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

Abstract

The Janzen-Connell (JC) hypothesis provides a conceptual 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 primarily 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. Here we use a common garden experiment in a lowland tropical forest in Panama to show that communities of seed-infecting fungi are structured predominantly by plant species, with only minor influences of factors such as local soil type, forest characteristics, or time in soil (1-12 months). Inoculation experiments confirmed that fungi affected seed viability and germination in a host-specific manner and that effects on seed viability preceded seedling emergence. Seeds are critical components of reproduction for tropical trees, and the factors influencing their persistence, survival, and germination shape the populations of seedlings and saplings on which current perspectives regarding forest dynamics are based. Together 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.

Relationships between plant diversity and soil microbial diversity vary across taxonomic groups and spatial scales

“…Previous studies have shown that microbial biogeographic distribution was associated with ecosystem types (Cornwell et al 2008, Bradford et al 2017. For example, the strong correlation may relate to the interactions of plant community with parasitic microbes in tropical forests (Bagchi et al 2014, Sarmiento et al 2017, whereas symbiotic fungi may contribute to the stronger plant-microbial correlation in temperate forests (Br eda et al 2006, Brzostek et al 2015. Or diverse litter quality fosters more divergent microbial communities in tropical forests (Cornwell et al 2008, Bradford et al 2017.…”

“…Tropical forests should have a higher plant-microbial correlation, considering the extraordinary high biodiversity and the strong interaction between plant community and parasitic microbes (Bagchi et al 2014, Sarmiento et al 2017). We investigated factors including targeted taxonomic group, microbial response type in diversity (richness, abundance, diversity index, and composition), microbial examination method, sampling extent (latitude and elevation cover range), biome type, soil type, and environmental factors (e.g., soil pH, total organic carbon, precipitation, and temperature) to assess the patterns of the plant-microbial correlation and variables explaining their variation.…”

Host plant phylogeny and abundance predict root‐associated fungal community composition and diversity of mutualists and pathogens

“…Similarly, the negative impact of soil fungi on seedling survival was shown to decrease with phylogenetic distance between hosts in a subtropical forest (Liu et al, ). Additionally, Sarmiento et al () showed that fungal seed pathogen communities were primarily structured by host species identity, and had correspondingly host‐specific impacts on seed viability and germination. Thus, our results contribute to a growing body of evidence showing that pathogen communities show host preference, as required for them to drive CNDD (Bagchi et al, ; Mangan et al, ; Sarmiento et al, ).…”

“…Additionally, Sarmiento et al () showed that fungal seed pathogen communities were primarily structured by host species identity, and had correspondingly host‐specific impacts on seed viability and germination. Thus, our results contribute to a growing body of evidence showing that pathogen communities show host preference, as required for them to drive CNDD (Bagchi et al, ; Mangan et al, ; Sarmiento et al, ). Furthermore, the fact that closely related host species shared more similar pathogen communities than distantly related host species is consistent with the possibility that RAF drive phylogenetic Janzen–Connell effects: which would serve to increase plant phylogenetic diversity (Liu et al, , Chen et al, , but see Lebrija‐Trejos, Wright, Hernández, & Reich, , Zhu et al, ).…”

“…Variation in the strength of CNDD likely affects the relative abundance of plant species (Comita, Muller‐Landau, Aguilar, & Hubbell, ; Wills, Condit, Foster, & Hubbell, ; Zhu, Comita, Hubbell, & Ma, ), and it may even affect forest diversity (Johnson et al, ; LaManna et al, , but see Chisholm & Fung, ; Hülsmann & Hartig, ). Although CNDD is considered a function of microbial community composition and structure (Bachelot, Uriarte, McGuire, Thompson, & Zimmerman, ; Sarmiento et al, ), RAF have been treated as a black box until recently. Direct investigations of RAF community composition and structure therefore promise to yield novel insights into processes affecting plant diversity and community composition.…”