Abstract
Vertebrate surface structures, including mammalian skin and hair structures, have undergone various modifications during evolution in accordance with functional specializations. Harbour seals rely on their vibrissal system for orientation and foraging. To maintain tactile sensitivity even at low temperatures, the vibrissal follicles are heated up intensely, which could cause severe heat loss to the environment. We analysed skin samples of different body parts of harbour seals, and expected to see higher hair densities at the vibrissal pads as a way to reduce heat loss. In addition to significantly higher hair densities around the vibrissae than on the rest of the body, we show a unique fur structure of hair bundles consisting of broad guard hairs along with hairs of a new type, smaller than guard hairs but broader than underhairs, which we defined as ‘intermediate hairs’. This fur composition has not been reported for any mammal so far and may serve for thermal insulation as well as drag reduction. Furthermore, we describe a scale-like skin structure that also presumably plays a role in drag reduction.
Keywords: guard hair, pilosebaceous unit, skin structure, intermediate hair, hydrodynamics, surface drag
1. Introduction
Pinnipeds and phocid seals in particular rely on their whiskers, i.e. the vibrissal system as hydrodynamic and tactile sense for orientation and foraging under water when vision is limited. Therefore, their vibrissal system is highly developed. In phocid seals, the vibrissal system consists of the mystacial vibrissae, arranged in rows on the vibrissal pads at the snout, 5–10 supraorbital vibrissae on small vibrissal pads above each eye as well as one small rhinal vibrissa above each nare (figure 1a). In humans, tactile sensitivity is affected by low ambient temperatures [2–4]. By contrast, in harbour seals, tactile sensitivity is not affected even at water temperatures down to 1.2°C [1]. One reason for this is a specific blubber composition of low melting fatty acids at the vibrissal pads, maintaining the flexibility of the vibrissal pads even at low ambient temperatures [5]. Furthermore, tactile sensitivity is maintained independent of ambient temperature owing to the heating of the vibrissal follicles [6]. Each vibrissal follicle is embedded in a follicle–sinus complex (F-SC) that contains large blood sinuses and huge numbers of free nerve endings and mechanoreceptor cells [7–10], illustrated in figure 1b. The F-SCs are heated by an upper cavernous sinus [6] that maintains a constant temperature of about 31.7°C, independent of ambient temperature [11]. This intense heating has the disadvantage of heat loss to the environment, which appears to be tolerated in favour of a functioning tactile sense. But, possibly heat loss at these sites would be even much higher if it was not for a special thermal insulation, namely the fur. In a recent study by Erdsack et al. [11], temperature differences up to 26.9 K between the skin and the outer surface of the fur were measured at the vibrissal pads of harbour seals, indicating a considerable insulating effect of the fur at these sites. Phocid seals rely mainly on their blubber as thermal insulation, which is nearly as effective in water as in air [12]. So far, the insulating value of phocid fur has been regarded negligible in water [13–16], but none of the investigations involved the fur on the seals' vibrissal pads.
Figure 1.
Vibrissal system of phocid seals. (a) Vibrissal system of a harbour seal (Phoca vitulina; Marine Science Center, Rostock): the mystacial vibrissae, arranged in rows on the vibrissal pads on the left and right side of the nose; 5–10 supraorbital vibrissae on small vibrissal pads above the eyes as well as one small rhinal vibrissa above each nare. (b) Follicle–sinus complex (F-SC) of a phocid seal (adapted with permission from Dehnhardt et al. [1]): the lower cavernous sinus (LCS) and the ring sinus (RS) are highly innervated, whereas the upper cavernous sinus (UCS) heats the main sensory areas below to maintain tactile sensitivity independent of ambient temperature.
Mammalian fur is generally arranged in hair bundles, the ‘pilosebaceous units’, consisting of one broad guard hair along with a variable number of underhairs (figure 2) or exclusively of fine underhairs [18]. Each hair originates in its own follicle, but all hairs of a bundle protrude from the skin through one common pilary canal [19–21]. Therefore, hair density can vary either by the number of hairs per bundle, or by the number of bundles per unit area, or by a combination of both. We expected a higher hair density at harbour seal vibrissal pads than on the trunk. We analysed hair density and distribution as well as hair and skin structure on the back, on top of the head and on the mystacial, supraorbital and rhinal vibrissal pads of four harbour seals using light and electron microscopy.
Figure 2.
Mammalian pilosebaceous unit (adapted with permission from Pabst et al. [17]). The typical mammalian pilosebaceous unit or hair bundle contains one broad guard hair along with a variable number (here three) of smaller underhairs, each hair rising from its own follicle. All follicles open into one common pilary canal along with the openings of sweat and sebaceous glands.
2. Methods
2.1. Samples
Investigations were carried out on tissue samples of four female harbour seal pups that had died of natural causes before weaning in the German North Sea. Samples were taken during autopsy performed by the Institute for Terrestrial and Aquatic Wildlife Research of the University of Veterinary Medicine Hannover, Büsum, Germany. Owing to the condition of the carcasses, the samples had different sizes (approx. 4–100 cm2) and shapes. Samples were kept frozen at −18°C to −23°C until examination.
2.2. Wet preparation and analysis of hair density, hair size and skin structure
After defrosting, the skins were rinsed with water to remove blood and other residues, dried and sheared with a hair trimmer (NE3150 Smart, Remington, Ellwangen, Germany). Afterwards, they were shaved with disposable double blade razors, leaving hair stumps of less than 1 mm length. Finally, the samples were rinsed and dried again to remove trimmed hairs.
Photographs of 4.05 × 2.71 mm size were taken from each sample with a digital single lens reflex camera (Nikon D3000, Düsseldorf, Germany) through a binocular microscope with fourfold magnification by means of an attached microscope adapter (Photo-Adapter 23 mm, Bresser, Rhede/Westfalen, Germany, combined with T2 Adapter for Nikon, Delamax, Berlin, Germany). For size calibration, a caliper gauge was photographed through the same optical apparatus.
We analysed samples from the trunk, the mystacial, supraorbital and rhinal vibrissal pad and the top of the head. Owing to the size and condition of the samples, not all body parts could be analysed in all individuals. Numbers of analysed samples per individual and body part are given in table 1.
Table 1.
Number and origin of tissue samples.
| body part | number of seals sampled | analysed sections/body part | analysed sections/body part: total |
|---|---|---|---|
| trunk | 4 | 9 | 36 |
| mystacial vibrissal pad | 4 | 9 | 36 |
| supraorbital vibrissal pad | 1 | 9 | 9 |
| rhinal vibrissal pad | 2 | 9 | 18 |
| top of head | 1 | 4 | 4 |
Hair diameter of the circular underhairs, width and thickness (shortest axis of the ellipsoid cross section) of the flattened hair types (guard hairs and ‘intermediate hairs’ as defined below) as well as width of skin lobes were measured in the digital images using the software ImageJ v. 1.45s (National Institute of Health, Bethesda, MD).
For analysis of hair density, hairs were counted in nine 1.5 × 1.5 mm sections of each sample using ImageJ (see above).
2.3. Preparation of thin sections
Frozen tissue samples were fixed in 4% formaldehyde in phosphate-buffered saline for 48 h, and afterwards dehydrated in alcohol with progressively increasing concentrations (70%, 80%, 90%, 96%, 100%). Afterwards, the samples were cleared in xylol, infiltrated with paraffin for 36 h in a tissue-processing apparatus (Histokinette) and finally embedded in paraffin. The hardened samples were cut into 5 µm thick sections by means of a rotary microtome, and sections were mounted on glass microscope slides. Sections were stained with AZAN trichrome stain and mounted with mounting medium Pertex (Histolab, Gothenburg, Sweden).
Images of the cross sections were taken with a Tucsen v. 5.0 camera and the software TSView v. 6.2.3.3 (Tucsen Imaging Technology Co., Ltd, Fujian, China), adapted to a universal photo microscope (Zeiss, Oberkochen, Germany).
2.4. Statistical analysis
Statistical analyses were conducted using SPSS 20.0. Statistical significance was determined using a one-way ANOVA with a post hoc Bonferroni correction.
3. Results
3.1. Hairs
Hairs were clustered in approximately equally distributed bundles in all investigated samples. Density of hair bundles per unit area was similar on trunk, mystacial and supraorbital vibrissal pads (8.2 ± 1.2 bundles mm−2 on the trunk, 8.7 ± 1.4 bundles mm−2 on the vibrissal pads), but significantly higher around the rhinal vibrissae (10.5 ± 1.1 bundles mm−2) than on the trunk (
) or the vibrissal pads (p = 0.001). In addition, total hair density was significantly higher at the rhinal vibrissal pads (46.4 ± 4.3 hairs mm−2) than at the other vibrissal pads (35.9 ± 7.1 hairs mm−2; 
) or on the trunk (29.8 ± 3.6 hairs mm−2; 
). Furthermore, hair density at the mystacial and supraorbital vibrissal pads was significantly higher than on the trunk (
).
The composition of hair bundles differed significantly between the investigated body sites. Hair bundles on the back and on top of the head of the animals each contained one guard hair along with two to four underhairs (figure 3a,b), corresponding to the typical mammalian hair bundle. By contrast, at the mystacial and supraorbital vibrissal pads, the hair bundles showed a totally different composition consisting of one broad guard hair along with two to four thinner guard hairs, which we named ‘intermediate hairs’. Underhairs were extremely reduced or lacking. Hair bundles at the supraorbital vibrissal pads comprised one guard hair with two to three intermediate hairs along with one single underhair at the utmost. At the mystacial vibrissal pads, hair bundles consisted of one guard hair along with three to four intermediate hairs (figure 3c–f and the electronic supplementary material, figure S1). In only two individuals were underhairs found at the vibrissal pads at all. Around the rhinal vibrissae, hair bundles contained one guard hair and one to two intermediate hairs along with two to three underhairs, thereby, together with the increased density of hair bundles, constituting the highest total hair density of all investigated body regions.
Figure 3.
Hair bundles in the skin of a harbour seal. (a) Seal's back: hairs are arranged in bundles of one coarse, flattened guard hair (red arrow) with two to four thin underhairs (green arrows). (b) Cross section through pilary canals (purple) on the seal's back: hair bundles consist of one broad guard hair (red arrow) and four to five fine underhairs (green arrows). (c) Vibrissal pad centre: hair bundles (red circle) consist of one broad guard hair along with three to four intermediate hairs. (d) Cross section through a hair bundle at the centre of a vibrissal pad, cut below the common pilary canal. The hair bundle contains one broad guard hair (red arrow) and four intermediate hairs (orange arrows), each in a single follicle (purple). (e) Vibrissal pad close to nare: hair bundles (red circle) consist of one broad guard hair and four to five intermediate hairs. (f) Cross section through a hair bundle close to the nare at the seal's vibrissal pad, cut below the common pilary canal. The hair bundle contains one broad guard hair (red arrow) and five intermediate hairs (orange arrows), each in a single follicle (purple). The light purple structures beside the hair follicles (d,f) are sebaceous and sweat glands.
The different numbers of hairs per bundle along with the differences in hair bundle density resulted in highly differing hair densities at the investigated body parts, which are shown in figure 4.
Figure 4.
Hair density in harbour seals. Density of hair bundles (white), guard hairs (vertical stripes), intermediate hairs (black), underhairs (diagonal stripes) and total hair density (grey) on the trunk, mystacial and rhinal vibrissal pads, along with standard deviation (black bars). Density of hair bundles at the rhinal vibrissae was significantly higher than on the trunk (
) or the mystacial vibrissal pads (p = 0.001). Total hair density was highest at the rhinal vibrissal pads too, and highly significantly higher than on the trunk or the mystacial vibrissal pads (
), whereas density of intermediate hairs was highest at the mystacial vibrissal pads (
).
Underhairs had a circular cross section with a mean diameter of 0.020 ± 0.006 mm (n = 57). By contrast, guard hairs in all body parts as well as intermediate hairs were strongly flattened, as typical in pinnipeds [22]. The width of the guard hairs at the vibrissal pads (0.127 ± 0.022 mm; n = 49) corresponded to the guard hair width at the trunk (0.120 ± 0.024 mm; n = 52; p = 1.0). The intermediate hairs were approximately half as broad as the guard hairs (0.067 ± 0.016 mm; n = 93; 
), but still three times broader than the underhairs (
).
Thickness (shortest axis of the ellipsoid cross section) of the guard hairs at the vibrissal pads (0.019 ± 0.006 mm; n = 14) and guard hairs on the trunk (0.020 ± 0.005 mm; n = 11) did not differ significantly (p = 1.0) and corresponded to underhair diameter (p = 1.0). However, all guard hairs were significantly thicker than the intermediate hairs (0.013 ± 0.004 mm; n = 25; 
). Nevertheless, the flatness ratio (width-to-thickness ratio) did not differ significantly between guard hairs on the trunk (6.28 ± 2.50), on the vibrissal pads (8.40 ± 3.12) and intermediate hairs (6.53 ± 1.80; p > 0.1).
3.2. Skin
The seals' skin possessed a scale-like structure, consisting of soft flexible overlapping lobes that covered the hair follicles and lower parts of the hair shafts, as shown in figure 5. The lobes were aligned parallel to the flow direction, like the hairs, and were significantly broader on the trunk (0.85 ± 0.37 mm; n = 41) than on the vibrissal pads (0.58 ± 0.20 mm; n = 41; 
).
Figure 5.
Skin surface structure of harbour seals. Sections of 1.5 × 1.5 mm, shaved. (a) Trunk, wet specimen: the soft lobes of different size are clearly visible with hair stumps in between. (b) Trunk, squash specimen: the scale-like arrangement of the soft lobes is clearly visible as well as the linear alignment. (c) Top of head: the alignment of the lobes is more compact than on the trunk. (d) Vibrissal pad: the different-sized lobes are visible as well as the sheared hairs emerging between the lobes.
4. Discussion
Our hypothesis of a higher hair density on the vibrissal pads than on the trunk of harbour seals was confirmed in this study. The analysed samples originated from preweaned pups that most likely died before the first postnatal moult. In adults, underhairs are extremely reduced or even totally lost, therefore, the differences in hair density between trunk and vibrissal pads will very probably be even larger in adults than in the present study. Scheffer [20], for example, counted a mean value of 21.2 hairs mm−2 in two adult harbour seals. In this study, at the mystacial and supraorbital vibrissal pads, hair density was increased exclusively by a higher number of hairs per bundle. At the rhinal vibrissae, the density of bundles per unit area was increased additionally, which resulted in the highest total hair density. This surprising result sheds new light on these short, thin and immobile single vibrissae above each nare that have been regarded of minor significance with their exact function still unknown.
Totally unexpected was the fur composition at the vibrissal pads, namely the grouping of up to five guard hairs with different sizes per bundle. While the grouping of hairs in bundles of one guard hair with several underhairs in mammalian fur was known [19], the arrangement of four to five guard hairs in a bundle has not been described so far, nor has the presence of different-sized guard hairs. Hair patterns in mammals have been the subject of many investigations, starting with De Meijere [19], who defined the model of the ‘basic trio’ consisting of one large hair between two small hairs, each with its own follicle but emerging from one corporate opening. The typical mammalian hair bundle was also reported for several aquatic mammalian species and pinnipeds in particular [20,23–26]. However, all studies on hair patterns, in mammals in general as well as in aquatic mammals and pinnipeds specifically, describe exclusively the pattern of hair bundles consisting of one single guard hair alone or along with a variable number of underhairs (0 up to 89 [27]), emerging from one pilary canal. One study on American minks reports hair bundles consisting exclusively of underhairs, lacking a guard hair [18].
Each bundle at the vibrissal pads contained only one guard hair as broad as the guard hairs on the trunk. The other guard hairs, which we named ‘intermediate hairs’, were about half as broad as the regular guard hairs but about three times as broad as underhairs. This indicates that the intermediate hairs have developed from underhairs in the course of the adaptation to the aquatic environment. Pinniped guard hairs are coarse, stiff and slightly curved with a flattened cross section [22], which makes the caudally aligned hairs lie flat on the surface in wet state. The same applies to the intermediate hairs. Although their width was only half that of guard hairs, their flatness, i.e. width-to-thickness ratio, was equal to guard hair flatness.
If the hairs around the vibrissae play any role in thermal insulation, the question arises why thermal insulation in these areas is increased by a higher number of coarse broad flat hairs instead of fine underhairs? Heat may be transferred through fur by conduction along the individual fibres, conduction through the fluid entrapped in the fur, and natural and forced convection of the fluid pervading the fur [28]. Frisch et al. [14] assumed on the one hand a reduced thermal insulating value of guard hair compared with underhair in harp seals (Pagophilus groenlandicus Erxleben, 1777), but stated on the other hand that guard hair reduces heat loss by forced convection. While the insulating value of underhair lies in the reduction of conductive and convective heat loss owing to a stagnant layer of air or water between the hairs, an insulating value of a compact smooth layer of broad flattened hairs that keeps the water flow away from the skin is plausible too. The vibrissal pads, along with the entire face region, are the most anterior part of a seal gliding through the water. Dynamic pressure will compress the fur on the vibrissal pads and would drastically reduce any insulating effect of a water layer retained by underhairs. A smooth compact layer of broad flat hairs (guard and intermediate hairs), by contrast, will divert the water stream and reduce contact with the vibrissal pad skin, thereby reducing heat loss by forced convection.
It is conceivable that the high abundance of guard and intermediate hairs around the vibrissae has further functions besides heat retention. First, the coarse stiff hair provides protection against mechanical injuries [29,30], which is all the more important at the sensitive vibrissal pads. Additionally, the flattened structure of guard hairs along with their alignment flat on the skin is generally assumed to reduce friction on the body surface of seals [30,31]. Because drag reduction is advantageous on the entire body surface of an aquatic mammal and not only on the face region, the question arises why harbour seals would reduce drag friction in particular at the vibrissae. Harbour seal vibrissae are highly sensitive for the detection of water movements [32–34], enabling the animals to follow hydrodynamic trails [35]. During trail following, the vibrissae remain erected transverse or even nearly opposed to the swimming direction in a stable position, owing to their flattened and undulated shape, which reduces vortex-induced vibrations [36]. The high amount of guard and intermediate hairs around the vibrissae potentially plays a role in stabilizing the vibrissae by reducing turbulence at the boundary layer in these areas.
The assumption of reduced drag by smooth surfaces is at first glance opposed to the theory of drag reduction by rough surfaces, well known in shark skin [37]. However, the scales on the leading sides of the shark's body, such as the rostrum and the leading edges of the fins, have smooth surfaces and do not possess ridges [38]. A smooth surface on the snout and around the seals' vibrissae, the first body parts of the seal that contact the water when swimming, appears to have evolved convergently to the respective surfaces in sharks. The smooth surface on the snout is likely one of several mechanisms of drag reduction in seals that require further investigation. A further question that is currently under investigation is the abundance of this new or a comparable hair type in other species, in particular in other phocids.
The role of the remarkable scale-like structure of the skin (figure 5) is not known. It might play a role in drag reduction in one or several ways. The scale-like soft lobes will most probably influence the alignment and mechanical behaviour of the hairs in the flow. The lobes might also directly influence a proportion of water flow that passes through the fur. Both the hairs and the lobes cover each other (the lower parts of the hairs are covered by the lobes, whereas the lobes are covered by the hairs), thereby constituting a compliant composite surface that needs to be investigated further. Compliant surfaces have been considered a possible means of drag reduction in dolphins. While earlier conjectures that their compliant skin might enable dolphins to maintain a laminar boundary layer and drastically reduce drag have been disproved [39], the skin may still modulate their turbulent boundary layer to avoid or delay detachment [40,41]. Choi et al. [42] measured drag in slender bodies of revolution with compliant versus rigid surfaces in a water tunnel under turbulent conditions. They found turbulent drag reduction of up to 7% compared with rigid surfaces at flow speeds of 2–6 m s−1, which includes the range of harbour seal swimming speeds [35,43]. Although not directly comparable, the function of the scale-like skin structure and its interaction with the fur leave space for interpretation and call for further investigation.
Williams & Kooyman [43] measured drag in harbour seals using a force balance while towing the animals, and video recordings of gliding animals. Drag could, depending on body posture, be exceptionally low, with drag coefficients based on frontal area between 0.038 and 0.088. These values were lower than found on a number of technical bodies such as submarines and torpedo shapes [43]. Lower drag coefficients were found in gliding seals when compared with towed animals, confirming a significant effect of body posture. However, the relative contributions of the harbour seal's body shape and its surface structure, consisting of skin and fur, to drag reduction have not yet been determined.
5. Summary and conclusion
Hair density around the harbour seals' vibrissae was significantly higher than on the trunk with highest densities at the rhinal vibrissae. Furthermore, the fur structure at all vibrissal pads differed from all mammalian hair patterns described until today: the hair bundles contained one broad guard hair along with up to four thinner guard hairs, defined as ‘intermediate hairs’, constituting a new hair type that presumably evolved from underhairs in the course of the adaptation to the aquatic environment. Beside of the (potential) reduction in heat loss by forced convection at the heated vibrissal regions, the dense covering with coarse stiff guard and intermediate hairs presumably has further functions, in particular, drag reduction. The seals' skin surface on all body parts consisted of soft flexible overlapping lobes, covering the hair follicles and lower parts of the hair shafts. Skin lobes and hairs were aligned parallel to the flow direction and presumably have an analogous function to fish scales or shark denticles by reducing frictional drag.
Supplementary Material
Acknowledgements
We thank Frauke Winzer from the anatomical institute for preparing the histological sections and Marcus Frank from the Centre for Electron Microscopy for preparing the electron microscope images.
Funding statement
This study was supported by a grant from the VolkswagenStiftung to G.D. and the Landesgraduiertenförderung Mecklenburg-Vorpommern to N.E.
References
- 1.Dehnhardt G, Mauck B, Hyvärinen H. 1998. Ambient temperature does not affect the tactile sensitivity of mystacial vibrissae in harbour seals. J. Exp. Biol. 201, 3023–3029. [DOI] [PubMed] [Google Scholar]
- 2.Green BG. 1977. Effects of skin temperature on vibrotactile sensitivity. Percept. Psychophys. 21, 243–248. ( 10.3758/bf03214234) [DOI] [Google Scholar]
- 3.Gescheider GA, Thorpe JM, Goodarz J, Bolanowski SJ. 1997. The effects of skin temperature on the detection and discrimination of tactile stimulation. Somatosens. Mot. Res. 14, 181–188. ( 10.1080/08990229771042) [DOI] [PubMed] [Google Scholar]
- 4.Mills AW. 1956. Finger numbness and skin temperature. J. Appl. Physiol. 9, 447–450. [DOI] [PubMed] [Google Scholar]
- 5.Käkelä R, Hyvärinen H. 1993. Fatty acid composition of fats around the mystacial and superciliary vibrissae differs from that of blubber in the Saimaa ringed seal (Phoca hispida saimensis). Comp. Biochem. Physiol. B 105, 547–552. ( 10.1016/0305-0491(93)90087-l) [DOI] [PubMed] [Google Scholar]
- 6.Mauck B, Eysel U, Dehnhardt G. 2000. Selective heating of vibrissal follicles in seals (Phoca vitulina) and dolphins (Sotalia fluviatilis guianensis). J. Exp. Biol. 203, 2125–2131. [DOI] [PubMed] [Google Scholar]
- 7.Marshall CD, Amin H, Kovacs KM, Lydersen C. 2006. Microstructure and innervation of the mystacial vibrissal follicle–sinus complex in bearded seals, Erignathus barbatus (Pinnipedia: Phocidae). Anat. Rec. A 288, 13–25. ( 10.1002/ar.a.20273) [DOI] [PubMed] [Google Scholar]
- 8.Hyvärinen H, Palviainen A, Strandberg U, Holopainen IJ. 2009. Aquatic environment and differentiation of vibrissae: comparison of sinus hair systems of ringed seal, otter and pole cat. Brain Behav. Evol. 74, 268–279. ( 10.1159/000264662) [DOI] [PubMed] [Google Scholar]
- 9.Hyvärinen H, Katajisto H. 1984. Functional structure of the vibrissae of the ringed seal (Phoca hispida Schr.). Acta Zool. Fenn. 171, 27–30. [Google Scholar]
- 10.Hyvärinen H. 1989. Diving in darkness: whiskers as sense organs of the ringed seal (Phoca hispida saimensis). J. Zool. 218, 663–678. ( 10.1111/j.1469-7998.1989.tb05008.x) [DOI] [Google Scholar]
- 11.Erdsack N, Dehnhardt G, Hanke W. 2014. Thermoregulation of the vibrissal system in harbor seals (Phoca vitulina) and Cape fur seals (Arctocephalus pusillus pusillus). J. Exp. Mar. Biol. Ecol. 452, 111–118. ( 10.1016/j.jembe.2013.12.011) [DOI] [Google Scholar]
- 12.Scholander PF, Walters V, Hock R, Irving L. 1950. Body insulation of some arctic and tropical mammals and birds. Biol. Bull. 99, 225–236. ( 10.2307/1538740) [DOI] [PubMed] [Google Scholar]
- 13.Kvadsheim PH, Aarseth JJ. 2002. Thermal function of phocid seal fur. Mar. Mamm. Sci. 18, 952–962. ( 10.1111/j.1748-7692.2002.tb01084.x) [DOI] [Google Scholar]
- 14.Frisch J, Øritsland NA, Krog J. 1974. Insulation of furs in water. Comp. Biochem. Physiol. A 47, 403–410. ( 10.1016/0300-9629(74)90002-4) [DOI] [PubMed] [Google Scholar]
- 15.Irving L, Krog J. 1955. Temperature of skin in the Arctic as a regulator of heat. J. Appl. Physiol. 7, 355–364. [DOI] [PubMed] [Google Scholar]
- 16.Tarasoff FJ, Fisher HD. 1970. Anatomy of the hind flippers of two species of seals with reference to thermoregulation. Can. J. Zool. 48, 821–829. ( 10.1139/z70-144) [DOI] [Google Scholar]
- 17.Pabst DA, Rommel SA, McLellan WA. 1999. The functional morphology of marine mammals. In Biology of marine mammals (eds Reynolds JE, III, Rommel SA.), pp. 15–72. Washington, DC: Smithsonian Institution Press. [Google Scholar]
- 18.Kondo K, Vanek M, Rasmussen PV, Blomstedt L. 2000. The beauty of mink pelage observed with SEM. J. Grad. Agric. Hokkaido Univ. 70, 1–8. [Google Scholar]
- 19.De Meijere JCH. 1894. Über die Haare der Säugethiere, besonders über ihre Anordnung. Gegenbaur‘s Morphologisches Jahrbuch 21, 312–424. [Google Scholar]
- 20.Scheffer VB. 1964. Hair patterns in seals (Pinnipedia). J. Morphol. 115, 291–304. ( 10.1002/jmor.1051150211) [DOI] [PubMed] [Google Scholar]
- 21.Scheffer VB. 1962. Pelage and surface topography of the northern fur seal. Washington DC: U. S. Fish and Wildlife Service. [Google Scholar]
- 22.Bergersen B. 1931. Beiträge zur Kenntnis der Haut einiger Pinnipedier, unter besonderer Berücksichtigung der Haut der Phoca groenlandica. Skrifter utgitt av Det Norske Videnskaps—Akademi i Oslo 5, 1–179. [Google Scholar]
- 23.Montagna W, Harrison RJ. 1957. Specializations in the skin of the seal (Phoca vitulina). Am. J. Anat. 100, 81–113. ( 10.1002/aja.1001000105) [DOI] [PubMed] [Google Scholar]
- 24.Ling JK. 1965. Hair growth and moulting in the southern elephant seal, Mirounga leonina (Linn.). In Symposium on the biology of the skin and hair growth (eds Lyne AG, Short BF.), pp. 525–544. Sydney, Australia: Angus and Robertson. [Google Scholar]
- 25.Sokolov W. 1962. Adaptations of the mammalian skin to the aquatic mode of life. Nature 195, 464–466. ( 10.1038/195464a0) [DOI] [Google Scholar]
- 26.Liwanag HEM, Berta A, Costa DP, Abney M, Williams TM. 2012. Morphological and thermal properties of mammalian insulation: the evolution of fur for aquatic living. Biol. J. Linn. Soc. 106, 926–939. ( 10.1111/j.1095-8312.2012.01900.x) [DOI] [Google Scholar]
- 27.Scheffer VB, Johnson AM. 1963. Molt in the northern fur seal. Washington, DC: U.S. Fish and Wildlife Service. [Google Scholar]
- 28.Hammel HT. 1955. Thermal properties of fur. Am. J. Physiol. 182, 369–376. [DOI] [PubMed] [Google Scholar]
- 29.Sokolov W. 1960. The skin structure in Pinnipedia of the U.S.S.R. fauna. J. Morphol. 107, 285–296. ( 10.1002/jmor.1051070304) [DOI] [Google Scholar]
- 30.Ling JK. 1970. Pelage and molting in wild mammals with special reference to aquatic forms. Q. Rev. Biol. 45, 16–54. ( 10.1086/406361) [DOI] [PubMed] [Google Scholar]
- 31.Noback CR. 1951. Morphology and phylogeny of hair. Ann. N.Y. Acad. Sci. 53, 476–492. ( 10.1111/j.1749-6632.1951.tb31950.x) [DOI] [PubMed] [Google Scholar]
- 32.Miersch L, Hanke W, Wieskotten S, Hanke FD, Oeffner J, Leder A, Brede M, Witte M, Dehnhardt G. 2011. Flow sensing by pinniped whiskers. Phil. Trans. R. Soc. B 366, 3077–3084. ( 10.1098/rstb.2011.0155). [DOI] [PMC free article] [PubMed] [Google Scholar]
- 33.Dehnhardt G, Mauck B, Bleckmann H. 1998. Seal whiskers detect water movements. Nature 394, 235–236. ( 10.1038/28303) [DOI] [Google Scholar]
- 34.Wieskotten S, Mauck B, Miersch L, Dehnhardt G, Hanke W. 2011. Hydrodynamic discrimination of wakes caused by objects of different size or shape in a harbour seal (Phoca vitulina). J. Exp. Biol. 214, 1922–1930. ( 10.1242/jeb.053926) [DOI] [PubMed] [Google Scholar]
- 35.Dehnhardt G, Mauck B, Hanke W, Bleckmann H. 2001. Hydrodynamic trail-following in harbor seals (Phoca vitulina). Science 293, 102–104. ( 10.1126/science.1060514) [DOI] [PubMed] [Google Scholar]
- 36.Hanke W, Witte M, Miersch L, Brede M, Oeffner J, Michael M, Hanke F, Leder A, Dehnhardt G. 2010. Harbor seal vibrissa morphology suppresses vortex-induced vibrations. J. Exp. Biol. 213, 2665–2672. ( 10.1242/jeb.043216) [DOI] [PubMed] [Google Scholar]
- 37.Reif WE, Dinkelacker A. 1982. Hydrodynamics of the squamation in fast swimming sharks. Neues Jahrbuch für Geologie und Palaeontologie. Abhandlungen 164, 184–187. [Google Scholar]
- 38.Reif WE. 1985. Morphology and hydrodynamic effects of the scales of fast swimming sharks. Prog. Zool. 30, 483–485. [Google Scholar]
- 39.Fish FE, Legac P, Williams TM, Wei T. 2014. Measurement of hydrodynamic force generation by swimming dolphins using bubble DPIV. J. Exp. Biol. 217, 252–260. ( 10.1242/jeb.087924) [DOI] [PubMed] [Google Scholar]
- 40.Fish FE. 2006. The myth and reality of Gray's paradox: implication of dolphin drag reduction for technology. Bioinspir. Biomim. 1, R17–R25. ( 10.1088/1748-3182/1/2/r01) [DOI] [PubMed] [Google Scholar]
- 41.Fish FE, Lauder GV. 2006. Passive and active flow control by swimming fishes and mammals. Annu. Rev. Fluid Mech. 38, 193–224. ( 10.1146/annurev.fluid.38.050304.092201). [DOI] [Google Scholar]
- 42.Choi KS, Yang X, Clayton BR, Glover EJ, Atlar M, Semenov BN, Kulik VM. 1997. Turbulent drag reduction using compliant surfaces. Proc. R. Soc. Lond. A 453, 2229–2240. ( 10.1098/rspa.1997.0119). [DOI] [Google Scholar]
- 43.Williams TM, Kooyman GL. 1985. Swimming performance and hydrodynamic characteristics of harbor seals Phoca vitulina. Physiol. Zool. 58, 576–589. [Google Scholar]
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