The complex circuitry of interactions determining coexistence among plants and mycorrhizal fungi.

We present a mechanistic model of coexistence among a mycorrhizal fungus and one or two plant species that compete for a single nutrient. Plant-fungal coexistence is more likely if the fungus is better at extracting the environmental nutrient than the plant and the fungus acquires carbon from the plant above a minimum rate. When they coexist, their interaction can shift from mutualistic to parasitic at high nutrient availability. The fungus is a second nutrient source for plants and can promote the coexistence of two plant competitors if one is better at environmental nutrient extraction and the other is better at acquiring the nutrient from the fungus. Because it extracts carbon from both plants, the fungus also serves as a conduit of apparent competition between the plants. Consequently, the plant with the lower environmental nutrient extraction rate can drive the plant with the higher environmental nutrient extraction rate extinct at high carbon supply rates. This model illustrates mechanisms to explain several observed patterns, including shifts in plant-mycorrhizal growth responses and coexistence along nutrient gradients, equivocal results among experiments testing the effect of mycorrhizal fungi on plant diversity, and differences in plant diversity among ecosystems dominated by different mycorrhizal groups.

Ecosystem and soil respiration radiocarbon detects old carbon release as a fingerprint of warming and permafrost destabilization with climate change.

The permafrost region has accumulated organic carbon in cold and waterlogged soils over thousands of years and now contains three times as much carbon as the atmosphere. Global warming is degrading permafrost with the potential to accelerate climate change as increased microbial decomposition releases soil carbon as greenhouse gases. A 19-year time series of soil and ecosystem respiration radiocarbon from Alaska provides long-term insight into changing permafrost soil carbon dynamics in a warmer world. Nine per cent of ecosystem respiration and 23% of soil respiration observations had radiocarbon values more than 50‰ lower than the atmospheric value. Furthermore, the overall trend of ecosystem and soil respiration radiocarbon values through time decreased more than atmospheric radiocarbon values did, indicating that old carbon degradation was enhanced. Boosted regression tree analyses showed that temperature and moisture environmental variables had the largest relative influence on lower radiocarbon values. This suggested that old carbon degradation was controlled by warming/permafrost thaw and soil drying together, as waterlogged soil conditions could protect soil carbon from microbial decomposition even when thawed. Overall, changing conditions increasingly favoured the release of old carbon, which is a definitive fingerprint of an accelerating feedback to climate change as a consequence of warming and permafrost destabilization. This article is part of the Theo Murphy meeting issue 'Radiocarbon in the Anthropocene'.

Differences in soil organic matter between EcM- and AM-dominated forests depend on tree and fungal identity.

As global change shifts the species composition of forests, we need to understand which species characteristics affect soil organic matter (SOM) cycling to predict future soil carbon (C) storage. Recently, whether a tree species forms a symbiosis with arbuscular (AM) versus ectomycorrhizal (EcM) fungi has been suggested as a strong predictor of soil C storage, but there is wide variability within EcM systems. In this study, we investigated how mycorrhizal associations and the species composition of canopy trees and mycorrhizal fungi related to the proportion of soil C and nitrogen (N) in mineral associations and soil C:N across four sites representing distinct climates and tree communities in the eastern US broadleaf forest biome. In two of our sites, we found the expected relationship of declining mineral-associated C and N and increasing soil C:N ratios as the basal area of EcM-associating trees increased. However, across all sites these soil properties strongly correlated with canopy tree and fungal species composition. Sites where the expected pattern with EcM basal area was observed were (1) dominated by trees with lower quality litter in the Pinaceae and Fagaceae families and (2) dominated by EcM fungi with medium-distance exploration type hyphae, melanized tissues, and the potential to produce peroxidases. This observational study demonstrates that differences in SOM between AM and EcM systems are dependent on the taxa of trees and EcM fungi involved. Important information is lost when the rich mycorrhizal symbiosis is reduced to two categories.

Beyond bulk: Density fractions explain heterogeneity in global soil carbon abundance and persistence.

Understanding the controls on the amount and persistence of soil organic carbon (C) is essential for predicting its sensitivity to global change. The response may depend on whether C is unprotected, isolated within aggregates, or protected from decomposition by mineral associations. Here, we present a global synthesis of the relative influence of environmental factors on soil organic C partitioning among pools, abundance in each pool (mg C g-1  soil), and persistence (as approximated by radiocarbon abundance) in relatively unprotected particulate and protected mineral-bound pools. We show that C within particulate and mineral-associated pools consistently differed from one another in degree of persistence and relationship to environmental factors. Soil depth was the best predictor of C abundance and persistence, though it accounted for more variance in persistence. Persistence of all C pools decreased with increasing mean annual temperature (MAT) throughout the soil profile, whereas persistence increased with increasing wetness index (MAP/PET) in subsurface soils (30-176 cm). The relationship of C abundance (mg C g-1  soil) to climate varied among pools and with depth. Mineral-associated C in surface soils (<30 cm) increased more strongly with increasing wetness index than the free particulate C, but both pools showed attenuated responses to the wetness index at depth. Overall, these relationships suggest a strong influence of climate on soil C properties, and a potential loss of soil C from protected pools in areas with decreasing wetness. Relative persistence and abundance of C pools varied significantly among land cover types and soil parent material lithologies. This variability in each pool's relationship to environmental factors suggests that not all soil organic C is equally vulnerable to global change. Therefore, projections of future soil organic C based on patterns and responses of bulk soil organic C may be misleading.

Five years of whole-soil warming led to loss of subsoil carbon stocks and increased CO2 efflux.

Subsoils below 20 cm are an important reservoir in the global carbon cycle, but little is known about their vulnerability under climate change. We measured a statistically significant loss of subsoil carbon (-33 ± 11%) in warmed plots of a conifer forest after 4.5 years of whole-soil warming (4°C). The loss of subsoil carbon was primarily from unprotected particulate organic matter. Warming also stimulated a sustained 30 ± 4% increase in soil CO2 efflux due to increased CO2 production through the whole-soil profile. The observed in situ decline in subsoil carbon stocks with warming is now definitive evidence of a positive soil carbon-climate feedback, which could not be concluded based on increases in CO2 effluxes alone. The high sensitivity of subsoil carbon and the different responses of soil organic matter pools suggest that models must represent these heterogeneous soil dynamics to accurately predict future feedbacks to warming.

Plants and earthworms control soil carbon and water quality trade-offs in turfgrass mesocosms.

Understanding how plants and earthworms regulate soil-based ecosystem services can guide design and management of built environments to improve environmental quality. We tested whether plant and earthworm activity results in trade-offs between soil carbon (C) retention and water quality. In a 2 × 2 factorial random block design, we introduced shrubs (Aronia melanocarpa) and earthworms (Lumbricus terrestris) to turfgrass (Lolium perenne) sandy loam mesocosms in a greenhouse. We measured soil respiration and soil microclimate every two weeks and leachate every two months. After 15 months, we assessed C and nitrogen (N) in bulk soil and aggregates (> 2000, 2000-250, 250-53 µm). Turfgrass mesocosms with earthworms retained less soil C (6.10 ± 0.20 kg/m2), especially when warmer. Soils planted with shrubs were drier and had 7% lower mean respiration rates than soils without shrubs. Turfgrass mesocosms with both shrubs and earthworms retained more soil C (6.66 ± 0.25 kg/m2), even when warmer, and held ~1.5 times more C in >2 mm aggregates than turfgrass-only mesocosms. Turfgrass mesocosms with shrubs and earthworms leached nitrate-N with increased respiration and retained phosphate-P and dissolved organic carbon (DOC) when wetter. In contrast, turfgrass mesocosms with only shrubs had the opposite response by leaching less nitrate-N with increased respiration, and more phosphate-P and DOC when wetter. Overall, shrub and earthworm activity in turfgrass mesocosms led to soil C-nutrient retention trade-offs. Our results reveal potential challenges in managing built environments to both retain soil C and improve water quality.

Drainage enhances modern soil carbon contribution but reduces old soil carbon contribution to ecosystem respiration in tundra ecosystems.

Warming temperatures are likely to accelerate permafrost thaw in the Arctic, potentially leading to the release of old carbon previously stored in deep frozen soil layers. Deeper thaw depths in combination with geomorphological changes due to the loss of ice structures in permafrost, may modify soil water distribution, creating wetter or drier soil conditions. Previous studies revealed higher ecosystem respiration rates under drier conditions, and this study investigated the cause of the increased ecosystem respiration rates using radiocarbon signatures of respired CO2 from two drying manipulation experiments: one in moist and the other in wet tundra. We demonstrate that higher contributions of CO2 from shallow soil layers (0-15 cm; modern soil carbon) drive the increased ecosystem respiration rates, while contributions from deeper soil (below 15 cm from surface and down to the permafrost table; old soil carbon) decreased. These changes can be attributed to more aerobic conditions in shallow soil layers, but also the soil temperature increases in shallow layers but decreases in deep layers, due to the altered thermal properties of organic soils. Decreased abundance of aerenchymatous plant species following drainage in wet tundra reduced old carbon release but increased aboveground plant biomass elevated contributions of autotrophic respiration to ecosystem respiration. The results of this study suggest that drier soils following drainage may accelerate decomposition of modern soil carbon in shallow layers but slow down decomposition of old soil carbon in deep layers, which may offset some of the old soil carbon loss from thawing permafrost.

Response to Comment on "The whole-soil carbon flux in response to warming".

Temperature records and model predictions demonstrate that deep soils warm at the same rate as surface soils, contrary to Xiao et al's assertions. In response to Xiao et al's critique of our Q10 analysis, we present the results with all data points included, which show Q10 values of >2 throughout the soil profile, indicating that all soil depths responded to warming.

The whole-soil carbon flux in response to warming.

Soil organic carbon harbors three times as much carbon as Earth's atmosphere, and its decomposition is a potentially large climate change feedback and major source of uncertainty in climate projections. The response of whole-soil profiles to warming has not been tested in situ. In a deep warming experiment in mineral soil, we found that CO2 production from all soil depths increased with 4°C warming; annual soil respiration increased by 34 to 37%. All depths responded to warming with similar temperature sensitivities, driven by decomposition of decadal-aged carbon. Whole-soil warming reveals a larger soil respiration response than many in situ experiments (most of which only warm the surface soil) and models.

Decadal warming causes a consistent and persistent shift from heterotrophic to autotrophic respiration in contrasting permafrost ecosystems.

Soil carbon in permafrost ecosystems has the potential to become a major positive feedback to climate change if permafrost thaw increases heterotrophic decomposition. However, warming can also stimulate autotrophic production leading to increased ecosystem carbon storage-a negative climate change feedback. Few studies partitioning ecosystem respiration examine decadal warming effects or compare responses among ecosystems. Here, we first examined how 11 years of warming during different seasons affected autotrophic and heterotrophic respiration in a bryophyte-dominated peatland in Abisko, Sweden. We used natural abundance radiocarbon to partition ecosystem respiration into autotrophic respiration, associated with production, and heterotrophic decomposition. Summertime warming decreased the age of carbon respired by the ecosystem due to increased proportional contributions from autotrophic and young soil respiration and decreased proportional contributions from old soil. Summertime warming's large effect was due to not only warmer air temperatures during the growing season, but also to warmer deep soils year-round. Second, we compared ecosystem respiration responses between two contrasting ecosystems, the Abisko peatland and a tussock-dominated tundra in Healy, Alaska. Each ecosystem had two different timescales of warming (<5 years and over a decade). Despite the Abisko peatland having greater ecosystem respiration and larger contributions from heterotrophic respiration than the Healy tundra, both systems responded consistently to short- and long-term warming with increased respiration, increased autotrophic contributions to ecosystem respiration, and increased ratios of autotrophic to heterotrophic respiration. We did not detect an increase in old soil carbon losses with warming at either site. If increased autotrophic respiration is balanced by increased primary production, as is the case in the Healy tundra, warming will not cause these ecosystems to become growing season carbon sources. Warming instead causes a persistent shift from heterotrophic to more autotrophic control of the growing season carbon cycle in these carbon-rich permafrost ecosystems.

Thawing permafrost increases old soil and autotrophic respiration in tundra: partitioning ecosystem respiration using δ(13) C and ∆(14) C.

Ecosystem respiration (Reco ) is one of the largest terrestrial carbon (C) fluxes. The effect of climate change on Reco depends on the responses of its autotrophic and heterotrophic components. How autotrophic and heterotrophic respiration sources respond to climate change is especially important in ecosystems underlain by permafrost. Permafrost ecosystems contain vast stores of soil C (1672 Pg) and are located in northern latitudes where climate change is accelerated. Warming will cause a positive feedback to climate change if heterotrophic respiration increases without corresponding increases in primary production. We quantified the response of autotrophic and heterotrophic respiration to permafrost thaw across the 2008 and 2009 growing seasons. We partitioned Reco using Δ(14) C and δ(13) C into four sources-two autotrophic (above - and belowground plant structures) and two heterotrophic (young and old soil). We sampled the Δ(14) C and δ(13) C of sources using incubations and the Δ(14) C and δ(13) C of Reco using field measurements. We then used a Bayesian mixing model to solve for the most likely contributions of each source to Reco . Autotrophic respiration ranged from 40 to 70% of Reco and was greatest at the height of the growing season. Old soil heterotrophic respiration ranged from 6 to 18% of Reco and was greatest where permafrost thaw was deepest. Overall, growing season fluxes of autotrophic and old soil heterotrophic respiration increased as permafrost thaw deepened. Areas with greater thaw also had the greatest primary production. Warming in permafrost ecosystems therefore leads to increased plant and old soil respiration that is initially compensated by increased net primary productivity. However, barring large shifts in plant community composition, future increases in old soil respiration will likely outpace productivity, resulting in a positive feedback to climate change.