Marine Mammal Hearing Research Articles

Underwater temporary threshold shift in pinnipeds: Effects of noise level and duration

Behavioral psychophysical techniques were used to evaluate the residual effects of underwater noise on the hearing sensitivity of three pinnipeds: a California sea lion (Zalophus californianus), a harbor seal (Phoca vitulina), and a northern elephant seal (Mirounga angustirostris). Temporary threshold shift (TTS), defined as the difference between auditory thresholds obtained before and after noise exposure, was assessed. The subjects were exposed to octave-band noise centered at 2500 Hz at two sound pressure levels: 80 and 95 dB SL (re: auditory threshold at 2500 Hz). Noise exposure durations were 22, 25, and 50 min. Threshold shifts were assessed at 2500 and 3530 Hz. Mean threshold shifts ranged from 2.9-12.2 dB. Full recovery of auditory sensitivity occurred within 24 h of noise exposure. Control sequences, comprising sham noise exposures, did not result in significant mean threshold shifts for any subject. Threshold shift magnitudes increased with increasing noise sound exposure level (SEL) for two of the three subjects. The results underscore the importance of including sound exposure metrics (incorporating sound pressure level and exposure duration) in order to fully assess the effects of noise on marine mammal hearing.

Testing marine mammal hearing with a vocal response paradigm and the method of free response

Behavioral hearing tests with marine mammals often use single interval experiments with a go/no-go paradigm, where the subject pushes a response paddle or similar device to indicate the presence of a hearing test tone. This approach is widely accepted, but the time required for the subject to physically move and/or interact with the response device and the requirement of one trial per reinforcement interval limit the speed at which data can be collected (typically 20–30 minutes for a threshold). An alternative to the single interval/paddle press approach is the use of a vocal response technique and the method of free response, where multiple trials are presented within a single reinforcement interval. An acoustic or vocal response eliminates the need for the subjects to physically move, allowing for faster responses and shorter inter-trial intervals. The method of free response allows multiple tone presentations between reinforcement periods, dramatically increasing the rate at which data may be collected, especially from diving marine mammals. This talk describes the application of these techniques to hearing tests of bottlenose dolphins, white whales, and California sea lions and the advantages and disadvantages compared to the single interval experiment. [Work supported by ONR.]

Estimating the risk of temporary acoustic threshold shift, caused by hydroacoustic devices, in whales in the Southern Ocean

There is a potential threat to marine mammals from acoustic signals emitted by hydroacoustic devices. The impact on the hearing of marine mammals depends on the technical parameters of the instruments and on the exposure of the animal to noise pulses, as well as on the properties of the biological system, that is to say, on the anatomy and the audiogram of the animal. Here, the blue whale, the sperm whale and the beaked whale are taken as examples in an investigation of the potential exposure to noise pulses from the hydroacoustic instruments Hydrosweep and Parasound. Diving depths of the whales and relative speeds of the animals with respect to the survey vessels are taken into account, as well as the area impacted by the equipment, in estimating the level of sound needed to produce “temporary threshold shift” in an animal. The results suggest that auditory damage is only likely if animals pass the transducer at close range and that the impact on marine mammals can be mitigated by implementing prior detection and shut down procedures.

Hearing in the North Atlantic right whale: Anatomical predictions

Understanding the hearing abilities of large whales is important to determine the impacts of anthropogenic sources of sound. Right whales are not amenable to traditional physiological techniques to test hearing. Previous research on the hearing of marine mammals has shown that functional morphometric models are reliable estimators of hearing sensitivity in marine species. Morphometric analyses of 18 inner ears from 13 stranded right whales were used in the development of a preliminary model of the frequency range of hearing. All ears were scanned with computerized tomography (CT). Four ears showing the best preservation were processed into slides for measurements of the basilar membrane. Calculated basilar-membrane length averaged 55.7 mm (range 50.5–61.7 mm). The ganglion cell density/mm averaged 1842 ganglion cells/mm. Membrane length and ganglion cell density were used to predict a total ganglion cell count of approximately 102<th>500 ganglion cells for right whales. The thickness/width measurements of the basilar membrane from slides resulted in an estimated frequency range of approximately 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. a)Currently at Cornell University Bioacoustics Research Program.

Water column pressures induced by vibrators operating on floating ice

Over the past 30 years, there has been an increased interest in the effects of anthropomorphically generated noise on the hearing of marine animals. In response to this concern, and to promote the conservation of marine environments, the U.S. Congress passed the Marine Mammal Protection Act (MMPA) in 1972. In essence, this act made it illegal to intentionally harass or harm any marine mammal. Because sound propagating through water has the potential to disrupt behavior patterns or impair the hearing of different species, several government regulatory agencies such as the National Marine Fisheries Service, the Fish and Wildlife Service, and the Minerals Management Service have developed programs to study these issues. Of particular concern are pressure waves generated by marine seismic air-gun arrays. It is feared that these high pressures may cause a temporary or permanent threshold shift in the hearing of certain marine mammals. To avoid this possibility, government regulatory agencies require a series of acoustic studies prior to seismic operations in offshore areas of the State of Alaska. This information is used to establish a safety radius for certain marine mammals. If an animal is observed to swim within this radius, the seismic vessel must stop operations. The MMPA does not specifically address the issue of harassment or harm to fish populations. Nevertheless, several federal, state, and local government agencies, as well as stakeholders, have expressed increasing concern over the effects of seismic noise on fish. The concerns are much the same as they are for marine mammals. Government biologists want to know if the sound levels produced by seismic sources have the potential to harm or kill local populations of fish. Actually these questions have been addressed many times over the last several years. Several studies have shown that air guns do not produce an acoustic field …

Three-dimensional modeling of hearing in Delphinus delphis.

Physical modeling is a fertile approach to investigating sound emission and reception (hearing) in marine mammals. A method for simulation of hearing was developed combining three-dimensional acoustic propagation and extrapolation techniques with a novel approach to modeling the acoustic parameters of mammalian tissues. Models of the forehead and lower jaw tissues of the common dolphin, Delphinus delphis, were created in order to simulate the biosonar emission and hearing processes. This paper outlines the methods used in the hearing simulations and offers observations concerning the mechanisms of acoustic reception in this dolphin based on model results. These results include: (1) The left and right mandibular fat bodies were found to channel sound incident from forward directions to the left and right tympanic bulla and to create sharp maxima against the lateral surfaces of each respective bulla; (2) The soft tissues of the lower jaw improved the forward directivity of the simulated receptivity patterns; (3) A focal property of the lower-jaw pan bones appeared to contribute to the creation of distinct forward receptivity peaks for each ear; (4) The reception patterns contained features that may correspond to lateral hearing pathways. A "fast" lens mechanism is proposed to explain the focal contribution of the pan bones in this dolphin. Similar techniques may be used to study hearing in other marine mammals.

Review of marine mammal temporary threshold shift (TTS) measurements and their application to damage-risk criteria

Intense anthropogenic underwater sound may adversely effect the hearing and behavior of many marine mammals. Exposure to intense sound may produce an elevated hearing threshold, also known as a threshold shift (TS). If the threshold returns to the pre-exposure level after a period of time, the TS is known as a temporary threshold shift (TTS); if the threshold does not return to the pre-exposure level, the TS is called a permanent threshold shift (PTS). PTS and TTS data were used to establish noise exposure limits in humans and TTS data are often used to help predict the effects of anthropogenic noise on marine mammals in the wild. Previous studies of TTS in marine mammals conducted at SSC San Diego have examined the effects of exposure to single 1 s pure tones and underwater impulsive waveforms. This paper reviews the TTS studies conducted at SSC San Diego over the last 5 years and summarizes the resulting data. The application of these data to the development of damage-risk criteria for marine mammals will also be discussed.

Anthropogenic ocean noise: Negligible or negligent impact?

The increasing use of the oceans is accompanied by rising acoustic pollution. From explosive transients to the nearly continuous drone of ships, anthropogenic noise accompanies virtually every human activity in the sea. Anthropogenic noise has the potential for significant impact on marine species, especially marine mammals, yet existing data are insufficient to predict accurately any but the grossest consequences. There are almost no controlled data on how the acoustic environment is changing as a result of human activity. There is also little information on how marine mammals respond physically and behaviorally, either to intense transients or to a long-term background increase in ambient noise. Ignorance and resulting caution in testing potentially harmful acoustic devices may be seriously hampering our learning progress and the development of effective acoustic deterrents that could decrease marine mammal by-catch. This work discusses the current understanding of acoustic trauma and ambient noise characteristics in the context of what is known about marine mammal hearing and its variations. The work focuses on how species vary in their potential for impact and on determining whether acoustically vulnerable species coincide with acoustic ‘‘hot spots’’ in the ocean where Man’s activities may damage hearing and disrupt key behaviors.

Validation of a system for synthesizing distant signatures of underwater explosions for sea mammal hearing studies

A system for synthesizing distant signatures of underwater explosions was described in an earlier talk [J. A. Clark and Jane A. Young, J. Acoust. Soc. Am. 102, 3177(A) (1997)]. The system is now being used to study expected temporary threshold shifts (TTS) of sea mammals near underwater explosive test ranges in the Baltic sea. The results of these studies will be used to define safe range criteria for mammal hearing which will then be incorporated into the methodology for assessing potential damage to marine mammal hearing. Typical underwater explosion signals (time histories) were selected from an extensive set of blast signals computed for a variety of charge weights, explosion depths, ranges from the blast, and water conditions specified by sound-speed profiles and water depths. The selected signals were synthesized and measured at the location of the test mammals (bottlenose dolphins). The fidelity of the synthesized signals to the computed waveforms was determined by comparing such characteristics as peak pressures, positions of major spikes in the time histories, and one-third octave band energy spectra. Examples of typical signals used for the TTS studies and their measured characteristics will be presented.

Marine mammal ears: An anatomical perspective on underwater hearing

Analyzing structure and function in specialized ears can produce new insights into fundamental hearing mechanisms and lead to technological advances. Research into dolphin echolocation is a classic example. Recently, however, concerns over anthropogenic sounds in the oceans pushed us to develop a broader knowledge of marine mammal hearing, and, in the last five years, hearing research on marine mammals expanded considerably. The resulting data on their hearing, ear anatomy, and vocalizations suggest that marine mammal ears are more diverse and complex than previously expected, with acoustic capabilities spanning infra to ultrasonic ranges. Seals are amphibious hearers with middle and inner ears similar to land carnivores, while the ears of whales are strikingly different and are adapted exclusively to hearing underwater. Consistent with high sound speeds in water, specialized fats, not air-filled canals, conduct sound to the ear, and both middle and inner ears are located well outside the skull. Vestibular components are reduced, consistent with cervical fusion related to hydrodynamic body shapes; but their cochlear components, particularly the auditory fibers, are hypertrophied. Neural hypertrophy may be adaptive for high background noise, but may also be related to exceptional signal processing mechanisms in both infra and ultrasonic whales.

The Office of Naval Research Program to determine the effects of man-made sound on marine mammals

Over the past 5 years the Office of Naval Research (ONR) has maintained a coordinated interdisciplinary research program focused on the auditory capabilities of marine mammals, and the potential impacts man-made noise might have by damaging or obscuring that sensory capability. Auditory studies have included behavioral determinations of thresholds to low-frequency sound, effects of depth (pressure) on auditory function, and temporary threshold shift studies. Anatomical data, auditory-evoked potentials and otoacoustic emissions have been explored with the goal of providing larger sampling of populations and enabling sampling of the larger and rarely encountered species, such as baleen whales. The data collected thus far have further strengthened the view that marine mammal hearing represents the pinnacle of development of auditory sensing. With our own use of underwater acoustic sensing in its infancy, it would be wise to closely monitor those activities which might obscure our window into the ocean environment as well as that of its inhabitants who have led us this far.

Blast injury in humpback whale ears: Evidence and implications

To date, there is no published report of effects on marine mammal hearing from underwater explosions. External injuries consistent with inner ear damage have been found in dolphins subjected to Class C explosives, but often little change is seen in surface animal behavior near blast areas [Richardson etal., OCS MMS/90-0093 (1991)]. In this study, temporal bones from two humpback whales, which died following a 5000-kg explosion in Trinity Bay, Newfoundland [Lien etal., J. Acoust. Soc. Am. 94, 1849(A) (1993)], were harvested, preserved in formalin, scanned with 1-mm-high resolution spiral CT, decalcified, and sectioned at 20 μ. Evidence of mechanical trauma was found in all four ears: Round window rupture, ossicular chain disruption, sero-sanguinous effusion of peribullar spaces, and dissection of the middle ear mucosa with pooled sera. In one animal, there were bilateral periotic fractures. These observations are consistent with blast injury reports in humans, particularly with damage to victims near the source who sustained massive, precipitous increases in cerebrospinal fluid pressure. There was no evidence that the pathologies found in these whales resulted from repeated barotrauma or chronic infection, and no similar abnormalities were found in control ears from humpbacks not exposed to blasts. While the results show whales, like other mammals, are subject to severe blast trauma, it remains unclear whether lower level stimuli induce temporary and/or acute threshold shifts in marine mammals. [Work supported by ONR Grant. No. N00014-92-J-4000.]

Underwater audiogram of the California sea lion by the conditioned vocalization technique.

Conditioning techniques were developed demonstrating that pure tone frequencies under water can exert nearly perfect control over the underwater click vocalizations of the California sea lion (Zalophus californianus). Conditioned vocalizations proved to be a reliable way of obtaining underwater sound detection thresholds in Zalophus at 13 different frequencies, covering a frequency range of 250 to 64,000 Hz. The audiogram generated by these threshold measurements suggests that under water, the range of maximal sensitivity for Zalophus lies between one and 28 kHz with best sensitivity at 16 kHz. Between 28 and 36 kHz there is a loss in sensitivity of 60 dB/octave. However, with relatively intense acoustic signals (> 38 dB re 1 mub underwater), Zalophus will respond to frequencies at least as high as 192 kHz. These results are compared with the underwater hearing of other marine mammals.

Simple Electrostatic Transducers for High-Frequency Sounds

Using aluminized Mylar film for diaphragms and sintered stainless-steel disks for backplates, one can easily assemble electrostatic transducers that operate at ultrasonic frequencies up to 150 kHz. Loudspeakers with 0.15-mil diaphragms and 34-in. diam backplates produce airborne sound from 30 to 150 kHz at 10–20 dyn/cm2 at a distance of 30 cm. Second harmonic distortion varies from −20 to −36 dB with fundamentals from 25 to 100 kHz, and electronic predistortion can considerably reduce these figures. With compensation for the 4–6 dB/oct increase in sound output with rising frequency, these transducer response curves fluctuate by only a few decibels from 30 to 150 kHz. Loudspeakers with 1-in. backplates generate up to 80 dyn/cm2 over their range. As microphones, these transducers yield 0.7 to 1.0 mV/dyn/cm2 ± 2 dB up to 110 kHz. These transducers have been used successfully in studies of echolocation and hearing in bats and, with an additional protective diaphragm, in studies of underwater hearing in marine mammals.