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.

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.

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.

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.

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.

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.

Unusual sound production mechanism in the triggerfish Rhinecanthus aculeatus (Balistidae).

The ability to produce sound has been known for decades in Balistidae. Sounds of many species have been recorded and a variety of sound-producing mechanisms have been proposed, including teeth stridulation, collision of the buccal teeth and movements of the fins. The best-supported hypothesis involves movements of the pectoral fin against the lateral part of the swimbladder, called a drumming membrane. In this study, we describe for the first time the sounds made by the blackbar triggerfish Rhinecanthus aculeatus, which are like short drum rolls with an average duration of 85 ms, 193 Hz dominant frequency and 136 dB SPL level at 3 cm distance. The sounds are a series of pulses that result from alternate sweeping movements of the right and left pectoral fins, which push a system of three scutes that are forced against the swimbladder wall. Pulses from each fin occur in consecutive pairs. High-speed videos indicate that each pulse consists of two cycles. The first part of each cycle corresponds to the inward buckling of the scutes, whereas the second part of the cycle corresponds to an apparent passive recoil of the scutes and swimbladder wall. This novel sound production mechanism is probably found in many members of Balistidae because these peculiar scutes occur in other species in the family. Comparison of sound characteristics from fishes of different sizes shows that dominant frequency decreases with size in juveniles but not in adults.

'Habitat-associated soundscape' hypothesis tested on several coral reefs within a lagoon (Bora-Bora Island, French Polynesia).

Coral reefs encompass different habitats that have their own living communities. The present study aimed to test the hypothesis that these different kinds of habitats were characterized by specific soundscapes. Within the lagoon of Bora-Bora, acoustic recordings and visual surveys of substrate type and fish communities were conducted on four reef sites belonging to the three main geomorphological habitats (fringing reef, channel reef, barrier reef) from February to April 2021. Two acoustic parameters were measured for each site and month, during the day and at night: the peak frequency (Fpeak, in Hz) and the corresponding power spectral density (PSDpeak, in dB re 1 µPa2 Hz-1). Our results showed that each geomorphological unit could be characterized by these two parameters and therefore had a specific acoustic signature. Moreover, our study showed that a higher living coral cover was significantly positively correlated with Fpeak in the low-frequency band (50-2000 Hz) during day-time. Although biodiversity indices based on visual surveys did not differ significantly, fish communities and soundscapes were significantly different between sites. Overall, our study underlines the importance of passive acoustics in coral reef monitoring as soundscapes are habitat specific. Supplementary Information: The online version contains supplementary material available at 10.1007/s00227-023-04206-3.

Ultrastructure of sonic muscles of piranhas (Serrasalmidae).

Among piranhas, different species are able to produce sounds but not all of them use the same mechanism. In all species, the sound-producing muscle originates on the second vertebra, but the insertion differs. Pygopristis denticulata can produce two kinds of pulsed sounds emitted in trains. Its sound production mechanism is mainly based on a muscle bundle that inserts between the two first ribs. In Catoprion mento, the anterior part of the sonic muscle inserts directly on the swim bladder. The most derived species (Serrasalmus and Pygocentrus) make all harmonic tonal sounds. Their sonic muscles constitute a single functional unit transversally surrounding the swim bladder. This study aims to study the ultrastructure of sonic muscles in nine species from these four genera. Epaxial muscles were compared with sonic muscles, and the sonic muscles of the different species were compared between them. Results confirmed ultrastructure modifications in the sonic muscles in comparison to epaxial muscles. Fibers of the sonic muscle are thinner and possess a thicker subsarcolemmal ring housing mitochondria. In sonic muscles, myofibrils are also proportionally less abundant, and their sarcomeres are longer and thinner. Some of these differences allows to separate basal species (e.g., P. denticulata) from more derived species (genera Pygocentrus and Serrasalmus) and supposedly support the observed differences in the acoustic abilities.

Use of bioacoustics in species identification: Piranhas from genus Pygocentrus (Teleostei: Serrasalmidae) as a case study.

The genus Pygocentrus contains three valid piranha species (P. cariba, P. nattereri and P. piraya) that are allopatric in tropical and subtropical freshwater environments of South America. This study uses acoustic features to differentiate the three species. Sounds were recorded in P. cariba, two populations of P. nattereri (red- and yellow-bellied) and P. piraya; providing sound description for the first time in P. cariba and P. piraya. Calls of P. cariba were distinct from all the other studied populations. Red- and yellow-bellied P. nattereri calls were different from each other but yellow-bellied P. nattereri calls were similar to those of P. piraya. These observations can be explained by considering that the studied specimens of yellow-bellied P. nattereri have been wrongly identified and are actually a sub-population of P. piraya. Morphological examinations and recent fish field recordings in the Araguari River strongly support our hypothesis. This study shows for the first time that sounds can be used to discover identification errors in the teleost taxa.

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.