Ultrafast sound production mechanism in one of the smallest vertebrates.

Motion is the basis of nearly all animal behavior. Evolution has led to some extraordinary specializations of propulsion mechanisms among invertebrates, including the mandibles of the dracula ant and the claw of the pistol shrimp. In contrast, vertebrate skeletal movement is considered to be limited by the speed of muscle, saturating around 250 Hz. Here, we describe the unique propulsion mechanism by which Danionella cerebrum, a miniature cyprinid fish of only 12 mm length, produces high amplitude sounds exceeding 140 dB (re. 1 µPa, at a distance of one body length). Using a combination of high-speed video, micro-computed tomography (micro-CT), RNA profiling, and finite difference simulations, we found that D. cerebrum employ a unique sound production mechanism that involves a drumming cartilage, a specialized rib, and a dedicated muscle adapted for low fatigue. This apparatus accelerates the drumming cartilage at over 2,000 g, shooting it at the swim bladder to generate a rapid, loud pulse. These pulses are chained together to make calls with either bilaterally alternating or unilateral muscle contractions. D. cerebrum use this remarkable mechanism for acoustic communication with conspecifics.

The ground offers acoustic efficiency gains for crickets and other calling animals.

Male crickets attract females by producing calls with their forewings. Louder calls travel further and are more effective at attracting mates. However, crickets are much smaller than the wavelength of their call, and this limits their power output. A small group called tree crickets make acoustic tools called baffles which reduce acoustic short-circuiting, a source of dipole inefficiency. Here, we ask why baffling is uncommon among crickets. We hypothesize that baffling may be rare because like other tools they offer insufficient advantage for most species. To test this, we modelled the calling efficiencies of crickets within the full space of possible natural wing sizes and call frequencies, in multiple acoustic environments. We then generated efficiency landscapes, within which we plotted 112 cricket species across 7 phylogenetic clades. We found that all sampled crickets, in all conditions, could gain efficiency from tool use. Surprisingly, we also found that calling from the ground significantly increased efficiency, with or without a baffle, by as much as an order of magnitude. We found that the ground provides some reduction of acoustic short-circuiting but also halves the air volume within which sound is radiated. It simultaneously reflects sound upwards, allowing recapture of a significant amount of acoustic energy through constructive interference. Thus, using the ground as a reflective baffle is an effective strategy for increasing calling efficiency. Indeed, theory suggests that this increase in efficiency is accessible not just to crickets but to all acoustically communicating animals whether they are dipole or monopole sound sources.

The domestication of the larynx: The neural crest connection.

Wolves howl and dogs bark, both are able to produce variants of either vocalization, but we see a distinct difference in usage between wild and domesticate. Other domesticates also show distinct changes to their vocal output: domestic cats retain meows, a distinctly subadult trait in wildcats. Such differences in acoustic output are well-known, but the causal mechanisms remain little-studied. Potential links between domestication and vocal output are intriguing for multiple reasons, and offer a unique opportunity to explore a prominent hypothesis in domestication research: the neural crest/domestication syndrome hypothesis. This hypothesis suggests that in the early stages of domestication, selection for tame individuals decreased neural crest cell (NCCs) proliferation and migration, which led to a downregulation of the sympathetic arousal system, and hence reduced fear and reactive aggression. NCCs are a transitory stem cell population crucial during embryonic development that tie to diverse tissue types and organ systems. One of these neural-crest derived systems is the larynx, the main vocal source in mammals. We argue that this connection between NCCs and the larynx provides a powerful test of the predictions of the neural crest/domestication syndrome hypothesis, discriminating its predictions from those of other current hypotheses concerning domestication.

Gekko gecko as a model organism for understanding aspects of laryngeal vocal evolution.

The ability to communicate through vocalization plays a key role in the survival of animals across all vertebrate groups. While avian reptiles have received much attention relating to their stunning sound repertoire, non-avian reptiles have been wrongfully assumed to have less elaborate vocalization types and little is known about the biomechanics of sound production and their underlying neural pathways. We investigated alarm calls of Gekko gecko using audio and cineradiographic recordings of their alarm calls. Acoustic analysis revealed three distinct call types: a sinusoidal call type (type 1), a train-like call type, characterized by distinct pulse trains (type 3), and an intermediary type, which showed both sinusoidal and pulse train components (type 2). Kinematic analysis of cineradiographic recordings showed that laryngeal movements differ significantly between respiratory and vocal behavior: during respiration, animals repeatedly moved their jaws to partially open their mouths, which was accompanied by small glottal movements. During vocalization, the glottis was pulled back, contrasting with what has previously been reported. In-vitro retrograde tracing of the nerve innervating the laryngeal constrictor and dilator muscles revealed round to fusiform motoneurons in the hindbrain-spinal cord transition ipsilateral to the labeled nerve. Taken together, our observations provide insight into the alarm calls generated by G. gecko, the biomechanics of this sound generation and the underlying organization of motoneurons involved in the generation of vocalizations. Our observations suggest that G. gecko may be an excellent non-avian reptile model organism for enhancing our understanding of the evolution of vertebrate vocalization.

Characterization of sound production by the pot-bellied seahorse (Hippocampus abdominalis) during feeding.

Sound production during feeding by the pot-bellied seahorse, Hippocampus abdominalis, was quantified with an observation of clicks (acoustic signal) and snicks (visual behavior). Female, male, and juvenile seahorses had feeding sounds characterized for peak (dominant) frequency (Hz), sound pressure level (SPL), and duration (ms). Subject body size and condition was estimated by standard length (SL, cm), to determine an estimate of body condition index (BCI). An inverse correlation between mean peak frequency (Hz) of clicks and SL was found for females. A negative correlation between peak frequency (Hz) of clicks and a residual BCI was determined for both males and females, suggesting that acoustic signals may contain information regarding fitness.

The potential impact of literacy intervention on speech sound production in students with intellectual disability and communication difficulties.

A small body of research and reports from educational and clinical practice suggest that teaching literacy skills may facilitate the development of speech sound production in students with intellectual disabilities (ID). However, intervention research is needed to test the potential connection. This study aimed to investigate whether twelve weeks of systematic, digital literacy intervention enhanced speech sound production in students with ID and communication difficulties. A sample of 121 students with ID were assigned to four different groups: phonics-based, comprehension-based, a combination with both phonics- and comprehension-based intervention and a comparison group with teaching-as-usual. Speech sound production was assessed before and after the intervention. The results on the data without the imputed variable suggested a significant positive effect of systematic, digital literacy interventions on speech sound production. However, results from sensitivity analyses with imputed missing data was more ambiguous, with the effect only approaching significance (ps = .05-.07) for one of the interventions. Nonetheless, we tentatively suggest that systematic, digital literacy intervention could support speech development in students with ID and communication difficulties. Future research should be done to confirm and further elucidate the functional mechanisms of this link, so that we may have a better understanding and can improve instruction and the pivotal abilities of speech and reading.

Functional plasticity of the swim bladder as an acoustic organ for communication in a vocal fish.

Teleost fishes have evolved a number of sound-producing mechanisms, including vibrations of the swim bladder. In addition to sound production, the swim bladder also aids in sound reception. While the production and reception of sound by the swim bladder has been described separately in fishes, the extent to which it operates for both in a single species is unknown. Here, using morphological, electrophysiological and modelling approaches, we show that the swim bladder of male plainfin midshipman fish (Porichthys notatus) exhibits reproductive state-dependent changes in morphology and function for sound production and reception. Non-reproductive males possess rostral 'horn-like' swim bladder extensions that enhance low-frequency (less than 800 Hz) sound pressure sensitivity by decreasing the distance between the swim bladder and inner ear, thus enabling pressure-induced swim bladder vibrations to be transduced to the inner ear. By contrast, reproductive males display enlarged swim bladder sonic muscles that enable the production of advertisement calls but also alter swim bladder morphology and increase the swim bladder to inner ear distance, effectively reducing sound pressure sensitivity. Taken together, we show that the swim bladder exhibits a seasonal functional plasticity that allows it to effectively mediate both the production and reception of sound in a vocal teleost fish.

Sound detection and production mechanisms in aquatic decapod and stomatopod crustaceans.

The sensory systems of crustaceans (aquatic decapods and stomatopods) have adapted to a diverse range of aquatic ecosystems. Sound production in aquatic crustaceans is more widespread than previously thought, and has been shown to play a major role in many of their life-history strategies; however, there are still many gaps in our understanding of their sound reception abilities. Crustaceans have three main sensory receptors for sound - the statocyst, superficial hair cells and chordotonal organs - which are all sensitive to the particle motion component of the sound field, rather than the pressure component. Our current understanding of these receptors is that they are sensitive to low-frequency sounds (<2000 Hz). There are a wide variety of sound-producing mechanisms employed by these animals, ranging from stridulation to implosive cavitation (see Glossary). These signals are used for a range of social behaviours, such as courtship, territorial defence and assessing 'resource guarding'. Furthermore, there are examples of sound signals that exceed their hearing range, highlighting a mismatch in our understanding of their hearing systems. This mismatch provides weight to the suggestion that another sound transmission channel - substrate-borne vibrations - might be at play, particularly because most crustaceans live on or near the seafloor. Finally, suggestions are made regarding potential future work that is needed to fill the substantial gaps in our understanding of how crustaceans hear and produce sound.

Form function of sulcus acusticus of the sagittal otolith in seven Sciaenidae (Acanthuriformes) species using geometric morphometrics (southwestern Atlantic).

The morphology of otoliths determines the function they perform, and it is influenced by genetic and environmental factors. Knowing those relationships is necessary to understand the role of hearing in fish. The objectives of this work were: exploring the shape of the sulcus of the sagittal otolith in seven species of Sciaenidae, in relation to sound production, and analyzing whether the shape and size of the sulcus can be used as a phylogenetic character. For this purpose, geometric morphometry analysis was carried out using landmarks data. It was found that there is an influence of size on the shape of the sulcus, and significant differences were found between the shapes of the sulcus (permutational multivariate analysis of variance). Three general shapes of the sulcus were identified (using principal component analysis, canonical variate analysis, and clustering): (1) in species that produce sounds at dominant frequencies <350 Hz, the deformation of the sulcus showed a tendency towards circularity of the ostium; (2) in those species that produce sounds at frequencies >350 Hz, the ostium showed a flattened ovoid shape, and the cauda increased its length; (3) the species that do not produce sounds, did not show any modifications, relative to the form of consensus. Despite finding sister species that presented similar sulcus shapes in the phylogeny, the results did not confirm that this can be used as a phylogenetic character. This work discusses whether the combined effects of phylogenetic legacy and natural functional selection have led to convergent evolution for the sulcus form. The differences presented by the sulcus of species that occupy the same clade, could indicate that there is a displacement of characters. The sagittal otolith and the sensory macula associated with the sulcus acusticus are highly plastic structures that are subject to strong evolutionary pressure in relation to environmental and behavioral factors, resulting in great variability in shapes that can be associated with a specific character. The variation in the shape of the sulcus would allow the analysed species to coexist in the same coastal soundscapes, without losing their particular hearing needs, even in case of overlapping their spatial and temporal distribution areas.

Acoustic and postural displays in a miniature and transparent teleost fish, Danionella dracula.

Acoustic behavior is widespread across vertebrates, including fishes. We report robust acoustic displays during aggressive interactions for a laboratory colony of Danionella dracula, a miniature and transparent species of teleost fish closely related to zebrafish (Danio rerio), which are hypothesized to be sonic based on the presence of a hypertrophied muscle associated with the male swim bladder. Males produce bursts of pulsatile sounds and a distinct postural display - extension of a hypertrophied lower jaw, a morphological trait not present in other Danionella species - during aggressive but not courtship interactions. Females show no evidence of sound production or jaw extension in such contexts. Novel pairs of size-matched or -mismatched males were combined in resident-intruder assays where sound production and jaw extension could be linked to individuals. In both dyad contexts, resident males produced significantly more sound pulses than intruders. During heightened sonic activity, the majority of the highest sound producers also showed increased jaw extension. Residents extended their jaw more than intruders in size-matched but not -mismatched contexts. Larger males in size-mismatched dyads produced more sounds and jaw extensions compared with their smaller counterparts, and sounds and jaw extensions increased with increasing absolute body size. These studies establish D. dracula as a sonic species that modulates putatively acoustic and postural displays during aggressive interactions based on residency and body size, providing a foundation for further investigating the role of multimodal displays in a new model clade for neurogenomic and neuroimaging studies of aggression, courtship and other social interactions.

The mechanics of acoustic signal evolution in field crickets.

Field crickets (Family Gryllidae, Subfamily Gryllinae) typically produce tonal calls with carrier frequencies in the range 3-8 kHz. In this study, we explored the use of a finite element model (FEM) of the stridulatory apparatus of a field cricket, Gryllus bimaculatus, based on experimental measurements of resonator geometry and mechanical properties, to predict the measured call carrier frequencies of eight other field cricket species, ranging between 3 and 7 kHz. The model allowed accurate predictions of carrier frequencies for all eight species to within a few hundred hertz from morphological measurements of their resonators. We then used the model to explore the plausible evolutionary design space for field cricket call carrier frequency along the axes of resonator size and thickness, and mapped the locations of the nine experimentally measured species in this design space. Although the nine species spanned the evolutionarily conserved spectrum of carrier frequency and body size in field crickets, they were clustered in a small region of the available design space. We then explored the reasons for this apparent evolutionary constraint on field cricket carrier frequencies at both the lower and higher limit. We found that body size and sound radiation efficiency were the main constraints at the lower limits, whereas the energetics of stridulation using the clockwork mechanism may pose a constraint at higher frequencies.

Multifunctional bilateral muscle control of vocal output in the songbird syrinx.

Songbirds produce complex vocalizations by coordinating neuromuscular control of syrinx, respiratory system, and upper vocal tract. The functional roles of syringeal muscles have been documented mainly with correlative data, which have suggested that synergistic activation plays a role in the fine control of vocal features. However, the specific involvement of individual muscles in achieving this fine control is still largely unknown. Here we investigate the contributions of the two main airflow controlling muscles, the dorsal and ventral tracheobronchial muscles in the zebra finch, through a new approach. Ablation of the muscle insertion on the cartilage framework reveals detailed insights into their respective roles in the fine control of song features. Unilateral ablation of a tracheobronchial muscle resulted in mostly subtle changes of the air sac pressure pattern and song features. Effects of ablation varied with the acoustic elements, thus indicating a context-dependent specific synergistic activation of muscles. High-frequency notes were most affected by the ablation, highlighting the importance of coordinated bilateral control. More pronounced effects on song features and air sac pressure were observed after bilateral ablation of the dorsal tracheobronchial muscles. The results illustrate that the gating muscles serve multiple functions in control of acoustic features and that each feature arises through context-dependent, synergistic activation patterns of syringeal muscles. Although many changes after the ablation are subtle, they fall within the perceptual range and thus may control behaviorally relevant features of sound. These data therefore provide important specific details about the underlying motor code for song production.NEW & NOTEWORTHY A new experimental approach was used to analyze the involvement of individual muscles in birdsong vocal control. Ablation of tracheobronchial muscles showed how these muscles contribute in manner specific to the acoustic structure of sound segments and how disruption of airflow regulation affects bilateral coordination. The results of this study illustrate that the gating muscles serve multiple functions in control of acoustic features and give further insight into the complex motor control of birdsong.

Whistling is metabolically cheap for communicating bottlenose dolphins (Tursiops truncatus).

Toothed whales depend on sound for communication and foraging, making them potentially vulnerable to acoustic masking from increasing anthropogenic noise. Masking effects may be ameliorated by higher amplitudes or rates of calling, but such acoustic compensation mechanisms may incur energetic costs if sound production is expensive. The costs of whistling in bottlenose dolphins (Tursiops truncatus) have been reported to be much higher (20% of resting metabolic rate, RMR) than theoretical predictions (0.5-1% of RMR). Here, we address this dichotomy by measuring the change in the resting O2 consumption rate (V̇O2 ), a proxy for RMR, in three post-absorptive bottlenose dolphins during whistling and silent trials, concurrent with simultaneous measurement of acoustic output using a calibrated hydrophone array. The experimental protocol consisted of a 2-min baseline period to establish RMR, followed by a 2-min voluntary resting surface apnea, with or without whistling as cued by the trainers, and then a 5-min resting period to measure recovery costs. Daily fluctuations in V̇O2  were accounted for by subtracting the baseline RMR from the recovery costs to estimate the cost of apnea with and without whistles relative to RMR. Analysis of 52 sessions containing 1162 whistles showed that whistling did not increase metabolic cost (P>0.1, +4.2±6.9%) as compared with control trials (-0.5±5.9%; means±s.e.m.). Thus, we reject the hypothesis that whistling is costly for bottlenose dolphins, and conclude that vocal adjustments such as the Lombard response to noise do not represent large direct energetic costs for communicating toothed whales.

Floating frogs sound larger: environmental constraints on signal production drives call frequency changes.

In animal communication, receivers benefit from signals providing reliable information on signalers' traits of interest. Individuals involved in conflicts, such as competition between rivals, should pay particular attention to cues that are "unfakeable" by the senders due to the intrinsic properties of the production process. In bioacoustics, the best-known example of such "index signals" is the relationship between a sender's body size and the dominant frequency of their vocalizations. Dominant frequency may, however, not only depend on an animal's morphology but also on the interaction between the sound production system and its immediate environment. Here, we experimentally altered the environment surrounding calling frogs and assessed its impact on the signal produced. Our results show that frogs that are floating are able to inflate their vocal sacs fully and that this change in inflation level is correlated with a decrease of call dominant frequency.

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.

Computation of Dolphins' Sound ASPL While Foraging.

Scheduled scientific surveys are a valuable asset in beginning to understand the behavior and vocalization of free-ranging cetaceans. The fortuity of a nonscheduled survey has proven to be beneficial as well. In October 2003 a team of biologist oceanographers began a trip aboard a 44.29 feet catamaran sailing boat from Piraeus Greece to Cape Verde Archipelago intending to observe free-ranging cetaceans. Acoustic recordings were conducted using a towed stereophonic hydrophone array consisted of two Benthos AQ4 type hydrophones. Photographs were taken in order to ensure species identification. Information on vocalization administration during foraging of Lagenodelphis hosei and Steno bredanensis has been acquired. Calculation of ASPL (apparent source power level) revealed that dolphins' vocalizations did not match to usual vocalization activities. The relation of vocalization administration by dolphins with brain to mash ratio (BMR) is introduced as an additional predator's strategy.

Comparison between covert sound-production task (sound-imagery) vs. motor-imagery for onset detection in real-life online self-paced BCIs.

BACKGROUND: Even though the BCI field has quickly grown in the last few years, it is still mainly investigated as a research area. Increased practicality and usability are required to move BCIs to the real-world. Self-paced (SP) systems would reduce the problem but there is still the big challenge of what is known as the 'onset detection problem'. METHODS: Our previous studies showed how a new sound-imagery (SI) task, high-tone covert sound production, is very effective for onset detection scenarios and we expect there are several advantages over most common asynchronous approaches used thus far, i.e., motor-imagery (MI): 1) Intuitiveness; 2) benefits to people with motor disabilities and, especially, those with lesions on cortical motor areas; and 3) no significant overlap with other common, spontaneous cognitive states, making it easier to use in daily-life situations. The approach was compared with MI tasks in online real-life scenarios, i.e., during activities such as watching videos and reading text. In our scenario, when a new message prompt from a messenger program appeared on the screen, participants watching a video (or reading text, browsing images) were asked to open the message by executing the SI or MI tasks, respectively, for each experimental condition. RESULTS: The results showed the SI task performed statistically significantly better than the MI approach: 84.04% (SI) vs 66.79 (MI) True-False positive rate for the sliding image scenario, 80.84% vs 61.07% for watching video. The classification performance difference between SI and MI was found not to be significant in the text-reading scenario. Furthermore, the onset response speed showed SI (4.08 s) being significantly faster than MI (5.46 s). In terms of basic usability, 75% of subjects found SI easier to use. CONCLUSIONS: Our novel SI task outperforms typical MI for SP onset detection BCIs, therefore it would be more easily used in daily-life situations. This could be a significant step forward for the BCI field which has so far been mainly restricted to research-oriented indoor laboratory settings.

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.

First report of luminous stimuli eliciting sound production in weevils.

Light-based stimuli elicited acoustic responses in male Hylesinus aculeatus Say (Curculionidae: Scolytinae: Hylesinina) instantaneously, with 100% reliability. Stridulations were elicited with a white light beam in a dark environment and recorded with an ultrasonic microphone. Acoustic responses were consistent, and, when compared with sounds produced under stressful conditions (i.e. physical stimulation), no significant differences were found. Hylesinus aculeatus possess an elytro-tergal stridulatory organ and acoustic communication is only present in males. This is also the first report of acoustic communication for this species. Instantaneous light-elicited acoustic communication has potential applications in the development of electronic traps and real-time acoustic detection and identification of beetles, border biosecurity, and noise-reduction in acoustic data collection.

Ecology of fish hearing.

Underwater sound is directional and can convey important information about the surrounding environment or the animal emitting the sound. Therefore, sound is a major sensory channel for fishes and plays a key role in many life-history strategies. The effect of anthropogenic noise on aquatic life, which may be causing homogenisation or fragmentation of biologically important signals underwater is of growing concern. In this review we discuss the role sound plays in the ecology of fishes, basic anatomical and physiological adaptations for sound reception and production, the effects of anthropogenic noise and how fishes may be coping to changes in their environment, to put the ecology of fish hearing into the context of the modern underwater soundscape.