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Measuring carbon gains from fungal networks in understory plants from the tribe Pyroleae (Ericaceae): a field manipulation and stable isotope approach

  • Physiological ecology - Original research
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Abstract

Partial mycoheterotrophy, a newly discovered form of mixotrophy in plants, has been described in at least two major lineages of angiosperms, the orchids and ericaceous plants in the tribe Pyroleae. Partial mycoheterotrophy entails carbon gains both directly from photosynthesis and via symbiotic mycorrhizal fungi, but determining the degree of plant dependence on fungal carbon is challenging. The purpose of this study was to determine if two chlorophyllous species of Pyroleae, Chimaphila umbellata and Pyrola picta, were receiving carbon via mycorrhizal networks and, if so, if their proportional dependency on fungal carbon gains increased under reduced light conditions. This was accomplished by a field experiment that manipulated light and plants’ access to mycorrhizal networks, and by using the stable carbon isotope composition (δ13C) of leaf soluble sugars as a marker for the level of mycoheterotrophy. Based on leaf soluble sugars δ13C values, we calculated a site-independent isotope enrichment factor as a measure of fungal contributions to plant C. We found that, under each treatment and over time, the two test species demonstrated different isotopic responses caused by their different intrinsic physiologies. Our data, along with previously published studies, suggest that Chimaphila umbellata is primarily an autotrophic understory plant, while Pyrola picta may be capable of partial mycoheterotrophy. However, in this study, a 50% decrease in light availability did not significantly change the relative dependency of P. picta on carbon gains via mycoheterotrophy.

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Acknowledgments

The authors would like to thank the following people for assistance with the sample processing for this project: Alexandra Grote, Olga Lastovetskaya, Celia Jeanningros and Joyce Lee. We would also like to acknowledge Marc-André Selosse and other anonymous reviewers for their helpful feedback on previous versions of this manuscript. Professor Gerhard Gebauer, Professor Thomas D. Bruns, and Dr. Katja Preiss also provided critical insights during the development and execution of this study. N.A. Hynson would like to thank the UC Dissertation-Year fellowship, Sonoma Mycological Society and the San Francisco Mycological Society for their support of this research. The stable isotope analyses were supported by the Center for Stable Isotope Biogeochemisty at UC Berkeley.

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Authors and Affiliations

  1. Department of Botany, University of Hawai‘i at Manoa, Honolulu, HI, USA

    Nicole A. Hynson & Anthony S. Amend

  2. Department of Integrative Biology, University of California Berkeley, Berkeley, CA, USA

    Stefania Mambelli & Todd E. Dawson

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  1. Nicole A. Hynson
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Correspondence to Nicole A. Hynson.

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Communicated by Rowan Sage.

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442_2011_2198_MOESM1_ESM.eps

Supplementary Fig. 1 Mean δ13C values of leaf soluble sugars between treatments at each sampling, Pyrola picta (dark gray bars), Chimaphila umbellata (light gray bars), reference plants from P. picta plots (black bars), autotrophic reference plants from C. umbellata plots (open bars), error bars represent one standard error. Treatment A = 50% shade screen, treatment B = 50% shade screen and 0.7 m deep trench, treatment C = 0.7 m deep trench, treatment D = control, treatment E = 50% shade screen applied to a neighboring conifer seedling no taller than 0.5 m. Each graph corresponds to one of four sampling times: a) day 0; b) day 16; c) day 31; d) day 44. Letters that are different per Pyroleae species and corresponding reference plants and within a sampling time are significant at α ≤ 0.05 (EPS 461 kb)

442_2011_2198_MOESM2_ESM.eps

Supplementary Fig. 2 Change in mean percent nitrogen in Pyrola picta (a) and Chimaphila umbellata (b) from sampling time 0 (prior to treatment) to sampling time 3 (44 days of treatment) in treatments A–E. Treatment A = 50% shade screen, treatment B = 50% shade screen and 0.7 m deep trench, treatment C = 0.7 m deep trench, treatment D = control, treatment E = 50% shade screen applied to a neighboring conifer seedling. Open bars represent percent leaf nitrogen at time 0 and black bars represent time 3. Different letters signify significant differences between percent leaf N at time 0 versus time 3 at ∝≤0.05. Error bars are one standard error (EPS 439 kb)

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Hynson, N.A., Mambelli, S., Amend, A.S. et al. Measuring carbon gains from fungal networks in understory plants from the tribe Pyroleae (Ericaceae): a field manipulation and stable isotope approach. Oecologia 169, 307–317 (2012). https://doi.org/10.1007/s00442-011-2198-3

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