Plant family identity distinguishes patterns of carbon and nitrogen stable isotope abundance and nitrogen concentration in mycoheterotrophic plants associated with ectomycorrhizal fungi

Abstract

These authors contributed equally to this work. Background and Aims Mycoheterotrophy entails plants meeting all or a portion of their carbon (C) demands via symbiotic interactions with root-inhabiting mycorrhizal fungi. Ecophysiological traits of mycoheterotrophs, such as their C stable isotope abundances, strongly correlate with the degree of species' dependency on fungal C gains relative to C gains via photosynthesis. Less explored is the relationship between plant evolutionary history and mycoheterotrophic plant ecophysiology. We hypothesized that the C and nitrogen (N) stable isotope compositions, and N concentrations of fully and partially mycoheterotrophic species differentiate them from autotrophs, and that plant family identity would be an additional and significant explanatory factor for differences in these traits among species. We focused on mycoheterotrophic species that associate with ectomycorrhizal fungi from plant families Ericaceae and Orchidaceae.Methods Published and unpublished data were compiled on the N concentrations, C and N stable isotope abundances (d 13 C and d 15 N) of fully (n ¼ 18) and partially (n ¼ 22) mycoheterotrophic species from each plant family as well as corresponding autotrophic reference species (n ¼ 156). These data were used to calculate siteindependent C and N stable isotope enrichment factors (e). Then we tested for differences in N concentration, 13C and 15 N enrichment among plant families and trophic strategies. Key Results We found that in addition to differentiating partially and fully mycoheterotrophic species from each other and from autotrophs, C and N stable isotope enrichment also differentiates plant species based on familial identity. Differences in N concentrations clustered at the plant family level rather than the degree of dependency on mycoheterotrophy.Conclusions We posit that differences in stable isotope composition and N concentrations are related to plant family-specific physiological interactions with fungi and their environments.

Mycorrhizal fungi affect orchid distribution and population dynamics

“…The extent to which OMFs contribute to the support of mature photosynthetic orchids is still an open question and likely varies among species and habitats (Girlanda et al ., ; Sommer et al ., ; Selosse & Martos, ; McCormick & Jacquemyn, ; Liebel et al ., ; Hynson et al ., ). Fungi almost certainly play an important role during periods of vegetative dormancy, a widespread phenomenon where plants, including many orchids, fail to produce any aboveground tissues, but remain physiologically active, during one or more growing seasons (Shefferson et al ., , , , ; Shefferson, ).…”

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.…”

“…Due to its cryptic manifestation, partial mycoheterotrophy has so far only been confirmed for over 20 species of Orchidaceae (Hynson et al, ; Schiebold et al, ), although it seems much more likely that many more orchid species, if not all, show evidence of partial mycoheterotrophy (Schiebold et al, ). Further evidence for partial mycoheterotrophy has been found in c. 8 species of Ericaceae (within Pyrola, Orthilia and possibly Chimaphila and Moneses ), a single species of Burmanniaceae ( Burmannia coelestis ), and has been suggested for Gentianaceae ( Bartonia virginica and Obolaria virginica ) (Cameron & Bolin, ; but see Hynson, Madsen, et al, ; Hynson, Weiss, et al, ).…”

Stable Isotopes from Museum Specimens May Provide Evidence of Long-Term Change in the Trophic Ecology of a Migratory Aerial Insectivore

“…In terrestrial communities, plant foliage forms the base of many food chains. Foliage isotope values vary across spatial and temporal scales depending on climate, disturbance, and nutrient availability (Amundson et al, 2003;Craine et al, 2009;Pardo and Nadelhoffer, 2010;Popa-Lisseanu et al, 2015;Moreno et al, 2016;Taki et al, 2017) and with physiological differences between plant species, including variation in photosynthetic pathways (Basu et al, 2015;Courty et al, 2015;Taki et al, 2017) and mycorrhizal associations (Evans, 2001;Craine et al, 2009;Hynson et al, 2016). At longer time scales changes in atmospheric baselines, climate, and habitat succession can all cause progressive change in foliage isotopic signatures (Evans and Belnap, 1999;FoxDobbs et al, 2007;Wang et al, 2007;Taki et al, 2017).…”