The gap between atmospheric nitrogen deposition experiments and reality

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Abstract

Anthropogenic activities have dramatically altered the global nitrogen (N) cycle. Atmospheric N deposition, primarily from combustion of biomass and fossil fuels, has caused acidification of precipitation and freshwater, and triggered intense research into ecosystem responses to this pollutant. Experimental simulations of N deposition have been the main scientific tool to understand ecosystem responses, revealing dramatic impacts on soil microbes, plants, and higher trophic levels. However, comparison of the experimental treatments applied in the vast majority of studies with observational and modelled N deposition reveals a wide gulf between research and reality. While the majority of experimental treatments exceed 100 kg N ha−1 y−1, global median land surface deposition rates are around 1 kg N ha−1 y−1 and only exceed 10 kg N ha−1 y−1 in certain regions, primarily in industrialized areas of Europe and Asia and particularly in forests. Experimental N deposition treatments are in fact similar to mineral fertilizer application rates in agriculture. Some ecological guilds, such as saprotrophic fungi, are highly sensitive to N and respond differently to low and high N availability. In addition, very high levels of N application cause changes in soil chemistry, such as acidification, meaning that unrealistic experimental treatments are unlikely to reveal true ecosystem responses to N. Hence, despite decades of research, past experiments can tell us little about how the biosphere has responded to anthropogenic N deposition. A new approach is required to improve our understanding of this important phenomenon. First, characterization of N response functions using observed N deposition gradients. Second, application of experimental N addition gradients at realistic levels over long periods to detect cumulative effects. Third, application of non-linear meta-regressions to detect non-linear responses in meta-analyses of experimental studies.

Introduction

Anthropogenic activities have dramatically altered the global biogeochemical cycling of nitrogen (N). The Earth's atmosphere is composed mainly of biologically-inert N2 gas, which must be oxidized or reduced to become reactive N and available to the biosphere. At the start of the 21st Century, biological N fixation by symbiotic and free-living bacteria delivers 58 ± 29 Tg N y−1 to terrestrial ecosystems, 140 ± 70 Tg N yr−1 to marine ecosystems, and 60 ± 18 Tg N yr−1 to agricultural systems, all as reduced N, NHx (Fowler et al., 2013). Industrial production of ammonia via the Haber Bosch process generates 120 ± 12 Tg N yr−1, compared with a mean estimate of 258 Tg N yr−1 for combined microbial fixation. Oxidized N, NOy, is generated by lightning (5 ± 2.5 Tg N yr−1) and combustion of fossil fuels (30 ± 3 Tg N y−1). Hence, total annual fixation of N is around 413 Tg N yr−1 but with very large uncertainties, of which around half is due to human activities (Fowler et al., 2013). Fixed N passes through a complex series of chemical and biochemical transformations before returning to the atmosphere as molecular N. Reactive N (Nr) is either sequestered by plants and microbes for protein synthesis, or metabolized by nitrification or denitrification to various gaseous forms. Hence, either through fixation of N by lightning or fossil fuel combustion, or microbial conversion of N in organic matter to NHx or NOy, the atmosphere contains a significant concentration of Nr. Dry or wet deposition of Nr carries around 70 Tg N yr−1 to the land surface and 30 Tg N yr−1 to the oceans, though with considerable uncertainty (Fowler et al., 2013). Wet deposition refers to the gaseous and particulate Nr compounds in the atmosphere scoured to the Earth's surface by precipitation, while dry deposition refers to the process by which gaseous and particulate Nr components in the atmosphere are deposited onto surfaces in the absence of precipitation, and direct diffusion into plant stomata (Hanson and Lindberg, 1991; Zhang et al., 2021).

Reactive N is vital to life and many Nr compounds have chemical properties (e.g. forming acidic solutions) that can affect biological processes. The potential for diverse impacts of N deposition on ecosystems have been recognized for many decades (Almer et al., 1974; Likens et al., 1972; Söderlund, 1977). Describing and quantifying the responses of ecosystems to N deposition, or ‘nitrogen pollution’, has been among most intensively studied areas of global change research. This corpus has revealed pervasive effects of N deposition on soil microbes (Cheng et al., 2019; Zhang et al., 2018), plants (Du and de Vries, 2018; Schulte-Uebbing and de Vries, 2018), and higher trophic levels in terrestrial ecosystems (Stevens et al., 2018). In contrast, biogeochemical cycle models which include negative feedbacks of N fixation suggest that marine ecosystems show limited responses of productivity to N deposition (Somes et al., 2016).

In terrestrial ecosystems, the concept of critical loads has been used to monitor the potential impacts of N deposition. The critical load is “The highest load that will not cause chemical changes leading to long-term harmful effects on most sensitive ecological systems” (Nilsson, 1988). Critical loads are related to N saturation levels, whereby N-limited ecosystem processes such as plant growth absorb additional N deposition. Experimental evidence suggests that N saturation for aboveground net primary production is 50–60 kg N ha−1 y−1 (Tian et al., 2016). Critical loads have proven useful policy tools, allowing agencies to monitor the occurrence of potentially harmful levels of N deposition while taking the varying sensitivities of different ecosystems into account (Pardo et al., 2011). Hence, policies to manage pollution from N deposition require understanding of the rate of N deposition, the critical load of the ecosystem, and the effects of varying N availability on different organisms and ecosystem functions. Controlled experiments that manipulate N levels and evaluate ecosystem responses are key to understanding the effects of N deposition and making informed policy decisions. However, to be of value, these experiments must employ experimental treatments that mimic realistic current or potential future deposition rates. This discussion suggests that our understanding of the effects of N deposition on natural ecosystems has been skewed by unrealistic experimental treatments that often greatly exceed deposition levels found in even the most heavily polluted settings.

Section snippets

Global N deposition rates

Ground-based and remote sensing measurements, coupled with biogeochemical and atmospheric transport models, provide estimates of global N deposition rates. In the following discussion, all deposition rates will be reported as kg N ha−1 y−1. While not strictly in SI units, this measure is most commonly used in the literature. The Inter-Sectoral Impact Model Intercomparison Project (ISIMIP) provides researchers with a consistent portfolio of datasets for assessing global change (Warszawski et

N deposition on forests

Experimental research on natural ecosystem responses to N deposition has commonly focussed on forests (Cheng et al., 2019; Knorr et al., 2005; Schmitz et al., 2019; Zhang et al., 2018). Forest deposition rates tend to be greater than open field, due to the high surface area and greater aerodynamic roughness of tree canopies (Ahrends et al., 2020). Schwede et al. (2018) compared two global N deposition estimates with high resolution land use maps to investigate variation in deposition rates

Experimental N deposition

Taken together, observational data and models suggest that global land surface N deposition rates rarely exceed 10 kg N ha−1 y−1. Most of the area with greater deposition rates is in highly industrialized regions of Europe and Asia, particularly forests, where mean deposition rates reach 15–30 kg N ha−1 y−1. Deposition rates of up to 50 kg N ha−1 y−1 occur very rarely, in cities (Decina et al., 2020) and other highly polluted locations. These values can be compared to experimental deposition

Comparison with other global change experimental systems

Perspective on the relative rates of experimental vs. actual N deposition can be gained by comparison with other experimental systems in global change research. In the field of climate change impacts, soil warming and free-air carbon dioxide enrichment (FACE) experiments are among the most common. Globally-averaged combined land and ocean surface temperatures increased by 0.85 °C over the period 1880 to 2012, driven largely by atmospheric CO2 concentration rise from around 280 to 400 ppm (IPCC,

Learning from N deposition gradients

High experimental N deposition treatments may be chosen in the hope of eliciting an ecosystem response during the short timeframes usually available for funded academic research. However, comparison of cumulative dose-response curves demonstrates that ecosystem responses can be fundamentally different under low and high N deposition rates (Schrijver et al., 2011). For example, tree growth rates were much lower under high compared with low N experimental addition rates, for the same total

Conclusions and recommendations

N is a major limiting nutrient and an important determinant of ecosystem productivity and function. Anthropogenic activities have dramatically altered the global carbon cycle, through application of mineral fertilizers in agriculture, and through atmospheric N deposition following biomass and fossil fuel combustion. Understanding the impacts of anthropogenic N has been a major goal of global change research, through observational and experimental studies. However, there remains a wide gulf

Data and methods

ISIMIP2b N deposition data used in Fig. 1, Fig. 2 and S1 were obtained from https://esg.pik-potsdam.de/projects/isimip/

Further information on ISIMIP2b data are available from https://www.isimip.org/gettingstarted/input-data-bias-correction/details/24/

Data on N deposition rates reported in meta-analyses and reviews (Fig. 3, Fig. 4, Fig. 5) were obtained from supplementary information published with these sources. No processing was conducted on these data other than conversion of units where

Declaration of competing interest

The author declares no conflict of interest.

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