| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
|
|
|
|||||||
|
|||||||||
Ecology |
2Department of Biology, Duke University, Durham, North Carolina 27708 USA; 3Department of Biology, Indiana University, Bloomington, Indiana 47405 USA
Received for publication October 18, 2001. Accepted for publication April 18, 2002.
 |
ABSTRACT |
|---|
 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
|---|
Key Words: coexistence • mutualism • mycorrhizae • niche partitioning • seasonal patterns • spatial patterns • sporulation • VAM (vesicular-arbuscular mycorrhizal) fungi
|
INTRODUCTION |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
|---|
); interest in the diversity of fungal communities is increasing because of a growing understanding of the impact of fungal diversity on plant communities. Arbuscular mycorrhizal (AM) fungi inhabit the roots of plants and provide phosphorous, and perhaps other benefits, to plants in exchange for photosynthetically derived carbon compounds. AM fungi are entirely dependent on plant hosts; fungi cannot be cultured axenically. Plant populations and communities are strongly influenced by AM fungi: fungi may increase or decrease plant fitness (Koide, Shumway, and Mabon, 1994
; Francis and Read, 1995
), regulate inter- or intraspecific competition (Fitter, 1977
; Hartnett et al., 1993
; Moora and Zobel, 1996
), and direct successional patterns (Gange, Brown, and Farmer, 1990
; Allen, 1991
). A number of studies have demonstrated that species of fungi cannot be substituted for each other within an experiment or habitat (Johnson et al., 1991
; Streitwolf-Engel et al., 1997
; van der Heijden et al., 1998a
); for example, Glomus macrocarpum causes tobacco stunt disease (Modjo and Hendrix, 1986
), while Glomus fasciculatum has no effect on tobacco growth (Modjo and Hendrix, 1986
) and Gigaspora margarita enhances tobacco growth (Csinos, 1981
). Because species of fungi are ecologically distinct, the diversity of an AM fungal community can have large effects on plant population and community dynamics (van der Heijden et al., 1998b
), and for this reason, factors that influence the diversity of fungal communities are of interest to plant ecologists. Although AM fungal communities of natural habitats are diverse (e.g., Morton, Bentivenga, and Bever, 1995
; Bever et al., 1996
; Stutz and Morton, 1996
), the specific mechanisms by which coexistence of diverse groups of fungi is facilitated are unknown.
Coexistence might be explained by the partitioning of various biotic or abiotic resources. Although associations between plants and AM fungi appear to be nonspecific, a number of recent studies have demonstrated that the population growth rates of fungal species are dramatically affected by the species of plant with which they are associated (Johnson, Tilman, and Wedin, 1992
; Sanders and Fitter, 1992a
; Bever et al., 1996
; Eom, Hartnett, and Wilson, 2000
); this host-specificity in AM fungal response might promote the coexistence of AM fungi. For example, the AM fungal species Acaulospora colossica (called A. D1 in Bever et al., 1996
) sporulates profusely with the plant Allium vineale but not with Plantago lanceolata; in contrast, Scutellospora calospora sporulates well with P. lanceolata but poorly with A. vineale (Bever et al., 1996
). Although both Ac. colossica and S. calospora are capable of infecting both A. vineale and P. lanceolata, the benefits to the fungi are variable; variable benefits might promote the coexistence of AM fungi within a diverse plant community. Coexistence might also be facilitated by the interaction of AM fungi with pathogens. Arbuscular mycorrhizal fungi are commonly infected by other fungi (Daniels and Menge, 1980
; Lee and Koske, 1994a
; Rousseau et al., 1996
) or actinomycetes (Lee and Koske, 1994a
) and variability in infection susceptibility might promote coexistence. In addition environmental parameters, for example, soil phosphorus levels (Miranda and Harris, 1994a
, b
) or pH (Clark, 1997
), may provide different species of AM fungi with unique niches (see also Johnson, Tilman, and Wedin, 1992
; Klironomos et al., 1993
; Schultz, 1996
).
The coexistence of AM fungal species might also result from fungal partitioning of temporal resources; for example, a fungus that grows in spring will not compete with a fungus that grows in fall. Temporal niche partitioning requires that fungi have distinct seasonalities. The coexistence of plant species is often facilitated by plants' heterogeneous seasonalities; for example, Fowler and Antonovics (1981)
documented two seasonal plant guilds within a North Carolina grassland. Species such as Allium vineale and Veronica arvensis dominate in the cool season, but species such as Cynodon dactylon and Paspalum spp. dominate in the warm season. AM fungi may demonstrate an analogous seasonality, and disparate seasonal phenologies may contribute to the maintenance of a diverse community of AM fungi.
Moreover, the coexistence of AM fungal species may be facilitated by the fine-scale spatial structure of fungal communities. As the aggregation of species distributions increases, AM fungi are increasingly likely to compete against individuals of the same species, thereby intensifying intraspecific competition relative to interspecific competition. This dynamic may facilitate the coexistence of competing fungal species (Pacala, 1986
). In fact, previous studies indicate that AM fungal communities are spatially clumped (Friese and Koske, 1991
; Bever et al., 1996
).
We investigated the seasonality of AM fungi within the same North Carolina grassland explored by Fowler and Antonovics (1981)
. The site supports a particularly diverse group of fungi; to date, 37 species have been recorded from approximately 1.5 ha (Bever et al., 1996
; Schultz, 1996
; J. D. Bever and P. Schultz, Indiana University, unpublished data). Host-specificity in fungal population growth rates may contribute to the maintenance of fungal diversity (Bever et al., 1996
); in addition, the high diversity of AM fungi might result from a temporal partitioning of the habitat. In fact, prior sampling suggests that fungi differ in their seasonalities: Schultz, Bever, and Morton (1999)
observed that Acaulospora colossica sporulates in spring, but other species, particularly Gigaspora gigantea, are observed to sporulate in winter (Schultz, 1996
). In this study, we aimed to rigorously test for the distinct seasonalities of Ac. colossica, Gi. gigantea, and other species of AM fungi within the North Carolina grassland. We focused on temporal patterns; however, the same data were used to compare the fine-scale spatial arrangements of collected AM fungi.
|
MATERIALS AND METHODS |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
|---|
; Clay, 1982
; Kelley, 1985
; Moloney, 1986
; Bever, 1992
; Schultz, 1996
) old field on the campus of Duke University, Durham, North Carolina, USA. Regular mowing over the last 50 yr has halted succession and kept the field as a species-rich grassland. Although certain plant species appear to dominate at specific times of year (e.g., Anthoxanthum odoratum in spring), careful observation reveals a mosaic of common plants that belong to a diversity of families (Fowler and Antonovics, 1981
). Soil is a sandy loam of the White Store series (Fowler and Antonovics, 1981
). Plants are divided into cool and warm season communities; cool season plants are active in fall, winter, and spring, and warm season plants are active in the spring, summer, and fall (Fowler and Antonovics, 1981
). The AM fungal community within the field is diverse: a variety of intensive collecting and trapping techniques have revealed 37 morphospecies (Bever et al., 1996
; Schultz, 1996
; J. D. Bever and P. Schultz, Indiana University, unpublished data), and these fungi are known to be ecologically distinct (Bever et al., 1996
; Schultz, 1996
; Pringle, 2001
).
Experimental approach and design
Arbuscular mycorrhizal fungi were sampled from an area of the field with a particularly rich fungal community; the site is known to maintain abundant populations of both Acaulospora colossica and Gigaspora gigantea (Schultz, 1996
). Our goal was to evaluate the seasonality of these, and other, fungal species by enumerating spore densities through time.
Numbers of healthy spores are likely to reflect the past physiological activity of an AM fungus. Sporulation can be correlated to the prior growth of a fungus within plant roots (Douds and Schenk, 1990
; Gazey, Abbott, and Robson, 1992
; see also Abbott and Gazey, 1994
), and in agricultural systems, sporulation is associated with plant senescence (see references in Gemma, Koske, and Carreiro, 1989
). This evidence suggests that spores form during the final stages of an association between plant and fungus. While this pattern may vary between fungal species, spore counts of Ac. colossica and Gi. gigantea are likely to reliably track periods of prior physiological activity. Acaulospora colossica is closely related to Ac. laevis (Schultz, Bever, and Morton, 1999
), and Ac. laevis has been shown to sporulate following periods of physiological activity (Gazey, Abbott, and Robson, 1992
). Moreover, Abbott and Robson (1981)
found that mycorrhizae of Ac. laevis were ineffective at colonizing new hosts following sporulation. Healthy spores are ephemeral in nature: spores are parasitized or germinated within months of creation. Lee and Koske (1994b)
have estimated that spores of Gi. gigantea are viable for approximately 5 mo in the field. Therefore, fluctuations in numbers of healthy spores should reflect prior periods of physiological activity, and greatest spore densities should follow peak periods of physiological activity.
Samples were collected from an approximately 36-m2 site, which represents a relatively small portion of the 1.5-ha field. By minimizing the size of the site, we intended to minimize spatial variability. Plots within the site were arranged in three rows of three plots each (Fig. 1). The nine plots were sampled every other month during the first year. To evaluate the consistencies of Ac. colossica and Gi. gigantea seasonalities, a subset of the nine sites was monitored in greater detail during the second year.
|
). Spores were identified to species based on spore wall characters using reference cultures from this site (Bever et al., 1996
) and from INVAM (International Culture Collection of Arbuscular and Vesicular-Arbuscular Mycorrhizal Fungi; Morton, Bentivenga, and Wheeler, 1993
). Essential features were noted for morphotypes that appeared to be distinct from any published species descriptions. Permanent slide vouchers of all species are available upon request from the authors.
Total numbers of healthy spores were recorded for each species. One species creates two kinds of spores, and the different morphologies were tracked individually and are called Archaeospora leptoticha and Glomus leptotichum (after Morton and Redecker, 2001
). A dissecting scope was used to count every spore of the subsample for most species; however, estimates were used to approximate the total number of the small and usually numerous spores of Acaulospora morrowiae (referred to as Ac. mellea in Bever et al., 1996
). We estimated the total number of Ac. morrowiae in a subsample by counting the number of spores in 40 randomly located optical squares (2.5 x 2.5 mm). Spores were judged to be healthy if they were completely filled with lipid droplets and devoid of parasitism.
Spores of Gi. gigantea were further categorized as either "new" or "old" on the basis of color (Lee and Koske, 1994b
); "old" spores are likely to be several months old. "New" spores of Gi. gigantea are bright yellow-green, but "old" spores are dull yellow or yellow-brown. Note that only spores with lipid contents were counted, i.e., dead spores were not counted. Differentiating "new" from "old" Gi. gigantea spores allowed us to more accurately judge the timing of sporulation for this species.
Sampling in year 2 (1997)
Results of sampling in year 1 confirmed that spores of Gi. gigantea and Ac. colossica were abundant at the study site, were distinctly seasonal, and had contrasting seasonalities. In year 2, sampling focused on Gi. gigantea and Ac. colossica. However, because of a large and consistent effect of plot identity on spore densities, in the second year sampling was adjusted to more formally evaluate the interaction between spatial and seasonal patterns. Cores were not homogenized; instead, spores were extracted and counted from 25 cm3 of soil of each core. By evaluating individual cores, we were able to test for the constancy of seasonal patterns within plots. In 1997, only plots A1, A3, B2, C1, and C3 were sampled (Fig. 1). Two 2 cm diameter soil cores were taken to a depth of 7 cm from two randomly chosen squares at each plot. Otherwise, methods were as described above.
Analyses
Only those species that were relatively common (found at every date and in most plots) were included in statistical analyses of spore densities (Table 1). To improve the normality of distributions and homogeneity of variances, spore counts of each species were ranked; further analyses were completed with ranked counts (as in Bever et al., 1996
). Multivariate analysis of variance (MANOVA) was used to test for general seasonal and spatial effects (completed with the general linear models procedure; SAS Institute, 1988
). Subsequently, a multivariate profile analysis was used to test the variability of fungal species' seasonal and spatial patterns (as developed in Bever et al., 1996
). The profile analysis specifically asks whether fungal species display different seasonalities and for this reason, the analysis directly tests the essential question of our study. Finally, significant multivariate effects were further dissected using univariate analyses of variance (ANOVA) on ranked counts of the individual species.
|
In the analyses described above, counts of new and old Gi. gigantea spores were added to give a single value for the total number of spores at each date in each plot. To confirm the seasonal patterns of Gi. gigantea that we had inferred from the total spore counts, we tested for seasonal differences in the densities of new and old spores. We predicted that the proportion of new spores would be highest after the fungi sporulate (while spore numbers are increasing) and lowest when fungi do not sporulate (and new spores develop into old spores). We tested our hypothesis by analyzing the effects of date and plot on the proportion of new spores (number of new spores divided by the total number of spores) with MANOVA, as described above, using data from 1996. A subsequent analysis evaluated the similiarity of seasonal patterns in 1996 and 1997 using ANOVA, as described above.
|
RESULTS |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
|---|
and Schultz (1996)
. Only seven of the species occurred frequently enough to include in statistical analyses (Table 1).
Seasonal patterns of the common species (1996)
Sporulation was distinctly seasonal, and seasonal differences between species were significant. Spore counts varied significantly with date, as indicated by the multivariate analysis of variance (Table 2). Seasonality is the result of differences in sporulation patterns between fungal species, as tested by the seasonal term within the multivariate profile analysis (interaction of species' profiles with sampling date: Table 3; Fig. 2). The latter analysis demonstrates that AM fungal species displayed contrasting seasonal patterns.
|
|
|
|
Seasonal patterns of new and old Gi. gigantea spores (1996 and 1997)
By comparing the seasonalities of new and old Gi. gigantea spores, we were able to confirm that Gi. gigantea sporulates in the cool season. In 1996, new spores were common in the cool months, but were rare in June (Fig. 2b). Older spores were consistently found in each month (Fig. 2b). Numbers of new Gi. gigantea spores varied significantly with date (F4 = 5.80, P < 0.0013), but numbers of old Gi. gigantea spores did not (F4 = 0.92, P < 0.46). Furthermore, ratios of new to old Gi. gigantea spores differed significantly with date (F4 = 4.15, P < 0.0083) and peaked in the cool months (Fig. 2b). By combining data for 1996 and 1997, we tested the consistency of the seasonal patterns across both years, again treating year as a random effect and using the interaction of date and year as an error term (as described above). In contrast to the results for total numbers of Gi. gigantea spores, date was a significant predictor of the ratio of new to old spores across years (F4,4 = 7.90, P < 0.034), even under this conservative test. Furthermore, ratios of new to old spores were not significantly different in the same month of different years, as tested by ANOVA (interaction of date and year, F4,33 = 0.32, P < 0.87).
Spatial patterns (1996 and 1997)
The seven common species displayed contrasting spatial distributions in 1996. The overall spatial effect on spore counts was highly significant in the multivariate analysis of variance (Wilks' lambda F56,183 = 6.93, P < 0.0001), with much of this effect being due to the consistent differences in spatial patterns between the fungal species as tested by profile analysis (interaction of species' profiles with site: Wilks' lambda F48,171 = 6.54, P < 0.0001). Spores of Ac. colossica, Gi. gigantea, S. calospora, and S. pellucida were extracted from every site (Fig. 3); however, analyses of the individual data sets indicated that spores were significantly more common in some sites versus others (Table 4). Both Ac. colossica and Gi. gigantea were particularly abundant at sites A3 and C3 (Fig. 3). Archaeospora leptoticha and Acaulospora morrowiae displayed significant spatial patterns (Table 4). Spores of Ar. leptoticha were generally restricted to sites C3 and C2 (Fig. 3) (as were spores of Glomus leptotichum). Acaulospora morrowiae spores were scattered throughout B and C sites, but were particularly common at site B2 (Fig. 3). Glomus clarum demonstrated no spatial pattern (Table 4); although a disproportionate number of spores appear to have been found at site A3 (Fig. 3), the data are biased by the exceptional number of spores found from this site in one month (44 of 160 total spores, December 1996). As the spatial pattern was not consistent through time, it was not significant.
|
Although spores of Gi. gigantea were found at the same sites in 1996 and 1997, spores of Ac. colossica were not. The test for a spatial profile effect (profile x site) using the interaction between the spatial profile effect and year (profile x site x year) as the error term (as described above) was not significant (Wilks' lambda F4,4 = 2.46, P < 0.20); Ac. colossica and Gi. gigantea did not maintain contrasting spatial distributions across the two years. This is probably a result of the shifting spatial patterns displayed by Ac. colossica: when year was treated as a random effect (as described above) spatial patterns proved to be predictable for Gi. gigantea (F4,4 = 13.09, P < 0.014) but not for Ac. colossica (F4,4 = 3.97, P < 0.11).
|
DISCUSSION |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
|---|
; Schultz, Bever, and Morton, 1999
). The seasonal differences in spore densities probably reflect seasonal differences in spore formation. As detailed in MATERIALS AND METHODS (Gemma, Koske, and Carreiro, 1989
; Douds and Schenk, 1990
; Gazey, Abbott, and Robson, 1992
), sporulation follows periods of physiological activity. Therefore, our data suggest that Ac. colossica is physiologically active in the cool season, while Gi. gigantea is physiologically active in the warm season.
Our data are supported by several additional lines of evidence. Gigaspora gigantea is easy to culture in a warm season greenhouse (Schultz, 1996
; personal observation), but Ac. colossica is very difficult to culture in a warm season greenhouse (Schultz, Bever, and Morton, 1999
). In contrast, Ac. colossica sporulates profusely in a cool season greenhouse (Bever et al., 1996
). Furthermore, when grown in a cool season greenhouse, Ac. colossica sporulates abundantly with a markedly cool season host (Allium vineale). Gigaspora gigantea sporulated poorly with this cool season host (Bever et al., 1996
); however, Gi. gigantea is easily cultured with the tropical grass Sorghum sudanense. Finally, developmental evidence suggests that Ac. colossica sporulates in late spring. Acaulospora colossica sporulates by developing a thin-walled saccule on the terminal branch of a fertile hypha; each saccule forms a spore. After spores are formed, the saccule degrades or breaks off (Schultz, Bever, and Morton, 1999
); in this study, saccules were only found in April (personal observation). Our data strongly imply that Ac. colossica is physiologically active in the cool season and lasts through the summer as a dormant spore. Conversely, Gi. gigantea is likely to be physiologically active in the warm season and over-winter as a dormant spore.
Populations of Gi. gigantea in coastal sand dune communities of the eastern United States also sporulate in late fall and winter. Gemma and Koske (1988)
recorded peak numbers of Gi. gigantea spores in late fall (November and December); Lee and Koske (1994b)
recorded peak numbers of healthy Gi. gigantea spores in winter (January and February). To our knowledge, the sand dunes of Rhode Island and grasslands of North Carolina have no species of plant in common. The climate of the two habitats is also very different. The concordance of data across different communities suggests that the seasonality of Gi. gigantea is a species-level property.
While our study was designed to document seasonal differences between Ac. collosica and Gi. gigantea, we found that most of the common fungi were significantly seasonal (Table 4). Many of these fungi seemed to sporulate in the fall (e.g., S. pellucida). However, S. calospora appeared to sporulate in the spring as well as the fall, and spores of Gl. clarum were most common in winter.
Aseasonal species may be cryptically seasonal. The data are observational and a conservative measure of AM fungal seasonality. For example, AM fungal species may experience differential parasitism or predation in nature: the spores of a palatable species will be ephemeral and the species' seasonality obvious; the spores of a resistant species will persist in the soil. The second species may appear aseasonal.
The unusual exponential pattern of Gl. clarum sporulation may have been caused by a hurricane that swept through our field site on 6 September 1996. The sporulation of Gl. clarum increased dramatically in October and December (Fig. 2). In February and April, Gl. clarum had been found in a single plot, but in October and December, Gl. clarum was recovered from each of the nine plots (data not shown). Glomus clarum may have responded to the extraordinary amounts of rain associated with the hurricane by invasively sporulating through the site, and perhaps the population of Gl. clarum at this site sporulates in association with exceptional amounts of precipitation.
The seasonality of AM fungal sporulation in natural habitats has been documented in only a few studies. In contrast, a number of classic papers explore temporal patterns of fungal sporulation in agricultural systems (Hayman, 1970
; Sutton and Barron, 1972
; Saif, 1977
; Rich and Schenck, 1981
); a majority of these studies record general increases in the sporulation of all species as crops mature and are harvested. Although work by Merryweather and Fitter (1998)
indicated that spores of AM fungi within sycamore- or oak-dominated woodlands are aseasonal, studies by Sylvia (1986)
, Gemma, Koske, and Carreiro (1992), and Stürmer and Bellei (1994)
in maritime dune systems of Florida, Massachusetts, and Santa Catarina Island (Brazil) suggested distinct seasonalities for different species of fungi within a single habitat. A study by Sanders and Fitter (1992b)
of root infection also demonstrated that mycorrhizal colonization of plants might be temporally variable, although in this study, fungi were not identified to species. Distinct seasonal guilds of AM fungi might be a typical feature of fungal communities.
The distinct seasonalities of AM fungal species suggest a temporal partitioning of plant resources; by specializing on cool or warm season plants, fungi would minimize interspecific competition for roots. In fact, our data suggest that fungi derive variable benefits from their associations with plants. For example, if Ac. colossica is a specialist of Allium vineale or other cool season plants, it will derive a limited benefit from associations with warm season plants; conversely, Gi. gigantea may derive its greatest benefit from associations with warm season plants. The divergent seasonalities of Ac. colossica, Gi. gigantea, and other fungi may facilitate the coexistence of a diverse group of AM fungal species within the North Carolina grassland. Our data also provide additional evidence for the distinct ecologies of fungi that coexist within a single site (e.g., Bever et al., 1996
; Van der Heijden, 1998a
).
Matching seasonalities of plants and AM fungi might reflect a level of specificity between plants and fungi. In fact, three lines of correlational evidence are suggestive of specificity between Ac. colossica and the cool season plant Allium vineale. First, Ac. colossica and A. vineale are both physiologically active during the cool season and dormant over the warm season. The peak sporulation period of Ac. colossica coincides with the period in which A. vineale dies back into its bulb (Fowler and Antonovics, 1981
). Second, as mentioned above, Ac. colossica sporulates preferentially with A. vineale when growth of Ac. colossica is compared in A. vineale and other cool season hosts (Bever et al., 1996
). Finally, the distributions of Ac. colossica and A. vineale are positively correlated in the field (Schultz, 1996
). Specificity between Ac. colossica and A. vineale could generate a positive feedback dynamic in which a high initial abundance of A. vineale would increase the abundance of Ac. colossica, thereby increasing the relative success of A. vineale (Bever, Westover, and Antonovics, 1997
; Bever, 1999
). However, a demonstration of this dynamic will require further experimentation.
Spatial patterns
Fine-scale spatial patterns were recorded for both common (Tables 2 and 3) and infrequent species. For example, the common fungus Archaeospora leptoticha was generally restricted to two plots (Table 4; Fig. 3); although the rare species S. reticulata sporulated in 5 mo, spores were only recovered from a single plot (Table 1). The spatial arrangements of Ac. leptoticha and its hypothesized synanamorph, Glomus leptotichum, provide further evidence of their formation from a common mycelium (Morton, Bever, and Pfleger, 1997
; Morton and Redecker, 2001
); although spores of Gl. leptotichum were rare, they were generally collected within the distribution of the more common Ac. leptoticha. The spatial structure of plant communities is obvious to ecologists, and this work demonstrates that fungal communities can also be spatially patterned. Fungal communities may be highly variable at a local scale; comparisons of the individual plots of this study show that the community of one site can be very different from the community of a second and nearby site (e.g., compare plots A3 and B3, Fig. 3).
Implications for plant ecology
The coexistence of disparately seasonal and spatial AM fungi illuminates our understanding of the interactions between AM fungi and plants. It suggests a mechanism through which the diversity of an AM fungal community might drive the diversity of a plant community, as has been demonstrated in experimental grasslands of North America and Europe (Van der Heijden et al., 1998b
). Our observations suggest that the success of cool and warm season guilds of plants is dependent upon plants' associations with cool and warm season guilds of fungi. The maintenance of a functionally diverse plant community may depend on the coexistence of guilds within the fungal community. Furthermore, spatial patterns within the fungal community might also have direct impacts on plant community diversity and structure. A local community of fungi may control the local composition and diversity of plants (van der Heijden et al., 1998b
). Therefore, the fine-scale heterogeneity of the fungal community may increase the regional diversity of the plant community. Small and diverse patches of AM fungi may structure the plant community as a mosaic of plant types, especially if some plants are restricted within the boundaries of a particularly effective symbiont. Clearly, the seasonal and spatial heterogeneity of the fungal community might have strong impacts on plant community processes.
|
FOOTNOTES |
|---|
4 Author for reprint requests, current address: Department of Plant and Microbial Biology, 111 Koshland Hall, University of California, Berkeley, California 94720-3102 USA (apringle{at}uclink.berkeley.edu
)
|
LITERATURE CITED |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
|---|
Abbott L. K. A. D. Robson 1981 Infectivity and effectiveness of vesicular arbuscular mycorrhizal fungi: effect of inoculum type. Australian Journal of Agricultural Research 32: 631-639[CrossRef][ISI]
Allen M. F. 1991 The ecology of mycorrhizae. Cambridge University Press, Cambridge, UK
Bever J. D. 1992 Ecological and evolutionary dynamics between plants and their soil Communities. Ph.D. dissertation, Duke University, Durham, North Carolina, USA
Bever J. D. 1999 Dynamics within mutualism and the maintenance of diversity: inference from a model of interguild frequency dependence. Ecology Letters 2: 52-61[CrossRef][ISI]
Bever J. D. J. B. Morton J. Antonovics P. A. Schultz 1996 Host-dependent sporulation and species diversity of arbuscular mycorrhizal fungi in a mown grassland. Journal of Ecology 84: 71-82[CrossRef]
Bever J. D. K. M. Westover J. Antonovics 1997 Incorporating the soil community into plant population dynamics: the utility of the feedback approach. Journal of Ecology 85: 561-573[CrossRef]
Clark R. B. 1997 Arbuscular mycorrhizal adaptation, spore germination, root colonization, and host plant growth and mineral acquisition at low pH. Plant and Soil 192: 15-22[CrossRef][ISI]
Clay K. 1982 Ecological and genetic consequences of cleistogamy in the grass Danthonia spicata. Ph.D. dissertation, Duke University, Durham, North Carolina, USA
Csinos A. S. 1981 Gigaspora margarita inoculation of Nicotiana tabacum: responses to fertilization. Canadian Journal of Botany 59: 101-103
Daniels B. A. J. A. Menge 1980 Hyperparasitism of vesicular-arbuscular mycorrhizal fungus. Phytopathology 70: 584-588[ISI]
Douds D. D. N. C. Schenck 1990 Relationship of colonization and sporulation by VA mycorrhizal fungi to plant nutrient and carbohydrate contents. New Phytologist 116: 621-627[CrossRef][ISI]
Eom A. H. D. C. Hartnett G. W. T. Wilson 2000 Host plant species effects on arbuscular mycorrhizal fungal communities in tallgrass prairie. Oecologia 122: 435-444[CrossRef][ISI]
Fitter A. H. 1977 Influence of mycorrhizal infection on competition for phosphorus and potassium by two grasses. New Phytologist 79: 119-125[CrossRef][ISI]
Francis R. D. J. Read 1995 Mutualism and antagonism in the mycorrhizal symbiosis, with special reference to impacts on plant community structure. Canadian Journal of Botany 73: (Supplement 1) S1301-S1309
Friese C. F. R. E. Koske 1991 The spatial dispersion of spores of vesicular-arbuscular mycorrhizal fungi in a sand dune: microscale patterns associated with the root architecture of American beachgrass. Mycological Research 95: 952-957[ISI]
Fowler N. L. 1978 Competition and coexistence in a North Carolina grassland. Ph.D. dissertation, Duke University, Durham, North Carolina, USA
Fowler N. L. J. Antonovics 1981 Competition and coexistence in a North Carolina grassland I. Patterns in undisturbed vegetation. Journal of Ecology 69: 825-841[CrossRef][ISI]
Gange A. C. V. K. Brown L. M. Farmer 1990 A test of mycorrhizal benefit in an early successional plant community. New Phytologist 115: 85-91[CrossRef][ISI]
Gazey C. L. K. Abbott A. D. Robson 1992 The rate of development of mycorrhizas affects the onset of sporulation and production of external hyphae by two species of Acaulospora. Mycological Research 96: 643-650[ISI]
Gemma J. N. R. E. Koske 1988 Seasonal variation in spore abundance and dormancy of Gigaspora gigantea and in mycorrhizal inoculum potential of a dune soil. Mycologia 80: 211-216[CrossRef][ISI]
Gemma J. N. R. E. Koske M. Carreiro 1989 Seasonal dynamics of selected species of V-A mycorrhizal fungi in a sand dune. Mycological Research 92: 317-321[ISI]
Hartnett D. C. B. A. D. Hetrick G. W. T. Wilson D. J. Gibson 1993 Mycorrhizal influence on intra- and inter-specific neighbor interactions among co-occuring prairie grasses. Journal of Ecology 81: 787-795[CrossRef][ISI]
Hayman D. S. 1970 Endogone spore numbers in soil and vesicular-arbuscular mycorrhiza in wheat as influenced by season and soil treatment. Transactions of the British Mycological Society 54: 53-63[ISI]
Johnson N. C. F. L. Pfleger R. K. Crookston S. R. Simmons 1991 Vesicular-arbuscular mycorrhizas respond to corn and soybean cropping history. New Phytologist 117: 657-664[CrossRef][ISI]
Johnson N. C. D. Tilman D. Wedin 1992 Plant and soil controls on mycorrhizal fungal communities. Ecology 73: 2034-2042[CrossRef][ISI]
Klironomos J. N. P. Moutoglis B. Kendrick P. Widden 1993 A comparison of spatial heterogeneity of vesicular-arbuscular mycorrhizal fungi in two maple-forest soils. Canadian Journal of Botany 71: 1472-1480
Kelley S. E. 1985 The mechanism of sib competition for the maintenance of sexual reproduction in Anthoxanthum odoratum L. Ph.D. dissertation, Duke University, Durham, North Carolina, USA
Koide R. T. D. L. Shumway S. A. Mabon 1994 Mycorrhizal fungi and reproduction of field population of Abutilon theophrasti Medic. (Malvaceae). New Phytologist 126: 123-130[CrossRef][ISI]
Lee P.-J. R. E. Koske 1994a Gigaspora gigantea: parasitism of spores by fungi and actinomycetes. Mycological Research 98: 458-466[ISI]
Lee P.-J. R. E. Koske 1994b Gigaspora gigantea: seasonal abundance and ageing of spores in a sand dune. Mycological Research 98: 453-457[ISI]
Merryweather J. A. Fitter 1998 The arbuscular mycorrhizal fungi of Hyacinthoides non-scripta. II. Seasonal and spatial patterns of fungal populations. New Phytologist 138: 131-142[CrossRef][ISI]
Miranda J. C. C. P. J. Harris 1994a The effect of soil phosphorus on the external mycelium growth of arbuscular mycorrhizal fungi during the early stages of mycorrhiza formation. Plant and Soil 166: 271-280[CrossRef][ISI]
Miranda J. C. C. P. J. Harris 1994b Effects of soil phosphorus on spore germination and hyphal growth of arbuscular mycorrhizal fungi. New Phytologist 128: 103-108[CrossRef][ISI]
Modjo H. S. J. W. Hendrix 1986 The mycorrhizal fungus Glomus macrocarpum as a cause of tobacco stunt disease. Phytopathology 76: 688-691[ISI]
Moloney K. A. 1986 Determinants of species distributions: Danthonia sericea as a model system. Ph.D. dissertation, Duke University, Durham, North Carolina, USA
Moora M. M. Zobel 1996 Effect of arbuscular mycorrhiza on inter- and intraspecific competition of two grassland species. Oecologia 108: 79-84[CrossRef][ISI]
Morton J. B. S. P. Bentivenga J. D. Bever 1995 Discovery, measurement, and interpretation of diversity in arbuscular endomycorrhizal fungi (Glomales, Zygomycetes). Canadian Journal of Botany 73: S25-S32
Morton J. B. S. P. Bentivenga W. W. Wheeler 1993 Germ plasm in the International Collection of Arbuscular and Vesicular-Arbuscular Mycorrhizal Fungi (INVAM) and procedures for culture development, documentation, and storage. Mycotaxon 48: 491-528[ISI]
Morton J. B. J. D. Bever F. L. Pfleger 1997 Taxonomy of Acaulospora gerdemannii and Glomus leptotichum, synanomorphs of an arbuscular mycorrhizal fungus in Glomales. Mycological Research 101: 625-631[CrossRef][ISI]
Morton J. B. D. Redecker 2001 Two new families of Glomales, Archaeosporaceae and Paraglomaceae, with two new genera Archaeospora and Paraglomus, based on concordant molecular and morphological characters. Mycologia 93: 181-195[CrossRef][ISI]
Pacala S. W. 1986 Neighborhood models of plant population dynamics. 2. Multispecies models of annuals. Theoretical Population Biology 29: 262-292
Pringle A. 2001 Ecology and genetics of arbuscular mycorrhizal fungi. Ph.D. dissertation, Duke University, Durham, North Carolina, USA
Rich J. R. N. C. Schenck 1981 Seasonal variations in populations of plant-parasitic nematodes and vesicular-arbuscular mycorrhizae in Florida field corn. Plant Disease 65: 804-807[ISI]
Rousseau A. N. Benhamou I. Chet Y. Piché 1996 Mycoparasitism of the extramatrical phase of Glomus intraradices by Trichoderma harzianum. Phytopathology 86: 434-443[CrossRef][ISI]
SAS Institute. 1988 SAS/STAT user's guide. Release 6.03. SAS Institute, Cary, North Carolina, USA
Saif S. R. 1977 The influence of state of host development on vesicular-arbuscular mycorrhizae and endogonaceous spore populations in field-grown vegetable crops I. Summer-grown crops. New Phytologist 79: 341-348[CrossRef][ISI]
Sanders I. R. A. H. Fitter 1992a Evidence for differential responses between host-fungus combinations of vesicular arbuscular mycorrhizas from a grassland. Mycological Research 96: 415-419[ISI]
Sanders I. R. A. H. Fitter 1992b The ecology and functioning of vesicular-arbuscular mycorrhizas in co-existing grassland species. New Phytologist 120: 517-524[CrossRef][ISI]
Schultz P. A. 1996 Arbuscular mycorrhizal species diversity and distribution in an old field community. Ph.D. dissertation, Duke University, Durham, North Carolina, USA
Schultz P. A. J. D. Bever J. B. Morton 1999 Acaulospora colossica sp. nov. from an old field in North Carolina and morphological comparisons with similar species, A. laevis and A. koskei. Mycologia 91: 676-683[CrossRef][ISI]
Smith S. E. D. J. Read 1997 Mycorrhizal symbiosis, 2nd ed. Academic Press, San Diego, California, USA
Streitwolf-Engel R. T. Boller A. Wiemken I. R. Sanders 1997 Clonal growth traits of two Prunella species are determined by co-occurring arbuscular mycorrhizal fungi from a calcareous grassland. Journal of Ecology 85: 181-191[CrossRef][ISI]
Sturmer S. L. M. M. Bellei 1994 Composition and seasonal variation of spore populations of arbuscular mycorrhizal fungi in dune soils on the island of Santa Catarina, Brazil. Canadian Journal of Botany 72: 359-363
Stutz J. C. J. B. Morton 1996 Successive pot cultures reveal high species richness of arbuscular endomycorrhizal fungi in arid ecosystems. Canadian Journal of Botany 74: 1883-1889
Sutton J. C. G. L. Barron 1972 Population dynamics of Endogone spores in soil. Canadian Journal of Botany 50: 1909-1914[ISI]
Sylvia D. M. 1986 Spatial and temporal distribution of vesicular-arbuscular mycorrhizal fungi associated with Uniola paniculata in Florida foredunes. Mycologia 78: 728-734[CrossRef][ISI]
Van der Heijden M. G. A. T. Boller A. Wiemken I. R. Sanders 1998a Different arbuscular mycorrhizal fungal species are potential determinants of plant community structure. Ecology 79: 2082-2091[CrossRef][ISI]
Van der Heijden M. G. A. J. N. Klironomos M. Ursic P. Moutoglis R. Streitwolf-Engel T. Boller A. Wiemken I. R. Sanders 1998b Mycorrhizal fungal diversity determines plant biodiversity, ecosystem variability and productivity. Nature 396: 69-72[CrossRef]
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
| HOME | HELP | FEEDBACK | SUBSCRIPTIONS |
