Evidence of indirect biotic resistance: native ants decrease invasive plant fitness by enhancing aphid infestation

Abstract

The biotic resistance hypothesis asserts that native species may hinder the invasion of exotic species, which can occur either directly or indirectly by influencing interactions between exotic and local species. Aphid-tending ants may play a key role in the indirect biotic resistance to plant invasion. Ants may protect aphids, thus increasing their negative effect on exotic plants, but may also deter chewing herbivores, thus benefiting exotic plants. We studied native aphid-tending ants (Dorymyrmex tener, Camponotus distinguendus, and Dorymyrmex richteri) on exotic nodding thistles (Carduus thoermeri), which are attacked by thistle aphids (Brachycaudus cardui) and thistle-head weevils (Rhinocyllus conicus). We evaluated the impact of ants, aphids, and weevils on thistle seed set. We compared ant species aggressiveness towards aphid predators and weevils and performed ant-exclusion experiments to determine the effects of ants on aphid predators and weevils. We analysed whether ant species affected thistle seed set through their effects on aphids and/or weevils. The ant D. tener showed the most aggressive behaviour towards aphid predators and weevils. Further, D. tener successfully removed aphid predators from thistles but did not affect weevils. Excluding D. tener from thistles increased seed set. Analyses supported a negative indirect pathway between the aggressive D. tener and thistle seed set through aphid populations, while the other ant species showed no indirect effects on thistle reproduction. Therefore, aggressive aphid-tending ants may enhance biotic resistance by increasing aphid infestation on exotic invasive plants. This study highlights the importance of indirect biotic resistance in modulating the success of invasive species.

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Data availability

The datasets generated during and/or analysed during the current study will be available in the Figshare Data Repository (https://figshare.com/).

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Acknowledgements

Thanks to M Rodriguez-Cabal who gave valuable suggestions to an earlier version of the manuscript. Thanks to A Lovrich, T Gonzalez, and D Gonzalez who assisted in the field, and L Ammassari who processed samples in the laboratory. Thanks to an anonymous reviewer who provided numerous recommendations that improved the clarity and quality of the manuscript. AM Devegili is supported by a doctoral fellowship from the Consejo Nacional de Investigaciones Científicas y Técnicas of Argentina.

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This study was conducted without funding.

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All authors conceived and designed the experiments; AMD collected the data and performed the experiments; AMD analysed the data; AMD led the writing of the manuscript, to which all authors contributed.

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Correspondence to Andrés M. Devegili.

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All applicable institutional and/or national guidelines for the care and use of animals were followed.

Additional information

Combining field observations and experiments, we show that aggressive aphid-tending ants can enhance biotic resistance by increasing aphid infestation on an exotic plant.

Communicated by Diethart Matthies.

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Devegili, A.M., Lescano, M.N., Gianoli, E. et al. Evidence of indirect biotic resistance: native ants decrease invasive plant fitness by enhancing aphid infestation. Oecologia (2021). https://doi.org/10.1007/s00442-021-04874-2

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Keywords

  • Exotic plants
  • Aphid
  • Aphid-tending ants
  • Biotic resistance
  • Indirect interactions