Abstract
Many plants and ants engage in mutualisms where plants provide food and shelter to the ants in exchange for protection against herbivores and competitors. Although several species of herbivores thwart ant defenses and extract resources from the plants, the mechanisms that allow these herbivores to avoid attack are poorly understood. The specialist insect herbivore, Piezogaster reclusus (Hemiptera: Coreidae), feeds on Neotropical bull-horn acacias (Vachellia collinsii) despite the presence of Pseudomyrmex spinicola ants that nest in and aggressively defend the trees. We tested three hypotheses for how P. reclusus feeds on V. collinsii while avoiding ant attack: (1) chemical camouflage via cuticular surface compounds, (2) chemical deterrence via metathoracic defense glands, and (3) behavioral traits that reduce ant detection or attack. Our results showed that compounds from both P. reclusus cuticles and metathoracic glands reduce the number of ant attacks, but only cuticular compounds appear to be essential in allowing P. reclusus to feed on bull-horn acacia trees undisturbed. In addition, we found that ant attack rates to P. reclusus increased significantly when individuals were transferred between P. spinicola ant colonies. These results are consistent with the hypothesis that chemical mimicry of colony-specific ant or host plant odors plays a key role in allowing P. reclusus to circumvent ant defenses and gain access to important resources, including food and possibly enemy-free space. This interaction between ants, acacias, and their herbivores provides an excellent example of the ability of herbivores to adapt to ant defenses of plants and suggests that herbivores may play an important role in the evolution and maintenance of mutualisms.
Highlights
Ant-plant mutualisms are a common and widespread feature of both temperate and tropical ecosystems [1,2]
Ant responses to extracted chemical compounds In the ‘‘cuticular compounds’’ experiment (Exp. 1a), cotton swabs treated with extracted cuticular compounds were attacked in 16% of encounters, significantly less often than lanolin-only controls, which were attacked in 33% of encounters (GLMM; X 2 = 12.73, df = 1, p = 0.00036; Fig. 2A)
In the ‘‘glandular compounds’’ experiment (Exp. 1b), cotton swabs treated with glandular compounds were attacked in 3% of encounters, significantly less often than controls, which were attacked in 77% of encounters (GLMM; X 2 = 51.51, df = 1, p,0.0001; Fig. 2B)
Summary
Ant-plant mutualisms are a common and widespread feature of both temperate and tropical ecosystems [1,2] These interactions generally involve plants providing food and/or shelter to ants in exchange for protection from herbivores and competitors [3,4,5]. Ant-plant mutualisms involve diverse taxa, in the tropics, including at least 100 plant genera and 40 species of ants that engage in interactions from generalized and facultative to highly specialized and obligate [6,7] These conspicuous examples of indirect plant defense are model systems for understanding plant defense theory, food web structure, species coexistence, plant/animal coevolution, and the evolutionary stability of mutualisms [8]. An improved understanding of these and other potential adaptations to ant-defense systems can provide insights into the evolutionary dynamics and maintenance of ant-plant-herbivore interactions, and the exploitation of mutualistic interactions in complex communities, in general
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