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Ecology |
2Division of Biology, Ackert Hall, Kansas State University, Manhattan, Kansas 66506-5502 USA 3Department of Plant Pathology, University of Arizona, Tucson, Arizona 85721-0036 USA
Received for publication May 26, 2000. Accepted for publication February 8, 2001.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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The pattern of responses of these three species to mycorrhizae differed considerably between the two sites of contrasting fire regime, indicating that the interaction of fire-induced shifts in resource availability and mycorrhizal symbiosis together modulates plant responses and the intensity and patterns of interspecific competition between and among tallgrass prairie grass and forb species. Further, the results indicate that effects of mycorrhizae on community structure are a result of interspecific differences in the balance between direct positive effects of the symbiosis on host plant performance and indirect negative effects mediated through altered competitive interactions.
Key Words: Artemisia ludoviciana • Aster sericeus • fire • mycorrhizae • Salvia azurea • tallgrass prairie
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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; Huntly, 1991
; Gurevich et al., 1992
). However, the importance of other biotic interactions such as those between plants and soil microorganisms have recently been recognized as well. Because arbuscular mycorrhizal (AM) fungi are abundant and ubiquitous in almost all natural communities and form associations with >80% of vascular plants (Harley and Harley, 1987
; Smith and Read, 1997
), it is likely that these symbiotic soil organisms have important influences on plant communities. An adequate understanding of the structure and dynamics of tallgrass prairie and other grassland plant communities requires a sound understanding of the underlying plant demographic processes and life history traits influencing plant population dynamics and how they are influenced by important biotic interactions such as mycorrhizal symbiosis.
Benefits from mycorrhizal fungi include improved access to limiting soil resources, especially immobile nutrients such as P, Cu, Zn, and ammonium, and these benefits may be significant. For example, Marschner and Dell (1994)
estimated that AM fungal hyphae could accumulate up to 80% of a plant's phosphorus requirements and 25% of a plant's nitrogen requirements. However, the responsiveness of plant species to AM colonization is highly variable (Hetrick, Wilson, and Todd, 1990, 1992
; Sanders, Koide, and Shumway, 1995
; Wilson and Hartnett, 1998
). Some species are obligate mycotrophs (i.e., nutrient acquisition and growth is severely limited in the absence of the symbiosis), while other species do not appear to be P-limited in the field even without mycorrhizal colonization (West, Fitter, and Watkinson, 1993
; Wilson and Hartnett, 1998
). While most mycorrhizal research has focused on individual host plant responses, recent work has indicated mycorrhizal symbiosis may influence host plant competitive ability, species composition, and diversity in herbaceous communities (e.g., Gange, Brown, and Sinclair, 1993
; Wilson and Hartnett, 1997
; Zobel and Moora, 1997
; Hartnett and Wilson, 1999
; Smith, Hartnett, and Wilson, 1999
).
The tallgrass prairie ecosystems of the eastern Great Plains are composed of a matrix of warm-season C4 and cool-season C3 grasses interspersed with a wide array of forbs. Although virtually all tallgrass prairie plant species form mycorrhizal associations, they differ considerably in their dependence on the symbiosis for nutrient acquisition and growth (Wilson and Hartnett, 1998
). The warm-season grasses and most forb species are extremely dependent (obligate mycotrophs), whereas cool-season grasses are significantly less dependent on the symbiosis (facultative mycotrophs) (Hetrick, Wilson, and Todd, 1990
; Wilson and Hartnett, 1998
). In addition, there is considerable variation in response to mycorrhizal symbiosis among different life history stages (e.g., seedling establishment, vegetative growth, and flowering) within species (Hartnett et al., 1994
; Wilson and Hartnett, 1997
). Previous research has suggested that, because co-occurring grasses and forbs in tallgrass prairie vary considerably in their dependency on mycorrhizal fungi for growth, variation in the activity of these fungi may strongly influence the competitive balance between obligately mycorrhizal-dependent, facultatively dependent, and nondependent plant species (Hartnett et al., 1993
; Hartnett and Wilson, 1999
). As a result of differential mycorrhizal dependency of co-occurring species and the strong competitive dominance of the most obligately mycotrophic species mycorrhizal activity in tallgrass prairie enhances dominance and reduces plant species diversity (Hartnett and Wilson, 1999
), a response opposite that of some other herbaceous communities (Grime et al., 1987
; Gange, Brown, and Farmer, 1990
; Gange, Brown, and Sinclair, 1993
). Because the competitive dominants in tallgrass prairie are the most strongly mycotrophic plant species, we hypothesized that suppression of AM fungi would increase the growth, reproduction, and relative densities of subdominant species in this system. Furthermore, we predicted that growth and demographic responses of these subdominant species to suppression of AM fungal activity in the field (in the presence of interspecific competition) may differ in direction and magnitude from their responses to mycorrhizal colonization under glasshouse conditions (in the absence of interspecific competition). To test these hypotheses, changes in stem densities, vegetative growth rates, and flowering of selected tallgrass prairie forbs (common, subdominant prairie species) were measured in a tallgrass prairie field experiment in which AM fungi were suppressed for six growing seasons.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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; nomenclature follows Great Plains Flora Association, 1986). Interspersed within this matrix is a highly diverse mixture of subdominant warm- and cool-season graminoid, forb, and woody species. Average monthly temperature ranges from a January low of –2.7°C to a July high of 26.6°C, and average annual total precipitation is 835 mm with 75% falling during the growing season (April–October). Konza Prairie contains 60 watershed units (average size = 60 ha), each subjected to different fire-frequency (1-, 2-, 4-, 10-, and 20-yr intervals) and grazing treatments (bison [Bos bison], cattle [Bos taurus], or ungrazed).
Two ungrazed watersheds, one annually burned in the spring (15 April ± 20 d) and one infrequently burned (approximately every 20 yr), were used in this study. The soil analysis from both these watersheds was typical of Konza soils with 3.5–6.0 µg/g P (bray test 1), pH of 6.0, 2.3–5.0% organic matter, 265–285 µg/g NO3-N, as determined by the Kansas State University Soil Testing Laboratory (Manhattan, Kansas, USA). To assess the AM fungi present in the native soil, spores were isolated from 100 g soil by wet-sieving, decanting, and centrifuging in a 20 : 40 : 60% sucrose density gradient (Daniels and Skipper, 1982
). Based on taxonomic criteria of Schenck and Perez (1990)
, spores of 13 species of mycorrhizal fungi were identified. In terms of spore densities, Glomus aggregatum Schenck & Smith emend. Koske, G. constrictum Trappe, and G. macrocarpum Tulasne & Tulasne were the dominant species of both watersheds.
In 1991, ten pairs of 2 x 2 m plots, each placed 2 m apart along a transect, were randomly located on an upland site (shallow, Florence cherty silt loam soil) within each watershed. Mycorrhizal suppression treatments (+benomyl, control) were assigned randomly to one member of each plot pair for a total of ten plots per treatment for each site. Benomyl was applied as a soil drench (7.5 L per plot) at the rate of 1.25 g/m every 2 wk throughout the growing season to the mycorrhizal suppression plots (+benomyl) beginning in 1991. The control plots received an equivalent amount of water only. Although the potential effects of benomyl on soil microflora components are not entirely known, benomyl is effective in reducing AM fungal colonization in the field (Fitter and Nichols, 1988
; Hartnett and Wilson, 1999; Smith, Hartnett, and Wilson, 1999
) and has no direct effects on the growth of a wide range of plants (Paul, Aryes, and Wyness, 1989
). Moreover, the effects of long-term (8 yr) applications of benomyl on microbial processes in soils from these plots were shown to be small relative to the effects on mycorrhizal root colonization (Smith, Hartnett, and Rice, 2000
).
In 1996, we assessed the effects of long-term mycorrhizal suppression on growth, flowering, and densities of three perennial forb species: Artemisia ludoviciana Nutt., Aster sericeus Vent., and Salvia azurea Lam. These three species all form multistemmed genets, are widespread across the tallgrass prairie landscape, but are patchily distributed and clearly subdominant to the abundant matrix grasses on tallgrass prairie. Stems (ramets) of each species were counted 7 wk after emergence within each 2 x 2 m plot in each site. Aster sericeus and S. azurea both form multistemmed genets with stems (ramets) arising from a branched caudex (Great Plains Flora Association, 1986). These forb species are characterized by a compact spatial arrangement of ramets within clones and the absence of rhizomes or stolons, similar to the caespitose growth form in graminoids (Briske and Derner, 1998
). Thus, for these two species both the number of genets (clones) per plot and ramets per genet were also assessed. Artemisia ludoviciana is a rhizomatous clonal perennial with widely dispersed ramets making the identity of individual genets impossible without excavation. Thirty-six individual ramets of each species were randomly selected within each plot and tagged. A. ludoviciana plants were not present in sufficient numbers on the plots (n = 3) in the infrequently burned site and, thus, were only assessed on the annually burned site.
Growth rates of the 36 individual ramets of each species were monitored using a nondestructive modification of standard techniques for determining relative growth rates (RGR) based on incremental increases in shoot volume rather than dry mass (Hunt, 1978
). Regression of shoot dry masses against shoot volume, derived from a separate set of randomly selected ramets, were used to assess the accuracy of shoot volume as a predictor of ramet aboveground biomass and RGR. Thirty-six randomly selected ramets were harvested from populations adjacent to each of the study plots in June 1996. Stem basal diameter, height, and biomass were measured for each ramet. Shoot volume was calculated as
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), and examined microscopically to assess percentage root colonization by mycorrhizal fungi using a petri dish scored in 1-cm squares (Daniels, McCool, and Menge, 1981
).
Effects of mycorrhizal suppression on mycorrhizal root colonization, ramet and genet densities, flowering, aboveground biomass, and ramet relative growth rates were analyzed separately for each plant species and site using one-way ANOVA (SAS v6.12; SAS, 1997
). When appropriate, differences between control and fungicide treatments were tested using least significant difference (LSD) tests. Effects of fungicide application on ramet growth, as estimated by stem volume or stem diameter, were analyzed for each site and species separately using repeated-measures ANOVA (PROC MIXED; SAS, 1997
) using an autoregressive covariance structure. Differences in ramet growth estimates with mycorrhizal suppression were also tested for each sampling date, plant, and site separately using one-way ANOVA. Differences between control and fungicide treatments were tested using LSD tests.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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0.05). Benomyl reduced mycorrhizal root colonization to an average of 4.2% in the mycorrhizal suppression plots, 
33% of the untreated control plots (13.7%). Mycorrhizal suppression did not affect percentage ramet survival from emergence to 19 wk (plant senescence) as there were no significant differences between control and fungicide-treated plants. Ramet survivorship was also similar among species examined in this study. Artemisia ludoviciana, A. sericeus, and S. azurea showed ramet survivorship rates of 74, 79, and 81%, respectively, with overall survivorship of 79%.
Suppression of mycorrhizal fungi resulted in large and significant (P 0.01) increases in the total ramet (stem) densities of A. ludoviciana, A. sericeus, and S. azurea (Table 1). After six growing seasons of mycorrhizal suppression, ramet densities in fungicide-treated plots were approximately double those of mycorrhizal plots. While the fungicide had no significant effect on the number of A. sericeus or S. azurea genets within each plot, number of ramets per genet significantly increased with mycorrhizal suppression (P 0.05), as compared to mycorrhizal controls (Table 1). Ramet growth rates and biomass of the three forb species varied in response to suppression of the symbiosis (Table 2). Although S. azurea ramet densities increased in response to fungicide application, the relative growth rate of ramets (based on stem volume) from emergence to peak ramet size, as well as final aboveground biomass (at 19 wk) of individual ramets was significantly lower with fungicide treatment (P 0.05) as compared to control plants on the annually burned watershed (Table 2). Also with annual burning, individual stem diameters of mycorrhizal plants were significantly (P 0.05) larger throughout the growing season, as compared to stems of mycorrhizal-suppressed plants (Fig. 1). However, in the infrequently burned sites, mycorrhizal suppression had no significant effect on ramet growth rate or size. By contrast, A. ludoviciana exhibited increases in ramet relative growth rates, final ramet biomass, and ramet density in response to fungicide application (Table 2). Aboveground ramet biomass of this forb, as estimated by stem volume, was greater in fungicide-treated plots each week throughout growing season (Fig. 2).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Previous studies (Hetrick, Wilson, and Todd, 1992
; Wilson and Hartnett, 1998
) have shown that the species studied here vary in their vegetative growth responses to mycorrhizal symbiosis under greenhouse conditions. Mycorrhizal dependency (or responsiveness, calculated as the proportional difference in biomass between mycorrhizal and nonmycorrhizal plants [Hetrick, Wilson, and Todd, 1990
]), of A. ludoviciana, A. sericeus, and S. azurea is 44, 76, and 87%, respectively. In the present study, these species also differed considerably in their growth and reproductive responses to mycorrhizal conditions in the field, but in ways that were not predictable from their responses when grown individually in the greenhouse.
The responses of Salvia azurea to mycorrhizal conditions included lower ramet densities, but greater relative growth rates, ramet size, and flower production compared to mycorrhizal suppressed conditions. This suggests a significant influence of mycorrhizal symbiosis on genet growth dynamics in this species. The observed pattern of fewer but larger ramets per genet under mycorrhizal conditions in S. azurea indicates greater intraclonal self-thinning, perhaps stimulated by increased resource availability associated with the mycorrhizal symbiosis. In A. sericeus populations, mycorrhizal colonization similarly resulted in decreased ramet densities and increased flower production, but it had no effect on ramet growth rates or size.
In A. ludoviciana populations under natural field conditions, mycorrhizae reduced ramet growth rates, size, and densities. This contrasts with responses of this species to mycorrhizae when grown as individual plants in the greenhouse, where it responds as a facultative mycotroph and shows some increased growth in the presence of AM fungi. This negative effect of mycorrhizae on plant performance in the field is most likely due to the fact that any potential direct beneficial effects of the symbiosis on A. ludoviciana are offset by greater competitive suppression by its interspecific neighbors, which are obligately mycotrophic and become much more strongly competitive under mycorrhizal conditions. Earlier studies of multispecies prairie microcosms conducted under greenhouse conditions (Wilson and Hartnett, 1997
), previous field studies Hartnett and Wilson, 1999
; Smith, Hartnett, and Wilson, 1999
; and this field study indicate that mycorrhizal symbiosis greatly increases the relative competitive ability of the dominant, warm-season grasses and that subordinate facultative mycotrophs competing with these highly mycorrhizal-dependent species experience competitive release when mycorrhizae are suppressed. In this study, all three forb species showed increased ramet densities with suppression of the symbiosis, presumably in response to a concomitant decline in abundance of the highly mycorrhizal-dependent dominant C4 grasses. The contrasting responses of these forb species grown individually in greenhouse studies with those observed here in natural communities supports the recent work of Facelli et al. (1999)
who emphasized that the effects of AM symbiosis at the individual plant level cannot be assumed to reflect effects at the population level, because of the influence of density-dependent processes. These results also support conclusions of a previous field experiment involving germination and emergence of tallgrass prairie species established from seed (Hartnett et al., 1994
) that responses to mycorrhizal symbiosis vary among different life history stages within species.
The patterns of responses of these species to mycorrhizae differed considerably between the two sites of contrasting fire regime. For example, in S. azurea the increase in ramet size under mycorrhizal conditions was only apparent in the annually burned site. This may be in response to a nutrient flush associate with burning (Knapp and Seastedt, 1986
). Nutrient pulses, such as those associated with burning, are likely to be especially important with resources of low mobility, such as phosphorus. Mycorrhizae have been shown to increase intraspecific competition through an increase in phosphorus availability and may have an important role in altering the dynamics of soil resources (Watkinson and Freckleton, 1997
; Facelli et al., 1999
). Mycorrhizal fungi provide enhanced nutrient acquisition, notably phosphorus, thereby giving colonized plants a competitive advantage, as they are able to capitalize on elevated nutrient levels following burning. In the absence of this nutrient flush, ramets of both the mycorrhizal and fungicide-treated plots in infrequently burned prairie were smaller than those in the annually burned mycorrhizal controls.
Mycorrhizae had a positive effect on flowering of both A. sericeus and S. azurea in infrequently burned prairie, but mycorrhizae had no effect on flowering in the annually burned watershed. Mycorrhizal plants have been shown to increase in seed number, seed mass, and P and N content as compared to nonmycorrhizal counterparts (Lu and Koide, 1994
). Enhanced efficiency of nutrient acquisition by mycorrhizal plants may allow more resources to be allocated to reproduction in the infrequently burned site. By contrast, with annual burning, the high dominance of the warm-season grasses may be limiting other resources not affected by mycorrhizae, and therefore, few flowers were produced regardless of mycorrhizal treatment. While this effect may be partially a result of other site differences not associated with burning, the trend of increased flowering in response to infrequent burning is consistent with earlier studies of fire effects in tallgrass prairie (e.g., Knapp, 1984
; Hartnett, 1990, 1991
). In general, these patterns of plant responses to mycorrhizae in tallgrass prairie sites of contrasting burn regimes indicate that the interaction of this large-scale disturbance (fire) and mycorrhizal symbiosis modulates the intensity and patterns of interspecific competition between and among tallgrass prairie grass and forb species.
Based on this and previous studies, it is apparent that arbuscular mycorrhizae can influence the coexistence and relative abundances of plant species both directly and indirectly. Direct effects include the modification of plant traits (e.g., seed reproduction, genet establishment, ramet growth, and survivorship) by AM fungi and, possibly, by transfer of resources via interplant hyphal connections (Fischer-Walter et al., 1996
). Indirect mechanisms include the possible impact of AM fungi on neighborhood interactions. Francis and Read (1995)
observed that while mycorrhizal fungi may indeed have a favorable impact on some species within a community, they are at the same time discriminating against others. The conflicting results of previous experiments assessing effects of AM symbiosis on plant communities (Allen and Allen, 1990
; Eissenstat and Newman, 1990
; Allsop and Stock, 1992
; Moora and Zobel, 1996
; Hartnett and Wilson, 1999
; Smith, Hartnett, and Wilson, 1999
) are likely explained by differences in interspecific patterns of mycorrhizal dependencies and resultant differences in the balance between direct positive effects of mycorrhizae on host plant growth and indirect negative effects mediated through altered competitive interactions. Furthermore, our results suggest that in grasslands, this balance and, hence, the role of mycorrhizal symbiosis, are also influenced by changes in plant resources driven by large-scale processes such as fire.
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FOOTNOTES |
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4 Author for reprint requests (gwtw{at}ksu.edu
).
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