Nitrous oxide emissions following dairy shed effluent application beneath Kunzea robusta (Myrtaceae) treesKunzea robusta（桃金娘科）树下施用牛棚废水后的氧化亚氮排放

Ecological

Ecological Engineering 99 (2017) 473–478 Contents lists available at ScienceDirect

Ecological Engineering

jo ur nal home p age: www.elsevier.com/locate/ecoleng

Short communication Nitrous oxide emissions following dairy shed effluent application beneath Kunzea robusta (Myrtaceae) trees

Hannah M. Franklin ^a,c,∗,1, Roshean R. Woods ^b,1, Brett Robinson ^b, Nicholas Dickinson ^a

a Department of Ecology, Lincoln University, PO Box 85084, Lincoln, 7647, Canterbury, New Zealand b Department of Soil and Physical Sciences, Lincoln University, PO Box 85084, Lincoln, 7647, Canterbury, New Zealand c Australian Rivers Institute, Nathan Campus, Griffith University, 170 Kessels Road Nathan, Queensland, 4111, Australia

a 林肯大学生态学系，PO Box 85084, Lincoln, 7647，坎特伯雷，新西兰 b 林肯大学土壤与物理科学系，PO Box 85084, Lincoln, 7647，坎特伯雷，新西兰 c 格里菲斯大学澳大利亚河流研究所，Nathan校区，170 Kessels Road Nathan, Queensland, 4111，澳大利亚

Sustainable agriculture 1. Introduction

Findings of a recent study suggest New Zealand members of the Myrtaceae family could mitigate the threat of microbial contamination of soil following the application of organic wastes (Prosser et al., 2016). The antimicrobial properties of Leptospermum (m¯anuka, tea-tree) and Kunzea (k¯anuka, white tea-tree) species were found to extend to the soil. However, this study did not consider soil N processes. Biological nitrification converts ammonium-N (NH₄⁺) in DSE to nitrate-N (NO₃⁻) in soil, which is the substrate for N₂O production via the nitrifier-denitrification and denitrification of anaerobic bacteria (Bolan et al., 2004). The antimicrobial properties of Myrtaceae could potentially influence these microbially driven soil N cycling processes and alter nitrate (NO₃⁻) production, denitrification and N₂O emissions. In this study, we investigated the suitability of Kunzea robusta for the disposal of DSE in terms of N₂O production.

近期一项研究结果表明，新西兰桃金娘科（Myrtaceae）植物可能减轻施用有机废弃物后土壤微生物污染的威胁（Prosser et al., 2016）。研究发现，Leptospermum（麦卢卡，茶树）和Kunzea（卡努卡，白茶树）属植物的抗菌特性可延伸至土壤中。然而，该研究未考虑土壤氮素过程。生物硝化作用将牛棚废水（DSE）中的铵态氮（NH₄⁺）转化为土壤中的硝态氮（NO₃⁻），后者是厌氧细菌通过硝化细菌反硝化和反硝化作用产生N₂O的底物（Bolan et al., 2004）。桃金娘科植物的抗菌特性可能影响这些由微生物驱动的土壤氮循环过程，并改变硝酸盐（NO₃⁻）的生成、反硝化作用及N₂O排放。本研究从N₂O产生的角度，探讨了Kunzea robusta用于消纳DSE的适宜性。

Nitrous oxide (N₂O) is a potent greenhouse gas with a global warming potential 298 times that of carbon dioxide (Myhre et al., 2013). New Zealand has a unique greenhouse gas profile where 93.4% of N₂O emissions are from agricultural soils (Ministry for the Environment, 2015). Land irrigation of dairy shed effluent (DSE) to pastures contributes to these N₂O emissions and is commonplace in New Zealand. Dairy shed effluent is typically a high-nitrogen (N) mixture of urine, dung, and wash-down water containing 44- 628 mg N L⁻¹; mostly in the form of organic N (Saggar et al., 2004).

氧化亚氮（N₂O）是一种强效温室气体，其全球增温潜势为二氧化碳的298倍（Myhre et al., 2013）。新西兰的温室气体构成独特，其93.4%的N₂O排放来自农业土壤（Ministry for the Environment, 2015）。在新西兰，将牛棚废水（DSE）灌溉至牧场十分普遍，并对上述N₂O排放有所贡献。牛棚废水通常是由尿液、粪便和冲洗水组成的高氮（N）混合物，含氮44- 628 mg N L⁻¹，且主要以有机氮形式存在（Saggar et al., 2004）。

the substrate for N2O and denitrification of antimicrobial properties these microbially driven (NO3⁻) production, we investigated the DSE in terms of N2O We hypothesized that reduce N2O emissions aim of the present study

in New (N)

DSE

hypothesized that application of DSE to K. robusta trees could N₂O emissions compared with application to bare soil. The the present study was to compare changes in N₂O emisand soil inorganic N concentrations from soil underneath

(H.M. Franklin).

¹ These authors contributed equally to practical work and to preparation of this manuscript.

sions and

soil from soil underneath inorganic concentrations

http://dx.doi.org/10.1016/j.ecoleng.2016.11.064 0925-8574/© 2016 Elsevier B.V. All rights reserved.

0925-8574/© 2016

Franklin al.

/ Ecological (2017)

Engineering 99 473–478

H.M.

et

Kunzea trees with bare soil areas following DSE application. We also compared N₂O emissions from Kunzea with emissions data from previous studies of DSE application to grazed pastures in New

Kunzea树下与裸土区域在施用DSE后的N₂O排放。我们还将Kunzea的排放与以往在新西兰放牧牧场施用DSE研究中的排放数据进行了比较

Zealand.

2. Materials and methods 2.1. Site description

2. 材料与方法 2.1. 研究区概况

Kunzea robusta is one of 10 species previously described as Kunzea ericoides (de Lange, 2014). The experimental site was a fenced, planted corner of the Lincoln University Dairy Farm, Canterbury, New Zealand that was retired from grazing in 2008 (1800 m², 43^◦38^′38.07” S, 172^◦26^′1.96” E, described in Franklin et al., 2015). The soil type was a Templeton silt loam (Immature Pallic, Hewitt, 1998; Udic Haplustept, Soil Survey Staff, 2014). Kunzea robusta trees were around 2 m tall and 5 years old, with a 5–10 mm litter layer.

Kunzea robusta是此前被描述为Kunzea ericoides的10个物种之一（de Lange, 2014）。试验地位于新西兰坎特伯雷林肯大学奶牛场一处有围栏的种植角落，该地块于2008年起停止放牧（1800 m²，43^◦38^′38.07” S，172^◦26^′1.96” E，详见Franklin et al., 2015）。土壤类型为Templeton粉砂壤土（Immature Pallic, Hewitt, 1998; Udic Haplustept, Soil Survey Staff, 2014）。Kunzea robusta树高约2 m，树龄5年，枯落物层厚5–10 mm。

zea ericoides (de Lange, planted corner of the New Zealand that was 43^◦38^′38.07” S, 172^◦26 The soil type was a 1998; Udic Haplustept,

zea ericoides（de Lange，……种植角落……新西兰，该地块……43^◦38^′38.07” S，172^◦26 土壤类型为……1998; Udic Haplustept，

were around约为

2.2. Treatment and experimental design

2.2. 处理与试验设计

On 26 July 2012, headspace chamber bases (0.48 m diam., 0.18 m², stainless steel) with an annular water trough were inserted 0.1 m into the soil (gas sampling plots, Fig. 1). During gas sampling events, insulated, stainless steel headspace covers created a gas-tight seal (∼0.14 m above the soil surface). Adjacent to each gas sampling chamber a metal ring (0.48 m diam., 0.18 m²) was inserted 0.1 m into the soil for destructive soil sampling (soil sampling plots, Fig. 1).

2012年7月26日，将带有环形水槽的顶空箱底座（直径0.48 m，0.18 m²，不锈钢）插入土壤0.1 m深（气体采样小区，图1）。气体采样期间，隔热不锈钢顶空箱盖形成气密密封（高出土壤表面约0.14 m）。在每个气体采样箱旁，将一个金属环（直径0.48 m，0.18 m²）插入土壤0.1 m深，用于破坏性土壤采样（土壤采样小区，图1）。

Five replicate K. robusta and bare soil locations (bare soil >1 m from the drip line of trees) were randomly selected. Each location consisted of two subplots to which DSE or control was applied (Fig. 1). Each subplot consisted of a pair of gas sampling/soil sampling plots (Fig. 1). Dairy shed effluent (450 mg N L⁻¹) was applied at 50 kg N ha⁻¹ to DSE subplots and an equal volume of untreated tap water (1.5 mg NO₃⁻-N L⁻¹ and 0.05 mg NH₄⁺-N L⁻¹) to the control subplots. Plots were established radially around K. robusta stems (0.2 m from the stem) and centers of bare soil locations, separated by >0.2 m, to avoid seepage between plots (Fig. 1). Treatments were applied to subplots (gas sampling/soil sampling pairs) randomly on the morning of 7 Aug. 2012. Dairy shed effluent was collected from the Lincoln University Dairy Farm storage pond on 9 Sept. 2011, homogenized, and stored at 5 ^◦C prior to use.

随机选取5个K. robusta重复位点和5个裸土重复位点（裸土距树冠滴水线>1 m）。每个位点包括两个子小区，分别施用DSE或对照处理（图1）。每个子小区由一对气体采样/土壤采样小区组成（图1）。DSE子小区以50 kg N ha⁻¹的量施用牛棚废水（450 mg N L⁻¹），对照子小区施用等体积未经处理的自来水（1.5 mg NO₃⁻-N L⁻¹和0.05 mg NH₄⁺-N L⁻¹）。各小区沿K. robusta树干（距树干0.2 m）及裸土位点中心呈放射状布设，小区间距>0.2 m，以避免小区间的渗流（图1）。于2012年8月7日上午将各处理随机施用于子小区（气体采样/土壤采样小区对）。牛棚废水于2011年9月9日采自林肯大学奶牛场储存池，经均质化后于5 ^◦C下保存直至使用。

pling plots water (1.5 mg subplots. Plots sampling, analysis, and meteorological measurements 2.3.

采样小区……水（1.5 mg……子小区。小区……采样、分析与气象测定 2.3.

measured on field moist soil (10:25 soil:water). Another 4 g subsample of field moist soil was shaken with 40 mL of 2 M KCl for 1 h, centrifuged (10 min at 2000 rpm) and then filtered (Whatman No. 41) (Blakemore et al., 1987). Extracts were analyzed for NH₄⁺-N and NO₃⁻-N by flow injection analysis (FOSS FIAstar 5000 triple channel with SoFIA software version 1.30; Foss Tecator, Hoganas, Sweden). Total C and N were measured on air-dried (35 ^◦C for 48 h), ground, and sieved (2 mm) soil using an Elementar Vario-Max CN Elemental Analyzer (Elementar GmbH, Hanau, Germany). Total organic C was measured using the loss on ignition method (Blakemore et al., 1987). Samples were also analyzed for Olsen P following Olsen et al.

在田间湿润土壤上测定（土水比10:25）。另取4 g田间湿润土壤子样，加入40 mL 2 M KCl振荡1 h，离心（2000 rpm，10 min）后过滤（Whatman No. 41）（Blakemore et al., 1987）。采用流动注射分析法（FOSS FIAstar 5000三通道分析仪，SoFIA软件1.30版；Foss Tecator, Hoganas, Sweden）测定提取液中的NH₄⁺-N和NO₃⁻-N。土壤经风干（35 ^◦C，48 h）、研磨并过筛（2 mm）后，使用Elementar Vario-Max CN元素分析仪（Elementar GmbH, Hanau, Germany）测定全碳和全氮。采用烧失量法测定总有机碳（Blakemore et al., 1987）。样品还按照Olsen et al.的方法测定了Olsen P

(1954).

Soil bulk density was tions in August 2015, been no stock access depth) were carefully (>48 h at 105 ^◦C) to give sity (g cm⁻³). Soil particle Water filled pore space from the experimental 2.4. Statistical analysis Tests for normality so these were log N2O flux data were bulk density was measured in K. robusta and bare soil locain August 2015, after the experimental period. There had no stock access since the trial. Cores (5.4 cm diam. × 5 cm were carefully pressed into the soil. These were oven-dried at 105 ^◦C) to give _g which was used to calculate bulk dencm⁻³). Soil particle density was assumed to be 2.65 g cm⁻³. filled pore space (WFPS) was calculated from these and _g the experimental period (Linn and Doran, 1984).

土壤容重于……2015年8月……，此后无牲畜进入……深度）小心……（105 ^◦C下>48 h）以得到……容重（g cm⁻³）。土壤颗粒……充水孔隙度根据试验期间的…… 2.4. 统计分析 正态性检验……因此对其进行对数……N2O通量数据…… 于试验期结束后的2015年8月，在K. robusta和裸土位点测定了土壤容重。试验结束后该地块一直无牲畜进入。将环刀（直径5.4 cm × 深5 cm）小心压入土壤，取出后于105 ^◦C下烘干，得到θ_g，并据此计算容重（g cm⁻³）。土壤颗粒密度假定为2.65 g cm⁻³。根据上述数据及试验期间的θ_g计算充水孔隙度（WFPS）（Linn and Doran, 1984）。

from the 2.4.

Tests for normality showed the N₂O flux data were skewed so these were log transformed (Ln[flux]). Daily and cumulative N₂O flux data were analyzed using analysis of variance (ANOVA), with a split–split plot design, effectively a special case of repeated measures ANOVA. Within whole plots (the 10 sampling locations), treatments (DSE and control) were randomly assigned to split-plots (subplots each consisting of a pair of gas/soil sampling plots). Within split-plots, sampling occurred on multiple dates (split–split plots). Plot type (K. robusta and bare soil), treatment (DSE and control) and time (Day) were factors. Three-way interactions were removed as the interpretation of such effects is complex. Soil WFPS, pH, NO₃⁻-N, and NH₄⁺-N were analyzed in the same manner. Daily data were compared using ANOVA (p < 0.05) when signifi- cant interactions with time occurred. Two-sample t tests compared background soil conditions between bare soil and K. robusta. Statistics were performed in R version 3.0.1 (R Development Core Team, 2013, Vienna, Austria, http://www.r-project.org/).

正态性检验表明N₂O通量数据呈偏态分布，因此对其进行了对数转换（Ln[通量]）。采用裂-裂区设计的方差分析（ANOVA）对日及累积N₂O通量数据进行分析，该设计实质上是重复测量ANOVA的一种特殊情形。在主区（10个采样位点）内，将处理（DSE和对照）随机分配至裂区（每个子小区由一对气体/土壤采样小区组成）。在裂区内，于多个日期进行采样（裂-裂区）。以小区类型（K. robusta和裸土）、处理（DSE和对照）和时间（天）为因子。由于三因素交互作用的解释较为复杂，故予以剔除。土壤WFPS、pH、NO₃⁻-N和NH₄⁺-N采用相同方法分析。当与时间存在显著交互作用时，采用ANOVA（p < 0.05）比较各日数据。采用双样本t检验比较裸土与K. robusta之间的土壤背景条件。统计分析使用R 3.0.1版完成（R Development Core Team, 2013, Vienna, Austria, http://www.r-project.org/）。

cant interactions background soil tics were performed 2013, Vienna, 3. Results 3.1. Nitrous oxide 3.

……显著交互作用……土壤背景……统计分析……2013, Vienna, 3. 结果 3.1. 氧化亚氮 3.

oxide fluxes 3.1.

Gas samples were taken the day prior to treatment application (Day 0), approximately 4 h after DSE application (Day 1), and on following Days: 2, 3, 9, 16 and 23. Sampling was conducted between 12:30 and 15:30 h. Headspace samples (10 mL) were taken manually 0, 20, and 40 min after positioning the cover and compressed into 6 mL Exetainer tubes (Labco Ltd., High Wycombe, UK). The headspace temperature was recorded in a representative chamber after initial checks found similarity between locations. Immediately prior to analysis, gas samples were brought to ambient pressure and N₂O concentrations were determined using a gas chromatograph (GC, SRI 8610; SRI Instruments, CA, USA) fitted with a ⁶³Ni electron capture detector (Gilson 222 XL; Gilson Inc., WI, USA) and calibrated using BOC  standards (BOC Scientific, New Zealand). Nitrous oxide fluxes were calculated following Hutchinson and Mosier (1981) after checking for linearity in N₂O concentration over time. Cumulative N₂O emissions were determined by integration. Soil core samples (2.5 cm diam. × 7.5 cm depth) were taken to monitor soil gravimetric moisture content (_g), pH, and inorganic- N concentrations. On Days: 0, 2, 3, 9, 16, and 23 three soil cores were taken at random, homogenized and sieved (≤4 mm). A subsample was dried at 105 ^◦C for 24 h to determine _g. Soil pH was (Day 0), approximately lowing Days: 2, 3, 9, 16 12:30 and 15:30 h. ally 0, 20, and 40 min into 6 mL Exetainer headspace temperature after initial checks found prior to analysis, gas and N2O concentrations graph (GC, SRI 8610; SRI graph (GC, SRI electron capture calibrated using Nitrous oxide Mosier (1981) after time. Cumulative

气体样品分别于处理施用前一天（第0天）、DSE施用后约4 h（第1天）以及随后的第2、3、9、16和23天采集。采样时间为12:30至15:30。在盖上箱盖后0、20和40 min时人工抽取顶空气体样品（10 mL），并压入6 mL Exetainer采样管（Labco Ltd., High Wycombe, UK）中。初步检查发现各位点间温度相近，因此在一个代表性采样箱中记录顶空温度。分析前将气体样品恢复至环境压力，采用配备⁶³Ni电子捕获检测器（Gilson 222 XL; Gilson Inc., WI, USA）的气相色谱仪（GC, SRI 8610; SRI Instruments, CA, USA）测定N₂O浓度，并以BOC 标准气体（BOC Scientific, New Zealand）进行校准。在确认N₂O浓度随时间呈线性变化后，按照Hutchinson and Mosier (1981)的方法计算氧化亚氮通量。累积N₂O排放量通过积分求得。采集土芯样品（直径2.5 cm × 深7.5 cm）以监测土壤质量含水量（θ_g）、pH和无机氮浓度。在第0、2、3、9、16和23天随机采集3个土芯，混匀后过筛（≤4 mm）。取子样于105 ^◦C下烘干24 h以测定θ_g。土壤pH…… （第0天），约……随后的第2、3、9、16……12:30至15:30。……0、20和40 min……压入6 mL Exetainer……顶空温度……初步检查发现……分析前，气体……N2O浓度……色谱仪（GC, SRI 8610; SRI……色谱仪（GC, SRI……电子捕获……校准采用……氧化亚氮……Mosier (1981)在……时间。累积

N concentrations. were taken at

氮浓度。……采集于

Prior to treatment application (Day 0) N₂O flux was similar between locations (Fig. 2a). K. robusta had significantly lower N₂O fluxes compared with bare soil following DSE application until after Day 9 (Fig. 2a). Plot type, treatment (p < 0.01) and sampling date (p < 0.05) significantly affected daily N₂O flux, with the treatment effect changing temporally (treatment x time, p < 0.05). Nitrous oxide flux from K. robusta-DSE plots rose significantly only on Day 1 (p < 0.001).

处理施用前（第0天），各位点间N₂O通量相近（图2a）。DSE施用后直至第9天之后，K. robusta的N₂O通量均显著低于裸土（图2a）。小区类型、处理（p < 0.01）和采样日期（p < 0.05）显著影响日N₂O通量，且处理效应随时间变化（处理 × 时间，p < 0.05）。K. robusta-DSE小区的氧化亚氮通量仅在第1天显著升高（p < 0.001）。

fluxes compared Day 9 (Fig. 2a). (p < 0.05) significantly effect changing oxide flux from

通量相比……第9天（图2a）。（p < 0.05）显著……效应随时间变化……氧化亚氮通量来自

Cumulative N₂O fluxes were higher (p < 0.001) from the bare soil-DSE plots (676 g N₂O N ha⁻¹ or 1.35% of applied N) compared with the bare soil-control (152 g N₂O–N ha⁻¹), K. robusta-DSE (133 g N₂O-N ha⁻¹ or 0.27% of applied N) and K. robusta-control plots (95 g N₂O–N ha⁻¹), which were similar. Plot type (p < 0.01), treatment (p < 0.05), time (p < 0.001), and the plot type x treatment interaction (p < 0.01) were significant.

裸土-DSE小区的累积N₂O通量（676 g N₂O N ha⁻¹，占施氮量的1.35%）高于（p < 0.001）裸土-对照小区（152 g N₂O–N ha⁻¹）、K. robusta-DSE小区（133 g N₂O-N ha⁻¹，占施氮量的0.27%）和K. robusta-对照小区（95 g N₂O–N ha⁻¹），后三者相近。小区类型（p < 0.01）、处理（p < 0.05）、时间（p < 0.001）以及小区类型 × 处理交互作用（p < 0.01）均显著。

plots (95 g N treatment (p interaction ( 3.2. Soil and and meteorological conditions 3.2.

小区（95 g N……处理（p……交互作用（ 3.2. 土壤与气象条件 3.2.

soil

centrated beneath集中于……之下

475 sampling plot content where pH

475 采样小区……含量……其中pH

Fig. 1. The sampling plot bare soil plots.图1. 采样小区……裸土小区。

Olsen-P and NH₄⁺-N did not differ between K. robusta and bare soil (Table 1).

Olsen-P和NH₄⁺-N在K. robusta与裸土之间无差异（表1）。

K. robusta plots had significantly lower (p < 0.001) WFPS than the bare soil plots (Fig. 2b), however, WFPS did not vary due to treatment (DSE or control) or time. Mean daily _g ranged from 27 to 32% for K. robusta and 31- 35% for bare soil plots. A total of 104 mm of rain fell during the experiment, consisting of one substantial event (75 mm, Day 8–10, Fig. 2b). The mean daily air temperature ranged from 6.7 to 14.9 ^◦C (Fig. 2b) and a spike later in the experiment corresponded to a decrease in soil moisture. Throughout the experiment soil pH was higher (p < 0.05) in the bare soil (mean of 5.8 ± 0.02) than K. robusta plots (5.5 ± 0.03), while treatment (DSE or control) and time did not affect pH. Soil NO₃⁻-N concentrations were higher (p < 0.01) in the K. robusta plots than bare soil (Fig. 3a) and were not affected by treatment or time. Ammonium-N concentrations were signifi- cantly higher (p < 0.05) in DSE than control plots, but did not differ between K. robusta and bare soil (Fig. 3b). Ammonium-N was simi- 32% for K. robusta of rain fell during event (75 mm, Day ranged from 6.7 to ment corresponded experiment soil pH 5.8 ± 0.02) than K.

K. robusta小区的WFPS显著低于（p < 0.001）裸土小区（图2b），但WFPS不因处理（DSE或对照）或时间而变化。K. robusta小区的日均θ_g为27%~32%，裸土小区为31- 35%。试验期间总降雨量为104 mm，其中包括一次较大降雨事件（75 mm，第8–10天，图2b）。日均气温为6.7~14.9 ^◦C（图2b），试验后期的气温骤升与土壤水分下降相对应。整个试验期间，裸土的土壤pH（均值5.8 ± 0.02）高于（p < 0.05）K. robusta小区（5.5 ± 0.03），而处理（DSE或对照）和时间对pH无影响。K. robusta小区的土壤NO₃⁻-N浓度高于（p < 0.01）裸土（图3a），且不受处理或时间影响。DSE小区的铵态氮浓度显著高于（p < 0.05）对照小区，但在K. robusta与裸土之间无差异（图3b）。铵态氮…… K. robusta为……32%……试验期间降雨……降雨事件（75 mm，第……为6.7至……试验……相对应……试验期间土壤pH……5.8 ± 0.02）高于K.

Soil NO3⁻-N robusta plots treatment or cantly higher (p

土壤NO3⁻-N……robusta小区……处理或……显著高于（p

between K.在K.之间

lar in all plots at the start of the experiment (Fig. 3b) and increased following treatment application (p < 0.001), but more so in DSE plots (treatment x time, p < 0.01). Ammonium-N spiked in control plots on Day 16 to match levels in DSE plots.

在试验开始时各小区的铵态氮浓度相近（图3b），施用处理后均有所升高（p < 0.001），但DSE小区升高更明显（处理 × 时间，p < 0.01）。第16天对照小区的铵态氮骤升，达到与DSE小区相当的水平。

plots 4. Discussion 4.1. Low nitrous oxide emissions under K. robusta

小区 4. 讨论 4.1. K. robusta下较低的氧化亚氮排放

Cumulative N₂O emissions following effluent application were 80% lower beneath K. robusta relative to the bare soil. No other studies have investigated N₂O emissions from soil planted with K. robusta receiving DSE. Mean N₂O emissions from K. robusta locations (0.095 and 0.133 kg N ha⁻¹ for control and DSE respectively) during the experimental period were close to background rates reported under Kunzea spp. elsewhere (below detection limits, Price et al., 2010; and 0.30 kg N ha⁻¹ yr⁻¹, Hedley et al., 2013). Nitrous oxide emissions following DSE application to K. robusta durstudies have K. robusta receiving locations (0.095 tively) during the rates reported 476 H.M. Franklin et al. / Ecological Engineering 99 (2017) 473–478 Fig. 2. Back-transformed mean (±SE) daily N₂O–N flux (a) and mean (±SE) water filled pore space and meteorological measurements (b) following the application of dairy shed effluent (DSE, 50 kg N ha⁻¹) and control treatments to K. robusta and bare soil plots (n = 5). Meteorological data were obtained from the nearby NIWA Broadfield Climate Station (43^◦37^′34.4” S, 172^◦28^′13.4 E). Water filled pore space data are for control plots only, dairy shed effluent plots not shown (no effect of treatment type). ing the 24-day experimental period (0.133 kg N₂O–N ha⁻¹, 0.27% of N applied) were at the low end of those found in the literature for similar DSE applications to grazed pastures in New Zealand (0.13- 1.08 kg N ha⁻¹). Following applications of 50–60 kg N ha⁻¹ DSE N₂O was emitted at rates of 0.13-0.48 (0.25-0.8% of N applied, Li et al., 2015) and 0.15-0.45 kg N ha⁻¹ (0.31-0.73% of N applied, Bhandral et al., 2007) during approximately 20 and 2 week experimental periods, respectively. While consecutive annual DSE applications of 56 and 43 kg N ha⁻¹ in the Canterbury region produced 0.665 and 1.08 kg N₂O-N ha⁻¹ yr⁻¹ (1.2 and 2.5% of N applied, van der Weerden et al., 2016). Consistent with the current study, others also report N₂O emissions returning to background levels rapidly (< 3 weeks) following effluent application (Barton and Schipper 2001; Bhandral et al., 2010). 4.2. Soil conditions and nitrous oxide emissions Water filled pore space was around 10% higher in bare soil than beneath K. robusta, likely due to transpiration by K. robusta and canopy rainfall interception. This was within the range suitable for denitrification (60–65%, Linn and Doran, 1984), however, WFPS in K. robusta plots were below this range. The corresponding aerobic conditions may have decreased N₂O-reductase activity in denitrification (Bakken and Dörsch, 2007) and potentially contributed to reduced emissions. Soil moisture has previously been associated with variation in N₂O emissions from Kunzea forests (Hedley et al., 2013). The dry sites which Kunzea spp. often dominate may explain the low reported background N₂O production rates (Hedley et al., 2013; Price et al., 2010). The control treatment 4.2. Soil conditions and nitrous oxide emissions Water filled pore space was around 10% higher in bare soil than beneath K. robusta, likely due to transpiration by K. robusta and canopy rainfall interception. This was within the range suitable for denitrification (60–65%, Linn and Doran, 1984), however, WFPS in K. robusta plots were below this range. The corresponding aerobic conditions may have decreased N₂O-reductase activity in denitrification (Bakken and Dörsch, 2007) and potentially contributed to reduced emissions. Soil moisture has previously been associated with variation in N₂O emissions from Kunzea forests (Hedley et al., 2013). The dry sites which Kunzea spp. often dominate may explain the low reported background N₂O production rates (Hedley et al., 2013; Price et al., 2010). The control treatment increased 10-fold immediately following DSE likely due to the high NH₄⁺ concentrations in the DSE. microbial immobilization, or oxidization to NO₃⁻ may

施用废水后，K. robusta下的累积N₂O排放量较裸土低80%。目前尚无其他研究考察种植K. robusta并接受DSE的土壤的N₂O排放。试验期间K. robusta位点的平均N₂O排放量（对照和DSE分别为0.095和0.133 kg N ha⁻¹）接近其他地区Kunzea spp.下报道的背景排放速率（低于检出限，Price et al., 2010；以及0.30 kg N ha⁻¹ yr⁻¹，Hedley et al., 2013）。向K. robusta施用DSE后的氧化亚氮排放……研究……K. robusta接受……位点（0.095……分别）在……期间……报道的速率 476 H.M. Franklin et al. / Ecological Engineering 99 (2017) 473–478 图2. 向K. robusta和裸土小区施用牛棚废水（DSE，50 kg N ha⁻¹）和对照处理后，回转换的日均（±SE）N₂O–N通量（a）以及平均（±SE）充水孔隙度和气象测定结果（b）（n = 5）。气象数据来自附近的NIWA Broadfield气象站（43^◦37^′34.4” S，172^◦28^′13.4 E）。充水孔隙度数据仅为对照小区数据，牛棚废水小区数据未列出（处理类型无影响）。在24天试验期内（0.133 kg N₂O–N ha⁻¹，占施氮量的0.27%），处于文献报道的新西兰放牧牧场类似DSE施用排放量的低端（0.13- 1.08 kg N ha⁻¹）。在施用50–60 kg N ha⁻¹ DSE后，在约20周和2周的试验期内，N₂O排放量分别为0.13-0.48（占施氮量的0.25-0.8%，Li et al., 2015）和0.15-0.45 kg N ha⁻¹（占施氮量的0.31-0.73%，Bhandral et al., 2007）。而在坎特伯雷地区连续两年分别施用56和43 kg N ha⁻¹的DSE，产生了0.665和1.08 kg N₂O-N ha⁻¹ yr⁻¹的排放（占施氮量的1.2%和2.5%，van der Weerden et al., 2016）。与本研究一致，其他研究也报道施用废水后N₂O排放迅速（< 3周）恢复至背景水平（Barton and Schipper 2001; Bhandral et al., 2010）。4.2. 土壤条件与氧化亚氮排放 裸土的充水孔隙度比K. robusta下高约10%，这可能是K. robusta的蒸腾作用和林冠截留降雨所致。裸土的WFPS处于适宜反硝化作用的范围内（60–65%，Linn and Doran, 1984），而K. robusta小区的WFPS低于该范围。相应的好氧条件可能降低了反硝化过程中N₂O还原酶的活性（Bakken and Dörsch, 2007），并可能促成了排放的减少。此前已有研究将土壤水分与Kunzea林N₂O排放的变异联系起来（Hedley et al., 2013）。Kunzea spp.通常占优势的干旱生境可能解释了已报道的较低背景N₂O产生速率（Hedley et al., 2013; Price et al., 2010）。对照处理 4.2. 土壤条件与氧化亚氮排放 裸土的充水孔隙度比K. robusta下高约10%，这可能是K. robusta的蒸腾作用和林冠截留降雨所致。裸土的WFPS处于适宜反硝化作用的范围内（60–65%，Linn and Doran, 1984），而K. robusta小区的WFPS低于该范围。相应的好氧条件可能降低了反硝化过程中N₂O还原酶的活性（Bakken and Dörsch, 2007），并可能促成了排放的减少。此前已有研究将土壤水分与Kunzea林N₂O排放的变异联系起来（Hedley et al., 2013）。Kunzea spp.通常占优势的干旱生境可能解释了已报道的较低背景N₂O产生速率（Hedley et al., 2013; Price et al., 2010）。对照处理……施用DSE后立即增加了10倍，这可能是由于DSE中NH₄⁺浓度较高。微生物固持或氧化为NO₃⁻可能

Plant uptake, microbial immobilization, or oxidization to NO3− may dry, aerated,植物吸收、微生物固持或氧化为NO3−可能……干燥、通气良好的

FranklinFranklin

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/ Ecological (2017)

EngineeringEngineering

99 473–478

H.M.

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N₂O production via denitrification. Differences in WFPS between K. robusta and bare soil confound the interpretation, meaning we cannot conclude whether inhibition of nitrification or denitrification occurred.

通过反硝化作用产生的N₂O。K. robusta与裸土之间WFPS的差异干扰了对结果的解释，因此我们无法断定是硝化作用还是反硝化作用受到了抑制。

Blakemore, L.C., Searle, P.L., Daly, B.K., 1987. Methods for chemical analysis of In: New Zealand Soil Bureau Report. New Zealand Soil Bureau, Lower Hutt,

Blakemore, L.C., Searle, P.L., Daly, B.K., 1987. Methods for chemical analysis of In: New Zealand Soil Bureau Report. New Zealand Soil Bureau, Lower Hutt,

soils.

New Zealand. Bolan, N.S., Saggar, nitrogen from

New Zealand. Bolan, N.S., Saggar, nitrogen from

from grazed Greenway, secondary Dickinson, nitrogen in agricultural Lambie, S.M., environmental implications, and mitigation. Adv. Agron. doi.org/10.1016/s0065-2113(04)84002-1. Bolton, K.G.E., Greenway, M., 1999. Nutrient sinks in a constructed receiving secondary treated effluent. Water Sci. Technol. dx.doi.org/10.1016/S0273-1223(99)00470-9. Franklin, H.M., Dickinson, N.M., Esnault, C.J., Robinson, B.H., and nitrogen in agricultural landscapes of New Zealand. 407–420, http://dx.doi.org/10.1007/s11104-015-2622-2..

from grazed Greenway, secondary Dickinson, nitrogen in agricultural Lambie, S.M., environmental implications, and mitigation. Adv. Agron. doi.org/10.1016/s0065-2113(04)84002-1. Bolton, K.G.E., Greenway, M., 1999. Nutrient sinks in a constructed receiving secondary treated effluent. Water Sci. Technol. dx.doi.org/10.1016/S0273-1223(99)00470-9. Franklin, H.M., Dickinson, N.M., Esnault, C.J., Robinson, B.H., and nitrogen in agricultural landscapes of New Zealand. 407–420, http://dx.doi.org/10.1007/s11104-015-2622-2..

4.3. Implications for future myrtaceae

4.3. 对未来桃金娘科研究的启示

Bolton, K.G.E., Greenway, M., 1999. Nutrient sinks in a constructed wetland receiving secondary treated effluent. Water Sci. Technol. 40, 341–347, http:// dx.doi.org/10.1016/S0273-1223(99)00470-9. Franklin, H.M., Dickinson, N.M., Esnault, C.J., Robinson, B.H., 2015. Native plants and nitrogen in agricultural landscapes of New Zealand. Plant Soil 394, 407–420, http://dx.doi.org/10.1007/s11104-015-2622-2. Hedley, C.B., Lambie, S.M., Dando, J.L., 2013. Edaphic and environmental controls of soil respiration and related soil processes under two contrasting manuka and kanuka shrubland stands in North Island, New Zealand. Soil Res. 51, 390–405, http://dx.doi.org/10.1071/SR12248.

Bolton, K.G.E., Greenway, M., 1999. Nutrient sinks in a constructed wetland receiving secondary treated effluent. Water Sci. Technol. 40, 341–347, http:// dx.doi.org/10.1016/S0273-1223(99)00470-9. Franklin, H.M., Dickinson, N.M., Esnault, C.J., Robinson, B.H., 2015. Native plants and nitrogen in agricultural landscapes of New Zealand. Plant Soil 394, 407–420, http://dx.doi.org/10.1007/s11104-015-2622-2. Hedley, C.B., Lambie, S.M., Dando, J.L., 2013. Edaphic and environmental controls of soil respiration and related soil processes under two contrasting manuka and kanuka shrubland stands in North Island, New Zealand. Soil Res. 51, 390–405, http://dx.doi.org/10.1071/SR12248.

We identified a significant reduction in N₂O production from soil beneath K. robusta following application of DSE, compared with bare soil. Constraints on the denitrification process in the dry K. robusta soil are a possible cause of reduced emissions (Hedley et al., 2013; Price et al., 2010). Nitrous oxide emissions from K. robusta were low compared to those following similar applications to dairy pastures, which typically have higher WFPS than that measured beneath K. robusta (Bhandral et al., 2007; Li et al., 2015). Irrigation of DSE onto K. robusta plantations may offer a sustainable disposal option for this high N waste, resulting in low N₂O emissions, even in the winter when emissions are typically higher. This would require a closed canopy prior to DSE application to minimize exposed bare soil which is likely to emit more N₂O. Kunzea plantations may also provide additional income to farms through the production of high value tea-tree oils and honey (Stephens et al., 2010). Other Myrtaceae, Eucalyptus (Tzanakakis et al., 2009) and Melaleuca spp. (Bolton and Greenway, 1999), have been successfully used in effluent land treatment systems to mitigate NO₃⁻ leaching and produce harvestable biomass, but associated N₂O emissions have not been investigated. Although suppression of denitrification is desirable, pollution swapping may occur through increased NO₃⁻ leaching. Kunzea robusta seedlings have demonstrated a capacity for luxury N uptake (Franklin et al., 2015). Nitrogen storage in K. robusta roots, wood and foliage may reduce the pool of soil nitrate available for both denitrification to N₂O, and NO₃⁻ leaching. Further research should simultaneously measure N₂O emissions, NO₃⁻ leaching and N uptake by K. robusta, to determine the net environmental effect of DSE irrigation onto K. robusta. In addition, future work should incorporate comparisons to other tree and grassland species to determine if this effect is unique to K. robusta. The environmental benefits of reduced N₂O emissions warrant a closer look at the effect of Myrtaceae on the soil N cycle worldwide.

我们发现，与裸土相比，施用DSE后K. robusta下土壤的N₂O产生量显著降低。干燥的K. robusta土壤中反硝化过程受到限制，可能是排放减少的原因（Hedley et al., 2013; Price et al., 2010）。与向奶牛牧场进行类似施用后的排放相比，K. robusta的氧化亚氮排放较低，而奶牛牧场的WFPS通常高于K. robusta下的测定值（Bhandral et al., 2007; Li et al., 2015）。将DSE灌溉至K. robusta人工林可能为这种高氮废弃物提供一种可持续的消纳途径，从而实现较低的N₂O排放，即使在排放通常较高的冬季亦是如此。这需要在施用DSE前形成郁闭林冠，以尽量减少可能排放更多N₂O的裸露土壤。Kunzea人工林还可通过生产高价值的茶树精油和蜂蜜为农场提供额外收入（Stephens et al., 2010）。其他桃金娘科植物，如Eucalyptus（Tzanakakis et al., 2009）和Melaleuca spp.（Bolton and Greenway, 1999），已成功应用于废水土地处理系统，以减轻NO₃⁻淋溶并生产可收获的生物量，但其相关的N₂O排放尚未得到研究。尽管抑制反硝化作用是可取的，但可能通过增加NO₃⁻淋溶而发生污染转移。Kunzea robusta幼苗已表现出奢侈吸氮的能力（Franklin et al., 2015）。K. robusta根系、木材和叶片中的氮储存可能减少土壤中可供反硝化生成N₂O和NO₃⁻淋溶的硝酸盐库。未来研究应同步测定N₂O排放、NO₃⁻淋溶和K. robusta的氮吸收，以确定向K. robusta灌溉DSE的净环境效应。此外，未来工作应与其他树种和草地物种进行比较，以确定该效应是否为K. robusta所特有。N₂O排放减少所带来的环境效益，值得在全球范围内进一步深入研究桃金娘科植物对土壤氮循环的影响。

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Hewitt, A.E., 1998. New Zealand soil classification. In: Landcare Research Science Series, 2nd edn. Manaaki Whenua Press, Lincoln, New Zealand. Hutchinson, G.L., Mosier, A.R., 1981. Improved soil cover method for field measurement of nitrous-oxide fluxes. Soil Sci. Soc. Am. J. 45, 311–316, http:// dx.doi.org/10.2136/sssaj1981.03615995004500020017x. Li, J., Luo, J., Shi, Y., Lindsey, S., Houlbrooke, D., Ledgard, S., 2015. Nitrous oxide emissions from dairy farm effluent applied to a New Zealand pasture soil. Soil Use Manage. 31, 279–289, http://dx.doi.org/10.1111/sum.12187. Linn, D.M., Doran, J.W., 1984. Effect of water-filled pore space on carbon dioxide and nitrous oxide production in tilled and nontilled soils. Soil Sci. Soc. Am. J. 48, 1267–1272, http://dx.doi.org/10.2136/sssaj1984.03615995004800060013x. Ministry for the Environment, 2015. New Zealand’s Greenhouse Gas Inventory 1990-2013. Ministry for the Environment, Wellington, New Zealand. Myhre, G., et al., 2013. Anthropogenic and natural radiative forcing. In: Stocker, T.F. (Ed.), Climate Change 2013: The Physical Science Basis. Contribution of Working Group I to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University Press, Cambridge, United Kingdom, New York, NY, USA. Olsen, S.R., Cole, C.V., Watanabe, F.S., Deans, L.A., 1954. Estimation of Available Phosphorus in Soils by Extraction with Sodium Bicarbonate. Price, S., Whitehead, D., Sherlock, R., McSeveny, T., Rogers, G., 2010. Net exchange of greenhouse gases from soils in an unimproved pasture and regenerating indigenous Kunzea ericoides shrubland in New Zealand. Soil Res. 48 (5), 385–394, http://dx.doi.org/10.1071/SR09156. Prosser, J.A., Woods, R.R., Horswell, J., Robinson, B.H., 2016. The potential in-situ antimicrobial ability of Myrtaceae plant species on pathogens in soil. Soil Biol. Biochem. 96, 1–3, http://dx.doi.org/10.1016/j.soilbio.2015.12.007. R Development Core Team, 2013. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URL http://www.R-project.org/. Saggar, S., Bolan, N.S., Bhandral, R., Hedley, C.B., Luo, J., 2004. A review of emissions of methane, ammonia, and nitrous oxide from animal excreta deposition and farm effluent application in grazed pastures. N. Z. J. Agr. Res. 47, 513–544, http://dx.doi.org/10.1080/00288233.2004.9513618. Soil Survey Staff, 2014. Keys to Soil Taxonomy, 12th edn. USDA-Natural Resources Conservation Service, Washington, DC. Stephens, J.M., Schlothauer, R.C., Morris, B.D., Yang, D., Fearnley, L., Greenwood, D.R., Loomes, K.M., 2010. Phenolic compounds and methylglyoxal in some New Zealand manuka and kanuka honeys. Food Chem. 120, 78–86, http://dx.doi. org/10.1016/j.foodchem.2009.09.074. Tzanakakis, V.A., Paranychianakis, N.V., Angelakis, A.N., 2009. Nutrient removal and biomass production in land treatment systems receiving domestic effluent. Ecol. Eng. 35, 1485–1492, http://dx.doi.org/10.1016/j.ecoleng.2009.06.009. Zhong, H., Kim, Y.-N., Smith, C., Robinson, B., 2014. Dickinson N Does rhizosphere and litter diversity mediate the biogeochemistry of restoration soils? In: 20th World Congress Of Soil Science, Jeju, South Korea, p. 304. de Lange, P.J., 2014. A revision of the New Zealand Kunzea ericoides (Myrtaceae) complex. PhytoKeys 40, 1–185, http://dx.doi.org/10.3897/phytokeys.40.7973. van der Weerden, T.J., Sherlock, R.R., Williams, P.H., Cameron, K.C., 1999. Nitrous oxide emissions and methane oxidation by soil following cultivation of two different leguminous pastures. Biol. Fert. Soil. 30, 52–60, http://dx.doi.org/10. 1007/s003740050587. van der Weerden, T.J., et al., 2016. Nitrous oxide emissions from urea fertiliser and effluent with and without inhibitors applied to pasture. Agri. Ecosys. Environ. 219, 58–70, http://dx.doi.org/10.1016/j.agee.2015.12.006.

a closed soil which soil which is likely to also provide additional of high value tea-tree Myrtaceae, Eucalyptus (Bolton and Greenway, ent land treatment harvestable biomass, investigated. Although pollution swapping tal benefits of effect of Myrtaceae Acknowledgements This research wish to thank Trevor Hendry University) for Tim Clough and

……封闭的……土壤，这些土壤可能……还提供额外的……高价值茶树……桃金娘科，Eucalyptus（Bolton and Greenway，……废水土地处理……可收获的生物量……研究。尽管……污染转移……环境效益……桃金娘科的影响 致谢 本研究……感谢Trevor Hendry……大学）……Tim Clough和

1Acknowledgements致谢

This research was funded by Lincoln University. The authors wish to thank Manjula Premaratne, Qian Liang, Roger Atkinson and Trevor Hendry (Faculty of Agriculture and Life Sciences, Lincoln University) for valuable technical assistance, as well as Professor Tim Clough and two anonymous reviewers for comments on the manuscript draft.

本研究由林肯大学资助。作者感谢Manjula Premaratne、Qian Liang、Roger Atkinson和Trevor Hendry（林肯大学农业与生命科学学院）提供的宝贵技术支持，并感谢Tim Clough教授和两位匿名审稿人对论文初稿提出的意见。

Zhong, H., Kim, Y.-N., and litter diversity World Congress de Lange, P.J., 2014.

Zhong, H., Kim, Y.-N., and litter diversity World Congress de Lange, P.J., 2014.

2References参考文献

Bakken, L.R., Dörsch, P., 2007. Nitrous oxide emission and global changes: modelling approaches. In: Bothe, H., Ferguson, S.J., Newton, W.E. (Eds.), Biology of the Nitrogen Cycle. Elsevier, Amsterdam, The Netherlands, pp. 382–395. Barton, L., Schipper, L.A., 2001. Regulation of nitrous oxide emissions from soils irrigated with dairy farm effluent. J. Environ. Qual. 30, 1881–1887, http://dx. doi.org/10.2134/jeq2001.1881.

irrigated with Bhandral, R., Bolan,

Bhandral, R., Bolan, N.S., Saggar, S., Hedley, M.J., 2007. Nitrogen transformation and nitrous oxide emissions from various types of farm effluents. Nutr. Cycl. Agroecosys. 79, 193–208, http://dx.doi.org/10.1007/s10705-007-9107-5. Bhandral, R., Bolan, N.S., Saggar, S., 2010. Nitrous oxide emission from farm dairy effluent application in grazed grassland. Revista de la ciencia del suelo y nutrición vegetal 10, 22–34, http://dx.doi.org/10.4067/S0718- 27912010000100003.

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