Air pollution agents interact when affecting biological
sinks for atmospheric CO
Biological sinks for atmospheric CO
Atmospheric N deposition exceeds critical loads in European lowlands, thus
increasing ecosystem productivity and affecting biodiversity (Bobbink et
al., 2010; Phoenix et al., 2012). Commonly, N deposition is much lower (ca. 5 kg ha
C storage in ecosystems begins with plant growth. It is thus reasonable to
expect that increased plant growth under increased N deposition has a
similarly positive effect on ecosystem C storage (Vitousek et al., 1997).
For example Ammann et al. (2009) found higher C sequestration in an
intensively managed, high-N-input (ca. 240 kg N ha
In the past, the scale for N input was often adopted from agronomic
practices. Experimentalists used single-dose, high-N-input treatments, and
even extensive analyses did not differentiate effects of high and low N
input doses (e.g., Liu and Greaver, 2010), summarizing N inputs from 10 to
650 kg N ha
Despite their applicability for the prediction of C sink properties under
changing environmental conditions, low input dose, multilevel N deposition
and multifactor experiments focusing on the carbon budget are rare in
(semi-)natural ecosystems. Those available usually studied one or more
potentially beneficial atmospheric inputs, e.g., multilevel N deposition,
multi-nutrient application (e.g., Fornara and Tilman, 2012; Fornara et al.,
2013; Fang et al., 2014) or N
An earlier analysis in the same project – applying a fully factorial,
multilevel N “interannual effects”, most importantly representing the weather
variability, cause the annual NEP to be positively correlated with
temperature, reflecting the positive effect of warmer growing seasons on
aboveground plant yield in this cold, high-altitude environment. SOC content
was expected to remain unchanged over 7 years. The grassland developed
under a low-intensity management that was unaltered for decades if not
centuries. We therefore considered SOC to be in steady state in a mid- and
long-term perspective. “air pollutant effects” (O
The study intends to improve the understanding of the C balance of extensively used, semi-natural grassland under realistic air pollution scenarios.
The experiment was located at 1990 m a.s.l., on a grassland plateau in the
Central Alps (46
Plots consisted of 180 intact turf monoliths (L
Accounting for 4 kg N ha
The free-air ozone fumigation system (for details see Volk et al., 2003) had
a control treatment (ambient [O
Annual mean accumulated exposure over a threshold of 40 ppb O
Aboveground plant biomass was cut annually at peak canopy development (end
of July), at 2 cm height. The harvested material was oven-dried and weighed
to yield dry matter (DM) mass. For details please refer to Bassin et al. (2007).
Belowground root biomass was assessed from soil cores covering a
subset of the monoliths (Volk et al., 2014). DM masses were expressed as
grams of carbon per square meter (g C m
Net ecosystem CO
We parameterized 7-year cumulative NEP CO
SOC data presented here derive from all 180 monoliths, covering all five N-
and three O
We measured soil organic C and N contents by elemental analysis (oxidation
of C to CO
Effects of treatments were tested in a split plot analysis using a linear
mixed-effect model (Pinheiro and Bates, 1996) with O
Split plot analysis of cumulative 7-year plant C yield. Effects
of block, ozone (O
Aboveground plant yield (grey bars) and net ecosystem
productivity (NEP; white bars) for the control treatment, and annual mean
soil temperature at 5 cm depth (
In the control treatment, the mean plant C contained in total above- and
belowground biomass was 591
Yield
In the control treatment the ecosystem CO
In NEP neither O
From 2003 to 2010 bulk soil C concentration in the 0–20 cm soil layer
(control treatments) increased from 61
The N-deposition-related C gain occurred mostly in the top 10 cm of the soil
column (Fig. 5). This soil layer shows a marginally significant N
Split plot analysis of cumulative 7-year net ecosystem
productivity (NEP). Effects of block, ozone (O
Seven-year cumulative aboveground plant C yield (O
Because O
Despite a decreasing N effect, Yield
Split plot analysis of change of soil organic carbon
concentration (0–10 cm layer) between 2003 and 2010. Effects of block, ozone
(O
Despite a substantial gain over 7 years, NEP
Seven-year cumulative NEP carbon gain (O
GPP parameterization is based on the comparatively small 2010 canopy (cf.
yield values Fig. 1), and NEP
Although this scaling exercise substantially increased NEP, interannual
comparison shows that canopy size and its influence on GPP play only a small
role for NEP, compared to the temperature effect on
Bulk soil (control treatment) organic carbon concentration in 2003 (grey bars) and 2010 (black bars) in the 0–10 and 10–20 cm soil layer.
Under air pollution treatment we found a unimodal/hump-shaped response
pattern of NEP
The
Skinner (2013) reports the same pattern from eddy covariance measurements in
a grassland fertilization experiment: in an initial 5-year period NEE
yielded C gains under low-N-deposition treatment (
SOC concentration values observed here are well within the established limits for this vegetation type. In the 0–20 cm layer of 15 grassland soils above 1000 m a.s.l., described by the Swiss National Soil Observatory (Desaules and Dahinden, 2000), SOC ranges from 3.5 to 8.7 % (mean: 5.4; SD: 1.40). In a literature overview Leifeld et al. (2005) calculated a mean of 6.07 % (SD: 3.31) for > 1000 m a.s.l. permanent grassland in Switzerland.
Absolute soil organic C stock gains during 7 years
(2003–2010) in the 0–10 cm (grey bars) and the 10–20 cm layer (black bars).
O
To convert the 2003 SOC concentrations into SOC stocks, we used the bulk soil density values established in 2010. Indeed soil bulk density often decreases in parallel with the input of fresh organic matter. This would imply a higher than assumed bulk density in 2003 and a smaller difference between SOC stocks in 2003 and 2010.
Suitable literature values with which to estimate the potential underestimation of bulk
soil density at the start of our experiment were not found, as the bulk of
the literature refers to restoration measures for overgrazed areas (e.g.,
Li et al., 2007), forest regrowth after abandonment (e.g., Guidi et
al., 2014) or afforestation (e.g., Hiltbrunner et al., 2013).
Therefore, in a thought experiment we followed the equal-soil-mass concept
(Ellert and Bettany, 1995) and assumed a 10 % density reduction to
coincide with the C concentration increase. In this scenario the 2010 0–20 cm depth
sampling campaign would cover only 90 % of the soil mass present
in the 2003 sample. The resulting error comes from the fact that the 0–20 cm
sampling of the reduced density soil of 2010 only goes to a layer that was
at ca. 18 cm in 2003. Consequently, to compare C content changes in the 2003
soil mass equivalent after 7 years, the 2010 sampling volume would have
to include an extra 10 %, equivalent to 2 cm depth. At our site the C concentration at
20 cm depth is
We assumed the management change did not result in decreased bulk soil
density from reduced trampling, because the Leifeld and Fuhrer (2009) study
in adjacent plots showed no differences, even 60 years after the
meadow/pasture management change. Both grasslands had a
The small decrease in SOC concentration under continued seasonal grazing found at the 2012 resampling of the site where the monoliths came from showed that the effect seen in the trial must have been a treatment effect or a side effect of the experimental management. The monoliths were slightly cooler compared to the original site, and our study found that soil temperature is by far the largest single factor determining the C balance of the mountain grassland. But judging from the sensitivity analysis mentioned above, we are confident that the insignificant temperature difference is responsible for a small effect on soil C stock only, if any.
We suggest that the newly introduced cutting at only 2.5 cm above the ground
represents a more intensive use, compared to selective grazing by cattle,
and that this has created a new SOC source. Because plants maintain a
functional root / shoot equilibrium (Poorter et al., 2012), the aboveground
harvest will cause a proportional root dieback. In the control treatment the
mean annual above- plus belowground live plant C content was > 500 g C m
Under N deposition air pollution treatment SOC mirrored the response pattern
seen in the 7-year NEP parameterization. The strong increase at low
but only small increase at high N deposition rates demands an asymmetric
promotion of C accumulation at different N deposition rates. Both soil
layers (Fig. 5) show this characteristic pattern, which makes it likely that
the same processes are active, only with a lag phase and at a slower rate in
the lower layer. This is because the top soil layer has a higher proportion
of recently assimilated, labile C, consisting of plant litter, roots,
microbial and fungal biomass, as indicated by the > 2
Some studies have suggested soil C content to increase by reducing organic matter decomposition following high N deposition, either as a result of abiotic interactions with microbial products or from effects on the decomposer community (Hobbie, 2008). High-lignin litter reduced decomposition in Dijkstra et al. (2004), while Waldrop et al. (2004) differentiate accelerated decomposition of easily decomposable litter and reduced decomposition of recalcitrant (high-lignin) litter.
But the Park Grass Experiment at Rothamsted, UK (Fornara et al., 2011), shows
no change of SOC content in N-fertilized plots (96 kg N ha
Increasing N doses were also found to decrease soil C content via higher
microbial activity. Generally speaking, microbial activity or population
size may suffer nutrient constraints similar to those of plant productivity (cf.
“law of the minimum”; von Liebig, 1840). N limitation of soil microbial
growth has been suggested based on theoretical considerations (Schimel and
Weintraub, 2003), and Stone et al. (2012) found increased activity of
extracellular hydrolytic enzymes from soil microbiota after long-term
25–35 kg ha
The quality of available C as a source of energy also plays an important role. Fontaine et al. (2003) describe a mechanism that may often stand behind substantial soil C losses in the face of increased plant growth: newly available carbohydrates in the soil create a competitive stimulation of microbial populations that results in strongly increased decomposition rates (priming effect).
But besides decomposition changes of uncertain direction, plant C allocation
plays an important role. In an earlier analysis Volk et al. (2014) had found
N deposition to change the shoot / root ratio (
Lacking low-dose, multilevel N deposition treatments, cases of tipping response functions could usually not be found as a consequence of the experimental design. But in the 19-year, multi-nutrient experiment described by Fornara et al. (2013), the effect of multiple nutrients may constitute an analogy to the effect of increasing N deposition levels. Smaller C sequestration was found in NP, PK and NPKMg treatments compared to the N-only application, while aboveground plant mass grew consistently with nutrient addition (control < N < NP < NPKMg). This is indirect evidence that a more effective plant fertilization does not necessarily result in higher SOC sequestration but instead creates a situation where decomposition or allocation changes are more favored than assimilation, at higher or combined nutrient addition treatments, with negative effects on soil C content.
Annual NEP was negatively correlated with soil temperature, not positively correlated with air temperature like plant yield. Contrary to expectations, soil C concentration in the subalpine grassland substantially increased over time. Thus, as an effect of management change from grazing to cutting, the soil was a strong C sink in the 2003–2010 period. Despite consistently positive responses of aboveground plant yield to increasing N deposition, SOC increased substantially only at low N deposition; it grew less at high deposition rates. NEE measurements suggest that N deposition caused extra C losses via higher microbial respiration after mitigation of N limitation or as a consequence of priming, resulting from the increased input of fresh organic plant material. Also plant C-allocation changes may have contributed to reduced soil C input from roots at high N deposition doses. These mechanisms are likely responsible for the hump-shaped response of SOC to increasing N deposition. Accordingly, N-deposition-driven yield increases in low-productivity grasslands may not be considered as a valid proxy for parallel ecosystem C-pool increases.
The data presented in this study are available for collaborative use; please contact the corresponding author for access to the data.
This study was supported by the Swiss Federal Office for the Environment in the framework of the International Cooperative Programme (ICP Vegetation) under the UNECE Convention on Long Range Transboundary Air Pollution (CLRTAP) and the EU project ECLAIRE. Local support by Victoria Spinas, Alfons Cotti and Gemeinde Sur is greatly acknowledged. Edited by: E. Veldkamp