Underwater high frequency noise: Biological responses in sea urchin Arbacia lixula (Linnaeus, 1758).

Marine life is extremely sensitive to the effects of environmental noise due to its reliance on underwater sounds for basic life functions, such as searching for food and mating. However, the effects on invertebrate species are not yet fully understood. The aim of this study was to determine the biochemical responses of Arbacia lixula exposed to high-frequency noise. Protein concentration, enzyme activity (esterase, phosphatase and peroxidase) and cytotoxicity in coelomic fluid were compared in individuals exposed for three hours to consecutive linear sweeps of 100 to 200 kHz lasting 1 s, and control specimens. Sound pressure levels ranged between 145 and 160 dB re 1µPa. Coelomic fluid was extracted and the gene and protein expression of HSP70 with RT-PCR was evaluated on coelomocytes. A significant change was found in enzyme activity and in the expression of the HSP70 gene and protein compared to the control. These results suggested that high-frequency stimuli elicit a noise-induced physiological stress response in A. lixula, confirming the vulnerability of this species to acoustic exposure. Furthermore, these findings provide the first evidence that cell-free coelomic fluid can be used as a signal to evaluate noise exposure in marine invertebrates.

Effects of acoustic stimulation on biochemical parameters in the digestive gland of Mediterranean mussel Mytilus galloprovincialis (Lamarck, 1819).

Underwater sounds generated by anthropogenic activity can cause behavior changes, temporary loss of hearing, damage to parts of the body, or death in a number of marine organisms and can also affect healing and survival. In this study, the authors examined the effects of high-frequency acoustic stimulations on a number of biochemical parameters in the Mediterranean mussel, Mytilus galloprovincialis. During the experiment, animals were placed in a test tank and exposed to acoustic signals [a linear sweep ranging from 100 to 200 kHz and lasting 1 s, with a sound pressure level range of between 145 and 160 dBrms (re 1µParms)] for 3 h. Total haemocyte count was assessed and glucose levels, cytotoxic activity and enzyme activity (alkaline phosphatase, esterase and peroxidase) in the digestive gland were measured. For the first time, this study suggests that high-frequency noise pollution has a negative impact on biochemical parameters in the digestive gland.

Underwater vocal complexity of Arctic seal Erignathus barbatus in Kongsfjorden (Svalbard).

In this study the description of underwater vocal repertoire of bearded seal in Svalbard (Norway) was extended. Two autonomous passive acoustic recorders were deployed for one year (August 2014-July 2015) in the inner and outer parts of the Kongsfjorden, and 1728 h were recorded and 17 220 vocalizations were found. Nine different vocalization classes were identified and characterized using ten acoustic parameters. The calls showed heterogeneous spectral features, but share the descending trend of frequency modulation. The different classes emerged were discriminated primarily by bandwidth and duration, and then by minimum frequency, central frequency, and maximum frequency in this order. This study represents a step forward to improve the understanding of the acoustic behaviour and the social function of these calls, and identified long passive acoustic monitoring as an effective method to assess vocal complexity and the ecology of marine species producing sounds.

Combining whistle acoustic parameters to discriminate Mediterranean odontocetes during passive acoustic monitoring.

Acoustic observation can complement visual observation to more effectively monitor occurrence and distribution of marine mammals. For effective acoustic censuses, calibration methods must be determined by joint visual and acoustic studies. Research is still needed in the field of acoustic species identification, particularly for smaller odontocetes. From 1994 to 2012, whistles of four odontocete species were recorded in different areas of the Mediterranean Sea to determine how reliably these vocalizations can be classified to species. Recordings were attributed to species by simultaneous visual observation. The results of this study highlight that the frequency parameters, which are linked to physical features of animals, show lower variability than modulation parameters, which are likely to be more dependent on complex eco-ethological contexts. For all the studied species, minimum and maximum frequencies were linearly correlated with body size. DFA and Classification Tree Analysis (CART) show that these parameters were the most important for classifying species; however, both statistical methods highlighted the need for combining them with the number of contour minima and contour maxima for correct classification. Generally, DFA and CART results reflected both phylogenetic distance (especially for common and striped dolphins) and the size of the species.

Fin whale song evolution in the North Atlantic.

Animal songs can change within and between populations as the result of different evolutionary processes. When these processes include cultural transmission, the social learning of information or behaviours from conspecifics, songs can undergo rapid evolutions because cultural novelties can emerge more frequently than genetic mutations. Understanding these song variations over large temporal and spatial scales can provide insights into the patterns, drivers and limits of song evolution that can ultimately inform on the species' capacity to adapt to rapidly changing acoustic environments. Here, we analysed changes in fin whale (Balaenoptera physalus) songs recorded over two decades across the central and eastern North Atlantic Ocean. We document a rapid replacement of song INIs (inter-note intervals) over just four singing seasons, that co-occurred with hybrid songs (with both INIs), and a clear geographic gradient in the occurrence of different song INIs during the transition period. We also found gradual changes in INIs and note frequencies over more than a decade with fin whales adopting song changes. These results provide evidence of vocal learning in fin whales and reveal patterns of song evolution that raise questions on the limits of song variation in this species.

Geographic variation of whistles of the striped dolphin (Stenella coeruleoalba) within the Mediterranean Sea.

The striped dolphin is a cosmopolitan species distributed worldwide. Morphological and genetic studies strongly suggest that the Mediterranean and eastern North Atlantic populations are isolated from each other. The Mediterranean population is considered a distinct conservation unit by International Union for the Conservation of Nature experts, classified as "vulnerable." This study describes the geographical variation of the striped dolphin whistles within the Mediterranean Sea. Recordings were collected from 1996 to 2003 throughout the basin, employing multiple platforms. Thirty-seven independent sightings with acoustic data collection were made, and 599 whistles were extracted and considered for statistical analysis. Whistle analysis enabled the identification of sub-populations of striped dolphins within the Mediterranean Sea. The acoustic diversity observed reflects the genetic differences recently found among striped dolphins inhabiting different Mediterranean regions. The results of this study support the hypothesis that gene flow reduction plays an important role in determining variation in whistle duration and frequency parameters, while ecological and social factors influence parameters of the modulation domains. The ability to acoustically identify distinct geographic sub-populations could provide a useful tool for the management of this protected species.

Geographic variability in the acoustic parameters of striped dolphin's (Stenella coeruleoalba) whistles.

Geographic variation in the acoustic features of whistles emitted by the striped dolphin (Stenella coeruleoalba) from the Atlantic Ocean (Azores and Canary Islands) and the Mediterranean was investigated. Ten parameters (signal duration, beginning, end, minimum and maximum frequency, the number of inflection points, of steps, of minima and maxima in the contour and the frequency range) were extracted from each whistle. Discriminant function analysis correctly classified 73% of sounds between Atlantic Ocean and Mediterranean Sea. A cline in parameters was apparent from the Azores to the Mediterranean, with a major difference between the Canaries and the Mediterranean than between Azores and Canaries. Signal duration, maximum frequency, and frequency range measured in the Mediterranean sample were significantly lower compared to those measured in the Atlantic. Modulation parameters played a considerable role in area discrimination and were the only parameters contributing to highlight the differences within the Atlantic Ocean. Results suggest that the acoustic features constrained by structural phenotype, such as whistle's frequency parameters, have a major effect on the Atlantic and Mediterranean separation while behavioral context, social, and physical environment may be among the main factors contributing to local distinctiveness of Atlantic areas. These results have potential passive acoustic monitoring applications.

Bray-Call Sequences in the Mediterranean Common Bottlenose Dolphin (Tursiops truncatus) Acoustic Repertoire.

Acoustic sequences are commonly observed in many animal taxa. The vast vocal repertoire of common bottlenose dolphins (Tursiops truncatus) also includes sequences of multi-unit rhythmic signals called bray-call which are still poorly documented, both functionally and geographically. This study aimed to (1) describe, classify, and characterize series of bray-call recorded in two sites of the Mediterranean basin (Rome-Tyrrhenian Sea and Mazara del Vallo-Strait of Sicily) and (2) investigate for the existence of possible geographic differences. The acoustic analysis identified 13 different sequence types, only two detected in both study areas. The Sørensen-Dice index revealed a low degree of similarity between the sequence repertoire of the two common bottlenose dolphin sub-populations, with the Tyrrhenian being more diversified and complex than the Sicilian one. The acoustic parameters also showed variability between the study area. Different variants of the main acoustic elements composing the bray-call sequences were detected in the Tyrrhenian Sea only. The Markov-chain model demonstrated that the transition probability between acoustic elements is not uniform, with specific combinations of elements having a higher probability of occurrence. These new findings on common bottlenose dolphin bray-call sequences highlight the structural complexity of these vocalizations and suggest addressing future research on the context of emissions and the possible function(s) of such acoustic arrangements.

Capitoline Dolphins: Residency Patterns and Abundance Estimate of Tursiops truncatus at the Tiber River Estuary (Mediterranean Sea).

Periodic assessments of population status and trends to detect natural influences and human effects on coastal dolphin are often limited by lack of baseline information. Here, we investigated for the first time the site-fidelity patterns and estimated the population size of bottlenose dolphins (Tursiops truncatus) at the Tiber River estuary (central Mediterranean, Tyrrhenian Sea, Rome, Italy) between 2017 and 2020. We used photo-identification data and site-fidelity metrics to study the tendency of dolphins to remain in, or return to, the study area, and capture-recapture models to estimate the population abundance. In all, 347 unique individuals were identified. The hierarchical cluster analysis highlighted 3 clusters, labeled resident (individuals encountered at least five times, in three different months, over three distinct years; n = 42), part-time (individuals encountered at least on two occasions in a month, in at least two different years; n = 73), and transient (individuals encountered on more than one occasion, in more than 1 month, none of them in more than 1 year; n = 232), each characterized by site-fidelity metrics. Open POPAN modeling estimated a population size of 529 individuals (95% CI: 456-614), showing that the Capitoline (Roman) coastal area and nearby regions surrounding the Tiber River estuary represent an important, suitable habitat for bottlenose dolphins, despite their proximity to one of the major urban centers in the world (the city of Rome). Given the high number of individuals in the area and the presence of resident individuals with strong site fidelity, we suggest that conservation plans should not be focused only close to the Tiber River mouths but extended to cover a broader scale of area.

Dolphin whistles can be useful tools in identifying units of conservation.

BACKGROUND: Prioritizing groupings of organisms or 'units' below the species level is a critical issue for conservation purposes. Several techniques encompassing different time-frames, from genetics to ecological markers, have been considered to evaluate existing biological diversity at a sufficient temporal resolution to define conservation units. Given that acoustic signals are expressions of phenotypic diversity, their analysis may provide crucial information on current differentiation patterns within species. Here, we tested whether differences previously delineated within dolphin species based on i) geographic isolation, ii) genetics regardless isolation, and iii) habitat, regardless isolation and genetics, can be detected through acoustic monitoring. Recordings collected from 104 acoustic encounters of Stenella coeruleoalba, Delphinus delphis and Tursiops truncatus in the Azores, Canary Islands, the Alboran Sea and the Western Mediterranean basin between 1996 and 2012 were analyzed. The acoustic structure of communication signals was evaluated by analyzing parameters of whistles in relation to the known genetic and habitat-driven population structure. RESULTS: Recordings from the Atlantic and Mediterranean were accurately assigned to their respective basins of origin through Discriminant Function Analysis, with a minimum 83.8% and a maximum 93.8% classification rate. A parallel pattern between divergence in acoustic features and in the genetic and ecological traits within the basins was highlighted through Random Forest analysis. Although it is not yet possible to establish a causal link between each driver and acoustic differences between basins, we showed that signal variation reflects fine-scale diversity and may be used as a proxy for recognizing discrete units. CONCLUSION: We recommend that acoustic analysis be included in assessments of delphinid population structure, together with genetics and ecological tracer analysis. This cost-efficient non-invasive method can be applied to uncover distinctiveness and local adaptation in other wide-ranging marine species.

Soundscape of green turtle foraging habitats in Fiji, South Pacific.

The soundscape features of the marine environment provide crucial information about ecosystem health for many species, and they are defined by the local biological, geophysical, and anthropogenic components. In this study, we investigated the soundscape at green turtle neritic foraging habitats in Fiji, South Pacific, with the aims of characterizing the contribution of each component and of comparing the levels of acoustic pressure among sites with different abundances of sea turtles. Four sites were selected at two islands, and one hydrophone was deployed at each site. Generalized additive models highlighted that sound pressure levels (SPLs) at low frequencies (125-250 Hz) were especially affected by wind conditions, while at higher frequencies (>250 Hz) SPLs were mostly influenced by fish and crustacean acoustic activity. Higher abundances of green turtles were found at sites with the highest levels of SPLs and the highest number of acoustic emissions by fishes and crustaceans but were not related to maximum seagrass and macroalgae coverage, or the highest number of fish. The selected coastal habitats have negligible anthropogenic noise, thus this study informs physiological and behavioral studies of the acoustic signatures that sea turtles might target and provides a baseline against which potential impact of soundscape changes on sea turtle spatial abundance and distribution can be evaluated.

Acoustic impact of a wave energy converter in Mediterranean shallow waters.

In this study, underwater noise from a full-scale wave energy converter system (ISWEC), installed on the coast of Pantelleria Island (central Mediterranean Sea), was characterized. The noise was measured using an autonomous acoustic recorder anchored to the sea bottom 40 m from the ISWEC hull. Acoustic monitoring continued for 15 months, starting 7 months before (PRE), 2 months during (INST) and 6 months after the ISWEC installation (POST). The levels of noise, assessed with power spectrum density and octave and third-octave band sound pressure levels (BSPLs), were higher during the POST period than during the PRE period at lower frequencies up to 4 kHz and increased with wave height. During the ISWEC activation for energy production (POST_ON) in the wave height range 1-2.9 m, the BSPLs increased much more at lower frequencies up to 4 kHz (the median BSPLs at 63 Hz for the PRE, POST, and POST_ON conditions were 73, 106, and 126 dB re 1µPa, respectively). Considering the biophonies that make up the soundscape of the area, we examined the possible masking of fish choruses due to ISWEC noise and highlighted that at a distance of 1000 m, the 800 Hz peak frequency was 10 dB above the ISWEC signal. Within this distance from ISWEC, a possible masking effect is supposed.

Social relationships and death-related behaviour in aquatic mammals: a systematic review.

Some aquatic mammals appear to care for their dead, whereas others abandon their live offspring when conditions are unfavourable. This incredible variety in behaviours suggests the importance of comparing and contrasting mechanisms driving death-related behaviours among these species. We reviewed 106 cases of aquatic mammals (81 cetaceans and 25 non-cetaceans) reacting to a death event, and extrapolated 'participant' (age class, sex, relationship and decomposition) and 'social' characteristics (escorting, calf dependence, alloparental care, herding and dispersal patterns) from published and unpublished literature. A multiple correspondence analysis (MCA) was performed to explore the relationships between these characteristics and death-related behaviours, with species clustered based on MCA scores. Results showed that both cetaceans and non-cetaceans react to death but in different ways. Non-cetaceans, characterized by a short maternal investment, were observed to protect the dead (defending it from external attacks), while cetaceans spent much longer with their offspring and display carrying (hauling, spinning, mouthing with the carcass and diving with it) and breathing-related (lifting and sinking the carcass) activities with the dead generally in association with other conspecifics. Our work emphasizes the need of increased documentation of death-related cases around the world to improve our understanding of aquatic mammals and their responses to death.This article is part of the theme issue 'Evolutionary thanatology: impacts of the dead on the living in humans and other animals'.

Long-Term Monitoring of Dolphin Biosonar Activity in Deep Pelagic Waters of the Mediterranean Sea.

Dolphins emit short ultrasonic pulses (clicks) to acquire information about the surrounding environment, prey and habitat features. We investigated Delphinidae activity over multiple temporal scales through the detection of their echolocation clicks, using long-term Passive Acoustic Monitoring (PAM). The Istituto Nazionale di Fisica Nucleare operates multidisciplinary seafloor observatories in a deep area of the Central Mediterranean Sea. The Ocean noise Detection Experiment collected data offshore the Gulf of Catania from January 2005 to November 2006, allowing the study of temporal patterns of dolphin activity in this deep pelagic zone for the first time. Nearly 5,500 five-minute recordings acquired over two years were examined using spectrogram analysis and through development and testing of an automatic detection algorithm. Echolocation activity of dolphins was mostly confined to nighttime and crepuscular hours, in contrast with communicative signals (whistles). Seasonal variation, with a peak number of clicks in August, was also evident, but no effect of lunar cycle was observed. Temporal trends in echolocation corresponded to environmental and trophic variability known in the deep pelagic waters of the Ionian Sea. Long-term PAM and the continued development of automatic analysis techniques are essential to advancing the study of pelagic marine mammal distribution and behaviour patterns.

Dolphins adjust species-specific frequency parameters to compensate for increasing background noise.

An increase in ocean noise levels could interfere with acoustic communication of marine mammals. In this study we explored the effects of anthropogenic and natural noise on the acoustic properties of a dolphin communication signal, the whistle. A towed array with four elements was used to record environmental background noise and whistles of short-beaked common-, Atlantic spotted- and striped-dolphins in the Canaries archipelago. Four frequency parameters were measured from each whistle, while Sound Pressure Levels (SPL) of the background noise were measured at the central frequencies of seven one-third octave bands, from 5 to 20 kHz. Results show that dolphins increase the whistles' frequency parameters with lower variability in the presence of anthropogenic noise, and increase the end frequency of their whistles when confronted with increasing natural noise. This study provides the first evidence that the synergy among SPLs has a role in shaping the whistles' structure of these three species, with respect to both natural and anthropogenic noise.

Size Distribution of Sperm Whales Acoustically Identified during Long Term Deep-Sea Monitoring in the Ionian Sea.

The sperm whale (Physeter macrocephalus) emits a typical short acoustic signal, defined as a "click", almost continuously while diving. It is produced in different time patterns to acoustically explore the environment and communicate with conspecifics. Each emitted click has a multi-pulse structure, resulting from the production of the sound within the sperm whale's head. A Stable Inter Pulse Interval (Stable IPI) can be identified among the pulses that compose a single click. Applying specific algorithms, the measurement of this interval provides useful information to assess the total length of the animal recorded. In January 2005, a cabled hydrophone array was deployed at a depth of 2,100 m in the Central Mediterranean Sea, 25 km offshore Catania (Ionian Sea). The acoustic antenna, named OνDE (Ocean noise Detection Experiment), was in operation until November 2006. OνDE provided real time acoustic data used to perform Passive Acoustic Monitoring (PAM) of cetacean sound emissions. In this work, an innovative approach was applied to automatically measure the Stable IPI of the clicks, performing a cepstrum analysis to the energy (square amplitude) of the signals. About 2,100 five-minute recordings were processed to study the size distribution of the sperm whales detected during the OνDE long term deep-sea acoustic monitoring. Stable IPIs were measured in the range between 2.1 ms and 6.4 ms. The equations of Gordon (1991) and of Growcott (2011) were used to convert the IPIs into measures of size. The results revealed that the sperm whales recorded were distributed in length from about 7.5 m to 14 m. The size category most represented was from 9 m to 12 m (adult females or juvenile males) and specimens longer than 14 m (old males) seemed to be absent.

Annual Acoustic Presence of Fin Whale (Balaenoptera physalus) Offshore Eastern Sicily, Central Mediterranean Sea.

In recent years, an increasing number of surveys have definitively confirmed the seasonal presence of fin whales (Balaenoptera physalus) in highly productive regions of the Mediterranean Sea. Despite this, very little is yet known about the routes that the species seasonally follows within the Mediterranean basin and, particularly, in the Ionian area. The present study assesses for the first time fin whale acoustic presence offshore Eastern Sicily (Ionian Sea), throughout the processing of about 10 months of continuous acoustic monitoring. The recording of fin whale vocalizations was made possible by the cabled deep-sea multidisciplinary observatory, "NEMO-SN1", deployed 25 km off the Catania harbor at a depth of about 2,100 meters. NEMO-SN1 is an operational node of the European Multidisciplinary Seafloor and water-column Observatory (EMSO) Research Infrastructure. The observatory was equipped with a low-frequency hydrophone (bandwidth: 0.05 Hz-1 kHz, sampling rate: 2 kHz) which continuously acquired data from July 2012 to May 2013. About 7,200 hours of acoustic data were analyzed by means of spectrogram display. Calls with the typical structure and patterns associated to the Mediterranean fin whale population were identified and monitored in the area for the first time. Furthermore, a background noise analysis within the fin whale communication frequency band (17.9-22.5 Hz) was conducted to investigate possible detection-masking effects. The study confirms the hypothesis that fin whales are present in the Ionian Sea throughout all seasons, with peaks in call detection rate during spring and summer months. The analysis also demonstrates that calls were more frequently detected in low background noise conditions. Further analysis will be performed to understand whether observed levels of noise limit the acoustic detection of the fin whales vocalizations, or whether the animals vocalize less in the presence of high background noise.