Soil carbon sequestration, plant nutrients and biological activities affected by organic farming system in tea (Camellia sinensis (L.) O. Kuntze) fields

Abstract

There is growing interest in investigations into soil carbon (C) sequestration, plant nutrients and biological activities in organic farming since it is regarded as a farming system that could contribute to climate mitigation and sustainable agriculture. However, most comparative studies have focused on annual crops or farming systems with crop rotations, and only a few on perennial crops without rotations, e.g. tea (Camellia sinensis (L.) O. Kuntze). In this study, we selected five pairs of tea fields under organic and conventional farming systems in eastern China to study the effect of organic farming on soil C sequestration, plant nutrients and biological activities in tea fields. Soil organic C, total nitrogen (N), phosphorus (P), potassium (K) and magnesium (Mg), available nutrients, microbial biomass, N mineralization and nitrification were compared. Soil pH, organic C and total N contents were higher in organic tea fields. Soil microbial biomass C, N and P, and their ratios in organic C, total N and P, respectively, net N mineralization and nitrification rates were significantly higher in organic fields in most of the comparative pairs of fields. Concentrations of soil organic C and microbial biomass C were higher in the soils with longer periods under organic management. However, inorganic N, available P and K concentrations were generally lower in the organic fields. No significant differences were found in available calcium (Ca), Mg, sodium (Na), iron (Fe), manganese (Mn), copper (Cu) and zinc (Zn) concentrations between the two farming systems. These findings suggest that organic farming could promote soil C sequestration and microbial biomass size and activities in tea fields, but more N-rich organic fertilizers, and natural P and K fertilizers, will be required for sustainable organic tea production in the long term.

Key words:

• carbon sequestration
• conventional farming
• microbial biomass
• organic farming
• tea

INTRODUCTION

There is growing interest in soil carbon (C) sequestration, plant nutrients and biological activities in organic farming since it is regarded as a farming system that could contribute to climate mitigation and sustainable agriculture. Organic farming systems are not permitted to use synthetic chemicals, such as inorganic fertilizers and chemical pesticides; instead crop rotation with legumes, green manures and compost are applied, and biological pest control systems are adopted. Many studies have shown that organic farming could improve soil health and productivity by increasing soil organic C, plant nutrients, biodiversity, microbial activities and even higher food supply compared to conventional farming systems (e.g. Mäder et al. 2002; Gosling and Shepherd 2005; Badgley et al. 2007; Fließbach et al. 2007; Leifeld and Fuhrer 2010; Gattinger et al. 2012). For example, Gattinger et al. (2012) found significant increases in organically farmed soils of 0.18% soil organic C concentrations, equivalent to 3.50 ± 1.08 million gram (Mg) C ha^–1 for organic C stocks, and 0.45 ± 0.21 Mg C ha^–1 y^–1 for sequestration rates compared with conventional management. These results were obtained from a meta-analysis of the data from 74 comparisons of organic vs. nonorganic farming systems. Fließbach et al. (2007) found that soil microbial biomass concentration and dehydrogenase activity were significantly higher, but the specific respiration rate lower in organic farming system than in conventional farming systems. Badgley et al. (2007) estimated, from model estimations, that organic farming could produce enough food on a global per capita basis to sustain the current human population, and potentially an even larger population, without increasing the agricultural land base. But other studies have not found such differences, and obtained opposite results (Kirchmann et al. 2007; Connor 2008; Leifeld et al. 2009; Leifeld 2012). Because of these contradictory findings, the advantages and disadvantages of organic farming systems vs. conventional farming systems remain controversial (Kirchmann et al. 2007; Leifeld and Fuhrer 2010; Leifeld 2012). These studies mainly focused on annual crops or on crop rotations, and there have been few studies on perennial crops without rotation in tropical and subtropical zones.

Tea (Camellia sinensis (L.) O. Kuntze) is a major cash crop and plays a very important role in both economic development and poverty reduction in tropical and subtropical regions. There were about 3.85 million ha of land under tea cultivation in the world in 2011 (ITC 2012). Tea is regarded as a healthy drink and public concerns over environmental health, food quality and safety have led to an increasing interest in organic farming practices. Organic tea production has increased very rapidly in China in the last decade. About 45,000 ha of tea fields were under organic management, with production of 35,000 tons in China in 2011. This represents an increase of 33 times in area and 43 times in production compared with that in 2000. Tea is a perennial crop and no crop rotation takes place in tea fields. Tea is also a leaf harvested crop and needs more nitrogen (N) than other crops with seeds or fruits as final products. N is a leading limiting factor for plant growth and tea productivity. However, long-term and over application of N leads to soil acidification. Tea is an unusual crop because the soil becomes strongly acidified following planting of tea and soil pH generally continues to decrease with the increase of stand age and tea productivity (Song and Liu 1990; Han et al. 2007a). Soil microbial biomass and activities are significantly affected by the productivity and the age of tea plants (Yao et al. 2000; Tokuda and Hayatsu 2002; Xue et al. 2006; Han et al. 2007a). However, there are no reports of changes of soil organic matter, plant nutrients, microbial biomass and activities in tea fields under organic management.

In this study, we collected soil samples from five locations, each with organic and conventional farming systems with different soil characteristics and durations of organic farming practices, in the Zhejiang province, eastern China. The main objectives were to evaluate the changes in soil organic C, total N, phosphorus (P) and potassium (K), available nutrients, microbial biomass, net N mineralization and nitrification under organic tea farming system. The aim was to provide new information on soil C sequestration and microbial biomass size and activities under organic farming system of the perennial crop, tea, without rotation.

MATERIALS AND METHODS

Site characteristics

Soil samples were collected from five pairs of farms located in the Zhejiang province, eastern China. This region has a subtropical monsoon climate with a clear division of four seasons and abundant sunshine. The mean annual temperatures in the five locations are around 16.5 to 17.7°C, ranging from 2°C in January to 33°C in July, based on the last three decades from 1981 to 2010. The mean annual precipitation ranges from 1326 to 1720 mm. About three quarters of this rain falls during the tea growing season from March to September. The soils are mainly red soils. Detailed information for the five tea farm locations is listed in Table 1.

Table 1 Selected information for the five experimental tea (Camellia sinensis (L.) O. Kuntze) fields located in Zhejiang province, China

Farm site	Site location	Mean annual temperature (°C)	Mean annual precipitation (mm)	Standing age of tea trees (years)	Year starting organic management	Soil parent material	Clay content (%)	US soil classification
Wuyi	119°59′ E 28°61′ N	16.9	1446	60	1996	Basalt	47.8	Ultisols
Yiwu	120°09′ E 29°47′ N	17.1	1326	50	1998	Sand stone	30.8	Ultisols
Shaoxin	120°71′ E 29°95′ N	16.5	1440	40	1999	Tuff	33.5	Ultisols
Lanxi	119°50′ E 29°14′ N	17.7	1440	30	2001	Quaternary clay	52.3	Oxisols
Jiangshan	118°50′ E 28°62′ N	17.1	1720	20	2004	Basalt	43.6	Oxisols

The selected farms have both organic and conventional tea gardens. The organic tea gardens were converted from conventional ones in different years. The farm of Shaoxin is a tea field undergoing conversion. It was also selected in order to investigate the changes in soil quality from conventional to organic management. The fertilizers applied in the organic and conventional systems are listed in Table 2. The organic fertilizers were applied twice a year in May and October in organic and conversional fields with 50% in each application. The mineral fertilizers were applied with four split dressings in February, May, July and October, and organic fertilizer was applied only in October in conventional fields. Soil tillage and weeding was done together with the application of organic fertilizers in both organic and conversional fields. No pesticides or bio-pesticides such as the nuclear polyhedrosis virus, Bacillus thuringiensis and matrine, or coloured sticky plates or frequency trembler grid lamps were used either in organic and conversional fields to control pests, and chemical pesticides were applied in conventional fields as required. Other field managements, such as pruning and plucking, were the same as applied locally.

Table 2 Fertilization employed and mean tea (Camellia sinensis (L.) O. Kuntze) productivity in organic and conventional tea fields at five farms studied

Farm	Management	Fertilizers and their quantities applied annually	Average yield after start of organicmanagement (kg ha^–1)
Wuyi	Organic	Commercial organic fertilizer 9000 kg ha^–1 for 11 years	4333
	Conventional	Commercial organic fertilizer 4500 kg ha^–1, mineral nitrogen (N), phosphorus pentoxide (P2O5) and potassium oxide (K2O) 600, 200 and 200 kg ha^–1, respectively	4667
Yiwu	Organic	Rape seed cake 4500 or compost 6000 kg ha^–1 for 9 years	2396
	Conventional	Rape seed cake 2250 kg ha^–1, mineral N, P2O5and K2O 450, 225 and 225 kg ha^–1, respectively	2605
Shaoxin	Organic	Compost 9000 kg ha^–1 for 8 years	1739
	Conversional	Compost 12000 kg ha^–1 for 2 years	1643
	Conventional	Compost 6000 kg ha^–1, mineral N, P2O5 and K2O 600, 300 and 300 kg ha^–1, respectively. Additional super phosphate applied sometimes	1819
Lanxi	Organic	Rape seed cake 4500 or compost 6000 kg ha^–1 for 6 years	2775
	Conventional	Compost 3000 kg ha^–1, mineral N, P2O5 and K2O 450, 225and 225 kg ha^–1, respectively	3150
Jiangshan	Organic	Compost 6000 kg ha^–1 for 3 years	2510
	Conventional	Mineral N, P2O5 and K2O 450, 225 and 225 kg ha^–1, respectively	2987

Soil sampling and treatment

For each farm, 400 m² representative tea fields under organic, one under conversion (only in Shaoxin farm) and conventional management, respectively, were selected for soil sampling in September 2007. In each sampled field, three independent soil samples were taken using a soil auger between tea rows. Each independent sample consisted of eight random sub-samples of 0–20 cm depth and mixed. Samples were transported in plastic bags to the laboratory as soon as possible. Plant residues, roots, stones and obvious macrofauna were removed by hand, then the soil was sieved at field moisture < 2 mm and stored at 4°C before analysis. Sub-samples were air-dried and ground < 160 µm for chemical analysis. Soil dry matter (105°C, 24 h) and water holding capacity (WHC) were determined, then the bulk soils were adjusted to ca. 40% WHC and pre-incubated aerobically at 25°C in the dark with water and soda-lime for 7 d before analysis of microbial biomass, net N mineralization and nitrification.

Soil analysis

Soil pH was determined using a combined glass electrode in 1:1 [weight:volume (w/v)] ratio of soil with distilled water. Soil organic C (C_org) and total N (N_tot) were determined by a Vario Max CN Analyzer (Elementar Analysensysteme GmbH, Germany). Soil total P (P_tot) and K were determined following digestion with a mixed solution of hydrofluoric acid, perchloric acid and concentrated nitric acid (HF-HClO₄-HNO₃) by using inductively coupled plasma atomic emission spectroscopy (ICP-AES) (JAC IRIS/AP, Thermo Jarrell Ash Corporation, Franklin, USA). Soil available P were extracted by Bray-1 solution (0.03 M ammonium fluoride (NH₄F) + 0.025 M hydrochloric acid (HCl)) and available potassium (K), calcium (Ca), magnesium (Mg) and sodium (Na) by 1 M ammonium acetate (NH₄OAC), at a 1:10 soil-solution ratio for 0.5 h. Soil available iron (Fe), manganese (Mn), copper (Cu) and zinc (Zn) were extracted by 0.1 M HCl at a 1:5 soil-solution ratio for 1 h. These elements were analyzed by ICP-AES.

Soil microbial biomass C, N (expressed as ninhydrin-N) and P were determined by the fumigation-extraction method (Brookes et al. 1985; Vance et al. 1987; Wu et al. 1990). Three replicates of both fumigated and non-fumigated soils were extracted with 0.5 M potassium sulphate (K₂SO₄) for 30 min (1:4 soil:extractant ratio). Organic C was measured by automated liquid organic C analysis. Microbial biomass C (C_mic) was calculated from:

(1)

where E_c = [(organic C extracted from fumigated soil) minus (organic C extracted from non-fumigated soil)] and k_c = 0.45. Biomass ninhydrin-N (Nnin_mic) concentrations were measured colorimetrically (Joergensen and Brookes 1990; Amato and Ladd 1994). Microbial biomass phosphorus (P_mic) was determined by the method of Wu et al. (2000). Soil samples were extracted by Bray-1 solution with a soil to solution ratio of 1:4 (w/v) for 30 min. The P concentrations were determined colorimetrically at 710 nm. P_mic was calculated from

(2)

where Ep = (inorganic P (Pi) extracted from chloroform (CHCl₃) fumigated soil) minus (Pi extracted from non fumigated soil); kp (the fraction of soil microbial P extracted from soil following fumigation) = 0.4 and R = % of inorganic P recovered from a spike of added inorganic P extracted from a non fumigated soil (Brookes et al. 1982). R ranged from 5 to 99% in the tested soils.

N mineralization was determined by aerobic incubation of replicate portions of bulk soils at 25°C in drums containing distilled water and soda-lime. After 0, 7, 14, 21 and 35 d, sub-samples were extracted with 0.5 M K₂SO₄ for 30 min (soil:extractant ratio of 1:4) and analysed for mineral N (ammonium (NH₄⁺), nitrate (NO₃^–)) by Flow Injection Analysis (Skalar SAN⁺⁺ system, Netherlands). Net rates of N mineralization and nitrification were calculated from the changes in total mineral N and NO₃^–-N pool sizes, respectively, during the incubations.

All results are expressed on an oven-dry soil basis (105°C, 24 h) and are the means of three replicate analyses.

Statistical analyses

The data were subject to one-way and two-way analysis of variance (ANOVA) by SPSS 13 for Windows. One-way ANOVA was used to compute means and least significant differences (LSD) with different management systems as a factor in different farms, with the significance level set at p < 0.05. Two-way ANOVA was performed to test farm site and management system effects. All the figures are made by SigmaPlot 11.0 and exported in TIFF format.

RESULTS

Soil pH, organic C, total N, P, K and Mg

The soil pH, organic C, total N, P, K and Mg contents in the five tea farms with different management systems are listed in Table 3. The soil pH and the contents of organic C and total N were consistently higher in organic than in conventional fields, although most differences were not statistically significant due to high variation of soil samples. In the Shaoxin farm, the soil pH was 4.21 following organic management for 8 years, significantly higher than the pH of 3.86 under conventional management, and the conversion soil was midway at pH 4.05. The differences in organic C and total N between the organic and the conventional fields were statistically significant at Wuyi farm, the oldest field under organic management. A significant relationship was found between the percentage increases of soil organic C and age of tea fields under organic management (Fig. 1). On average, the organic C and total N in organic fields were increased by 7.2 and 7.7%, respectively, compared with the conventional fields. However, the total P was quite different and higher in most of the conventional fields. In the Shaoxin and Wuyi sites, a significant difference was found due to superphosphate applied in the conventional fields. The soil total K and Mg concentrations in the different managements were not significantly different though a little lower in organic fields in most pairs of soils.

Table 3 Soil pH, organic carbon (C), total nitrogen (N), phosphorus (P), potassium (K) and magnesium (Mg) contents in the fields under different management systems in five farms

Farm (F)	Management (M)	pH (H2O)	Organic C (g kg^–1)	Total N (g kg^–1)	Total P (g kg^–1)	Total K (g kg^–1)	Total Mg (g kg^–1)
Wuyi	Organic	3.86 ± 0.11	19.1 ± 0.3 a	1.89 ± 0.04 a	0.56 ± 0.03 a	7.66 ± 0.20	1.91 ± 0.10
	Conventional	3.53 ± 0.07	17.5 ± 0.2 b	1.70 ± 0.02 b	0.73 ± 0.03 b	7.93 ± 0.16	2.05 ± 0.07
Yiwu	Organic	4.40 ± 0.30	14.2 ± 0.8	1.23 ± 0.09	0.57 ± 0.08	8.00 ± 0.05	2.17 ± 0.10
	Conventional	3.72 ± 0.12	13.3 ± 1.5	1.00 ± 0.06	0.50 ± 0.11	8.12 ± 0.19	2.19 ± 0.05
Shaoxin	Organic	4.21 ± 0.08 a	20.7 ± 1.7	1.63 ± 0.09	0.45 ± 0.07 a	10.51 ± 0.30	2.53 ± 0.05
	Conversional	4.05 ± 0.08 a	18.2 ± 1.5	1.47 ± 0.01	0.64 ± 0.08 a	10.62 ± 0.23	2.48 ± 0.03
	Conventional	3.86 ± 0.01 b	18.7 ± 0.4	1.53 ± 0.15	1.45 ± 0.12 b	11.23 ± 0.47	2.63 ± 0.14
Lanxi	Organic	3.95 ± 0.21	14.7 ± 0.6	1.15 ± 0.15	1.07 ± 0.33	7.71 ± 0.12	1.88 ± 0.03
	Conventional	3.73 ± 0.24	14.3 ± 3.6	1.20 ± 0.10	1.57 ± 0.02	7.87 ± 0.02	1.88 ± 0.03
Jiangshan	Organic	4.07 ± 0.05	9.6 ± 0.3	0.70 ± 0.00	0.36 ± 0.01	7.96 ± 0.25	4.22 ± 0.08
	Conventional	3.81 ± 0.08	9.3 ± 0.3	0.70 ± 0.00	0.35 ± 0.00	7.60 ± 0.51	4.07 ± 0.08
ANOVA test (F value)
Factor	F	2.30	20.84***	47.20***	23.58***	63.23***	221.33***
	M	12.23**	1.79	1.89	17.21***	0.00	0.09
	F × M	0.88	0.16	1.16	11.02***	0.56	1.23

Means are presented ± standard error (SE). The following different letters within a column in the same farm denote significant difference (p < 0.05) between field managements. The data of conversional management in Shaoxin farm were excluded during the two-way analysis of variance (ANOVA) test. *, **, *** after F value mean p < 0.05, 0.01 and 0.001, respectively.

Figure 1 Relationship between percentage increase in soil organic carbon (C) and age of tea (Camellia sinensis (L.) O. Kuntze) fields under organic management. The line is predicted relationship and points are % increases in soil organic C in the fields under organic management compared to the conventional management from the tested farms.

Soil available nutrients

The soil available P, K, Ca, Mg, Na, Fe, Mn, Cu and Zn concentrations in the tea fields with different management systems in five farms are listed in Table 4. Except for available K in Jiangshan farm, the available P and K concentrations were lower in the organic fields due to the application of chemical P and K fertilizers in the conventional fields. There were significant differences between conventional and organic systems in available P in Yiwu, Shaoxin, Lanxi and Jiangshan farms, and available K in Wuyi. The same trend did not occur in available Ca, Mg and Na concentrations. Significantly higher available Ca and Mg were found only in the conventional field of Wuyi, the longest under organic management. The concentrations of available Fe, Mn, Cu and Zn were generally higher in the organic fields than in the conventional fields. The Fe and Zn concentrations in the organic fields in Shaoxin farm were significantly higher as was the Cu concentration in Wuyi farm than the conventional fields. An opposite result also occurred in soils of Jiangshan farm, while the concentrations of Fe and Cu were significantly lower in the organic fields. However, two-way ANOVA test results showed no significant differences between organic and conventional farming systems for all these available metal elements (Table 4).

Table 4 Concentrations of available nutrients in the fields of different management systems in five farms (mg kg^–1)

Farm (F)	Management (M)	Phosphorus (P)	Potassium (K)	Calcium (Ca)	Magnesium (Mg)	Sodium (Na)	Iron (Fe)	Manganese (Mn)	Copper (Cu)	Zinc (Zn)
Wuyi	Organic	73.1 ± 15.1	64.7 ± 4.5 a	191.5 ± 2.5 a	20.0 ± 1.9 a	13.6 ± 1.0	39.8 ± 4.4	33.0 ± 3.7	2.65 ± 0.09 a	11.48 ± 1.42
	Conventional	104.1 ± 8.1	154.6 ± 3.3 b	230.6 ± 5.8 b	29.5 ± 1.5 b	12.6 ± 0.3	32.6 ± 1.5	35.6 ± 5.4	2.09 ± 0.11 b	8.12 ± 0.10
Yiwu	Organic	21.3 ± 4.9 a	66.2 ± 10.0	221.1 ± 12.3	38.9 ± 5.0	27.8 ± 4.3	37.5 ± 14.0	42.6 ± 15.0	2.62 ± 0.80	18.73 ± 5.34
	Conventional	113.5 ± 11.5 b	166.6 ± 44.6	325.1 ± 78.2	77.7 ± 35.1	32.7 ± 1.3	44.4 ± 21.4	17.5 ± 10.1	1.71 ± 0.04	16.45 ± 2.01
Shaoxin	Organic	14.4 ± 2.2 a	116.0 ± 6.1	274.5 ± 30.4	32.9 ± 2.1	27.9 ± 2.5	75.9 ± 4.7 a	89.1 ± 5.5	3.96 ± 0.20	11.22 ± 0.49 a
	Conversional	61.4 ± 11.0 b	92.1 ± 24.4	184.8 ± 48.3	35.2 ± 8. 4	28.8 ± 1.2	54.4 ± 21.2ab	65.2 ± 15.7	3.42 ± 0.88	11.70 ± 0.47 a
	Conventional	113.2 ± 22.1 c	146.5 ± 19.5	244.4 ± 26.6	50.1 ± 9.4	32.0 ± 1.4	25.2 ± 2.4 b	62.6 ± 4.6	2.44 ± 0.07	8.27 ± 0.35 b
Lanxi	Organic	19.4 ± 7.0 a	121.0 ± 13.0	268.1 ± 78.1	57.4 ± 15.5	33.8 ± 2.0	36.4 ± 5.3	33.7 ± 19.0	1.85 ± 0.06	16.61 ± 0.92
	Conventional	104.6 ± 16.4 b	139.0 ± 3.4	352.5 ± 65.8	37.7 ± 6.0	31.2 ± 1.1	37.0 ± 5.2	122.5 ± 57.7	4.00 ± 2.10	15.05 ± 3.95
Jiangshan	Organic	17.9 ± 1.5 a	282.1 ± 32.0	274.0 ± 49.6	74.0 ± 28.7	42.6 ± 7.0	21.6 ± 0.7 a	57.2 ± 12.1	1.62 ± 0.01 a	14.76 ± 2.48
	Conventional	26.1 ± 0.8 b	240.2 ± 9.3	214.7 ± 11.7	44.4 ± 2.3	34.6 ± 0.3	32.1 ± 1.4 b	20.8 ± 0.5	2.04 ± 0.01 b	9.09 ± 0.25
ANOVA test (F value)
Factor	F	6.83**	22.35***	1.42	1.71	41.85***	1.37	4.52*	1.90	4.31*
	M	40.71***	2.10	1.03	0.10	0.14	3.49	0.00	2.09	1.47
	F × M	12.10***	3.35*	1.34	1.45	2.94	2.74	4.36*	2.72	0.79

Means are presented ± standard error (SE). The following different letters within a column in the same farm denote significant difference (p < 0.05) between field managements. The data of conversional management in Shaoxin farm were excluded during the two-way analysis of variance (ANOVA) test. *, **, *** after F value mean p < 0.05, 0.01 and 0.001, respectively.

Microbial biomass C, N, P and their contribution to organic C, total N and P

The different management systems had great impacts on the size of the microbial communities in soils under tea cultivation (Fig. 2). Microbial biomass C, N and P in soils of organic fields were significantly higher than those in conventional fields in Wuyi and Shaoxin farms. There were also significant differences in biomass N and P in Yiwu farm, and biomass P in Lanxi farm. In other comparative pairs, the biomasses were all higher in organic fields although the differences were not statistically significant. This was so even at Jiangshan farm, where the organic management system was only employed for 3 years. There was a significant positive linear correlation between percentage increase in soil microbial biomass C and age of tea fields under organic management (Fig. 3).

Figure 2 Soil microbial biomass carbon (C), ninhydrin-nitrogen (N) and phosphorus (P) in tea (Camellia sinensis (L.) O. Kuntze) fields under different management systems. Vertical bars are standard errors. Different letters denote significant differences (p < 0.05) between management in the same farm. The analysis of variance (ANOVA) results are inset. S, experimental sites; M, management systems. The data of conversional management in Shaoxin farm were excluded during the two-way ANOVA test. *, **, *** after F value mean p < 0.05, 0.01 and 0.001, respectively.

Figure 3 Relationship between percentage increase in soil microbial biomass carbon (C) and age of tea (Camellia sinensis (L.) O. Kuntze) fields under organic management. The line is predicted relationship and points are % increases in soil microbial biomass C in the fields under organic management compared to the conventional ones from the tested farms.

The ratios of C_mic:C_org, Nnin_mic:N_tot and P_mic:P_tot under the different management systems are shown in Fig. 4. These ratios were higher in organic fields than in conventional ones. Significant or noticeable differences were found in Wuyi, Yiwu and Shaoxin farms, where the organic management system was employed for at least 8 years. These ratios in the conversion field in Shaoxin farm were mid-way between conventional and organic fields, indicating that the organic farming system had a positive impact on the size of the soil microbial communities.

Figure 4 Ratios of soil microbial biomass carbon (C), ninhydrin-nitrogen (N) and biomass phosphorus (P) to organic C, total N and P, respectively, under the different management systems. Vertical bars are standard errors. Different letters denote significant differences (p < 0.05) between management in the same farm. The analysis of variance (ANOVA) results are inset. S, experimental sites; M, management systems. The data of conversional management in Shaoxin farm were excluded during the two-way ANOVA test. *, **, *** after F value mean p < 0.05, 0.01 and 0.001, respectively.

The results of two-way ANOVA with farm site and management system as factors also showed significant differences among sites and between farming systems. This indicates that organic farming could significantly increase the microbial biomass in tea fields (Figs. 2 and 4).

Net N mineralization and nitrification

The initial soil NH₄⁺, NO₃^– concentrations, net N mineralization and nitrification rates in the soils under different management systems are listed in Table 5. The initial NO₃^–-N concentrations were significantly lower in the soils of the organic tea fields compared to the conventional fields in all five farms. The NH₄⁺-N concentrations were also significantly lower in the Yiwu, Lanxi and Jiangshan farms under organic management due to the application of urea in the conventional fields. However, the soil net N mineralization and nitrification rates under organic management were higher in most of the comparative pairs. Opposite results were also found in Yiwu and Jiangshan farms with conventional fields having significantly higher nitrification rates. This was probably due to the significantly higher concentrations of NH₄⁺-N, the substrate of nitrification in these two fields.

Table 5 Soil net nitrogen (N) mineralization and nitrification rates under different management systems in five farms

Farm (F)	Management (M)	Initial ammonium(NH4^+)-N (mg kg^–1)	Initial nitrate (NO3^–)-N (mg kg^–1)	Mineralization rate (mg kg^–1 d^–1)	Nitrification rate (mg kg^–1 d^–1)
Wuyi	Organic	2.0 ± 0.2	13.8 ± 0.5 a	0.68 ± 0.07	1.03 ± 0.10 a
	Conventional	1.8 ± 0.4	52.6 ± 5.4 b	0.44 ± 0.09	0.59 ± 0.02 b
Yiwu	Organic	3.9 ± 0.2 a	35.8 ± 2.6 a	0.62 ± 0.06 a	0.54 ± 0.05 a
	Conventional	57.8 ± 5.3 b	130.0 ± 4.9 b	1.19 ± 0.18 b	1.93 ± 0.17 b
Shaoxin	Organic	2.3 ± 0.1	20.4 ± 2.8 a	1.35 ± 0.21 a	1.29 ± 0.20 a
	Conversional	2.4 ± 0.1	24.4 ± 2.8 a	0.79 ± 0.08 b	0.77 ± 0.08 b
	Conventional	2.5 ± 0.0	60.2 ± 10.0 b	0.69 ± 0.06 b	0.67 ± 0.06 b
Lanxi	Organic	17.8 ± 2.5 a	31.8 ± 3.5 a	1.44 ± 0.06 a	2.00 ± 0.07 a
	Conventional	38.5 ± 1.4 b	245.0 ± 29.2 b	1.15 ± 0.08 b	1.37 ± 0.08 b
Jiangshan	Organic	14.8 ± 1.6 a	35.9 ± 0.5 a	3.54 ± 0.20 a	2.67 ± 0.03 a
	Conventional	50.8 ± 1.8 b	144.5 ± 0.4 b	1.90 ± 0.09 b	3.20 ± 0.06 b
ANOVA test (F value)
Factor	F	115.9***	35.1***	120.9***	146.3***
	M	289.6***	237.6***	44.3***	0.6
	F × M	64.4***	24.6***	27.7***	40.2***

Means are presented ± standard error (SE). The following different letters within a column in the same farm denote significant difference (p < 0.05) between field managements. The data of conversional management in Shaoxin farm were excluded during the two-way analysis of variance (ANOVA) test. *, **, *** after F value mean p < 0.05, 0.01 and 0.001, respectively.

DISCUSSION

Soil pH and C sequestration

Soil pH is a primary regulator of soil nutrient cycling. There are few reactions involving soil or its biology that are not affected by soil pH, and this sensitivity must be recognized in any soil-management system. Higher soil pH is typically observed in organic compared to conventional management (Reganold et al. 1993; Clark et al. 1998; Fließbach et al. 2007). The present study is consistent with these findings. Soil pH in organic management was higher in all five comparative pairs, and there were significant differences between management types in a two-way ANOVA analysis (Table 3). It is understandable that organic fertilizers can increase soil buffering capacity and prevent pH swings in soils, but the chemical fertilizers, especially N fertilizers, cause soil acidification. The raising of soil pH is beneficial to balance nutrient availability and improve soil biodiversity, since pH in tea soils is too low and the pH of about 50% of tea soils is less than 4.5 in the typical tea-producing regions in China (Han et al. 2002).

Organic farming is believed to improve soil fertility by enhancing soil organic matter content. The present study demonstrated that soil organic C was significantly or observably higher in the soils under organic management. Soil organic C was increased by 7.2% compared to the conventional fields, expressed as a mean over the five comparable pairs. The mean organic matter content was 6.4% higher in organic managed fields than the conventional ones, calculated from a meta-analysis (Mondelaers et al. 2009). The current study also showed that the longer the field was held under organic management, the higher was the soil organic C. A significant relationship was found between the percentage increase in soil organic C and age of tea fields under organic management (Fig. 3). These results indicate that organic tea cultivation could improve soil C sequestration without the use of rotations. This could be attributed to the following mechanisms:

1. Higher organic C input rate. A meta-analysis showed that the highest C sequestration was achieved by those practices supplying the largest C inputs (Aguilera et al. 2013). Without manure application, organic C could decline by 14–22% in a 21-year long-term experiment (Fließbach et al. 2007). In this study, the organic tea fields received almost twice as much organic fertilizer as did the conventional fields.

2. Conservation tillage practices. No-tillage or reduced tillage could significantly promote C sequestration. No tillage showed an average increase of 11.4% in soil organic C and 0.44 Mg C ha^–1 yr^–1 in C sequestration rate (Aguilera et al. 2013).

3. Lower microbial biomass C specific respiration rate (SRR), defined as:

   (3)

• Compared to conventional farming systems, organic farming could cause a decrease of 21% in the specific respiration rate (Fließbach et al. 2007). Tea soil has a lower specific respiration rate than other soils growing vegetables, citrus, paddy and forest, which is also beneficial to C accumulation and soil quality improvement (Yao et al. 2000; Han et al. 2007a).

Soil total and available nutrients

Plant growth and ecosystem productivity are significantly affected by the availability of plant nutrients, with N, P and K being the main growth-limiting nutrients for plant production. N is stored in soil primarily in organic matter, from which it is mineralized to ammonium-N by the action of soil micro-organisms. Organic farms rely heavily on soil biological activity and crop rotation with legume crops to provide N to plants (Mäder et al. 2002; Tu et al. 2006; Fließbach et al. 2007; Moeskops et al. 2010). Tea is a leaf harvested mono perennial crop and large amounts of N fertilizer are applied in conventional tea fields (Tokuda and Hayatsu 2000; Han and Li 2002). However, chemical fertilizer is not permitted in organic tea fields. Therefore sufficient plant nutrients, particular N availability for tea growth and quality, are often a concern for organic tea producers. The present study showed that soil total N gradually increased due to the higher application rate of organic fertilizers. However, N availability, i.e. the mineral N concentration, was significantly lower in the soils of organic tea fields compared to that in the conventional fields, thought there is generally higher mineralization and nitrification rates in soils from organic fields. It was lowest in the Wuyi organic tea field, the farm under the longest organic management. The mean yield of organic tea fields was 10% lower than that of the conventional fields in this study (Table 2), indicating that the mineral N absorbed by tea plants was lower in the organic tea fields. These results show that the mineral N supply is insufficient in organic tea fields, though the soils receive a greater amount of organic fertilizers and have higher mineralization rates compared to the conventional fields. In addition, the total P and K and available P and K concentrations in organic fields were generally lower due to non-application of mineral fertilizers. Other studies also showed that organic management could utilize reserves of P and K, accumulated during conventional management (Oehl et al. 2002; Gosling and Shepherd 2005).

The available Ca, Mg, Na and Mn concentrations were the same in the two farming systems in our study. However, Clark et al. (1998) and Bulluck et al. (2002) reported that these elements were higher in organic farming systems. The difference is probably because the period under organic management in our study was insufficient since some available nutrients decreased after converting to organic management, but increased under longer periods of organic management (Coll et al. 2011). These results indicate that the low yield of organic tea is probably due to the limitation of available nutrients, especially N, P and K. Therefore, it is important in organic tea fields that a relatively large amount of N-rich organic fertilizers, and sufficient natural P and K fertilizers, should be applied in order to insure a sufficiently high yield in the long term.

Soil microbial biomass size and microbial activities

The soil microbial biomass is both a labile nutrient pool and an agent of transformation and cycling of organic matter and plant nutrients in soils. It is one of the most important soil organic fractions although comprising only a small proportion (typically 1–5%) of soil organic matter (Sparling 1997). It responds more rapidly to changes in soil management than soil organic matter and, consequently, may provide an early and sensitive indicator of soil quality change (Sparling 1992; Zagal 2009). The proportion of microbial biomass C relative to soil organic C has been used as an indicator of C availability (Insam and Domsch 1988; Yan et al. 2003) and can also provide an effective early indicator of the improvement or deterioration of soil quality. The present study showed that organic management can significantly increase soil microbial biomass C, ninhydrin-N and biomass P contents compared to conventional farming systems. More importantly, the ratios of C_mic:C_org, Nnin_mic:N_tot and P_mic:P_tot were significantly or noticeable higher in the organic fields than in the conventional ones. In the conversion field of Shaoxin, these ratios were mid-way between those in conventional and organic fields, indicating that changing from conventional to organic farming system increased the size of the microbial biomass. There was a significant positive relationship between the increase in soil microbial biomass C and age of tea fields under organic management (Fig. 4), These results are consistent with previous findings (Fließbach and Mäder 2000; Araujo et al. 2008; Coll et al. 2011), indicating that perennial tea crop under organic farming system can improve soil quality. The higher microbial size and ratios of C_mic:C_org, Nnin_mic:N_tot and P_mic:P_tot in the organic fields were attributed to higher organic matter contents and increasing soil pH (Yao et al. 2000; Han et al. 2007a). They were also attributed to no use of herbicides and pesticides (Muñoz-Leoz et al. 2011). Blagodatskaya and Anderson (1999) found that at soil pH 3, biomass C was only 0.5% of organic C, but it was 2.4% at pH 7. We found that the soil pH was significantly related to C_mic (r = 0.645, n = 33, p < 0.001) and the ratio of C_mic:C_org (r = 0.655, n = 33, p < 0.001), and total organic C was significantly related to C_mic (r = 0.510, n = 33, p < 0.01) and P_mic (r = 0.618, n = 33, p < 0.001). This may be related to the effects of soil pH on substrate availability for microorganisms. Several mechanisms may account for this:

1. Metabolic functions of the soil microorganisms may be impaired by lower soil pH, directly via proton toxicity or by larger concentrations of available toxic metals. A greater proportion of heavy metals are complexed on soluble organic matter at higher soil pHs. These heavy metals tend to become bioavailable and have increased toxicity as soil pH declines (Sanders 1983; Han et al. 2006, 2007b).

2. Low pH may cause changes in the chemical configuration and reactions of humic substances (Schnitzer 1980). Humic and fulvic acids aggregate at low pH because of hydrogen bonding, van der Waal’s interactions, interactions between π electrons of adjacent molecules and homolytic reactions between free radicals. At higher pH, these forces are weaker and increased ionization of carboxylic acids and phenolic hydroxyl groups cause particles to separate and repel each other, resulting in smaller and more oriented molecular arrangements (Schnitzer 1980).

3. Application of large amount of chemical fertilizers, especially N fertilizers, lowers soil pH, which decreases biomass concentrations (Nioh et al. 1993; Ge et al. 2010). Thus, the tea soil received three times the rate of N (1200 kg N ha^–1 as ammonium sulphate) yet contained only 17% of biomass C compared to the soil receiving standard N application (Nioh et al. 1993).

4. Tea roots exude large quantities of organic acids, such as oxalic acid, citric acid and malate. These contribute to localized acidification (Wang 1994), which suppresses the microbial biomass (Pandey and Palni 1996).

The microbial mineralization of soil organic matter, manure or litter to ammonium and nitrate are the principal sources of plant available N in organic farming systems since no inorganic N fertilizer is applied. It was estimated that 50% of crop N uptake on average in conventional systems is derived from fertilizers in the year of application with the remainder from mineralization of soil organic matter (Jarvis et al. 1996). In organic farming systems, with an absence of soluble fertilizers, the importance of mineralization in the supply of nutrients to plants is clearly increased. Therefore, the rates of mineralization and nitrification play a key role in the N cycle by making N available for plants and microbes in the soils (Fließbach and Mäder 2000). Not only the available N, but the available P and K in the soil solution pool are partly derived from the mineralization of soil organic matter and crop residues (Stockdale et al. 2002). The present study shows that soil net N mineralization and nitrification rates under organic management were higher than these in some of the fields under conventional management. However, the opposite results were also found in Yiwu and Jiangshan farms with conventional fields having significantly higher nitrification rates (Table 5). This is probably because the chemically N fertilized soils have a higher nitrification substrate, nitrifying activity and an accelerated growth of the nitrifying population (Chu et al. 2008; Gong et al. 2011; Han et al. 2012). In this study, we found these two farms had higher initial NH₄⁺-N compared to other sites, and the initial NH₄⁺-N concentration was significantly correlated with the nitrification rate (r = 0.683, n = 11, p < 0.05).

CONCLUSIONS

Soil pH, organic C and total N contents were higher in the organic fields mainly due to higher inputs of organic fertilizer and no chemical fertilizers used. The microbial biomass C, ninhydrin-N and biomass P, and the ratios of C_mic:C_org, Nnin_mic:N_tot, P_mic:P_tot, the net N mineralization and nitrification rates were significantly higher in the organic fields in most of the comparative pairs. The longer the field was under organic management, the more organic C and microbial biomass C were present. However, inorganic N, available P and K concentrations were generally lower in organic fields. No significant differences were found in available Ca, Mg, Na, Fe, Mn, Cu and Zn concentrations between the two farming systems. These findings suggest that organic farming could promote soil C sequestration and microbial biomass size and activities in tea fields without crop rotation, but more N-rich organic fertilizers, natural P and K fertilizers will be required for sustainable organic tea production in the long term.

ACKNOWLEDGMENTS

This work was supported by the National Natural Science Foundation of China (Project No. 41171218, 40771113), the Ministry of Science and Technology of China (No. 2011BAD01B02) and the Common Fund for Commodities (No. CFC/FIGT/04). We appreciate Prof PC Brookes in Rothamsted Research and Dr GV Pangga in University of the Philippines for their meaningful comments and suggestions.