Biomineral armor in leaf-cutter ants

Hongjie Li,John H Fournelle,Hans A Bechtel,Huifang Xu,Jeffrey Sosa-Calvo,Pupa U P A Gilbert,Ted R Schultz,Chang-Yu Sun,Caitlin M Carlson,Yihang Fang,Ana Ješovnik,David R Andes,Cameron R Currie,Robert Zarnowski

doi:10.1038/s41467-020-19566-3

Abstract

Although calcareous anatomical structures have evolved in diverse animal groups, such structures have been unknown in insects. Here, we report the discovery of high-magnesium calcite [CaMg(CO3)2] armor overlaying the exoskeletons of major workers of the leaf-cutter ant Acromyrmex echinatior. Live-rearing and in vitro synthesis experiments indicate that the biomineral layer accumulates rapidly as ant workers mature, that the layer is continuously distributed, covering nearly the entire integument, and that the ant epicuticle catalyzes biomineral nucleation and growth. In situ nanoindentation demonstrates that the biomineral layer significantly hardens the exoskeleton. Increased survival of ant workers with biomineralized exoskeletons during aggressive encounters with other ants and reduced infection by entomopathogenic fungi demonstrate the protective role of the biomineral layer. The discovery of biogenic high-magnesium calcite in the relatively well-studied leaf-cutting ants suggests that calcareous biominerals enriched in magnesium may be more common in metazoans than previously recognized.

Highlights

Calcareous anatomical structures have evolved in diverse animal groups, such structures have been unknown in insects
C Backscattered electron (BSE) image of a polished cuticular cross-section of an ant. This layer is brighter than the cuticle in backscattered electron (BSE) mode scanning electron microscopy (SEM), indicating that it consists of heavier elements and is continuous, covering nearly the entire surface
Based on combined data from in situ X-ray diffraction (XRD), electron microscopy, electron backscatter diffraction (EBSD), quantitative electron probe micro-analysis (EPMA), and Raman and attenuated total reflectance Fourier-transform infrared (ATR-FTIR) spectroscopy, we report here that this coating is a mineral layer covering the ant exoskeleton

Summary

Introduction

Calcareous anatomical structures have evolved in diverse animal groups, such structures have been unknown in insects. Leafcutting ants (genera Acromyrmex and Atta), a phylogenetically derived lineage that arose within the fungus-growing ants around million years ago, harvest fresh vegetation as the substrate on which they grow their fungal mutualists. They are ecologically dominant herbivores in the New World tropics[20,21] and serve important roles in carbon and nitrogen cycling[22]. In addition to the leaf-cutters, 17 other genera of ants occur within the Attina, all of which grow fungus gardens, form colonies of hundreds to a few thousand workers, and use dead vegetative matter or caterpillar frass rather than fresh leaves and grasses as substrates for their gardens. Atta leaf-cutter ants, which use their powerful zinc-enriched mandibles to defend their colonies’ territories against other, encroaching ant species[31,32,33]

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Conclusion