Evolutionary novelties underlie sound production in baleen whales.

Baleen whales (mysticetes) use vocalizations to mediate their complex social and reproductive behaviours in vast, opaque marine environments1. Adapting to an obligate aquatic lifestyle demanded fundamental physiological changes to efficiently produce sound, including laryngeal specializations2-4. Whereas toothed whales (odontocetes) evolved a nasal vocal organ5, mysticetes have been thought to use the larynx for sound production1,6-8. However, there has been no direct demonstration that the mysticete larynx can phonate, or if it does, how it produces the great diversity of mysticete sounds9. Here we combine experiments on the excised larynx of three mysticete species with detailed anatomy and computational models to show that mysticetes evolved unique laryngeal structures for sound production. These structures allow some of the largest animals that ever lived to efficiently produce frequency-modulated, low-frequency calls. Furthermore, we show that this phonation mechanism is likely to be ancestral to all mysticetes and shares its fundamental physical basis with most terrestrial mammals, including humans10, birds11, and their closest relatives, odontocetes5. However, these laryngeal structures set insurmountable physiological limits to the frequency range and depth of their vocalizations, preventing them from escaping anthropogenic vessel noise12,13 and communicating at great depths14, thereby greatly reducing their active communication range.

Hector's dolphins (Cephalorhynchus hectori) produce both narrowband high-frequency and broadband acoustic signals.

Odontocetes produce clicks for echolocation and communication. Most odontocetes are thought to produce either broadband (BB) or narrowband high-frequency (NBHF) clicks. Here, we show that the click repertoire of Hector's dolphin (Cephalorhynchus hectori) comprises highly stereotypical NBHF clicks and far more variable broadband clicks, with some that are intermediate between these two categories. Both NBHF and broadband clicks were made in trains, buzzes, and burst-pulses. Most clicks within click trains were typical NBHF clicks, which had a median centroid frequency of 130.3 kHz (median -10 dB bandwidth = 29.8 kHz). Some, however, while having only marginally lower centroid frequency (median = 123.8 kHz), had significant energy below 100 kHz and approximately double the bandwidth (median -10 dB bandwidth = 69.8 kHz); we refer to these as broadband. Broadband clicks in buzzes and burst-pulses had lower median centroid frequencies (120.7 and 121.8 kHz, respectively) compared to NBHF buzzes and burst-pulses (129.5 and 130.3 kHz, respectively). Source levels of NBHF clicks, estimated by using a drone to measure ranges from a single hydrophone and by computing time-of-arrival differences at a vertical hydrophone array, ranged from 116 to 171 dB re 1 µPa at 1 m, whereas source levels of broadband clicks, obtained from array data only, ranged from 138 to 184 dB re 1 µPa at 1 m. Our findings challenge the grouping of toothed whales as either NBHF or broadband species.

Response of Eurasian otters (Lutra lutra) to underwater acoustic harassment device sounds.

Seal scarers (or acoustic harassment devices, AHDs) are designed to deter seals from fishing gear and aquaculture operations, as well as to prevent seals from entering rivers to avoid predation on valuable fish. Our study investigated the potential effects of AHDs on non-target species, specifically the Eurasian otters (Lutra lutra), by testing the reaction of two rehabilitated otters to simulated AHDs sounds at 1 and 14 kHz, with a received sound intensity of 105-145 dB re 1 µPa rms. The 1 kHz sounds were used to investigate alternative frequencies for scaring seals without scaring otters. The otters reacted to both 1 and 14 kHz tonal signals when retrieving fish from a feeding station 0.8 m below the surface. Their diving behaviour and time to extract food progressively increased as sound intensity increased for all tested sound levels. Notably, the sound levels used in our tests were significantly lower (40-80 dB) than the source levels from commercial AHDs. These findings highlight the importance of caution when using AHDs in river and sea habitats inhabited by otters, as AHDs can change their behaviour and potentially result in habitat exclusion.

Computed Tomography as a Method for Age Determination of Carnivora and Odontocetes with Validation from Individuals with Known Age.

Traditional methods for age determination of wildlife include either slicing thin sections off or grinding a tooth, both of which are laborious and invasive. Especially when it comes to ancient and valuable museum samples of rare or extinct species, non-invasive methods are preferable. In this study, X-ray micro-computed tomography (µ-CT) was verified as an alternative non-invasive method for age determination of three species within the order of Carnivora and suborders Odontoceti. Teeth from 13 red foxes (Vulpes vulpes), 2 American mink (Neogale vison), and 2 harbor porpoises (Phocoena phocoena) of known age were studied using µ-CT. The number of visible dental growth layers in the µ-CT were highly correlated with true age for all three species (R2 = 96%, p < 0.001). In addition, the Bland-Altman plot showed high agreement between the age of individuals and visible dental layers represented in 2D slices of the 3D µ-CT images. The true age of individuals was on average 0.3 (±0.6 SD) years higher than the age interpreted by the µ-CT image, and there was a 95% agreement between the true age and the age interpreted from visible dental layers in the µ-CT.

Survival improvements of marine mammals in zoological institutions mirror historical advances in human longevity.

An intense public debate has fuelled governmental bans on marine mammals held in zoological institutions. The debate rests on the assumption that survival in zoological institutions has been and remains lower than in the wild, albeit the scientific evidence in support of this notion is equivocal. Here, we used statistical methods previously applied to assess historical improvements in human lifespan and data on 8864 individuals of four marine mammal species (harbour seal, Phoca vitulina; California sea lion, Zalophus californianus; polar bear, Ursus maritimus; common bottlenose dolphin, Tursiops truncatus) held in zoos from 1829 to 2020. We found that life expectancy increased up to 3.40 times, and first-year mortality declined up to 31%, during the last century in zoos. Moreover, the life expectancy of animals in zoos is currently 1.65-3.55 times longer than their wild counterparts. Like humans, these improvements have occurred concurrently with advances in management practices, crucial for population welfare. Science-based decisions will help effective legislative changes and ensure better implementation of animal care.

Wild harbour porpoises startle and flee at low received levels from acoustic harassment device.

Acoustic Harassment Devices (AHD) are widely used to deter marine mammals from aquaculture depredation, and from pile driving operations that may otherwise cause hearing damage. However, little is known about the behavioural and physiological effects of these devices. Here, we investigate the physiological and behavioural responses of harbour porpoises (Phocoena phocoena) to a commercial AHD in Danish waters. Six porpoises were tagged with suction-cup-attached DTAGs recording sound, 3D-movement, and GPS (n = 3) or electrocardiogram (n = 2). They were then exposed to AHDs for 15 min, with initial received levels (RL) ranging from 98 to 132 dB re 1 µPa (rms-fast, 125 ms) and initial exposure ranges of 0.9-7 km. All animals reacted by displaying a mixture of acoustic startle responses, fleeing, altered echolocation behaviour, and by demonstrating unusual tachycardia while diving. Moreover, during the 15-min exposures, half of the animals received cumulative sound doses close to published thresholds for temporary auditory threshold shifts. We conclude that AHD exposure at many km can evoke both startle, flight and cardiac responses which may impact blood-gas management, breath-hold capability, energy balance, stress level and risk of by-catch. We posit that current AHDs are too powerful for mitigation use to prevent hearing damage of porpoises from offshore construction.

Adaptive echolocation behavior of bats and toothed whales in dynamic soundscapes.

Journal of Experimental Biology has a long history of reporting research discoveries on animal echolocation, the subject of this Centenary Review. Echolocating animals emit intense sound pulses and process echoes to localize objects in dynamic soundscapes. More than 1100 species of bats and 70 species of toothed whales rely on echolocation to operate in aerial and aquatic environments, respectively. The need to mitigate acoustic clutter and ambient noise is common to both aerial and aquatic echolocating animals, resulting in convergence of many echolocation features, such as directional sound emission and hearing, and decreased pulse intervals and sound intensity during target approach. The physics of sound transmission in air and underwater constrains the production, detection and localization of sonar signals, resulting in differences in response times to initiate prey interception by aerial and aquatic echolocating animals. Anti-predator behavioral responses of prey pursued by echolocating animals affect behavioral foraging strategies in air and underwater. For example, many insect prey can detect and react to bat echolocation sounds, whereas most fish and squid are unresponsive to toothed whale signals, but can instead sense water movements generated by an approaching predator. These differences have implications for how bats and toothed whales hunt using echolocation. Here, we consider the behaviors used by echolocating mammals to (1) track and intercept moving prey equipped with predator detectors, (2) interrogate dynamic sonar scenes and (3) exploit visual and passive acoustic stimuli. Similarities and differences in animal sonar behaviors underwater and in air point to open research questions that are ripe for exploration.

Visual deprivation induces a stronger dive response in a harbor porpoise.

The dive response allows marine mammals to perform prolonged breath-hold dives to access rich marine prey resources. Via dynamic adjustments of peripheral vasoconstriction and bradycardia, oxygen consumption can be tailored to breath-hold duration, depth, exercise, and even expectations during dives. By investigating the heart rate of a trained harbor porpoise during a two-alternative forced choice task, where the animal is either acoustically masked or blindfolded, we test the hypothesis that sensory deprivation will lead to a stronger dive response to conserve oxygen when facing a more uncertain and smaller sensory umwelt. We show that the porpoise halves its diving heart rate (from 55 to 25 bpm) when blindfolded but presents no change in heart rate during masking of its echolocation. Therefore, visual stimuli may matter more to echolocating toothed whales than previously assumed, and sensory deprivation can be a major driver of the dive response, possibly as an anti-predator measure.

ANIMAL-SPOT enables animal-independent signal detection and classification using deep learning.

Bioacoustic research spans a wide range of biological questions and applications, relying on identification of target species or smaller acoustic units, such as distinct call types. However, manually identifying the signal of interest is time-intensive, error-prone, and becomes unfeasible with large data volumes. Therefore, machine-driven algorithms are increasingly applied to various bioacoustic signal identification challenges. Nevertheless, biologists still have major difficulties trying to transfer existing animal- and/or scenario-related machine learning approaches to their specific animal datasets and scientific questions. This study presents an animal-independent, open-source deep learning framework, along with a detailed user guide. Three signal identification tasks, commonly encountered in bioacoustics research, were investigated: (1) target signal vs. background noise detection, (2) species classification, and (3) call type categorization. ANIMAL-SPOT successfully segmented human-annotated target signals in data volumes representing 10 distinct animal species and 1 additional genus, resulting in a mean test accuracy of 97.9%, together with an average area under the ROC curve (AUC) of 95.9%, when predicting on unseen recordings. Moreover, an average segmentation accuracy and F1-score of 95.4% was achieved on the publicly available BirdVox-Full-Night data corpus. In addition, multi-class species and call type classification resulted in 96.6% and 92.7% accuracy on unseen test data, as well as 95.2% and 88.4% regarding previous animal-specific machine-based detection excerpts. Furthermore, an Unweighted Average Recall (UAR) of 89.3% outperformed the multi-species classification baseline system of the ComParE 2021 Primate Sub-Challenge. Besides animal independence, ANIMAL-SPOT does not rely on expert knowledge or special computing resources, thereby making deep-learning-based bioacoustic signal identification accessible to a broad audience.

Pavlovian conditioning of gentoo penguins (Pygoscelis papua) to underwater sound.

Penguins are known to react to underwater noise, but it is unknown if they make use of sound cues while diving. We tested whether captive gentoo penguins (Pygoscelis papua) can pair underwater sounds with food through Pavlovian conditioning. Two seconds after an underwater sound (a 1-4 kHz sweep with a received level of 130 dB re 1 µPa RMS) was played back to one or two unidentifiable penguins, a dead fish was flushed into the water close to the underwater sound source. After 8 weeks of conditioning, one or more individual penguins approached the sound source after sound emission in 78.3% out of 230 trials. In 43 intermixed control trials with no sound preceding the fish, the penguins did not show any reaction in the pre-flush period. In an additional experiment, three identified penguins reacted to the sound in 66.7-100% out of 30 trials, with 0% reactions in five intermixed control trials. Our experiments demonstrate that gentoo penguins can be conditioned to underwater sound and that they associate underwater sounds with food. It is possible that gentoos, as well as other species of penguins, use sound cues while foraging. This may explain why penguins have been observed to react negatively to anthropogenic noise.

Age and lunar cycle predict harbor porpoise bycatch in the south-western Baltic Sea.

The harbor porpoise, Phocoena phocoena, is the only cetacean regularly occurring in the Baltic Sea. During the last decades, several anthropogenic activities have affected porpoises in the Baltic region. Most notably is bycatch in static fishing gear, such as gill nets, which is the main human-induced cause of death in odontocetes. There is still considerable uncertainty about which factors influence the amount of bycatch. In the present study, we reviewed bycatch data collected from 1987 to 2016 from the south-western Baltic Sea. There was a significant difference in bycatch due to seasonality and region, and there was a higher bycatch rate in juveniles than in adults. The only abiotic factor associated with bycatch was the lunar cycle, with more animals bycaught during a full moon. These results improve our understanding of which biotic and abiotic factors are associated with bycatch of Baltic harbor porpoises, which can be used to strengthen conservation endeavors such as managing fishing efforts.

Toothed whale auditory brainstem responses measured with a non-invasive, on-animal tag.

Empirical measurements of odontocete hearing are limited to captive individuals, constituting a fraction of species across the suborder. Data from more species could be available if such measurements were collected from unrestrained animals in the wild. This study investigated whether electrophysiological hearing data could be recorded from a trained harbor porpoise (Phocoena phocoena) using a non-invasive, animal-attached tag. The results demonstrate that auditory brainstem responses to external and self-generated stimuli can be measured from a stationary odontocete using an animal-attached recorder. With additional development, tag-based electrophysiological platforms may facilitate the collection of hearing data from freely swimming odontocetes in the wild.

Are Icelandic harbor seals acoustically cryptic to avoid predation?

Male harbor seals (Phoca vitulina) produce stereotypic underwater roars during the mating season. It remains unclear to what extent roar structures vary due to predation levels. Here, seal roars from waters with many (Iceland) and few (Denmark and Sweden) predators were compared. Most Icelandic roars included a long pulse train and a pause. Icelandic roars occurred less frequently, lasted longer (20.3 ± 6.5 s), and were recorded with lower received sound levels (98.3 ± 8.9 dB re 1 µPa root mean square) than roars from Denmark and Sweden. Local extrinsic factors may shape sound production in harbor seals more than previously reported.

The diel pattern in harbour porpoise clicking behaviour is not a response to prey activity.

Wild harbour porpoises (Phocoena phocoena) mainly forage during the night and, because they rely on echolocation to detect their prey, this is also when they are most acoustically active. It has been hypothesised that this activity pattern is a response to the diel behaviour of their major prey species. To test this hypothesis, we monitored the acoustic activity of two captive harbour porpoises held in a net pen continuously during a full year and fed by their human keepers during daylight hours, thus removing the influence of prey activity. The porpoises were exposed to similar temperature and ambient light conditions as free-ranging animals living in the same region. Throughout the year, there was a pronounced diel pattern in acoustic activity of the porpoises, with significantly greater activity at night, and a clear peak around sunrise and sunset throughout the year. Clicking activity was not dependent on lunar illumination or water level. Because the porpoises in the pen are fed and trained during daylight hours, the results indicate that factors other than fish behaviour are strongly influencing the diel clicking behaviour pattern of the species.

The common murre (Uria aalge), an auk seabird, reacts to underwater sound.

Marine mammals have fine-tuned hearing abilities, which makes them vulnerable to human-induced sounds from shipping, sonars, pile drivers, and air guns. Many species of marine birds, such as penguins, auks, and cormorants, find their food underwater where light is often limited, suggesting sound detection may play a vital role. Yet, for most marine birds, it is unknown whether they are using, and can thereby be affected by, underwater sound. The authors conducted a series of playback experiments to test whether Alcid seabirds responded to and were disrupted by, underwater sound. Underwater broadband sound bursts and mid-frequency naval 53 C sonar signals were presented to two common murres (Uria aalge) in a quiet pool. The received sound pressure levels varied from 110 to 137 dB re 1 µPa. Both murres showed consistent reactions to sounds of all intensities, as compared to no reactions during control trials. For one of the birds, there was a clearly graded response, so that more responses were found at higher received levels. The authors' findings indicate that common murres may be affected by, and therefore potentially also vulnerable to, underwater noise. The effect of man-made noise on murres, and possibly other marine birds, requires more thorough consideration.

Embracing Their Prey at That Dark Hour: Common Cuttlefish (Sepia officinalis) Can Hunt in Nighttime Light Conditions.

Cuttlefish are highly efficient predators, which strongly rely on their anterior binocular visual field for hunting and prey capture. Their complex eyes possess adaptations for low light conditions. Recently, it was discovered that they display camouflaging behavior at night, perhaps to avoid detection by predators, or to increase their nighttime hunting success. This raises the question whether cuttlefish are capable of foraging during nighttime. In the present study, prey capture of the common cuttlefish (Sepia officinalis) was filmed with a high-speed video camera in different light conditions. Experiments were performed in daylight and with near-infrared light sources in two simulated nightlight conditions, as well as in darkness. The body of the common cuttlefish maintained a velocity of less than 0.1 m/s during prey capture, while the tentacles during the seizing phase reached velocities of up to 2.5 m/s and accelerations reached more than 450 m/s2 for single individuals. There was no significant difference between the day and nighttime trials, respectively. In complete darkness, the common cuttlefish was unable to catch any prey. Our results show that the common cuttlefish are capable of catching prey during day- and nighttime light conditions. The common cuttlefish employ similar sensory motor systems and prey capturing techniques during both day- and nighttime conditions.

Amphibious hearing in a diving bird, the great cormorant (Phalacrocorax carbo sinensis).

Diving birds can spend several minutes underwater during pursuit-dive foraging. To find and capture prey, such as fish and squid, they probably need several senses in addition to vision. Cormorants, very efficient predators of fish, have unexpectedly low visual acuity underwater. So, underwater hearing may be an important sense, as for other diving animals. We measured auditory thresholds and eardrum vibrations in air and underwater of the great cormorant (Phalacrocorax carbo sinensis). Wild-caught cormorant fledglings were anaesthetized, and their auditory brainstem response (ABR) and eardrum vibrations to clicks and tone bursts were measured, first in an anechoic box in air and then in a large water-filled tank, with their head and ears submerged 10 cm below the surface. Both the ABR waveshape and latency, as well as the ABR threshold, measured in units of sound pressure, were similar in air and water. The best average sound pressure sensitivity was found at 1 kHz, both in air (53 dB re. 20 µPa) and underwater (58 dB re. 20 µPa). When thresholds were compared in units of intensity, however, the sensitivity underwater was higher than in air. Eardrum vibration amplitude in both media reflected the ABR threshold curves. These results suggest that cormorants have in-air hearing abilities comparable to those of similar-sized diving birds, and that their underwater hearing sensitivity is at least as good as their aerial sensitivity. This, together with the morphology of the outer ear (collapsible meatus) and middle ear (thickened eardrum), suggests that cormorants may have anatomical and physiological adaptations for amphibious hearing.

Spatial and Temporal Variability of Ambient Underwater Sound in the Baltic Sea.

During last decades, anthropogenic underwater sound and its chronic impact on marine species have been recognised as an environmental protection challenge. At the same time, studies on the spatial and temporal variability of ambient sound, and how it is affected by biotic, abiotic and anthropogenic factors are lacking. This paper presents analysis of a large-scale and long-term underwater sound monitoring in the Baltic Sea. Throughout the year 2014, sound was monitored in 36 Baltic Sea locations. Selected locations covered different natural conditions and ship traffic intensities. The 63 Hz, 125 Hz and 2 kHz one-third octave band sound pressure levels were calculated and analysed. The levels varied significantly from one monitoring location to another. The annual median sound pressure level of the quietest and the loudest location differed almost 50 dB in the 63 Hz one-third octave band. Largest difference in the monthly medians was 15 dB in 63 Hz one-third octave band. The same monitoring locations annual estimated probability density functions for two yearly periods show strong similarity. The data variability grows as the averaging time period is reduced. Maritime traffic elevates the ambient sound levels in many areas of the Baltic Sea during extensive time periods.

Memory for own behaviour in pinnipeds.

Pinnipeds are aquatic predators feeding on a vast range of prey, and their social behaviour differs greatly between species (from extreme polygyny in some sea lions to monogamy in some true seals). It has been hypothesised that the foraging and social complexity of their lifestyle should drive the evolution of their cognitive abilities. To investigate how aware pinnipeds are of their own behaviour, a grey seal (Halichoerus grypus), two harbour seals (Phoca vitulina) and four South American sea lions (Otaria flavescens) were trained to repeat their own behaviour on command. Three already trained behaviours were used, and the animal was asked to repeat the behaviour twice to ensure that the animal recalled its own behaviour and not the command given for the previous behaviour. All three species could recall their own behaviour significantly better than by chance. The duration for which the animals could recall their behaviour was tested using a staircase paradigm. A delay was implemented between the completion of the behaviour and the command to repeat it. The delay was increased after correct responses and decreased after incorrect responses. The performance of all species fell towards chance level after 12-18 s, with no significant difference between species. These results indicate that sea lions and true seals are aware of their own behaviour and that true seals have similar short-term memory abilities. It also shows that pinnipeds have less developed short-term memory abilities compared to other aquatic predators, such as the bottlenose dolphin. The complexity of pinniped foraging and social behaviour does not seem to have driven the evolution of short-term memory abilities in these animals but might have contributed to their ability to recall their own behaviour.

Field-based hearing measurements of two seabird species.

Hearing is a primary sensory modality for birds. For seabirds, auditory data is challenging to obtain and hearing data are limited. Here, we present methods to measure seabird hearing in the field, using two Alcid species: the common murre Uria aalge and the Atlantic puffin Fratercula arctica Tests were conducted in a portable semi-anechoic crate using physiological auditory evoked potential (AEP) methods. The crate and AEP system were easily transportable to northern Iceland field sites, where wild birds were caught, sedated, studied and released. The resulting data demonstrate the feasibility of a field-based application of an established neurophysiology method, acquiring high quality avian hearing data in a relatively quiet setting. Similar field methods could be applied to other seabirds, and other bird species, resulting in reliable hearing data from a large number of individuals with a modest field effort. The results will provide insights into the sound sensitivity of species facing acoustic habitat degradation.