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Title: Do leaf-cutter ants Atta colombica obtain their magnetic sensors from soil?

Author
item RIVEROS, ANDRE - Smithsonian Tropical Research
item ESQUIVEL, DARCI - Brazilian Center For Physics Research
item WAJNBERG, ELIANE - Brazilian Center For Physics Research
item Srygley, Robert

Submitted to: Behavioral Ecology and Sociobiology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 8/14/2013
Publication Date: 1/15/2014
Citation: Riveros, A.J., Esquivel, D.M., Wajnberg, E., Srygley, R.B. 2014. Do leaf-cutter ants Atta colombica obtain their magnetic sensors from soil? Behavioral Ecology and Sociobiology. 68(1):55-62.

Interpretive Summary: We are interested in spatial orientation of the leaf-cutter ants, an important nutrient recycler of tropical forest and major agricultural pest. Previously we have shown that leaf-cutter ants use a magnetic compass to update the direction of their path-integrated home vector. Ferromagnetoreception by animals is conventionally attributed to biomineralized particles. We challenge this by asking whether contact with soil is necessary for ants to have a magnetic sense. Here we compare ants from a captive colony that was free of soil to a control colony nesting naturally in the soil to determine: 1) whether soil-free ants are insensitive to shifts in the horizontal component of the magnetic field and 2) whether they lack ferromagnetic properties. As predicted, we found that soil-free ants were insensitive to the shift in the magnetic field, and yet they were capable of orienting homeward despite the shift in the magnetic field. This feat could only be accomplished by an additional compass: one that uses proprioceptive information to measure rotation on the ground and through the air. Contact with soil was necessary to sense the horizontal component of the magnetic field. For the first time we discriminate a second set of biomineralized magnetic particles that differ in composition or arrangement from the soil-derived ones. These might be involved in a novel magnetic compass insensitive to the horizontal shift or in detection of rotation, analogous to statoliths. Although our results raise many new questions, they advance our understanding of the composition of magnetic compasses in ants and the nature of spatial orientation in insects in general.

Technical Abstract: How animals sense, process and use magnetic information has remained largely elusive. In insects, ferromagnetic particles are candidates for a magnetic sensor. Recent studies suggest that ferromagnetic minerals from soil can be incorporated into the antennae of the migratory ant Pachycondola marginata (Oliveira et al. 2010). We used Neotropical leaf-cutter ants Atta colombica to test whether soil contact is necessary for the acquisition and use of a magnetic compass. Atta colombica typically relies on pheromonal trails, but is the only invertebrate known to use a magnetic compass to update a calculated path integrated home vector (Riveros and Srygley 2008). Here we show that contact with soil is necessary for A. colombica to incorporate magnetic particles that can be used as a magnetic compass, and yet we also show that ants can biosynthesize magnetic particles. Workers from a soil-free colony ignored a 90° shift in the horizontal component of the magnetic field, yet significantly oriented homeward despite the experimental occlusion of any geocentric cues. In contrast, workers from a soil-exposed colony oriented homeward, shifted with the magnetic field or oriented in an intermediate direction. Homeward orientations under shifted magnetic fields suggest that leaf-cutter ants are able to determine a path integrated home vector in conditions where only proprioceptive information is available. Strikingly, ants from the soil-free colony also had ferromagnetic particles, yet, as observed by Ferromagnetic Resonance (FMR), these particles differed from those in soil-exposed ants and evidently were not associated with a magnetic compass sensitive to the horizontal shift in the magnetic field.