Bite forces play a key role in animal ecology: they affect mating behaviour, fighting success, and the ability to feed. Although feeding habits of arthropods have a significant ecological and economical impact, we lack fundamental knowledge on how the morphology and physiology of their bite apparatus controls bite performance, and its variation with mandible gape. To address this gap, we derived a biomechanical model that characterizes the relationship between bite force and mandibular opening angle from first principles. We validate this model by comparing its geometric predictions with morphological measurements on the muscoloskeletal bite apparatus of Atta cephalotes leaf-cutter ants, using computed tomography (CT) scans obtained at different mandible opening angles. We then demonstrate its deductive and inductive utility with three examplary use cases: Firstly, we extract the physiological properties of the leaf-cutter ant mandible closer muscle from in vivo bite force measurements. Secondly, we show that leaf-cutter ants are specialized to generate extraordinarily large bite forces, equivalent to about 2600 times their body weight. Thirdly, we discuss the relative importance of morphology and physiology in determining the magnitude and variation of bite force. We hope that a more detailed quantitative understanding of the link between morphology, physiology, and bite performance will facilitate future comparative studies on the insect bite apparatus, and help to advance our knowledge of the behaviour, ecology and evolution of arthropods. 

A biomechanical model for the relation between bite force and mandibular opening angle in arthropods

Atta leaf-cutter ants are the prime herbivore in the Neotropics: differently-sized foragers harvest plant material to grow a fungus as crop. Efficient foraging involves complex interactions between worker-size, task-preferences and plant-fungus-suitability; it is, however, ultimately constrained by the ability of differently-sized workers to generate forces large enough to cut vegetation. In order to quantify this ability, we measured bite forces of A. vollenweideri leaf-cutter ants spanning more than one order of magnitude in body mass. Maximum bite force scaled almost in direct proportion to mass; the largest workers generated peak bite forces 2.5 times higher than expected from isometry. This remarkable positive allometry can be explained via a biomechanical model that links bite forces with substantial size-specific changes in the morphology of the musculoskeletal bite apparatus. In addition to these morphological changes, we show that bite forces of smaller ants peak at larger mandibular opening angles, suggesting a size-dependent physiological adaptation, likely reflecting the need to cut leaves with a thickness that corresponds to a larger fraction of the maximum possible gape. Via direct comparison of maximum bite forces with leaf-mechanical properties, we demonstrate (i) that bite forces in leaf-cutter ants need to be exceptionally large compared to body mass to enable them to cut leaves; and (ii), that the positive allometry enables colonies to forage on a wider range of plant species without the need for extreme investment into even larger workers. Our results thus provide strong quantitative arguments for the adaptive value of a positively allometric bite force.

/pdf/strong-positive-allometry-of-bite-force-in-leaf-cutter-ants-3voe62a8.pdf

Strong positive allometry of bite force in leaf-cutter ants increases the range of cuttable plant tissues

Bite forces play a key role in animal ecology: they affect mating behaviour, fighting success, and the ability to feed. Although feeding habits of arthropods have an enormous ecological and economical impact, we lack fundamental knowledge on how the morphology and physiology of their bite apparatus controls bite performance and its variation with mandible gape. To address this gap, we derived a comprehensive biomechanical model that characterises the relationship between bite force and mandibular opening angle from first principles. We validate the model by comparing its geometric predictions with morphological measurements on CT-scans of Atta cephalotes leaf-cutter ants. We then demonstrate its deductive and inductive power with three exemplary use cases: First, we extract the physiological properties of the leaf-cutter ant mandible closer muscle from in-vivo bite force measurements. Second, we show that leaf-cutter ants are extremely specialised for biting: they generate maximum bite forces equivalent to about 2600 times their body weight. Third, we discuss the relative importance of morphology and physiology in determining the magnitude and variation of bite force. We hope that our work will facilitate future comparative studies on the insect bite apparatus, and advance our knowledge of the behaviour, ecology and evolution of arthropods.

/pdf/a-biomechanical-model-for-the-relation-between-bite-force-2omyal2t.pdf

Recent studies of insect anatomy evince a trend towards a comprehensive and integrative investigation of individual traits and their evolutionary relationships. The abdomen of ants, however, remains critically understudied. To address this shortcoming, we describe the abdominal anatomy of Amblyopone australis Erichson, using a multimodal approach combining manual dissection, histology, and microcomputed tomography. We focus on skeletomusculature, but additionally describe the metapleural and metasomal exocrine glands, and the morphology of the circulatory, digestive, reproductive, and nervous systems. We describe the muscles of the dorsal vessel and the ducts of the venom and Dufour's gland, and characterize the visceral anal musculature. Through comparison with other major ant lineages, apoid wasps, and other hymenopteran outgroups, we provide a first approximation of the complete abdominal skeletomuscular groundplan in Formicidae, with a nomenclatural schema generally applicable to the hexapod abdomen. All skeletal muscles were identifiable with their homologs, while we observe potential apomorphies in the pregenital skeleton and the sting musculature. Specifically, we propose the eighth coxocoxal muscle as an ant synapomorphy; we consider possible transformation series contributing to the distribution of states of the sternal apodemes in ants, Hymenoptera, and Hexapoda; and we address the possibly synapomorphic loss of the seventh sternal–eighth gonapophyseal muscles in the vespiform Aculeata. We homologize the ovipositor muscles across Hymenoptera, and summarize demonstrated and hypothetical muscle functions across the abdomen. We also give a new interpretation of the proximal processes of gonapophyses VIII and the ventromedial processes of gonocoxites IX, and make nomenclatural suggestions in the context of evolutionary anatomy and ontology. Finally, we discuss the utility of techniques applied and emphasize the value of primary anatomical research.

https://publikationen.bibliothek.kit.edu/1000146068/148761738

The ant abdomen: The skeletomuscular and soft tissue anatomy of Amblyopone australis workers (Hymenoptera: Formicidae)

Abstract The fossil record allows a unique glimpse into the evolutionary history of organisms living on Earth today. We discovered a specimen of the stem group ant †Gerontoformica gracilis (Barden and Grimaldi, 2014) in Kachin amber with near-complete preservation of internal head structures, which we document employing µ-computed-tomography-based 3D reconstructions. We compare †Gerontoformica to four outgroup taxa and four extant ant species, employing parsimony and Bayesian ancestral state reconstruction to identify morphological differences and similarities between stem and crown ants and thus improve our understanding of ant evolution through the lens of head anatomy. Of 149 morphological characters, 87 are new in this study, and almost all applicable to the fossil. †Gerontoformica gracilis shares shortened dorsal tentorial arms, basally angled pedicels, and the pharyngeal gland as apomorphies with other total clade Formicidae. Retained plesiomorphies include mandible shape and features of the prepharynx. Implications of the reconstructed transitions especially for the ant groundplan are critically discussed based on our restricted taxon sampling, emphasizing the crucial information derived from internal anatomy which is applied to deep time for the first time. Based on the falcate mandible in †Gerontoformica and other Aculeata, we present hypotheses for how the shovel-shaped mandibles in crown Formicidae could have evolved. Our results support the notion of †Gerontoformica as ‘generalized’ above-ground predator missing crucial novelties of crown ants which may have helped the latter survive the end-Cretaceous extinction. Our study is an important step for anatomical research on Cretaceous insects and a glimpse into the early evolution of ant heads. Graphical Abstract

The First Reconstruction of the Head Anatomy of a Cretaceous Insect, †Gerontoformica gracilis (Hymenoptera: Formicidae), and the Early Evolution of Ants

The extraordinary success of social insects is partially based on division of labour, i.e. individuals exclusively or preferentially perform specific tasks. Task preference may correlate with morph...

Morphological determinants of bite force capacity in insects: a biomechanical analysis of polymorphic leaf-cutter ants.

Herbivores large and small need to mechanically process plant tissue. Their ability to do so is determined by two forces: the maximum force they can generate, and the minimum force required to fracture the plant tissue. The ratio of these forces determines the required relative mechanical effort; how this ratio varies with animal size is challenging to predict. We measured the forces required to cut thin polymer sheets with mandibles from leaf-cutter ant workers which vary by more than one order of magnitude in body mass. Cutting forces were independent of mandible size, but differed by a factor of two between pristine and worn mandibles. Mandibular wear is thus likely a more important determinant of cutting force than mandible size. We rationalise this finding with a biomechanical analysis which suggests that pristine mandibles are ideally ‘sharp’ – cutting forces are close to a theoretical minimum, which is independent of tool size and shape, and instead solely depends on the geometric and mechanical properties of the cut tissue. The increase of cutting force due to mandibular wear may be particularly problematic for small ants, which generate lower absolute bite forces, and thus require a larger fraction of their maximum bite force to cut the same plant.

/pdf/biomechanics-of-cutting-sharpness-wear-sensitivity-and-the-1l8bnkjw.pdf

Biomechanics of cutting: sharpness, wear sensitivity, and the scaling of cutting forces in leaf-cutter ant mandibles

Many social insects display age polyethism: young workers stay inside the nest, and only older workers forage. This behavioural transition is accompanied by genetic and physiological changes, but the mechanistic origin of it remains unclear. To investigate if the mechanical demands of foraging effectively prevent young workers from partaking, we studied the biomechanical development of the bite apparatus in Atta vollenweideri leaf-cutter ants. Fully-matured foragers generate peak in-vivo bite forces of around 100 mN, more than one order of magnitude in excess of those measured for freshly-eclosed callows of the same size. This change in bite force was accompanied by a sixfold increase in the volume of the mandible closer muscle, and by a substantial increase of the flexural rigidity of the head capsule, driven by a significant increase in both average thickness and indentation modulus of the head capsule cuticle. Consequently, callows lack the muscle force capacity required for leaf-cutting, and their head capsule is so compliant that large muscle forces may cause damaging deformations. On the basis of these results, we speculate that continued biomechanical development post eclosion may be a key factor underlying age polyethism, wherever foraging is associated with mechanical demands on the musculoskeletal system.

/pdf/developmental-biomechanics-and-age-polyethism-in-leaf-cutter-eantaanh.pdf

Frederik Püffel

Papers

Morphological determinants of bite force capacity in insects: a biomechanical analysis of polymorphic leaf-cutter ants.

Strong positive allometry of bite force in leaf-cutter ants increases the range of cuttable plant tissues

A biomechanical model for the relation between bite force and mandibular opening angle in arthropods

Biomechanics of cutting: sharpness, wear sensitivity, and the scaling of cutting forces in leaf-cutter ant mandibles

Developmental biomechanics and age polyethism in leaf-cutter ants