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, 9 (4), e94341
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Variation in Butterfly Larval Acoustics as a Strategy to Infiltrate and Exploit Host Ant Colony Resources

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Variation in Butterfly Larval Acoustics as a Strategy to Infiltrate and Exploit Host Ant Colony Resources

Marco Sala et al. PLoS One.

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.

Conflict of interest statement

Competing Interests: The authors have declared that no competing interests exist.

Figures

Figure 1
Figure 1. The two playback experimental setups.
In the first set of playback bioassays (Type 1) the sounds emitted by Myrmica scabrinodis queens and workers and pre- and post-adoption Maculinea alcon and M. teleius larvae (stimuli) were tested against a white noise (control). In the second experimental setup (Type 2) we tested simultaneously two acoustic stimuli: the sounds of pre-adoption larvae of the two parasite species (M. alcon pre vs. M. teleius pre), the acoustic emissions produced by integrated parasite larvae (M. alcon post- vs. M. teleius post-adoption) and the sound of M. scabrinodis castes (Queen vs. Worker).
Figure 2
Figure 2. Sound emissions of Maculinea larvae and Myrmica ants.
Example waveforms (upper traces) and spectrograms (lower traces) of sounds emitted by pre-adoption and post-adoption larvae of the two parasites (Maculinea alcon and M. teleius) and stridulations produced by Myrmica scabrinodis queens and workers. Mean ± SD of the four pulse parameters are also reported for each insect category.
Figure 3
Figure 3. Principal Components Analysis (PCA) on the four sound parameters.
(a) Two-dimensional plot of the first two factors extracted by principal components analysis over all individual measurements of the four sound parameters (peak frequency, peak power, IQRBW and pulse length) for each insect category - Myrmica scabrinodis queens and workers and Maculinea alcon and M. teleius pre- and post-adoption caterpillars. Ellipses indicate 95% confidence intervals; squares show the centroids for each category. (b) The component loadings extracted by PCA from the four sound parameters are reported in the table. ANOVA based on the 6 groups of samples are also reported.
Figure 4
Figure 4. Worker ant reactions to sound stimuli and white noise.
When the sound stimuli (color bars) were played simultaneously against the white noise (white bars), they always elicited higher behavioural responses on worker ants (experimental setup Type 1). Comparing the sound stimuli, we found that stridulations produced by queens caused stronger reactions in M. scabrinodis ants than those emitted by workers (red vs. yellow bars). Workers reacted more frequently to sounds produced by M. alcon integrated larvae than those emitted by M. alcon pre-adoption caterpillars (dark green vs. pale green) while on the contrary, the sounds emitted by M. teleius pre-adoption larvae caused more frequent reactions in workers than those produced by post-adoption larvae (light blue vs. dark blue) significantly for “antennating”. Different letters indicate significantly different behavioural responses elicited by sound stimuli (Chi square Yates' correction). Significantly (p<0.05) different behavioural frequencies between white noises and sound stimuli are indicated by asterisks. ns  =  statistically not significant.

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References

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Publication types

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.
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