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Do leaf cutting ants cut undetected? Testing the effect of ant-induced plant defences on foraging decisions in Atta colombica.

Kost C, Tremmel M, Wirth R - PLoS ONE (2011)

Bottom Line: 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.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.

View Article: PubMed Central - PubMed

Affiliation: Department of Bioorganic Chemistry, Max Planck Institute for Chemical Ecology, Jena, Germany. christiankost@gmail.com

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.

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Hierarchical clustering (UPGMA) of the volatile blends emitted from differentially treated plants.Each tip corresponds to one replicate. Plant treatments were: untreated control (□); LCA herbivory (⧫); scissor damage (▴); pincushion damage (•); JA-treatment (★); LCA-herbivory with subsequent JA-treatment (▪).
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pone-0022340-g002: Hierarchical clustering (UPGMA) of the volatile blends emitted from differentially treated plants.Each tip corresponds to one replicate. Plant treatments were: untreated control (□); LCA herbivory (⧫); scissor damage (▴); pincushion damage (•); JA-treatment (★); LCA-herbivory with subsequent JA-treatment (▪).

Mentions: According to a cluster analysis of all plants that had received one of the five treatments and of which the amounts of each of eight most dominantly emitted VOCs had been quantified (Table 1), the VOC profile emitted from LCA-damaged plants (treatment I) clustered together with undamaged controls and mechanically damaged plants (treatments II and III). In contrast, the JA-treated and ‘JA + LCA-damage’-treated plants (treatments IV and V) that showed the highest emission levels of VOCS (Fig 1A) formed a separate cluster that was distinct from all other treatments (Fig. 2).


Do leaf cutting ants cut undetected? Testing the effect of ant-induced plant defences on foraging decisions in Atta colombica.

Kost C, Tremmel M, Wirth R - PLoS ONE (2011)

Hierarchical clustering (UPGMA) of the volatile blends emitted from differentially treated plants.Each tip corresponds to one replicate. Plant treatments were: untreated control (□); LCA herbivory (⧫); scissor damage (▴); pincushion damage (•); JA-treatment (★); LCA-herbivory with subsequent JA-treatment (▪).
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC3140513&req=5

pone-0022340-g002: Hierarchical clustering (UPGMA) of the volatile blends emitted from differentially treated plants.Each tip corresponds to one replicate. Plant treatments were: untreated control (□); LCA herbivory (⧫); scissor damage (▴); pincushion damage (•); JA-treatment (★); LCA-herbivory with subsequent JA-treatment (▪).
Mentions: According to a cluster analysis of all plants that had received one of the five treatments and of which the amounts of each of eight most dominantly emitted VOCs had been quantified (Table 1), the VOC profile emitted from LCA-damaged plants (treatment I) clustered together with undamaged controls and mechanically damaged plants (treatments II and III). In contrast, the JA-treated and ‘JA + LCA-damage’-treated plants (treatments IV and V) that showed the highest emission levels of VOCS (Fig 1A) formed a separate cluster that was distinct from all other treatments (Fig. 2).

Bottom Line: 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.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.

View Article: PubMed Central - PubMed

Affiliation: Department of Bioorganic Chemistry, Max Planck Institute for Chemical Ecology, Jena, Germany. christiankost@gmail.com

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.

Show MeSH
Related in: MedlinePlus