FEMS Microbiology Ecology, 92, 2016, fiw097
doi: 10.1093/femsec/fiw097
Advance Access Publication Date: 8 May 2016
Research Article
RESEARCH ARTICLE
Symbiont dynamics during ecosystem succession:
co-occurring plant and arbuscular mycorrhizal
fungal communities
David Garcı́a de León∗ , Mari Moora, Maarja Öpik, Lena Neuenkamp,
Maret Gerz, Teele Jairus, Martti Vasar, C. Guillermo Bueno, John Davison
and Martin Zobel
Department of Botany, Institute of Ecology and Earth Sciences, University of Tartu, Tartu 51005, Estonia
∗
Corresponding author: Department of Botany, Tartu Ulikooli Okoloogia ja Maateaduste Instituut, Lai 40, Tartu 51005, Estonia. Tel: +3727375835;
Fax: +3727375822; E-mail: [email protected]
One sentence summary: Arbuscular mycorrhizal (AM) fungi are efficient colonizers during succession and exhibit lower dispersal limitation than
plants. Allied with correlated community composition, this suggests that AM fungi are important drivers of plant communities.
Editor: Petr Baldrian
ABSTRACT
Although mycorrhizas are expected to play a key role in community assembly during ecological succession, little is known
about the dynamics of the symbiotic partners in natural systems. For instance, it is unclear how efficiently plants and
arbuscular mycorrhizal (AM) fungi disperse into early successional ecosystems, and which, if either, symbiotic partner
drives successional dynamics. This study describes the dynamics of plant and AM fungal communities, assesses correlation
in the composition of plant and AM fungal communities and compares dispersal limitation of plants and AM fungi during
succession. We studied gravel pits 20 and 50 years post abandonment and undisturbed grasslands in Western Estonia. The
composition of plant and AM fungal communities was strongly correlated, and the strength of the correlation remained
unchanged as succession progressed, indicating a stable dependence among mycorrhizal plants and AM fungi. A relatively
high proportion of the AM fungal taxon pool was present in early successional sites, in comparison with the respective
fraction of plants. These results suggest that AM fungi arrived faster than plants and may thus drive vegetation dynamics
along secondary vegetation succession.
Keywords: arbuscular mycorrhiza; chronosequence; covariation; dispersal limitation; plant-fungal interactions; species pool
INTRODUCTION
There is an increasing interest in interactions between aboveand below-ground communities when explaining biodiversity
patterns and ecosystem functioning (Bardgett and van der Putten 2014). The arbuscular mycorrhizal (AM) symbiosis is one of
the most ubiquitous interactions between plants and soil organisms. AM fungi (Phylum Glomeromycota) are an ancient group of
root symbionts that associate with >80% of plants in terrestrial
ecosystems (Smith and Read 2008). The symbiosis has multiple
impacts on plant communities (Moora and Zobel 2010), which
are linked to the ability of AM fungi to provide nutrients and
stress tolerance to plants (Smith and Read 2008).
Microcosm (Vogelsang, Reynolds and Bever 2006) and field
(Yang et al. 2014) experiments have shown that the presence
of AM fungi influences plant community composition and diversity, mostly due to changes in host plant growth and/or
Received: 6 January 2016; Accepted: 2 May 2016
C FEMS 2016. All rights reserved. For permissions, please e-mail: [email protected]
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FEMS Microbiology Ecology, 2016, Vol. 92, No. 7
phosphorus acquisition. Furthermore, plants preferentially allocate carbohydrates to the more beneficial symbionts (Bever et al.
2009; Kiers et al. 2011; Pendergast, Burke and Carson 2013), and
there is evidence that the identity and abundance of host plants
can influence AM fungal assemblages (Bever et al. 1996; Johnson
et al. 2004; Davison et al. 2015; Martı́nez-Garcı́a et al. 2015).
There has been a strong theoretical debate about the forces
determining plant-AM fungal relationships in natural systems
(Dickie et al. 2015). Hart, Reader and Klironomos (2001) put forward the so-called Driver (AM fungi determine plant community structure) and Passenger (AM fungal communities depend
on plants) Hypotheses. Zobel and Öpik (2014) suggested that
the Driver Hypothesis influences plant community changes during secondary succession, while the Passenger Hypothesis influences primary succession. These authors, in turn, added the
Habitat Hypothesis—that plant and AM fungal communities respond independently to the same environmental variability—
and noted that there may be no covariation between communities of plants and AM fungi. Understanding the dynamics of
plant and AM fungal communities is a key step in ecosystem
management, rehabilitation and restoration. For instance, disentangling whether AM fungal community composition drives
plant assemblages may help restoration ecologists to make decisions about inoculation with AM fungi in order to enhance the
recovery of plant diversity in abandoned arable fields or industrial wastelands (Maltz and Treseder 2015; Torrez et al. 2016).
The mutual relationships between plant and AM fungal communities at any given site may depend on the timing of arrival
of species within each group. Zobel and Öpik (2014) suggested
that plant establishment may be inhibited due to symbiont limitation when AM fungi arrive later. On the other hand, early arriving fungi may be limited due to the lack of host plants, though
they may persist in the soil as spores, where their presence can
provide favourable conditions for plant colonizers (Varga et al.
2015).
While dispersal of plants and the effect of dispersal limitation on plant communities is relatively well studied (Tamme
et al. 2013), knowledge about AM fungal dispersal is scarce. In
principle, AM fungi can be expected to possess low dispersal
capacity as they are hypogeous, producing hyphae and large
spores (0.03–1 mm) in the soil (Smith and Read 2008). Although
earlier studies have reported a scarcity or even absence of AM
fungi in early successional stages, followed by a gradual increase
in the number of spores and taxa, and in the degree of root colonization (Allen and Allen 1980; Allen 1988; Allen et al. 1992;
Titus, Whitcomb and Pitoniak 2007), more precise information
about the dispersal of AM fungi has only recently started to accumulate (Egan, Li and Klironomos 2014; Kivlin et al. 2014). To the
best of our knowledge, this study is the first attempt to directly
compare the arrival of plant and AM fungal taxa in successional
ecosystems.
The same holds true for the question of whether plant and
AM fungal communities covary in nature, which has received
little attention to date. This is surprising given that both theoretical and experimental studies have repeatedly addressed how
the relationships between plant and AM fungal species might
determine plant and AM fungal community assembly. Although
there are studies reporting variation in AM fungal communities among vegetation types or biomes (e.g. Lekberg et al. 2011;
Öpik et al. 2013; Martı́nez-Garcı́a et al. 2015), we are aware of only
two studies where small-scale covariation of plant and AM fungal communities have been explicitly studied in nature: Landis,
Gargas and Givnish (2004) reported a positive correlation in
richness and composition between plants and AM fungal
spore (altogether 18 taxa) communities; and Hiiesalu et al. (2014)
reported a positive correlation between small-scale plant and
AM fungal richness.
In this study, we addressed covariation in plant and AM fungal community composition and structure in a secondary vegetation succession. By comparing sites of varying successional
age, we were able to compare the arrival of taxa and the subsequent structural and compositional trajectories of plant and AM
fungal communities. The specific objectives of the study were:
(i) to describe the successional dynamics of plant and AM fungal communities, (ii) to assess the strength of correlation in the
composition of plant and AM fungal communities and (iii) to infer the relative efficiency of local dispersal among plants and AM
fungi during secondary succession.
MATERIALS AND METHODS
Study sites
The study was conducted on two of the largest islands in the
eastern Baltic Sea: Muhu and Saaremaa (Estonia). The climate
of the study area is mild-maritime, with 500–700 mm annual
precipitation and 17◦ C and –5◦ C mean temperatures in July and
January, respectively (Jaagus 1999). The soil is a rendzic leptosol, with a humus layer of 2–20 cm thickness, lying on Silurian limestone parent material (Pärtel et al. 1999). The vegetation represents alvar grasslands of the Festucetum alvarense type,
with a diverse low herbaceous plant community and scattered
juniper shrubs (Pärtel et al. 1999). Alvar grasslands have been
maintained for centuries by extensive livestock grazing (mostly
sheep) (Pärtel et al. 1999). However, these areas have also been
used for excavating limestone gravel, and whenever the gravel
pits are abandoned, secondary vegetation succession follows on
the bare soil cover.
We sampled successional series on Muhu and Saaremaa,
each represented by three stages, resulting in six study sites,
all within a matrix of alvar grasslands: young stages in gravel
pits abandoned around 1980 (in Koguva and Koorunõmme); intermediate stages in gravel pits abandoned around 1960 (in
Koguva and Ilpla) and mature undisturbed open grasslands (in
Nõmmküla and Lõo) (Table S1, Supporting Information). As far
as we know, the management history of the study sites has not
included any restoration schemes. The size of gravel pits varied
from ∼0.6 × 0.4 km to 1.4 × 0.4 km. Sample plots were always
located 30–50 m from the gravel pit margins. The distance between sites of young and old successional stages within islands
was 1–40 km, while the distance between sites on the different
islands was 50–100 km (Table S1, Supporting Information).
Sampling and analyses
At each study site, 10 vegetation plots were arranged at random
within a uniform vegetation area of ∼100 × 100 m. Sampling was
conducted in July 2014. Altogether, 60 plots of 1 × 1 m were sampled. One square meter plots are widely used in grasslands for
describing small-scale diversity patterns (Reitalu et al. 2014). In
each plot, the percent cover of each plant species was estimated.
Taraxacum spp., Hieracium spp. and Euphrasia spp. were identified
to genus level. At the centre of each 1 × 1 m plot, a 0.1 × 0.1 m
sub-plot was described, and sixty 10 × 10 cm soil core and plant
mixed roots samples were collected. Soil depth was 5 ± 4 cm.
Soil and roots for DNA extraction were carefully separated by
hand as quickly as possible following the procedure described in
Öpik et al. (2013). Root samples were dried for 24 h at 50˚C and
Garcı́a de León et al.
then stored dry at room temperature. Prior to DNA extraction,
roots were thoroughly mixed and ground in liquid nitrogen. A
total of 10 g of soil was collected from each soil core, dried with
silica gel and stored air-tight at room temperature. DNA was extracted from 70 mg of each dried and ground root sample using
the PowerSoil-htp 96-Well Soil DNA Isolation Kit (MO BIO Laboratories, Inc., Carlsbad, CA, USA) following Saks et al. (2014), and
5 g of each dry soil sample using the PowerMax Soil DNA Isolation Kit (MO BIO Laboratories, Inc., Carlsbad, CA, USA), according
to Gazol et al. 2016. To increase DNA yield, bead solution tubes
were shaken at 60◦ C for 10 min at 100 rpm in a shaking incubator. To remove traces of ethanol, samples were allowed to dry for
10 min at room temperature under the fume hood before adding
the final elution buffer. AM fungal DNA was amplified using the
SSU rRNA gene primers NS31 and AML2 (Simon, Lalonde and
Bruns 1992; Lee, Lee and Young 2008) and 454-pyrosequenced as
described in Saks et al. (2014).
Bioinformatics
Bioinformatic analyses were implemented following the analytical workflow of Davison et al. (2012). Sequence reads were
first quality-filtered: reads were only retained if they contained
the correct forward primer which were ≥170 bp long (excluding
primers and barcodes) and had an average quality score ≥25.
Longer sequences were trimmed to 520 bp. A total of 273 991
reads were obtained, among which 2.3% potentially chimeric
reads were detected and removed using USEARCH (Edgar 2010).
The chimera free dataset was subjected to a BLAST search
against the MaarjAM database of published Glomeromycota SSU
rRNA gene sequences in order to identify AM fungal reads (Öpik
et al. 2010; accessed April 2015). The MaarjAM database contains
AM fungal sequences covering the NS31/AML2 amplicon from
ecological and taxonomic publications. In April 2015, it contained a total 352 Virtual Taxa (VT). Criteria for a BLAST match
were as in Davison et al. (2012): sequence similarity ≥ 97%; an
alignment length not differing from the length of the shortest
query 454-read and reference database sequence by >5%; and a
BLAST e-value < 1e-50.
The BLAST against the MaarjAM database assigned 171 513
reads (63% of quality filtered reads) to 130 VT—including 18
singletons that were omitted from further analyses. Remaining reads were subjected to a further BLAST search against
the International Nucleotide Sequence Database with 90% sequence identity threshold. To avoid BLAST matches to low
quality sequences due to homopolymer errors, a gap penalty
(G-parameter = –3) was included. We identified 563 further
potential glomeromycotan sequences. In order to check their
identity, these sequences were subjected to phylogenetic analysis together with all VT type sequences from the MaarjAM
database (accessed April 2015). Potential glomeromycotan sequences were first clustered with 97% similarity using BLASTclust (Altschul et al. 1990). Four sequences from each cluster
containing >10 reads, were aligned together with the VT sequences and representatives of previously recorded VT from the
study site (664 sequences in total) using MAFFT (Osaka, Japan,
Kazukata Katoh) multiple sequence alignment web service implemented in JALVIEW version 2.8.2.b1 (Waterhouse et al. 2009).
A neighbour-joining phylogenetic analysis was run in TOPALi
v2.5 (Milne et al. 2009). Using this approach, we identified three
novel VT. Representative sequences for these VT were selected,
added to the reference dataset, and a BLAST run again as above
to generate a final sample by VT matrix. Two representative sequences of each VT from each site were submitted to European
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Molecular Biology Laboratory (EMBL) under the accession numbers LN899838-LN901090.
Statistical analyses
Variability in AM fungal and plant communities
Community composition (=richness or taxon incidence) and
structure (=relative abundance or taxon prevalence) were analysed and compared for plants and AM fungi. To compare AM
fungal richness and plant abundance and richness at different
successional stages, we used linear mixed models (LMM) and
Tukey post hoc-tests with successional stage as an explanatory
factor; site was included as a random factor to account for the
non-independence of sampling within sites (Zuur et al. 2009).
Our analysis was designed to investigate the effect of successional stage on symbiont communities, while we were not directly interested in the effect of island. The inclusion of site as
a random factor accounted for the variability attributable to island. The number of VT in the data set where samples were rarefied to the minimum number of reads per sample (282 reads
for soil samples and 556 for root samples) was used as a proxy
of AM fungal richness. Rarefied richness was computed using
the function rarefy in the vegan R package (Oksanen et al. 2015).
Taxon accumulation curves, in which it is indicated what effect
rarefaction had, are shown in Fig. S1 (Supporting Information).
The relative proportion of sequences corresponding to different
AM fungal VT was used as an indicator of relative taxon abundance in each sample and hence a semi-quantitative measure
of community structure. The richness and abundance of plant
species were estimated from species counts and estimates of
relative cover in 1 × 1 m plots.
Bray–Curtis dissimilarity was used as a measure of distance
between communities, and non-metric multidimensional scaling (NMDS) was used to visualize the separation of communities
using the function monoMDS from the vegan R package (Oksanen et al. 2015; R Core Team 2015). Indicator values for AM fungal
and plant species were inferred using the function indval from
the labdsv R package (Roberts 2015).
Assessing the strength of association between plant and AM fungal
communities
We used procrustean randomization tests to evaluate the
strength of relationships between AM fungal and plant communities. Procrustes analysis is an established statistical tool
for studying correlation among two or more datasets. However,
its application in ecology is relatively recent: only in recent
decades, randomization-based tests of procrustean correlation
(PROTEST) have been promoted as a more powerful alternative
to Mantel tests for studying covariation between communities
of organisms (Jackson 1995; Peres-Neto and Jackson 2001; Lisboa et al. 2014). We rotated the axes of the NMDS ordinations
of AM fungal communities in soil and roots to minimize the
sum of squared deviations in relation to plant community NMDS
axis scores. To test the significance of the procrustean correlation, we performed 9999 randomizations of procrustean associations. Procrustean association metrics—the residuals from
procrustean solutions—were used to assess differences in the
strength of plant-AM fungal association among successional
stages. As far as we know, there are not any straightforward ways
to implement a random factor in the procrustean randomization
test. Therefore, we attempt to interpret our results in light of this
limitation. Furthermore, analysis of the procrustean association
metrics was based on linear mixed modelling, which accounts
for the non-independence of sampling.
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FEMS Microbiology Ecology, 2016, Vol. 92, No. 7
Figure 1. Differences among successional stages in vegetation cover (a), plant richness (b), AM fungal richness per sample (number of virtual taxa, rarefied to minimum
number of sequences) in soil (c) and in roots (d). Different lowercase letters within panels indicate significant differences according to post-hoc multiple comparison
tests (Tukey).
Dispersal limitation of plants and AM fungi
In order to compare the relative dispersal limitation of plant and
AM fungal communities, the completeness of plant and AM fungal community assembly was estimated at each of the successional stages as the ratio of the number of taxa present in each
plot to the total number of taxa observed in the regional taxon
pool. We expected that the lower the percentage of the species
pool present in a given community, the stronger the dispersal
limitation. LMM and Tukey post-hoc analysis were used to assess the effect of successional stage and symbiont identity (AM
fungi or plant) on the completeness of community assembly.
RESULTS
Successional dynamics of plant and AM fungal
communities
Plant abundance increased along the successional gradient
(Fig. 1a). A total of 89 plant species were recorded (Table S2, Supporting Information), and the richness of plants increased from
young to intermediate grasslands (Fig. 1b; Fig. S2, Supporting Information).
Totals of 69 566 and 102 510 AM fungal reads (median length
514 bp) were recorded from 59 soil and 51 root samples (total
AM fungal read count 172 076). In total, 133 AM fungal VT were
identified (Table S3, Supporting Information). The richness of
AM fungi tended to increase from young to intermediate grasslands in soil and root (non-significant) samples (Fig. 1c and d).
Ordination revealed a clear contrast between the young and
later (intermediate and mature) successional stages in the structure of the plant and AM fungal communities (Fig. 2). A total of
30% of plant species were shared among all three stages (Fig. S3a,
Supporting Information). A total of 42% of VT in soil (Fig. S3b,
Supporting Information), 48% of VT in roots (Fig. S3c, Supporting Information) and 51% of all VT were shared among all three
stages (Fig. S3d, Supporting Information). A total of 99.5%, 99.6%
and 99.7% of VT in young, intermediate and mature stages, respectively, were shared among soil and roots (Fig. S4, Supporting
Information). The indicator plant species of intermediate stages
were Festuca ovina Hackel and Achillea millefolium L. The indicator
Garcı́a de León et al.
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Figure 2. Non-metric multidimensional scaling plot showing the community composition of plants (a), AM fungi in soil (b) and AM fungi in roots (c) in different
successional stages. FESRU: Festuca rubra, ACHMI: Achillea millefolium; FRAVE: Fragaria vesca. Only the species scores of indicator taxa (Table 1) are shown. Each data
point represents a plot. Stress values of the 3D analyses are indicated.
plant species of mature grasslands was Fragaria viridis Duchesne
(Table 1). There was no clear indicator plant species for the earliest successional stage. There was also no AM fungal indicator in
soil for the early successional stages. Claroideoglomus (VT56), was
indicative of AM fungal root communities in young grasslands
(Table 1). Glomus VT were dominant in all successional stages.
Covariation of plant and AM fungal communities
Procrustean randomization tests revealed highly significant covariation between plant and AM fungal communities in soil and
roots (Fig. 3a and b). Analyses of procrustean residuals indicated
that the strength of the relationship between plant and AM fungal communities in soil (LMM, F = 0.53, P = 0.64; Fig. 3a) and in
roots (LMM, F = 2.26, P = 0.25; Fig. 3b) did not change with successional age.
Dispersal limitation of plants and AM fungi
Our measure of community completeness represents the proportion of a local taxon pool that is present in a given successional stage. For instance, 100% means that all taxa in the local pool are present in a particular successional stage. Community completeness was calculated for each taxon and habitat (=soil or root) separately, and was higher among AM fungal than plant communities (Fig. 4; Fig. S5, Supporting Information), indicating that the proportion of taxa from the
available taxon pool present in individual samples was higher
among AM fungi than plants. The community completeness
of plant communities increased steadily during succession,
while the corresponding increase for AM fungal communities
in both roots and soil was steeper between the young and intermediate stages than between the intermediate and mature
stages (Fig 4).
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FEMS Microbiology Ecology, 2016, Vol. 92, No. 7
Table 1. Plant and arbuscular mycorrhizal fungal (AMF) indicator taxa.
Plants
Successional
stage
Indicator
Young
Intermediate
AMF in soil
Indicator
value
P
Indicator
value
Indicator
–
AMF in roots
p
–
Festuca ovina
Achillea millefolium
0.21
0.36
<0.01
0.04
Glomus VT130
Glomus VT301
0.35
0.5
0.01
0.03
Fragaria viridis
0.65
0.02
Glomus VT149
0.48
0.04
Mature
Indicator
Indicator
value
p
Glomus VT 92
Claroideoglomus VT56
Glomus VT105
0.95
0.83
0.86
0.03
0.04
0.04
–
Glomus VT186
Glomus VT214
0.43
0.86
0.04
0.02
Figure 3. Histogram of the procrustean residuals calculated by rotating the axes of an NMDS ordination of AM fungal communities in soil (a) and roots (b) such that
the sum of squared deviations from the axis scores of a NMDS ordination of plant communities is minimized.
DISCUSSION
Mutual relationships between plant and AM fungal communities have been addressed experimentally, but very little is known
about their covariation in nature. Our study revealed strong correlations between plant and AM fungal communities and that
the strength of the correlation remained stable during secondary
succession, despite a major change in plant community structure. Our results support the view that AM fungi are efficient colonizers of successional sites and, as such, might drive the successional dynamics of their host plants.
Garcı́a de León et al.
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Figure 4. The proportions (%) of taxa present in each plot relative to the total number of taxa observed for all successional stages on each island (regional taxon pool)
for plants (solid line), arbuscular mycorrhizal (AM) fungi in soil (dashed line) and AM fungi in roots (dotted line). Community completeness is a relative measure that
was calculated for each taxon and habitat (=soil or root) separately.
Successional dynamics of plant and AM fungal
communities
Plant cover and richness increased along the successional gradient as described elsewhere (Pickett, Cadenasso and Meiners
2012). AM fungal richness increased as well. Early AM fungal
colonizers such as Glomus spp. and Claroideoglomus spp. were
followed by other Glomus spp. in the later successional stages.
In a 2-year pot experiment, López-Garcı́a et al. (2014) found
that Diversisporaceae were early colonizers (R-strategists), that
Claroideoglomus spp. became dominant in the mid-stage and
that various Glomeraceae became dominant during the midto-late stage. It is worth noting that some AM fungal taxa
found by López-Garcı́a et al. (2014) were also found in our
study (Claroideoglomus VT56 and Glomus VT105 early and midsuccessional stages, Glomus VT149 late successional stage). Furthermore, Martı́nez-Garcı́a et al. (2015), studying primary succession over a much longer time scale, found that representatives of Glomeraceae, Archaeosporaceae, Diversisporaceae and
Acaulosporaceae predominated in the early successional stages
and that members of Glomeraceae persisted into the later
stages.
Strength of relationships between plant and AM fungal
communities
Correlation between plant and AM fungal communities was
strong, suggesting that an increase in the abundance or richness
of one partner is likely to be associated with predictable changes
in the counter-partner. This result is consistent with those of
Landis, Gargas and Givnish (2004) and Hiiesalu et al. (2014), who
reported that small-scale plant richness was reflected in AM
fungal richness, both in soil and in roots. However, there is no
previous information about the relatedness of plant community
and AM fungal community composition in roots. Correlation between plant and AM fungal communities may be related to preferential carbon allocation by plants to the more beneficial fungal
partners (Kiers et al. 2011) and to the differential effects of AM
fungal taxa on particular plant partners (Uibopuu et al. 2012).
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FEMS Microbiology Ecology, 2016, Vol. 92, No. 7
Dispersal limitation in both AM symbiosis partners
FUNDING
The share of regionally available taxa represented in local taxon
pools was higher among AM fungi than among plants, and increased more rapidly during succession, suggesting relatively
more efficient dispersal among AM fungi than plants. This suggests that AM fungi are overall relatively efficient colonizers,
although early successional AM fungal communities also appeared dispersal limited to a certain degree. Our results are consistent with those of Lekberg et al. (2011), who found that local
patterns of AM fungal communities were largely driven by environmental conditions rather than dispersal limitation. Davison
et al. (2015) showed that many AM fungal VT are widespread, although the dispersal underlying this pattern probably occurred
over geological time scales. The present study shows that local
dispersal of AM fungi may happen over successional time scales.
Efficient AM fungal dispersal ability may, on one hand, mean
that the development of AM fungal communities could be
slowed by host limitation (e.g. Hausmann and Hawkes 2010;
Silva et al. 2014; Davison et al. 2016). On the other hand, if AM
fungal propagules temporarily persist in the absence of suitable
hosts, their presence may improve the local environment for arriving plant partners. Evidence from other studies has shown
that the existence of suitable symbiont communities facilitates
the performance of establishing plants (Williams, Ridgway and
Norton 2011; Uibopuu et al. 2012; Torrez et al. 2016).
This work was supported by the Estonian Research Council [
IUT 20-28], the Estonian Science Foundation [ 9050, 9157] and
the European Regional Development Fund (Centre of Excellence
EcolChange).
CONCLUSION
Our findings demonstrate that plant and AM fungal community
composition and structure are strongly correlated at small spatial and temporal scales. Despite the previously assumed low
dispersal capacity of AM fungi, they appear to arrive earlier than
plants during vegetation succession. Our study provides field evidence that AM fungi are successful colonizers of disturbed sites
and may thus drive plant community composition and diversity
during succession. In this study, we described the pattern of successional dynamics, and found some support for the Driver Hypothesis. While this study was not designed to provide a mechanistic explanation for the correlation of plant and AM fungal
communities, we envisage that future studies may attempt to
identify the mechanisms underlying the relationship.
DATA ACCESSIBILITY
Two representative sequences of each virtual taxon from each
site were submitted to the archive of EMBL under accession
numbers LN899838-LN901090.
SUPPLEMENTARY DATA
Supplementary data are available at FEMSEC online.
ACKNOWLEDGEMENTS
Preparatory procedures for 454 sequencing were performed by
BiotaP Ltd (Tallinn, Estonia).
AUTHORSHIP
MM, MÖ, JD and MZ conceived and designed the study. TJ, MG
and LN collected data. DG, GB, JD and MV analysed data. DG and
MZ wrote first draft of the manuscript and all co-authors contributed to revisions.
Conflict of interest. None declared.
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