The Pied Piper: A Parasitic Beetle’s Melodies Modulate Ant Behaviours

Abstract

Ants use various communication channels to regulate their social organisation. The main channel that drives almost all the ants’ activities and behaviours is the chemical one, but it is long acknowledged that the acoustic channel also plays an important role. However, very little is known regarding exploitation of the acoustical channel by myrmecophile parasites to infiltrate the ant society. Among social parasites, the ant nest beetles (Paussus) are obligate myrmecophiles able to move throughout the colony at will and prey on the ants, surprisingly never eliciting aggression from the colonies. It has been recently postulated that stridulatory organs in Paussus might be evolved as an acoustic mechanism to interact with ants. Here, we survey the role of acoustic signals employed in the Paussus beetle-Pheidole ant system. Ants parasitised by Paussus beetles produce caste-specific stridulations. We found that Paussus can “speak” three different “languages”, each similar to sounds produced by different ant castes (workers, soldiers, queen). Playback experiments were used to test how host ants respond to the sounds emitted by Paussus. Our data suggest that, by mimicking the stridulations of the queen, Paussus is able to dupe the workers of its host and to be treated as royalty. This is the first report of acoustic mimicry in a beetle parasite of ants.

Acoustic communication within ant societies and its mimicry by mutualistic and socially parasitic myrmecophiles

“…Barbero, Thomas et al, 2009;DeVries, 1990DeVries, , 1991aPierce et al, 2002). However, similar phenomena were recently described from adults of a socially parasitic beetle, Paussus favieri (Di Giulio et al, 2015), where males and females emit mimetic stridulations using a row of scrapers on the proximal abdominal segment rasping across a file located on the hind femora (see Fig. 1p-t).…”

“…Acoustic patterns also signal caste and hierarchical status in at least two genera of Myrmicinae ants: Myrmica (Barbero, Thomas et al, 2009) and Pheidole (Di Giulio et al, 2015). In both taxa, the queens produce distinctive stridulations which, when played back to kin workers, elicit additional 'royal' protective behaviours compared with responses to worker signals (Barbero, Bonelli, Thomas, Balletto, & Schönrogge, 2009;Barbero & Casacci, 2015;Barbero, Thomas et al, 2009;Casacci et al, 2013;Ferreira, Poteaux, Delabie, Fresneau, & Rybak, 2010).…”

“…In both taxa, the queens produce distinctive stridulations which, when played back to kin workers, elicit additional 'royal' protective behaviours compared with responses to worker signals (Barbero, Bonelli, Thomas, Balletto, & Schönrogge, 2009;Barbero & Casacci, 2015;Barbero, Thomas et al, 2009;Casacci et al, 2013;Ferreira, Poteaux, Delabie, Fresneau, & Rybak, 2010). In addition, in Pheidole pallidula the soldier and minor worker castes also make distinctive vibroacoustic signals (Di Giulio et al, 2015). Unlike Pachycondyla species, little inter-specific variation was detected in either the queen-or worker-sounds made by closelyrelated sympatric species of Myrmica (Barbero et al, 2012;Barbero, Thomas et al, 2009; Thomas, Schönrogge, Bonelli, Barbero, & Balletto, 2010), which are instead clearly demarcated by unique hydrocarbon profiles (Elmes, Akino, Thomas, Clarke, & Knapp, 2002).…”

Phylogeny of PaussusL. (Carabidae: Paussinae): unravelling morphological convergence associated with myrmecophilous life histories

“…Moreover, both P. favieri and the host queen stridulate back and forth during this interaction. Indeed, acoustic communication and deception appear to play an important role in their integration into the ant society (Di Giulio et al, 2015). Females lay their eggs in the ant nest and this is where the beetle larvae develop.…”

Strategies of the beetle Oochrotus unicolor (Tenebrionidae) thriving in the waste dumps of seed‐harvesting Messor ants (Formicidae)

“…The strategies of inquilines living in the brood chambers of social insects are much better explored (Hölldobler, ; Cammaerts, ; Akino & Knapp, ; Di Giulio et al ., ) than those of other niches. It would be useful to broaden our knowledge on the adaptations and strategies of social insect associates that colonise non‐brood associated niches such as waste dumps.…”