanical properties of the spine and not just its length are an important component of this defensive adaptation.

Characterization and generation of male courtship song in Cotesia congregata (Hymenoptera: Braconidae).

BACKGROUND: Male parasitic wasps attract females with a courtship song produced by rapid wing fanning. Songs have been described for several parasitic wasp species; however, beyond association with wing fanning, the mechanism of sound generation has not been examined. We characterized the male courtship song of Cotesia congregata (Hymenoptera: Braconidae) and investigated the biomechanics of sound production. METHODS AND PRINCIPAL FINDINGS: Courtship songs were recorded using high-speed videography (2,000 fps) and audio recordings. The song consists of a long duration amplitude-modulated "buzz" followed by a series of pulsatile higher amplitude "boings," each decaying into a terminal buzz followed by a short inter-boing pause while wings are stationary. Boings have higher amplitude and lower frequency than buzz components. The lower frequency of the boing sound is due to greater wing displacement. The power spectrum is a harmonic series dominated by wing repetition rate ∼220 Hz, but the sound waveform indicates a higher frequency resonance ∼5 kHz. Sound is not generated by the wings contacting each other, the substrate, or the abdomen. The abdomen is elevated during the first several wing cycles of the boing, but its position is unrelated to sound amplitude. Unlike most sounds generated by volume velocity, the boing is generated at the termination of the wing down stroke when displacement is maximal and wing velocity is zero. Calculation indicates a low Reynolds number of ∼1000. CONCLUSIONS AND SIGNIFICANCE: Acoustic pressure is proportional to velocity for typical sound sources. Our finding that the boing sound was generated at maximal wing displacement coincident with cessation of wing motion indicates that it is caused by acceleration of the wing tips, consistent with a dipole source. The low Reynolds number requires a high wing flap rate for flight and predisposes wings of small insects for sound production.

Description and scaling of pectoral muscles in ictalurid catfishes.

The pectoral spine of catfishes is an antipredator adaptation that can be bound, locked, and rubbed against the cleithrum to produce stridulation sounds. We describe muscle morphology of the pectoral spines and rays in six species in four genera of North American ictalurid catfishes. Since homologies of catfish pectoral muscles have not been universally accepted, we designate them functionally as the spine abductor and adductor and the arrector dorsalis and ventralis. The four muscles of the remaining pectoral rays are the superficial and deep (profundal) abductors and adductors. The large spine abductor and spine adductor are responsible for large amplitude movements, and the smaller arrector dorsalis and arrector ventralis have more specialized functions, that is, spine elevation and depression, respectively, although they also contribute to spine abduction. Three of the four spine muscles were pennate (the abductor and two arrectors), the spine adductor can be pennate or parallel, and ray muscles have parallel fibers. Insertions of pectoral muscles are similar across species, but there is a shift of origins in some muscles, particularly of the superficial abductor of the pectoral rays, which assumes a midline position in Ictalurus and increasingly more lateral placement in Ameiurus (one quarter way out from the midline), and Pylodictis and Noturus (half way out). Coincident with this lateral shift, the attachments of the hypaxial muscle to the ventral girdle become more robust. Comparison with its sister group supports the midline position as basal and lateral migration as derived. The muscles of the pectoral spine are heavier than muscles of the remaining rays in all species but the flathead, supporting the importance of specialized spine functions above typical movement. Further, spine muscles were larger than ray muscles in all species but the flathead catfish, which lives in water with the fastest currents.

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.

Calls of the black drum (Pogonias cromis: Sciaenidae): geographical differences in sound production between northern and southern hemisphere populations.

Because of apparent reproductive isolation between Northern and Southern hemisphere populations of the black drum Pogonius cromis, we tested the hypothesis that advertisement calls from a southern population would differ from known calls of North American populations. Additionally, we quantified disturbance and advertisement calls, their changes with fish size and sex, not previously examined in this species. Unlike most sciaenids, both sexes of P. cromis possess robust sonic muscles, and both produce disturbance calls when handled. However, only males produce an advertisement call used in courtship. The disturbance call consists of a variable train of short-duration pulses (average 23 ms). The duration, interpulse interval, and dominant frequency of pulses are similar in males and females and change developmentally: pulse duration and interpulse interval increase and dominant frequency decreases with fish size. Advertisement calls, recorded in the field and in captivity, are long-duration (average 184 ms) and tonal. Based on variation in fundamental frequency, which decreases with fish size, field choruses are composed of different-sized individuals. The duration of advertisement calls, about a third of those from Florida populations, suggests genetic differentiation between northern and southern populations.

Changes in age composition and growth characteristics of Atlantic sturgeon (Acipenser oxyrinchus oxyrinchus) over 400 years.

Populations of sturgeon (Acipenseridae) have experienced global declines, and in some cases extirpation, during the past century. In the current era of climate change and over-harvesting of fishery resources, climate models, based on uncertain boundary conditions, are being used to predict future effects on the Earth's biota. A collection of approximately 400-year-old Atlantic sturgeon spines from a midden in colonial Jamestown, VA, USA, allowed us to compare the age structure and growth rate for a pre-industrial population during a 'mini-ice age' with samples collected from the modern population in the same reach of the James River. Compared with modern fish, the colonial population was characterized by larger and older individuals and exhibited significantly slower growth rates, which were comparable with modern populations at higher latitudes of North America. These results may relate to higher population densities and/or colder water temperatures during colonial times.