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available at www.sciencedirect.com
journal homepage: www.elsevier.com/locate/funeco
Climate change feedbacks to microbial decomposition
in boreal soils
Steven D. ALLISONa,b,*, Kathleen K. TRESEDERa
a
Department of Ecology and Evolutionary Biology, University of California, Irvine, 321 Steinhaus, Irvine, CA 92697, USA
Department of Earth System Science, University of California, Irvine, 321 Steinhaus, Irvine, CA 92697, USA
b
article info
abstract
Article history:
Boreal ecosystems store 10e20 % of global soil carbon and may warm by 4e7 C over the
Received 21 September 2010
next century. Higher temperatures could increase the activity of boreal decomposers and
Revision received 19 January 2011
indirectly affect decomposition through other ecosystem feedbacks. For example, perma-
Accepted 24 January 2011
frost melting will likely alleviate constraints on microbial decomposition and lead to
Available online -
greater soil CO2 emissions. However, wet boreal ecosystems underlain by permafrost are
Corresponding editor:
€ rn Lindahl
Bjo
often CH4 sources, and permafrost thaw could ultimately result in drier soils that consume
CH4, thereby offsetting some of the greenhouse warming potential of soil CO2 emissions.
Climate change is also likely to increase winter precipitation and snow depth in boreal
Keywords:
regions, which may stimulate decomposition by moderating soil temperatures under the
Bacteria
snowpack. As temperatures and evapotranspiration increase in the boreal zone, fires may
Boreal forest
become more frequent, leading to additional permafrost loss from burned ecosystems.
Climate warming
Although post-fire decomposition could also increase due to higher soil temperatures,
Community composition
reductions in microbial biomass and activity may attenuate this response. Other feedbacks
Decomposition
such as soil drying, increased nutrient mineralization, and plant species shifts are either
Feedbacks
weak or uncertain. We conclude that strong positive feedbacks to decomposition will likely
Fire
depend on permafrost thaw, and that climate feedbacks will probably be weak or negative
Nitrogen
in boreal ecosystems without permafrost. However, warming manipulations should be
Permafrost
conducted in a broader range of boreal systems to validate these predictions.
Soil carbon
Introduction
Boreal forests occupy 8e11 % of the Earth’s land surface and
store a large fraction of global terrestrial carbon (Whittaker
1975). The boreal zone includes large regions of Alaska,
Canada, Scandinavia, and Siberia for a total of 11.2e15.8
million km2 worldwide (Chapin & Matthews 1993; Gower et al.
2001). Although estimates vary, these regions contain 60e110
Pg carbon (C) in plant biomass (Schlesinger 1977; Apps et al.
1993) and 90e230 Pg C in upland forest soil (Schlesinger
1977; Post et al. 1982; Oechel & Billings 1992; Apps et al. 1993).
ª 2011 Elsevier Ltd and The British Mycological Society.
Boreal peat soils are estimated to store an additional 420e455
Pg C (Gorham 1991). All of these values may be underestimates
because they are based on surface soils (generally <1 m
depth), and a recent analysis suggests that deep high-latitude
soils may store >1670 Pg C, although this estimate also
includes tundra ecosystems (Schuur et al. 2008). Overall,
boreal soils probably contain at least 10e20 % of the global
gy & Jackson 2000).
total of w2300 Pg soil C (Jobba
Because there is so much C stored in boreal ecosystems,
they have the potential to effect feedbacks between climate
and the global C cycle. Increasing concentrations of
* Corresponding author. Tel.: þ1 (949) 824 9423; Fax: þ1 (949) 824 2181.
E-mail address: [email protected] (S.D. Allison).
1754-5048/$ e see front matter ª 2011 Elsevier Ltd and The British Mycological Society.
doi:10.1016/j.funeco.2011.01.003
Please cite this article in press as: Steven D Allison, Kathleen K Treseder, Climate change feedbacks to microbial decomposition
in boreal soils, Fungal Ecology (2011), doi:10.1016/j.funeco.2011.01.003
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greenhouse gases due to human activities are increasing
global mean temperatures, and feedbacks in the climate
system are expected to cause disproportionate warming at
high latitudes (IPCC 2007). These systems have already
warmed by w1.5 C (Moritz et al. 2002), and are expected to
warm by 4e7 C in the next century (IPCC 2007). Warming of
this magnitude is expected to alter many processes that affect
C cycling in boreal ecosystems (McGuire et al. 2009). For
example, climate warming may increase plant biomass and
litter inputs if higher temperatures result in faster rates of
plant growth and soil nutrient mineralization. Conversely,
warmer temperatures may stimulate C losses from boreal
soils through increased rates of decomposition. Carbon has
accumulated in boreal soils primarily because cold temperatures and permafrost (perennially frozen soil) reduce decomposition rates relative to C inputs from primary production
(Stokstad 2004). These thermal constraints are further reinforced by plantesoil feedbacks that lead to poor litter quality
(Hobbie et al. 2000) and a high relative abundance of ectomycorrhizal fungi that may inhibit decomposition by saprotrophic fungi in boreal soils (Lindahl et al. 2002).
Given that boreal ecosystems contain 10e20 % of global soil
C, climate change could have large impacts on global C
balance through effects on decomposition. The decomposition of soil C is a biological process controlled primarily by
micro-organisms such as fungi and bacteria (Swift et al. 1979).
The direct and indirect effects of climate change will therefore
mediate boreal C cycling through effects on decomposer
communities, and these interactions will be the focus of our
review (Fig 1). Climate change may influence decomposer
S.D. Allison, K.K. Treseder
microbes directly through changes in temperature or precipitation (IPCC 2007). Indirect effects include changes in soil
moisture due to increased evapotranspiration and melting of
permafrost (Potter et al. 2001; Zimov et al. 2006; Schuur et al.
2008). If rates of decomposition increase, nutrient availability to decomposers may increase through faster rates of
mineralization (Rustad et al. 2001). Climate may also indirectly
affect microbial decomposers through changes in fire
frequency and plant community composition (Kasischke &
Stocks 2000; Hollingsworth et al. 2008); either of these
changes may affect the chemical and physical environment
for decomposition.
Since climate change will affect soil C decomposition
directly and indirectly through microbial communities, the
goal of this synthesis is to evaluate the feedbacks among
climate change, microbes, and decomposition in boreal
ecosystems. By understanding these feedbacks, we aim to
improve models and predictions of boreal C storage and global
climate in the coming decades. Specifically, we will address
the following questions: (1) What is the diversity and distribution of decomposer microbes relevant for decomposition in
boreal forests? (2) How do microbial communities and
decomposition respond directly to temperature increase? (3)
What are the responses to indirect climate feedbacks, such as
permafrost thaw, soil drying, increases in fire frequency,
increased nutrient mineralization, and changes in plant
community composition? We conclude with a summary of
predictions for boreal C storage in the face of climate change
and recommendations for increasing the accuracy of uncertain predictions.
Microbial abundance and community structure
in boreal soils
Fig 1 e Predicted direct and indirect effects of global
warming on microbial CO2 production in boreal
ecosystems, based on data from laboratory and field
studies. The integrated effect of global warming will
depend on the relative strength of each effect, and the
distribution of permafrost in boreal forests. We predict that
the strongest effects will be derived from permafrost thaw
and increased fire frequency. Permafrost thaw should
increase microbial CO2 production owing to thicker active
layers and drainage of water-saturated soils. More
frequent fires may also lead to greater permafrost loss, but
may reduce microbial CO2 production due to declines in
microbial biomass. Solid lines [ direct effects; dashed
[ indirect. Thicker lines [ stronger predicted effects.
Fungi are the most well-studied microbes in boreal soils,
although bacteria and archaea may also act as decomposers
(Thormann et al. 2004). Separating the contribution of each
microbial domain to decomposition is challenging and has
rarely if ever been quantified in any ecosystem. Fungi are
assumed to be important for boreal decomposition because of
their enzymatic potential to decompose recalcitrant forms of
soil C and their tolerance of the acidic pH values typical of
€ gberg et al. 2007). While there are many
most boreal soils (Ho
studies demonstrating that boreal fungi are important for
decomposition (Lindahl et al. 2002; Virzo De Santo et al. 2002;
Read et al. 2004; Allison et al. 2009; LeBauer 2010), there are
few to support the assertion that bacteria and archaea are
unimportant. It is therefore clear that more studies are warranted to determine the quantitative importance of fungi,
bacteria, and archaea for decomposition in boreal soils.
Boreal soils contain a high diversity of saprotrophic and
mycorrhizal fungi that participate in the breakdown of soil
organic matter. Arbuscular mycorrhizas are present in many
boreal ecosystems, but their role in decomposition is thought
to be relatively minor (Read & Perez-Moreno 2003; Treseder
et al. 2004; Treseder & Cross 2006), so they will not be
considered further here. Many saprotrophic fungi found in
boreal ecosystems produce extracellular enzymes capable of
degrading the major chemical compounds found in plant litter
Please cite this article in press as: Steven D Allison, Kathleen K Treseder, Climate change feedbacks to microbial decomposition
in boreal soils, Fungal Ecology (2011), doi:10.1016/j.funeco.2011.01.003
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Climate change feedbacks to microbial decomposition
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Change running header to "Climate change
feedbacks to boreal decomposition"
and humus, such as cellulose, lignin, tannins, protein, and
chitin (Lindahl & Finlay 2006; Allison et al. 2009; LeBauer 2010).
Ericoid and ectomycorrhizal taxa also possess genes for
oxidative and hydrolytic enzymes that may be expressed to
decompose soil organic compounds (Read & Perez-Moreno
e et al.
2003; Lindahl & Taylor 2004; Courty et al. 2005; Bue
€ deker et al. 2009). Although they may not decompose
2007; Bo
soil C as effectively as saprotrophs on a per-biomass basis
(Baldrian 2009), the high relative abundance of ericoid and
ectomycorrhizal fungi in many boreal ecosystems suggests
that they may be quantitatively important for soil C turnover
(Lindahl et al. 2007, 2010; Allison et al. 2008; Talbot et al. 2008).
There is clear evidence that fungal community composition differs vertically through the soil profile. Wood decay
fungi, especially brown-rot and white-rot basidiomycetes,
colonize standing dead or fallen coarse woody debris
(Berglund et al. 2005). In a boreal forest dominated by Scots
pine, surface litter horizons were dominated by saprotrophic
basidiomycetes and ascomycetes, whereas humus layers
and mineral soils were dominated by ectomycorrhizal fungi
(Lindahl et al. 2007, 2010). This segregation of fungal functional groups probably occurs because mycorrhizal fungi can
access labile C from host plants in deeper soil layers where
C availability may limit saprotrophs. However, ectomycorrhizal fungi occur throughout the soil profile, with different
taxa found in organic versus mineral layers (Tedersoo et al.
2003).
Distributions and functions of boreal bacteria and archaea
are not well understood. Studies based on phospholipid fatty
acid (PLFA) data suggest that some boreal soils may be dominated by Gram-negative bacteria (Demoling et al. 2008),
whereas others may be dominated by Gram-positive bacteria
€ gberg et al. 2003). This latter study also found that the ratio
(Ho
of Gram-negative:Gram-positive bacteria declined with soil
depth, from the F to the H horizon. In wetter bog environments, Jaatinen et al. (2007) found that Gram-negative bacteria
dominated surface soils, and decreased relative to Grampositive bacteria in deeper soil horizons in two of three
Finnish study sites. They also found a relatively high abundance of actinobacterial PLFA markers in a mineral-rich bog
site and suggested that these microbes may contribute to
decomposition due to their ability to produce degradative
enzymes. However, the functional roles of bacteria within
these broad groups are highly diverse, so changes in bacterial
community composition are difficult to link with decomposition rates. Fierer et al. (2007) have proposed a functional
classification scheme for bacteria, but both oligotrophic and
copiotrophic classes occur within the Gram-negative bacteria,
so measurements of bacterial community composition must
occur at finer taxonomic resolution than PLFA groups to be
functionally relevant.
Archaea also occur in boreal forest soils, and may
contribute to decomposition through mineralization of labile
organic matter in the rhizosphere. Crenarchaeota appear to be
the dominant taxon in soil (Jurgens et al. 1997) and are known
to occur in preferential association with mycorrhizal plant
roots where they may metabolize plant exudates (Bomberg
et al. 2003; Bomberg & Timonen 2009). Euryarchaeota have
also been observed to associate with Pinus sylvestris mycorrhizas (Bomberg & Timonen 2007).
3
Direct effect of warming on microbial processes
and soil C cycling
A major concern with climate change in boreal regions is that
rising temperatures will increase the metabolic rates of
decomposer microbes, thereby mobilizing the large C stocks
in boreal soils (McGuire et al. 2009). Temperature manipulations in boreal systems can provide information about the
direct response of microbial communities and decomposition
rates to climate warming. However, given their importance for
the global C cycle, relatively few warming manipulations have
been carried out in boreal ecosystems. In particular, we know
of no experiments that have examined microbial responses to
warming in the Siberian boreal zone or in boreal bogs which
together store the majority of C in boreal ecosystems globally.
Therefore our current knowledge is mainly restricted to the
upland boreal forests of Alaska, Canada, and Scandinavia.
Warming manipulations in these boreal regions have
yielded conflicting results (Table 1). In an Alaskan boreal
forest underlain by permafrost, warming during three
growing seasons resulted in a 20 % reduction in forest floor
biomass, suggesting increased microbial activity and decomposition (Van Cleve et al. 1990). Several other studies have also
found that soil respiration and possibly decomposition
increase with warming, although these measurements cannot
easily distinguish root and heterotrophic responses
€ mgren 2001; Bergner et al. 2004; Niinisto
€ et al. 2004;
(Stro
Bronson et al. 2008). In contrast, some researchers have
found negative soil respiration responses to warming (Allison
& Treseder 2008), including Bronson et al. (2008), who observed
that a positive response turned negative when air was
warmed in addition to soil (Table 1). Although the mechanism
for negative responses to warming is not entirely clear,
concomitant declines in soil moisture or physiological stress
on roots and soil microbes are possible explanations. Studies
by Verburg et al. (1999) and Allison et al. (2010b) found no
response of litter decomposition and soil respiration, respectively, to warming. For logistical reasons, most of the manipulations in Table 1 were carried out only during the growing
season, but climate warming is expected to occur during the
winter and to increase growing season length, which could
result in greater warming responses on an annual basis
€ mgren 2001; Euskirchen et al. 2006).
(Stro
Predicting the direct response of microbes and decomposition to warming is further complicated by potential changes
in microbial community composition and physiology. Initial
responses to higher temperature could change if warming
causes microbes with different functional characteristics to
become dominant in boreal soils. In addition, microbial
communities could adapt to warming through physiological
adjustments in rates of metabolism, or evolution of proteins
with different thermal optima (Hochachka & Somero 2002;
Bradford et al. 2008). All of these responses could contribute
to altered sensitivities of key processes related to decomposition, such as extracellular enzyme catalysis and microbial
respiration. Although there is some evidence that boreal soil
€ mgren 2001), there are
respiration may adapt to warming (Stro
as yet few studies of microbial community responses. Our
work in recently burned and mature Alaskan boreal forests
Please cite this article in press as: Steven D Allison, Kathleen K Treseder, Climate change feedbacks to microbial decomposition
in boreal soils, Fungal Ecology (2011), doi:10.1016/j.funeco.2011.01.003
Q1
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FUNECO123_proof ■ 28 February 2011 ■ 4/13
Dabros & Fyles (2010)
Allison et al. (2010b)
Soil respiration
Litter mass loss 0 % to 3 %
ND
NA
ND
1e2 C
0.5 C
3e5 C
1.2 C
1 C
(cooling)
3 Growing seasons
2 yr
3 Growing seasons
2 yr
No
No change
5 C
5.4e5.9 C
No
NA
Delta Junction, AK, USA
CLIMEX: Risdalsheia,
Norway
Delta Junction,
AK, USA
James Bay, Quebec, Canada Open top chamber
2 Growing seasons
Soil warming
(heating cables)
Soil warming þ
closed chamber
Closed chamber
Soil warming
(heating cables)
Closed chamber
3.1e4.5 C
No
No
Burned ecosystem
7 yr post-fire
Possible drying effect
Allison & Treseder (2008)
Verburg et al. (1999)
Soil respiration
No
Soil respiration
No
5 C
2e4 C
4 yr
Closed chamber
€ rvi Research
Mekrija
Station, Finland
Thompson, Manitoba,
Canada
Delta Junction, AK, USA
23 % to 31 % Irrigated; Picea
mariana in chambers
Soil respiration 22 %
Possible drying effect
Litter mass loss No change
Possible drying effect
þ20 %
Soil respiration
0.4 C
0.9 C
No
Burned ecosystem
Bergner et al. (2004)
2 yr post-fire
€ et al. (2004)
þ27 % to þ43 % Irrigated; Pinus sylvestris Niinisto
in chambers
þ11 % to þ24 % Irrigated
Bronson et al. (2008)
€ mgren (2001)
Stro
þ10 % to þ20 % Irrigated and fertilized
NA
5 C
No
Van Cleve et al. (1990)
20 %
Forest floor
biomass
Soil respiration
NA
Washington Creek,
AK, USA
Flakaliden, Sweden
Soil warming
3 Growing seasons
(resistance tape)
Soil warming
6 Growing seasons
(heating cables)
Open top chamber 3 Growing seasons
8e10 C
Yes
Comments
% Change
Response
variable
Soil
Air
Permafrost
warming warming
Duration
Method
Site
Table 1 e Summary of warming manipulations in boreal ecosystems.
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S.D. Allison, K.K. Treseder
Reference
4
has shown relatively little change in fungal community
composition after 2e3 growing seasons of warming, although
there was a 50 % reduction in microbial biomass in the mature
forest site (Bergner et al. 2004; Allison & Treseder 2008; Allison
et al. 2010b).
Aside from direct manipulations, climate gradients can
also provide insight into ecosystem responses to warming.
Consistent with the prediction that warming will lead to soil C
loss, Kane et al. (2005) used a climate and productivity gradient
in Alaskan black spruce forests to show that soil organic C
stocks decrease with increasing soil temperature, particularly
in mineral horizons. Across a climate gradient spanning 1 C
to 5 C mean annual temperature in boreal peatlands of
northern Manitoba, Camill & Clark (1998) assessed the relative
importance of regional climate versus local factors in
controlling permafrost dynamics, which strongly influence
soil C storage. This study showed that local factors such as
topography, aspect, and vegetation communities mediated
the response of permafrost to regional temperature. The
importance of local processes may help explain why direct
manipulations of temperature at single sites often yield conflicting results (Table 1).
Direct effect of precipitation change on microbial
processes and soil C cycling
Increased atmospheric moisture content due to regional
warming in the high latitudes will likely lead to increased
precipitation in most boreal ecosystems. In the Eurasian
boreal zone, nearly all climate models predict increased
precipitation, particularly in winter (IPCC 2007). Most models
also predict increased autumn and winter precipitation in the
North American boreal zone, with relatively small changes in
summer precipitation (IPCC 2007). Increased winter precipitation will fall as snow, which will likely increase snow depth
and potentially moderate the temperatures experienced by
soil microbes during winter. In alpine forests, winters with
deeper snowpack are associated with increased soil temperatures and greater soil CO2 efflux (Monson et al. 2006).
Although deeper snowpack may stimulate decomposition, the
effects of increased snowmelt and rainfall are less certain and
may depend on soil hydrology. Decomposition is more likely
to respond positively to increased precipitation in soils with
better drainage and more frequent moisture limitation
compared to poorly drained soils with anaerobic conditions
(Rapalee et al. 1998; Preston et al. 2006). Overall, it appears that
decomposition responses to precipitation increase will be
positive, but interactions with temperature, soil hydrology,
snow dynamics, and vegetation change will likely mediate the
response.
Indirect effects of warming on microbial
processes and C cycling
Aside from the direct effects, climate change in the boreal
zone will likely lead to indirect feedbacks that also have the
potential to affect microbial communities and rates of C loss
(Fig 1). In some cases, these indirect effects may be more
Please cite this article in press as: Steven D Allison, Kathleen K Treseder, Climate change feedbacks to microbial decomposition
in boreal soils, Fungal Ecology (2011), doi:10.1016/j.funeco.2011.01.003
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important than the direct response to warming. A major
challenge in predicting boreal responses to climate change is
estimating the magnitude and direction of these feedbacks.
Therefore we focus the remainder of this review on indirect
effects resulting from climate change in the boreal zone.
Permafrost thaw
Permafrost exerts a strong influence over C balance in highlatitude ecosystems (Carrasco et al. 2006; Zimov et al. 2006;
Schuur et al. 2008; Ping et al. 2010). Permafrost soils often
store large amounts of C because low temperatures and
limited diffusion of oxygen and solutes constrain the activity
of microbial decomposers in frozen soil. Furthermore,
permafrost impedes soil drainage, leading to waterlogging
and low oxygen availability in surface soil horizons. If
permafrost melts under warmer conditions, all of these
constraints could be alleviated, resulting in a rapid release of
stored soil C (Schuur et al. 2008).
In the boreal zone, permafrost thaw is likely to represent
an important but spatially heterogeneous feedback to microbial activity and decomposition. Unlike tundra ecosystems,
permafrost is not found in all boreal soils, and permafrost
feedbacks will not occur in many boreal systems. Overall, we
estimate that 40e55 % of the boreal zone is underlain by
permafrost (Fig 2). This estimate is based on the boreal forest
extent from Larsen (1980) and the distribution of permafrost
extent from Brown et al. (1998). Based on these distributions,
we visually estimated the fraction of the boreal zone underlain by continuous, discontinuous, sporadic, isolated, and no
permafrost. These classes represent 90e100 %, 50e90 %,
10e50 %, 0e10 %, and 0 % permafrost coverage, respectively.
We then calculated the average permafrost coverage for the
whole boreal zone, weighted by the fraction of boreal forest in
each permafrost class. Our range of estimates (40e55 %) is
based on using the low versus high limit of coverage for each
permafrost class.
In boreal forests with permafrost, microbial feedbacks to
decomposition under climate warming are likely to be strong.
The boreal zone encompasses the southern boundary of
permafrost extent, so permafrost soils in this region may
become destabilized with relatively little warming. In the
mineral horizon of an Alaskan boreal forest, the relative
abundance of fungi was lower in permafrost soils compared to
non-permafrost soils, whereas the potential activity of polyphenol oxidase enzyme was greater (Waldrop & Harden 2008).
At a single Alaskan site with permafrost, abundances of
bacteria and fungi were lower in permafrost than in the
overlying active layer (Waldrop et al. 2010). Chemical analyses
at this site also indicated that organic compounds in permafrost are relatively labile. Overall, these results suggest that
decomposition of permafrost C is limited by low microbial
activity, but high potential enzyme activity and an abundance
of available C could result in rapid losses of soil C following
permafrost thaw (Freeman et al. 2001, 2004). This conclusion is
supported by radiocarbon measurements of soil respiration in
the arctic which suggest large losses of C greater than 50 yr old
from melted permafrost soils (Schuur et al. 2009).
5
Although increased soil CO2 emissions following permafrost thaw would provide a positive feedback to climate
warming, changes in CH4 cycling could provide a negative
feedback. Methane is a potent greenhouse gas produced
through anaerobic decomposition and microbial reduction of
CO2. Whereas upland boreal soils can be a sink for methane,
bogs and waterlogged soils underlain by permafrost can be
methane sources (Whalen et al. 1991; Whalen & Reeburgh
1996; Burke et al. 1997; Gulledge & Schimel 2000; Panikov &
Dedysh 2000; Kim et al. 2007). Therefore conversion of
permafrost to non-permafrost soils could ultimately reduce
the amount of CH4 emitted from boreal soils, although CH4
emissions could increase during the thaw process, which may
€ nen et al. 1998; Kim & Tanaka 2003).
take several decades (Nyka
In Alaskan tundra, transition to drier conditions occurred
within 50 yr of permafrost thaw (Schuur et al. 2009), and in
Finland, conversion from wetland to forest vegetation
occurred within 50 yr after mires were drained (Laine et al.
1995).
Soil drying
Climate warming in boreal ecosystems will likely lead to
increased rates of evapotranspiration and substantial soil
drying, particularly in surface horizons. However, the effect of
reduced soil moisture on decomposition rates will probably
depend on the initial moisture and permafrost status of the
soil (Fan et al. 2008). Drying may inhibit microbial activity in
well-drained upland boreal soils, but stimulate microbial
decomposition in poorly drained and permafrost soils. These
changes are important because wetter soils tend to store more
C and support lower rates of decomposition (Trumbore &
Harden 1997; Rapalee et al. 1998; Preston et al. 2006; Ping
et al. 2010).
Evidence from warming manipulations generally supports
the prediction that decomposition in relatively dry soils tends
to respond negatively to additional drying. Soil C cycling in
boreal sites that were not irrigated or underlain by permafrost
generally showed weak or negative responses to warming and
involved indirect drying effects (Table 1; Allison & Treseder
2008; Allison et al. 2010b). In contrast, drying of a Finnish
boreal fen resulted in a threefold increase in soil respiration,
increases in microbial biomass, and a shift in microbial
community composition toward fungal taxa (Jaatinen et al.
2008). However, it should be noted that the effect of drying
on CH4 emissions from wet soils is likely to be negative
€ nen et al. 1998), so positive CO2 feedbacks from drying
(Nyka
boreal wetlands may be partially countered by negative
feedbacks from reduced CH4 emissions.
Changes in fire regime
Each year, wildfires consume an average of w110,000 km2, or
w1 %, of the boreal forest in Asia and North America, implying
a fire return interval of w100 yr (Giglio et al. 2006). Although
there is large inter-annual variation (Wein & MacLean 1983),
modelling studies in Canadian boreal forest suggest that fire
may consume w10e30 % of NPP based on long-term averages
Please cite this article in press as: Steven D Allison, Kathleen K Treseder, Climate change feedbacks to microbial decomposition
in boreal soils, Fungal Ecology (2011), doi:10.1016/j.funeco.2011.01.003
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S.D. Allison, K.K. Treseder
Please publish
Fig. 2 in color if
possible.
Fig 2 e Extent of northern boreal forest (blue lines) adapted from Larsen (1980) overlain on permafrost distributions adapted
from Brown et al. (1998) and the National Snow and Ice Data Center, Atlas of the Cryosphere (http://nsidc.org/data/atlas/
atlas_info.html).
for C loss through burning (Harden et al. 2000). Warmer
temperatures and potential soil drying in the boreal zone may
lead to increases in fire frequency, intensity and extent
(Kasischke et al. 1995; Kasischke & Stocks 2000; Kasischke &
Turetsky 2006).
Changes in fire dynamics are important because fires have
dramatic impacts on decomposition, microbial communities,
and other ecosystem properties. Initially, boreal fires mobilize
large amounts of C from biomass and organic soils through
combustion. During recovery from wildfire, further decomposition losses of C are hypothesized to occur due to elevated
soil temperatures that can increase by 3e8 C compared to
unburned areas (Burke et al. 1997; Richter et al. 2000; O’Neill
et al. 2002; Kim & Tanaka 2003; Treseder et al. 2004). Fires
also lead to the formation of black carbon, which decomposes
very slowly with turnover times on the order of millennia
(Preston & Schmidt 2006; Kuzyakov et al. 2009). However, the
net effect of black carbon on decomposition is unclear
because it has been found to increase humus decay rates in
boreal soils, potentially by providing a favorable physical
substrate for microbial decomposers (Wardle et al. 2008).
Based on measurements of soil respiration per unit area,
many investigators have concluded that decomposition
increases following fire. In upland Canadian boreal forest,
Burke et al. (1997) found that total rates of soil respiration were
maintained immediately following fire, then declined after
2 yr and subsequently recovered to pre-burn levels 7 yr after
fire. They concluded that increased microbial respiration
immediately after burning may have offset a decline in autotrophic respiration, but that substrate depletion limited
microbial respiration after 2e5 yr. Kim & Tanaka (2003) found
22e50 % reductions in soil respiration rates 0e2 yr after fire in
boreal forests of interior Alaska, but concluded
Q2:that
thismicrobial
is fine
respiration had increased based on the assumption that only
20 % of pre-burn soil respiration was microbial. Similarly, Q2
O’Neill et al. (2003) found that soil respiration was 40e50 %
lower in recently burned black spruce forests in Alaska, but
suggested that decomposition rates had increased by >3-fold
based on a C balance model and prior lab incubation results
(Richter et al. 2000; O’Neill et al. 2006). Similar conclusions were
drawn based on data from a fire chronosequence in Siberian
boreal forest (Sawamoto et al. 2000).
These reported increases in microbial respiration are
difficult to reconcile with microbial community responses to
fire, which are consistently negative. Burning removes surface
soil horizons that are rich in labile C, halts plant root exudation, reduces substrate availability, and generates recalcitrant
combustion products that may constrain microbial
Please cite this article in press as: Steven D Allison, Kathleen K Treseder, Climate change feedbacks to microbial decomposition
in boreal soils, Fungal Ecology (2011), doi:10.1016/j.funeco.2011.01.003
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decomposition (Certini 2005; Harden et al. 2006). Bergner et al.
(2004) found lower rates of soil respiration and non-detectable
fungal biomass in severely burned soils of boreal Alaska.
Using a nearby set of fire chronosequence sites, Treseder et al.
(2004) found that the diversity of bacteria and the abundance
of ectomycorrhizal fungi required >15 yr to recover to preburn levels. Fungal biomass, polyphenol oxidase activity, and
rates of lignin decomposition also declined significantly 5 yr
after fire in these sites (Waldrop & Harden 2008). Declines in
microbial biomass C, fungal hyphal length, and basal soil
respiration from lab incubations were likewise found 0e2 yr
€ inen & Fritze
after fire in Scandinavian boreal forests (Pietika
1996).
Large increases in microbial respiration following fire are
therefore surprising given the concurrent declines in microbial biomass and function. To increase heterotrophic respiration, fire would have to dramatically increase soil massspecific rates of decomposition to compensate for combustion
losses of C from the soil profile, which would tend to reduce
heterotrophic respiration on an area basis. There is some
evidence for increased mass-specific microbial respiration in
burned soils (O’Neill et al. 2006), but these results were based
on lab incubations of humic soil from a single site that had
burned two weeks earlier, and are inconsistent with the
€ inen & Fritze (1996). Thus, it is not clear how
findings of Pietika
long after fire increases in substrate quality and microbial
decomposition persist, or if decomposition shows the same
fire response under field conditions.
Since the decomposition potential of the microbial
community appears to decline following fire, other mechanisms may be required to explain observed rates of soil
respiration. One such explanation may be root respiration
from burned plantsdCzimczik et al. (2006) found that soil
respiration was w50 % lower in black spruce forest that
burned recently in Canada, but 14C signatures provided no
indication for an increase in heterotrophic respiration.
Instead, they concluded that respiration from the roots of
burned black spruce trees could account for 50e80 % of soil
respiration. Respiration from dying roots and associated
mycorrhizas has also been shown to persist for w1 yr after
tree girdling (Bhupinderpal et al. 2003). These results suggest
that other studies may have overestimated heterotrophic
respiration following fire if they assumed that root respiration
was zero. Nonetheless, even low rates of heterotrophic
respiration will cause burned ecosystems to lose C until inputs
from NPP begin to recover after several years (Bond-Lamberty
et al. 2004).
Resolving the source of soil respiration and the rate of
decomposition in burned boreal ecosystems is important for
determining the ultimate feedback to global climate change. It
has been hypothesized that decomposition following fire may
release as much C as the fire itself (Richter et al. 2000). One
implication of increased fire frequency is that a greater fraction of the boreal zone will be occupied by forests that have
recently lost soil and biomass C but have not accumulated
large humus stocks, resulting in lower levels of C storage
(Kasischke et al. 1995; Wirth et al. 2002; Wardle et al. 2003).
However, changes in albedo may cancel and even reverse the
positive climate feedbacks associated with CO2 release from
boreal forest fires (Randerson et al. 2006). Therefore, the
7
magnitude as well as the sign of climate feedbacks arising
from increased boreal fire frequency may depend on the
amount of soil C mobilized by microbes, a parameter that
remains uncertain. Addressing this uncertainty will require
additional measurements of soil C stocks at high temporal
resolution across fire chronosequences and concurrent
assessment of the heterotrophic contribution to soil
respiration.
Changes in plant species composition
Changes in fire properties and climate may alter plant species
composition in boreal forests which may in turn influence
microbial decomposition. For example, increased fire
frequency will increase the dominance of early-successional
species such as grasses, forbs and deciduous trees in boreal
ecosystems (Mack et al. 2008). The resulting differences in
litter quality and chemistry among plant species may then
affect litter decay rates (Anderson 1991) and levels of soil C
storage. Many deciduous and early-successional plant species
produce litter that decomposes more rapidly than the moss
and coniferous litter produced in late-successional forests
(Moore et al. 2005; Turetsky et al. 2008). Furthermore, dominance by early-successional species such as grasses could
alter fungal community composition by favoring arbuscular
over ectomycorrhizal fungi (Treseder et al. 2004). A shift
toward arbuscular mycorrhizas may speed the accumulation
of soil C through production of the fungal glycoprotein glomalin (Treseder et al. 2007) and through reduced decomposition by extracellular enzymes derived from ectomycorrhizal
fungi (Read & Perez-Moreno 2003; Talbot et al. 2008). Although
there is scant empirical evidence, it is also possible that
arbuscular biomass decomposes more rapidly than ectomycorrhizal biomass, which would reduce soil C accumulation
under early-successional plant species (Treseder & Allen
2000).
Climate-induced changes in vegetation communities are
also expected to alter decomposition rates through litter and
physical effects. After several decades, water table drawdown
in Finnish peat bogs shifts the plant community toward
woody plants that produce litter with slow decay rates (Laine
et al. 2010). In Alaskan boreal forests, the
et al. 1995; Strakova
presence of particular plant species such as black spruce (Picea
mariana) and sphagnum moss are correlated with higher
levels of soil organic C and potentially lower decomposition
rates (Hollingsworth et al. 2008). Such differences may arise
not only because of low litter quality, but also due to plantinduced changes in temperature and hydrology, such as
shading from coniferous trees and soil insulation from
mosses (Hollingsworth et al. 2008).
Feedbacks from increased nitrogen
mineralization
If decomposition rates increase in a warmer climate, the
nutrients bound up in organic matter may be released and
increase nutrient availability for plants and microbes (Rustad
et al. 2001; Hobbie et al. 2002). Higher nutrient levels could then
Please cite this article in press as: Steven D Allison, Kathleen K Treseder, Climate change feedbacks to microbial decomposition
in boreal soils, Fungal Ecology (2011), doi:10.1016/j.funeco.2011.01.003
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feedback to affect litter quality, microbial activity and rates of
decomposition. Many of these feedbacks have been observed
in warming manipulations around the globe, with average
increases of 46 % for N mineralization and 19 % for plant
productivity (Rustad et al. 2001). However, measurements of N
cycling in boreal warming experiments are scarce, with only
a few studies reporting changes in N availability. In the CLIMEX experiment in Norwegian boreal forest, whole-catchment warming increased nitrate and ammonium losses in
runoff by 11 % and 60 %, respectively, although there were no
€ kewille &
apparent changes in litter decomposition rates (Lu
Wright 1997; Verburg et al. 1999). Similarly, available nitrate,
ammonium, and phosphate increased by up to 34 %, 14-fold,
and 60 %, respectively, in organic horizons of warmed black
spruce soils in Alaska (Van Cleve et al. 1990). Soil potassium
concentrations also increased, and foliar N concentrations
were elevated by 38 %. In contrast, open top chambers did not
increase nutrient supply rates in a Canadian boreal forest,
possibly because the treatments were not effective at warming the soil (Dabros & Fyles 2010). Similarly, we have found
relatively little effect of warming treatments on resin-available N and phosphorus in Alaskan boreal ecosystems (Allison
& Treseder 2008; Allison et al. 2010b).
Although the effect of climate warming on nutrient availability is uncertain in boreal forests, many studies have
examined the consequences of increased nutrient availability
for microbial communities and decomposition. In general,
these studies show that increased availability of nutrients
(mainly N) strongly impacts microbial communities, but has
inconsistent effects on decomposition. Mycorrhizal fungi are
particularly sensitive to N availability, and frequently decline
in response to N deposition and fertilization (Arnolds 1991;
Brandrud & Timmermann 1998; Lilleskov et al. 2001). Certain
nitrophilic taxa of mycorrhizas may persist under high N
conditions (Boxman et al. 1998; Strengbom et al. 2001; Lilleskov
et al. 2002), but overall abundance declines, possibly due to
reductions in belowground C allocation by host plants
€ gberg et al. 2003; Allison et al. 2008). There is some evidence
(Ho
for N-limitation of saprotrophic fungi from boreal forests, but
only at relatively low levels of N addition (Allison et al. 2010a);
high levels of N addition have been hypothesized to negatively
affect decomposer fungi (Fog 1988). Demoling et al. (2008)
found that fungal biomass and bacterial growth rates
declined by >40 % in response to N addition in Swedish boreal
forests. We observed a similar response in an early-successional boreal forest in Alaska, but no response of microbial
biomass in an adjacent unburned forest (Allison et al. 2008;
Allison et al. 2010a). However, both ecosystems showed
significant changes in fungal community composition.
It is not yet clear how microbial responses to nutrients will
affect decomposition processes in boreal forests. Studies from
other ecosystems suggest that decomposition responses to N
are variable and depend on many factors such as litter quality,
ecosystem type and level of nutrient addition (Carreiro et al.
2000; Neff et al. 2002; Waldrop et al. 2004; Knorr et al. 2005).
Long-term fertilization with N and phosphorus in the Alaskan
arctic led to massive losses of C and N from the soil profile,
accompanied by large changes in bacterial community
composition (Mack et al. 2004; Campbell et al. 2010). Similar
levels of N addition in an early-successional boreal site in
S.D. Allison, K.K. Treseder
Alaska increased organic C-decomposition enzyme activities
and litter decomposition rates, and appeared to cause
substantial losses of soil C (Allison et al. 2010a). However, there
was no evidence for increased rates of soil C loss through soil
respiration at a nearby mature forest site (Allison et al. 2008).
Other fertilization studies in Swedish and Finnish boreal
forests imply that soil organic C decomposition slows down
€ kipa
€a
€ 1995; Olsson et al. 2005). Together,
with N addition (Ma
the relatively weak response of nutrient mineralization to
warming and the inconsistent response of decomposition to N
addition suggest that indirect climate feedbacks involving
nutrient availability will be relatively weak in boreal forests.
However, fertilization experiments may be poor analogs for
changes in nutrient availability under climate warming since
low levels of nutrient addition may have stronger or distinct
impacts on C cycling relative to typical fertilizer levels (Allison
et al. 2009).
Interactive effects
As the boreal climate warms, direct and indirect effects will
occur simultaneously, leading to the potential for interactions
and additional feedbacks. Here we will focus mainly on
feedbacks involving fire and permafrost that may be particularly strong and relevant for decomposition in boreal ecosystems. Fire is critical because it has rapid and dramatic effects
on soil temperature, permafrost dynamics, microbial
communities, vegetation communities and nutrient availability (Wein & MacLean 1983; Dyrness et al. 1986). Therefore
fire leads to a cascade of additional indirect effects that may
alter decomposition and C storage for decades. Similarly,
permafrost meltingdwhether caused by fire or climate warmingdalso impacts biological communities, nutrient availability and C storage over the long term.
Fire appears to increase the sensitivity of boreal ecosystems to other environmental changes. For example, increased
N availability had no effect on soil respiration in mature
Alaskan boreal forest, but reduced soil C pools and ultimately
soil respiration in an adjacent burned ecosystem (Allison et al.
2008; Allison et al. 2010a). Soil respiration in the burned
ecosystem also showed an initial positive response to experimental warming, whereas the unburned system showed
a negative response (Bergner et al. 2004; Allison & Treseder
2008). Increases in soil temperature also make recently
burned ecosystems highly susceptible to permafrost thaw
(O’Neill et al. 2002). These systems typically experience
increases in active layer depth and reductions in soil moisture, leading to higher C losses through soil respiration (Brown
1983; Dyrness et al. 1986; Kasischke & Stocks 2000). Losses of
permafrost and reductions in the depth of insulating organic
horizons can then feedback positively to warmer, drier soils
that support different vegetation communities and are more
susceptible to future fire (Harden et al. 2000, 2006).
Whether due to fire or direct warming, permafrost loss will
affect decomposition through other ecosystem feedbacks. For
example, increased active layer depth and access of decomposer microbes to available forms of organic matter may
stimulate nutrient mineralization more strongly than in nonpermafrost soils (Van Cleve et al. 1990). Permafrost soils are
Please cite this article in press as: Steven D Allison, Kathleen K Treseder, Climate change feedbacks to microbial decomposition
in boreal soils, Fungal Ecology (2011), doi:10.1016/j.funeco.2011.01.003
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also associated with different vegetation communities. In
Alaskan ecosystems, black spruce-sphagnum moss communities typically grow on permafrost soils and produce recalcitrant litter with slow decomposition rates (Kasischke &
Stocks 2000). In contrast, white spruce (Picea glauca) and
aspen (Populus tremuloides) communities are more common on
drier, non-permafrost soils (Van Cleve & Yarie 1986) and may
produce litter with higher decomposition rates. These
systems may in turn be more susceptible to fire. Together
these processes will likely lead to increased loss of soil C from
boreal ecosystems.
Conclusions
Climate change will clearly impact boreal ecosystems and
decomposition processes through direct and indirect mechanisms. It is likely that feedbacks involving permafrost and fire
will impact boreal microbes, decomposition and C storage
most strongly. Within the boreal zone, permafrost soils may
represent only w50 % of the land area, but they contain the
vast majority of soil C stocks (Schuur et al. 2008). As a result,
permafrost loss will have a dramatic impact on the C balance
of boreal ecosystems, as predicted for tundra ecosystems as
well. Increases in fire frequency will probably lead to further
loss of permafrost, thereby accelerating a positive feedback to
decomposition. However, the greenhouse warming impact of
this decomposition feedback may be at least partly offset by
long-term changes in albedo (Randerson et al. 2006) and
reductions in the activity of decomposer microbes following
fire (Waldrop & Harden 2008).
The boreal zone is large and heterogeneous, with permafrost absent from many southern and Scandinavian boreal
forests (Fig 2). These regions will probably experience much
weaker feedbacks to decomposition as a result of climate
warming. Ecosystems on well-drained soils lacking permafrost may show small or negative responses to climate
warming due to soil drying and moisture limitation of
decomposer organisms. Decomposition in these systems
may, however, respond positively to predicted increases in
precipitation. Microbial communities may respond to vegetation shifts or changes in nutrient mineralization in both
non-permafrost and permafrost soils, but the few studies that
have examined these feedbacks suggest that they will be
small relative to changes in permafrost and fire. One important implication of these conclusions is that global models
need to account for the spatial distributions of fire and
permafrost in the boreal zone in order to accurately predict C
fluxes under climate change.
Although it will be helpful to revise models, we also
emphasize that accurate predictions of global change feedbacks
will require a greater empirical focus on undersampled regions
of the boreal zone. Siberia contains by far the largest fraction of
boreal land area and soil C, yet Siberian ecosystems have
received much less attention in the literature than have Alaskan, Canadian and Scandinavian boreal forests. Warming
manipulations should therefore be conducted in a wider range
of ecosystems to better represent the heterogeneity within the
boreal zone. It is problematic that only one of the warming
studies in Table 1 was conducted on permafrost soils, and none
9
of them was located in Siberian boreal forest. Warming
manipulations in peat bogs, which store a large fraction of
boreal soil C (Gorham 1991), are similarly lacking. Integrating
spatially resolved models with targeted empirical studies is
absolutely essential for evaluating the mechanisms and feedbacks predicted to occur under global change in the boreal zone.
Acknowledgments
This work was funded by a NOAA Climate and Global Change
Postdoctoral Fellowship to SDA and National Science Foundation grants to KKT.
references
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soil respiration under nitrogen addition in Alaskan boreal
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