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Soil Fertility and Biodiversity in Organic Farming 

Science v.296, n.5573, 31may02

Paul Mäder,1* Andreas Fliebach,,1 David Dubois,2 Lucie Gunst,2 Padruot Fried,2 Urs Niggli1

An understanding of agroecosystems is key to determining effective farming systems. Here we report results from a 21-year study of agronomic and ecological performance of biodynamic, bioorganic, and conventional farming systems in Central Europe. We found crop yields to be 20% lower in the organic systems, although input of fertilizer and energy was reduced by 34 to 53% and pesticide input by 97%. Enhanced soil fertility and higher biodiversity found in organic plots may render these systems less dependent on external inputs.

1 Research Institute of Organic Agriculture, Ackerstrasse, CH-5070 Frick, Switzerland.
2 Swiss Federal Research Station for Agroecology and Agriculture, Reckenholzstrasse 191, CH-8046 Zürich, Switzerland.
* To whom correspondence should be addressed. E-mail: paul.maeder@fibl.ch 

Intensive agriculture has increased crop yields but also posed severe environmental problems (1). Sustainable agriculture would ideally produce good crop yields with minimal impact on ecological factors such as soil fertility (2, 3). A fertile soil provides essential nutrients for crop plant growth, supports a diverse and active biotic community, exhibits a typical soil structure, and allows for an undisturbed decomposition. Organic farming systems are one alternative to conventional agriculture. In some European countries up to 8% of the agricultural area is managed organically according to European Union Regulation (EEC) No. 2092/91 (4). But how sustainable is this production method really? The limited number of long-term trials show some benefits for the environment (5, 6). Here, we present results from the 21-year "DOK" system comparison trial (bio-Dynamic, bio-Organic, and "Konventionell"), which is based on a ley rotation. The field experiment was set up in 1978 on a loess soil at Therwil, Switzerland [(7) and supporting online material). Two organic farming systems (biodynamic, BIODYN; bioorganic, BIOORG) and two conventional systems (using mineral fertilizer plus farmyard manure: CONFYM; using mineral fertilizer exclusively: CONMIN) are emulated in a replicated field plot experiment (table S1 and fig. S1). Both conventional systems were modified to integrated farming in 1985. Crop rotation, varieties, and tillage were identical in all systems (table S2).

We found nutrient input (N, P, K) in the organic systems to be 34 to 51% lower than in the conventional systems, whereas mean crop yield was only 20% lower over a period of 21 years (Fig. 1, Table 1), indicating an efficient production. In the organic systems, the energy to produce a crop dry matter unit was 20 to 56% lower than in conventional and correspondingly 36 to 53% lower per unit of land area (tables S4 and S5).


Fig. 1. Yield of winter wheat, potatoes, and grass-clover in the farming systems of the DOK trial. Values are means of six years for winter wheat and grass-clover and three years for potatoes per crop rotation period. Bars represent least significant differences (P < 0.05). 

Key: A=Winter Wheat Grain Yield (t dry matter ha-1), B=Potato Tuber Yield (t fresh matter ha-1), 
        C
=Grass-Clover Yield (t dry matter ha-1)


Table 1. Input of nutrients, pesticides, and fossil energy to the DOK trial systems. Nutrient input is the average of 1978-1998 for BIODYN, BIOORG, and CONFYM and 1985-1998 for CONMIN. Soluble nitrogen is the sum of NH4-N and NO3-N. The input of active ingredients of pesticides was calculated for 1985-1991. Energy for production of machinery and infrastructure, in fuel, and for the production of mineral fertilizer and pesticides has been calculated for 1985-1991.

KEY:
A = Total nitrogen (kg N ha1 year1), 
B = Soluble nitrogen (kg N ha1 year1), 
C = Phosphorus (kg P ha1 year1), 
D = Potassium (kg K ha1 year1), 
E = Pesticides (kg active ingredients ha1 year1), 
F = Energy (GJ ha1 year1)Farming Total Soluble nitrogen (kg N ha1 year1) 
	A	C	D	E	F	G
BIODYN 	99	34 	24 	158 	0 	12.8
BIOORG 	93 	31 	28 	131 	0.21 	13.3
CONFYM 	149 	96 	43 	268 	6 	20.9
CONMIN 	125 	125 	42 	253 	6 	24.1

Potato yields in the organic systems were 58 to 66% of those in the conventional plots (Fig. 1), mainly due to low potassium supply and the incidence of Phytophtora infestans. Winter wheat yields in the third crop rotation period reached an average of 4.1 metric tons per hectare in the organic systems. This corresponds to 90% of the grain harvest of the conventional systems, which is similar to yields of conventional farms in the region (8). Differences in grass-clover yields were small.

Cereal crop yields under organic management in Europe typically are 60 to 70% of those under conventional management, whereas grassland yields are in the range of 70 to 100%. Profits of organic farms in Europe are similar to those of comparable conventional farms (9). Appropriate plant breeding may further improve cereal yields in organic farming. There were minor differences between the farming systems in food quality (10).

The maintenance of soil fertility is important for sustainable land use. In our experimental plots, organically managed soils exhibit greater biological activity than the conventionally managed soils. In contrast, soil chemical and physical parameters show fewer differences (Fig. 2).


Fig. 2. Physical, chemical, and biological soil properties in soils of the DOK farming systems. Analyses were done within the plough horizon (0 to 20 cm) except for soil fauna. Results are presented relative to CONFYM (= 100%) in four radial graphs. Absolute values for 100% are as follows. (A) Percolation stability, 43.3 ml min1; aggregate stability, 55% stable aggregates > 250 µm; bulk density, 1.23 g cm3. (B) pH(H2O), 6.0; organic carbon, 15.8 g Corg kg1; phosphorus, 21.4 mg P kg1; potassium, 97.5 mg K kg1; calcium, 1.7 g Ca kg1; magnesium, 125 mg Mg kg1. (C) Microbial biomass, 285 mg Cmic kg1; dehydrogenase activity, 133 mg TPF kg1 h1; protease activity, 238 mg tyrosine kg1 h1; alkaline phosphatase, 33 mg phenol kg1 h1; saccharase, 526 mg reduced sugar kg1 h1; mycorrhiza, 13.4% root length colonized by mycorrhizal fungi. (D) Earthworm biomass, 183 g m2; earthworm abundance, 247 individuals m2; carabids, 55 individuals; staphylinids, 23 individuals; spiders, 33 individuals. Arthropods have not been determined in the CONMIN system because of the field trial design. Significant effects were found for all parameters except for bulk density, Corg, and potassium (analysis of variance; P < 0.05). For methods, see table S3. 


Soil aggregate stability as assessed by the percolation method (11) and the wet sieving method (12) was 10 to 60% higher in the organic plots than in the conventional plots (Fig. 2A). These differences reflect the situation as observed in the field (Fig. 3, A and B), where organic plots had a greater soil stability. We found a positive correlation between aggregate stability and microbial biomass (r = 0.68, P < 0.05), and between aggregate stability and earthworm biomass (r = 0.45, P < 0.05).


Fig. 3. Biodynamic (A) and conventional (B) soil surface in winter wheat plots. Earthworm casts and weed seedlings are more frequent in the biodynamic plot. Disaggregation of soil particles in the conventional plots leads to a smoother soil surface. Wheat row distance is 0.167 m. Source: T. Alföldi, Research Institute of Organic Agriculture [Forschungsinstitut für biologischen Landbau (FiBL)].


Soil pH was slightly higher in the organic systems (Fig. 2B). Soluble fractions of phosphorus and potassium were lower in the organic soils than in the conventional soils, whereas calcium and magnesium were higher. However, the flux of phosphorus between the matrix and the soil solution was highest in the BIODYN system (13). Soil microorganisms govern the numerous nutrient cycling reactions in soils. Soil microbial biomass increased in the order CONMIN < CONFYM < BIOORG < BIODYN (Fig. 2C). In soils of the organic systems, dehydrogenase, protease, and phosphatase activities were higher than in the conventional systems, indicating a higher overall microbial activity and a higher capacity to cleave protein and organic phosphorus (12). Phosphorus flux through the microbial biomass was faster in organic soils, and more phosphorus was bound in the microbial biomass (14, 15). Evidently, nutrients in the organic systems are less dissolved in the soil solution, and microbial transformation processes may contribute to the plants' phosphorus supply.

Mycorrhizae as members of the soil community ameliorate plant mineral nutrition and contribute to soil aggregate formation (16). Root length colonized by mycorrhizae in organic farming systems was 40% higher than in conventional systems (7) (Fig. 2C).

Biomass and abundance of earthworms were higher by a factor of 1.3 to 3.2 in the organic plots as compared with conventional (17) (Fig. 2D). We also investigated epigaeic arthropods that live above ground, because they are important predators and considered sensitive indicators of soil fertility. Average activity density of carabids, staphylinids, and spiders in the organic plots was almost twice that of the conventional plots (18) (Fig. 2D).

Healthy ecosystems are characterized by high species diversity. The DOK trial shows that organic farming allows the development of a relatively diverse weed flora. Nine to 11 weed species were found in organically managed wheat plots and one species in conventional plots. Between 28 and 34 carabid species were found in the BIODYN system, 26 to 29 species in the BIOORG system, and 22 to 26 species in the CONFYM system (18). Some specialized and endangered species were present only in the two organic systems. Apart from the presence and diversity of weeds, direct effects of pesticides and the density of the wheat crop stand are most likely influencing arthropod activity and diversity.

One of the particularly remarkable findings, presented in Fig. 4, was a strong and significant increase in microbial diversity (BIOLOG Inc., Hayward, CA) in the order CONMIN, CONFYM < BIOORG < BIODYN, and an associated decrease in the metabolic quotient (qCO2) (19). According to Odum's theory on the strategy of ecosystem development, the ratio of total respiration to total biomass decreases during succession in an ecosystem (20). This quotient has been adapted to soil organisms (21), where CO2 evolution is a biological process mainly governed by microorganisms. The lower qCO2 in the organic systems, especially in the BIODYN system, indicates that these communities are able to use organic substances more for growth than for maintenance.


Fig. 4. Soil microbial functional diversity (Shannon index H') and metabolic quotient (qCO2 = soil basal respiration/soil microbial biomass) correlate inversely. A higher diversity in the organic plots is related to a lower qCO2, indicating greater energy efficiency of the more diverse microbial community. The Shannon index is significantly different between both conventional systems (CONFYM, CONMIN) and the BIODYN system, the qCO2, between CONMIN and BIODYN (P < 0.05). 


Under controlled conditions, the diverse microbial community of the BIODYN soil decomposed more 14C-labeled plant material than the ones of the conventional soils (22). In the field, light fraction particulate organic matter, indicating undecomposed plant material, decayed more completely in organic systems (23). Hence, microbial communities with an increased diversity in organic soils transform carbon from organic debris into biomass at lower energy costs, building up a higher microbial biomass. Accordingly, the functional role of diverse plant communities in soil nitrate utilization has been quoted (24), as well as the significance of mycorrhizal diversity for phosphorus uptake and plant productivity (25). The consistent results of these two studies (24, 25) and our own within the soil-plant system support the hypothesis that a more diverse community is more efficient in resource utilization. The improvement of biological activity and biodiversity below and above ground in initial stages of food webs in the DOK trial is likely to provide a positive contribution toward the development of higher food web levels including birds and larger animals.

The organic systems show efficient resource utilization and enhanced floral and faunal diversity, features typical of mature systems. There is a significant correlation (r = 0.52, P < 0.05) between above-ground (unit energy per unit crop yield) and below-ground (CO2 evolution per unit soil microbial biomass) system efficiency in the DOK trial. We conclude that organically manured, legume-based crop rotations utilizing organic fertilizers from the farm itself are a realistic alternative to conventional farming systems.

REFERENCES AND NOTES

1. D. Pimentel, et al., Science 267, 1117 (1995) .

2. D. Tilman, Proc. Nat. Acad. Sci. U.S.A. 96, 5995 (1999) [Abstract/Full Text].

3. D. Pimentel, et al., Bioscience 47, 747 (1997) .

4. www.organic.aber.ac.uk/stats.shtml 

5. L. E. Drinkwater, P. Wagoner, M. Sarrantonio, Nature 396, 262 (1998) .

6. J. P. Reganold, J. D. Glover, P. K. Andrews, H. R. Hinman, Nature 410, 926 (2001) [Medline].

7. P. Mäder, S. Edenhofer, T. Boller, A. Wiemken, U. Niggli, Biol. Fertil. Soils 31, 150 (2000) .

8. P. Simon, Landwirtschaftliches Zentrum Ebenrain, CH-4450 Sissach/BL, personal communication.

9. F. Offermann, H. Nieberg, Economic Performance of Organic Farms in Europe (University of Hohenheim, Hago Druck & Medien, Karlsbad-Ittersbach, Germany, 2000), vol. 5.

10. T. Alföldi et al., unpublished observations.

11. S. Siegrist, D. Schaub, L. Pfiffner, P. Mäder, Agric. Ecosys. Environ. 69, 253 (1998) .

12. F. Schinner, R. Öhlinger, E. Kandeler, R. Margesin, Bodenbiologische Arbeitsmethoden (Springer Verlag, Berlin Heidelberg, ed. 2, 1993).

13. A. Oberson, J.-C. Fardeau, J.-M. Besson, H. Sticher, Biol. Fertil. Soils 16, 111 (1993) .

14. A. Oberson, J.-M. Besson, N. Maire, H. Sticher, Biol. Fertil. Soils 21, 138 (1996) .

15. F. Oehl, et al., Biol. Fertil. Soils 34, 31 (2001) .

16. S. E. Smith, D. J. Read, Mycorrhizal Symbiosis (Academic Press, London, ed. 2, 1997).

17. L. Pfiffner and P. Mäder, Biol. Agric. Hortic. 15, 3 (1997) .

18. L. Pfiffner and U. Niggli, Biol. Agric. Hortic. 12, 353 (1996) .

19. A. Fliebach, P. Mäder, in Microbial Communities--Functional versus Structural Approaches, H. Insam, A. Rangger, Eds. (Springer, Berlin, 1997), pp. 109-120.

20. E. P. Odum, Science 164, 262 (1969) [Medline].

21. H. Insam and K. Haselwandter, Oecologia 79, 174 (1989) .

22. A. Fliebach, P. Mäder and U. Niggli, Soil Biol. Biochem. 32, 1131 (2000) .

23. A. Fliebach, P. Mäder, Soil Biol. Biochem. 32, 757 (2000) .

24. D. Tilman, D. Wedin, J. Knops, Nature 379, 718 (1996) .

25. M. G. A. van der Heijden, et al., Nature 396, 69 (1998) .

26. We sincerely thank all co-workers in the DOK trial, especially W. Stauffer and R. Frei and the farmer groups. We also thank T. Boller and A. Wiemken and two unknown referees for their helpful comments. This work was supported by the Swiss Federal Office for Agriculture and the Swiss National Science Foundation. 

Fig. Sl. DOK field trial design: treatments under study.

Crop 1998

CONFYM BIOORG BIODYN CONMIN grass-clover ley
CONFYM BIOORG BIODYN CONMIN beetroots
CONFYM BIOORG BIODYN CONMIN winter wheat
BIODYN CONMIN CONFYM BIOORG beetroots
BIODYN CONMIN CONFYM BIOORG winter wheat
BIODYN CONMIN CONFYM BIOORG grass-clover ley
BIOORG CONFYM CONMIN BIODYN winter wheat
BIOORG CONFYM CONMIN BIODYN grass-clover ley
BIOORG CONFYM CONMIN BIODYN beetroots
CONMIN BIODYN BIOORG CONFYM grass-clover ley
CONMIN BIODYN BIOORG CONFYM beetroots
CONMIN BIODYN BIOORG CONFYM winter wheat

Table S1. Main differences between the farming systems of the DOK trial. The CONMIN plots remained unfertilized during the first crop rotation (1978–1984). The biodynamic preparations (P) consist of the following: P 500: cow-manure fermented in a cow horn; P 501: silica fermented in a cow horn. These were applied at rates of 250 and 4 g ha–1 respectively. Composting additives are yarrow flowers (P 502, Achillea millefolium, L.), camomile flowers (P 503, Matricaria recutita, L.), stinging nettle (P 504, Urticaria dioica, L.), oak bark (P 505, Quercus robur, L.), dandelion flowers (P 506, Taraxacum officinale, Wiggers), and valerian flowers (P 507, Valeriana officinalis, L.). A decoction of field horsetail (Equisetum arvense, L.) is applied once during the vegetative growth of wheat and potatoes as a protective agent against plant diseases at rates of 1.5 kg ha–1. Herbicides (1 to 2 treatments yr–1). Fungicides (2 to 3 treatments yr–1) based on threshold values, plant growth regulators were applied routinely to winter wheat. Insect control was required regularly in potatoes and rarely in winter wheat.

											.
Farming systems 		Organic systems 		Integrated systems
			biodynamic	bioorganic	with manure	without manure	
			BIODYN		BIOORG		CONFYM		CONMIN		
Fertilization		composted FYM	rotted FYM and	stacked FYM	
Farmyard		and slurry	aerated slurry	and slurry			
manure (FYM)										
Livestock units		1.4 		1.4 		1.4 		
per ha											
Mineral fertilizers	small amounts 	NPK fertilizer	exclusively	
					of rockdust,	as supplement	mineral NPK	
					K Magnesia					.
Plant protection	 								
Weed control		mechanical 	mechanical 	mechanical and	mechanical and	
							herbicides	herbicides	
Disease control 	indirect  	indirect 	fungicides	fungicides	
			methods		methods, CuSO4 	(thresholds)	(thresholds)	
					on potatoes 					
					until 1991					
Insect control 		plant extracts,	plant extracts,	insecticides	insecticides	
			biocontrol	biocontrol	(thresholds)	(thresholds)	.
Special			biodynamic			plant growth	plant growth	
treatments		preparations			regulators	regulators	.


Table S2. The crop rotation in the DOK field trial
									        .
Year 		1978–1984 		1985–1991 		1992–1998       .
	1.Crop rotation period	2.Crop rotation period  3.Crop rotation period  .
1 	   Potatoes 		   Potatoes 		   Potatoes		.
	   Green manure 	   Green manure					.
2 	   Winter wheat 1 	   Winter wheat 1 	   Winter wheat 1	.
	   Fodder intercrop 	   Fodder intercrop 	   Fodder intercrop	.
3 	   White cabbage 	   Beetroots 		   Beetroots		.
4 	   Winter wheat 2 	   Winter wheat 2 	   Winter wheat 2	.
5 	   Winter barley 	   Winter barley 	   Grass-clover 1	.
6 	   Grass-clover 1 	   Grass-clover 1 	   Grass-clover 2	.
7 	   Grass-clover 2 	   Grass-clover 2	   Grass-clover 3	.

Table S3. Methods for determining soil fertility (methodological information to accompany Fig. 2 in the text.)

										           .
Method 			Crop, year of the study 	Reference                          .
Percolation stability 	winter wheat, 1993 		water percolation rate with soil
							aggregates 1 to 2 mm               .
Aggregate stability 	winter wheat, 1999 		stable aggregates > 250 µm after
							wet sieving                        ..
Bulk density 		winter wheat, 1991 		weight of an undisturbed soil   
							sample                             .
pH 			winter wheat, 1998 		in water suspension (1:10; wt/vol) .
Organic carbon 		winter wheat, 1998 		wet oxidation			   .
Phosphorus 		winter wheat, 1998 		double lactic acid extract	   .
Potassium 		winter wheat, 1998 		double lactic acid extract	   .
Calcium 		winter wheat, 1998 		HCl/H2SO4-extract		   .
Magnesium 		winter wheat, 1998 		double lactic acid extract	   .
Microbial biomass 	winter wheat, 1998 		chloroform fumigation extraction   .
Dehydrogenase		winter wheat, 1998 		reduction of 2,3,5-
activity						triphenyltetrazolium chloride
							(TTC) to triphenyl formazan (TPF)  .
Protease activity 	winter wheat, 1991 		casein hydrolization		   .
Alcaline phosphatase	winter wheat, 1991 		hydrolysis of phenylphosphate
activity										   .
Saccharase activity 	winter wheat, 1991 		hydrolysis of sucrose              .
Mycorrhiza 		winter wheat,			percentage of root length colonized
			grass-clover, 1989–1993		by mycorrhizal fungi		   .
Earthworm biomass 	winter wheat, beetroots,
			potatoes, 1990, 1991, 1992	hand sorting                       .
Earthworm abundance 	winter wheat, beetroots,
			potatoes, 1990, 1991, 1992	hand sorting and classification    .
Carabid activity	winter wheat, 1988, 1990, 	pit fall trapping
density			1991								   .
Staphylinid activity	winter wheat, 1988, 1990, 	pit fall trapping
density			1991					                           .
Spider activity density	winter wheat, 1988, 1990, 	pit fall trapping
			1991							           ..

Table S4. Energy input per unit land area (GJ ha–1) in the 2nd crop rotation (n = 3) Difference BIOORG and CONFYM = 36%, Difference between BIODYN and CONMIN = 53%. Note: grass-clover sawing in the year of barley cultivation. Source: T. Alföldi, Research Institute of Organic Agriculture [Forschungsinstitut für biologischen Landbau (FiBL)], internal report.

					      .
Crop 		BIODYN 	BIOORG 	CONFYM 	CONMIN.
Potatoes 	26.39 	28.42 	39.85 	40.69 .
Winter wheat 1 	12.52 	11.56 	18.88 	19.74 .
Beetroots 	16.31 	15.14 	28.53 	31.56 .
Winter wheat 2 	10.31 	9.79 	20.49 	21.81 .
Barley 		8.82 	9.62 	16.29 	15.78 .
Grass-clover  	6.43 	7.63 	6.78 	6.75  .
  sawing year				      .
Grass-clover  	3.91 	4.27 	5.22 	11.75 .
  1st year				      .
Grass-clover 	4.86 	6.48 	9.98 	20.47 .
  2nd year 				      .
Sum 		89.55 	92.91 	146.02 	168.55.
Mean (energy 	12.79 	13.27 	20.86 	24.08 .
input per				      .
year, sum/7)				      .
Mean% (CONFYM =	61 	64 	100 	115   .
100%)					      .

Table S5. Energy input per unit crop yield (GJ/metric tons dry matter) in the 2nd crop rotation (n = 3).

					      .
Crop 		BIODYN 	BIOORG 	CONFYM 	CONMIN.
Potatoes 	4.23 	3.70 	3.81 	3.98  .
Winter wheat 1 	3.51 	2.93 	4.01 	4.22  .
Beetroots 	1.91 	1.75 	2.48 	3.67  .
Winter wheat 2 	2.60 	2.35 	3.90 	3.88  .
Barley 		2.46 	2.68 	3.39 	3.19  .
Grass-clover	2.83 	3.35 	3.44 	3.92  .
  sawing year				      .
Grass-clover  	0.27 	0.29 	0.34 	0.83  .
  1st year				      .
Grass-clover  	0.42 	0.53 	0.70 	1.62  .
  2nd year				      .

 

21 February 2002; accepted 26 April 2002

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