Hydration-induced reversible deformation of the pine cone

Abstract

The scales of pine cones undergo reversible deformation due to hydration changes in order to optimize seed dispersal. This improves the survivability of the pine. The reversible flexing of the scales is caused by two tissue layers arranged in a sandwich configuration: a layer composed of sclereid cells and a sclerenchyma layer. They expand differentially upon hydration (and contract upon dehydration) due to differences in the structure that are analyzed here for Torrey pine (Pinustorreyana) cones. In addition to this well-known mechanism by which the cellulose microfibrils in the scales vary their angle with the wood cell axis, we confirm the presence of a porosity gradient in the sclereid cells and calculate, using a model consisting of three layers, the stresses generated upon dehydration taking into account the effect of hydration on the elastic modulus. Our quantitative analysis reveals that this gradient structure can significantly decrease the stress concentrations due to the mismatch between the two layers, and show that this is an ingenious design to increase the interfacial toughness to improve the robustness of pine cone scales. We also show that each individual layer of sclereid cells and sclerenchyma fibers undergoes bending when hydrated separately, and suggest that the two layers operate synergistically to effect the required deformation for seed release. A synthetic bioinspired analog consisting of hydrogels with different porosities is used to confirm this principal actuation mechanism. These findings may inspire the materials science and mechanical engineering communities to develop more robust, biocompatible and energy-efficient actuation systems. Statement of significanceSome biological structures can exhibit reversible deformation enabled by water inflow and outflow of their structure. We analyse the reversible motion of pine cone scales. The dehydration produces their flexure and opening, resulting in the release of seeds and their dispersal, when conditions are right. This process is reversible, and rehydration of the pine cone recloses the scales. The processes of flexing and straightening are governed by shrinking and swelling which are directed by differences in the arrangement of cellulose microfibrils in a bilayer construct. We demonstrate that the scales are more complex than a simple bilayer structure and that they actually have gradients, which significantly reduce the internal stresses and ensure their integrity. We analyse the process of opening and closing of the scales for a gradient structure in the Torrey pine cone using a simple idealized trilayer model. The results demonstrate a significant decrease in internal stresses produced by the gradient structure. Using the lessons learned from the pine cone, we produce a bilayer junction using hydrogels with different porosities which exhibit the same reversible bending response.