Nitrogen fixers in tropical forests face a major cost to herbivory
The ability to fix nitrogen (N2) confers an advantage to trees in tropical forests by supplying the nitrogen needed during periods of high net biomass accumulation, and would appear to benefit all tropical trees at some point in their lifetime or evolution. Surprisingly, the trait is constrained to a relatively small proportion of trees and species across tropical forests, raising the question of why it is not more widespread. Previous hypotheses have focused on the metabolic cost that a N2-fixing tree must pay its rhizobial symbionts, and on the potential cost of deploying a facultative strategy. Yet fixers may face high herbivore pressure due to their nitrogen-rich leaves, suggesting that any costs associated with carbon and nitrogen lost in leaf tissue caused by herbivory must also be considered. We test the hypothesis that tropical N2fixers pay an additional, large and constant cost due to herbivore preference for their nitrogen-rich leaves.
We establish a herbivore-exclosure experiment with 86 N2-fixing and non-fixing trees at the Agua Salud Project in Panama to quantify herbivory rates. We pair measurements of herbivory with leaf nitrogen and toughness as potential mechanisms to explain herbivore pressure. Finally, we calculate the carbon and nitrogen costs of herbivory.
We found that N2-fixing trees lost 9% of leaf tissue over a three-month time period, while non-fixing trees lost 3% of leaf tissue. This resulted in 20% more leaf tissue lost by N2 fixers than non-fixers when extrapolated over a one-year period with a compound-interest approach. When considering the potential carbon assimilation forgone to loss in leaf tissue and the allocation of carbon and nitrogen to replacing leaf tissue lost to herbivory, we found that the cost of herbivory was equal if not larger than the metabolic cost of fixation. Our results indicate that, in addition to the metabolic costs fixers face, herbivory presents an additional major expense to fixers, regardless of whether they are actively fixing N2. The herbivory cost may significantly reduce the competitive advantage of fixers and may explain why they do not become more abundant in tropical forest communities and why the fixation trait has not evolved across more taxa. The findings give fresh insight into how we think about food webs and trophic interactions in tropical forests, and introduce a potential mechanism for how herbivores alter biogeochemical cycles.