Jillian M. Sills

Comparative assessment of amphibious hearing in pinnipeds

Auditory sensitivity in pinnipeds is influenced by the need to balance efficient sound detection in two vastly different physical environments. Previous comparisons between aerial and underwater hearing capabilities have considered media-dependent differences relative to auditory anatomy, acoustic communication, ecology, and amphibious life history. New data for several species, including recently published audiograms and previously unreported measurements obtained in quiet conditions, necessitate a re-evaluation of amphibious hearing in pinnipeds. Several findings related to underwater hearing are consistent with earlier assessments, including an expanded frequency range of best hearing in true seals that spans at least six octaves. The most notable new results indicate markedly better aerial sensitivity in two seals (Phoca vitulina and Mirounga angustirostris) and one sea lion (Zalophus californianus), likely attributable to improved ambient noise control in test enclosures. An updated comparative analysis alters conventional views and demonstrates that these amphibious pinnipeds have not necessarily sacrificed aerial hearing capabilities in favor of enhanced underwater sound reception. Despite possessing underwater hearing that is nearly as sensitive as fully aquatic cetaceans and sirenians, many seals and sea lions have retained acute aerial hearing capabilities rivaling those of terrestrial carnivores.

Amphibious hearing in spotted seals (Phoca largha): underwater audiograms, aerial audiograms and critical ratio measurements

Spotted seals (Phoca largha) inhabit Arctic regions that are facing both rapid climate change and increasing industrialization. While little is known about their sensory capabilities, available knowledge suggests that spotted seals and other ice seals use sound to obtain information from the surrounding environment. To quantitatively assess their auditory capabilities, the hearing of two young spotted seals was tested using a psychophysical paradigm. Absolute detection thresholds for tonal sounds were measured in air and under water over the frequency range of hearing, and critical ratios were determined using octave-band masking noise in both media. The behavioral audiograms show a range of best sensitivity spanning four octaves in air, from approximately 0.6 to 11 kHz. The range of sensitive hearing extends across seven octaves in water, with lowest thresholds between 0.3 and 56 kHz. Critical ratio measurements were similar in air and water and increased monotonically from 12 dB at 0.1 kHz to 30 dB at 25.6 kHz, indicating that the auditory systems of these seals are quite efficient at extracting signals from background noise. This study demonstrates that spotted seals possess sound reception capabilities different from those previously described for ice seals, and more similar to those reported for harbor seals (Phoca vitulina). The results are consistent with the amphibious lifestyle of these seals and their apparent reliance on sound. The hearing data reported herein are the first available for spotted seals and can inform best management practices for this vulnerable species in a changing Arctic.

Amphibious hearing in ringed seals (Pusa hispida): underwater audiograms, aerial audiograms and critical ratio measurements

ABSTRACT Ringed seals (Pusa hispida) are semi-aquatic marine mammals with a circumpolar Arctic distribution. In this study, we investigate the amphibious hearing capabilities of ringed seals to provide auditory profiles for this species across the full range of hearing. Using psychophysical methods with two trained ringed seals, detection thresholds for narrowband signals were measured under quiet, carefully controlled environmental conditions to generate aerial and underwater audiograms. Masked underwater thresholds were measured in the presence of octave-band noise to determine critical ratios. Results indicate that ringed seals possess hearing abilities comparable to those of spotted seals (Phoca largha) and harbor seals (Phoca vitulina), and considerably better than previously reported for ringed and harp seals. Best sensitivity was 49 dB re. 1 µPa (12.8 kHz) in water, and −12 dB re. 20 µPa (4.5 kHz) in air, rivaling the acute hearing abilities of some fully aquatic and terrestrial species in their respective media. Critical ratio measurements ranged from 14 dB at 0.1 kHz to 31 dB at 25.6 kHz, suggesting that ringed seals – like other true seals – can efficiently extract signals from background noise across a broad range of frequencies. The work described herein extends similar research on amphibious hearing in spotted seals recently published by the authors. These parallel studies enhance our knowledge of the auditory capabilities of ice-living seals, and inform effective management strategies for these and related species in a rapidly changing Arctic environment. Summary: Psychophysical experiments with trained ringed seals show acute hearing abilities in both air and water, which are comparable to those of other phocid seals and considerably better than previously reported for this species.

Low-frequency temporary threshold shift not observed in spotted or ringed seals exposed to single air gun impulsesa)

Underwater hearing thresholds were measured at 100 Hz in trained spotted (Phoca largha) and ringed seals (Pusa hispida) before and immediately following voluntary exposure to impulsive noise from a seismic air gun. Auditory responses were determined from psychoacoustic data and behavioral responses were scored from video recordings. Four successive exposure conditions of increasing level were tested, with received unweighted sound exposure levels from 165 to 181 dB re 1 μPa2 s and peak-to-peak sound pressures from 190 to 207 dB re 1 μPa. There was no evidence that these single seismic exposures altered hearing-including in the highest exposure condition, which matched previous predictions of temporary threshold shift (TTS) onset. Following training at low exposure levels, relatively mild behavioral responses were observed for higher exposure levels. This demonstrates that individuals can learn to tolerate loud, impulsive sounds, but does not necessarily imply that similar sounds would not elicit stronger behavioral responses in wild seals. The absence of observed TTS confirms that regulatory guidelines (based on M-weighting) for single impulse noise exposures are conservative for seals. However, additional studies using multiple impulses and/or higher exposure levels are needed to quantify exposure conditions that do produce measurable changes in hearing sensitivity.

Active touch in sea otters: in-air and underwater texture discrimination thresholds and behavioral strategies for paws and vibrissae

ABSTRACT Sea otters (Enhydra lutris) are marine predators that forage on a wide array of cryptic, benthic invertebrates. Observational studies and anatomical investigations of the sea otter somatosensory cortex suggest that touch is an important sense for detecting and capturing prey. Sea otters have two well-developed tactile structures: front paws and facial vibrissae. In this study, we use a two-alternative forced choice paradigm to investigate tactile sensitivity of a sea otter subjects paws and vibrissae, both in air and under water. We corroborate these measurements by testing human subjects with the same experimental paradigm. The sea otter showed good sensitivity with both tactile structures, but better paw sensitivity (Weber fraction, c=0.14) than vibrissal sensitivity (c=0.24). The sea otters sensitivity was similar in air and under water for paw (cair=0.12, cwater=0.15) and for vibrissae (cair=0.24, cwater=0.25). Relative to the human subjects we tested, the sea otter achieved similar sensitivity when using her paw and responded approximately 30-fold faster regardless of difficulty level. Relative to non-human mammalian tactile specialists, the sea otter achieved similar or better sensitivity when using either her paw or vibrissae and responded 1.5- to 15-fold faster near threshold. Our findings suggest that sea otters have sensitive, rapid tactile processing capabilities. This functional test of anatomy-based hypotheses provides a mechanistic framework to interpret adaptations and behavioral strategies used by predators to detect and capture cryptic prey in aquatic habitats. Highlighted Article: A sea otter demonstrates sensitive, rapid touch using either paw or whiskers, both in air and under water. Tactile sensitivity is comparable with that of other tactile specialists, including humans.

The influence of temporally varying noise from seismic air guns on the detection of underwater sounds by sealsa)

Standard audiometric data are often applied to predict how noise influences hearing. With regard to auditory masking, critical ratios-obtained using tonal signals and flat-spectrum maskers-can be combined with noise spectral density levels derived from 1/3-octave band levels to predict signal amplitudes required for detection. However, the efficacy of this conventional model of masking may vary based on features of the signal and noise in question. The ability of resource managers to quantify masking from intermittent seismic noise is relevant due to widespread geophysical exploration. To address this, spotted and ringed seals with previously measured critical ratios were trained to detect low-frequency tonal signals within seismic pulses recorded 1 and 30 km from an operational air gun array. The conventional model of masking accurately predicted the extent of masking only in certain cases. When noise amplitude varied significantly in time, the results suggested that detection was driven by higher signal-to-noise ratios within time windows shorter than the full signal duration. This study evaluates when it is appropriate to use average noise levels and critical ratios to predict auditory masking experienced by marine mammals, and suggests how masking models can be improved by incorporating time-based analyses of signals and noise.

Complex masking scenarios in Arctic environments

Critical ratios obtained using octave-band noise and narrowband signals provide a useful first approximation for understanding the effects of noise on hearing. When considering realistic listening scenarios, it may be necessary to examine the effects of spectrally complex, time-varying noise sources on an animal’s ability to detect relevant signals. In the case of Arctic seals, the increasing prevalence of seismic exploration makes an examination of masking by impulsive sounds particularly relevant. However, the characteristics of received sounds from airgun operations vary dramatically depending on the seismic source, environmental parameters, and distance. In order to determine the potential for auditory masking by airguns, we developed a paradigm to quantify the influence of spectral and temporal variations in typical seismic noise on signal detectability. This method calls for calculation of detection probabilities for seals listening for the same signal embedded at different time windows within a bac...

The production and reception of underwater sound in Hawaiian monk seals (Neomonachus schauinslandi)

The endangered Hawaiian monk seal is a primitive phocid (true) seal endemic to the tropical Hawaiian Islands. At present, there is a lack of substantive bioacoustic information available for this species, with no formal descriptions of underwater vocalizations and limited data concerning underwater hearing. To address these knowledge gaps, we are working to better understand species-typical auditory capabilities and sound production by thoroughly evaluating a single individual living in human care. A mature male monk seal was trained to perform an auditory go/no-go signal detection task in water. Detection thresholds were measured for narrowband tones across the frequency range of hearing to generate a full underwater audiogram. Additionally, an acoustic recorder was placed in this monk seal’s living enclosure for a full year, enabling characterization of his underwater repertoire and seasonal trends in vocal behavior. This study presents the first examination of underwater vocalizations in Hawaiian monk seals, provides insight into the perceptual abilities of this species and the evolution of underwater hearing within the phocid lineage, and enables improved assessments of noise effects on these vulnerable seals. [Work supported by Navy’s Living Marine Resources Program.]The endangered Hawaiian monk seal is a primitive phocid (true) seal endemic to the tropical Hawaiian Islands. At present, there is a lack of substantive bioacoustic information available for this species, with no formal descriptions of underwater vocalizations and limited data concerning underwater hearing. To address these knowledge gaps, we are working to better understand species-typical auditory capabilities and sound production by thoroughly evaluating a single individual living in human care. A mature male monk seal was trained to perform an auditory go/no-go signal detection task in water. Detection thresholds were measured for narrowband tones across the frequency range of hearing to generate a full underwater audiogram. Additionally, an acoustic recorder was placed in this monk seal’s living enclosure for a full year, enabling characterization of his underwater repertoire and seasonal trends in vocal behavior. This study presents the first examination of underwater vocalizations in Hawaiian monk ...

Psychophysical audiogram of a California sea lion (Zalophus californianus) listening for airborne tonal sounds in an acoustic chamber

Many species-typical audiograms for marine mammals are based on data from only one or a few individuals that are not always tested under ideal conditions. Here, we report auditory thresholds across the frequency range of hearing for a healthy, five-year-old female California sea lion identified as Ronan. Ronan was trained to enter a hemi-anechoic acoustic chamber to perform a go/no-go audiometric experiment. Auditory sensitivity was measured first by an adaptive staircase procedure and then by the method of constant stimuli. Minimum audible field measurements were obtained for 500 ms frequency-modulated tonal upsweeps with 10% bandwidth and 5% rise and fall times. Thresholds were measured at 13 frequencies: in one-octave frequency steps from 0.1 to 25.6 kHz, and additionally at 18.0, 22.0, 36.2, and 40.0 kHz. Sensitivity was greatest between ~0.9 and 23 kHz, with best hearing of 0 dB re 20 μPa at 12.8 kHz. Hearing range, determined at the 60 dB re 20 μPa level, extended from ~0.2 kHz to 38 kHz. Sensitivit...

Acoustic habitat utilized by ice-living seals: Hearing and masking in natural noise environments

Acoustic habitat is a fundamental but poorly understood resource for marine mammals, including seals. To evaluate the soundscapes experienced by seals in dynamic Arctic environments, two DSG-Ocean Acoustic Dataloggers were deployed in Kotzebue Sound, Alaska from September 2014 through September 2015, providing a full year of acoustic coverage for this region of the Chukchi Sea. The recorders were placed in an area of seasonal fast ice where spotted, ringed, and bearded seals are all found at various times of year. The data describe the acoustic conditions typically experienced by these ecologically and culturally important seal species, including variations in noise up to 48 kHz within and across scales of hours, days, months, and seasons. The noise profiles provide an ecological framework for laboratory studies of hearing with trained seals, allowing for improved understanding of their sensory biology in the context of their acoustic habitat. The integration of these noise measurements with hearing and a...