A materials perspective of Martyniaceae fruits: Exploring structural and micromechanical properties

Abstract

Several species of the plant family Martyniaceae are characterised by unique lignified capsules with hook-shaped extensions that interlock with hooves and ankles of large mammals to disperse the seeds. The arrangement of fruit endocarp fibre tissues is exceptional and intriguing among plants. Structure-function-relationships of these slender, curved, but mechanically highly stressed fruit extensions are of particular interest that may inspire advanced biomimetic composite materials. In the present study, we analyse mechanical properties and fracture behaviour of the hook-shaped fruit extensions under different load conditions. The results are correlated with calculated stress distributions, the specific cell wall structure, and chemical composition, providing a detailed interpretation of the complex fruit tissue microstructure. At the cell wall level, both a large microfibril angle and greater strain rates resulted in Young's moduli of 4-9 GPa, leading to structural plasticity. Longitudinally arranged fibre bundles contribute to a great tensile strength. At the tissue level, transversely oriented fibres absorb radial stresses upon bending, whereas cells encompass and pervade longitudinal fibre bundles, thus, stabilise them against buckling. During bending and torsion, microcracks between axial fibre bundles are probably spanned analogous to a circular anchor. Our study fathoms a highly specialized plant structure, substantiating former assumptions about epizoochory as dispersal mode. While the increased flexibility allows for proper attachment of fruits during dynamical locomotion, the high strength and stability prevent a premature failure due to heavy loads exerted by the animal.

Keywords: Fruit endocarp; Fruit hooks; Functional anatomy; Plant biomechanics; Structural hierarchy.