Chemical camouflage--a frog's strategy to co-exist with aggressive ants - PubMed (original) (raw)

Chemical camouflage--a frog's strategy to co-exist with aggressive ants

Mark-Oliver Rödel et al. PLoS One. 2013.

Abstract

Whereas interspecific associations receive considerable attention in evolutionary, behavioural and ecological literature, the proximate bases for these associations are usually unknown. This in particular applies to associations between vertebrates with invertebrates. The West-African savanna frog Phrynomantis microps lives in the underground nest of ponerine ants (Paltothyreus tarsatus). The ants usually react highly aggressively when disturbed by fiercely stinging, but the frog is not attacked and lives unharmed among the ants. Herein we examined the proximate mechanisms for this unusual association. Experiments with termites and mealworms covered with the skin secretion of the frog revealed that specific chemical compounds seem to prevent the ants from stinging. By HPLC-fractionation of an aqueous solution of the frogs' skin secretion, two peptides of 1,029 and 1,143 Da were isolated and found to inhibit the aggressive behaviour of the ants. By de novo sequencing using tandem mass spectrometry, the amino acid sequence of both peptides consisting of a chain of 9 and 11 residues, respectively, was elucidated. Both peptides were synthesized and tested, and exhibited the same inhibitory properties as the original frog secretions. These novel peptides most likely act as an appeasement allomone and may serve as models for taming insect aggression.

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Conflict of interest statement

Competing Interests: This is to certify that Reto Stocklin is the co-founder, owner, president and CEO of Atheris Laboratories, a biotechnology company working in the field of discovery of bio-active molecules from animal venoms and other natural origins. This does not alter the authors′ adherence to all the PLOS ONE policies on sharing data and materials of the work submitted, and the authors hereby certify that there is no financial or non-financial competing of interest for this manuscript to be published, in accordance with the PLOS ONE policies.

Figures

Figure 1

Figure 1. Time from first ant, Paltothyreus tarsatus, contact with termites (left; inlet A) or mealworms (right), coated with the skin secretion of Phrynomantis microps, until stinging (inlet B).

Control groups are termites or mealworms coated with water. Boxplots show the median and the interquartiles of time from first ant contact with a termite or mealworm until stinging. Coated insects were stung significantly later than control insects.

Figure 2

Figure 2. Fractionation of the skin secretion from Phrynomantis microps by reversed-phase HPLC on a LiChroCART column, 125×4 mm (Merck, Darmstadt) which was eluted with a linear gradient from 0 to 60% acetonitrile in 0.1% trifluoroacetic acid (dotted line) over 60 min at a flow rate of 0.5 ml/min.

Absorbance was monitored at 220(above). Below: Total ion chromatogram (TIC) of liquid chromatography-time-of-flight mass spectrometry (LC/TOF MS) analysis of the HPLC fraction containing two peptides: m/z 1029.506 and m/z 1143.548 (non-protonated). De novo sequencing of the peptides suggested the tentative sequences as indicated in the chromatograms. Inlet picture: adult Phrynomantis microps examined by Paltothyreus tarsatus workers.

Figure 3

Figure 3. Effect of the two peptides from the skin secretion of Phrynomantis microps applied to termite, Macrotermes bellicosus, soldiers and delaying the aggressive behaviour and stinging of Paltothyreus tarsatus ants.

Maximum observation time was 20

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Grants and funding

This study was part of the BIOLOG-program of the German Ministry of Education and Science (BMB+F, http://www.bmbf.de/; Project BIOTA-West III, amphibian projects, 01LC0617J). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

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