The role of herbivory in governing tropical nitrogen fixation

A growing body of evidence suggests that periods of nitrogen limitation on plant growth are common across tropical forests and that nitrogen-fixing trees alleviate this limitation and promote tropical forest carbon sequestration. However, fixers rarely exceed ~5-15% of basal area in tropical forests, limiting the role of fixation in mitigating nitrogen limitation. Existing hypotheses have not sufficiently explained this low abundance of fixers. I examine the previously untested hypothesis that tropical nitrogen fixation is constrained by a high herbivory cost for fixers. I evaluate (1) if nitrogen-fixing trees have higher herbivory than non-fixers; and, whether this cost constrains symbiotic nitrogen fixation in tropical forests by governing (2) the fixation rates of individual trees and (3) fixer demographic traits. I first conduct a field survey of herbivory on 1,632 leaves from 350 seedlings across 43 tree species in Panama to determine if fixers undergo higher herbivory than non-fixers and use species leaf traits to assess what drives herbivory differences between the two groups. I find that fixers undergo more herbivory and that this constitutes a significant carbon cost. Second, I use greenhouse experiments with 200 seedlings from five fixer species to test if herbivory regulates plant-level fixation rates. Surprisingly, I find up to ten-fold increases in fixation rates following herbivory, possibly to replace lost leaf nitrogen. Third, using a census of >200,000 seedlings over 14 years, with herbivory measured on a subset of seedlings, I determine if herbivory drives differences in the growth, survival, and strength of negative density-dependent effects between fixers and non-fixers. I find that herbivory contributes to stronger negative density-dependence for fixers, which could cap neotropical fixer abundances. My findings demonstrate that high herbivory for fixer species governs individual fixation rates and may constrain fixer abundances, with combined consequences for the tropical carbon sink.