Functional morphology and biomechanics of arthropods

As the largest phylum of animals, arthropods live all over the world occupying terrestrial, aquatic, arboreal, and subterranean niches. The distinct living environments resulted in evolving numerous complex adaptations associated with movement and other mechanical functions. Schroeder et al. (2018) proposed that such functions as locomotion, mechanical detection, adhesion, sound production, communication, etc., result from specific combinations of cuticle-derived exoskeleton. Although the exoskeleton in arthropods is mainly formed by three main constituents (chitin, proteins, and lipids), hierarchically structured materials with tremendous diversity of properties have evolved resulting in different morphological features and specific biomechanical characteristics. It has been previously reported by Vincent and Wegst (2004) that insect cuticles have seven-order range of Young’s modulus, ranging from 1 kPa for soft cuticles, like in the case of intersegmental membranes, to 20 GPa for sclerotized cuticle, such as in the beetle elytra. The distinct elastic properties greatly satisfy the mechanical requirements of the cuticles for realizing a wide range of biomechanical and other physiological functions.

To better understand the extraordinary mechanical behaviors of biological materials, numerous studies have been performed using imaging techniques, experimental measurements, and numerical simulations. Interesting recent findings include the presence of gradient elasticity in adhesive tarsal setae of beetles caused by inhomogeneous resilin distribution (Peisker et al. 2013), anti-friction properties of porous fluid-filled sand hopper cuticle surface (Wan and Gorb 2020), and fracture resistance of multi-layered locust semi-lunar process cuticle (Wan and Hao 2020), to name a few.

In addition to the reinforcement mechanism of the functional biological materials, scientists and engineers are also interested in revealing how specific materials and structures of arthropods are related to their properties and functions. However, investigations should not just report some statistical relations between anatomical features and performance characteristics, to speculate about potential reasons. Instead, multidisciplinary methodology should be implemented to explore the key mechanisms and principles behind their outstanding performance. This is quite a difficult task, because many different features in organisms are simultaneously adapted, to achieve multi-optimized properties, rather than a single one. The reason for multi-optimized properties is that organisms are usually adapted to different environmental stresses and sometimes face unexpected risks. The protective shell of the mussel Mytilus edulis (though it is not representative of Arthropoda) is a good long-term studied example to explain this viewpoint. Its shell is a multi-layered biomineralized system consisting of several different materials for protecting its soft body inside. Compared to the outer prismatic calcite in the shell, the inner nacre layer is stronger, although from the engineering point of view should be actually deposited outside the shell for providing more effective protection against external impacts. However, this disagrees with the natural situation that nacre is situated on the inner side of the shell rather than on the outer side. Both acid etching test and mechanical loading tests (including static loading and dynamic impact) were performed in our previous research (Wan et al. 2019), revealing an interesting compromise of the mussel shell in that the current pattern of outside prismatic calcite and inside nacre can provide optimal multi-protection against both mechanical and chemical stresses. Perhaps, in view of just mechanical protection, the current pattern of layers is not the best solution, but the present evolutionary optimized distribution of layers offers the mussel sufficient multi-protective abilities against complex environmental stresses (like acid attack of dog whelk gastropods and mechanical attack of decapod crabs).

Due to the complexity of the research object of biological materials, modern imaging and characterization techniques must be simultaneously used to decode the mysteries of the arthropods. General technologies include imaging techniques (micro-CT, transmission electron microscope, scanning electron microscope), compositional identification (X-ray energy spectrometry, Fourier transform infrared spectroscopy, Raman spectrometry, immunohistological staining, confocal laser scanning microscopy), mechanical testing (nanoindentation, atomic force microscopy, universal material testing technology, adhesion force testers, and various tribometers), movement capture (high-speed videography, videography under synchrotron radiation light source), and numerical simulations (finite element modeling, computational fluid dynamics simulation, fluid–solid coupling modeling, multibody dynamics simulation).

In this special issue of the Journal of Comparative Physiology A, some recent research on functional morphology and biomechanics of arthropods will be presented to link morphology and biomechanics of materials and structures to their mechanical functions, such as flapping flight, legged locomotion, and gripping.

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