C H A P T E R T W O

Soil Sulfur Cycling in Temperate

Agricultural Systems
Jrgen Eriksen

Contents
1. Introduction: The Role of Sulfur in Agroecosystems 56
2. Soil Sulfur Pools 59
2.1. Soil organic sulfur pools 59
2.2. Microbial biomass sulfur 61
2.3. Mineralization of soil organic sulfur 63
2.4. Soil inorganic sulfur 66
2.5. Conceptual model for sulfur cycling in temperate
agricultural soils 67
3. Sulfur Amendments to Soil 68
3.1. Inorganic sulfur fertilizer 68
3.2. Animal manure 69
3.3. Other organic materials 73
4. Soil Sulfur Accumulation and Losses in Farming Systems 75
4.1. Sulfur mass balances 75
4.2. Long-term experiments 78
5. Perspectives for Sulfur Use Efficiency in Agriculture 79
6. Conclusions 81
Acknowledgments 82
References 83

Abstract
Despite the essential role of sulfur for plant growth, it has historically received
little attention because of an ample supply from the atmosphere and commer-
cial fertilizers. However, during the last 2030 years the situation has changed
dramatically and today we face the challenge of optimizing sulfur availability in
cropping systems in synchrony with plant demand and in the required form and
quantity. Soil sulfur exists in numerous forms and its dynamics play an impor-
tant role for the sulfur application to plants. Soil organic sulfur has been

Department of Agroecology and Environment, Faculty of Agricultural Sciences, Aarhus University,

Tjele, Denmark

Advances in Agronomy, Volume 102 # 2009 Elsevier Inc.

ISSN 0065-2113, DOI: 10.1016/S0065-2113(09)01002-5 All rights reserved.

55
56 Jrgen Eriksen

separated into broadmostly chemically definedfractions, reflecting land

use and fertilizer practice, but these are of limited value for predicting plant
availability. There are several reasons for this: firstly, soil organic sulfur consists
of a continuum of fractions with different timescales for mineralization; sec-
ondly, the association to soil particles provides physical protection of soil
organic sulfur against decomposition; and, finally, mineralization only constitu-
tes 0.53% per year of the soil organic sulfur pool. The transient nature of plant-
available sulfur makes soil sulfur testing a difficult task and often sulfur balance
considerations provide a better background for fertilizer sulfur recommenda-
tions. Compared to other macronutrients, the sulfur use efficiency is low. In
Danish agriculture the overall use efficiency is 25%. The sulfur surplus relates
to both livestock and arable production. In the arable production there is a
potential to reduce the surplus by ensuring a closer and more site-specific
match of sulfur with plant demand and by using catch crops to reduce sulfate
leaching. Also, the sulfur demand in mineral fertilizer can be reduced in case of
manure application. The surplus from animal production is expected to be
emitted as gaseous sulfur, mostly from animal manure.

1. Introduction: The Role of Sulfur in

Agroecosystems
Sulfur is one of the essential elements required for plant growth and
it plays a role in many plant processes (Blair, 2002; De Kok et al., 2002)
such as:
 Synthesis of the essential amino acids cysteine and methionineboth
building blocks for protein
 Synthesis of coenzyme A, biotin, thiamine, and glutathione
 Synthesis of chlorophyll
 Synthesis of secondary sulfur compounds (allins, glucosinolates, phyto-
chelatins) primarily in members of the families Cruciferae and Liliaceae
 Fixation of nitrogen by leguminous plants
Several of the sulfur compounds are of particular importance for plant
protection against pests and environmental stress, for food quality and for
the production of phytopharmaceutics (De Kok et al., 2002). Sulfur is
therefore considered one of the four major nutrients, together with nitro-
gen, phosphorus, and potassium. Plant sulfur requirements are equal to and
sometimes exceed those for phosphorus. For the synthesis of the sulfur-
containing amino acids, assimilatory reduction of both sulfate and nitrate is
necessary and therefore nitrogen and sulfur uptake and assimilation are
closely linked (Brunold, 1993).
Increasing sulfur deficiency in previously sulfur sufficient areas has been
reported in many parts of the world. The main reasons are (1) the environmental
Soil Sulfur Cycling 57

control of sulfur dioxide emissions in industrial areas, (2) the increasing use
of high-analysis, low-sulfur-containing fertilizers, (3) the increase in yields
obtained as a result of other technological advances, and (4) the decreasing
use of sulfur-containing pesticides and fungicides (Blair, 2002).
Historically, many European countries saw rising emissions of sulfur
dioxide due to industrialization and the use of coal as the predominant
energy source starting in the nineteenth century, but particularly in the
twentieth century (McGrath et al., 2002). A similar development in atmo-
spheric sulfur deposition took place in Denmark since year 1800 (Fig. 1).
The deposition peaked in 1970, since when legislation to reduce sulfur
dioxide emissions was introduced. Interestingly, the atmospheric sulfur
deposition today is similar to or approaching preindustrial levels 100150
years ago. At the peak of deposition the global annual transportation of sulfur
to the atmosphere was approx. 405 million tonnes, of which only about 20%
originated from anthropogenic activity (Siman and Jansson, 1976). How-
ever, 93% of the anthropogenic emission was from the Northern hemisphere
and 20% was from the industrialized part of Europe that covers only 1% of
the Earths surface (Saxe and Andersen, 1986). Emissions of sulfur, particu-
larly atmospheric sulfur dioxide, but also dissolved in rain as sulfate, are of
concern for two reasons (1) high sulfur dioxide concentrations in air have
been responsible for a number of respiratory problems and even deaths and
(2) sulfur deposition is one of the most important causes of acidification of
natural ecosystems, also known as acid rain (McGrath et al., 2002).
The use of sulfur in commercial fertilizers has in Denmark like in many
other countries dramatically increased from the beginning of the nineteenth
century until the mid-1960s (Fig. 2). In this period the consumption was a
result of sulfur being part of phosphorus (super phosphate with 13% sulfur)
and nitrogen fertilizer (ammonium sulfate with 24% sulfur). The use of

30
Sulphur deposition (kg ha1 yr1)

20

10

0
1800 1850 1900 1950 2000

Figure 1 Historic atmospheric sulfur deposition in Denmark. Based on actual values

(symbols, Ellermann et al., 2007) and scaling of the relative time series developed by
Alveteg et al. (1998).
58 Jrgen Eriksen

30

Sulfur fertilizer (kg ha1 yr1)

20

10

0
1900 1925 1950 1975 2000

Figure 2 Sulfur consumption in commercial fertilizer 19102005 to Danish agricul-

tural soils. Source: Statistics Denmark (1968, 19652005).

these increased from 1910, temporarily interrupted by World Wars I and II.
The decrease from 1965 was caused by the introduction of compound
fertilizer and triple super phosphate containing only 1.3% sulfur. The
increase in fertilizer sulfur from 1990 onwards was for the first time in
the history of mineral fertilization caused by the deliberate use of sulfur
following observations of sulfur deficiency symptoms in crops. Sulfur defi-
ciency in crops started to appear in the late 1980s, first in sulfur-demanding
crops such as oilseed rape and later also in cereals, and since the mid-1990s,
sulfur fertilization has been recommended for all crops (Pedersen et al.,
1998). Similar observations have been made throughout Europe. In a
review of crop responses to sulfur fertilization, Zhao et al. (2002) concluded
that today sulfur has become one of the most limiting nutrients for
agricultural production in many European countries.
Sulfur fertilization is not expected to have any adverse environmental
consequences as natural ecosystems are usually not sulfate-limited. How-
ever, there is an EEC guideline for sulfate in drinking water (250 ppm) and
with long-term annual application this limit will eventually be reached, if
rates are not adjusted to crop requirements.
A key point in estimating the requirement of different crops in different
cropping systems is a detailed understanding of the sulfur cycle. The overall
objective of the work presented here was to obtain the knowledge required
to optimize plant availability of sulfur in appropriate quantities and in
synchrony with plant demand. An important part of this was to analyze:
 Soil sulfur cycling: ability of soils and soil organic matter to accumulate and
release sulfur and the supporting mechanisms
 Organic amendments to soil: the ability of organic manures and crop residues
to supply sulfur to plants
 Sulfur supply in farming systems: soil sulfur accumulation, losses, and
balances in different farming systems
Soil Sulfur Cycling 59

2. Soil Sulfur Pools

Soil sulfur exists in organic and inorganic forms. From a plant-nutritional
viewpoint inorganic sulfate is the most important, since this is the form
assimilated by plant roots. However, sulfatewhich is the stable form of
inorganic sulfur in aerobic soilsconstitutes only a small part of total-S in
soils. Generally, more than 95% of soil sulfur is organically bonded with several
hundred kilograms of organic sulfur present in the upper horizons of most
soils. Although not readily plant available, this large organic sulfur pool may
potentially be an important source of sulfur to plants in deficiency situations.

2.1. Soil organic sulfur pools

2.1.1. Characterization
Organic sulfur in soils is a heterogeneous mixture of soil organisms and
partly decomposed plant, animal, and microbial residues and little is know
about the identity of individual compounds. However, choline sulfate,
sulfolipids, sulfonic acids, the sulfur-containing amino acids cysteine and
methionine, and sulfated polysaccharides have been found in soils (Freney,
1986). Several different approaches have been used to separate soil organic
sulfur into broad fractions representing distinct forms and properties.

2.1.2. Separation according to reactivity with reducing agents

The traditional way of separating organic sulfur is according to reactivity
with reducing agents (Tabatabai, 1982). Two distinct groups of sulfur com-
pounds are obtained (1) organic sulfur not directly bonded to C, which can
be reduced to H2S by hydroiodic acid, and (2) organic sulfur, which is
directly bonded to C (CS). The first group is composed primarily of sulfate
esters (COS) and the second includes sulfur-containing amino acids,
mercaptans, disulfides, sulfones, and sulfonic acids (Freney, 1986). Generally,
total sulfur content decreases with depth in line with the organic carbon
content, and the percentage of organic sulfur present as sulfate esters increases
with depth (Eriksen, 1996; Tabatabai and Bremner, 1972).

2.1.3. Physical separation into mineral and aggregate size fractions

Fractionation of soil and organic matter into primary particle size separates
has been used as a tool for studying soil organic matter distribution and
dynamics, since a significant part of organic matter is closely associated with
soil minerals (Christensen, 1992). A considerable sulfur enrichment of the
clay fractions has been found similar to that found for C and N. The ratios of
C/S decrease dramatically with decreasing particle size and for some soils
the N/S ratio also decreases, showing differences in the nature of the
60 Jrgen Eriksen

organic materials associated with different particle size fractions (Anderson

et al., 1981; Hinds and Lowe, 1980).
The interaction with clay can protect some of the more easily decom-
posable organic matter from microbial breakdown (Ladd et al., 1993) and
this interaction seems even more important for sulfur than for C and N. The
increase in the percentage of HI-reducible sulfur (sulfate esters), which is
believed to be the more labile form of organic sulfur (Biederbeck, 1978),
with decreasing particle size suggests that organic sulfurclay interactions are
the major mechanisms protecting organic sulfur from mineralization.

2.1.4. Chemical extraction followed by

physicalchemical separations
Soil sulfur has been studied using conventional organic matter fractionation
into humic acids, fulvic acids, and humin. By using a sonification procedure
in combination with the extraction, humic and fulvic acids are obtained,
some of which are intimately associated with clay minerals and humin
(Bettany et al., 1979, 1980). Although this type of chemical extraction has
been widely used to study soil organic matter dynamics, it is questionable if
it is useful for studying soil organic sulfur because of possible artifact
formation caused by the strongly alkaline reagent (Freney, 1986).

2.1.5. Molecular weight fractionation

Sephadex gel filtration has been used in a number of studies to obtain
fractions of organic matter extracts with different molecular size and nomi-
nal molecular weight (MW) (e.g., Keer et al., 1990; Scott and Anderson,
1976). Generally, much of the organic sulfur is found in fractions with a
very high MW (>100,000 Da), but a significant proportion also has MWs of
less than 10,000 Da. Eriksen et al. (1995c) showed that in the short term,
little sulfur cycling takes place in fractions >5000 Da. During 8 weeks of
incubation, carrier-free 35S was initially incorporated into the <700 Da
MW fraction and then recycled into the 7005000 Da fraction. Keer et al.
(1990) noted that high MW organic matter was enriched with compounds
in the sulfate ester form. More than 75% of total organic sulfur was in the
form of sulfate esters in organic matter with MWs greater than 200,000 Da.
This agrees with the finding that the percentage of sulfate esters increased
with decreasing particle size, since high MW compounds are better
adsorbed to clay particles because of the presumed aliphatic nature of high
MW organic matter (Anderson et al., 1974).

2.1.6. Fractionation according to physical protection

of soil organic sulfur
Extraction of organic sulfur has been carried out using acetylacetone, which
works by complexing with the metals that link organic matter and mineral
particles together, and the organic matter is then extracted by water
Soil Sulfur Cycling 61

(Giovannini and Sequi, 1976). Acetylacetone extraction of organic matter in

conjunction with ultrasonic dispersion has been used, for example, by
Halstead et al. (1966), Keer et al. (1990), and Scott and Anderson (1976).
It was suggested by Eriksen et al. (1995b) that organic sulfur that could only be
extracted by acetylacetone when subjected to ultrasonic dispersion was phys-
ically protected in soil aggregates, and it was shown that sulfur turnover in this
fraction was slow. Thus, using the combined dispersionextraction procedure
by Eriksen et al. (1995b), organic matter was assumed to be divided into
unprotected, protected, and insoluble organic sulfur, where protected means
isolated from decomposers inside water-stable aggregates. It has been demon-
strated that physical protection of soil organic sulfur caused by soil aggregation
plays an important role in the turnover of soil sulfur (Eriksen et al., 1995c).
In an incubation experiment it was found that much of the organic sulfur was
physically protected inside aggregates, and that turnover in this protected
fraction was slow (Table 1). It has also been demonstrated that sulfur is initially
immobilized into organic matter not protected by soil structure and then
gradually into physically protected organic matter (Eriksen, 1997b).

2.1.7. XANES spectroscopy

A nondestructive technique that has been widely used in speciation studies
of environmental and geochemical samples is X-ray absorption fine struc-
ture spectroscopy. A version of this, X-ray adsorption near-edge structure
(XANES), provides specific information on the functional groups
containing sulfur because of its sensitivity to electric structure, oxidation
state, and geometry of neighboring atoms (Vairavamurthy et al., 1997), and
the technique has been used as a tool for understanding sulfur dynamics in
soil organic matter. The advantage over wet chemical methods is that
intermediate oxidation states can be identified.
Long-term agricultural management has been shown to have a significant
effect on sulfur speciation (Solomon et al., 2003) and investigations by Zhao
et al. (2006) indicate that sulfur species in the reduced and intermediate
oxidation states are the main sources of organic sulfur for mineralization.
One problem, however, is that XANES is applied to humic extracts from
agricultural soils, which may not reflect the in situ speciation in soil. Soil
organic sulfur, moreover, exists in many subcompartments in the soil with
widely differing availability, a factor not reflected in the oxidation states. Still,
XANES is a promising technique that needs to be tested on more soils and the
relation to sulfur mineralization potential should be further investigated.

2.2. Microbial biomass sulfur

The microbial biomass plays a major role in soil sulfur cycling and an
understanding of the mechanisms and forms of sulfur involved is thus very
important. Biomass sulfur has been measured as the flush of extractable
Table 1 Distribution of 35S in sulfur fractions after 8 weeks of incubation at 25 C, calculated as percentage of 35S added at incubation start
(Eriksen et al., 1995c)

Inorganic Nonprotected Protected

sulfur organic S organic S Total
35
Clay (%) Carbon (%) Recovery of S added (%)
St. Jyndevad (DK) 3.6 1.5 73 32 1 106
Lundgaard (DK) 4.6 1.4 42 62 3 107
Uralla (AUS) 12.2 0.8 28 56 12 96
Warialda Cult. (AUS) 13.2 0.7 44 50 14 108
Warialda Native (AUS) 15.3 1.5 22 42 29 93
Duri (AUS) 51.4 1.2 23 47 26 96
Soil Sulfur Cycling 63

sulfur following chloroform fumigation, analogous to the way biomass C is

determined (Banerjee et al., 1993; Saggar et al., 1981). Microbial biomass
sulfur forms only a small part of soil organic sulfur, accounting for 0.92.6%
of total organic sulfur in agricultural soils (Chapman, 1987) and 2.2% and
1.2% in a hardwood and a conifer forest, respectively (Strick and Nakas,
1984).
It has been suggested that fluctuations in microbial biomass sulfur may be
related to levels of inorganic sulfate in soils (Chapman, 1987). Biomass sulfur
might become available to plants in a period of decreasing biomass and
sulfate may be immobilized during a period of biomass increase. However,
results by Wu et al. (1993) show that once sulfur has been immobilized by
the microbial biomass, it is directly transformed into soil organic sulfur,
remaining unavailable to plants until remineralized. The activity of the
microbial pool influences turnover rates rather than the size of microbial
biomass sulfur, and in agricultural soils good correlations have been found
between sulfur mineralization and microbial activity (Sparling and Searle,
1993). In a forest soil Autry and Fitzgerald (1993) similarly found a signifi-
cant correlation between organosulfur formation and ATP content.
In experiments with 35S-labeling of the sulfate pool, the labeling of
microbial biomass sulfur has been shown to be relatively constant over
time, both under controlled and field conditions even though immobiliza-
tion took place (Eriksen, 1997b; Wu et al., 1995). This indicates that 35S
immobilized by the microbial biomass is transformed directly into soil
organic sulfur.

2.3. Mineralization of soil organic sulfur

In soils the processes responsible for sulfur transformations such as minerali-
zation, immobilization, oxidation, and reduction are mainly microbially
mediated. Therefore, factors that affect the microbial activity such as tem-
perature, moisture, pH, and substrate availability also affect these processes.
In aerobic agricultural soils, the main process of interest is the release of
inorganic, plant-available sulfate from organic matter. Since mineralization
and immobilization of sulfur happen concurrently (Eriksen, 1997a; Ghani
et al., 1993; Maynard et al., 1983), the release or incorporation of inorganic
sulfate is the net result of several processes.

2.3.1. Biological and biochemical mineralization

McGill and Cole (1981) proposed a conceptual model for the cycling of
organic carbon, nitrogen, sulfur, and phosphorus through soil organic matter,
in which the mineralization of sulfur involves two different processes
biological and biochemical mineralization. Biological mineralization is believed
to be driven by the microbial need for organic C to provide energy, and sulfur
released as sulfate is a byproduct of the oxidation of C to carbon dioxide.
64 Jrgen Eriksen

Biochemical mineralization is the release of sulfate from the sulfate ester pool
through enzymatic hydrolysis. Whereas mineralization of C-bonded sulfur is
strictly dependent on microbial activity, the sulfate esters can be readily
hydrolyzed by sulfatase enzymes in the soil, and therefore the biochemical
mineralization is controlled by the supply of sulfur rather than the need for
energy. In situations where microbial demands cannot be met by soil inorganic
sulfate, sulfatase enzymes are used to hydrolyze sulfate esters and, conversely,
high levels of sulfate will inhibit biological mineralization.
Although the conceptual model can be criticized as an oversimplification
of a much more complex system, it does provide insight into the funda-
mental differences between the processes for different nutrients. Originally,
it was thought that because of the close relationship between sulfur and
nitrogen in organic matter, the ratio between mineralized nitrogen and
sulfur would be the same as in soil organic matter (Walker, 1957; White,
1959). This is in conflict with many studies that have shown considerable
deviations from this. Results range from a much wider ratio (Kowalenko
and Lowe, 1975) to a narrower (Tabatabai and Al-Khafaji, 1980) N/S ratio
in mineralization products than in soil organic matter. Considering the two
mineralization mechanisms in the McGill and Cole (1981) model for sulfur,
these observations are not surprising. Whereas C-bonded sulfur and nitrogen
are stabilized together and released through biological mineralization, the
sulfate esters can be mineralized independently. Thus, net mineralization of
sulfur depends on the rates of the two reactions and the N/S ratio in
mineralized material will vary accordingly.

2.3.2. Sulfatase enzymes

Because much of the soil organic sulfur exists as sulfate esters that can be
mineralized through enzymatic hydrolysis, the sulfatases responsible have
gained some interest. Bacteria and fungi are major sources in the soil, but
also plant roots and possibly mammalian urine may contain these enzymes
(Fitzgerald, 1976; Klose et al., 1999). Sulfatases are classified according to the
sulfate esters they hydrolyze and the main groups are aryl-, alkyl-, steroid,
gluco-, condro-, and mycosulfatases, but only arylsulfatases have been
measured in soils (Germida et al., 1992). Strong correlations have been
found between arylsulfatase activity and soil organic C content (Elsgaard
et al., 2002) and good correlations have been found between sulfur minerali-
zation and arylsulfatase activity (Castellano and Dick, 1991; Lee and Speir,
1979), but this may be due to factors that affect enzyme activity in general.
Since arylsulfatase is only one of many enzymes involved in the mineralization
process, it is unlikely that this alone can explain variations in mineralization of
sulfur (Germida et al., 1992). Little is known about the substrate specificity of
sulfatases, but the activity of arylsulfatases in the soil does not appear to
constitute a rate-limiting factor in the hydrolysis of sulfate esters
(Ganeshamurthy and Nielsen, 1990; Houghton and Rose, 1976).
Soil Sulfur Cycling 65

2.3.3. Sulfur mineralization potential

The potential mineralization of soil organic sulfur has been estimated by
kinetic equations for sulfur mineralization based on the release of sulfur
from incubated soils (Ghani et al., 1991; Pirela and Tabatabai, 1988). The
validity of this approach may be questionable, since mineralization of sulfur
strongly depends on the incubation technique used (Maynard et al., 1983;
Valeur and Nilsson, 1993). It is probably also impossible to identify a
kinetically homogeneous potential mineralizable pool, since the miner-
alization mechanisms consist of several substrates, biochemical pathways,
and microbial communities (Ellert and Bettany, 1988). Besides, kinetic
mechanisms change with temperature (Ellert and Bettany, 1992), which
implies that a true measure of mineralizable sulfur in soils is best achieved
when field conditions are closely simulated.
Under such conditions, Eriksen et al. (1995d) found that the contribu-
tion from mineralization to the supply of sulfur to plants was small (37 mg
S g soil 1 yr 1), but differences between soils were very consistent. The
amount of sulfur mineralized constituted 1.73.1% per year of the organic
sulfur pool in the soil, in agreement with other findings on the mineraliza-
tion of sulfur in the order of 0.53% of the soil organic sulfur pool (Freney,
1986; Keer et al., 1986). Mineralization following the addition of organic
material to soils is discussed below.

2.3.4. Gross sulfur mineralizationimmobilization turnover

The release or incorporation of inorganic nutrients is the net result of
mineralization and immobilization processes. Quantification of gross nutri-
ent fluxes has been used successfully to understand the fundamentals of these
processes for both nitrogen (Murphy et al., 2003) and phosphorus (Di et al.,
1994) using isotopic dilution techniques. The principle of this methodology
is to label the mineral nutrient pool with an isotopic tracer and measure the
change with time. The rates of influx to and outflux from the labeled pool
are then calculated using equations based on tracer kinetics. Although these
equations were developed as early as the 1950s (Kirkham and Bartholomew,
1954), this technique has not been widely used until recently (Di et al.,
2000; Murphy et al., 2003). The 35S tracer has been used to study sulfur
transformations in soil without organic matter addition (e.g., Eriksen,
1997a; Ghani et al., 1993; Goh and Pamidi, 2003; Vong et al., 2003),
following addition of urinary or fecal sulfur (e.g., Blair et al., 1994;
Nguyen and Goh, 1994b; Williams and Haynes, 2000) and plant residues
(Wu et al., 1993, 1995), but the use of the tracer dilution method to
determine gross sulfur transformation rates has rarely been attempted.
Although the use of isotopic dilution techniques has limitations due to the
assumptions of the techniques, they have proved valuable for the mechanis-
tic modeling of gross N fluxes and for our understanding of the fundamental
66 Jrgen Eriksen

processes of the soil internal N cycle and individual microbial pathways

(Murphy et al., 2003). Some recent studies indicate that the isotopic dilution
technique has a similar potential to increase our knowledge of the soil sulfur
cycle (Eriksen, 2005; Nziguheba et al., 2005).

2.4. Soil inorganic sulfur

Sulfur can have any oxidation number from 2 (sulfide) to +6 (sulfate). In
agricultural soils where conditions are mostly aerobic, the dominant and
stable form of inorganic sulfur is sulfate, and only negligible quantities of
lower oxidation state compounds are present (Bohn et al., 1986). Conse-
quently, sulfate is often referred to as inorganic sulfur in the literature.
Concentrations of sulfate in soils fluctuate throughout the year because of
changes in the balance between atmospheric inputs, decomposition of
plants, fertilizer addition, leaching, plant uptake, and microbial activity.
Usually low levels of sulfate are observed over winter and spring due to
leaching, plant uptake, and low mineralization rates associated with low
temperatures (Castellano and Dick, 1990; Ghani et al., 1990). Sulfate exists
as water-soluble salt and as sulfate adsorbed to soil inorganic components.
The soluble sulfate plus most of the adsorbed sulfate is generally believed to
be plant available.

2.4.1. Adsorption of sulfate

The retention of sulfate in soils is dependent on the nature of the colloidal
system, the pH, the sulfate concentration, and the concentration of other
ions in the solution (Harward and Reisenauer, 1966). Sulfate is adsorbed by
hydrous oxides of Fe and Al and by surfaces of clay particles (Parfitt, 1978).
It has been proposed that sulfate is adsorbed by purely electrostatic mechan-
isms (Marsh et al., 1987), but also chemisorption with ligand displacement
of OH and OH2 has been shown to take place (Parfitt and Smart, 1978).
The amount of sulfate adsorbed depends on the surface area of the clay and
the surface charge, and therefore the higher the Al content, the greater the
anion adsorption (Bohn et al., 1986).
The effect of pH on sulfate adsorption is related to the net charge of the
Fe and Al oxides. If the pH in the soil is lower than zero point of charge
(ZPC), it will lead to a positive surface because of hydration of the metal
oxides, and sulfate will be adsorbed in the soil. Thus, acid subsoils (e.g.,
under forest vegetation) and peat soils typically have large storage capacities
for adsorbed sulfate. In agricultural soils, however, the pH is often higher
than the ZPC, leading to a low retention of sulfate in the soils. Thus, Curtin
and Syers (1990) found that virtually all sulfate in soils with pH > 6 was in
solution. Liming, moreover, has been demonstrated to increase sulfur
leaching (Bolan et al., 1988; Chao et al., 1962b) because of desorption of
sulfate and increased mineralization. Even for soils with a marked capacity
Soil Sulfur Cycling 67

to retain sulfate, the strength of the retention seems weak and Chao et al.
(1962a) found that repeated extraction with water removed adsorbed
sulfate.
Sulfate adsorption is influenced by the presence of other anions. The
order of adsorption strength of anions in soils is hydroxyl > phosphate >
sulfate > nitrate = chloride (Tisdale et al., 1984). The stronger adsorption of
phosphate than sulfate is the basis for extraction of adsorbed sulfate
(Tabatabai, 1982) and addition of phosphate to soils has been shown to
increase sulfur leaching (Bolan et al., 1988; Chao et al., 1962b).

2.5. Conceptual model for sulfur cycling in temperate

agricultural soils
Because of the complex nature of soil organic matter, any procedure
attempting to divide organic sulfur into a few biologically meaningful
fractions is a rough simplification. On the other hand, there is some truth
to the various fractions identified above. Clearly the carbon-bonded sulfur
and the sulfate esters have chemically distinct properties important in sulfur
cycling. In some stable and clay-protected organic sulfur pools, however,
these differences are overruled by the physical properties of the soils, as
illustrated in Fig. 3, where the organic sulfur compounds of different
oxidation states such as sulfate esters and C-bonded sulfur fractions are
integrated parts of other mainly physically determined pools. It is, therefore,

Atmospheric S

Fertilizer Plants Animals

Plant residues
Microbial S
Solution sulphate Reduced S
Intermediate S
Oxidized S
Stable
Inorganic Stable organic S
S Physically (residual S)
Adsorbed
Labile protected
sulphate
organic S organic S
Reduced S Reduced S Reduced S
Leaching Intermediate S Intermediate S Intermediate S
Oxidized S Oxidized S Oxidized S
110 yr 50100 yr 1000 yr

Figure 3 Conceptual diagram of the sulfur cycle.

68 Jrgen Eriksen

not surprising that carbon-bonded sulfur and sulfate ester determination on

whole soils offers little information regarding plant availability of the organic
sulfur. On this matter, Scherer (2001) concluded in a review that the
complicated dynamics of organic sulfur compounds in soil make it difficult
to estimate the sulfur delivery to plants. However, as short-term sulfur
cycling probably involves only a small fraction of total organic sulfur, it is
essential to identify the more active parts to obtain a better understanding of
factors determining plant availability. A key point is the physical protection
of soil organic sulfur.

3. Sulfur Amendments to Soil

3.1. Inorganic sulfur fertilizer
The use of sulfur fertilizers has been reviewed elsewhere (e.g., Blair, 2002;
Messick et al., 2002), but, generally, there are two types of sulfur fertilizers
(1) those where sulfur is in the sulfate form and readily available to plants
and (2) those where sulfur needs to be oxidized to sulfate to become
available to plants.
The advantage of sulfate fertilization, in addition to it being in the plant-
available form, is that sulfate is easily incorporated in multinutrient fertili-
zers, which is a cost-efficient way of fertilizer application. However, in
some cases their use may give an unbalanced nutrient supply. One example
is the widely used ammonium sulfate, where its use as a nitrogen source
applies much more sulfur than typically required. Since sulfate is readily
leached from the soil, there is no point in attempting to raise soil sulfur levels
by excessive fertilization (Eriksen, 1996; Knights et al., 2000).
Studies have shown the importance of the availability of sulfur during
grain-filling (Eriksen et al., 2001; Fitzgerald et al., 1999; Monaghan et al.,
1999), where shortage is caused by the limited redistribution of sulfur from
the vegetative tissue to grain (Eriksen et al., 2001; Zhao et al., 1999). The
application of a sulfate-containing fertilizer in the spring carries the risk of
sulfur intended for the grain-filling period either being leached, immobilized
in soil/microbial biomass or in vegetative plant parts. The use of elemental
sulfur fertilizer offers several advantages, including slow release over time as
it is gradually converted to sulfate. The effectiveness of elemental sulfur is
governed by oxidation carried out principally by bacteria and depends on
temperature, moisture, and particle size. Blair et al. (1993) developed a
model for matching the oxidation rate of sulfur from elemental sulfur
with plant requirements. Elemental sulfur is also the most concentrated
form of sulfur, which cuts transport and application costs, it acts as a
reservoir because of the oxidation process and it may be incorporated in
compound fertilizers (Messick et al., 2002).
Soil Sulfur Cycling 69

3.2. Animal manure

On a global scale, total sulfur excretion from domestic animals is estimated
at around 8 million tonnes per year, corresponding to about 13% of world
sulfur production or 80% of the world consumption for manufactured
mineral fertilizer (Eriksen, 2002). However, it is difficult to utilize this
potential source of fertilizer sulfur.
Of this total, developed countries contribute 2.6 million tonnes and
developing countries 5.5 million tonnes. In developed countries, 54% of the
excretion occurs during grazing, whereas in the developing countries this
figure is 65%. The sulfur excreted during grazing is difficult to utilize.
Excremental sulfur may be lost from the main grazing area to unproductive
sites by excremental transfer (Nguyen and Goh, 1994a) and even when
deposited within the productive area, it may not be efficiently recycled
because of nonuniform distribution and losses (Nguyen and Goh, 1994b;
Till et al., 1994; Williams and Haynes, 1992).
Much of the sulfur excreted within a housing system may be collected
and applied to agricultural land as a fertilizer, provided the technical facilities
are in place. The sulfur content of manure collected from cattle and pigs
(1 million tonnes sulfur per year) has a potential as a sulfur fertilizer especially
in the developed countries, as regulations on the utilization of manure
N and/or P already stipulate that animal wastes are used as fertilizers. In
countries with a large animal production, the potential sulfur contribution
can be significant and it is important to establish to what extent the sulfur
content in animal manure is available to plants.

3.2.1. Sulfur content of animal manure

Animal manure is a very variable substance, and its composition is a
product of many factors, for example, animal species, feed composition,
production system and time, and conditions of storage. As stored manure
may be a mixture of excreta of different ages from animals fed different
diets and possibly even from different animal species, the sulfur content
can be quite variable. The concentrations of total-S in slurry typically
vary between 0.15 and 0.7 kg sulfur m 3 of slurry (Eriksen et al., 1995a)
and the mean value in farmyard manure (FYM) is around 1 kg sulfur t 1
FYM.
The question is how much does slurry sulfur contribute to the sulfur
supply of plants? Average values of around 0.35 kg total sulfur m 3 are
commonly found in cattle slurry (Eriksen et al., 1995a; Lloyd, 1994; Watson
and Stevens, 1986). Using this value, a dressing of 50 m3 cattle slurry would
provide 17.5 kg sulfur ha 1, corresponding to the sulfur requirement of, for
example, cereals. However, the total sulfur content is of limited value in
predicting fertilizer value.
70 Jrgen Eriksen

3.2.2. Plant availability of manure sulfur in the short term

The composition of sulfur in slurry and the content of plant-available sulfate
may vary depending on feeding and storage. As a consequence, different
slurries may be expected to have different levels of plant availability of
sulfur. Unfortunately, there is a lack of information on feeding and slurry
storage in the literature covering plant availability of manure sulfur, which
makes it difficult to generalize results.
Lloyd (1994) found an effectiveness of sulfur in cattle slurry of 55%
compared with sulfur in gypsum when applied to grass for silage. This is
much higher than the effectiveness of 5% found by Eriksen et al. (1995a)
when applying slurry to spring oilseed rape in a pot experiment. The low
plant availability of sulfur in slurry was most likely due to transformations in
the slurry during storage, where plant-available inorganic sulfate is incorpo-
rated into organic sulfur or reduced to sulfide (Fig. 4). Sulfide is expected to
be readily oxidized to plant-available sulfate when the slurry is applied to soil.
However, the low plant uptake of slurry sulfur suggests this did not happen.

Cattle slurry
100 C-bonded

50
Sulphate
g S g1 slurry

Sulphide
0
Pig slurry
300
C-bonded
200

Sulphate
100

Sulphide
0
20
Temp. (C)

10

0
0 10 20 30 40 50
Weeks

Figure 4 Variations in S composition of slurry during storage from February to

November. Error bars: SE.
Soil Sulfur Cycling 71

The possibilities are that sulfide was either emitted from the slurry as H2S or
immobilized in the soil as metallic sulfides or by sorption to soil particles
(Bremner and Steele, 1978).
The differences in effectiveness between studies may be explained by
differences in feeding and storage. Often, the sulfur content of feed is
tailored to animal requirements and the storage time is usually many months.
This combination minimizes the content of inorganic plant-available sulfur.
The results from the pot experiment are supported by experiments by
Pedersen et al. (1998). In eight field trials, they found a response to a mineral
fertilizer application of 40 kg sulfur ha 1 to winter oilseed rape despite
applications of animal manure.

3.2.3. Plant availability of manure sulfur in the long term

A low efficiency of sulfur in animal slurry is mainly attributed to slurry sulfur
being in organic forms not available to plants. This suggests that soils with an
annual application of slurry or other organic manures will release more
plant-available inorganic sulfate than unmanured soils. To get an idea of the
residual effect of sulfur added in animal manure, some plots in the Askov
long-term field experiments (Denmark) were examined for their content of
organic C and S and inorganic sulfate (Eriksen and Mortensen, 1999).
The original experiments started in 1894 on both sandy and loamy soils
with the objective of comparing the effect of animal manure with equal
dressings of N, P, and K in mineral fertilizers and unmanured treatments
(Christensen, 1996). Fertilization with animal manure or NPK fertilizer
increased the content of soil organic C compared with unfertilized plots
(Fig. 5). On the sandy soil, the buildup of organic C was followed by a
similar buildup of organic sulfur. Thus, in the mineral-fertilized plots,
organic C and S were on average increased by 26% and 19%, respectively,
compared with the unfertilized plots, and in the organic-manured plots
organic C and S were increased by 51% and 56%, respectively. On the clay
soil, the buildup of organic Con average 17% in the NPK plots and 24%
in organic-manured plotswas followed by insignificant increases in
organic sulfur content of 24% and 5%, respectively.
The increased organic sulfur content did not significantly affect soil
inorganic sulfate levels in the spring. This could be due to leaching losses
during the winter, especially in the sandy soil, or alternatively it could
indicate that organic sulfur in the soil originating from increased fertilization
is no more readily mineralized than the bulk of soil organic sulfur. Similarly,
Knights et al. (2001) found that 153 years of manure application in the
Broadbalk experiment in England increased soil organic C and S contents,
but the long-term application of inorganic sulfur-containing fertilizers had
little effect. They found similarly low inorganic sulfate levels in all arable
plots. However, they did find increased mineralization rates when incubating
soil from the FYM plot compared to the inorganic fertilizer treatments,
72 Jrgen Eriksen

1.6
Organic C
1.4
1.2

%
1.0
0.8
0.6
Organic S
200
g g1 soil

150

100

Inorganic S
8

6
g g1 soil

0
0 1 1 0 1 1 1 1
Sandy soil Clay soil

Unfertilized
NPK fertilizer
Organic fertilizer (AM)

Figure 5 The effect of fertilizer history on the soil content of organic C, organic and
inorganic S in selected plots in the Askov long-term field experiment. Error bars: SE.

indicating that organic manure application indeed does have a potential long-
term effect on the sulfur-supplying capacity to crops. Reddy et al. (2001) found
increased sulfur mineralization when incubating soil subjected to 27 years of
manure application, but also mineral sulfur applications showed increased
mineralization levels.
Annual applications of organic manure increase the soil organic sulfur
content and thus the sulfur mineralization rate. The extent of this increase
depends on soil type, cropping system, and management. Therefore, a
residual sulfur effect of long-term organic manure application must be
expected, although there is no indication that the sulfur from manure will
mineralize more readily than the bulk of soil organic sulfur. The ability of a
cropping system to use mineralized sulfur depends on the length of the
growing season of the crops, but mineralization in unlikely to fully meet the
sulfur demand of a crop.
Soil Sulfur Cycling 73

3.3. Other organic materials

Other organic materials such as sewage sludge, green manure, and compost
may be applied to agricultural land. The plant availability of organic-bonded
sulfur in these depends on the mineralization rates. It is generally believed
that sulfate is released from organic material when C/S ratios are less than 200
and is immobilized if C/S is above 400, whereas a C/S between 200 and 400
can cause both mineralization and immobilization (Barrow, 1960). This rule
seems to apply across different organic materials such as sludge, animal
manure, and plant material. Figure 6 gives data from three studies involving
incorporation of different types of organic material in pot or incubation
experiments. The regression line explains 65% of the variation in minerali-
zation, which is a rather good correlation considering the comprehensive-
ness of soils and organic materials used in the experiment. Straw or other
strongly immobilizing materials were not included as they do not exhibit the
same relationship and it is always advisable to use supplemental sulfur
fertilizers during the incorporation of such materials (Chowdhury et al.,
2000). For straw, it has been estimated that a C/S ratio of 340 is the critical
level for immobilization (Chapman, 1997). Sewage sludge was a good source
of sulfur in this example (Fig. 6) as sulfur mineralization was high due to low
C/S ratios. The C/S ratios of solid animal manure ranged from 22 for poultry
manure to 297 for horse manure. These differencesprobably largely due to
differences in straw contentresulted in much decreased sulfur mineralization
levels in soils amended with a high C/S ratio material.

100
S mineralization (% of added)

75

50

25

25
0 100 200 300
C/S-ratio

Sewage sludge
Green manure
Farmyard manure

Figure 6 Mineralization of S after soil incorporation of sewage sludge (Tabatabai and

Chae, 1991), green manure (Eriksen and Thorup-Kristensen, 2002; Reddy et al., 2002;
Tabatabai and Chae, 1991) and farmyard manure (Reddy et al., 2002; Tabatabai and
Chae, 1991) as a function of total C/S ratio.
74 Jrgen Eriksen

3.3.1. Green manure/catch crop

A green manure is a crop grown primarily for the purpose of being
ploughed in to add nutrients and organic matter to the soil. It has been
demonstrated that a catch crop succeeding the main crop can absorb sulfate
from the root zone during autumn and winter and thereby reduce nitrate
leaching (Eriksen and Thorup-Kristensen, 2002). The catch crop/green
manure is incorporated prior to the sowing of the next crop and ideally
the nutrient content of the residues should quickly become plant available as
illustrated in Fig. 7. To maintain sufficient soil sulfate levels, it is important
not only to capture the sulfate leached in the autumn, but also to make sure
that it is released in time for the following crop to use it efficiently. If the
mineralization of catch crop sulfur is not synchronized with plant sulfur
uptake, there is a risk of leaching losses prior to or after the growing season
of the following crop. Most nonlegume species release both N and S soon
after incorporation, especially the crucifers having low C/N and C/S ratios
(Eriksen et al., 2004). Legumes are generally not as effective as they have
high C/S ratios, which may retard sulfur mineralization considerably or
even lead to immobilization of sulfur.
In sulfur-deficient crop rotations, the release of sulfur from incorporated
catch crops will not be able to fulfill the needs of sulfur-demanding crops
such as oilseed rape, grass ley, kale, or onion and these will probably always
need supplemental sulfur fertilizer. However, the mineralization of catch

Late Autumn Spring

(with catch crop) (crop incorporated)
0

25

50
Depth (cm)

75

100

125

150
0 2 4 6 8 10 12 2 4 6 8 10 12
g SO4-S g1 soil

Bare soil
Italian ryegrass
Fodder radish

Figure 7 Soil sulfate concentrations under different catch crops in autumn and after
incorporation the following spring. Error bars: SE.
Soil Sulfur Cycling 75

crop sulfur will be able to contribute considerably to the sulfur nutrition of

cereals, especially from cruciferous catch crops (Eriksen and Thorup-
Kristensen, 2002).

4. Soil Sulfur Accumulation and Losses in

Farming Systems
4.1. Sulfur mass balances
Mass balances may give an indication of the status of a particular crop or
farming system, but may also be useful when calculated at a regional or
national level. The primary purpose of this is to evaluate the use efficiency of
a particular nutrient within the agricultural sector. In Danish agriculture, the
sulfur surplus was calculated as described by Kyllingsbk and Hansen (2007)
for nitrogen, phosphorus, and potassium. Using this approach, the sulfur
surplus for Danish agriculture (input minus output) decreased from 38 kg
S ha 1 in 1980 to 2530 kg during the last 1015 years (Fig. 8). As a result the
use efficiency of sulfur (total output in % of total input) increased from 13%
to 25%. For comparison, the efficiency of nitrogen increased from 20% to
37%, phosphorus from 23% to 52%, and potassium from 18% to 43% from
1980 to 2004 (Kyllingsbk and Hansen, 2007). The lower efficiency of
sulfur compared to other macronutrients is probably the result of less focus
on sulfur surplus and also because sulfur is lost relatively easily from agricul-
tural systems. Options for improving sulfur use efficiency are addressed in
Section 5.

40

Feed stuff etc.

Input/output (kg S ha1)

30
Atmospheric
deposition
20

10 Fertilizer

0 Plant products
Animal products
10
1980 1985 1990 1995 2000 2005

Figure 8 Sulfur balance for Danish agriculture 19802006. Inputs shown as positive
bars and outputs as negative.
76 Jrgen Eriksen

Generally, the advantages of the mass balances are their quantitative

nature and value as a management tool, but they also have some serious
shortcomings, the main one being the inability to estimate internal flows
which is a major drawback when applying nutrient balances to estimate
potential losses, and the fact that they only address nutrient amounts and
ignore availability (Oborn et al., 2003). This also applies to sulfur balances,
especially when used at farm or field level. One pitfall is the inclusion in
animal manure of sulfur that is partly in organic form and therefore not
immediately plant available. The underlying assumption is that annual
applications of organic sulfur in animal manure will eventually increase
sulfur mineralization. However, the organic fertilizer history may not
always be well described and it is virtually impossible to know if equilibrium
will ever be reached between organic sulfur input and mineralization for the
individual soil. Besides, as mentioned above, the mineralization of organic
sulfur, whether in manure or in crop residues, may not be synchronized
with plant demand. Much of the mineralization may take place during
summer when soil temperatures are highest, which, in the case of cereals,
may be too late to prevent sulfur deficiency (Haneklaus et al., 1995). The
additional consequence of this situation is that substantial sulfate leaching
can take place in the autumn and winter following a sulfur-responsive
spring-sown cereal (Eriksen et al., 2002).
In the same way that a positive sulfur balance may not always result in crop
sulfur sufficiency, a negative balance may not always mean sulfur deficiency.
When inputs such as atmospheric deposition are declining, sulfate leaching
will for a whiledepending on soil type and climatic conditionsreflect
previous inputs more than the actual inputs. Obviously, when basing sulfur
balances partly on historical data or literature values, great care should be taken
that especially sulfate leaching reflects current sulfur inputs.

4.1.1. Example: Organic farming

In conventional farming, sulfur deficiency is easily corrected by applying
inorganic sulfur fertilizer once a deficiency has been identified. In organic
farming systems, this is usually not an option and it seems obvious that sulfur
deficiency will eventually occur. However, the timescale for this to happen
and the severity depends on a number of aspects that are well illustrated by
sulfur balances. Table 2 shows sulfur balances for two organic crop rota-
tionscereal and dairy production, the cereal rotation being at three sites.
Included are the significant parameters described below, whereas parameters
such as volatilization from crops or soil and weight gain by cattle are
considered insignificant (Eriksen and Askegaard, 2000).
Atmospheric Deposition. It used to contribute significantly to the sulfur
balance in parts of the world but the inputs have declined and are also
variable, even on a smaller geographical scale. Today, the atmospheric input
Soil Sulfur Cycling 77

Table 2 Sulfur balance (kg ha 1 yr 1) in crop rotations for organic cereal and dairy
production, from Eriksen and Askegaard (2000) and Eriksen et al. (2002)

Jyndevad Flakkebjerg Foulum Foulum

Clay content (%) 5 16 9 8
Organic system Cereal production Dairy farming
Organic since 1997 1987
Experiment period 19971999 19941997
Input
Atmosphere 10 13 7 11
Manure 4 5 2 12
Irrigation 15 0 0 10
Output
Plants 2 2 3 10
Leaching 32 20 34 20
Balance 6 4 28 3

is only 5060% of what it was when the balances in Table 2 were established
about 10 years ago. Furthermore, the depositions during autumn and winter
are prone to sulfate leaching prior to the growing season of plants.
Manure. In the cereal production systems, only little sulfur was applied in
manure due to restrictions on the import of manure, in contrast to the dairy
system where the manure is produced on the farm. It is important to keep in
mind, though, that this may not all be plant available. In fact, following from
the above, the immediate effect of sulfur in manure must be expected to be
low for the cereal rotations, probably less than 1 kg S ha 1 yr 1.
Irrigation. On the irrigated sites, the input through irrigation water was
significant compared to the sulfur removed in plant material. The sulfur in
this case originates from ground water, which typically contains 5100 mg
l 1 of sulfate in temperate regions (Eriksen et al., 1998). Furthermore,
irrigation is well timed with plant growth and thus nutrient requirement.
Plants. One very distinct difference between the dairy and the cereal
systems was the yield levels as determined by N availability. In the dairy
system nitrogen-fixing crops such as clover produced an ample supply of N
giving high yields, thus creating higher sulfur need and sulfur uptake.
Leaching. Sulfur leaching in cereal production was followed for 3 years
following conversion to organic farming. The conversion was of pivotal
importance for leaching losses. Leaching reflects previous management and
it actually fell during the experiment, especially on the lighter soil types.
78 Jrgen Eriksen

Eventually, the leaching losses will approach those of the dairy system that
was converted to organic farming 7 years prior to experiment start.
Balance. Negative sulfur balances were found in organic cereal crop rota-
tions caused by low inputs in manure and no irrigation at two sites. Leaching
losses in the cereal rotation were considerable, but probably reflected site
history more than current management, as sulfate leaching decreased con-
siderably following conversion to organic management irrespective of soil
type (Eriksen et al., 2002). This would partly have compensated for the
reductions in input. One very important aspect is the very low removal of
plant sulfur in the cereal rotation. This was caused by low yields due to
nitrogen limitation and production of green manure that is recycled in the
crop rotation instead of being removed. So despite negative balances, the
cereal crop rotations are less sensitive to sulfur shortage than might be
expected. However, great care should be taken to ensure availability and
synchrony of the limited sulfur resources with plant needs. For the organic
dairy farming system the balance was positive, but with declining atmo-
spheric input and low plant availability of manure sulfur, the positive sign of
the balance relies on sulfur in irrigation, which will vary between years due
to differences in climatic conditions. In contrast to the cereal rotations, the
dairy system was organic for many years and therefore plant sulfur removal
and sulfate leaching are expected to reflect organic management. So
although immediate sulfur deficiency may not occur, in the longer term a
negative sulfur balance must be expected in this crop rotation. Thus, it will
become necessary to use a plant-available sulfur source approved for organic
farming in this crop rotation to avoid the negative effects of sulfur deficiency.

4.2. Long-term experiments

The soil sulfur status caused by a particular land use or fertilizer practice may
also be evaluated from the changes in the total soil pool. Since most
management-related changes have relatively little effect on the large soil
sulfur pool in the short term, long-term experiments offer the best
possibility to investigate these changes.
Generally, the long-term experiments point in the same direction: a
buildup of the soil organic sulfur pool only occurs if there is a concomitant
input of C to the soil, be it in the form of manure or plant material. Thus,
long-term applications (35153 years) of inorganic sulfur have in some
studies hardly had any effect on soil organic sulfur contents (Kirchmann
et al., 1996; Knights et al., 2001), probably because the additions were in
excess of crop uptake and therefore lost through leaching. In a situation
with sulfur deficiency in a pasture, the inorganic sulfur application has been
shown to increase the amount of sulfur in the soil because of increased crop
production and hence greater organic C input to the soil (Bhupinderpal-
Singh et al., 2004).
Soil Sulfur Cycling 79

Changes in land use also affect soil sulfur stocks. When comparing
permanent pasture with medium- to long-term cultivation (11 and 30
years, respectively), soil sulfur was reduced and it was significantly related
to the decrease in soil C, a well-known consequence of pasture cultivation
(Bhupinderpal-Singh et al., 2004). In the Broadbalk experiment, organic
sulfur accumulation was found to be much higher in permanent grassland
and woodland than in arable cropping systems, but annual applications of
FYM equivalent to 7 t DM ha 1 to the arable system was able to maintain soil
total sulfur content at the same level as permanent pasture and woodland,
which in turn was 2.7 times higher than the sulfur content of mineral-
fertilized arable land (Knights et al., 2001). In the Askov long-term experi-
ments on animal manure and mineral fertilizer (initiated 1894) and in other
studies, soil C and S contents were found to be correlated, but their isotopic
signatures were not (Bol et al., 2005). This indicates that although sulfur in
the longer term is stabilized in association with C in soil organic matter, the
short-term cycles are not necessarily so closely linked.

5. Perspectives for Sulfur Use Efficiency

in Agriculture
Compared to other macronutrients, the use efficiency of sulfur is low.
In the Danish case the overall use efficiency was 25% (Section 4.1). In a
situation where the sulfur nutrition of plants is expected to be balanced, this
indicates that an extensive loss of sulfur occurs. To reduce these losses, it is
necessary to know more about the quantities lost from different compart-
ments. Figure 9 shows a mass flow diagram with current inputs and outputs,
again using Danish agriculture as an example. The quantities were calculated
by combining numbers in Fig. 8 and separate estimates of the sulfur balance

Feed stuff Atmospheric Commercial

etc. deposition fertilizer
5 6 22
Agriculture

Manure
Animal 6 Livestock 8 Arable 2 Plant
products 14 products

Surplus: 5 Feed Surplus: 20

Figure 9 Sulfur mass flow diagram balance for Danish agriculture 2006 (kg S ha 1)
with internal flows between arable and livestock sectors.
80 Jrgen Eriksen

of agricultural land (Eriksen, 1997c), making it possible to divide the

sulfur surplus into contributions from arable and livestock production.
The diagram shows that in 2006 arable land received a total input of 36 kg
S ha 1 with commercial fertilizer as the main source (22 kg S). Sulfur in
harvested crops was 16 kg ha 1 and most of this sulfur was used for feeding
livestock, so only 2 kg S ha 1 was exported from the agricultural sector,
reflecting the intensity of livestock farming in Denmark. Overall, arable land
had a sulfur surplus of 20 kg S ha 1. Livestock farming received 5 kg S ha 1
in the form of feedstuff and a net input from the arable land of 6 kg S ha 1. As
the output in animal products was 6 kg S ha 1, the sulfur surplus of animal
production was 5 kg ha 1. Thus, in both livestock and arable sectors, there is
a need for increasing the efficiency and also a potential for doing so.
Arable Production. Several options exist for reducing the surplus of 20 kg
sulfur ha 1 in the field:
 Quantitatively, the surplus corresponds to sulfate leaching, as gaseous losses
from agricultural land have been found to be insignificant ( Janzen and Ellert,
1998). Our research shows a considerable potential for catch crops to reduce
this sulfate leaching, but to have an effect on the use efficiency of sulfur not
only should catch crop strategies be employed, but the saved sulfur should
also be counterbalanced by reductions in sulfur fertilizer inputs.
 As sulfur fertilization is not expected to have any adverse natural envi-
ronmental consequences, application generally has a, in some cases con-
siderable, safety margin. A closer match of sulfur with plant demand and
also more site-specific applications based on balance considerations prob-
ably have the potential to increase sulfur use efficiency, which will, in the
long term, keep us under the limit of 250 ppm for sulfate in drinking
water. If the consequence of this is lowerbut not criticalconcentra-
tions of sulfur in feed crops, it may potentially also increase the sulfur use
efficiency of livestock production.
 There is evidence that low nitrogen availability gives a higher sulfur
fertilizer efficiency in plants. This has been demonstrated in both cereals
(Eriksen et al., 2001) and legumes (Sunarpi and Anderson, 1997), the
reason being that higher in-plant mobility of sulfur during grain-filling
increases redistribution from older leaves. This can be utilized in low-
input farming systems and may also explain the modest responses to sulfur
application in organic farming systems (Eriksen et al., 2002). However,
care should be taken to avoid hidden sulfur deficiency with reduced
quality or yield without deficiency symptoms (Schnug, 1991). Further-
more, sulfur shortage also affects the efficiency of other nutrients and
given the choice, high nitrogen and phosphorus efficiency would usually
be given priority at the expense of sulfur.
As a consequence of an expected, low, short-term availability of manure
sulfur, Danish farmers are recommended not to reduce the sulfur level in
Soil Sulfur Cycling 81

mineral fertilizer in the year of manure application, whereas the long-term

effect of organic manure to some extent is taken into account (Eriksen,
2002). However, the short-term availability may vary considerably and to
ensure plant requirements are met an option would be to include plant-
available sulfate to increase sulfur use efficiency. In this context, there is a
need to investigate rapid analysis for sulfate in manure.
Livestock Production. The surplus from animal production of 5 kg sulfur
ha 1 (Fig. 9) is expected to be emitted as gaseous sulfur mostly from animal
manure. Except for the loss of plant-available sulfur from the manure, the
consequence may be the development of malodorous, volatile, sulfur-
containing compounds. Several hundred malodorous compounds have
been identified in pig manure. They can be divided into four groups (1)
volatile fatty acids, (2) indoles and phenols, (3) ammonia and volatile
amines, and (4) volatile sulfur-containing compounds (Zhu, 2000). Of the
compounds that have the lowest odor detection thresholds for humans, six
contain sulfur and the three with the lowest detection threshold all contain
sulfur (ONeill and Phillips, 1992). Hydrogen sulfide and methanethiol are
the two sulfurous compounds most commonly causing offensive smells in
pig manure (Spoelstra, 1980). Some studies have shown correlations
between hydrogen sulfide and odor concentration (Clanton and Schmidt,
2001; Hobbs et al., 2000), whilst others show no such correlations (Le et al.,
2005). Apart from odor, hydrogen sulfide is increasingly associated with
health hazards. Maximum atmospheric concentrations have been derived
based on respiratory effects for inhalation exposures (WHO, 2003). It may
be speculated how we can avoid emissions of odorous compounds. Tech-
nical solutions are being investigated (Eriksen et al., 2008; Smet et al., 1999),
but another option is to reduce sulfur inputs in feed either directly by
reducing the content of sulfur amino acids (Le et al., 2006) or indirectly
by establishing a closer match of sulfur with plant demand in the field.
Currently an investigation is in progress on how emissions of sulfurous
compounds may be reduced.

6. Conclusions
Despite the essential role of sulfur for plant growth, it has historically
received little attention because of an ample supply from the atmosphere
and commercial fertilizers. However, during the last 2030 years, the
situation has changed dramatically and it has been necessary to give sulfur
in cropping systems greater consideration. Today, we face a challenge of
optimizing sulfur availability in cropping systems in synchrony with plant
demand and in the required form and quantity.
82 Jrgen Eriksen

Organic sulfur in soil forms a highly complex system of compounds, the

mineralization of which occurs along a continuum of different timescales.
This makes prediction of the potential plant availability of soil organic sulfur
difficult and methods based on identification of compounds or groups of
compounds with distinct chemical properties have failed, although they
often reflect the long-term agricultural management. This is, at least partly,
because association with soil particles and aggregates provides extensive
physical protection of soil organic sulfur against decomposition. As an
alternative, balance considerations will often be able to provide a better
background for fertilizer recommendations, keeping in mind that
availability and synchrony are ignored using this approach.
The efficiency of sulfur in organic manures, especially animal manure,
seems underexplored, considering the focus on animal manure management
in large parts of the world. Although part of the sulfur in animal manure is plant
available to the crop in the year of application (the extent depending on
feeding and storage conditions), most of the residual sulfur will probably not
mineralize any more readily than the bulk of soil organic sulfur. Furthermore,
as a source of sulfur for plants, mineralization of residual and soil organic sulfur
may not be in synchrony with the demand of crops with a short growing
season and may even lead to increased leaching losses of sulfate.
In some cases catch crops, especially crucifers, have been shown to serve
the double purpose of reducing sulfate leaching and increasing synchrony
with crop demand. However, when planning catch crop strategies, priority
is usually given to maximizing N efficiency, and it is in this context the
effect of catch crops on sulfur nutrition should be seen.
Compared to other macronutrients, the use efficiency of sulfur is low. In
the case of Danish agriculture the overall use efficiency was 25%. Of the
sulfur surplus 20% (5 kg ha 1) was related to livestock production and 80%
(20 kg ha 1) to arable production. In arable production, there is a potential
for a closer and more site-specific match of sulfur with plant demand, catch
crops can reduce sulfate leaching, and the sulfur demand in mineral fertilizer
can be reduced where animal manure applications are used. The surplus
from animal production is expected to be emitted as gaseous sulfur mostly
from animal manure. Except for the loss of plant-available sulfur from the
manure, the consequence may be development of malodorous, volatile,
sulfur-containing compounds. There are ways to avoid this, including
technical solutions and a reduction of the sulfur content in animal feeds.

ACKNOWLEDGMENTS
Dr. Thomas Ellermann is gratefully acknowledged for advice on estimates of historical sulfur
deposition, and Dr. Arne Kyllingsbk is acknowledged for invaluable assistance in calculation
national sulfur balances. Figure 6 is reprinted with permission from The International
Fertiliser Society.
Soil Sulfur Cycling 83

REFERENCES
Alveteg, M., Walse, C., and Warfvinge, P. (1998). Reconstructing historic atmospheric
deposition and nutrient uptake from present day values using MAKEDEP. Water Air Soil
Poll. 104, 269283.
Anderson, D. W., Paul, E. A., and St. Arnaud, R. J. (1974). Extraction and characterization
of humus with reference to clay-associated humus. Can. J. Soil Sci. 54, 317323.
Anderson, D. W., Saggar, S., Bettany, J. R., and Stewart, J. W. B. (1981). Particle size
fractions and their use in studies of soil organic matter. I. The nature and distribution of
forms of carbon, nitrogen and sulfur. Soil Sci. Soc. Am. J. 45, 767772.
Autry, A. R., and Fitzgerald, J. W. (1993). Relationship between microbial activity, biomass
and organosulfur formation in forest soil. Soil Biol. Biochem. 25, 3339.
Banerjee, M. R., Chapman, S. J., and Killham, K. (1993). Factors influencing the determi-
nation of microbial biomass sulphur in soil. Commun. Soil Sci. Plant Anal. 24, 939950.
Barrow, N. J. (1960). A comparison of the mineralization of nitrogen and of sulfur from
decomposing organic materials. Aust. J. Agric. Res. 11, 960969.
Bettany, J. R., Stewart, J. W. B., and Saggar, S. (1979). The nature and forms of sulfur in
organic matter fractions of soils selected along an environmental gradient. Soil Sci. Soc.
Am. J. 43, 981985.
Bettany, J. R., Saggar, S., and Stewart, J. W. B. (1980). Comparison of the amount and forms
of sulfur in soil organic matter fractions after 65 years of cultivation. Soil Sci. Soc. Am. J.
44, 7075.
Bhupinderpal-Singh, M. J., Hedley, M. J., Saggar, S., and Francis, G. S. (2004). Chemical
fractionation to characterize changes in sulphur and carbon in soil caused by manage-
ment. Eur. J. Soil Sci. 55, 7990.
Biederbeck, V. O. (1978). Soil organic sulfur and fertility. In Soil Organic Matter
(M. Schnitzer and S. U. Khan, Eds.), pp. 273310. Elsevier, Amsterdam.
Blair, G. J. (2002). Sulphur fertilisers: A global perspective. Proceedings No. 498. Interna-
tional Fertiliser Society, York, UK.
Blair, G. J., Lefroy, R. B., Dana, M., and Anderson, G. C. (1993). Modelling of sulphur
oxidation from elemental sulfur. Plant Soil 155/156, 379382.
Blair, G. J., Till, A. R., and Boswell, C. (1994). Rate of recycling of sulphur from urine,
faeces and litter applied to the soil surface. Aust. J. Soil Res. 32, 543554.
Bohn, H. L., Barrow, N. J., Rajan, S. S. S., and Parfitt, R. L. (1986). Reactions of inorganic
sulfur in soils. In Sulfur in Agriculture (M. A. Tabatabai, Ed.), pp. 233249. ASA
CSSASSSA, Madison.
Bol, R., Eriksen, J., Smith, P., Garnett, M. H., Coleman, K., and Christensen, B. T. (2005).
The natural abundance of 13C, 15N, 34S and 14C in archived (19232000) plant and soil
samples from the Askov long-term experiments on animal manure and mineral fertilizer.
Rapid Commun. Mass Spectrom. 19, 32163226.
Bolan, N. S., Syers, J. K., Tillman, R. W., and Scotter, D. R. (1988). Effect of liming and
phosphate additions on sulphate leaching in soils. J. Soil Sci. 39, 493504.
Bremner, J. M., and Steele, C. G. (1978). Role of microorganisms in the atmospheric sulfur
cycle. In Advances in Microbial Ecology (M. Alexander, Ed.), pp. 273310. Plenum
Press, London.
Brunold, C. (1993). Regulatory interactions between sulphate and nitrate assimilation.
In Sulfur Nutrition and Assimilation in Higher Plants (L. J. De Kok, I. Stulen,
H. Rennenberg, C. Brunold, and W. E. Rauser, Eds.), pp. 6175. SPB Academic
Publishing, The Hague.
Castellano, S. D., and Dick, R. P. (1990). Cropping and sulfur fertilization influence on
sulfur transformations in soil. Soil Sci. Soc. Am. J. 54, 114121.
84 Jrgen Eriksen

Castellano, S. D., and Dick, R. P. (1991). Modified calibration procedure for the measure-
ment of microbial sulfur in soil. Soil Sci. Soc. Am. J. 55, 283285.
Chao, T. T., Harward, M. E., and Fang, S. C. (1962a). Movement of 35S tagged sulfate
through soil columns. Soil Sci. Soc. Am. Proc. 26, 2731.
Chao, T. T., Harward, M. E., and Fang, S. C. (1962b). Adsorption and desorption
phenomena of sulfate ions in soils. Soil Sci. Soc. Am. Proc. 26, 234237.
Chapman, S. J. (1987). Microbial sulphur in some Scottish soils. Soil Biol. Biochem. 19,
301305.
Chapman, S. J. (1997). Barley straw decomposition and S immobilisation. Soil Biol. Biochem.
29, 109114.
Clanton, C. J., and Schmidt, D. R. (2001). Sulfur compounds in gases emitted from stored
manure. Trans. ASAE 43, 12291239.
Chowdhury, M. A. K., Kouno, K., Ando, T., and Nagaoka, T. (2000). Microbial biomass, S
mineralisation and S uptake by African millet from soil amended with various composts.
Soil Biol. Biochem. 32, 845852.
Christensen, B. T. (1992). Physical fractionation of soil and organic matter in primary
particles and density separates. Adv. Soil Sci. 20, 187.
Christensen, B. T. (1996). The Askov long-term experiments on animal manure and mineral
fertilizers. In Evaluation of Soil Organic Matter Models (D. S. Powlson, P. Smith, and
J. U. Smith, Eds.), NATO ASI Series, Vol. I 38, pp. 301312. Springer-Verlag, Berlin.
Curtin, D., and Syers, J. K. (1990). Extractability and adsorption of sulphate in soils. J. Soil
Sci. 41, 295304.
De Kok, L. J., Castro, A., Durenkamp, M., Stuiver, C. E., Westerman, S., Yang, L., and
Stulen, I. (2002). Sulphur in plant physiology. Proceedings No. 500. International
Fertiliser Society, York, UK.
Di, H. J., Harrison, R., and Campbell, A. S. (1994). Assessment of methods for studying the
dissolution of phosphate fertilizers of differing solubility in soil. I. An isotopic method.
Fertil. Res. 38, 19.
Di, H. J., Cameron, K. C., and McLaren, R. G. (2000). Isotopic dilution methods to
determine the gross transformation rates of nitrogen, phosphorus, and sulphur in soil:
A review of the theory, methodologies, and limitations. Aust. J. Soil Res. 38, 213230.
Ellermann, T., Andersen, H. V., Bossi, R., Christensen, J., Frohn, L. M., Geels, C.,
Kemp, K., Lfstrm, P., Mogensen, B. B., and Monies, C. (2007). Atmosfrisk deposi-
tion fra 2006. NOVANA, Aarhus Universitet, Danmarks Miljundersgelser. 62 p.
Faglig rapport fra DMU no. 645.
Ellert, B. H., and Bettany, J. R. (1988). Comparison of kinetic models describing net sulfur
and nitrogen mineralization. Soil Sci. Soc. Am. J. 52, 16921702.
Ellert, B. H., and Bettany, J. R. (1992). Temperature dependence of net sulfur and nitrogen
mineralisation. Soil Sci. Soc. Am. J. 56, 11331141.
Elsgaard, L., Hastrup Andersen, G., and Eriksen, J. (2002). Measurement of arylsulphatase
activity in agricultural soils using a simplified assay. Soil Biol. Biochem. 34, 7982.
Eriksen, J. (1996). Incorporation of S into soil organic matter in the field as determined by
the natural abundance of stable S isotopes. Biol. Fertil. Soils 22, 149155.
Eriksen, J. (1997a). Sulphur cycling in Danish agricultural soils: Inorganic sulphate dynamics
and plant uptake. Soil Biol. Biochem. 29, 13791385.
Eriksen, J. (1997b). Sulphur cycling in Danish agricultural soils. Turnover in organic S
fractions. Soil Biol. Biochem. 29, 13711377.
Eriksen, J. (1997c). Animal manure as S fertilizer. Sulphur Agric. 20, 2730.
Eriksen, J. (2002). Organic manures as sources of fertiliser sulphur. Proceedings No. 505.
International Fertiliser Society, York, UK.
Eriksen, J. (2005). Gross sulphur mineralisationimmobilisation turnover in soil amended
with plant residues. Soil Biol. Biochem. 37, 22162224.
Soil Sulfur Cycling 85

Eriksen, J., and Askegaard, M. (2000). Sulphate leaching in an organic crop rotation on sandy
soil in Denmark. Agric. Ecosyst. Environ. 78, 107114.
Eriksen, J., and Mortensen, J. (1999). Soil sulphur status following long-term annual
application of animal manure and mineral fertilizers. Biol. Fertil. Soils 28, 416421.
Eriksen, J., and Thorup-Kristensen, K. (2002). The effect of catch crops on sulphate leaching
and availability of S in the succeeding crop on sandy loam soil in Denmark. Agric. Ecosyst.
Environ. 90, 247254.
Eriksen, J., Mortensen, J., Kjellerup, V. K., and Kristjansen, O. (1995a). Forms and plant-
availability of sulfur in cattle and pig slurry. Z. Pflanzenernahr. Bodenk. 158, 113116.
Eriksen, J., Lefroy, R. D. B., and Blair, G. J. (1995b). Physical protection of soil organic
sulfur studied using acetylacetone at various intensities of ultrasonic dispersion. Soil Biol.
Biochem. 27, 10051010.
Eriksen, J., Lefroy, R. D. B., and Blair, G. J. (1995c). Physical protection of soil organic
sulfur studied by extraction and fractionation of soil organic matter. Soil Biol. Biochem. 27,
10111016.
Eriksen, J., Mortensen, J. V., Dissing Nielsen, J., and Nielsen, N. E. (1995d). Sulphur
mineralisation in five Danish soils as measured by plant uptake in a pot experiment.
Agric. Ecosyst. Environ. 56, 4351.
Eriksen, J., Murphy, M., and Schnug, E. (1998). The soil sulphur cycle. In Sulphur in
Agroecosystems (Nutrients in Ecosystems) (E. Schnug, Ed.), pp. 3973. Kluwer Aca-
demic Publishers, Dordrecht.
Eriksen, J., Nielsen, M., Mortensen, J. V., and Schjrring, J. K. (2001). Redistribution of
sulphur during generative growth of barley with different sulphur and nitrogen status.
Plant Soil 230, 239246.
Eriksen, J., Olesen, J. E., and Askegaard, M. (2002). Sulphate leaching and sulphur balances
of an organic crop rotation on three Danish soils. Eur. J. Agron. 17, 19.
Eriksen, J., Thorup-Kristensen, K., and Askegaard, M. (2004). Plant-availability of catch
crop S following spring incorporation. J. Plant Nutr. Soil Sci. 167, 609615.
Eriksen, J., Srensen, P., and Elsgaard, L. (2008). The fate of sulphate in acidified slurry
during storage and following application to cropped soil. J. Environ. Qual. 37, 280286.
Fitzgerald, J. W. (1976). Sulfate ester formation and hydrolysis: A potentially important yet
often ignored aspect of the sulphur cycle of aerobic soils. Bacteriol. Rev. 40, 698721.
Fitzgerald, M. A., Ugalde, M. T., and Anderson, J. W. (1999). Sulphur nutrition changes the
sources of S in vegetative tissue of wheat during generative growth. J. Exp. Bot. 50,
499508.
Freney, J. R. (1986). Forms and reactions of organic sulfur compounds in soils. In Sulfur in
Agriculture (M. A. Tabatabai, Ed.), pp. 207232. ASACSSASSSA, Madison.
Ganeshamurthy, A. N., and Nielsen, N. E. (1990). Arylsulphatase and the biochemical
mineralisation of soil organic sulphur. Soil Biol. Biochem. 22, 11631165.
Germida, J. J., Wainwright, M., and Gupta, V. V. S. R. (1992). Biochemistry of sulfur
cycling in soil. In Soil Biochemistry (G. Stotzky and J.-M. Bollag, Eds.), 7, pp. 153.
Marcel Dekker, New York.
Ghani, A., McLaren, R. G., and Swift, R. S. (1990). Seasonal fluctuations of sulfur and soil
microbial biomass-S in the surface of a Wakanui soil. N. Z. J. Agric. Res. 33, 467472.
Ghani, A., McLaren, R. G., and Swift, R. S. (1991). Sulphur mineralisation in some New
Zealand soils. Biol. Fertil. Soils 11, 6874.
Ghani, A., McLaren, R. G., and Swift, R. S. (1993). Mobilization of recently-formed soil
organic sulphur. Soil Biol. Biochem. 25, 17391744.
Giovannini, G., and Sequi, P. (1976). Iron and aluminium as cementing substances of soil
aggregates. I. Acetylacetone in benzene as an extractant of fractions of soil iron and
aluminium. J. Soil Sci. 27, 140147.
86 Jrgen Eriksen

Goh, K. M., and Pamidi, J. (2003). Plant uptake of sulphur as related to changes in the HI-
reducible and total sulphur fractions in soil. Plant Soil 250, 113.
Halstead, R. L., Anderson, G., and Scott, N. M. (1966). Extraction of organic matter from
soils by means of ultrasonic dispersion in aqueous acetylacetone. Nature 211, 14301431.
Haneklaus, S., Murphy, D. P. L., Nowak, G., and Schnug, E. (1995). Effects of the timing of
sulphur application on grain yield and yield components of wheat. Z. Pflanzenernahr.
Bodenk. 158, 8385.
Harward, M. E., and Reisenauer, H. M. (1966). Reactions and movement of inorganic soil
sulfur. Soil Sci. 101, 326335.
Hinds, A. A., and Lowe, L. E. (1980). Distribution of carbon, nitrogen, sulphur and
phosphorus in particle-size separates from gleysolic soils. Can. J. Soil Sci. 60, 783786.
Hobbs, P. J., Misselbrook, T. H., Dhanoa, M. S. and Persaud, K. C. (2001). Development of
a relationship between olfactory response and major odorants from organic wastes. J. Sci.
Food Agric. 81, 188193.
Houghton, C., and Rose, F. A. (1976). Liberation of sulfate from sulfate esters by soils. Appl.
Environ. Microbiol. 31, 969976.
Janzen, H. H., and Ellert, B. H. (1998). Sulfur dynamics in cultivated, temperate agroeco-
systems. In Sulphur in the Environment (D. G. Maynard, Ed.), pp. 1143. Marcel
Dekker, New York.
Keer, J. I., McLaren, R. G., and Swift, R. S. (1986). The sulphur status of intensive grassland
sites in southern Scotland. Grass Forage Sci. 41, 183190.
Keer, J. I., McLaren, R. G., and Swift, R. S. (1990). Acetylacetone extraction of soil organic
sulphur and fractionation using gel chromatography. Soil Biol. Biochem. 22, 97104.
Kirchmann, H., Pichlmayer, F., and Gerzabek, M. H. (1996). Sulfur balances and sulfur-34
abundance in a long-term fertilizer experiment. Soil Sci. Soc. Am. J. 59, 174178.
Kirkham, D., and Bartholomew, W. V. (1954). Equations for following nutrient transfor-
mations in soil, utilizing tracer data. Soil Sci. Soc. Am. Proc. 18, 3334.
Klose, S., Moore, J. M., and Tabatabai, M. A. (1999). Arylsulfatase activity of microbial
biomass in soils as affected by cropping system. Biol. Fertil. Soils 29, 4654.
Knights, J. S., Zhao, F. J., Spiro, B., and McGrath, S. P. (2000). Long-term effects of land use
and fertiliser treatments on sulfur cycling. J. Environ. Qual. 29, 18671874.
Knights, J. S., Zhao, F. J., McGrath, S. P., and Magan, N. (2001). Long-term effects of land
use and fertiliser treatments on sulphur transformations in soils from the Broadbalk
experiment. Soil Biol. Biochem. 33, 17971804.
Kowalenko, C. G., and Lowe, L. E. (1975). Mineralisation of sulfur from four soils and its
relationship to soil carbon, nitrogen and phosphorus. Can. J. Soil Sci. 55, 914.
Kyllingsbk, A., and Hansen, J. F. (2007). Development in nutrient balances in Danish
agriculture. Nutr. Cycl. Agroecosyst. 79, 267280.
Ladd, J. N., Foster, R. C., and Skjemstad, J. O. (1993). Soil structure: Carbon and nitrogen
metabolism. Geoderma 56, 401434.
Le, P. D., Aarnink A. J. A., Ogink, N. W. M., Becker, P. M. and Verstegen, M. W. A.
(2005). Odour from animal production facilities: Its relationship to diet. Nutr. Res. Rev.
18, 330.
Le, P. D., Aarnink, A. J. A., Jongbloed, A. W., van der Peet Schwering, C. M. C.,
Ogink, N. W. M., and Verstegen, M. W. A. (2006). Effect of crystalline amino acid
supplementation to the diet on odor from pig manure. J. Anim. Sci. 85, 791801.
Lee, R., and Speir, T. W. (1979). Sulphur uptake by ryegrass and its relationship to inorganic
and organic sulphur levels and sulphatase activity in soil. Plant Soil 53, 407425.
Lloyd, A. (1994). Effectiveness of cattle slurry as a sulphur source for grass cut for silage. Grass
Forage Sci. 49, 203208.
Marsh, K. B., Tillman, R. W., and Syers, J. K. (1987). Charge relationship of sulphate
sorption by soils. Soil Soc. Am. J. 51, 318323.
Soil Sulfur Cycling 87

Maynard, D. G., Stewart, J. W. B., and Bettany, J. R. (1983). Sulfur and nitrogen minerali-
zation in soils compared using two incubation techniques. Soil Biol. Biochem. 17,
127134.
McGill, W. B., and Cole, C. V. (1981). Comparative aspects of cycling or organic C, N, S
and P through soil organic matter. Geoderma 26, 267286.
McGrath, S. P., Zhao, F. J., and Blake-Kalff, M. M. A. (2002). History and outlook for
sulphur fertilizers in Europe. Proceedings No. 497. International Fertiliser Society, York,
UK.
Messick, D. L., de Brey, C., and Fan, M. X. (2002). Sources of sulphur, their processing and
use in fertiliser manufacture. Proceedings No. 502. International Fertiliser Society, York,
UK.
Monaghan, J. M., Scrimgeour, C., Zhao, F. J., and Evans, E. J. (1999). Sulphur accumula-
tion and redistribution in wheat (Triticum aestivum): A study using stable sulphur isotope
ratios as a tracer system. Plant Cell Environ. 22, 831840.
Murphy, D. V., Recous, S., Stockdale, E. A., Fillery, I. R. P., Jensen, L. S., Hatch, D. J., and
Goulding, K. W. T. (2003). Gross nitrogen fluxes in soil: Theory, measurement and
application of 15N pool dilution techniques. Adv. Agron. 79, 69118.
Nguyen, M. L., and Goh, K. M. (1994a). Sulphur cycling and its implications on sulphur
fertilizer requirements of grazed grassland ecosystems. Agric. Ecosyst. Environ. 49,
173206.
Nguyen, M. L., and Goh, K. M. (1994b). Distribution, transformations and recovery of
urinary sulphur and sources of plant-available soil sulphur in irrigated pasture soil-plant
systems treated with 35sulphur-labelled urine. J. Agric. Sci. (Camb.) 122, 91105.
Nziguheba, G., Smolders, E., and Merckx, R. (2005). Sulphur immobilization and avail-
ability in soils assessed using isotope dilution. Soil Biol. Biochem. 37, 635644.
Oborn, I., Edwards, A. C., Witter, E., Oenema, O., Ivarsson, K., Withers, P. J. A.,
Nilsson, S. I., and Richert Stinzing, A. (2003). Element balances as a tool for sustainable
nutrient management: A critical appraisal of their merits and limitations within an
agronomic and environmental context. Eur. J. Agron. 20, 211225.
ONeill, D. H., and Phillips, V. R. (1992). A review of the control of odour nuisance from
livestock buildings. Part 3. Properties of the odorous substances which have been
identified in livestock wastes or in the air around them. J. Agric. Eng. Res. 53, 2350.
Parfitt, R. L. (1978). Anion adsorption by soils and soil materials. Adv. Agron. 30, 150.
Parfitt, R. L., and Smart, R. S. T. C. (1978). The mechanism of sulfate adsorption on iron
oxides. Soil Sci. Soc. Am. J. 42, 4850.
Pedersen, C. A., Knudsen, L., and Schnug, E. (1998). Sulphur fertilization. In Sulphur in
Agroecosystems (E. Schnug, Ed.), pp. 115134. Kluwer Academic Publishers, Dordrecht.
Pirela, H. J., and Tabatabai, M. A. (1988). Sulphur mineralisation rates and potentials of soils.
Biol. Fertil. Soils 6, 2632.
Reddy, K. S., Singh, M., Tripathi, A. K., Swarup, A., and Dwivedi, A. K. (2001). Changes
in organic and inorganic sulfur fractions and S mineralisation in a Typic Haplustert after
long-term cropping with different fertiliser and organic manure inputs. Aust. J. Soil Res.
39, 737748.
Reddy, K. S., Singh, M., Swarup, A., Rao, A. S., and Sing, K. N. (2002). Sulfur miner-
alisation in two soils amended with organic manures, crop residues, and green manures.
J. Plant Nutr. Soil Sci. 165, 167171.
Saggar, S., Bettany, J. R., and Stewart, J. W. B. (1981). Sulfur transformations in relation to
carbon and nitrogen in incubated soils. Soil Biol. Biochem. 13, 499511.
Saxe, H., and Andersen, A. S. (1986). Luftforurening. In Miljforvaltning, pp. 273310.
DSR forlag, Landbohjskolen, Kbenhavn.
Scherer, H. W. (2001). Sulphur in crop productionInvited paper. Eur. J. Agron. 14,
81111.
88 Jrgen Eriksen

Schnug, E. (1991). Sulphur nutritional status of European crops and consequences for
agriculture. Sulphur Agric. 15, 712.
Scott, N. M., and Anderson, G. (1976). Sulphur, carbon, and nitrogen contents of organic
fractions from acetylacetone extracts of soils. J. Soil Sci. 27, 324330.
Siman, G., and Jansson, S. L. (1976). Sulphur exchange between soil and atmosphere, with
special attention to sulphur release directly to the atmosphere. Swedish J. Agric. Res. 6,
3745.
Smet, E., Van Langenhove, H., and De Bo, I. (1999). The emission of volatile compounds
during the aerobic and the combined anaerobic/aerobic composting of biowaste. Atmos.
Environ. 33, 12951303.
Solomon, D., Lehmann, J., and Martinez, C. A. (2003). Sulfur K-edge XANES spectros-
copy as a tool for understanding sulfur dynamics in soil organic matter. Soil Sci. Soc. Am. J.
67, 17211731.
Sparling, G. P., and Searle, P. L. (1993). Dimethyl sulphoxide reduction as a sensitive
indicator of microbial activity in soil: The relationship with microbial biomass and
mineralization of nitrogen and sulphur. Soil Biol. Biochem. 25, 251256.
Spoelstra, S. F. (1980). Origin of objectionable odorous components in piggery wastes and
the possibility of applying indicator components for studying odour development. Agric.
Environ. 5, 241260.
Statistics Denmark. (1968). Landbrugstatistik 19001965. Bind I Landbrugsareal og
hstudbytte samt gdningsforbrug Statistiske undersgelser Nr. 22. Statistics Denmark,
Copenhagen.
Statistics Denmark. (19652005). Agricultural Statistics. Statistics Denmark, Copenhagen.
Strick, J. E., and Nakas, J. P. (1984). Calibration of a microbial sulfur technique for use in
forest soils. Soil Biol. Biochem. 16, 289291.
Sunarpi, J. W., and Anderson, J. W. (1997). Effect of nitrogen nutrition on remobilization of
protein sulphur in leaves of vegetative soybean and associated changes in soluble sulphur
metabolites. Plant Physiol 115, 16711680.
Tabatabai, M. A. (1982). Sulfur. In Methods of Soil Analysis (A. L. Page, Ed.), Part 2
pp. 501538. SSSA, Madison.
Tabatabai, M. A., and Al-Khafaji, A. A. (1980). Comparison of nitrogen and sulfur miner-
alisation in soils. Soil Sci. Soc. Am. J. 44, 10001006.
Tabatabai, M. A., and Bremner, J. M. (1972). Forms of sulfur, and carbon, nitrogen and
sulfur relationships in Iowa soils. Soil Sci. 114, 380386.
Tabatabai, M. A., and Chae, Y. M. (1991). Mineralization of sulfur in soils amended with
organic wastes. J. Environ. Qual. 20, 684690.
Till, A. R., Blair, G. J., and Boswell, C. C. (1994). Sulfur leaching from soil columns treated
with 35S-labelled urine. Aust. J. Soil Res. 32, 535542.
Tisdale, S. L., Nelson, W., and Beaton, J. D. (1984). Soil Fertility and Fertilizers.
Macmillan Publishing Company, New York.
Vairavamurthy, M. A., Maletic, D., Wang, S., Manowitz, B., Eglinton, T., and Lyons, T.
(1997). Characterization of sulfur-containing functional groups in sedimentary humic
substances by X-ray absorption near-edge structure spectroscopy. Energy Fuels 11,
546553.
Valeur, I., and Nilsson, I. (1993). Effects of lime and two incubation techniques on sulfur
mineralisation in a forest soil. Soil Biol. Biochem. 25, 13431350.
Vong, P.-C., Dedourge, O., Lasserre-Joulin, F., and Guckert, A. (2003). Immobilized-S,
microbial biomass-S and soil arylsulfatase activity in the rhizosphere soil of rape and barley
as affected by labile substrate C and N additions. Soil Biol. Biochem. 35, 16511661.
Walker, T. W. (1957). The sulphur cycle in grassland soils. J. Br. Grassland Soc. 12, 1018.
Watson, C. J., and Stevens, R. J. (1986). The sulphur content of slurries and fertilizers. Rec.
Agric. Res. 34, 57.
Soil Sulfur Cycling 89

White, J. G. (1959). Mineralisation of nitrogen and sulphur in sulphur-deficient soils. N. Z.

J. Agric. Res. 2, 255259.
WHO. (2003). In Hydrogen sulfide: Human health aspects. Concise international chemical
assessment document 53, p. 26. World Health Organization, Geneva.
Williams, P. H., and Haynes, R. J. (1992). Transformations and plant uptake of urine-
sulphate in urine-affected areas of pasture soil. Plant Soil 145, 167175.
Williams, P. H., and Haynes, R. J. (2000). Transformations and plant uptake of urine N and
S in long and short-term pastures. Nutr. Cycl. Agroecosyst. 56, 109116.
Wu, J., ODonnell, A. G., and Syers, J. K. (1993). Microbial growth and sulphur immobili-
zation following the incorporation of plant residues into soil. Soil Biol. Biochem. 25,
15671573.
Wu, J., ODonnell, A. G., and Syers, J. K. (1995). Influences of glucose, nitrogen and plant
residues on the immobilization of sulphate-S in soil. Soil Biol. Biochem. 27, 13631370.
Zhao, F. J., Hawkesford, M. J., and McGrath, S. P. (1999). Sulphur assimilation and effects
on yield and quality of wheat. J. Cereal Sci. 30, 117.
Zhao, F. J., McGrath, S. P., Blake-Kalff, M. M. A., Link, A., and Tucker, M. (2002). Crop
responses to sulphur fertilisation in Europe. Proceedings No. 504. International Fertiliser
Society, York, UK.
Zhao, F. J., Lehmann, J., Solomon, D., Fox, M. A., and McGrath, S. P. (2006). Sulphur
speciation and turnover in soils: Evidence from sulphur K-edge XANES spectroscopy
and isotope dilution studies. Soil Biol. Biochem. 38, 10001007.
Zhu, J. (2000). A review of microbiology in swine manure odor control. Agric. Ecosyst.
Environ. 78, 93106.