Abstract

Introduction: Herbivores specialized in consuming ant-defended plants evolve strategies to prevent the attack of ant workers. When the plant can associate with more than one ant species, the herbivore evasion strategies may either be species-specific, or flexible enough to successfully deter workers of different ant-plant species. Objectives: We studied the behavior of an herbivore bug (Piezogaster reclusus) on ant-defended acacia trees (Vachellia collinsii), which associates with one of three mutualistic Pseudomyrmex ant species, and report the geographical distribution of the acacia bug species of Costa Rica and Panama. Methods: We tested whether herbivore bugs (1) associate with a particular ant species; (2) use chemical or behavioral strategies to evade the ant workers; (3) adjust the evasion strategy to the ant species living on the acacia tree. We also compared collected acacia bugs with Museum specimens to clarify the identification from Costa Rica and Panama. Results: We found bugs more often on trees with ants, particularly Ps. spinicola, and never on trees with Ps. nigrocinctus. To avoid ant attacks, bugs use evasive behaviors to prevent encounters with the ant workers, that depended on the ant species. Also, indirect evidence of intra and interspecific transfer experiments suggest species-specific chemical camouflage or repellence. We also report an expansion of the Southern limit of Pi. reclusus distribution in Central Panama, and reduced the distribution of Pi. chontalesis to the Chiriquí region. Conclusions: Similar to herbivores specialized on chemically defended plants, herbivores on ant-defended trees could evolve specific mechanisms to deal with the plant defenses. However, plants associated with multiple partners are a challenge to herbivore specialization, and might require behavioral plasticity, as our evidence suggests.

Highlights

  • Herbivores specialized in consuming ant-defended plants evolve strategies to prevent the attack of ant workers

  • Bug transfers: The proportion of ants attacking bugs that were transferred to other trees with the same ant species was similar to the control, in bugs originally found on trees with Ps. spinicola (Fig. 3A; Wilcoxon matched-pairs test, V = 4, P = 0.85, N = 5) or Ps. flavicornis (Fig. 3C; Wilcoxon matched-pairs test, V = 4, P = 0.43, N = 5)

  • In the protective mutualism of acacia ants, we found that sap-feeding Pi. reclusus bugs are four times more likely to be associated with acacias inhabited by one of three mutualistic ant species

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Summary

Introduction

Herbivores specialized in consuming ant-defended plants evolve strategies to prevent the attack of ant workers. Objectives: We studied the behavior of an herbivore bug (Piezogaster reclusus) on antdefended acacia trees (Vachellia collinsii), which associates with one of three mutualistic Pseudomyrmex ant species, and report the geographical distribution of the acacia bug species of Costa Rica and Panama. Methods: We tested whether herbivore bugs (1) associate with a particular ant species; (2) use chemical or behavioral strategies to evade the ant workers; (3) adjust the evasion strategy to the ant species living on the acacia tree. Bugs use evasive behaviors to prevent encounters with the ant workers, that depended on the ant species. Conclusions: Similar to herbivores specialized on chemically defended plants, herbivores on ant-defended trees could evolve specific mechanisms to deal with the plant defenses. Plants associated with multiple partners are a challenge to herbivore specialization, and might require behavioral plasticity, as our evidence suggests

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