Applications of stable isotope ratio mass spectrometry in cattle dung carbon cycling studies

RAPID COMMUNICATIONS IN MASS SPECTROMETRY

Rapid Commun. Mass Spectrom. 2010; 24: 495–500

) DOI: 10.1002/rcm.4332
Published online in Wiley InterScience (www.interscience.wiley.com
Applications of stable isotope ratio mass spectrometry in

cattle dung carbon cycling studiesy

Jennifer A. J. Dungait1*, Roland Bol1, Elisa Lopez-Capel2, Ian D. Bull3, David Chadwick1,

Wulf Amelung4, Steven J. Granger1, David A. C. Manning2 and Richard P. Evershed3

1Soil Cross Institute Programme, North Wyke Research, Okehampton EX20 2SB, UK2School of Civil Engineering and Geosciences, Drummond Building, University of Newcastle, Newcastle upon Tyne NE1 7RU, UK3Organic Geochemistry Unit, Bristol Biogeochemistry Research Centre, School of Chemistry, University of Bristol, Cantock’s Close, Bristol BS8

1TS, UK4INRES-Bodenwissenschaften, University of Bonn, Nusallee-13, D-53115 Bonn, Germany

Received 31 July 2009; Revised 7 October 2009; Accepted 8 October 2009

*Correspogramme,E-mail: jeyPresenteUniversit

Understanding the fate of dung carbon (C) in soils is challenging due to the ubiquitous presence of the

plant-derived organic matter (OM), the source material from which both dung-derived OM and soil

organic matter (SOM) predominantly originate. A better understanding of the fate of specific

components of this substantial source of OM, and thereby its contribution to C cycling in terrestrial

ecosystems, can only be achieved through the use of labelled dung treatments. In this short review, we

consider analytical approaches using bulk and compound-specific stable carbon isotope analysis that

have been utilised to explore the fate of dung-derived C in soils. Bulk stable carbon isotope analyses

are now used routinely to explore OM matter cycling in soils, and have shown that up to 20% of

applied dung C may be incorporated into the surface soil horizons several weeks after application,

with up to 8% remaining in the soil profile after one year. However, whole soil d13C values represent

the average of a wide range of organic components with varying d13C values andmean residence times

in soils. Several stable 13C isotope ratio mass spectrometric methods have been developed to qualify

and quantify different fractions of OM in soils and other complex matrices. In particular, thermo-

gravimetry-differential scanning calorimetry-isotope ratio mass spectrometry (TG-DSC-IRMS) and

gas chromatography-combustion-IRMS (GC-C-IRMS) analyses have been applied to determine the

incorporation and turnover of polymeric plant cell wall materials from C4 dung into C3 grassland soils

using natural abundance 13C isotope labelling. Both approaches showed that fluxes of C derived from

polysaccharides, i.e. as cellulose or monosaccharide components, were more similar to the behaviour

of bulk dung C in soil than lignin. However, lignin and its 4-hydroxypropanoid monomers were

unexpectedly dynamic in soil. These findings provide further evidence for emerging themes in

biogeochemical investigations of soil OMdynamics that challenge perceived concepts of recalcitrance

of C pools in soils, which may have profound implications for the assessment of the potential of

agricultural soils to influence terrestrial C sinks. Copyright # 2010 John Wiley & Sons, Ltd.

Natural abundance stable 13C isotope labelling is one of the

few proven techniques available for the examination of soil C

dynamics in naturally functioning ecosystems. Compared

with 14C radioisotope labelling, it is a safe and cost effective

method that gives an accurate interpretation of processes in

complex systems, such as soils. Isotope ratio mass spec-

trometry (IRMS) is widely used to determine the difference

in natural abundance of 13C between C3 (d13C¼�32 to

�20%) and C4 (d13C¼�9 to �17%) vegetation which

provides the basis for estimating the contribution of 13C-

enriched C4 sources to soil organic matter (SOM) in

ecosystems otherwise dominated by C3 vegetation.1 Follow-

ndence to: J. A. J. Dungait, Soil Cross Institute Pro-North Wyke Research, Okehampton EX20 2SB, [email protected] at SIMSUG 2009, held 14–15 January 2009 at they of Glasgow.

ing changes in land use from a C3 to C4 vegetation, bulk SOM

d13C values have been used to investigate organic matter

(OM) turnover in soils,2 particle size fractions3,4 and soil

aggregates.5 Naturally, the d13C values of cattle products

reflect the stable isotope values of their feed;6 therefore, cattle

that are fed naturally 13C-enriched C4 species forage, i.e. Zea

mays, produce a convenient source of natural abundance 13C-

labelled dung that can be applied as a treatment to soils in C3

ecosystems to explore the cycling of dung C. Thus, by using

bulk and compound-specific IRMS, the spatiotemporal

dynamics of whole dung C cycling, and that of specific

biochemical components of dung in the soil, can be

determined.

The mean residence times of C pools have been shown to

increase with the application of manure.7 In the Hoosfield

Classical Experiment at Rothamsted, annual applications of

manure at a rate of 35 t ha�1 over 140 years resulted in a three-

Copyright # 2010 John Wiley & Sons, Ltd.

496 J. A. J. Dungait et al.

fold increase in soil organic C levels over that in unfertilised

plots, and about 50% higher than in unfertilised plots 104

years after manure addition had been discontinued.8 This

and other long-term studies (20–120 years) in the UK,

Denmark, USA and Canada have indicated that manure can

play a positive role in increasing soil C stocks in soils.9

However, other studies have concluded that dung appli-

cation may have a limited effect10,11 or indeed a negative

effect on soil C sequestration.12 Clearly, the dynamics of

incorporation of dung C into soil are not well understood,

but they are known to be highly variable in both space and

time.13,14 The time taken for 75% of cow dung to disappear is

reported to range from 32 to 450 days;15 the initial quality of

dung affects rates of decay,16 and environmental variables,

such as temperature and rainfall, strongly influence

decomposition.13

Although many studies have determined the concen-

trations of inorganic components in dung and dung-treated

soils that directly affect plant growth, e.g. N, P, K, Mg and

Ca,17–20 or act as pollutants,21–23 e.g. heavy metals,24,25

relatively little work has been carried out to identify and

quantify the biochemical components that contribute to

SOM. Cow dung is a complex mixture of biochemical

components that are likely to decompose at different rates

(Fig. 1). Gravimetric procedures are the most widely applied

to estimate the contribution of different biochemical fractions

to dung and studies have shown that the major component is

undigested lignocellulosic plant cell wall material.26 Haynes

and Williams27 reported that cattle dung comprised 47–68%

‘fibre’ (the sum of hemicellulose, cellulose and lignin), and

Dungait et al.28,29 estimated that cow dung derived from

Lolium perenne and Z. mays forages was 20–30% hemicellu-

lose, 20–30% cellulose, 7% lignin, 12% crude protein and

3–5% fats using the ‘Forage Fibre Analysis’ procedure

described by Van Soest.26 Currently, no reliable estimates

exist for the concentration of dung lignin due to the

challenges presented by extraction of monomers with

subsequent quantification against an internal standard.

Analyses of dung carbohydrates analysed as alditol acetates

using gas chromatography (GC) determined concentrations

of up to 80% dry weight as sugars in dung due to the

inclusion of the soluble components, which may also derive

from microbial debris, lost during Forage Fibre Analysis.30

Figure 1. Ruminant digestion and the origin of faecal matter,

showing major components of dung (adapted from Van

Soest26).


Bull et al.31 investigated the lipid components of farmyard

manure (FYM) in order to assess the effect that variable

manure application has on the free lipid content of the soil.

The lipids in dung were dominated by 5b-stanols and C26 n-

alkanol, with relatively minor contributions from carboxylic

acids, wax esters and n-alkanes.

Different components of plant-derivedOM are also known

to have a range of d13C values due to fractionations against

the heavier isotope during biosynthesis. Lignin and lipids are

depleted compared with bulk plant tissue, while cellulose

and hemicellulose are 1–2% more 13C-enriched.1,32 Dungait

et al.33 used off-line pyrolysis to extract lignin monomers

from dung and dung-treated soils for stable 13C-isotope

analysis using GC-combustion-IRMS (GC-C-IRMS). The m/z

44 ion current and the instantaneous ratio of m/z 45/44 ions

recorded for the off-line pyrolysate of lipid-extracted C4

dung, displaying base-line resolved pyrolysis products for

which compound-specific d13C values could be obtained, are

shown in Fig. 2. Dung lignin-derived moieties in the

pyrolysate were up to 7% 13C-depleted relative to bulk

dung, although syringol and 4-vinylguaiacol were 13C-

enriched by up to 4% and 2%, respectively. The 13C-depleted

values are in agreement with earlier studies, which indicated

that plant tissues yield lignin products 2–7% depleted in 13C

comparedwith whole tissue, although Kracht and Gleixner34

determined up to 5% 13C-enrichment of lignin moieties

compared with bulk values in lignin pyrolysates of peat. The

d13C values determined for lipids as n-carboxylic acids

(iC14:0–C30:0) extracted from C3 and C4 dung (Fig. 3) also

showed depletion of up to ca. 6% compared with bulk dung,

with increasing depletion with hydrocarbon chain length in

very long chain fatty acids (VLCFA) >C20.28 Carbohydrate

d13C values determined for arabinose, xylose, galactose and

glucose extracted from C4 dung and analysed as their alditol

acetates were �10.4� 0.5%, �10.4� 0.4%, �8.3� 1.6% and

�11.5� 0.6%, respectively (bulk d13C value �12.6� 0.3%),

which are similar to values reported for Z. mays leaf by

Derrien et al.,35 and values for C3 dung �26.8� 1.1%,

�28.7� 0.9, �27.4� 2.6% and �29.9� 0.7% (bulk d13C value

�31.3� 0.1%) were similar to those derived from ryegrass

(L. perenne28). The variability in concentration and d13C

values between individual components of dung-derived OM

drives the need to develop and apply sensitive tools to

determine their contribution to bulk values in order to

understand C cycling in soils treated with manures as soil

improvers or under livestock management.

Bulk stable 13C isotope IRMSNatural abundance 13C-labelled C4 plant matter can be

applied to restricted areas of experimental plots, and is

especially useful for short-term bulk decomposition studies.

Amelung et al.36 and Bol et al.37 developed a method using the

difference in natural abundance 13C values between C4 dung

(d13C¼�15.4%) andC3 dung (d13C¼�25.6%) applied to a C3

soil (d13C¼�27.9%) in trace bulk dung C incorporation into

soils using continuous flow (CF)-IRMS. Bulk d13C values of C3

and C4 dung-treated soil were used in a simple mixing model

to estimate dung C incorporation after dung deposition. This

approachwas also used to trace dung-derived C into soils,29,37

soil particulate size fractions,38,39 and leachates.37,40 The


DOI: 10.1002/rcm

Figure 2. The m/z 44 ion current (above) and instantaneous ratio of m/z 45/44 ions

(below) recorded for the off-line pyrolysate of lipid-extracted C4 dung derived from Zea

mays silage showing base-line-resolved pyrolysis products analysed as their trimethyl-

silylated derivatives using GC-C-IRMS.28

Applications of IRMS in cattle dung C cycling studies 497

percentage of applied dung C that had been incorporated into

the soil was estimated using stable C-isotope determinations.

A maximum of 20% and 12% dung C was determined in the

top 5 cm soil horizon of dung-treated soils after autumn37 and

Figure 3. d13C values of fatty acids extracted

methyl esters using GC-C-IRMS.24


spring29 applications, respectively. In the autumn, the

incorporation of dung C was more rapid and fluctuated

more widely than after spring application (Fig. 4).29,36,37 After

372 days in the spring experiment, 8% of the dung-derived C

from C3 and C4 dung analysed as their


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Figure 4. Comparison of data from dung application exper-

iments after autumn and spring deposition showing differential

incorporation of percentage applied dung C between seasons

calculated using bulk d13C stable isotope determinations ana-

lysed using CF-IRMS (adapted from Dungait et al.33).

Figure 5. Proportion of dung-derived C incorporation in C3

and C4 dung-treated soils at various temperature intervals

during thermal decomposition estimated using TG-DSC-

IRMS.49


remained in the soil, providing direct evidence for the

mechanism for increasing C stocks in soils treated annually

with manures. Amelung et al.36 traced dung-derived C into

particle-size fractions in the top 1–5 cm of soil. As the particle

size diameter increased, the d13C values increased. The

proportion of dung C in fine clay (<0.2mm) maximised after

42 days, coinciding with a maximum in the bulk soil d13C

values and leaching rate. Thepercentage of particulateC in the

coarse sand fraction (250–2000mm) increased until the end of

the experiment, and it was suggested that undigested

polyphenolic substances, such as lignin, contributed an

increasing proportion to dung-derived C.

Due to the diversity in the decomposition dynamics and

the d13C values of individual biochemical components of

dung, fluxes in bulk d13C values in C4 dung-treated soil may

not imply a total loss or gain of dung C. For instance,

depletion in bulk d13C values may simply provide evidence

for the decline of labile, relatively 13C-enriched dung-derived

components, such as carbohydrates, from the soils. Indeed,

initial characterisation of components (NDF, ADF, ADF-

lignin, Kjedahl N and fats) of C4 and C3 dung using forage

fibre analysis29 and GC analysis of polysaccharides,30

lignin33 and lipid28 fractions of C3 and C4 dung revealed

differences between the composition of the two dung types

which may have affected the parity of their incorporation

into soil. Therefore, the later study of dung incorporation

after spring application29 used the d13C values of bulk soil

and individual compounds extracted from C4 dung-treated

and untreated (control) soils as end members in the mixing

model to estimate dung C incorporation and turnover. Thus,

it is essential that the contributions of individual biochemical

components to bulk dung C, and the residence times of those

individual components in the soil, are investigated in order

to adequately understand spatiotemporal fluxes of C in

dung-treated soils.

Compound-specific stable 13C-isotope IRMSThe most abundant constituents of soil C are carbohydrates

derived from the endogenous plant litter that comprises up

to 50% of SOM. Recent studies have questioned both the


perceived lability of carbohydrates in soils35,41,42 and the

recalcitrance of lignin,33,43–46 suggesting that carbohydrates

have a considerable role to play in C sequestration in soils.

Plant cell walls are the major components of dung and SOM

in grassland systems, but their identification and quantifi-

cation pose analytical challenges due to the chemically

intractable nature of lignin and polysaccharide polymers,

and their ubiquitous nature in edaphic systems. Here, the

application of two complementary compound-specific stable

isotope approaches: (1) thermogravimetry-differential scan-

ning calorimetry-IRMS (TG-DSC-IRMS) and (2) GC-C-IRMS

to the investigation of dung C dynamics in grassland soils,

are considered.

TG-DSC-IRMSThermogravimetry (TG) combined with differential scan-

ning calorimetry (DSC) has been applied to explore the

chemical changes in OM during decomposition, especially

with regard to the composition of the bulk constituents of

degrading plant material.47–49 TG-DSC analysis involves

continuous and simultaneous measurement of weight-loss

(TG) and energy change (DSC) during heating. Exothermic

decomposition of aliphatic and carboxyl groups predomi-

nates at temperatures of 300–3508C, with more refractory

aromatic C being lost at higher temperatures of around 400–

4508C. Coupled to IRMS this analytical approach allows the

d13C values of volatile organic components evolved during

heating to be determined during a single heating experiment,

providing valuable insights into the dynamics of labile and

recalcitrant components of SOM.

Lopez-Capel et al.50 applied TG-DSC-IRMS to describe and

characterise the changes in C4 dung-derived C over 70 days

after autumn application of dung in the same grassland soil

previously analysed using CF-IRMS (see above). d13C values

were more depleted with increasing combustion tempera-

tures, with cellulosic components being around 4% more13C-enriched than more refractory components, i.e. lignin.

Using the dung C incorporation equation,29 the percentage of

dung C incorporated into soil using the exothermic peak

between 400–4508C suggestedmajor incorporation of dung C

after 40 days in line with the bulk isotope study described

(Fig. 4). However, Fig. 5 also illustrates that aromatic dung C


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Figure 6. d13C values for xylose extracted from 0–1 cm (top)

and 1–5 cm (bottom) soil horizons of control and C4 dung-

treated soils 7, 14, 28, 56, 12, 224 and 372 days after spring

application, determined using GC-C-IRMS.25

Applications of IRMS in cattle dung C cycling studies 499

was degraded relatively rapidly between 40 and 70 days after

incorporation into the soil, with biphasic loss of different

aromatic organic components indicated by different straight

line relationships of the exothermic peaks at 4008C and

4508C. The component indicated by the exothermic peak at

4508C shows a loss from ca. 43% (40 days) to 18% (70 days),

while the percentage of the aromatic component indicated by

the 4008C exothermic peak appears to be stabilised. This

supports the conclusions of recent work by Bahri et al.43 and

Dungait et al.33 that lignin turnover in soils is monomer-

specific.

GC-C-IRMSThe use of GC techniques to investigate the turnover of

specific monomers of dung-derived OM is constrained by

the challenge of isolating representative monomers of

polymers for analysis that are properly resolved in order to

obtain robust compound-specific d13C values using GC-C-

IRMS. Lignin is particularly difficult to analyse due to its

apparently highly random, macromolecular structure that

requires relatively harsh heat and/or chemical treatment to

release monolignols for analysis. In studies of dung-

derived lignin in soil, off-line pyrolysis has been used to

successfully isolate lignin derivatives from dung (Fig. 2)

and dung-treated soil for GC-C-IRMS.33 This revealed

that the incorporation, degradation or transformation of

lignin in soils varied between individual constituents of

lignin, thereby supporting the hypothesis that lignin

turnover in soils is monomer-specific. The analyses also

suggested that the turnover of lignin in the soil is relatively

rapid, although lignin moieties with propene side chains

appear to be relatively stable after one year. The finding

that dung contains a range of components, including

lignin, with different degradation dynamics in soils,

supports the conclusions of the TG-DSC-IRMS study

described above.

The major components of dung are carbohydrates derived

from the plant cell wall, i.e. cellulose and hemicelluloses. The

concentrations and d13C values of individual monosacchar-

ides glucose, xylose, arabinose, galactose and mannose

extracted from the soil in a recent study showed that

the incorporation and turnover of dung carbohydrates were

dynamic and complex, and varied between monosaccharide

types,30 as was also observed in a short-term study of slurry

carbohydrate incorporation using similar analytical

approaches.51 A maximum of 60% of the dung C in soil

was derived from carbohydrates at peak dung C incorpora-

tion 56 days after spring application. Like the TG-DSC-IRMS

study previously described, the dynamics of total dung-

derived monosaccharides in the top 5 cm of the soil were

comparable with the incorporation and flux of bulk dung C,

previously estimated using bulk d13C values (Fig. 4). These

compound-specific d13C values indicated the persistence of

dung-derived monosaccharides in soils. In fact, a significant

increase in xylose and arabinose d13C values at the end of the

experiment suggested reintroduction of these pentose sugars

into the top horizon of the soil (Fig. 6 shows the d13C values of

dung-derived xylose in soils up to 372 days after spring

application of C4 dung). This demonstrates the unique

ability of stable isotope methodology to track ubiquitous


compounds in field-scale experiments for over a year, even at

the natural abundance level.

CONCLUSIONS

This short review has shown the value of stable isotope

approaches in the study of dung C fluxes in soils. The

production of natural abundance 13C-labelled experimental

dung is straightforward through the use of a C4 grass diet

fed to cattle to produce C4 dung. The controlled application

of C4 dung to soil in discrete field plots allows the C

dynamics in the associated environment to be explored

through the use of IRMS to differentiate between dung-

derived OM and SOM. Bulk stable isotope determinations

are useful for assessing gross incorporation of dung C into

surface soil horizons, but they can only be used as an

estimate due to the known error associated with the variety

of individual organic components that contribute to bulk

d13C values. The application of compound-specific stable13C-isotope IRMS methods, such as TG-DSC-IRMS and

GC-C-IRMS, enhance the understanding of dung C turn-

over by revealing the differential turnover dynamics of

individual C4 dung-derived biomolecules. Both approaches

allow the major organic components of dung derived from

plant cell wall polymers, i.e. lignin and polysaccharides, to

be tracked from dung into soil over time. These

complementary techniques have shown that dung-derived

lignin is comparatively dynamic in surface soil horizons

compared with carbohydrate components of dung, i.e.

xylose, glucose, arabinose and galactose. These findings

provide further evidence for emerging themes in biogeo-

chemical investigations of soil OM dynamics that challenge

perceived concepts of the recalcitrance of C pools in soils,

which may have profound implications for the assessment

of the potential of agricultural soils to influence terrestrial C

sinks.


DOI: 10.1002/rcm


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DOI: 10.1002/rcm

Applications of stable isotope ratio mass spectrometry in cattle dung carbon cycling studies

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