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By Daniel B. Metcalfe
Soils are the largest single terrestrial source of carbon dioxide (CO2), but hese emissions are highly sensitive to a range of factors associated with climate change and human land use (1). Researchers have long sought to
better understand the underlying drivers
of soil CO2 emissions, but the duration of
experiments is all too often constrained by
project deadlines and personnel contracts,
hampering our ability to understand and
predict the many gradual but important
processes that occur in soils (2). On page 101
of this issue, Melillo et al. ( 3) report on an
intriguing 26-year record of soil respiration
responses to warming in a temperate forest.
The results from this unusually long time
series highlight both the potential pitfalls
of drawing hasty conclusions from short-term studies and the importance of long-term experiments in ecosystem and climate
science.
Shifts in the terrestrial carbon store, of
which soils constitute around 70%, are one
of the most important but least under-
stood drivers of variation in atmospheric
CO2 levels ( 4, 5). Soil carbon is sensitive to
a wide range of factors, of which tempera-
ture is one of the most important from a
climate change perspective ( 6). Generally,
warm conditions promote microbial activ-
ity. Global warming would therefore be ex-
pected to increase microbial breakdown of
organic carbon and subsequent release as
CO2, but demonstrating this conclusively
has proved difficult.
Several approaches have been used to
examine patterns in, and regulators of, soil
carbon cycling. Multiple controlled experiments have repeatedly shown increasing
soil respiration under warmer conditions
( 6, 7). A comprehensive global synthesis
of soil respiration measurements found an
increase associated with rising air temperatures since the 1960s, but the exact mechanisms linking temperature and soil carbon
cycling remain unclear ( 8). Furthermore, it
is not well known how much soil carbon is
readily available for microbial breakdown
versus how much is locked up in recalcitrant material and to what extent this could
shift with climate change ( 6, 9).
Melillo et al. make important advances in
addressing these gaps with one of the most
detailed pictures yet of the responses of
soil microbes and carbon cycling over more
than two decades of experimental warming.
Their results will be invaluable in ongoing
efforts to better predict and mitigate carbon
losses from soils that face rapid warming
associated with climate change.
The authors compare soil respiration in
forest plots heated with buried cables with
soil respiration in untouched plots. The in-
sights derived from these measurements are
amplified by repeating these measurements
for so long. The authors also draw from a
wide range of shorter-term published ex-
periments from the same site to elucidate
the mechanisms that control observed
shifts in respiration between plots and
over time. Over the 26-year period of the
experiment, they observed three multiyear
phases of soil respiration (see the figure). In
the first phase, soil respiration steadily de-
creased under warmed conditions. This was
followed by a second phase where warming
induced little change in respiration, and
then a third phase of steadily rising respira-
tion. At the time of publication, the experi-
ment is entering a fourth phase where soil
respiration is again gradually declining.
The authors conclude that decades-long
warming stimulates phases of minimal
warming-induced respiration, correspond-
ing to widespread soil microbial commu-
ECOLOGY
Microbial change in warming soils
Long-term reorganization of microbial communities leads to pulses in carbon release
1991 2001 2007 2012 2016
Phase 1 Phase 2 Phase 3 Phase 4
300
0
(g CO2–C m–2 year–1)
Changes in soil
CO2 emissions
in heated plots
relative to
control plots
Temperature
5°C above
ambient
temperature
Carbon forms in soil
Labile and recalcitrant
Microbial types in soil
Fungi and bacteria
Microbial carbon starvation
Decline in labile carbon, microbial
biomass, and soil respiration
Impoverished
microbial
community
Reorganized
microbial
community
Initial conditions
at onset of
warming
Continued microbial shift
Rise in breakdown of lignin
and soil respiration
1991 2001 2007 2012 2016
Phase 1 Phase 2 Phase 3
300
ove
Decline
in lignin and soil
respiration
Department of Physical Geography and Ecosystem Science,
Lund University, Sölvegatan 12, SE 223 62, Lund, Sweden, and
Department of Ecology and Environmental Science, Umeå
University, Linnaeus väg 6, SE 901 87, Umeå, Sweden.
Email: dbmetcalfe@googlemail.com
6 OCTOBER 2017 • VOL 358 ISSUE 6359 41
Long-term reorganization of soil microbial communities under warming
In a 26-year warming experiment, carbon dioxide emissions from heated plots changed with time as microbial communities reorganized.