Marine Mammal Hearing Research Articles

Noise-induced hearing loss in marine mammals: A review of temporary threshold shift studies from 1996 to 2015.

One of the most widely recognized effects of intense noise exposure is a noise-induced threshold shift—an elevation of hearing thresholds following cessation of the noise. Over the past twenty years, as concerns over the potential effects of human-generated noise on marine mammals have increased, a number of studies have been conducted to investigate noise-induced threshold shift phenomena in marine mammals. The experiments have focused on measuring temporary threshold shift (TTS)—a noise-induced threshold shift that fully recovers over time—in marine mammals exposed to intense tones, band-limited noise, and underwater impulses with various sound pressure levels, frequencies, durations, and temporal patterns. In this review, the methods employed by the groups conducting marine mammal TTS experiments are described and the relationships between the experimental conditions, the noise exposure parameters, and the observed TTS are summarized. An attempt has been made to synthesize the major findings across experiments to provide the current state of knowledge for the effects of noise on marine mammal hearing.

200 kHz commercial sonar systems generate lower frequency side lobes audible to some marine mammals.

The spectral properties of pulses transmitted by three commercially available 200 kHz echo sounders were measured to assess the possibility that marine mammals might hear sound energy below the center (carrier) frequency that may be generated by transmitting short rectangular pulses. All three sounders were found to generate sound at frequencies below the center frequency and within the hearing range of some marine mammals, e.g. killer whales, false killer whales, beluga whales, Atlantic bottlenose dolphins, harbor porpoises, and others. The frequencies of these sub-harmonic sounds ranged from 90 to 130 kHz. These sounds were likely detectable by the animals over distances up to several hundred meters but were well below potentially harmful levels. The sounds generated by the sounders could potentially affect the behavior of marine mammals within fairly close proximity to the sources and therefore the exclusion of echo sounders from environmental impact analysis based solely on the center frequency output in relation to the range of marine mammal hearing should be reconsidered.

Behavioral responses by grey seals (Halichoerus grypus) to high frequency sonar

The use of high frequency sonar is now commonplace in the marine environment. Most marine mammals rely on sound to navigate, and for detecting prey, and there is the potential that the acoustic signals of sonar could cause behavioral responses. To investigate this, we carried out behavioral response tests with grey seals to two sonar systems (200 and 375kHz systems). Results showed that both systems had significant effects on the seals behavior; when the 200kHz sonar was active, seals spent significantly more time hauled out and, although seals remained swimming during operation of the 375kHz sonar, they were distributed further from the sonar. The results show that although peak sonar frequencies may be above marine mammal hearing ranges, high levels of sound can be produced within their hearing ranges that elicit behavioral responses; this has clear implications for the widespread use of sonar in the marine environment.

Acoustic deterrent devices to prevent pinniped depredation: efficiency, conservation concerns and possible solutions

Acoustic deterrent devices (ADDs) to prevent pinniped predation on fish farms and fisheries are widely used, but show highly varying success. Recently, ADDs have also been high- lighted as a conservation concern due to their adverse impact on toothed whales. We review the available literature on the efficiency of commercial ADDs, evaluate the unintended impact on behaviour, communication and hearing of marine life, and suggest solutions based on psycho- physiological predictions. The main problems associated with ADDs are a lack of long-term effi- ciency, introduction of substantial noise pollution to the marine environment and long-term effects on target and non-target species. Odontocetes have more sensitive hearing than pinnipeds at the frequencies where most ADDs operate, which may explain the reported large-scale habitat exclu- sion of odontocetes when ADDs are used. Furthermore, long-term exposure to ADDs may damage the hearing of marine mammals. Fish and invertebrates have less sensitive hearing than marine mammals and fewer efforts have been made to quantify the effects of noise on these taxa. Solu- tions can be found by decreasing sound exposure, exploiting neuronal reflex arcs associated with flight behaviour and making use of differences in species' hearing abilities to increase target specificity. To minimise adverse effects, environmental impact assessments should be carried out before deploying ADDs and only effective and target-specific devices should be used.

HOW NOISE POLLUTION BATTERS BELUGA HEARING

The ocean is no longer the silent haven that it once was. Massive ships churn the sea; submarine explosions and ear-splitting construction can wreck the peace. Alexander Supin from the Russian Academy of Sciences explains that aquatic mammals are particularly vulnerable to noise pollution as they depend on their hearing for orientation, navigation and communication. Even a temporary loss of hearing could cause disoriented animals to beach in shallow water. ‘It is very important to know how severe the influence of noise is on cetacean hearing and which restrictions are necessary to minimise the impact and to speed recovery’, says Supin. However, sound can damage hearing in many different ways: a continual low-volume squeal can be as harmful as an explosion if the animal's hearing is particularly susceptible. Supin, Vladimir Popov and their colleagues explain that measuring the impact of multiple acoustic factors on cetaceans is challenging. They decided to measure the electrical activity in an animal's auditory system at the surface of the skin (auditory evoked potential) to rapidly assess the effect of various acoustic factors on the hearing of two captive belugas and to find out how quickly they recover from loud noise pollution (p. 1587).Supin and colleagues travelled to the Utrish Marine Station, situated on the Russian Black Sea coast, to test the animals' hearing. ‘The belugas were very cooperative, otherwise it would hardly be possible to perform the study’, he recalls. Gently lowering each animal into a small tank, the team measured the electrical activity produced by the animal's auditory system as it listened to soft sounds over frequencies ranging from 8 to 128 kHz to establish the minimum sound intensity that the animal could hear. Then, having established the whale's hearing threshold, the team played a loud sound – to simulate the kind of noise pollution that the whale might encounter – before monitoring the temporary effect that it had on the whale's ability to hear and the animal's recovery.Repeating the experiment while varying the pitch of the simulated noise pollution from 11.2 kHz up to 90 kHz, the intensity from 145 dB to 165 dB, and playing the sound for periods lasting from 1 to 30 min, the team found that the whales' hearing always recovered completely within a day. However, unexpectedly the whales' hearing took longer to recover after experiencing the lower pitched noises (11.2 and 22.5 kHz) than the higher pitched noises (45 and 90 kHz). ‘A commonly adopted point of view is that high frequencies are the most susceptible to any influence causing hearing loss’, says Supin, ‘but in our experiments, the middle frequency range [20–30 kHz] displayed the largest post-exposure loss of sensitivity’.In addition, the whales found it harder to hear sounds that were half an octave higher than the noise that they had just experienced, and when the team tracked the whales' recovery, they found that the longer the noise exposure, the longer it took the animals' hearing to recover. Finally, the team compared the impact that noise had on the two animals and they were surprised to find that the hearing of one of the animals was much more sensitive to noise than the other's, even though they were the same age and their initial hearing was equally good.Having discovered that the hearing of belugas is particularly sensitive to noise of specific frequencies, Supin is optimistic that the team's discoveries will help us to design better regulations for aquatic noise reduction in order to protect the hearing of marine mammals better.

Numerical simulations of acoustic emissions due to offshore‐pile installation

AbstractThe use of renewable energy is growing due to economic reasons and a spreading sense of ecology. One possible source for renewable energy is wind energy. It is predicted that the number of offshore wind parks will be increasing within the next ten years. The foundation piles of offshore wind power plants are normally installed by impact driving. This leads to an emission of acoustic noise which possibly influences or even damages the sense of hearing of marine mammals like seals and whales.In this contribution the propagation of acoustic waves in air and water due to pile driving is investigated using the finite element method (FEM) with an explicit time integration scheme. In the analyses a mass representing the pile hammer falls on an elastically modeled offshore monopile. The surrounding media is varied between air and water in order to investigate the acoustic emissions due to the pile driving process with respect to the medium. The numerical results are compared to measurements which can be found in literature to verify the numerical models. Furthermore, as a practical example the numerical model can be used in order to simulate noise reduction techniques such as the bubble curtain. (© 2011 Wiley‐VCH Verlag GmbH & Co. KGaA, Weinheim)

Auditory effects of multiple underwater impulses on bottlenose dolphins (Tursiops truncatus)

It is becoming increasingly clear that noise may adversely affect the hearing and behavior of many marine mammals, including dolphins and whales. One of the possible consequences of noise exposure is a temporary loss of hearing sensitivity, called a temporary threshold shift (TTS). Previous studies of TTS in marine mammals have used only steady-state and single impulsive sounds; however, many naval, seismic survey, and construction activities generate multiple underwater impulsive sounds. To investigate the auditory effects of multiple underwater impulses, auditory thresholds were measured in bottlenose dolphins before and after exposure to a series of impulses produced by a seismic airgun. Hearing thresholds were compared to determine the amount of TTS as a function of exposure level and the number of impulses. Thresholds were measured by using both psychophysical and auditory evoked potential methods. Preliminary results reveal no measurable TTS after exposure to 10 impulses, with a total cumulative sound exposure level of approximately 195 dB re 1 μPa2 s. [Work supported by the EP Sound and Marine Life Joint Industry Programme.]

Dolphin and sea lion auditory evoked potentials in response to single and multiple swept amplitude tones

Measurement of the auditory steady-state response (ASSR) is increasingly used to assess marine mammal hearing. These tests normally entail measuring the ASSR to a sequence of sinusoidally amplitude modulated tones, so that the ASSR amplitude function can be defined and the auditory threshold estimated. In this study, an alternative method was employed, where the ASSR was elicited by an amplitude modulated stimulus whose sound pressure level was slowly varied, or "swept," over a range of levels believed to bracket the threshold. The ASSR amplitude function was obtained by analyzing the resulting grand average evoked potential using a short-time Fourier transform. The suitability of this technique for hearing assessment of bottlenose dolphins and California sea lions was evaluated by comparing ASSR amplitude functions and thresholds obtained with swept amplitude and discrete, constant amplitude stimuli. When factors such as the number of simultaneous tones, the number of averages, and the frequency analysis window length were taken into account, the performance and time required for the swept-amplitude and discrete stimulus techniques were similar. The decision to use one technique over another depends on the relative importance of obtaining suprathreshold information versus the lowest possible thresholds.

Marine mammal auditory evoked potential measurements using swept amplitude stimuli.

Auditory evoked potentials are routinely used to characterize hearing in marine mammals for whom behavioral testing is not practical. For frequency-specific audiometry, the most popular evoked potential method has been the measurement of the auditory steady state response (ASSR). These tests normally entail measuring the ASSR to a sequence of sinusoidally amplitude modulated tones so that the ASSR input-output function can be defined and the auditory threshold estimated. In this study, an alternative method was employed, where thresholds were estimated in response to a single amplitude modulated stimulus whose sound pressure level varied linearly with time. The tone sound pressure was therefore swept over a range of levels believed to bracket the threshold. The input-output function was obtained by analyzing the resulting grand average evoked potential using a short-time Fourier transform. The swept amplitude technique was performed with bottlenose dolphins and California sea lions, with the resulting thresholds similar to those obtained with constant amplitude tones. The tradeoffs between the swept amplitude technique and the traditional, constant amplitude approach will be discussed. [Work supported by ONR.]

Using auditory evoked potentials to measure marine mammal hearing.

The use of auditory evoked potential (AEP) measurements for examining the hearing of marine mammals was accelerated by the need to rapidly test hearing following sound exposures during temporary threshold shift experiments. AEP measures have allowed quick measurements of hearing following intense noise exposures of sounds ranging from filtered white noise to 53‐C sonars. The refinement of AEP hearing measurements with envelope following response measures leads to comparisons between behavioral and AEP hearing thresholds. These comparisons have allowed an expansion of basic hearing measurements including measures of new species such as the white‐beaked dolphin and polar bear, measures of increased numbers of the same species in order to better examine population audiogram estimates and variability, and testing of hearing of animals in the field. AEP measures have also allowed the measurement of hearing during echolocation. A false killer whale has been shown to hear its own outgoing signal 40 dB down from the same sort of signal presented directly in front of it, actively control the level of its hearing of echolocation returns in an automatic gain control of hearing, and hear sounds other than echolocation sounds 20 dB differently when it is echolocating depending on target condition.

Non anthropogenic deafness in marine mammals: Hearing that is going, going, gone.

In humans, hearing is absent or diminished as a result of congenital defects, aging, noise exposures, traumatic events, and disease. Until concern arose about anthropogenic noise impacts on marine mammals, little was known about the mechanisms or incidence of marine mammal hearing losses. Over the past decade, we have gained substantial information from behavioral and electrophysiologic audiometres, in vivo imaging, and postmortem examinations. Dr. Sam Ridgway has been a pivotal element in these investigations, pioneering many of the techniques and facilitating broad collaborative studies. In this paper, the results of computerized tomographic and histologic studies of pinniped and cetacean ears, the majority of which Dr. Ridgway supplied, will be presented. The data show that marine mammals sustain precipitous and progressive hearing loss from multiple etiologies, including labyrinthitis, infestations, trauma, chronic multistage otitis, and presbycusis. In particular, older dolphins and seals develop degenerative pathologies (neural, hair cell, support cell loss, and demineralization) paralleling presbycusic changes in older humans. For captive cases, the distribution of inner ear pathologies will be compared with their premortem hearing curves to demonstrate the feasibility of back-projection hearing analyses on ears from noncaptive animals to better understand hearing status of wild populations. [Work supported by the ONR and the NIH/NIDCD]

Progress in clinical hearing evaluation of bottlenose dolphins (Tursiops truncatus).

It has long been recognized that the need to train experimental subjects is a major obstacle to large scale behavioral hearing studies of marine mammals. The time and level of access required for behavioral audiometry have not only prevented hearing assessment in wild individuals but have also limited attempts to assess auditory system fitness in captive populations. Ridgway and co‐workers of electrophysiological methods were quick to realize that auditory evoked potential (AEP) measurements could be used to assess marine mammal hearing without lengthy training. Ridgway performed some of the earliest work to characterize dolphin evoked potentials and to develop fast techniques for threshold measurement. In addition to hearing assessment in larger whales not routinely kept in captivity, Ridgway has also strived to develop techniques that would allow routine clinical hearing assessment of captive animals. This talk reviews the development of AEP techniques for rapid large‐scale hearing assessment in dolphins at the US Navy Marine Mammal Program. Topics range from Ridgway’s early work on dolphin AEP threshold measurements to recent efforts to acquire longitudinal audiometric data from a large population of dolphins. [Work supported by ONR.]

Evoked potential and behavioral hearing thresholds in nine bottlenose dolphins (Tursiops truncatus)

Auditory evoked potentials are popular for assessing hearing in marine mammals because they do not require the same access to and training of animals as behavioral methods; however, within-subject comparisons of behavioral and electrophysiological thresholds are still necessary to benchmark evoked potential results against the more universally accepted behavioral data. In this study, auditory thresholds were measured in nine dolphins using both behavioral and electrophysiological methods. Subjects included eight males and one female, ages 21-43 yrs. Some had a full-range of hearing and others exhibited high-frequency hearing loss. Tests were conducted in-air, in San Diego Bay, and/or in quiet pools. Hearing test stimuli included frequency-modulated, amplitude-modulated, or pure tones projected in the direct field or via a "jawphone" contact transducer. Comparisons reveal good agreement between the evoked potential and behavioral methods, particularly when the testing environments, stimulus delivery methods, and stimulus waveforms are similar. The results show that evoked potential thresholds obtained in a variety of conditions provide reasonable approximations to underwater sensitivity, especially with respect to the shape of the audiogram and the upper limit of hearing.

Proposed Marine Mammal Noise Exposure Criteria: Current Data Base, Limitations, and Research Needs

This paper presents the findings of an inter-disciplinary expert panel based on comprehensive review of hearing and noise effects data for marine and land mammals. The principal motivation for the review was to assist formulation of data-based noise exposure criteria in light of rapidly evolving research advances in marine mammal hearing and underwater noise effects. Levels estimated to induce permanent hearing loss were determined for single exposure events for cetaceans (in water) and pinnipeds (in air and water) for each of 15 sound type/animal group combinations. These recommendations represent a current best estimate only and are modular, with modifiable key variables; e.g., source and exposure, to facilitate revision as data improve. In some cases, relatively explicit injury limits are proposed, e.g., 186 dB re: 1μPa2-s (frequency-weighted sound exposure level) and 218 dB re: 1μPapeak (unweighted peak sound pressure level) for pinnipeds in water exposed to multiple sound pulses. In others, particularly for behavioural effects of multiple-pulse and non-pulse exposures, response severity and significance are quantitatively scored, but the data do not allow identification of specific broadly-applicable disturbance thresholds. These findings are a current best effort and include a discussion of limitations and recommended research needed to address data gaps.

Electrophysiological and behavioral measures of temporary threshold shift in a bottlenose dolphin (Tursiops truncatus)

Auditory evoked potentials are being increasingly applied to more advanced studies of marine mammal hearing, such as frequency selectivity, temporal processing, and temporary threshold shift (TTS). In this study, both behavioral and electrophysiological techniques were used to measure TTS in a bottlenose dolphin exposed to 20‐kHz tones. Behavioral hearing thresholds were estimated using a modified staircase procedure and a whistle response. Electrophysiological thresholds were assessed using the multiple auditory steady‐state response. Evoked potential stimuli consisted of seven frequency‐modulated tones having carrier frequencies from 10‐70 kHz and unique modulation rates. Tones were simultaneously presented and the evoked response at each modulation rate independently tracked to test hearing at all seven frequencies simultaneously. The behavioral and evoked response data both showed frequency‐dependent patterns of TTS, with the largest shifts at 30 kHz; however, TTS measured using evoked potentials (up to 40‐45 dB) was always larger than that observed behaviorally (19‐33 dB). This discrepancy may be the result of the evoked response input‐output function, which can be represented as the sum of two processes, a low threshold, saturating process and a higher threshold linear process, that react and recover to fatigue at different rates.

Anatomical predictions of hearing in the North Atlantic right whale

Some knowledge of the hearing abilities of right whales is important for understanding their acoustic communication system and possible impacts of anthropogenic noise. Traditional behavioral or physiological techniques to test hearing are not feasible with right whales. Previous research on the hearing of marine mammals has shown that functional models are reliable estimators of hearing sensitivity in marine species. Fundamental to these models is a comprehensive analysis of inner ear anatomy. Morphometric analyses of 18 inner ears from 13 stranded North Atlantic right whales (Eubalaena glacialis) were used for development of a preliminary model of the frequency range of hearing. Computerized tomography was used to create two-dimensional (2D) and 3D images of the cochlea. Four ears were decalcified and sectioned for histologic measurements of the basilar membrane. Basilar membrane length averaged 55.7 mm (range, 50.5 mm-61.7 mm). The ganglion cell density/mm averaged 1,842 ganglion cells/mm. The thickness/width measurements of the basilar membrane from slides resulted in an estimated hearing range of 10 Hz-22 kHz based on established marine mammal models. Additional measurements from more specimens will be necessary to develop a more robust model of the right whale hearing range.

Bottlenose dolphin (Tursiops truncatus) steady-state evoked responses to multiple simultaneous sinusoidal amplitude modulated tones

Auditory steady-state evoked potentials were measured in a bottlenose dolphin (Tursiops truncatus) in response to single and multiple sinusoidal amplitude modulated (SAM) tones. Tests were conducted in air using a "jawphone" sound projector. Evoked potentials were recorded noninvasively using surface electrodes embedded in suction cups. Sound stimuli consisted of SAM tones with 1, 2, 3, or 4 carrier frequencies (10, 20, 30, 40 kHz), each with a unique modulation frequency. Stimulus sound pressure levels were varied in 5-dB steps from approximately 120 to 60-75 dB re 1 microPa, depending on frequency. Evoked potentials followed the temporal envelope of each stimulus, resulting in spectral components at each unique modulation frequency. Spectral analysis was used to evaluate the response amplitude for each carrier as a function of stimulus level. There were no significant differences between thresholds obtained with single and multiple stimuli at 10, 30, and 40 kHz. At 20 kHz, thresholds obtained with three components were higher than those obtained with four components, possibly revealing interactions between stimuli with less than one octave frequency separation. The use of multiple SAM stimuli may offer substantial advantages for studies of marine mammal hearing, where testing time and access to subjects are typically limited.

Measurement and Response Characteristics of Auditory Brainstem Responses in Pinnipeds

The measurement of auditory evoked potentials (AEPs) has proven to be a useful tool for examining the auditory physiology of odontocete cetaceans and there is growing interest in applying this electrophysiological approach to study the hearing of other marine mammals. The aim of the current investigation was to examine some of the basic measurement and response characteristics of the auditory brainstem response (ABR) in pinnipeds. The subjects were California sea lions (Zalophus californianus), harbor seals (Phoca vitulina), and northern elephant seals (Mirounga angustirostris) that were awake, sedated, or anesthetized during in-air testing. Auditory stimuli were broadband clicks and Hanning-gated tone bursts that were presented binaurally in a direct field. The amplitude and waveform of the ABRs were evaluated as a function of subject state, electrode type and position, analog bandpass filtering, stimulus presentation rate, and stimulus bandwidth. Results indicate that the ABRs were of highest amplitude when measured from subdermal electrodes arranged in a common reference configuration, with the cephalic electrode placed 2 to 4 cm forward of the ears on the dorsal midline of the head. The ABR waveforms were generally similar among the species tested, although the amplitude of the elephant seal ABR was much smaller than that of the other two species at similar stimulus levels. Bandpass filtering of the ABR resulted in improved signal-tonoise ratios but also caused reduction in response amplitude and distortion of the ABR waveform at high-pass settings above 65 Hz. Five-cycle tone bursts provided the best tradeoff between response amplitude and frequency specificity. The amplitude of ABRs evoked by clicks and tone bursts as a function of stimulus level was approximately linear for California sea lions and harbor seals over a range of ~25 dB. Visually estimated thresholds for California sea lions were noise limited but were sensitive enough to show hearing loss in one older subject. These findings should inform future research efforts involving electrophysiological assessment of auditory function, hearing sensitivity, and noise impacts in pinnipeds.

Long-term trends in ocean noise

The effect of ocean noise, particularly from anthropogenic sources such as Navy sonar systems, on marine mammal hearing, behavior, and reproduction is of great concern. However, relatively few studies exist to make a definitive conclusion regarding rising ambient noise levels, due largely to the dearth of information over sufficiently long time periods for a sufficient number of geographical locations. A few studies have estimated that ocean noise is rising at a rate of approximately 3–5 dB per decade at some frequencies in some locations. This study is based upon ambient noise measurements from U.S. Navy sonobuoys deployed by operational units between 1993 and 2004. Data and analysis are presented for three areas of the ocean—the Northwestern Atlantic Ocean, the Greenland-Iceland-United Kingdom (GIUK) gap, and the Mediterranean Sea. Analysis of this data demonstrates a less significant increase, and in some cases, a decrease, in ocean noise for these three ocean areas at frequencies between 50 and 2000 Hz. Ocean noise levels in this study are comparable to measured ocean noise levels reported in the literature during the 1960’s.

Wind turbine underwater noise and marine mammals: implications of current knowledge and data needs

The demand for renewable energy has led to construction of offshore wind farms with high-power turbines, and many more wind farms are being planned for the shallow waters of the world's marine habitats. The growth of offshore wind farms has raised concerns about their impact on the marine environment. Marine mammals use sound for foraging, orientation and communication and are therefore possibly susceptible to negative effects of man-made noise generated from con- structing and operating large offshore wind turbines. This paper reviews the existing literature and assesses zones of impact from different noise-generating activities in conjunction with wind farms on 4 representative shallow-water species of marine mammals. Construction involves many types of activities that can generate high sound pressure levels, and pile-driving seems to be the noisiest of all. Both the literature and modeling show that pile-driving and other activities that generate intense impulses during construction are likely to disrupt the behavior of marine mammals at ranges of many kilometers, and that these activities have the potential to induce hearing impairment at close range. The reported noise levels from operating wind turbines are low, and are unlikely to impair hearing in marine mammals. The impact zones for marine mammals from operating wind turbines depend on the low-frequency hearing-abilities of the species in question, on sound-propagation conditions, and on the presence of other noise sources such as shipping. The noise impact on marine mammals is more severe during the construction of wind farms than during their operation.