Cholla cactus frames as lightweight and torsionally tough biological materials

Biological materials tested in compression, tension, and impact inspire designs for strong and tough materials, but torsion is a relatively neglected loading mode. The wood skeletons of cholla cacti, subject to spartan desert conditions and hurricane force winds, provide a new template for torsionally resilient biological materials. Novel mesostructural characterization methods of laser-scanning and photogrammetry are used alongside traditional optical microscopy, scanning electron microscopy, and micro-computed tomography to identify mechanisms responsible for torsional resistance. These methods, in combination with finite element analysis reveal how cholla meso and macro-porosity and fibril orientation contribute to highly density-efficient mechanical behavior. Selective lignification and macroscopic tubercle pore geometry contribute to density-efficient shear stiffness, while mesoscopic wood fiber straightening, delamination, pore collapse, and fiber pullout provide extrinsic toughening mechanisms. These energy absorbing mechanisms are enabled by the hydrated material level properties. Together, these hierarchical behaviors allow the cholla to far exceed bamboo and trabecular bone in its ability to combine specific torsional stiffness, strength, and toughness. Statement of Significance The Cholla cactus experiences, due to the high velocity desert winds, high torsional loads. Our study has revealed the amazingly ingenious strategy by which the tubular structure containing arrays of voids intermeshed with wood fibers resists these high loads. Deformation is governed by compressive and tensile stresses which are greatest at 45 degrees to the cross section. It proceeds by stretching, sliding, and bending of the wood fibers which are coupled with the pore collapse, resulting in delayed failure and a high torsional toughness.