Mechanical and elemental characterization of ant mandibles: consequences for bite mechanics

Abstract

Chewing with the mandibles is a food processing behavior observed in most current insect lineages. Mandible morphology has an essential role in biting behavior and food processing capacity. However, the mandible cuticle can have regional differences in its mechanical properties, associated or not with the accumulation of elements that increase cuticle stiffness. The effects of such a heterogeneous distribution of cuticle material properties in the mandible responses to biting loading are still poorly explored in chewing insects. Here we measured the elemental composition and material properties of workers of an ant species, Formica cunicularia, and tested the effects of the cuticular variation in Youngs modulus (E) under bite-loading with Finite Element Analysis (FEA). We divided worker mandibles into four regions that we expect would vary in elemental composition and material properties, namely the masticatory margin, mandible blade, ventral (VMA), and dorsal (DMA) mandibular articulations with the head. Specifically, we expect the masticatory margin will show higher cuticular hardness (H) and E values, followed by the mandibular joints and the mandible blade. We also predict that such cuticle material properties variation is functionally relevant under bite-loading, changing stress patterns when compared to the mechanical responses of a mandible with a homogeneous distribution of material properties. To measure elemental composition, we used energy disperse X-ray spectroscopy, while H and E were accessed through nanoindentation tests. Mandible mechanical responses to bite-loading were tested with FEA, comparing a mandible with a homogeneous versus a heterogeneous E distribution. As expected, the mandibular regions showed distinct proportions of relevant elements, like Cu and Zn, with the masticatory margin showing the higher levels of those elements, followed by the mandibular articulations with the head and the mandible blade. The same pattern was observed regarding the values of cuticle H and E. When incorporated into FEA, this variation in E effectively changed mandible stress patterns, leading to a higher concentration of stresses in the stiffer mandibular regions, letting the softer mandible blade with relatively lower stress levels. Our results demonstrated the relevance of cuticle heterogeneity in mechanical properties to deal with bite-loading demands and suggest that the accumulation of transition metals such as Cu and Zn has a relevant correlation with such mechanical characteristics of the mandible in this ant species.