The effect of fire, mowing and fertilizer amendment on arbuscular mycorrhizas in tallgrass prairie.
Arbuscular mycorrhizal (AM) fungi are obligate symbiotic fungi that form mutualistic relationships with most terrestrial plant species. AM fungi are ubiquitous in most soils and are believed to be among the most abundant soil fungi (Gerdemann and Nicolson, 1963). In the tallgrass prairie, where inorganic phosphorus levels are typically low, arbuscular mycorrhizas are widespread, and most grasses and forbs are highly colonized by these fungi (Anderson et al., 1984; Miller, 1987). Greenhouse and field studies indicate that many tallgrass prairie plants benefit significantly from this symbiosis (Hetrick et al., 1990a, 1992; Wilson and Hartnett, 1998). Mycorrhizal plants typically have higher uptake of some inorganic nutrients and water, and are more tolerant of many kinds of environmental stresses than are nonmycorrhizal plants (Harley and Smith, 1983; Nelsen, 1987). Previous studies have shown that AM fungi influence the demography and competitive relationships of tallgrass prairie grasses and forbs (Hartnett et al., 1993, 1994; Wilson and Hartnett, 1997)
AM fungal species composition can be affected by edaphic factors such as pH, organic carbon, available phosphorus (Rathore and Singh, 1995), total soil carbon and nitrogen (.Johnson et al., 1991) and by changes in plant community composition (Johnson et al., 1991; Aziz et al., 1995). Decreases in species diversity and abundance in AM fungal communities have been reported when natural ecosystems are disturbed by human activities (Johnson and Pfleger, 1992; Giovannetti and Gianinazzi-Pearson, 1994). Grassland management practices such as burning, mowing, grazing and fertilization can influence the composition of AM fungi in tallgrass prairie (Dhillion et al., 1988; Bentivenga and Hetrick, 1992; Dhillion and Anderson, 1993a, b) and in other grasslands. However, the effects of these factors on AM fungal populations and mechanisms controlling fungal species composition and diversity are poorly understood, and few studies have considered long-term effects of these management practices. Although these fungi have been considered generally non-host-specific, strong evidence of host-dependent differentiation of AM fungal communities was observed recently by Bever et al. (1996).
Bentivenga and Hetrick (1992) examined the AM fungal species composition in Kansas tallgrass prairie plots subjected to annual burning, mowing and N and P fertilization regimes 1 y and 3 y after treatment initiation, but found no significant effects of these management practices on AM fungal species composition. However, significant changes in soil and/or host plant properties that may influence these fungal communities or the mycorrhizal symbiosis may emerge under different management regimes over longer time scales. Thus, responses of AM fungal populations may become more apparent over several seasons. The objective of our research was to examine the long-term effects of these prairie management practices, alone and in combination, on the fungal community of these same tallgrass prairie plots after ten y. We hypothesized that gradual cumulative changes in resource limitation, and/or in host plant growth and nutrient status over several years, would result in significant changes in fungal communities and the development of the mycorrhizal symbiosis. We assessed AM fungal species richness, evenness of species abundances and diversity and measures indicative of the development of the mycorrhizal symbiosis including total spore abundance, root colonization and extraradical mycorrhizal hyphae (EMH) development. Understanding these effects is important because, whether mediated by changes in soil properties or host plants, changes in mycorrhizal communities and the function of this symbiosis resulting from different management practices may have large effects on the structure and dynamics of host plant communities in grasslands.
MATERIALS AND METHODS
Study site. - The study was conducted at the Konza Prairie Research Natural Area (KPRNA) near Manhattan, Kansas. KPRNA is a 3547 ha native tallgrass prairie preserve owned by The Nature Conservancy and Kansas State University and managed for long-term ecological research by the Division of Biology. The field plots sampled in this study were initiated in 1986 in an area mapped as Irwin silty clay loam (fine, mixed, mesic, Pachic Argiustolls). Available N (1.64 g N [kg.sup.-1]) and P (7.2 g P [kg.sup.-1]) are both low.
The vegetation in the area is typical of native tallgrass prairie and is dominated by a matrix of [C.sub.4] grasses such as big bluestem (Andropogon gerardii Vitm.), little bluestem (Schizachyrium scoparium (Michx.) Nash) Indiangrass (Sorghastrum nutans (L.) Nash), and switchgrass (Panicum virgatum L.) with subdominant [C.sub.3] grasses such as Junegrass (Koeleria pyramidata L.), Kentucky bluegrass (Poa pratensis L.), Smooth bromegrass (Bromus inermis Leyss.) and Canada wild rye (Elymus canadensis L.). A diverse array of interstitial forbs occur within this grass matrix, including many species of composites, legumes and other taxa. The vascular flora of KPRNA includes over 500 species representing 93 families (Freeman and Hulbert, 1985).
Experimental design. - As part of the KPRNA long-term ecological research (LTER) program, 64 plots (12.5 m x 12.5 m) were established in April 1986. These plots were arranged in a split-split plot design with main plots arranged in a randomized complete block, with four blocks. Main plots correspond to the prescribed burning treatments, subplots to mowing treatments and sub-subplots to fertilization treatments. One half of the plots in each block were burned annually in late April or early May. One half of the burned and unburned plots were mowed once each year in late June. There were four fertilizer treatments, applied annually in late April or early May: N at 10 g N [m.sup.-2], applied as ammonium nitrate pellets, P at 1 g P [m.sup.-2], applied as superphosphate, N+P (at the above rates) and a nonamended reference. This amount of nitrogen was in excess of plant needs and minimized nitrogen immobilization (Seastedt et al., 1991), resulting in increased root nitrogen concentration and total root mass in fertilized plots, after four years of treatment (Benning and Seastedt, 1997). Phosphorus was added at a rate which maintained a 1:10 P:N ratio typical of native grassland soils (Stevenson, 1986).
Arbuscular mycorrhizal fungal spore collection. - In August 1995, soil samples were collected from each plot using a soil corer (5 cm diam x 15 cm depth). A sampling depth of 15 cm was chosen because AM propagule densities are generally greatest in the surface 15 cm (An et al., 1990). Three cores per plot were collected randomly anti manually homogenized. Soils were placed in polyethylene bags and stored at 4 C until they were processed. AM fungal spores were extracted from 100 g dry weight of soil using wet-sieving and sucrose density gradient centrifugation (Daniels and Skipper, 1982). The extracted spores were observed and counted under a light microscope and identified to species following the descriptions of Schenck and Perez (1990). Only spores which appeared to be viable (based on color, shape, surface conditions and examination of spore contents) were counted. Voucher specimens of the species sampled are maintained at Kansas State University.
The relative density of each fungal species was estimated based on spore counts. AM fungal species richness, Brillouin index of species diversity and species equitability were calculated for mycorrhizal fungal community analysis. Species richness (R) is the number of species detected in a treatment. Because not all AM fungal species sporulate to the same degree under a given set of environmental conditions, not all fungal species present have an equal probability of detection via the sampling method. Thus, Brillouin's index is a more appropriate diversity index than the Shannon index which assumes an equal probability of capture/encounter of species. Study plots were replicated (n = 4 per treatment combination), all located on the same soil types and similar in initial (pretreatment) plant community composition. In addition, relative rather than absolute spore abundances were used in the analyses. Thus, differences in composition and diversity of AM fungi can confidently be attributed to treatment effects. Brillouin indices of species diversity (H) and species evenness (E) (Magurran, 1988) were calculated according to the following formulas:
[Mathematical Expression Omitted]
N = Total number of individuals in entire community sample
[n.sub.1] = Number of individuals belonging to species 1
[n.sub.2] = Number of individuals belonging to species 2 (etc.)
E = H/[H.sub.max]
[H.sub.max] = Maximum value of H
[Mathematical Expression Omitted]
S = Number of species in sample
I = Integer value of N/S
J = Remainder of individuals = [N - (S) (1)]
Root colonization and extraradical mycorrhizal hyphae. - Live roots were isolated from the soil samples, washed free of soil and stained in trypan blue (Phillips and Hayman, 1970). Roots were then examined microscopically using a petri dish scored in 1 cm squares to assess the percentage of roots colonized by AM fungi (Daniels et al., 1981).
Quantification of extraradical mycorrhizal hyphae followed the protocol of Miller et al. (1995). Two undried 10 g subsamples of each core (with roots, rhizomes and large organic debris removed) were placed in separate beakers of sodium hexametaphosphate solution (35.7 g [1.sup.-1]), soaked overnight, sonicated for 20-25 s at 120 W and then diluted (1:20). A 20-ml aliquot of the diluted suspension was centrifuged at 1000 g, and the pellet was resuspended in 50% glycerol with a vortex mixer. After centrifugation at 75 g for 30 s, the supernatant was filtered through a 20 [[micro]meter] mesh filter. The mesh filter was placed in a staining solution of lactic trypan blue, and hyphae were resuspended with vortex mixer. After 1.5 h, the staining solution was quantitatively filtered through a cellulose nitrate membrane filter with a 0.8 [[micro]meter] pore size.
When dry, filters were mounted on slides with immersion oil and were viewed at 250x. One hundred random fields of view were scored by the gridline intercept method and converted to hyphal lengths (Newman, 1966). Hyphae were recognized as mycorrhizal based on morphological characteristics (e.g., Nicholson, 1959).
Plant species composition. - Canopy cover of vascular plants in a centrally located 10 [m.sup.2] circular area in each study plot was visually estimated using categories described by Daubenmire (1959), modified by the addition of a [less than]1% category. Thus, the following categories were used: 1 = [less than]1%; 2 = [greater than]1-[less than]5%; 3 = 5-25%; 4 = 25-50%; 5 = 50-75%; 6 = 75-95%; anti 7 = 95-100%. Plots were surveyed in late August. The mid point of the canopy cover categories were square root arcsine transformed and analyzed by ANOVA.
Statistical analysis. - Analysis of variance was performed using SAS (SAS Institute, Inc., 1989) to evaluate the effects of fire, mowing and fertilization on percent mycorrhizal root colonization, extraradical mycorrhizal hyphae, AM fungal species richness, evenness, species diversity and abundance of each AM fungi species and total spore numbers. Before analysis, fungal species community data were rank-transformed (Conover and Iman, 1981), and percentage mycorrhizal root colonization and extraradical hyphae data were subjected to [log.sub.10] transformation. Within each treatment, correlation and stepwise regression analyses were used to examine relationships between mycorrhizal fungal spore abundance and plant species composition. Plant species that were present in over 10% of the plots were included in treatment correlation and stepwise regression analysis.
AM fungal spore abundance and species diversity - A total of 17 species of AM fungi were isolated from the study sites, including 13 species within the genus Glomus, and one species each of Acaulospara, Entrophospora, Gigaspora and Scutellospora. Glomus etunicatum was the most abundant AM fungal species in all treatments sampled (Table I).
Spring burning significantly reduced AM fungal species diversity (Table 2, [ILLUSTRATION FOR FIGURE 1 OMITTED]). This reflected primarily a decrease in species richness, as the evenness of fungal species abundances was not significantly affected by burning (Table 2, [ILLUSTRATION FOR FIGURE 2 OMITTED]). There were no significant effects of mowing or fertilizer amendment treatments on AM fungal species diversity, however a significant burn x mowing interaction reduced both species diversity and evenness (Table 2, [ILLUSTRATION FOR FIGURE 2 OMITTED]). Fungal species richness was significantly increased by nitrogen addition, [TABULAR DATA FOR TABLE 1 OMITTED] burn x nitrogen interaction, nitrogen x phosphorus interaction, and burn x mow x phosphorus interaction (Table 2). Addition of nitrogen significantly increased species richness in both burned, and burned and mowed plots, but not in unburned plots [ILLUSTRATION FOR FIGURE 3 OMITTED]. In general, the various management treatments had larger effects on the species richness component than on the evenness component of AM fungal species diversity.
Abundance (total spore numbers) was significantly increased by spring burning (Table 2, [ILLUSTRATION FOR FIGURE 4 OMITTED]). There was a significant burn x mowing interaction, reflected in a greater burning-induced increase in fungal abundance in plots that were burned only, compared to burned and mowed plots (Table 2, [ILLUSTRATION FOR FIGURE 4 OMITTED]). Within each of the various burn and mowing treatments, there were no significant effects of nitrogen or phosphorus amendments on total spore abundance [ILLUSTRATION FOR FIGURE 4 OMITTED]. However, a significant burn x nitrogen interaction resulted from a large increase in total spore numbers with burning only, but no significant increase when burned plots were also fertilized with nitrogen [ILLUSTRATION FOR FIGURE 4 OMITTED].
AM fungal species responses. - AM fungal species differed substantially in both the direction and magnitude of their responses to the various treatment combinations (Table 3). Burning significantly decreased the abundance of Glomus aggregatum and significantly increased the abundances of G. etunicatum and G. fecundisporum (Table 3). In addition, the abundances of these species were influenced by several significant treatment interactions (Table 3). The only fungal species that responded to the mowing treatments was G. constrictum, which significantly decreased in abundance in mowed relative to unmowed plots (Table 3). Gigaspora gigantea and Glomus mosseae increased with nitrogen addition and Entrophospora infrequens decreased with the same treatment (Table 3). Only Glomus rubiforme [TABULAR DATA FOR TABLE 2 OMITTED] showed a significant decrease in spore numbers with addition of phosphorus. No other species showed significant responses to the phosphorus treatment.
Overall, two species, Glomus etunicatum and G. fecundisporum, showed a large and significant increase in abundance in response to burning, nine other species showed trends of greater abundance in burned plots relative to unburned plots and only one species, G. aggregatum, declined significantly in response to burning [ILLUSTRATION FOR FIGURE 5 OMITTED]. Thus, the increase in overall abundance (total spore number) with burning was not attributable to large increases in just one or two species. Two species, Glomus clarum and G. sinuosum, were only present in unburned plots, and one species, G. macrocarpum, was only found in burned sites. However, these three were all rare species that did not contribute significantly to total spore abundance.
EMH and root colonization. - In contrast to their large effects on AM fungal community composition and diversity, burning and mowing had no significant effects on mycorrhizal colonization of roots or extraradical mycorrhizal hyphal development (Table 9). Nitrogen fertilization, however, significantly increased both EMH and percent root colonization by 15% and 23%, respectively. Conversely, EMH growth was significantly decreased by phosphorus addition, from 26.1 [mg.sup.-1] soil of hyphae in reference plots to 21.6 [mg.sup.-1] in P amended plots. In addition, ANOVA of EMH development revealed several significant interactions (Table 2). Addition of nitrogen resulted in a large increase in EMH in mowed and unburned plots, but not in unmowed plots or mowed and burned plots. Addition of phosphorus resulted in a significant decrease in EMH in mowed plots, but not in unmowed plots. Nitrogen addition significantly increased percent mycorrhizal root colonization from 16.4% in unfertilized plots to 21.3% in N amended plots. Other than this large influence of nitrogen, there were no other treatment main effects or interactions influencing root colonization by AM fungi.
Correlations of fungal and plant species compositions. - Glomus aggregatum and G. clarum were positively correlated with forb cover and negatively correlated with [C.sub.4] grass cover. Abundance of G. aggregatum was significantly reduced in annually burned plots (Table 3) where forb cover was lowest.
Acaulospora longula, Glomus fecundisporum and G. macrocarpum and an unidentified Glomus species were positively correlated with cover of the dominant tallgrass prairie grass A. gerardii (r = 0.50, P = 0.02). Glomus mosseae and the unidentified Glomus species were negatively correlated with the introduced exotic grass species Andropogon bladhii (r = -0.47, P = 0.07). However, 10 of the 17 fungal species showed no correlation with any host plant species. In fact, the most abundant and frequent fungal species such as G. etunicatum, E. infrequens and G. constrictum displayed no host preference in any of these treatment plots.
Tallgrass prairie management practices including burning, mowing and nutrient fertilization significantly influence the abundance and species diversity of mycorrhizal fungi and the development of the mycorrhizal symbiosis with prairie plants. Spring burning reduced AM fungal species diversity, but increased total AM fungal spore abundance. Nitrogen fertilization increased both EMH development and root colonization, whereas phosphorus addition decreased EMH growth.
Environmental factors such as soil moisture, temperature, carbon, nitrogen, pH and host plant species influence mycorrhizal fungal communities (St. John and Coleman, 1983; Wang et al., 1985; Stahl and Christensen, 1991; Bever, 1996). In successional grasslands in Minnesota, Johnson et al. (1991, 1992) found that fungal species composition changed with changing plant species and soil factors during succession, with highest AM fungal species diversity at successionally intermediate sites. Gryndler and Lipavsky (1995) reported that long-term phosphate over-fertilization influenced AM fungal species composition and Johnson et al. (1991) found that mycorrhizal species diversity, was positively correlated with soil C and N in successional grasslands. Grassland management practices may significantly influence AM fungal communities through their effects on these soil factors. For example, spring fires in tallgrass prairie significantly increase soil temperatures and alter soil moisture during the growing season (Knapp and Seastedt, 1986). Frequent spring burning also decreases available nitrogen and increases soil C:N (Ojima et al., 1994). Grazing by large ungulates may also influence AM fungal communities through changes in plant carbon and nitrogen, and through soil compaction and changes in soil structure and water availability.
Tallgrass prairie is often N-limited (Owensby et al., 1969) particularly when frequently burned (Seastedt et al., 1991), despite low levels of inorganic P in the soil. The obligate mycorrhizal symbiosis of dominant [C.sub.4] tallgrass prairie grasses and most forbs overcomes any inherent P-limitations (Hetrick et al., 1990a, 1992). With N fertilization, the low levels of inorganic P in tallgrass prairie can become a limiting factor to plant growth, even when the symbiotic fungi are present (Hetrick et al., 1989). In our study, N fertilization significantly increased host plant root colonization and EMH development in plots that were unburned and unmowed. This increase in hyphal growth presumably compensates for the increased demand of P acquisition as N becomes less limiting and plant biomass production increases in response to N fertilization.
Although there were no significant independent effects of fertilizer amendment on spore abundance or species diversity, nitrogen amendment increased total spore abundance in burned plots. This interaction is not surprising as N-limitation conditions of the tallgrass prairie are intensified with annual burning (Seastedt et al., 1991; Ojima et al., 1994). Therefore, fertilization affected spore populations in the short term, but its effect was not large enough to change species composition over a longer (10-y) time scale.
The removal of significant amounts of aboveground plant tissues by mowing or repeated grazing may reduce the available carbon supply from the host plant to the fungi, thus influencing colonization and hyphal development. However, there were no significant effects of mowing on root colonization, EMH or species diversity and abundances in this study. In previous studies, grazing or clipping showed either no effects (Bethlenfalvay et al., 1985; Wallace, 1987), or decreases in root colonization (Bethlenfalvay and Dakessian, 1984, Hetrick et al., 1990b; Trent et al. 1988). In a study with two semiarid tussock grasses, Allen et al. (1989) found no significant effect of clipping on spore abundance, but total spore numbers were higher in the rhizosphere of the more grazing-tolerant species.
In most years, soil in burned prairie maintains higher temperatures than soil in unburned sites in the season following burning (Hulbert, 1988). In addition, soil nutrient availability, soil organisms and plant growth rates are all influenced by burning. These factors also affect mycorrhizal fungal sporulation and plant and fungal community structure. However, previous reports on the effects of burning on AM fungi varied. Mycorrhizal root colonization has been reported to increase (Bentivenga and Hetrick, 1991), decrease (Rashid et al., 1997) and be unaffected (Anderson and Menges, 1997) by burning. These conflicting results may be a reflection of the dominant host plants or soil type of these communities, or the amount of time after burning that sampling is conducted. Bentivenga and Hetrick (1991) reported an increase in AM colonization 16 d after burning, but no effect 32 d after burning, suggesting only a transient stimulation of mycorrhizal activity. Thus, it is not surprising [TABULAR DATA FOR TABLE 3 OMITTED] there were no burning effects on AM root colonization in our study, as samples were taken 5 mo after burning.
Disparity among previous studies is also evident for burning effects on AM fungal species abundances and composition. Spore abundances have been shown to decrease (Dhillion and Anderson, 1993b), increase (Vilarino and Arines, 1991) or remain unaffected by burning (Bentivenga and Hetrick, 1992; Rashid et al., 1997). In our study, burning increased AM fungal species diversity and decreased spore abundance. However, whether these changes are due to postfire changes in the soil resources or microclimate, or to shifts in host plant species composition, is unclear. As host-plant community composition shifts in response to these management treatments, mycorrhizal fungal species may also shift if these fungi have some degree of host specificity. A growing body of work, including this study, suggests that some ecological specificity, or the preferential association of certain fungi with certain hosts, may occur (Harley and Smith, 1983; Sanders and Fitter, 1992; Bever et al., 1996). The interspecific differences in the levels of colonization by host plants (Molina et al., 1978; Koske, 1981) and different growth responses of tallgrass prairie grasses and forbs to mycorrhizal colonization (Hetrick et al., 1990a, 1992; Wilson and Hartnett, 1998) indicates that some specificity occurs in these grassland communities.
In our study, some fungal species were positively correlated with certain host plants. Several species were positively associated with dominant [C.sub.4] grasses, whereas others were negatively associated with these grasses but positively associated with forbs. Two species exhibited significant negative correlations with the cover of the nonnative grass Andropogon bladhii. Because these significant correlations were observed within treatments, this suggests significant effects of the host plant species themselves (e.g., Andropogon gerardii, [C.sub.4] grasses, [C.sub.3] grasses, forbs, etc.) independent of the effects of the various management treatments. Further work is necessary to determine whether host-specificity of AM fungi in these grasslands is generally important at the plant species level or at the broader level of these growth form classes.
Spore densities do not necessarily reflect the functional importance of individual species within the mycorrhizal fungal community to the symbiosis with plants. Some fungi may be prolific sporulators even when they are in relatively low abundance within the plant roots. For example, sporulation of Glomus aggregatum is prolific and this species is common in prairie soils (Gibson and Hetrick, 1988; Johnson et al., 1992; this study), yet it has little effect on the growth of the dominant prairie grass Andropogon gerardii, in greenhouse studies (Hetrick and Wilson, 1991). Further, because roots of a given host plant may be colonized by more than one AM fungal species (Sanders and Fitter, 1992) and temporal shifts occur in sporulation between AM fungal species (Wilson and Trinick, 1982), it is likely that the spore abundances of some species may be a reflection of differential sporulation frequencies rather than changes in their overall abundances within plant roots. However, in our study, samples collected from these sites in both May and July 1996 had similar AM species composition and relative dominance (N. C. Johnson, pers. comm.), indicating that the fungal community, structure does not change significantly during the growing season. Thus, our results indicate that these management practices caused the significant effects on the AM fungal community, composition, as well as fungal associations within the plant roots and rhizosphere although effects of these management practices on the composition and diversity of fungi functioning symbiotically with the plants may be different.
An understanding of how different environmental factors and management practices influence AM fungal populations is important because species of these fungi have been reported to vary greatly in their effects on plants, ranging from strongly mutualistic to neutral to pathogenic (Carling and Brown 1980; Schubert and Cammarata, 1986; Johnson et al., 1992 1997). Tallgrass prairie grass and forb species differ greatly in their dependency and growth responses to mycorrhizal colonization, ranging from obligate - to facultative - to nonmycotrophic (Hetrick et al., 1990a, 1992; Wilson and Hartnett, 1998). Given these differential mycorrhizal species effects and plant species responses, and the strong influence of the symbiosis on plant growth and responses to competitors, herbivores and other biotic and abiotic factors (Hartnett et al., 1993; Hetrick et al., 1990, 1994; Pedersen and Sylvia, 1996), the patterns of AM spore abundances and diversity revealed in this study indicate that effects of management practices on tallgrass prairie aboveground plant communities are likely mediated, in part, through their effects on mycorrhizal fungi and belowground processes.
Acknowledgments. - The authors would like to thank Gene Towne for conducting the aboveground plant community sampling on these plots. This research was supported by NSF grant DEB-9317976 to DCH and grant BSR 9011662 for Long-Term Ecological Research on Konza Prairie. This paper is contribution No. 97-304-J from the Kansas Agriculture Experiment Station, Kansas State University, Manhattan, Kansas.
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|Author:||Eom, Ahn-Heum; Hartnett, David C.; Wilson, Gail W.T.; Figge, Deborah A.H.|
|Publication:||The American Midland Naturalist|
|Date:||Jul 1, 1999|
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