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Dillapiole in Piper holtonii as an Inhibitor of the Symbiotic Fungus Leucoagaricus gongylophorus of Leaf-Cutting Ants

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Abstract

Plants of the Piperaceae family are studied for their diverse secondary metabolism with a vast array of compounds that act as chemical defense agents against herbivores. Of all the agricultural pests, the management of insects is a highly significant challenge in the Neotropics, and ants of the Attini tribe pose a major problem. Due to their symbiotic association with the fungus Leucoagaricus gongylophorus (Möller) Singer (Agaricaceae), the species of Atta and Acromyrmex have exhaustive foraging activity which has intensified as deforestation and monoculture farming have increased. The control of leaf-cutting ants is still carried out with synthetic products with negative consequences to the environment and human health. In search for natural and sustainable alternatives to synthetic pesticides, Piper holtonii C. DC. was selected among other plant species after field observations of the foraging activity of Atta cephalotes, which revealed that P. holtonii was never chosen by ants. In vitro evaluation of an ethanol extract of the leaves of P. holtonii resulted in promising inhibitory activity (IC50 102 ppm) against L. gongylophorus. Subsequently, bioassay-guided fractionation led to the isolation of the phenylpropanoid dillapiole, which was also detected in the essential oil. This compound demonstrated inhibition of the fungus with an IC50 of 38 ppm. Considering the symbiotic relationship between the Attini ants and L. gongylophorus, the negative effect on the survival of one of the organisms will affect the survival of the other, so dillapiole or standardized essential oil extracts of P. holtonii containing this active principle could be a unique and useful source as a control agent for leaf cutting-ants.

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Acknowledgements

Authors acknowledge the “Departamento Administrativo de Ciencia, Tecnología e Innovación, COLCIENCIAS” for the financial support under the project 495–2009. Also, the authors thank Empresas Publicas de Medellin (EPM) and Fundacion Berta Arias de Botero (FUNDARIAS) for allowing the collection of the material on their land. We are thankful to Professor Álvaro Duque for his advice in the statistical analysis and Professor Emeritus Geoffrey A. Cordell for reviewing the manuscript and the language structure prior to submission.

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Authors and Affiliations

  1. Escuela de Química, Facultad de Ciencias, Universidad Nacional de Colombia-sede Medellín, Cra 65 59ª-110, Medellín, Colombia

    Lina Cristina Salazar

  2. Grupo de Grupo de Sustancias Activas y Biotecnología (SaBio), Escuela de Biociencias, Universidad Nacional de Colombia-sede Medellín, Cra 65 59ª-110, Medellín, Colombia

    Adriana Ortiz-Reyes

  3. Escuela de Biociencias, Universidad Nacional de Colombia- sede Medellín, Cra 65 59ª-110, Medellín, Colombia

    Diana Marcela Rosero

  4. Grupo de Química de los Productos Naturales, Escuela de Química, Universidad Nacional de Colombia-sede Medellín, Cra 65 59ª-110, 0000-0002, 2609-491X, Medellín, Colombia

    Tatiana Lobo-Echeverri

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  1. Lina Cristina Salazar
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Salazar, L.C., Ortiz-Reyes, A., Rosero, D.M. et al. Dillapiole in Piper holtonii as an Inhibitor of the Symbiotic Fungus Leucoagaricus gongylophorus of Leaf-Cutting Ants. J Chem Ecol 46, 668–674 (2020). https://doi.org/10.1007/s10886-020-01170-w

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