Vocal tract dynamics shape the formant structure of conditioned vocalizations in a harbor seal.

Formants, or resonance frequencies of the upper vocal tract, are an essential part of acoustic communication. Articulatory gestures-such as jaw, tongue, lip, and soft palate movements-shape formant structure in human vocalizations, but little is known about how nonhuman mammals use those gestures to modify formant frequencies. Here, we report a case study with an adult male harbor seal trained to produce an arbitrary vocalization composed of multiple repetitions of the sound wa. We analyzed jaw movements frame-by-frame and matched them to the tracked formant modulation in the corresponding vocalizations. We found that the jaw opening angle was strongly correlated with the first (F1) and, to a lesser degree, with the second formant (F2). F2 variation was better explained by the jaw angle opening when the seal was lying on his back rather than on the belly, which might derive from soft tissue displacement due to gravity. These results show that harbor seals share some common articulatory traits with humans, where the F1 depends more on the jaw position than F2. We propose further in vivo investigations of seals to further test the role of the tongue on formant modulation in mammalian sound production.

An Ecological and Neural Argument for Developing Pursuit-Based Cognitive Enrichment for Sea Lions in Human Care.

While general enrichment strategies for captive animals attempt to elicit variable and species-typical behaviors, approaches to cognitive enrichment have been disappointingly one-size-fits-all. In this commentary, we address the potential benefit of tailoring cognitive enrichment to the "cognitive niche" of the species, with a particular focus on a reasonably well-studied marine carnivore, the sea lion. Sea lions likely share some cognitive evolutionary pressures with primates, including complex social behavior. Their foraging ecology, however, like that of many terrestrial carnivores, is based on the rapid and behaviorally flexible pursuit of avoidant prey. Unlike terrestrial carnivores, sea lions carry out this pursuit in a truly fluid three-dimensional field, computing and executing sensorimotor transformations from any solid angle to any other. The cognitive demands of flexible prey pursuit are unlikely to be fully elicited by typical stationary puzzle box style foraging enrichment devices or screen-based interactive games. With this species, we recommend exploring more water-based movement activities generally, and complex pursuit challenges specifically.

Auditory masking in odobenid and otariid carnivoresa).

As the only living species within the odobenid lineage of carnivores, walruses (Odobenus rosmarus) have no close relatives from which auditory information can be extrapolated. Sea lions and fur seals in the otariid lineage are the nearest evolutionary outgroup. To advance understanding of odobenid and otariid hearing, we conducted behavioral testing with two walruses and one California sea lion (Zalophus californianus). Detection thresholds for airborne sounds were measured from 0.08 to at least 16 kHz in ambient noise conditions and then re-measured in the presence of octave-band white masking noise. Walruses were more sensitive than the sea lion at lower frequencies and less sensitive at higher frequencies. Critical ratios for the walruses ranged from 20 dB at 0.2 kHz to 32 dB at 10 kHz, while critical ratios for the sea lion ranged from 16 dB at 0.2 kHz to 35 dB at 32 kHz. The masking values for these species are comparable to one another and to those of terrestrial carnivores, increasing by about 3 dB per octave with increasing frequency. Despite apparent differences in hearing range and sensitivity, odobenids and otariids have a similar ability to hear signals in noisy conditions.

Maintaining control: metabolism of molting Arctic seals in water and when hauled out.

Seals haul out of water for extended periods during the annual molt, when they shed and regrow their pelage. This behavior is believed to limit heat loss to the environment given increased peripheral blood flow to support tissue regeneration. The degree to which time in water, particularly during the molt, may affect thermoregulatory costs is poorly understood. We measured the resting metabolism of three spotted seals (Phoca largha), one ringed seal (Pusa hispida) and one bearded seal (Erignathus barbatus) during and outside the molting period, while resting in water and when hauled out. Metabolic rates were elevated in spotted and ringed seals during molt, but comparable in water and air for individuals of all species, regardless of molt status. Our data indicate that elevated metabolism during molt primarily reflects the cost of tissue regeneration, while increased haul out behavior is driven by the need to maintain elevated skin temperatures to support tissue regeneration.

Anatomy of the sense of touch in sea otters: Cutaneous mechanoreceptors and structural features of glabrous skin.

Sea otters (Enhydra lutris) demonstrate rapid, accurate tactile abilities using their paws and facial vibrissae. Anatomical investigations of neural organization in the vibrissal bed and somatosensory cortex coincide with measured sensitivity, but no studies describe sensory receptors in the paws or other regions of glabrous (i.e., hairless) skin. In this study, we use histology to assess the presence, density, and distribution of mechanoreceptors in the glabrous skin of sea otters: paws, rhinarium, lips, and flipper digits, and we use scanning electron microscopy to describe skin-surface texture and its potential effect on the transduction of mechanical stimuli. Our results confirm the presence of Merkel cells and Pacinian corpuscles, but not Meissner corpuscles, in all sea otter glabrous skin. The paws showed the highest density of Merkel cells and Pacinian corpuscles. Within the paw, relative densities of mechanoreceptor types were highest in the distal metacarpal pad and digits, which suggests that the distal paw is a tactile fovea for sea otters. In addition to the highest receptor density, the paw displayed the thickest epidermis. Rete ridges (epidermal projections into the dermis) and dermal papillae (dermal projections into the epidermis) were developed across all glabrous skin. These quantitative and qualitative descriptions of neural organization and physical features, combined with previous behavioral results, contribute to our understanding of how structure relates to function in the tactile modality. Our findings coincide with behavioral observations of sea otters, which use touch to maintain thermoregulatory integrity of their fur, explore objects, and capture visually cryptic prey.

In-situ observations of the sensory hairs of Antarctic minke whales (Balaenoptera bonaerensis).

The sense of touch in the largest marine mammals is poorly understood. While mysticetes possess specialized sensory hairs that are present through adulthood, descriptions of these structures are based almost entirely on examination of tissues in post-mortem individuals. Sensory hairs have rarely been observed and described in living whales. We photographed Antarctic minke whales Balaenoptera bonaerensis in the Western Antarctic Peninsula and used high-resolution images to describe the number, distribution, orientation, and relative size of sensory hairs in freely swimming individuals. Sensory hairs were well developed. They were distributed on the tip of the lower jaw, the margins of the upper and lower jaw, and near the blowhole. Far fewer hairs were observed than reported for other mysticete species, including the related species Balaenoptera acutorostrata. Placement and apparent stiffness of sensory hairs within living tissue combined with observations and images of moving whales suggest these structures aid in detecting air and ice interfaces, and possibly, the boundaries of submerged prey fields.

Maternal responses to pup calls in a high-cost lactation species.

Bonding between mothers and their young is fundamental to mammalian reproductive behaviour and individual fitness. In social systems where the risk of confusing filial and non-filial offspring is high, mothers should demonstrate early, strong and consistent responses to their kin throughout the period of offspring dependence, irrespective of maternal traits. We tested this hypothesis through playback experiments in the northern elephant seal Mirounga angustirostris, a phocid species that breeds in high-density colonies. We found that mothers recognized their offspring throughout lactation and as early as 1-2 days after parturition. Measures of experience (age) and temperament (aggressivity) did not predict their response strength to filial playback treatments, nor did pup age or sex. Some mothers showed great consistency in behavioural responses throughout the lactation period, while others were less predictable. The strength of a female's response did not influence her pup's weaning weight; however, more consistent females weaned pups of higher mass. This is a rare demonstration of individual recognition among phocid mothers and their offspring, and suggests that consistency in maternal responsiveness may be an important social factor influencing the pup's growth and survival.

Walruses produce intense impulse sounds by clap-induced cavitation during breeding displays.

Male walruses produce some of the longest continuous reproductive displays known among mammals to convey their physical fitness to potential rivals and possibly to potential mates. Here, we document the ability of a captive walrus to produce intense, rhythmic sounds through a non-vocal pathway involving deliberate, regular collision of the fore flippers. High-speed videography linked to an acoustic onset marker revealed sound production through cavitation, with the acoustic impulse generated by each forceful clap exceeding a peak-to-peak sound level of 200 dB re. 1 µPa. This clapping display is in some ways quite similar to the knocking display more commonly associated with walruses in rut but is produced through a very different mechanism and with much higher amplitudes. While this clapping behaviour has not yet been documented in wild individuals, it has been observed among other mature male walruses living in human care. Production of intense sounds through cavitation has previously been documented only in crustaceans but may also be an effective means of sound production for some aquatic mammals.

In-air hearing in Hawaiian monk seals: implications for understanding the auditory biology of Monachinae seals.

The auditory biology of Monachinae seals is poorly understood. Limited audiometric data and certain anatomical features suggest that these seals may have reduced sensitivity to airborne sounds compared to related species. Here, we describe the in-air hearing abilities of a Hawaiian monk seal (Neomonachus schauinslandi) trained to participate in a psychophysical paradigm. We report absolute (unmasked) thresholds for narrowband signals measured in quiet conditions across the range of hearing and masked thresholds measured in the presence of octave-band noise at two frequencies. The behavioral audiogram indicates a functional hearing range from 0.1 to 33 kHz and poor sensitivity, with detection thresholds above 40 dB re 20 µPa. Critical ratio measurements are elevated compared to those of other seals. The apparently reduced terrestrial hearing ability of this individual-considered with available auditory data for a northern elephant seal (Mirounga angustirostris)-suggests that hearing in Monachinae seals differs from that of the highly sensitive Phocinae seals. Exploration of phylogenetic relationships and anatomical traits support this claim. This work advances understanding of the evolution of hearing in amphibious marine mammals and provides updated information that can be used for management and conservation of endangered Hawaiian monk seals.

Molting strategies of Arctic seals drive annual patterns in metabolism.

Arctic seals, including spotted (Phoca largha), ringed (Pusa hispida) and bearded (Erignathus barbatus) seals, are directly affected by sea ice loss. These species use sea ice as a haul-out substrate for various critical functions, including their annual molt. Continued environmental warming will inevitably alter the routine behavior and overall energy budgets of Arctic seals, but it is difficult to quantify these impacts as their metabolic requirements are not well known-due in part to the difficulty of studying wild individuals. Thus, data pertaining to species-specific energy demands are urgently needed to better understand the physiological consequences of rapid environmental change. We used open-flow respirometry over a four-year period to track fine-scale, longitudinal changes in the resting metabolic rate (RMR) of four spotted seals, three ringed seals and one bearded seal trained to participate in research. Simultaneously, we collected complementary physiological and environmental data. Species-specific metabolic demands followed expected patterns based on body size, with the largest species, the bearded seal, exhibiting the highest absolute RMR (0.48 ± 0.04 L O2 min-1) and the lowest mass-specific RMR (4.10 ± 0.47 ml O2 min-1 kg-1), followed by spotted (absolute: 0.33 ± 0.07 L O2 min-1; mass-specific: 6.13 ± 0.73 ml O2 min-1 kg-1) and ringed (absolute: 0.20 ± 0.04 L O2 min-1; mass-specific: 7.01 ± 1.38 ml O2 min-1 kg-1) seals. Further, we observed clear and consistent annual patterns in RMR that related to the distinct molting strategies of each species. For species that molted over relatively short intervals-spotted (33 ± 4 days) and ringed (28 ± 6 days) seals-metabolic demands increased markedly in association with molt. In contrast, the bearded seal exhibited a prolonged molting strategy (119 ± 2 days), which appeared to limit the overall cost of molting as indicated by a relatively stable annual RMR. These findings highlight energetic trade-offs associated with different molting strategies and provide quantitative data that can be used to assess species-specific vulnerabilities to changing conditions.

An MRI protocol for anatomical and functional evaluation of the California sea lion brain.

BACKGROUND: Domoic acid (DOM) is a neurotoxin produced by some harmful algae blooms in coastal waters. California sea lions (Zalophus californianus) exposed to DOM often strand on beaches where they exhibit a variety of symptoms, including seizures. These animals typically show hippocampal atrophy on MRI scans. NEW METHOD: We describe an MRI protocol for comprehensive evaluation of DOM toxicosis in the sea lion brain. We intend to study brain development in pups exposed in utero. The protocol depicts the hippocampal formation as the primary region of interest. We include scans for quantitative morphometry, functional and structural connectivity, and a cerebral blood flow map. RESULTS: High-resolution 3D anatomical scans facilitate post hoc slicing in arbitrary planes and accurate morphometry. We demonstrate the first cerebral blood flow map using MRI, and the first structural tractography from a live sea lion brain. COMPARISON WITH EXISTING METHODS: Scans were compared to prior anatomical and functional studies in live sea lions, and structural connectivity in post mortem specimens. Hippocampal volumes were broadly in line with prior studies, with differences likely attributable to the 3D approach used here. Functional connectivity of the dorsal left hippocampus matched that found in a prior study conducted at a lower magnetic field, while structural connectivity in the live brain agreed with findings observed in post mortem studies. CONCLUSIONS: Our protocol provides a comprehensive, longitudinal view of the functional and anatomical changes expected to result from DOM toxicosis. It can also screen for other common neurological pathologies and is suitable for any pinniped that can fit inside an MRI scanner.

In vivo measurement of lung volume in ringed seals: insights from biomedical imaging.

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 computed tomography (CT) images were used to quantify total lung capacity (TLC), respiratory dead space, minimum air volume and total body volume to improve assessment of lung oxygen storage capacity, scaling relationships and buoyant force estimates. The results suggest that lung oxygen stores determined in vivo are smaller than those derived from postmortem measurements. We also demonstrate that, whereas 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 body density and net vertical forces in the water column that influence costs associated with diving and foraging in free-ranging seals.

Evaluating temporary threshold shift onset levels for impulsive noise in seals.

The auditory effects of single- and multiple-shot impulsive noise exposures were evaluated in a bearded seal (Erignathus barbatus). This study replicated and expanded upon recent work with related species [Reichmuth, Ghoul, Sills, Rouse, and Southall (2016). J. Acoust. Soc. Am. 140, 2646-2658]. Behavioral methods were used to measure hearing sensitivity before and immediately following exposure to underwater noise from a seismic air gun. Hearing was evaluated at 100 Hz-close to the maximum energy in the received pulse, and 400 Hz-the frequency with the highest sensation level. When no evidence of a temporary threshold shift (TTS) was found following single shots at 185 dB re 1 µPa2 s unweighted sound exposure level (SEL) and 207 dB re 1 µPa peak-to-peak sound pressure, the number of exposures was gradually increased from one to ten. Transient shifts in hearing thresholds at 400 Hz were apparent following exposure to four to ten consecutive pulses (cumulative SEL 191-195 dB re 1 µPa2 s; 167-171 dB re 1 µPa2 s with frequency weighting for phocid carnivores in water). Along with these auditory data, the effects of seismic exposures on response time, response bias, and behavior were investigated. This study has implications for predicting TTS onset following impulsive noise exposure in seals.

Adaptations for amphibious vision in sea otters (Enhydra lutris): structural and functional observations.

Sea otters (Enhydra lutris) are amphibious mammals that maintain equal in-air and underwater visual acuity. However, their lens-based underwater accommodative mechanism presumably requires a small pupil that may limit sensitivity across light levels. In this study, we consider adaptations for amphibious living by assessing the tapetum lucidum, retina, and pupil dynamics in sea otters. The sea otter tapetum lucidum resembles that of terrestrial carnivores in thickness and fundic coverage. A heavily rod-dominated retina appears qualitatively similar to the ferret and domestic cat, and a thick outer nuclear layer relative to a thinner inner nuclear layer is consistent with nocturnal vertebrates and other amphibious carnivores. Pupil size range in two living sea otters is smaller relative to other amphibious marine carnivores (pinnipeds) when accounting for test conditions. The pupillary light response seems slower than other aquatic and terrestrial species tested in comparable brightness, although direct comparisons require further assessment. Our results suggest that sea otters have retained features for low-light vision but rapid adjustments and acute underwater vision may be constrained across varying light levels by a combination of pupil shape, absolute eye size, and the presumed coupling between anterior lens curvature and pupil size during accommodation.

In Vivo Measurements of Lung Volumes in Ringed Seals: Insights from Biomedical Imaging.

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 computed tomography (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 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 body density and net vertical forces in the water column that influence costs associated with diving and foraging in free-ranging seals.

Long-term evidence of noise-induced permanent threshold shift in a harbor seal (Phoca vitulina).

In psychophysical studies of noise-induced hearing loss with marine mammals, exposure conditions are often titrated from levels of no effect to those that induce significant but recoverable loss of auditory sensitivity [temporary threshold shift (TTS)]. To examine TTS from mid-frequency noise, a harbor seal was exposed to a 4.1-kHz underwater tone that was incrementally increased in sound pressure level (SPL) and duration. The seal's hearing was evaluated at the exposure frequency and one-half octave higher (5.8 kHz) to identify the noise parameters associated with TTS onset. No reliable TTS was measured with increasing sound exposure level until the second exposure to a 60-s fatiguing tone of 181 dB re 1 µPa SPL (sound exposure level 199 dB re 1 µPa2s), after which an unexpectedly large threshold shift (>47 dB) was observed. While hearing at 4.1 kHz recovered within 48 h, there was a permanent threshold shift of at least 8 dB at 5.8 kHz. This hearing loss was evident for more than ten years. Furthermore, a residual threshold shift of 11 dB was detected one octave above the tonal exposure, at 8.2 kHz. This hearing loss persisted for more than two years prior to full recovery.

Comparative Health Assessments of Alaskan Ice Seals.

Bearded (Erignathus barbatus), ringed (Pusa hispida), spotted (Phoca largha), and ribbon (Histriophoca fasciata) seals rely on seasonal sea-ice in Arctic and sub-Arctic regions. Many aspects of the biology and physiology of these seals are poorly known, and species-typical health parameters are not available for all species. Such information has proven difficult to obtain due to the challenges of studying Arctic seals in the wild and their minimal historic representation in aquaria. Here, we combine diagnostic information gathered between 2000 and 2017 from free-ranging seals, seals in short-term rehabilitation, and seals living in long-term human care to evaluate and compare key health parameters. For individuals in apparent good health, hematology, and blood chemistry values are reported by the source group for 10 bearded, 13 ringed, 73 spotted, and 81 ribbon seals from Alaskan waters. For a smaller set of individuals handled during veterinary or necropsy procedures, the presence of parasites and pathogens is described, as well as exposure to a variety of infectious diseases known to affect marine mammals and/or humans, with positive titers observed for Brucella, Leptospira, avian influenza, herpesvirus PhHV-1, and morbillivirus. These data provide initial baseline parameters for hematology, serum chemistries, and other species-level indicators of health that can be used to assess the condition of individual seals, inform monitoring and management efforts, and guide directed research efforts for Alaskan populations of ice-associated seals.

High-amplitude vocalizations of male northern elephant seals and associated ambient noise on a breeding rookery.

Northern elephant seals (Mirounga angustirostris) are massive, land-breeding marine mammals that produce loud, stereotyped calls during annual breeding seasons. To determine vocalization source levels emitted by competing males on a mainland breeding rookery, aerial calls were measured on-axis at 1 m from adult males using three different sound pressure level metrics. Time-averaged (1 min) ambient noise was also measured under variable environmental and social conditions. Results indicate that male northern elephant seals emit high amplitude airborne calls with little variation in call amplitude. Mean source levels ranged from 98 to 114 dB re: 20 µPa [root-mean-square (rms) -fast], 102-116 dB re: 20 µPa (rms-impulse), and 120-131 dB re: 20 µPa (peak) and average standard deviations for all metrics were <2.3 dB. Further, these seal rookeries exhibit high variability in ambient noise (in terms of both spectrum and amplitude) from biotic and environmental sources. Finally, males sampled did not adjust call amplitude to compensate for higher background noise levels and thus did not exhibit a Lombard effect. These findings reinforce the view that the remarkable vocalizations of male northern elephant seals serve as rigid and powerful signals that convey individual identity within noisy breeding colonies rather than as honest indicators of size, status, or motivation.

The rise and fall of dialects in northern elephant seals.

Vocal dialects are fundamental to our understanding of the transmission of social behaviours between individuals and populations, however few accounts trace this phenomenon among mammals over time. Northern elephant seals (Mirounga angustirostris) provide a rare opportunity to examine the trajectory of dialects in a long-lived mammalian species. Dialects were first documented in the temporal patterns of the stereotyped vocal displays produced by breeding males at four sites in the North Pacific in 1968 and 1969, as the population recovered from extreme exploitation. We evaluated the longevity of these geographical differences by comparing these early recordings to calls recently recorded at these same locations. While the presence of vocal dialects in the original recordings was re-confirmed, geographical differences in vocal behaviour were not found at these breeding rookeries nearly 50 years later. Moreover, the calls of contemporary males displayed more structural complexity after approximately four generations, with substantial between-individual variation and call features not present in the historical data. In the absence of measurable genetic variation in this species-owing to an extreme population bottleneck-a combination of migration patterns and cultural mutation are proposed as factors influencing the fall of dialects and the dramatic increase in call diversity.