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

Abstract

Atta leaf-cutter ants are the prime herbivore in the Neotropics: polymorphic foragers harvest plant material from the nest surroundings to grow a fungus as crop. Efficient foraging involves complex interactions between worker-polymorphism, 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 larger workers. Our results thus provide strong quantitative arguments for the adaptive value of a positively allometric bite force.

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

“…Leaf-cutter ants may thus adjust their cutting behaviour in accordance with the steep decrease of bite force for opening angles > 75°. These results represent a key step towards understanding the intricate relationship between cutting behaviour, maximum bite force and mandibular opening angle in Atta foraging [also see 113].…”

“…The following 3D coordinates were extracted from the video frame corresponding to the peak bite force: the bite contact point (most distal tooth tip), joint centre, and the geometric centres of both eyes. The depth component of the 3D coordinates was measured from the mirrored side view [113]. The vectors connecting mandible joint with both eyes E l and E r were used to define a local head-fixed coordinate system: e 1 = E l /| E l |, e 3 = ( E l × E r )/| E l × E r | and e 2 = e 3 × e 1 .…”

“…The sensor was calibrated by suspending calibration weights from the bite plate of the pivoting lever [see 113, for more details]. Twelve weights between 10 and 150g were used for calibration, exceeding the range of measured bite forces (109 - 1172 mN).…”

“…In order to extract the force-length properties of the mandible closer muscle, we measured bite forces of A. cephalotes majors using a custom-built setup, described in detail in Püffel et al [113]. In brief, a capacitive force sensor (maximum load: 1 N, resolution: 0.002 N) is compressed when a force is applied to a bite plate connected to a pivoting lever (see Fig.…”

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

“…To extract the force–length properties of the mandible closer muscle, we measured bite forces of A. cephalotes majors using a custom-built setup, described in detail in the study by Püffel et al [ 118 ]. In brief, a capacitive force sensor (maximum load: 1 N, resolution: 0.002 N) is compressed when a force is applied to a bite plate connected to a pivoting lever ( figure 2 a ).…”