The homogenous alternative to biomineralization: Zn- and Mn-rich materials enable sharp organismal “tools” that reduce force requirements

Abstract

We measured hardness, modulus of elasticity, and, for the first time, loss tangent, energy of fracture, abrasion resistance, and impact resistance of zinc- and manganese-enriched materials from fangs, stings and other “tools” of an ant, spider, scorpion and nereid worm. The mechanical properties of the Zn- and Mn-materials tended to cluster together between plain and biomineralized “tool” materials, with the hardness reaching, and most abrasion resistance values exceeding, those of calcified salmon teeth and crab claws. Atom probe tomography indicated that Zn was distributed homogeneously on a nanometer scale and likely bound as individual atoms to more than ¼ of the protein residues in ant mandibular teeth. This homogeneity appears to enable sharper, more precisely sculpted “tools” than materials with biomineral inclusions do, and also eliminates interfaces with the inclusions that could be susceptible to fracture. Based on contact mechanics and simplified models, we hypothesize that, relative to plain materials, the higher elastic modulus, hardness and abrasion resistance minimize temporary or permanent tool blunting, resulting in a roughly 2/3 reduction in the force, energy, and muscle mass required to initiate puncture of stiff materials, and even greater force reductions when the cumulative effects of abrasion are considered. We suggest that the sharpness-related force reductions lead to significant energy savings, and can also enable organisms, especially smaller ones, to puncture, cut, and grasp objects that would not be accessible with plain or biomineralized “tools”.

Material Properties and Morphology of Prestomal Teeth in Relation to the Feeding Habits of Diptera (Brachycera)

“…stercoraria and St. calcitrans to have higher amounts of inorganic elements than species of other feeding habits, but this was not observed (Table 3). Metal ions and other inorganic elements are known to enhance the material properties of insect cuticles, particularly on structures that rasp or pierce hard substrates [35][36][37][38]. Here, the studied cuticular elements were in low concentrations (mostly <1%) for all species.…”

The mechanical characterization of the legs, fangs, and prosoma in the spider Harpactira curvipes (Pocock 1897)

“…the penetration of surfaces as well as the durability and wear resistance of the tool 19 . From this point of view, a recent work showed that the actions of penetrating surfaces as well as resisting wear and tear are aided by metals inclusion in the cuticle 12 . This is in accordance with a previous study, which showed the presence of metal ions in the fangs of the spiders that act as reinforcing elements 12 , 14 .…”

“…From this point of view, a recent work showed that the actions of penetrating surfaces as well as resisting wear and tear are aided by metals inclusion in the cuticle 12 . This is in accordance with a previous study, which showed the presence of metal ions in the fangs of the spiders that act as reinforcing elements 12 , 14 . Moreover, the different microstructural organization of the cuticle body parts (legs, prosoma, outer layer, and inner layer of the fangs) has been related to the polymorphic forms differentiated into their crystal structure 48 .…”

“…The samples’ preparation followed common protocols for the nanoindentation of biological materials, spiders tissue included 10 , 12 – 14 , 29 – 33 . The dissected parts were positioned in a plexiglass sample holder and included in an epoxy resin matrix, which was purchased from Hardrock 554® (Remet).…”

“…The fangs present a well-defined architecture composed of a structural/material gradient that is adapted to allow the spider to feed, defend itself and dig, all of which require resistance to wear 11 . Interestingly, the optimization of such functions has been recently linked to the metal inclusions in the animals’ cuticles 12 .…”