Long-term human interactions with the natural landscape have produced a plethora
of trends and patterns of environmental disturbances across time and space.
Nitrogen deposition, closely tracking energy and land use, is known to be
among the main drivers of pollution, affecting both freshwater and terrestrial
ecosystems. We present a statistical approach for investigating the historical
and geographical distribution of nitrogen deposition and the impacts of
accumulation on recent soil carbon-to-nitrogen ratios in Europe. After the
second Industrial Revolution, large
swaths of land emerged characterized by different atmospheric deposition patterns caused by
industrial activities or intensive agriculture. Nitrogen
deposition affects soil C : N ratios in a still recognizable way
despite the abatement of oxidized and reduced nitrogen emissions during the
last 2 decades. Given a seemingly disparate land-use history, we focused
on
The global cycle of nitrogen is highly sensitive to human activities (Galloway et al., 2004; Costanza et al., 2007; Doney et al., 2007; Fowler et al., 2013). Shifts in nitrogen availability alter the carbon cycle and litter decomposition (Vitousek et al., 1997; Stevens et al., 2004; Reich, 2009), affecting the heterotrophic component of ecosystem respiration (Janssens et al., 2010). In terrestrial ecosystems, atmospheric nitrogen deposition is also a major source of concern because it induces soil acidification by decreasing the exchangeable cation pools (Bowman et al., 2008). Moreover, nutrient enrichment directly influences the biodiversity and ecological stoichiometry of vascular plants through the soil (Stevens et al., 2004; Mulder et al., 2013).
Public and political concerns for current agricultural and environmental policies have focused on the loss of biodiversity and the impacts on ecosystem services related to nitrogen deposition (Reis et al., 2012; Sutton et al., 2014). It is widely accepted that correct relative proportions of physiologically required nutrients will promote the growth of plant species, influence their diversity and finally drive vegetation succession (Sterner and Elser, 2002; Hillebrand et al., 2014). Among such chemical elements, carbon (C) and nitrogen (N) are the most important, which makes the determination of relationships between soil C : N and nitrogen deposition interesting.
To investigate such correlations, we used 19 458 sites in 23 European
countries to quantify the effect of atmospheric deposition of nitrogen
compounds on soil C : N measurements. We separately investigated the effects
of nitrogen oxides (NO
Nitrogen deposition and the recent soil C : N ratios (mass units).
Spatial clusters (shown clockwise) of NO
Given the rapid expansion in Europe of industrial technology and intensive agriculture during the second Industrial Revolution (Mokyr, 1990), we chose 1880 as the starting point of our time series under the hypothesis that accumulated nitrogen deposition since 1880 may contribute the most to the spatial variability of recent soil C : N ratios. The statistical relationship between long-term nitrogen deposition and recent soil C : N ratio was tested by exploring whether spatial clusters of accumulated nitrogen deposition exist and if chemical footprints on soil C : N occur. This large-scale statistical comparison was made possible by using consistent data from one single survey in which all soils were sampled according to the same protocol and analysed in the same laboratory.
Between 1880 and 2010, estimated nitrogen emissions in each country for
every 5 years until 1990 and each year afterwards were used to compute
depositions with the aid of atmospheric dispersion models. Annual-average
deposition time series of total (wet and dry) oxidized and reduced
nitrogen were obtained from simulations with a Eulerian atmospheric
dispersion model (Simpson et al., 2012; for a comparison with measurements
see Simpson et al., 2006), operated and maintained by the European
Monitoring and Evaluation Programme (EMEP) at the Norwegian Meteorological
Institute and routinely used in European air pollution assessments
(
Total oxidized N deposition is the sum of NO
We collected data from a recent European Soil Survey study known as LUCAS (Land
Use/Cover Area frame Survey):
Total soil carbon (g C kg
To explore the similarities of the time series from 1880 to 2010, we used the TwoStep Clustering method implemented in SPSS, which is suitable for very large data sets. The first step of the two-step algorithm is a BIRCH algorithm to define pre-clusters (Zhang et al., 1996, 1997); in the second step, using an agglomerative hierarchical algorithm, these pre-clusters are merged stepwise until all locations hierarchically close to each other fall within the same cluster (SPSS, 2001). The numbers of clusters are determined with a two-phase estimator like the Akaike's information criterion (AIC) and a (ratio of) distance measure in both pre-cluster and cluster steps. AIC is a relative measure of goodness of fit and is used to compare different hierarchical solutions with different numbers of clusters: any “correct” good hierarchical solution will have a reasonably large ratio of AIC changes with the distance ratio measuring the most reliable current number of clusters against alternative solutions.
The TwoStep Clustering method became rapidly accepted when Chiu et al. (2001) demonstrated that such a technique was able to identify objectively the correct number of clusters for more than 98 % of a large number of simulated data sets. This clustering method for very large databases has been used in many different fields, including biochemistry, genetics, molecular biology (e.g. Lazary et al., 2014) and medicine (e.g. Kretzschmar and Mikolajczyk, 2009). Here we identified seven clusters running TwoStep Clustering separately for the three N deposition categories: nitrogen oxides, atmospheric ammonia and reactive nitrogen (see Tables S1–S3).
Our statistical clustering enables the objective detection of sites with
similar historical paths of nitrogen deposition, showing how much sites
respond to nitrogen supply through atmospheric deposition over time. Figure
1 shows the distribution of hotspots and spatial aggregations
in all forms of nitrogen deposition across Europe. The ammonia clusters are distinct (the
high load is more than two-fold the low load) and Deposition Cluster I
visualizes an emerging cocktail of manure and synthetic fertilizers due to
intensive agriculture (Fig. 1, upper left). In contrast, long-term
deposition of NO
There are multiple fates for atmospheric N, and its sources have changed substantially
(Holtgrieve et al., 2011; Steffen et al., 2015). Within a century, the
average of Nr increased more than two-fold everywhere between 1880 and 1980.
In 2010 the Nr deposition was still much higher than in 1880, and only 16
sites (0.082 %) exhibited a lower Nr deposition in 2010 than in 1880,
with the highest increase in southern Europe (up to 8 times the Nr
deposition of 1880). Shortly after World War II, NH
Temporal cluster vector means (averages and standard errors of the
series) of the depositions of NH
Clustering highly increased the discrimination power to establish historical
shifts in recent soil C : N ratios (Table 1). We used these nitrogen
deposition clusters to assess the spatial distribution of recent soil C : N
assuming the existence a long-term footprint in soil C : N ratios due to
atmospheric deposition, although some authors claim that significant
correlations between the nitrogen of mineral soils and the anthropogenic
nitrogen deposition are either weak or far from causal (Nadelhoffer et al.,
1999; Aber et al., 2003). Our soil C : N ratio averages 16.18 (
Soil C : N values clearly differ by nitrogen deposition cluster.
The soil C : N ratios are given as cluster-specific averages (
To investigate the extent to which atmospheric nitrogen deposition affects
terrestrial ecosystems, we compared geospatial patterns of recent soil C : N
ratios with temporal trends in nitrogen deposition, keeping in mind that
time is one-dimensional and directional, whereas space is two-dimensional
and non-directional (White, 2007). Overall, a generalized linear model (here
as GLM with normal distribution, identity link) for soil C : N as a function of
historical depositions showed a temporal increase in Wald's
We analysed the clusters separately with high versus low nitrogen loads as
classification variables, and detected a comparable
Focusing on unmanaged ecosystems, the same type of GLM was performed for the
recent soil C : N as function of accumulated Nr, assuming that all locations
sampled in 2009 and classified as nature were definitely unmanaged 5 years
before sampling and most probably even unmanaged 50 years before sampling.
For the soil C : N ratios of the unmanaged ecosystems under chronic
pollution,
there was a significant increase of explanatory power by reduced time spans
of accumulated Nr deposition (
Cumulative Nr deposition of the last 5 years prior to sampling and soil C : N ratios: negative power functions of soil C : N ratios in nature (measured in 2009) as predicted by cumulative Nr deposition. Upper panel: 9888 unmanaged sites belonging to the cluster with low Nr load but chronic exposure to nitrogen (Deposition Cluster VI); lower panel: 1546 unmanaged sites under excessive Nr load (Deposition Cluster VII). This last cluster acts as a kind of envelope which incorporates sites with low soil C : N ratios. We were not able to extract a significant deposition effect for managed ecosystems although long-term inverse relationships between Nr and soil C : N hold (see Table S4).
Such a conclusion is indirectly supported by the lack of any significant
trend in the other (semi-)natural ecosystems, all located within Deposition
Cluster VII (Fig. 3, lower panel), given that these areas are associated with
intense human activity, high emissions and soil saturation due to elevated
nitrogen loads. Soil C : N of (semi-)natural sites seem to be the most
sensitive to 5-year pulses of atmospheric nitrogen supply; short-term
deposition is clearly the best predictor for recent soil C : N ratios under
chronic nitrogen deposition (
In summary, spatial clustering reveals long-term effects of atmospheric nitrogen deposition on the recent soil C : N ratios in Europe. While an inverse correlation between this anthropogenic input and soil C : N seems to be intuitive, the extent to which this relationship holds has never been investigated before. Our results show that the C : N ratio varies more across the soils of (semi-)natural ecosystems with a history of low (chronic) nitrogen pollution and that it remains surprisingly constant elsewhere. Moreover, despite the investigated deposition of nitrogen since the 1880s, it turns out that soils supposed to be under low pressure are not only the most affected by nitrogen accumulation, but also the most responsive to a short-term supply of atmospheric nitrogen in the recent past.
Statistical signals from responsive chronic nitrogen pollution became detectable only after clustering the nitrogen deposition, and we were able to provide novel evidence that the soil C : N of (semi-)natural ecosystems is highly responsive to Nr. We detected where nitrogen supply through atmospheric Nr deposition affects (semi-)natural ecosystems. As examining the soil black box is now at the “front line” of research (Schmidt et al., 2011; Amundson et al., 2015), mapping the soil and the air compartments together can contribute to a better conservation of our unmanaged environment.
It is challenging to find a mechanistical explanation of why the atmospheric nitrogen supply does not also seem to affect managed ecosystems: for instance, are many exploited soils N-saturated? How much anthropogenic nitrogen becomes mediated through soil processes has to be addressed in the future, given the long history of land (ab)use in Europe that has until now hampered the detection of robust effects directly attributable to nitrogen deposition.
C. Mulder and J.-P. Hettelingh developed the study. L. Montanarella and M. Posch collected soil C : N coverage and atmospheric deposition data. M. R. Pasimeni and G. Zurlini contributed nitrogen deposition clusters. C. Mulder, W. Voigt and G. Zurlini analysed the data. All authors had input on the composition of the manuscript.
This research was partially funded by the Dutch Ministry of Infrastructure and the Environment, the Working Group on Effects within the effect-oriented activities under the UNECE Convention on Long-range Transboundary Air Pollution and the 7th EU Framework Programme, Theme ENV.2011.1.1.2-1, project agreement no. 282910: Effects of Climate Change on Air Pollution Impacts and Response Strategies for European Ecosystems. The EMEP MSC-W at the Norwegian Meteorological Institute is acknowledged for providing deposition calculations over the last 3 decades. Edited by: A. Neftel