Roots and Associated Fungi Drive Long-Term Carbon Sequestration in Boreal Forest

Abstract

Boreal forest soils function as a terrestrial net sink in the global carbon cycle. The prevailing dogma has focused on aboveground
plant litter as a principal source of soil organic matter. Using 14C bomb-carbon modeling, we show that 50 to 70% of stored carbon in a chronosequence of boreal forested islands derives from
roots and root-associated microorganisms. Fungal biomarkers indicate impaired degradation and preservation of fungal residues
in late successional forests. Furthermore, 454 pyrosequencing of molecular barcodes, in conjunction with stable isotope analyses,
highlights root-associated fungi as important regulators of ecosystem carbon dynamics. Our results suggest an alternative
mechanism for the accumulation of organic matter in boreal forests during succession in the long-term absence of disturbance.

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DOI: 10.1126/science.1231923
, 1615 (2013);339 Science et al.K. E. Clemmensen
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Roots and Associated Fungi Drive Long-Term Carbon Sequestration
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We have found major changes in a plant-
pollinator network over the past 120 years. This
is partly explained by the nonrandom extirpation
of bee species that are expected to be the most
vulnerable to land-use and climate change, such
as rare and specialized species, species occupying
higher trophic levels, and cavity-nesting species.
We found large changes in phenology of both
forbs and pollinators and the potential for inter-
action mismatches, and these phenological changes
can explain some of the species and interaction
losses observed in this system. Our more opti-
mistic finding was that plant-pollinator interac-
tion networks were quite flexible in the face of
strong phenological change and bee species ex-
tirpations, with many extant species gaining inter-
actions through time. However, the redundancy
in network structure has been reduced, interac-
tion strengths have weakened, and the quan-
tity and quality of pollinator service has declined
through time. Further interaction mismatches
and reductions in population sizes are likely to
have substantial negative consequences for this
crucial ecosystem service.
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Acknowledgments: M.Bujnak,A.David,M.Dust,J.Hopwood,
M. Jean, R. Jean, S. Mulhern, Z. Portman, and J. Wray provided
exceptional help in the field and laboratory. M. Arduser and
J. Gibbs aided in bee identification. Historic data and specimen
access were provided by J. Memmott and P. Tinerella, respectively.
Access to current data is available at http://datadryad.org. We are
grateful to Beaver Dam State Park, Moores Cemetery Woods,
Bethel Ridge Cemetery, Culp Conservancy Woods, E. Swiatkowsk,
and the Parlodi family for field site access. Funding was provided
by NSF DEB 0934376 and NSF 06-520 DRL-0739874. Three
anonymous reviewers provided comments on earlier drafts.
Supplementary Materials
www.sciencemag.org/cgi/content/full/science.1232728/DC1
Materials and Methods
Supplementary Text
Figs. S1 to S10
Tables S1 to S3
References (33–37)
13 November 2012; accepted 6 February 2013
Published online 28 February 2013;
10.1126/science.1232728
Roots and Associated Fungi Drive
Long-Term Carbon Sequestration
in Boreal Forest
K. E. Clemmensen,
1
*A. Bahr,
2
O. Ovaskainen,
3
A. Dahlberg,
1,4
A. Ekblad,
5
H. Wallander,
2
J. Stenlid,
1
R. D. Finlay,
1
D. A. Wardle,
6
B. D. Lindahl
1
Boreal forest soils function as a terrestrial net sink in the global carbon cycle. The prevailing
dogma has focused on aboveground plant litter as a principal source of soil organic matter.
Using
14
C bomb-carbon modeling, we show that 50 to 70% of stored carbon in a chronosequence
of boreal forested islands derives from roots and root-associated microorganisms. Fungal
biomarkers indicate impaired degradation and preservation of fungal residues in late successional
forests. Furthermore, 454 pyrosequencing of molecular barcodes, in conjunction with stable
isotope analyses, highlights root-associated fungi as important regulators of ecosystem carbon
dynamics. Our results suggest an alternative mechanism for the accumulation of organic matter
in boreal forests during succession in the long-term absence of disturbance.
Globally, the boreal forest biome covers
11% of the land surface (1) and con-
tains 16% of the carbon (C) stock se-
questered in soils (2). Aboveground plant litter
quality and decomposition rates have been pro-
posed as the fundamental determinants of long-
term soil organic matter accumulation (3–6).
However, a large proportion of photosynthet-
ically fixed C is directed belowground to roots
and associated microorganisms (7,8), potentially
affecting C sequestration either positively or neg-
atively (9–12). A better mechanistic understanding
of how the belowground allocation of C affects
long-term sequestration rates is crucial for pre-
dictions of how the currently large C stock in
boreal forest soils may respond to altered forest
management practices, climate change, elevated
CO
2
levels, and other environmental shifts.
Here we present evidence from a fire-driven
boreal forest chronosequence that enables the
study of soil C sequestration over time scales of
centuries to millennia. The system consists of for-
ested islands in two adjacent lakes, Lake Hornavan
and Lake Uddjaure (65°55′to 66°09′N; 17°43′
to 17°55′E), in northern Sweden. The islands in
these lakes were formed after the most recent
glaciation and have since been subjected to sim-
ilar extrinsic factors. Larger islands, however, burn
more frequently because they have a larger area
to intercept lightning strikes (6,13); several large
islands have burned in the past century, whereas
some small islands have not burned in the past
5000 years. It has previously been shown that as
the time since fire increases, soil and total eco-
system C accumulates unabated and linearly
(6,14), leading to humus layers that can exceed
1 m in depth on the smallest islands. This has
been attributed to a decline in the quality of
aboveground litter inputs and impaired litter de-
composition as the chronosequence proceeds
(6,14,15). We studied organic soil profiles on
30 islands representing three size classes with
increasing belowground C stocks (14): 10 large
islands (>1.0 ha; on average, 6.2 kg of C m
−2
accumulated belowground; mean time since fire
585 years), 10 medium islands (0.1 to 1.0 ha,
11.2 kg of C m
−2
, 2180 years), and 10 small
islands (<0.1 ha, 22.5 kg of C m
−2
, 3250 years).
1
Department of Forest Mycology and Plant Pathology, Uppsala
BioCenter, Swedish University of Agricultural Sciences, Box
7026, SE-75007 Uppsala, Sweden.
2
Department of Biology,
Microbial Ecology Group, Lund University, Box 117, SE-221
00 Lund, Sweden.
3
Department of Biosciences, University of
Helsinki, Box 65, FI-00014 University of Helsinki, Finland.
4
Swedish Species Information Centre, Swedish University of
Agricultural Sciences, Box 7007, SE-750 07 Uppsala, Sweden
5
School of Science and Technology, Örebro University, SE-701
82 Örebro, Sweden.
6
Department of Forest Ecology and Man-
agement, Swedish University of Agricultural Sciences, SE-901
83 Umeå, Sweden.
*Corresponding author. E-mail: karina.clemmensen@slu.se
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We explored C dynamics across the chrono-
sequence by analyzing bomb
14
C(16) to deter-
mine the age since fixation of soil C, and then
fitted a mathematical model to measurements
of C mass and age distribution across vertical
organic matter profiles for six representative is-
lands; three large and three small (Fig. 1) (17).
The model assumes two sources of C inputs: (i)
a series of consecutively deposited cohorts of
aboveground plant litter with negligible vertical
mixing, and (ii) belowground inputs through
root transport and rhizosphere processes. The
dynamics of both C sources were estimated by a
Bayesian parameterization of the model. The
observed distribution of C mass and age was
adequately predicted only when root C import
was accounted for (Table 1 and figs. S1 and S2).
The parameterized model estimates that the
proportion of root-derived C accumulated over
the past 100 years is larger on small islands (70%)
than on large islands (47%), and the larger total
C sequestration on small islands during this
period can be explained entirely by root-derived
inputs (Fig. 1). Differences in organic matter ac-
cumulation between islands were primarily deter-
mined by processes at the interface between the
fragmented litter (F) and humus (H) layers, which
corresponded to the zone of highest root density
(Fig. 2B) and where the aboveground litter was
10 to 60 years old. The model was run for 100 years,
covering almost the entire humus profile of the
large islands, but on small islands a major propor-
tion of C is stored in deeper horizons that are
older than this. However, the model indicates that
below 20 cm depth, root-derived C inputs are low
and the C remaining from the horizons above
decomposes slowly, as is also supported by
14
C
depletion in the deeper layers of small islands
(Table 1). Thus, root-mediated C input to the up-
per part of the profile represents a major contribu-
tion to the long-term buildup of humus, especially
in late successional ecosystems.
Fungi play central roles in boreal forest eco-
systems, both as decomposers of organic matter
and as root-associated mediators of belowground
C transport and respiration. We profiled the rel-
ative abundance of major functional groups of
fungi through the depth profile of each island
by DNA barcoding based on 454 pyro sequencing
of the ITS2 region of ribosomal RNA genes
(17,18). These analyses suggest that fungal
communities in the uppermost litter layers were
dominated by free-living saprotrophs, whereas
mycorrhizal and other root-associated fungi dom-
inated at greater depth (Fig. 2A). Thus, root-
associated fungi dominate the part of the soil
profile where the model indicates the largest dif-
ference in C sequestration between the island
size classes. At this depth, free-living saprotrophs
(mainly molds and yeasts) make a much reduced
contribution, suggesting a correspondingly greater
role of root-associated fungi in the regulation of
organic matter dynamics.
The increase in root-derived C sequestration
as the chronosequence proceeds is matched by a
shift in the balance between the production and
decomposition of fungal mycelium in the F-H
transition zone of the soil profile. We measured
the fungal-specific cell membrane lipid ergosterol
as a marker for fungal biomass throughout each
soil profile. Even though standing fungal bio-
mass, as indicated by total (free plus bound) er-
gosterol (Fig. 3, A and B) and ITS copy numbers
(table S1), was roughly similar on all islands, free
ergosterol (characteristic of newly formed myce-
lia) (19–21) was about 20 times more abundant
on large than on small islands, indicating a larger
proportion of freshly produced mycelium and
thus greater mycelial production. In contrast,
bound ergosterol (the proportion of which in-
creases during mycelial senescence) (19,20)
was more abundant on smaller islands, indicat-
ing older mycelium with slower biomass turnover.
Furthermore, the fungal cell-wall polysaccharide
chitin (Fig. 3C) peaked in the F layer and declined
in lower horizons of large islands, but remained
at high concentrations at greater depths on the
small islands. Chitin persists longer than ergos-
terol in fungal tissues after death (21), and the
high level of chitin on small islands suggests re-
tarded decomposition of fungal cell wall resi-
dues. Thus, in spite of supposedly greater mycelial
production on the large islands, less mycelial
necromass accumulated there than on small is-
lands, suggesting that the large production was
counterbalanced by faster decomposition of my-
celial remains. Correspondingly, the
14
C model
indicated faster decomposition of root-derived C
on large islands, despite inputs being conserva-
tively constrained to be equal across all islands.
Taken together, our results point to impaired
Fig. 1. Carbon dynamics in vertically stratified organic horizons of forested islands. Model estimates of
C from aboveground litter (solid lines) and C introduced belowground via root transport (broken lines)
are shown. C mass was modeled to a horizon age of 100 years, based on C mass and
14
Cmeasurements
in profiles from three large (A)andthreesmall(B) islands. Dotted lines show the 95% central
credibility intervals around posterior means. The posterior probability that the root-derived fraction is
larger on small islands than on large islands is 0.97. Approximate depths are indicated for transitions
between the main categories of horizons sampled; L, litter; F, fragmented litter; H, humus.
Table 1. C mass,
14
C abundance, and estimated C mean age of sampled organic layers on large
and small islands. Means TSE, n=3(n= 2 for the deepest layer in both size classes; both values
are given).
Layer
Large islands Small islands
C mass
(g m
−2
)
∆
14
C
(‰)
C age
(years)
C mass
(g m
−2
)
∆
14
C
(‰)
C age
(years)
Litter, on surface 103 T370T37T095T762T16T0
Litter, 0 to 2 cm 185 T17 81 T17 9 T3 180 T11 84 T11 9 T2
Fragmented litter,
2to7cm
454 T91 118 T12 15 T2 539 T63 101 T14 12 T2
Fragmented litter,
7to10cm
493 T76 165 T19 20–39* 494 T77 136 T718T1
Humus, 10 to 16 cm 1170 T90 150 T31 42–51* 1150 T165 191 T14 23–33*
Humus, 16 to 20 cm 1620 T230 21 T16 53 T1 910 T105 195 T17 34–50*
Humus, 20 to 40 cm 3410, 1846 9.4, -14.3 53, 57 6440 T815 14 T15 59 T7
Humus, 40 to 60 cm 7660 T700 –99 T14 780 T120
Humus, 60 to 80 cm 7380 T1760 –194 T9 1670 T90
Humus, 80 to 100 cm 5620, 3650 –285, –267 2628, 2432
*The mean age is within the given interval in samples that include the 1960s peak in bomb
14
C.
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decomposition of fungal residues as an impor-
tant regulator of C accumulation as the chrono-
sequence proceeds.
The often observed increases in
13
Cand
15
N
abundances with soil depth have been inter-
preted as evidence of increasing contributions
of enriched microbial components to residual
soil organic matter (22–24). In our system, where
the dominant plant species form ecto- or ericoid
mycorrhizal associations, the d
13
Candd
15
Nsig-
natures in the uppermost organic layers were sim-
ilar to those of leaves (25), whereas signatures in
humus layers were closer to those of rhizosphere
mycelium (Fig. 3, D and E, and table S1) and
mycorrhizal fungal sporocarps (26). Plant C al-
located belowground is relatively enriched in
13
C, and this enrichment is further accentuated
during C transfer to mycorrhizal fungi (27).
However, historic changes in atmospheric d
13
C
(28) may also contribute to the depth gradient
(22,24). Mycorrhizal fungi also have higher d
15
N
signatures than their host plants, because they
supply N to their hosts that is
15
N-depleted rela-
tive to that retained in their own mycelium (29).
Thus, the incorporation of isotopically enriched
root and fungal remains is likely to be an im-
portant mechanism behind the increasing stable
isotope signatures with soil depth in this system.
This is consistent with the observation that iso-
topic signatures remain relatively constant in the
initial litter decomposition phase and only increase
when root-associated fungi dominate C and N
dynamics (Figs. 2 and 3) (30,31).
Previous studies in this (6,14) and other
(3,4) systems have pointed to the input and
quality of aboveground litter as important reg-
ulators of C and N sequestration during long-
term ecosystem development and succession.
Our results show that aboveground plant litter
dynamics on its own cannot explain the increas-
ing rate of organic matter accumulation with
time since wildfire, and that the dynamics of
roots and associated fungi is an important addi-
tional factor explaining C accumulation in boreal
forests. Although we observe less C accumulation
on large islands, it is reasonable to assume that
C allocation to roots and associated mycelium is
greatest on those islands, especially given their
higher root densities (Fig. 2B), free ergosterol
levels (Fig. 3A), and net primary productivity
(6). This apparent contradiction corroborates re-
cent results (32,33) showing that increased C
input to roots in response to CO
2
enrichment
accelerates the turnover of soil organic matter,
counteracting C accumulation and enhancing
N cycling through the microbial pools. In our
system, a similar stimulation of N recycling by
large C inputs is supported by the steeper
15
N
gradient (31) and higher C:N-ratio in the humus
of large islands (Fig. 3, E and F) (30). In contrast,
the less steep
15
N gradient and lower C:N-ratio
on smaller islands suggest impaired mycorrhizal
N mobilization (31) and accumulation of N in
biochemically stabilized fungal remains, consist-
ent with the high levels of bound ergosterol and
Fig. 2. Depth profiles of the relative abundance of fungal functional groups (percent of amplified ITS
sequences) (A) and root (1 to 5 mm in diameter) density (B) on large and small forested islands. The
profile corresponds to the organic layers L, F, and H. Functional groups comprise identified species
with known function (unshaded) and species putatively assigned to a function (shaded) (17). The data
set contains 650,000 sequence reads, and the globally most abundant 583 clusters are analyzed,
covering 82 to 95% of the reads in individual sample types. The total ITS copy number was not
affected by island size but decreased with depth (with 3 × 10
9
,4×10
8
,and2×10
7
copies g
−1
of
organic matter in L, F, and H layers, respectively) (table S1). The abundances of different functional
groups should be compared with caution because of possible differences in ITS copy numbers per unit
of biomass. All values are based on means of n=10 islands (except that n= 2, 5, and 7 for the lowest
horizons) (17).
Fig. 3. Depth profiles of fungal biochemical markers (Ato C), d
13
C(D), d
15
N(E), and the C/N ratio
(F) in organic soil profiles of large (solid lines) and small (broken lines) forested islands. All data
are means TSE, n=10 (except that n= 3 for glucosamine and n= 2, 5, and 7 for the lowest
horizons) (17). Medium-sized islands are not shown but are included in the statistical analyses
presented in table S1. In the lower panel, levels measured in roots (R) 1 to 5 mm in diameter and
mycorrhizal mycelium (M) sampled at 10 cm depth are given for reference.
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chitin on those islands. The consequential reduced
N availability to plants leads to progressive nu-
trient limitation and compositional changes in the
vegetation with increasing time since a major dis-
turbance (14,34). Changes in plant productivity
and community composition may, in turn, influ-
ence total belowground C allocation and distribu-
tion to fungal associates. Together, these feedbacks
result in continuing C and N accumulation in the
humus layer and decreasing plant production, and
this process is only reset by major disturbances,
such as wildfire.
Our results elucidate the mechanisms under-
pinning C sequestration in boreal forests and
highlight the importance of root-associated fungi
for ecosystem C balance and, ultimately, the
global C cycle. We challenge the previous dogma
that humus accumulation is regulated primarily
by saprotrophic decomposition of aboveground
litter, and envisage an alternative process in which
organic layers grow from below through the con-
tinuous addition of recently fixed C to the organic
matter profile in the form of remains from roots
and associated mycelium. Environmental changes,
such as N fertilization and deposition, forest man-
agement, and elevated atmospheric CO
2
concen-
trations, are therefore likely to greatly affect soil
C sequestration through their alteration of rhizo-
sphere processes. These processes are not well
described in current models of ecosystem and
global C dynamics, and their more explicit in-
clusion is likely to improve both the mechanistic
realism and future predictive power of models.
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Acknowledgments: The molecular data are archived at the
Sequence Read Archive under accession number SRP016090
(www.ncbi.nlm.nih.gov/sra). This research was supported by the
7th European Community Framework Program (a Marie Curie
Intra-European Fellowship to K.E.C.), Lammska Stiftelsen, the
research center LUCCI at Lund University, FORMAS grants
(2007-1365 and 2011-1747 to B.D.L.), a Wallenberg Scholar
award to D.A.W., the European Research Council (grant
205905 to O.O.), and KoN grants to R.D.F. and J.S. by the
Swedish University of Agricultural Sciences. We gratefully
acknowledge M. Brandström-Durling for development of the
SCATA bioinformatics pipeline, T. Näsholm for help with the
chitin analyses, G. Nyakatura at LGC Genomics for assistance
with sequencing, and G. Possnert at the Tandem Laboratory for
help with
14
C dating.
Supplementary Materials
www.sciencemag.org/cgi/content/full/339/6127/1615/DC1
Materials and Methods
Figs. S1 to S3
Table S1
Model Code S1
References (35–48)
23 October 2012; accepted 1 February 2013
10.1126/science.1231923
The Biological Underpinnings
of Namib Desert Fairy Circles
Norbert Juergens
The sand termite Psammotermes allocerus generates local ecosystems, so-called fairy circles,
through removal of short-lived vegetation that appears after rain, leaving circular barren patches.
Because of rapid percolation and lack of evapotranspiration, water is retained within the circles.
This process results in the formation of rings of perennial vegetation that facilitate termite survival
and locally increase biodiversity. This termite-generated ecosystem persists through prolonged droughts
lasting many decades.
Fairy circles (FCs) are large, conspicuous,
circular patches devoid of vegetation in
the center but with perennial grasses at the
margin. These patches occur in large numbers in
the desert margin grasslands of southern Africa
(Fig. 1, A and B). Early observers considered
poisonous plants, ants, or termites as causal fac-
tors; however, most of these early hypotheses
were systematically tested and rejected (1,2).
Ithasalsobeenproposedthatanunknownsemi-
volatile substance in the soil might be respon-
sible for the absence of grass within the FCs
(2,3). In fact, a wide range of volatile organic
compounds are found in FCs (4). Measurements
of carbon monoxide and hydrocarbons in the
soil led to the proposal of a geochemical ori-
gin of FCs (5). Carnivorous ants (6) and “self-
organizing vegetation dynamics”(7) have also
been considered as causes for FCs. Despite the
many hypotheses, the origin and the ecosystem
function of FCs are still a much-debated mys-
tery. I used a long-term data set describing the
environmental and biogeographical characteris-
tics and dynamics of FCs to identify the most
likely cause of these unique formations. Addition-
ally, I analyze the function of FCs in terms of
water management, biodiversity, and adaptation
to arid conditions.
FCs occur along a narrow belt at the eastern
margin of the Namib Desert, running from mid-
Angola to northwestern South Africa. The area
of distribution is closely associated with the
isohyet of 100-mm mean annual precipitation
(MAP) (Fig. 1B). The disjunct occurrence of FCs
is caused by their pronounced restriction to
sandy soils.
High soil humidity within FCs has been ob-
served previously (1,2). To confirm and quanti-
fy this potentially adaptive function, I measured
volumetric soil water content (m
3
/m
3
× 100) from
2006 to 2012 within and around FCs. At sites
with a MAP of 100 mm, more than 53 mm of
water were stored in the upper 100 cm of soil,
even during the driest time of the year (table S1).
At a depth >40 cm, a soil humidity of more than
5% volumetric water content was recorded over
4years.
Higher temporal resolution of water flux was
gained by automatic measurements recorded
every hour within the bare patch and the grass
matrix at 10-, 30-, 60-, and 90-cm depths using
FDR sensors. During the observation period of
4 years, the humidity at 60-cm depth within the
FC was either at or well above 5% volumetric
water content (Fig. 2A). In the typical sand tex-
ture of FC soils with dominant grain sizes around
Biocenter Klein Flottbek, University of Hamburg, Ohnhorststrasse
18, 22609 Hamburg, Germany. E-mail: norbert.juergens@
t-online.de
29 MARCH 2013 VOL 339 SCIENCE www.sciencemag.org1618
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