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

Di Giulio A, Maurizi E, Barbero F, Sala M, Fattorini S, Balletto E, Bonelli S - PLoS ONE (2015)

Bottom Line: We found that Paussus can "speak" three different "languages", each similar to sounds produced by different ant castes (workers, soldiers, queen).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.

View Article: PubMed Central - PubMed

Affiliation: Department of Science, University Roma Tre, Viale G. Marconi 446, I-00146 Rome, Italy.

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.

No MeSH data available.


Related in: MedlinePlus

Playback experiments.Behavioural responses of Pheidole pallidula colonies to sound recordings of Paussus favieri (single pulses), P. favieri (trains), Pheidole pallidula queens, P. pallidula soldiers, P. pallidula workers, and to two controls (white noise and silence) are shown. Five benevolent behaviours were observed; no antagonistic behaviour was observed. GLM testing for the effect of sounds and colony showed a significant overall difference in responses occurred within five behaviours (N = 140; Walking: Fstimuli = 22.623, df = 6, P < 0.001, Fnest = 1.253, df = 9, P = 0.284; Antennate: F stimuli = 39.414, df = 6, P < 0.001, Fnest = 1.221, df = 9, P = 0.302; Guarding: F stimuli = 12.942, df = 6, P < 0.001, Fnest = 1.388, df = 9, P = 0.216; Digging: Fstimuli = 2.667, df = 6, P = 0.024, Fnest = 0.667, df = 9, P = 0.735; Staying: Fstimuli = 5.083, df = 6, P = 0.004, Fnest = 1.856, df = 9, P = 0.079). The letters above each column indicate significance (P < 0.05) in pairwise post hoc Tukey tests. The same letter indicates no significant difference within each type of behaviour.
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pone.0130541.g004: Playback experiments.Behavioural responses of Pheidole pallidula colonies to sound recordings of Paussus favieri (single pulses), P. favieri (trains), Pheidole pallidula queens, P. pallidula soldiers, P. pallidula workers, and to two controls (white noise and silence) are shown. Five benevolent behaviours were observed; no antagonistic behaviour was observed. GLM testing for the effect of sounds and colony showed a significant overall difference in responses occurred within five behaviours (N = 140; Walking: Fstimuli = 22.623, df = 6, P < 0.001, Fnest = 1.253, df = 9, P = 0.284; Antennate: F stimuli = 39.414, df = 6, P < 0.001, Fnest = 1.221, df = 9, P = 0.302; Guarding: F stimuli = 12.942, df = 6, P < 0.001, Fnest = 1.388, df = 9, P = 0.216; Digging: Fstimuli = 2.667, df = 6, P = 0.024, Fnest = 0.667, df = 9, P = 0.735; Staying: Fstimuli = 5.083, df = 6, P = 0.004, Fnest = 1.856, df = 9, P = 0.079). The letters above each column indicate significance (P < 0.05) in pairwise post hoc Tukey tests. The same letter indicates no significant difference within each type of behaviour.

Mentions: In playback experiments, we did not observe any antagonistic or alarmed ant behaviour, but always non-aggressive responses involving attraction (walking, antennating and staying) and interaction with other ant castes (guarding, digging). A GLM analysis showed that workers’ reactions to the sound stimuli were significantly different from controls for all observed behaviours. Behaviours such as guarding, digging and staying were not produced by controls (Fig 4). Pheidole pallidula ants were attracted to and induced to “walk” on the speaker by all the sound stimuli, showing no differences in the frequency of responses to the beetle’s or ant castes’ stridulations. Interestingly, playback of P. favieri’s stridulations produced a number of antennations similar to that elicited by sounds emitted by Pheidole pallidula queens. Soldiers’ stridulations elicited a smaller amount of antennations, but not statistically different from those elicited by Paussus favieri single pulses or worker stridulations. Results for antennation are remarkable because this behaviour is known to be linked to nest-mate recognition, recruitment, or to facilitate trophallaxis or pheromone emission [25–27]. Guarding was only induced by Paussus favieri and queens’ sounds. Workers responded to these stimuli by assuming a posture similar to that adopted when they attended queens or objects of great value to their society [2,28]. The queen’s sounds produced the highest occurrences of guarding, which is consistent with the high status and protection afforded to queens in the colony’s hierarchy. One of the most stunning results of the present study is that the emission of single pulses (Pc) of Paussus favieri elicited in worker ants a guarding behaviour that is statistically no different than when presented with emissions of the queen (Fig 4). These findings, together with the highest similarity between Pc and queen stridulations (demonstrated by both uni- and multivariate analyses), support our hypothesis that single pulses are used by the beetle to be treated like a queen by its host ants.


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

Di Giulio A, Maurizi E, Barbero F, Sala M, Fattorini S, Balletto E, Bonelli S - PLoS ONE (2015)

Playback experiments.Behavioural responses of Pheidole pallidula colonies to sound recordings of Paussus favieri (single pulses), P. favieri (trains), Pheidole pallidula queens, P. pallidula soldiers, P. pallidula workers, and to two controls (white noise and silence) are shown. Five benevolent behaviours were observed; no antagonistic behaviour was observed. GLM testing for the effect of sounds and colony showed a significant overall difference in responses occurred within five behaviours (N = 140; Walking: Fstimuli = 22.623, df = 6, P < 0.001, Fnest = 1.253, df = 9, P = 0.284; Antennate: F stimuli = 39.414, df = 6, P < 0.001, Fnest = 1.221, df = 9, P = 0.302; Guarding: F stimuli = 12.942, df = 6, P < 0.001, Fnest = 1.388, df = 9, P = 0.216; Digging: Fstimuli = 2.667, df = 6, P = 0.024, Fnest = 0.667, df = 9, P = 0.735; Staying: Fstimuli = 5.083, df = 6, P = 0.004, Fnest = 1.856, df = 9, P = 0.079). The letters above each column indicate significance (P < 0.05) in pairwise post hoc Tukey tests. The same letter indicates no significant difference within each type of behaviour.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4496082&req=5

pone.0130541.g004: Playback experiments.Behavioural responses of Pheidole pallidula colonies to sound recordings of Paussus favieri (single pulses), P. favieri (trains), Pheidole pallidula queens, P. pallidula soldiers, P. pallidula workers, and to two controls (white noise and silence) are shown. Five benevolent behaviours were observed; no antagonistic behaviour was observed. GLM testing for the effect of sounds and colony showed a significant overall difference in responses occurred within five behaviours (N = 140; Walking: Fstimuli = 22.623, df = 6, P < 0.001, Fnest = 1.253, df = 9, P = 0.284; Antennate: F stimuli = 39.414, df = 6, P < 0.001, Fnest = 1.221, df = 9, P = 0.302; Guarding: F stimuli = 12.942, df = 6, P < 0.001, Fnest = 1.388, df = 9, P = 0.216; Digging: Fstimuli = 2.667, df = 6, P = 0.024, Fnest = 0.667, df = 9, P = 0.735; Staying: Fstimuli = 5.083, df = 6, P = 0.004, Fnest = 1.856, df = 9, P = 0.079). The letters above each column indicate significance (P < 0.05) in pairwise post hoc Tukey tests. The same letter indicates no significant difference within each type of behaviour.
Mentions: In playback experiments, we did not observe any antagonistic or alarmed ant behaviour, but always non-aggressive responses involving attraction (walking, antennating and staying) and interaction with other ant castes (guarding, digging). A GLM analysis showed that workers’ reactions to the sound stimuli were significantly different from controls for all observed behaviours. Behaviours such as guarding, digging and staying were not produced by controls (Fig 4). Pheidole pallidula ants were attracted to and induced to “walk” on the speaker by all the sound stimuli, showing no differences in the frequency of responses to the beetle’s or ant castes’ stridulations. Interestingly, playback of P. favieri’s stridulations produced a number of antennations similar to that elicited by sounds emitted by Pheidole pallidula queens. Soldiers’ stridulations elicited a smaller amount of antennations, but not statistically different from those elicited by Paussus favieri single pulses or worker stridulations. Results for antennation are remarkable because this behaviour is known to be linked to nest-mate recognition, recruitment, or to facilitate trophallaxis or pheromone emission [25–27]. Guarding was only induced by Paussus favieri and queens’ sounds. Workers responded to these stimuli by assuming a posture similar to that adopted when they attended queens or objects of great value to their society [2,28]. The queen’s sounds produced the highest occurrences of guarding, which is consistent with the high status and protection afforded to queens in the colony’s hierarchy. One of the most stunning results of the present study is that the emission of single pulses (Pc) of Paussus favieri elicited in worker ants a guarding behaviour that is statistically no different than when presented with emissions of the queen (Fig 4). These findings, together with the highest similarity between Pc and queen stridulations (demonstrated by both uni- and multivariate analyses), support our hypothesis that single pulses are used by the beetle to be treated like a queen by its host ants.

Bottom Line: We found that Paussus can "speak" three different "languages", each similar to sounds produced by different ant castes (workers, soldiers, queen).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.

View Article: PubMed Central - PubMed

Affiliation: Department of Science, University Roma Tre, Viale G. Marconi 446, I-00146 Rome, Italy.

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.

No MeSH data available.


Related in: MedlinePlus