Tree seedling shade tolerance arises from interactions with microbes and is mediated by functional traits

Shade tolerance is a central concept in forest ecology and strongly
influences forest community dynamics. However, the plant traits and
conditions conferring shade tolerance are yet to be resolved. We propose
that shade tolerance is shaped not only by responses to light but also by
a species’ defense and recovery functional traits, soil microbial
communities, and interactions of these factors with light availability. We
conducted a greenhouse experiment for three temperate species in the genus
Acer that vary in shade tolerance. We grew newly germinated seedlings in
two light levels (2% and 30% sun) and controlled additions of microbial
filtrates using a wet-sieving technique. Microbial filtrate treatments
included: <20 µm, likely dominated by pathogenic microbes; 40-250
µm, containing arbuscular mycorrhizal fungi (AMF); combination, including
both filtrate sizes; and sterilized combination. We monitored survival for
nine weeks and measured fine root AMF colonization, hypocotyl phenolics,
stem lignin, and stem+root nonstructural carbohydrates (NSC) at three-week
intervals. We found that differences in seedling survival between low and
high light only occurred when microbes were present. AMF colonization,
phenolics, and NSC generally increased with light. Phenolics were greater
with <20 µm microbial filtrate, suggesting that soil-borne
pathogens may induce phenolic production and NSC was greater with 40-250
µm filtrate, suggesting that mycorrhizal fungi may induce NSC production.
Across species, microbe treatments, and light availability, survival
increased as phenolics and NSC increased. Therefore, shade tolerance can
be explained by interactions among soil-borne microbes, seedling traits,
and light availability, providing a more mechanistic and trait-based
explanation of shade tolerance and thus forest community dynamics.