The importance of underwater sounds to gadoid fishes.

The codfish family includes more than 500 species that vary greatly in their abundance in areas like the North Sea and are widely fished. Gadoids (codfish) gather at particular locations to spawn, where they exhibit complex reproductive behavior with visual and acoustic displays. Calls have been described from seven species, including the Atlantic cod and haddock. They vocalize by means of a specialized apparatus, consisting of rapidly contracting striated muscles (the drumming muscles) attached to the gas-filled swim bladder. Several gadoids, such as the ling and the Greenland cod, possess drumming muscles and are likely to make sounds. Non-vocal gadoids, such as the poor cod, lack these muscles. It is suggested that the sonic apparatus was present in the early species of the gadoids, with some species having lost their sonic ability. Interestingly, silent gadoids are mainly small schooling fishes. Gadoid species are most sensitive to sounds from 30 to 500 Hz. Gadoid hearing can be masked by ambient sound but also by anthropogenic sounds, which may therefore adversely affect their reproduction, with potential effects upon discrete local stocks. Listening for gadoid sounds provides a reliable, non-invasive way of locating spawning sites, which can enhance the protection of reproducing fish from human impacts.

Communicating the Issue of Underwater Noise Pollution: The Deaf as a Fish Project.

Aquatic noise pollution is largely ignored by the lay public. How experts communicate this issue is critical to move public opinion. In 2010, the Cassa di Risparmio di Gorizia (CaRiGO) bank sponsored the Deaf as a Fish project that included local underwater noise monitoring, a boat census, a pamphlet for nonexperts, and some seminars and public meetings. This project allowed us to raise interest in this issue. Using accurate and understandable language in a light-humored setting goes far toward cultivating trust from a public audience that can be intimidated or suspicious of complicated scientific messaging.

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.

Are the 1/3-Octave Band 63- and 125-Hz Noise Levels Predictive of Vessel Activity? The Case in the Cres-Losinj Archipelago (Northern Adriatic Sea, Croatia).

A 3-years sea ambient-noise (SAN) monitoring was carried out in the Cres-Losinj Archipelago (Croatia), where a bottlenose dolphin population is threatened by unregulated nautical tourism. A total of 540 5-min SAN samples were collected and analyzed in an Indicator 11.2.1 (Marine Strategy Framework Directive) perspective. The 1/3-octave band center frequencies of 63 and 125 Hz (re 1 µPa.rms) proved to be predictive of local predominant ship type over time. However, the noisiest band level was centered on 200 Hz. We therefore suggest measuring a wider frequency band than those requested in Indicator 11.2.1.

How effective are acoustic signals in territorial defence in the Lusitanian toadfish?

The function of fish sounds in territorial defence, in particular its influence on the intruder's behaviour during territorial invasions, is poorly known. Breeding Lusitanian toadfish males (Halobatrachus didactylus) use sounds (boatwhistles) to defend nests from intruders. Results from a previous study suggest that boatwhistles function as a 'keep-out signal' during territorial defence. To test this hypothesis we performed territorial intrusion experiments with muted Lusitanian toadfish. Males were muted by making a cut and deflating the swimbladder (the sound-producing apparatus) under anaesthesia. Toadfish nest-holder males reacted to intruders mainly by emitting sounds (sham-operated and control groups) and less frequently with escalated bouts of fighting. When the nest-holder produced a boatwhistle, the intruder fled more frequently than expected by chance alone. Muted males experienced a higher number of intrusions than the other groups, probably because of their inability to vocalise. Together, our results show that fish acoustic signals are effective deterrents in nest/territorial intrusions, similar to bird song.

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.

Electric boat underwater radiated noise and its potential impact on species of conservation interest.

Electric boats are thought to be noiseless, but in-situ measurements are generally rare. The Underwater Radiated Noise (URN) of 8-m Trimaran Pontoon Boat with two outboard electric engines was measured in the Miramare Marine Protected Area (Trieste, Italy), together with the URN of a fibreglass 5-m boat, with a outboard gasoline engine, for comparisons. International standards and guidelines for shallow waters were considered. URN were provided in one-third octave band and in narrow band spectra. The electric boat produced a low input of underwater noise at low frequencies. Given a low-frequency hearing sensitivity, the listening space reduction (LSR) was lower when generated by the electric than by combustion engine boat for the brown meagre, a local Teleost fish. No difference was found for the bottlenose dolphin LSR although continuous, tonal, high frequency components generated by the electric boat are expected to be highly detrimental for the bottlenose dolphin.

Addressing underwater noise: Joint efforts and progress on its global governance.

Underwater noise generated by human activities has become a major reason of concern over the past decades as human exploitation of world seas became more intense. A key to reduce human-generated acoustic pressure on aquatic ecosystems depends on an approach based on international cooperation. Over the past years, scientists worldwide worked together to assess trends in underwater noise levels in order to develop mitigation measures that would allow the effective protection of endangered species without reducing the possibilities for a sustainable use of seas. This review focused on international programmes dedicated to underwater noise monitoring, mapping and to programs dedicated to mitigate noise and its effects on marine fauna. All together this review shows the existence of a growing, general, international consensus on the fact that anthropogenic underwater noise should be significantly reduced by setting appropriate mitigation measures and effective regulatory actions.

First basin scale spatial-temporal characterization of underwater sound in the Mediterranean Sea.

Anthropogenic underwater noise is an emergent pollutant. Despite several worldwide monitoring programs, only few data are available for the Mediterranean Sea, one of the global biodiversity hotspots. The results of the first continuous acoustic programme run at a transnational basin scale in the Mediterranean Sea are here presented. Recordings were done from March 2020 to June 2021, including the COVID-19 lockdown, at nine stations in the Northern Adriatic Sea. Spatial-temporal variations of the underwater sound are described, having one third octave band sound pressure levels (SPLs) from 10 Hz to 20 kHz as metrics. Higher and more variable SPLs, mainly related to vessel traffic, were found close to harbours, whereas Natura 2000 stations experienced lower SPLs. Lower values were recorded during the lockdown in five stations. Median yearly SPLs ranged between 64 and 95 as well as 70 and 100 dB re 1 µPa for 63 and 125 Hz bands, respectively. These values are comparable with those previously found in busy shallow EU basins but higher levels are expected during a business-as-usual period. This is a baseline assessment for a highly impacted and environmental valuable area, that needs to be managed in a new sustainable blue growth strategy.

First assessment of underwater sound levels in the Northern Adriatic Sea at the basin scale.

The protection of marine habitats from human-generated underwater noise is an emerging challenge. Baseline information on sound levels, however, is poorly available, especially in the Mediterranean Sea. To bridge this knowledge gap, the SOUNDSCAPE project ran a basin-scale, cross-national, long-term underwater monitoring in the Northern Adriatic Sea. A network of nine monitoring stations, characterized by different natural conditions and anthropogenic pressures, ensured acoustic data collection from March 2020 to June 2021, including the full lockdown period related to the COVID-19 pandemic. Calibrated stationary recorders featured with an omnidirectional Neptune Sonar D60 Hydrophone recorded continuously 24 h a day (48 kHz sampling rate, 16 bit resolution). Data were analysed to Sound Pressure Levels (SPLs) with a specially developed and validated processing app. Here, we release the dataset composed of 20 and 60 seconds averaged SPLs (one-third octave, base 10) output files and a Python script to postprocess them. This dataset represents a benchmark for scientists and policymakers addressing the risk of noise impacts on marine fauna in the Mediterranean Sea and worldwide.

Brown meagre vocalization rate increases during repetitive boat noise exposures: a possible case of vocal compensation.

This study investigated whether or not boat noise causes variations in brown meagre (Sciaena umbra) vocalizations recorded in a nearshore Mediterranean marine reserve. Six nocturnal experimental sessions were carried out from June to September 2009. In each of them, a recreational boat passed over vocalizing fish 6 times with 1 boat passage every 10 min. For this purpose three different boats were used in random order: an 8.5-m cabin-cruiser (CC), a 5-m fiberglass boat (FB), and a 7-m inflatable boat (INF). In situ continuous acoustic recordings were collected using a self-standing sonobuoy. Because boat noise levels largely exceeded both background noise and S. umbra vocalizations in the species' hearing frequency range, masking of acoustic communication was assumed. Although no immediate effect was observed during a single boat passage, the S. umbra mean pulse rate increased over multiple boat passages in the experimental condition but not in the control condition, excluding that the observed effect was due to a natural rise in fish vocalizations. The observed vocal enhancement may result either from an increased density of callers or from an increased number of pulses/sounds produced by already acoustically active individuals, as a form of vocal compensation. These two explanations are discussed.

Boat-induced pressure does not influence breeding site selection of a vulnerable fish species in a highly anthropized coastal area.

The brown meagre (Sciaena umbra) is a vulnerable vocal fish species that may be affected by boat noise. The breeding site distribution along the anthropized Venice sea inlets was investigated, by using the species' chorusing activity as a proxy of spawning. Passive acoustic campaigns were repeated at 40 listening points distributed within the three inlets during three-time windows in both summer 2019 and 2020. The role of temporal, morphological, and hydrodynamic variables explaining the observed distribution patterns was evaluated using a GLM approach, considering also human-induced pressures among the candidate predictors. The GLM analysis indicates a higher probability of recording S. umbra chorus after sunset in deeper areas of the inlets, characterized by low water current, while the underwater noise overlapping the species' hearing range and boat abundance did not play any role. This suggests that the species' breeding site choice in the inlets was not influences by boat-induced pressure.

Characterization of the underwater noise produced by recreational and small fishing boats (<14 m) in the shallow-water of the Cres-Losinj Natura 2000 SCI.

Recreational boats are a dominant source of underwater noise in coastal areas, but reliable boat noise assessment is generally lacking. Here the Underwater Radiated Noise (URN) of seven recreational and small fishing boats moving at two different speeds was measured in the shallow waters of the Cres-Losinj Natura 2000 SCI (Croatia). Measurements were undertaken considering the internationally recognized standards and published guidelines for shallow waters. URN was provided in 1/3 octave band spectra and in narrow band spectra, to highlight the tonal components. Engine power and type rather than the boat length and design result to be more predictive of URN. Highest speeds induce highest noise levels only in a very limited frequency range and different boats with similar speed but different engines show a shift in the spectra. Relevance of the achieved results for the tested area is further discussed.

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.

Influence of foraging context on the whistle structure of the common bottlenose dolphin.

Sounds are particularly important for animals that live in complex social communities. In this study, we assessed the communication calls (whistles) that common bottlenose dolphins emit during their foraging activities in the absence and presence of motor boats and during dolphin depredation on trawlers, in Alghero (Sardinia, Italy) and Cres-Losinj Archipelago (Croatia). The latter behaviour involves foraging on concentrated food sources during very noisy human activity and may require the emission of distinctive whistles. Thus, we investigated if whistle structure, in terms of frequency and time parameters, changes depending on these three foraging contexts. In Sardinia, during foraging in interaction with trawlers, whistles differed from those emitted during the other foraging contexts. Conversely, in Cres-Losinj, significant variations in whistles were found to be related mainly to the presence of motor boats. This study represents the first report on how two dolphin populations adopt different acoustic tactics in the context of similar foraging behaviour. By investigating the effects of opportunistic foraging on acoustic repertoires, we provide new findings on the acoustic adaptation of dolphins to local conditions and contribute to understanding the relationships between dolphins and human activities, such as fishing and boat traffic.

Marine soundscape and fish biophony of a Mediterranean marine protected area.

BACKGROUND: Marine soundscape is the aggregation of sound sources known as geophony, biophony, and anthrophony. The soundscape analysis, in terms of collection and analysis of acoustic signals, has been proposed as a tool to evaluate the specific features of ecological assemblages and to estimate their acoustic variability over space and time. This study aimed to characterise the Capo Caccia-Isola Piana Marine Protected Area (Italy, Western Mediterranean Sea) soundscape over short temporal (few days) and spatial scales (few km) and to quantify the main anthropogenic and biological components, with a focus on fish biophonies. METHODS: Within the MPA, three sites were chosen each in a different protection zone (A for the integral protection, B as the partial protection, and C as the general protection). In each site, two underwater autonomous acoustic recorders were deployed in July 2020 at a depth of about 10 m on rocky bottoms. To characterise the contribution of both biophonies and anthrophonies, sea ambient noise (SAN) levels were measured as sound pressure level (SPL dB re: 1 µ Pa-rms) at eight 1/3 octave bands, centred from 125 Hz to 16 kHz, and biological and anthropogenic sounds were noted. Fish sounds were classified and counted following a catalogue of known fish sounds from the Mediterranean Sea based on the acoustic characteristic of sound types. A contemporary fish visual census had been carried out at the test sites. RESULTS: SPL were different by site, time (day vs. night), and hour. SPLs bands centred at 125, 250, and 500 Hz were significantly higher in the daytime, due to the high number of boats per minute whose noise dominated the soundscapes. The loudest man-made noise was found in the A zone, followed by the B and the C zone, confirming that MPA current regulations do not provide protection from acoustic pollution. The dominant biological components of the MPA soundscape were the impulsive sounds generated by some invertebrates, snapping shrimps and fish. The vast majority of fish sounds were recorded at the MPA site characterized by the highest sound richness, abundance, and Shannon-Wiener index, coherently with the results of a fish visual census. Moreover, the acoustic monitoring detected a sound associated with a cryptic species (Ophidion spp.) never reported in the study area before, further demonstrating the usefulness of passive acoustic monitoring as a complementary technique to species census. This study provides baseline data to detect future changes of the marine soundscapes and some suggestions to reduce the impact of noise on marine biodiversity.

Sound pressure and particle acceleration audiograms in three marine fish species from the Adriatic Sea.

Fishes show great variability in hearing sensitivity, bandwidth, and the appropriate stimulus component for the inner ear (particle motion or pressure). Here, hearing sensitivities in three vocal marine species belonging to different families were described in terms of sound pressure and particle acceleration. In particular, hearing sensitivity to tone bursts of varying frequencies were measured in the red-mouthed goby Gobius cruentatus, the Mediterranean damselfish Chromis chromis, and the brown meagre Sciaena umbra using the non-invasive auditory evoked potential-recording technique. Hearing thresholds were measured in terms of sound pressure level and particle acceleration level in the three Cartesian directions using a newly developed miniature pressure-acceleration sensor. The brown meagre showed the broadest hearing range (up to 3000 Hz) and the best hearing sensitivity, both in terms of sound pressure and particle acceleration. The red-mouthed goby and the damselfish were less sensitive, with upper frequency limits of 700 and 600 Hz, respectively. The low auditory thresholds and the large hearing bandwidth of S. umbra indicate that sound pressure may play a role in S. umbra's hearing, even though pronounced connections between the swim bladder and the inner ears are lacking.