Descriptions of underwater vocalizations produced by aquatically mating phocids are available for many species, but are lacking for the endangered Hawaiian monk seal (Neomonachus schauinslandi). We obtained simultaneous year-round audio and video recordings of a captive adult male Hawaiian monk seal to evaluate underwater vocal repertoire and characterize seasonal trends in vocal behavior. A discriminant function analysis based on 17 acoustic parameters revealed that this seal produced at least six discrete underwater vocalizations. Spontaneous aquatic calls were most commonly produced from September through January, during a period coincident with elevated blood testosterone levels and prior to the annual molt. These seasonal patterns in sound production confirm a protracted reproductive season for this tropical species. While limited to a single individual, this first report of underwater sound production expands our understanding of reproductive behavior in Neomonachus schauinslandi, and establishes a foundation for future research and population monitoring efforts using passive acoustics.

Like other marine mammals, True seals (Family Phocidae) rely on acoustic cues for orientation, communication, and prey and predator detection. Because of their amphibious life histories, the auditory systems of seals must operate efficiently both in air and water—environments with very different physical characteristics. While all seals exhibit common evolutionary traits related to hearing, the extent of auditory adaptations varies between phylogenetic lineages and, in some cases, may differ among species. The functional significance of these differences remains to be resolved. The most complete dataset describing amphibious hearing in seals is for the Phocinae subfamily (most temperate and polar phocid species of the Northern Hemisphere). There are few hearing data available for seals from the Monachinae subfamily (the Southern Ocean seals, monk seals, and elephant seals). However, the limited evidence suggests potential subfamily-level differences in hearing. Additional audiometric measurements are needed within the Monachinae lineage of seals to inform our understanding of auditory adaptations from an evolutionary perspective.

The first two chapters of this dissertation aim to expand knowledge of amphibious hearing in seals—particularly from the lesser known Monachinae lineage—by utilizing classic behavioral methods with two individual Hawaiian monk seals (Neomonachus schauinslandi) conditioned to voluntarily participate in hearing trials. These efforts generated and validated the first terrestrial audiogram, provided the first auditory masking measurements, and resolved discrepancies between two prior underwater hearing profiles for monk seals. The findings suggest reduced terrestrial hearing sensitivity may be related to physiological differences in soft tissue within the peripheral auditory system among seal species, which could inhibit the reception of airborne sound. Together, the results confirm that the hearing abilities of monk seals differ from those of related species and are informative for evolutionary considerations of hearing in seals.

From an applied perspective, these hearing data suggest that terrestrial communication is limited for the species. However, a lack of data describing the amplitude of Hawaiian monk seal airborne vocalizations has precluded any communication range estimates. For Chapter 3, I describe the spectral characteristics of and provide the first source level measurements for low-frequency calls emitted by this species in air. These amplitude and spectral data are combined with hearing thresholds and representative ambient noise levels to estimate the distances over which these seals can effectively communicate with conspecifics. Findings suggest that terrestrial communication is limited by the poor hearing sensitivity and moderate vocal amplitudes of the species and is further constrained by ambient noise in the environment.

This series of audiometric measurements advances knowledge of acoustic sensitivity in an endangered species, contributes comparative information about hearing for a data-poor marine mammal lineage, and increases our understanding of the evolution of hearing in the amphibious true seals. Finally, by combining hearing data with information about sound production, we can better understand the acoustic communication system of Hawaiian monk seals, ultimately supporting conservation and management efforts for this endangered species.

The auditory biology and acoustic behavior of Arctic seals are incompletely understood, in large part due to the significant challenges of studying ice-living seals in natural habitats. Consequently, many questions regarding their perception of acoustic cues in the marine environment, and the ways in which increasing anthropogenic noise may influence their ability to detect biologically relevant sounds, remain unanswered. This dissertation describes a series of behavioral studies conducted in the laboratory to characterize the auditory capabilities of trained spotted (Phoca largha, Pallas 1811) and ringed seals (Pusa hispida, Schreber 1775) in quiet conditions, in the presence of controlled noise, and in real-world listening scenarios. The first two chapters comprise a set of three standard audiometric studies for each species, including aerial audiograms, underwater audiograms, and critical ratio measurements in both media. The results presented in Chapter 1 are the first hearing data available for spotted seals, and provide insight into the acoustic ecology of this minimally studied species. The results presented in Chapter 2 are the most comprehensive hearing data available thus far for ringed seals, and offer an updated perspective on the auditory capabilities of this species relative to historical data. Chapter 3 builds upon these standard examinations of hearing to investigate auditory performance in more complex acoustic environments—specifically, habitats altered by seismic noise from geophysical exploration. Taken together, these experiments provide fundamental knowledge about the sensory biology of spotted and ringed seals, which can be applied to management decisions for these species in an increasingly human-influenced Arctic environment.

Arctic seals live in dynamic environments characterized by seasonally changing sea ice and extremely cold temperatures. Spotted (Phoca largha), ringed (Pusa hispida), and bearded seals (Erignathus barbatus) are physiologically adapted to an amphibious lifestyle, relying primarily on sea ice as haul-out substrate but spending more than half their time submerged. Projected habitat changes emphasize the importance of in-water activities when considering the energy budgets of free-ranging seals, but estimates of activity-specific costs are not available for these species. We used open-flow respirometry to compare resting metabolic rates (RMR) with the energetic costs of submerged behaviors in five adult seals. Individuals were trained to voluntarily complete a stationary breath hold under water or a continuous submerged swim before surfacing in a metabolic dome to measure rate of oxygen consumption. Metabolic rates decreased 11- 24% relative to RMR for the spotted and ringed seals while diving for 3, 5, or 7 min, and did not change with increasing duration. The bearded seal did not show evidence of a similar dive response. All individuals exhibited notably increased costs to support exercise while swimming for 2-3 min. These elevations were 243% and 114% above resting costs for spotted and ringed seals, and only 60% for the bearded seal. These results highlight the unique physiological responses of the bearded seal, and help to explain how seals resolve conflicting pressures of metabolic suppression during diving and the oxygen requirements of exercise. The costs of submerged activity can now be considered in quantitative models of ice seal energy budgets to inform how species differences will influence tolerance to the rapidly changing Arctic.

Increasing levels of anthropogenic noise in the world’s oceans are a matter of concern for the conservation of pinnipeds (seals, sea lions, and walruses). Sound from noise-generating human activities—such as marine construction, oil exploration, and shipping traffic—may alter the lives of pinnipeds in a variety of ways. For example, anthropogenic noise can interfere with an individual’s ability to detect calls from conspecifics or the sound of an approaching predator; and loud, aversive sounds can cause animals to abandon preferred habitats. Laboratory studies of hearing in pinnipeds over the past 50 years have expanded knowledge of the basic auditory capabilities of certain species, and data from these studies are currently being used to predict how specific noise-generating activities may affect wild animals. However, predicting the effects of anthropogenic noise is a complex process, and certain knowledge gaps must be addressed before accurate predictions can be made. First, it is unclear how well standard hearing data—which are generated using simple, synthetic sounds—can predict pinniped auditory sensitivity to spectrally and temporally complex anthropogenic sounds. Second, hearing sensitivity data above 80 kHz are scarce for most species, which is problematic given the recent proliferation of high-frequency, high-energy acoustic marine technologies such as commercial sonar and recreational fish finders. The research described in this dissertation addresses these two knowledge gaps using behavioral hearing experiments with trained pinniped subjects combined with mathematical models of hearing and sound propagation.

The data presented here improve the ability of regulators to predict the effects of anthropogenic noise on pinnipeds and indicate future research directions. The reported sensitivity data for complex sounds show that certain spectral and temporal features can significantly alter detectability. Comparison of detection thresholds for complex stimuli to predictions from hearing models based on standard hearing metrics showed differences of up to 8 dB in both quiet and noisy conditions. Such discrepancies indicate the need for future research into how complex features influence the detectability of underwater sound. High-frequency sensitivity data for two seals and one sea lion show that these animals can detect underwater sound at frequencies well above their traditional high-frequency hearing limits, with all three subjects able to detect tonal signals centered at 180 kHz. The shapes of the sensitivity profiles for all subjects indicate that the idea of a traditional high-frequency hearing limit is problematic for underwater pinniped listeners, a fact that regulators must take into account.

Marine mammals rely on oxygen stored in blood, muscle, and lungs to support breath-hold diving and foraging at sea. Here, we used biomedical imaging to examine lung oxygen stores and other key respiratory parameters in living ringed seals (Pusa hispida). Three-dimensional models created from CT images were used to quantify total lung capacity (TLC), respiratory dead space, minimum air volume, and total body volume to improve assessments of lung oxygen storage capacity, scaling relationships, and buoyant force estimates. Results suggest that lung oxygen stores determined in vivo are smaller than those derived from typical postmortem measurements. We also demonstrate that—while established allometric relationships hold well for most pinnipeds—these relationships consistently overestimate TLC for the smallest phocid seal. Finally, measures of total body volume reveal differences in calculated body density and net buoyant force that would influence costs associated with diving and foraging in free-ranging seals.

Despite its importance within marine habitats, most of what we know about auditory masking is based on terrestrial species and theoretical assumptions about signal processing in animals. To fill data gaps and improve models that predict active listening space for marine mammals, I have measured hearing thresholds for tonal sounds with highly trained sea lions, walruses, and seals in the presence of precisely and experimentally varied background noise conditions. My aim is to provide empirical measurements of frequency-dependent masking parameters to inform a quantitative understanding of the acoustic scenarios encountered by free-ranging individuals. Three frequency-dependent aspects of masking are considered: critical ratios, critical bandwidths, and masker level effects. Critical ratios (CR), or the signal-to-noise ratios required for auditory detection of pure tones embedded in controlled, spectrally-flat noise, were measured for sea lion and walrus subjects across a frequency span from 0.2 to 16 kHz. Despite differences in hearing sensitivity, these masking metrics were similar for the subjects and followed expected frequency-dependent trends observed in terrestrial carnivores. When compared to published data for seals, sea lion and walrus CRs were generally higher, indicating that, among these marine Carnivores, seals are especially adapted for hearing in noise. To evaluate how the spectral content of noise contributes to masking, I determined the frequency bandwidth of noise that interferes with the detection of a given tonal signal, the ‘critical bandwidth’ (CBW). I conducted hearing measurements with three subjects–a sea lion, walrus, and seal–while varying the frequency content of surrounding noise. The study subjects showed an expected increase in absolute CBW with increasing frequency. While data for the sea lion and walrus were similar, the seal exhibited narrower CBWs that increased as a constant percentage of center frequency, further suggesting additional specialization for hearing in noise for this group. Finally, to explore how noise level contributes to masking, I conducted a series of tone detection measurements with one California sea lion in a highly controlled acoustic environment. Across experimental trials, I gradually increased the amplitude of surrounding noise from a level of no effect to capture masking onset. The data revealed a frequency-and bandwidth-dependent transition zone that occurs before complete masking is evident. The reported masking parameters provide insight into how some marine mammals hear within noisy conditions. These data, obtained using behavioral, psychoacoustic methods, can be applied to estimate masking effects for amphibious marine carnivores listening in air or water. Further, because they extend to lower frequencies where noise tends to be high and few hearing data are available, these results have clear and actionable outcomes and implications for real-world scenarios and conservation. The findings identify the frequencies where these species are most vulnerable to noise, highlight differences in auditory biology among pinniped lineages, and enable improved predictions of the extent of masking in marine environments dominated by natural and anthropogenic noise.