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.

One-Year Follow-Up of Subthalamic Nucleus Deep Brain Stimulation in SNCA Mutation Parkinsonism: A Case Report.

Background: Deep brain stimulation (DBS) has shown some efficacy in monogenic Parkinson's disease; however, data about its long-term benefit in SNCA mutations remain scarce. Case report: Subthalamic nucleus DBS was implanted in a 60-year-old female patient with Parkinson's disease due to SNCA duplication. One year later, the patient walked unassisted and was independent for most activities of daily living, without requiring any anti-Parkinson's medication. Discussion: To our knowledge, four cases of bilateral subthalamic DBS have been reported previously. This case report adds an additional body of evidence of improved one-year outcome after DBS surgery in a patient with SNCA mutation. Highlights: This is a case report of a patient with genetic parkinsonism due to SNCA duplication undergoing bilateral subthalamic nucleus (STN) deep brain stimulation (DBS) surgery. The outcome was favorable one year after implantation, with the patient coming off all anti-Parkinson's medications. This further clarifies DBS outcome in monogenic Parkinson's disease.

Correction: Vocal repertoire and consistency of call features in the meagre Argyrosomous regius (Asso, 1801).

[This corrects the article DOI: 10.1371/journal.pone.0241792.].

Endemic fish calling: Acoustics and reproductive behaviour of the Neretva dwarf goby Orsinigobius croaticus.

The Neretva dwarf goby Orsinigobius croaticus (Gobiiformes, Gobionellidae) is an endemic fish native to the freshwaters of the Adriatic Basin in Croatia and Bosnia and Herzegovina, a Mediterranean Biodiversity Hotspot. Due to its limited distribution range, specific karst habitat and endangered status, laboratory studies on reproductive biology are scarce but crucial. Herein, we investigated the sound production and acoustic behaviour of the endangered O. croaticus during reproductive intersexual laboratory encounters, utilising an interdisciplinary approach. We also performed dissections and micro-computed tomography (µCT) scanning of the pectoral girdle to explore its potential involvement in sound production. Finally, comparative acoustic analysis was conducted on sounds produced by previously recorded soniferous sand gobies to investigate whether acoustic features are species-specific. The endemic O. croaticus is a soniferous species. Males of this species emit pulsatile sounds composed of a variable number of short (~15 ms) consecutive pulses when interacting with females, usually during the pre-spawning phase in the nest, but also during courtship outside the nest. Pulsatile sounds were low-frequency and short pulse trains (~140 Hz, <1000 ms). Male visual behaviour rate was higher when co-occurring with sounds and females entered the male's nest significantly more frequently when sounds were present. Characteristic body movements accompanied male sound production, such as head thrust and fin spreading. Furthermore, µCT scans and dissections suggest that O. croaticus shares certain anatomical similarities of the pectoral girdle (i.e. osseous elements and arrangement of levator pectoralis muscles) to previously studied sand gobies that could be involved in sound production. Multivariate comparisons, using sounds produced by eight soniferous European sand gobies, effectively distinguished soniferous (and sympatric) species based on their acoustic properties. However, the discrimination success decreased when temperature-dependent features (sound duration and pulse repetition rate) were excluded from the analysis. Therefore, we suggest both spectral and temporal features are important for the acoustic differentiation of sand gobies.

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.

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.

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.

'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.

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.

A primer on rhythm quantification for fish sounds: a Mediterranean case study.

We have used a lately established workflow to quantify rhythms of three fish sound types recorded in different areas of the Mediterranean Sea. So far, the temporal structure of fish sound sequences has only been described qualitatively. Here, we propose a standardized approach to quantify them, opening the path for assessment and comparison of an often underestimated but potentially critical aspect of fish sounds. Our approach is based on the analysis of inter-onset-intervals (IOIs), the intervals between the start of one sound element and the next. We calculate exact beats of a sequence using Fourier analysis and IOI analysis. Furthermore, we report on important parameters describing the variability in timing within a given sound sequence. Datasets were chosen to depict different possible rhythmic properties: Sciaena umbra sounds have a simple isochronous-metronome-like-rhythm. The /Kwa/ sound type emitted by Scorpaena spp. has a more complex rhythm, still presenting an underlying isochronous pattern. Calls of Ophidion rochei males present no rhythm, but a random temporal succession of sounds. This approach holds great potential for shedding light on important aspects of fish bioacoustics. Applications span from the characterization of specific behaviours to the potential discrimination of yet not distinguishable species.

Changes to an urban marina soundscape associated with COVID-19 lockdown in Guadeloupe.

In 2020, the COVID-19 pandemic led to government-enforced limits on activities worldwide, causing a marked reduction of human presence in outdoors environments, including in coastal areas that normally support substantial levels of boat traffic. These restrictions provided a unique opportunity to quantify the degree to which anthropogenic noise contributes to and impacts underwater soundscapes. In Guadeloupe, French West Indies, a significantly lower number of motor boats were recorded in the vicinity of the major urban marina during the peak of the first COVID-19 lockdown (April-May 2020), compared with the number recorded post-lockdown. The resumption of human activities at the end of May was correlated with a maximum increase of 6 decibels in the ambient noise level underwater. The change in noise level did not impact daily sound production patterns of vocal fishes, with increased activity at dusk seen both during and after the lockdown period. However, during the lockdown vocal activity was comprised of a reduced number of sounds, suggesting that anthropogenic noise has the potential to interfere with vocalization behaviours in fishes.

Parkinson's disease multimodal imaging: F-DOPA PET, neuromelanin-sensitive and quantitative iron-sensitive MRI.

Parkinson's disease (PD) is a neurodegenerative synucleinopathy characterized by the degeneration of neuromelanin (NM)-containing dopaminergic neurons and deposition of iron in the substantia nigra (SN). How regional NM loss and iron accumulation within specific areas of SN relate to nigro-striatal dysfunction needs to be clarified. We measured dopaminergic function in pre- and postcommissural putamen by [18F]DOPA PET in 23 Parkinson's disease patients and 23 healthy control (HC) participants in whom NM content and iron load were assessed in medial and lateral SN, respectively, by NM-sensitive and quantitative R2* MRI. Data analysis consisted of voxelwise regressions testing the group effect and its interaction with NM or iron signals. In PD patients, R2* was selectively increased in left lateral SN as compared to healthy participants, suggesting a local accumulation of iron in Parkinson's disease. By contrast, NM signal differed between PD and HC, without specific regional specificity within SN. Dopaminergic function in posterior putamen decreased as R2* increased in lateral SN, indicating that dopaminergic function impairment progresses with iron accumulation in the SN. Dopaminergic function was also positively correlated with NM signal in lateral SN, indicating that dopaminergic function impairment progresses with depigmentation in the SN. A complex relationship was detected between R2* in the lateral SN and NM signal in the medial SN. In conclusion, multimodal imaging reveals regionally specific relationships between iron accumulation and depigmentation within the SN of Parkinson's disease and provides in vivo insights in its neuropathology.

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.

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.

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.

Morphological diversity of acoustic and electric communication systems of mochokid catfish.

Mochokid catfish offer a distinct opportunity to study a communication system transitioning to a new signaling channel because some produce sounds and others electric discharges. Both signals are generated using an elastic spring system (ESS), which includes a protractor muscle innervated by motoneurons within the protractor nucleus that also has a motoneuron afferent population. Synodontis grandiops and S. nigriventris produce sounds and electric discharges, respectively, and their ESSs show several morphological and physiological differences. The extent to which these differences explain different signal types remains unclear. Here, we compare ESS morphologies and behavioral phenotypes among five mochokids. S. grandiops and S. nigriventris were compared with Synodontis eupterus that is known to produce both signal types, and representative members of two sister genera, Microsynodontis cf. batesii and Mochokiella paynei, for which no data were available. We provide support for the hypothesis that peripheral and central components of the ESS are conserved among mochokids. We also show that the two nonsynodontids are only sonic, consistent with sound production being an ancestral character for mochokids. Even though the three sound producing-only species differ in some ESS characters, several are similar and likely associated with only sound production. We propose that the ability of S. eupterus to generate both electric discharges and sounds may depend on a protractor muscle intermediate in morphology between sound producing-only and electric discharge-only species, and two separate populations of protractor motoneurons. Our results further suggest that an electrogenic ESS in synodontids is an exaptation of a sound producing ESS.

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.

Vocal repertoire and consistency of call features in the meagre Argyrosomous regius (Asso, 1801).

Passive Acoustic Monitoring (PAM) is a non-intrusive and cost-effective method capable of providing high-resolution, long-term information on the status and health of vocal populations and communities. To successfully monitor the same species over wide geographical and temporal scales, it is necessary to characterise the range of sound variability, as well as the consistency of sound features between populations. The meagre (Argyrosomus regius, Asso 1801) is an interesting case study because recent investigations suggest a wider vocal repertoire than previously described. In this study, meagre vocalizations were recorded and analysed from a variety of settings, ranging from rearing facilities to wild populations to provide a comprehensive characterisation of its vocal repertoire, while investigating the consistency of spawning sound features between populations. All sounds presented a similar acoustic structure in their basic unit (i.e. the pulse), while an important variability was found in the number of pulses; the meagre can emit sounds made of one single pulse or many pulses (up to more than 100). High level of overlap in the Principal Component Analysis made difficult to differentiate sound type clusters. Despite this, two sound types were identifiable: knocks (sounds from 1 to 3 pulses) and long grunts (sounds with more than 29 pulses). Discriminant Analysis carried out on PCA residuals showed that knock had the highest proportion of correct placement (92% of the observations correctly placed) followed by long grunts (80%). All other previously described sound types (intermediate grunt, short grunt and disturbance sounds) could not be separated and presented low levels of correct placement, suggesting that care should be taken when defining these as independent sound types. Finally, acoustic features consistency was found in meagre grunts emitted by different populations during spawning nights; statistical differences could be explained by recording settings and fish conditions. The results of this study provide important information for fostering PAM programs of wild meagre populations, while contributing to the discussion around the definition of fish sound types in vocal fish communities. Studies of this kind, which evaluate both variability and consistency of sound features, are of fundamental importance for maximising PAM efforts in the wild, at both the specific and the community level.

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.