Tropics change the rule! Heterotrophic plants using carbon from soil fungi (myco-heterotrophy): Contrasting strategies in fungal association and carbon source between temperate and tropical regions

Background/Question/Methods Most plant ecophysiology is shaped by symbioses in which plant roots associate with soil fungi to form mycorrhizae. Fungi exploit soil mineral nutrients that are shared with the plant, and receive carbon as a reward. Moreover, several forest-understorey achlorophyllous plants, once thought to be saprophytic, are now shown to receive carbon from their mycorrhizal fungi and are therefore called mycoheterotrophs (MH). In the many investigated temperate MH species, including many orchids, the associated fungi in turn form mycorrhizae with surrounding plants that are the ultimate carbon source of the entire system. Direct and indirect evidences support the latter point, especially isotopic methods (13C contents are similar to mycorrhizal fungi and 15N contents suggest a high position in trophic chains, above fungi). The ability of mycorrhizal fungi to link different plants therefore allows sufficient inter-plant carbon transfers to support MH growth. Furthermore, all temperate species studied so far indicate a high specificity of each MH species to a narrow fungal clade. However, most MH plants live under the tropics. Here, we investigate tropical MH orchids to (i) identify their mycorrhizal partners, using molecular methods and (ii) confirm their carbon source, using stable isotopes.

Results/Conclusions We studied six tropical orchid species from Asia, Africa and the Caribbean islands, including several populations for each of them. They revealed contrasting features as compared to the ‘temperate rule’. Species from Asian Dipterocarpaceae forest shared diverse ectomycorrhizal species with the later trees; their isotopic content clearly indicated that, exactly as temperate models, they received carbon from this source. However, they were not specific, and had up to four different partner species per individual (and eight per population). The other models from Africa and the Caribbean islands, from forests devoid of the mycorrhizal fungal species usually colonizing MH orchids, associate with saprobic fungi. Together with the identity of the fungi, isotopic studies showed that the ultimate carbon source was, respectively, dead wood and dead leaves. These examples, obtained in the same phylogenetic context as the models studied in temperate regions, are unlikely to represent specific idiosyncrasies, but rather emphasize functional differences of tropical ecosystems, especially for fungi. We hypothesize that (1) a wetter climate allows saprophytic fungi to be sufficiently active over the rain season to provide carbon to MH plants and (2) a higher availability of photosynthates for tropical mycorrhizal fungi reduce arm race with exploiting MH orchids, and thus evolution toward specificity.