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Comparative assessment of amphibious hearing in pinnipeds

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Abstract

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.

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Acknowledgments

This work was conducted over a period of many years and was supported by the contributions of several individuals. It is important for us to acknowledge that Dr. David Kastak conceived, planned, and conducted much of this research. His long-standing interest in the trade-offs between aerial and underwater hearing in marine mammals stimulated countless discussions, careful experiments, and thoughtful revisions of earlier ideas. Dr. Ronald Schusterman encouraged us during this research and reminded us of the value of viewing science as a self-correcting process. Drs. Bertel Møhl, Jack Terhune, and Patrick Moore influenced this research by sharing their perspectives during early phases of data collection. This research would not have been possible without the participation of many members of our research program at Long Marine Laboratory, especially Amy Bernard, Asila Ghoul, Andrew Rouse, and Brendan Wakefield, and we thank the entire team for their hard work and partnership. Support for this research was provided by the Office of Naval Research through awards N00014-99-1-0164, B00014-02-1-0159, N00014-04-1-0248, and N00014-06-1-0295 and DURIP through award N00014-99-1-0686. This manuscript was improved by the helpful comments of JCP-A Editor Dr. Wolf Hanke and two anonymous reviewers.

Ethical standards

Animal welfare considerations were consistent with the current laws of the United States. Federal authorization for marine mammal research was granted by the National Marine Fisheries Service under scientific research permits 887, 259-1481, 1072-1771, and 14535 to RJ Schusterman and C Reichmuth. The animal protocols associated with this research were reviewed and approved by the US Department of Defense and by the Institutional Animal Care and Use Committee at the University of California Santa Cruz.

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Authors and Affiliations

  1. Long Marine Laboratory, Institute of Marine Sciences, University of California Santa Cruz, Santa Cruz, CA, 95060, USA

    Colleen Reichmuth & Brandon L. Southall

  2. Conservation Biology Division, Northwest Fisheries Science Center, National Marine Fisheries Service, National Oceanic and Atmospheric Administration, 2725 Montlake Blvd. East, Seattle, WA, 98112, USA

    Marla M. Holt

  3. National Marine Mammal Foundation, 2240 Shelter Island Drive, # 200, San Diego, CA, 92106, USA

    Jason Mulsow

  4. Long Marine Laboratory, Department of Ocean Sciences, University of California Santa Cruz, 100 Shaffer Road, Santa Cruz, CA, 95060, USA

    Jillian M. Sills

  5. SEA Inc., 9099 Soquel Drive, Suite 8, Aptos, CA, 95003, USA

    Brandon L. Southall

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  1. Colleen Reichmuth
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  2. Marla M. Holt
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  3. Jason Mulsow
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  4. Jillian M. Sills
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Correspondence to Colleen Reichmuth.

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Submitted to the Journal of Comparative Physiology A: Special Issue on the Sensory Biology of Aquatic Mammals.

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Procedural depiction of an experimental session for the aerial audiogram. Several signal-present trials and control (blank) trials are shown for the harbor seal subject tested in the hemi-anechoic chamber. Signals are 500 ms pure tones with frequency of 400 Hz (MPG 58692 kb)

Procedural depiction of an experimental session for the underwater audiogram. Several signal-present trials and control (blank) trials are shown for the sea lion subject tested in the pool. Signals are 500 ms narrow-band, FM sweeps centered at 800 Hz (MPG 62250 kb)

359_2013_813_MOESM3_ESM.pdf

The psychometric functions associated with aerial auditory thresholds for the harbor seal subject (Sprouts) at each test frequency. The X-axis of each plot shows the sound pressure level in dB re 20 μPa. The Y-axis shows the percent correct detection on signal-present trials during MCS testing. Probit analysis was used to fit the psychometric function to the observed proportion of correct detections at each stimulus level. An inverse prediction (not shown) was then used to determine the threshold, defined as the 50 % correct detection probability (depicted by the dotted lines) (PDF 132 kb)

359_2013_813_MOESM4_ESM.pdf

The psychometric functions associated with aerial auditory thresholds for the northern elephant seal subject (Burnyce) at each test frequency. The X-axis of each plot shows the sound pressure level in dB re 20 μPa. The Y-axis shows the percent correct detection on signal-present trials during MCS testing. Probit analysis was used to fit the psychometric function to the observed proportion of correct detections at each stimulus level. An inverse prediction (not shown) was then used to determine the threshold, defined as the 50 % correct detection probability (depicted by the dotted lines) (PDF 135 kb)

359_2013_813_MOESM5_ESM.pdf

The psychometric functions associated with aerial auditory thresholds for the California sea lion subject (Rio) at each test frequency. The X-axis of each plot shows the sound pressure level in dB re 20 μPa. The Y-axis shows the percent correct detection on signal-present trials during MCS testing. Probit analysis was used to fit the psychometric function to the observed proportion of correct detections at each stimulus level. An inverse prediction (not shown) was then used to determine the threshold, defined as the 50 % correct detection probability (depicted by the dotted lines) (PDF 137 kb)

359_2013_813_MOESM6_ESM.pdf

The psychometric functions associated with underwater auditory thresholds for the harbor seal subject (Sprouts) at each test frequency. The X-axis of each plot shows the sound pressure level in dB re 1 μPa. The Y-axis shows the percent correct detection on signal-present trials during MCS testing. Probit analysis was used to fit the psychometric function to the observed proportion of correct detections at each stimulus level. An inverse prediction (not shown) was then used to determine the threshold, defined as the 50 % correct detection probability (depicted by the dotted lines) (PDF 85 kb)

359_2013_813_MOESM7_ESM.pdf

The psychometric functions associated with underwater auditory thresholds for the California sea lion subject (Ronan) at each test frequency. The X-axis of each plot shows the sound pressure level in dB re 1 μPa. The Y-axis shows the percent correct detection on signal-present trials during MCS testing. Probit analysis was used to fit the psychometric function to the observed proportion of correct detections at each stimulus level. An inverse prediction (not shown) was then used to determine the threshold, defined as the 50 % correct detection probability (depicted by the dotted lines) (PDF 128 kb)

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Reichmuth, C., Holt, M.M., Mulsow, J. et al. Comparative assessment of amphibious hearing in pinnipeds. J Comp Physiol A 199, 491–507 (2013). https://doi.org/10.1007/s00359-013-0813-y

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