Biology subjects

Pueffel, F.

Publications and source records attributed to Pueffel, F..

4 recordsLinked to original sources

bioRxiv2023

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

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.

evolutionary biology↗

bioRxiv2023

Developmental biomechanics and age polyethism in leaf-cutter ants

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.

developmental biology↗

bioRxiv2022

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

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.

biophysics↗

bioRxiv2021

Morphological determinants of bite force capacity in insects: a biomechanical analysis of polymorphous leaf-cutter 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 morphological adaptations so implying task-specialisation, but the extent of such specialisation can be difficult to determine. Here, we demonstrate how the physical foundation of some tasks can be leveraged to quantitatively link morphology and performance. We study the allometry of bite force capacity in Atta vollenweideri leaf-cutter ants, polymorphic insects in which the mechanical processing of plant material is a key aspect of the behavioural portfolio. Through a morphometric analysis of tomographic scans, we show that the bite force capacity of the heaviest colony workers is twice as large as predicted by isometry. This disproportionate boost is predominantly achieved through increased investment in muscle volume; geometrical parameters such as mechanical advantage, fibre length or pennation angle are likely constrained by the need to maintain a constant mandibular opening range. We analyse this preference for an increase in size-specific muscle volume and the adaptations in internal and external head anatomy required to accommodate it with simple geometric and physical models, so providing a quantitative understanding of the functional anatomy of the musculoskeletal bite apparatus in insects.

evolutionary biology↗