Mycorrhizal Associations and Trophic Modes in Coexisting Orchids: An Ecological Continuum between Auto- and Mixotrophy

Abstract

Two distinct nutritional syndromes have been described in temperate green orchids. Most orchids form mycorrhizas with rhizoctonia fungi and are considered autotrophic. Some orchids, however, associate with fungi that simultaneously form ectomycorrhizas with surrounding trees and derive their carbon from these fungi. This evolutionarily derived condition has been called mixotrophy or partial mycoheterotrophy and is characterized by 13C enrichment and high N content. Although it has been suggested that the two major nutritional syndromes are clearly distinct and tightly linked to the composition of mycorrhizal communities, recent studies have challenged this assumption. Here, we investigated whether mycorrhizal communities and nutritional syndromes differed between seven green orchid species that co-occur under similar ecological conditions (coastal dune slacks). Our results showed that mycorrhizal communities differed significantly between orchid species. Rhizoctonia fungi dominated in Dactylorhiza sp., Herminium monorchis, and Epipactis palustris, which were autotrophic based on 13C and N content. Conversely, Liparis loeselii and Epipactis neerlandica associated primarily with ectomycorrhizal fungi but surprisingly, 13C and N content supported mixotrophy only in E. neerlandica. This, together with the finding of some ectomycorrhizal fungi in rhizoctonia-associated orchids, suggests that there exists an ecological continuum between the two syndromes. The presence of a large number of indicator species associating with individual orchid species further confirms previous findings that mycorrhizal fungi may be important factors driving niche-partitioning in terrestrial orchids and therefore contribute to orchid coexistence.

Mycorrhizal symbioses and the evolution of trophic modes in plants

“…After the pioneering work of Gebauer and Meyer () and Trudell et al (), many studies have applied stable isotope analyses to assess the trophic modes of plants (e.g. Bidartondo, Burghardt, Gebauer, Bruns, & Read, ; Abadie et al, ; Tedersoo, Pellet, Kõljalg, & Selosse, ; Zimmer et al, ; Hynson, Preiss, Gebauer, & Bruns, ; Johansson, Mikusinska, Ekblad, & Eriksson, ; Hynson, Schiebold, & Gebauer, ; Jacquemyn, Waud, et al, ). Bidartondo et al (), for example, analysed isotope signatures in several orchid species inhabiting forest habitats and showed that orchids that associated primarily with rhizoctonia fungi were not significantly enriched in 13 C, whereas orchids associated with ectomycorrhizal fungi showed both significant enrichment in 13 C and 15 N. Similarly, Hynson et al () showed evidence for mycoheterotrophy on ectomycorrhizal fungi in several species of the tribe Pyroleae.…”

“…However, the assumed autotrophy of rhizoctonia‐associated orchid species has recently been challenged (Gebauer et al, ; Schiebold et al, ; Schweiger et al, ). Moreover, detailed molecular analyses using high‐throughput sequencing techniques have shown that many so‐called ‘rhizoctonia‐associated’ species also associate with ectomycorrhizal fungi and vice versa (Jacquemyn et al, ; Jacquemyn, Brys, Waud, Busschaert, & Lievens, ; Jacquemyn, Waud, et al, ), indicating that a strict distinction between rhizoctonia‐associated and ectomycorrhiza‐associated species cannot be maintained, neither based on their stable isotope signatures nor their mycorrhizal communities. Similar results have been observed in other genera displaying autotrophy and mycoheterotrophy.…”

“…A similar comparison of the mycorrhizal communities of two Epipactis species that co‐occur in dune slacks showed that the putatively autotrophic Epipactis palustris mainly associated with fungi of the genera Tulasnella and Ceratobasidium , whereas fungal communities in the partially mycoheterotrophic E. helleborine subsp. neerlandica were primarily dominated by members of the ectomycorrhizal genera Tuber and Geopara (Jacquemyn, Waud, et al, ; Jacquemyn, Waud, Lievens, & Jacquemyn, ) (Figure ). Interestingly, several ectomycorrhizal genera were also present in E. palustris , albeit at much lower abundances.…”

“…neerlandica . In the latter, fungal communities were primarily dominated by members of the ectomycorrhizal genera Tuber and Geopara (data from Jacquemyn et al, ; Jacquemyn, Waud, et al, )…”

Latitudinal variation in mycorrhizal diversity associated with a European orchid

“…S spiralis and S. novae‐zelandiae ; Frericks, Munkacsi, Ritchie, Luo, & Lehnebach, ; Tondello et al., ). Indeed, a recent study showed that this primer pair was able to detect a large number of Tulasnellaceae OTUs in typical rhizoctonia associated orchids ( Dactylorhiza fuchsii and D. incarnata ) (Jacquemyn, Waud, et al., ). Therefore, our results should reflect the overall influence of latitude and longitude on OMF diversity in S. spiralis .…”