A Specialist Herbivore Uses Chemical Camouflage to Overcome the Defenses of an Ant-Plant Mutualism

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.