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.
Competing Interest Statement
The authors have declared no competing interest.
Footnotes
We have edited the method section, and added 3 SI sub figures and several equations on the variation of morphological force determinants with opening angle.
Nomenclature
- Aphys
- Physiological cross-sectional area of the mandible closer muscle
- α
- Misalignment angle between Fb,m and Fb
- β
- Muscle force-length shape parameter
- e1, e2, e3
- Local head coordinate system
- Γ
- Correction term for differences in lever arm around the beam pivot (correction ii)
- Fb
- Applied bite force
- Fb,m
- Measured bite force
- Fb,θ
- Maximum bite force at opening angle θ
- Fb,max
- Maximum bite force at an equivalent mandibular opening angle, θmax
- F∗
- Bite force-opening angle relationship, normalised with its maximum
- Relative bite force at opening angle θ
- Lf
- verage muscle fibre length
- Li,e f f
- Effective mandible inlever
- Lo,c
- Mandible outlever at bite contact point
- Lo,e f f,c
- Effective mandible outlever at bite contact point
- Lo,d
- Most distal (largest) mandible outlever
- Lo,e f f,d
- Most distal (largest) effective mandible outlever
- Lopt
- Optimal muscle fibre length at which muscle stress is maximal
- Lp
- Lever arm length around the beam pivot during biting experiment
- Lp,cal
- Lever arm length around the beam pivot during sensor calibration
- φ
- Average fibre pennation angle
- Rotational axis of the mandible joint
- Sl
- Vector connecting joint centre with left head spike
- Sr
- Vector connecting joint centre with right head spike
- σ
- Muscle stress
- σmax
- Maximum muscle stress
- θ
- Mandibular opening angle
- θmax
- Mandibular opening angle at which bite force is maximal
- θopt
- Mandibular opening angle at which muscle stress is maximal