Ecology, 84(9), 2003, pp. 2292–2301
q 2003 by the Ecological Society of America
VARIATION IN PLANT RESPONSE TO NATIVE AND EXOTIC
ARBUSCULAR MYCORRHIZAL FUNGI
JOHN N. KLIRONOMOS1
Special Feature
Department of Botany, University of Guelph, Guelph, Ontario, Canada N1G 2W1
Abstract. High variability in plant-growth response to the presence of different mycorrhizal fungi can be a major determinant of local plant species diversity. Multiple species
of arbuscular mycorrhizal fungi can coexist in terrestrial ecosystems, and co-occurring
plants can differ in their response to colonization by these different fungi. However, the
range of mycorrhizal plant-growth responses that can occur within communities has not
been determined. In the present study, I crossed a large number of plant and fungal species
that co-occur to determine the range of responses that can exist within an ecosystem. I also
crossed exotic fungal isolates vs. local plant isolates and local fungal isolates vs. exotic
plant isolates to determine whether the range of plant growth responses differs when using
foreign genotypes. The data indicate that plant growth responses to mycorrhizal inoculation
within an ecosystem can range from highly parasitic to highly mutualistic. In this study,
the direction and magnitude of the response depended on the combination of plant and
fungal species. No plant did best with the same fungal isolate. The range of responses was
greatest when using local plants and fungi. Whereas parasitic and mutualistic responses
were also detected when using foreign plant or fungal genotypes, the range of responses
was significantly reduced, as was the relative frequency of positive responses. Overall, this
study suggests that, within ecosystems, arbuscular mycorrhizal fungi can function along a
continuum from parasitism to mutualism, and that extreme responses are more common
when using locally adapted plants and fungi. This high variation in plant growth response
may be a large contributor to plant species coexistence and the structure of plant communities.
Key words:
exotic; mycorrhiza; native; plant–microbe interactions; soil ecology.
INTRODUCTION
Arbuscular mycorrhizal fungi (AMF) (Phylum
Glomeromycota) are symbionts that infect the roots of
most terrestrial plants, and provide their hosts with a
wide variety of soil resources in exchange for photosynthate (Smith and Read 1997). The interaction between plants and AMF has traditionally been regarded
as a mutualism, in that both partners benefit from the
association. AMF are obligate biotrophs, so they typically gain by interacting with plants (Smith and Read
1997). However, recent evidence indicates that the
costs and benefits of maintaining a symbiosis with
AMF can differ significantly for plants, and the resulting plant responses can vary widely (Powell et al.
1982, Jensen 1984, Haas et al. 1987, Raju et al. 1990,
Streitwolf-Engel et al. 1997, van der Heijden et al.
1998a, Klironomos 2000). Since it is possible for AMF
to confer high costs on plants, it is not appropriate to
assume that AMF always stimulate the growth of plants
in natural ecosystems. Plant growth responses may
range from positive (mutualism) to neutral (commensalism) and even to negative (parasitism), so the symbiosis should more accurately be defined as a continManuscript received 11 July 2002; revised 14 October 2002;
accepted 16 October 2002. Corresponding Editor: M. Parker. For
reprints of this Special Feature, see footnote 1, p. 2256.
1 E-mail: [email protected]
uum from parasitism to mutualism (Johnson et al.
1997).
A better understanding of the factors that influence
the positioning of AMF along the parasitism–mutualism continuum would lead to a better appreciation of
the roles of AMF in natural ecosystems. Whether plants
benefit from the association depends on a number of
factors, including the genotypes of the organisms involved, and the environmental conditions under which
they interact. A significant amount of research has focused on the influence of environmental conditions,
mainly the availability of nutrients (Habte and Manjunath 1991, Koide 1991, Hetrick et al. 1992). Also,
we have made significant progress in our understanding
of what plant taxa are likely to form the symbiosis
(Harley and Harley 1987, Newman and Reddell 1987),
and to some degree, which will most likely require
AMF to successfully establish and compete for nutrient
resources (Janos 1980, Allen and Allen 1984, 1990,
Miller 1987). However, very little is known about the
effects of AMF genotype on plant growth, even though
it has been recognized that, everything else being
equal, AMF taxa can differ significantly in their growth
strategies (Hart and Reader 2002) and in their influence
on plant growth and development (Sanders and Fitter
1992, Streitwolf-Engel et al. 1997, van der Heijden et
al. 1998a).
2292
September 2003
UNDERGROUND PROCESSES
of nonmycorrhizal controls. I selected 10 plant species
that coexist within the old-field community and crossed
each one with one of 10 AMF species that also coexist
at the same field site. To determine the magnitude of
variation in growth response that is possible with a
single AMF species, I also inoculated one AMF isolate
onto each of 64 plant species. Finally, my final objective was to assess whether the source of AMF is an
important determinant of host response, because it is
currently not known if exotic AMF are as effective as
locally adapted isolates. To determine this I grew (a)
home plants with home AMF, (b) home plants with
foreign AMF, and (c) foreign plants with home AMF.
MATERIALS
AND
METHODS
Plant material
The 64 plant species that were used in this study are
listed in Table 1. These plants coexist in an old-field
community at the LTMRS, University of Guelph
(438329300 N, 808139000 W). Seeds were collected during the growing seasons of 1997–1999 and they were
then stored at 48C until ready to be used in experiments.
Only 10 of these species were used in Experiment 1
(see list in Table 1). For these 10 species, additional
seeds were also collected from various other locations
throughout southern Ontario and Quebec to test for
differences among ‘‘home’’ and ‘‘foreign’’ plants.
‘‘Home’’ plants are those that originated from the
LTMRS. ‘‘Foreign’’ plants are those that originated
from other locations. The remaining plant species listed
on Table 1 were used only in Experiment 2, which
required only ‘‘home’’ material.
Fungal material
AMF species that were used in this study are listed
in Table 2. The 10 AMF species were isolated from
the LTMRS (referred to as ‘‘home AMF’’), and also
from various other locations (referred to as ‘‘foreign
AMF’’). Home AMF were isolated from field soil by
first allowing the AMF to sporulate in trap cultures
containing Allium porrum L. cv. Giant Musselburgh,
and then using single AMF spores to start single species
cultures (Brundrett 1996). Some of the foreign AMF
were also isolated in the same way from foreign meadow or grassland ecosystems, whereas others purchased
from the INVAM culture collection. For a period of
two years prior to setting up the experiments described
below, all AMF were grown in dual pot culture with
the host Allium porrum under similar greenhouse conditions. During that time, AMF were subcultured at
three month intervals to keep the cultures clean and
viable. All AMF are stored in the University of Guelph
(LTMRS) culture collection.
Experimental set-up and design
Experiment 1.—This experiment was set up using a
factorial design of 11 AMF 3 10 plants 3 3 sources
Special Feature
Although AMF differ in their abilities to influence
plant growth, it is currently not possible to categorize
them along the parasite–mutualist continuum because
not all infected plants seem to do ‘‘best’’ with the same
AMF (Sanders and Fitter 1992, van der Heijden et al.
1998a, Kiers et al. 2000, Klironomos 2000). Even when
a few co-occurring plant and AMF taxa are studied,
there is a strong interaction between plant and AMF
taxa in plant growth response (Sanders and Fitter 1992,
van der Heijden et al. 1998b). Terrestrial ecosystems
contain many AMF and plant species that coexist in
communities (Johnson et al. 1991, Allen et al. 1995,
Sanders et al. 1996, Helgasson et al. 1998, Picone 2000,
Ergeton-Warburton and Allen 2000), so the influence
of AMF on growth of plants may be very complex.
To date, there is little appreciation of the range of
plant-growth responses that can occur within any AMF
community. Yet, such information would be valuable
for the development of plant community models because the variation in AMF–host response within a
community is believed to be a driving force behind the
structuring of AMF and plant communities (Grime et
al. 1987, Bever et al. 1996, van der Heijden et al.
1998b, Hartnett and Wilson 1999, Marler et al. 1999,
Smith et al. 1999). Ecological studies on plant–AMF
interactions have typically taken one of three approaches when choosing AMF inoculum for experimentation.
The first approach has been to use AMF inoculum from
foreign soils, usually isolates that have been stored in
a culture collection. The benefit of this approach is that
AMF can be accessed very quickly, but unfortunately
interactions between plants and ‘‘foreign’’ AMF may
have little relevance to the interactions that occur locally, and observed responses may not represent the
suite of responses that plants would normally encounter
at ‘‘home.’’ A second approach has been to use local,
but ‘‘whole-soil’’ inoculum. Whereas this is more appropriate than the first option, it does not provide information on the effects and responses of individual
fungal taxa. The third approach has been to use multiple
local AMF, but this rarely occurs because of the time
and resources required to successfully isolate and culture individual AMF from the field. Even when this
third approach is taken, a small number of isolates are
typically compared.
The present study was designed to answer a number
of questions related to variation in plant-growth response to AMF. The research was conducted with plants
and AMF from an old-field plant community within the
Long-Term Mycorrhiza Research Site (LTMRS), which
is located at the University of Guelph, Ontario, Canada.
This site was chosen because a large number of AMF
have been isolated and maintained in culture (van der
Heijden et al. 1998b, Klironomos 2000). First, I wanted
to determine whether mutualistic interactions are more
common than parasitic interaction between plants and
AMF that coexist in communities. This was done by
comparing the growth of mycorrhizal plants with that
2293
Special Feature
2294
JOHN N. KLIRONOMOS
of origin. The AMF factor consisted of one of 10 AMF
species or the non-AMF control (Table 2). The plant
factor consisted of one of 10 plant species (Table 1).
The source of origin factor consisted of one of either
(a) home AMF and home plants, (b) foreign AMF and
home plants, or (c) home AMF and foreign plants. Each
treatment combination consisted of 10 replicated units,
for a grand total of 3300 experimental units. Each unit
was positioned in a completely randomized design on
benches in a greenhouse. The experiment ran from May
through August 1999 under ambient light conditions,
23.7:18.48C mean day:night temperatures, and 50.2:
71.4% mean day : night relative humidity.
Each experimental unit consisted of a pot (15 cm
diameter 3 60 cm length) containing a sterile soil/silica
sand mix, AMF inoculum, and an individual plant. The
sandy loam soil was collected from the LTMRS (total
N 5 83.1 mmol/kg; total P 5 6.2 mmol/kg; percentage
of organic matter 5 6.1). It was mixed together with
silica sand at a 1:1 ratio, autoclaved, and then added
to individual pots. At a depth of 2 cm below the surface
of the soil, we added a band of AMF inoculum with a
mass of 1 g. This inoculum was composed of sheared
Allium porrum roots (precolonized by one of the AMF
isolates) and ;100 spores. The nonmycorrhizal experimental units received an equal total amount of uncolonized Allium porrum roots. To correct for possible
differences in microbial communities, each experimental unit received a 50-mL filtered washing comprised of microbial extract from every AMF isolate
used (Koide and Li 1989). Plant seeds were germinated
in a growth chamber at 208C on moist filter paper.
Individual seedlings were then transferred to the pots.
We initially added two seedlings, but after one week
we removed one plant. The remaining plant in each pot
was left to grow for a period of 16 weeks. All plants
were watered every two days or as needed with deionized water. They were also fertilized once per week
with a modified Long-Ashton Nutrient solution (half
strength P; Hewitt 1966).
Experiment 2.—This experiment was set up using a
factorial design of 2 AMF 3 64 plant species. The AMF
factor consisted of either the addition of Glomus etunicatum from the LTMRS or a nonmycorrhizal control.
The 64 plant species are listed in Table 1, and they all
originated from the LTMRS. Each treatment combination consisted of 10 replicated experimental units.
There was a total of 1280 experimental units, each
randomly positioned in a greenhouse for the duration
of the experiment. The experiment ran from May
through August 2000 under ambient light conditions,
24.3:19.58C mean day : night temperatures, and 53.1:
74.5% mean day : night relative humidity. The construction of experimental units was similar to those
described for Experiment 1. Plants were allowed to
grow for 16 weeks. They were watered every two days
or as needed with deionized water, and fertilized once
TABLE 1.
Ecology, Vol. 84, No. 9
Plant species used in Experiments 1 and 2.
Plant species
1. Achillea millefolium L.
2. Agrostis gigantea Roth.
3. Agrostis scabra L.
4. Apocynum cannabinum L.
5. Asclepias syriaca L.
6. Asparagus officinalis L.
7. Aster novae-angliae L.
8. Aster lanceolatus Willd.
9. Aster lateriflorus (L.) Britton.
10. Bromus inermis Leysser
11. Carex aurea Nutt.
12. Carex flava L.
13. Carex flacca Schreber.
14. Carex granularis Muhl.
15. Centaurea jacea L.
16. Cerastium vulgatum L.
17. Chenopodium ambroisioides L.
18. Chrysanthemum leucanthemum L.
19. Cichorium intybus L.
20. Circium arvense (L.) Scop.
21. Circium vulgare (Savi) Tenore.
22. Convolvulus arvensis L.
23. Coronilla varia L.
24. Dactylis glomerata L.
25. Daucus carota L.
26. Echium vulgare L.
27. Erigeron philadelphicus L.
28. Erigeron strigosus Muhl.
29. Fragaria virginiana Duchesne
30. Galium mollugo L.
31. Galium palustre L.
32. Geum aleppicum Jacq.
33. Hieracium auranticum L.
34. Hieracium pilosella L.
35. Hieracium lachenalii C. Gmelin.
36. Hypericum perforatum L.
37. Juncus dudleyi (Weieg.) F. J. Herm.
38. Linaria vulgaris Miller.
39. Medicago lupulina L.
40. Oenothera biennis L.
41. Oenothera perennis L.
42. Panicum lanuginosum Elliott.
43. Phleum pratense L.
44. Plantago lanceolata L.
45. Poa compressa L.
46. Poa pratensis L.
47. Potentilla recta L.
48. Prunella vulgaris L.
49. Ranunculus acris L.
50. Rudbeckia hirta L.
51. Rudbeckia serotina Farw.
52. Satureja vulgaris (L.) Fritsch.
53. Silene vulgaris (Moench) Garcke.
54. Solidago canadensis L.
55. Solidago graminifolia L.
56. Solidago nemoralis Aiton.
57. Solidago rugosa Miller.
58. Taraxacum officinale Weber ex Wiggers.
59. Tragopogon pratensis L.
60. Trifolium pratense L.
61. Trifolium repens L.
62. Veronica officinalis L.
63. Vicia cracca L.
64. Viccia sativa L.
Used in
experiment no.
2
1,
2
2
2
2
1,
2
2
1,
2
2
2
2
2
2
2
1,
2
2
2
2
2
2
1,
2
2
2
1,
2
2
2
2
2
2
2
2
2
2
1,
2
2
2
1,
2
2
2
2
2
1,
2
2
2
1,
2
2
2
2
2
2
2
2
2
2
2
2
2
2
2
2
2
2
2
2
UNDERGROUND PROCESSES
September 2003
TABLE 2.
2295
Fungal species used in Experiments 1 and 2.
Home isolate
Acaulospora denticulata Sieverding and Toro
Acaulospora morrowiae Spain & Schenck
Gigaspora margarita Becker & Hall
Gigaspora rosea Nicolson & Schenck
Glomus intraradices Schenck & Smith
Glomus etunicatum Becker & Gerdemann
Glomus geosporum (Nicolson & Gerdemann) Walker
Glomus mosseae (Nicolson & Gerdemann) Gerdemann & Trappe
Scutellospora calospora (Nicol. & Gerd.) Walker & Sanders emend.
Koske & Walker
Scutellospora pellucida (Nicolson & Schenck) Walker & Sanders
emend. Koske & Walker
Guelph011
Guelph020
Guelph035
Guelph064
Guelph004
Guelph009
Guelph017
Guelph041
Guelph022
INVAM: CL 139-3
INVAM: NC 148
INVAM: NC 175
INVAM: KS 885
Guelph001
Guelph005
INVAM: PA 126
Guelph004
INVAM: NC 153
1
1
1
1
1
1, 2
1
1
1
Guelph051
INVAM: WV848B-1
1
corrhizal plants was less than nonmycorrhizal controls,
then mycorrhizal dependency 5 (21 1 [Sa/bn]) 3
100%. ‘‘Mycorrhizal species sensitivity’’ refers to the
variation in plant growth response when associated
with different AMF (van der Heijden 2002). For each
plant species it was calculated as the coefficient of
variation on the dry mass in response to different AMF
treatments (van der Heijden 2002).
RESULTS
Experiment 1
At the time of harvest, all plants growing in the AMF
treatments were infected by fungal hyphae and the vast
majority of plants were infected by one or both of the
AMF-specific structures (arbuscules, vesicles). In only
the following plant/fungal combinations did we not detect any AMF structures: A. gigantea (home)/G. geosporum (home), A. novae-angliae (home)/A. morrowiae (home), O. biennis (home)/A. morrowiae (home),
A. gigantea (home)/A. denticulata (foreign), S. canadensis (home)/ S. pellucida (foreign), B. inermis (foreign)/G. geosporum (home), C. leucanthemum (foreign)/G. mosseae (home), C. leucanthemum (foreign)/
S. pellucida (home), S. canadensis (foreign)/A. morrowiae (home). Furthermore, arbuscules or vesicles
were not detected in any of the plants grown in the
non-AMF treatments.
The presence of AMF often significantly affected the
growth of plants, but the direction and magnitude of
this effect was dependent on the specific combination
of AMF species and plant species, and also on their
source of origin (Figs. 1–3). AMF species and plant
species main effects were not significant (P . 0.05),
however the source of origin main effect was significant (P 5 0.014). Also there were significant interaction effects between AMF species 3 plant species (P
5 0.0001), AMF species 3 source of origin (P 5
0.0001), plant species 3 source of origin (P 5 0.0001),
and AMF species 3 plant species 3 source of origin
(P 5 0.0001).
No plant or AMF species was consistently associated
with either positive or negative plant growth responses.
Special Feature
per week with a modified Long-Ashton Nutrient solution (half strength P; Hewitt 1966).
Response variables measured and statistical analysis.—For both experiments, plant shoots and roots were
harvested at the end of the 16-wk period. Plant material
was then dried at 608C for 36 h and then weighed to
determine biomass. Prior to drying, a subsample of
roots was taken from each pot and stored in 50% ethanol. This subsample of roots was then cleared in 10%
potassium hydroxide, and stained with Chlorazol Black
E (Brundrett et al. 1984) to confirm the presence of
AMF structures. The abundance of AMF structures in
plant roots was not assessed in this study because in
an earlier study (Klironomos 2000) I found no relationship between percentage root colonization and
plant growth response for a subset of the plant species
tested here.
The data in this study are presented as the percentage
difference in plant growth between mycorrhizal and
nonmycorrhizal treatments. To calculate 95% confidence intervals of these estimates, I took a bootstrap
sample of the plant biomass values for a particular
plant/AMF combination, and a second bootstrap sample of the nonmycorrhizal controls, calculated the percentage difference, and repeated 999 times. The data
in both experiments were analyzed with factorial ANOVA to determine the significance of main factor effects and interactions. Chi-square analyses were used
to compare the frequencies of positive and negative
interactions. Comparisons of response frequency distributions between native and exotic fungi was assessed
using Kolmogorov-Smirnov goodness-of-fit tests.
‘‘Mycorrhizal dependency’’ typically refers to the
difference in plant growth between mycorrhizal and
nonmycorrhizal treatments. Mycorrhizal dependency
was calculated for each plant species following the formulas by van der Heijden (2002). When the mean mass
of mycorrhizal plants was greater than nonmycorrhizal
controls, then mycorrhizal dependency 5 (1 2 [bn/Sa])
3 100%, where b is the mean dry mass of the nonmycorrhizal treatment, n is the number of treatments
containing AMF, and a is the mean dry mass of a treatment containing AMF. When the mean mass of my-
Foreign isolate
Experiment no.
Fungal species
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JOHN N. KLIRONOMOS
Ecology, Vol. 84, No. 9
Special Feature
FIG. 1. The influence of different ‘‘home’’ arbuscular mycorrhizal fungi on the growth of different ‘‘home’’ plants
(Experiment 1). Bars represent the percentage change in biomass of mycorrhizal plants compared to nonmycorrhizal controls.
The mean 95% confidence interval for all the treatments is 618%.
Growth responses to interactions between ‘‘home’’
plants and ‘‘home’’ fungi are found in Fig. 1. The number of negative and positive responses was approximately equal (53 and 47, respectively, Fig. 4a), and the
magnitude of plant growth response ranged from 249%
to 146%. When foreign plants or AMF were used,
negative and positive responses were also detected, but
some notable differences occurred. First, the direction
and magnitude of each response differed, even though
the same ‘‘species’’ was used. Second, the shape of the
frequency distributions (Fig. 4) differed (foreign AMF/
home plants, Kolmogorov-Smirnov Z 5 1.20, P 5
FIG. 2. The influence of different ‘‘foreign’’ arbuscular mycorrhizal fungi on the growth of different ‘‘home’’ plants
(Experiment 1). Bars represent the percentage change in biomass of mycorrhizal plants compared to nonmycorrhizal controls.
The mean 95% confidence interval for all the treatments is 612%.
UNDERGROUND PROCESSES
September 2003
2297
0.111; home AMF/foreign plants, Kolmogorov-Smirnov Z 5 1.49, P 5 0.024). The ratio of negative:positive responses was shifted from 53:47 (home AMF/
home plants, x2 5 0.64, P 5 0.424) to 55:45 (foreign
AMF/home plants, x2 5 1.00, P 5 0.317) and 61:39
(home AMF/foreign plants, x2 5 7.84, P 5 0.005). The
range of responses was smaller (238% to 124% when
using foreign AMF/home plants; 230% to 119% when
using home AMF/foreign plants).
The high variation in plant growth response to different AMF resulted in high mycorrhizal species sensitivity for the plant species tested (Fig. 5). Mycorrhizal
species sensitivity was highest when home plants were
associated with home fungi. However, regardless of the
source of the plant and AMF isolates, overall mycorrhizal dependency was low. No significant relationship
was detected between mycorrhizal dependency and mycorrhizal species sensitivity (Fig. 5).
Experiment 2
The majority of plants (home) that co-occur at the
LTMRS were successfully infected by Glomus etunicatum (home). Of the 64 plants tested, only the following plants were not found to contain any arbuscules
or vesicles at time of harvest: Apocynum cannabinum,
Carex aurea, Carex flava, Carex flacca, Carex granularis, Chenopodium ambrosioides, Convolvulus arvensis, Juncus dudleyi. Overall, there was a large variation in plant growth response among the plants when
grown in the presence of this one AMF isolate (Fig.
6). The majority of responses were small, and not significantly different from the nonmycorrhizal controls,
but the range (246 to 148) was similar to that observed
in experiment 1, where 10 plants were crossed with 10
fungi.
DISCUSSION
These data clearly show that plant responses to colonization by AMF can range from highly positive to
highly negative. It was proposed by Johnson et al.
(1997) that mycorrhizal associations could be considered symbioses that functionally range along a continuum of parasitism to mutualism, and that environmental condition, particularly the abundance of soil nutrients, could determine the position of AMF along that
continuum. The present data supports the parasitism–
mutualism hypothesis, and furthermore, it indicates
that the frequency of parasitic vs. mutualistic interactions can be equal even with communities of plants and
AMF that grow in a common environment.
Clearly, it is inaccurate to refer to arbuscular mycorrhizal symbioses only as mutualisms. This ignores
the prevalence of parasitism within this symbiosis. Parasitism may be more frequent under certain environmental conditions, such as in agricultural soils that
have been repeatedly fertilized (Johnson 1993). However, it is also frequent in more natural systems. The
present site (LTMRS) has not been disturbed for ;35
years (it is an abandoned farmland), and has low to
moderate nutrient levels. Fungi isolated from this site
and tested for host response under low nutrient conditions seemed equally likely to be parasites or mutualists. To complicate matters even more, it does not
seem possible to place AMF taxa into one of two cat-
Special Feature
FIG. 3. The influence of different ‘‘home’’ arbuscular mycorrhizal fungi on the growth of different ‘‘foreign’’ plants
(Experiment 1). Bars representage the percentage change in biomass of mycorrhizal plants compared to nonmycorrhizal
controls. The mean 95% confidence interval for all the treatments is 614%.
Special Feature
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JOHN N. KLIRONOMOS
Ecology, Vol. 84, No. 9
mean biomass for each plant species across all AMF
treatments was similar to that of their nonmycorrhizal
counterparts. This indicates that high mycorrhizal species sensitivity does not necessarily translate to high
overall mycorrhizal dependency, even though a positive relationship has been shown between these two
variables in at least one other ecosystem (van der Heijden 2002).
The composition of AMF communities has been
shown to greatly influence plant diversity and ecosystem functioning at the LTMRS (van der Heijden et al.
1998b), the same site where plant and fungi were collected for the present experiments. Based on the present
results, the effect of AMF on plant diversity and productivity reported earlier is not likely a result of differences in mycorrhizal dependency among plant species, since the plant species tested had similar overall
mycorrhizal dependency. Mycorrhizal dependency was
calculated as a mean response to the various AMF,
using a random draw of AMF taxa from the site. However, we know that AMF are not randomly or even
homogenously distributed at the site (Hart and Klironomos 2002). Rather they follow different and patchy
spatial distributions. Furthermore, there is evidence
that plants select for AMF that benefit them most (Klironomos 2002), creating a positive feedback between
species of plants and AMF in local environments. Thus,
at small spatial scales, distinct AMF communities are
formed, and certain plants benefit more than others,
depending on their responses to the local AMF. At larg-
FIG. 4. The frequency distribution of plant-growth responses in Experiment 1 (10 plant species crossed with 10
fungal species).
egories (mutualist or parasite). AMF do have a taxonomic basis to their own growth and development (Hart
and Reader 2002), but their influence on plant growth
is highly dependent on the plant genotype with which
they are associated. For example, whereas the AMF,
Acaulospora morrowiae, stimulated the growth of Rudbeckia hirta by 45%, the same AMF isolate reduced
the growth of Plantago lanceolata by 47%. Conversely,
the AMF, Gigaspora rosea, stimulated Plantago lanceolata by 41% and reduced the growth of Rudbeckia
hirta by 40%. The frequency curve of host responses
observed with a single individual AMF (as demonstrated with Glomus etunicatum crossed with 64 plant
species) follows a normal distribution (KolmogorovSmirnov 5 0.056, df 5 64, P 5 0.020).
Also it is difficult to determine mycorrhizal dependency (the extent to which a plant benefits from the
presence of AMF) for individual plant species. All
plants tested in this study varied widely in their response to individual AMF taxa (high mycorrhizal species sensitivity (see van der Heijden 2002), yet the
FIG. 5. The relationship between mycorrhizal dependency
and mycorrhizal species sensitivity (Experiment 1): (a) home
arbuscular mycorrhizal fungi vs. home plants, y 5 20.09x 1
24.8, r2 5 0.01, P 5 0.824; (b) foreign arbuscular mycorrhizal
fungi vs. home plants, y 5 20.32x 1 13.6, r2 5 0.17, P 5
0.724; (c) home arbuscular mycorrhizal fungi vs. foreign
plants, y 5 20.24x 1 12.0, r2 5 0.71, P 5 0.792.
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UNDERGROUND PROCESSES
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Special Feature
FIG. 6. The influence of Glomus etunicatum (home) on the growth of 64 home plants (Experiment 2). Bars represent the
percentage change in biomass of mycorrhizal plants compared to nonmycorrhizal controls. The mean 95% confidence interval
for all the treatments is 617%. The plant species names are in Table 1.
er scales within the plant community, no plant species
can dominate because no plant does best with all AMF
at the site. By this logic, mycorrhizal species sensitivity
may promote plant species coexistence and diversity
within the LTMRS, even though overall mycorrhizal
dependency is very low.
If mycorrhizal species sensitivity is an important determinant of diversity within plant communities, then
native AMF will be more influential on plant communities than exotic AMF. In this study, mycorrhizal
species sensitivity was significantly reduced when exotic AMF or plants were used. This suggests that plant
and AMF communities are locally adapted, and that
similar, but exotic, AMF taxa affect plants to a lesser
degree. This data has implications for restoration practitioners that may wish to add AMF into the soil to
help plant establishment and growth (Haselwandter
1997). If the plan is to incorporate AMF inoculum comprised of a single AMF isolate, then the present study
offers little direction. There is no evidence that a single
local or foreign AMF isolate can effectively promote
growth of all plant species in a community. However,
if a goal of restoration is to establish and maintain a
diverse plant community, then the present results would
suggest the addition of a diverse, and locally adapted,
AMF community to the restoration protocol.
In summary, AMF can influence the structure of
plant communities, but not because they always stimulate the growth of mycorrhizal plants. It is the parasitism–mutualism nature of plant/AMF interactions and
the high mycorrhizal species sensitivity of individual
plant species that may be the principal factors in the
maintenance of plant community structure. Also, even
though any one individual exotic AMF may not function any differently from a native counterpart, exotic
AMF communities offer less variation in plant response
than native AMF. Finally, the present results and conclusions may be of general significance to all terrestrial
2300
JOHN N. KLIRONOMOS
ecosystems, or they may only be applicable to herbaceous plant communities with generally low mycorrhizal dependency. This can only be determined after
similar research is conducted in a variety of plant
growth forms and ecosystem types.
Special Feature
ACKNOWLEDGMENTS
The author would like to thank A. Jones, G. LaPierre, G.
Lewis, D. MacIntosh, J. Martin, J. Mosquin, P. Moutoglis,
and A. Shaw for lab assistance. This work was supported by
a grant from the Natural Sciences and Engineering Research
Council of Canada.
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