The damping properties of the foam-filled shaft of primary feathers of the pigeon Columba livia.

The avian feather combines mechanical properties of robustness and flexibility while maintaining a low weight. Under periodic and random dynamic loading, the feathers sustain bending forces and vibrations during flight. Excessive vibrations can increase noise, energy consumption, and negatively impact flight stability. However, damping can alter the system response, and result in increased stability and reduced noise. Although the structure of feathers has already been studied, little is known about their damping properties. In particular, the link between the structure of shafts and their damping is unknown. This study aims at understanding the structure-damping relationship of the shafts. For this purpose, laser Doppler vibrometry (LDV) was used to measure the damping properties of the feather shaft in three segments selected from the base, middle, and tip. A combination of scanning electron microscopy (SEM) and micro-computed tomography (µCT) was used to investigate the gradient microstructure of the shaft. The results showed the presence of two fundamental vibration modes, when mechanically excited in the horizontal and vertical directions. It was also found that the base and middle parts of the shaft have higher damping ratios than the tip, which could be attributed to their larger foam cells, higher foam/cortex ratio, and higher percentage of foam. This study provides the first indication of graded damping properties in feathers.

The role of mucilage envelope in the endozoochory of selected plant taxa.

Myxodiaspory (formation of mucilage envelope around seeds and fruits) is a common adaptation to dry habitats known in many families of Angiosperms. The mucilage envelope of some seeds seems to be also a unique morphological adaptation which protects myxospermatic diaspores while passing through the bird's digestive system. To evaluate the protective potential of mucilage, we fed the diaspores of seven plant species (representing three different mucilage types and three species of non-mucilaginous plants) to pigeons, Columba livia domestica. Twenty-four hours later, we collected the droppings of pigeons and examined a total of 18,900 non-destroyed diaspores to check for mucilage presence and germination ability. Out of all the examined diaspores, 4.5% were mucilaginous seeds. Among them, the highest number (12.2-13.5%) of viable diaspores belonged to the hemicellulosic type of mucilage (from Plantago species). Only 3.7% of germinating diaspores with pectic mucilage (Linum usitatissimum) were collected, and no seeds representing cellulosic mucilage (e.g., Ocimum basilicum). For non-mucilaginous plants, we collected only a few individual seeds (0.1% out of 8100 seeds used). We noted that the mucilaginous seeds found in the droppings were able to germinate; however, the germination ability was generally smaller in comparison to the control (i.e., not digested) seeds. Our results revealed that the presence of mucilage envelope has an impact on diaspore dispersal and survivability. With our experiments, we demonstrated for the first time that the mucilage envelope, especially of the non-cellulosic type, supports endozoochory. We also showed that non-mucilaginous seeds can be occasionally dispersed via endozoochory and are able to germinate. The results of our studies can explain the ways of plants distribution at a small, local scale as well as in long-distance dispersal, e.g., between islands or even continents.

Comparison of tarsal attachment in two closely related leaf beetle species.

Green dock beetles Gastrophysa viridula and Colorado potato beetles Leptinotarsa decemlineata having distinctly different body mass and gait habits were compared with respect to their tarsal morphology and attachment ability. The focus laid on shapes and dimensions of tenent setae related to the peeling line, i.e., the sum of widths of all thin-film elements participating in contact. High-speed rotation of the two leaf beetle species attached to the horizontal and vertical sides of a Plexiglass drum resulted in higher attachment forces of the heavier beetle species that has a larger number of tarsal setae and a larger peeling line length. However, normalizing the measured forces with the corresponding peeling line lengths led to a reversed relationship. This allowed us to assume that the design of adhesive setae in different leaf beetle species matches the requirements imposed by their habitats. In accordance with the theory of thin film peeling, tangential forces were found to be higher than normal forces. The attachment system of females was found to exhibit stronger functional efficiency, which can be correlated to the morphology of their setae.

Biological adhesion in seagrasses: The role of substrate roughness in Posidonia oceanica (L.) Delile seedling anchorage via adhesive root hairs.

Seagrasses are marine flowering plants that developed several adaptive traits for living in submerged waters. Among this group, Posidonia oceanica (L.) Delile is the dominant species of the Mediterranean Sea, forming persistent meadows that provide valuable ecosystem services to human communities. P. oceanica seedlings can anchor to rocky substrates through adhesive root hairs. Here we investigate, for the first time, the bioadhesion process in seagrasses. Seedlings were grown on substrates provided with different roughness in order to identify mechanisms involved in the adhesion process. Root anchorage strength was measured through a peel test and hair morphology at different micro-roughness was analysed by electron and fluorescence microscopy. Maximum anchorage strength was recorded at roughness levels between 3 and 26 µm, while on finer (0.3) and coarser (52, 162 µm) roughness attachment was weaker. No attachment was obtained on smooth surfaces. Accordingly, root hair tip morphology strongly responded to the substrate. Morphological adaptation of the root hairs to surface topography and mechanical interlocking into the micro-roughness of the substrate appear the main mechanisms responsible for bioadhesion in the system under study. Substrate roughness at the scale of microns and tens of microns is pivotal for P. oceanica seedling attachment to take place. These findings contribute to identification of features of optimal microsite for P. oceanica seedling settlement and to the development of novel approaches to seagrass restoration that take advantage of species' key life history traits.

Persistence of plastic debris and its colonization by bacterial communities after two decades on the abyssal seafloor.

The fate of plastic debris entering the oceans is largely unconstrained. Currently, intensified research is devoted to the abiotic and microbial degradation of plastic floating near the ocean surface for an extended period of time. In contrast, the impacts of environmental conditions in the deep sea on polymer properties and rigidity are virtually unknown. Here, we present unique results of plastic items identified to have been introduced into deep-sea sediments at a water depth of 4150 m in the eastern equatorial Pacific Ocean more than two decades ago. The results, including optical, spectroscopic, physical and microbial analyses, clearly demonstrate that the bulk polymer materials show no apparent sign of physical or chemical degradation. Solely the polymer surface layers showed reduced hydrophobicity, presumably caused by microbial colonization. The bacterial community present on the plastic items differed significantly (p < 0.1%) from those of the adjacent natural environment by a dominant presence of groups requiring steep redox gradients (Mesorhizobium, Sulfurimonas) and a remarkable decrease in diversity. The establishment of chemical gradients across the polymer surfaces presumably caused these conditions. Our findings suggest that plastic is stable over extended times under deep-sea conditions and that prolonged deposition of polymer items at the seafloor may induce local oxygen depletion at the sediment-water interface.

Functional morphology of the sting in two digger wasps (Hymenoptera: Crabronidae) with different types of prey transport.

Digger wasps of the family Crabronidae (Insecta: Hymenoptera) are generally known to use their sting to paralyze or kill a prey. However, only a few species of digger wasps transport their prey to the nest impaled on the sting. How sting morphology correlates with this peculiar type of prey carriage is still unclear. We examined the sting morphology of two phylogenetically closely-related species of digger wasps of similar size, which hunt for similar preys but use different types of prey transportation. Data from light microscopy (LM), scanning electron microscopy (SEM) and confocal laser scanning microscopy (CLSM) were analyzed to find possible correlations between shape, material composition, and function of the stings. The similarity of the material composition in the stings of the two species suggests that the material of stings does not play a dominant role in their functional differences. On the contrary, differences in the curvature and surface sculpture of sting elements likely result in different stress distributions under mechanical loading.

On the fracture resistance of dragonfly wings.

The biological success of insects is attributed to evolution of their wings. Over 400 million years of evolution, insect wings have become one of the most complex and adaptive locomotor structures in the animal kingdom. Although seemingly fragile, they satisfactorily perform their intended function under millions of cycles of repeated stress without failure. However, mechanistic origins of wing resistance to failure remain largely unknown. Most of our understanding of biomechanics of insect wing and flight is based on computer simulations and laboratory experiments. While those studies are needed to reveal certain aspects of wing design, a full understanding can be achieved only by linking obtained data with results of studies in natural conditions. In this study, we tracked the initiation and progression of wing damage of dragonflies in their natural habitats. By quantifying wing area loss over the flight season, we aimed to find a link between the wing structure and accumulated damage. Our results showed that dragonfly wings are exceptionally damage tolerant. Even at the very end of the flight season, the mean wing area loss does not exceed 1.3% of the total wing area. Crack termination, deflection, bifurcation and bridging are the mechanisms that raise the resistance of wings to fracture. This study suggests that insect wings are adapted not only for flight efficiency, but also for damage tolerance. Hence, they should be studied not only from the perspective of aerodynamic performance, but also from that of fracture mechanics.

Material stiffness variation in mosquito antennae.

The antennae of mosquitoes are model systems for acoustic sensation, in that they obey general principles for sound detection, using both active feedback mechanisms and passive structural adaptations. However, the biomechanical aspect of the antennal structure is much less understood than the mechano-electrical transduction. Using confocal laser scanning microscopy, we measured the fluorescent properties of the antennae of two species of mosquito- Toxorhynchites brevipalpis and Anopheles arabiensis-and, noting that fluorescence is correlated with material stiffness, we found that the structure of the antenna is not a simple beam of homogeneous material, but is in fact a rather more complex structure with spatially distributed discrete changes in material properties. These present as bands or rings of different material in each subunit of the antenna, which repeat along its length. While these structures may simply be required for structural robustness of the antennae, we found that in FEM simulation, these banded structures can strongly affect the resonant frequencies of cantilever-beam systems, and therefore taken together our results suggest that modulating the material properties along the length of the antenna could constitute an additional mechanism for resonant tuning in these species.

"Cylindrical worlds" in biology: Does the aggregation strategy give a selective advantage?

Tree trunks and other cylindrical objects, where aggregated insects live, represent a very specific world for predator-prey interactions, which must differ from the situation on a 2D plane. In the present paper, in order to gain a better understanding of the specificity of predator-prey interaction in a cylindrical space, we applied a theoretical approach. Here we introduce a numerical model that allows us to test the effect of different interaction properties between predator and aggregated prey on the plane (2D) and on a cylinder (3D), taking into consideration different abilities of predators to visually detect the prey in these two types of space. The main aim was to test these interactions in an environment, which more realistically reproduces the conditions where aggregated insects usually live. We showed that the aggregation in conjunction with a specific environment may bring additional advantages for the prey. When one prey subgroup aggregates on the other side of the tree trunk and becomes invisible behind the horizon of events for the predator, the subgroup will survive with an extremely high probability. After all, the predator moving along one side of the tree will finally loose the major group completely.

A simple, high-resolution, non-destructive method for determining the spatial gradient of the elastic modulus of insect cuticle.

Nature has evolved structures with high load-carrying capacity and long-term durability. The principles underlying the functionality of such structures, if studied systematically, can inspire the design of more efficient engineering systems. An important step in this process is to characterize the material properties of the structure under investigation. However, direct mechanical measurements on small complex-shaped biological samples involve numerous technical challenges. To overcome these challenges, we developed a method for estimation of the elastic modulus of insect cuticle, the second most abundant biological composite in nature, through simple light microscopy. In brief, we established a quantitative link between the autofluorescence of different constituent materials of insect cuticle, and the resulting mechanical properties. This approach was verified using data on cuticular structures of three different insect species. The method presented in this study allows three-dimensional visualisation of the elastic modulus, which is impossible with any other available technique. This is especially important for precise finite-element modelling of cuticle, which is known to have spatially graded properties. Considering the simplicity, ease of implementation and high-resolution of the results, our method is a crucial step towards a better understanding of material-function relationships in insect cuticle, and can potentially be adapted for other graded biological materials.

Numerical simulation of the pattern formation of the springtail cuticle nanostructures.

Springtails (Collembola) are known to exhibit complex hierarchical nanostructures of their exoskeleton surface that repels water and other fluids with remarkable efficiency. These nanostructures were previously widely studied due to their structure, chemistry and fluid-repelling properties. These ultrastructural and chemical studies revealed the involvement of different components in different parts of the nanopattern, but the overall process of self-assembly into the complex rather regular structures observed remains unclear. Here, we model this process from a theoretical point of view partially using solutions related to the so-called Tammes problem. By using densities of three different reacting substances, we obtained a typical morphology that is highly similar to the ones observed on the cuticle of some springtail species. These results are important not only for our understanding of the formation of hierarchical nanoscale structures in nature, but also for the fabrication of novel surface coatings.

Both stiff and compliant: morphological and biomechanical adaptations of stick insect antennae for tactile exploration.

Active tactile exploration behaviour is constrained to a large extent by the morphological and biomechanical properties of the animal's somatosensory system. In the model organism Carausius morosus, the main tactile sensory organs are long, thin, seemingly delicate, but very robust antennae. Previous studies have shown that these antennae are compliant under contact, yet stiff enough to maintain a straight shape during active exploration. Overcritical damping of the flagellum, on the other hand, allows for a rapid return to the straight shape after release of contact. Which roles do the morphological and biomechanical adaptations of the flagellum play in determining these special mechanical properties? To investigate this question, we used a combination of biomechanical experiments and numerical modelling. A set of four finite-element (FE) model variants was derived to investigate the effect of the distinct geometrical and material properties of the flagellum on its static (bending) and dynamic (damping) characteristics. The results of our numerical simulations show that the tapered shape of the flagellum had the strongest influence on its static biomechanical behaviour. The annulated structure and thickness gradient affected the deformability of the flagellum to a lesser degree. The inner endocuticle layer of the flagellum was confirmed to be essential for explaining the strongly damped return behaviour of the antenna. By highlighting the significance of two out of the four main structural features of the insect flagellum, our study provides a basis for mechanical design of biomimetic touch sensors tuned to become maximally flexible while quickly resuming a straight shape after contact.

Micro-morphological adaptations of the wing nodus to flight behaviour in four dragonfly species from the family Libellulidae (Odonata: Anisoptera).

Adult dragonflies can be divided into two major groups, perchers and fliers, exhibiting notably different flight behaviour. Previous studies have yielded conflicting results regarding the link between the wing macro-morphology and flight style in these two groups. In this study, we present the first systematic investigation of the micro-morphological differences of wings of percher and flier dragonflies in four closely related species from the family Libellulidae. Our results suggest that the shape and material composition of wing microstructural components and, in particular, the nodus are adapted to facilitate the specific wing functioning in fliers and perchers. The findings further indicate a decreasing trend in the area proportion of the soft resilin-dominated cuticle in the nodus in the series of species from typical perchers to typical fliers. Such a reduction in the resilin proportion in the nodus of fliers is associated with an increase in the wing aspect ratio. The knot-shaped protrusion at the nodus of perchers, which becomes notably smaller in that of strong fliers, is likely to act as a mechanical stopper, avoiding large wing displacements. This study aims to develop a novel framework for future research on the relationship between wing morphology and flight behaviour in dragonflies.

The eversible tentacle organs of Polyommatus caterpillars (Lepidoptera, Lycaenidae): Morphology, fine structure, sensory supply and functional aspects.

In their late (3rd and 4th) larval stages, caterpillars of the myrmecophilous lycaenid (Lepidoptera) species Polyommatus coridon and Polyommatus icarus, possess on their 8th abdominal segment two eversible so called tentacle organs (TOs). Previous histological and behavioural results have proposed that the TOs may release a volatile substance that elicits "excited runs" in attendant ants. In our study we investigated for the first time the temporal in- and eversion pattern of TOs. Using nerve tracing, Micro-CT, light- and electron microscopy techniques we studied (i) the histology of the 8th abdominal segment, (ii) the fine structure of the cuticular and cellular apparatus of the TOs, (iii) the attachment sites of the retractor muscle of each TO and (iv) the fine structure of the long slender tentacle hairs which are exposed to the outside, when the TOs are everted and fold back into the TO-sac during inversion. Our data show that the tentacle hairs are typical insect mechanoreceptors, each innervated by a small bipolar sensory cell with a tubular body in the tip of the outer dendritic segment. The latter is enclosed by a cuticular sheath previously called the "internal cuticular duct" and misinterpreted in earlier studies as the space, where the tentacle hairs actively secrete fluids. However, we found no glandular structures nearby or in the wall of the TO-sac. Also we did not reveal any conspicuous signs of secretory activity in one of the enveloping cells belonging to a tentacle hair. Although highly unusual features for an insect mechanoreceptor are: (a) the hair-shaft lumen of tentacle hairs contains flocculent material as well small vesicles and (b) the thin cuticular wall of the hair-shaft and its spines possess few tiny pores. Our data do not support the assumption of previous studies that volatile substances are released via the tentacle organs during their interactions with ants which in turn are supposed to cause excited runs in ants.

Simple contact mechanics model of the vertebrate cartilage.

We study a simple contact mechanics model of the vertebrate cartilage, which includes (bulk) osmotic effects. The surface roughness power spectrum of a pig cartilage is obtained from the measured surface topography. Using the Reynolds equations with fluid flow factors, calculated using the Persson contact mechanics theory and the Bruggeman effective medium theory, we show how the area of contact and the average interfacial separation change with time. We found that in most cases the contact area percolates, resulting in islands of confined fluid which carry most of the external load. Most importantly, we find that the pressure in the area of real contact is nearly independent of the external load, and well below 1 MPa. This allows the surfaces in the area of "real contact", to be separated (at nanometer range separation distance) by osmotic repulsion, resulting in a very small (breakloose) friction force observed even after a long time of stationary contact.

Stiffness distribution in insect cuticle: a continuous or a discontinuous profile?

Insect cuticle is a biological composite with a high degree of complexity in terms of both architecture and material composition. Given the complex morphology of many insect body parts, finite-element (FE) models play an important role in the analysis and interpretation of biomechanical measurements, taken by either macroscopic or nanoscopic techniques. Many previous studies show that the interpretation of nanoindentation measurements of this layered composite material is very challenging. To develop accurate FE models, it is of particular interest to understand more about the variations in the stiffness through the thickness of the cuticle. Considering the difficulties of making direct measurements, in this study, we use the FE method to analyse previously published data and address this issue numerically. For this purpose, sets of continuous or discontinuous stiffness profiles through the thickness of the cuticle were mathematically described. The obtained profiles were assigned to models developed based on the cuticle of three insect species with different geometries and layer configurations. The models were then used to simulate the mechanical behaviour of insect cuticles subjected to nanoindentation experiments. Our results show that FE models with discontinuous exponential stiffness gradients along their thickness were able to predict the stress and deformation states in insect cuticle very well. Our results further suggest that, for more accurate measurements and interpretation of nanoindentation test data, the ratio of the indentation depth to cuticle thickness should be limited to 7% rather than the traditional '10% rule'. The results of this study thus might be useful to provide a deeper insight into the biomechanical consequences of the distinct material distribution in insect cuticle and also to form a basis for more realistic modelling of this complex natural composite.

Dragonfly wing nodus: A one-way hinge contributing to the asymmetric wing deformation.

Dragonfly wings are highly specialized locomotor systems, which are formed by a combination of several structural components. The wing components, also known as structural elements, are responsible for the various aspects of the wing functionality. Considering the complex interactions between the wing components, modelling of the wings as a whole is only possible with inevitable huge oversimplifications. In order to overcome this difficulty, we have recently proposed a new approach to model individual components of complex wings comparatively. Here, we use this approach to study nodus, a structural element of dragonfly wings which has been less studied to date. Using a combination of several imaging techniques including scanning electron microscopy (SEM), wide-field fluorescence microscopy (WFM), confocal laser scanning microscopy (CLSM) and micro-computed tomography (micro-CT) scanning, we aim to characterize the spatial morphology and material composition of fore- and hindwing nodi of the dragonfly Brachythemis contaminata. The microscopy results show the presence of resilin in the nodi, which is expected to help the deformability of the wings. The computational results based on three-dimensional (3D) structural data suggest that the specific geometry of the nodus restrains its displacements when subjected to pressure on the ventral side. This effect, resulting from an interlocking mechanism, is expected to contribute to the dorso-ventral asymmetry of wing deformation and to provide a higher resistance to aerodynamic forces during the downstroke. Our results provide an important step towards better understanding of the structure-property-function relationship in dragonfly wings. STATEMENT OF SIGNIFICANCE: In this study, we investigate the wing nodus, a specialized wing component in dragonflies. Using a combination of modern imaging techniques, we demonstrate the presence of resilin in the nodus, which is expected to facilitate the wing deformability in flight. The specific geometry of the nodus, however, seems to restrain its displacements when subjected to pressure on the ventral side. This effect, resulting from an interlocking mechanism, is suggested to contribute to dorso-ventral asymmetry of wing deformations and to provide a higher resistance to aerodynamic forces during the downstroke. Our results provide an important step towards better understanding of the structure-property-function relationship in dragonfly wings and might help to design more efficient wings for biomimetic micro-air vehicles.

Wing cross veins: an efficient biomechanical strategy to mitigate fatigue failure of insect cuticle.

Locust wings are able to sustain millions of cycles of mechanical loading during the lifetime of the insect. Previous studies have shown that cross veins play an important role in delaying crack propagation in the wings. Do cross veins thus also influence the fatigue behaviour of the wings? Since many important fatigue parameters are not experimentally accessible in a small biological sample, here we use the finite element (FE) method to address this question numerically. Our FE model combines a linear elastic material model, a direct cyclic approach and the Paris law and shows results which are in very good agreement with previously reported experimental data. The obtained results of our study show that cross veins indeed enhance the durability of the wings by temporarily stopping cracks. The cross veins further distribute the stress over a larger area and therefore minimize stress concentrations. In addition, our work indicates that locust hind wings have an endurance limit of about 40% of the ultimate tensile strength of the wing material, which is comparable to many engineering materials. The comparison of the results of the computational study with predictions of two most commonly used fatigue failure criteria further indicates that the Goodman criterion can be used to roughly predict the failure of the insect wing. The methodological framework presented in our study could provide a basis for future research on fatigue of insect cuticle and other biological composite structures.

Resilin microjoints: a smart design strategy to avoid failure in dragonfly wings.

Dragonflies are fast and manoeuvrable fliers and this ability is reflected in their unique wing morphology. Due to the specific lightweight structure, with the crossing veins joined by rubber-like resilin patches, wings possess strong deformability but can resist high forces and large deformations during aerial collisions. The computational results demonstrate the strong influence of resilin-containing vein joints on the stress distribution within the wing. The presence of flexible resilin in the contact region of the veins prevents excessive bending of the cross veins and significantly reduces the stress concentration in the joint.

Basal Complex and Basal Venation of Odonata Wings: Structural Diversity and Potential Role in the Wing Deformation.

Dragonflies and damselflies, belonging to the order Odonata, are known to be excellent fliers with versatile flight capabilities. The ability to fly over a wide range of speeds, high manoeuvrability and great agility are a few characteristics of their flight. The architecture of the wings and their structural elements have been found to play a major role in this regard. However, the precise influence of individual wing components on the flight performance of these insects remains unknown. The design of the wing basis (so called basal complex) and the venation of this part are responsible for particular deformability and specific shape of the wing blade. However, the wing bases are rather different in representatives of different odonate groups. This presumably reflects the dimensions of the wings on one hand, and different flight characteristics on the other hand. In this article, we develop the first three-dimensional (3D) finite element (FE) models of the proximal part of the wings of typical representatives of five dragonflies and damselflies families. Using a combination of the basic material properties of insect cuticle, a linear elastic material model and a nonlinear geometric analysis, we simulate the mechanical behaviour of the wing bases. The results reveal that although both the basal venation and the basal complex influence the structural stiffness of the wings, it is only the latter which significantly affects their deformation patterns. The use of numerical simulations enabled us to address the role of various wing components such as the arculus, discoidal cell and triangle on the camber formation in flight. Our study further provides a detailed representation of the stress concentration in the models. The numerical analysis presented in this study is not only of importance for understanding structure-function relationship of insect wings, but also might help to improve the design of the wings for biomimetic micro-air vehicles (MAVs).