Seal whiskers vibrate over broad frequencies during hydrodynamic tracking

© The Author(s), 2017. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Scientific Reports 7 (2017): 8350, doi:10.1038/s41598-017-07676-w.Although it is known that seals can use their whiskers (vibrissae) to extract relevant information from complex underwater flow fields, the underlying functioning of the system and the signals received by the sensors are poorly understood. Here we show that the vibrations of seal whiskers may provide information about hydrodynamic events and enable the sophisticated wake-tracking abilities of these animals. We developed a miniature accelerometer tag to study seal whisker movement in situ. We tested the ability of the tag to measure vibration in excised whiskers in a flume in response to laminar flow and disturbed flow. We then trained a seal to wear the tag and follow an underwater hydrodynamic trail to measure the whisker signals available to the seal. The results showed that whiskers vibrated at frequencies of 100–300 Hz, with a dynamic response. These measurements are the first to capture the incoming signals received by the vibrissae of a live seal and show that there are prominent signals at frequencies where the seal tactogram shows good sensitivity. Tapping into the mechanoreceptive interface between the animal and the environment may help to decipher the functional basis of this extraordinary hydrodynamic detection ability.Funding was provided by the NSF GRFP and NISE section 219 to C. Murphy and by the Office of Naval Research (N000141910468) to B. Calhoun

Vocal Behavior in Spotted Seals (Phoca largha) and Implications for Passive Acoustic Monitoring

Passive acoustic methods enable remote monitoring of marine species and habitats. These methods can be applied to investigate distribution and abundance of populations, to evaluate behavioral and physiological states of individuals, and to inform management efforts for animals that live in hard-to-reach places. Spotted seals (Phoca largha) inhabit high-latitude, light-limited sub-Arctic and Arctic waters and move seasonally with unstable sea ice. They are high trophic level predators vulnerable to changing conditions associated with environmental warming. At present, an incomplete characterization of the spotted seal vocal repertoire limits our ability to monitor this species acoustically. Captive studies can inform passive acoustic efforts by describing fundamental features of species-typical vocalizations emitted by known individuals. These features include acoustic parameters as well as developmental, seasonal, and sex-specific patterns in vocal behavior. Here, we studied several male spotted seals in captivity from age 6 months through adulthood (10 years). Vocal behavior was scored daily and opportunistically recorded. The production of underwater calls emerged during sexual maturation, at age 4. To evaluate vocal repertoire and fine-scale temporal patterns of sound production in adult seals, an underwater acoustic recorder was continuously deployed with two seals at age 7 years. The spotted seals produced at least eight distinctive underwater call types with dominant energy below 1 kHz. The amplitude of the most common vocalization was ∼140 dB re 1 μPa (sound pressure level at 1 m). There was a marked peak in vocal activity in springtime, prior to onset of the annual molt. This period coincided with increased aggressive behavior, presence of a notable musky odor, and urogenital swelling indicative of heightened reproductive status. These results from developing male spotted seals reared in human care confirm the production of recognizable, stereotypic underwater calls associated with the breeding season. Description of vocal behavior improves knowledge of this species’ biology, and informs the potential use of autonomous acoustic recorders to track the presence and movements of free-ranging spotted seals in remote habitats

Rapid behavioural diagnosis of domoic acid toxicosis in California sea lions

Domoic acid is a neurotoxic metabolite of widely occurring algal blooms that has caused multiple marine animal stranding events. Exposure to high doses of domoic acid, a glutamate agonist, may lead to persistent medial temporal seizures and damage to the hippocampus. California sea lions (Zalophus californianus) are among the most visible and frequent mammalian victims of domoic acid poisoning, but rapid, reliable diagnosis in a clinical setting has proved difficult owing to the fast clearance of the toxin from the blood stream. Here, we show that the behavioural orienting responses of stranded sea lions diagnosed with domoic acid toxicosis habituate more slowly to a series of non-aversive auditory stimuli than do those of sea lions with no apparent neurological deficits. A signal detection analysis based on these habituation measures was able to correctly identify 50 per cent of subjects with domoic acid toxicosis while correctly rejecting approximately 93 per cent of controls, suggesting potential diagnostic merit

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

Energy-Rich Mesopelagic Fishes Revealed as a Critical Prey Resource for a Deep-Diving Predator Using Quantitative Fatty Acid Signature Analysis

Understanding the diet of deep-diving predators can provide essential insight to the trophic structure of the mesopelagic ecosystem. Comprehensive population-level diet estimates are exceptionally difficult to obtain for elusive marine predators due to the logistical challenges involved in observing their feeding behavior and collecting samples for traditional stomach content or fecal analyses. We used quantitative fatty acid signature analysis (QFASA) to estimate the diet composition of a wide-ranging mesopelagic predator, the northern elephant seal (Mirounga angustirostris), across five years. To implement QFASA, we first compiled a library of prey fatty acid (FA) profiles from the mesopelagic eastern North Pacific. Given the scarcity of a priori diet data for northern elephant seals, our prey library was necessarily large to encompass the range of potential prey in their foraging habitat. However, statistical constraints limit the number of prey species that can be included in the prey library to the number of dietary FAs in the analysis. Exceeding that limit could produce non-unique diet estimates (i.e., multiple diet estimates fit the data equally well). Consequently, we developed a novel ad-hoc method to identify which prey were unlikely to contribute to diet and could, therefore, be excluded from the final QFASA model. The model results suggest that seals predominantly consumed small mesopelagic fishes, including myctophids (lanternfishes) and bathylagids (deep sea smelts), while non-migrating mesopelagic squids comprised a third of their diet, substantially less than suggested by previous studies. Our results revealed that mesopelagic fishes, particularly energy-rich myctophids, were a critical prey resource, refuting the long-held view that elephant seals are squid specialists

Ultrastructure of the organ of Corti in harbor seals (Phoca vitulina)

Ultrastructural descriptions of the inner ear of highly sound-dependent mammalian species are lacking and needed to gain a better understanding of the hearing sense. Here, we present the first morphometric descriptions of the sensory cells of the inner ear in the harbor seal (Phoca vitulina), a mammal with broadly sensitive amphibious hearing. Scanning electron micrographs of the apical surface of the outer hair cells (OHCs) and inner hair cells (IHCs) within the organ of Corti were obtained from five individuals and analyzed by linear and geometric morphometrics. Measurements were taken at regular locations along the cochlea. The spiral shape of the seal cochlea contained two and a half turns. The organ of Corti had an average length of 27.7 mm with 12,628 OHCs (12,400-12,900). Six linear morphometric parameters showed significant patterns of change associated with their location within the cochlear spiral. Likewise, these trends were similarly expressed in cell configuration (cell blocks with 57 landmarks in 12 representative cells) revealed by geometric morphometry. Cell configuration varied predictably with position in the cochlea according to clustering analyses and Procrustes ANOVA (F= 25.936, p<0001). Changes associated with OHCs were primarily responsible for observed changes in cell configuration. An integration trend in cell shape change was also observed in which IHCs and OHCs share features in their morphological variation by the two-block partial least squares analysis (CR=0.987, p<0.001) and the modularity hypothesis (CV=0.99, p=0.05). These descriptive and quantitative findings provide a baseline for the morphology and morphometry of the sensory cells of the organ of Corti in harbor seals, allowing for comparisons between normal and pathological features. This initial morphological description should enable the correlation between position, morphometric features, and frequency coding along the spiral of the inner ear in this species, whose hearing ability is well studied

Energy-Rich Mesopelagic Fishes Revealed as a Critical Prey Resource for a Deep-Diving Predator Using Quantitative Fatty Acid Signature Analysis

Understanding the diet of deep-diving predators can provide essential insight to the trophic structure of the mesopelagic ecosystem. Comprehensive population-level diet estimates are exceptionally difficult to obtain for elusive marine predators due to the logistical challenges involved in observing their feeding behavior and collecting samples for traditional stomach content or fecal analyses. We used quantitative fatty acid signature analysis (QFASA) to estimate the diet composition of a wide-ranging mesopelagic predator, the northern elephant seal (Mirounga angustirostris), across five years. To implement QFASA, we first compiled a library of prey fatty acid (FA) profiles from the mesopelagic eastern North Pacific. Given the scarcity of a priori diet data for northern elephant seals, our prey library was necessarily large to encompass the range of potential prey in their foraging habitat. However, statistical constraints limit the number of prey species that can be included in the prey library to the number of dietary FAs in the analysis. Exceeding that limit could produce non-unique diet estimates (i.e., multiple diet estimates fit the data equally well). Consequently, we developed a novel ad-hoc method to identify which prey were unlikely to contribute to diet and could, therefore, be excluded from the final QFASA model. The model results suggest that seals predominantly consumed small mesopelagic fishes, including myctophids (lanternfishes) and bathylagids (deep sea smelts), while non-migrating mesopelagic squids comprised a third of their diet, substantially less than suggested by previous studies. Our results revealed that mesopelagic fishes, particularly energy-rich myctophids, were a critical prey resource, refuting the long-held view that elephant seals are squid specialists