Structural and compositional dimensions of phytochemical diversity in the genus Piper reflect distinct ecological modes of action

Context: An increasing number of ecological studies have used chemical diversity as a functionally relevant, scalable measure of phytochemical mixtures, demanding more rigorous attention to how chemical diversity is estimated. Most studies have focused on the composition of phytochemical mixtures and have largely ignored structural concerns, which may have greater importance for ecological function. Here we explore the development of structural complexity and compositional diversity resulting from different biotic and abiotic interactions in Piper kelleyi Tepe (Piperaceae). We also describe how variation in structural complexity and compositional diversity differ between two congeners, P. kelleyi and Piper reticulatum. To better interpret these results, we have developed a hypothesis-driven framework for interpreting these dimensions of chemical diversity in phytochemical mixtures.

Approach: We used the tropical shrub, P. kelleyi, as a model system to examine interactions between ecological factors and dimensions of phytochemical diversity. We also compared compositional diversity and metabolic complexity in P. kelleyi and P. reticulatum using liquid chromatography and ¹H NMR respectively to examine tradeoffs between compositional diversity and structural complexity. A framework is provided to generate meaningful estimates of the structural complexity of phytochemical mixtures as measured by ¹H NMR.

Results and Conclusions: Piper is an abundant plant genus that supports diverse insect communities throughout the tropics. Subtle changes in understory forest light were associated with increases in herbivory that directly increased compositional diversity and indirectly decreased structural complexity in P. kelleyi. This was attributed to the production of oxidation products resulting from herbivory-driven decomposition of structurally complex defense compounds. This type of complex result would remain undetected using standard chemical ecology approaches and accounts for the detailed molecular changes that are likely to affect species interactions.

Synthesis: Our quantitative framework provides a method for considering tradeoffs between structural complexity and compositional diversity and the interpretation of analytical approaches for each. This methodology will provide new theoretical insights and a more sophisticated model for examining the ecology and evolution of chemically mediated interactions.