Abstract

BackgroundAnt colonies are plagued by a diversity of arthropod guests, which adopt various strategies to avoid or to withstand host attacks. Chemical mimicry of host recognition cues is, for example, a common integration strategy of ant guests. The morphological gestalt and body size of ant guests have long been argued to also affect host hostility, but quantitative studies testing these predictions are largely missing. We here evaluated three guest traits as triggers of host aggression—body size, morphological gestalt, and accuracy in chemical mimicry—in a community of six Eciton army ant species and 29 guest species. We quantified ant aggression towards 314 guests in behavioral assays and, for the same individuals, determined their body size and their accuracy in mimicking ant cuticular hydrocarbon (CHC) profiles. We classified guests into the following gestalts: protective, myrmecoid, staphylinid-like, phorid-like, and larval-shaped. We expected that (1) guests with lower CHC mimicry accuracy are more frequently attacked; (2) larger guests are more frequently attacked; (3) guests of different morphological gestalt receive differing host aggression levels.ResultsArmy ant species had distinct CHC profiles and accuracy of mimicking these profiles was variable among guests, with many species showing high mimicry accuracy. Unexpectedly, we did not find a clear relationship between chemical host similarity and host aggression, suggesting that other symbiont traits need to be considered. We detected a relationship between the guests’ body size and the received host aggression, in that diminutive forms were rarely attacked. Our data also indicated that morphological gestalt might be a valuable predictor of host aggression. While most ant-guest encounters remained peaceful, host behavior still differed towards guests in that ant aggression was primarily directed towards those guests possessing a protective or a staphylinid-like gestalt.ConclusionWe demonstrate that CHC mimicry accuracy does not necessarily predict host aggression towards ant symbionts. Exploitation mechanisms are diverse, and we conclude that, besides chemical mimicry, other factors such as the guests’ morphological gestalt and especially their body size might be important, yet underrated traits shaping the level of host hostility against social insect symbionts.

Highlights

  • Ant colonies are plagued by a diversity of arthropod guests, which adopt various strategies to avoid or to withstand host attacks

  • We recently showed that 62 species of ant guests, or myrmecophiles, from diverse taxa infiltrate the colonies of Eciton army ants in a Costa Rican population [75]

  • Using standardized behavioral tests in laboratory nests, we studied the effect of three guest traits on the degree of host aggression towards Eciton myrmecophiles: accuracy in chemical mimicry of host recognition cues, body size, and morphological gestalt

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Summary

Introduction

Ant colonies are plagued by a diversity of arthropod guests, which adopt various strategies to avoid or to withstand host attacks. The colonies of social insects are plagued by numerous predators, parasitoids, parasites, and commensals [1,2,3,4] Among these are organisms as diverse as chimpanzees and anteaters preying on social insects [5,6,7,8], endoparasitic nematodes and fungi altering the behavior of social insect workers [3, 9,10,11,12], and various arthropods taking advantage of the abundant resources accumulating in and around social insect colonies [13,14,15,16]. Besides chemical mimicry and chemical hiding (sensu [32]), behavioral adaptations, vibroacoustic mimicry, chemical trickery (e.g., adoption glands [37]) and chemical weaponry (e.g., defensive glands [21]), as well as the morphological gestalt and body size of social insect guests might be important for successful exploitation of host colonies [23, 27, 37,38,39,40,41]

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