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Bacteria may enhance species association in an ant–aphid mutualistic relationship

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Abstract

The mutualistic relationships between certain ant and aphid species are well known, the primary benefits being protection for the aphids and carbohydrate-rich honeydew for the ants. Questions remain, however, as to the exact semiochemical factors that establish and maintain such relationships. In this study, we used a series of treatments and associated controls placed at the end of a two-way olfactometer to determine the degree of attractiveness of a complete plant–aphid–honeydew system as well as individual components of that system. Both the olfactometer branch selected by the black garden ant (Lasius niger) and the linear speed with which ants moved through the device were measured. Study results showed that ants were attracted not just to the complete plant system and the honeydew itself, but also to the microbial flora in the absence of plant or honeydew, and specifically to a bacterium from the black bean aphid (Aphis fabae) honeydew, Staphylococcus xylosus. This bacterium produces a blend of semiochemicals that attract the ant scouts. This information suggests the presence of a naturally occurring, reliable biotic cue for detection of potential aphid partners. This would have to be confirmed in natural conditions by further field experiments. Rather than being opportunistic species that coincidentally colonize a sugar-rich environment, microorganisms living in aphid honeydew may be able to alter emissions of volatile organic compounds (VOCs), thus significantly mediating partner attraction. A bacterial involvement in this mutualistic relationship could alter the manner in which these and similar relationships are viewed and evaluated. Future studies into mutualism stability and function among macroscopic partners will likely need for transition from a two-partner perspective to a multiple-partner perspective, and consider the microbial component, with the potential for one or more taxa making significant contributions to the relationship.

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Acknowledgments

The authors wish to thank Dr. M. Vanderplanck, MSc H. Cawoy, Mr O. Piraux and Mr P. Hacourt for their support during this project. Christophe Fischer is financially supported by a PhD grant from the Fonds pour la formation à la Recherche dans l’Industrie et l’Agriculture (FRIA). This project is also financially supported by a Fonds de la Recherche Fondamentale Collective (F.R.F.C.–F.N.R.S.) research project (2.4600.09).

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Authors and Affiliations

  1. Laboratory of Analytical Chemistry, University of Liege, Gembloux Agro-Bio Tech, Passage des Déportés 2, 5030, Gembloux, Belgium

    Christophe Y. Fischer & Georges C. Lognay

  2. Unit of Social Ecology, Université Libre de Bruxelles, CP231, 50 avenue F. Roosevelt, 1050, Brussels, Belgium

    Claire Detrain

  3. Departamento de Ingenieria Genética, Centro de Investigacion y de Estudios Avanzados del Instituto Politécnico Nacional, Irapuato, Km. 9.6 Libramiento Norte, CP 36821, Irapuato, Guanajuato, Mexico

    Martin Heil

  4. Walloon Center of Industrial Biology, University of Liege, B40, 4000, Sart-Tilman, Belgium

    Alina Grigorescu, Ahmed Sabri & Philippe Thonart

  5. Department of Functional and Evolutionary Entomology, University of Liege, Gembloux Agro-Bio Tech, Passage des Déportés 2, 5030, Gembloux, Belgium

    Eric Haubruge & François J. Verheggen

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  1. Christophe Y. Fischer
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  2. Georges C. Lognay
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  4. Martin Heil
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Correspondence to Christophe Y. Fischer.

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Fischer, C.Y., Lognay, G.C., Detrain, C. et al. Bacteria may enhance species association in an ant–aphid mutualistic relationship. Chemoecology 25, 223–232 (2015). https://doi.org/10.1007/s00049-015-0188-3

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