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


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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
in Boreal Forest
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.
References and Notes
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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 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
Materials and Methods
Supplementary Text
Figs. S1 to S10
Tables S1 to S3
References (3337)
13 November 2012; accepted 6 February 2013
Published online 28 February 2013;
Roots and Associated Fungi Drive
Long-Term Carbon Sequestration
in Boreal Forest
K. E. Clemmensen,
*A. Bahr,
O. Ovaskainen,
A. Dahlberg,
A. Ekblad,
H. Wallander,
J. Stenlid,
R. D. Finlay,
D. A. Wardle,
B. D. Lindahl
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.
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 (36).
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 (912). 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
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°55to 66°09N; 17°43
to 17°55E), 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
accumulated belowground; mean time since fire
585 years), 10 medium islands (0.1 to 1.0 ha,
11.2 kg of C m
, 2180 years), and 10 small
islands (<0.1 ha, 22.5 kg of C m
, 3250 years).
Department of Forest Mycology and Plant Pathology, Uppsala
BioCenter, Swedish University of Agricultural Sciences, Box
7026, SE-75007 Uppsala, Sweden.
Department of Biology,
Microbial Ecology Group, Lund University, Box 117, SE-221
00 Lund, Sweden.
Department of Biosciences, University of
Helsinki, Box 65, FI-00014 University of Helsinki, Finland.
Swedish Species Information Centre, Swedish University of
Agricultural Sciences, Box 7007, SE-750 07 Uppsala, Sweden
School of Science and Technology, Örebro University, SE-701
82 Örebro, Sweden.
Department of Forest Ecology and Man-
agement, Swedish University of Agricultural Sciences, SE-901
83 Umeå, Sweden.
*Corresponding author. E-mail: SCIENCE VOL 339 29 MARCH 2013 1615
on March 30, 2013www.sciencemag.orgDownloaded from
We explored C dynamics across the chrono-
sequence by analyzing bomb
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
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) (1921) 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
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
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,
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).
Large islands Small islands
C mass
(g m
C age
C mass
(g m
C age
Litter, on surface 103 T370T37T095T762T16T0
Litter, 0 to 2 cm 185 T17 81 T17 9 T3 180 T11 84 T11 9 T2
Fragmented litter,
454 T91 118 T12 15 T2 539 T63 101 T14 12 T2
Fragmented litter,
493 T76 165 T19 2039* 494 T77 136 T718T1
Humus, 10 to 16 cm 1170 T90 150 T31 4251* 1150 T165 191 T14 2333*
Humus, 16 to 20 cm 1620 T230 21 T16 53 T1 910 T105 195 T17 3450*
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
29 MARCH 2013 VOL 339 SCIENCE www.sciencemag.org1616
on March 30, 2013www.sciencemag.orgDownloaded from
decomposition of fungal residues as an impor-
tant regulator of C accumulation as the chrono-
sequence proceeds.
The often observed increases in
abundances with soil depth have been inter-
preted as evidence of increasing contributions
of enriched microbial components to residual
soil organic matter (2224). In our system, where
the dominant plant species form ecto- or ericoid
mycorrhizal associations, the d
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
C, and this enrichment is further accentuated
during C transfer to mycorrhizal fungi (27).
However, historic changes in atmospheric d
(28) may also contribute to the depth gradient
(22,24). Mycorrhizal fungi also have higher d
signatures than their host plants, because they
supply N to their hosts that is
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
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
gradient (31) and higher C:N-ratio in the humus
of large islands (Fig. 3, E and F) (30). In contrast,
the less steep
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
copies g
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
C(D), d
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. SCIENCE VOL 339 29 MARCH 2013 1617
on March 30, 2013www.sciencemag.orgDownloaded from
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
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
( 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
C dating.
Supplementary Materials
Materials and Methods
Figs. S1 to S3
Table S1
Model Code S1
References (3548)
23 October 2012; accepted 1 February 2013
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).
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
× 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
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@
29 MARCH 2013 VOL 339 SCIENCE www.sciencemag.org1618
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... Recent research [4], investigating the transfer of carbon between trees in a fixed area, under the effect of a specific microclimate, highlights the role of the rhizosphere in nutrient dynamics. Mycorrhizal networks play the role of mediators of interactions between trees and plants surrounding the understory [7][8][9]. ...
... As in forest ecosystems, it is common to have processes occurring on different time scales [7,14], in the modeling developed with TA different scales are combined. While the parameter t indicates the real-time scale, the parameters s and p -introduced ahead denote other time scales, in which forest dynamics phenomena studied here have patterns that preserve quantities of interest, obeying the principle of conservation of the energy in the allometric space. ...
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Models based on analytical trophodynamics (AT) method have provided an analytical framework for modeling in ecology, including the dynamical flux of nutrients present in the soil for a fixed region. Dynamics occurring concurrently in different time scales are modeled. Through a mathematical treatment of the elements of both biotic and abiotic factors, is established  stability and conservation laws for growing trajectories, whose solutions of the second-order differential systems equations known as Volterra–Hamilton systems. All solutions trajectories obtained to follow the biological principles of energy conservation. The tensors of AT were computed with the computational algebraic package FINSLER. Moreover, in this chapter, we present an overview of the last results and actual status of research in this area.
... The soil environment is one of the largest pools of carbon in terrestrial ecosystems. Mycorrhizal fungi and plant roots, especially the most distal fine roots, play a crucial role in underground carbon turnover [7]. The highest amounts of carbon produced by photosynthesis are transported directly to these roots [8]. ...
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Fine roots are a key component of carbon turnover in the terrestrial environment. Therefore, their distribution allows for the estimation of areas of carbon in the soil. The vertical distribution of roots is the result of both the tree species and various environmental factors. Research on the architecture of root systems most often includes seedlings and young trees growing under experimental conditions; however, little is known about trees in their natural habitats. The aim of this study is to analyze the fine root distribution of mature white poplar trees in natural riverside temperate zone forests of Central Europe (Poland) periodically flooded and in dry hydrological conditions. The length, diameter, and area of the fine roots, as well as the specific root length (SRL) and specific root area (SRA) of white poplar were measured in three layers of the soil, 0–10 cm, 10–20 cm, and 20–30 cm depths, in three forest sites. Two of the sites experience periodic floods, and one has been without flooding for 80 years, due to the construction of a flood embankment. The highest values of the lengths and surface areas of the poplar fine roots were observed at a depth of 0–10 cm at all sites. Soil moisture was positively correlated with the analyzed root parameters. The presence of understory plant roots contributed to the reduction in the fine root length of poplar in the subsurface layer, compared to the site that was not affected by the presence of plants other than poplar. The distribution of fine roots, the most dynamic part of the plant root system, reflects the most active areas in the soil profile. The presented research will allow for a better understanding of the functioning of natural riverside ecosystems, as well as show the great adaptability of white poplar fine roots to various conditions in the soil.
... Forest ecosystems harbour a large diversity of soil fungi that regulate plant community dynamics (Averill et al. 2014;Molina and Horton 2015) and biogeochemical processes (van der Heijden 2008; Clemmensen et al. 2013). Fungi drive many classical ecological phenomena in forests, e.g., conspecific density dependence (Janzen 1970;Connell 1971;Chen et al. 2019) as well as the observed relationships between soil fertility and plant community structure (Mao et al. 2019). ...
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Background Rhizosphere fungi play an important role in plant community dynamics and biogeochemical cycling. While the drivers of fungal community assembly have been studied in varied ecosystems, it is still unclear how these processes function for rhizosphere soil fungi in temperate forests. Furthermore, it is unknown whether the relative contributions of important determinants remain consistent or vary across fungal ecological guilds. This study used high-throughput next-generation sequencing to characterize the fungal communities of 247 rhizosphere soil samples from 19 tree species in a temperate forest within Northeast China. We aimed to investigate how three important determinants in temperate forests (host tree species, neighbouring plant communities, and edaphic properties) influence the community assembly of fungal functional guilds in the rhizosphere soil of trees. Results We found that host tree species contributed more to plant pathogens’ community composition than ectomycorrhizal fungi, and plant pathogens consistently showed higher host specialization than ectomycorrhizal fungi. Saprotrophs also showed high host specialization, which was mediated by the tree species’ effect on rhizosphere soil pH. Although neighboring plant communities contributed remarkably to richness of all fungal guilds, this effect on fungal composition varied across functional guilds, with stronger effect for biotrophic guilds (plant pathogens and ectomycorrhizal fungi) than for non-biotrophic guild (saprotrophs). Neighboring plant communities shaped the ectomycorrhizal community composition strongly in all samples regardless of host trees’ mycorrhizal type, whereas edaphic properties were the most important drivers for this guild in samples from only ectomycorrhizal-associated trees. Edaphic properties played an important role in shaping ectomycorrhizal and saprotrophic fungal compositions, indicating the importance of edaphic properties on the fungal functional guilds associated with the absorption and decomposition of nutrients. Conclusions These results demonstrated that rhizosphere soil fungal community assembly determinants varied across fungal guilds, reflecting their different ecological functions in temperate forest ecosystems.
... Although increased mean temperature and temperature fluctuation had dissimilar effects on specific taxa in the fungal community ( Supplementary Fig. 3c,d), the results indicated that both of these variables could have a positive effect on R mass by promoting shifts in fungal composition and synchronously increasing enzyme activities (Fig. 4). Fungi are considered the major decomposers in forest ecosystems, and substrate preferences vary among fungal taxa, meaning that changes in structure-function relationships in fungal communities are probably prerequisites for the optimization of soil substrate utilization 41 . We demonstrated that shifts in the fungal community induced positive feedback in various patterns of temperature-related changes in enzyme activities, thus resulting in continuous soil carbon loss. ...
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The magnitude of the feedback between soil microbial respiration and increased mean temperature may decrease (a process called thermal adaptation) or increase over time, and accurately representing this feedback in models improves predictions of soil carbon loss rates. However, climate change entails changes not only in mean temperature but also in temperature fluctuation, and how this fluctuation regulates the thermal response of microbial respiration has never been systematically evaluated. By analysing subtropical forest soils from a 2,000 km transect across China, we showed that although a positive relationship between soil microbial biomass-specific respiration and temperature was observed under increased constant incubation temperature, an increasing temperature fluctuation had a stronger negative effect. Our results further indicated that changes in bacterial community composition and reduced activities of carbon degradation enzymes promoted the effect of temperature fluctuation. This adaptive response of soil microbial respiration suggests that climate warming may have a lesser exacerbating effect on atmospheric CO2 concentrations than predicted.
... In some cases, the dangers facing beneficial fungi mirror those for other species, and the same conservation strategies could benefit fungi (Minter 2011). For example, Clemmensen et al. (2013) found that habitat fragmentation, a common threat to biodiversity, is also a concern for mycorrhizal fungi and conservation mycology. Thus, conservation programs targeting the mitigation of fragmentation could benefit both charismatic taxa and lesser known taxa like mycorrhizal fungi. ...
During the United Nation's Decade on Ecosystem Restoration, planting material shortages are constraining restoration, while climate change exacerbates the need for restoration and reduces recruitment. Concurrently, research shows that native mycorrhizal fungi (symbiotic with plant roots) appropriate to plant provenance and site conditions significantly accelerate restoration, support crucial ecosystem services, and provide natural climate solutions (sequestering carbon), and nature‐based solutions for climate change (climate adaptation). We reviewed 130 management plans for natural areas in the United States to evaluate whether restoring native mycorrhizal communities has translated into implementation. While management plans frequently discussed the ecosystem services mycorrhizal fungi provide, nearly one half (46%) viewed fungi solely as pathogens or ignored them altogether. Only 8% of plans mentioned mycorrhizal fungi. Only one plan mentioned that mycorrhizae were potentially helpful to natural regeneration, while one other mentioned utilizing soil as a restoration tool. Our examination of publicly available data and case studies suggests that relatively meager protections for fungi, limited research funding and resulting data, research difficulty, and limited access to mycology experts and training contribute to this gap between science and implementation. A database of literature showcasing mycorrhizal ecosystem services and benefits is provided to highlight when and why mycorrhizae should be considered in management, regeneration, and restoration. Three action items are recommended to safeguard native mycorrhizal fungal communities and accelerate restoration and regeneration. Ten implementation tips based in scientific literature are provided to clarify the need and methods for mycorrhizal restoration. This article is protected by copyright. All rights reserved.
... Soils are also an important component of terrestrial carbon sinks. For example, 50-70% of the carbon in boreal forests is stored in the soils, particularly in roots and root-associated fungi (Clemmensen et al., 2013). Furthermore, some regions, such as tropical forests and peatlands (e.g., Baccini et al., 2017) are vulnerable to becoming large CO 2 emitters when there is a change in their structure and resulting function (e.g., due to land-use change). ...
... Recently, the decomposition mechanisms regulated by soil microorganisms during plant residue transformation have attracted considerable attention [1][2][3][4]. Plant residue inputs are the primary driver of soil microbial maintenance activity [5,6], significantly affecting organic matter turnover in the topsoil [7,8]. As regulators of global biogeochemical cycles [9], soil microorganisms participate in core ecosystem processes through ex vivo modifications (extracellular enzymes attack and transform plant residues) or in vivo turnovers (cell uptake-biosynthesis-growth-death), such as soil organic matter decomposition, turnover, and sequestration [10]. ...
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Extracellular enzymes are the major mediators of plant residue and organic matter decomposition in soil, frequently associated with microbial metabolic processes and the biochemical cycling of nutrients in soil ecosystems. However, the dynamic trends and driving factors of extracellular enzymes and their stoichiometry during plant residue transformation remain to be further studied. Here, we investigated the dynamics of extracellular enzymes and enzymatic stoichiometry in the “litter-soil” transformation interface soil (TIS) layer, an essential occurrence layer for microbially-mediated C transformation. The results indicated an unbalanced relationship between substrate resource supply and microbial metabolic demand. Microbial metabolism was limited by C (C/N-acquiring enzymes > 1) and P (N/P-acquiring enzymes < 1) throughout the observed stages of plant residue transformation. The initially higher extracellular enzyme activity reflected the availability of the active components (dissolved carbon (DC), nitrogen (DN), microbial biomass carbon (MBC), nitrogen (MBN), and phosphorus (MBP)) in the substrate and the higher intensity of microbial metabolism. With the transformation of plant residues, the active fraction ceased to be the predominant microbial C source, forcing the secretion of C-acquiring enzymes and N-acquiring enzymes to obtain C sources and N nutrients from refractory substrates. Moreover, C/N-acquiring enzymes decreased, while C/P-acquiring enzymes and N/P-acquiring enzymes subsequently increased, which suggested that the microbial demand for N gradually increased and for P relatively decreased. Soil microorganisms can be forced into dormancy or intracellular mineralization due to the lack of substrate resources, so microbial biomass and extracellular enzyme activities decreased significantly compared to initial values. In summary, the results indicated that soil nutrients indirectly contribute to extracellular enzymes and their stoichiometry by affecting microbial activities. Furthermore, extracellular enzymes and their stoichiometry were more sensitive to the response of soil microbial biomass carbon.
... On a broader perspective, anthropogenic global nitrogen dynamics are spatially variable [42] but may affect global fungal vegetative and reproductive biomass, with potential effects on hyphal-driven ecosystem processes [43,44], and mushroom-driven food webs [45]. Thus, the issue of how additional nitrogen sources or nitrogen pollution of oligotrophic forest ecosystems will affect the growth of different fungi and species composition should be assessed, e.g., by assays with multiple species in one experimental setup. ...
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The Black Poplar Mushroom Cyclocybe aegerita (syn. Agrocybe aegerita) is a white-rot fungus that naturally fruits from woody substrates, including buried wood. It is known for its substrate versatility and is equipped with a respective carbohydrate-active enzyme repertoire being intermediate between typical white-rot fungi and plant litter decomposers. Given relative nitrogen scarcity in wood, mobilization of nitrogen from surrounding litter is known as a way to meet nitrogen requirements for cellular homeostasis and reproduction of wood decay fungi. However, the effect of added nitrogen on vegetative and reproductive biomass has not yet been studied in a uniform min-imalistic laboratory setup. For C. aegerita, such a growth and fruiting setup has been developed. In the present study, this white-rot fungus has been grown with and without additional β-adenosine, an organic nitrogen source present in plant litter. Elevated β-adenosine levels increased aerial my-celium weight by 30% (1 × β-adenosine) and 55% (10 × β-adenosine), reproductive biomass by 75% (1 × β-adenosine) and by 100% (10 × β-adenosine), number of primordia by 127% (10 × β-adenosine) and accelerated primordium formation by 1.6 days (10 × β-adenosine), compared to the control treatment. These findings imply that C. aegerita invests additional organic nitrogen resources into direct vegetative and reproductive biomass build-up at the same time. Colonization of niches with accessory nitrogen sources, like buried wood, which is near the plant litter layer, may thus provide an evolutionary fitness advantage. Globally anthropogenically altered nitrogen dynamics may affect hyphal-driven processes as well as fruit body-driven food webs.
Forests are critical ecosystems to understand the global carbon budget, due to their carbon sequestration potential in both above‐ and belowground compartments, especially in species‐rich forests. Soil carbon sequestration is strongly linked to soil microbial communities, and this link is mediated by the tree community, likely due to modifications of micro‐environmental conditions (i.e., biotic conditions, soil properties, and microclimate). We studied soil carbon concentration and the soil microbial biomass of 180 local neighborhoods along a gradient of tree species richness ranging from 1 to 16 tree species per plot in a Chinese subtropical forest experiment (BEF‐China). Tree productivity and different tree functional traits were measured at the neighborhood level. We tested the effects of tree productivity, functional trait identity and dissimilarity on soil carbon concentrations, and their mediation by the soil microbial biomass and micro‐environmental conditions. Our analyses showed a strong positive correlation between soil microbial biomass and soil carbon concentrations. Besides, soil carbon concentration increased with tree productivity and tree root diameter while it decreased with litterfall C:N content. Moreover, tree productivity and tree functional traits (e.g. root fungal association and litterfall C:N ratio) modulated micro‐environmental conditions with substantial consequences for soil microbial biomass. We also showed that soil history and topography should be considered in future experiments and tree plantations, as soil carbon concentrations were higher where historical (i.e., at the beginning of the experiment) carbon concentrations were high, themselves being strongly affected by the topography. Altogether, these results imply that the quantification of the different soil carbon pools is critical for understanding microbial community–soil carbon stock relationships and their dependence on tree diversity and micro‐environmental conditions. This article is protected by copyright. All rights reserved.
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Plant litter stocks are critical, regionally for their role in fueling fire regimes and controlling soil fertility, and globally through their feedback to atmospheric CO2 and climate. Here we employ two global databases linking plant functional types to decomposition rates of wood and leaf litter (Cornwell et al., 2008; Weedon et al., 2009) to improve future projections of climate and carbon cycle using an intermediate complexity Earth System model. Implementing separate wood and leaf litter decomposabilities and their temperature sensitivities for a range of plant functional types yielded a more realistic distribution of litter stocks in all present biomes with the exception of boreal forests and projects a strong increase in global litter stocks by 35 Gt C and a concomitant small decrease in atmospheric CO2 by 3 ppm by the end of this century. Despite a relatively strong increase in litter stocks, the modified parameterization results in less elevated wildfire emissions because of a litter redistribution towards more humid regions.
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Here, species composition and biomass production of actively growing ecto-mycorrhizal (EM) mycelia were studied over the rotation period of managed Norway spruce (Picea abies) stands in southwestern Sweden. • The EM mycelia were collected using ingrowth mesh bags incubated in the forest soil during one growing season. Fungal biomass was estimated by ergosterol analysis and the EM species were identified by 454 sequencing of internal transcribed spacer (ITS) amplicons. Nutrient availability and the fungal biomass in soil samples were also estimated. • Biomass production peaked in young stands (10–30 yr old) before the first thinning phase. Tylospora fibrillosa dominated the EM community, especially in these young stands, where it constituted 80% of the EM amplicons derived from the mesh bags. Species richness increased in older stands. • The establishment of EM mycelial networks in young Norway spruce stands requires large amounts of carbon, while much less is needed to sustain the EM community in older stands. The variation in EM biomass production over the rotation period has implications for carbon sequestration rates in forest soils.
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Radiocarbon data from soil organic matter and soil respiration provide powerful constraints for determining carbon dynamics and thereby the magnitude and timing of soil carbon response to global change. In this paper, data from three sites representing well-drained soils in boreal, temperate, and tropical forests are used to illustrate the methods for using radiocarbon to determine the turnover times of soil organic matter and to partition soil respiration. For these sites, the average age of bulk carbon in detrital and Oh/A-horizon organic carbon ranges from 200 to 1200 yr. In each case, this mass-weighted average includes components such as relatively undecomposed leaf, root, and moss litter with much shorter turnover times, and humified or mineral-associated organic matter with much longer turnover times. The average age of carbon in organic matter is greater than the average age predicted for CO2 produced by its decomposition (30, 8, and 3 yr for boreal, temperate, and tropical soil), or measured in total soil respiration (16, 3, and 1 yr). Most of the CO2 produced during decomposition is derived from relatively short-lived soil organic matter (SOM) components that do not represent a large component of the standing stock of soil organic matter. Estimates of soil carbon turnover obtained by dividing C stocks by heterotrophic respiration fluxes, or from radiocarbon measurements of bulk SOM, are biased to longer time scales of C cycling. Failure to account for the heterogeneity of soil organic matter will result in underestimation of the short-term response and overestimation of the long-term response of soil C storage to future changes in inputs or decomposition. Comparison of the 14C in soil respiration with soil organic matter in temperate and boreal forest sites indicates a significant contribution from decomposition of organic matter fixed >2 yr but
A comprehensive tropospheric 14 CO 2 data set of quasi-continuous observations covering the time span from 1959 to 2003 is presented. Samples were collected at 3 European mountain sites at height levels of 1205 m (Schauinsland), 1800 m (Vermunt), and 3450 m asl (Jungfraujoch), and analyzed in the Heidelberg Radiocarbon Laboratory. The data set from Jungfraujoch (1986–2003) is considered to represent the free tropospheric background level at mid-latitudes of the Northern Hemisphere, as it compares well with recent (yet unpublished) measurements made at the marine baseline station Mace Head (west coast of Ireland). The Vermunt and Schauinsland records are significantly influenced by regional European fossil fuel CO 2 emissions. The respective Δ 14 CO 2 depletions, on an annual mean basis, are, however, only 5 less than at Jungfraujoch. Vermunt and Schauinsland both represent the mean continental European troposphere.
This chapter describes the ergosterol analysis as a means of quantifying mycorrhizal biomass. A fundamental problem concerns the concept of fungal biomass: while the chitin content may be assumed to be roughly proportional to the total amount of cell wall, the amount of cell wall is certainly not proportional to the amount of cytoplasm, which is normally concentrated at the tips, leaving the bulk of the hyphae highly vacuolated. Another fungus-specific compound, ergosterol, is a principal component of membranes, and should therefore provide a better correlation with the metabolically active biomass of a fungus. The chapter briefly discusses development and current procedure technique. The chapter also evaluates the methods—namely, sensitivity and replicability, variation in ergosterol levels within the same species, and applications in mycorrhiza research. The basic shortcomings of the method are those of variation in the ergosterol content depending on growing conditions, and interspecies variation.
This paper reports on the boreal forest, a broad, circumpolar mixture of cool coniferous and deciduous tree species which covers over 14.7 million km{sup 2}, or 11%, of the earth's terrestrial surface. At these latitudes, a strong correlation exists between the seasonal dynamics of atmospheric carbon dioxide and the seasonal dynamics of the greenness of the earth. A possible causal relation, in which the dynamics of the forests at these latitudes regulates the atmospheric carbon concentrations, appears to be consistent with the present-day understanding of ecological processes in these ecosystems. Along with its familiar role in plant photosynthesis, carbon dioxide is a greenhouse gas that markedly affects the heat budget of the earth. Thus the possibility that boreal forests may actively participate in the dynamics of atmospheric carbon dioxide is of considerable significance, especially since the climatic response to elevated atmospheric carbon dioxide concentrations seems to be strongly directed to the boreal forests of the world.
Soil organic carbon in active exchange with the atmosphere constitutes approximately two-thirds of the carbon in terrestrial ecosystems1,2. The relatively large size and long residence time of this pool (of the order of 1,200 yr) make it a potentially important sink for carbon released to the atmosphere by fossil fuel combustion; however, in many cases, human disturbance has caused a decrease in soil carbon storage3,4. Various recent estimates place the global total of soil carbon between 700 (ref. 2) and 2,946 × 1015 g (ref. 5) with several intermediate estimates: 1,080 (ref. 1), 1,392 (ref. 6), 1,456 (ref. 3), and 2,070 × 1015g (ref. 7). Schlesinger's3 estimate seems to be based on the most extensive data base (~200 observations, some of which are mean values derived from large studies in particular areas) and is widely cited in carbon cycle studies. In addition to estimating the world soil carbon pool, it is important to establish the relationships between the geographical distribution of soil carbon and climate, vegetation, human development and other factors as a basis for assessing the influence of changes in any of these factors on the global carbon cycle. Our analysis of 2,700 soil profiles, organized on a climate basis using the Holdridge life-zone classification system8, indicates relationships between soil carbon density and climate, a major soil forming factor. Soil carbon density generally increases with increasing precipitation, and there is an increase in soil carbon with decreasing temperature for any particular level of precipitation. When the potential evapotranspiration equals annual precipitation, soil carbon density9 is ~10 kg m−2, exceptions to this being warm temperate and subtropical soils. Based on recent estimates of the areal extent of major ecosystem complexes9,10 which correspond well with climatic life zones, the global soil organic carbon pool is estimated to be ~1,395 × 1015g.