Schiebold, JMI; Bidartondo, MI; Lenhard, F; Makiola, A; Gebauer, G: Exploiting mycorrhizas in broad daylight: Partial mycoheterotrophy is a common nutritional strategy in meadow orchids, Journal of Ecology, 106, 168-178 (2018), doi:10.1111/1365-2745.12831

1. Partial mycoheterotrophy (PMH) is a nutritional mode in which plants utilise organic matter, i.e. carbon, both from photosynthesis and a fungal source. The latter reverses the direction of plant-to-fungus carbon flow as usually assumed in mycorrhizal mutualisms. Based on significant enrichment in the heavy isotope 13C, a growing number of PMH orchid species have been identified. These PMH orchids are mostly associated with fungi simultaneously forming ectomycorrhizas with forest trees. In contrast, the much more common orchids that associate with rhizoctonia fungi, who are decomposers, have stable isotope profiles most often characterised by high 15N enrichment and high nitrogen concentrations but either an insignificant 13C enrichment or depletion relative to autotrophic plants. Using hydrogen stable isotope abundances recent investigations showed PMH in rhizoctonia-associated orchids growing under light-limited conditions. Hydrogen isotope abundances can be used as substitute for carbon isotope abundances in cases where autotrophic and heterotrophic carbon sources are insufficiently distinctive to indicate PMH.

2. To determine whether rhizoctonia-associated orchids growing in habitats with high irradiance feature PMH as a nutritional mode, we sampled 13 orchid species growing in montane meadows, four forest orchid species and 34 autotrophic reference species. We analysed δ2H, δ13C, δ15N and δ18O and determined nitrogen concentrations. Orchid mycorrhizal fungi were identified by DNA sequencing.

3. As expected, we found high enrichments in 2H, 13C, 15N and nitrogen concentrations in the ectomycorrhiza-associated forest orchids, and the rhizoctonia-associated Neottia cordata from a forest site was identified as PMH. Most orchids inhabiting sunny meadows lacked 13C enrichment or were even significantly depleted in 13C relative to autotrophic references. However, we infer PMH for the majority of these meadow orchids due to both significant 2H and 15N enrichment and high nitrogen concentrations. Pseudorchis albida was the sole autotrophic orchid in this study as it exhibited neither enrichment in any isotope nor a distinctive leaf nitrogen concentration.

4. Synthesis Our findings demonstrate that PMH is a trophic continuum between the extreme endpoints of autotrophy and full mycoheterotrophy, ranging from marginal to pronounced. In rhizoctonia-associated orchids, PMH plays a far greater role than previously assumed, even in full light conditions.

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