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Light limitation and partial mycoheterotrophy in rhizoctonia-associated orchids

Abstract

Partially mycoheterotrophic (PMH) plants obtain organic molecules from their mycorrhizal fungi in addition to carbon (C) fixed by photosynthesis. Some PMH orchids associated with ectomycorrhizal fungi have been shown to flexibly adjust the proportion of organic molecules obtained from fungi according to the habitat’s light level. We hypothesise that Neottia ovata and Ophrys insectifera, two orchids associated with saprotrophic rhizoctonia fungi, are also able to increase uptake of organic molecules from fungi as irradiance levels decrease. We continuously measured light availability for individuals of N. ovata and O. insectifera at a grassland and a forest during orchid flowering and fruiting. We repeatedly sampled leaves of N. ovata, O. insectifera and autotrophic reference species for stable isotope natural abundances (δ13C, δ15N, δ2H, δ18O) and C and N concentrations. We found significant 13C enrichment in both orchids relative to autotrophic references at the forest but not the grassland, and significant 2H enrichment at both sites. The 13C enrichment in O. insectifera was linearly correlated with the habitat’s irradiance levels. We conclude that both species can be considered as PMH and at least in O. insectifera, the degree of partial mycoheterotrophy can be fine-tuned according to light availability. However, exploitation of mycorrhizal fungi appears less flexible in saprotroph-associated orchids than in orchids associated with ectomycorrhizal fungi.

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Acknowledgements

The authors thank Christine Tiroch and Petra Eckert (BayCEER—Laboratory of Isotope Biogeochemistry) for skilful technical assistance with stable isotope abundance measurements. We also thank the Regierung von Oberfranken for authorisation to collect the orchid samples.

Funding

The study was funded by the German Research Foundation (DFG Ge 565/7-2).

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Authors and Affiliations

Authors

Contributions

GG conceived this study. JM-IS and CK conducted fieldwork and prepared samples for stable isotope analyses. JM-IS and MIB generated sequencing data and conducted molecular analyses, JM-IS performed the statistical analyses and drafted the manuscript. All authors contributed to the manuscript.

Corresponding author

Correspondence to Gerhard Gebauer.

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Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Communicated by Nina Buchmann.

Electronic supplementary material

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442_2019_4340_MOESM1_ESM.pdf

Suppl. Fig. 1 Mean irradiance at (a) the grassland site and (b) the forest site overlaid by the mean carbon concentration ± SD; yellow triangles for Neottia ovata and blue circles for Ophrys insectifera; unfilled symbols at the grassland site, filled symbols at the forest site; solid green lines represent the mean values of the autotrophic references ± SD (dashed lines). The figure is available in colour in the online version

442_2019_4340_MOESM2_ESM.pdf

Suppl. Fig. 2 Enrichment factors ε18O and ε13C of Neottia ovata (yellow triangles) and Ophrys insectifera (blue circles) at the grassland site (unfilled symbols) and the forest site (filled symbols) (n = 5 per species and site); the green box represents mean enrichment factors ± SD for the autotrophic reference plants (n = 42) that were sampled together with the two orchid species whereas mean ε values of reference plants are zero by definition. The figure is available in colour in the online version

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Schweiger, J.MI., Kemnade, C., Bidartondo, M.I. et al. Light limitation and partial mycoheterotrophy in rhizoctonia-associated orchids. Oecologia 189, 375–383 (2019). https://doi.org/10.1007/s00442-019-04340-0

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  • DOI: https://doi.org/10.1007/s00442-019-04340-0

Keywords

  • Neottia ovata
  • Ophrys insectifera
  • Orchidaceae
  • Stable isotopes
  • Mycoheterotrophy
  • Mycorrhiza