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Phillips, Richard P.

Publications and source records attributed to Phillips, Richard P..

At least 19 records

Extreme drought impacts have been underestimated in grasslands and shrublands globally

Climate change is increasing the frequency and severity of short-term (~1 y) drought events—the most common duration of drought—globally. Yet the impact of this intensification of drought on ecosystem functioning remains poorly resolved. This is due in part to the widely disparate approaches ecologists have employed to study drought, variation in the severity and duration of drought studied, and differences among ecosystems in vegetation, edaphic and climatic attributes that can mediate drought impacts. To overcome these problems and better identify the factors that modulate drought responses, we used a coordinated distributed experiment to quantify the impact of short-term drought on grassland and shrubland ecosystems. With a standardized approach, we imposed ~a single year of drought at 100 sites on six continents. Here we show that loss of a foundational ecosystem function—aboveground net primary production (ANPP)—was 60% greater at sites that experienced statistically extreme drought (1-in-100-y event) vs. those sites where drought was nominal (historically more common) in magnitude (35% vs. 21%, respectively). This reduction in a key carbon cycle process with a single year of extreme drought greatly exceeds previously reported losses for grasslands and shrublands. Our global experiment also revealed high variability in drought response but that relative reductions in ANPP were greater in drier ecosystems and those with fewer plant species. Overall, our results demonstrate with unprecedented rigor that the global impacts of projected increases in drought severity have been significantly underestimated and that drier and less diverse sites are likely to be most vulnerable to extreme drought.

54 ENVIRONMENTAL SCIENCES↗

Effects of root litter traits on soil organic matter dynamics depend on decay stage and root branching order

Decaying roots contribute disproportionately to soil organic carbon (SOC) stocks in many ecosystems, yet few studies have examined the afterlife effects of root trait variability on the formation, stability and mineralization of SOC. In order to assess how root functional class (absorptive vs. transport) and mycorrhizal association (ectomycorrhizal vs. arbuscular mycorrhizal fungi) affect both formation and loss of SOC, we decayed lower-order absorptive (orders 1–2) and higher-order transport (orders 3–4) roots from six arbuscular mycorrhizal (AM) and six ectomycorrhizal (EcM) associated hardwood tree species in an isotopically distinct soil under laboratory conditions. We found that root litter effects on SOC differed significantly among root functional classes and mycorrhizal types. AM absorptive and transport roots (high in nitrogen and soluble compounds) contributed more to the formation of new mineral-associated organic carbon (MAOC), but also contributed to higher mineralization of native SOC (via priming effects). Moreover, absorptive AM roots formed MAOC gradually and rates saturated, whereas ECM roots formed MAOC more quickly, despite slower decay (via greater formation efficiency). Altogether, these findings demonstrate how different combinations of root traits might contribute to soil C balance, and that failure to account for the chemical and morphological heterogeneity of roots, as well their interactions with microbes over time, may lead to incorrect projections of SOC stocks and turnover.

59 BASIC BIOLOGICAL SCIENCES↗

Imprint of tree species mycorrhizal association on microbial‐mediated enzyme activity and stoichiometry

Abstract Understanding the effects of tree species and their mycorrhizal association on soil processes is critical for predicting the ecosystem consequences of species shifts owing to global change and forest management decisions. While it is well established that forests dominated by different mycorrhizal types can vary in how they cycle carbon (C), nitrogen (N) and phosphorus (P), the degree to which these patterns are driven by microbial‐mediated enzyme activity (EA) and ecoenzymatic stoichiometry (ES) remains elusive. Here, we synthesized the effects of mycorrhizal association on seven soil enzymes involved in microbial C, N and P acquisition and ES using data from 56 peer‐reviewed papers. We found that relative to soil in ectomycorrhizal (EcM) trees, soil in arbuscular mycorrhizal (AM) trees exhibited greater activity of some C acquisition enzymes (e.g. beta‐glucosidase; BG) and higher ecoenzymatic ratios of BG/NAG (N‐acetyl‐glucosaminidase) and BG/AP (acid phosphatase). These results supported that AM trees had rapid C and nutrient turnover rates, inorganic nutrient economics and high soil microbial C limitation. We also found evidence for an organic nutrient economy and greater soil microbial demand for nutrients in EcM trees compared to AM trees. In addition, the effect of mycorrhizal association on the activity of certain soil enzymes and enzymatic stoichiometry (i.e. BG and BG/NAG ratio) appeared to be associated with the differences in soil pH, phylogenetic group (i.e. conifers and broadleaves) and leaf habit (i.e. evergreen and deciduous) between AM and EcM trees. The results from the global meta‐analysis suggested that soil EA and ES appear to play critical roles in shaping the differences in the nutrient economy between AM and EcM tree species, but leaf morphology and soil conditions should be considered in evaluations of soil processes in forests of different mycorrhizal associations. Given that most of the studies in the database were from the temperate and subtropical regions, further research in other biomes is needed to elucidate the underlying mechanisms driving the mycorrhizal effect at the global scale. Read the free Plain Language Summary for this article on the Journal blog.

54 ENVIRONMENTAL SCIENCES↗

Climate, soil mineralogy and mycorrhizal fungi influence soil organic matter fractions in eastern US temperate forests

Identifying the primary controls of particulate (POM) and mineral-associated organic matter (MAOM) content in soils is critical for determining future stocks of soil carbon (C) and nitrogen (N) across the globe. However, drivers of these soil organic matter fractions are likely to vary among ecosystems in response to climate, soil type and the composition of local biological communities. We tested how soil factors, climate and plant–fungal associations influenced the distribution and concentrations of C and N in MAOM and POM in seven temperate forests in the National Ecological Observatory Network (NEON) across the eastern United States. Samples of upper mineral horizon soil within each forest were collected in plots representing a gradient of dominant tree–mycorrhizal association, allowing us to test how plant and microbial communities influenced POM and MAOM across sites differing in climate and soil conditions. We found that concentrations of C and N in soil organic matter were primarily driven by soil mineralogy, but the relative abundance of MAOM versus POM C was strongly linked to plot-level mycorrhizal dominance. Furthermore, the effect of dominant tree mycorrhizal type on the distribution of N among POM and MAOM fractions was sensitive to local climate: in cooler sites, an increasing proportion of ectomycorrhizal-associated trees was associated with lower proportions of N in MAOM, but in warmer sites, we found the reverse. As an indicator of soil carbon age, we measured radiocarbon in the MAOM fraction but found that within and across sites, Δ 14 C was unrelated to mycorrhizal dominance, climate, or soil factors, suggesting that additional site-specific factors may be primary determinants of long-term SOM persistence. Our results indicate that while soil mineralogy primarily controls SOM C and N concentrations, the distribution of SOM among density fractions depends on the composition of vegetation and microbial communities, with these effects varying across sites with distinct climates. Here we also suggest that within biomes, the age of mineral-associated soil carbon is not clearly linked to the factors that control concentrations of MAOM C and N.

54 ENVIRONMENTAL SCIENCES↗

Arbuscular Mycorrhizal Tree Communities Have Greater Soil Fungal Diversity and Relative Abundances of Saprotrophs and Pathogens than Ectomycorrhizal Tree Communities

Trees associating with different mycorrhizas often differ in their effects on litter decomposition, nutrient cycling, soil organic matter (SOM) dynamics, and plant-soil interactions. For example, due to differences between arbuscular mycorrhizal (AM) and ectomycorrhizal (ECM) tree leaf and root traits, ECM-associated soil has lower rates of C and N cycling and lower N availability than AM-associated soil. These observations suggest that many groups of nonmycorrhizal fungi should be affected by the mycorrhizal associations of dominant trees through controls on nutrient availability. To test this overarching hypothesis, we explored the influence of predominant forest mycorrhizal type and mineral N availability on soil fungal communities using next-generation amplicon sequencing. Soils from four temperate hardwood forests in southern Indiana, United States, were studied; three forests formed a natural gradient of mycorrhizal dominance (100% AM tree basal area to 100% ECM basal area), while the fourth forest contained a factorial experiment testing long-term N addition in both dominant mycorrhizal types. We found that overall fungal diversity, as well as the diversity and relative abundance of plant pathogenic and saprotrophic fungi, increased with greater AM tree dominance. Additionally, tree community mycorrhizal associations explained more variation in fungal community composition than abiotic variables, including soil depth, SOM content, nitrification rate, and mineral N availability. Our findings suggest that tree mycorrhizal associations may be good predictors of the diversity, composition, and functional potential of soil fungal communities in temperate hardwood forests. These observations help explain differing biogeochemistry and community dynamics found in forest stands dominated by differing mycorrhizal types.

59 BASIC BIOLOGICAL SCIENCES↗

The xylem of anisohydric Quercus alba L. is more vulnerable to embolism than isohydric codominants

Abstract The coordination of plant leaf water potential (Ψ L ) regulation and xylem vulnerability to embolism is fundamental for understanding the tradeoffs between carbon uptake and risk of hydraulic damage. There is a general consensus that trees with vulnerable xylem more conservatively regulate Ψ L than plants with resistant xylem. We evaluated if this paradigm applied to three important eastern US temperate tree species, Quercus alba L., Acer saccharum Marsh. and Liriodendron tulipifera L., by synthesizing 1600 Ψ L observations, 122 xylem embolism curves and xylem anatomical measurements across 10 forests spanning pronounced hydroclimatological gradients and ages. We found that, unexpectedly, the species with the most vulnerable xylem ( Q. alba ) regulated Ψ L less strictly than the other species. This relationship was found across all sites, such that coordination among traits was largely unaffected by climate and stand age. Quercus species are perceived to be among the most drought tolerant temperate US forest species; however, our results suggest their relatively loose Ψ L regulation in response to hydrologic stress occurs with a substantial hydraulic cost that may expose them to novel risks in a more drought‐prone future.

Benson, Michael C.↗

Mycorrhizal associations of tree species influence soil nitrogen dynamics via effects on soil acid–base chemistry

Across all spatial scales, ECM-dominated forests were associated with greater soil acidity. In particular, ECM-dominated soils exhibited lower soil pH and base cations, although the magnitude of mycorrhizal-associated differences in soil acid–base chemistry depended on the biomes, with differences being more pronounced in temperate than in sub/tropical forests. Higher lignin and lower base cations in ECM tree leaf litter were related to greater soil acidity in ECM-dominated forests. Moreover, the lower inorganic N concentrations and slower N transformation rates in ECM-dominated forests were associated with their greater soil acidity. Our results indicate that the scale-invariant feedbacks between plant nutrient-use strategies and soil properties have the potential to impact forest community assembly and ecosystem processes, particularly in the context of global change.

37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CH↗

Mycorrhizal Distributions Impact Global Patterns of Carbon and Nutrient Cycling

Most tree species predominantly associate with a single type of mycorrhizal fungi, which can differentially affect plant nutrient acquisition and biogeochemical cycling. Uncertainties in mycorrhizal distributions are non-trivial, and current estimates disagree in up to 50% over 40% of the land area, including tropical forests. Remote sensing capabilities for mycorrhizal detection show promise for refining these estimates further. Here, we address for the first time the impact of mycorrhizal distributions on global carbon and nutrient cycling. Using the state-of-the-art carbon-nitrogen economics within the Community Land Model version 5, we found Net Primary Productivity (NPP) increased throughout the 21st century by 20%; however, as soil nitrogen has progressively become limiting, the costs to NPP for nitrogen acquisition—that is, to mycorrhizae—have increased at a faster rate by 60%. This suggests that nutrient acquisition will increasingly demand a higher portion of assimilated carbon to support the same productivity.

54 ENVIRONMENTAL SCIENCES↗

Tree Canopies Reflect Mycorrhizal Composition

Mycorrhizae alter global patterns of CO 2 fertilization, carbon storage, and elemental cycling, yet knowledge of their global distributions is currently limited by the availability of forest inventory data. Here, we show that maps of tree-mycorrhizal associations (hereafter “mycorrhizal maps”) can be improved by the novel technology of imaging spectroscopy because mycorrhizal signatures propagate up from plant roots to impact forest canopy chemistry. We analyzed measurements from 143 airborne imaging spectroscopy surveys over 112,975 individual trees collected across 13 years. Results show remarkable accuracy in capturing ground truth observations of mycorrhizal associations from canopy signals across disparate landscapes (R 2 = 0.92, p < 0.01). Additionally, upcoming imaging spectroscopy satellite missions can reveal new insights into landscape-scale variations in water, nitrogen, phosphorus, carotenoid/anthocyanin, and cellulose/lignin composition. Applied globally, this approach could improve the spatial precision of mycorrhizal distributions by a factor of roughly 104 and facilitate the incorporation of dynamic shifts in forest composition into Earth system models.

58 GEOSCIENCES↗

Carbon–Nutrient Economy of the Rhizosphere: Improving Biogeochemical Prediction and Scaling Feedbacks from Ecosystem to Regional Scales

Our project has advanced the science of plant-soil-microbial dynamics across these areas: i) nutrient cycling and plant uptake; ii) root exudation and priming; and, iii) mycorrhizal dynamics. Our project has accomplished 5 main developments: 1) Incorporation of phosphorus cycling into the Fixation & Uptake of Nutrients (FUN 3.0) model. 2) Coupling of FUN 3.0 into the E3SM Land Model (ELM). 3) Data collection across a large mycorrhizal gradient in the US, as well data in the tropics, to parameterize, test, and validate the model. 4)Scaling up mycorrhizal association measurements across landscapes using airborne hyperspectral remote sensing data. 5) Evaluation of global carbon and nutrient cycle impacts in the Community Land Model (CLM5.0) from a suite of new global mycorrhizal association maps. Over 25 publications resulted from this project, with more continuing past the project funded lifetime. Paper highlights from most of these publications have already been submitted to the DOE paper submission online system. These publications include journals such as Science and PNAS, as well as top disciplinary journals from the Nature journals, Global Change Biology, New Phytologist, and Ecology Letters, for example. Our project also contributed to improving the process representation, capabilities, and accuracy of the DOE ELM. Overall, this project significantly advanced the science of belowground plant-soil-microbial interactions as well as technical capabilities from remote sensing to modeling.

59 BASIC BIOLOGICAL SCIENCES↗

Arbuscular mycorrhizal trees cause a higher carbon to nitrogen ratio of soil organic matter decomposition via rhizosphere priming than ectomycorrhizal trees

Tree roots and their associated microbes can significantly influence soil organic matter (SOM) decomposition, i.e., the rhizosphere priming effect. This effect is expected to be greater in trees associated with arbuscular mycorrhizal (AM) fungi, which produce higher extracellular enzymes especially surrounding hyphae, than in trees associated with ectomycorrhizal (ECM) fungi. In this work, we selected five tree species associated with AM (Juglans mandshurica Maxim. and Cunninghamia lanceolata (Lamb.) Hook.) or ECM (Picea koraiensis Nakai, Quercus mongolica Fischer ex Turcz. and Larix kaempferi (Lamb.) Carriere). We grew tree seedlings inside of cores lined with different mesh sizes to investigate how roots, hyphae and exudates influence soil carbon (C) and nitrogen (N) mineralization via the rhizosphere priming effect, using a 13 C natural abundance approach and a 15 N pool dilution method, concurrently. We found that tree seedlings significantly accelerated soil C decomposition by on average 78%, i.e., positive priming, compared to unplanted control pots. AM-associated trees induced 2.1 times greater soil C decomposition than ECM-associated trees across all mesh sizes. In contrast, gross N mineralization did not differ between tree-mycorrhizal associations. Compared to ECM counterparts, AM-associated trees had higher C- and lower N-degrading enzyme activities. Consequently, AM-associated trees induced a significantly higher C:N ratio of SOM decomposition than their ECM counterparts, which could be associated with the differences in soil enzyme activities for C and N degradation. Further, for both AM- and ECM-associated trees, we found no significant influences of mesh size on soil C decomposition, suggesting that the rhizosphere priming effect of mycorrhizal symbiosis was predominantly driven by root exudates. We conclude that SOM decomposition caused by AM-associated trees may have a higher C:N ratio than that by ECM-associated trees mainly due to differences in microbial enzyme investment. Our findings imply that tree-mycorrhizal associations are capable of modulating soil biogeochemical cycling via the rhizosphere priming effect.

54 ENVIRONMENTAL SCIENCES↗

A trade-off between plant and soil carbon storage under elevated CO 2

Terrestrial ecosystems remove about 30 per cent of the carbon dioxide (CO 2 ) emitted by human activities each year, yet the persistence of this carbon sink depends partly on how plant biomass and soil organic carbon (SOC) stocks respond to future increases in atmospheric CO 2 . Although plant biomass often increases in elevated CO 2 (eCO 2 ) experiments, SOC has been observed to increase, remain unchanged or even decline. The mechanisms that drive this variation across experiments remain poorly understood, creating uncertainty in climate projections. In this study we synthesized data from 108 eCO 2 experiments and found that the effect of eCO 2 on SOC stocks is best explained by a negative relationship with plant biomass: when plant biomass is strongly stimulated by eCO 2 , SOC storage declines; conversely, when biomass is weakly stimulated, SOC storage increases. This trade-off appears to be related to plant nutrient acquisition, in which plants increase their biomass by mining the soil for nutrients, which decreases SOC storage. We found that, overall, SOC stocks increase with eCO 2 in grasslands (8 ± 2 per cent) but not in forests (0 ± 2 per cent), even though plant biomass in grasslands increase less (9 ± 3 per cent) than in forests (23 ± 2 per cent). Ecosystem models do not reproduce this trade-off, which implies that projections of SOC may need to be revised.

54 ENVIRONMENTAL SCIENCES↗

Variation in hyphal production rather than turnover regulates standing fungal biomass in temperate hardwood forests

Abstract Soil fungi link above‐ and belowground carbon (C) fluxes through their interactions with plants and contribute to C and nutrient dynamics through the production, turnover, and activity of fungal hyphae. Despite their importance to ecosystem processes, estimates of hyphal production and turnover rates are relatively uncommon, especially in temperate hardwood forests. We sequentially harvested hyphal ingrowth bags to quantify the rates of Dikarya (Ascomycota and Basidiomycota) hyphal production and turnover in three hardwood forests in the Midwestern United States, where plots differed in their abundance of arbuscular (AM)‐ vs. ectomycorrhizal (ECM)‐associated trees. Hyphal production rates increased linearly with the percentage of ECM trees and annual production rates were 66% higher in ECM‐ than AM‐dominated plots. Hyphal turnover rates did not differ across the mycorrhizal gradient (plots varying in their abundance of AM vs. ECM trees), suggesting that the greater fungal biomass in ECM‐dominated plots relates to greater fungal production rather than slower fungal turnover. Differences in hyphal production across the gradient aligned with distinctly different fungal communities and activities. As ECM trees increased in dominance, fungi inside ingrowth bags produced more extracellular enzymes involved in degrading nitrogen (N)‐bearing relative to C‐bearing compounds, suggesting greater fungal (and possibly plant) N demand in ECM‐dominated soils. Collectively, our results demonstrate that shifts in temperate tree species composition that result in changes in the dominant type of mycorrhizal association may have strong impacts on Dikarya hyphal production, fungal community composition and extracellular enzyme activity, with important consequences for soil C and N cycling.

59 BASIC BIOLOGICAL SCIENCES↗