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Temporary shift in masked hearing thresholds in odontocetes after exposure to single underwater impulses from a seismic watergun

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Abstract

A behavioral response paradigm was used to measure masked underwater hearing thresholds in a bottlenose dolphin (Tursiops truncatus) and a white whale (Delphinapterus leucas) before and after exposure to single underwater impulsive sounds produced from a seismic watergun. Pre- and postexposure thresholds were compared to determine if a temporary shift in masked hearing thresholds (MTTS), defined as a 6-dB or larger increase in postexposure thresholds, occurred. Hearing thresholds were measured at 0.4, 4, and 30 kHz. MTTSs of 7 and 6 dB were observed in the white whale at 0.4 and 30 kHz, respectively, approximately 2 min following exposure to single impulses with peak pressures of 160 kPa, peak-to-peak pressures of 226 dB re 1 microPa, and total energy fluxes of 186 dB re 1 microPa2 x s. Thresholds returned to within 2 dB of the preexposure value approximately 4 min after exposure. No MTTS was observed in the dolphin at the highest exposure conditions: 207 kPa peak pressure, 228 dB re 1 microPa peak-to-peak pressure, and 188 dB re 1 microPa2 x s total energy flux.
... Given the dependency of marine mammals on sound-and hence on their hearing-for underwater communication, orientation, and foraging, it is important to understand how the hearing of these animals is affected by exposure to anthropogenic noise. Several factors can affect the impact of anthropogenic noise exposure on marine mammal hearing, such as the noise's intensity (Kastak et al., 2005;Kastak et al., 2007;Kastelein et al., 2013;Kastelein et al., 2014b;Mooney et al., 2009a), spectral content (Finneran et al., 2005;Kastak et al., 1999;Kastak et al., 2005;Nachtigall et al., 2004;Popov et al., 2011;Popov et al., 2013;Popov et al., 2015), impulsiveness (Finneran et al., 2002;Finneran et al., 2003;Kastelein et al., 2016b;Kastelein et al., 2017c;Kastelein et al., 2018a;Kastelein et al., 2020f;Lucke et al., 2009;Sills et al., 2020), duty cycle (Finneran et al., 2010;Kastelein et al., 2014a;Kastelein et al., 2015a;Kastelein et al., 2016a), and duration (Kastak et al., 2005;Kastak et al., 2007;Kastelein et al., 2012b;Kastelein et al., 2012a;Kastelein et al., 2014b;Kastelein et al., 2015a;Kastelein et al., 2016b;Kastelein et al., 2017a;Mooney et al., 2009a;Popov et al., 2011). Anthropogenic noise can affect hearing by means of a temporary increase in the hearing threshold [temporary hearing threshold shift (TTS)] as a result of reversible damage to hair cell stereocilia or synapses (Kurabi et al., 2017). ...
... Most studies on the susceptibility of marine mammals to TTS investigate the effect of specific fatiguing sounds (sounds intended to cause hearing shifts) that are often complex in nature and that vary in temporal and spectral characteristics, such as sonar sweeps (Kastelein et al., 2014a;Kastelein et al., 2017a;Mooney et al., 2009b), pile driving sounds (Kastelein et al., 2016b;Kastelein et al., 2018a), or seismic airgun sounds (Finneran et al., 2002;Finneran et al., 2015;Lucke et al., 2009;Kastelein et al., 2017c). Fatiguing sounds are often quantified as a function of sound exposure level (SEL), which is a composite metric that takes both the duration of the sound and the sound pressure level (SPL) into account; it is especially useful if the data fit the equalenergy hypothesis, which states that equal SELs result in equal TTSs. ...
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When they are exposed to loud fatiguing sounds in the oceans, marine mammals are susceptible to hearing damage in the form of temporary hearing threshold shifts (TTSs) or permanent hearing threshold shifts. We compared the level-dependent and frequency-dependent susceptibility to TTSs in harbor seals and harbor porpoises, species with different hearing sensitivities in the low- and high-frequency regions. Both species were exposed to 100% duty cycle one-sixth-octave noise bands at frequencies that covered their entire hearing range. In the case of the 6.5 kHz exposure for the harbor seals, a pure tone (continuous wave) was used. TTS was quantified as a function of sound pressure level (SPL) half an octave above the center frequency of the fatiguing sound. The species have different audiograms, but their frequency-specific susceptibility to TTS was more similar. The hearing frequency range in which both species were most susceptible to TTS was 22.5–50 kHz. Furthermore, the frequency ranges were characterized by having similar critical levels (defined as the SPL of the fatiguing sound above which the magnitude of TTS induced as a function of SPL increases more strongly). This standardized between-species comparison indicates that the audiogram is not a good predictor of frequency-dependent susceptibility to TTS.
... 6 dB. Finneran et al. (2002) reported behaviorally measured TTSs of 6 and 7 dB in a beluga (Delphinapterus leucas) exposed to single impulses from a seismic water gun. Lucke et al. (2009) reported AEP-measured TTS from 7 to 20 dB in a harbor porpoise (Phocoena phocoena) exposed to single impulses from a seismic air gun. ...
... Nearly all exposures in this study induced low to moderate amounts (< 20 dB) of TTS in all the subjects, although TTS magnitudes were often greater than those in previous marine mammal studies that used broadband impulsive sources with primarily low-frequency characteristics (Finneran et al., 2002;Lucke et al., 2009;Sills et al., 2020). An exception was the single exposure (11 May 2021) in OLY that resulted in 29-and 35-dB TSs at 8 and 11.3 kHz, respectively (previous studies have also found that the largest shift occurs one half-octave above the exposure frequency for TTS greater than approximately 10 dB, see Kastelein et al., 2014b andKastelein et al., 2019). ...
Article
Studies of marine mammal temporary threshold shift (TTS) from impulsive sources have typically produced small TTS magnitudes, likely due to much of the energy in tested sources lying below the subjects' range of best hearing. In this study of dolphin TTS, 10-ms impulses centered at 8 kHz were used with the goal of inducing larger magnitudes of TTS and assessing the time course of hearing recovery. Most impulses had sound pressure levels of 175-180 dB re 1 μPa, while inter-pulse interval (IPI) and total number of impulses were varied. Dolphin TTS increased with increasing cumulative sound exposure level (SEL) and there was no apparent effect of IPI for exposures with equal SEL. The lowest TTS onset was 184 dB re 1 μPa2s, although early exposures with 20-s IPI and cumulative SEL of 182-183 dB re 1 μPa2s produced respective TTS of 35 and 16 dB in two dolphins. Continued testing with higher SELs up to 191 dB re 1 μPa2s in one of those dolphins, however, failed to result in TTS greater than 14 dB. Recovery rates were similar to those from other studies with non-impulsive sources and depended on the magnitude of the initial TTS.
... However little data exists for the potential effects of bubble curtain and other methods to reduce the effect of these noise sources. In particular studies have shown that the low frequency hearing responses of species such as the harbour porpoise [7,8] can overlap with the contribution from both piling and airgun transmissions and mitigation methods are highly relevant to ongoing and future offshore operations ...
... The Arctic has warmed at rates more than three times the global mean, and sea ice extent at its September minimum has declined by more than 12% per decade (relative to 1981IPCC, 2022;Onarheim et al., 2018;Rantanen et al., 2022). Greater accessibility in Arctic waters has spurred increased human activities, such as commercial shipping and oil and gas exploration, that have heightened underwater noise levels and the risk of acoustic disturbance (e.g., behavioral changes, masking, or hearing damage) to marine mammals (Erbe et al., 2016;Finneran et al., 2002;Halliday et al., 2020;Southall et al., 2021). Studies using passive acoustics effectively track changes to natural and anthropogenic sounds, but they require knowledge of unique properties of specific sounds to accurately identify them in recordings. ...
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Passive acoustic monitoring has been an effective tool to study cetaceans in remote regions of the Arctic. Here, we advance methods to acoustically identify the only two Arctic toothed whales, the beluga (Delphinapterus leucas) and narwhal (Monodon monoceros), using echolocation clicks. Long-term acoustic recordings collected from moorings in Northwest Greenland were analyzed. Beluga and narwhal echolocation signals were distinguishable using spectrograms where beluga clicks had most energy >30 kHz and narwhal clicks had a sharp lower frequency limit near 20 kHz. Changes in one-third octave levels (TOL) between two pairs of one-third octave bands were compared from over one million click spectra. Narwhal clicks had a steep increase between the 16 and 25 kHz TOL bands that was absent in beluga click spectra. Conversely, beluga clicks had a steep increase between the 25 and 40 kHz TOL bands that was absent in narwhal click spectra. Random Forest classification models built using the 16 to 25 kHz and 25 to 40 kHz TOL ratios accurately predicted the species identity of 100% of acoustic events. Our findings support the use of echolocation TOL ratios in future automated click classifiers for acoustic monitoring of Arctic toothed whales and potentially for other odon-tocete species.
... The results from this study and similar studies (Johnson, 1968;Kastelein et al., 2010a) indicate that marine mammals are less sensitive to signals with duration less than the auditory integration time. When auditory weighting functions are applied to relatively shortduration signals, the weighting function may overestimate perceived loudness and thus, overestimate detection ranges associated with communication space models (Jensen et al., 2012;McKenna et al., 2009), behavioral response thresholds (Southall et al., 2021), levels related to TTS and PTS onset (Finneran et al., 2002;Hamernik et al., 2002), and sound isopleths used to mitigate these effects (Aerts and Streever, 2016). One solution has been to combine auditory weighting functions with weighting in the time domain (Tougaard and Beedholm, 2019). ...
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A psychophysical procedure was used to measure pure-tone detection thresholds for a killer whale (Orcinus orca) as a function of both signal frequency and signal duration. Frequencies ranged between 1 and 100 kHz and signal durations ranged from 50 μs to 2 s, depending on the frequency. Detection thresholds decreased with an increase in signal duration up to a critical duration, which represents the auditory integration time. Integration times ranged from 4 ms at 100 kHz and increased up to 241 ms at 1 kHz. The killer whale data are similar to other odontocete species that have participated in similar experiments. The results have implications for noise impact predictions for signals with durations less than the auditory integration time.
... Behavioral hearing test methods were similar to those used during previous TTS studies in San Diego Bay Finneran et al., 2002;Finneran et al., 2015). Behavioral hearing tests with each dolphin were conducted over 2-3 min time intervals. ...
Article
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This paper aims to review and evaluate published literature on the impact of anthropogenic sound on marine mammals. A systematic method was utilized to access research works of literature on "Impact of Anthropogenic Sound on Marine Mammals". A total of seventy-seven (77) research papers published between the years 1959 to 2022 were accumulated and used for this review. A subjective approach was used to select the topics: impact of anthropogenic sound and marine mammals. In this paper, six (6) detrimental impacts of anthropogenic sound on marine mammals were evaluated and presented. Anthropogenic sounds originate from a variety of sources such as explosions, commercial shipping, seismic exploration, sonar, research sound source, acoustic deterrent devices and pingers, polar icebreakers, industrial activities, offshore drilling, construction, small ships, boats, and personal watercraft. Among the main impacts identified were that anthropogenic sounds affect marine mammals by causing hearing loss, masking, change in behavior, habituation shift and mass stranding. A mini checklist of several species of marine mammals and different types of anthropogenic noise that affect them are presented. Marine mammals are capable of self-generating their own sounds and they are also affected by anthropogenic sounds that are not native to their natural environments. The published literature that was reviewed established that the global marine mammal population dynamics, abundance, distribution, navigation, ecology and behavior are all affected by anthropogenic sounds. This review highlights the fact that more extensive studies on the impact of anthropogenic sound on marine mammals should be done in neotropical countries since there are gaps of such information on research and published data in these biodiversity-rich regions.
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Temporary threshold shifts can be short‐lived in the bottlenosed dolphin and therefore difficult to measure with conventional trained behavioral psychophysical techniques. The time course of recovery from temporary threshold shifts was measured using evoked auditory potentials collected from a bottlenosed dolphin trained to wear rubber suction cups containing human EEG skin surface electrodes. During each session, following an initial measure of hearing thresholds using the evoked auditory potential procedure, the animal voluntarily positioned within a hoop 1 m underwater while 160 dB re 1 micropascal noise between 4 and 11 kHz was presented for 30 min. Immediately following the noise exposure, evoked thresholds were again obtained. The dolphin swam down into a second hoop located one meter in front of a calibrated hydrophone. Evoked potential thresholds were obtained 5, 10, 15, 25, 45, and 105 min following the exposure for amplitude modulated pure tones of 8, 11.2, 16, 22.5, and 32 kHz. Maximum shifts occurred 5 min following exposure and rapidly recovered. As has been observed with other animals and humans, threshold shifts depended on frequency. Shifts occurred at 8, 11.2, and 16 kHz but no shifts were detected at 22.5 and 32 kHz.
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The results of a series of studies, using normal ears, on the effects of broad-band noise (a noise having equal energy in all octave bands from 75 to 10 000 cps), can be summarized in two equations. The growth of temporary threshold shift (TTS) at 4 kc is given by TTS2 = 1.06R(S − 85)[log10(T/1.7)], where TTS2 is the TTS in db 2 min after cessation of a T-minute exposure to a noise having a sound pressure level (SPL) of S db; R is the fraction of the time that the noise is on. This equation holds for T>5 min, 85<S<110 db (perhaps higher), and all values of R provided that the noise bursts are 250 msec to 1 min long. The recovery from 2-hour exposures is described by TTSt = TTS2[1−0.37 log10(t/2)], where TTSt is the TTS remaining after t minutes of recovery. This equation holds when t is 2 min or more, and when TTS2 does not exceed 50 db. Thus the relation between intensity and duration for constant TTS at 4 kc is much more complicated than predicted by the equation IT = K of classical psychophysics, or the I12T = k recently suggested, although both are approximately true in particular regions. Furthermore, it is evident that a noise on only part of the time is much less dangerous than one on continuously.
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Captive schools of Blueback Herring ( Alosa aestivalis) were subjected to 1‐h long treatments of short 118‐kHz sounds applied from a piezoelectric transducer submerged outside a vinylized canvas pen that was suspended in Richard B. Russell Reservoir on the Savannah River. In the experiments reported here, the effect on herring distrbution of 3.8‐ms long bursts at 13 repetitions/s (5% duty cycle) was compared to the effect of both another 118‐kHz sound treatment (with a different duty cycle but the same source level) and a sound‐off treatment. Each experiment compared herring distributions in the pen with the three treatments applied in a cross‐over design. The experiments lasted six days each with six 1‐h treatments per day. All of the several combinations of pulse duration and repetition rate contained the herring near the end of the pen farthest from the sound source but hour‐long continuous wave treatments produced only a brief startle response at stimulus onset. [Work supported by U.S. Army Engineer District, Savannah of the U.S. Army Corps of Engineers.]
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Temporary threshold shift in hearing at 7.5 kHz was studied with an Atlantic bottlenose dolphin. Immediately following a threshold measurement, the animal was required to station in a hoop and be exposed to an octave band of continuous noise from 5 to 10 kHz. Noise exposure sessions lasted about 50 min, with the requirement that the animal spend a total of 30 min in the hoop. The dolphin also had two preferred locations both about a meter to the side of the hoop, one at the surface, and the other at the hoop depth. The noise levels at the hoop and to the side were about the same but with different spectra. The noise at the surface was about 3‐dB lower. After exposure to the fatiguing stimulus, the animal’s hearing sensitivity was immediately measured. The animal’s hearing was not affected when the noise was 171 dB at 1 μPa with a total energy flux density of 205 dB at 1 μPa2 s. Temporary threshold shifts of 12–18 dB were obtained when the noise increased to 179 dB with an energy flux density of 213 dB or 1330 J/m2. The fatiguing stimulus was about 96 dB above the animal’s pure tone threshold of 84 dB. [Work supported by ONR.]
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Masking noise is often used in hearing tests to create a floor effect in the presence of ambient noise or to examine specific features of the auditory system (e.g., the critical bandwidth). One of the chief requirements of the masking noise is that it possess a flat frequency spectrum within some user?defined bandwidth. Generation of suitable masking noise is complicated by the frequency response of the sound projector, which may possess a frequency?dependent transmitting sensitivity and/or exhibit resonances within the desired frequency range. At low frequencies acoustic standing waves may also alter the noise frequency spectrum. To overcome these limitations, a technique has been developed to generate bandlimited noise whose frequency content is compensated in order to flatten peaks or valleys in the measured frequency spectrum. Compensation is performed by passing white noise through a digital filter whose coefficients are determined from previous measurements of the acoustic system frequency response. The system has been implemented using a personal computer with commercial hardware and custom software. The method has been used to quickly generate bandlimited Gaussian and uniform white noise for studies of masked underwater hearing thresholds in marine mammals. [Work supported by ONR and the NRC Research Associateship Program.]