Rhythmic properties of Sciaena umbra calls across space and time in the Mediterranean Sea.

In animals, the rhythmical properties of calls are known to be shaped by physical constraints and the necessity of conveying information. As a consequence, investigating rhythmical properties in relation to different environmental conditions can help to shed light on the relationship between environment and species behavior from an evolutionary perspective. Sciaena umbra (fam. Sciaenidae) male fish emit reproductive calls characterized by a simple isochronous, i.e., metronome-like rhythm (the so-called R-pattern). Here, S. umbra R-pattern rhythm properties were assessed and compared between four different sites located along the Mediterranean basin (Mallorca, Venice, Trieste, Crete); furthermore, for one location, two datasets collected 10 years apart were available. Recording sites differed in habitat types, vessel density and acoustic richness; despite this, S. umbra R-calls were isochronous across all locations. A degree of variability was found only when considering the beat frequency, which was temporally stable, but spatially variable, with the beat frequency being faster in one of the sites (Venice). Statistically, the beat frequency was found to be dependent on the season (i.e. month of recording) and potentially influenced by the presence of soniferous competitors and human-generated underwater noise. Overall, the general consistency in the measured rhythmical properties (isochrony and beat frequency) suggests their nature as a fitness-related trait in the context of the S. umbra reproductive behavior and calls for further evaluation as a communicative cue.

Characterization of the vocal behavior of the miniature and transparent fish model, Danionella cerebruma).

Danionella cerebrum has recently been proposed as a promising model to investigate the structure and function of the adult vertebrate brain, including the development of vocal-auditory neural pathways. This genetically tractable and transparent cypriniform is highly vocal, but limited information is available on its acoustic behavior and underlying biological function. Our main goal was to characterize the acoustic repertoire and diel variation in sound production of D. cerebrum, as well as to investigate the relationship between vocal behavior and reproduction. Sound recordings demonstrated high vocal activity, with sounds varying from short sequences of pulses known as "bursts" (comprising up to 15 pulses) to notably longer sounds, termed "long bursts", which extended up to 349 pulses with over 2.7 s. Vocal activity peaked at midday and it was very low at night with only a few bursts. While the number of pulses was higher during the daytime, the interpulse interval was longer at night. In addition, calling time was positively associated with the number of viable eggs, suggesting that acoustic communication is important for reproduction. These preliminary findings reveal the potential of using D. cerebrum to investigate vocal plasticity and the implications for sexual selection and reproduction in a novel vertebrate model for neuroscience.

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.].

Detection of invasive fish species with passive acoustics: Discriminating between native and non-indigenous sciaenids.

Invasive alien species have been rising exponentially in the last decades impacting biodiversity and ecosystem functioning. The soniferous weakfish, Cynoscion regalis, is a recent invasive sciaenid species in the Iberian Peninsula and was first reported in the Tagus estuary in 2015. There is concern about its possible impacts on native species, namely the confamiliar meagre, Argyrosomus regius, as there is overlap in their feeding regime, habitat use, and breeding behaviour. Here, we characterised the sciaenid-like sounds recently recorded in the Tagus estuary and showed that they are made by weakfish as they have similar numbers of pulses and pulse periods to the sounds made by captive breeding weakfish. We further demonstrate that breeding grunts from weakfish and the native sciaenid, recorded either in captivity or Tagus estuary, differ markedly in sound duration, number of pulses and pulse period in the two species, but overlap in their spectral features. Importantly, these differences are easily detected through visual and aural inspections of the recordings, making acoustic recognition easy even for the non-trained person. We propose that passive acoustic monitoring can be a cost-effective tool for in situ mapping of weakfish outside its natural distribution and an invaluable tool for early detection and to monitor its expansion.

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.

A state-space model to derive motorboat noise effects on fish movement from acoustic tracking data.

Motorboat noise is recognized as a major source of marine pollution, however little is known about its ecological consequences on coastal systems. We developed a State Space Model (SSM) that incorporates an explicit dependency on motorboat noise to derive its effects on the movement of resident fish that transition between two behavioural states (swimming vs. hidden). To explore the performance of our model, we carried out an experiment where free-living Serranus scriba were tracked with acoustic tags, while motorboat noise was simultaneously recorded. We fitted the generated tracking and noise data into our SSM and explored if the noise generated by motorboats passing at close range affected the movement pattern and the probability of transition between the two states using a Bayesian approach. Our results suggest high among individual variability in movement patterns and transition between states, as well as in fish response to the presence of passing motorboats. These findings suggest that the effects of motorboat noise on fish movement are complex and require the precise monitoring of large numbers of individuals. Our SSM provides a methodology to address such complexity and can be used for future investigations to study the effects of noise pollution on marine fish.

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.

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.

Temperate freshwater soundscapes: A cacophony of undescribed biological sounds now threatened by anthropogenic noise.

The soundscape composition of temperate freshwater habitats is poorly understood. Our goal was to document the occurrence of biological and anthropogenic sounds in freshwater habitats over a large (46,000 km2) area along the geographic corridors of five major river systems in North America (Connecticut, Kennebec, Merrimack, Presumpscot, and Saco). The underwater soundscape was sampled in 19 lakes, 17 ponds, 20 rivers and 20 streams, brooks and creeks that were grouped into broad categories (brook/creek, pond/lake, and river). Over 7,000 sounds were measured from 2,750 minutes of recording in 173 locations over a five-week period in the spring of 2008. Sounds were classified into major anthropophony (airplane, boat, traffic, train and other noise) and biophony (fish air movement, also known as air passage, other fish, insect-like, bird, and other biological) categories. The three most significant findings in this study are: 1) freshwater habitats in the New England region of North America contain a diverse array of unidentified biological sounds; 2) fish air movement sounds constitute a previously unrecognized important component of the freshwater soundscape, occurring at more locations (39%) and in equal abundance than other fish sounds; and 3) anthropogenic noises dominate the soundscape accounting for 92% of the soundscape by relative percent time. The high potential for negative impacts of the anthropophony on freshwater soundscapes is suggested by the spectral and temporal overlap of the anthropophony with the biophony, the higher received sound levels of the anthropophony relative to the biophony, and observations of a significant decline in the occurrence, number, percent time, and diversity of the biophony among locations with higher ambient received levels. Our poor understanding of the biophony of freshwater ecosystems, together with an apparent high temporal exposure to anthropogenic noise across all habitats, suggest a critical need for studies aimed at identification of biophonic sound sources and assessment of potential threats from anthropogenic noises.

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.

Air movement sound production by alewife, white sucker, and four salmonid fishes suggests the phenomenon is widespread among freshwater fishes.

We sought to describe sounds of some of the common fishes suspected of producing unidentified air movement sounds in soundscape surveys of freshwater habitats in the New England region of North America. Soniferous behavior of target fishes was monitored in real time in the field in both natural and semi-natural environments by coupling Passive Acoustic Monitoring (PAM) with direct visual observation from shore and underwater video recording. Sounds produced by five species including, alewife (Alosa pseudoharengus, Clupeidae), white sucker (Catastomus commersonii, Catostomidae), brook trout (Salvelinus fontinalis, Salmonidae), brown trout (Salmo trutta, Salmonidae), and rainbow trout (Oncorhynchus mykiss, Salmonidae) were validated and described in detail for the first time. In addition, field recordings of sounds produced by an unidentified salmonid were provisionally attributed to Atlantic salmon (Salmo salar, Salmonidae). Sounds produced by all species are of the air movement type and appear to be species specific. Our data based on fishes in three distinct orders suggest the phenomenon may be more ecologically important than previously thought. Even if entirely incidental, air movement sounds appear to be uniquely identifiable to species and, hence, hold promise for PAM applications in freshwater and marine habitats.

Acoustic communication in marine shallow waters: testing the acoustic adaptive hypothesis in sand gobies.

Acoustic communication is an important part of social behaviour of fish species that live or breed in shallow noisy waters. Previous studies have shown that some fish species exploit a quiet window in the background noise for communication. However, it remains to be examined whether hearing abilities and sound production of fish are adapted to marine habitats presenting high hydrodynamism. Here, we investigated whether the communication system of the painted (Pomatoschistus pictus) and the marbled (Pomatoschistus marmoratus) gobies is adapted to enhance sound transmission and reception in Atlantic shallow water environments. We recorded and measured the sound pressure levels of social vocalisations of both species, as well as snapshots of ambient noise of habitats characterised by different hydrodynamics. Hearing thresholds (in terms of both sound pressure and particle acceleration) and responses to conspecific signals were determined using the auditory evoked potential recording technique. We found that the peak frequency range (100-300 Hz) of acoustic signals matched the best hearing sensitivity in both species and appeared well adapted for short-range communication in Atlantic habitats. Sandy/rocky exposed beaches presented a quiet window, observable even during the breaking of moderate waves, coincident with the main sound frequencies and best hearing sensitivities of both species. Our data demonstrate that the hearing abilities of these gobies are well suited to detect conspecific sounds within typical interacting distances (a few body lengths) in Atlantic shallow waters. These findings lend support to the acoustic adaptive hypothesis, under the sensory drive framework, proposing that signals and perception systems coevolve to be effective within local environment constraints.

Acoustic Complexity of vocal fish communities: a field and controlled validation.

The Acoustic Complexity Index (ACI) is increasingly applied to the study of biodiversity in aquatic habitats. However, it remains unknown which types of acoustic information are highlighted by this index in underwater environments. This study explored the robustness of the ACI to fine variations in fish sound abundance (i.e. number of sounds) and sound diversity (i.e. number of sound types) in field recordings and controlled experiments. The ACI was found to be sensitive to variations in both sound abundance and sound diversity, making it difficult to discern between these variables. Furthermore, the ACI was strongly dependent on the settings used for its calculation (i.e. frequency and temporal resolution of the ACI algorithm, amplitude filter). Care should thus be taken when comparing ACI absolute values between studies, or between sites with site-specific characteristics (e.g. species diversity, fish vocal community composition). As the use of ecoacoustic indices presents a promising tool for the monitoring of vulnerable environments, methodological validations like those presented in this paper are of paramount importance in understanding which biologically important information can be gathered by applying acoustic indices to Passive Acoustic Monitoring data.

Is the Venice Lagoon Noisy? First Passive Listening Monitoring of the Venice Lagoon: Possible Effects on the Typical Fish Community.

Three passive listening surveys have been carried out in two of the three Venice lagoon tide inlets and inside the Venice island. The spectral content and the intensity level of the underwater noise as well as the presence or absence of Sciaena umbra and the distribution of its different sound patterns have been investigated in all the recording sites. The passive listening proved to be successful in detecting S. umbra drumming sounds in both Venice lagoon tide inlets. Our results indicate that the spectral content and the level of underwater noise pollution in the Venice lagoon could affect fish acoustic communication.