Variation in butterfly larval acoustics as a strategy to infiltrate and exploit host ant colony resources

PLoS One. 2014 Apr 9;9(4):e94341. doi: 10.1371/journal.pone.0094341. eCollection 2014.

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.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Acoustic Stimulation
  • Acoustics*
  • Animals
  • Ants / parasitology*
  • Behavior, Animal
  • Butterflies / physiology*
  • Larva / physiology
  • Parasites
  • Principal Component Analysis
  • Sound
  • Tape Recording

Grant support

This research was carried out within the project CLIMIT (Climate Change Impacts on Insects and their Mitigation; Settele & Kühn, 2009; Thomas, Simcox & Clarke, 2009) funded by DLR-BMBF (Germany), NERC and DEFRA (UK), ANR (France), Formas (Sweden), and Swedish EPA (Sweden) through the FP6 BiodivERsA Eranet, as well as by the project ‘A multitaxa approach to study the impact of climate change on the biodiversity of Italian ecosystems’ of the Italian Ministry of Education, University and Research (MIUR). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.