Widespread Chemical Detoxification of Alkaloid Venom by Formicine Ants

Abstract

The ability to detoxify defensive compounds of competitors provides key ecological advantages that can influence community-level processes. Although common in plants and bacteria, this type of detoxification interaction is extremely rare in animals. Here, using laboratory behavioral assays and analyses of videotaped interactions in South America, we report widespread venom detoxification among ants in the subfamily Formicinae. Across both data sets, nine formicine species, representing all major clades, used a stereotyped grooming behavior to self-apply formic acid (acidopore grooming) in response to fire ant (Solenopsis invicta and S. saevissima) venom exposure. In laboratory assays, this behavior increased the survivorship of species following exposure to S. invicta venom. Species expressed the behavior when exposed to additional alkaloid venoms, including both compositionally similar piperidine venom of an additional fire ant species and the pyrrolidine/pyrroline alkaloid venom of a Monomorium species. In addition, species expressed the behavior following exposure to the uncharacterized venom of a Crematogaster species. However, species did not express acidopore grooming when confronted with protein-based ant venoms or when exposed to monoterpenoid-based venom. This pattern, combined with the specific chemistry of the reaction of formic acid with venom alkaloids, indicates that alkaloid venoms are targets of detoxification grooming. Solenopsis thief ants, and Monomorium species stand out as brood-predators of formicine ants that produce piperidine, pyrrolidine, and pyrroline venom, providing an important ecological context for the use of detoxification behavior. Detoxification behavior also represents a mechanism that can influence the order of assemblage dominance hierarchies surrounding food competition. Thus, this behavior likely influences ant-assemblages through a variety of ecological pathways.

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Acknowledgments

We thank Thanapat Pongwarin for technical assistance. Nathan Jones and Rob Plowes provided useful discussion. Alex Wild and James Trager contributed to species identification. Two anonymous reviewers improved the quality of the manuscript. Donald H. Feener was a Co-PI on the NSF grant funding the original Brazil research. Texas Parks and Wildlife, Chaparral Wildlife Management Area and Conselho Nacional de Desevolvimento Cientifico e Tecnológico (CNPq) provided permission to conduct research. Universidade Federal do Mato Grosso do Sul provided access to Base de Estudos do Pantanal, and Sergio Seike and Woody Benson coordinated the Brazilian research. Funding was provided by Lee and Ramona Bass Foundation (to LEG) and National Science Foundation, U.S.A. (DEB - 9528120 to LEG and DHF). Data are available on the Dryad Digital Repository.

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Correspondence to Edward G. LeBrun.

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LeBrun, E.G., Diebold, P.J., Orr, M.R. et al. Widespread Chemical Detoxification of Alkaloid Venom by Formicine Ants. J Chem Ecol 41, 884–895 (2015). https://doi.org/10.1007/s10886-015-0625-3

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Keywords

  • Antibiosis
  • Formicinae
  • Alkaloid
  • Venom
  • Ant assemblage
  • Tawny crazy ant