Abstract
Plant interactions with other organisms are mediated by chemistry, yet chemistry varies among conspecific and within individual plants. The foliar metabolome—the suite of small-molecule metabolites found in the leaf—changes during leaf ontogeny and is influenced by the signaling molecule jasmonic acid. Species differences in secondary metabolites are thought to play an important ecological role by limiting the host ranges of herbivores and pathogens, and hence facilitating competitive coexistence among plant species in species-rich plant communities such as tropical forests. Yet it remains unclear how inducible and ontogenetic variation compare with interspecific variation, particularly in tropical trees. Here, we take advantage of novel methods to assemble mass spectra of all compounds in leaf extracts into molecular networks that quantify their chemical structural similarity in order to compare inducible and ontogenetic chemical variation to among-species variation in species-rich tropical tree genera. We ask (i) whether young and mature leaves differ chemically, (ii) whether jasmonic acid-inducible chemical variation differs between young and mature leaves, and (iii) whether interspecific exceeds intraspecific chemical variation for four species from four hyperdiverse tropical tree genera. We observed significant effects of the jasmonic acid treatment for three of eight combinations of species and ontogenetic stage evaluated. Three of the four species also exhibited large metabolomic differences with leaf ontogenetic stage. The profound effect of leaf ontogenetic stage on the foliar metabolome suggests a qualitative turnover in secondary chemistry with leaf ontogeny. We also quantified foliar metabolomes for 45 congeners of the four focal species. Chemical similarity was much greater within than between species for all four genera, even when within-species comparisons included leaves that differed in age and jasmonic acid treatment. Despite ontogenetic and inducible variation within species, chemical differences among congeneric species may be sufficient to partition niche space with respect to chemical defense.
Highlights
A substantial proportion of the local species richness of many tropical forests is comprised of a small number of exceptionally species-rich woody plant genera (Gentry, 1982)
The effect of treatment with the defense-inducing plant hormone jasmonic acid varied by species, by leaf ontogenetic stage, and by the metric used to measure the effect in ways that suggest that inducible chemical defenses may not be universal in tropical trees (Bixenmann et al, 2016) and may vary widely among species
In contrast. young, expanding leaves consistently differed in their chemical composition compared to fully mature leaves in all four focal species and interspecific chemical variation was much greater than variation within species for all four genera, even when within-species comparisons included leaves that differed in age and jasmonic acid treatment
Summary
A substantial proportion of the local species richness of many tropical forests is comprised of a small number of exceptionally species-rich woody plant genera (Gentry, 1982). High local species richness of congeneric plants poses a challenge to our understanding of diversity maintenance in tropical forests because closely related species are likely to share natural enemies (Novotny et al, 2002; Odegaard, Diserud & Ostbye, 2005; Gilbert & Webb, 2007) and density-dependent recruitment limitation that should result in competitive exclusion of related species and preclude closely related species from coexisting ecologically (Sedio & Ostling, 2013). Species niche differences defined by secondary metabolites might contribute to the local diversity of species-rich tree genera if congeneric species differ chemically sufficiently to avoid sharing natural enemies (Salazar, Jaramillo & Marquis, 2016; Forrister et al, 2019). Sedio et al (2017) did not consider inducible variation in the metabolome, and other studies of inducible chemical variation in tropical trees have been limited to seasonal, deciduous forests (Boege, 2004, but see Bixenmann et al, 2016)
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