Camellia oleifera Abel. is one of the four woody edible oil trees around the world, which is also an important economic species in subtropical China. It is mainly cultivated in subtropical region, where the soil constrains the yield of C. oleifera oil due to its low fertility and pH. Thereby, intensive management including fertilization practice, especially intensive nitrogen (N) input, has been developed as a vital way to enhance oil yield in C. oleifera plantations. However, excessive nitrogen input increases soil nitrous oxide (N2O) emissions and soil acidification, limiting sustainable development of economic forests. As one of the important greenhouse gases, N2O is 265 times greater than carbon dioxide in global warming potential on 100-year scale. To mitigate soil N2O emissions and soil acidification, soil amelioration, including applications of biochar, nitrification inhibitors, and urease inhibitors, played an important role in sustainable management of C. oleifera plantations. This chapter reviewed soil nitrogen cycling, N2O emissions, and soil amelioration in C. oleifera plantations, which will benefit the sustainable management of C. oleifera plantations and hence the development of C. oleifera industries.
- Camellia oleifera
- nitrification inhibitor
- soil amelioration
- sustainable forest management
- urease inhibitor
1. Camellia oleifera
Camellia oleifera Abel. as a native edible oil tree has a long cultivation history in subtropical China . It is a perennial and evergreen species with synchronous flowers and fruits. The cultivation area and total product value of C. oleifera have reached 4.47 million ha and 102.4 billion Chinese yuan, respectively . With rapid development, the C. oleifera oil accounted for 80% domestic high-end vegetable edible oils in 2018 from China. High habitat suitability area for C. oleifera cultivation in China has been up to 4.94% .
Specially, C. oleifera oil and oils derived from palm, olive, and coconut are the four major woody edible oils in the world . The C. oleifera oil is characterized by remarkable antioxidant activity  and high content of unsaturated fatty acids (about 83%) .
Camellia oleifera can survive and adapt to low-fertility acid soil. Generally, it usually is used in the conservation of soil and water as well as afforestation in barren hill. Therefore, C. oleifera is an excellent species with both ecological and economic advantages. Development of C. oleifera industry would be beneficial for the safety of edible oil and the conservation of soil and water in China.
As a typical economic tree, intensification such as water management, fertilization, and trimming takes an important part in the management of C. oleifera plantations. Notably, organic matter, available phosphorus, and pH value was low in C. oleifera plantation soils , constraining the yield of C. oleifera oil. Therefore, intensive management with fertilization is often performed in C. oleifera plantations .
Fertilization is the major way of intensive management, efficiently improving the yield of oil in C. oleifera plantations. However, a large amount of nitrogen (N) input increased the risk of soil N leaching and gaseous N (e.g., nitrous oxide (N2O), nitric oxide (NO), ammonia (NH3)) losing . In addition, excessive N input induced soil acidification .
2.1 Nitrous oxide emissions
Nitrous oxide, as the major ozone-depleting substance , has been recognized to be an important greenhouse gas. Especially, the potential of N2O for global warming is 265 times than that of carbon dioxide . The concentration of N2O is ranging from 270 ppb in pre-industrial period to 329.9 ppb in 2017 .
Soil systems contributed the largest source of N2O emissions (13 Tg N2O-N yr−1), of which human activities accounted for 54% . Nitrogen input such as N deposition and N fertilization often increased N2O emissions and altered the process of N transformation [14, 15, 16, 17]. Generally, soil N2O emissions had a positive and linear relationship with N input . About 120 Tg N was contributed by human activities per year . Therefore, intensive N input often leads to high emissions of soil N2O .
2.1.1 Nitrification and denitrification
2.1.2 Influence factors
220.127.116.11 Soil moisture
Soil moisture is a vital factor that affects soil N2O emissions. Generally, soil N2O emission rates reached the peak when soil water-filled pore space (WFPS) was 60–70% . For example, soil N2O emissions were significantly higher under 60% WFPS conditions than that under flooded conditions .
18.104.22.168 Soil temperature
Effects of soil temperature on N2O emissions were more complex than that of soil moisture. For example, warming increased soil N2O emissions from boreal peatland  and alpine meadow . Soil N2O emissions had an exponential increased relationship with incubation temperatures . A significant positive correlation was presented in N2O emissions and soil temperature from different soil types (paddy, orchard, forest, and mountain) . Although warming did not affect soil N2O emissions from northern peatlands, it suppressed N2O emissions under N addition conditions . By contrast, the effects of warming on soil N2O emissions from alpine meadow soil were not observed . Consistently, no significant increase of soil N2O emissions was found with increasing incubation temperatures . Previous study reported that soil moisture and temperature can explain 86% of soil N2O emissions .
22.214.171.124 Soil O2 concentration
Soil O2 concentration was closely related with soil moisture and soil mechanical composition. Generally, soil with higher water content and larger clay fraction had lower soil O2 concentrations. Lower soil O2 concentrations mainly promoted soil N2O emissions via denitrification [20, 35]. The production of N2O and NO was increased when O2 concentration decreased from 21% to 0.5% in a laboratory study . Similarly, field study reported that soil N2O emissions increased with increasing soil O2 concentrations in wetland .
126.96.36.199 Soil pH
pH played an important role in the activity of microbes . Indeed, soil acidification  and soil pH amelioration  significantly influenced soil N2O emissions. However, other researchers reported that there was no significant correlation between N2O emissions and pH .
pH influenced the activity of nitrification- and denitrification-related enzymes . Generally, soil acidification increased N2O emissions . Compared with ammonia-oxidizing bacteria (AOB), ammonia-oxidizing archaea (AOA) were higher in activity and resistance from acid soil . However, the domination of AOB was increased by increasing soil pH . Additionally, archaeal amoA genes had a wide pH range of about 3.7–8.65, which had high activity in extreme environments such as high temperature and extreme acid .
2.1.3 Nitrous oxide emissions from Camellia oleifera plantation soils
Our previous field study (1 year) found that soil N2O emissions were 92.14 ± 47.01 mg m−2 in control treatment and were 375.10 ± 60.30 mg m−2 in fertilization treatment (400 kg NH4NO3-N ha−1) from C. oleifera plantations .
2.2 Soil acidification
Acid soil (pH < 5.5) as a main soil type covers about 30% free ice land . However, soil acidification has been becoming more and more serious . Soil acidification should be taken into consideration due to its constraint in the sustainable development of agricultural sector . In China, soil pH (except alkaline soils at pH 7.10–8.80) from crop fields reduced by 0.13–0.76 during the year 1980–2000 . For example, soil pH (surface layer) decreased by 0.30 units from 1981 to 2012 in Sichuan Province, China .
With a long cultivation history, C. oleifera was widely cultivated in acid or strongly acid soil in subtropical China . The optimum pH for the growth of C. oleifera is 5.5–6.5 . However, acid deposition  and intensive N input  may stimulate soil acidification from C. oleifera plantations. Additionally, long-term N input may also increase the toxicity of aluminum (Al) , limiting the sustainable development of C. oleifera.
Soil acidification from C. oleifera plantations is mainly related to the following factors.
Long-term precipitation increased the loss of base cations such as Ca2+, Mg2+, K+, and Na+, reducing the soil pH buffering capacity. In addition, long-term precipitation promoted the accumulation of Al3+ and Fe3+ in soil, which could further hydrolyze to Fe(OH)3 or Al(OH)3 and release 3H+.
2.2.2 Plant physiology
When plant roots absorb a NH4+ from soil, an H+ will release into soil; in turn, absorbing a NO3− from soil will release an OH− into soil .
Organic acid (R▬COOH) from root exudates can release an H+ after hydrolysis. In addition, anions of organic acids (e.g., citric acid and malic acid) can chelate with Al3+ in the soil and inhibit the root system that absorbs Al3+, alleviating Al3+ toxicity to plant growth [48, 54, 55].
Plants such as C. oleifera  can uptake Al3+ by roots, promoting the accumulation of Al3+ in surface soil via litter decomposition . The accumulation of Al3+ can replace the base cations such as Ca2+, Mg2+, K+, and Na+ and accelerate leaching, hence reducing the pH buffering capacity of top soil.
2.2.3 Microbial-mediated nitrification
For example, NH4+ transfers to NO3− along with the 2H+ release (NH4+ + 2O2 → NO3− + H2O + 2H+) . AOB, AOA, and fungi can participate in the process of nitrification . Nitrification includes the pathway of ammonia oxidation to hydroxylamine, the pathway of hydroxylamine oxidation to nitrite, and the pathway of nitrite oxidation to nitrate (Figure 1) . Ammonia can be oxidized by AOA or AOB to hydroxylamine via ammonia monooxygenase (amo). Hydroxylamine can be oxidized to nitrite by hydroxylamine oxidoreductase. Nitrite can be oxidized to nitrate by nitrite oxidoreductase.
2.2.4 Oxidation of sulfur-containing organics
Oxidation of sulfur mineral, for example, oxidation of FeS2, will produce 2H+ (2FeS2 + 7O2 + 2H2O → 2Fe2+ + 4SO42− + 4H+).
Oxidation of sulfur-containing organics will release 4H+ (2Organic-S + 3O2 + 2H2O → 2SO42− + 4H+).
2.2.5 Intensive nitrogen fertilization
Intensive NH4+ input can replace the base cations such as Ca2+, Mg2+, K+, and Na+ and accelerate leaching, reducing the pH buffering capacity of top soil . Hydrolysis of soil NH4+ will generate NH3 (gas) and consume an OH− (NH4+ + OH− = NH3↑ + H2O) .
Acidic fertilizers such as Ca(H2PO4)2 will gradually release H+, hence increasing soil acidification (Ca(H2PO4)2 → CaHPO4 + H3PO4, H3PO4 → H+ + H2PO4 → 2H+ + HPO42− → 3H+ + PO43−).
2.2.6 Acid deposition
Acid deposition (water-soluble acid gases such as CO2 and sulfur dioxide) and N deposition (especially NH4+-N) increased soil acidification . Precipitation with H+ can replace the soil base cations such as Ca2+, Mg2+, K+, and Na+, which directly reduce the soil pH buffering capacity .
2.2.7 Other factors
For example, deforestation and other land uses can reduce litter accumulation in surface soil, hence declining the accumulation of base cations such as Ca2+, Mg2+, K+, and Na+ that generate from litter decomposition .
2.3 Effects of soil acidification on nitrous oxide emissions
Acid soils have been facing an increased risk of acidification due to human activities, especially intensive N fertilization [47, 49, 62]. For example, after 6 years of application of 600 kg Urea-N ha−1 yr−1, soil pH was significantly decreased (soil pH in control and fertilization treatment was 5.1 and 4.9, respectively) from a tea plantation in Yixing City, Jiangsu Province, China . A meta-analysis of 1104 field data showed that a negative correlation between soil N2O emissions and pH (3.34–8.7) (N2O-N = −0.67x + 6.55, R = 0.22) is negatively related with N fertilization . Moreover, deposition of sulfur dioxide increased soil acidification, stimulating soil N2O emissions .
The mechanism of soil acidification on the stimulation of soil N2O emissions is complex, which may include (but not limited to) the following points.
2.3.1 Chemical decomposition of nitrous acid
Under acidic conditions, pH < 5.5, NO2− (HNO2, pKa = 3.3) will naturally decompose into NO and/or NO2 (3HNO2 ⇌ 2NO + HNO3 + H2O or 2HNO2 ⇌ NO + NO2 + H2O) . Soil NO can be further transformed to N2O with Fe2+ when it was not escaping soil .
2.3.2 Shifts in microbial communities and abundance
Generally, the abundance of AOB was lower in soil pH < 5.5 than that in neutral soil pH. Here, nitrification was weak and almost disappears at soil pH < 4 . However, AOA could mediate the process of ammonia oxidation in extremely strong acidity soil (pH: 4.2–4.47) . Another study reported that the abundance of AOB was positively correlated with pH (R2 = 0.2807), while the abundance of AOA was negatively correlated with pH (R2 = 0.2141) . For example, AOA dominated in acid paddy soil (pH 5.6), while AOB dominated in alkaline soil (pH 8.2) . Previous research indicated that fungi were the main microbial community that mediated N2O emissions in acid soil [69, 70]. Additionally, fungi-mediated denitrification accounted for 70% soil N2O emissions from a 100-year-old tea plantation (soil pH 3.8) .
In acid soils, the activity of N2O reductase was inhibited, leading to higher N2O emissions in lower soil pH . Indeed, there was a positive correlation between the abundance of nirS, nirK, or nosZ and soil pH (4.0–8.0) and a negative correlation between N2O/(N2O + N2) and soil pH . In agreement, N2O/(N2O + N2) was negatively correlated with soil pH (3.7–8.0) (R2 = 0.759, P < 0.001), and lime addition decreased N2O/(N2O + N2) . The ratio of N2O/(N2O + N2) increased with decreasing pH (5.57–7.06) (R2 = 0.82) . Consistently, soil pH was negatively correlated with N2O/N2 . Intensive management consistently decreased soil pH and increased the ratio of N2O/(N2O + N2) . Increasing dolomite dosage increased soil pH and hence increased the transcription of nosZ genes and reduced the potential of N2O production in acid soils .
2.3.3 Microbes increased resistance to soil acidification
Laboratory study showed that the potential of soil N2O emissions was increased with decreasing pH (soil pH ranging from 2.96 to 6.26) from tea plantations in Japanese . In addition, higher soil N2O emissions and lower abundance of nosZ genes were observed in soil pH at 3.71 (control) than in pH at 5.11, 6.19, and 7.41 (lime amelioration) under NO3−-N fertilization (50, 200, and 1000 mg kg−1) from a 100-year-old tea plantation . Field study found a negative correlation between soil N2O emissions and pH (pH 3.6–5.9) (N2O-N = 636.6* e−0.8028 * pH, R = −0.93) from Betula pendula Roth forest . Thus, denitrifying microorganisms may have been adapted extremely to acid soil environments, resulting in high N2O emissions when soil acidification happened.
3. Sustainable forest management
Soil amelioration (e.g., application of lime, biochar nitrification inhibitors, and urease inhibitors) plays an important role in mitigation of soil acidification and N2O emissions.
Lime as an ameliorant was often used to amend acid soils in southern China due to increasing soil pH. It can relieve the toxic effect of soil Al3+ on plant growth by reducing soil exchangeable H+ . Lime addition increased soil pH and salt saturation . In addition, application of lime can reduce soil N2O emissions . For example, under 60% WFPS or flooded conditions, dolomite addition at medium- or high-dose levels (1 or 2 g kg−1 soil) can reduce N2O emissions and increase the transcription of nosZ genes (N2O → N2) by increasing acid soil pH from a rice-rapeseed rotation system . However, lime addition reduced the content of soluble organic carbon in the soil layer 10–30 cm . Consistently, long-term lime addition increased the soil pH but stimulated the decomposition of soil organic carbon .
Biochar was stable in the soil from Amazon basin of Brazil, and biochar input improved soil fertility . This discovery accelerated the development of technologies for biochar application in soil amelioration.
Biochar is a carbon (C)-rich solid material by pyrolyzing of organic biomass such as crop straw, forestry by-products, urban waste, industrial by-products, animal manure, and urban sludge at low oxygen and high temperature (250–700°C) condition . Biochar has been characterized by a high pH, specific surface area, degree of aromatization, and porosity. In addition, biochar is rich in C-containing functional groups (e.g., C–H, C–O, C=C and C=O) and relatively stable organic C. The physicochemical properties of biochar were mainly determined by pyrolysis temperature .
Presently, biochar was widely used as a soil ameliorant in agriculture and forestry field. For example, our previous studies reported that C. oleifera fruit shells are ideal feedstock for producing biochar as they are rich in C and N [1, 88]. Biochar includes the following advantages:
Carbon recalcitrance of biochar can increase soil C pool. The potential of biochar in mitigation of greenhouse gas emissions was 1.0–1.8 Pg CO2-Ceq yr−1 .
Biochar had excellent physicochemical characteristics in soil nutrient retention and utilization [90, 91] and water conservation . Additionally, biochar can increase the plant resistance to Al3+ toxicity , the clone of arbuscular mycorrhizal fungi, and crop yield [93, 94]. It can decrease continuous cropping obstacles such as root-knot nematode  and Ralstonia solanacearum .
Biochar is rich in macro- and microelements , which can reduce the dosage of fertilizer.
3.2.1 Effects of biochar on soil nitrous oxide emissions
The physicochemical properties of biochar and soil can interactively influence soil N2O emissions . However, the effects of biochar on soil N2O emissions varied, including positive effects , negative effects , and no effects .
Biochar addition increased soil N2O emissions with the release of N from biochar . By contrast, biochar reduced soil N2O emissions with (1) increased NO3−-N immobilization ; (2) increased copy numbers of nosZ gene [104, 105]; and (3) increased toxic effects of polycyclic aromatic hydrocarbons and other toxic substances (pyrolysis by-products) on N-cycle microorganisms .
3.2.2 Effects of biochar on soil pH buffer capacity
Biochar that increased soil pH buffer capacity may predominantly correlate with biochar riches in oxygen-containing functional groups in surface. The anions of weakly acidic functional groups can associate with H+, hence increasing soil pH. Meanwhile, exchangeable base cations can release into the solution, thus increasing soil pH buffer capacity [107, 108]. In addition, soluble silicon (Si) such as H3SiO4− (present at a high pH) can combine with H+ and generate H2SiO3 precipitation [107, 108].
3.3 Nitrification inhibitor
Nitrification inhibitors are a class of organic compounds that can inhibit the activity of nitrifying bacteria.
Nitrification inhibitors, especially synthetic nitrification inhibitors (e.g., dicyandiamide (DCD) and 3,4-dimethylpyrazole phosphate (DMPP)), were widely used in agriculture for improving N use efficiency. Ammonia-oxidizing bacteria and AOA are the major microbial communities in nitrification and denitrification, and both contain amo enzyme that can catalyze ammonia oxidation (NH4+-N → NH2OH). Synthetic nitrification inhibitors such as DCD and DMPP mainly inhibit nitrification by suppressing the activity of amo enzyme (a Cu-copper cofactor enzyme). In addition, biological nitrification inhibitors also can inhibit soil nitrification [109, 110]. In the mid-1980s, researchers found that Brachiaria humidicola cv. Tully (CIAT 679), a single community forage, had lower nitrification rates than a single legume community or bare land . This phenomenon stimulated further studies on biological nitrification inhibitors. The first biological nitrification inhibitor (methyl 3-(4-hydroxyphenyl) propionate: MHPP) was identified from the root exudate of Sorghum bicolor in 2008, which mainly inhibited the activity of amo enzyme . Subsequently, biological nitrification inhibitor (brachialactone) from the root exudate of Brachiaria humidicola was found to inhibit the activity of amo enzyme . The Nanjing Soil Research Institute of China firstly found and identified a biological nitrification, 1,9-decanediol, from the root exudate of rice, which can inhibit the activity of amo enzyme .
Ammonium N can be adsorbed by soil colloids, while soil NO3−-N (the end product of nitrification) easily can be leached to groundwater by precipitation. In addition, microbial-mediated nitrification is closely related with soil N2O emissions [20, 21, 22]. Nitrification inhibitors can effectively inhibit soil nitrification, slowing the transformation of NH4+-N to NO3−-N and hence reducing the NO3−-N leaching and N2O emissions.
An evaluation from 62 field studies showed that although nitrification inhibitors increased 20% NH3 emissions, they reduced 48% inorganic N leaching, 44% N2O emissions, and 24% NO emissions and increased 58% plant N utilization, 9% grain yield, 5% straw yield, and 5% vegetable yield . Consistently, other studies evaluated that nitrification inhibitors decreased by 38% , 50% , or 73%  N2O emissions and decreased by 0.3 t CO2e ha−1 yr−1 . Similarly, DCD did not increase crop yields but reduced 35% N2O emissions . A meta-analysis showed that DCD rather than DMPP significantly increased 6.5% crop yield as well as DCD and DMPP decreased N2O emissions by 44.7% and 47.6%, respectively .
Therefore, application of nitrification inhibitors could reduce N2O emissions and mitigate environmental pollution after intensive N inputs.
3.4 Urease inhibitors
Urease inhibitors are a class of compounds that can slow soil urease activity (Figure 2). Addition of urease inhibitors after urea input can inhibit the hydrolysis of urea via inhibiting the activity of urease, hence reducing NH3 volatilizations and N2O emissions. Additionally, the application of urease inhibitors also contributes to increase N utilization efficiency and reduce NO3−-N leaching. N-(n-butyl)thiophosphoric triamide (NBPT) is one of the most wide and effective urease inhibitors.
Urease, a Ni-copper enzyme, has two Ni−O bidentate ligands, specifically catalyzing urea into NH3 and CO2. Urea only can bind with one specific Ni−O ligand of urease, but NBPT can bind with two Ni−O bidentate ligands of urease and generate a tridentate ligand , hence inhibiting the activity of urease.
Presently, a meta-analysis reported that a nonlinear response was presented in soil NH3 volatilizations and N input . Application of NBPT can effectively inhibit NH3 volatilizations. For example, 530 mg NBPT kg−1 urea treatment delayed NH3 volatilizations and decreased accumulation of NH3 volatilizations compared with the control treatment. NH3 volatilizations were linearly related with the NBPT dosage in the range of 0–1000 mg NBPT kg−1 Urea (0, 530, 850, 1500, and 2000 mg NBPT kg−1 Urea) . Other study reported that NBPT increased 27% oat yield and 33% crop N uptake .
The effects of NBPT on N2O emissions were controversial. For example, NBPT can reduce 80% N2O emissions . No effects of NBPT (0.07%, NBPT/Urea-N, w/w) on N2O emissions were observed . Similarly, there was no change of N2O emissions with NBPT (250 mg NBPT kg−1 Urea) addition from urea-fertilized (50 kg Urea-N ha−1) soil .
Additionally, NBPT can reduce N2O emissions from alkaline soils but has no effects on acidic soils , which indicated that pH plays a key role in the regulation of NBPT effects on N2O emissions. Further laboratory study showed that NBPT inhibited nitrification, stimulating N2O emissions from alkaline soils (pH 8.05) but not affecting N2O emissions from acid soils (pH 4.85). This finding suggested that the effect of NBPT on soil N2O emissions is not only influenced by pH but also by other unknown factors .
Generally, urease inhibitors correlated with nitrification inhibitor could mitigate N2O emissions. A meta-analysis showed that urease inhibitors and nitrification inhibitors interactively reduced 30% N2O emissions . For example, a field study reported that the combination of NBPT (0.3%, NBPT/Urea-N, w/w) and DCD (0.3%, DCD/Urea-N, w/w) reduced 32.1% soil N2O emissions with the addition of 519 kg Urea-N ha−1 from banana plantation, but did not affect the yield of banana .
4. Sustainable management in Camellia oleifera plantations
Our previous incubation study found that although biochar application increased N2O emissions, DCD addition decreased soil N2O emissions under urea fertilization from C. oleifera field . Our field study showed that N2O emission rates were inhibited by biochar or DCD application and the effects of biochar application on mitigation of cumulative N2O were comparable to DCD addition in C. oleifera plantations . Compared with control treatment, available N (NH4+-N and NO3−-N) was not affected by NH4NO3, NH4NO3 + DCD, or NH4NO3 + biochar treatment . In addition, the seed yield of C. oleifera was higher in NH4NO3 or NH4NO3 + biochar treatment than that in control or NH4NO3 + DCD treatment (Figure 3). Soil amelioration is necessary and improves N use efficiency and pH, mitigating N2O emissions. Soil amelioration plays an important role in the sustainable management of oil safety in C. oleifera plantations.
Soil acidification, especially induced by N fertilization, will inhibit the activity of N2O reductase and increase the abundance of N2O-producing fungi as well as the acid resistance of N2O-producing microorganisms, hence the ratio of N2O/(N2O + N2). In addition, NO2− will generate NO under soil pH < 5.5 condition, which will further transform into N2O. Under the background of global acidification, the soil from C. oleifera forest also suffers the potential risks of soil acidification and N2O emissions. Mitigation of soil acidification and N2O emissions by soil amelioration is necessary and improves N use efficiency and soil pH from C. oleifera plantations. Soil amelioration such as biochar and nitrification inhibitor plays an important role in sustainable forest management in C. oleifera plantations.
The National Natural Science Foundation of China (grant number: 41967017 and 41501317), Jiangxi and China Postdoctoral Science Foundation (grant number: 2017M106153 and 2017KY18), and Jiangxi Education Department (Project Number: GJJ160348) support this work.
Conflict of interest
The authors declare no conflict of interest.