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Duncan N.L. Menge

Publications and source records attributed to Duncan N.L. Menge.

11 recordsLinked to original sources

Global carbon investment in terrestrial biological nitrogen fixation

Biological nitrogen (N) fixation (BNF) provides the N needed to produce proteins and other biological building blocks, helping feed humanity and mitigate climate change. Due to its high energetic cost compared to other forms of N acquisition, biotic investment in BNF indicates N limitation. Globally gridded BNF flux data provide an opportunity to determine the energetic investment in BNF across ecosystems, which would help reconcile conflicting indicators of N limitation. Here, we use a new BNF synthesis to quantify the relative importance of BNF in different N-fixing niches, in different biomes, and across the globe by calculating the fraction of net primary productivity (NPP) invested in BNF and the fraction of plant N acquisition provided by BNF. Larger fractions of non-agricultural NPP were invested in BNF in less-productive, higher-latitude biomes. This pattern was driven by biocrusts and mosses. Similarly, non-agricultural symbiotic N-fixing plants invested relatively more of their own NPP in BNF in less-productive, higher-latitude biomes. This symbiotic plant pattern was driven by shrubs and herbs, overriding the opposite pattern in trees. Symbiotic plants also acquired a higher fraction of their N from BNF at higher latitudes and in less productive biomes. Investments in symbiotic BNF were 10× higher in agricultural (2.9% of NPP) versus natural (0.29%) biomes, providing 26% versus 3.1% of ecosystem-scale plant N acquisition. These results support the paradigm of strong N limitation at higher latitudes, help understand the rarity of N-fixing trees at higher latitudes, underscore the dominance of human activity, and inform terrestrial biosphere models.

Global Biogeochemical Cycles

Overestimated natural biological nitrogen fixation translates to an exaggerated CO2 fertilization effect in Earth System Models

CO 2 fertilization of the terrestrial biosphere is limited by nitrogen. Biological nitrogen fixation (BNF) is the dominant natural nitrogen source to the terrestrial biosphere and can alleviate nitrogen limitation but is poorly constrained in Earth system models (ESMs). Here, we compare terrestrial BNF from an ensemble of ESMs of the 6th Coupled Model Intercomparison Project to a new global synthesis of observations across natural and agricultural biomes. We find that compared to observations, ESMs underestimate agricultural BNF but overestimate natural BNF in the present day by over 50%. Natural BNF is overestimated in the most productive ecosystems that contribute most to the terrestrial carbon sink (forests and grasslands). ESMs with different BNF representations yield a range of BNF responses to CO 2 enrichment. Some ESMs with phenomenological representations of BNF predict a natural BNF increase in response to a doubling of CO 2 that aligns with a meta-analysis of CO 2 enrichment experiments (31% increase) but fail to account for the substantial carbon cost of BNF. In contrast, ESMs with mechanistic representations of BNF account for its carbon cost as well as its regulation by nitrogen limitation but overestimate the BNF response to a doubling of CO 2 (135% increase). Overall, all current BNF representations in ESMs fall short of fully capturing its response to rising atmospheric CO 2 . Finally, we find a positive correlation between modeled present-day natural BNF and the CO 2 fertilization effect across ESMs, suggesting that overestimated natural BNF translates to an exaggerated CO 2 fertilization effect of approximately 11% in ESMs.

PNAS

A global dataset of terrestrial biological nitrogen fixation

Biological nitrogen fixation (BNF) is the main natural source of new nitrogen inputs in terrestrial ecosystems, supporting terrestrial productivity, carbon uptake, and other Earth system processes. We assembled a comprehensive global dataset of field measurements of BNF in all major N-fixing niches across natural terrestrial biomes derived from the analysis of 376 BNF studies. The dataset comprises 32 variables, including site location, biome type, N-fixing niche, sampling year, quantification method, BNF rate (kg N ha −1 y −1 ), the percentage of nitrogen derived from the atmosphere (%N dfa ), N fixer or N-fixing substrate abundance, BNF rate per unit of N fixer abundance, and species identity. Overall, the dataset combines 1,207 BNF rates for trees, shrubs, herbs, soil, leaf litter, woody litter, dead wood, mosses, lichens, and biocrusts, 152 herb %N dfa values, 1,005 measurements of N fixer or N-fixing substrate abundance, and 762 BNF rates per unit of N fixer abundance for a total of 424 species across 66 countries. This dataset facilitates synthesis, meta-analysis, upscaling, and model benchmarking of BNF fluxes at multiple spatial scales.

Scientific Data

Global terrestrial nitrogen fixation and its modification by agriculture

Biological nitrogen fixation (BNF) is the largest natural source of new nitrogen (N) that supports terrestrial productivity 1,2 , yet estimates of global terrestrial BNF remain highly uncertain 3,4 . Here we show that this uncertainty is partly because of sampling bias, as field BNF measurements in natural terrestrial ecosystems occur where N fixers are 17 times more prevalent than their mean abundances worldwide. To correct this bias, we develop new estimates of global terrestrial BNF by upscaling field BNF measurements using spatially explicit abundances of all major biogeochemical N-fixing niches. We find that natural biomes sustain lower BNF, 65 (52–77) Tg N yr −1 , than previous empirical bottom-up estimates 3,4 , with most BNF occurring in tropical forests and drylands. We also find high agricultural BNF in croplands and cultivated pastures, 56 (54–58) Tg N yr −1 . Agricultural BNF has increased terrestrial BNF by 64% and total terrestrial N inputs from all sources by 60% over pre-industrial levels. Our results indicate that BNF may impose stronger constraints on the carbon sink in natural terrestrial biomes and represent a larger source of agricultural N than is generally considered in analyses of the global N cycle 5,6 , with implications for proposed safe operating limits for N use 7,8 .

Nature

Symbiotic nitrogen fixation does not stimulate soil phosphatase activity under temperate and tropical trees

Symbiotic nitrogen (N)-fixing plants can enrich ecosystems with N, which can alter the cycling and demand for other nutrients. Researchers have hypothesized that fixed N could be used by plants and soil microbes to produce extracellular phosphatase enzymes, which release P from organic matter. Consistent with this speculation, the presence of N-fixing plants is often associated with high phosphatase activity, either in the soil or on root surfaces, although other studies have not found this association, and the connection between phosphatase and rates of N fixation—the mechanistic part of the argument—is tenuous. Here, we measured soil phosphatase activity under N-fixing trees and non-fixing trees transplanted and grown in tropical and temperate sites in the USA: two sites in Hawaii, and one each in New York and Oregon. This provides a rare example of phosphatase activity measured in a multi-site field experiment with rigorously quantified rates of N fixation. We found no difference in soil phosphatase activity under N-fixing vs. non-fixing trees nor across rates of N fixation, though we note that no sites were P limited and only one was N limited. Our results add to the literature showing no connection between N fixation rates and phosphatase activity.

Oecologia

Tree symbioses sustain nitrogen fixation despite excess nitrogen supply

Symbiotic nitrogen fixation (SNF) is a key ecological process whose impact depends on the strategy of SNF regulation—the degree to which rates of SNF change in response to limitation by N versus other resources. SNF that is obligate or exhibits incomplete downregulation can result in excess N fixation, whereas a facultative SNF strategy does not. We hypothesized that tree-based SNF strategies differed by latitude (tropical vs. temperate) and symbiotic type (actinorhizal vs. rhizobial). Specifically, we expected tropical rhizobial symbioses to display strongly facultative SNF as an explanation of their success in low-latitude forests. In this study we used 15 N isotope dilution field experiments in New York, Oregon, and Hawaii to determine SNF strategies in six N-fixing tree symbioses. Nitrogen fertilization with +10 and +15 g N m −2 year −1 for 4–5 years alleviated N limitation in all taxa, paving the way to determine SNF strategies. Contrary to our hypothesis, all six of the symbioses we studied sustained SNF even at high N. Robinia pseudoacacia (temperate rhizobial) fixed 91% of its N (%N dfa ) in controls, compared to 64% and 59% in the +10 and +15 g N m −2 year −1 treatments. For Alnus rubra (temperate actinorhizal), %N dfa was 95%, 70%, and 60%. For the tropical species, %N dfa was 86%, 80%, and 82% for Gliricidia sepium (rhizobial); 79%, 69%, and 67% for Casuarina equisetifolia (actinorhizal); 91%, 42%, and 67% for Acacia koa (rhizobial); and 60%, 51%, and 19% for Morella faya (actinorhizal). Fertilization with phosphorus did not stimulate tree growth or SNF. These results suggest that the latitudinal abundance distribution of N-fixing trees is not caused by a shift in SNF strategy. They also help explain the excess N in many forests where N fixers are common.

Hawai'i, New York, Oregon

Exploring the role of cryptic nitrogen fixers in terrestrial ecosystems: A frontier in nitrogen cycling research

Biological nitrogen fixation represents the largest natural flux of new nitrogen (N) into terrestrial ecosystems, providing a critical N source to support net primary productivity of both natural and agricultural systems. When they are common, symbiotic associations between plants and bacteria can add more than 100 kg N ha −1 y −1 to ecosystems. Yet, these associations are uncommon in many terrestrial ecosystems. In most cases, N inputs derive from more cryptic sources, including mutualistic and/or free-living microorganisms in soil, plant litter, decomposing roots and wood, lichens, insects, and mosses, among others. Unfortunately, large gaps remain in the understanding of cryptic N fixation. We conducted a literature review to explore rates, patterns, and controls of cryptic N fixation in both unmanaged and agricultural ecosystems. Our analysis indicates that, as is common with N fixation, rates are highly variable across most cryptic niches, with N inputs in any particular cryptic niche ranging from near zero to more than 20 kg ha −1 y −1 . Such large variation underscores the need for more comprehensive measurements of N fixation by organisms not in symbiotic relationships with vascular plants in terrestrial ecosystems, as well as identifying the factors that govern cryptic N fixation rates. We highlight several challenges, opportunities, and priorities in this important research area, and we propose a conceptual model that posits an interacting hierarchy of biophysical and biogeochemical controls over N fixation that should generate valuable new hypotheses and research.

Ecosystems

N supply mediates the radiative balance of N2O emissions and CO2 sequestration driven by N-fixing vs. non-fixing trees

Forests are a significant CO 2 sink. However, CO 2 sequestration in forests is radiatively offset by emissions of nitrous oxide (N 2 O), a potent greenhouse gas, from forest soils. Reforestation, an important strategy for mitigating climate change, has focused on maximizing CO 2 sequestration in plant biomass without integrating N 2 O emissions from soils. Although nitrogen (N)-fixing trees are often recommended for reforestation because of their rapid growth on N-poor soil, they can stimulate significant N 2 O emissions from soils. Here, we first used a field experiment to show that a N-fixing tree ( Robinia pseudoacacia ) initially mitigated climate change more than a non-fixing tree ( Betula nigra ). We then used our field data to parameterize a theoretical model to investigate these effects over time. Under lower N supply, N-fixers continued to mitigate climate change more than non-fixers by overcoming N limitation of plant growth. However, under higher N supply, N-fixers ultimately mitigated climate change less than non-fixers by enriching soil N and stimulating N 2 O emissions from soils. These results have implications for reforestation, suggesting that N-fixing trees are more effective at mitigating climate change at lower N supply, whereas non-fixing trees are more effective at mitigating climate change at higher N supply.

New York

A roadmap for sampling and scaling biological nitrogen fixation in terrestrial ecosystems

Accurately quantifying rates and patterns of biological nitrogen fixation (BNF) in terrestrial ecosystems is essential to characterize ecological and biogeochemical interactions, identify mechanistic controls, improve BNF representation in conceptual and numerical modelling, and forecast nitrogen limitation constraints on future carbon (C) cycling. While many resources address the technical advantages and limitations of different methods for measuring BNF, less systematic consideration has been given to the broader decisions involved in planning studies, interpreting data, and extrapolating results. Here, we present a conceptual and practical road map to study design, study execution, data analysis and scaling, outlining key considerations at each step. We address issues including defining N‐fixing niches of interest, identifying important sources of temporal and spatial heterogeneity, designing a sampling scheme (including method selection, measurement conditions, replication, and consideration of hotspots and hot moments), and approaches to analysing, scaling and reporting BNF. We also review the comparability of estimates derived using different approaches in the literature, and provide sample R code for simulating symbiotic BNF data frames and upscaling. Improving and standardizing study design at each of these stages will improve the accuracy and interpretability of data, define limits of extrapolation, and facilitate broader use of BNF data for downstream applications. We highlight aspects—such as quantifying scales of heterogeneity, statistical approaches for dealing with non‐normality, and consideration of rates versus ecological significance—that are ripe for further development.

Methods in Ecology and Evolution

A spatially explicit, empirical estimate of tree-based biological nitrogen fixation in forests of the United States

Quantifying human impacts on the nitrogen (N) cycle and investigating natural ecosystem N cycling depend on the magnitude of inputs from natural biological nitrogen fixation (BNF). Here, we present two bottom‐up approaches to quantify tree‐based symbiotic BNF based on forest inventory data across the coterminous United States and SE Alaska. For all major N‐fixing tree genera, we quantify BNF inputs using (1) ecosystem N accretion rates (kg N ha −1 yr −1 ) scaled with spatial data on tree abundance and (2) percent of N derived from fixation (%N dfa ) scaled with tree N demand (from tree growth rates and stoichiometry). We estimate that trees fix 0.30–0.88 Tg N yr −1 across the study area (1.4–3.4 kg N ha −1 yr −1 ). Tree‐based N fixation displays distinct spatial variation that is dominated by two genera, Robinia (64% of tree‐associated BNF) and Alnus (24%). The third most important genus, Prosopis , accounted for 5%. Compared to published estimates of other N fluxes, tree‐associated BNF accounted for 0.59 Tg N yr −1 , similar to asymbiotic (0.37 Tg N yr −1 ) and understory symbiotic BNF (0.48 Tg N yr −1 ), while N deposition contributed 1.68 Tg N yr −1 and rock weathering 0.37 Tg N yr −1 . Overall, our results reveal previously uncharacterized spatial patterns in tree BNF that can inform large‐scale N assessments and serve as a model for improving tree‐based BNF estimates worldwide. This updated, lower BNF estimate indicates a greater ratio of anthropogenic to natural N inputs, suggesting an even greater human impact on the N cycle.

Global Biogeochemical Cycles

Biological nitrogen fixation: rates, patterns and ecological controls in terrestrial ecosystems

New techniques have identified a wide range of organisms with the capacity to carry out biological nitrogen fixation (BNF)—greatly expanding our appreciation of the diversity and ubiquity of N fixers—but our understanding of the rates and controls of BNF at ecosystem and global scales has not advanced at the same pace. Nevertheless, determining rates and controls of BNF is crucial to placing anthropogenic changes to the N cycle in context, and to understanding, predicting and managing many aspects of global environmental change. Here, we estimate terrestrial BNF for a pre-industrial world by combining information on N fluxes with 15 N relative abundance data for terrestrial ecosystems. Our estimate is that pre-industrial N fixation was 58 (range of 40–100) Tg N fixed yr −1 ; adding conservative assumptions for geological N reduces our best estimate to 44 Tg N yr −1 . This approach yields substantially lower estimates than most recent calculations; it suggests that the magnitude of human alternation of the N cycle is substantially larger than has been assumed.

Philosophical Transactions of the Royal Society B: