Leaf-cutter ants with worn mandibles cut half as fast, spend twice the energy, and tend to carry instead of cut

Abstract

The importance of mechanical wear in the behavioral ecology and energetics of small organisms is an open question. We investigated wear in leaf-cutter ants, Atta cephalotes, because their cutting technique can be imitated and the leaves are the main energy source for the colony. We found that a razor-sharp (50-nm radius) “V-blade” that cuts leaves between the first and second mandibular teeth was dulled (∼10-μm radius) and often nearly worn away on foragers. We found that the force required to cut standard leaves, using mandibles removed from foragers cutting in the wild, varied by a factor of 2.5 with tooth wear, defined as the difference between pupal and actual tooth length. We also found that wear significantly reduced the cutting rate. From the distribution of wear among the cutting foragers, we estimated that the wild colony would have spent 44% less of both energy and time making the observed cuts if the cutters’ mandibles had all been pristine. Finally, wear correlated with behavioral differences—foragers with the most worn 10% of mandibles almost exclusively carried rather than cut. This previously unreported form of task partitioning suggests that eusociality may extend useful lifespans by making it possible to switch tasks as skills decline. We developed a model, assuming that ants do work at a constant rate proportional to their mass, to predict the cutting rate from head width, tooth wear, and force to cut leaves with a scalpel (R = 0.62), and we used this estimate to argue that the partitioning of cutting and carrying was sub-optimal but better than random. Wear’s strong effect on performance may promote wear-avoiding behavior and wear-resistant mandible composition; it may affect leaf selection and worker lifespan and it raises the possibility that wear is a similarly important constraint for many other small organisms.

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Acknowledgements

We are grateful to Hubert Herz and to anonymous reviewers for advice. Elisa Alphandary, Corina Lewis, Evan Stewart, Kevin Mergel, and Feargus Tyler helped with data collection and analysis. We thank the Smithsonian Tropical Research Institute and the Panamanian government for logistical support and access. This work was supported by National Science Foundation grant IOS 0422234.

Ethical standards

The experiments described in this paper complied with the current laws of the Republic of Panama and of the United States of America.

Conflicts of interest

The authors declare that they have no conflicts of interest.

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Correspondence to Robert M. S. Schofield.

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Communicated by J. Heinze

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View from below of laboratory colony ants, Atta cephalotes, cutting leaves. In off-vein regions, the surface of the leaf opposite the ant tends to be cut by the proximal blade of the distal tooth (first tooth) as the tooth rides along the surface. In the first three clips, the ants are cutting Rubus armeniacus leaves (approximately 0.08 mm or 0.14 mm without and with the trichome [hair] mat), in the last 2 clips the ants are cutting approximately 0.25 mm thick Prunus lusitanica leaves. While the thicknesses of the leaves are sometimes greater than the distance between the two distal teeth for some of these foragers, these foragers tend to be smaller than wild colony foragers (see Figure 4 of the paper). The distance between the first and second tooth of an average sized wild colony cutter was about 0.15 mm, so the approximately 0.13 mm thick O. macrantha leaves would have been cut mainly by the V-blade between the first and second tooth. For veins, a sawing action is employed. Movies were made using a Nikon Coolpix 4500 mounted on a Zeiss dissection microscope. The frame rate has not been altered to speed up or slow down action in any of the three movies. (MOV 53 574 kb)

View from above of laboratory colony ants, Atta cephalotes, cutting leaves. The leading mandible is often used to partially cut through the leaf in advance of the lagging mandible, and is used as an anchor to pull the lagging mandible against in order to complete the partial cut. For increasingly larger veins, the mandibles are used with increasing symmetry in a sawing action. In the fifth clip, showing cutting of a large vein, the mouth parts of the ant are extended at one point, possibly to ingest sap. In the first 6 clips, the ants are cutting Rubus armeniacus leaves, in the last clip the ant was cutting a Prunus lusitanica leaf. (MOV 58 417 kb)

Two laboratory colony ants, Atta cephalotes, with highly worn mandibles appear to be having difficulties cutting Prunus lusitanica leaves. In the first clip an ant with a blunted distal tooth on the leading mandible appears to have difficulties using it as an anchor and to partially cut the leaf. The second clip shows a second ant cutting with blunted teeth in a view from below. (MOV 33 929 kb)

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Schofield, R.M.S., Emmett, K.D., Niedbala, J.C. et al. Leaf-cutter ants with worn mandibles cut half as fast, spend twice the energy, and tend to carry instead of cut. Behav Ecol Sociobiol 65, 969–982 (2011). https://doi.org/10.1007/s00265-010-1098-6

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Keywords

  • Atta cephalotes
  • Task allocation
  • Energetics
  • Cutting rate
  • Wear
  • Task partitioning
  • Aging