Diving into dual functionality: Swim bladder muscles in lionfish for buoyancy and sonic capabilities.

Although the primary function of the swim bladder is buoyancy, it is also involved in hearing, and it can be associated with sonic muscles for voluntary sound production. The use of the swim bladder and associated muscles in sound production could be an exaptation since this is not its first function. We however lack models showing that the same muscles can be used in both movement and sound production. In this study, we investigate the functions of the muscles associated with the swim bladder in different Pteroinae (lionfish) species. Our results indicate that Pterois volitans, P. radiata and Dendrochirus zebra are able to produce long low-frequency hums when disturbed. The deliberate movements of the fin spines during sound production suggest that these sounds may serve as aposematic signals. In P. volitans and P. radiata, hums can be punctuated by intermittent louder pulses called knocks. Analysis of sonic features, morphology, electromyography and histology strongly suggest that these sounds are most likely produced by muscles closely associated with the swim bladder. These muscles originate from the neurocranium and insert on the posterior part of the swim bladder. Additionally, cineradiography supports the hypothesis that these same muscles are involved in altering the swim bladder's length and angle, thereby influencing the pitch of the fish body and participating in manoeuvring and locomotion movements. Fast contraction of the muscle should be related to sound production whereas sustained contractions allows modifications in swim bladder shape and body pitch.

Invertebrate sounds from photic to mesophotic coral reefs reveal vertical stratification and diel diversity.

Although mesophotic coral ecosystems account for approximately 80% of coral reefs, they remain largely unexplored due to their challenging accessibility. The acoustic richness within reefs has led scientists to consider passive acoustic monitoring as a reliable method for studying both altiphotic and mesophotic coral reefs. We investigated the relationship between benthic invertebrate sounds (1.5-22.5 kHz), depth, and benthic cover composition, key ecological factors that determine differences between altiphotic and mesophotic reefs. Diel patterns of snaps and peak frequencies were also explored at different depths to assess variations in biorhythms. Acoustic recorders were deployed at 20 m, 60 m, and 120 m depths across six islands in French Polynesia. The results indicated that depth is the primary driver of differences in broadband transient sound (BTS) soundscapes, with sound intensity decreasing as depth increases. At 20-60 m, sounds were louder at night. At 120 m depth, benthic activity rhythms exhibited low or highly variable levels of diel variation, likely a consequence of reduced solar irradiation. On three islands, a peculiar peak in the number of BTS was observed every day between 7 and 9 PM at 120 m, suggesting the presence of cyclic activities of a specific species. Our results support the existence of different invertebrate communities or distinct behaviors, particularly in deep mesophotic reefs. Overall, this study adds to the growing evidence supporting the use of passive acoustic monitoring to describe and understand ecological patterns in mesophotic reefs.

A new organisational design in skeletal muscle fibres.

In vertebrate skeletal muscles, the architecture of myofibrils is particularly well conserved throughout the taxa. It is composed of suites of repeating functional units called sarcomeres which give the muscle its striated structure. Here, we show that the skeletal sound producing muscles of the cusk eel Parophidion vassali have a different organisation, distinct from the classical type found in textbooks. Within sarcomeres, filaments are not straight lines but have a Y-shaped structure. This looks like chicken wire, with one branch connecting to a branch from the myofibril above and the other connecting to a branch from the myofibril below. This organisation seems to be an adaptation to counteract a trade-off between the speed and force. The low ratio of myofibrils within cell muscles and the high volume of sarcoplasmic reticulum strongly suggest that these muscles are capable of fast contractions. In parallel, the Z-bands are quite wide about 30% of the sarcomere length. This extraordinary long Z-band could smooth out the tension variations found in high-speed muscle contraction, helping to produce sounds with low variabilities in the sound features. Simultaneously, the Y-shaped structure allows having more cross-bridges, increasing the force in this high-speed muscle.

Reliable characterization of sound features in fishes begins in open-water environmentsa).

Many fishes use sounds to communicate in a wide range of behavioral contexts. In monitoring studies, these sounds can be used to detect and identify species. However, being able to confidently link a sound to the correct emitting species requires precise acoustical characterization of the signals in controlled conditions. For practical reasons, this characterization is often performed in small sized aquaria, which, however, may cause sound distortion, and prevents an accurate description of sound characteristics that will ultimately impede sound-based species identification in open-water environments. This study compared the sounds features of five specimens of the silverspot squirrelfish Sargocentron caudimaculatum recorded at sea and in aquaria of different sizes and materials. Our results point out that it is preferable to record fish sounds in an open-water environment rather than in small aquaria because acoustical features are affected (sound duration and dominant frequency) when sounds are recorded in closed environments as a result of reverberation and resonance. If not possible, it is recommended that (1) sound recordings be made in plastic or plexiglass aquaria with respect to glass aquaria and (2) aquaria with the largest dimensions and volumes be chosen.

Bioacoustics supports genus identification in piranhasa).

In different teleost species, sound production can utilize specific coding schemes to avoid confusion between species during communication. Piranhas are vocal Neotropical fishes, and both Pygocentrus and Serrasalmus produce similar pulsed sounds using the same sound-producing mechanism. In this study, we analysed the sounds of three Pygocentrus and nine Serrasalmus species to determine whether sounds can be used to discriminate piranha species at both the species and genus levels. Our analysis of temporal and frequency data supports the idea that the sounds of Serrasalmus and Pygocentrus species are species specific, and that different acoustic features can be used to differentiate taxa at the genus level. Specifically, the sounds of Serrasalmus species are shorter, louder, and have a shorter pulse period (as determined after correction for standard length). This suggests that sounds can be used to support taxonomy at the genus level as well as the species level.

Familiarity reduces aggression but does not modify acoustic communication in pairs of Nile tilapia (Oreochromis niloticus) and black-chinned tilapia (Sarotherodon melanotheron).

Reproduction involves multiple complex behaviours, and the effects of familiarity on such social interactions are seldom described in fish. This is particularly true for sound production and communication within aggressive or non-aggressive context. This study explores the effects of a common garden rearing without parental care of two closely related cichlid species (Nile tilapia Oreochromis niloticus and black-chinned tilapia Sarotherodon melanotheron) on their sound production features and social interactions. After 9 months in common garden rearing, from embryonic stage to first maturity, sound production and associated behaviours were recorded on specimens of the two species in intraspecific and interspecific pairings. The authors found that fish were able to produce the same kind of sounds as those recorded in similar context for their parents. Drum sounds were associated to chasing, lateral attack and courtship in O. niloticus and only to fleeing or avoidance in S. melanotheron. Specific grunts were produced in chasing, after biting and in nest building by O. niloticus, and specific rolling sounds were associated to courtship in S. melanotheron. Sound production and behaviours were not correlated to sex steroid levels, but the number of sounds recorded in aggressive context was correlated to dominance in O. niloticus. The authors conclude that one generation of common garden rearing does not modify sound features, which remain specific and innate in the two cichlids. Despite the familiarity, O. niloticus remained dominant on S. melanotheron, but the aggressiveness between the two species decreased.

Unprecedented Biting Performance in Herbivorous Fish: How the Complex Biting System of Pomacentridae Circumvents Performance Trade-Offs.

AbstractIt is well accepted that the complexity of functional systems may mitigate performance trade-offs. However, data supporting this theory are hard to find because they need to be based on a functional system with different complexity levels in closely related species. The Pomacentridae (damselfishes) provide an excellent opportunity to test this hypothesis because most of the species have two mouth-closing systems: the first using the adductor mandibulae, as in all teleost fishes, and the second relying on the ceratomandibular (cmd) ligament, a synapomorphic trait of the family. Interestingly, some pomacentrids have secondarily lost the cmd ligament during evolution and therefore have a less complex mouth-closing system. Using dissection, kinematic analysis, and mathematical modeling, we demonstrated that the possession of two mouth-closing systems enabled grazing damselfishes to have a forceful and extremely fast bite. This combination challenges a major functional trade-off in fish jaw dynamics, as systems better suited for force transmission are usually less suited for speed transmission, and vice versa. The combination of grazing behavior, small and robust lower jaws (conferring high biting force), and an ultrafast bite is unusual within actinopterygians. These attributes and their associated performance seem to be required conditions to colonize the ecological niche of farming, that is, the maintenance of small filamentous algae crops serving as both food and storage.

Sound production, hearing sensitivity, and in-depth study of the sound-producing muscles in the cowfish (Lactoria cornuta).

The ability to produce sounds has been reported in various Ostraciidae but not deeply studied. In some Ostracion species, two different sound-producing muscles allow these boxfishes to produce two different kinds of sounds in a sequence. This study investigates sound production in another Indo-Pacific species, the longhorn cowfish Lactoria cornuta that also possesses two pairs of sonic muscles associated with the swim bladder: extrinsic sonic muscles (ESMs) and intrinsic sonic muscles (ISMs). The cowfish produces two kinds of sounds called hums and clicks. Hums are made of trains of low amplitude pulses that last for long periods of time, suggesting that they are produced by fatigue-resistant muscles, whereas clicks correspond to shorter sounds with greater amplitude than the hums, suggesting that they result from more powerful contractions. Ultra-structural differences are found between extrinsic and intrinsic sonic muscles. According to features such as long sarcomeres, long I-bands, a high number of mitochondria, and a proliferation of sarcoplasmic reticulum (SR), ESMs would be able to produce fast, strong, and short contractions corresponding to clicks (the shortest sounds with the greatest amplitude). ISMs have the thinnest cells, the smallest number of myofilaments that have long I-bands, the highest volume of mitochondria, and well-developed SR supporting these muscles; these features should generate fast and prolonged contractions that could correspond to the hums that can be produced over long periods of time. A concluding figure shows clear comparisons of the different fibers that were studied in L. cornuta. This study also compared the call features of each sound with the cowfish's hearing ability and supports L. cornuta was more sensitive to frequencies ranging between at least 100 and 400 Hz with thresholds of 128-143 dB re 1 µPa over this range, meaning that they are sensitive to the frequencies produced by conspecifics.

Sound production in piranhas is associated with modifications of the spinal locomotor pattern.

In piranhas, sounds are produced through the vibration of the swim bladder wall caused by the contraction of bilateral sonic muscles. Because they are solely innervated by spinal nerves, these muscles likely evolved from the locomotor hypaxial musculature. The transition from a neuromuscular system initially shaped for slow movements (locomotion) to a system that requires a high contraction rate (sound production) was accompanied with major peripheral structural modifications, yet the associated neural adjustments remain to this date unclear. To close this gap, we investigated the activity of both the locomotor and the sonic musculature using electromyography. The comparison between the activation patterns of both systems highlighted modifications of the neural motor pathway: (1) a transition from a bilateral alternating pattern to a synchronous activation pattern, (2) a switch from a slow- to a high-frequency regime, and (3) an increase in the synchrony of motor neuron activation. Furthermore, our results demonstrate that sound features correspond to the activity of the sonic muscles, as both the variation patterns of periods and amplitudes of sounds highly correspond to those seen in the sonic muscle electromyograms (EMGsonic). Assuming that the premotor network for sound production in piranhas is of spinal origin, our results show that the neural circuit associated with spinal motor neurons transitioned from the slow alternating pattern originally used for locomotion to a much faster simultaneous activation pattern to generate vocal signals.

Acoustic homogeneity in the piranha Serrasalmus maculatus.

Different studies suggest some social calls could be used in fish identification if their specificity is unambiguously assessed. Sounds of different populations of piranhas Serrasalmus maculatus Kner, 1858 were recorded to determine their homogeneity between rivers inside a single basin (Araguari and Grande River, upper Paraná River basin) and between separated basins (Amazon and Paraná basins). All fish from the different populations produced sounds with similar acoustic features. Consequently, the populations were not discernible based on individual sound characteristics. This high homogeneity between sounds from different populations indicates their usefulness for conservation projects using passive acoustic monitoring in piranhas. Moreover, it supports the use of acoustic features as complementary key characteristics in taxonomic studies.

Microstructural and compositional variation in pacu and piranha teeth related to diet specialization (Teleostei: Serrasalmidae).

In any vertebrate group, tooth shape is known to fit with a biological function related to diet. However, little is known about the relationships between diet and tooth microstructure and composition in teleost fishes. In this work, we describe the external morphology, internal microstructure and elemental composition of the oral teeth of three representative species of the family Serrasalmidae having different feeding habits (herbivorous vs. omnivorous vs. carnivorous). We used backscattered-electron imaging and low vacuum environmental scanning electron microscope to compare the organization and mineralization of tooth layers as well as energy dispersive X-ray microanalysis and Raman microspectrometry to investigate the elemental composition, Ca/P ratio and mineralogy of the most superficial layers. Oral teeth of each serrasalmid species have the same internal organization based on five distinctive layers (i.e. pulp, dentine, inner enameloid, outer enameloid and cuticle) but the general tooth morphology is different according to diet. Microstructural and compositional variation of the cuticle and iron-enrichment of superficial layers were highlighted between herbivorous and carnivorous species. Iron is more concentrated in teeth of the herbivorous species where it is associated with a thicker cuticle explaining the more intense red-pigmentation of the cutting edges of oral teeth. The iron-enrichment is interpreted as a substitution of Ca by Fe in the hydroxyapatite. These traits are discussed in the light of the evolutionary history of the family. Further considerations and hypotheses about the formation and origin of the mineralized tooth layers and especially the iron-rich superficial layers in teleost fishes are suggested.

The development of hearing abilities in the shark Scyliorhinus canicula.

The few works on audition in sharks and rays concern only adult specimens. We report the hearing abilities in the dogfish Scyliorhinus canicula at different stages, from embryos that still have their yolk sac inside their egg, to juveniles. Hearing development corresponds to an increase in the frequency range from 100-300 Hz in early pre-hatching stages to 100-600 Hz in juveniles. Modifications in hearing abilities correspond to the development of the brain, the increase of the volume of the membranous labyrinth, the growth of the sensory epithelium, and the development of stereocilia in addition to kinocilium before hatching. This work offers solid insights into the development of hearing abilities that usually can only be inferred from the anatomy of vertebrates or after birth/hatching. It shows also that shark can be sensitive to background noise during development.

Local sonic activity reveals potential partitioning in a coral reef fish community.

How vocal organisms share acoustic space has primarily received attention in terrestrial environments. Comparable studies in marine environments, however, remain rare. By recording sounds on a coral reef in French Polynesia for 48 h and 24 h, this study provides first insights on how different sound types are distributed within the acoustic space and may create acoustic niches optimizing acoustic communication within a highly diverse community containing numerous soniferous fish species. Day-time was dominated by two to six sound types, while recordings performed at night revealed a more diverse vocal community made of up to nineteen sound types. Calling activity was distributed over time allowing each sound type to dominate the soundscape sequentially. Additionally, differences in the acoustic features of sounds occurring during the same period were observed. Such partitioning in time and acoustic spaces would reduce potential overlaps of sounds produced by vocal species living in sympatry in coral reefs.

Fish biophony in a Mediterranean submarine canyon.

Although several bioacoustics investigations have shed light on the acoustic communication of Mediterranean fish species, the occurrence of fish sounds has never been reported below -40 m depth. This study assessed the occurrence of fish sounds at greater depths by monitoring the soundscape of a Mediterranean submarine canyon (Calvi, France) thanks to a combination of Static Acoustic Monitoring (three stations, from -125 to -150 m depth, 3 km from coastline) and of hydrophone-integrated gliders (Mobile Acoustic Monitoring; from -60 to -900 m depth, 3-6 km from coastline). Biological sounds were detected in 38% of the audio files; ten sound types (for a total of more than 9.000 sounds) with characteristics corresponding to those emitted by vocal species, or known as produced by fish activities, were found. For one of these sound types, emitter identity was inferred at the genus level (Ophidion sp.). An increase of from 10 to 15 dB re 1 µPa in sea ambient noise was observed during daytime hours due to boat traffic, potentially implying an important daytime masking effect. This study shows that monitoring the underwater soundscape of Mediterranean submarine canyons can provide holistic information needed to better understand the state and the dynamics of these heterogeneous, highly diverse environments.

Yellow-eyed piranhas produce louder sounds than red-eyed piranhas in an invasive population of Serrasalmus marginatus.

Serrasalmus marginatus is a piranha species native from the lower Paraná River basin and has been invasive in the upper Paraná River basin since the 1980s. In piranhas, sounds of different species have different features. The aim of this study was to investigate if the sounds produced by this species could be used to distinguish two morphotypes: red- and yellow-eyed S. marginatus from the Araguari River (upper Paraná River basin). All the temporal and frequency features of the sounds were equivalent in both groups of eye colour; it corresponds to the species-specific signature described for S. marginatus. Nonetheless, the amplitude features were all statistically different between red- and yellow-eyed piranhas. Yellow-eyed specimens produced louder sounds. In different fish species, colour change in eyes can be due to the absence or the presence of a dominant allele. It can also be involved in social rank or during reproduction. Different hormones and neuropeptides can modulate vocal features. It is hypothesized that a mutation or different hormonal concentrations could explain both sound amplitude and eye colour playing a role in animal communication in S. marginatus.

Divergent evolutionary morphology of the axial skeleton as a potential key innovation in modern cetaceans.

Cetaceans represent the most diverse clade of extant marine tetrapods. Although the restructuring of oceans could have contributed to their diversity, other factors might also be involved. Similar to ichthyosaurs and sharks, variation of morphological traits could have promoted the colonization of new ecological niches and supported their diversification. By combining morphological data describing the axial skeleton of 73 cetacean species with phylogenetic comparative methods, we demonstrate that the vertebral morphology of cetaceans is associated with their habitat. All riverine and coastal species possess a small body size, lengthened vertebrae and a low vertebral count compared with open ocean species. Extant cetaceans have followed two distinct evolutionary pathways relative to their ecology. Whereas most offshore species such as baleen whales evolved towards an increased body size while retaining a low vertebral count, small oceanic dolphins underwent deep modifications of their axial skeleton with an extremely high number of short vertebrae. Our comparative analyses provide evidence these vertebral modifications have potentially operated as key innovations. These novelties contributed to their explosive radiation, resulting in an efficient swimming style that provides energetic advantages to small-sized species.

Sea chordophones make the mysterious /Kwa/ sound: identification of the emitter of the dominant fish sound in Mediterranean seagrass meadows.

The /Kwa/ vocalization dominates the soundscape of Posidonia oceanica meadows but the identity of the species emitting this peculiar fish sound remains a mystery. Information from sounds recorded in the wild indicates that the emitting candidates should be abundant, nocturnal and benthic. Scorpaena spp. combine all these characteristics. This study used an interdisciplinary approach to investigate the vocal abilities of Scorpaena spp.; morphological, histological and electrophysiological examinations were interpreted together with visual and acoustic recordings conducted in semi-natural conditions. All observed Scorpaena spp. (S. porcus, S. scrofa and S. notata) share the same sonic apparatus at the level of the abdominal region. This apparatus, present in both males and females, consists of 3 bilaterally symmetrical muscular bundles, having 3-5 long tendons, which insert on ventral bony apophyses of the vertebral bodies. In all chordophones (stringed instruments), the frequency of the vibration is dependent on the string properties and not on the rate at which the strings are plucked. Similarly, we suggest that each of the 3-5 tendons found in the sonic mechanism of Scorpaena spp. acts as a frequency multiplier of the muscular bundle contractions, where the resonant properties of the tendons determine the peak frequency of the /Kwa/, its frequency spectra and pseudo-harmonic profile. The variability in the length and number of tendons found between and within species could explain the high variability of /Kwa/ acoustic features recorded in the wild. Finally, acoustic and behavioural experiments confirmed that Scorpaena spp. can emit the /Kwa/ sound.

Sound production mechanism in triggerfish (Balistidae): a synapomorphy.

The ability to produce sounds for acoustic communication is known in different Balistidae species but the eventual synapomorphic aspect of the mechanism remains to be shown. In Rhinecanthus aculeatus, sounds result from alternate sweeping movements of the right and left pectoral fins, which push a system of three scutes against the swim bladder wall. In this study, we made a comparison between the sounds produced by this species and two additional ones (Balistapus undulatus and Rhinecanthus rectangulus) using hand-held specimens to provide a description of the sound mechanism. The results highlighted that the sound production mechanism is similar in the three species. According to recent phylogenetic data and shared morphological features, this mechanism could be common to the majority of Balistidae family members and all species could be capable of sound production using pectoral fins.

Environmental constraints drive the partitioning of the soundscape in fishes.

The underwater environment is more and more being depicted as particularly noisy, and the inventory of calling fishes is continuously increasing. However, it currently remains unknown how species share the soundscape and are able to communicate without misinterpreting the messages. Different mechanisms of interference avoidance have been documented in birds, mammals, and frogs, but little is known about interference avoidance in fishes. How fish thus partition the soundscape underwater remains unknown, as acoustic communication and its organization have never been studied at the level of fish communities. In this study, passive acoustic recordings were used to inventory sounds produced in a fish community (120 m depth) in an attempt to understand how different species partition the acoustic environment. We uncovered an important diversity of fish sounds, and 16 of the 37 different sounds recorded were sufficiently abundant to use in a quantitative analysis. We show that sonic activity allows a clear distinction between a diurnal and a nocturnal group of fishes. Moreover, frequencies of signals made during the day overlap, whereas there is a clear distinction between the different representatives of the nocturnal callers because of a lack of overlap in sound frequency. This first demonstration, to our knowledge, of interference avoidance in a fish community can be understood by the way sounds are used. In diurnal species, sounds are mostly used to support visual display, whereas nocturnal species are generally deprived of visual cues, resulting in acoustic constraints being more important.

Sound-production mechanism in Pomatoschistus pictus.

Fish acoustic signals play a major role during agonistic and reproductive interactions. Among the sound-generating fish, Gobiidae, a large fish family with 1866 valid species, is one of the most studied groups of acoustic fishes, with sound production being documented in a number of species. Paradoxically, the sound-producing mechanism remains poorly studied in this group. The painted goby, Pomatoschistus pictus, produces two distinct sounds called drums and thumps. A combination of morphological and experimental analyses involving high-speed videos synchronized with sound recordings supports that drums are produced during lateral head movements involving at least the alternate contractions of the levator pectoralis muscles originating on the skull and inserting on the pectoral girdle. These movements are reported in many Gobiidae species, suggesting the pectoral-girdle-based mechanism is common in the family and could have evolved from locomotory movements.