Nanomechanics of mandible wear in insects.

Abstract

Many animals rely on specialised mouthparts to process food. Because this is a mechanically demanding task, mouthparts often wear, with potentially serious consequences for feeding performance and thus fitness. The biomechanics of wear are therefore of clear biological relevance, but remain poorly understood, especially in insects, where conventional engineering wear tests are hard to implement. Here, we present a nanomechanical characterisation of the mandibular epicuticle of three insect species: two leaf-cutting specialists, one with and one without transition-metal inclusions, and an omnivore. Contrary to predictions from simple engineering wear theory, wear resistance was neither directly proportional to indentation hardness nor inversely proportional to wear load. We suggest that this discrepancy arises in part from the high hardness-to-modulus ratio of mandibular epicuticle, which renders indentation hardness a poor proxy for resistance to plastic deformation. A simple elasto-plastic wear model qualitatively captures the main discrepancies between experiment and theory, and points to a revised set of wear proxies that may allow at least a qualitative ranking of biological materials via iso-performance lines on Ashby plots. Yet, as with most wear models, the wear coefficient remains unpredictable, a limitation strikingly illustrated by the increase in epicuticular wear resistance upon hydration despite a decrease in both hardness and modulus. Together, these observations suggest that purely plastic wear models may often be inadequate for biological materials with a high hardness-to-modulus ratio, and that even elasto-plastic models require careful validation against experimental wear assays. Significance statement Wear limits the functional lifespan of biological tools; however, quantifying, let alone predicting, wear in small, heterogeneous materials is often challenging. In this study, we directly measure nanoscale wear in insect mandibular cuticle and compare our findings with predictions derived from common mechanical wear models. Because of its high hardness-to- modulus ratio, insect epicuticle-like many biomaterials-exhibits an elasto-plastic mechanical response, which can be captured by extending existing approaches with a lumped-parameter elasto-plastic model. The agreement between the model and experiment reveals why using standard proxies can yield even qualitatively incorrect wear rankings and suggests updated elasto-plastic metrics for comparing wear resistance across cuticles and other polymeric biomaterials.