Abstract
Social insect colonies are organized without central control, and must not only accomplish many tasks, such as foraging and nest construction, but must also respond to changing conditions by adjusting the number of workers performing each task1,2. Here we use chemically treated, artificial ants to show that cuticular hydrocarbons, which differ according to task, are used by workers of the red harvester ant (Pogonomyrmex barbatus) to recognize the tasks of the ants that they encounter. Encounters with other ants thus inform a worker's decision on whether to perform a particular task.
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A mature colony of the red harvester ant, a seed-eating desert species, consists of a single queen and 10,000–12,000 workers. We focused on two task groups: foragers, who collect food; and patrollers, who scout the foraging area each morning. If patrollers do not return safely, foragers will not leave the nest to search for seeds3. Nest-maintenance workers are active at the same time as patrollers and do not stimulate foraging4. A social-insect worker can become active or switch task as conditions are altered — depending, for example, on the number of other workers who are currently engaged in a particular task5,6,7.
Communication in social insects occurs mostly by chemical and tactile means8, with cuticular hydrocarbons often acting as recognition cues9. A harvester ant's task decisions depend on its interaction, by antennal contact, with ants at the nest entrance10 — ants in different task groups differ in their cuticular hydrocarbon profiles11. Foragers, for example, spend more time outside the nest and so are exposed to warmer, drier conditions than nest-maintenance workers, who mostly stay inside. This causes the foragers to have higher ratios of n-alkanes to n-alkenes and branched alkanes in their cuticular hydrocarbon profiles12.
For field experiments, we used nine mature colonies at a long-term study site near Rodeo, New Mexico, in the United States13. We first inhibited foraging by removing returning patrollers. After 30 min of inactivity, we mimicked the flow of returning patrollers by dropping glass beads (3 mm in diameter) that had been coated with one ant-equivalent of extract into the nest at a rate of one every 10 seconds. The coating on the beads consisted of patroller cuticular lipids, patroller hydrocarbons, nest-maintenance hydrocarbons (which acted as a control for task specificity), or plain solvent (blank control). As a positive control for forager activity, we used live patrollers that were captured and then immediately returned to the nest. Cuticular lipids were extracted in 100% pentane for 10 min9,11 and hydrocarbons were purified from cuticular lipids by using column chromatography9.
The number of beads added to a nest was roughly equal to the number of patrollers collected. We then measured foraging activity by counting the number of active foragers outside the nest within 1 m of the entrance, every 10 min for 60 min. All colonies received each treatment in a random order; for each colony, we carried out one trial per day for five consecutive days. We normalized for variation among colonies in absolute forager number by dividing each mean number foraging per trial by the largest number of foragers ever observed for that colony.
Task-specific cuticular hydrocarbons from patrollers were sufficient to rescue foraging activity (Fig. 1). However, the behaviour is not a simple response to patroller extract alone. Our results, including preliminary data (not shown), indicate that in this patroller-mimic assay, all of the following are necessary to stimulate foraging activity: a one-ant equivalent concentration of hydrocarbon extract, location just inside the nest entrance, sequential presentation, and the time of day at which the colony is ready to begin foraging.
A brief encounter with a nestmate influences an ant's task decision because the encounter identifies the task of the other worker, cued by subtle features of other ants' hydrocarbon profiles. Encounters between ants thus provide information used for task allocation. These encounters in the aggregate produce a dynamic network that regulates the colony's behaviour.
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Greene, M., Gordon, D. Cuticular hydrocarbons inform task decisions. Nature 423, 32 (2003). https://doi.org/10.1038/423032a
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DOI: https://doi.org/10.1038/423032a
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