Soilborne fungi have host affinity and host-specific effects on seed germination and survival in a lowland tropical forest

Authors: SARMIENTO, CAROLINA - Smithsonian Tropical Research; ZALAMEA, PAUL - Smithsonian Tropical Research; DALLING, JAMES - University Of Illinois; Davis, Adam; STUMP, SIMON - University Of Arizona; ARNOLD, ELIZABETH - University Of Arizona

Submitted to: Proceedings of the National Academy of Sciences (PNAS)
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 9/1/2017
Publication Date: 10/2/2017
Citation: Sarmiento, C., Zalamea, P.C., Dalling, J.W., Davis, A.S., Stump, S.M., Arnold, E.A. 2017. Soilborne fungi have host affinity and host-specific effects on seed germination and survival in a lowland tropical forest. Proceedings of the National Academy of Sciences. doi: 10.1073/pnas.1706324114.
DOI: https://doi.org/10.1073/pnas.1706324114

Interpretive Summary: Population dynamics models show that depleting buried soil reserves of weed seeds would be more beneficial to integrated weed management than any current weed methods. However, in order to kill buried weed seeds, we need improved knowledge of how soil microbes attack seeds. Seeds of tropical pioneer trees offer a good study system for this problem because they have seeds that are similar to those of arable weeds, but have fast seed decay rates because of heavy microbial pressure in the moist soils of these forests. Using a common garden experiment in a lowland tropical forest in Panama, we showed that plant species had the greatest effect on which fungi they were infected by, regardless of soil type, forest age, canopy species composition, or time in soil (1 - 12 months). Inoculation experiments demonstrated host-specific effects of fungi on seed germination and viability, revealing impacts on seeds prior to seedling emergence. Our results provide strong evidence that seed-infecting fungi show host preference and demonstrate the capacity of these fungi to alter seed germination and survival in a plant species-specific manner. These findings indicate that seeds are vulnerable to a set of species-specific pathogenic fungi, regardless of location. Future research should focus on identifying the soil environmental conditions that hasten seed-infection by its focal group of soil fungi.

Technical Abstract: The Janzen-Connell (JC) hypothesis provides a powerful framework for explaining the maintenance of tree diversity in tropical forests. Its central tenet -- that recruits experience high mortality near conspecifics and at high densities -- assumes a degree of host specialization in interactions between plants and natural enemies. Studies confirming JC effects have focused on spatial distributions of seedlings and saplings, leaving major knowledge gaps regarding the fate of seeds in soil and the specificity of the soilborne fungi that are their most important antagonists. Using a common garden experiment in lowland tropical forest in Panama, we show that communities of seed-infecting fungi are structured predominantly by plant species, regardless of soil type, forest age, canopy species composition, or time in soil (1 - 12 months). Inoculation experiments demonstrated host-specific effects of fungi on seed germination and viability, revealing impacts on seeds prior to seedling emergence. Our results provide strong evidence that seed-infecting fungi show host preference and demonstrate the capacity of these fungi to alter seed germination and survival in a tree species-specific manner. These findings bring seed dynamics to light in the context of the JC hypothesis, implicating them directly in the processes that have emerged as critical for diversity maintenance in species-rich tropical forests.