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Resource‐ratio theory predicts mycorrhizal control of litter decomposition


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Ecosystems with ectomycorrhizal plants have high soil carbon:nitrogen ratios, but it is not clear why. The Gadgil effect, where competition between ectomycorrhizal and saprotrophic fungi for nitrogen slows litter decomposition, may increase soil carbon. However, experimental evidence for the Gadgil effect is equivocal. Here, we apply resource‐ratio theory to assess whether interguild fungal competition for different forms of organic nitrogen can affect litter decomposition. We focus on variation in resource input ratios and fungal resource use traits, and evaluate our model's predictions by synthesizing prior experimental literature examining ectomycorrhizal effects on litter decomposition. In our model, resource input ratios determined whether ectomycorrhizal fungi suppressed saprotrophic fungi. Recalcitrant litter inputs favored the former over the latter, allowing the Gadgil effect only when such inputs predominated. Though ectomycorrhizal fungi did not always hamper litter decomposition, ectomycorrhizal nitrogen uptake always increased carbon:nitrogen ratios in litter. Our meta‐analysis of empirical studies supports our theoretical results: ectomycorrhizal fungi appear to slow decomposition of leaf litter only in forests where litter inputs are highly recalcitrant. We thus find that the specific contribution of the Gadgil effect to high soil carbon:nitrogen ratios in ectomycorrhizal ecosystems may be smaller than previously predicted. This article is protected by copyright. All rights reserved.
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Resource-ratio theory predicts mycorrhizal control of litter
Gabriel R. Smith
*and Joe Wan
Department of Biology, Stanford University, 371 Serra Mall, Stanford, CA, USA;
Department of Environmental Systems Science, ETH Zurich, 8092, Zurich, Switzerland
Author for correspondence:
Gabriel R. Smith
Tel: +1 650 723 0552
Received: 11 October 2018
Accepted: 24 February 2019
New Phytologist (2019) 223: 1595–1606
doi: 10.1111/nph.15884
Key words: biogeochemistry, forest ecology,
Gadgil effect, litter decomposition,
mycorrhizal fungi, nitrogen limitation,
resource-ratio theory.
Ecosystems with ectomycorrhizal plants have high soil carbon : nitrogen ratios, but it is not
clear why. The Gadgil effect, where competition between ectomycorrhizal and saprotrophic
fungi for nitrogen slows litter decomposition, may increase soil carbon. However, experimen-
tal evidence for the Gadgil effect is equivocal.
Here, we apply resource-ratio theory to assess whether interguild fungal competition for dif-
ferent forms of organic nitrogen can affect litter decomposition. We focus on variation in
resource input ratios and fungal resource use traits, and evaluate our model’s predictions by syn-
thesizing prior experimental literature examining ectomycorrhizal effects on litter decomposition.
In our model, resource input ratios determined whether ectomycorrhizal fungi suppressed
saprotrophic fungi. Recalcitrant litter inputs favored the former over the latter, allowing the
Gadgil effect only when such inputs predominated. Although ectomycorrhizal fungi did not
always hamper litter decomposition, ectomycorrhizal nitrogen uptake always increased car-
bon : nitrogen ratios in litter.
Our meta-analysis of empirical studies supports our theoretical results: ectomycorrhizal
fungi appear to slow decomposition of leaf litter only in forests where litter inputs are highly
recalcitrant. We thus find that the specific contribution of the Gadgil effect to high soil
carbon : nitrogen ratios in ectomycorrhizal ecosystems may be smaller than predicted previously.
Soil holds more carbon than all plants and the atmosphere
together (Batjes, 1996) and is a major component of the land car-
bon sink, which absorbs almost a third of our annual CO
sions (Canadell et al., 2007). Terrestrial decomposition
influences the size of soil carbon stocks by facilitating the return
of carbon contained in organic matter to the atmosphere and also
is a fundamental process underlying ecosystem productivity
(Swift et al., 1979). Understanding the factors that determine
decomposition speed is therefore key to developing accurate
models of the Earth’s carbon cycle, and to predicting the
responses of soil carbon stocks to environmental change.
Nearly a century of research into plant litter decomposition
has established climate and substrate quality as major rate deter-
minants (Tenney & Waksman, 1929; Swift et al., 1979). Litter
chemistry, especially the concentration of lignin and nitrogen, is
said to govern decomposition speed within climatic constraints,
with high-lignin and/or low-nitrogen litters usually decomposing
most slowly (Meentemeyer, 1978; Aerts, 1997). Recent evidence
continues to support climate and chemistry as key controls
(Cornwell et al., 2008) but new research also challenges the com-
pleteness of this perspective, indicating greater potential for
community composition of microbes to affect decomposition
(Bradford et al., 2017; Glassman et al., 2018). This emerging
view is exemplified by findings suggesting that slowed decompo-
sition caused by interactions between two trophic guilds of soil
fungi, ectomycorrhizal and saprotrophic fungi may, in fact, be a
stronger determinant of soil carbon and nitrogen stocks than cli-
matic variables (Averill et al., 2014).
Even independently, ectomycorrhizal and saprotrophic fungi
powerfully influence the biogeochemical cycles of their environ-
ments. In return for up to 20% of their host’s net primary pro-
ductivity (Hobbie, 2006), ectomycorrhizal fungi help plants to
obtain crucial limiting nutrients such as nitrogen, mediating the
carbon and nitrogen cycles of boreal and temperate forests (Read
& Perez-Moreno, 2003; Zak et al., 2019). Free-living sapro-
trophic fungi consume abundant, recalcitrant plant polymers
such as cellulose (Cooke & Rayner, 1984; van der Wal et al.,
2013) and contribute to heterotrophic soil respiration, one of the
Earth’s largest carbon fluxes (Bond-Lamberty et al., 2018).
Although ectomycorrhizal and saprotrophic fungi rely on differ-
ent sources of carbon, they are closely related evolutionarily (Ted-
ersoo & Smith, 2013) and share aspects of their ecologies. In
fact, some ectomycorrhizal fungi oxidize organic matter as sapro-
trophic fungi do (Rineau et al., 2012; Shah et al., 2016; Op De
Beeck et al., 2018), probably not to obtain carbon but to acquire
nitrogen instead (Lindahl & Tunlid, 2015).
*These authors contributed equally to this work.
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Despite their trophic differences, ectomycorrhizal and sapro-
trophic fungi can thus both participate in enzymatic processing
of soil organic matter (Bodeker et al., 2016). This overlap in fun-
damental niche space creates opportunities for interaction
between the two trophic guilds. For example, the presence of
ectomycorrhizal fungi can suppress saprotrophic activity, slowing
decomposition of leaf litter (Gadgil & Gadgil, 1971). This phe-
nomenon is called the Gadgil effect, and could explain why
ecosystems characterized by ectomycorrhizal plants have high soil
carbon : nitrogen ratios relative to other ecosystem types (Averill
et al., 2014). Although there is not yet general consensus concern-
ing the main driver of the Gadgil effect (Fernandez & Kennedy,
2016), the ubiquity of terrestrial nitrogen limitation (LeBauer &
Treseder, 2008) and the important role that ectomycorrhizal
fungi play in plant nitrogen nutrition points to nitrogen competi-
tion between ectomycorrhizal and saprotrophic fungi as a likely
cause. This mechanism is further supported by evidence for ecto-
mycorrhizal utilization of organic nitrogen sources both in vitro
(Rineau et al., 2012; Shah et al., 2016; Op De Beeck et al., 2018)
and in situ (Talbot et al., 2013; Bodeker et al., 2014; Sterkenburg
et al., 2018), as well as ecosystem models showing that soil carbon
stocks can be influenced by ectomycorrhizal nitrogen uptake
(Orwin et al., 2011; Baskaran et al., 2017).
The Gadgil effect, mediated by nitrogen competition between
ectomycorrhizal and saprotrophic fungi, thus provides a parsimo-
nious explanation for the observed effects of ectomycorrhizal fungi
on soil corbon:nitrogen ratios (Averill et al., 2014). However,
empirical evidence for the Gadgil effect is uneven. Although ecto-
mycorrhizal fungi sometimes slow decomposition in experimental
trials (Gadgil & Gadgil, 1971; Sterkenburg et al., 2018), they also
frequently exert no observable effect (Mayor & Henkel, 2006;
Brzostek et al., 2015), and sometimes even accelerate decomposi-
tion (Zhu & Ehrenfeld, 1996; Subke et al., 2011). The dependence
of such findings on experimental context confounds our ability to
directly link the Gadgil effect to soil carbon dynamics. Here, we
seek to resolve this problematic uncertainty using theoretical com-
munity ecology. We expand upon prior efforts by incorporating
biogeochemical cycling into resource-ratio theory (Tilman, 1982),
explicitly linking fungal communities and ecosystem function.
Applying this analytically tractable and well-studied community
ecology framework, we derive the general mathematical conditions
required for nitrogen competition to cause the Gadgil effect. We
complement our analytical results with a meta-analysis of experi-
ments investigating the Gadgil effect. In doing so, we reveal which
fungal and plant traits control the effect of ectomycorrhizal fungi
on decomposition and show that inconsistent experimental evi-
dence for the Gadgil effect points to a simple, consistent root cause.
Materials and Methods
Theoretical model
Incorporating the effects of fungal stoichiometry, mycorrhizal
resource exchange and variation in substrate quality, we apply the
mechanistic consumerresource framework of Tilman (1982)
and Chase & Leibold (2003) to link fungal nitrogen competition
within leaf litter to the dynamics of substrate carbon. Using this
approach, we derive analytical expressions for the conditions
which allow ectomycorrhizal fungi to suppress saprotrophic activ-
ity through competition for nitrogen, resulting in the Gadgil
Model structure
Our model is summarized visually in Fig. 1, and its state vari-
ables, trait parameters, and resource fluxes are defined in Table 1.
A full model description is given in Supporting information
Methods S1. Here, we describe the structure and biological moti-
vation of the model, outlining its relationship to the classic mod-
els of Tilman (1982) and Chase & Leibold (2003).
Following the two-resource competition models of Tilman
(1982), we model a saprotrophic fungus Sand an ectomycor-
rhizal fungus Mcompeting for two nutrient pools, labile nitrogen
and recalcitrant nitrogen N
. Nitrogen from leaf litter enters
these two pools at the constant rates I
and I
, respectively. The
saprotrophic fungus and ectomycorrhizal fungus take up N
per-capita rates R
and N
at per-capita rates L
, resulting
in growth at per-capita rates G
. As either form of nitrogen
may satisfy growth requirements, N
and N
are substitutable
resources sensu Tilman (1982). Furthermore, the two species of
fungi experience mortality at a fixed per-capita rate, D. Although
dead fungal mycelium can make large contributions to soil car-
bon stocks (Clemmensen et al., 2013), Gadgil experiments usu-
ally focus on quantifying leaf litter decomposition without
considering necromass dynamics (Fernandez & Kennedy, 2016).
We thus consider removal of fungal necromass from the system
to be an appropriate simplification.
The two nitrogen pools, N
and N
representing variation in nitrogen substrate quality. Rather than
focusing on particular chemical forms of nitrogen, we categorize
these resources according to the cost of their acquisition, thereby
Fig. 1 Resource pools (circles), populations (squares), and fluxes (nitrogen,
blue; carbon, orange) in our theoretical model. Parameters are given in
Table 1.
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capturing the sum of physical and chemical factors. By this
approach N
thus refers to nitrogen protected by refractory plant
polymers (e.g. nitrogen physically protected within lignified plant
tissue), which is energetically costly to take up (e.g. due to the ther-
modynamic cost of oxidizing lignin). By contrast, N
forms of nitrogen whose uptake does not incur a cost (e.g. inorganic
nitrogen or physically unprotected organic nitrogen). These cate-
gories correspond to the litter quality distinction encoded by some
ecosystem models (e.g. the structural and metabolic litter pools of
Orwin et al., 2011), plant competition models (e.g. the readily and
slowly decomposable organic nutrient pools of Miki et al., 2010),
and plant population dynamic models (e.g. the available and non
available pools of Pastor et al., 2006).
We extend the classic two-resource framework to incorporate
carbon cycling by including a litter carbon pool C. Carbon from
litter enters this pool at a constant rate I
. Rather than enforcing
the coupling of the carbon pool to nitrogen dynamics, we allow
this coupling to dynamically emerge from the interaction of sub-
strate chemistry with the population dynamics of our stoichio-
metrically-constrained consumers. Saprotrophic fungus Stakes
up carbon from the environment at a per-capita rate K, whereas
ectomycorrhizal fungus Mobtains its carbon through biotrophic
exchange with an external plant host. Thus, G
is a function of
, and C, whereas G
is a function only of N
and N
. Car-
bon is required for growth of both species, and also must be
respired to mine nitrogen protected by recalcitrant plant poly-
mers (e.g. lignocellulose). In either case, carbon may limit growth
when it is not sufficient to meet these demands, as discussed in
the ‘Linking nutrient fluxes and growth’ subsection below.
Our model isolates biotic control of substrate resources by
excluding leaching. This allows us to easily discern limiting
resources in the model system: all resources not under biotic con-
trol accumulate indefinitely rather than reaching equilibrium,
demonstrating a qualitative difference from those that are under
biotic control. Scenarios in which the presence of the ectomycor-
rhizal fungus releases Cfrom biotic control of the saprotrophic
fungus are considered to show evidence of the Gadgil effect.
Although these resource dynamics differ from those generally
observed in microbially-explicit carbon cycle models, we note
that many such models also omit leaching (e.g. Allison et al.,
2010) and maintain carbon equilibrium by enforcing biotic con-
trol of carbon. To this familar perspective, our model simply
adds the possibility for stoichiometry to dynamically affect such
biotic control. Nonetheless, we demonstrate that incorporating
leaching into the model makes biotic control less obvious, but
does not impact our qualitative predictions (Methods S6).
In summary, the dynamics of our model’s five state variables
(saprotrophic fungal population S, ectomycorrhizal fungal popu-
lation M, litter carbon C, labile nitrogen N
, and recalcitrant
nitrogen N
) are described by the following system of ordinary
differential equations:
dt¼GSSDS Eqn 1
dt¼GMMDM Eqn 2
dt¼IcKS Eqn 3
dt¼IrRSSRMMEqn 5
Consumer population dynamics are determined by the balance
between growth and death, whereas resource dynamics are deter-
mined by the balance between resource inputs (I
and I
) and
biotic uptake by consumers.
Linking nutrient fluxes and growth
We mechanistically link resource uptake to biomass production.
Biomass production in our model requires a constant stoichio-
metric ratio of carbon to nitrogen. Because C,N
and N
Table 1 Description and dimensions of parameters and variables in the
Symbol Description Dimensions
State variables
SBiomass of saprotrophic fungus biomass
MBiomass of ectomycorrhizal fungus biomass
Labile nitrogen level N (as equivalent
Recalcitrant nitrogen level N (as equivalent
CCarbon level C (as equivalent
Species traits
Labile nitrogen uptake constant (time biomass)
Recalcitrant nitrogen uptake constant (time biomass)
Carbon uptake constant (sap. only) (time biomass)
Marginal carbon cost of recalcitrant
nitrogen uptake
C : N (ratio)
vEctomycorrhizal trading rate C : N (ratio)
Population rates
DPer-capita death rate (constant; identical
for both species)
Per-capita growth rate time
Resource input rates
Input rate of labile nitrogen (constant) N/time
Input rate of recalcitrant nitrogen
Input rate of carbon (constant) C/time
Biotic resource fluxes
Per-capita labile nitrogen use (maximum:
N/(time biomass)
Per-capita recalcitrant nitrogen use
(maximum: r
N/(time biomass)
KPer-capita carbon use (sap. only;
maximum: r
C/(time biomass)
XPer-capita nitrogen allocation to trade
(ecto. only)
N/(time biomass)
Carbon (C) and nitrogen (N) are measured as equivalent biomass, but are
distinguished for clarity when indicating dimensions.
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measured in units of equivalent hyphal biomass, our model is
scaled such that this stoichiometric ratio is unity. This emphasizes
biotic controls on biogeochemistry by facilitating the interpreta-
tion of substrate stoichiometry and species traits relative to fungal
demand. Because Mdoes not access C, it must instead satisfy its
carbon requirement by trading nitrogen to its plant host at per-
capita rate X, receiving vunits of carbon for each unit of nitrogen
Both species can allocate carbon toward energetically expensive
uptake, at the species-specific costs of q
units of Cper
unit of N
acquired. Accordingly, growth, nitrogen flux into
biomass, and carbon flux into biomass are related by Eqns 6 & 7:
nitrogen flux
carbon flux
Eqn 6
nitrogen flux
carbon flux
Eqn 7
In our model, resource uptake rates are constrained by species-
specific maximum physiological rates. Uptake abilities, a species-
specific trait measured by the rconstants (Table 1), determine
the strength of the linear relationship between resource availabil-
ity and maximum physiological uptake rate. That is, uptake of C,
and N
by Scannot exceed r
, and r
, respectively,
whereas uptake of N
and N
by Mcannot exceed r
Rather than treating nutrient acquisition strategy as a fixed
trait, we allow each fungus to maximize its growth rate by adjust-
ing resource uptake and allocation within the constraints
imposed by stoichiometry and physiology. Sachieves this by
modulating its N
uptake, R
, whereas Mmodulates both its N
uptake of, R
, and its plant-directed nitrogen transfer, X.
Whereas fungi will always find at least one resource limiting,
plasticity in resource allocation traits sometimes allows them to
escape the single-resource limitation expected under a strict inter-
pretation of Liebig’s law of the minimim (von Liebig, 1840).
After finding the optimal strategy, we solve for each of the
fluxes and growth functions. These expressions are piecewise con-
tinuous functions of resource levels, reflecting changes in nutrient
limitation according to resource availability. By substituting into
Eqns 1–5, we derive the fully-specified model equations, which
are given in Methods S1.
Parameter choices and model analysis
Following empirical evidence for resource partitioning between
saprotrophic and ectomycorrhizal fungi, we focused our analysis
on cases in which Mwas a superior competitor for N
, but not
for N
. Although ectomycorrhizal fungi have reduced genetic
capacity for enzyme production compared to saprotrophic rela-
tives and enzymatic capacity varies among differing lineages
(Kohler et al., 2015; Pellitier & Zak, 2018), laboratory experi-
ments have found that examined ectomycorrhizal fungi produce
more peroxidase enzyme per unit fungal biomass in vitro than
saprotrophs (Talbot et al., 2015), and soil peroxidase activity in
nature correlates positively with greater ectomycorrhizal abun-
dance relative to saprotrophs (Bodeker et al., 2014; Talbot et al.,
2014; Sterkenburg et al., 2018).
Additionally, ectomycorrhizal fungi have access to large pools
of biotrophic carbon (Hobbie, 2006) and thus are well-equipped
to carry out degradation of refractory plant compounds such as
lignin, whose breakdown involves an energy-intensive,
cometabolic process (Kirk & Farrell, 1987). Finally, resource-ra-
tio theory requires that species specialize on (that is, have a lower
R*for) different resources in order to potentially coexist with one
another (Tilman, 1982). For these reasons, the results presented
in the main text refer to this scenario (but an overview of all cases
can be found in Methods S2).
We considered the effect of variation in resource input ratios
on the ability of the ectomycorrhizal fungus to induce or exacer-
bate nitrogen limitation in the saprotroph. This can be inferred
by accumulation of carbon because we exclude resource leaching.
When Sis limited by the availability of nitrogen more than by
that of carbon, accumulation of carbon occurs because the rate of
carbon use by Sis lower than the rate of carbon input. We there-
fore sought specifically to determine the necessary conditions for
Mto suppress growth of Sto a degree sufficient to cause carbon
accumulation, as is consistent with the Gadgil effect. Details of
our approach are summarized in Methods S2.
We coded empirical studies of ectomycorrhizal influence on litter
decomposition compiled by Fernandez & Kennedy (2016)
according to whether the Gadgil effect was observed. In these
studies, researchers examined decomposition, measured by mass
loss of a leaf litter test medium or of the forest litter layer, as a
function of ectomycorrhizal colonization. In most experiments,
ectomycorrhizal presence was manipulated by trenching or by
girdling of trees, whereas one used a correlational approach
(Koide & Wu, 2003). We excluded one study in which the test
medium was not a natural substrate, Fisher & Gosz (1986), and
added two further studies, Subke et al. (2011) and Sterkenburg
et al. (2018), for a total of 12 experiments.
Our model focuses on the potential for variation in resource
inputs to influence the Gadgil effect, so we collected data on leaf
litter traits of test species from prior published literature, using
the median values where we found multiple sources. We focused
on lignin and nitrogen because lignin can contribute to nitrogen
immobilization and is considered resistant to microbial decay
(Couteaux et al., 1995). Ratios of lignin : nitrogen in litter thus
correspond to I
in our model.
For Brzostek et al. (2015), in which a mixture of Q. rubra and
Q. alba litter was used, we averaged values for these two species.
For Subke et al. (2011), in which green Tsuga heterophylla needles
were used as a decomposition substrate rather than
T. heterophylla litter, we used foliar lignin and nitrogen measure-
ments rather than those of litter tissue. We were unable to locate
data for Dicymbe corymbosa, the test litter of two experiments
(Mayor & Henkel, 2006; McGuire et al., 2010), so samples of
mature D. corymbosa leaves were analyzed for nitrogen content
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using a Carlo-Erba NA 1500 elemental analyzer (Waltham, MA,
USA), and were sent to Cumberland Valley Analytical Services
(Waynesboro, PA, USA) for lignin analysis according to Goering
& van Soest (1970). We adjusted the measured nitrogen content
of D. corymbosa before statistical analysis to account for resorp-
tion, using the average resorption efficiency of tropical ectomyc-
orrhizal trees as calculated by Zhang et al. (2018). Data used for
the meta-analysis are available in Table S1.
We used a Welch’s t-test to determine whether the lignin : nitro-
gen ratios of litter were significantly greater in studies where the
Gadgil effect was observed. We further tested the robustness of our
result with a non parametric unpaired Wilcoxon rank sum test.
Data accessibility
All data used for this manuscript appear in the paper or in the
supporting information.
In our model, resource input rates determine the impact of ecto-
mycorrhizal fungi on litter carbon dynamics. Here, we highlight
key analytical results describing this relationship. In brief, we find
that the ectomycorrhizal fungus is able to suppress saprotrophic
growth and promote carbon accumulation only when nitrogen
inputs to the system are predominantly recalcitrant. This is in
accordance with the predictions of resource-ratio theory, as recal-
citrant nitrogen is the form for which the ectomycorrhizal fungus
is a superior competitor. Our analysis shows, therefore, that the
Gadgil effect is not a universal consequence of nitrogen competi-
tion, but ectomycorrhizal fungi can alter substrate carbon : nitro-
gen ratios even when they do not suppress litter decomposition.
Model outcomes
The outcome of competition and resulting carbon dynamics
depends on resource input, as illustrated by the numerical simu-
lations in Fig. 2. Rather than representing a specific ecosystem,
we choose parameter values (Methods S7) that allow us to high-
light the full range of outcomes possible under the model. Our
conclusions are not based upon these particular parameter values
but rather on the general mathematical analysis presented in the
next section. For ease of interpretation, we shall nevertheless
begin by discussing these illustrative simulations because they
provide a useful way to visualize the outcomes of our model.
In Fig. 2, we vary resource input rates and introduce the ecto-
mycorrhizal fungus Mafter the saprotroph Sis near equilibrium
with its limiting resources. Successful invasion by the ectomycor-
rhizal fungus always increases recalcitrant nitrogen utilization
(Fig. 2ad), but its effects on carbon vary. The ectomycorrhizal
fungus can exclude the saprotroph from the system, suppressing
all carbon utilization (Fig. 2a). Under other circumstances, the
ectomycorrhizal fungus coexists with the saprotroph and initiates
(Fig. 2a,b) or accelerates (Fig. 2c) carbon accumulation. We con-
sider all of these outcomes, including not only total exclusion of
the saprotroph but also initiation or acceleration of carbon
accumulation, to be representative of the Gadgil effect. At other
resource input rates, the ectomycorrhizal fungus has no long-term
impact on carbon dynamics (Fig. 2d) or cannot invade the sapro-
troph-only community (Fig. 2e).
These divergent outcomes are linked to the nutrient limitation
status of the saprotophic fungus. Because the saprotroph is the
sole consumer of litter carbon, carbon accumulates only when
saprotrophic growth is limited by nitrogen. This can occur even
in a saprotrophic monoculture, as evidenced by the two cases
where nitrogen was lowest relative to carbon (Fig. 2c,e). In cases
where N
is high relative to N
, competition between the two
fungi for nitrogen induces nitrogen limitation where it does not
already occur (Fig. 2a,b) or exacerbates existing nitrogen limita-
tion (Fig. 2c). Nonetheless, in the two cases where recalcitrant N
input is lowest, the ectomycorrhizal fungus does not affect the
nutrient limitation status of the saprotroph (Fig. 2d,e).
The ectomycorrhizal fungus also can influence elemental
cycling in litter without inducing the Gadgil effect. For instance,
the illustrative simulations include cases where the ectomycor-
rhizal fungus suppresses the accumulation of N
and N
affecting the nitrogen limitation status of the saprotroph (Figs 2d,
S2). Thus, in our model, it is possible for ectomycorrhizal nitro-
gen uptake to elevate of carbon : nitrogen ratios without inducing
the Gadgil effect.
Examination of model outcomes for a full range of resource
input ratios confirms the trends observed from individual simula-
tions: the ectomycorrhizal fungus promotes the Gadgil effect only
when N
is high relative to N
. Noting that model outcomes can
be predicted by resource input ratios alone, we visualize competi-
tive outcomes and nutrient dynamics as a function of the labile
nitrogen-to-carbon input ratio, I
, and recalcitrant nitrogen-to-
carbon input ratio, I
(Fig. 3); the remaining parameters have
values identical to those used in Fig. 2. For the saprotrophic fun-
gus growing in isolation, carbon only accumulates when both
forms of nitrogen input are low relative to carbon input (Fig. 3a,
orange zone). When both species are present, carbon accumulation
is possible under a greater range of conditions. If N
is sufficiently
high relative to N
, the ectomycorrhizal fungus induces (Fig. 3b,
regions A and B) or increases (Fig. 3b, region C) carbon accumula-
tion. This change in carbon accumulation rate is quantitatively
shown in Fig. 3(c), where a nitrogen-mediated Gadgil effect occurs
at high N
input (above the gray and orange solid lines of Fig. 3b).
Analytical results
Here, we highlight key results from the analytical treatment of
our model, corresponding to each of the boundary lines of Fig. 3.
A full set of analytical expressions for the outcomes of our model
is presented in Methods S2, and detailed derivations are given in
Methods S3S5.
In a saprotroph-only system (as in Fig. 3a), nitrogen and car-
bon cycling are tightly linked. Carbon accumulation is deter-
mined solely by the relative stoichiometry of nitrogen and carbon
inputs to the system. Analytically, we find that carbon accumu-
lates when the following condition, corresponding to the solid
orange boundary in Fig. 3(a), holds:
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Ic[IþIrþqSIrEqn 8
Because our model is scaled to facilitate comparison of
resource inputs to consumer stoichiometric requirements, this
inequality demands that carbon input exceeds the rate needed to
make fungal biomass from nitrogen input (I
) after account-
ing for the cost of utilizing recalcitrant nitrogen (q
Two conditions determine whether the ectomycorrhizal fun-
gus can cause the Gadgil effect (Methods S2S5). First, the ecto-
mycorrhizal fungus must be able to successfully compete with the
saprotroph for nitrogen. This condition allows the ectomycor-
rhizal fungus to persist if both fungi become nitrogen-limited
due to carbon accumulation. Here, we show this for the biologi-
cally realistic case in which the ectomycorrhizal fungus specializes
on N
, but an analysis of all possible R*values demonstrates that
this requirement is general: Mmust have a lower R*for at least
one resource in order for the Gadgil effect to occur (see analysis
for all cases in Methods S2). Second, carbon and nitrogen
dynamics must be decoupled. Stated simply, the ectomycorrhizal
fungus must suppress saprotrophic growth to the extent that the
saprotroph does not use all available carbon. Together, these con-
ditions ensure that carbon accumulates indefinitely.
Condition 1: ectomycorrhizal competition for nitrogen
When the Gadgil effect occurs in our model, both fungal species
are limited by nitrogen. Here, we can apply the classic resource-
ratio theory of Tilman (1982) for analysis. Resource require-
ments are thus summarized by R*, the level of resource Rat
which a species can maintain a constant population. A lower R*
(a) (b)
(d) (e)
Ti Ti Ti
Ti Ti
Fig. 2 Numerical model simulations. Species
populations and resources are plotted as a
function of time, excluding N
, which is held
at so low a level as to not be visible.
Saprotrophic fungus Senters at time 0; entry
of ectomycorrhizal fungus Mis marked by a
vertical line. Resource input ratios I
vary across the simulations, creating different
outcomes (see Supporting Information
Methods S6 for parameters and simulation
(a) (b) (c)
Fig. 3 Equilibria and carbon dynamics of the model at different resource input ratios. As model behavior depends only on the ratio of resource inputs, the
axes show the ratio of each form of nitrogen to carbon, scaled so that a value of 1 is the stoichiometric ratio required to make fungal biomass. (a) Resource
limitation status and nutrient dynamics of a saprotrophic monoculture at steady state for different resource input ratios. (b) Competitive outcomes and
effects on nutrient dynamics for two-species system. Hatched regions indicate resource ratios at which the two species cannot coexist. Boundaries from (a)
are overlaid to highlight changes in resource limitation. Regions AE correspond to the panels of Fig. 2(ae). (c) The strength of the Gadgil effect, measured
as the difference in carbon accumulation rate between the saprotroph-only and coexistence (or ectomycorrhizal-only) equilibria. The scale expresses this
change as a percentage of the carbon input rate I
. The boundaries of (b) are overlaid for clarity.
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implies greater competitive ability for that resource. For the
saprotroph, these values are inversely proportional to uptake abil-
ity (r
and r
, respectively):
Eqn 9
Thus, competitive ability is determined by the ability to take
up enough nitrogen to make up for the rate of mortality, D. For
the ectomycorrhizal fungus, we find the following R*values:
Eqn 10
Ectomycorrhizal R*values are also inversely proportional to
uptake ability (r
), but each expression contains a further
term representing the additional nitrogen cost incurred by
resource trade with an external plant host.
Our focal scenario, where the ectomycorrhizal fungus is a
superior competitor for N
, corresponds to the assumption that
the ectomycorrhizal fungus has a lower R*for N
and a higher R*
for N
than the saprotrophic fungus does: Nr
S. Applying the graphical zero net-growth isocline
approach of (Tilman, 1982) to this case illustrates the conditions
which determine competitive outcomes (Fig. 4a). Though the
zero net-growth isoclines differ from the model of (Tilman,
1982) when carbon is low enough to limit saprotrophic growth,
such conditions do not enable the Gadgil effect and are not
examined here (Fig. 4b).
Three conditions determine competitive outcome in the model
of Tilman (1982): the relative positions of the zero net-growth iso-
clines, the resource consumption of the competing species at equi-
librium, and the supply of resources. Under the case we consider
here, the first two conditions are fixed: the zero net-growth isolines
cross and each species consumes relatively more of the resource
that has a greater impact on its growth (Fig. 4a). By contrast, we
allow resource supply to vary. As such, depending on I
ectomycorrhizal fungus may competitively exclude the saprotroph
(Fig. 4a, region I), the two species may coexist (region II), or the
saprotroph may exclude the ectomycorrhizal fungus (region III).
In particular, we find that if I
is above a critical threshold
, the ectomycorrhizal fungus competitively excludes the
[QM;where QM¼rrM
Eqn 11
This inequality corresponds to the solid green line of Fig. 3(b).
Here, Q
is the product of two terms representing ectomycor-
rhizal specialization on N
and the ratio of ectomycorrhizal com-
petitive dominance for N
to saprotrophic competitive
dominance for N
. When this condition holds, the saprotrophic
fungus is driven to extinction and carbon accumulates at the
maximum possible rate (as in Fig. 2a). It therefore represents the
strongest possible Gadgil effect.
If instead I
is below Q
but above the threshold for sapro-
trophic dominance Q
, the ectomycorrhizal fungus coexists with
the saprotroph:
\QM;where QS¼rrS
Eqn 12
This inequality represents the solid gray line of Fig. 3(b). The
two terms in the expression for Q
are analogous to those in the
expression for Q
. The first term represents the relative ability of
the saprotrophic fungus (instead of the ectomycorrhizal fungus) to
use N
, the second term is the ratio of ectomycorrhizal
competitive dominance for N
to saprotrophic competitive domi-
nance for N
Condition 2: decoupling of carbon and nitrogen dynamics
The second condition for the Gadgil effect is that the ectomycor-
rhizal fungus must decouple carbon and nitrogen dynamics by
suppressing saprotrophic growth. This is possible because the
ectomycorrhizal fungus obtains carbon from its plant host, allow-
ing it to suppress saprotrophic uptake of litter carbon while
remaining independent of the litter carbon pool.
Our analysis of nitrogen competition demonstrated that high
favor ectomycorrhizal competitive dominance. Considering the
second condition, we find that N
also determines the degree to
which the ectomycorrhizal fungus suppresses saprotrophic carbon
utilization. In order for carbon to accumulate, I
must be greater
than the following threshold:
IcEqn 13
This inequality defines the solid orange line in Fig. 3(b). The
first term in the right-hand expression (Q
) requires that N
input be high enough to compensate for I
. The second term (I
multiplied by a negative constant) indicates that as carbon input
increases, carbon has a greater tendency to accumulate, and thus
is required to induce carbon accumulation.
Finally, we note that nitrogen use by the ectomycorrhizal fun-
gus always draws nitrogen availability down to a stable equilib-
rium (given by the analytical expressions in Methods S3.4S3.7),
invariably altering nitrogen cycling regardless of its ability to
induce the Gadgil effect. Fueled by plant photosynthate, the ecto-
mycorrhizal fungus can take up nitrogen at its maximum physio-
logical rate, which makes its nitrogen acquisition complementary
to that of the saprotroph. Because the ectomycorrhizal fungus
does not directly interact with litter carbon in our model, its pres-
ence always elevates carbon : nitrogen ratios.
We tested whether our model could adequately predict occur-
rence of the Gadgil effect in ectomycorrhizal forests by compar-
ing our findings to the results of prior empirical investigations.
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Our analysis showed that higher I
promoted the Gadgil effect.
Because lignin : nitrogen ratios in decomposition test substrates
are functionally analogous to I
, we hypothesized that lignin :
nitrogen ratios would be significantly higher in experiments
where the Gadgil effect was observed than in those where it was
not. A Welch’s t-test showed that lignin : nitrogen ratios were
indeed significantly higher in studies showing the Gadgil effect,
supporting our theoretical results (Fig. 5; t=5.271, P=0.0002).
A non-parametric Wilcoxon rank sum test returned qualitatively
equivalent results (P=0.0028), underscoring the robustness of
this finding.
Chemical recalcitrance has long been supported alongside climate
as a major factor affecting litter decomposition speed (Tenney &
Waksman, 1929; Swift et al., 1979; Cornwell et al., 2008). A
growing body of literature now shows that ecological factors such
as decomposer community composition may be of equal or
greater importance, however (Gadgil & Gadgil, 1971; Bradford
et al., 2017; Glassman et al., 2018). Here, we have found that
interactions between ecological and chemical factors jointly influ-
ence this important ecosystem function. Concisely, while climatic
conditions constrain decomposer physiology, substrate stoi-
chiometry selects for different decomposers.
Our model analysis showed that decomposition can indeed be
inhibited by ectomycorrhizal nitrogen uptake, but that this out-
come is not universal. The ability of ectomycorrhizal fungi to
induce nitrogen limitation in co-occurring saprotrophs is a func-
tion of the nitrogen use traits of the two fungal guilds and the
chemistry of their substrate. In accordance with empirical evi-
dence, ectomycorrhizal fungi in our model are superior competi-
tors for recalcitrant nitrogen sources, and were thus favored by
litter inputs with higher ratios of recalcitrant to labile nitrogen.
When ratios were sufficiently high, ectomycorrhizal fungi
excluded saprotrophic fungi and thereby hindered carbon uptake,
demonstrating the Gadgil effect. By contrast, lower input ratios
of recalcitrant to labile nitrogen benefited saprotrophic fungi,
which were then able to evade nitrogen limitation even when
ectomycorrhizal fungi were present. Substrate chemistry deter-
mined whether the Gadgil effect was possible, but ectomycor-
rhizal fungi always increased substrate carbon : nitrogen ratios,
even when the Gadgil effect did not occur.
We determined moreover that ectomycorrhizal nitrogen use
traits are key controllers of the Gadgil effect. Ectomycorrhizal
fungi benefit from reduced carbon limitation thanks to their pho-
tosynthetic host, but this alone cannot provide the advantage
required for them to limit saprotrophic activity. Fundamentally,
if nitrogen competition is to cause the Gadgil effect, this must be
a result not only of differences in carbon acquisition traits, but
also of differences in nitrogen acquisition traits. Specifically, ecto-
mycorrhizal fungi must be superior competitors sensu Tilman
(a) (b)
Fig. 4 Graphical analysis of the resource competition model. We plot the zero net-growth isoclines (solid lines) and resource consumption vectors (solid
arrows) of both fungi at high and low levels of substrate carbon C. (a) When carbon is high and does not limit growth, the model represents the
substitutable resource case of Tilman (1982). The system’s equilibrium point is found where the isoclines cross and the consumption vectors ensure that
stable coexistence is possible. Here, the outcome of competition is determined by resource input relative to the inverse of the resource consumption vectors
(dashed lines). If recalcitrant inputs predominate (region I), the ectomycorrhizal fungus excludes the saprotroph. Coexistence occurs at intermediate ratios
of recalcitrant to labile nitrogen inputs (region II, highlighted). If labile inputs predominate (region III), the saprotroph excludes the ectomycorrhizal fungus.
(b) When saprotrophic growth is limited by carbon availability, the isoclines no longer conform to any of the classic cases outlined by Tilman (1982) and the
conditions for two-resource competition no longer apply. We therefore do not depict the outcome of competition for this case.
Fig. 5 Lignin : nitrogen ratios predict the occurrence of the Gadgil effect in
12 empirical studies. See Supporting Information Table S1 for studies used
and trait data. Welch’s two sample t-test confirms the significance of the
difference (t= 5.271, P= 0.0002).
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(1982) for at least one form of nitrogen, enabling more efficient
growth at a given environmental nitrogen level compared to
saprotrophic fungi. In fact, they must acquire nitrogen far more
efficiently than saprotrophs because they must balance both their
own budget and that of their host.
As predicted by our model, recalcitrant litter appears to be a
prerequisite for the Gadgil effect in empirical trials. Consistent
with ectomycorrhizal specialization on recalcitrant nitrogen
sources, experiments using test litters with high lignin : nitrogen
ratios found ectomycorrhizal retardation of decomposition,
whereas those using more labile litters did not. Furthermore, all
experiments in the former category occurred in coniferous forests.
We have found no direct evidence for the Gadgil effect in tem-
perate or tropical broadleaf forests (Mayor & Henkel, 2006;
McGuire et al., 2010; Brzostek et al., 2015) despite development
of typical ectomycorrhizal nutrient economies in these environ-
ments (Phillips et al., 2013; Corrales et al., 2016). Taken
together, our results indicate that the specific influence of the
Gadgil effect may be restricted to ectomycorrhizal ecosystems
where recalcitrant litter already slows decomposition.
Like that of Tilman (1982), our model focuses on interactions
between ecological communities and resources. Although we cap-
ture interguild differences in resource-use traits between microbes
in greater detail than do many larger-scale ecosystem models
(Sulman et al., 2018), we do not explicitly represent a complete
carbon or nitrogen cycle. Omitting respiration and nitrogen min-
eralization, we do not track total ecosystem carbon and nitrogen
stocks. As such, we also omit direct coupling of these elemental
cycles. The model’s strong concordance with empirical evidence
indicates that it can successfully answer our specific question:
does uptake of nitrogen by ectomycorrhizal fungi cause sapro-
trophic fungi to become nitrogen-limited, and thereby slow the
decomposition of leaf litter? However, many further questions
For example, there is now wide recognition that a narrow focus
on litter decomposition excludes many other processes mediating
soil carbon storage (Jackson et al., 2017). Indeed, although his-
torical perspectives emphasize the accumulation of undecom-
posed plant polymers as a driver of soil carbon stocks (Lehmann
& Kleber, 2015), new conceptual and empirical discoveries high-
light the significant contributions of microbial residues and
necromass (Clemmensen et al., 2013; Cotrufo et al., 2013). As
our model does not include recycling of dead fungal mycelium,
we cannot here make predictions concerning the effects of ecto-
mycorrhizal nitrogen uptake on the formation and stability of
microbially-derived soil organic matter. In light of our findings,
we nevertheless speculate that this comparatively understudied
subject may be of greater relevance for total soil carbon stocks
than the Gadgil effect sensu stricto.
Community interactions not present in our model also may be
of major importance in assessing the total environmental effects
of ectomycorrhizal fungi. Enzyme production by ectomycorrhizal
mycelium could subsidize saprotrophic growth by increasing car-
bon availability (Baskaran et al., 2017), or even contribute
directly to carbon mineralization (Hofrichter et al., 1999). This
would likely slow carbon accumulation, even when the Gadgil
effect occurs. Differences in the modeled fate of carbon-rich ecto-
mycorrhizal decomposition products in prior work contribute to
opposite predictions for total soil carbon stocks (Orwin et al.,
2011; Baskaran et al., 2017), underscoring the significance of this
Finally, interactions between individual plants and fungi in
symbiosis may be consequential as well. We here used fixed trad-
ing rates of nitrogen and carbon between the ectomycorrhizal
fungus and its external host (v). Because the relative profitability
of the trade for the ectomycorrhizal partner in our model affects
its nitrogen uptake and thus the nitrogen nutrition of its host,
extensions including context-dependency and fluctuation of this
value could reveal interesting feedbacks between aboveground
and belowground compartments with potential impacts on
decomposition. Prior work incorporating flexible trading rates
and multiple potential fungal partners shows that plant carbon
allocation towards ectomycorrhizal fungi may be highly depen-
dent in particular on ecological marketplace dynamics (Franklin
et al., 2014), which do not generally appear in models addressing
effects of mycorrhizal fungi on decomposition (Orwin et al.,
2011; Baskaran et al., 2017), ours included.
We have not found evidence for a globally significant Gadgil
effect mediated by nitrogen competition, and thus conclude
that its contribution to high soil carbon : nitrogen ratios in
ectomycorrhizal soils may not be as large as anticipated (Averill
et al., 2014). We observe, however, that introducing the ecto-
mycorrhizal fungus to a saprotrophic monoculture in our
model always lowers nitrogen levels, regardless of its effect on
carbon, simply due to more efficient utilization of the total
nitrogen pool. Several studies show that differences in soil car-
bon : nitrogen ratios in forests with trees of different mycor-
rhizal type are better explained by variation in nitrogen stocks
than in carbon stocks (Craig et al., 2018; Zhu et al., 2018),
consistent with this simpler mechanism. We fully expect that a
shift in soil stoichiometry facilitated by ectomycorrhizal fungi is
likely to have important consequences for process rates in many
ecosystems, potentially resulting in decreased decomposition
and/or increased primary productivity. However, we caution
that inferring this from variation in stock sizes alone risks con-
flating cause and effect.
Evidence that mycorrhizal associations are perhaps the most
important plant traits controlling not only ecosystem biogeo-
chemistry (Phillips et al., 2013; Averill et al., 2014), but also
responses to global change pressures (Terrer et al., 2016; Averill
et al., 2018) continues to mount. Interest in the effects of ecto-
mycorrhizal fungi on soil carbon dynamics has grown accordingly
(Zak et al., 2019). Here, we have used theoretical community
ecology to show that a nitrogen-mediated Gadgil effect, hypothe-
sized to explain globally significant biogeochemical patterns, lacks
strong general support. We emphasize that this result does not
undermine findings of ectomycorrhizal importance in global car-
bon and nitrogen cycling (Averill et al., 2014). It does, however,
demonstrate that conclusions regarding the mechanisms driving
observed variation are likely premature and that there exists an
urgent need for further research clarifying the role of fungi in soil
carbon and nitrogen dynamics. We anticipate that many exciting
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Phytologist Research 1603
discoveries in this area are waiting to be made, and that the devel-
opment and application of ecological theory will prove invaluable
in revealing them.
We thank K. G. Peay, E. A. Mordecai, P-J. Ke, K. C. Abbott, C.
Averill, and members of the Peay and Abbott Labs for valuable
constructive comments. We thank B. D. Lindahl and three
anonymous reviewers for recommendations that led to the sub-
stantial improvement of this manuscript. Finally, we thank T. W.
Henkel for providing D. corymbosa samples for analysis. The
work of GRS is funded by a US NSF Graduate Research Fellow-
Author contributions
GRS and JW contributed equally to this work.
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Supporting Information
Additional Supporting Information may be found online in the
Supporting Information section at the end of the article.
Fig. S1 Zero net-growth isoclines for saprotrophic fungus Sand
ectomycorrhizal fungus M.
Fig. S2 Full set of numerical model simulations.
Fig. S3 Equilibria of the model at different resource input ratios,
with limitation status indicated.
Methods S1 Full description of the model.
Methods S2 Overview of analytical results.
Methods S3 Feasibility and persistence of model equilibria.
Methods S4 Stability of model equilibria.
Methods S5 Invasibility analysis.
Methods S6 Numerical simulation of the model.
Methods S7 Model with leaching.
Table S1 Data used for the meta-analysis appearing in the main
Please note: Wiley Blackwell are not responsible for the content
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... Substrate quality has been found to be an important factor in explaining the discrepancies in litter decomposition rates with or without ectomycorrhizal fungi (Smith & Wan 2019). The substrate quality mechanism specifies that in systems with lower litter quality (i.e. ...
... This difference in substrate preference is revealed in the realized niche differences between saprotrophic and ectomycorrhizal fungi in boreal forest soils; the carbon to nitrogen ratio decreases with depth in the boreal forest, and saprotrophs are found more abundantly in the upper part of the soil profile while mycorrhizal fungi are found in deeper organic and mineral horizons (Lindahl et al. 2007). These theoretical and experimental underpinnings support research showing that the Gadgil effect is most commonly demonstrated in high-latitude ecosystems with higher lignin:N and C:N ratios dominated by species in the genus Pinus (Fernandez & Kennedy 2016;Sterkenburg et al. 2018;Maaroufi et al. 2019;Smith & Wan 2019;Fernandez et al. 2020). ...
... This has could be interpreted as a Gadgil effect (Rhyti et al., 2021), whereby the nitrogen immobilized in root and fungal necromass becomes accessible to nitrogen limited saprotrophs, increasing decomposition as seen in increases in respiration. Interpretations of the Gadgil effect may vary as strictly litter decomposition (Smith & Wan 2019) or even changes in bulk soil organic carbon (Harmer & Alexander 1985;Staaf 1988), which could also confound interpretations and inconsistencies in experimental results. In contrast, the rhizosphere is also an important component of 'priming' other free-living soil organisms with a consistent turnover of dead roots and mycelium, which we saw an overall lower amount of soil respiration in Paper I in the third year (2019) from the free-living heterotrophic component. ...
The immense diversity and biomass of ericoid-, ectomycorrhizal, and saprotrophic fungal guilds in boreal forest soils make them vital components of conservation and ecosystem processes, and in particular, many ectomycorrhizal fungi are considered species of conservation concern. However, amalgamated information on the functions and relationships of soil fungi to perceived forest conservation values, and how inter and intra-guild interactions affect the accretion and decomposition of soil organic matter is lacking. In a long-term factorial shrub removal and pine root exclusion experiment, I assessed guild contributions to soil respiration and decomposition of organic substrates guided by ecological theory. Then in the northern and southern boreal forest, I evaluated whether forest conservation values are aligned with the diversity of ectomycorrhizal fungi. Overall, the ericoid guild makes a significant contribution to total soil respiration (11 ± 9%), and ericoid activities appeared to be more sensitive to periods of drought compared to ectomycorrhizal (43 ± 1%) and saprotrophic (53 ± 5%) guilds. Saprotrophic-ectomycorrhizal interactions during decomposition led to a modest, yet inconsistent Gadgil effect (10%) for early-stage litter decomposition. Ericoid and ectomycorrhizal guilds interactions were determined to be more important for late-stage organic matter balance in boreal forest soils. Ectomycorrhizal species richness was significantly higher in the southern boreal forest compared to the north. Furthermore, forest conservation values across the boreal forest were not adequately related to ectomycorrhizal diversity through DNA-metabarcoding. Instead, soil fertility, corresponding to tree species basal area, was the clearest indicator of ectomycorrhizal diversity and composition in both regions. Mycorrhizal guilds may be underappreciated and understudied in terms of conservation, but their functional roles in the accumulation and decomposition of organic matter in long-term soil carbon pools emphasizes the importance of evaluating the many dimensions of fungal conservation in boreal forests.
... This suppressive effect appears to be strongest for ECM fungi with greater decay capacities, possibly because these taxa can compete more strongly with saprotrophic fungi for the same resources (Fernandez et al. 2020). Furthermore, the Gadgil effect may also be stronger for lignin-rich litter due to resource limitation (Smith & Wan 2019;Fernandez et al. 2020), suggesting it could be a particularly important control over the decay of fine roots. At the same time, there is some evidence from boreal forests that decay by ECM fungi with peroxidases restricts the accumulation of SOM (Sterkenburg et al. 2018;Clemmensen et al. 2021;Lindahl et al. 2021). ...
... Studies of mycorrhizae and SOM in temperate forests have primarily focused on how soil C storage differs between ecosystems dominated by ECM or arbuscular mycorrhizae (Phillips et al. 2013;), yet our observations suggest compositional turnover within ECMdominated fungal communities is also an important control over SOM dynamics. Because ECM fungi do not assimilate or respire the organic C compounds they decay while acquiring organic N (Treseder et al. 2006;Baldrian 2009;Lindahl & Tunlid 2015), many conceptualizations assume ECM fungi selectively liberate N from SOM (Orwin et al. 2011;Smith & Wan 2019;Fernandez et al. 2020). However, ECM lineages that have retained peroxidases from ligninolytic saprotrophic ancestors are unlikely to liberate N from SOM without also extensively decaying lignin-derived SOM, because peroxidases and ancillary enzymes fully and extracellularly oxidize lignin-derived compounds to CO2 (Kirk & Farrell 1987;Hofrichter 2002;Pellitier & Zak 2018). ...
... Similarly, fine root decay likely decreased with increasing abundances of ECM fungi with peroxidases (Figure 4.3a) because resource limitation of saprotrophic growth is greater for lignin-rich litter and competitive suppression by ECM is stronger (Smith & Wan 2019;Fernandez et al. 2020). We propose that the uniquely high lignin concentrations of fine roots An important limitation of this study is that our results are based on correlations between fine root decay, genetic potentials, fungal community composition, and the environment. ...
A central goal in ecology is to understand how the environment modifies the composition of ecological communities and, in turn, the functioning of ecosystems. Fine root litter accounts for half of plant litter production in forest ecosystems and is a primary source of soil organic matter. However, the ecological factors controlling the decay of fine root litter remain a critical gap in our understanding of the terrestrial carbon cycle and its responses to environmental change. Using experimental and observational approaches, I explored how microbial community composition influences the decay of fine root litter into soil organic matter in temperate forest ecosystems. First, I tested whether shifts in fungal and bacterial community composition have slowed fine root litter in a long-term (ca. 20 years) field experiment simulating future rates of anthropogenic atmospheric nitrogen deposition in northern hardwood forests. My work revealed that experimental nitrogen deposition reduced the relative abundance of saprotrophic Agaricomycete fungi that use peroxidase enzymes to fully oxidize lignin. In contrast, experimental nitrogen deposition favored Actinobacteria, which only partially decay lignin. Furthermore, molecular characterization using pyrolysis gas chromatography-mass spectrometry demonstrated that nitrogen deposition increased the abundance of lignin-derived compounds in soil organic matter. Previous studies have shown that anthropogenic nitrogen deposition slows fine root decay and enhances soil carbon storage – plausibly acting as a sink for anthropogenic carbon dioxide emissions – and my findings demonstrate that shifts in microbial community composition that slow the decay of lignin in fine root litter underlie these biogeochemical responses. Second, I explored how turnover in fungal community composition along a natural soil inorganic nitrogen gradient across northern temperate forests influences fine root decay and the accumulation of soil organic matter. I found that differences in the composition of fungal communities inhabiting decomposing fine root litter did not explain soil organic matter stocks and biochemistry across the soil nitrogen gradient. However, within the soil fungal community, the relative abundance of ectomycorrhizal fungi that have retained genes encoding peroxidase enzymes declined with increasing inorganic nitrogen availability. This response was correlated with an increase in lignin-derived soil organic matter and overall soil carbon storage, suggesting that the decomposition of lignin-derived soil organic matter by certain symbiotic ectomycorrhizal fungi with peroxidase enzymes constrains soil organic matter accumulation across soil nitrogen gradients. Lastly, I used a field decay study with fine root litterbags to quantify the relative importance of environmental and fungal controls over fine root decay rates. I found that ligninolytic saprotrophs, ectomycorrhizal fungi with peroxidases, and their influence on community-level genetic potential for decay, better predict rates of fine root decay than environmental factors. Together, these findings provide evidence that microbial community composition and its responses to the environment regulate the decay of fine roots into soil organic matter. Thus, explicitly accounting for turnover in microbial community composition and its implications for community functioning may improve our ability to accurately predict terrestrial carbon cycling and its responses to environmental change.
... One mechanism for this suppression is that peroxidase-capable EcM fungi may induce saprotrophic N limitation by mining N from organic matter (Averill and Hawkes 2016). While experiments testing whether EcM fungi suppress decomposition (i.e., the Gadgil effect) have had equivocal results (e.g., Brzostek et al. 2015, Lang et al. 2021, one recent study suggested the Gadgil effect predominantly occurs in systems with high lignin:N litter inputs (Smith and Wan 2019), which would apply to the GA and NH sites where Pinaceae and Fagaceae dominated the EcM plots and where peroxidase-capable EcM fungi were more prevalent. Differences in EcM fungi's ability to mine N from SOM is a potential, yet unexplored, reason for the contextdependency of the Gadgil effect. ...
As global change shifts the species composition of forests, we need to understand which species characteristics affect soil organic matter cycling to predict future soil carbon
... Although the 'Gadgil effect' has been experimentally tested by several studies over the past half century, the results among those studies are largely inconsistent (Fernandez & Kennedy, 2016). The lack of consistency across studies and systems may be driven by variation in environmental factors, such as soil fertility and soil moisture (Koide & Wu, 2003;Smith & Wan, 2019), substrate quality (Sieti€ o et al., 2019;Fernandez et al., 2020) or the position within the soil profile (B€ odeker et al., 2016;Clemmensen et al., 2021;Lindahl et al., 2021). For instance, Sterkenburg et al. (2018) demonstrated that the 'Gadgil effect' was restricted to the surface litter, mainly because saprotrophs were unable to exploit substrates with a low proportion of hydrolysable compounds in deeper horizons, irrespective of EMF presence. ...
• Mycorrhizal fungi associated with boreal trees and ericaceous shrubs are central actors in organic matter (OM) accumulation through their belowground carbon allocation, their potential capacity to mine organic matter for nitrogen (N) and their ability to suppress saprotrophs. Yet, interactions between co-occurring ectomycorrhizal fungi (EMF), ericoid mycorrhizal fungi (ERI), and saprotrophs are poorly understood. • We used a long-term (19 year) plant functional group manipulation experiment with removals of tree roots, ericaceous shrubs and mosses and analyzed responses of different fungal guilds (assessed by metabarcoding) and their interactions in relation to OM quality (assessed by mid-infrared spectroscopy and nuclear magnetic resonance) and decomposition (litter mesh-bags) across a 5000-year post-fire boreal forest chronosequence. • We found that removal of ericaceous shrubs and associated ERI changed the composition of EMF communities, with larger effects occurring at earlier stages of the chronosequence. Removal of shrubs was associated with enhanced N availability, litter decomposition, and enrichment of the recalcitrant OM fraction. • We conclude that increasing abundance of slow-growing ericaceous shrubs and associated fungi contributes to increasing nutrient limitation, impaired decomposition and progressive OM accumulation in boreal forests, particularly towards later successional stages. These results are indicative of the contrasting roles of EMF and ERI in regulating belowground OM storage.
... Following a fire, fungal communities respond rapidly within days or few weeks (Reazin et al. 2016), albeit the post-fire communities may remain distinct from those present before fire for years or decades (Dooley and Treseder 2012;. Fire alters fungal successional dynamics (e.g., Lombao et al. 2020;Pressler et al. 2019;Smith and Wan 2019) that may be related to a number of factors, including (i) population mortality and differential community recovery driven by dispersal, colonization probabilities, and priority effects; (ii) shifting edaphic conditions that facilitate emergent niche partitioning in surviving fungi; (iii) differential utilization of pyrogenic substrates (e.g., biochar or fire-generated necromass); or (iv) perhaps, collections of taxa that act in concert as interacting fire-resilient subcommunities (i.e., consortia; Paerl and Pinckney 1996). All of these may be operating simultaneously, and it seems certain that their relative importance to postfire fungal succession differs based on fire regime, ecosystem, and a range of related environmental factors. ...
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Fires occur in most terrestrial ecosystems where they drive changes in the traits, composition, and diversity of fungal communities. Fires range from rare, stand-replacing wildfires to frequent, prescribed fires used to mimic natural fire regimes. Fire regime factors, including burn severity, fire intensity, and timing, vary widely and likely determine how fungi respond to fires. Despite the importance of fungi to post-fire plant communities and ecosystem functioning, attempts to identify common fungal responses and their major drivers are lacking. This synthesis addresses this knowledge gap and ranges from fire adaptations of specific fungi to succession and assembly fungal communities as they respond to spatially heterogenous burning within the landscape. Fires impact fungi directly and indirectly through their effects on fungal survival, substrate and habitat modifications , changes in environmental conditions, and/or physiological responses of the hosts with which fungi interact. Some specific pyrophilous, or "fire-loving," fungi often appear after fire. Our synthesis explores whether such taxa can be considered cosmopolitan, and whether they are truly fire-adapted or simply opportunists adapted to rapidly occupy substrates and habitats made available by fires. We also discuss the possible inoculum sources of post-fire fungi and explore existing conceptual models and ecological frameworks that may be useful in generalizing fungal fire responses. We conclude with identifying research gaps and areas that may best transform the current knowledge and understanding of fungal responses to fire.
... Among plant species associating with AMF, there may be a trade-off between allocation to defensive compounds and investment into mycorrhizal symbiosis (Xia et al., 2021), which may equalize PSFs across the gradient of mycorrhizal dependency. Mycorrhizal fungi can also interfere with saprotroph activity by modifying belowground C transfer and litter decomposition (Kaiser et al., 2015;Smith & Wan, 2019) and competing for nutrients (Averill et al., 2014;Franklin et al., 2014). ...
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Feedback between plants and soil microbial communities can be a powerful driver of vegetation dynamics. Plants elicit changes in the soil microbiome that either promote or suppress conspecifics at the same location, thereby regulating population density‐dependence and species coexistence. Such effects are often attributed to the accumulation of host‐specific antagonistic or beneficial microbiota in the rhizosphere. However, the identity and host‐specificity of the microbial taxa involved are rarely empirically assessed. Here we review the evidence for host‐specificity in plant‐associated microbes and propose that specific plant‐soil feedbacks can also be driven by generalists. We outline the potential mechanisms by which generalist microbial pathogens, mutualists and decomposers can generate differential effects on plant hosts and synthesise existing evidence to predict these effects as a function of plant investments into defence, microbial mutualists and dispersal. Importantly, the capacity of generalist microbiota to drive plant‐soil feedbacks depends not only on the traits of individual plants but also on the phylogenetic and functional diversity of plant communities. Identifying factors that promote specialisation or generalism in plant‐microbial interactions and thereby modulate the impact of microbiota on plant performance will advance our understanding of the mechanisms underlying plant‐soil feedback and the ways it contributes to plant coexistence.
Understanding how genetic differences among soil microorganisms regulate spatial patterns in litter decay remains a persistent challenge in ecology. Despite fine root litter accounting for ~50% of total litter production in forest ecosystems, far less is known about the microbial decay of fine roots relative to aboveground litter. Here, we evaluated whether fine root decay occurred more rapidly where fungal communities have a greater genetic potential for litter decay. Additionally, we tested if linkages between decay and fungal genes can be adequately captured by delineating saprotrophic and ectomycorrhizal fungal functional groups based on whether they have genes encoding certain ligninolytic class II peroxidase enzymes, which oxidize lignin and polyphenolic compounds. To address these ideas, we used a litterbag study paired with fungal DNA barcoding to characterize fine root decay rates and fungal community composition at the landscape scale in northern temperate forests, and we estimated the genetic potential of fungal communities for litter decay using publicly available genomes. Fine root decay occurred more rapidly where fungal communities had a greater genetic potential for decay, especially of cellulose and hemicellulose. Fine root decay was positively correlated with ligninolytic saprotrophic fungi and negatively correlated with ECM fungi with ligninolytic peroxidases, likely because these saprotrophic and ectomycorrhizal functional groups had the highest and lowest genetic potentials for plant cell wall degradation, respectively. These fungal variables overwhelmed direct environmental controls, suggesting fungal community composition and genetic variation are primary controls over fine root decay in temperate forests at regional scales.
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Soil functioning is closely linked to the interactions between biological communities with the physical environment. Yet, the impact of plant community attributes on metabolic processes promoting soil nutrient cycling remains largely unknown. We hypothesized that the plant community acts as a regulating agent of nutrient mobilization in soils according to the phylogenetic and morpho-functional traits of plant species of which it is composed. Rhizosphere soils were collected in autumn and spring under 32 tree and shrub species in two Mediterranean mixed forests (four plots in each) located in southern Spain, and nine soil enzymatic activities related to C, N and P mobilization were assessed. Phylogeny and morpho-functional traits of plant species were recorded and their imprint in soil enzymatic activities across forests was determined. The results showed a plant phylogenetic signal for N mobilization in both forests, while it varied across forests for non-labile C and P mobilization. The plant phylogenetic signals were primarily driven by lineages that diversified through the Miocene, about 25 Myr ago. In addition, leaf traits and plant’s mycorrhizal type explained soil enzymatic activities independently from phylogeny. C and P mobilization increased under ectomycorrhizal plants, whilst enhanced N mobilization did occur under arbuscular mycorrhizal ones. The plant community composition led to a different carbon and nutrient mobilization degree, which in turn was mediated by distinct microbial communities mirroring differentiated resource-acquisition strategies of plants. Our results highlight the role of plant traits and mycorrhizal interactions in modulating carbon and nutrient cycling in Mediterranean mixed forest soils.
Mycorrhizae are mutualisms between plants and fungi that evolved over 400 million years ago. This symbiotic relationship commenced with land invasion, and as new groups evolved, new organisms developed with varying adaptations to changing conditions. Based on the author's 50 years of knowledge and research, this book characterizes mycorrhizae through the most rapid global environmental changes in human history. It applies that knowledge in many different scenarios, from restoring strip mines in Wyoming and shifting agriculture in the Yucatán, to integrating mutualisms into science policy in California and Washington, D.C. Toggling between ecological theory and natural history of a widespread and long-lived symbiotic relationship, this interdisciplinary volume scales from structure-function and biochemistry to ecosystem dynamics and global change. This remarkable study is of interest to a wide range of students, researchers, and land-use managers.
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Intrinsic soil properties have been shown to mediate the effects of ectomycorrhizal (ECM) fungi and their associated trees on soil organic matter (SOM) and nitrogen (N) cycling, but variation in the contribution of fungal communities to ECM effects across different forests remains uncertain. To investigate the potential role of fungal communities in driving observed variation in ECM effects, we characterized fungal community composition and function using DNA sequence variability of the ITS2 region of the fungal rRNA operon and measured chemical properties of forest floor leaf litter, soil organic horizon, and soil mineral horizons (0–5cm, 15–20 cm depth) beneath ECM-associated Oreomunnea mexicana focal trees. We sampled beneath focal trees in arbuscular mycorrhizal (AM)- and ECM-dominated stands within four adjacent watersheds that differed in underlying soil pH and fertility. We found that overall fungal community composition and the ratio of ECM to saprotrophic fungi differed between AM- and ECM-dominated stands in the lowest pH and fertility watershed but were similar between stand mycorrhizal types in the highest pH and fertility watershed. Patterns in fungal community composition and function aligned with patterns in N isotopic composition of forest floor leaf litter and mineral soil, which could reflect greater ECM transfer of N to the trees and greater contribution of hyphal biomass to SOM in the lowest pH and fertility watershed. Overall, our results suggest the potential for watershed-scale variation in soil pH and fertility to mediate fungal community contributions to variation in ECM effects on biogeochemical syndromes.
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The extent to which ectomycorrhizal (ECM) fungi enable plants to access organic nitrogen (N) bound in soil organic matter (SOM) and transfer this growth‐limiting nutrient to their plant host, has important implications for our understanding of plant–fungal interactions, and the cycling and storage of carbon (C) and N in terrestrial ecosystems. Empirical evidence currently supports a range of perspectives, suggesting that ECM vary in their ability to provide their host with N bound in SOM, and that this capacity can both positively and negatively influence soil C storage. To help resolve the multiplicity of observations, we gathered a group of researchers to explore the role of ECM fungi in soil C dynamics, and propose new directions that hold promise to resolve competing hypotheses and contrasting observations. In this Viewpoint, we summarize these deliberations and identify areas of inquiry that hold promise for increasing our understanding of these fundamental and widespread plant symbionts and their role in ecosystem‐level biogeochemistry.
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Significance We overcame the difficulty of disentangling biotic and abiotic effects on decomposition by using the largest field-based reciprocal transplant experiment to date. We showed that decomposition responses to climate depend on the composition of microbial communities, which is not considered in terrestrial carbon models. Microbial communities varied in their effects on both mass loss and types of carbon decomposed in an interactive manner not predicted by current theory. Contrary to the traditional paradigm, bacterial communities appeared to have a stronger impact on grassland litter decomposition rates than fungi. Furthermore, bacterial communities shifted more rapidly in response to changing climates than fungi. This information is critical to improving global terrestrial carbon models and predicting ecosystem responses to climate change.
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Soils contain more carbon than plants or the atmosphere, and sensitivities of soil organic carbon (SOC) stocks to changing climate and plant productivity are a major uncertainty in global carbon cycle projections. Despite a consensus that microbial degradation and mineral stabilization processes control SOC cycling, no systematic synthesis of long-term warming and litter addition experiments has been used to test process-based microbe-mineral SOC models. We explored SOC responses to warming and increased carbon inputs using a synthesis of 147 field manipulation experiments and five SOC models with different representations of microbial and mineral processes. Model projections diverged but encompassed a similar range of variability as the experimental results. Experimental measurements were insufficient to eliminate or validate individual model outcomes. While all models projected that CO2 efflux would increase and SOC stocks would decline under warming, nearly one-third of experiments observed decreases in CO2 flux and nearly half of experiments observed increases in SOC stocks under warming. Long-term measurements of C inputs to soil and their changes under warming are needed to reconcile modeled and observed patterns. Measurements separating the responses of mineral-protected and unprotected SOC fractions in manipulation experiments are needed to address key uncertainties in microbial degradation and mineral stabilization mechanisms. Integrating models with experimental design will allow targeting of these uncertainties and help to reconcile divergence among models to produce more confident projections of SOC responses to global changes.
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Global soils store at least twice as much carbon as Earth's atmosphere1,2. The global soil-to-atmosphere (or total soil respiration, RS) carbon dioxide (CO2) flux is increasing3,4, but the degree to which climate change will stimulate carbon losses from soils as a result of heterotrophic respiration (RH) remains highly uncertain5-8. Here we use an updated global soil respiration database9 to show that the observed soil surface RH:RS ratio increased significantly, from 0.54 to 0.63, between 1990 and 2014 (P = 0.009). Three additional lines of evidence provide support for this finding. By analysing two separate global gross primary production datasets10,11, we find that the ratios of both RH and RS to gross primary production have increased over time. Similarly, significant increases in RH are observed against the longest available solar-induced chlorophyll fluorescence global dataset, as well as gross primary production computed by an ensemble of global land models. We also show that the ratio of night-time net ecosystem exchange to gross primary production is rising across the FLUXNET201512 dataset. All trends are robust to sampling variability in ecosystem type, disturbance, methodology, CO2 fertilization effects and mean climate. Taken together, our findings provide observational evidence that global RH is rising, probably in response to environmental changes, consistent with meta-analyses13-16 and long-term experiments17. This suggests that climate-driven losses of soil carbon are currently occurring across many ecosystems, with a detectable and sustained trend emerging at the global scale.
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Symbiotic ectomycorrhizal fungi have received increasing attention as regulators of below-ground organic matter storage. They are proposed to promote organic matter accumulation by suppressing saprotrophs, but have also been suggested to play an active role in decomposition themselves. Here we show that exclusion of tree roots and associated ectomycorrhizal fungi in a boreal forest increased decomposition of surface litter by 11% by alleviating nitrogen limitation of saprotrophs–a “Gadgil effect”. At the same time, root exclusion decreased Mn-peroxidase activity in the deeper mor layer by 91%. Our results show that ectomycorrhizal fungi may hamper short-term litter decomposition, but also support a crucial role of ectomycorrhizal fungi in driving long-term organic matter oxidation. These observations stress the importance of ectomycorrhizal fungi in regulation of below-ground organic matter accumulation. By different mechanisms they may either hamper or stimulate decomposition, depending upon stage of decomposition and location in the soil profile.
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The ability of plant litter to adsorb water is important for wildland fire, hydrological, and biogeochemical processes. Variation in water adsorption has largely been attributed to physical differences across species, with the role of litter chemistry in moisture dynamics receiving little attention. We hypothesized that lower specific leaf area (SLA, cm2/g) and higher concentrations of hydrophobic lignin and lipid biomolecules would be associated with decreased litter water adsorption. Because plant biochemistry is tied to litter elemental and structural traits via biophysics and leaf economics, we expected to observe a suite of linked traits that were related to water adsorption, including element concentrations, carbon oxidation state, and energy concentration (ΔHc). In litter from 22 species, we observed greater than fourfold variation in the maximum amount of liquid water adsorbed (adsorption capacity, g/g) and in the rate at which dry litter adsorbed water vapor (adsorption rate, mg g−1 min−1); there was a significant positive relationship between adsorption capacity and adsorption rate. Broadly, litter with low SLA had a low carbon oxidation state, low oxygen and ash concentrations, and high concentrations of carbon, hydrogen, lignin, and lipids. The two metrics of water adsorption had significant negative relationships with concentrations of energy, lignin, carbon, and hydrogen, and positive relationships with litter SLA and carbon oxidation state. However, water adsorption was better predicted by combinations of SLA with chemical and energy traits. Several traits associated with decreased litter water adsorption, such as concentrations of lignin and energy, also directly influence some of the same ecosystem processes affected by litter moisture (e.g., decomposition, wildland fires). In particular, because plants with the hydrophobic traits identified in this study are more abundant in dry environments, our observations suggest a mechanism that could accentuate the influence of litter traits on ecosystem processes and which merits further research. Understanding the role of these traits in water adsorption could be used to help predict shifts in ecosystem function as plant communities reassemble as result of climate change as well as provide quantitative information on how plant species influence wildland fire dynamics.
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Forest soils store large amounts of carbon (C) and nitrogen (N), yet how predicted shifts in forest composition will impact long‐term C and N persistence remains poorly understood. A recent hypothesis predicts that soils under trees associated with arbuscular mycorrhizas (AM) store less C than soils dominated by trees associated with ectomycorrhizas (ECM), due to slower decomposition in ECM‐dominated forests. However, an incipient hypothesis predicts that systems with rapid decomposition – e.g., most AM‐dominated forests – enhance soil organic matter (SOM) stabilization by accelerating the production of microbial residues. To address these contrasting predictions, we quantified soil C and N to 1 m depth across gradients of ECM‐dominance in three temperate forests. By focusing on sites where AM‐ and ECM‐plants co‐occur, our analysis controls for climatic factors that co‐vary with mycorrhizal dominance across broad scales. We found that while ECM stands contain more SOM in topsoil, AM stands contain more SOM when subsoil to 1 m depth is included. Biomarkers and soil fractionations reveal that these patterns are driven by an accumulation of microbial residues in AM‐dominated soils. Collectively, our results support emerging theory on SOM formation, demonstrate the importance of subsurface soils in mediating plant effects on soil C and N, and indicate that shifts in the mycorrhizal composition of temperate forests may alter the stabilization of SOM. This article is protected by copyright. All rights reserved.
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The distribution of mycorrhizal associations across biomes parallels a distinct gradient of soil carbon (C) and nitrogen (N) stocks, raising the question of how mycorrhizal traits relate to ecosystem properties. Arbuscular mycorrhizal (AM) and ectomycorrhizal (EM) hosts and fungi employ contrasting strategies for N acquisition, which may manifest in differences in soil C and N pools and/or soil C:N. However, cross-biome comparisons are confounded with climatic and edaphic gradients as well as phylogenetic and functional trait distributions of component plant species. Here, we test emerging hypotheses that soil C, N and C:N are related to the dominance of EM trees within a temperate forest region where AM and EM trees largely coexist but vary in local abundance. To determine the importance of mycorrhizal type on soil C and N, we analysed data from c. 1,000 forest inventory plots in the eastern United States. For each plot, we quantified the dominance of trees with different mycorrhizal associations and accounted for potentially confounding variables including phylogeny (angiosperm or gymnosperm), leaf N, soil clay content and climate. We used hierarchical Bayesian models to determine how these variables explained the patterns of soil C and N in the forest floor and mineral soil layers. Increasing EM dominance was associated with higher C:N across all soil layers. This relationship remained even after accounting for tree phylogeny, leaf N content, soil clay content, temperature and precipitation, which were all important for explaining soil C:N. However, this mycorrhizal pattern of soil C:N was not related to increases in soil C content; rather, increasing EM dominance was associated with reductions in soil N. Synthesis. Our findings are consistent with the proposition that mycorrhizal associations are related to terrestrial ecosystem properties. The mycorrhizal effect on soil C:N may result from differences in how arbuscular mycorrhizal and ectomycorrhizal plants interact with their fungal symbionts, decomposers and organic matter, to sustain differential cycling of C and N. Alternatively, these patterns could arise from differential success of the two mycorrhizal types in contrasting soil conditions; both processes may occur simultaneously, leading to a self-reinforcing positive feedback. © 2018 The Authors. Journal of Ecology
Most tree roots on Earth form a symbiosis with either ecto‐ or arbuscular mycorrhizal fungi. Nitrogen fertilization is hypothesized to favor arbuscular mycorrhizal tree species at the expense of ectomycorrhizal species due to differences in fungal nitrogen acquisition strategies, and this may alter soil carbon balance, as differences in forest mycorrhizal associations are linked to differences in soil carbon pools. Combining nitrogen deposition data with continental‐scale US forest data, we show that nitrogen pollution is spatially associated with a decline in ectomycorrhizal vs. arbuscular mycorrhizal trees. Furthermore, nitrogen deposition has contrasting effects on arbuscular vs. ectomycorrhizal demographic processes, favoring arbuscular mycorrhizal trees at the expense of ectomycorrhizal trees, and is spatially correlated with reduced soil carbon stocks. This implies future changes in nitrogen deposition may alter the capacity of forests to sequester carbon and offset climate change via interactions with the forest microbiome. Responses of arbuscular and ectomycorrhizal trees to atmospheric nitrogen deposition.
Aim Trees associating with ectomycorrhizal (ECM) fungi typically occur in infertile soils and use nutrients more conservatively than arbuscular mycorrhizal (AM) trees. We hypothesized that ECM trees would have greater nutrient resorption (i.e., proportion of nutrients resorbed during leaf senescence) than AM trees. Location Global. Methods We synthesized nitrogen (N) and phosphorus (P) resorption data from 378 species from sub/tropical, temperate and boreal forests, including 43 studies where ECM and AM trees co‐occurred, and conducted a meta‐analysis. Additionally, we quantified N resorption in 45 plots varying in ECM‐AM tree abundances in the temperate deciduous forests of southern Indiana, USA. Results Overall, resorption patterns were driven primarily by mycorrhizal type, climate zone, and to a lesser degree, leaf habit. In the boreal forest, P resorption was 76% greater for ECM than AM trees (p < .05). In the sub/tropics, AM trees resorbed 30% more N than ECM trees. At the sites where AM and ECM trees co‐occurred, ECM trees resorbed more N in temperate forests (15% greater; p < .001) whereas AM trees tended to resorb more N in sub/tropical forests (by 29%; p = .08). Besides, deciduous ECM trees resorbed more N (10%) and P (15%) than deciduous AM trees, while evergreen ECM and AM trees did not differ. In the deciduous forests of Indiana, where ECM and AM trees co‐occurred, the relative abundance of ECM trees in a plot was positively correlated to plot‐scale N resorption (R² = .25, p = .001), indicating greater nutrient conservatism with increasing ECM‐dominance. Main conclusions Our results indicate that mycorrhizal association – in addition to other factors – is correlated with the degree to which trees recycle nutrients, with the strongest effects occurring for N resorption by temperate deciduous trees.