Abstract

Tropical forests are biodiversity hotspots, but it is not well understood how this diversity is structured and maintained. One hypothesis rests on the generation of a range of metabolic niches, with varied composition, supporting a high species diversity. Characterizing soil metabolomes can reveal fine-scale differences in composition and potentially help explain variation across these habitats. In particular, little is known about canopy soils, which are unique habitats that are likely to be sources of additional biodiversity and biogeochemical cycling in tropical forests. We studied the effects of diverse tree species and epiphytes on soil metabolomic profiles of forest floor and canopy suspended soils in a French Guianese rainforest. We found that the metabolomic profiles of canopy suspended soils were distinct from those of forest floor soils, differing between epiphyte-associated and non-epiphyte suspended soils, and the metabolomic profiles of suspended soils varied with host tree species, regardless of association with epiphyte. Thus, tree species is a key driver of rainforest suspended soil metabolomics. We found greater abundance of metabolites in suspended soils, particularly in groups associated with plants, such as phenolic compounds, and with metabolic pathways related to amino acids, nucleotides, and energy metabolism, due to the greater relative proportion of tree and epiphyte organic material derived from litter and root exudates, indicating a strong legacy of parent biological material. Our study provides evidence for the role of tree and epiphyte species in canopy soil metabolomic composition and in maintaining the high levels of soil metabolome diversity in this tropical rainforest. It is likely that a wide array of canopy microsite-level environmental conditions, which reflect interactions between trees and epiphytes, increase the microscale diversity in suspended soil metabolomes.

Highlights

  • Soil metabolomes differed as a result of their sample location and their association with other plants (Tables 1 and 2)

  • An abundance of 2496 of the 2757 metabolite signals were higher in suspended soils than in forest floor soils, for groups that include phenolic, aliphatic, and polycyclic aromatic compounds; unsaturated fatty acids; terpenes; most sugars; organic and amino acids associated with the Krebs cycle; and those with nitrogenous bases

  • Our results showed a clear effect of tree species on canopy soil metabolomic profiles, regardless of association with epiphytes, indicating that species-specific environmental conditions in the canopy influence canopy soil processes

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Summary

Introduction

Tropical rainforests are one of the world’s most biodiverse [1,2,3], yet threatened ecosystems [4,5], in which the origin and maintenance of high levels of local-scale tree species coexistence [3,6] have been explained by several factors, including heterogeneity of levels of disturbance [1] and soil traits and nutrients [2,7,8,9,10,11,12], micro-site singularities [13], topographical features [14] Suspended soils along tree trunks and branches retain nutrients and water essential for the development of epiphytic plants [26] that directly depend on these limited pools of available nutrients [27]. These plants are morphologically and physiologically adapted to facilitate the accumulation of leaf litter and water and to maximize atmospheric and invertebrate-mediated delivery of nutrients [15,28,29] in the physically harsh and variable environmental conditions that prevail within the canopy [30]. Certain members of the Bromeliaceae family form water and litter-storing phytotelmata and take up nutrients through leaf-absorbing trichomes [29,34,35], whilst Asplenium ferns intercept falling leaf litter, which is stored as organic matter adjacent to the roots [27,36]

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