Multitrophic interactions below and above ground: en route to the next level

Authors

  • Nicole M. van Dam,

    1. Radboud University Nijmegen, Institute for Water and Wetland Research (IWWR), PO Box 9010, 6500 GL Nijmegen, The Netherlands
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  • Martin Heil

    Corresponding author
    1. Departamento de Ingeniería Genética, CINVESTAV – Irapuato, Km. 9.6 Libramiento Norte, 36821 Irapuato, Guanajuato, México
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Correspondence author. E-mail: mheil@ira.cinvestav.mx

Summary

1. Plants mediate multiple interactions between below-ground (BG) and above-ground (AG) heterotrophic communities that have no direct physical contact. These interactions can be positive or negative from the perspective of each player, can go from the BG to the AG community or vice versa, and comprise representatives of different phyla. Here we highlight emerging general patterns and discuss future research directions.

2. Ecologists initially postulated that root herbivores induce general stress responses, which increase the levels of primary (nutritional) compounds in the undamaged plant compartment and thereby facilitate future attack by AG herbivores. However, damage can also reduce the levels of primary compounds or increase contents of secondary (defensive) metabolites. Both effects may cause resistance phenotypes that play an important role in mediating BG–AG interactions. Systemically induced resistance does not only affect other herbivores but also pathogens in the AG and BG compartment and may inhibit beneficial organisms such as natural enemies of herbivores, microbial root symbionts and pollinators. Conversely, symbiotic mutualists such as mycorrhiza and rhizobia may affect AG and BG defence levels. Finally, BG–AG interactions may be costly if they impede optimal defence strategies in the undamaged compartment.

3.Synthesis. In order to better understand the adaptive value of BG–AG induced responses for the players involved and to identify the driving evolutionary forces, we need a better integration of studies at the community level with experiments on model systems that allow unravelling the genetic and physiological mechanisms of BG–AG interactions. Experiments preferably should be carried out at realistic densities and using the natural temporal sequence at which the various associations are established, because we can expect plants to be adapted only to events that are common over evolutionary time spans. Detailed mechanistic knowledge will help to reproduce relevant interactions in experiments that study multiple species in the field. This step will ultimately allow us to evaluate the importance of plant-mediated interactions between BG and AG communities for the fitness of the species involved and for the structuring of natural communities.

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