Mechanical behavior of ctenoid scales: Joint-like structures control the deformability of the scales in the flatfish Solea solea (Pleuronectiformes).

Ctenoid scales protect the fish body against predators and other environmental impacts. At the same time, they allow for sufficient degree of flexibility to perform species-specific locomotion. The scales of the flatfish Solea solea were chosen to study the specific mechanical behavior and material properties of the ctenoid scales. Using scanning electron microscopy and micro-computed tomography, three-dimensional asymmetric structures of the stacked mineralized ctenial spines in the posterior field, which is a part of the scales exposed to the environment, were examined in detail. Nanoindentations on the surface of the ctenial spines indicated that the elastic modulus and hardness of these mineralized structures are about 14 GPa and 0.4 GPa, respectively. The spines appeared to be connected to each other by means of joint-like structures containing soft tissues. Bending tests showed that the ctenoid scales have two functional zones: a stiff supporting main body and an anisotropically deformable posterior field. While the stiff plate-like main body provides support for the whole scale, the deformable joint-like structures in the ctenial spines increase the deformability of the posterior field in downward bending. During upward bending, however, the spines prevent complete folding of the posterior field by an interlocking effect. STATEMENT OF SIGNIFICANCE: In contrast to the continuously mineralized cycloid scales, ctenoid scales combine two conflicting properties: They are hard to protect the body of fish against predators and other environmental impacts, yet flexible enough to allow for sufficient degree of body bendability for locomotion. To understand the structural background underlying this specific biomechanical feature, here we investigated the scales of the flatfish Solea solea. For the first time, we demonstrated the presence of joint-like structures within the scales, which increase scale deformability during downward bending, but prevent scale deformation during upward bending by interlocking. Our results shed lights on the material-structure-function relationships in ctenoid scales, as well as on their functional adaptations to the specific environment.

Enhanced Locomotion Efficiency of a Bio-inspired Walking Robot using Contact Surfaces with Frictional Anisotropy.

Based on the principles of morphological computation, we propose a novel approach that exploits the interaction between a passive anisotropic scale-like material (e.g., shark skin) and a non-smooth substrate to enhance locomotion efficiency of a robot walking on inclines. Real robot experiments show that passive tribologically-enhanced surfaces of the robot belly or foot allow the robot to grip on specific surfaces and move effectively with reduced energy consumption. Supplementing the robot experiments, we investigated tribological properties of the shark skin as well as its mechanical stability. It shows high frictional anisotropy due to an array of sloped denticles. The orientation of the denticles to the underlying collagenous material also strongly influences their mechanical interlocking with the substrate. This study not only opens up a new way of achieving energy-efficient legged robot locomotion but also provides a better understanding of the functionalities and mechanical properties of anisotropic surfaces. That understanding will assist developing new types of material for other real-world applications.

Key role of scale morphology in flatfishes (Pleuronectiformes) in the ability to keep sand.

Flatfishes bury themselves for camouflage and protection. Whereas species-specific preferences for certain sediments were previously shown, the role of scales in interaction with sediment has not been investigated. Here, scale morphology and sediment friction were examined in four European pleuronectiforms: Limanda limanda, Platichthys flesus, Pleuronectes platessa, and Solea solea. All species had different scale types ranging from cycloid to ctenoid scales. On the blind side, the number of scales is higher and scales have less ctenial spines than on the eye side. The critical angle of sediment sliding (static friction) significantly depended on the grain size and was considerably higher on the eye side. The effect of mucus was excluded by repeated measurements on resin replicas of the skin. Our results demonstrate the impact of scale morphology on sediment interaction and give an insight about the ability of scales to keep sand. Exposed scales and a higher number of ctenial spines on the eye side lead to an increase of friction forces, especially for sediments with a smaller grain size. Our results suggest that the evolution of scales was at least partly driven by their interactions with sediment which confirms the relevance of sediment for the distribution and radiation of Pleuronectiformes.

Sticky fingers: Adhesive properties of human fingertips.

Fingertip friction is a rather well studied subject. Although the phenomenon of finger stickiness is known as well, the pull-off force and the adhesive strength of human finger tips have never been previously quantified. For the first time, we provided here characterization of adhesive properties of human fingers under natural conditions. Human fingers can generate a maximum adhesive force of 15mN on a smooth surface of epoxy resin. A weak correlation of the adhesive force and the normal force was found on all test surfaces. Up to 300mN load, an increase of the normal force leads to an increase of the adhesive force. On rough surfaces, the adhesive strength is significantly reduced. Our data collected from untreated hands give also an impression of an enormous scattering of digital adhesion depending on a large set of inter-subject variability and time-dependent individual factors (skin texture, moisture level, perspiration). The wide inter- and intra-individual range of digital adhesion should be considered in developing of technical and medical products.

Evidence of a molecular boundary lubricant at snakeskin surfaces.

During slithering locomotion the ventral scales at a snake's belly are in direct mechanical interaction with the environment, while the dorsal scales provide optical camouflage and thermoregulation. Recent work has demonstrated that compared to dorsal scales, ventral scales provide improved lubrication and wear protection. While biomechanic adaption of snake motion is of growing interest in the fields of material science and robotics, the mechanism for how ventral scales influence the friction between the snake and substrate, at the molecular level, is unknown. In this study, we characterize the outermost surface of snake scales using sum frequency generation (SFG) spectra and near-edge X-ray absorption fine structure (NEXAFS) images collected from recently shed California kingsnake (Lampropeltis californiae) epidermis. SFG's nonlinear optical selection rules provide information about the outermost surface of materials; NEXAFS takes advantage of the shallow escape depth of the electrons to probe the molecular structure of surfaces. Our analysis of the data revealed the existence of a previously unknown lipid coating on both the ventral and dorsal scales. Additionally, the molecular structure of this lipid coating closely aligns to the biological function: lipids on ventral scales form a highly ordered layer which provides both lubrication and wear protection at the snake's ventral surface.

Morphology and frictional properties of scales of Pseudopus apodus (Anguidae, Reptilia).

In the lizard family Anguidae different levels of limb reduction exist up to a completely limbless body. The locomotion patterns of limbless anguid lizards are similar to the undulating and concertina movements of snakes. Additionally, anguid lizards frequently use a third mode of locomotion, called slide-pushing. During slide-pushing the undulating moving body slides on the ground, while the posterior part of the body is pressed against the substrate. Whereas the macroscopic and microscopic adaptations of snake scales to limbless locomotion are well described, the micromorphology of anguid lizard scales has never been examined. Therefore we studied the macro- and micromorphology of the scales of Pseudopus apodus, an anguid lizard with a snakelike body. In addition, we measured the frictional properties of Pseudopus scales. Our data show that the microstructures of the ventral scales of this anguid lizard are less developed than in snakes. We found, however, a rostro-caudal gradient in macroscopic structuring. Whereas the ventral side of the anterior body was nearly unstructured, the tail had macroscopic longitudinal ridges. Our frictional measurements on rough substrates revealed that the ridges provide a frictional anisotropy: friction was higher in the lateral than in the rostral direction. The observed frictional properties are advantageous for a tail-based slide-pushing locomotion, for which a tail with a high lateral friction is most effective in generating propulsion.

Microornamentation of leaf chameleons (Chamaeleonidae: Brookesia, Rhampholeon, and Rieppeleon)--with comments on the evolution of microstructures in the Chamaeleonidae.

Chameleons (Chamaeleonidae) feature many adaptations to their arboreal lifestyle, including zygodactylous feet, a prehensile tail, and epidermal microstructures. In arboreal tree chameleons, the substrate-contacting site of the feet and tail is covered by microscopic hair-like structures (setae) of 6-20 µm length. Their friction enhancing function has been shown in recent studies. Leaf chameleons and one representative of the tree chameleons (Chamaeleo namaquensis) secondarily have become ground-dwelling. Because leaf chameleons are paraphyletic, one could expect that in the three leaf chameleon genera Brookesia, Rhampholeon, and Rieppeleon and the tree chameleon Ch. namaquensis, epidermis has adapted independently to terrestrial locomotion. Using scanning electron microscopy, we investigated the substrate-contacting surfaces of the feet (subdigital) of 17 leaf chameleon species and five tree chameleon species that have not yet been examined. Additionally, surfaces not involved in locomotion, the flanks (dorsolateral), and scale interstices, were examined. Although the subdigital microstructures in leaf chameleons are more diverse than in tree chameleons, we found some features across the genera. The subdigital microornamentation of Rhampholeon spinosus consists of long thin setae and spines, comparable to those of tree chameleons. All other Rhampholeon species have spines or short but broad setae. Rh. spectrum had tooth-like structures instead of setae. Subdigital scales of Brookesia have either thorns or conical scale-tops in the center and feature honeycomb microstructures. In Rieppeleon, subdigital scales have a thorn. Scale surfaces are covered by honeycombs and short hair-like structures (spines). As subdigital scales with a thorn in the center and honeycomb microstructures were also found in the terrestrial tree chameleon Ch. namaquensis, one can assume that this geometry is a convergent adaptation to terrestrial locomotion. Despite the great number of genus-specific traits, the convergent evolution of honey-comb structures in Brookesia, Rieppeleon, and Ch. namaquensis and the high variability of spines and setae in Rhampholeon suggests a rapid adaptation of subdigital microornamentation in Chamaeleonidae.

Biofilm formation of mucosa-associated methanoarchaeal strains.

Although in nature most microorganisms are known to occur predominantly in consortia or biofilms, data on archaeal biofilm formation are in general scarce. Here, the ability of three methanoarchaeal strains, Methanobrevibacter smithii and Methanosphaera stadtmanae, which form part of the human gut microbiota, and the Methanosarcina mazei strain Gö1 to grow on different surfaces and form biofilms was investigated. All three strains adhered to the substrate mica and grew predominantly as bilayers on its surface as demonstrated by confocal laser scanning microscopy analyses, though the formation of multi-layered biofilms of Methanosphaera stadtmanae and Methanobrevibacter smithii was observed as well. Stable biofilm formation was further confirmed by scanning electron microscopy analysis. Methanosarcina mazei and Methanobrevibacter smithii also formed multi-layered biofilms in uncoated plastic µ-dishes(TM), which were very similar in morphology and reached a height of up to 40 µm. In contrast, biofilms formed by Methanosphaera stadtmanae reached only a height of 2 µm. Staining with the two lectins ConA and IB4 indicated that all three strains produced relatively low amounts of extracellular polysaccharides most likely containing glucose, mannose, and galactose. Taken together, this study provides the first evidence that methanoarchaea can develop and form biofilms on different substrates and thus, will contribute to our knowledge on the appearance and physiological role of Methanobrevibacter smithii and Methanosphaera stadtmanae in the human intestine.

Subdigital setae of chameleon feet: friction-enhancing microstructures for a wide range of substrate roughness.

Hairy adhesive systems of microscopic setae with triangular flattened tips have evolved convergently in spiders, insects and arboreal lizards. The ventral sides of the feet and tails in chameleons are also covered with setae. However, chameleon setae feature strongly elongated narrow spatulae or fibrous tips. The friction enhancing function of these microstructures has so far only been demonstrated in contact with glass spheres. In the present study, the frictional properties of subdigital setae of Chamaeleo calyptratus were measured under normal forces in the physical range on plane substrates having different roughness. We showed that chameleon setae maximize friction on a wide range of substrate roughness. The highest friction was measured on asperities of 1 µm. However, our observations of the climbing ability of Ch. calyptratus on rods of different diameters revealed that also claws and grasping feet are additionally responsible for the force generation on various substrates during locomotion.

Non-contaminating camouflage: multifunctional skin microornamentation in the West African Gaboon viper (Bitis rhinoceros).

The West African Gaboon viper (Bitis rhinoceros) has an extraordinary coloration of pale brown and velvety black markings. The velvety black appearance is caused by a unique hierarchical surface structures which was not found on the pale brown scales. In the present study we examined the wettability of the vipers scales by measuring contact angles of water droplets. Velvet black scale surfaces had high static contact angles beyond 160° and low roll-off angles below 20° indicating an outstanding superhydrophobicity. Our calculations showed that the Cassie-Baxter model describes well wettability effects for these surfaces. Self-cleaning capabilities were determined by contaminating the scales with particles and fogging them until droplets formed. Black scales were clean after fogging, while pale scales stayed contaminated. Black scales feature multifunctional structures providing not only water-repellent but also self-cleaning properties. The pattern of nanoridges can be used as a model for surface-active technical surfaces.

Snake velvet black: hierarchical micro- and nanostructure enhances dark colouration in Bitis rhinoceros.

The West African Gaboon viper (Bitis rhinoceros) is a master of camouflage due to its colouration pattern. Its skin is geometrically patterned and features black spots that purport an exceptional spatial depth due to their velvety surface texture. Our study shades light on micromorphology, optical characteristics and principles behind such a velvet black appearance. We revealed a unique hierarchical pattern of leaf-like microstructures striated with nanoridges on the snake scales that coincides with the distribution of black colouration. Velvet black sites demonstrate four times lower reflectance and higher absorbance than other scales in the UV-near IR spectral range. The combination of surface structures impeding reflectance and absorbing dark pigments, deposited in the skin material, provides reflecting less than 11% of the light reflected by a polytetrafluoroethylene diffuse reflectance standard in any direction. A view-angle independent black structural colour in snakes is reported here for the first time.

Subdigital and subcaudal microornamentation in Chamaeleonidae--a comparative study.

Locomotion on horizontal and vertical substrates requires effective attachment systems. In three clades of arboreal and rupicolous Iguanidae, Gekkota and Scincidae adhesive systems consisting of microscopic hair-like structures (setae) have been evolved independently. Also the substrate contacting sites on toes and tails of chameleons (Chamaeleonidae) are covered with setae. In the present comparative scanning electron microscopy study, we show that representatives from the chamaeleonid genera Calumma, Chamaeleo, Furcifer, and Trioceros feature highly developed setae that are species-specific and similar on their feet and tail. These 10 µm long, unbranched setae rather resemble those in anoline and scincid lizards than the larger and branched setae of certain gecko species. In contrast to the thin triangular tips of other lizards, all examined species of the genera Furcifer and Calumma and one of the five examined species of the genus Trioceros have spatulate tips. All other examined species of genera Trioceros and Chamaeleo bear setae with narrowed, fibrous tips. Unlike the setae of other lizards, chamaeleonid setal tips do not show any orientation along the axis of the toes, but they are flexible to bend in any direction. With these differences, the chameleon's unique microstructures on the zygodactylous feet and prehensile tail rather increase friction for arboreal locomotion than being a shear-induced adhesive system as setal pads of other lizards.