Abstract
About 10,000 arthropods live as ants' social parasites and have evolved a number of mechanisms allowing them to penetrate and survive inside the ant nests. Many of them can intercept and manipulate their host communication systems. This is particularly important for butterflies of the genus Maculinea, which spend the majority of their lifecycle inside Myrmica ant nests. Once in the colony, caterpillars of Maculinea “predatory species” directly feed on the ant larvae, while those of “cuckoo species” are fed primarily by attendance workers, by trophallaxis. It has been shown that Maculinea cuckoo larvae are able to reach a higher social status within the colony's hierarchy by mimicking the acoustic signals of their host queen ants. In this research we tested if, when and how myrmecophilous butterflies may change sound emissions depending on their integration level and on stages of their life cycle. We studied how a Maculinea predatory species (M. teleius) can acoustically interact with their host ants and highlighted differences with respect to a cuckoo species (M. alcon). We recorded sounds emitted by Maculinea larvae as well as by their Myrmica hosts, and performed playback experiments to assess the parasites' capacity to interfere with the host acoustic communication system. We found that, although varying between and within butterfly species, the larval acoustic emissions are more similar to queens' than to workers' stridulations. Nevertheless playback experiments showed that ant workers responded most strongly to the sounds emitted by the integrated (i.e. post-adoption) larvae of the cuckoo species, as well as by those of predatory species recorded before any contact with the host ants (i.e. in pre-adoption), thereby revealing the role of acoustic signals both in parasite integration and in adoption rituals. We discuss our findings in the broader context of parasite adaptations, comparing effects of acoustical and chemical mimicry.
Highlights
Ants dominate most terrestrial ecosystems [1] and their colonies are so aggressively defended that they may act as shelters for any similar-sized organisms having evolved the necessary strategies to penetrate and live in their nests [2,3,4,5]
We assayed the functions of these sounds in playback experiments, and our data revealed that stridulations made by M. scabrinodis queens resulted in more obvious reactions from the ants compared to stridulations produced by their own workers, for almost all observed behaviours (Fig. 4; Experiment Type 2)
We demonstrated the ability of two Maculinea species to break their host’s communication code by mimicking the acoustic signals of the host ants (Fig. 4)
Summary
Ants dominate most terrestrial ecosystems [1] and their colonies are so aggressively defended that they may act as shelters for any similar-sized organisms having evolved the necessary strategies to penetrate and live in their nests [2,3,4,5]. Ants have evolved a complex set of signals which allow colony members to distinguish between nest-mates and intruders. Even though sound production is not usually the dominant strategy, acoustic communication plays a wide range of roles in the ants’ social behaviour, from reciprocal attraction to inter-caste interactions and it has been suggested that sounds are involved in the modulation of other signals Sound stimuli are effective only at small distances and are mainly used by ants for forager recruitment, mating requests, intimidation, aposematic ‘‘threatening’’, or as signals of alarm [1,14,15,16] (see [17] for a review of intracolony vibroacoustic communication)
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