Gaseous Nitrogen and Carbon Losses from Pig Manure Derived from Different Diets
Gerard L. Velthof,* Jaap A. Nelemans, Oene Oenema, and Peter J. Kuikman
ABSTRACT
Manipulation of the diets of pigs may alter the composition of the
manure and thereby the environmental and agricultural qualities of
Reproduced from Journal of Environmental Quality. Published by ASA, CSSA, and SSSA. All copyrights reserved.
the manure. Laboratory studies were performed to quantify the effect
of manipulation of pig diets on the chemical composition of the derived
manure (slurry), the potential emission of methane (CH4) and ammo-
nia (NH3) during anaerobic storage of the manure, and the potential
nitrous oxide (N2O) and carbon dioxide (CO2) emission after applica-
tion of the manure to soil. The diets differed in contents of crude protein
and salt (CaSO4), and the type and contents of nonstarch polysaccha-
rides (NSP). Emissions of NH3 and CH4 during storage were smaller
at a low than at a high dietary protein content. The emission of NH3
was significantly related to the contents of ammonium (NH4), total N,
and pH. The emission of CH4 was significantly related to contents of
dry matter, total C, and volatile fatty acids in the manure. The effect
of manure composition on N2O emission markedly differed between
the two tested soils, which points at interactions with soil properties
such as the organic matter content. These types of interactions require
soil-specific recommendations for mitigation of N2O emission from
soil-applied pig manure by manipulation of the diet. From the tested
diets, decreasing the protein content has the largest potential to simul-
taneously decrease NH3 and CH4 emissions during manure storage
and N2O emission from soil. An integral assessment of the environ-
mental and agricultural impact of handling and application of pig
manure as a result of diet manipulation provides opportunities for
farmers to maximize the value of manures as fertilizer and soil condi-
tioner and to minimize N and C emissions to the environment.
T he number of pigs in the world has doubled since
the early 1960s and reflects the increase in pork
consumption. The volume of produced pig manure has
correspondingly increased. Manure produced in inten-
sive livestock systems is generally recycled inefficiently
and leads to leaching of nitrogen (N) and phosphorus
(P) to ground and surface waters and emissions of green-
house gases (CH4, N2O, and CO2) and other harmful
gases (NH3 and NOx) to the atmosphere (Berges and
Crutzen, 1996; Ferm et al., 1999; Husted, 1994; Sherlock
et al., 2002; Smith et al., 1998). Environmental legisla-
tion and the public concerns about the ecological risk
of pig farming have increased pressure on pig farmers
to minimize unwanted emissions. Measures and tools
for farmers are required to achieve agricultural systems
in which high quality food is produced with a minimal
negative environmental impact.
The impact of nutritional measures on the perfor-
mance and profitability of animal production has tradi-
G.L. Velthof, O. Oenema, and P.J. Kuikman, Alterra, Wageningen
University and Research Centre, P.O. Box 47, 6700 AA Wageningen,
the Netherlands. J.A. Nelemans, Department of Soil Quality, Wagen-
ingen University and Research Center, P.O. Box 8005, 6700 EC Wa-
geningen, the Netherlands. Received 23 July 2004. *Corresponding
author (gerard.velthof@wur.nl).
Published in J. Environ. Qual. 34:698–706 (2005).
© ASA, CSSA, SSSA
677 S. Segoe Rd., Madison, WI 53711 USA
698
tionally been the prime focus in livestock nutrition re-
search. However, animal nutrition also strongly affects
the plant availability of nutrients in the manure and the
nitrogen and carbon transformations and losses during
its storage and after its application to soil (Canh et al.,
1998a; Gerdemann et al., 1999; Jongbloed and Lenis,
1998; Kreuzer et al., 1998; Misselbrook et al., 1998; Paul
et al., 1998; Sørensen and Fernandez, 2003). Knowledge
about the integral effects of dietary composition on ma-
nure composition and N and C losses during manure
storage and after application to soil is required to de-
crease the emissions of harmful compounds from inten-
sive animal production systems to the environment.
The content of plant-available N (NH4 and easily min-
eralizable organic N) in manures strongly determines
the value of animal manures as N fertilizer. Manures
rarely contain NO3, because the anaerobic conditions
during storage inhibit nitrification and any formed NO3
is rapidly denitrified. The percentage of NH4–N in total
N of animal manures increases as the diet contains more
protein (Canh et al., 1998a). Part of the organic N in
manures is rapidly mineralized after soil application and
considered readily available for plants. Chadwick et al.
(2000) showed that the N mineralization rate is nega-
tively related to the C to organic N ratio of manures.
Sørensen and Fernandez (2003) found similar results
and showed that the plant availability of pig manure N
decreased when the contents of low-fermentable fibers
in the diet increased.
Gaseous C and N emissions to the atmosphere occur
at various stages in the chain of manure production,
storage, and application to the fields. Changes in manure
management may affect the emissions in different parts
of this chain. Good insight in the C and N flows in the
whole chain and interactions between these flows is
required to derive mitigation options and to avoid un-
wanted trade-offs. Robertson et al. (2000) showed that
whole system analysis of greenhouse emissions from
agricultural soils reveals a number of mitigation options.
Emission of NH3 from animal manure during storage
is largely controlled by the NH4 content and the pH of
animal excreta. The NH4 content can be adjusted by
changing the protein content in the diet and the pH by
adding acidifying salts or changing carbohydrate compo-
sition in the diet. The NH3 emission from stored pig
manures decreased with 10 to 12.5% for each percent
decrease in the content of dietary crude protein (Canh
et al., 1998a). The NH3 emission from soil-applied ma-
nure is not only affected by the NH4 content and pH
of the manure, but also by the application technique,
weather conditions, and soil properties (Huisman et al.,
1997). The production of CH4 during anaerobic storage
of animal manure is controlled by type and contents of
Abbreviations: DM, dry matter; DOC, dissolved organic carbon; NSP,
nonstarch polysaccharides; VFA, volatile fatty acids.
 VELTHOF ET AL.: GASEOUS N AND C LOSSES FROM PIG MANURE
organic compounds in the manure. Changes in type and
content of proteins and polysaccharides in the diet alter
the manure composition (Canh et al., 1998b) and may
influence CH4 emission. Emission of N2O from soil-
applied animal manures is controlled by the amount of
applied N and C (e.g., Velthof et al., 2003). The larger
the amount of applied mineral N and easily mineraliz-
Reproduced from Journal of Environmental Quality. Published by ASA, CSSA, and SSSA. All copyrights reserved.
able N, the larger the risk on N2O emission. Moreover,
application of easily degradable C with manures in-
creases potential denitrification in the soil and thereby
risk of N2O emission. Paul and Beauchamp (1989)
showed that volatile fatty acids (VFA) in animal ma-
nures are effective C sources for denitrifying soil bacte-
ria. Increasing contents of fermentable polysaccharides
in the pig diet increase the contents of VFA in pig
excreta (Canh et al., 1998b) and may thus enhance deni-
trification and N2O emission after application to soil.
This paper presents results of an integral study in
which the effects of dietary composition on N and C
transformations and losses during manure storage and
after manure application to soil are quantified. A series
of laboratory studies were performed to quantify the
effect of changes in dietary composition of pigs on the
chemical composition of the produced manure, the po-
tential emission of CH4 and NH3 during anaerobic stor-
age of the manure, and the potential N2O and CO2
emission after application of the manure to soil. The
diets differed in protein content, salt content, and the
content and type of NSP, by which a wide range of C
and N contents and pH of the manures were obtained.
The integral effects of changes in dietary composition
on environmental and agricultural performance of the
pig manure are discussed.
MATERIALS AND METHODS
A series of experiments and chemical analyses were per-
formed using 10 manures selected from a feeding trial with
pigs with four dietary factors (Fig. 1), as described by Bakker
et al. (2004).
Fig. 1. Schematic presentation of the different experiments and analyses.
699
Feeding Trial with Pigs
A feeding trial with pigs was performed in 2000 to test the
effects of four dietary factors on animal performance and NH3
emission (Bakker et al., 2004), namely, (i) the crude protein
content; (ii) the addition of urine acidifying salt (CaSO4); (iii)
the content of NSP (the total content of organic compounds
minus crude protein content minus crude fat content minus
sugar content minus starch content); and (iv) the content of
fermentable NSP (NSP degraded by bacteria within the ani-
mal). The pigs were kept individually in metabolism cages
(1.2 ⫻ 0.6 m) in an environmentally controlled room (20⬚C
and 55% relative humidity), that allowed separate collection
of urine and feces. For each dietary treatment there was one
cage. The experimental period consisted of an adaptation pe-
riod of three weeks followed by two experimental periods of
each five days in which the urine and feces of each cage were
separately collected. Urine was collected in a bucket via a
funnel below the cage. Feces were collected in plastic bags
(15 ⫻ 30 cm). The urine buckets and feces bags were changed
twice a day, and mixed according to their original excretion
ratio. Samples of 2 kg of the mixtures of urine and feces, from
now on referred to as manures, were frozen in closed plastic
bottles until examination (about two months later). The sam-
ples were thawed at 5⬚C. To activate bacteria, 1 mL of an
extract of fresh pig manure was added to 1 L of manure and
the manure was incubated for three days at 20⬚C. Possible N
and C losses during this activation period were not recorded.
Thereafter, chemical analyses and the experiments were per-
formed. Dietary composition may also affect the volume of
excreted N (e.g., Canh et al., 1998a, 1998b), but these effects
fall outside of the scope of the current study. The focus of
the current study was to quantify the effects of dietary compo-
sition on manure composition and on gaseous N and C losses
during storage and after soil application. Ten dietary treat-
ments were selected to obtain a wide range in manure compo-
sition. The effect of protein content can be assessed by compar-
ison of Manures A and B and Manures C and D, that of
addition of acidifying salt (CaSO4) by comparing Manures A
and C and Manures B and D, that of addition of NSP by
comparing Manures E and F, Manures G and H, and Manures
B and I, and that of addition of fermentable NSP by comparing
Manures E and G and Manures F and H (Table 1).
 700 J. ENVIRON. QUAL., VOL. 34, MARCH–APRIL 2005

Table 1. Contents of crude protein, CaSO4, and nonstarch poly- Table 2. Properties of the tested soils.
saccharides (NSP) of the tested diets.
Sandy soil from arable Clay soil from arable
NSP Property land in Wageningen land in Betuwe
Crude
Manure protein CaSO4 Total Fermentable pH (0.01 M CaCl2) 5.8 7.5
Particles ⬍ 2 ␮m, % 6 29
g kg⫺1 Total N content, g kg⫺1 1.5 1.5
A 142 0 189 83 Total C content, g kg⫺1 23.0 10.2
B 180 0 189 83 Soluble C content 126 53
Reproduced from Journal of Environmental Quality. Published by ASA, CSSA, and SSSA. All copyrights reserved.

C 142 17 189 83 (0.01 M CaCl2), mg kg⫺1

D 180 17 189 83
E 161 8.5 129 62
F 161 8.5 245 62
G 161 8.5 129 104
H 161 8.5 245 104
I 180 0 129 83
J 161 8.5 189 83
Characterization of the Manures
Before analysis for contents of total N and C, all manures
were acidified to pH 4.0 with 4 M HCl to avoid NH3 losses
and were dried at 70⬚C. Total C was determined using Kurmies
method, that is, wet oxidation by sulfochromic acid (Houba
et al., 1997), and total N was determined using spectroscopy
after digestion of manure with H2SO4–salicylic acid–H2O2 and
selenium (Temminghoff et al., 2000). All other analyses were
performed in manure samples that were not acidified. The
contents of NH4 and NO3 in the manure were determined
using spectroscopy, after extraction of 500 mg of manure with
25 mL of 0.01 M CaCl2 (Houba et al., 2000). The dissolved C
content in the 0.01 M CaCl2 extract was determined using a
TOC/DOC analyzer (Houba et al., 2000). The contents of
VFA in the manures were measured after extraction of 15 g
of manure in 60 mL of water. The extracts were centrifuged,
filtrated, and diluted with water (1:1), after which the VFA
contents were determined with a Hewlett-Packard (Palo Alto,
CA) 5890 gas chromatograph equipped with a flame ionization
detector and using N2 as carrier gas (injection volume was 1
␮L, internal diameter of the column was 2 mm, column was
packed with 10% Fluorad FC-341 on Supelcoport 100-200
mesh). Column temperature, detection temperature, and in-
jection temperature were 130, 280, and 200⬚C, respectively.
All chemical analyses of the manures were performed on
single samples.
Potential Emissions of Methane
and Ammonia during Storage
To assess potential CH4 and NH3 emission during storage,
samples of 200 mL of manure were anaerobically incubated
at 35⬚C during 90 d. The high temperature was chosen to
enhance emissions during the relatively short period of storage
of 90 d. In practice in the Netherlands, manures are stored at
lower temperature (⬍20⬚C), but for a longer time. The ma-
nures were incubated in 500-mL serum bottles with a stopper
with septum. The experiment consisted of 30 bottles (i.e., 10
manures times 3 replicates). The bottles were randomly placed
in the incubator and emissions of CH4 were measured 21 times
during 97 d. The measurement frequency decreased from three
times per week during the first two weeks to once per week
from Week 5 onward. At each measurement time, the bottles
were flushed with N2 for 10 min and closed with the stopper.
The CH4 concentration in the headspace of the bottles was
measured 180 min after closing the bottles using a Bruël &
Kjær (Nærum, Denmark) photo-acoustic gas monitor (Ya-
mulki and Jarvis, 1999). The inlet and outlet of the gas monitor
was attached to the bottles with two Teflon tubes with needles
that were inserted through the septa. In each bottle with ma-
nure, a small container with 3 mL of 3.2 M H2SO4 was placed
Denitrification potential, 11 3
mg N kg⫺1 d⫺1
NO3⫺ content, mg N kg⫺1 19 32
NH4⫹ content, mg N kg⫺1 11 8
to trap the NH3 volatilized from the manures. The H2SO4 was
refreshed after 1, 8, 15, 22, 40, 62, 76, and 90 d. At the end,
the NH4 contents of the mixed H2SO4 samples were analyzed
to quantify the total NH3 emission during the incubation pe-
riod of 90 d. After the incubation, the manures were analyzed
for contents of dry matter, total N, and total C.
Potential Denitrification after Application to Soil
The potential denitrification was assessed in an incubation
study with the 0- to 30-cm layer of a sandy soil from arable
land in Wageningen (Table 2), using the acetylene inhibition
technique (Yoshinari et al., 1977). The potential denitrification
is here defined as the maximum rate at which NO3 will be
reduced under anaerobic conditions at 20⬚C without addition
of reductant. Differences in potential denitrification are
mainly caused by differences in degradable C in the soil. Soil
mixed with manure and an excess of NO3 was anaerobically
incubated in incubation bottles with a stopper at 20⬚C. Ma-
nures were added at a rate of 100 mg N kg⫺1 soil and NO3 was
added as KNO3 at a rate of 200 mg N kg⫺1. After application of
manure and KNO3 the bottles were closed and flushed for 15
min with N2, and acetylene (C2H2) was added in the headspace
with a syringe to adjust the headspace concentration of C2H2
to 5% (v/v). The soil moisture content was at field capacity.
To increase microbial activity, a diluted extract of fresh pig
manure (130 mL kg⫺1 soil of an extract of 50 g of fresh manure
in 1 L of water) was added and the soil was pre-incubated
before manure application for 4 d at 20⬚C. Any change in N2O
concentration was measured 24, 48, and 72 h after closing of
the stopper using a Bruël & Kjær photo-acoustic gas analyzer.
All treatments were performed in triplicate.
Potential Emissions of Nitrous Oxide and Carbon
Dioxide after Application to Soil
The N2O and CO2 emissions following soil application of
the manure were determined in an incubation study with the
0- to 30-cm layer of a sandy soil and a clay soil (Table 2).
Samples of 120 g moist soil were incubated in 500-mL incuba-
tion bottles at 20⬚C. To increase microbial activity, a diluted
extract of fresh pig manure (200 mL kg⫺1 soil of an extract
of 50 g of fresh manure in 1 L of water) was added to both
soils. Soils were pre-incubated before manure application for
4 d at 20⬚C. Manures were mixed through the soil. Soil mois-
ture content was kept at field capacity for 14 d. Fluxes of N2O
and CO2 were assessed from the increase in N2O and CO2
concentrations in the headspace following the closure of the
bottles for 1 h. Concentrations of N2O and CO2 were measured
using a Bruël & Kjær photo-acoustic gas analyzer. Emission
of N2O and CO2 were measured 16 times during a period of
44 d. The total N2O and CO2 emission were calculated by
linear interpolation of the measured fluxes at different times.
Between the measurement times, the bottles were left open.
 VELTHOF ET AL.: GASEOUS N AND C LOSSES FROM PIG MANURE 701

Table 3. Chemical composition of the manures. All contents are expressed on a fresh weight basis.
Volatile fatty acids (VFA)
Total C to C to N Iso- and Iso- and
0.01 M CaCl2 extraction
Dry total N organic Total Acetic Propionic n-butyric n-valeric
Manure pH matter Total C Total N ratio ratio NO3–N NH4–N DOC† NH4 ⫹ NO3 content acid acid acid acid
g kg⫺1 g kg⫺1 % total N g C kg⫺1 % of total VFA carbon
A 7.9 95 34.2 4.4 7.8 16 0.0 2.3 2.8 52 2.6 64 14 13 9
Reproduced from Journal of Environmental Quality. Published by ASA, CSSA, and SSSA. All copyrights reserved.

B 8.4 110 36.5 6.8 5.4 14 0.0 4.1 2.9 61 3.4 70 10 13 7

C 7.1 107 40.1 5.0 8.0 13 0.0 2.0 4.2 40 2.8 47 18 23 12
D 7.8 110 38.7 7.0 5.5 18 0.0 4.8 3.8 69 4.3 57 12 22 10
E 8.0 82 28.9 5.0 5.8 15 0.0 3.1 2.9 62 2.8 60 12 18 10
F 7.7 125 45.4 5.5 8.3 20 0.0 3.3 3.4 60 3.1 63 14 15 8
G 8.5 57 14.3 5.0 2.9 10 0.0 3.6 2.4 71 2.2 63 11 17 9
H 7.9 121 47.2 5.7 8.3 18 0.0 3.2 3.5 55 3.1 58 13 18 12
I 8.5 70 22.4 5.7 3.9 12 0.0 3.8 1.8 67 2.4 65 11 16 8
J 7.8 104 36.8 4.9 7.5 18 0.0 2.8 3.3 58 2.9 65 13 14 8
† Dissolved organic carbon.

The manures were applied as N fertilizer at a rate of 100 mg of organic matter, and increased the VFA content. A
total N kg⫺1 dry soil. The N2O and CO2 emissions from a high level of NSP enhances microbial activity in the gut
control treatment (i.e., no fertilizer) and a treatment with of pigs, favors the formation of VFA in excreta, and
NH4NO3 fertilizer (application rate 100 mg total N kg⫺1 dry lowers the pH. Canh et al. (1998b) found that increased
soil) were also determined. After 14 d, the moisture contents
levels of NSP in the pig diet increased the fecal contents
in both soils were increased to the liquid limit by adding 60 mL
water kg⫺1 soil for the sandy soil and 15 mL kg⫺1 for the of VFA and decreased the pH of the produced manure.
clayey soil (McBride, 1993). This was performed to simulate
a wet period with high potential for denitrification following Potential Emission of Methane
a relative dry period with high potential for mineralization and Ammonia during Storage
and nitrification. All treatments were performed in triplicate.
A lower protein content in the diet resulted in less
NH3 emission (comparison of Manures A vs. B and C
Statistical Analyses vs. D; Table 4). Adding acidifying salts reduced the NH3
Differences between treatments were statistically assessed emission at high crude protein contents (comparison of
using ANOVA and LSD. Linear regression analyses were Manures B and D), but had no effect at a low protein
carried to assess relations between the N and C losses and content (Manures A and B). The emission of NH3 was
chemical composition of the manures. All statistical analyses positively and significantly (P ⬍ 0.05) related to NH4
were performed with Genstat 5 (Genstat 5 Committee, 1993). content, total N content, and pH (Table 5). A multiple
linear regression model with NH4 content and pH as
RESULTS AND DISCUSSION explanatory variables explained 80% of the variance in
Effects of Dietary Composition on Chemical NH3 emission:
Composition of the Manure NH3 (g N kg⫺1 manure in 90 d) ⫽ ⫺2.64 ⫹ 0.397 ⫻
From a comparison between Manures A and B and NH4 (g N kg⫺1 manure) ⫹ 0.373 ⫻ pH
between Manures C and D it follows that a higher di-
The CH4 fluxes during anaerobic storage ranged from
etary protein content resulted in a higher pH, a higher ⬍0.01 to 0.25 L CH4 per kg manure per day (not shown).
total N content, similar total C content, and a higher
This is in the range of CH4 fluxes commonly found
fraction of NH4 in total N in the manure (Table 3). The during anaerobic fermentation of pig manure (Zeeman,
low manure N contents by low protein diets are due to
1991). The emission of CH4 was positively related to
low urinary N excretion. Canh et al. (1998a) showed contents of dry matter, total C, and VFA (Table 5).
that a lowered protein content in the pig diet decreased
The total emission of CH4 was smaller at lower protein
total N excretion up to 35%. This was caused by a de- content of the diet, especially for the non-acidified ma-
crease in urine N excretion. Excretion of fecal N was
not significantly affected by a lowered dietary protein Table 4. Potential emissions of NH3 and CH4 during storage (90 d
content. at 35ⴗC).
Differences between Manures A and C and between Treatment NH3 CH4
Manures B and D suggest that addition of acidifying
gN kg⫺1 manure g C kg⫺1 manure
salt resulted in a lower pH, a higher total N content, A 1.1 4.8
and a higher VFA content of the manure. The higher B 2.4 6.1
total N contents in acidified Manures B and D are proba- C 1.1 5.0
D 2.2 5.5
bly due to differences in N losses in the period before E 1.3 4.4
the manure was collected and in the activation period F 1.4 5.8
of three days. G 2.0 1.8
H 1.3 5.0
Increasing the content of NSP in the diet (comparison I 2.1 3.3
of Manures E and F, G and H, and B and I) decreased J 1.5 5.4
LSD0.05 0.2 0.7
pH, increased total C and N, increased the C to N ratio
 702 J. ENVIRON. QUAL., VOL. 34, MARCH–APRIL 2005

Table 5. Dependence of CH4 and NH3 emission from manures during storage on selected manure properties (regression analysis).
NH3 emission (g N kg⫺1) CH4 emission (g C kg⫺1)
Independent variable† Significance R2 Equation Significance R2 Equation
pH 0.016 0.54 Y ⫽ ⫺4.92 ⫹ 0.82X NS‡
DM content (g kg⫺1) NS 0.000 0.82 Y ⫽ ⫺0.44 ⫹ 0.05X
Total C content (g kg⫺1) NS 0.001 0.76 Y ⫽ 0.91 ⫹ 0.11X
Total N content (g kg⫺1) 0.012 0.57 Y ⫽ ⫺0.79 ⫹ 0.44X NS
Reproduced from Journal of Environmental Quality. Published by ASA, CSSA, and SSSA. All copyrights reserved.

NH4 content (g N kg⫺1) 0.001 0.77 Y ⫽ ⫺0.05 ⫹ 0.51X NS

VFA content (g kg⫺1) NS 0.021 0.51 Y ⫽ 1.93 ⫹ 1.31X
NH3 emission (g kg⫺1) – – – NS
† DM, dry matter; VFA, volatile fatty acids.
‡ Not significant when P ⬎ 0.05.

nure (comparison of Manures A and B and Manures C for degradable C. The potential denitrification rate was
and D; Table 4). This effect is likely related to the low also significantly related to the CO2 emission during
VFA content in the manures produced from the low aerobic soil incubation (Table 7). Production of CO2 in
protein diet (Table 3) as during anaerobic manure stor- soil is an indicator for respiration and for the amount
age VFA can be transformed into CH4 (Zeeman, 1991). of easily degradable organic material. Denitrifying bac-
The emission of CH4 increased at higher total contents teria use organic carbon as energy source and increasing
of NSP, especially when the content of fermentable NSP degradable C in the soil increases potential denitrifica-
was high (Manures E and F and G and H). Emission tion rate. Paul and Beauchamp (1989) showed that VFA
of CH4 was lowest for the manure derived from the diet are effective energy sources for denitrifiers. Because the
with lowest contents of NSP (Manure G) and this low manures in our study were applied at equal N rates,
emission is attributed to the low contents of total C and the highest denitrification potential were found for the
VFA in this manure (Table 3). manures with the highest ratio of C to N (Tables 3 and
Emissions of CH4 and NH3 from stored manure were 7). Changes in the diet that result in a high ratio of C
not related (Table 4) and have independent controlling to N, such as decreasing protein and/or increasing NSP,
factors. The emission of CH4 is controlled by the type increase the risk on denitrification losses when manure
and total amount of C in the manure, and of NH3 by is used as N fertilizer.
the type and amount N and by the pH of the manure
(Table 5). Potential Emission of Nitrous Oxide and
Carbon Dioxide after Soil Application
Potential Denitrification after Soil Application Potential emissions of N2O and CO2 were consider-
Denitrification in agricultural soil is unwanted be- ably higher from the unfertilized sandy soil than from
cause N is lost and it may give yield depression. More- the unfertilized clay soil (Fig. 2 and Table 6). This is
over, denitrification is a major source of the greenhouse probably caused by the higher denitrification potential
gas N2O. Application of manure strongly increased the in the sandy soil (Table 2), suggesting a higher content
potential denitrification of the soil (Table 6). From re- of degradable C in the sandy soil than in the clay soil.
gression analyses with the 10 manures it is concluded Also, the effect of manure addition on N2O emission
that the potential denitrification after manure applica- differed between the two soils. The N2O emission factors
tion to soil was positively related to the amounts of that were found are (much) higher than those generally
added VFA and total C, but not to the amount of added found under field conditions, especially for the sandy
dissolved organic carbon (DOC) (Table 7). The latter soil (e.g., Van Groenigen et al., 2004). In an incubation
result suggests that DOC in manure is not an indicator study there is no N uptake by the crop and no N is
Table 6. Potential emission of N2O and CO2 and potential denitrification following application of manures to soil.
Sandy soil Clay soil
N2O emission CO2 emission N2O emission CO2 emission
Amount Percent of Amount Percent of Amount Percent of Amount Percent of
Manure Potential denitrification in 44 d N applied† in 44 d C applied‡ in 44 d N applied† in 44 d C applied‡
mg N kg⫺1 soil d⫺1 mg N kg⫺1 soil % mg C kg⫺1 soil % mg N kg⫺1 soil % mg C kg⫺1 soil %
None 11 10.3 – 394 – 0.6 – 284 –
A 84 10.4 0.1 642 32 1.7 1.1 564 36
B 61 28.2 17.9 572 33 1.3 0.7 519 44
C 67 17.6 7.3 621 28 3.2 2.6 641 45
D 75 19.6 9.3 571 32 1.4 0.8 513 41
E 68 15.5 5.2 593 34 2.3 1.7 547 45
F 84 19.8 9.5 673 34 3.4 2.8 700 50
G 52 26.9 16.6 450 20 1.8 1.1 494 74
H 80 21.3 11.0 616 27 2.5 1.9 598 38
I 68 28.9 18.5 518 32 1.6 0.9 422 35
J 73 25.1 14.8 595 27 2.8 2.2 588 40
LSD0.05 14 6.1 – 39 1.3 33
† [(N2O–N emission treatment) ⫺ (N2O-N emission control)]/(N applied) ⫻ 100.
‡ [(CO2–C emission treatment) ⫺ (CO2–C emission control)]/(C applied) ⫻ 100.
 VELTHOF ET AL.: GASEOUS N AND C LOSSES FROM PIG MANURE 703

Table 7. Dependence of potential denitrification from the sandy piration rates coincide with a high oxygen consumption.
soil after application of manures on CO2 emission during aero- The oxygen content affects the N2 to N2O ratio of the
bic incubation and manure characteristics (regression analysis).
denitrification products (i.e., this ratio shifts toward N2
Independent variable† Significance R2 Equation when the soil becomes more anaerobic) (e.g., Weier et
Added DM, mg kg⫺1 soil 0.011 0.57 Y ⫽ 37.14 ⫹ 0.02X al., 1993). We suggest that the negative relationship
Added total C, mg C kg⫺1 soil 0.007 0.61 Y ⫽ 44.57 ⫹ 0.04X
Added DOC, mg C kg⫺1 soil NS‡ NS NS
between N2O and CO2 emissions in the sandy soil is
Added VFA, mg C kg⫺1 soil 0.050 0.40 Y ⫽ 19.86 ⫹ 0.96X caused by an increased respiration on application of
Reproduced from Journal of Environmental Quality. Published by ASA, CSSA, and SSSA. All copyrights reserved.

Total C to total N ratio 0.007 0.61 Y ⫽ 45.11 ⫹ 4.12X
CO2 emission, mg C kg⫺1 soil 0.003 0.69 Y ⫽ ⫺7.98 ⫹ 0.14X
† DM, dry matter; DOC, dissolved organic carbon; VFA, volatile fatty acid.
‡ Not significant when P ⬎ 0.05.
leached, thereby increasing mineral N contents in the
soil for a more prolonged period than in the field. There-
fore, the emission factors in Table 6 cannot be used for
estimation of manure N2O emission in the field.
Regression analyses showed that N2O emission from
the sandy soil was negatively correlated with the CO2
emission and the amounts of added VFA (Table 8). By
contrast, the N2O emission from the clayey soil was
positively related to the CO2 emission, and the amounts
of total C and DOC applied. The N2O emission from
the soils was not significantly related to the amount of
mineral N applied with the manures. The total C and
DOC contents and the potential denitrification were
much higher in the sandy soil than in the clayey soil
(Table 2) and this may be the reason for the observed
differences in manure-derived N2O emissions. High res-
manure and a subsequent shift in the N2 to N2O ratio
toward N2. We postulate that for the clayey soil addition
of degradable C with the manures more strongly af-
fected the potential denitrification than in the sandy soil
and that the effect of the enhanced potential denitrifica-
tion on N2O emission was larger than a shift in N2 to
N2O ratio. Chantigny et al. (2004) also pointed at effects
of soil type on transformations of applied pig slurry N.
Using 15N labeled pig slurry, they showed that soil type
significantly influenced the distribution of slurry N over
the various soil and plant pools. Nitrification was higher
in a sandy soil and ammonium fixation was higher in
the clayey soil. Though emissions of N2O were not mea-
sured in their study, the observed differences might re-
sult in different N2O emissions of applied slurry N.
The absence of straightforward effects of dietary com-
position on N2O emission from the produced manure
is most likely due to interactions with soil properties,
including degradable C contents and actual oxygen con-
sumption. These interactions strongly hamper a uniform

Fig. 2. Time course of N2O fluxes (left figures) and CO2 fluxes (right figures) from the sandy soil (upper figures) and clayey soil (lower figures).
Fluxes of the control, NH4NO3 fertilizer, and the manures with the lowest (A for the sand and B for the clay) and highest (I for the sand
and F for the clay) total N2O emission are presented. Fluxes of the other manures are within the range of the presented manures.
 704 J. ENVIRON. QUAL., VOL. 34, MARCH–APRIL 2005

Table 8. Dependence of N2O and CO2 emission in 44 d after soil application of manures on the added amounts of dry matter (DM),
mineral N, total C, dissolved organic carbon (DOC), and volatile fatty acid (VFA) (regression analysis). All manures were applied
at a total N rate of 100 mg N kg⫺1.
Sandy soil Clay soil
Dependent
variable Independent variable Significance R2 Equation Significance R2 Equation
N2O emission CO2 emission (mg C kg⫺1 soil) 0.043 0.42 Y ⫽ 56.94 ⫺ 0.06X 0.001 0.75 ⫺2.57 ⫹ 0.009X
(mg N kg⫺1 soil) DM (mg kg⫺1) NS† 0.022 0.50 ⫺0.19 ⫹ 0.001X
Reproduced from Journal of Environmental Quality. Published by ASA, CSSA, and SSSA. All copyrights reserved.

mineral N (mg N kg⫺1) NS NS

total C (mg C kg⫺1) NS 0.026 0.48 0.44 ⫹ 0.003X
DOC (mg C kg⫺1) NS 0.018 0.53 ⫺0.08 ⫹ 0.04X
VFA (mg C kg⫺1) 0.021 0.51 Y ⫽ 54.81 ⫺ 0.62X NS
CO2 emission DM (mg kg⫺1) 0.000 0.86 Y ⫽ 328 ⫹ 0.14X 0.001 0.78 Y ⫽ 257 ⫹ 0.17X
(mg C kg⫺1 soil) mineral N (mg N kg⫺1) 0.036 0.44 Y ⫽ 859 ⫺ 4.61X 0.049 0.40 Y ⫽ 882 ⫺ 5.43X
total C (mg C kg⫺1) 0.000 0.88 Y ⫽ 389 ⫹ 0.31X 0.002 0.73 Y ⫽ 339 ⫹ 0.35X
DOC (mg C kg⫺1) 0.047 0.41 Y ⫽ 420 ⫹ 2.88X 0.005 0.64 Y ⫽ 304 ⫹ 4.46X
VFA (mg C kg⫺1) 0.015 0.55 Y ⫽ 216 ⫹ 6.88X NS
† Not significant when P ⬎ 0.05.

strategy to mitigate N2O emission from soil-applied pig
manure by manipulation of the diet. Soil-specific recom-
mendations are thus required, but these recommenda-
tions demand a thorough understanding of the effects
of soil and manure composition and their interactions
on N2O emission.
Manure as a Source of Organic Matter
Organic matter in soils controls chemical, physical,
and biological soil fertility. Soil organic matter is micro-
bially degraded and organic matter should be added to
the soil via manure and crop residues to maintain or
increase the organic matter content. Manures consist of
organic matter that is a mixture of readily degradable
and more stable organic matter. The “stable” organic
matter in manure is a prime source of soil organic mat-
ter. Stable organic matter is defined in the current study
as the organic matter that is not emitted as CO2 within
44 d of aerobic soil incubation at 20⬚C. Figure 3 shows
large differences in the amounts of added stable organic
matter between the 10 manures. At an equal N applica-
tion rate, the amount of added stable organic matter
was highest for manures produced with diets with high
content of NSP (Manures F and H) or low content of
crude protein contents (Manures A and C). Sørensen
and Fernandez (2003) found a significant relationship
between the C mineralization of pig slurry and the total
content of fibers. However, the crude protein content
was not significantly related to slurry C mineralization
in their study. The dietary crude protein contents were
generally lower and the total C contents and the C to
N ratio of the manures higher in the current study than

Fig. 3. Amounts of applied stable and easily mineralizable organic C added to soil by manure at a rate of 100 mg N per kg soil. Easily mineralizable
C is defined as the C that mineralized during aerobic incubation for 44 d at 20ⴗC, while stable C is defined as the C that remained after this
incubation (see Table 6). The left bars are results for the sandy soil and the right bars for the clay soil.
 VELTHOF ET AL.: GASEOUS N AND C LOSSES FROM PIG MANURE 705

in the study of Sørensen and Fernandez (2003). This
may have contributed to the different effect of crude
protein content on C mineralization of soil-applied
slurry. Recommendations for farmers to apply organic
matter to their soil are often based on a default manure
composition. The results of Fig. 3 indicate that insight
in the diet or chemical composition of the manure would
Reproduced from Journal of Environmental Quality. Published by ASA, CSSA, and SSSA. All copyrights reserved.
content the value of the manure as soil conditioner
increased. However, this was at the expense of the N
fertilizer value of the manure, because the risk on N
losses by denitrification increased and the amount of
directly plant-available N decreased. If the amount of
applied plant-available manure N is not sufficient to
meet crop demand, farmers may choose to apply addi-

enhance the validity of prognoses on effectiveness of
using pig manure to maintain or increase levels of soil
organic matter.
Integral Effects of Dietary Composition
We have shown that diet affects both the amount and
composition of N and C in pig manure and thereby the
potential gaseous N and C emissions, the amount of
directly plant-available N, and the value of the manure
as soil conditioner (i.e., source of stable organic matter).
Changing the diet to decrease one specific gaseous emis-
sion may result in an unwanted increase in another
gaseous emission (Fig. 4). A lower dietary protein con-
tent decreased potential emissions of NH3 and CH4 from
storage and potential N2O emission from the sandy soil,
but increased potential denitrification of the sandy soil
and potential N2O emission from the clayey soil (Fig. 4).
This illustrates the potential to achieve lower emissions
of CH4, NH3, and N2O from pig manure by decreasing
the protein content of the feed. At lower dietary protein
tional chemical N fertilizer. The pigs need protein in
terms of amino acids rather than in terms of total crude
protein. There is a clear scope for farmers to lower dietary
crude protein content by optimizing the diet composition
and by supplementing essential amino acids to the pig
diet with no effect on animal performance (Jongbloed
and Lenis, 1998).
The effect of the other tested diet manipulations were
smaller and show partly opposite effects on the emis-
sions (Fig. 4). Adding salts affected emissions and com-
position of the manure to a lower extent than decreasing
protein content. Increasing the content of total NSP
strongly increased the CH4 emission from the manure
during storage (Fig. 4). The effects on NH3 and N2O
emissions were relatively small in comparison with the
effect on CH4. A higher content of fermentable NSP
strongly decreased emission of CH4, but increased emis-
sions of NH3 and N2O from the sandy soil. The amount
of stable organic matter was also smaller at higher con-
tents of fermentable NSP.

Fig. 4. Effects of lowered protein content (comparison of Manures B and A), adding acidifying salt (Manures B and D), increasing total nonstarch
carbohydrate contents (Manures I and B), and fermentable nonstarch carbohydrate content (Manures E and G) on potential NH3 and CH4
emission during anaerobic storage, denitrification potential (DNP) after soil application, potential N2O emission after application to a sandy
and clayey soil, the content of mineral N in the manure, and the content of stable organic matter (OM) in the manure (i.e., the residual
organic matter after incubation of manure in soil at 20ⴗC during 44 d).
 706 J. ENVIRON. QUAL., VOL. 34, MARCH–APRIL 2005
CONCLUSIONS
Manipulation of the diet of pigs strongly affected the
composition of the manure, the potential NH3 and CH4
emissions during storage, potential N2O and CO2 emis-
sion after soil application, the content of plant-available
N, and the value of the manure as source of stable
organic matter. From the tested diets, decreasing the
Reproduced from Journal of Environmental Quality. Published by ASA, CSSA, and SSSA. All copyrights reserved.
crude protein content of the diet had the largest poten-
tial to simultaneously decrease NH3 and CH4 emissions
during manure storage and N2O emission from soil. The
effect of manure composition on N2O emission mark-
edly differed between the two tested soils, which points
at interactions with soil properties such as the organic
matter content. These types of interactions require soil-
specific recommendations for mitigation of N2O emis-
sion from soil-applied pig manure by manipulation of
the diet. Field trails in combination with modeling will
provide insight in the overall agricultural and environ-
mental performance of soil-applied manure. An integral
assessment of the environmental and agricultural impact
of handling and application of pig manure as a result
of diet manipulation provide opportunities for farmers
to maximize the value of manures as fertilizer and soil
conditioner and to minimize N and C emissions to the en-
vironment.
ACKNOWLEDGMENTS
We acknowledge Willeke van Tintelen for invaluable tech-
nical assistance during incubation studies and Gertruud Bak-
ker for providing the pig manures. This study was financed
by the Dutch programme ROB (Reduction programme on
non-CO2 greenhouse gases) under Contract 374299/0021 of
NOVEM and the Dutch Ministry of Agriculture, Nature and
Food Quality (Programme 415).
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