Abstract
Leaf-cutting ants (LCAs) are polyphagous, yet highly selective herbivores. The factors that govern their selection of food plants, however, remain poorly understood. We hypothesized that the induction of anti-herbivore defences by attacked food plants, which are toxic to either ants or their mutualistic fungus, should significantly affect the ants' foraging behaviour. To test this “induced defence hypothesis,” we used lima bean (Phaseolus lunatus), a plant that emits many volatile organic compounds (VOCs) upon herbivore attack with known anti-fungal or ant-repellent effects. Our results provide three important insights into the foraging ecology of LCAs. First, leaf-cutting by Atta ants can induce plant defences: Lima bean plants that were repeatedly exposed to foraging workers of Atta colombica over a period of three days emitted significantly more VOCs than undamaged control plants. Second, the level to which a plant has induced its anti-herbivore defences can affect the LCAs' foraging behaviour: In dual choice bioassays, foragers discriminated control plants from plants that have been damaged mechanically or by LCAs 24 h ago. In contrast, strong induction levels of plants after treatment with the plant hormone jasmonic acid or three days of LCA feeding strongly repelled LCA foragers relative to undamaged control plants. Third, the LCA-specific mode of damaging leaves allows them to remove larger quantities of leaf material before being recognized by the plant: While leaf loss of approximately 15% due to a chewing herbivore (coccinelid beetle) was sufficient to significantly increase VOC emission levels after 24 h, the removal of even 20% of a plant's leaf area within 20 min by LCAs did not affect its VOC emission rate after 24 h. Taken together, our results support the “induced defence hypothesis” and provide first empirical evidence that the foraging behaviour of LCAs is affected by the induction of plant defence responses.
Highlights
Leaf-cutting ants (LCAs) are among the most polyphagous and voracious herbivorous insects known of the Neotropics, cutting up to 15% of the standing leaf crop [1,2] and up to 50% of the species available in the vicinity of their colonies [2,3]
Volatile Emission 24 h after LCA Damage Lima bean plants responded to the different treatments with strong and significant differences in the total amount of volatile organic compounds (VOCs) emitted (Fig. 1A; Welch test: F5, 109 = 7.864, P,0.001)
The most dominant VOCs emitted from jasmonic acid (JA)-treated plants or plants that experienced a combination of LCA damage and JA treatment were (3Z)-hex-3-enyl acetate, (E)-b-ocimene, (R)-(-)linalool, (3E)-4,8-dimethylnona-1,3,7-triene (DMNT), (3E,5E)-2,6dimethyl-1,3,5,7-octatetraene (C10H14), 2,6-dimethylocta-3,5,7triene-2-ol (C10H16O), (3E,7E)-4,8,12-trimethyltrideca-1,3,7,11tetraene (TMTT) (Table 1)
Summary
Leaf-cutting ants (LCAs) are among the most polyphagous and voracious herbivorous insects known of the Neotropics, cutting up to 15% of the standing leaf crop [1,2] and up to 50% of the species available in the vicinity of their colonies [2,3]. As central-place foragers, LCA are expected to minimize the costs of their leaf harvest (i.e. time spend during foraging, trail construction and maintenance) and at the same time maximise their gain in terms of energy intake. This idea, which is encapsulated in the so-called ‘optimal foraging theory’ (OFT, [11]), predicts for an environment with a patchy distribution of food resources that once a suitable food plant has been detected by scouting ants, foraging workers will defoliate it to a point, at which the rate of food intake drops below the average rate for the rest of the habitat. Another prediction made by the OFT is that given two plant individuals with equal leaf qualities (e.g. same plant species), foraging ants should always select the plant individual that is closest to the nest to reduce travelling time
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