© 2006 Nature Publishing Group
Temperature sensitivity of soil carbon
decomposition and feedbacks to climate
Eric A. Davidson1& Ivan A. Janssens2
Significantly more carbon is stored in the world’s soils—including peatlands, wetlands and permafrost—than is present in
the atmosphere. Disagreement exists, however, regarding the effects of climate change on global soil carbon stocks. If
carbon stored belowground is transferred to the atmosphere by a warming-induced acceleration of its decomposition, a
positive feedback to climate change would occur. Conversely, if increases of plant-derived carbon inputs to soils exceed
increases in decomposition, the feedback would be negative. Despite much research, a consensus has not yet emerged
on the temperature sensitivity of soil carbon decomposition. Unravelling the feedback effect is particularly difficult,
because the diverse soil organic compounds exhibit a wide range of kinetic properties, which determine the intrinsic
temperature sensitivity of their decomposition. Moreover, several environmental constraints obscure the intrinsic
temperature sensitivity of substrate decomposition, causing lower observed ‘apparent’ temperature sensitivity, and
these constraints may, themselves, be sensitive to climate.
topic is high because of its importance in the global carbon (C) cycle
and potential feedbacks to climate change15. This recent controversy
has focused primarily on organic matter in upland mineral soils.
These soils have reasonably good drainage and aeration, allowing
rootsand soil fauna to penetrate intomineral soil layers,thus mixing
SOM with mineral particles. Conditions in upland mineral soils are
also generally favourable for decomposition, resulting in relatively
low carbon densities. In contrast, in wetlands and peatlands where
anaerobic conditions frequently persist, decomposition proceeds
much more slowly, and deep layers of organic matter accumulate
on top of mineral layers. In soils with permanently frozen layers
(permafrost), drainage is also often poor, and organic matter may
become buried in deep soil layers through cryoturbation16. Thus,
wetlands, peatlands and permafrost soils generally contain higher
carbon densities than upland mineral soils, and together they make
up enormous stocks of carbon globally (Table 1). Moreover, perma-
where warming is expected to be greatest, and, indeed, has already
begun17,18. In this review, we emphasize that decomposition of all
types of belowground organic matter should be described by a
common set of principles of kinetic theory and environmental
constraints. Our objective is to clarify the issues regarding tempera-
ture sensitivity of decomposition within a framework that helps to
focus the ensuing debate and research.
he temperature sensitivity of decomposition of the enormous
global stocks of soil organic matter (SOM)1–4has recently
received considerable interest, including several high-profile
publications supporting opposing views5–14. Interest in this
Factors controlling decomposition of organic matter
The stocks of organic matter in soils result from the balance between
inputs and outputs of carbon within the belowground environment
(Fig.1).Inputs are primarily fromleafandrootdetritus. Outputs are
dominated by the efflux of carbon dioxide (CO2) from the soil
surface, although methane (CH4) efflux and hydrologic leaching of
dissolved and particulate carbon compounds can also be important.
The production of CO2 in soils is almost entirely from root
respiration and microbial decomposition of organic matter. Like
all chemical and biochemical reactions, these processes are tempera-
ture-dependent. Root respiration and microbial decomposition are
also subject to water limitation. Hence, most empirical models relate
the efflux of CO2from soils (often lumping microbial and root
respiration together as ‘soil respiration’) to temperature and often
also to some scalar of soil water content or precipitation19–24. This
much is not controversial.
controversial. Activation energies are related to the ambient tempera-
ture and to the molecular structure of the organic-C reactant. The
Table 1 | Sizes and vulnerabilities of belowground carbon stocks
Carbon ‘pool’ Global
of size (Pg)
Potential loss by
2100 due to global
Upland soil inventory (3m depth)
Simulated upland soil (litter layer)
Simulated upland soil
(mineral layer to 1m depth)
Peatlands (3m depth)
Permafrost (3m depth)
Although the estimates here are highly uncertain (all estimates are rounded to one
significant figure), they help to frame the debate about the relative importance of each
type of belowground carbon as a potential feedback to climate change over the next few
1The Woods Hole Research Center, PO Box 296, Woods Hole, Massachusetts 02543, USA.2Department of Biology, University of Antwerpen, Universiteitsplein 1, B-2610,
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© 2006 Nature Publishing Group
Box 1|Must the Q10of decomposition equal 2?
The Q10for a reaction rate is defined as the factor by which the rate
increases with a 108 rise in temperature. A rule of thumb widely
accepted in the biological research community is that the rate of
decomposition of SOM, like any other biological reaction rate, tends
to double for every 108 rise in temperature (that is, the Q10of
decomposition is two). The origin of this rule-of-thumb, however,
and the limits to its validity are less well known. Early experiments by
van ’t Hoff and colleagues indicated that, around room temperature,
reaction rates “roughly double or triple” for every 108 rise in
temperature (that is, reaction rates have Q10values of the order of
two to three)84. Thus, historically, there has never been any
suggestion that the Q10should equal two on the basis of first
principles. Moreover, an exponential equation does not always
provide the desired relationship between the reaction rate and the
temperature. Arrhenius noticed that a Q10as high as two or three
cannot originate from the increasing frequency of collisions between
the reacting molecules, which only increases by about 1.5% for every
108 rise in temperature. Arrhenius also noticed that chemical
reactions, even exergonic ones, often require a little ‘push’ to
proceed, which he called the “activation energy” (Ea). He concluded
that the explanation for the unexpected high temperature sensitivity
of reaction rates had to be found in the amounts of reactants that
possessed sufficient energy to react. Although the actual
concentration of a reactant may be relatively constant with
temperature, the active fraction that actually takes part in the
reaction increases rapidly with temperature. Thus, Arrhenius
developed the following equation85: k ¼ aexp(2Ea/RT) where k is
the reaction rate constant; a is a frequency or pre-exponential factor
(that is, the theoretical reaction rate constant in the absence of
activation energy); Eais the required activation energy; R is the gas
constant (8.314JK21mol21); and T is the temperature in Kelvin. The
term exp(2Ea/RT) determines for any given temperature the
fraction of the molecules present with energies equal to or in excess
of the required activation energy. The Arrhenius function reveals
some important properties of the reactions that it describes. For
reactants with an Eaaround 50kJmol21, and at temperatures
between 273K and 303K, the Q10of a chemical reaction is
around two (Box 1 Figure, upper panel), in agreement with the
rule-of-thumb cited above. However, the Arrhenius equation also
predicts that the Q10of chemical reactions decreases with
increasing temperature (in Box 1 Figure, upper panel), as is also
commonly observed in nature86. The theoretical explanation for the
decrease in Q10with increasing temperature is that as temperature
increases, there is a declining relative increase in the fraction of
molecules with sufficient energy to react. The Arrhenius function
also shows that reactants with higher activation energies (that is,
less reactive and more recalcitrant) should have higher temperature
sensitivities (Box 1 Figure, upper panel). Hence, theoretical and
experimental evidence shows that the Q10of decomposition equals
two only under specific conditions.
Box 1 Figure | Surface plots of the effects of temperature and activation
Reaction rate constants are presented relative to that of glucose at room
temperature. For clarity, the logarithm of this value is indicated. The red
arrows indicate increasing trends and the blue arrows indicate decreasing
trends. That the arrows switch colour between the two panels indicates
that both temperature and activation energy have opposite effects on Q10
and on the reaction rate. The letters represent glucose (G) and tannin (T)
inthese graphicpresentationsof theQ10andreaction rateconstant values
at room temperature.
Figure 1 | Diagramof factors controllingthe main
inputs and outputs of soil carbon, superimposed
over a global map of soil organic carbon stocks.
While CO2is the main product of decomposition
in soil, CH4, dissolved organic carbon (DOC),
particulate organic carbon (POC) in water, and
dissolved inorganic carbon (DIC) are also
significant exports from some soils. The
background soil organic carbon (SOC) map
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temperature sensitivity of decomposition increases with increasing
molecular complexity of the substrate (Boxes 1 and 2). The reaction
rates are also modified by substrate concentrations and affinities of
the enzymes for the substrates (Box 3).
In applying this knowledge to soil environments the controversy
begins (hereafter we use ‘soil’ loosely to include wetlands, peatlands
different organic-C compounds, each with its own inherent kinetic
properties. Not only do plants produce a wide range of carbon
substrates, but plant detritus also undergoes transformations by
microbial degradation or by abiotic condensation reactions that
produce new aromatic structures, larger molecular weights, insolu-
bility, or other molecular architectures that affect the types and
efficacies of enzymes that can degrade them25,26. These complex
molecular attributes are characterized by low decomposition
rates, high activation energies, and inherently high temperature
sensitivity (Box 1). We shall call the inherent kinetic properties
based on molecular structure and ambient temperature the ‘intrinsic
temperature sensitivity’ of decomposition.
Second, the enzymes for decomposition may be physically or
chemically excluded from many of the organic-C substrates within
the heterogeneous soil environment26, causing substrate limitation at
reaction microsites (Box 3). The observed response to temperature
under these environmental constraints, whichwe shall call the ‘appar-
ent temperature sensitivity’, may be much lower than the intrinsic
temperature sensitivity of the substrate (Fig. 2). Conversely, if a
temperature-sensitive process alleviates an environmental constraint
to decomposition, then the subsequent increase in substrate avail-
ability could result in the apparent temperature sensitivity tempor-
arily exceeding the intrinsic temperature sensitivity of the substrate.
affect apparent temperature sensitivities of decomposition include
(1) Physical protection. Organic matter may become physically
and their enzymes may have limited access and where oxygen
concentrations may also be low. Similarly, organic compounds can
they have low water solubility or if they occur in hydrophobic
domains of humified organic matter29.
(2) Chemical protection. Organic matter may become adsorbed
onto mineral surfaces through covalent or electrostatical bonds,
thus chemically protecting it from decomposition27.
(3) Drought. Drought reduces the thickness of soil water films, thus
inhibiting diffusion of extracellular enzymes and soluble organic-C
substrates and lowering substrate availability at reaction microsites.
In fire-prone or drought-prone regions, deposition of volatilized
hydrophobic molecules can create water-repellency30, which also
restricts diffusion of organic matter and enzymes in water films.
(4) Flooding. Flooding slows oxygen diffusion to decomposition
reaction sites, often allowing only anaerobic decomposition, which
includes fewer and generally slowerdegradativeenzymatic pathways.
(5) Freezing. Although enzymatic reactions can occur below 08C
(refs 31, 32), the diffusion of substrates and extracellular enzymes
within the soil is extremely slow where the extracellular soil water is
Each of these environmental constraints affects decomposition
reaction rates, directly or indirectly, by decreasing substrate concen-
trations at enzymatic reaction sites. Instead of viewing decomposition
Box 3|The effect of substrate availability on Q10
The applicability of Arrhenius kinetics may be limited under
conditions of changing substrate availability. The importance of
substrate availability can easily be demonstrated in models of
enzyme-catalysed processes. Enzymes affect reaction rates
primarily by decreasing the required activation energy, such that
they can occur at ambient temperatures. The importance of
substrate availability in enzyme-catalysed reactions is described by
Michaelis–Menten kinetics88: the reaction rate is
Vmax£ [S]/(Kmþ [S]) where [S] is the substrate availability (that
is the substrate concentration at the active site of the enzyme),
Vmaxis the maximum reaction rate at a given temperature, and Km
is the Michaelis–Menten constant, representing the substrate
concentration at which the reaction rate equals Vmax/2. When [S] is
abundant, Kmbecomes insignificant, and the temperature response
of Vmaxdetermines that of the reaction rate. Vmaxincreases with
temperature89,90up to an optimum temperature (typically well
above ambient conditions), beyond which the enzyme starts to
denature and Vmaxdeclines rapidly. Therefore, when [S] is abundant
and the temperature does not exceed the optimum temperature,
Vmaxfollows Arrhenius kinetics and the theory explained in Box 1 is
valid. However, when [S] is low, Kmbecomes relevant. Because the
Kmof most enzymes increases with temperature, the temperature
sensitivities of Kmand Vmaxcan neutralize each other, creating very
low apparent Q10values90,91. Thus, in addition to substrate quality
and temperature, temporal and spatial differences in substrate
availability can also contribute to the large variability in Q10
observed in nature. This effect of substrate limitation on the
temperature sensitivity of decomposition has not yet been
incorporated into carbon cycle models. Even when combined,
Arrhenius and Michaelis–Menten kinetics may not always describe
decomposition reactions. First, these kinetics assume constant
enzyme concentrations, which may not be the case when microbial
populations fluctuate. Second, temperature can also affect enzyme
conformation92, isozyme production (isozymes have similar
functions but different temperature responses)93,94, and microbial
community structure (and thus enzymatic spectrum)54. Changes in
enzymatic properties, commonly referred to as ‘temperature
acclimation’, could offset temperature-induced increases in
respiratory activity. However, although the existence of these
processes is beyond doubt, their ecological importance remains to
Box 2|Relative versus absolute changes in decomposition rates
The Arrhenius equation describes changes in relative reaction rates
as a function of temperature, but the change in the absolute rate of
the reaction is what concerns us most. While the relative rate of
decomposition of recalcitrant soil organic matter with high
activation energy may be very sensitive to temperature, the change
in absolute rate may be small and difficult to detect in experiments.
For example, in a temperate ecosystem and under current climate
conditions, the annual decomposition of glucose (an easily
degradable compound with an Eaof about 30kJmol21; ref. 87)
would proceed 6.5 million times faster than annual decomposition of
a tannin compound with an Eaof about 70kJmol21(assuming equal
and unlimited pool sizes; Box 1 Figure, lower panel). If the
temperature were to increase by two degrees over the year, glucose
decomposition would accelerate by 10%. Because of its higher
temperature sensitivity, decomposition of the more recalcitrant
tannin would accelerate by 21%. In absolute numbers, this difference
in temperature response appears trivial, because glucose would still
decompose 5.8 million times faster than the more recalcitrant
tannin. Moreover, at similar levels of substrate availability, the
warming-induced increase in C losses from glucose will be much
larger than those associated with the decomposition of tannin,
despite the lower Q10of glucose decomposition. Hence, it is difficult
to determine temperature responses of decomposition of
recalcitrant organic matter in the presence of more labile
compounds, and it is tempting to classify the temperature response
of recalcitrant compounds as irrelevant. However, in most
environments the stocks of labile and recalcitrant compounds are
not equal, with recalcitrant compounds being much more abundant
than easily degradable compounds. Thus, even a small change in
their decomposition rate could become significant, albeit only at
decadal or longer timescales. Hence, sensitivity to temperature
changes must be evaluated within the context of pre-existing
decomposition rates and substrate availability.
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rates only through the lens of the temperature-dependent Arrhenius
function of the maximum enzymatic reaction rate (Vmax; Box 1), the
substrate concentration and the affinity of the enzyme for the
substrate (kM, as in Michaelis–Menten kinetics; Box 3) are also
crucial for understanding the reaction rate and its sensitivity to
temperature. Indeed, conditions of low substrate concentrations at
active sites of enzymes may be the rule rather than the exception
within the soil matrix.
Common approaches to modelling decomposition
Most efforts to characterize the kinetics of SOMdecomposition have
stratified carbon compounds into ‘pools’ that share similar mean
decomposition reaction rate (k) and therefore reflects a combination
of inherent reactivity of the compound and the environmental
constraints on its decomposition. The two best-known biogeo-
chemical models of soil carbon dynamics—the CENTURY33
and ROTH-C34models—compartmentalize soil carbon into 5–7
conceptual pools, including 2–4 pools of decomposable plant
material near the soil surface (litter layer) and three pools of carbon
in the mineral soil, with MRTs ranging from years to millennia
(Fig. 3). Decomposition of the plant detritus in the litter layers is
decomposability, such as carbon-to-nitrogen ratios and lignin
content35,36. The three C pools in the mineral soil, from the most
labile to the most recalcitrant to decomposition, are called ‘fast’,
‘slow’ and ‘passive’ in CENTURYand ‘microbial biomass’, ‘humified
organic matter’ and ‘inert’ in ROTH-C. Many attempts have been
made with partial success to measure these various pools through
physical and chemical fractionation of the soil13,28, but they remain
largely simplified modelling constructs. In lieu of discrete pools, a
continuum of soil C substrates of varying chemical complexity and
MRTs has also been used to simulate soil C dynamics37.
Although direct measurements of the sizes and MRTs of these
conceptual pools of soil C remain imperfect, a consensus has
emerged that using multi-pool soil C models to simulate changes
in soil C stocks is a major improvement over treating soil C as a
single, homogeneous pool38–40. A substantial fraction of the SOM
resides in the most recalcitrant pool that decomposes very slowly.
The importance of this model structure was demonstrated when the
multipool ROTH-C model was used in lieu of a single soil C pool
model for a global simulation of climate change using the Hadley
general circulation climate model. Soil C losses and gains were less
severe with the multipool model, both regionally and globally38.
While these models have proven effective for explaining local and
regional variation in current soil C stocks and changes in stocks due
to management and land-use change, a consensus has not emerged
for their applicability to climate change. Typically, most models of
soil C dynamics assume that decomposition of all SOM is nearly
be slow (and MRTs may be long) either because the complex
structures of the molecules render them resistant to decomposition,
or because environmental constraints restrict access of enzymes to
themolecules, or becauseofacombination ofthesetwofactors.Both
protected simple compounds and more complex unprotected com-
pounds might be lumped together into a common pool with
common MRTs. If the causes of varying MRTs and their potential
for change are to be understood, the distinction between intrinsic
and apparent temperature sensitivities needs to be addressed
Evidence for a decomposition feedback to warming
Discussions of biospheric feedbacks to climatic disruption have been
influenced by the perspective that temperature is the dominant
limiting factor of respiration, whereas photosynthesis is limited by
multiple factors, including light, CO2concentration, water stress,
and nutrient availability44. Woodwell45and Jenkinson et al.46argued
that respiration of terrestrial ecosystems, including microbial
decomposition of SOM, would be more sensitive to global warming
than would gross primary productivity. Global warming would thus
lead to a net increase of C release to the atmosphere by the terrestrial
biosphere). However, in the absence of a consensus on the tempera-
ture sensitivity of decomposition of a large fraction of soil C stocks,
the significance of this positive feedback continues to be debated.
Current geographical relationships between climate and SOM
stocks provide important clues, such as the presence of large soil C
Figure 2 | Factors affecting the ‘apparent’ sensitivity of decomposition of
soil organic matter. The intrinsic temperature sensitivity (as in Arrhenius
the decomposability of the molecule and the ambient temperature. In
general, more complex molecular structures have higher activation energies
and, hence, higher temperature sensitivity. However, several environmental
constraints on decomposition can dampen or obscure the intrinsic
temperature sensitivity by reducing substrate availability, often causing the
measured (or ‘apparent’) temperature sensitivity to be less than expected.
functions (for example, melting of permafrost) may be more realistic for
Figure 3 | Diagram of properties of conceptual pools of belowground
carbonstocksin twowell-knownmodels. The CENTURY33and ROTH-C34
roughly along a continuum of decomposability and MRT in the soil. The
is the subject of recent debate. Much of this confusion is due to the fact that
the recalcitrant pools are mixtures of simple compounds that have long
MRTs owing to physical or chemical protection from decomposition and
more complex compounds that have inherently low reactivity and require
high activation energy for decomposition.
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stocks at high latitudes (Fig. 1). Inferences about the effects of
changing climate based on current geographic patterns, however,
require the tenuous assumption that a space-for-time substitution
adequately describes projections of future scenarios of changing
carbon stocks. Nevertheless, in his classical work on soil-forming
factors, Jenny47,48described howsoil N concentrations (which covary
with soil C) increased with decreasing temperature and increasing
precipitation across the Great Plains of central North America.
Kirschbaum49pointed out that Jenny’s results imply that decompo-
sition does indeed increase more with temperature than does net
primary productivity across this gradient, supporting Woodwell’s
hypothesis45. Post et al.50demonstrated similar trends globally,
although strong relationships were apparent only for very wet and
very dry climates, suggesting that soil water content also plays an
important role for constraining rates of decomposition.
Not all gradient studies have supported temperature sensitivity of
decomposition11, and thereare numerous possible explanations. Not
withstanding Jenny’s example47,48it is possible that growing-season
length along some north–south gradients could affect gross primary
productivity, and thus C inputs to soil, as much or more than
temperature affects respiration, thus obscuring the effect of tem-
perature on decomposition when interpreting variation in SOM
stocks51. Environmental constraints to decomposition could also
covary with temperature along a particular study transect if factors
such as mineralogy, clay content, aggregation, or soil water content
also covaried along the same gradient. For example, the presence of
clay-sized minerals that effectively adsorb organic matter and
retain soil moisture can be related to temperature-dependent
processes, such as the effects of previous glaciations that expose
new bedrock and biogenic production of acids that promote
mineral weathering52. Finally, in the example of an observed
positive relationship between temperature and soil C stocks
along a climate gradient in Finland11, the inferred temperature-
insensitivity of decomposition of a large fraction of SOM could be
an artefact of model assumptions about fixed or variable mean
residence times of conceptualized soil C pools53. We will return to
this issue of the consequences of model assumptions on interpreted
When analysing any geographical trend, it is important to remem-
ber that instantaneous temperature responses of decomposition of
current C stocks reflect the relative abundances of organic-C sub-
strates of differing kinetic properties. Those relative substrate abun-
dances result, in part, from environmental constraints to
decomposition during the climate and disturbance history of the
soil. For example, the decomposition of organic matter in a highly
weathered mature tropical forest soil with high clay content may, on
average, have low apparent temperature sensitivity because of
chemical protection of a large fraction of soil C on mineral surfaces.
In contrast, the apparent temperature sensitivity may, on average, be
higher in a recently tilled temperate prairie soil because of lower
proportions of substrates under environmental constraints to
decomposition. Giardina and Ryan6ignored this variation in relative
abundances of different soil substrates when they calculated MRTs of
a single homogeneous soil C pool for a number of soil samples from
different latitudes and under different temperature regimes in
laboratory experiments. Not surprisingly, they found no correlation
between calculated total soil C MRTs and either laboratory incu-
bation temperature or the mean annual ambient temperature of
the field locations. They correctly proposed that substrate quality
and other stabilization mechanisms are important factors affecting
variation of soil C stocks among study sites, but they incorrectly
concluded that the temperature sensitivity of decomposition is
unimportant. Temperature insensitivity implies zero activation
energies of decomposition, which is impossible for biochemical
processes. The analysis by Giardina and Ryan6also did not take
into account that the abundance of the various carbon substrates (or
‘pools’), with differing intrinsic temperature sensitivity and under
differing constraints to decomposition, are themselves partly the
result of climate effects (Box 4).
In addition to observations of natural gradients, several studies of
the temperature sensitivity of decomposition have been carried out
applied multiple cycles of varying temperature during a 108-day
incubation and estimated the temperature sensitivity for each cycle.
different for the most labile carbon that was respired early in the
incubation and for the less labile carbon being respired at the end of
the incubation period. They also conducted the experiment on soils
having more recalcitrant C associated with mineral surfaces. Again,
no statistically significant differences in temperature sensitivities
were observed. While the results of Fang et al.9refuted the notion
proposed by others6,11,54,55that decomposition of the more recalci-
trant pools would be less sensitive to temperature than the more
labile pools, their results are still contrary to kinetic theory, which
indicates higher intrinsic temperature sensitivity for decomposition
of the recalcitrant C pools.
In contrast, Knorr et al.10came to a conclusion consistent with
experiment56to a multi-pool soil C model. They calculated not only
that decomposition responded positively to temperature for a highly
labilepool, butalso that decomposition ofalesslabilepoolexhibited
higher temperature sensitivity. Most of the SOM resided in a third
recalcitrant pool that did not decompose significantly during the
Box 4|Assumptions of curve fitting
In the Arrhenius function shown in Box 1, Eais clearly a variable that
is fitted to observational data to determine a temperature sensitivity
of a reaction. A debate has recently emerged, however, whether the
pre-exponential factor (a), should be a constant or a variable57,61,62.
From a purely mathematical perspective, the statistical fits of Eaand
a are not independent, and so the decision to keep a constant or
allow it to vary affects the fitted value of Ea(ref. 62). Because the
a-term is defined as the theoretical reaction rate constant in the
absence of activation energy, it makes sense that it might have
different values for different substrates53. Hence, model fits in which
all variation in decomposition rates and temperature sensitivity is
attributed to Eaare likely to overemphasize the differences in Ea
among compounds. Nonetheless, there is overwhelming evidence
that Eadoes vary considerably among compounds, and that
decomposition of recalcitrant SOM has higher intrinsic temperature
sensitivity than decomposition of labile SOM (Box 1). Because the
statistical fits of Eaand a are not independent, however, curve fitting
is unlikely to have sufficient power to resolve exactly to what degree
decomposition of recalcitrant compounds should have higher
intrinsic temperature sensitivities. A conceptually separate, but
mathematically similar, issue arises when applying the rate constant
(k) from the Arrhenius function to simulate decomposition of
various soil C pools, using the form: gðtÞ ¼Pcie2kit, where g(t) is
initial sizes of carbon ‘pools’ of varying degrees of decomposability.
Note the mathematical similarity between this function and the
Arrhenius function (Box 1), from which the kivalue for each ciin this
equation is derived. Just as the variability of the a-term in the
Arrhenius function is being debated, a debate has also emerged in
the literature as to whether temperature dependence should reside
only in the ki-terms or also in the ci-terms96–99. While the ki-term
describes the current instantaneous decomposition rate and its
temperature sensitivity, the relative sizes of the carbon pools (ci) of
varying degrees of decomposability were determined over longer
timescales and may also partially be a consequence of climatic
history, including temperature. In many statistical fits of
observational data, these two terms (kiand ci) are correlated98, and
so it is impossible to determine where the temperature sensitivity
lies by statistical curve fitting alone.
the remaining carbon fitted to observational data and ciare the
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of recalcitrant organic matter would obscure the temperature sensi-
tivity of the twosmaller, more labile pools. Experimental support for
kinetic theory was also obtained fromincubation experiments of leaf
and root litter with varying substrate quality14.
However, each of these studies9–11,14relied upon curve fitting to
demonstrate temperature sensitivities to decomposition, and doubts
may arise from the underlying assumptions of the models and the
power of the statistical tests to detect significantly different curve-
fitting parameters.Itispossible, forexample, that Fang et al.9didnot
find significantly higher temperature sensitivity of the more recalci-
trant C pools because of a type II error—accepting a null hypothesis
of no statistically significant differences among fitted Eaterms. On
an artefact of different temperature sensitivities (Eaterms) between
pools because of a model assumption of fixed a-terms in the
Arrhenius function (ref. 57; Boxes 1 and 4). Furthermore, environ-
mental constraints to decomposition of some of the substrates may
have been present during these incubations.
evidence regarding the temperature sensitivity of decomposition. In
experimental warming has been observed, but this measurable pulse
in decomposition often disappears within a few years54,55,58,59. This
result, however, must be interpreted with caution because high
spatial and temporal variability of measured CO2efflux rates often
precludepowerfulstatistical tests of small treatmenteffects, resulting
in possible type II errors. Nonetheless, one interpretation of these
ephemeral responses has been that only decomposition of the most
labile soil C pool was sensitive to the warming treatment, and that
decomposition of the older, more recalcitrant soil C was not
temperature sensitive. Another interpretation has been that roots
and soil microbial communities ‘acclimate’ to the higher-tempera-
ture conditions by gradually adapting their metabolism, so that the
newly acclimated communities return to respiration rates similar to
the pre-treatment levels within a relatively short time (Box 3).
However, recent modelling studies10,59,60have demonstrated that
these field experimental data are also consistent with a model of a
small, labile pool that is quickly exhausted and a larger less-labile
pool that is also temperature sensitive, but that decomposes
much more slowly. Model fits of these studies appear better with
the multipool models, and neither temperature insensitivity nor
acclimation needs to be invoked to explain the observations.
Unfortunately, curve fitting of data from laboratory incu-
bations6,9–11,14and soil warming experiments in the field54,55,58–60is
unlikely to resolve the debate about the underlying mechanisms of
and Fang et al.9papers, the same data fit equally well models with
different assumptions and, hence, different interpretations of the
temperature sensitivity of decomposition of recalcitrant SOM
(refs 57, 61, 62; Box 4). Another limitation to curve fitting is that it
focuses on the relationship between measured apparent temperature
sensitivity and estimated MRTs of experimentally defined soil C
pools, rather than attempting to distinguish between intrinsic and
apparent temperature sensitivity of the substrates of decomposition.
Despite these controversies, the observational data are converging
continuum (Fig. 3) decomposes with detectable apparent tempera-
ture sensitivity. Neither the observational data nor the soil C model
simulations, however, have been able to demonstrate a consistent
apparent temperature sensitivity of decomposition along the entire
spectrum of recalcitrant pools of SOM.
It is tempting to assume that the temperature sensitivity of
decomposition of the more recalcitrant forms of SOM is trivial
with respect to current concern about feedbacks to global warming,
because decomposition of these substrates, even if it is accelerated,
contributes so little to instantaneous CO2fluxes. Nonetheless,
because of their large contribution to the soil C stocks, even small
do not know where along the soil-C continuum or among the
discrete conceptual pools of SOM (Fig. 3) apparent temperature
sensitivity may become irrelevant to contemporary issues of carbon
cycling. More importantly, might the existing environmental con-
straints to decomposition change with changing climate, thus
exposing to decomposition SOM with high intrinsic temperature
sensitivity? In our opinion, answering this question would be more
correlation between current apparent temperature sensitivity and
MRTs of soil C pools.
Temperature dependence of environmental constraints
According to kinetic theory, the constraints to decomposition that
are caused by biological and chemical processes must themselves be
affected by temperature8and perhaps other climatic drivers. Let us
now reexamine the five environmental constraints to decomposition
listed above in light of the question of their own dependence on
(1) Both climate and management affect aggregate formation
(through growth of fungal hyphae and activity of soil fauna),
which physically protects SOM. The breakdown of aggregates can
also be enzymatic26, as the biogenic ‘glue’ that holds the aggregates
together is decomposed. In addition, however, purely physical
processes, such as ploughing and the impact of raindrops, also
destroy aggregates26. These processes are not directly temperature
dependent, but are often influenced by climate.
(2) Temperature affects the chemical processes of SOM adsorption
and desorption onto mineral surfaces, but little is known about the
activation energies of these processes.
(3) Theclimate-drivenhydrologicbalanceamong drainage,precipi-
tation, and evapotranspiration determines soil water film thickness
through which the diffusion of soluble organic-C substrates and
extracellular enzymes occurs. Likewise leaf litter hydrophobicity
associated with drought-prone and fire-prone ecosystems is also
affected by climate.
(4) Climate-driven flooding of wetlands and peatlands determines
oxygen supply for decomposition. Both precipitation and evapo-
transpiration arelikely tochangeinmany regionsoftheworldowing
to climatic disruption63, tipping the hydrologic balance towards
summertime drying of many mid-continental peatlands and wet-
lands and thus exposing large stocks of carbon substrates to aerobic
(5) Melting of permafrost will expose organic matter with wide-
ranging kinetic properties that are not currently expressed in frozen
soil. Once thesoil thaws,amajorconstrainttodecompositionwillbe
decomposition of organic matter in mineral soils concerns only
physical and chemical protection within the mineral soil matrix.
While these processes are extremely important contributors to
variability of soil carbon stocks and soil fertility, the extent to
which they will participate in positive or negative feedbacks
to climate change is not clear. Adsorption and desorption processes
are both temperature sensitive and might both increase such that the
net effect would be minimal over the next few decades. In contrast,
the last two constraints to decomposition—frozen soils and oxygen
limitation due to flooding—are likely to be subject to rapid changes
under plausible climate change scenarios.
When decomposition in wetlands and peatlands slows owing to
lack of oxygen during periods of flooding, the low oxygen concen-
trations inhibit the activity of phenol oxidase, causing accumulation
of phenolic compounds64. These phenolic compounds inhibit the
activity of hydrolase enzymes responsible for decomposition, thus
slowing decomposition further. This inhibition is quickly reversible
NATURE|Vol 440|9 March 2006
© 2006 Nature Publishing Group
once peat becomes aerobic. Hence, the 400–500Pg (1Pg ¼ 1015g)
carbon in wetlands and peatlands4,65, which has been accumulating
over centuries and millennia, is ‘stable’ only as long as anaerobic
soil moisture is expected to decrease63, the upper layers of peat could
dry out. An estimated 100Pg carbon could become aerobic and thus
available for decomposition (Table 1; ref. 4). Evidence that this
process may already be occurring comes from recently repeated
inventories of soils of England and Wales, which show that peat
soils and bogs lost carbon at a faster rate than upland soils over the
last 25years (ref. 5).
Carbon losses from peatlands will not necessarily enhance global
warming if an increased emission of CO2is compensated by a
decrease in the current net emissions of CH4(ref. 66). The green-
house warming potential of CH4on a per molecule basis is 23 times
higher thanCO2ona100-year timescale67.Likewise,growthofforest
vegetation on previously flooded land could sequester significant
amounts of C in wood68, although the net carbon balance remains
uncertain69. On the other hand, carbon in desiccated peat is also
carbon to the atmosphere. Siberian and Canadian peatlands are
already subject to important peat losses during fire-prone dry years70
and the combination of higher temperatures and peat drying
may increase fire frequency and severity71. During the 1997 El Nin ˜o,
0.6–0.8Pg of C (10% of anthropogenic emissions) was lost owing to
Permafrost soils store a similar amount of organic matter as
peatlands (Table 1). In these soils with permanently frozen layers,
plant litter accumulates both at the surface and on top of the
permafrost table through a mixing process called cryoturbation16.
When permafrost thaws, large amounts of otherwise mostly unpro-
tected carbon become available for decomposition74,75. A gradual net
loss of deep soil C in a boreal forest has also been attributed to
warming-induced deepening of the layer of seasonal biological
activity76. One estimate suggests that global warming could thaw
25% of the permafrost area by 2100 (ref. 77), thus rendering about
100Pg carbon vulnerable to decay (Table 1; ref. 4).
Permafrost thaw creates a mosaic of flooded areas interspersed
within higher dry areas. In the drier thawed areas, much of the large
substrate pool is likely to decompose relatively quickly. Within the
flooded thawed areas (thermokarst lakes), however, anaerobic
decomposition of organic matter is likely to proceed more slowly,
but produces large CH4emissions78, which could constitute a
stronger feedback to the climate system than the larger soil C
losses from the drier areas. To further complicate matters, recent
evidence indicates that thermokarst lakes are increasing in abun-
dance in the most northern range of permafrost, owing to an initial
increase in thermokarst development in response to warming,
whereas thermokarst lakes are draining and disappearing in the
southern range of permafrost, owing to more advanced degradation
Frozen and anaerobic conditions merely suspend organic matter
in decomposition time, rather than transform it into inherently
recalcitrant material. The term ‘stabilization’ has not been rigorously
defined with respect to soil carbon dynamics, and it would be
misleading to refer to organicC in wetlands and permafrost as
‘stabilized’ in the same sense that organicC is stabilized in mineral
interiors. In both cases, intrinsic kinetic properties of decomposition
of the organic-C substrates are suppressed by environmental con-
straints (Fig. 2), but the anaerobic and frozen conditions of wetland,
peatland, and permafrost soils are more likely to be subject to rapid
regarding peatlands and permafrost is not the degree to which the
currentlyconstrained decomposition rates are temperaturesensitive,
but rather how much permafrost is likely to melt and how much of
the peatland area is likely to dry significantly. Such regional changes
in temperature, precipitation, and drainage are still difficult to
predict in global circulation models. Hence, the climate change
predictions, as much as our understanding of carbon dynamics,
limit our ability to predict the magnitude of likely vulnerability of
peat and permafrost carbon to climate change. Assuming that 25%
of the estimated stocks of carbon in peatlands and permafrost is
subject to loss due to global warming in the twenty-first century,
this potential loss would be two to three times larger than simulated
C losses from mineral soils using current soil C models (Table 1;
refs 38, 42).
Other global change processes, such as CO2fertilization, N
deposition, improved soil management (for example, conservation
tillage), and land-use change could also change soil carbon stocks.
We have not addressed these changes, partly because our charge in
this review is to focus on the temperature sensitivitycontroversy, but
also because compelling evidence is lacking for globally significant
soil C sinks by these processes15,80–83. In contrast, those belowground
carbon pools where environmental constraints to decomposition are
themselves highly sensitive to climate may become increasingly
important positive feedbacks as global climatic disruption becomes
Conclusions and future research directions
A significant fraction of relatively labile SOM is clearly subject to
temperature-sensitive decomposition, but another significant frac-
tion of SOM remains under environmental constraints that often
obscure the intrinsic temperature sensitivity of its decomposition.
The interpretations of natural climatic gradients and of laboratory
and field experiments designed to quantify various carbon fractions
and degrees of temperature sensitivity are highly dependent upon
model assumptions and curve fitting techniques. Such studies have
yielded valuable insight into soil carbon dynamics, but they have not
resolved the overall response of global soil C stocks or the magnitude
of expected feedbacks to climatic disruption. Moreover, dividing
SOM into only temperature-sensitive and apparently temperature-
insensitive pools is far too simplistic.
Extrapolation of decomposition rates into a future warmer world
based on observations of current apparent temperature sensitivities
is inadequate. Rather, we need to understand how substrate avail-
ability will change and how a changing set of environmental
constraints to decomposition in a future climate will determine the
future apparent temperature sensitivity of decomposition. Perhaps a
between inherent kinetic properties of individual substrates and the
suite of environmental constraints to decomposition that frequently
exist in situ. Our ability to identify and characterize soil substrates is
growing with new developments in nuclear magnetic resonance and
other technologies, but the task is enormous given the diversity of
soil C substrates common in soils. Even when structures are identi-
fied within the soil, their concentrations at reactive sites of enzymes
are more difficult to estimate. Nevertheless, merging the concepts of
substrate availability, such as Michaelis–Menten kinetics, with the
temperature sensitivity prescribed by Arrhenius kinetics may
provoke new measurement and modelling approaches for soil C
dynamics. The multiple processes of environmental constraints that
govern availability of substrates to enzymes should be explicitly
described and studied within the context of climate change.
Regardless of the experimental and modelling approaches used,
the debate about the temperature sensitivity of decomposition
should be broadened beyond upland mineral soils specifically to
include wetlands, peatlands and permafrost soils. These are the most
obvious environments in which current constraints on decompo-
sition are likely to change as a result of climatic disruption, thus
potentially exposing large stocks of C to less constrained decompo-
NATURE|Vol 440|9 March 2006
© 2006 Nature Publishing Group
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Acknowledgements We thank G. A˚gren, R. Houghton, C. Potter, D. Sampson,
J. Schimel, P. Smith and D. Thompson for comments on earlier drafts of this
paper. We thank M. Ernst for assistance with graphics. E.A.D. acknowledges
support from the Northeast Regional Center of the National Institute for Global
Environmental Change of the Department of Energy and by the National Science
Foundation. I.A.J. acknowledges the European Commission for support via
CarboEurope-IP. Financial support does not constitute an endorsement by DOE
or NSF of the views expressed in this article.
Author Information Reprints and permissions information is available at
npg.nature.com/reprintsandpermissions. The authors declare no competing
financial interests. Correspondence should be addressed to E.A.D.
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