Suzanne W. Simard

Net transfer of carbon between ectomycorrhizal tree species in the field

Different plant species can be compatible with the same species of mycorrhizal fungi, and be connected to one another by a common mycelium,. Transfer of carbon, nitrogen, and phosphorus, through interconnecting mycelia has been measured frequently in laboratory experiments, but it is not known whether transfer is bidirectional, whether there is a net gain by one plant over its connected partner, or whether transfer affects plant performance in the field,. Laboratory studies using isotope tracers show that the magnitude of one-way transfer can be influenced by shading of ‘receiver’ plants,, fertilization of ‘donor’ plants with phosphorus, or use of nitrogen-fixing donor plants and non-nitrogen-fixing receiver plants,, indicating that movement may be governed by source–sink relationships. Here we use reciprocal isotope labelling in the field to demonstrate bidirectional carbon transfer between the ectomycorrhizal tree species Betula papyrifera and Pseudotsuga menziesii, resulting in net carbon gain by P. menziesii. Thuja plicata seedlings lacking ectomycorrhizae absorb small amounts of isotope, suggesting that carbon transfer between B. papyrifera and P. menziesii is primarily through the direct hyphal pathway. Net gain by P. menziesii seedlings represents on average 6% of carbon isotope uptake through photosynthesis. The magnitude of net transfer is influenced by shading of P. menziesii, indicating that source–sink relationships regulate such carbon transfer under field conditions.

Carbon and Nutrient Fluxes Within and Between Mycorrhizal Plants

Mycorrhizal fungi are involved in the uptake of nutrients in exchange for C from host plants, and possibly in the transfer of C and nutrients between plants. Ecto-mycorrhizal fungi (EMF) increase uptake rates of nutrients by a variety of mechanisms, including increased physical access to soil, changes to mycorrhizosphere or hyphosphere chemistry, and alteration of the bacterial community in the mycorrhizosphere. They influence mycorrhizosphere chemistry through release of organic acids and production of enzymes. Movement of nutrients within an ecto-mycorrhizal (EM) mycelial network, as well as exchange of C and nutrients between symbionts, appear to be regulated by source-sink relationships. Estimates of the quantity of plant C partitioned belowground (to roots and EMF) varies widely (40–73%) depending on the methodology used and ecosystem studied, and is affected by several factors such as the identity of plant and fungal species, plant nutrient content, and EM age.

Long-term warming alters the composition of Arctic soil microbial communities

Despite the importance of Arctic soils in the global carbon cycle, we know very little of the impacts of warming on the soil microbial communities that drive carbon and nutrient cycling in these ecosystems. Over a 2-year period, we monitored the structure of soil fungal and bacterial communities in organic and mineral soil horizons in plots warmed by greenhouses for 18 years and in control plots. We found that microbial communities were stable over time but strongly structured by warming. Warming led to significant reductions in the evenness of bacterial communities, while the evenness of fungal communities increased significantly. These patterns were strongest in the organic horizon, where temperature change was greatest and were associated with a significant increase in the dominance of the Actinobacteria and significant reductions in the Gemmatimonadaceae and the Proteobacteria. Greater evenness of the fungal community with warming was associated with significant increases in the ectomycorrhizal fungi, Russula spp., Cortinarius spp., and members of the Helotiales suggesting that increased growth of the shrub Betula nana was an important mechanism driving this change. The shifts in soil microbial community structure appear sufficient to account for warming-induced changes in nutrient cycling in Arctic tundra as climate warms.

Architecture of the wood-wide web: Rhizopogon spp. genets link multiple Douglas-fir cohorts.

*The role of mycorrhizal networks in forest dynamics is poorly understood because of the elusiveness of their spatial structure. We mapped the belowground distribution of the fungi Rhizopogon vesiculosus and Rhizopogon vinicolor and interior Douglas-fir trees (Pseudotsuga menziesii var. glauca) to determine the architecture of a mycorrhizal network in a multi-aged old-growth forest. *Rhizopogon spp. mycorrhizas were collected within a 30 x 30 m plot. Trees and fungal genets were identified using multi-locus microsatellite DNA analysis. Tree genotypes from mycorrhizas were matched to reference trees aboveground. Two trees were considered linked if they shared the same fungal genet(s). *The two Rhizopogon species each formed 13-14 genets, each colonizing up to 19 trees in the plot. Rhizopogon vesiculosus genets were larger, occurred at greater depths, and linked more trees than genets of R. vinicolor. Multiple tree cohorts were linked, with young saplings established within the mycorrhizal network of Douglas-fir veterans. A strong positive relationship was found between tree size and connectivity, resulting in a scale-free network architecture with small-world properties. *This mycorrhizal network architecture suggests an efficient and robust network, where large trees play a foundational role in facilitating conspecific regeneration and stabilizing the ecosystem.

Viewing forests through the lens of complex systems science

Complex systems science provides a transdisciplinary framework to study systems characterized by (1) heterogeneity, (2) hierarchy, (3) self-organization, (4) openness, (5) adaptation, (6) memory, (7) non-linearity, and (8) uncertainty. Complex systems thinking has inspired both theory and applied strategies for improving ecosystem resilience and adaptability, but applications in forest ecology and management are just beginning to emerge. We review the properties of complex systems using four well-studied forest biomes (temperate, boreal, tropical and Mediterranean) as examples. The lens of complex systems science yields insights into facets of forest structure and dynamics that facilitate comparisons among ecosystems. These biomes share the main properties of complex systems but differ in specific ecological properties, disturbance regimes, and human uses. We show how this approach can help forest scientists and managers to conceptualize forests as integrated social-ecological systems and provide concrete examples of how to manage forests as complex adaptive systems.

From Lilliput to Brobdingnag: Extending Models of Mycorrhizal Function across Scales

ABSTRACT Mycorrhizae occur in nearly all terrestrial ecosystems. Resource exchange between host plants and mycorrhizal fungi influences community, ecosystem, and even global patterns and processes. Understanding the mechanisms and consequences of mycorrhizal symbioses across a hierarchy of scales will help predict system responses to environmental change and facilitate the management of these responses for sustainability and productivity. Conceptual and mathematical models have been developed to help understand and predict mycorrhizal functions. These models are most developed for individual- and population-scale processes, but models at community, ecosystem, and global scales are also beginning to emerge. We review seven types of mycorrhizal models that vary in their scale of resolution and dynamics, and discuss approaches for integrating these models with each other and with general models of terrestrial ecosystems.

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.In preparation for the two experiments, we first identified the appropriate 13CO2(gas) pulse-chase regime for labeling seedlings: a range of pulse (100-mL and 200-mL 99 atom%13 CO2(gas)) and chase (0, 3 and 6 d) treatments were applied to one year-old t B. papyrifera and t P. menziesii seedlings. The amount of 13CO2 fixed immediately after 1.5 h exposure was greatest for both t B. papyrifera (40.8 mg excess 13C) and t P. menziesii (22.9 mg excess 13C) with the 200-mL pulse, but higher 13C loss and high sample variability resulted in little difference in excess13 C content between pulse treatments after 3 d for either species. The average excess 13C root/shoot ratio of t B. papyrifera and t P. menziesii changed from 0.00 immediately following the pulse to 0.61 and 0.87 three and six days later, which reflected translocation of 75% of fixed isotope out of foliage within 3 d following the pulse and continued enrichment in fine roots over 6 d. Based on these results, the 100-mL CO2(gas) and 6-d chase were considered appropriate for the carbon allocation and belowground transfer experiments.In the carbon allocation experiment, we found after 6 d that t B. papyrifera allocated 49% (average 9.5 mg) and t P. menziesii 41% (average 5.8 mg) of fixed isotope to roots, of which over 55% occurred in fine roots in both species. Species differences in isotope allocation patterns paralleled differences in tissue biomass distribution. The greater pulse labeling efficiency of t B. papyrifera compared to t P. menziesii was associated with its two-fold and 13- fold greater leaf and whole seedling net photosynthetic rates, respectively, 53% greater biomass, and 35% greater root/shoot ratio.For the carbon transfer experiment, t B. papyrifera and t P. menziesii were grown together in laboratory rootboxes, with their roots intimately mingled. A pulse of 100 mL13 CO2(gas) was applied to paper birch and one-way transfer to neighboring t P. menziesii was measured after 6 d. Of the excess 13C fixed by t B. papyrifera, 4.7% was transferred to neighboring t P. menziesii, which distributed the isotope evenly between roots and shoots. Of the isotope received by t P. menziesii, we estimated that 93% was taken up through belowground pathways, and the remaining 7% taken up by foliage as13 CO2(gas) respired by t B. papyrifera shoots. These two experiments indicate that t B. papyrifera fixes more total carbon and allocates a greater proportion to its root system than does t P. menziesii, giving it a competitive edge in resource gathering; however, below-ground carbon sharing is of sufficient magnitude that it may help ensure co-existence of the two species in mixed communities.

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.

Aboveground biomass and nutrient accumulation in an age sequence of paper birch (Betula papyrifera) in the Interior Cedar Hemlock zone, British Columbia

Abstract The aboveground biomass and nutrient content (N, P, K, Ca, Mg) of stands of Betula papyrifera Marsh, aged 2, 8, 15, 45, 60, 75 years were measured in the Thompson Moist Warm Interior Cedar Hemlock variant (ICHmw3) of the southern interior of British Columbia. For four of these ages (2, 8, 60 and 75 years) measurements were made on good, medium and poor sites. For the other two ages, only stands on good sites coulde be located. Allometric equations relating dry weights of stemwood, stembark, branches and leaves to tree diameter at breast height (DBH) were developed to estimate aboveground tree biomass. Equations were not significantly different among the three site qualities. Average total aboveground tree biomass for all sites increased with stand age from 1.4 t ha −1 in 2-year-old stands (varying from 0.45 to 2.1 t ha −1 on poor and good sites, respectively) to 202 t ha −1 in the 75-year-old stand (156 and 234 t ha −1 on poor and good sites, respectively). As stand age increased, an increasing proportion of annual biomass increment was allocated to stems, but nutrients were preferentially accumulated in the leaves. Nutrient content of aboveground tree biomass increased with stand age and was generally in the order of N > Ca > K > Mg > P. Average rates of nutrients accumulation in biomass were greatest in the early stages of stand development, and less marked as stands aged. The concentrations of nutrients in tissues decreased in the following order: leaf > branch > stembark > stemwood. Understory minor vegetation contributed little to the nutrient pool of these paper birch ecosystems. Mineral soil contained the largest amount of nutrients among the various ecosystem components.

Influence of soil nutrients on ectomycorrhizal communities in a chronosequence of mixed temperate forests

Many factors associated with forests are collectively responsible for controlling ectomycorrhizal (ECM) fungal community structure, including plant species composition, forest structure, stand age, and soil nutrients. The objective of this study was to examine relationships among ECM fungal community measures, local soil nutrients, and stand age along a chronosequence of mixed forest stands that were similar in vegetation composition and site quality. Six combinations of age class (5-, 26-, 65-, and 100-year-old) and stand initiation type (wildfire and clearcut) were replicated on four sites, each representing critical seral stages of stand development in Interior Cedar-Hemlock (ICH) forests of southern British Columbia. We found significant relationships between ECM fungal diversity and both available and organic P; available P was also positively correlated with the abundance of two ECM taxa (Rhizopogon vinicolor group and Cenoccocum geophilum). By contrast, ECM fungal diversity varied unpredictably with total and mineralizable N or C to N ratio. We also found that soil C, N, available P, and forest floor depth did not exhibit strong patterns across stand ages. Overall, ECM fungal community structure was more strongly influenced by stand age than specific soil nutrients, but better correlations with soil nutrients may occur at broader spatial scales covering a wider range of site qualities.