Belowground Carbon Transfer Research Articles

Belowground carbon transfer across mycorrhizal networks among trees: Facts, not fantasy.

The mycorrhizal symbiosis between fungi and plants is among the oldest, ubiquitous and most important interactions in terrestrial life on Earth. Carbon (C) transfer across a common mycorrhizal network (CMN) was demonstrated over half a century ago in the lab ( Reid & Woods, 1969), and later in the field ( Simard et al., 1997a). Recent years have seen ample progress in this research direction, including evidence for ecological significance of carbon transfer ( Klein et al., 2016). Furthermore, specific cases where the architecture of mycorrhizal networks have been mapped ( Beiler et al., 2015) and CMN-C transfer from mature trees to seedlings has been demonstrated ( Orrego, 2018) have suggested that trees in forests are more connected than once thought ( Simard, 2021). In a recent Perspective, Karst et al. (2023) offered a valuable critical review warning of over-interpretation and positive citation bias in CMN research. It concluded that while there is evidence for C movement among plants, the importance of CMNs remains unclear, as noted by others too ( Henriksson et al., 2023). Here we argue that while some of these claims are justified, factual evidence about belowground C transfer across CMNs is solid and accumulating.

Asymmetric belowground carbon transfer in a diverse tree community.

Mycorrhizal fungi can colonize multiple trees of a single or multiple taxa, facilitating bidirectional exchange of carbon between trees. Mycorrhiza‐induced carbon transfer was shown in the forest, but it is unknown whether carbon is shared symmetrically among tree species, and if not, which tree species are better donors and which are better recipients. Here, we test this question by investigating carbon transfer dynamics among five Mediterranean tree species in a microcosm system, including both ectomycorrhizal (EM) and arbuscular (AM) plants. Trees were planted together in “community boxes” using natural soil from a mixed forest plot that serves as a habitat for all five tree species and their native mycorrhizal fungi. In each box, only the trees of a single species were pulse‐labelled with 13CO2. We found that carbon transfer was asymmetric, with oak being a better donor, and pistacia and cypress better recipients. Shared mycorrhizal species may have facilitated carbon transfer, but their diversity did not affect the amount, nor timing, of the transfer. Overall, our findings in a microcosm system expose rich, but hidden, belowground interactions in a diverse population of trees and mycorrhizal fungi. The asymmetric carbon exchange among cohabiting tree species could potentially contribute to forest resilience in an uncertain future.

Asymmetric belowground carbon transfer in a diverse tree community- Analysis

Asymmetric belowground carbon transfer in a diverse tree community- Analysis

Ectomycorrhizal fungi mediate belowground carbon transfer between pines and oaks.

Inter-kingdom belowground carbon (C) transfer is a significant, yet hidden, biological phenomenon, due to the complexity and highly dynamic nature of soil ecology. Among key biotic agents influencing C allocation belowground are ectomycorrhizal fungi (EMF). EMF symbiosis can extend beyond the single tree-fungus partnership to form common mycorrhizal networks (CMNs). Despite the high prevalence of CMNs in forests, little is known about the identity of the EMF transferring the C and how these in turn affect the dynamics of C transfer. Here, Pinus halepensis and Quercus calliprinos saplings growing in forest soil were labeled using a 13CO2 labeling system. Repeated samplings were applied during 36 days to trace how 13C was distributed along the tree-fungus-tree pathway. To identify the fungal species active in the transfer, mycorrhizal fine root tips were used for DNA-stable isotope probing (SIP) with 13CO2 followed by sequencing of labeled DNA. Assimilated 13CO2 reached tree roots within four days and was then transferred to various EMF species. C was transferred across all four tree species combinations. While Tomentella ellisii was the primary fungal mediator between pines and oaks, Terfezia pini, Pustularia spp., and Tuber oligospermum controlled C transfer among pines. We demonstrate at a high temporal, quantitative, and taxonomic resolution, that C from EMF host trees moved into EMF and that C was transferred further to neighboring trees of similar and distinct phylogenies.

Below-ground nitrogen transfer from oak seedlings facilitates Molinia growth: 15N pulse-chase labelling

Belowground carbon transfer from plant to plant has been extensively described, but such transfer for nitrogen has been less thoroughly investigated when the donor is a non-N2-fixing species. This study, applied to forest regeneration, aimed to determine whether tree seedlings facilitated neighbouring grass growth through nitrogen transfer at an early stage of development, thus facilitating nitrogen acquisition by understory species. Quercus petraea seedlings were planted in pots either sole-grown or mixed-grown with Molinia caerulea tufts or another oak seedling. 15N-urea pulse-chase labelling (cotton wick method) was performed in oak shoots and the fate of 15N in each soil and plant compartment was tracked for one year. N transfer pathways were investigated using two degrees of physical separation between root systems. Molinia dry weight was higher when mixed-grown with oak seedlings than when sole-grown. Increase in grass dry weight correlated with N transfer from donor oak to receiver Molinia. Interestingly, the presence of Molinia increased N rhizodeposition of oak. N allocation in donor oak towards root in winter and shoot in spring was enhanced. Oak seedlings facilitated Molinia growth through rapid N transfer, underlining the ability of non-N2-fixing species to supply N to neighbours. 15N allocation within donor oak and its rhizodeposition depended on neighbour identity.

Share the wealth: Trees with greater ectomycorrhizal species overlap share more carbon.

The mutualistic symbiosis between forest trees and ectomycorrhizal fungi (EMF) is among the most ubiquitous and successful interactions in terrestrial ecosystems. Specific species of EMF are known to colonize specific tree species, benefitting from their carbon source, and in turn, improving their access to soil water and nutrients. EMF also form extensive mycelial networks that can link multiple root-tips of different trees. Yet the number of tree species connected by such mycelial networks, and the traffic of material across them, are just now under study. Recently we reported substantial belowground carbon transfer between Picea, Pinus, Larix and Fagus trees in a mature forest. Here, we analyze the EMF community of these same individual trees and identify the most likely taxa responsible for the observed carbon transfer. Among the nearly 1,200 EMF root-tips examined, 50%-70% belong to operational taxonomic units (OTUs) that were associated with three or four tree host species, and 90% of all OTUs were associated with at least two tree species. Sporocarp 13 C signals indicated that carbon originating from labelled Picea trees was transferred among trees through EMF networks. Interestingly, phylogenetically more closely related tree species exhibited more similar EMF communities and exchanged more carbon. Our results show that belowground carbon transfer is well orchestrated by the evolution of EMFs and tree symbiosis.

Below-ground carbon transfer among Betula nana may increase with warming in Arctic tundra

• Shrubs are expanding in Arctic tundra, but the role of mycorrhizal fungi in this process is unknown. We tested the hypothesis that mycorrhizal networks are involved in interplant carbon (C) transfer within a tundra plant community. • Here, we installed below-ground treatments to control for C transfer pathways and conducted a (13)CO(2)-pulse-chase labelling experiment to examine C transfer among and within plant species. • We showed that mycorrhizal networks exist in tundra, and facilitate below-ground transfer of C among Betula nana individuals, but not between or within the other tundra species examined. Total C transfer among conspecific B. nana pairs was 10.7 ± 2.4% of photosynthesis, with the majority of C transferred through rhizomes or root grafts (5.2 ± 5.3%) and mycorrhizal network pathways (4.1 ± 3.3%) and very little through soil pathways (1.4 ± 0.35%). • Below-ground C transfer was of sufficient magnitude to potentially alter plant interactions in Arctic tundra, increasing the competitive ability and mono-dominance of B. nana. C transfer was significantly positively related to ambient temperatures, suggesting that it may act as a positive feedback to ecosystem change as climate warms.

Pathways for below-ground carbon transfer between paper birch and Douglas-fir seedlings

Background: Carbon can move below ground between ectomycorrhizal plants, but the relative importance of transfer through common mycorrhizal networks (CMNs) or soil pathways remains unclear. We studied carbon transfer between paper birch (Betula papyrifera) and Douglas-fir (Pseudotsuga menziesii) seedlings grown in adjacent root-restrictive pouches inside root chambers. Aims: The objective of this study was to compare transfer between CMN pathways and soil pathways by testing if: (1) carbon transfer between paper birch and Douglas-fir is bi-directional, (2) there is a net gain in carbon by one of the tree species; and (3) more carbon is transferred through the CMN pathway than the soil pathway. Methods: Following 8 months in the greenhouse, hyphal linkages crossing root pouches were either severed or left intact. Seedlings were then reciprocally labelled with 13CO2 and 14CO2. Results: We found carbon was transferred bi-directionally, with a 2–3% net gain in carbon by Douglas-fir from paper birch. Both bi-directional and net transfer occurred where the CMN was severed, but transfer was greater where it was left intact, indicating that carbon was transferred through both the soil and CMN pathways. Conclusions: Our results suggest that significant amounts of labelled carbon were transferred between plant species, showing for the first time in a balanced pulse-labelling experiment that approximately three times as much carbon was transferred through CMN pathways than soil pathways. That most carbon transfer occurred through CMNs could affect competitive interactions between establishing seedlings, favouring some included in the CMN while disadvantaging others, thus fundamentally altering our understanding of how interspecific interactions alter community structure.

Role of Soil Organisms in the Maintenance of Species‐Rich Seminatural Grasslands through Mowing

Abstract To preserve species‐rich grasslands, management practices such as mowing are often required. Mowing is known to promote aboveground conditions that help to maintain plant species richness, but whether belowground effects are important as well is not known. We hypothesized that if mowing decreases belowground carbon transfer by reducing root mass, this will reduce the abundance and activity of soil decomposers and lead to diminished nutrient availability in soil. In grasslands, this would provide a means to mitigate the negative effects of nitrogen enrichment on plant species richness. We established experimental plots on grassland with one‐third of plots growing untouched, one‐third mowed once a summer, and one‐third mowed twice a summer for three growing seasons. Root and soil attributes were measured at each plot 1 month after each mowing. Mowing decreased root mass but had few effects on belowground biota and soil NH4‐N, NO3‐N, and PO4‐P concentrations. Mowing did not affect root N concentrations. Our results show that despite reducing root mass, mowing may have few effects on those soil biota that control nutrient supply and, as a result, have no clear‐cut effects on nutrient availability in soil. This suggests that the effects of mowing on soil decomposers and soil nutrient availability may not provide an effective means to mitigate N enrichment and enhance plant species richness in grasslands in a timescale of a few years. Whether such effects could, however, be achieved with longer lasting mowing remains open.

Minimum pulses of stable and radioactive carbon isotopes to detect belowground carbon transfer between plants

Methodological problems, such as unwanted shifts in plant carbon allocation patterns following large isotopic labeling pulses, have hindered accurate quantification of belowground carbon movement in plant–soil systems. These problems must be addressed before we can understand the factors regulating carbon movement between plants and soils and the importance of this movement to the global carbon cycle. We studied the effects of pulse-label size on carbon allocation and transfer between ectomycorrhizal paper birch (Betula papyrifera Marsh.) and Douglas-fir (Pseudotsuga menziesii (Mirb.) Franco) seedlings using increasing pulse levels of either 13C or 14C in two separate laboratory experiments. Our specific objectives were: (1) to determine the minimum pulse of 13CO2 or 14CO2 for detecting carbon movement between plants through belowground transfer pathways, (2) to determine whether carbon allocation patterns within these plants change when exposed to short pulses of elevated carbon dioxide and, (3) to determine whether carbon allocation patterns are similar when using two different carbon isotopes. We detected carbon movement between plants at each 13C and 14C pulse level. There was a tendency for the amount of interplant carbon transfer to increase with increasing 13C pulse level, but the same amount of transfer occurred at all 14C pulses between 0.19 and 0.56 MBq. Carbon allocation patterns did not change with pulse level but they were affected by the choice of carbon isotope. We conclude that at least 8 ml of 13C or 0.19 MBq of 14C is sufficient to detect belowground carbon transfer in small seedlings growing in close proximity.

Interaction between foliar-feeding insects, mycorrhizal fungi, and rhizosphere protozoa on pea plants

Summary Pea plants ( Pisum sativum ) were grown in pots with and without the arbuscular mycorrhizal fungus (AMF) Glomus intraradices . Plants in each AM treatment were subjected to adult weevils ( Sitona lineatus ) during the periods 15–25 d or 23–39 d and were harvested at day 25 or day 39. Herbivory stimulated AMF root colonisation of mycorrhizal plants at the first harvest and stimulated rhizosphere protozoa in the absence of AMF. At the second harvest, herbivory decreased AMF colonization and had no effect on rhizosphere protozoa. The presence of AMF had no effect on herbivory at the first harvest but decreased herbivory at the second harvest. Below-ground respiration was stimulated by herbivory and this effect was most pronounced during vegetative growth. The results therefore suggest, that herbivory stimulated below-ground carbon transfer in young plants in the nutrient acquisition phase as opposed to the reproductive phase where herbivory had no such effect. This herbivory-induced carbon transfer will benefit the AMF symbiont when present and the free-living rhizosphere micro-organisms – here represented by the bacterivorous protozoa – in the absence of AMF.

Carbon allocation and carbon transfer between t Betula papyrifera and t Pseudotsuga menziesii seedlings using a 13C pulse-labeling method

Here we describe a simple method for pulse-labeling tree seedlings with 13CO2(gas), and then apply the method in two related experiments: t (i) comparison of carbon allocation patterns between t Betula papyrifera Marsh. and t Pseudotsuga menziesii (Mirb.) Franco, and t (ii) measurement of one-way belowground carbon transfer from t B. papyrifera to t P. menziesii. Intraspecific carbon allocation patterns and interspecific carbon transfer both influence resource allocation, and consequently development, in mixed communities of t B. papyrifera and t P. menziesii.