Download Mycorrhizal networks mediate overstorey

Ecology Letters, (2004) 7: 538–546
doi: 10.1111/j.1461-0248.2004.00605.x
REPORT
Mycorrhizal networks mediate overstoreyunderstorey competition in a temperate forest
Michael G. Booth
School of Forestry and
Environmental Studies,
Yale University, New Haven,
CT 06511, USA
E-mail: [email protected]
Abstract
In forests, common mycorrhizal networks (CMNs) often connect the roots of
neighbouring plants. Observations of material flows between hosts connected by CMNs
have given rise to the hypothesis that CMNs limit the negative effects of competition by
overstorey trees on seedlings recruiting underneath them. I conducted an experiment in a
temperate forest dominated by ectomycorrhizal conifers and hardwoods to isolate the
effects of CMNs on the growth and survival of four tree species that co-occur in the
understorey. Ectomycorrhizal networks had strong negative effects on the survival of an
arbuscular mycorrhizal species, Acer rubrum, and neutral effects on the survival of three
ectomycorrhizal species, Betula allegheniensis, Pinus strobus, and Tsuga canadensis. CMNs had
positive effects on the growth of at least one ectomycorrhizal species, P. strobus.
Interspecific differences in juvenile responses to CMNs may influence forest community
development, promoting coexistence of some tree species while limiting the success of
others.
Keywords
Common mycorrhizal networks, ecology, ectomycorrhiza, facilitation, forest succession,
plant competition.
Ecology Letters (2004) 7: 538–546
INTRODUCTION
Seedlings recruiting in forest understoreys often experience
severe resource limitations owing to size-asymmetric competition with overstorey trees (Grubb 1977). Generally,
foresters and ecologists consider light to be the single most
limiting resource with respect to the growth and survival of
juvenile trees (Shugart 1984; Oliver & Larson 1996), and
they explain patterns of secondary succession in terms of
speciesÕ shade-tolerances or light response curves (e.g.
Pacala et al. 1996). But a growing number of fertilization and
trenching experiments (reviewed in Coomes & Grubb 2000)
and studies of juvenile tree performance across natural
fertility gradients (Kobe et al. 1995; Walters & Reich 1997;
Bigelow & Canham 2002) confirm that many temperate and
tropical species respond positively to release from root
competition and increased belowground resources, even at
very low light levels. These results suggest that speciesÕ
shade tolerances are, to various degrees, contingent on local
water and nutrient availabilities (Chapin et al. 1987; Tilman
1988). Thus, species differences in juvenile responses to
both above- and belowground competition may influence
the development of forest communities over time.
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Common mycorrhizal networks (CMNs), wherein
mycorrhizal mycelia link compatible roots of the same and
different tree species, have been identified as potential
mediators of competition for both light and nutrients
(Newman 1988; Perry et al. 1989; Read 1997). Such networks
are common among forest canopy trees (Horton & Bruns
1998; Cullings et al. 2000) and between mature overstorey
trees and juvenile understorey plants (Visser 1995; Jonsson
et al. 1999; Kennedy et al. 2003). CMNs can occur over areas
up to several square meters (e.g. Sawyer et al. 1999; Redecker
et al. 2001) and are capable of redistributing limiting
resources among linked individuals (Newman 1988). For
example, a study of paper birch (Betula papyrifera) and Douglas
fir (Pseudotsuga menziesii) linked by ectomycorrhizal (ECM)
mycelia demonstrated a net carbon (C) transfer from paper
birch to Douglas fir equivalent to 10% of the net recipient’s
primary production when Douglas fir was shaded (Simard
et al. 1997a, but see Robinson & Fitter 1999). Similarly,
studies of nitrogen (N) transfer between plants connected by
ECM and arbuscular mycorrhizal (AM) networks (reviewed
in Simard et al. 2002 and He et al. 2003) have shown that N
moves in CMNs toward plants with high N demand relative
to soil N availability.
Mycorrhizal networks and plant competition 539
From such studies has emerged the hypothesis that
CMNs redistribute resources in plant communities and
offset interspecific competition by allowing C and nutrients
to flow along source-sink gradients, from resource rich
plants to resource poor ones (Perry 1998; Wilkinson 1998,
but see Fitter et al. 1999). If CMNs operate this way in
nature, networks between forest overstorey trees and
juveniles should increase the availability of resources to
the smaller trees and allow them to grow faster or survive
longer at understorey light levels. This mechanism could
prolong the time required for competitive exclusion of
compatible juvenile populations. Thus, interspecific differences in juvenile responses to CMNs could be early
influences on trajectories of forest community development.
Some evidence supports the hypothesis that CMNs
facilitate growth and survival of seedlings recruiting under
established plants (Horton et al. 1999; Onguene & Kuyper
2002), but no published study has manipulated CMNs
independently of other relevant factors like root interaction
in order to isolate the effects of mycorrhizal networks on
plant performance. Here I present the results of a large-scale
field experiment designed to elucidate how CMNs influence
the strength of competition between overstorey trees and a
suite of co-occurring seedlings in a temperate, ECM forest.
By applying a novel combination of trenching and screening
treatments to both ECM and AM seedlings, I was able to
distinguish the effects of overstorey competition on seedling
performance from the effects of seedling interactions with
CMNs. This allowed me to test directly the hypothesis that
CMNs promote the growth and survival of compatible
species recruiting in a forest understorey.
MATERIALS AND METHODS
Study site
I conducted this study over the 2002 and 2003 growing
seasons in a mature, mixed hardwood-conifer stand within
Great Mountain Forest (GMF), located in northwestern
Connecticut, USA (42N, 7315¢W). Average annual precipitation at GMF is 1200 mm, and mean monthly temperatures range from 7 C in January to 19 C in July (Winer
1955). The overstorey community in the 2 ha experiment
area is comprised of four ECM species (ordered by total
basal area, from greatest to least): Pinus strobus (eastern white
pine), Tsuga canadensis (eastern hemlock), B. allegheniensis
(yellow birch), and B. lenta (black birch). In the understorey,
2–4 m saplings of Fagus grandifolia (American beech) are also
common. At the time of the experiment, no AM tree species
were growing in the overstorey or as saplings. The soil
underlying the site is a sandy Enfield silt loam (an acidic
Inceptisol; Gonick et al. 1970) with 0–8% slope. Throughout the experiment area the soil typically has a 3 cm surface
layer of undecomposed needles and leaves underlain by a
2 cm layer of humic matter, a 5 cm A horizon, and a 50 cm
B horizon underlain by coarse sand and gravel. Ninety-five
per cent of roots observed in soil pits occurred in the top
30 cm of soil.
Study species
Seedlings of three ECM species, B. allegheniensis, P. strobus,
and T. canadensis, and one AM species, Acer rubrum (red
maple) were selected as subjects for this experiment. All four
species co-occur and are abundant in tree-fall gaps within
GMF. The ECM species represent a broad range of common
shade tolerance classifications, T. canadensis being the most
tolerant and B. allegheniensis being the most light demanding
(Burns & Hankala 1990). Acer rubrum is a moderately shade
tolerant species that responded to both light and nutrient
additions in the understorey of another temperate, mixed
conifer-hardwood forest (Beckage & Clark 2003).
All ECM seedlings used in the experiment were grown
from seeds. Seeds collected from single, regional sources of
each ECM species were stratified in moist sand at 4 C for
8 weeks and germinated in StyroBlock containers (Steuwe &
Sons, Corvallis, OR, USA) in March 2002. The seedlings
were maintained in a greenhouse for 8 weeks until planting.
Immediately before planting, 10 randomly sampled individuals of each ECM species did not appear to be colonized by
mycorrhizal fungi when examined under a dissecting
microscope. Maple seedlings with one pair of leaves were
harvested from a single tree-fall gap near the experiment
area in May 2002, transferred to StyroBlock containers, and
maintained for 2 weeks in the greenhouse until replanting.
Experimental design and sampling
In May 2002, seedlings of all four species were randomly
assigned and planted into four belowground ÔnetworkingÕ
treatments designed to decouple the effects of seedlingoverstorey root interactions and interactions between seedlings and overstorey mycorrhizal networks. Each speciestreatment combination was replicated once in each of forty
12 m · 12 m blocks (Fig. 1). Three seedlings were planted
in each replicate, and they were allowed to grow together
through the first growing season. At the end of the first
growing season, replicates with two or three remaining
seedlings were thinned to one, leaving whichever was largest.
ÔControlÕ seedlings were planted in the forest floor and
were able to interact directly with overstorey tree roots.
ECM control seedlings could be colonized by ECM
networks naturally occurring in the forest floor and soil,
whereas AM maple seedlings could not form CMNs with
overstorey trees. Seedlings subjected to a ÔNo Roots or
NetworksÕ treatment (NRoN-1) were planted within circular
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540 M. G. Booth
Figure 1 A typical block with a replicate of each species-treatment
combination, not drawn to scale. Replicates, indicated by the first
initial of each speciesÕ scientific name, were spaced 3 m apart.
Control seedlings were planted directly into the forest floor.
Seedlings in the No Roots or Networks 1 (NRoN-1) treatment
were planted into circular slit trenches, 0.5 m in diameter (solid
lines). Seedlings in the Common Mycorrhizal Network (CMN)
treatment were planted into Ônetworking cylindersÕ, 15 cm in
internal diameter (dashed lines, and illustrated in detail). Seedlings
in the NRoN-2 treatment were planted in networking cylinders and
also trenched. Species and treatments were assigned randomly to
positions within blocks, and blocks were distributed randomly in
the 2 ha stand.
slit trenches, 0.5 m deep · 0.5 m diameter, that prevented
all species from interacting with both overstorey roots and
mycorrhizal mycelia. Trenches were cut immediately prior to
planting in May 2002. To ensure that roots or mycorrhizal
networks did not reinvade trenches while allowing natural
flow of water in the soil around seedlings, the circular slits
were re-cut with a long-bladed landscaping shovel each
month from May through October in 2002 and from May
through August in 2003.
Seedlings in a ÔCMNÕ treatment were planted into custom
Ônetworking cylindersÕ (Fig. 1) that were designed to protect
seedlings from direct competition with overstorey tree roots
but allow external mycorrhizal hyphae to invade and form
CMNs with compatible ECM seedlings. Networking cylinders were fabricated from sections of PVC pipe (schedule
40) that had 15 cm internal diameters and were 20 cm deep
(Modern Plastics, Bridgeport, CT, USA). The walls of the
pipe segments were bored to 50% openness with a 1.5 cm
drill bit and were wrapped tightly with 44 lm stainless steel
mesh (TWP, Inc., Berkeley, CA, USA). Stainless steel mesh
wrappers were bonded to the PVC cylinders with Loctite
Hysol U-04L, a flexible, temperature- and moisture-resistant
urethane adhesive (Henkel CA, Avon, OH, USA). The
cylinders were fixed with bottoms cut from flat PVC sheets
(schedule 40) and routed to fit flush with the external
circumferences of the cylinders. Like the cylinder walls, the
bottoms were drilled to 50% openness and fixed with
44 lm stainless steel mesh to permit drainage.
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The cylindersÕ dimensions were selected to optimize the
amount of space that seedling roots would have to grow
without restriction and the distance external mycorrhizal
hyphae would have to travel through the cylinder to reach
seedling roots. Networking cylinders were installed in
experimental treatment blocks in March and April 2002,
and mycelia of overstorey mycorrhizal networks were
allowed to colonize cylinders for 6–8 weeks prior to
planting and the start of the experiment. To minimize soil
disturbance and maximize recolonization by external
mycelia, networking cylinders were inserted into formfitting holes that were excavated with PVC cores of identical
dimensions. Each installed cylinder was refilled with the
intact soil core and the surface organic matter removed
from its location. Upon harvesting seedlings from the
cylinders at the end of the experiment, no seedling’s roots
appeared to be constrained by container volume, and many
cylinders had visible rhizomorphs of mycorrhizal fungi on
their inner walls.
To control for cylinder effects other than the prevention
of direct root interactions, seedlings in a fourth treatment
group were planted into networking cylinders that were
prepared and installed as those in the CMN treatment and
then trenched like replicates in the NRoN-1 treatment. This
second ÔNo Roots or NetworksÕ treatment (NRoN-2) also
restricted seedling interactions with both roots and
mycorrhizal networks. If cylinders in the CMN treatment
retained moisture or increased nutrient mineralization rates
to the benefit of seedlings, these effects would be detectable
as a performance difference between seedlings in NRoN-1
and NRoN-2. Using both ECM and AM species and a novel
combination of trenching and root-screening methods, this
experimental design included almost all possible combinations of mycorrhizal networking and direct root interaction
between overstorey trees and recruiting seedlings. This
approach allowed me to decompose a complex interaction
in nature and delineate the different effects of root
competition and mycorrhizal networking on seedlings
recruiting in a mature forest.
Four indicators of seedling performance were monitored
to evaluate seedling responses to competition and mycorrhizal networking: mortality, height growth, leaf number, and
total leaf length. In the first month after planting, seedling
mortality was monitored weekly. Seedling deaths during this
period were considered artefacts of planting, and dead
seedlings were replaced. Thereafter, mortality was assessed
monthly during the growing seasons in 2002 (May to
October) and 2003 (May to August harvest). For the
purpose of survival analyses, I only considered data
collected in the second year after thinning treatment
replicates to one seedling each. Several B. allegheniensis and
A. rubrum seedlings were browsed by deer in the second year
of the experiment, and a few of these died. Mortality
Mycorrhizal networks and plant competition 541
resulting from deer browse was excluded from assessments
of treatment-related survivorship and considered separately.
Seedling heights, leaf numbers, and total leaf lengths were
recorded immediately after leaf-out in April 2003 and again
in the week before harvest at the end of August 2003. For the
deciduous species, final seedling height was used as the index
of growth in analysis. Seedlings of these species grew taller
throughout the experiment, and seedling height correlated
strongly and positively with both leaf number and total leaf
length. Final height, instead of height increment, was used
for both species because initial heights were relatively small
(2–4 cm). Seedlings that were browsed by deer and later
produced new shoots were excluded from height growth
comparisons. Pinus strobus and T. canadensis seedlings exhibited relatively little height growth over the course of the
experiment, but, on average, they multiplied their needle
numbers one to four times. Height did not correlate strongly
with needle number for either species, thus final needle
number was used as an alternative to height in the analysis of
conifer seedling growth. Final needle number was used
instead of needle production because initial needle numbers
were not recorded for every individual, although mean initial
needle numbers for each species were estimated by random
samples of 10 replicates at the time of planting.
In order to distinguish treatment effects on seedling
performance from possible effects of light, I assessed
light availability for individual replicates using hemispherical canopy photographs (Canham 1988). Over three
uniformly cloudy days in 1 week of August 2002, digital
photos were taken at 0.5 m directly above each replicate
using a Nikon CoolPix 990 camera body (3.4 mega pixel
resolution) with a Nikon FC-E8 fisheye lens (180)
(Nikon USA, Melville, NY, USA). Before taking each
picture, the camera was levelled and oriented northward.
The digital images were analysed using GLI/C software
(C.D. Canham, Institute of Ecosystem Studies, Millbrook,
NY, USA). Blue light thresholds for each photo were
determined manually, and the software calculated per cent
open sky, per cent of direct beam radiation, per cent
diffuse radiation, and gap light index (GLI, direct plus
diffuse radiation).
Statistical analysis
Seedling survival analyses were performed for each speciestreatment combination and species groups overall using the
Kaplan–Meier survival function estimator built into SPSS
statistical analysis software (SPSS, Inc., Chicago, IL, USA).
Differences between the estimated mortality risks associated
with treatments for each species and between estimated
mortality risks of species within each treatment group were
evaluated with a Breslow–Gehan–Wilcoxon test (Fleming &
Harrington 1981).
Treatment effects on seedling growth were investigated
by analysis of covariance (GLM procedure, SPSS) to
determine whether there were any interactive effects of
light (GLI) and treatment on growth. Finding no significant
effects of light or interactions between light and belowground treatments on seedling growth, I performed simple
one-way analyses of variance (ANOVA procedure, SPSS) to
detect belowground treatment effects on height or needle
number for each species. Within each species group,
treatments were assigned to homogenous subsets according
to Tukey honestly significant difference tests of all pairwise
treatment combinations.
RESULTS
Seedling survival, pooled across treatments, differed among
species. Pinus strobus experienced the highest total survivorship with no seedling mortality in the second year
(S[160] ¼ 1.0), and T. canadensis had the lowest survivorship
(S[160] ¼ 0.53). Betula allegheniensis and A. rubrum were
intermediate and had similar survivorships (S[160] ¼ 0.88,
S[160] ¼ 0.89, respectively). Within species, trenching and
mycorrhizal networking treatments influenced survival
(Fig. 2). Betula allegheniensis seedlings planted directly into
the forest floor (ÔControlÕ seedlings) experienced the highest
mortality over the course of the experiment (S[40] ¼ 0.57),
while those subjected to the ÔNo Roots or NetworksÕ
treatments, NRoN-1 an NRoN-2, had limited mortality
(S[40] ¼ 0.95, (S[40] ¼ 0.98, respectively), and no mortality
occurred among those protected from root competition but
permitted to form mycorrhizal networks with the overstorey
in the CMN treatment had no loss (S[40] ¼ 1.0). Like
B. allegheniensis, T. canadensis seedlings had the highest
mortality in the Control treatment (S[40] ¼ 0.23), intermediate mortality in the NRoN-1 (S[40] ¼ 0.50) and NRoN-2
(S[40] ¼ 0.63) treatments, and the least mortality when able
to form mycorrhizal networks in the CMN treatment
(S[40] ¼ 0.73). In contrast, A. rubrum experienced the least
mortality in the NRoN-1 (S[40] ¼ 0.98) and NRoN-2
(S[38] ¼ 0.97) treatments and had the highest mortality
rates in the Control (S[40] ¼ 0.83) and CMN (S[38] ¼ 0.79)
treatments.
Rank orders of speciesÕ estimated mortality risks varied
among treatments. In both the NRoN-1 and NRoN-2
treatments, the mortality risks of P. strobus, B. allegheniensis,
and A. rubrum were grouped into a statistically homogeneous
subset and were significantly lower than the mortality risk of
T. canadensis (P < 0.001). In the CMN treatment, the
mortality risks of P. strobus and B. allegheniensis were identical
and lower than the statistically equivalent mortality risks of
A. rubrum (P ¼ 0.003) and T. canadensis (P < 0.001). In the
Control treatment, the mortality risk of P. strobus was
significantly lower than the next greater mortality risk of
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542 M. G. Booth
Figure 2 Kaplan–Meier estimated survival curves and percent mortality for each species, by treatment.
A. rubrum (P ¼ 0.006). Acer rubrum had a lower mortality
risk than B. allegheniensis (P ¼ 0.005), and B. allegheniensis had
a lower mortality risk than T. canadensis (P ¼ 0.004).
Analysis of covariance revealed that, within the range of
gap light indices measured at the site (GLI, 2.5–14.5%),
neither light nor interactions between light and treatment
had significant effects on seedling growth [for A. rubrum:
P ¼ 0.100 (light), 0.339 (light · treatment); B. allegheniensis:
P ¼ 0.057, 0.163; P. strobus: P ¼ 0.266, 0.364; T. canadensis:
P ¼ 0.076, 0.167]. Trenching and networking treatments
alone explained significant variation in seedling growth
within species groups (Fig. 3). Betula allegheniensis height
growth responded positively to trenching, with and without
networking cylinders (P £ 0.003). Betula allegheniensis seedlings grown in networking cylinders alone also grew taller
than those in the Control treatment (P ¼ 0.005), but they
were not significantly different from seedlings in the
NRoN-1 (P ¼ 1.000) and NRoN-2 (P ¼ 0.964) treatments.
Relative to seedling height growth in the Control treatment,
A. rubrum seedlings grew taller in the NRoN-1, NRoN-2,
and CMN treatments (P £ 0.003), but, like B. allegheniensis,
differences among the non-control treatments were not
significant (P ‡ 0.136). Pinus strobus seedlings had fewer
needles in the Control treatment than in the NRoN-1
(P ¼ 0.002) and NRoN-2 (P ¼ 0.032) treatments and had
more needles in the CMN treatment than in the NRoN-1
(P ¼ 0.035) and NRoN-2 (P ¼ 0.002) treatments. Needle
numbers of T. canadensis seedlings trended higher in the
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trenching and CMN treatments compared to the Control
treatment but did not differ significantly among any of the
treatments (P ‡ 0.071).
The percentage of B. allegheniensis and A. rubrum seedlings
browsed by deer also varied across treatments (Fig. 4). No
Control seedlings of either species were browsed. Ten per
cent of B. allegheniensis seedlings in the NRoN-1 and
NRoN-2 treatments were browsed, while 22.5% of seedlings
in the CMN treatment were damaged by deer. Ten per cent
of A. rubrum seedlings also were browsed the NRoN-1 and
NRoN-2 treatments, but only 5% were browsed in the
CMN treatment.
DISCUSSION
Common mycorrhizal networks between overstorey trees
and juveniles growing in a forest understorey are hypothesized to offset to some degree the negative effects of sizeasymmetric competition on juveniles and facilitate their
growth and survival (Newman 1988; Perry et al. 1989; Read
1997). If this is true in my study system, seedlings of ECM
species should grow more or have higher survivorship in the
mycorrhizal networking treatment than in either of the
trenched treatments. At the same time, AM seedlings should
not respond more positively to the presence of ECM
networks, alone, than to the absence of both ECM networks
and roots. AM seedlings may even respond negatively to
ECM networks.
Mycorrhizal networks and plant competition 543
Figure 3 Mean height growth (B. allegheniensis and A. rubrum) and
needle number (P. strobus and T. canadensis) by treatment. Letters
indicate homogeneous subsets according to Tukey honestly
significant difference tests.
Consistent with my predictions, the ECM species
B. allegheniensis and T. canadensis experienced less mortality
in the CMN treatment than in either the NRoN-1 or
NRoN-2 treatments. However, the estimated mortality risks
of these species were not significantly less in the CMN
treatment. Thus, I could not reject the null hypothesis that
CMNs have no effect on mortality risks of ECM species.
Estimated mortality risks of B. allegheniensis and T. canadensis
seedlings were significantly less in both trenched and
networking treatments than in the Control treatment. These
differences suggest that root competition for belowground
resources limited seedling survival of these species.
Both ECM networks and direct interactions with overstorey roots had strong negative effects on both percent
survival and estimated mortality risk of the AM species,
A. rubrum. Moreover, the presence of networks alone in the
CMN treatment was responsible for as much seedling
mortality as were networks and root interactions combined
in the Control treatment. This result suggests that belowground resources limited the survival of A. rubrum and that
ECM mycelia are largely responsible for the negative effects
of the overstorey on A. rubrum in this system. It also puts
the neutral effects of CMNs on the survival of the ECM
species into an interesting perspective. Although mycorrhizal mycelia supported by overstorey trees clearly have the
ability to preempt resources in and remove them from
seedlingsÕ soil environments, recruits that are able join
CMNs appear not to lose resources to these networks.
I found evidence that CMNs had positive effects on the
growth of at least one species, P. strobus. Pinus strobus seedlings
in the CMN treatment had, on average, at least 12% more
total needles than seedlings in either of the trenching
treatments. Unlike the seedlings of other species used in this
experiment, P. strobus seedlings were planted after producing
a large fraction of the leaves that they had at the end of the
experiment. On average, seedlings had 34 needles immediately prior to planting. Assuming that they did not lose any
first-year needles, P. strobus seedlings in the CMN treatment
produced c. 23% more needles than seedlings in the NRoN-1
treatment and 33% more needles than seedlings in the
NRoN-2 treatment. The difference between needle production in the CMN treatment and the NRoN treatments can be
viewed as an estimate of the degree to which trees would
further negatively affect the growth of P. strobus seedlings if
the seedlings were not able to form CMNs. These results
contrast with the lack of differences in needle numbers of
T. canadensis seedlings among all treatments.
The effect of CMNs on the growth of B. allegheniensis was
less obvious. The mean height of non-browsed B. allegheniensis
seedlings in the CMN treatment was not significantly different
from the mean heights of non-browsed seedlings in the
NRoN-1 and NRoN-2 treatments. However, more than twice
as many B. allegheniensis seedlings were browsed in the CMN
treatment than in either of the trenching treatments. In a
separate study conducted at GMF, deer showed a preference
for B. allegheniensis juveniles that grew faster and had higher
shoot N concentration as a result of fertilization (Tripler et al.
2002). It is reasonable that deer browse in this study is also an
indicator of seedling height growth and nutrient status. A
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544 M. G. Booth
Figure 4 Percentage of seedlings browsed
by deer in the second growing season.
comparison of non-browsed seedling heights among treatments may thus significantly underestimate the effects of
CMNs on the growth of B. allegheniensis seedlings independent
of herbivory. If this is the case, the strong preference of deer
for A. rubrum seedlings in the NRoN-1 and NRoN-2
treatments but not in the CMN treatment also supports the
hypothesis that ECM networks confer no performance
benefits on AM species and even affect their growth
negatively. This observation raises a question of trade-offs.
If being connected to a CMN confers nutritional or growth
benefits to a seedling, does the probability of rapid establishment and eventual emergence in the canopy offset the risk of
being preferentially browsed by deer?
Whether CMNs between overstorey trees and juveniles
play a meaningful role in the development of forest
communities depends on whether these networks have
different effects on seedlings and saplings of different
species. This experiment shows that ECM mycelia supported
by the overstorey had deleterious effects on the survival and
possibly the growth of incompatible A. rubrum seedlings. At
the same time, mycorrhizal networks had neutral or positive
effects on the growth and survival of seedlings of all the
ECM species. Comparisons of the rank orders of survival
curves among treatments indicate that in the absence of
mycorrhizal networks A. rubrum would be a superior
competitor in the understorey compared with B. allegheniensis.
Thus, it is conceivable that mycorrhizal networks could
influence forest succession by limiting the abilities of AM
species to persist under and recruit into ECM overstorey
communities.
What is less clear is how CMNs differentially affect
compatible species growing in forest understoreys. In this
case, P. strobus was the only ECM seedling species to show
an unequivocal, positive growth response in the CMN
treatment compared with the two trenching treatments.
Betula allegheniensis might have shown a growth response to
CMNs in the absence of herbivory, and it is plain that
T. canadensis did not respond to the CMN or any other
treatment. Without a definite sense of how CMNs
influenced the growth of B. allegheniensis, and without a
comparable measure of growth for coniferous and decidu2004 Blackwell Publishing Ltd/CNRS
ous trees of this size, it is difficult to hypothesize about rules
that govern the relative degrees to which co-occurring
species benefit from CMNs.
One way to approach this problem is to think of CMNs
simply as increased resource supplies for compatible recruits.
Three mechanisms that have been proposed as modes by
which CMNs could facilitate seedling growth and survival
include (1) rapid mycorrhizal colonization of seedling roots
with highly advantageous but ÔexpensiveÕ fungi that seedlings
could not afford on their own (e.g. Simard et al. 1997b);
(2) the ability of seedlings in CMNs to access larger nutrient
pools than are available to them locally, and (3) the active
transport of N and other nutrients from resource-rich regions
of networks to resource-poor areas (Newmann 1988).
Juveniles of different species might respond to increased
nutrients made available by CMNs in the same fashion that
they respond to trenching or fertilization. Coomes & Grubb
(2000) concluded from their review of trenching experiments
in forests worldwide that effects of increased soil resources
on juvenile growth and survivorship are generally greater on
infertile than fertile soils, greater in treefall gaps than in
understorey conditions, and greater under lightly than deeply
shading overstorey trees. They further concluded that light
demanding species generally respond most rapidly to release
from belowground competition and that increased soil
resource availabilities allow light demanding species to persist
longer in deep shade (but see Catovsky & Bazzaz 2002).
These observations suggest that CMNs might confer greater
advantage on fast-growing, shade-intolerant species in the
understorey and increase the time required for overstorey
trees to exclude these species. While the results of this
experiment do not support this hypothesis unequivocally,
they also do not rule it out.
Carbon flow along source-sink gradients from overstorey
trees to understorey seedlings has also been proposed as a
possible facilitation mechanism (Read 1997; Simard et al.
1997a; Perry 1998; Wilkinson 1998). Carbon transport in
CMNs does not seem to be directly analogous to either
increased light availability or release from root competition,
and more research is needed to understand if and how
different ecophysiological strategies and environmental
Mycorrhizal networks and plant competition 545
conditions influence the amount of carbon that moves in
CMNs and the degree to which net recipients respond to it.
The host-specificity and autecology of dominant
mycorrhizal fungi in a stand should also play an important
role in determining the probability that a seedling of a
particular species is able to participate in a CMN with
overstorey trees (Horton & Bruns 2001) and the efficiency
with which CMNs supply resources to all compatible
seedlings (Finlay 1989). Ectomycorrhizal fungi are known to
exhibit a broad range of specificity with respect to plant
hosts (Molina et al. 1992). In the experiment presented here,
the strong growth response of P. strobus to CMNs relative to
the responses of other ECM species could reflect the
predominance of P. strobus in the forest overstorey if
mycorrhizal fungi associating with this species in this stand
are sufficiently host specific.
Mycorrhizal fungal community structure also may be
relevant when considering mycorrhizal networking in stands
of different ages. Communities of ectomycorrhizal fungi
have been shown to undergo succession as individual trees
and forests age, and it is speculated that Ôlate stageÕ fungi
command more carbon in order to build long-lived
structures and produce enzymes that mobilize organic
nutrients (Dighton & Mason 1985; Last et al. 1987).
Whether seedlings connected to CMNs incur a significant
C cost and whether this cost varies with fungal succession is
unknown. It is conceivable that a positive response to
trenching by ECM seedlings in a mature ECM forest could
reflect release from the obligation to provide C to relatively
expensive fungi and alternately being colonization by
disturbance selected fungi in the absence of CMNs.
However, if this were the case in the experimental stand
in GMF, ECM seedlings in the CMN treatment would have
fared worse, not indifferently or better, than those in the
trenched treatments. A separate study of mycorrhizal fungal
communities on the roots of seedlings grown in this
experiment using molecular methods is underway to address
questions of host-specificity and differences in mycorrhizal
fungal taxa between treatments.
The experiment at GMF shows that root competition for
belowground resources limits growth and survivorship of
recruiting tree seedlings in this stand, as has been shown for
a number forest communities (Coomes & Grubb 2000). At
the same time, it shows that ECM networks, independently
of direct root interactions, affect the performance of
understorey seedlings and may influence the trajectory of
forest development. While these networks had strong
negative effects on the survival of an incompatible species,
A. rubrum, they did not limit the survival of any ECM
species. Furthermore, access to mycorrhizal networks in the
CMN treatment increased needle production of P. strobus
during the experiment by 23–33% over production in the
trenching treatments. Thus, mycorrhizal networks may slow
the succession of incompatible species in a forest stand and
may buffer some compatible species against severe effects
of size-asymmetric competition. How compatible understorey species differ in their responses to mycorrhizal
networking, and whether CMNs meaningfully influence
forest community dynamics, probably depends on multiple
variables including light and belowground resource availabilities and the taxonomy and physiological ecology of
networked plants and fungi. A better understanding of the
mechanisms by which CMNs distribute C and other
resources among plants in controlled greenhouse experiments and more intensive tests of the effects of CMNs on
seedling performance in the field are required to explain the
ecological relevance of CMNs in forests.
ACKNOWLEDGEMENTS
I thank Oswald Schmitz, Kristiina Vogt, Tom Horton, and
Charlie Canham for their encouragement, stimulating conversations, and criticism of this work. I also thank Jason
Hoeksema, David Wilkinson and an anonymous reviewer for
thoughtful feedback that helped me to improve this
manuscript greatly. Mark Ashton, Tim Gregoire, Lisa
Curran, and Ofer Ovadia provided valuable consultations,
and Catherine Burns, Jason Grear, and Elizabeth Kalies were
generous with their field assistance and support. Miroslav
Kummel, Deborah Goldberg, Jim Bever, and David Perry
helped me to clarify my early thoughts on this subject. Star
Childs made this study possible by providing access to Great
Mountain Forest. This work is funded by the NSF (DEB0309225 and a Graduate Research Fellowship to M.G.
Booth), the Andrew W. Mellon Foundation (grant to P.M.S.
Ashton), Sigma-Xi, the New England Botanical Club, and
the Yale School of Forestry and Environmental Studies.
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Editor, John Klironomos
Manuscript received 11 February 2004
First decision made 22 March 2004
Manuscript accepted 6 April 2004