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Indirect effects of mutualism: ant–treehopper associations deter pollinators and reduce reproduction in a tropical shrub

  • Plant-microbe-animal interactions - original research
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Abstract

Animal-pollinated plants can be susceptible to changes in pollinator availability. Honeydew-producing treehoppers frequently occur on inflorescences, potentially enhancing ant-mediated negative effects on pollination services. However, the effect of ant-attended, honeydew-producing insects on plant reproduction remains uncertain. We recorded the abundance of treehoppers and ants on Byrsonima intermedia (Malpighiaceae), and monitored floral visitors in a Brazilian cerrado savanna. We manipulated the presence of ants and ant–treehopper associations on inflorescences to assess their effect on pollination and fruit formation. We used dried ants pinned to inflorescences to evaluate the effect of ant presence and ant identity on potential pollinators. Results show that the presence of treehoppers increases ant abundance on flowers and disrupts pollination by oil-collecting bees, decreasing the frequency and duration of floral visits and reducing fruit and seed set. Treehopper herbivory has no direct effect on fruit or seed production, which are independent of treehopper density. Pinned ants promote avoidance by floral visitors, reducing the number of visits. Ant identity mediates visitation decisions, with Ectatomma brunneum causing greater avoidance by floral visitors than Camponotus rufipes. Field videos show that pollinating bees are harassed by ants near flowers, prompting avoidance behavior by the bees. This is the first demonstration of indirect effects by honeydew-gathering ants, via disrupted pollination, on plant reproduction in tropical cerrado savanna. Our results highlight the importance of studying other interactions near flowers, in addition to just observing pollinators, for a proper understanding of plant reproduction.

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Fig. 1

Photo credits: J. Ibarra-Isassi (a, b); H. Soares Jr (c)

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Acknowledgements

We thank A. Freitas, S. Sendoya, R. Cogni, M. Vidal, A. Nogueira, C. Vieira, and M. Azevedo-Silva for reading early drafts of the manuscript. The final version was considerably improved by comments from S. Koptur, L. Lach, S. Murphy, and M. Pareja. Constructive criticisms from the handling editor, S. Whitehead, and two anonymous reviewers greatly enhanced the revised manuscript. A. Tacioli helped in the field, and S. Sendoya assisted with the statistical analyses. We also thank M. Azevedo-Silva for help with the figures, and H. Soares Jr for editing the videos and for the flower photo. JI-I was supported by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior and the São Paulo Research Foundation (2014/12486-8); PSO was supported by the São Paulo Research Foundation (2014/23141-1), and the Brazilian Research Council (306115/2013-1).

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  1. Javier Ibarra-Isassi

    Present address: Department of Biology, Concordia University, Montreal, QC, H4B-1R6, Canada

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  1. Departamento de Biologia Animal, Universidade Estadual de Campinas, Campinas, SP, 13083-862, Brazil

    Javier Ibarra-Isassi & Paulo S. Oliveira

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  1. Javier Ibarra-Isassi
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JI-I and PSO conceived and designed the experiments. JI-I performed the experiments and analyzed the data. JI-I and PSO wrote the manuscript.

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Correspondence to Paulo S. Oliveira.

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Communicated by Susan Whitehead.

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Ibarra-Isassi, J., Oliveira, P.S. Indirect effects of mutualism: ant–treehopper associations deter pollinators and reduce reproduction in a tropical shrub. Oecologia 186, 691–701 (2018). https://doi.org/10.1007/s00442-017-4045-7

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