Differences in volatile terpene composition between the bark and leaves of tropical tree species
Graphical abstract
A study on 55 tropical tree species indicate that bark hold a distinct and more diverse blend of volatile terpenes than leaves.
Highlights
► We measured volatile terpenes in bark and leaves of 55 tropical tree species. ► The blend released by bark is more diverse than that released by leaves. ► Bark terpene composition is different than leaves terpene composition.
Introduction
Biogenic volatile organic compounds (VOCs) are implicated in direct plant defense through herbivore repulsion, cytotoxic activity against fungi and pathogens and indirect defense through the attraction of herbivore predators or parasitoids (Pichersky and Gershenzon, 2002, Unsicker et al., 2009). Although the defensive role of VOCs in leaves is well documented (Unsicker et al., 2009), other vegetative tissues such as roots and bark are also known to synthesize volatile compounds, especially when damaged (Mumm and Hilker, 2006, Rasmann and Turlings, 2007). A large proportion of these VOCs are terpenes, either monoterpenes (with 10 carbon atoms), or sesquiterpenes (with 15 carbon atoms) and these compounds are highly diverse both within and among species (Dudareva et al., 2004).
Why do organisms produce an enormous diversity of secondary metabolites instead of just one or two compounds? The many hypotheses posited to explain the possible value of complex terpenes mixtures were reviewed by Gershenzon and Dudareva (2007). First, a diverse combination of terpenes may help provide protection against a diversity of herbivores, parasites and competitors (Pimentel and Bellotti, 1976) and reduce the potential number of herbivore species (Kursar et al., 2009). Second, having a diverse mixture allows each plant to play a slightly different defense strategy than its conspecific neighbors, reducing the likelihood for an enemy to evolve resistance (Price et al., 1980). Moreover, compounds may act synergistically to provide greater toxicity or deterrence than the equivalent amount of a single substance, for instance if some chemicals increase the persistence of others by inhibiting detoxification or excretion in enemies (Berenbaum and Neal, 1985). Finally, individual chemicals may not be useful under normal environmental conditions but become critical in extreme environments (Gershenzon and Dudareva, 2007). They may also indicate the “ghost of herbivory past” (Jones and Firn, 1991, Firn and Jones, 2003), i.e. compounds that do not currently play a defensive role may have been effective against now-extinct herbivores.
There is, however, a cost to maintaining a diverse set of VOCs. The biosynthesis of volatile terpenes is especially costly, due to a high demand in ATP (adenosine triphosphate) and NADPH and the need for highly specific enzymes (terpene synthases) that are unique to these biosynthetic pathways (Gershenzon, 1994). Most enzymes of terpenoid biosynthesis that catalyze general types of reactions have high substrate specificities (Gershenzon, 1994). Therefore, synthesizing more diverse mixtures increases the cost of production due the cost of the synthesis of multiple specific enzymes. From a biochemical point of view, the production of a diverse set of VOCs in a given plant tissue therefore indicates a significant investment of resources into the biochemical pathways leading to these compounds (Gershenzon, 1994).
Optimal defense theory predicts that plants allocate chemical defenses to different tissues relative to the intrinsic risk of herbivory faced by the plant tissue, the tissue’s value to plant fitness, and the cost of the chemical defense (McKey, 1974). There is substantial experimental evidence in support of optimal defense theory (Zangerl and Rutledge, 1996, Ohnmeiss and Baldwin, 2000, Kaplan et al., 2008, Radhika et al., 2008) but most of the previous studies deal with roots, leaves and flowers (McCall and Fordyce, 2010). In woody plant species, chemical defense can be allocated differentially in bark (for wood protection) and in leaf tissues. For most of the species, wood and leaves have a similar construction cost (Poorter and Villar, 1997) and both attack on wood and leaves have an impact on plant fitness. High defoliation rates reduce growth rate and seed production as found for the tropical shrub Piper arieaianum, Piperaceae (Marquis, 1984). Nonetheless, studies show that most woody species can compensate for a relatively high level of defoliation, up to 25% for the tropical species Casearia nitida (Boege, 2005). Nonetheless, attacks on wood by pathogens and xylophagous insects may have a stronger impact on plant fitness as they compromise the mechanical, hydraulic, and physiological integrity of a tree. Herbivory on phloem dramatically increases the risk of secondary infection (Pearce, 1996, Romero and Bolker, 2008) and exposes the plant to an increased risk of breakage (Franklin et al., 1987), whereas leaves can be more easily shed and replaced following damage (Schowalter et al., 1986). In the mangrove forests of coastal Belize, primary consumption by woodborers may be responsible for greater losses from the canopy than consumption by folivores (Feller and Mathis, 1997): by girdling, pruning, and hollowing, woodborers killed over 50% of the Rhizophora mangle canopy in experimental plots and leaf-feeding herbivores removed less than 6% of the canopy (Feller, 2002). Thus, for long-lived trees, preventing damage to the living tissues of the trunk is essential and we predict that VOCs should be more diverse in bark, the outmost part of the stems of woody plants, than in the leaves.
Moreover, in a given species, wood and leaves are usually attacked by different communities of insect herbivores (Novotny et al., 2003). Leaf-eating insects mostly belong to the Lepidoptera, Coleoptera and Orthoptera orders (Novotny et al., 2003), while wood-specialized insects belong to the Auchenorrhyncha (Novotny and Wilson, 1997) or Cerambycidae family (Tavakilian et al., 1997). Moreover, wood pathogens are largely non-overlapping with leaf pathogens (Gilbert and Hubbell, 1996). Thus, the distinct repertoire of herbivore and pathogen pressures on bark and leaves should favor a distinct allocation of defensive compounds in the tree, such that some terpenes may be specialized to non-overlapping communities of herbivores. In a study concerning the phytoalexins from the leaves, cortex and xylem of mulberry (Morus alba) it has been found that the compounds accumulating in the different tissues were chemically distinct (Pearce, 1996). Moreover, previous studies on the essential oil constituents of bark and leaves already pointed out that even if overlaps exist between these two tissues there are also differences in terpene composition (Lago et al., 2004, Singh et al., 2007).
Here we test two hypotheses related to the allocation of volatile terpenes in tropical trees: (1) leaves should emit a less diverse array of volatile terpenes than bark, as expected under the optimal defense theory, (2) bark and leaves of the same species should hold a distinct array of compounds. We tested these hypotheses by collecting terpenes from bark and leaves of 55 species of trees in French Guiana and then comparing the kind, amount, and diversity of compounds in these tissues.
Section snippets
Effect of the plant organ on the diversity of the terpenes blend
Across the 55 species with more than two individuals analyzed, bark tends to emit more compounds than leaves (Wilcoxon one-sided test, W = 11221.5, P < 0.001) with a mean of 25 VOCs per individual in bark samples and a mean of 19 VOCs per individual in leaves. More specifically, 40 species of the 55 sampled emitted more compounds in bark than in leaves (Fig. 1). This pattern was similar for all terpenes and also when monoterpenes and sesquiterpenes were examined separately (Fig. 1).
Overall, and for
Conclusions
In this study, we found that bark of tropical tree species tend hold a distinct and more diverse blend of volatile terpenes than leaves. Future studies should be conducted to precise the effect of terpenes diversity on the diversity and density of herbivores. Moreover, we focused only on volatile defensive compounds and non-volatiles can also control the distribution of insect herbivores (Meurer-Grimes and Tavakilian, 1997). Such a negative correlation between chemical diversity and the number
Study sites
This study was conducted at three sites in the Neotropical forest of French Guiana: Paracou Research Station (5°15′ N; 52°55′ W), Nouragues Research Station (4°05′ N, 52°40′ W) and Montagne Tortue (4°18′ N; 52°22′ W). All three sites are covered with pristine tropical rain forest. Annual rainfall is 2990 mm for Nouragues, 3160 mm for Paracou and ca. 3500 mm for Montagne Tortue. In five plots of one hectare each, we sampled all trees with a diameter at breast height (dbh) greater than 10 cm (Baraloto et
Acknowledgments
This work is a contribution of the BRIDGE (Bridging Information on Tree Diversity in French Guiana, and a Test of Ecological Theories) project, funded by the Agence Nationale pour la Recherche (ANR-Biodiversité program). We thank all participants of the BRIDGE project, especially, Julien Engel for assistance with botanical identifications, Antoine Stevens and Institut Pasteur Guyane in Cayenne for providing laboratory facilities. We thank P.D. Coley, H. Jactel, L. Poorter, F.E. Putz, Richard J.
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