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: 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.

Large deformation diffeomorphic mapping of 3D shape variation reveals two distinct mandible and head capsule morphs in Atta vollenweideri leaf‐cutter worker ants

“…The change in head capsule shape arises partially from a faster growth of head width compared to head length (Figure 2a and Püffel et al., 2021 ), and this differential growth likely carries functional significance: it enables a disproportionate increase in physiological cross‐sectional area of the muscle, and thus a substantial increase in size‐specific bite force (Püffel et al., 2021 ). As a result, the largest foragers generate bite forces more than two times larger than the isometric expectation; this boost provides colonies with access a larger range of plant material, without requiring an extreme investment in even larger workers (Püffel, Roces, et al., 2023 ). The functional morphology of minim heads is considerably harder to assess, as the demands placed on head capsules by gardening or brood care are not well known.…”

“…Famed for their fungal agriculture system, leaf‐cutter ant workers cut leaves at an industrial rate to maintain a fungal crop, which serves as food for the colony. Larger leaf‐cutter ants possess relatively more muscle mass and thus can generate larger bite forces (Püffel et al., 2021 ), providing the colony with access to a larger range of plant material (Püffel, Roces, et al., 2023 ). Indeed, larger workers are more likely to cut tougher leaves (Clark, 2006 ; Evison & Ratnieks, 2007 ; Nichols‐Orians, 1991 ), illustrating how size‐differences can be functionally advantageous.…”

Three-dimensional kinematics of leaf-cutter ant mandibles: not all dicondylic joints are simple hinges

“…All these parameters play a crucial role in determining insect bite performance [41]. All previous work in insects implicitly or explicitly assumed that the mandible rotational axis has a fixed orientation and location, so that a unique instantaneous mechanical advantage can be defined [25,33,35,40,41,86,88,89]. Our results in A. vollenweideri indeed suggest that the rotational axis has an approximately fixed position, but for two reasons, this should only be a minor source of comfort for those interested in exact mechanical models of insect bite performance.…”

Mandible elemental composition and mechanical properties from distinct castes of the leafcutter ant Atta laevigata (Attini; Formicidae)

“…[2]). This can be associated with morphological adaptations as muscle and mandible size and shape, leading to improved performance in their respective roles [2][3][4][5][6][7][8][9][10].…”

“…Later with the colony development, workers with a head width of 0.8–1.0 mm are necessary for fungal gardening, while a head width of 1.6 mm on average is required for cutting tough leaves. Throughout colony growth, the spectrum extends in both directions, with small workers having a head width of less than 0.7 mm and large workers exceeding 5 mm in head width, increasing the range of used plant tissues [ 6 ]. The quantity of small workers in growing colonies is significantly higher than that of large workers and the size range is more dependent on colony size than age [ 14 ].…”