Benton N. Taylor’s research while affiliated with Harvard University and other places

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Publications (15)


Schematic overview of carbon (C) fluxes (red arrows), scales, and linkages addressed. Root exudates are examined at the branch level (SER, Specific Exudation Rate from fine roots), as fine-root exudate C flux per soil surface area (TER, Total Exudation Rate; i.e. SER that is upscaled to the fine-root system of an individual tree), and as relative exudation indicating the relationship between the exudate C flux and rate of net primary productivity (NPP) (REF, Root Exudation Fraction).
Schematic overview of the exudate collection approach. Root biomass and distribution are accessed e.g. via root boxes, and distal fine root branches are carefully excavated for exudate collection (A), cleaned with equilibrium solution and forceps, and allowed a pre-equilibration period. The system (B) is flushed at least once before exudate collection, which should span at least one diurnal cycle. Blanks are included for reference and all samples are filtered (pore size 0.22 µm). The exudate collection system (B) consists of several components. Prior to use, all syringes and glass beads are thoroughly cleaned with a muffle furnace and acid washing (preferably nitric acid). The root is immersed in an equilibrium solution (1) to maintain optimal conditions. A syringe or pump (2) is used to induce negative pressure, while another syringe (3) collects the exudates from the cleaned and living root (4). The syringe is sealed by a septum (5) to prevent contamination. Glass beads (6) provide support for the root, separated by a mesh (7). Exudates are collected in a glass vial (8) and passed through a 0.22 µm filter (9). For upscaling exudation rates (i.e., TER), information on root system biomass and distribution can be taken from minirhizotron and soil coring (A).
Tree carbon allocation to root exudates: Implications for carbon budgets, soil sequestration, and drought response
  • Article

March 2025

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306 Reads

Tree Physiology

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Carsten W Mueller

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Nikhil R Chari

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Root carbon (C) exudation plays a central role in nutrient acquisition, microbially mediated organic matter decomposition and many other critical ecosystem processes. While it is well known that roots respond strongly to belowground resources, we have a limited quantitative understanding about C allocation to exudates and its fate in soil under changing water availability. This review synthesizes the importance of exudate C fluxes, summarizes studies quantifying mass-specific exudation rate (SER), total exudation rate (TER) and root exudate fraction (REF; the proportion of TER in a plant’s C allocation), examines drought effects and highlights key research priorities to advance the understanding of C allocation to exudates in forest ecosystems. On average, SER is often <1 mg C gdry root−1 day−1, TER is 3.8 Pg C year−1 and REF varies between 1 and 17% of net primary production. Spatiotemporal variations in exudation, including seasonal and daily patterns and subsoil exudation, remain critical knowledge gaps. We show that many studies report a 1.2- to 11-fold increase in SER and REF in response to drought. However, TER often remains unchanged, suggesting that absolute exudate C inputs to the soil may stay constant under drought conditions. Disentangling the individual impacts of soil and air drought as well as drought legacy impacts on ecosystem C dynamics are overlooked aspects. By estimating the differences in rhizosphere formation and exudation across various forest biomes, we find that exudate-affected soil volumes are highest in tropical forests and lowest in boreal forests. While current research emphasizes significant C allocation from the canopy to soil via exudates, understanding exudation dynamics and biome-specific responses to drought by using standardized protocols is essential. Expanding these insights is critical for comprehending the role of root exudates in soil organic matter formation, ecosystem resilience and adaptation to climate change.


Symbiotic nitrogen fixation in trees: Patterns, controls, and ecosystem consequences

December 2024

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20 Reads

Tree Physiology

Symbiotic nitrogen fixation (SNF) represents the largest natural input of bioavailable nitrogen into the biosphere, impacting key processes spanning from local community dynamics to global patterns of nutrient limitation and primary productivity. While research on SNF historically focused largely on herbaceous and agricultural species, the past two decades have seen major advances in our understanding of SNF by tree species in forest and savanna communities. This has included important developments in the mathematical theory of SNF in forest ecosystems, experimental work on the regulators of tree SNF, broad observational analyses of tree N-fixer abundance patterns, and increasingly process-based incorporation of tree SNF into ecosystem models. This review synthesizes recent work on the local and global patterns, environmental drivers, and community and ecosystem effects of nitrogen-fixing trees in natural ecosystems. By better understanding the drivers and consequences of SNF in forests, this review aims to shed light on the future of this critical process and its role in forest functioning under changing climate, nutrient cycling, and land use.


Effects of warming on root biomass (a), specific root length (b), and average root diameter (c) of AM and EM roots in control (grey) and warmed (red) plots. Error bars are standard error.
Root exudation (a, b) and root respiration (c, d) from AM and EM tree species in response to soil warming, standardized by root surface area (a, c) and root biomass (b, d). Error bars are standard errors.
Relationships between exudation and respiration (a, b) and specific root length (SRL) and exudation (c, d) in AM (gold circles) and EM (purple triangles) trees in control (a, c) and warmed (b, d) plots. We note that the relationships observed in (a) and (c) remain significant when the far right points are removed from the data (Figure S4).
Mycorrhizal colonization rates of (a) AM root systems and (b) EM root systems in response to warming. AM colonization is measured as a percentage of root tissue colonized and EM colonization is measured as percentage of root tips colonized. Error bars are standard error. The asterisks (***) mean that p < 0.001.
Biplots for principal components analyses of belowground C allocation patterns for (a) AM roots and (b) EM roots. Each dot is from a control sub‐plot (shaded white ellipse) and each triangle is from a heated sub‐plot (shaded pink ellipse). Arrows show different C allocation pathways, where AFRB and TFRB (absorptive and transport fine root biomass) are “exploratory,” myc. col. (mycorrhizal colonization) is “symbiotic,” and exudation is “exudative.” Ellipses represent 68% confidence intervals.
Long‐Term Soil Warming Drives Different Belowground Responses in Arbuscular Mycorrhizal and Ectomycorrhizal Trees
  • Article
  • Publisher preview available

November 2024

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36 Reads

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3 Citations

The ability of trees to acquire soil nutrients under future climate conditions will influence forest composition and function in a warmer world. Rarely are multiple belowground carbon allocation pathways measured simultaneously in large global change experiments, restricting our understanding of how trees may shift their allocation of resources to different nutrient acquisition mechanisms under future climates. Leveraging a 20‐year soil warming experiment, we show that ectomycorrhizal (EM) trees reduce mycorrhizal colonization and root exudation while increasing fine root biomass, while arbuscular mycorrhizal (AM) trees largely maintained their belowground carbon allocation patterns in warmer soils. We suggest that AM trees may be better adapted to thrive under global warming due to higher rates of nitrogen mineralization in warmer soils and the ability of their mycorrhizal symbiont to acquire mineralized inorganic nutrients, whereas EM trees may need to alter their belowground carbon allocation patterns to remain competitive as global temperatures rise.

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Representation of carbon and nutrient pathways in EcM–plant–herbivore interactions. Red and blue arrows represent carbon and nutrient pathways, respectively. (1) As hypothesised by the carbon/nutrient balance, as atmospheric CO2 increases plants will allocate more resources to build more C‐based chemical defences. (2) Elevated CO2 (eCO2) increases EcM colonisation, providing extra nutrients to the host plant. (3) As eCO2 increases EcM colonisation there may be an increase in the mantle thickness, associated with a change in EcM fungi composition. It is still unclear if this thickness could directly influence root herbivores. However, the mantle trichome‐like structures might act as a physical barrier against root herbivores. (4) EcM‐associated plants have high xylem nutrient contents, which specifically benefits xylem feeders. (5) Elevated CO2 dilutes plant nutrient concentrations, but EcM could maintain high N levels, meaning that higher herbivory rates could increase C lost to herbivores. EcM, ectomycorrhizal.
Published data on the response of herbivory to elevated CO2 (eCO2) for arbuscular mycorrhizal (AM), both AM and ectomycorrhizal (EcM) (Dual), and EcM tree species for in‐situ forested CO2 manipulation experiments. Point colours respond to the tree genus studied, with the mycorrhizal association of each genus specified in the legend. Points are jittered within each mycorrhizal type for visibility. The full data set and a description of the data collection process can be found in the S1.
Shifting interactions between ectomycorrhizae, plants and insect herbivores in a CO2‐enriched world

October 2024

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85 Reads

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1 Citation

Increasing atmospheric CO2 concentrations are changing how plants interact with their biotic mutualists and antagonists, but few syntheses consider how the three‐way interactions between mycorrhizae, plants and herbivores will shift under rising CO2. We summarise the mechanisms by which ectomycorrhizal (EcM)‐associated plants, their mycorrhizae and insect herbivores interact with each other under current conditions and evaluate a set of expectations for how these interactions might shift under higher CO2. We then outline priorities for future work on EcM–plant–herbivore interactions as atmospheric CO2 continues to rise. EcM colonisation has variable but often positive effects on herbivory, while herbivory has consistently negative impacts on EcM colonisation. Mechanistic evidence suggests that the positive EcM effect on herbivory will strengthen and the negative impact of herbivory on EcM will be ameliorated under higher CO2. Synthesis: While more empirical evidence on fungal–plant–herbivore interactions is needed in EcM systems, our synthesis suggests that EcM associations may play an under‐recognised role in dictating future terrestrial carbon capture by mediating herbivory and the ability of plants to compensate for herbivory as atmospheric CO2 continues to rise.


More diverse rhizobial communities can lead to higher symbiotic nitrogen fixation rates, even in nitrogen-rich soils

July 2024

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50 Reads

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2 Citations

Symbiotic nitrogen (N) fixation (SNF) by legumes and their rhizobial partners is one of the most important sources of bioavailable N to terrestrial ecosystems. While most work on the regulation of SNF has focussed on abiotic drivers such as light, water and soil nutrients, the diversity of rhizobia with which individual legume partners may play an important but under-recognized role in regulating N inputs from SNF. By experimentally manipulating the diversity of rhizobia available to legumes, we demonstrate that rhizobial diversity can increase average SNF rates by more than 90%, and that high rhizobial diversity can induce increased SNF even under conditions of high soil N fertilization. However, the effects of rhizobial diversity, the conditions under which diversity effects were the strongest, and the likely mechanisms driving these diversity effects differed between the two legume species we assessed. These results provide evidence that biodiversity–ecosystem function relationships can occur at the scales of an individual plant and that the effects of rhizobial diversity may be as important as long-established abiotic factors, such as N availability, in driving terrestrial N inputs via SNF.


CoRRE Trait Data: A dataset of 17 categorical and continuous traits for 4079 grassland species worldwide

July 2024

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565 Reads

Scientific Data

In our changing world, understanding plant community responses to global change drivers is critical for predicting future ecosystem composition and function. Plant functional traits promise to be a key predictive tool for many ecosystems, including grasslands; however, their use requires both complete plant community and functional trait data. Yet, representation of these data in global databases is sparse, particularly beyond a handful of most used traits and common species. Here we present the CoRRE Trait Data, spanning 17 traits (9 categorical, 8 continuous) anticipated to predict species’ responses to global change for 4,079 vascular plant species across 173 plant families present in 390 grassland experiments from around the world. The dataset contains complete categorical trait records for all 4,079 plant species obtained from a comprehensive literature search, as well as nearly complete coverage (99.97%) of imputed continuous trait values for a subset of 2,927 plant species. These data will shed light on mechanisms underlying population, community, and ecosystem responses to global change in grasslands worldwide.


a distribution of sites in the dataset on the globe colored by biome, b proportional distribution of plant functional types in the dataset, c proportional distribution of mycorrhizal types in the dataset. The numbers in (b) and (c) are the number of observations of each type. While the number of observations (n = 149) are presented in this figure, the analyses of paper were carried out based on the number of studies (n = 44), as many studies include multiple observations
Conceptual figure illustrating the scaling process described in Methods. Specific root exudation rates (expressed on a per root mass basis) were scaled spatially using estimates of absorptive fine root biomass and temporally using estimates of growing season length to get exudate C flux estimates on a per-meter ground area basis (Fex). Estimates of Fex were scaled by land surface area as described in Methods to determine a global root exudate C flux estimate (Gex)
Exudation rates by biome. a mass-specific exudation rate, b soil area specific exudate C flux, c proportion of GPP released as root exudates. For each biome, horizontal lines represent the median and boxes represent the inter-quartile range and whiskers represent 1.5 times the interquartile range. Colored dots represent individual data points (studies) used in our analyses and corresponding black dots represent outliers. Panel-wide black horizontal lines are cross-biome geometric means
The proportion of the global root exudate flux from each biome (left) and the proportion of studies represented in our dataset from each biome (right). The left bar shows the proportional contribution of each biome to the global root exudate flux (Table 1). The right bar shows the proportion of studies in our dataset from each biome. The total number of data points for the right bar is 44 independent studies
Estimating the global root exudate carbon flux

July 2024

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302 Reads

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9 Citations

Biogeochemistry

Root exudation, the export of low-molecular weight organic carbon (C) from living plant roots to soil, influences microbial activity, nutrient availability, and ecosystem feedbacks to climate change, but the magnitude of this C flux at ecosystem and global scales is largely unknown. Here, we synthesize in situ measurements of root exudation rates and couple those to estimates of fine root biomass to estimate global and biome-level root exudate C fluxes. We estimate a global root exudate flux of 13.4 (10.1–20.2) Pg C y⁻¹, or about 9% (7–14%) of global annual gross primary productivity. We did not find differences in root mass-specific exudation rates among biomes, though total exudate fluxes are estimated to be greatest in grasslands owing to their high density of absorptive root biomass. Our synthesis highlights the global importance of root exudates in the terrestrial C cycle and identifies regions where more in situ measurements are needed to improve future estimates of root exudate C fluxes.


Damage to tropical forests caused by cyclones is driven by wind speed but mediated by topographical exposure and tree characteristics

May 2024

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260 Reads

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7 Citations

Each year, an average of 45 tropical cyclones affect coastal areas and potentially impact forests. The proportion of the most intense cyclones has increased over the past four decades and is predicted to continue to do so. Yet, it remains uncertain how topographical exposure and tree characteristics can mediate the damage caused by increasing wind speed. Here, we compiled empirical data on the damage caused by 11 cyclones occurring over the past 40 years, from 74 forest plots representing tropical regions worldwide, encompassing field data for 22,176 trees and 815 species. We reconstructed the wind structure of those tropical cyclones to estimate the maximum sustained wind speed (MSW) and wind direction at the studied plots. Then, we used a causal inference framework combined with Bayesian generalised linear mixed models to understand and quantify the causal effects of MSW, topographical exposure to wind (EXP), tree size (DBH) and species wood density (ρ) on the proportion of damaged trees at the community level, and on the probability of snapping or uprooting at the tree level. The probability of snapping or uprooting at the tree level and, hence, the proportion of damaged trees at the community level, increased with increasing MSW, and with increasing EXP accentuating the damaging effects of cyclones, in particular at higher wind speeds. Higher ρ decreased the probability of snapping and to a lesser extent of uprooting. Larger trees tended to have lower probabilities of snapping but increased probabilities of uprooting. Importantly, the effect of ρ decreasing the probabilities of snapping was more marked for smaller than larger trees and was further accentuated at higher MSW. Our work emphasises how local topography, tree size and species wood density together mediate cyclone damage to tropical forests, facilitating better predictions of the impacts of such disturbances in an increasingly windier world.


Belowground foundations of tropical forest restoration

February 2024

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51 Reads

Biotropica

There is great global interest in tropical forest restoration, but many restoration efforts are not effective. Here we argue for the importance of belowground processes in tropical forest restoration and provide suggestions of next steps to advance our understanding of belowground processes in tropical forest restoration success.


The global root exudate carbon flux

February 2024

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467 Reads

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2 Citations

Root exudation, the export of low-molecular weight organic carbon (C) from living plant roots to soil, influences microbial activity, nutrient availability, and ecosystem feedbacks to climate change, but the magnitude of this C flux at ecosystem and global scales is largely unknown. Here, we synthesize in situ measurements of root exudation rates and couple those to estimates of fine root biomass to estimate global and biome-level root exudate C fluxes. We estimate a global root exudate flux of 15.2 PgC y ⁻¹ , or about 10% of global annual gross primary productivity. We found no differences in root mass-specific exudation rates among biomes, though total exudate fluxes are estimated to be greatest in grasslands owing to their high density of absorptive root biomass. Our synthesis highlights the global importance of root exudates in the terrestrial C cycle and identifies regions where more in situ measurements are needed to improve future estimates of root exudate C fluxes.


Citations (8)


... For EM trees, however, proliferating absorptive roots could achieve greater efficiency of inorganic nutrient acquisition than facilitating EM mycelia proliferation (Fig. 1c). This is because the EM mycelia are poor in directly absorbing inorganic nutrients (Liese et al., 2018;Chari et al., 2024) and have higher maintenance costs than EM roots (Řezáčová et al., 2017;Hawkins et al., 2023). Absorptive roots of EM trees are also generally finer (and thus cheaper) than those of AM trees (Comas et al., 2014;. ...

Reference:

Complementary foraging of roots and mycorrhizal fungi among nutrient patch types in four subtropical monospecific broadleaved tree plantations
Long‐Term Soil Warming Drives Different Belowground Responses in Arbuscular Mycorrhizal and Ectomycorrhizal Trees

... We have assembled a range of reviews, mini-reviews and research articles that investigate different aspects of mutualist-plant-enemy interactions and their effects on plant communities. These papers investigate multitrophic interactions from the molecular level (Cheng & Yu, 2024;Cibils-Stewart et al., 2024;Fernández et al., 2024) through to the consequences for plant community structure (Bryant & Bever, 2024;Duell et al., 2024;Milici et al., 2024;Pajares-Murgó et al., 2024;Zalamea et al., 2023;Zehr et al., 2024) and plant-microorganism coevolution (Eagar et al., 2024). Here, we provide a brief introduction to the Cross-Journal Special Feature. ...

Shifting interactions between ectomycorrhizae, plants and insect herbivores in a CO2‐enriched world

... As a major component of cell walls, the content of C is mainly controlled by genetic characteristics [26]. The small increase in C contents after stumping may be ascribed to the rapid synthesis of new tissue and the carbon sequestration caused by increased root secretion [27]. ...

Estimating the global root exudate carbon flux

Biogeochemistry

... Previous research shows that a TC causes total defoliage, uprooting and snapping in a mangrove forest (Smith et al. 2009). The degree of defoliage and the number of uprooting is directly related to the intensity of the cyclone (Ibanez et al. 2024). Because, if wind intensity increases then drag force also increases according to the following drag force equation (White 2016): = 1 2 2 where, Fd = drag force, Cd = drag coefficient, A = frontal area of the object and, υ = wind velocity. ...

Damage to tropical forests caused by cyclones is driven by wind speed but mediated by topographical exposure and tree characteristics

... Intensifying typhoons can alter the vegetation canopy structure and the photosynthetic capacity, primarily through mechanical disruption from gale-force winds [ 16 ]. The vegetation canopy is disproportionately exposed to typhoons, suffering from varying levels of defoliation [ 17 ], which will subsequently diminish its carbon sequestration capacity [ 18 ]. ...

Widespread stem snapping but limited mortality caused by a category 5 hurricane on the Caribbean Island of Dominica
  • Citing Article
  • March 2023

Forest Ecology and Management

... In the 30-60 cm layer, the δ 13 C of MAOC was statistically indistinguishable between 0, 4, 6, 14 and 30 years of recultivation (variation from − 25.0 to − 26.5 ‰). Additionally, plant biomass, compost, and root-derived C input to soil and N fertilization of crops possibly promoted positive priming of MAOC (Thiessen et al., 2013;Shahbaz et al., 2017;Chari and Taylor, 2022;Tian et al., 2024), including the subsoil (Schiedung et al., 2023), ultimately preventing a more pronounced increase in MRT of SOC with recultivation age. This may be investigated in future studies. ...

Soil organic matter formation and loss are mediated by root exudates in a temperate forest

... Given the challenges of measuring N fixation (Winbourne et al. 2018a;Soper et al. 2021) and the challenges of studying timescales relevant to forest succession (Chazdon et al. 2007;Feldpausch et al. 2007), it is not a surprise that we do not have a definitive answer to these questions. There is a growing number of studies looking at symbiotic N fixation through forest succession (e.g., Pearson and Vitousek 2001;Batterman et al. 2013;Sullivan et al. 2014;Bauters et al. 2016;Winbourne et al. 2018b;Taylor et al. 2019), including excellent work with Robinia Swank 1984a, 1984b;Wurzburger et al. 2022). ...

A roadmap for sampling and scaling biological nitrogen fixation in terrestrial ecosystems
  • Citing Article
  • March 2021

... belonging to the superclade V/ Kakadu supergroup. This suggests that S. longifolia would seem rather to be a specialist than a generalist, thus probably obtaining more benefits from this symbiont, as suggested by Taylor et al. (2020). The same authors added that if the dominant legume species overloads the soil bacterial community with its rhizobial partner, it may facilitate its own growth at the expense of other legume species. ...

More Than a Functional Group: Diversity within the Legume–Rhizobia Mutualism and Its Relationship with Ecosystem Function