The effect of land use change from grassland to bioenergy crops Miscanthus and reed canary grass on nitrous oxide emissions

Biomass and Bioenergy 120 (2019) 396–403

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Research paper

The effect of land use change from grassland to bioenergy crops Miscanthus and reed canary grass on nitrous oxide emissions

T

D.J. Krola,∗, M.B. Jonesb, M. Williamsb, Ó. Ní Choncubhaira, G.J. Lanigana a b

Teagasc, Environment, Soils and Land Use Department, Johnstown Castle, Wexford, Ireland Botany Department, Trinity College Dublin, University of Dublin, Dublin 2, Ireland

A R T I C LE I N FO

A B S T R A C T

Keywords: Nitrous oxide Miscanthus x giganteus Phalaris arundinacea Energy crops Greenhouse gas Denitrification

Bioenergy crop production can enhance greenhouse gas (GHG) mitigation, whilst producing feedstocks for energy generation. However, the GHG balance of these ecosystems is intimately linked to crop selection, previous and current land management and the effects of land conversion. This study aims to quantify nitrous oxide (N2O) emissions from the early stage of land-use change (LUC) from perennial grassland to two perennial rhizomatous grasses in a temperate climate: Miscanthus and reed canary grass (RCG) in the south of Ireland. Emissions of N2O were measured during the first two years of RCG and Miscanthus establishment. Miscanthus stands emitted 7.7 ± 1.6 and 2.3 ± 0.2 kg N2O-N ha−1 yr−1 in the first and the second year, respectively, while RCG produced 1.1 ± 0.2 kg N2O-N ha−1 yr−1 in the first year following LUC. Temporal fluxes of N2O were generally low, however peak emissions observed in the first year contributed approximately 83% of annual N2O in the Miscanthus treatment. This peak occurred in wet (50 mm rainfall in the week preceding the peak) and warm (> 18.5 °C in the top 5 cm of soil) weather conditions and was significantly affected (R2 = 0.77) by the soil moisture deficit. However large, annual N2O losses from Miscanthus and RCG found in this study are well within the range of those from grassland soils in temperate climate, drawing conclusions that any short-term increases in N2O production will soon be offset by the reduced future fertilisation, carbon sequestration and produced bioenergy feedstock.

1. Introduction The European Union (EU) 2020 Climate and Energy Package has committed to a 20% GHG reduction compared to 1990 baseline as well as a target of 20% renewables share in the energy market and 20% increase in energy efficiency by 2020 [1]. Future targets to 2030 under the Climate and Energy Framework will increase these targets to a 40% reduction in emissions with a 27% renewable share of the energy mix [2]. Outside the EU, other countries such as United States and Brazil have also introduced specific policies to facilitate the shift towards bioenergy crops production [3]. Limitations identified in first-generation liquid biofuels [4] have led to a gain in popularity of biomass crops such as short rotation coppice (SRC) and perennial rhizomatous grasses (PRGs), such as Miscanthus × giganteus and reed canary grass (Phalaris arundinacea) (RCG) as a non-food source, dedicated bioenergy lignocellulosic crops [5–7]. Perennial bioenergy crops, specifically SRC, have been included in the EU's greening measures of the Common Agricultural Policy (CAP) [8]. This development is significant for any EU countries where the contribution of grassland in the total agricultural

∗

area is substantially above the 5% threshold, as any restriction in ploughing of permanent grassland will be unlikely. Recently, the Paris Agreement highlighted the use of techniques such as bioenergy coupled with carbon capture and storage (BECCS), and afforestation to facilitate large-scale carbon dioxide (CO2) removal from the atmosphere to limit climate change, putting bioenergy crops at the forefront of change [9–11]. However, the carbon (C) neutrality of bioenergy crops has been questioned by a number of scientific studies [7,12]. Nitrous oxide (N2O) emission from first generation bioenergy crops can negate the benefits achieved by the fossil fuel savings [12,13], although second generation perennial crops can have more favourable GHG balance [14,15]. Similarly, the assessment of GHG balance of bioenergy crops through life cycle analysis (LCA) models can underestimate N2O emissions from nitrogen (N) fertiliser use [16] and soil GHG emissions during cultivation [17]. Indeed [18], estimated that GHG emissions from a variety of bioenergy crops in New York State were primarily due to N cycling and N2O losses. Therefore [19] called for future research to better quantify N2O from various feedstocks grown in different regions in

Corresponding author. E-mail address: [email protected] (D.J. Krol).

https://doi.org/10.1016/j.biombioe.2018.11.033 Received 18 February 2018; Received in revised form 19 November 2018; Accepted 22 November 2018 Available online 11 December 2018 0961-9534/ © 2018 Elsevier Ltd. All rights reserved.

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order to optimise management and minimise emissions. To date, little is known about the consequences of land-use change (LUC) to bioenergy crops on N2O emissions [20], especially in temperate climates. Since Ireland is projected to miss its overall national target of 16% of renewables in the energy mix by 2020 by between one and two percent [21], and with approximately 64% of total land area used for agriculture, 91% of which is grassland [22], there is a potential for a large scale deployment of bioenergy crops at the expense of managed grassland. This land-use change includes ploughing of permanent grassland and in the case of the first generation bioenergy crops also fertilisation, both resulting in elevated soil mineral N levels that are vulnerable to gaseous losses or losses to water bodies [23,24]. However, bioenergy crops such as PRGs Miscanthus and RCG, preferred in temperate climates [25], are characterised by high potential biomass production with a low N requirement owing to intensive N uptake and fertiliser N remobilisation [26,27]. Therefore the principal losses will be associated with perennial crop establishment. The ploughing of grassland results in the breakup of soil aggregates, thereby exposing previously protected soil organic matter (SOM) to decomposition [28]. However, the impact of tillage will also depend on soil type, previous land-use and climatic conditions [29]. Previous studies on ploughing of poorly-drained soils have demonstrated a reduction in N2O due to increased soil porosity [30] while other studies have shown large increases in emissions [31]. In addition, biomass inputs associated with the previous land-use provide an extra pool of SOM for decomposition. Decomposition of SOM releases significant quantities of inorganic N into the soil, which can be nitrified and denitrified and subsequently lost through N2O. Biomass crops in Ireland are projected to be cultivated mainly on poorly-drained, relatively less productive soils such as gleysols and podzols which currently support less profitable farming systems e.g. beef production. Change within such farming systems will also not jeopardise crop production for food. These soils have previously been demonstrated to have a high denitrification potential, due to high clay content (resulting in high water-filled pore space) which in turn has been shown to result in high partial and total denitrification rates and high N2O emission factors [32,33]. As a result, the impact of LUC from grassland to perennial bioenergy crops in temperate climates on N2O emissions is still unclear. In order to address it, we aim to quantify N2O emissions from the early stage of LUC from perennial grassland to Miscanthus and RCG in a field-scale experiment. We hypothesise that in the field setting, soil N2O emissions can be enhanced in the short term following planting and during the early establishment phase of the crops due to enhanced N mineralisation following ploughing, reduced plant cover and subsequent uptake, however in the medium term, N2O emission should taper off due to reduced N inputs in comparison with managed grassland.

Table 1 Soil characteristics of both sites a) measured at soil depth 0–10 cm in both 3ha grassland sites at the commencement of experimental work in 2009 and b) measured again at soil depth 0–15 cm in 2011. Values in 2011 represent average of two 2ha Miscanthus plots and two 1ha RCG plots. Parameters reported are bulk density (BD), pH, total carbon (TC), total organic carbon (TOC) total nitrogen (TN) and soil texture. Site

BD g cm

a) Grassland 1 Grassland 2 b) Miscanthus RCG

pH

TC

TOC

TN

-3

Sand

Silt

Clay

%

1.11 1.13

6.2 6.3

2.9 2.7

2.9 2.7

0.3 0.3

51 52

32 30

18 19

0.98 0.97

6.4 6.7

3.2 2.8

2.4 2.2

0.3 0.3

50 48

32 33

18 19

fine loams classified as Brown Earth, with pH 6.25 ± 0.45 (standard error, SE, n = 3), soil organic carbon C 2.8% ± 0.38 and total N 0.29% ± 0.03 (Table 1). More detailed information on the management history of the sites used in this study can be found in Ref. [34]. Rainfall, air and soil temperature during the experiment were recorded at the meteorological station 1 km from the experimental site. On the 1st April 2009, both sites were sprayed with glyphosate to eradicate the extant vegetation. At the time of spraying, grassland was at a height of approximately 8.5 cm which equates to 2.1 t DM/ha [35]. Assuming an average grass N content of 4%, this amount of vegetation contained 85 kg N/ha. Both 3 ha sites were split into two smaller plots of 2 ha and 1ha in area in 2009 creating four plots in total. All four plots were conventionally tilled between 27th and 29th April 2009 using mouldboard plough to a depth of 20 cm with incorporation of vegetation residue, and power-harrowed on the 1st and 5th of June 2009. Energy crops were established and managed following standard practice [36,37]. Miscanthus rhizomes were planted at a rate of 16,000 rhizomes per hectare in order to get an establishment of 10,000 rhizomes per hectare [36] on 9th and 10th June 2009 on both 2 ha plots and the soil was consolidated with a heavy roller a week later. Miscanthus plots received additional herbicides in the early establishment phase to reduce competition from grass and broad-leaf weeds. The 1 ha plots were left fallow in the first year and sown with RCG at the rate of 30 kg ha−1 on 16th April 2010 following power-harrowing. Miscanthus was harvested in March 2010 and 2011 but the limited biomass material that was cut was left on the ground, whereas RCG was harvested in October 2010. The Miscanthus trial lasted two years while the RCG trial was limited to one year (first year left fallow). This time difference reflects differences in plant establishment and time required to produce the first harvestable yield. No fertilisers were applied during this study.

2. Materials and methods 2.2. N2O emission sampling and analysis 2.1. Study site and experimental design Nitrous oxide fluxes were measured using the static chamber method [38] and in adherence to the latest N2O chamber methodology guidelines [39]. N2O was measured on a weekly to bi-monthly basis for two years (April 2009–April 2011) with 7–8 chambers in the fallowRCG plots and 10–11 in the Miscanthus plots. Measurements followed a prescribed sampling schedule with additional measurements taken at times when higher fluxes were expected i.e. large rainfall forecasted, field operations. Chambers consisted of square stainless steel collars of 40 cm by 40 cm and matching lids (10 cm high) which formed a total headspace volume of approximately 16 L. The collars were manually inserted into the soil to a depth of a minimum of 8 cm, levelled and left to adapt for at least 48 h prior to first gas measurement. Collars were left in the soil in the same positions for the duration of the experiment and were only removed to facilitate machinery access and were immediately re-installed in the same positions. Gas sampling took place at least 24 h following installation or re-installation of collars to allow

The experiment was carried out at Teagasc, Environment, Soils and Land Use Research Centre in Johnstown Castle, Co. Wexford, Ireland (6° 30′ W/52° 17″ N) between February 2009 and April 2011. The location has a maritime temperate climate with a mean annual precipitation of 1038 mm and mean temperature of 10.4 °C (30-year long term average, 1981–2010; Met Eireann, 2015). Two 3 ha sites approximately 100 m apart from each other chosen for the experiment were maintained as long-term grasslands (37 years) and had been managed organically for beef production since 2006. One of the 3 ha sites had been conventionally tilled and reseeded with perennial ryegrass in 2000 and surface seeded with white clover in 2005, while the other site had been conventionally tilled and reseeded with perennial ryegrass and red clover in 2005. The sites were grazed every 3–4 weeks until October 2008. The sites received organic fertiliser between 2005 and 2008 in the form of farmyard manure and cattle slurry. Soils at both sites were 397

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positions on a following sampling date were sampled from the dataset. Then, data in between the two sampling dates was extrapolated using the trapezoidal method, whereas for data from the two sampling dates, the slope ± SE was used. Cumulative N2O fluxes varied on average by ± 2%, and by a maximum of ± 4%.

equilibration of soil gas exchange. Chambers were distributed evenly approximately every 10 m along transects in the plots. The reason for choosing transects was to fall within a carbon footprint of the nearby eddy covariance tower [34]. In Miscanthus, one half of the chambers were placed within, and another half between rows. Chambers placed within rows did not include plants, as this would require special chamber design to accommodate the growing crop, however they were placed in close proximity to Miscanthus plants. Gas sampling was performed between 10.00 and 14.00 h, as this time period is reported to be most representative of the average daily N2O flux [40,41]. Sampling was performed plot by plot. At each sampling occasion a 10 mL sample was drawn with a plastic 20 mL syringe with a hypodermic needle (both Becton Dickinson, UK) immediately after chamber closure, then 15 and 30 min after chamber closure, through a rubber septum (Becton Dickinson, UK). Sample was injected into pre-evacuated (to −1000 mbar) 7 mL screw-cap septum glass vials (Labco, UK). The syringe was flushed once with ambient air before collecting sample for the chamber. Ten ambient air samples were collected each time in order to determine background N2O concentration and to calculate the precision limit of the site, which equated to a minimum detectable flux of 0.45 g N2O-N ha−1 d−1 [39]. Extensive linearity tests for this type of chamber were described by Refs. [33,42]. For example, Harty et al. performed 365 and 383 runs on the sites located on the same experimental farm in 2013 and 2014, respectively, and reported that 93% and 95% of fluxes were linear in both years, respectively. Samples were analysed with gas chromatography (GC) (Varian CP 3800 GC, Varian, USA) fitted with a 63 Ni electron capture detector (ECD) with high purity helium as a carrier gas. Samples were returned to ambient pressure immediately before analysis. The GC was calibrated daily and a reference gas standard of known concentration was analysed every eight samples. Areas under N2O peaks were integrated using Star Chromatography Workstation (Varian, USA). Hourly N2O emissions were calculated based on the linear rate of change in N2O concentration within the chamber during the measurement period taking into account air temperature, atmospheric pressure, and the ratio of surface area to chamber volume [39]. Hourly N2O flux was assumed to be representative of the average hourly flux of the day and was subsequently used to calculate daily emissions (in g N2O-N ha−1 d−1). Cumulative emissions were calculated by integrating the calculated daily fluxes and linearly interpolating between measurement points [39]. There is uncertainty associated with each step of N2O measurements, from field sampling to calculating cumulative fluxes. Ref. [43] proposed a framework of 11 uncertainty sources and magnitudes in N2O measurements. Out of 11 terms, five have relatively small to negligible effects (temperature, volume, pressure, water dilution and standards accuracy) [43]; therefore only the remaining six are addressed here. These are: model choice, model lack-of-fit, outlier filtering, time resolution, standards range and GC repeatability. Regarding model choice and lack-of-fit, a linear model was used due to the N2O measurement methodology collecting three time points per chamber. According to extensive linearity tests [33], a linear model was appropriate on average 94% of the time. Outlier filtering was not used in this dataset and therefore had no bearing on uncertainty. Time resolution, defined as accurate recording of sampling time, could be responsible for a maximum of 3% uncertainty (given by a 30 s deviation for a 15 min sampling interval) since time was measured and recorded using an electronic stopwatch. Standards available in the laboratory range from 200 ppb to 20 ppm N2O. The range of standards used for analysis reflects sample N2O concentration and the high concentration standards are only used when required. Repeatability of two GC instruments used in a laboratory on-site has coefficients of variation at 1.1% and 2.4% and precision of 1.9% relative standard deviation. Regarding uncertainty in calculating cumulative fluxes, a statistical approach was used where five random measurements on a given sampling date and five measurements corresponding to the same chamber

2.3. Soil sampling and analysis Soil samples were collected at the beginning of the experiment at 0–10 cm depth to characterise experimental sites for texture, pH, C and N contents. Soil texture was analysed in an external laboratory according to its standard procedure (Natural Resource Management Ltd, Bracknell Berkshire, UK). Soil pH was measured in a 1:2 suspension of deionised water with a digital pH meter with glass and calomel electrodes following drying at 40 °C. Soil C and N contents were measured on soils previously dried at 60 °C and ground with a ball mill. The analysis was carried out on a TruSpec CN elemental analyser with combustion at 950 °C. Soil bulk density was determined using the core method [44] twice, once at the beginning and once at the end of the experiment. Soil samples were collected on six occasions throughout the experiment to assess mineral N content. Five replicates per field were collected at 0–10 cm depth. Samples were kept in closed plastic bags in cool conditions and analysed within 24 h of collection. Fresh soil samples were sieved (< 4 mm), extracted with 2 M KCl (40 g of soil in 100 mL KCl) by shaking on a reciprocating shaker for 1 h and filtering using Whatman Qualitative Filter Paper: Grade 2. Mineral N concentration in the extract was determined using an Aquakem 600 discrete analyser. Concentrations of ammonium (NH4-N) and nitrate (NO3N) were analysed according to [45,46]. It was not possible to measure mineral N at a higher temporal resolution due to resource constraints. Volumetric soil moisture content and temperature were measured regularly in 2010 with a calibrated Theta Probe (WET-2 type sensor connected to a HH2 Meter), (both from Delta-T Devices Ltd, Cambridge, UK) at the time of N2O measurements. Measurements were taken at 0–6 cm depth beside the static chambers. Volumetric soil moisture content was converted into water filled pore space (WFPS) following the equation in Ref. [47]. Due to issues with probe breakages causing limited availability, high resolution soil moisture and temperature data from the Eddy covariance towers was used to describe environmental conditions during the experiment (Fig. 1 a, b), while the Theta Probe data was used to compare the two crops taking into account spatial resolution. Modelled soil moisture deficit (SMD), which is a variable describing the amount of rainfall needed to bring the soil to field capacity, was calculated using a modified Penman–Monteith equation [48,49]. 2.4. Statistical analysis Data were analysed using SAS 9.1 statistical package (© 2002–2010, SAS Institute Inc., Cary, NC, USA, 2011). All data were tested for normal distribution, and log transformed as appropriate. A repeated measures two-way ANOVA followed by a Least Significant Difference (LSD) post test was conducted using PROC MIXED procedure [50] to test the effects of treatment and time on N2O, WFPS, and soil temperature. A mixed linear model procedure of SAS (PROC MIXED) followed by a Tukey's multiple comparison post test was used to determine differences between treatments on cumulative N2O data. All data were expressed as mean and associated standard error (SE) values. Mean daily nitrous oxide emissions from Miscanthus during the 24/ 06/2009–05/08/2009 high flux period were modelled with stepwise multiple regression analysis against weather data using the GLMSELECT procedure in SAS 9.3 (© 2002–2010, SAS Institute Inc., Cary, NC, USA, 2011). The explanatory variables were fitted as polynomial effects allowing main effects, interactions and quadratic terms. Stepwise selection was used to assess explanatory variables. The entry criterion was 398

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Fig. 1. Mean temporal traces of (a) soil water-filled pore space, (b) soil temperature and (c) soil NH4-N and NO3-N (0–10 cm) concentrations in Miscanthus (two years from planting) and fallow - RCG (one year of fallow followed by one year of RCG establishment) plots.

set to 0.15 to allow flexible entry with a retention threshold of p = 0.05. Selected models were fitted with the MIXED procedure to allow residual checks to ensure that the assumptions of the analysis were met.

significant crop × time interaction (P < 0.05), meaning that time affected both crops differently. However, both NH4-N and NO3-N fluctuated around background concentrations of between 0 and 4 mg N kg soil−1 throughout the experiment.

3. Results

3.3. Nitrous oxide emissions

3.1. Environmental variables

Fig. 2 presents temporal fluxes of N2O from Miscanthus and fallow RCG treatments measured for two years between April 2009 and April 2011. Mean daily N2O emissions varied between −0.66 ± 0.42 and 224 ± 47.9, and between 0.97 ± 0.35 and 40.8 ± 4.71 g N2O-N ha−1 d−1 for Miscanthus in the first and the second year, respectively. Emissions for the fallow treatment in the first year ranged from −0.13 ± 0.50 and 84.2 ± 19.7, while in the second year, after the RCG was sown, N2O ranged from −0.31 ± 0.72 to 15.8 ± 5.97 g N2O-N ha−1 d−1. Minimum, maximum and median fluxes are summarized in Table 2. Mean daily N2O emissions were low to moderate, with the majority of the losses caused by one major high flux period each year. High flux periods appeared in the first measurement year running from 24/06/ 2009 to 5/08/2009 and contributed between 47% and 83% of the cumulative annual N2O from fallow and Miscanthus in the first year, respectively. Drivers of these peak N2O emissions from both treatments were assessed using a stepwise multiple regression analysis (Table 3 a, b). The analysis of weather parameters included cumulative rainfall, mean daily soil and air temperature and SMD as a proxy for soil moisture. The model showed that 77% of the variation in nitrous oxide emissions in the Miscanthus plots (P < 0.001) could be explained by soil moisture conditions (SMD) (Table 3 a). The relationship with SMD

Mean average air temperatures were 10.6, 9.9 and 10.9 °C for 2009, 2010 and 2011, respectively. January, February and November 2010 were the coldest for at least 25 years, while December was the coldest on record with temperatures dropping to −15 °C. Summer 2010 was warmer than usual, and May and July were also unusually wet, while the 2011 summer months were cooler than normal. Soil moisture was described by WFPS and SMD. Lowest SMD corresponded with the highest WFPS observed in winter months. Soil was at saturation point for 30% of the experimental period (SMD = 0) (Fig. 2). Soil moisture and temperature measured by the Theta Probe at the time of N2O measurements showed there were no significant differences between the two crops (data not shown). 3.2. Mineral N Seasonal patterns of soil mineral N (NH4-N, NO3-N) concentrations in the 0–10 cm soil depth over the experimental period are presented in Fig. 1 c. A repeated measures two-way ANOVA revealed a significant temporal effect (P < 0.05) on soil NH4-N. However there were no differences between the crops. Soil NO3-N levels were affected by a 399

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Fig. 2. Mean temporal trace of N2O fluxes from Miscanthus (two years from planting) and RCG (one year of fallow followed by one year of RCG establishment) treatments and soil moisture deficit during the experimental period. Error bars represent standard error of the mean.

significant difference between treatments (P < 0.001) and between the two measurement years (P < 0.0001). Nitrous oxide emissions from Miscanthus were higher than those from fallow - RCG, and similarly emissions were higher in the first year and reduced in the second year in both treatments.

Table 2 Summary of annual and daily N2O fluxes from Miscanthus (two years from planting) and fallow - RCG (one year of fallow followed by one year of RCG establishment) treatments. SEM indicates standard error of the mean. Mean

Median

Min

Max

SEM

n

N2O (kg N2O-N ha−1 yr−1) Year 1 Miscanthus 7.7 Fallow 4.5 Year 2 Miscanthus 2.3 RCG 1.1

4.8 3.9 2.2 0.9

1.6 1.6 1.0 0.4

26.4 12.6 3.8 2.6

1.6 0.6 0.2 0.2

20 20 20 15

N2O (g N2O-N ha−1 d−1) Year 1 Miscanthus Fallow Year 2 Miscanthus RCG

1.2 2.4 2.9 1.3

−6.2 −7.6 −5.4 −8.9

1334 298.2 95.59 62.07

19.8 6.5 0.6 0.4

615 540 420 315

17.1 11.4 7.6 3.3

4. Discussion Land-use conversion into Miscanthus and RCG resulted in large N2O losses in the first year post-LUC. These findings are consistent with the study of [51] where LUC to willow and poplar plantations was a source of large N2O and NO3-N leaching losses. Miscanthus N2O losses found in this study, at 7.7 and 2.3 kg N2O-N ha−1 yr−1 in the first and second year, respectively, were large in comparison with those from established bioenergy crops, especially with the work of [52] on Miscanthus on a loamy sand soil, but also large in comparison with a grassland control used in a nearby experiment. Between April 2009 and August 2011 [53] reported emissions of 0.3 kg N2O-N ha−1 yr−1 from unfertilised grassland plots located on the same farm on the same soil type. However, emissions were comparable or lower than N2O from grazed and/or fertilised temperate grassland. Temperate grassland soils are known as hotspots of reactive N emissions due to compaction, high fertilisation rates, and high rainfall [54]. Recent studies found N2O emissions in the range of 0.02–6.3 kg N2O-N ha−1yr−1 from extensively managed temperate grasslands [55–58], while emissions from intensive management can be substantially larger with 18.5 kg N2O-N ha−1yr−1

was better described by a squared term rather than a linear fit indicating that this relationship is similar to that of a bell-shaped curve describing N2O response to WFPS. In the case of the fallow plots, the model was able to explain 59% of variation in the N2O peak through soil moisture deficit and air temperature (Table 3 b). Cumulative losses of N2O are shown in Table 2. Nitrous oxide ranged from 1.1 ± 0.2 to 7.7 ± 1.6 kg N2O-N ha−1 yr−1 from RCG in Year 2 and Miscanthus in Year 1 of the experiment, respectively. Twoway ANOVA followed by a Tukey's multiple comparison post-test found

Table 3 Full fixed model of multiple regression analysis for mean daily N2O flux (g N2O-N ha−1 d−1) from a) Miscanthus and b) fallow-RCG treatment during the 24/06/ 2009–05/08/2009 high flux period using weather data. a)

Parameter

Estimate

Std. Error

Adjusted R-Square

t

F

Pr > F

1 1 1ˆ2 1 2 1 Parameters: 1 Mean daily soil moisture deficit 2 1ˆ2 + mean daily air temperature

0.014619 −0.001877 −0.095152

0.016598 0.000443 0.049362

0.70 0.77 0.79

0.88 −4.24 −1.93

94.28 17.60 3.72

< 0.001 0.0001 0.0612

b)

Estimate

Std. Error

Adjusted R-Square

t

F

Pr > F

−0.029596 −0.189110

0.005025 0.051891

0.46 0.59

−5.89 −3.64

37.14 13.28

< 0.0001 0.0008

Parameter

DF

DF

1 1 2 1 Parameters: 1 Mean daily soil moisture deficit 2 1 + mean daily air temperature

400

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Table 4 Comparison of nitrous oxide emissions from establishment phase and mature bioenergy crops, mainly Miscanthus and RCG, and grassland. Land use/crop

Location

Cumulative N2O emission kg (N2O-N ha−1 yr−1)

Research note

Reference

Miscanthus Giganteus Miscanthus Giganteus

Germany Denmark

0.0 0.14

[67] Gauder et al. (2012) [68] Jørgensen et al. (1997)

Miscanthus Sinensis Miscanthus Giganteus Miscanthus Giganteus Miscanthus Giganteus Miscanthus Giganteus Miscanthus Giganteus Miscanthus Giganteus Reed canary grass Reed canary grass Reed canary grass

Japan England Ireland Ireland Ireland United States United States Estonia Canada Finland

0.22 0.30 0.38 0.46 0.61 0.75 and 0.35 1.40 0.10 0.20 5.0 and 11.3

Willow Poplar Poplar Willow

United States United States Belgium United States

Poplar

United States

Grassland

Ireland

9.80 12.60 5.5 and 0.9 1.11–40.02 0.55–7.50 1.07–31.35 0.73–6.77 0.3

Grassland Grassland Grassland

Ireland Ireland Ireland

0.21 0.4–0.9 2.38 and 7.82

Grassland

Ireland

4.21 and 4.66

Grassland

Ireland

6.45 and 18.51

Grassland Grassland

Ireland review

1.7–6.3 1.00

mature crop measurements during growing period, April–August on mature crop naturally established mature crop mature crop mature crop mature crop establishment phase mature crop; emissions from 2009 to 2010, respectively post/establishment phase crop established on abandoned peat extraction area mature crop fertilised with 60 kg N ha−1 yr−1; emissions from 2011 to 2012, respectively establishment phase establishment phase first and second year of establishment, respectively range of sites in the first year of establishment range of sites in the second year of establishment range of sites in the first year of establishment range of sites in the second year of establishment ungrazed unfertilised grassland, experiment carried out on the same farm on the same soil type ungrazed unfertilised grassland ungrazed unfertilised grassland ungrazed unfertilised grassland and grazed fertilised at 226 kg N ha−1 yr−1 grassland, respectively grazed unfertilised grassland; emissions from 2002 to 2003, respectively grazed fertilised at 225 kg N ha−1 yr−1 grassland; emissions from 2002 to 2003, respectively ungrazed unfertilised grassland; emissions from 2008 to 2012 unfertilised grassland

Grassland

review

1.00

unfertilised grassland

Grassland Grassland

review review

0.03–4.80 0.3–18.16

unfertilised grassland fertilised grassland

[69] [70] [52] [71] [52] [72] [73] [74] [75] [76]

Toma et al. (2011) Drewer et al. (2012) Roth et al. (2013) Roth et al. (2015) Roth et al. (2013) Behnke et al. (2012) Smith et al. (2013) Mander et al. (2012) Wile et al. (2014) Epie et al. (2015)

[51] [51] [77] [78]

Nikiéma et al. (2012) Nikiéma et al. (2012) Zona et al. (2013) Palmer et al. (2014)

[78] Palmer et al. (2014) [53] Bourdin et al. (2014) [52] Roth et al. (2013) [33] Harty et al. (2016) [61] Li et al. (2011) [56] Hyde et al. (2006) [56] Hyde et al. (2006) [55] Burchill et al. (2014) [79] Bouwman & Boumans (2002) [80] Stehfest & Bouwman (2006) [81] Jensen et al. (2012) [81] Jensen et al. (2012)

time of renovation, which would equate to an input of 85 kg N ha−1. Subsequent decomposition of residues would release significant quantities of inorganic N into the soil, which is further transformed via nitrification and denitrification. Peak N2O emissions were correlated with an increase in soil moisture due to a rain event that followed an extended dry period. This event and the previous tillage event would result in slaking of macro- and microaggregates which, in turn exposes previously protected soil organic matter (SOM) to decomposition. Indeed, an increase in soil CO2 respiration rates were observed in conjunction with the increases in N2O, implying increased microbial activity [60]. Grassland undergoing conversion in this experiment was previously managed organically for livestock production, therefore it would have been associated with N2O emissions resulting from manure application and animal returns through grazing, most probably in the range of values reported by Ref. [56]. In this context, emissions from Miscanthus and the plot left fallow in the first year post-LUC are similar to those from the previous land-use, while emissions from the second year of Miscanthus and from RCG are more on par with those of unfertilised and ungrazed grassland [61]. Emissions are expected to further decrease over time, through lack of disturbance and reduced fertiliser requirement in the energy crops production [36] compared to intensive grassland [62], while substantial gains in the quantity of produced biomass are also expected [26,27]. In this study Miscanthus only reached a yield of 13 t DM ha−1 in the third year post-establishment [34], after the N2O measurements ceased, however RCG provided 6.4 t DM ha−1 from the first year of cultivation onwards, leading to N2O emission intensity of 0.36 kg N2O-N t−1 DM in the first year, and 7.85 t

reported by Ref. [56]. [34] reported two of the same experimental plots to be a net source and a small sink of C for Miscanthus and RCG, respectively, in the first year following LUC. Miscanthus was still a small net source of C in the second year however it switched to a net sink in the third year. When net emissions of CO2 and N2O are added together on a CO2-eq basis for a more comprehensive estimate of GHG losses following LUC it is clear that N2O is a strong driver of the overall GHG balance in the case of Miscanthus, which is characterised by slower establishment and low above-ground biomass production in the initial establishment stages compared to RCG. In the period between 28/04/2009 and 31/12/2009 (measurement periods adapted from Ref. [34], N2O accounted for 39% of overall emissions, while in 2010 this share increased to 68% reflecting low biomass production and high N2O losses. Contrary to this, RCG was a C sink from the first production season with N2O negating only 3% of the C sink. This estimation only includes the net effect of ecosystem CO2 uptake and release (net ecosystem exchange) and N2O losses, however this balance would change dramatically for RCG when C offtake through harvest is taken into account. Similarly, a full GHG balance would require incorporation of emissions from field operations [59]. During this experiment, rainfall in the first year of Miscanthus establishment was on average 20% higher than the long-term average, and soil remained at saturation point for 30% of time. High soil moisture content together with high clay content of the soil created favourable conditions for high partial and total denitrification and high N2O emissions. Grass sward biomass was 2.1 tonnes of dry matter per hectare at the 401

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DM ha−1 in the second year, with 0.14 kg N2O-N t−1 DM. N2O flux generally showed relatively little temporal variability, however peak emissions observed in the first year contributed up to 83% of annual N2O in the Miscanthus treatment. This peak occurred in wet and warm weather conditions and was significantly affected (R2 = 0.77) by the SMD. Soil moisture deficit is complementary to precipitation and soil moisture which are two of the main drivers of N2O emission [63–66], with N2O increasing with higher rainfall, higher soil moisture and lower SMD. Low SMD represents restricted oxygen concentration in soil leading to anaerobic conditions stimulating denitrification. In the seven days leading up to the highest measured mean daily N2O, the soil received nearly 50 mm of rain and the SMD fluctuated around 0, while the average WFPS measured in the plot on that day was 62%. At the same time, soil temperature in the top 5 cm reached 18.5 °C. Such a large contribution of one N2O peak in the annual emission is not uncommon. Ref. [77] reported one week-long N2O peak contributing 42% of a two-year N2O budget from a short rotation poplar newly established after conversion from agricultural land. It is reasonable to assume that N2O emissions after converting from grassland can be larger compared to those of cropland. Regarding high temperature during the N2O peak period, [82] found a very high sensitivity of denitrification to temperature and low activation energy for the process in Irish sandy loam pasture soil. The study of [70] also found highest N2O emissions when soil temperature exceeded 15 °C. Moreover, this peak of N2O occurred shortly after soil disturbance, which points to the role of mineralisation of soil organic matter in the high emission, and reduced N uptake due to low crop cover [83]. As part of the conversion of grassland to energy crops production, green cover at the experimental site was killed off with herbicide and incorporated at ploughing providing a large source of organic matter for mineralisation. No evident peak was seen in soil mineral N levels due to low temporal resolution of measurements, however it can be hypothesised that a high mineralisation occurred following disturbance of permanent grassland [84]. The Paris Agreement and the EU Climate and Energy Policy put perennial bioenergy crops such as Miscanthus and RCG at the forefront of anticipated changes. Therefore these crops are becoming a more common choice to achieve dual targets of GHG reduction and increased renewables share in energy generation. Large scale deployment of these crops is intricately connected to LUC and soil disturbance. To date, there are only a few N2O datasets from bioenergy crops (Table 4) and these focused on mature crops [68,70], bar for studies from the US [51,73,85]. Therefore this work generates much needed data on N2O emissions from the early-establishment phase of these crops in the temperate climate of northern Europe and highlights the role of soil disturbance in the magnitude of N2O losses. However large, these losses are well within the range of those found in grassland soils in this climate. Therefore it was concluded that these findings confirm the original hypothesis of this study and any short-term increases in N2O production will soon be offset by the reduced future fertilisation, carbon sequestration and produced bioenergy feedstock.

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Funding This work was supported by the National Development Plan, through the Research Stimulus Fund, administered by the Department of Agriculture, Food and the Marine (RSF 10/RD/SC/716).

Acknowledgements The authors would like to thank the laboratory and field staff at Teagasc Johnstown Castle for their assistance on this project.

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