Foliar bacteria and soil fertility mediate seedling performance: a new and cryptic dimension of niche differentiation

Abstract

Abstract. The phyllosphere (comprising the leaf surface and interior) is one of the world's largest microbial habitats and is host to an abundant and diverse array of bacteria. Nonetheless, the degree to which bacterial communities are benign, harmful, or beneficial to plants in situ is unknown. We tested the hypothesis that the net effect of reducing bacterial abundance and diversity would vary substantially among host species (from harmful to beneficial) and this would be strongly mediated by soil resource availability. To test this, we monitored tree seedling growth responses to commercial antibiotics among replicated resource supply treatments (N, P, K) in a tropical forest in Panama for 29 months. We applied either antibiotics or control water to replicated seedlings of five common tree species (Alseis blackiana, Desmopsis panamensis, Heisteria concinna, Sorocea affinis, and Tetragastris panamensis). These antibiotic treatments significantly reduced both the abundance and diversity of bacteria epiphytically as well as endophytically. Overall, the effect of antibiotics on performance was highly host specific. Applying antibiotics increased growth for three species by as much as 49% (Alseis, Heisteria, and Tetragastris), decreased growth for a fourth species by nearly 20% (Sorocea), and had no impact on a fifth species (Desmopsis). Perhaps more importantly, the degree to which foliar bacteria were harmful or not varied with soil resource supply. Specifically, applying antibiotics had no effect when potassium was added but increased growth rate by almost 40% in the absence of potassium. Alternatively, phosphorus enrichment caused the effect of bacteria to switch from being primarily beneficial to harmful or vice versa, but this depended entirely on the presence or absence of nitrogen enrichment (i.e., important and significant interactions). Our results are the first to demonstrate that the net effect of reducing the abundance and diversity of bacteria can have very strong positive and negative effects on seedling performance. Moreover, these effects were clearly mediated by soil resource availability. Though speculative, we suggest that foliar bacteria may interact with soil fertility to comprise an important, yet cryptic dimension of niche differentiation, which can have important implications for species coexistence.

Plant responses to fertilization experiments in lowland, species‐rich, tropical forests

“…Fertilization often increases tissue nutrient concentrations (Fig. Potassium addition also reduced net adverse effects of foliar bacteria in our experiment (Griffin et al 2016). Two fertilization experiments conducted in LSRTF considered herbivory.…”

Pervasive interactions between foliar microbes and soil nutrients mediate leaf production and herbivore damage in a tropical forest

“…We previously demonstrated that Agry‐gent and Agri‐mycin significantly decreased mean abundance of epiphytic and endophytic bacteria by over 50% on our focal species and also decreased microbial morphotype richness by over 20% (Griffin et al ., ). Each of these antibiotic treatments were equally effective and remained so over time; also, their impact was very similar among nutrient treatments and plant species (Griffin et al ., ). Thus, our antibiotics worked in the sense that they reduced foliar bacterial loads, although our results are likely conservative because we only reduced bacterial abundance and richness by c .…”

“…Overall, our findings support recent studies that challenge the conventional wisdom that light is only a limiting resource for tropical seedlings and moreover demonstrate that soil nutrient availability and foliar bacteria are major drivers of plant performance (e.g. Pasquini & Santiago, ; Santiago et al ., ; Pasquini et al ., ; Griffin et al ., ).…”

“…For example, for our five species, antibiotic applications changed the rank‐order performance for two of five species for leaf‐production and herbivore damage, and four of five species for seedling growth (Fig. S2; growth data from Griffin et al ., ). Notably, however, Griffin et al .…”

“…In a recent study, Griffin et al . () demonstrated that foliar bacteria in a tropical forest caused up to a 49% reduction in growth rates for seedlings of three common tree species. These results suggest that foliar bacteria are commonly pathogenic and may typically regulate leaf dynamics, although data are nearly nonexistent (but cf.…”