Wavy Whiskers in Wakes: Explaining the Trail-Tracking Capabilities of Whisker Arrays on Seal Muzzles.

Seals can detect prey up to 180 m away using only their flow-sensing whiskers. The unique undulating morphology of Phocid seal whiskers reduces vortex-induced vibrations (VIVs), rendering seals highly sensitive to biologically relevant flow stimuli. In this work, digital models of harbor and grey seal whiskers are extracted using 3D scanning and a mathematical framework that accurately recreates their undulating geometry is proposed. Through fluid-structure interaction studies and experimental investigations involving a whisker array mounted on 3D-printed microelectromechanical systems sensors, the vibration characteristics of the whisker array and the interaction between neighboring whiskers in steady flows and fish-wake-like vortices are explained for the first time. Results reveal that the downstream vortices intensity and resulting VIVs are consistently lower for grey than harbor seal whiskers and a smooth cylinder, suggesting that the grey seal whisker geometry can be an ideal template for the biomimetic design of VIV-resistant underwater structures. In addition, neighboring whiskers in an array influence one another by resulting in greater flow vorticity fluctuation and distribution area, thus causing increased vibrations than an isolated whisker, which indicates the possibility of a signal-strengthening effect in whisker arrays.

Morphological peculiarities of a harbour seal (Phoca vitulina) whisker revealed by normal skeletonisation.

Of all mammalian vibrissae, those of certain species of pinnipeds are exceptional. Researchers believe that their curious undulating form evolved for hydrodynamic detection. Our understanding of how these whiskers work depends on a geometrical model that captures the crucial pertinent features of the natural vibrissae including its tapering and curvature. It should also account for the form of the whisker when it flexes under external loading. We introduce and study a normal skeleton of a two-dimensional projection of a harbour seal whisker. The normal skeleton is a complete shape descriptor that involves reduction to the centreline equipped with a thickness function of the orthogonal cross-section. The contours of the whisker shape are extracted from a 2D greyscale scan. Our analysis reveals correspondence between the undulations of the width and oscillations of the centreline curvature as functions of arc length. We discuss two possible explanations for that remarkable feature: one based on consideration of growth and the other of plastic deformation. For the latter we employ a mechanical model to demonstrate appearance of curvature oscillations caused by extensive deflection of the undulating whisker due to external loading.

Flow over seal whiskers: Importance of geometric features for force and frequency response.

The complex undulated geometry of seal whiskers has been shown to substantially modify the turbulent structures directly downstream, resulting in a reduction of hydrodynamic forces as well as modified vortex-induced-vibration response when compared with smooth whiskers. Although the unique hydrodynamic response has been well documented, an understanding of the fluid flow effects from each geometric feature remains incomplete. In this computational investigation, nondimensional geometric parameters of the seal whisker morphology are defined in terms of their hydrodynamic relevance, such that wavelength, aspect ratio, undulation amplitudes, symmetry and undulation off-set can be varied independently of one another. A two-factor fractional factorial design of experiments procedure is used to create 16 unique geometries, each of which dramatically amplifies or attenuates the geometric parameters compared with the baseline model. The flow over each unique topography is computed with a large-eddy simulation at a Reynolds number of 500 with respect to the mean whisker thickness and the effects on force and frequency are recorded. The results determine the specific fluid flow impact of each geometric feature which will inform both biologists and engineers who seek to understand the impact of whisker morphology or lay out a framework for biomimetic design of undulated structures.

Does Vibrissal Innervation Patterns and Investment Predict Hydrodynamic Trail Following Behavior of Harbor Seals (Phoca vitulina)?

Our understanding of vibrissal function in pinnipeds is poor due to the lack of comparative morphological, neurobiological, and psychophysical performance data. In contrast, the function of terrestrial mammalian vibrissae is better studied. Pinnipeds have the largest vibrissae of all mammals, and phocids may have the most modified vibrissae. The tactile performance for pinniped vibrissae is well known for harbor seals (Phoca vitulina). Harbor seals display at least two types of tactile behavior involving their mystacial vibrissae: a fine discriminatory capability using active touch and hydrodynamic trail following (the ability to detect and follow turbulent trails). This study investigated innervation patterns of harbor seal follicle-sinus complexes (F-SCs) to test the hypothesis that the whiskers used in hydrodynamic trail following possess increased innervation investment compared to other phocids. Therefore, the most lateral vibrissae from five harbor seals were histologically processed so that morphometric measurements and axon counts could be collected. Vibrissae from one harbor seal were immunolabeled with anti-protein gene product (PGP 9.5) to document the pattern of deep vibrissal nerve innervation of the F-SCs. Overall, harbor seals showed an innervation pattern (axons/F-SC and axons/muzzle) similar to other phocids. The ventrolateral vibrissae, involved in hydrodynamic trail following, have greater axon density in harbor seals than harp seals, suggesting harbor seal F-SC innervation patterns could explain their performance at trail following. The combination of microstructural, innervation investment, and behavioral data provides a foundation for functional inference regarding this tactile behavior in harbor seals and also facilitates future comparative work for other pinniped species. Anat Rec, 302:1837-1845, 2019. © 2019 American Association for Anatomy.

A mark-recapture approach for estimating population size of the endangered ringed seal (Phoca hispida saimensis).

Reliable population estimates are fundamental to the conservation of endangered species. We evaluate here the use of photo-identification (photo-ID) and mark-recapture techniques for estimating the population size of the endangered Saimaa ringed seal (Phoca hispida saimensis). Photo-ID data based on the unique pelage patterns of individuals were collected by means of camera traps and boat-based surveys during the molting season in two of the species' main breeding areas, over a period of five years in the Pihlajavesi basin and eight years in the Haukivesi basin. An open model approach provided minimum population estimates for these two basins. The results indicated high survival rates and site fidelity among the adult seals. More accurate estimates can be obtained in the future by increasing the surveying effort both spatially and temporally. The method presented here proved effective for evaluating population size objectively, whereas the results of the current snow lair censuses are dependent on varying winter conditions, for instance. We therefore suggest that a photo-ID-based non-invasive mark-recapture method should be used for estimating Saimaa ringed seal abundances in order to ensure reliable, transparent population monitoring under changing climatic conditions.

Host characteristics and infection level of an intestinal parasite Corynosoma strumosum (Acanthocephala) in the Kuril harbor seal of Erimo Cape, Hokkaido, Japan.

The Kuril harbor seal around Hokkaido is presently recovering from a resource crisis while conflicts with local fisheries have become a concern. However, its feeding habits, which are fundamental information for taking proper preventive measures, are still poorly understood. We thus examined the infection status of a trophically-transmitted parasite, Corynosoma strumosum in the seals of Erimo Cape, to assess the host's feeding habits with a practical view of the parasite as a biological indicator. A total of 2802 worms were found from 20 male and 20 female by-caught animals in salmon set nets within local fisheries during August to November 2014. The parasite abundance was explained mainly by the host's developmental stage and intestinal length while weakly affected by gender and body size, through an estimation of generalized linear models combined with hierarchical partitioning. Considering the past records that demersal fishes are the probable main sources of infection, the infection level may owe to individual host differences regarding these sources and/or feeding grounds with relating the host characteristics. This supports that the resource management of Kuril harbor seals requires careful consideration of the individual differences in feeding behavior.

Sensing the flow beneath the fins.

Flow sensing, maneuverability, energy efficiency and vigilance of surroundings are the key factors that dictate the performance of marine animals. Be it swimming at high speeds, attack or escape maneuvers, sensing and survival hydrodynamics are a constant feature of life in the ocean. Fishes are capable of performing energy efficient maneuvers, including capturing energy from vortical structures in water. These impressive capabilities are made possible by the uncanny ability of fish to sense minute pressure and flow variations on their body. This is achieved by arrays of biological neuromast sensors on their bodies that 'feel' the surroundings through 'touch at a distance' sensing. The main focus of this paper is to review the various biomimetic material approaches in developing superficial neuromast inspired ultrasensitive MEMS sensors. Principals and methods that translate biomechanical filtering properties of canal neuromasts to benefit artificial MEMS sensors have also been discussed. MEMS sensors with ultrahigh flow sensitivity and accuracy have been developed mainly through inspiration from the hair cell and cupula structures in the neuromast. Canal-inspired packages have proven beneficial in hydrodynamic flow filtering in artificial sensors enabling signal amplification and noise attenuation. A special emphasis has been placed on the recent innovations that closely mimic the structural and material designs of stereocilia of neuromasts by exploring soft polymers.

Mechanical properties of harbor seal skin and blubber - a test of anisotropy.

The skin and blubber of marine mammals provides protection from the surrounding environment, whether that be temperature, microbes, or direct mechanical impacts. To understand the ability of harbor seals' (Phoca vitulina) skin and blubber to resist blunt force trauma, we tested the material properties of these tissues. We quantified two mechanical properties of the tissue: tensile strength and tensile stiffness, at two test speeds, three sample orientations, and two age groups. We found significant differences in material properties between test speeds, orientation, and age of the animal, but did not find a large difference with orientation. From this analysis, we conclude that harbor seal skin and blubber should be modeled as an isotropic non-linear elastic material with strain rate dependence. Moreover, we were interested in the effects of freezing on the biomechanical properties. The material was tested fresh and after being frozen for four months. Frozen data revealed an increase in stiffness and strength for the skin (epidermis and dermis), but did not show a conclusive trend in the blubber material properties. While the availability of frozen marine mammal tissue is greater than that of fresh material, frozen tissue of harbor seals, especially the skin, cannot serve as an accurate replacement for testing of fresh material.

Genital interactions during simulated copulation among marine mammals.

Genitalia are morphologically variable across many taxa and in physical contact during intromission, but little is known about how variation in form correlates with function during copulation. Marine mammals offer important insights into the evolutionary forces that act on genital morphology because they have diverse genitalia and are adapted to aquatic living and mating. Cetaceans have a fibroelastic penis and muscular vaginal folds, while pinnipeds have a baculum and lack vaginal folds. We examined copulatory fit in naturally deceased marine mammals to identify anatomical landmarks in contact during copulation and the potential depth of penile penetration into the vagina. Excised penises were artificially inflated to erection with pressurized saline and compared with silicone vaginal endocasts and within excised vaginas in simulated copulation using high-resolution, diffusible iodine-based, contrast-enhanced computed tomography. We found evidence suggestive of both congruent and antagonistic genital coevolution, depending on the species. We suggest that sexual selection influences morphological shape. This study improves our understanding of how mechanical interactions during copulation influence the shape of genitalia and affect fertility, and has broad applications to other taxa and species conservation.

Seal Whiskers Vibrate Over Broad Frequencies During Hydrodynamic Tracking.

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.

Characterization of seal whisker morphology: implications for whisker-inspired flow control applications.

Seals with beaded whiskers-the majority of true seals (Phocids)-are able to trace even minute disturbance caused by prey fish in the ambient flow using only sensory input from their whiskers. The unique three-dimensional undulating morphology of seal whiskers has been associated with their capability of suppressing vortex-induced vibration and reducing drag. The exceptional hydrodynamic traits of seal whiskers are of great interest in renovating the design of aero-propulsion flow components and high-sensitivity flow sensors. It is essential to have well-documented data of seal whisker morphology with statistically meaningful generalization, as the solid foundation for whisker-inspired flow control applications. However, the available whisker morphology data is either incomplete, with measurements of only a few key parameters, or based on a very limited sample size in case studies. This work characterizes the morphology of 27 beaded seal whiskers (harbor seal and elephant seal), using high-resolution computer-tomography scanning at NASA's Glenn Research Center in Cleveland, OH. Over two thousand cross-sectional slices for every individual whisker sample are reconstructed, to generate three-dimensional morphology. This is followed by detailed statistical analysis of a set of key parameters, under an established framework (Hanke et al 2010 J. Exp. Biol. 213 2665-72). While the length parameters are generally consistent with previous studies, we note that the angle of incidence of elliptical cross-sections varies in a wide range, with a majority falling between [Formula: see text] and [Formula: see text]. Angles of incidence at both peaks and troughs appear to roughly follow a Gaussian distribution, but no clear preference of orientation is identified. We discuss the current knowledge of whisker-inspired flow studies, focusing on choices of morphology parameters. The new understanding of whisker morphology can better inform future design of high-sensitivity flow sensors and aero-propulsion flow structures.

Development of an artificial sensor for hydrodynamic detection inspired by a seal's whisker array.

Nature has shaped effective biological sensory systems to receive complex stimuli generated by organisms moving through water. Similar abilities have not yet been fully developed in artificial systems for underwater detection and monitoring, but such technology would enable valuable applications for military, commercial, and scientific use. We set out to design a fluid motion sensor array inspired by the searching performance of seals, which use their whiskers to find and follow underwater wakes. This sensor prototype, called the Wake Information Detection and Tracking System (WIDTS), features multiple whisker-like elements that respond to hydrodynamic disturbances encountered while moving through water. To develop and test this system, we trained a captive harbor seal (Phoca vitulina) to wear a blindfold while tracking a remote-controlled, propeller-driven submarine. After mastering the tracking task, the seal learned to carry the WIDTS adjacent to its own vibrissal array during active pursuit of the target. Data from the WIDTS sensors describe changes in the deflection angles of the whisker elements as they pass through the hydrodynamic trail left by the submarine. Video performance data show that these detections coincide temporally with WIDTS-wake intersections. Deployment of the sensors on an actively searching seal allowed for the direct comparison of our instrument to the ability of the biological sensory system in a proof-of-concept demonstration. The creation of the WIDTS provides a foundation for instrument development in the field of biomimetic fluid sensor technology.

Macroscopic Anatomy of the Saimaa Ringed Seal (Phoca hispida saimensis) Lower Respiratory Tract.

We studied the macroscopic anatomy of the lower respiratory tract of the endangered Saimaa ringed seal (Phoca hispida saimensis). Examination of one adult and one young individual found dead showed that trachea had 85 and 86 complete cartilage rings. The adjacent cartilages exhibited very few random anastomoses. There was variation in the confirmation of the trachea between the cranial and caudal part of the trachea. The right lung was divided by partly incomplete inter-lobar fissures into cranial, middle, caudal, and accessory lobes. The left lung consisted of cranial, middle, and caudal lobes. The lungs were characterized by a high amount of interlobular connective tissue. Silicone casts were prepared of the two specimens to visualize the tracheobronchial branching which was similar to that of marine ringed seals but in the Saimaa ringed seal the right middle lobar bronchus originated at the same level as the accessory lobar bronchus.

A Comparative Morphometric Analysis of Three Cranial Nerves in Two Phocids: The Hooded Seal (Cystophora cristata) and the Harbor Seal (Phoca vitulina).

While our knowledge about the senses of pinnipeds has increased over the last decades almost nothing is known about the organization of the neuroanatomical pathways. In a first approach to this field of research, we assessed the total number of myelinated axons of three cranial nerves (CNs) in the harbor (Phoca vitulina, Pv) and hooded seal (Cystophora cristata, Cc). Axons were counted in semithin sections of the nerves embedded in Epon and stained with toluidine blue. In both species, the highest axon number was found within the optic nerve (Pv 187,000 ± 8,000 axons, Cc 481,600 ± 1,300 axons). Generally, considering absolute axon numbers, far more axons were counted within the optic and trigmenial nerve (Pv 136,700 ± 2,500 axons, Cc 179,300 ± 6,900 axons) in hooded in comparison to harbor seals. The axon counts of the vestibulocochlear nerve are nearly identical for both species (Pv 87,100 ± 8,100 axons, Cc 86,600 ± 2,700 axons). However, when comparing cell density, the cell density is almost equal for all nerves for both species except for the optic nerve in which cell density was particularly higher than in the other nerves and higher in hooded in comparison to harbor seals. We here present the first comparative analysis of three CNs in two phocid seals. While the CNs of these closely related species share some general characteristics, pronounced differences in axon numbers/densities are apparent. These differences seem to reflect differences in e.g. size, habitat, and/or functional significance of the innervated sensory systems.

Comparative anatomy of the ophthalmic rete and its relationship to ocular blood flow in three species of marine mammal.

OBJECTIVE: To examine the blood supply to the eyes of bottlenose dolphin (Tursiops truncatus), spotted seal (Phoca largha), and California sea lion (Zalophus californianus). Emphasis is placed on exploring the anatomic function in the context of aquatic life. PROCEDURE: Methyl methacrylate casts were prepared and studied using a scanning electron microscope. Infrared images of the eye were recorded using a thermocamera. RESULTS: In all three marine species, blood is supplied to the ophthalmic rete. The main source of blood supply to the rete is the basilar rete via the spinal rete in the dolphin and via the ophthalmic artery in the seal and sea lion. The retinal and choroidal arteries are derived from the rete. The dolphin rete showed a very well-developed arterial network occupying most of the orbit. The rete in pinnipeds was less developed with several entwining arteries, unlike that in cetaceans. Thermographic examination revealed that the eye shows a higher degree of thermal emission than adjacent areas of the skin in these 3 species. DISCUSSION: The role of the rete in aquatic mammals appears to conserve ocular temperature so that the appropriate operating temperature for photoreceptors and ocular muscles can be maintained in a cold ambient temperature. Additionally, the rete might have a flow-damping effect by maintaining resistance to blood flow in the orbit. This study highlights the special nature of ocular vascular anatomy and function that enabled the unique adaptation of aquatic mammals to life in aquatic habitats.

Vibrissal touch sensing in the harbor seal (Phoca vitulina): how do seals judge size?

"Whisker specialists" such as rats, shrews, and seals actively employ their whiskers to explore their environments and extract object properties such as size, shape, and texture. It has been suggested that whiskers could be used to discriminate between different sized objects in one of two ways: (i) to use whisker positions, such as angular position, spread or amplitude to approximate size; or (ii) to calculate the number of whiskers that contact an object. This study describes in detail how two adult harbor seals use their whiskers to differentiate between three sizes of disk. The seals judged size very fast, taking <400 ms. In addition, they oriented their smaller, most rostral, ventral whiskers to the disks, so that more whiskers contacted the surface, complying to a maximal contact sensing strategy. Data from this study supports the suggestion that it is the number of whisker contacts that predict disk size, rather than how the whiskers are positioned (angular position), the degree to which they are moved (amplitude) or how spread out they are (angular spread).

Demonstration of free fatty acids in the integument of semi-aquatic and aquatic mammals.

The sensitive red fluorescence dye BODIPY® 665/676, and embedding in the water-soluble resin Technovit® 7100 were used to demonstrate free fatty acids in the epidermis of seven semi-aquatic and aquatic mammalian species with a sparse or dense hair coat. The staining generally marked lipid layers of varying thickness between the lamellae of the Stratum corneum, as found particularly in very densely haired species (otter), but also in rather sparsely haired animals (beaver, nutria), and especially in the seal. The very sparsely haired capybara contained no free fatty acids in the corneal layer system, but exhibited an accumulation of such substances in the vital epidermis. All haired species showed a strongly positive reaction staining of the sebaceous glands. In the hairless species, a distinct intracellular staining was restricted to cells of the thick vital epidermis in the hippopotamus, whereby in the Str. corneum positive intercellular reactions appeared. In the dolphin, on the contrary, positive intercellular reactions became visible in the vital epidermis, whereas in the Str. corneum the lipids concentrated in large longitudinal intracellular vesicles.

Harbor seal vibrissa morphology suppresses vortex-induced vibrations.

Harbor seals (Phoca vitulina) often live in dark and turbid waters, where their mystacial vibrissae, or whiskers, play an important role in orientation. Besides detecting and discriminating objects by direct touch, harbor seals use their whiskers to analyze water movements, for example those generated by prey fish or by conspecifics. Even the weak water movements left behind by objects that have passed by earlier can be sensed and followed accurately (hydrodynamic trail following). While scanning the water for these hydrodynamic signals at a swimming speed in the order of meters per second, the seal keeps its long and flexible whiskers in an abducted position, largely perpendicular to the swimming direction. Remarkably, the whiskers of harbor seals possess a specialized undulated surface structure, the function of which was, up to now, unknown. Here, we show that this structure effectively changes the vortex street behind the whiskers and reduces the vibrations that would otherwise be induced by the shedding of vortices from the whiskers (vortex-induced vibrations). Using force measurements, flow measurements and numerical simulations, we find that the dynamic forces on harbor seal whiskers are, by at least an order of magnitude, lower than those on sea lion (Zalophus californianus) whiskers, which do not share the undulated structure. The results are discussed in the light of pinniped sensory biology and potential biomimetic applications.

Histological assessment of selected blood vessels of the phocid seals (northern elephant and harbour seals).

Phocid seals exhibit vascular adaptations that allow them to undertake prolonged deep dives. These vascular adaptations are either unique to phocids, or are modified vascular equivalents to those present in terrestrial mammals. One such adaptation, the aortic bulb, is a spherical enlargement of the ascending aorta specific to phocid seals. Its histological make-up consists of a reinforced tunica media with circular and longitudinal layers of elastic fibres. This reinforcement enables multi-axial deformation of the aortic bulb, thus complementing its function as a prominent elastic reservoir or 'windkessel'. A second adaptation, the hepatic sinus, is an asymmetrical dilation of the abdominal portion of the caudal vena cava and accompanying hepatic veins. The hepatic sinus is comprised of a relatively thin tunica media, with a scant smooth muscle component. The bulk of the sinus wall is comprised of tunica adventitia. A third vascular adaptation distinctive to the phocids is the pericardial venous plexus, composed of convoluted veins circumnavigating the perimeter of the heart. Microscopically, these veins have a thick tunica media and also contain valves. Smaller arteries, venules and distinct capillary beds are observed interspersed in-between these veins. It can be hypothesized, that in seals, certain vascular embryonic development may be arrested at an earlier embryonic stage, resulting in these unusual vascular formations. These modifications play a vital role in blood pressure regulation and distribution of oxygenated blood during prolonged deep diving. The purpose of this work was to elucidate the histological aspects of these unique vascular modifications and relate them to specific function.