, 988 (2011);
, et al.Yude Pan
A Large and Persistent Carbon Sink in the World's Forests
This copy is for your personal, non-commercial use only.
clicking here. colleagues, clients, or customers by
, you can order high-quality copies for your
If you wish to distribute this article to others
The following resources related to this article are available online at
here.following the guidelines
can be obtained by
Permission to republish or repurpose articles or portions of articles
Updated information and services,
): August 18, 2011 www.sciencemag.org (this infomation is current as of
version of this article at:
including high-resolution figures, can be found in the online
can be found at:
Supporting Online Material
, 11 of which can be accessed free:
cites 33 articles
This article appears in the following
registered trademark of AAAS.
is a Science 2011 by the American Association for the Advancement of Science; all rights reserved. The title
CopyrightAmerican Association for the Advancement of Science, 1200 New York Avenue NW, Washington, DC 20005.
(print ISSN 0036-8075; online ISSN 1095-9203) is published weekly, except the last week in December, by theScience
on August 18, 2011
propagation are directly accessible to anyone
with basic statistical knowledge. This should ul-
timately open the way for a complete character-
and bottom-up mechanisms involved in the reg-
and how this in turn affects transmission and
The underlying process of bursting infected
RBCs and invasion of uninfected RBCs is com-
mon to blood-phase malaria across animal taxa.
The methods we introduce will consequently be
generally applicable. The strength of the mouse
unaware of any experimental time series in hu-
man patients in which these parameters were
directly measured, but our analyses suggest that
future longitudinal studies of individual patients
that undertake the simple assays required to di-
densities will lead to considerable insights into
the factors regulating human malaria.
References and Notes
1. R. Carter, D. Walliker, Ann. Trop. Med. Parasitol. 69,
2. L. Molineaux, M. Träuble, W. E. Collins, G. M. Jeffery,
K. Dietz, Trans. R. Soc. Trop. Med. Hyg. 96, 205 (2002).
3. K. Dietz, G. Raddatz, L. Molineaux, Am. J. Trop. Med. Hyg.
75 (suppl.), 46 (2006).
4. D. T. Haydon, L. Matthews, R. Timms, N. Colegrave,
Proc. R. Soc. B 270, 289 (2003).
5. R. M. Ribeiro et al., J. Virol. 84, 6096 (2010).
6. O. N. Bjørnstad, B. Finkenstädt, B. T. Grenfell,
Ecol. Monogr. 72, 169 (2002).
7. R. M. Anderson, R. M. May, Infectious Diseases of
Humans (Oxford Univ. Press, Oxford, 1991).
8. M. A. Nowak, R. M. May, Virus Dynamics: Mathematical
Principles of Immunology and Virology (Oxford Univ.
Press, Oxford, 2000).
9. M. M. Stevenson, E. M. Riley, Nat. Rev. Immunol. 4,
10. M. Walther et al., J. Immunol. 177, 5736 (2006).
11. M. R. Miller, L. Råberg, A. F. Read, N. J. Savill,
PLOS Comput. Biol. 6, e1000946 (2010).
12. N. Mideo et al., Am. Nat. 172, E214 (2008).
13. R. Antia, A. Yates, J. C. de Roode, Proc. R. Soc. B 275,
14. B. F. Kochin, A. J. Yates, J. C. de Roode, R. Antia,
PLoS ONE 5, e10444 (2010).
15. A. Handel, I. M. Longini Jr., R. Antia, J. R. Soc. Interface
7, 35 (2010).
16. C. L. Ball, M. A. Gilchrist, D. Coombs, Bull. Math. Biol.
69, 2361 (2007).
17. A. S. Perelson, Nat. Rev. Immunol. 2, 28 (2002).
18. R. A. Saenz et al., J. Virol. 84, 3974 (2010).
19. K. A. Lythgoe, L. J. Morrison, A. F. Read, J. D. Barry,
Proc. Natl. Acad. Sci. U.S.A. 104, 8095 (2007).
20. L. Molineaux, K. Dietz, Parassitologia 41, 221
21. R. Killick-Kendrick, W. Peters, Eds., Rodent Malaria
(Academic Press, London, 1978).
22. V. C. Barclay et al., Proc. R. Soc. B 275, 1171
23. S. Huijben, thesis, University of Edinburgh (2010).
24. G. H. Long, B. H. K. Chan, J. E. Allen, A. F. Read,
A. L. Graham, BMC Evol. Biol. 8, 128 (2008).
25. See supporting material on Science Online.
26. P. G. McQueen, F. E. McKenzie, Proc. Natl. Acad.
Sci. U.S.A. 101, 9161 (2004).
27. B. Hellriegel, Proc. R. Soc. B 250, 249 (1992).
28. C. Hetzel, R. M. Anderson, Parasitology 113, 25
29. W. Jarra, K. N. Brown, Parasitology 99, 157 (1989).
30. A. A. Lamikanra et al., Blood 110, 18 (2007).
31. S. S. Pilyugin, R. Antia, Bull. Math. Biol. 62, 869
32. R. Antia, J. C. Koella, J. Theor. Biol. 168, 141 (1994).
33. J. R. Glynn, D. J. Bradley, Parasitology 110, 7 (1995).
34. M. S. Russell et al., J. Immunol. 179, 211 (2007).
35. D. L. Chao, M. P. Davenport, S. Forrest, A. S. Perelson,
Immunol. Cell Biol. 82, 55 (2004).
36. R. Stephens, J. Langhorne, PLoS Pathog. 6, e1001208
37. C. Othoro et al., J. Infect. Dis. 179, 279 (1999).
38. F. P. Mockenhaupt et al., Blood 104, 2003 (2004).
39. S. Wambua, J. Mwacharo, S. Uyoga, A. Macharia,
T. N. Williams, Br. J. Haematol. 133, 206 (2006).
40. K. Baer, C. Klotz, S. H. Kappe, T. Schnieder, U. Frevert,
PLoS Pathog. 3, e171 (2007).
41. N. J. Savill, W. Chadwick, S. E. Reece, PLOS Comput. Biol.
5, e1000416 (2009).
42. Z. Su, A. Fortin, P. Gros, M. M. Stevenson, J. Infect. Dis.
186, 1321 (2002).
43. G. H. Long, B. H. K. Chan, J. E. Allen, A. F. Read,
A. L. Graham, Parasitology 133, 673 (2006).
44. K.-H. Chang, M. Tam, M. M. Stevenson, J. Infect. Dis.
189, 735 (2004).
Acknowledgments: Our empirical work was funded by the
Wellcome Trust (A.F.R., V.C.B., G.H.L.), the Darwin
Trust of the University of Edinburgh (S.H.), and the UK
Biotechnology and Biological Sciences Research Council
(A.L.G., G.H.L.), and the theoretical work by the Bill
and Melinda Gates Foundation (C.J.E.M., B.T.G., O.N.B.),
the RAPIDD program of the Science and Technology
Directorate (B.T.G., A.L.G., A.F.R.), and National Institute
of General Medical Sciences grant R01GM089932
(B.G., O.N.B., A.F.R.). We thank N. Mideo and P. Klepac
for extensive discussion. All authors discussed the
results and implications and commented on the
manuscript at all stages. C.J.E.M. and O.N.B. developed
the statistical approach; A.F.R., V.B., and S.H. designed
and performed the dose-dependent and CD4+T cell–
depleted mice experiments; A.L.G. and G.H.L. designed
and performed the innate immunity experiments.
The authors declare no competing interests.
Supporting Online Material
Materials and Methods
Figs. S1 to S12
21 February 2011; accepted 22 June 2011
A Large and Persistent Carbon Sink
in the World’s Forests
Yude Pan,1* Richard A. Birdsey,1Jingyun Fang,2,3Richard Houghton,4Pekka E. Kauppi,5
Werner A. Kurz,6Oliver L. Phillips,7Anatoly Shvidenko,8Simon L. Lewis,7Josep G. Canadell,9
Philippe Ciais,10Robert B. Jackson,11Stephen W. Pacala,12A. David McGuire,13Shilong Piao,2
Aapo Rautiainen,5Stephen Sitch,7Daniel Hayes14
The terrestrial carbon sink has been large in recent decades, but its size and location remain
uncertain. Using forest inventory data and long-term ecosystem carbon studies, we estimate a
total forest sink of 2.4 T 0.4 petagrams of carbon per year (Pg C year–1) globally for 1990 to 2007.
We also estimate a source of 1.3 T 0.7 Pg C year–1from tropical land-use change, consisting of a
gross tropical deforestation emission of 2.9 T 0.5 Pg C year–1partially compensated by a carbon
sink in tropical forest regrowth of 1.6 T 0.5 Pg C year–1. Together, the fluxes comprise a net global
forest sink of 1.1 T 0.8 Pg C year–1, with tropical estimates having the largest uncertainties. Our total
forest sink estimate is equivalent in magnitude to the terrestrial sink deduced from fossil fuel
emissions and land-use change sources minus ocean and atmospheric sinks.
negotiations to limit greenhouse gases require
an understanding of the current and potential
future role of forest C emissions and sequestra-
orests have an important role in the global
tion in both managed and unmanaged forests.
mate Change (IPCC) show that the net uptake by
terrestrial ecosystems ranges from less than 1.0
to as much as 2.6 Pg C year–1for the 1990s (1).
More recent global C analyses have estimated a
terrestrial C sink in the range of 2.0 to 3.4 Pg C
year–1on the basis of atmospheric CO2obser-
vations and inverse modeling, as well as land
observations (2–4). Because of this uncertainty
and the possible change in magnitude over time,
constraining these estimates is critically impor-
tant to support future climate mitigation actions.
1U.S. Department of Agriculture Forest Service, Newtown
Square,PA 19073, USA.2Key Laboratory for Earth Surface Pro-
China.3State Key Laboratory of Vegetation and Environmental
Change, Institute of Botany, Chinese Academy of Sciences,
Resources Canada, Canadian Forest Service, Victoria, BC, V8Z
1M5, Canada.7School of Geography, University of Leeds, LS2
9JT, UK.8International Institute for Applied Systems Analysis,
entific and Industrial Research Organization Marine and Atmo-
France.11Duke University, Durham, NC 27708, USA.12Prince-
ton University, Princeton, NJ 08544, USA.13U.S. Geological
Survey, Alaska Cooperative Fish and Wildlife Research Unit,
University of Alaska, Fairbanks, AK 99775, USA.14Oak Ridge
National Laboratory, Oak Ridge, TN 37831, USA.
*To whom correspondence should be addressed. E-mail:
19 AUGUST 2011VOL 333
on August 18, 2011
Here, we present bottom-up estimates of C
stocks and fluxes for the world’s forests based on
recent inventory data and long-term field obser-
vations coupled to statistical or process models
comprehensive C pools of the forest sector (dead
wood, harvested wood products, living biomass,
in C stocks across countries, regions, and conti-
nents representing boreal, temperate, and tropical
forests (5, 6). To gain full knowledge of the trop-
ical C balance, we subdivided tropical forests in-
is an overlooked category, and its C uptake is
usually not reported but is implicit in the tropical
land-use change emission estimates. Although
deforestation, reforestation, afforestation and the
carbon outcomes of various management prac-
tices are included in the assessments of boreal
and temperate forest C sink estimates, we sepa-
rately estimated three major fluxes in the tropics:
C uptake by intact forests, losses from deforesta-
tion, and C uptake of forest regrowth after an-
thropogenic disturbances. The area of global
fluxes is 3.9 billion ha, representing 95% of the
world’s forests (7) (table S2).
Global forest C stocks and changes. The
current C stock in the world’s forests is estimated
soil (to 1-m depth), 363 T 28 Pg C (42%) in live
biomass (above and below ground), 73 T 6 Pg C
(8%)indeadwood,and 43T 3PgC (5%)inlitter
(table S3). Geographically, 471 T 93 Pg C (55%)
is stored in tropical forests, 272 T 23 Pg C (32%)
in boreal, and 119 T 6 Pg C (14%) in temperate
whereas the density in temperate forests is ~60%
of the other two biomes (155 Mg C ha–1).
Although tropical and boreal forests store the
most carbon, there is a fundamental difference in
their carbon structures: Tropical forests have 56%
of carbon stored in biomass and 32% in soil,
whereas boreal forests have only 20% in biomass
and 60% in soil.
The average annual change in the C stock of
established forests (Table 1) indicates a large
uptake of 2.5 T 0.4 Pg C year–1for 1990 to 1999
and a similar uptake of 2.3 T 0.5 Pg C year–1for
2000 to 2007. Adding the C uptake in tropical
regrowth forests to those values indicates a
persistent global grossforestC sinkof 4.0T0.7
1990, our analysis revealed important regional
in temperate forests increased by 17% in 2000 to
2007 compared with 1990 to 1999, in contrast to
C uptake in intact tropical forests, which de-
creased by 23% (but nonsignificantly). Boreal
forests, on average, showed little difference be-
tween the two time periods (Fig. 1). Subtract-
ing C emission losses from tropical deforestation
and degradation, the global net forest C sink
was 1.0 T 0.8 and 1.2 T 0.9 Pg C year–1for
1990 to 1999 and 2000 to 2007, respectively
Forest carbon sinks by regions, biomes, and
average sink of 0.5 T 0.1 Pg C year–1for two dec-
ades (Table 2, 20 and 22% of the global C sinks
in established forests). However, the overall sta-
bility of the boreal forest C sink is the net result
countries and regions associated with natural dis-
turbances and forest management. Asian Russia
had the largest boreal sink, but that sink showed
no overall change, even with increased emissions
from wildfire disturbances (8). In contrast, there
was a notable sink increase of 35% in European
Russia (Fig. 1) attributed to several factors: in-
creased areas of forests after agricultural aban-
donment, reduced harvesting, and changes of
forest age structure to more productive stages,
particularly for the deciduous forests (8). In con-
trast to the large increase of biomass sinks in
European Russia and northern Europe (8, 9), the
reduced by half between the two periods, mostly
due to the biomass loss from intensified wildfires
and insect outbreaks (10, 11). A net loss of soil C
in northern Europe was attributed to shifts of
forest to nonforest in some areas. Overall, the
relativelystable boreal C sinkis thesum of anet
reduction in Canadian biomass sink offset by
and a balance between decreased litter and soil C
sinks in northern Eurasia and a region-wide in-
0.1 and 0.8 T 0.1 Pg C year–1(27 and 34%) to
the global C sinks in established forests for two
decades (Table 2). The primary reasons for the
increased C sink in temperate forests are the
increasing density of biomass and a substantial
increase in forest area (12, 13). The U.S. forest
C sink increased by 33% from the 1990s to
2000s, caused by increasing forest area; growth
of existing immature forests that are still recover-
ing from historical agriculture, grazing, harvesting
(12, 14); and environmental factors such as CO2
fertilization and Ndeposition(15).However,for-
ests in the western United States have shown
considerably increased mortality over the past
few decades, related to drought stress, and in-
creased mortality from insects and fires (16, 17).
The European temperate forest sink was stable
between 1990 to 1999 and 2000 to 2007. There
was a large C sink in soil due to expansion of
2000s (7,18).However, theincreased C sink in
biomass during the second period (+17%)
helped to maintain the stability of the total C sink.
China’s forest C sink increased by 34% between
sink almost doubling (Table 2). This was caused
primarily by increasing areas of newly planted
forests, the consequence of an intensive national
afforestation/reforestation program in the past
few decades (table S2) (19).
Table 1. Global forest carbon budget (Pg C year–1) over two time periods. Sinks are positive values;
sources are negative values.
Carbon sink and source in biomes 1990–1999 2000–20071990–2007
Tropical intact forest*
Total sink in global established forests†
0.50 T 0.08
0.67 T 0.08
1.33 T 0.35
2.50 T 0.36
0.50 T 0.08
0.78 T 0.09
1.02 T 0.47
2.30 T 0.49
0.50 T 0.08
0.72 T 0.08
1.19 T 0.41
2.41 T 0.42
Tropical regrowth forest‡
Tropical gross deforestation emission§
Tropical land-use change emission||
1.57 T 0.50
–3.03 T 0.49
–1.46 T 0.70
1.72 T 0.54
–2.82 T 0.45
–1.10 T 0.70
1.64 T 0.52
–2.94 T 0.47
–1.30 T 0.70
Global gross forest sink¶
Global net forest sink#
4.07 T 0.62
1.04 T 0.79
4.02 T 0.73
1.20 T 0.85
4.05 T 0.67
1.11 T 0.82
Equations of global forest C fluxes
Festablished forests= Fboreal forests+ Ftemperate forests+ Ftropical intact forests
Ftropical land-use change= Ftropical gross deforestation+ Ftropical regrowth forests
Fgross forest sink= Festablished forests+ Ftropical regrowth forests
Fnet forest sink= Festablished forests+ Ftropical land-use change
*Tropical intact forests: tropical forests that have not been substantially affected by direct human activities; flux accounts for the
plus afforested land in boreal and temperate biomes, in additiontointact forest in the tropics (Eq. 1).
tropical forests that are recovering frompast deforestationand logging.
fromtropicalland-use change,whichisa net balance oftropicalgrossdeforestationemissionsand Cuptakeinregrowthforests (Eq.2).
It may be referenced as a tropical net deforestation emission in the literature.
global established forests and tropical regrowth forests (Eq. 3).
(Eq. 4). It can be calculated in two ways: (i) total sink in global established forests minus tropical land-use change emission or (ii) total
global gross forest sink minus tropical gross deforestation emission.
‡Tropical regrowth forests:
§Tropical gross deforestation: the total C emissions from
¶Global gross forest sink:the sum of total sinks in
#Global net forest sink: the net budget of global forest fluxes
VOL 33319 AUGUST 2011
on August 18, 2011
Tropical intact forests (1392 Mha) represent
~70% of the total tropical forest area (1949 Mha)
that accounts for the largest area of global forest
biomes (~50%). We used two networks of per-
manent monitoring sites spanning intact tropical
forest across Africa (20) and South America (21)
and assumed that forest C stocks of Southeast
Asia (9% of total intact tropical forest area) are
changing at the mean rate of Africa and South
America, as we lack sufficient data in Southeast
Asia to make robust estimates. These networks
are large enough to capture the disturbance-
recovery dynamics of intact forests (6, 20, 22).
year–1for 1990 to 1999 and 2000 to 2007,
Table 2. Estimated annual change in C stock (Tg C year–1) by biomes by country or region for the time periods of 1990 to 1999 and 2000 to 2007. Estimates
material. ND, data not available; , litter is included in soils.
wood Litter Soil
(Mg C ha–1
wood Litter Soil
(Mg C ha–1
(Tg C year–1) (Tg C year–1)
61 6663 45 19 25564 0.39 6997 43 42 13264 660.39
0.44 103 125 132101
1001572 0.911001692 1.05
1.03345 673454 156777
1630204 166 2862092494 3630.731444 273158 23018922944890.69
2991 204166 49820940686151.04 2941273158 456 1894017 7281.04
*Carbon outcomes of forest land-use changes (deforestation, reforestation, afforestation, and management practices) are included in the estimates in boreal and temperate forests.
the area that includes Norway, Sweden, and Finland.‡Estimates for the continental U.S. and a small area in southeast Alaska.
all tropical forests including tropical intact and regrowth forests.¶Areas excluded from this table include interior Alaska (51 Mha in 2007), northern Canada (118 Mha in 2007), and “other wooded
land” reported to the Food and Agriculture Organization.
||Estimates for §Estimates for global established forests.
19 AUGUST 2011 VOL 333
on August 18, 2011
0.4 Pg C year–1for 1990 to 2007 is approx-
imately half of the total global C sink in estab-
lished forests (2.4 T 0.4 Pg C year–1) (Table 1).
When only the biomass sink is considered, about
two-thirds of the global biomass C sink in estab-
lished forests is from tropical intact forests (1.0
period 2000 to 2007 (–23%) was caused by
deforestation reducing intact forest area (–8%)
appeared strong enough to affect the tropics-wide
decadal C sink estimate (–15%). Except for the
Amazon drought, the recent excess of biomass C
ests appears to result from progressively enhanced
productionshouldleadtoenhancedsoil C seques-
tration, but we lack data about changesinsoil C
stocks for tropical intact forests, so the C sink for
tropical intact forests may be underestimated.
Tropical land-use changes have caused net
C releases in tropical regions by clearing forests
for agriculture, pasture, and timber (24), second
in magnitude to fossil fuel emissions (Table 3).
Tropical land-use change emissions are a net
balance of C fluxes consisting of gross tropical de-
forestation emissions partially compensated by C
sinks in tropical forest regrowth. They declined
from1.5T 0.7PgCyear–1inthe1990sto1.1T 0.7
Pg C year–1for 2000 to 2007 (Table 1) due to
reduced rates of deforestation and increased for-
est regrowth (25). The tropical land-use change
emissions were approximately equal to the total
global land-use emissions (Tables 1 and 3), be-
cause effects of land-use changes on C were
roughly balanced in extratropics (7, 24, 25).
Tropical deforestation produced significant
gross C emissions of 3.0 T 0.5 and 2.8 T 0.5 Pg
However, these large emission numbers are usu-
ally neglected because more than one half was
offset by large C uptake in tropical regrowth for-
ests recovering from the deforestation, logging,
or abandoned agriculture.
Tropical regrowth forests (557 Mha) repre-
sent ~30% of the total tropical forest area. The
C uptake by tropical regrowth forests is usually
implicitly included in estimated net emissions
independently as a sink (24). We estimate that
Regions of the World
No Data/Other Countries
Continental US & S. Alaska
Carbon Flux 2000-2007
Forest Carbon Flux
Carbon Flux 1990-1999
Forest Carbon Flux
Tropical Gross Deforestation
C Emissions 1990-1999
Tropical Gross Deforestation
C Emissions 2000-2007
Fig. 1. Carbon sinks and sources (Pg C year–1) in the world’s forests. Colored
bars in the down-facing direction represent C sinks, whereas bars in the
upward-facing direction represent C sources. Light and dark purple, global
established forests (boreal, temperate, and intact tropical forests); light and
dark green, tropical regrowth forests after anthropogenic disturbances; and
light and dark brown, tropical gross deforestation emissions.
Table 3. Theglobalcarbonbudgetfortwotimeperiods(PgCyear−1).Therearedifferentarrangementsto
sources and the sinks in the atmosphere and oceans. We used the C sink in globalestablished forests as a
proxy for the terrestrial sink.
Sources and sinks1990–19992000–2007
Sources (C emissions)
Fossil fuel and cement*
6.5 T 0.4
1.5 T 0.7
8.0 T 0.8
7.6 T 0.4
1.1 T 0.7
8.7 T 0.8
Sinks (C uptake)
Terrestrial (established forests)§
3.2 T 0.1
2.2 T 0.4
2.5 T 0.4
7.9 T 0.6
4.1 T 0.1
2.3 T 0.4
2.3 T 0.5
8.7 T 0.7
Global residuals||0.1 T 1.0 0.0 T 1.0
of C sinks in the global established forests (that are outside the areas of tropical land-use changes) from this study. Note that the
carbon sink in tropical regrowth forests is excluded because it is included in the term of land-use change emission (see above and
land sink or source in the212 Mha of forest not included here, onnonforest land, or systematic error in other source (overestimate) or
sink (underestimate) terms, or both.
†See (4, 7, 25). The global land-use change emission is approximately equal to the tropical land-use change emission,
VOL 33319 AUGUST 2011
on August 18, 2011
the C sinkbytropical regrowth forestswas1.6T
0.5 and 1.7 T 0.5 Pg C year–1, respectively, for
1990 to 1999 and 2000 to 2007. Our results in-
C sinks than the intact forests due to rapid bio-
mass accumulation under succession, but these
data (table S4) (6). Although distinguishing a C
sink in tropical regrowth forests does not affect
the estimated net emissions from tropical land-
use changes, an explicit estimate of this compo-
nent facilitates evaluating the complete C sink
capacity of all tropical and global forests.
When all tropical forests, both intact and
regrowth, are combined, the tropical sinks sum
to 2.9 T 0.6 and 2.7 T 0.7 Pg C year–1over the
~70% of the gross C sink in the world forests
(~4.0 Pg C year–1). However, with equally
significant gross emissions from tropical de-
forestation (Table 1), tropical forests were nearly
largest forest area, the most intense contemporary
land-use change, and the highest C uptake, but
also the greatest uncertainty, showing that invest-
ment in better understanding carbon cycling in
the tropics should be a high priority in the future.
Deadwood, litter, soil, and harvested wood
the importance of including these components
(Table 2 and table S3). Compared with biomass,
estimates of these terrestrial carbon pools are gen-
erally less certain because of insufficient data.
For deadwood, there was a large sink increase in
recent increase in natural disturbances in Siberia
and Canada. Increased deadwood carbon thus
makes a major (27%) but possibly transient con-
tribution to the total C sink in the boreal zone.
Changes in litter C accounted for a relatively
small and stable portion of the global forest C
sink. However, litter C accumulation contributed
20% of the total C sink in boreal forests and, like
deadwood, is vulnerable to wildfire disturbances.
Changes in soil C stocks accounted for more
largely driven by land-use changes. We may un-
derestimate global soil C stocks and fluxes be-
cause the standard 1-m soil depth excludes some
deep organic soils in boreal and tropical peat for-
ests (26–28). We estimate the net C change in har-
vested wood products (HWP), including wood in
use and disposed in landfills, as described in the
to the region where the wood was harvested. Car-
bon sequestration in HWP accounted for ~8% of
the total sink in established forests. This sink re-
mained stable for temperate and tropical regions
of reduced harvest in Russia in the past decade.
Data gaps, uncertainty, and suggested im-
provements in global forest monitoring. We es-
timated uncertainties based on a combination
of quantitative methods and expert opinions (6).
There are critical data gaps that affected both the
results presented here and our ability to report
and verify changes in forest C stocks in the fu-
ture. Data are substantially lacking for areas of
the boreal forest in North America, including
Alaska (51 Mha) and Canadian unmanaged for-
ests (118 Mha) (table S5). The forests in these
regions could be a small C source or sink, based
on the estimate of Canadian managed forests (10)
and modeling studiesin Alaska (30).There is also
a lack of measurement data of soil C flux in trop-
ical intact forests, which may cause uncertainty
in tropical Asia, due to the absence of long-term
field measurements, and a notable lack of data
Prioritized recommendations for improve-
ments in regional forest inventories to assess C
density, uptake, and emissions for global-scale
aggregation include the following: (i) Land mon-
itoring should be greatly expanded in the tropics
and in unsampled regions of northern boreal
forests. (ii) Globally consistent remote sensing of
land-cover change and forest-area is required to
combine the strengths of two observation sys-
tems: solid ground truth of forest C densities
from inventories and reliable forest areas from
remote sensing.(iii)Improved methodsandgreater
sampling intensity are needed to estimate non-
(iv) Better data are required in most regions for
estimating lateral C transfers in harvested wood
products and rivers.
Forestcarbonintheglobalcontext. The new
C sink estimates from world’s forests can con-
tribute to the much needed detection and attri-
bution that isrequiredin the contextof the global
within the limits of reported uncertainty, the en-
of global established forests (Table 3), as the
with T1.0 Pg C year–1uncertainty for both 1990
ly, our results imply that nonforest ecosystems
are collectively neither a major (>1 Pg) C sink
nor a major source over the two time periods that
we monitored. Because the tropical gross de-
forestation emission is mostly compensated by
forests (Fig. 1 and Table 1), the net global forest
C sink (1.1 T 0.8 Pg C year–1) resides mainly in
the temperate and boreal forests, consistent with
previous estimates (31, 32). Notably, the total
gross C uptake by the world’s established and
tropical regrowth forests is 4.0 Pg C year–1,
which is equivalent to half of the fossil fuel C
emissions in 2009 (4). Over the period that we
studied (1990 to 2007), the cumulative C sink
and 73 Pg C for the established plus regrowing
forests; the latter equivalent to 60% of cumula-
Clearly, forests play a critical role in the Earth’s
terrestrial C sinks and exert strong control on the
evolution of atmospheric CO2.
Drivers and outlook of forest carbon sink.
The mechanisms affecting the current C sink in
determine its future longevity. The C balance of
boreal forests is driven by changes in harvest
patterns, regrowth over abandoned farmlands,
of temperate forests is primarily driven by forest
management, through low harvest rates (Europe)
(33), recovery from past harvesting and agricul-
tural abandonment (U.S.) (34), and large-scale
afforestation (China) (19). For tropical forests,
deforestation and forest degradation are dom-
inant causes of C emissions, with regrowth and
an increase in biomass in intact forests being the
main sinks balancing the emissions (23, 24).
Changes in climate and atmospheric drivers
C balance of forests, but it is difficult to separate
their impacts from other factors using ground
observations. For Europe, the U.S., China, and
the tropics, evidence from biogeochemical pro-
cess models suggests that climate change, in-
creasing atmospheric CO2, and N deposition are,
at different levels, important factors driving the
long-term C sink (15, 18, 20, 23, 34). Drought
in all regions and warmer winters in boreal re-
gions reduce the forest sink through suppressed
gross primary production, increased tree mortal-
ity, increased fires, and increased insect damage
(8, 10, 18, 21, 30, 35, 36).
Our estimates suggest that currently the glob-
al established forests, which are outside the areas
of tropical land-use changes, alone can account
for the terrestrial C sink (~2.4 Pg C year–1). The
tropics are the dominant terms in the exchange
large amount of atmospheric CO2has been se-
offset by the C losses from tropical deforestation
(~2.9 Pg C year–1). This result highlights the po-
from Deforestation and Degradation program to
lessen the risk of climate change. However, an
important caveat is that adding geological carbon
from fossil fuels into the contemporary carbon
cycle and then relying on biospheric sequestra-
tion is not without risk, because such sequestra-
tion is reversible from either climate changes, direct
human actions, or a combination of both.
Nonetheless, C sinks in almost all forests
across the world (Fig. 1) may suggest overall fa-
and wood products. Our analysis also suggests
that there are extensive areas of relatively young
forests with potential to continue sequestering
C in the future in the absence of accelerated
natural disturbance, climate variability, and land-
use change. As a result of the large C stocks in
both boreal forest soils and tropical forest bio-
mass, warming in the boreal zone, deforestation,
19 AUGUST 2011VOL 333
on August 18, 2011
and occasional extreme drought, coincident with Download full-text
fires in the tropics, represent the greatest risks
to the continued large C sink in the world’s for-
ests (21, 24, 30, 37). A better understanding of
for projecting future atmospheric CO2growth
and guiding the design and implementation of
Reference and Notes
1. G. J. Nabuurs et al., in Climate Change 2007: Mitigation,
(Cambridge Univ. Press, Cambridge, 2007), pp. 542–584.
2. J. G. Canadell et al., Proc. Natl. Acad. Sci. U.S.A. 104,
3. S. Khatiwala, F. Primeau, T. Hall, Nature 462, 346 (2009).
4. C. Le Quéré et al., Nat. Geosci. 2, 831 (2009).
5. R. K. Dixon et al., Science 263, 185 (1994).
6. Details of data sources, accounting, and estimation
methods used for each country, region, and C component
are provided in the supporting online material.
7. Food and Agriculture Organization, Global Forest
Resources Assessment 2010 (Food and Agriculture
Organization, Rome, 2010), forestry paper 163.
8. A. Z. Shvidenko, D. G. Schepaschenko, S. Nilsson, in
Basic Problems of Transition to Sustainable Forest
Management in Russia, V. A. Sokolov, A. Z. Shvidenko,
O. P. Vtorina, Eds. (Russian Academy of Sciences,
Krasnoyarsk, Russia, 2007), pp. 5–35.
9. P. E. Kauppi et al., For. Ecol. Manage. 259, 1239 (2010).
10. W. A. Kurz, G. Stinson, G. J. Rampley, C. C. Dymond,
E. T. Neilson, Proc. Natl. Acad. Sci. U.S.A. 105, 1551 (2008).
11. G. Stinson et al., Glob. Change Biol. 17, 2227 (2011).
12. R. Birdsey, K. Pregitzer, A. Lucier, J. Environ. Qual. 35,
13. P. E. Kauppi et al., Proc. Natl. Acad. Sci. U.S.A. 103,
14. Y. Pan et al., Biogeosciences 8, 715 (2011).
259, 151 (2009).
16. P. J. van Mantgem et al., Science 323, 521 (2009).
17. D. D. Breshears et al., Proc. Natl. Acad. Sci. U.S.A. 102,
18. P. Ciais et al., Nat. Geosci. 1, 425 (2008).
19. J. Fang, A. Chen, C. Peng, S. Zhao, L. Ci, Science 292,
20. S. L. Lewis et al., Nature 457, 1003 (2009).
21. O. L. Phillips et al., Science 323, 1344 (2009).
22. M. Gloor et al., Glob. Change Biol. 15, 2418 (2009).
23. S. L. Lewis, J. Lloyd, S. Sitch, E. T. A. Mitchard,
W. F. Laurance, Annu. Rev. Ecol. Syst. 40, 529 (2009).
24. R. A. Houghton, Annu. Rev. Earth Planet. Sci. 35, 313 (2007).
25. P. Friedlingstein et al., Nat. Geosci. 3, 811 (2010).
26. C. Tarnocai et al., Global Biogeochem. Cycles 23,
27. A. Hooijer et al., Biogeosciences 7, 1505 (2010).
28. S. E. Page, J. O. Rieley, C. J. Banks, Glob. Change Biol.
17, 798 (2011).
29. Intergovernmental Panel on Climate Change, IPCC
Guidelines for National Greenhouse Gas Inventories
(Institute for Global Environmental Strategies, Japan, 2006);
30. A. D. McGuire et al., Ecol. Monogr. 79, 523 (2009).
31. C. L. Goodale et al., Ecol. Appl. 12, 891 (2002).
32. J. L. Sarmiento et al., Biogeosciences 7, 2351 (2010).
33. E. D. Schulze et al., Nat. Geosci. 2, 842 (2009).
34. S. W. Pacala et al., Science 292, 2316 (2001).
35. O. L. Phillips et al., Philos. Trans. R. Soc. London Ser. B
359, 381 (2004).
36. J. M. Metsaranta, W. A. Kurz, E. T. Neilson, G. Stinson,
Tellus 62B, 719 (2010).
37. M. Zhao, S. W. Running, Science 329, 940 (2010).
38. R. A. Houghton, Tellus 55B, 378 (2003).
Acknowledgments: This study is the major output of two
workshops at Peking Univ. and Princeton Univ. Y.P.,
R.A.B., and J.F. were lead authors and workshop
organizers; Y.P., R.A.B., J.F., R.H., P.E.K., W.A.K., O.L.P.,
A.S., and S.L.L. contributed primary data sets and
analyses; J.G.C., P.C., R.B.J., and S.W.P. contributed
noteworthy ideas to improve the study; A.D.M., S.P.,
A.R., S.S., and D.H. provided results of modeling or
data analysis relevant to the study; and all authors
contributed in writing, discussions, or comments. We
thank K. McCullough for helping to make the map in
Fig. 1 and C. Wayson for helping to develop a
Monte-Carlo analysis. This work was supported in part
by the U.S. Forest Service, NASA (grant 31021001), the
National Basic Research Program of China on Global
Change (2010CB50600), the Gordon and Betty Moore
Foundation, Peking Univ., and Princeton Univ. This work
is a contribution toward the Global Carbon Project’s aim
of fostering an international framework to study the
global carbon cycle.
Supporting Online Material
Materials and Methods
Tables S1 to S6
13 December 2010; accepted 29 June 2011
Published online 14 July 2011;
Detection of Emerging Sunspot
Regions in the Solar Interior
Stathis Ilonidis,* Junwei Zhao, Alexander Kosovichev
Sunspots are regions where strong magnetic fields emerge from the solar interior and where major
eruptive events occur. These energetic events can cause power outages, interrupt telecommunication
and navigation services, and pose hazards to astronauts. We detected subsurface signatures of
emerging sunspot regions before they appeared on the solar disc. Strong acoustic travel-time anomalies
of an order of 12 to 16 seconds were detected as deep as 65,000 kilometers. These anomalies were
associated with magnetic structures that emerged with an average speed of 0.3 to 0.6 kilometer per
second and caused high peaks in the photospheric magnetic flux rate 1 to 2 days after the detection of
the anomalies. Thus, synoptic imaging of subsurface magnetic activity may allow anticipation of large
sunspot regions before they become visible, improving space weather forecast.
riesassume thatsunspotregions aregeneratedby
a dynamo action at the bottom of the convection
to support this idea, and dynamo mechanisms op-
nderstanding solar magnetism is among
ics and astrophysics (1–5). Modern theo-
in the near-surface shear layer have been pro-
posed as well (6, 7). Investigation of emerging
understanding of sunspots and active regions.
Active regions on the Sun produce flares and
mass eruptions that may cause power outages
on Earth, satellite failures, and interruptions of
telecommunication and navigation services. Moni-
toring solar subsurface processes and predict-
ing magnetic activity would also improve space
Time-distance helioseismology (8) is one of
the local helioseismology techniques that image
acoustic perturbations in the interior of the Sun
(9). Acoustic waves are excited by turbulent con-
vection near the surface, propagate deep inside
the Sun, and are refracted back to the surface
(Fig. 1). Time-distance helioseismology measures
travel times of acoustic waves propagating to dif-
ferent distances by computing cross-covariances
between the oscillation signals observed at pairs
of locations on the solar photosphere. Varia-
tions in acoustic travel times are caused mainly
by thermal perturbations, magnetic fields, and
flows. Previous studies of emerging sunspot re-
gions (10–14) have found difficulties in detect-
ing signals deeper than 30 Mm and before the
initial magnetic field becomes visible on the sur-
face because of the fast emergence speed and low
signal-to-noise ratio (15). Here, we present a deep-
focus time-distance measurement scheme, which
allows us to detect signals of emerging magnetic
regions in the deep solar interior (16, 17).
We have used Doppler observations (18) from
Michelson Doppler Imager (MDI) (19) onboard
the Solar and Heliospheric Observatory (SOHO)
and computed travel-time maps of four emerging
flux regions and nine quiet regions. In Fig. 2, we
present the results of our analysis for Active Re-
gion (AR) 10488, which started emerging on the
solar disc at 09:30 UT, 26 October 2003, about
W. W. Hansen Experimental Physics Laboratory, Stanford
University, Stanford, CA 94305–4085, USA
*To whom correspondence should be addressed. E-mail:
VOL 333 19 AUGUST 2011
on August 18, 2011