Thermal insulation design bioinspired by microstructure study of penguin feather and polar bear hair

Thermal insulation design bioinspired by microstructure study of penguin feather and polar bear hair

Acta Biomaterialia xxx (xxxx) xxx Contents lists available at ScienceDirect Acta Biomaterialia journal homepage: www.elsevier.com/locate/actabiomat ...

9MB Sizes 0 Downloads 3 Views

Acta Biomaterialia xxx (xxxx) xxx

Contents lists available at ScienceDirect

Acta Biomaterialia journal homepage: www.elsevier.com/locate/actabiomat

Full length article

Thermal insulation design bioinspired by microstructure study of penguin feather and polar bear hair Sara Metwally, Sara Martínez Comesaña, Mateusz Zarzyka, Piotr K. Szewczyk, Joanna E. Karbowniczek, Urszula Stachewicz ⇑ International Centre of Electron Microscopy for Materials Science, Faculty of Metals Engineering and Industrial Computer Science, AGH University of Science and Technology, Al. A. Mickiewicza 30, 30-059 Kraków, Poland

a r t i c l e

i n f o

Article history: Received 24 October 2018 Received in revised form 2 April 2019 Accepted 11 April 2019 Available online xxxx Keywords: Fibers Keratin Feather Hair Porosity Polar bear Penguin

a b s t r a c t Nature is an amazing source of inspiration for the design of thermal insulation strategies, which are key for saving energy. In nature, thermal insulation structures, such as penguin feather and polar bear hair, are well developed; enabling the animals’ survival in frigid waters. The detailed microscopy investigations conducted in this study, allowed us to perform microstructural analysis of these thermally insulating materials, including statistical measurements of keratin fiber and pore dimensions directly from high resolution Scanning Electron Microscope (SEM) images. The microscopy study revealed many similarities in both materials, and showed the importance of their hierarchically-organized porous structure. Finally, we propose the schematic configuration of a thermally-insulating structure, based on the penguin feather and polar bear hair. These optimized thermal-insulator systems indicate the road maps for future development, and new approaches in the design of material properties. Statement of significance We present the first detailed comparison of microstructures of penguin feather and polar bear hair for designing optimum thermal insulation properties. This unique study involves the measurement of the sizes of pores and fibers of these two keratin-based materials, including the investigation of their 3D arrangements. We revealed porosity interconnection, especially in polar bear hair, which is one of the key designs exhibited by thermal insulation materials. Ó 2019 Acta Materialia Inc. Published by Elsevier Ltd. All rights reserved.

1. Introduction Multifunctional properties of natural materials have been studied over many years. Recently, increasing attention has focused on thermal insulation properties [1], bioinspired by feather, hair, fur or wool [2–5], which are all keratin-based materials. Keratin is one of the most studied structural proteins, similar to collagen [6], and it is an important building block found in many natural materials, which display unique material properties. Keratin is assembled by keratinocytes that die after keratin production; leading to keratin-based materials being porous and having tile structures, with overlapping layers densely stacked up together at the outer surfaces [7]. Keratin itself is considered a composite material of fibers that are made of crystalline keratin and a reinforced poly-

mer layer, which is amorphous keratin [8]. Keratin can be found in many places, for example in hooves and horns [9–11]. Importantly, in keratin-based materials the mechanical strength decreases with increased water content [12], but keratin is very effective in maintaining tension, for example, wool [5] and hooves [13,14]. Pioneering research on keratin was done on the structure of Rhinoceros horn [15], and was followed by further investigations, including Toucan beak [16]. Additionally, keratin is of great interest in the field of peptide-chemistry for developing water-soluble keratin polypeptides from sheep wool [17]. Most keratin-based materials are porous [18], which is a key construction strategy for lightweight materials with high mechanical strength. The microstructure and porosity provide not only a mechanical strength, but also enhanced aerodynamic properties [19]. Feather is one of the most common light and aerodynamic structures that has been widely studied in terms of its mechanical properties [20,21],

⇑ Corresponding author. E-mail address: [email protected] (U. Stachewicz). https://doi.org/10.1016/j.actbio.2019.04.031 1742-7061/Ó 2019 Acta Materialia Inc. Published by Elsevier Ltd. All rights reserved.

Please cite this article as: S. Metwally, S. Martínez Comesaña, M. Zarzyka et al., Thermal insulation design bioinspired by microstructure study of penguin feather and polar bear hair, Acta Biomaterialia, https://doi.org/10.1016/j.actbio.2019.04.031

2

S. Metwally et al. / Acta Biomaterialia xxx (xxxx) xxx

super-hydrophobicity [22], and other properties such as acoustic attenuation [23]. For many animals, keeping a constant body temperature is the key to survival, which is achieved by covering the body with naturally-porous insulating materials [1]. The aim of insulation is to retain body heat and maintain stable body temperature. One of the best examples is polar bear hair, where the porosity of hair helps them to convert sunlight energy into thermal energy through a photothermal conversion process [24]. The polar bear has been the bioinspiration for synthetic materials with excellent UV absorption properties [5]. There are attempts at biomimicking thermal conductivity by aligning pore structures [3], where infrared light reflectance was achieved. Another example is penguin feathers, which have inspired anti-icing structures [25]. Many different types of penguins’ feathers are well studied but only a small number of studies have examined the microstructure of polar bear hair, and fewer have compared both microstructures. Therefore, this study evaluated the porous structure of two species: penguins and polar bears. Both animals are able to swim in cold streams and survive in very low temperatures. Penguin feather and polar bear hair prevent penetration of cold seawater to the skin and play an insulating role. As the afterfeather has a branched structure, thermal insulation in penguin feather is related not only to the internal structure but also to the geometric arrangements [26]. The geometric arrangements and material properties define the water spreading abilities [27], as the branching and surface roughness increases the feather’s ability to capture air and decreases the surface free energy of materials [28]. Microscopy investigations are important for understanding the designs that have been already optimized by nature. We studied the detailed microstructure of penguin feather and polar bear hair to show the importance of their 3D structure and hierarchical approach by comparing their submicron structure. Both materials, penguin feather and polar bear hair, are keratin-based but with different molecular arrangements. Hair is usually composed of alphakeratin, with coiled-coil molecular structure whereas feathers are built out of beta-keratin sheets [8]. Although these structures are different, their microstructures have many similarities such as

interconnected porosity, which indicates the importance of porosity in adaptive thermal insulation. We conclude our analysis by discussing the similarities between these structures to understand the strategies for the design of the insulating material structure. 2. Materials and methods The feather samples were taken from African penguins (Spheniscusdemersus). The samples were obtained from the Wrocław Zoo and Płock Zoo in Poland, collected from the ground (see examples in Fig. 1). Classification of penguin feather samples was based on previous descriptions [29]. The polar bear (Ursus maritimus) hair samples were obtained from various locations. Samples cut during a medical check-up were obtained from Warsaw Zoo, and samples collected from the ground were from the Zoo am Meer in Germany, Polar Bear Habitat of Cochrane in Canada, and Highland Wildlife Park, Kincraig in Scotland, UK. Cross-sections of each sample were then prepared by cutting with a sharp scalpel and freeze-fractured to reveal undeformed surfaces and longitudinal or transverse cross-sections. All the samples were coated with 3 nm gold layer using a rotary-pump sputter coater (Q150RS, Quorum Technologies, UK) and imaged using scanning electron microscopy (SEM, Merlin Gemini II, Zeiss, Germany). The diameters of pores and fibers were measured from SEM images using ImageJ (J1.46r, Fiji, USA). Approximately 100 measurements per histogram were performed, with the error calculated as a standard deviation. 3. Results and discussion 3.1. Penguin feathers The feather is a complex structure. The structure varies between penguin species and between different parts of a penguin’s body [30], as it serves many functions including thermal insulation and water resistance. The two main types of feather are shown in Fig. 1: contours that cover the entire body, and down feathers (also called afterfeather or plumulaceous) that lie just beneath the contours and insulate the body. Penguin feather, sim-

Fig. 1. Four samples of penguin feather A) ventral contour with afterfeather (plumulaceous), B) dorsal C) ventral primary and D) head contour.

Please cite this article as: S. Metwally, S. Martínez Comesaña, M. Zarzyka et al., Thermal insulation design bioinspired by microstructure study of penguin feather and polar bear hair, Acta Biomaterialia, https://doi.org/10.1016/j.actbio.2019.04.031

S. Metwally et al. / Acta Biomaterialia xxx (xxxx) xxx

ilarly to other birds’ feathers, is hierarchically ordered with a branched structure built around the main shaft, with a top part called pennaceous. For this study we selected a few examples of penguin feather: ventral, dorsal and head (see examples in Fig. 1). The feathers from penguins’ heads are usually puffier with down feather rather than the ventral primary feather (Fig. 1C and 1D), so penguins can raise and lower a crest depending on their mood [30]. All feathers consist of a shaft with calamus, which is located closer to the skin of birds. With regards to the overall structure, barbs exist from rachis, and barbules exist from barbs. From barbules, hamuli protrude, which are also called hooks [31] (see Fig. 2). The examples in Fig. 1A show ventral feather with afterfeather, which is placed usually at the calamus. Ventral contour feathers with plumulaceous afterfeathers are connected by a long, thin hyporachis at the top of the calamus, very close to the base of the rachis. The contour feathers have a broad and flattened rachis. Fig. 2 also shows the main difference in the organization of barb and barbule in pennaceous and plumulaceus part of the ventral feather. The barb sizes are between 10 and 20 mm (see example in Fig. 2B), and the diameter of barbules reaches a few microns. The barb surface in ventral feather is grooved and wrinkled, but the surface of rachis is also porous. In Fig. 3 we present an example of head contour feather with the average pore diameter on the rachis reaching 0.19 ± 0.05 mm. The surface roughness and branched organization of the feather structure make it an excellent hydrophobic and ice-phobic surface [25], as the air can be easily trapped in this type of surface roughness to decrease the surface free energy [28,32]. The controlled surface roughness is often used in synthetic materials as a tool to control wetting properties [32,33]. The feather is hierarchically constructed of the primary barb, which is supported by rachis, with the main cortex based on the cellular core. The porosity inside the main shaft increases gradually

3

as shown in Fig. 4, from the edges of the cortex to the center, and from the calamus, which is located at the bottom part of the barb, to the tip. In Fig. 4A we present a longitudinal cross-section, clearly showing the calamus, rachis, and transition between these two structures. The calamus is divided into large empty sections, separated by layered keratin cuticula membranes (Fig. 4E) with a distance of approximately 230 mm, which decreases as it approaches the rachis. The rachis is a well-organized porous structure, with an average internal pore diameter of 11 ± 4 mm. Note that the compressed pores between the substantia fibrosa and the foam, visible on the left side in Fig. 4B, are called the septum. In the fractured samples, the delamination is visible at the cortex showing the cuticula layers, next to the substantia fibrosa, with aligned keratin fibers along the shaft. The foam pores are isotropic, as observed in Fig. 4B in the longitudinal cross-sections, with a close-up showing fibers matted together (Fig. 4C). The cellular part of the rachis is covered with layers of substantia fibrosa, which consists of aligned keratin fibers forming bundles. External layers are built of cuticula, with keratin fibers arranged at a different angle for each layer – creating a lamellar structure that is 1–2 mm thick. The transverse cross-section in Fig. 5, shows the cellular core, the pores being very similar in shape and size to the foam structure in the rachis (Fig. 4B). The average pore diameter the transverse section is approximately 15 mm. The medullary pith is foamy, and it is present in rachis and barbs as well, (Fig. 5E). In Fig. 6, we show a cross-section that is cut along the rachis, at an angle in the dorsal feather. From the same cut, pores were also measured in the undeformed direction, reaching the average pore diameter of 12 mm. Another longitudinal cross-section of the calamus cortex in the dorsal feather (Fig. 7) showed a similar laminated structure of keratin fibers to the one presented in the ventral feather (Fig. 4). This section through the calamus partly revealed fractured keratin fibers with an average diameter of 0.16 ± 0.04 mm. We also verified the keratin fiber diameter from the ventral primary feather in the

Fig. 2. SEM micrographs of a ventral feather with afterfeather A) showing barb and barbule B) zoom in to barb with a diameter of 12 mm and with its wrinkled surface, C) close-up of barbule with hamuli indicated with arrows, D) showing barbs in afterfeather with E) close-up of barbules and hamuli indicated with an arrow.

Please cite this article as: S. Metwally, S. Martínez Comesaña, M. Zarzyka et al., Thermal insulation design bioinspired by microstructure study of penguin feather and polar bear hair, Acta Biomaterialia, https://doi.org/10.1016/j.actbio.2019.04.031

4

S. Metwally et al. / Acta Biomaterialia xxx (xxxx) xxx

Fig. 3. SEM micrograph of A) head feather structure with B) close-up of the rachis surface showing wrinkled surfaces with pores and C) histogram with pore size distribution on rachis, reaching average pore diameter of 0.19 ± 0.05 mm.

Fig. 4. SEM micrographs of longitudinal cut through the ventral feather with afterfeather, showing A) the difference between the rachis and cortex, B) foamy structure of the rachis with pores, C) zoomed in, rounded cross-sections of pores made of keratin fibers, with strut formed between pores, D) histogram of pore diameters, giving the average values of 11 ± 4 mm, and E) calamus with divided cortex, with the cuticula membranes.

transverse section of the barb (Fig. 8), measuring average values of 0.14 ± 0.06 mm. It was also observed that the fibers stick together and form bundles, which are typically up to 0.5 mm in diameter. The last type of penguin feather we characterized was the head contour, presented in Fig. 9. The longitudinal cross-section along the feather revealed very different details about the pore structure, with interconnecting struts built out of keratin fibers (Fig. 9 C). The pores are formed from randomly oriented keratin fibers stuck together, with an average diameter of 0.21 ± 0.06 mm (Fig. 9 D, F). The fibers have the appearance of being pressed and embedded in the keratin membrane. These results suggest similar dimensions of keratin fibers are present in different parts of the feathers. Interestingly, the average fiber diameter of keratin fibers in the pores is slightly higher than those in the cortex, see Table 1. Importantly, the pore membrane is itself porous, as has been seen in other birds,

such as the peacock (Pevocristatus) [19] and owl (Otusleucotus) that have pores built of keratin fibrous membranes, and connected via struts [34]. Struts found in feathers are similar to those observed in dandelions [19], indicated in Figs. 4C and 9C, also a very light and aerodynamic structure. 3.2. Polar bear hair Polar bear hair is broadly divided into two types: ground and guard hair, as shown in Fig. 10. Both types of hair, but especially the ground hair, are known to provide thermal insulation for polar bears. The guard hairs are pigment-free, 5–15 cm long, and are responsible for capturing UV energy from sunlight to generate heat, which is transported through the hollow shaft [24]. However, the main purpose of hair is to prevent heat loss, which depends on

Please cite this article as: S. Metwally, S. Martínez Comesaña, M. Zarzyka et al., Thermal insulation design bioinspired by microstructure study of penguin feather and polar bear hair, Acta Biomaterialia, https://doi.org/10.1016/j.actbio.2019.04.031

S. Metwally et al. / Acta Biomaterialia xxx (xxxx) xxx

5

Fig. 5. SEM micrograph revealing the porosity of the rachis in a ventral feather with afterfeather A) transverse cross-section of the rachis, B) foam structure of the rachis, C) zoomed in to the organization of cellular cortex, D) histogram of pore diameter distribution, and E) cross-sections of barbs, showing very similar pore geometry and pore size as observed in the rachis.

Fig. 6. SEM micrographs of dorsal feather A) with the exposed porous structure through a cut in the rachis, B) cellular cortex and C) histogram showing the distribution of the pore diameter in the foam part.

hair density and length [4], especially true of ground hair. The external structure of polar bear hairs varies and depends of which part of the body the hair originates, see the examples in Fig. 11. The roughness of the polar bear hairs comes from cuticle layers, which are formed by dead keratinocytes overlapping each other and forming protective scales. The cuticles are the outermost layer of the hair shaft [19] and are responsible for the scale pattern on the hair, not only of polar bears, but also otters and seals [35]. We have observed pores on the surface of the guard hair. The size of the pores is between 2 and 5 mm, are located on scales, as shown in Fig. 12, and are connecting through the cortex and hollow

core (medulla), see Figs. 13, 15A and 18E. The external pores are interconnected with the hollow shaft, which has not been reported before. This porosity on the outer surface of polar bear hair was seen on specimens taken from the shoulder, neck and abdomen. Polar bear hairs are similar to other hairs, such as human, and are composed by cuticle, cortex and medulla. The diameter of the medulla in polar bear hair is in the range of 20–30 mm. The cortex is composed of cortical cells and the cortex is tightly packed with bundles of keratin fibers, see Figs. 13 and 14. The average diameter of keratin fibers measured from the dorsal samples was 0.19 ± 0.05 mm, which was slightly higher than the overall average

Please cite this article as: S. Metwally, S. Martínez Comesaña, M. Zarzyka et al., Thermal insulation design bioinspired by microstructure study of penguin feather and polar bear hair, Acta Biomaterialia, https://doi.org/10.1016/j.actbio.2019.04.031

6

S. Metwally et al. / Acta Biomaterialia xxx (xxxx) xxx

Fig. 7. SEM micrograph of a dorsal feather showing A) cross-section of calamus in the barb with B) keratin fibers exposed in the lateral wall of cortex, and C) histogram showing the distribution of keratin fiber diameters with an average value of 0.16 ± 0.04 mm.

Fig. 8. SEM micrographs of the cross-section of a ventral primary feather showing A) the transition between the calamus and the rachis with B) close-up on the fractured keratin fibers, and C) histogram of keratin fiber diameter distribution.

values, equal to 0.16 ± 0.04 mm, see Table 1. The histograms comparing the keratin fiber size distribution from polar bear samples are presented in Fig. 14B.

Polar bear hair is composed of twisted peptide chains of alphakeratin, which is a coiled-coil a-helix protein [8]. Keratin fibers run parallel to each other along the length of the hair shaft. Between

Please cite this article as: S. Metwally, S. Martínez Comesaña, M. Zarzyka et al., Thermal insulation design bioinspired by microstructure study of penguin feather and polar bear hair, Acta Biomaterialia, https://doi.org/10.1016/j.actbio.2019.04.031

7

S. Metwally et al. / Acta Biomaterialia xxx (xxxx) xxx

Fig. 9. SEM micrographs of penguin head feather, A) fractured cross-section along the barb, B) internal porosity, C) close-up to the pore structure D) porous membrane inside pores, E) fractured surface showing keratin fibers and F) histograms with fiber diameter distribution from pores and along the rachis.

Table 1 Summary of all the keratin fibers and pore measurements in penguin feather and polar bear hair. Sample Penguin feather

Polar bear hair

Keratin fiber diameter [mm]

Pore diameter inside [mm]

Dorsal rachis Ventral contour with afterfeather- rachis

-

Ventral primary Dorsal calamus Head contour rachis Head contour in pores From various places Dorsal back

0.14 ± 0.06 0.16 ± 0.04 0.11 ± 0.06 0.21 ± 0.06 0.16 ± 0.04 0.19 ± 0.05

12 ± 3 11 ± 4 15 ± 2 -

Pore diameter outside [mm]

Figure number

0.19 ± 0.05

6 3–5 8 7 9 14

Fig. 10. Polar bear hair with ground and guard hair sample.

bundles of keratin fibers, tubules occur, as indicated by the arrows in Figs. 13A and 15. These tubules between fibers hinder crack propagation, offering increased fracture resistance, and provide

flexibility and tensile strength to the hair cortex. Fig. 16 shows the transverse cross-section of a polar bear hair. In Fig. 16 the medulla, an air-filled channel in the center of the hair, can be seen,

Please cite this article as: S. Metwally, S. Martínez Comesaña, M. Zarzyka et al., Thermal insulation design bioinspired by microstructure study of penguin feather and polar bear hair, Acta Biomaterialia, https://doi.org/10.1016/j.actbio.2019.04.031

8

S. Metwally et al. / Acta Biomaterialia xxx (xxxx) xxx

Fig. 11. SEM micrographs of the outer surface of polar bear hair, showing cuticle with overlapping scales from the keratinization process on A) neck and both B) and C) from the abdomen.

Fig. 12. SEM micrography of the polar bear from neck region showing A) pores outside with indicated two pores presented in B) and C) with higher magnifications, D) pore outside the other fiber also from the neck, E) deep pores interconnected with the microstructure inside.

Please cite this article as: S. Metwally, S. Martínez Comesaña, M. Zarzyka et al., Thermal insulation design bioinspired by microstructure study of penguin feather and polar bear hair, Acta Biomaterialia, https://doi.org/10.1016/j.actbio.2019.04.031

S. Metwally et al. / Acta Biomaterialia xxx (xxxx) xxx

9

Fig. 13. SEM micrograph of the longitudinal cut through the polar bear hair exposing the internal structure with A) hollow channels through the cortex, interconnecting pores at the hair surface with medulla, the arrow on the left side of the image B) the medulla with the cortex consisting of aligned keratin fibers.

Fig. 14. The cross-section of the polar bear hair showing A) aligned keratin fibers in the cortex, just behind the cuticle layers and B) histogram comparing keratin fiber diameter measured in various samples and in the dorsal sample from the back of the bear.

which is also shown in the longitudinal cut in Fig. 13. The cuticle layers are visible in cross-section in Fig. 16C. The number of layers is usually from 1 to 6, but can be more, with the thickness ranging from 0.2 to 0.5 mm per layer. The cuticle is a layer of protective scales, composed of non-pigmented, flattened horny cells. There are clear borders observed between them, relating to the different angle of the keratin fiber alignment. The variation in layers may differ, and is possibly related to the reorientation of keratin fibers, similar to lamellar structures observed in collagen fiber systems [21]. In Fig. 17 the fracture has caused delamination, showing the glassy membrane between layers, probably residual cell membrane from fiber formation. The remaining cell matrix proteins ensure a strong cuticular cohesion, providing an intercellular lipoprotein cement. The keratin fibers are embedded in cells that are bound by a lipidrich cell membrane complex, visible in the medulla, as indicated in

Fig. 18. Cells from the medulla form spherical hollow vacuoles, therefore large pores are created on keratinization. The diameter of the medulla in guard hair is between 20–30 mm and in ground hair approximately 10 mm. The main canal is segmented, with membranes spanning at intervals of approximately 30 mm, which is similar to the size of cells. In the membranes, we observe a fibrous structure, see Fig. 19, which also appeared to contain porosity. It has been reported that the excellent thermal insulation of polar bear hair is because of the medulla; however, it is observed that other species also have a hollow core, including human hair. The hollow shaft in the polar bear hair is also responsible for light energy collection [24], therefore we think the interconnection between pores outside of hair to inside medulla through the cortex (see Fig. 18E) is crucial in understanding the light conversion. However, there are few studies on the porosity and geometry of polar bear hair.

Please cite this article as: S. Metwally, S. Martínez Comesaña, M. Zarzyka et al., Thermal insulation design bioinspired by microstructure study of penguin feather and polar bear hair, Acta Biomaterialia, https://doi.org/10.1016/j.actbio.2019.04.031

10

S. Metwally et al. / Acta Biomaterialia xxx (xxxx) xxx

Fig. 15. SEM micrographs of a freeze-fractured cross-section of polar bear hair A) The side view showing B) the tubular structure between bundles of keratin fibers, indicated with arrows and C) zoom in to the circled region.

Fig. 16. SEM micrographs showing A) Cross-section of polar bear hair from the neck with the hollow shaft (medulla) in the middle. Two circled regions are shown with higher magnification: B) fracture surface of the outer layers showing the cross-sectioned pores along the hair, tubular structures indicated with arrows and C) the fracture of the outer surface clearly showing cuticle layers.

3.3. Microstructure comparison between penguin feathers and polar bear hair The microstructures we investigated show the importance of hierarchical porosity in two different types of keratin-based materials. Polar bear hair is composed of coiled-coil alpha-keratin and penguin feather of sheets of beta-keratin. We present observations of porosity from the macroscopic, down to the sub-micron level, see Table 1. The main observable difference in penguin feather

and polar bear hair is in medulla construction; in the feather the porosity in the shaft is ‘‘foamy”, see Figs. 4 and 5, whilst in the polar bear hair it has hollow vacuoles. The pores observed on the exterior of both materials are also different, as penguin feather pores are at least ten times smaller than those on polar bear hairs, see Figs. 3 and 12. However, these two keratin-based materials have many more similarities. The comparison between the two structures lead us to list the common features these two biological materials have as follows:

Please cite this article as: S. Metwally, S. Martínez Comesaña, M. Zarzyka et al., Thermal insulation design bioinspired by microstructure study of penguin feather and polar bear hair, Acta Biomaterialia, https://doi.org/10.1016/j.actbio.2019.04.031

S. Metwally et al. / Acta Biomaterialia xxx (xxxx) xxx

11

Fig. 17. SEM micrographs of three examples of a cross-section of polar bear hair showing layers or reoriented keratin fibers covering the cortex.

- the outside surface is wrinkled or has scales - the porosity is present in the main shafts and on the external surfaces - the cortex is based on aligned bundles of keratin fibers, with the average diameter 0.3–0.6 mm - fibers run parallel to each other along the length of the shaft - keratin fibers have a similar diameter in the range of 0.14– 0.18 mm, see Fig. 20 - there is tubular porosity between the bundles of keratin fibers - hierarchical porosity observed at different structural levels that are often interconnected. The hierarchical structures at micron and submicron level enable optimization of many important properties in materials, such as flexibility, water repellency, density, and thermal insulation. However, thermal insulation in penguin feather and polar bear hair is related not only to the internal structure but also to their arrangements on the skin. The obvious difference between them is the shape; branching structure of the feather, including barbs and barbules, providing additional protection in terms of thermal insulation and anti-wetting. Afterfeather and ground hair, observed close to the skin, have a similar function; capturing air to form an additional insulation layer in freezing weather conditions. The potential benefits of this comparative analysis lie in the design of synthetic structures, mimicking those found in nature. Based on this detailed microstructural study of penguin feather and polar bear hair, we were able to create a schematic of a principle design to follow in constructing thermally insulating

materials. We propose the following design, based on our investigation, presented in Fig. 21. The design consists of three main elements; the exterior of the tube is made of several layers of crosslaminated fibers, the main body of the tubular structure contains longitudinally-oriented fiber bundles, enclosing a highly porous core. An important feature of naturally insulating materials is low density/high porosity, which increases the surface area of the structures, and features heavily in this design. We propose utilizing sub-micron polymer fibers in constructing this hierarchical composite structure as polymer already afford thermal and electrical insulation properties and can be readily aligned and woven to form the desired structural components. Conclusions Materials in nature, that have evolved over many millions of years, provide elegant solutions to the problems faced by different organisms, and our increasing understanding of which structural elements are found to recur, and how these systems function, allow us the produce synthetic analogues for our own applications. Our findings from a unique comparison between two keratinbased materials, penguin feather and polar bear hair, shed new light on how their microstructure is optimized to form highly insulating materials. High-resolution scanning electron microscopy allows us to observe their 3D structure, including statistical measurements of keratin fiber and pore diameters, in greater detail than previous studies [24,25,29,30]. The observed structural features, common to both of the biomaterials in this study, and

Please cite this article as: S. Metwally, S. Martínez Comesaña, M. Zarzyka et al., Thermal insulation design bioinspired by microstructure study of penguin feather and polar bear hair, Acta Biomaterialia, https://doi.org/10.1016/j.actbio.2019.04.031

12

S. Metwally et al. / Acta Biomaterialia xxx (xxxx) xxx

Fig. 18. SEM micrographs of polar bear hair showing A) cross-section along the fiber porous structure with B) and C) showing the membranes dividing the medulla, D) crosssection of hollow shaft showing the regular division with the approximate spacing between membranes of 30 mm, E) close up of the pores’ interconnection with the medulla.

Fig. 19. SEM micrograph of a longitudinal cross-section showing A) Cell membranes in the hollow core of polar bear hair B) close-up on the membrane with an arrow indicating the porous structure of keratin fibers.

Please cite this article as: S. Metwally, S. Martínez Comesaña, M. Zarzyka et al., Thermal insulation design bioinspired by microstructure study of penguin feather and polar bear hair, Acta Biomaterialia, https://doi.org/10.1016/j.actbio.2019.04.031

S. Metwally et al. / Acta Biomaterialia xxx (xxxx) xxx

13

Fig. 20. SEM image of keratin fibers from the cross-section of A) penguin feather and B) polar bear hair.

Fig. 21. Schematic design of fiber structure with high insulation properties inspired by penguin feather and polar bear hair, A) showing the main design in the form of a tube with the scales on the outermost layer, B) the top view with the foamy core and C) cortex is built of the aligned fibers with tubular porosity.

spanning several orders of magnitude in length-scale, have allowed us to propose a structure for a synthetic fiber that is structurally robust, light weight, and highly thermally insulating. Acknowledgments The authors thank Paweł Borecki from Wrocław Zoo and Jacek Je˛drzejewski from Płock Zoo for the African penguin sample sand Dr Joachim Schöne, Zoo am Meer, Bremerhaven in Germany Kerri Chase from Polar Bear Habitat of Cochrane, Ontario in Canada,

Una Richardson from RZSS Highland Wildlife Park, Kincraig, Scotland, UK, and special thanks to Maria Krakowiak and Dr Anna Jakucin´ska from Warsaw Zoo, for polar bear hair samples used in this study. We also thank Stanisław Malik for photography of polar bear hair, in Fig. 10, and Dr Anke Husmann and Dr Russell Bailey for the proofreading of the manuscript. Sara Martínez Comesaña thanks the SOCRATE-ERASMUS funding, and Piotr Szewczyk Sonata Bis 5 project from National Science Centre, Poland, No 2015/18/E/ ST5/00230 for PhD scholarship. The microscopy study was conducted within the statutory funding No 11.11.110.229 and sup-

Please cite this article as: S. Metwally, S. Martínez Comesaña, M. Zarzyka et al., Thermal insulation design bioinspired by microstructure study of penguin feather and polar bear hair, Acta Biomaterialia, https://doi.org/10.1016/j.actbio.2019.04.031

14

S. Metwally et al. / Acta Biomaterialia xxx (xxxx) xxx

ported by the infrastructure at International Centre of Electron Microscopy for Materials Science (IC-EM) at AGH University of Science and Technology. The material design study was conducted within ‘Nanofiber-based sponges for atopic skin treatment’ project, which is carried out within the First TEAM programme of the Foundation for Polish Science co-financed by the European Union under the European Regional Development Fund, project no POIR.04.04.00-00- 4571/18-00. Data availability The raw/processed data required to reproduce these findings are available on request. Disclosure statement The authors declare no competing financial interest. Appendix A. Supplementary data Supplementary data to this article can be found online at https://doi.org/10.1016/j.actbio.2019.04.031. References [1] B. Wicklein, A. Kocjan, G. Salazar-Alvarez, F. Carosio, G. Camino, M. Antonietti, L. Bergström, Thermally insulating and fire-retardant lightweight anisotropic foams based on nanocellulose and graphene oxide, Nat. Nanotechnol. 10 (2015) 277–283. [2] J.R.E. Taylor, Thermal Insulation of the down and Feathers of Pygoscelid Penguin Chicks and the Unique Properties of Penguin Feathers, Am. Ornithol. Union. 103 (1986) 160–168. [3] Y. Cui, H. Gong, Y. Wang, D. Li, H. Bai, A Thermally Insulating Textile Inspired by Polar Bear Hair, Adv. Mater. 30 (2018) 1–8. [4] P. Simonis, M. Rattal, E.M. Oualim, A. Mouhse, J.-P. Vigneron, Radiative contribution to thermal conductance in animal furs and other woolly insulators, Opt. Express. 22 (2014) 1940. [5] H. Jia, J. Guo, J. Zhu, Comparison of the Photo-thermal Energy Conversion Behavior of Polar Bear Hair and Wool of Sheep, J. Bionic Eng. 14 (2017) 616– 621. [6] P. Fratzl, K. Misof, I. Zizak, G. Rapp, H. Amenitsch, S. Bernstorff, Fibrillar Structure and Mechanical Properties of Collagen, J. Struct. Biol. 122 (1997) 119–122. [7] S.E. Naleway, M.M. Porter, J. McKittrick, M.A. Meyers, Structural Design Elements in Biological Materials: Application to Bioinspiration, Adv. Mater. 27 (2015) 5455–5476. [8] M.J. Greenwold, W. Bao, E.D. Jarvis, H. Hu, C. Li, M.T.P. Gilbert, G. Zhang, R.H. Sawyer, Dynamic evolution of the alpha (a) and beta (b) keratins has accompanied integument diversification and the adaptation of birds into novel lifestyles, BMC Evol. Biol. 14 (2014) 1–16. [9] J.E.A. Bertram, J.M. Gosline, Fracture toughness design in horse hoof keratin, J. Exp. Biol. 125 (1986) 29–47. [10] A. Kitchner, J.F. Vincent, Composite theory and the effect of water on the stiffness of horn keratin, J. Mater. Sci. 22 (1987) 1385–1389. [11] L. Tombolato, E.E. Novitskaya, P.Y. Chen, F.A. Sheppard, J. McKittrick, Microstructure, elastic properties and deformation mechanisms of horn keratin, Acta Biomater. 6 (2010) 319–330.

[12] A. Kitchener, Effect of water on the linear viscoelasticity of horn sheath keratin, J. Mater. Sci. Lett. 6 (1987) 321–322. [13] M. Kasapi, J.M. Gosline, Strain-rate-dependent mechanical properties of the equine hoof wall, J. Exp. Biol. 199 (1996) 1133–1146. [14] M.A. Kasapi, J.M. Gosline, Design complexity and fracture control in the equine hoof wall, J. Exp. Biol. 200 (1997) 1639–1659. [15] M.L. Ryder, Structure of Rhinoceros Horn, Nature 193 (1962) 1199. [16] Y. Seki, S.G. Bodde, M.A. Meyers, Toucan and hornbill beaks: a comparative study, Acta Biomater. 6 (2010) 331–343. [17] F. Pan, Z. Lu, I. Tucker, S. Hosking, J. Petkov, J.R. Lu, Surface active complexes formed between keratin polypeptides and ionic surfactants, J. Colloid Interface Sci. 484 (2016) 125–134. [18] J.G. Rouse, M.E. Van Dyke, A review of keratin-based biomaterials for biomedical applications, Materials (Basel) 3 (2010) 999–1014. [19] Z.Q. Liu, D. Jiao, M.A. Mayers, Z.F. Zhang, Structure and mechanical properties of naturally occurring lightweight foam-filled cylinder – the peacock’s tail coverts shaft and its components, Acta Biomater. 17 (2015) 137–151. [20] R.H.C. Bonser, P.P. Purslow, The Young’S Modulus of Feather Keratin, J. Exp. Biol. 198 (1995) 1029–1033. [21] H.S. Gupta, U. Stachewicz, W. Wagermaier, P. Roschger, H.D. Wagner, P. Fratzl, Mechanical modulation at the lamellar level in osteonal bone, J. Mater. Res. 21 (2006) 1913–1921. [22] B. Bhushan, Y.C. Jung, Natural and biomimetic artificial surfaces for superhydrophobicity, self-cleaning, low adhesion, and drag reduction, Prog. Mater. Sci. 56 (2011) 1–108. [23] S. Huda, Y. Yang, Feather fiber reinforced light-weight composites with good acoustic properties, J. Polym. Environ. 17 (2009) 131–142. [24] H. Jia, J. Zhu, Z. Li, X. Cheng, J. Guo, Design and optimization of a photo-thermal energy conversion model based on polar bear hair, Sol. Energy Mater. Sol. Cells. 159 (2017) 345–351. [25] S. Wang, Z. Yang, G. Gong, J. Wang, J. Wu, S. Yang, L. Jiang, Icephobicity of Penguins Spheniscus Humboldti and an Artificial Replica of Penguin Feather with Air-Infused Hierarchical Rough Structures, J. Phys. Chem. C. 120 (2016) 15923–15929. [26] D. Grémillet, C. Chauvin, R.P. Wilson, Y. Le Maho, D. Grmillet, S. Wanless, Unusual feather structure allows partial plumage wettability in diving great cormorants Phalacrocorax carbo, J. Avian Biol. 36 (1005) 55–63. [27] C. Duprat, S. Protière, A.Y. Beebe, H.A. Stone, Wetting of flexible fibre arrays, Nature 482 (2012) 510–513. [28] P.K. Szewczyk, D.P. Ura, S. Metwally, J. Knapczyk-Korczak, M. Gajek, M.M. Marzec, A. Bernasik, U. Stachewicz, Roughness and Fiber Fraction Dominated Wetting of Electrospun Fiber-Based Porous Meshes, Polymers 11 (2019) 34. [29] C.L. Williams, J.C. Hagelin, G.L. Kooyman, Hidden keys to survival: the type, density, pattern and functional role of emperor penguin body feathers, Proc. R. Soc. B - Biol. Sci. 282 (2015) 20152033. [30] F.B. Kulp, L. D’Alba, M.D. Shawkey, J.A. Clarke, Keratin nanofiber distribution and feather microstructure in penguins Keratin nanofiber distribution and feather microstructure in penguins, Auk Ornithol. Adv. 135 (2018) 777–787. [31] T. Lingham-Soliar, N. Murugan, A New Helical Crossed-Fibre Structure of bKeratin in Flight Feathers and Its Biomechanical Implications, PLoS One. 8 (2013) e65849. [32] U. Stachewicz, R.J. Bailey, H. Zhang, C.A. Stone, C.R. Willis, A.H. Barber, Wetting Hierarchy in Oleophobic 3D Electrospun Nanofiber Networks, ACS Appl. Mater. Interfaces 7 (2015) 16645–16652. [33] P.K. Szewczyk, D.P. Ura, S. Metwally, J. Knapczyk-Korczak, A. Gruszczyn´ski, U. Stachewicz, Biomimicking wetting properties of spider web from Linothele megatheloides with electrospun fibers, Mater. Lett. 233 (2018) 211–214. [34] T. Lingham-Soliar, Feather structure, biomechanics and biomimetics: The incredible lightness of being, J. Ornithol. 155 (2014) 323–336. [35] H.E.M. Liwanag, A. Berta, D.P. Costa, S.M. Budge, T.M. Williams, Morphological and thermal properties of mammalian insulation: the evolutionary transition to blubber in pinnipeds, Biol. J. Linn. Soc. 107 (2012) 774–787.

Please cite this article as: S. Metwally, S. Martínez Comesaña, M. Zarzyka et al., Thermal insulation design bioinspired by microstructure study of penguin feather and polar bear hair, Acta Biomaterialia, https://doi.org/10.1016/j.actbio.2019.04.031