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Department of Plant Biology, University of Minnesota, 1445 Gortner Avenue, St Paul, Minnesota 55108, and Department of Botany, The Field Museum, 1400 South Lakeshore Drive, Chicago, Illinois 60605
Iris Charvat
Department of Plant Biology, University of Minnesota, 1445 Gortner Avenue, St Paul, Minnesota 55108
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMETHODSRESULTSDISCUSSIONLITERATURE CITED |
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The inoculum of ectomycorrhizal (EM) fungi was examined in a 16 y long nitrogen fertilization experiment maintained in a temperate oak savanna. To measure EM fungal inoculum, bur oak seedlings were grown in three types of bioassays: (i) intact soil cores that measure inoculum such as spores, mycelia and mycorrhizal roots; (ii) resistant propagule bioassays that measure inoculum types resistant to soil drying; and (iii) previously mycorrhizal root bioassays that measure the ability of EM fungi to colonize new roots from mycorrhizal roots. Colonization of bur oak seedlings was characterized by morphotyping and where necessary by restriction analysis and internal transcribed spacer (ITS) sequencing. Fourteen morphotypes were found in intact soil core bioassays with species of Cortinarius, Cenococcum and Russula abundant. Five morphotypes were found in resistant propagule bioassays with Cenococcum, a thelephoroid morphotype and a Wilcoxina-like ascomycete abundant and frequent. In intact soil core bioassays total percent root colonization and number of morphotypes were not affected by N supply in 2000 and 2001. However the composition of EM fungi colonizing oak seedling roots was different with increased N supply such that Russula spp. (primarily Russula aff. amoenolens) were most abundant at the highest level of N supply. Dominant Russula spp. did not colonize any roots in resistant propagule bioassays but did colonize oak seedling roots from previously mycorrhizal roots. Results suggest that in this savanna N supply can influence the kinds of inoculum propagules present and thereby might affect the dynamics of ectomycorrhizal communities by differentially influencing reproductive and colonization strategies.
Key words: Cenococcum, Cortinarius, ectomycorrhizal fungi, inoculum bioassay, nitrogen, oak seedlings, Russula
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONLITERATURE CITED |
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), the impact of increased N on the colonization strategies and inoculum of EM fungi is not clear. EM fungi grow from a diverse pool of propagules to colonize host plant roots. Colonization of roots can occur by the development of hyphae from spores produced in sporocarps or sclerotia and also by contact with hyphae growing from previously colonized roots (Brundrett et al 1996). Variation in colonization strategy by way of differences in inoculum likely contributes to the dynamics of EM communities and to the maintenance of their impressively high species diversity (Taylor and Bruns 1999). However, how environmental factors influence EM inoculum and how this in turn is related to EM fungal communities is not known.
EM fungal communities respond to increased N with decreased production and diversity of sporocarps aboveground and radical shifts in the species composition of EM fungi colonizing roots below-ground (Avis et al 2003; Lilleskov et al 2001, 2002; Peter et al 2001; Taylor et al 2000). How N increase affects EM colonization of roots from inoculum has not been investigated although inoculum abundance and composition might be directly related to the responses of the above and belowground components of EM communities. Considering the dramatic decreases in sporocarp production and diversity caused by increased N, EM fungi dependent upon inoculum produced in sporocarps may decrease in abundance. EM fungi that colonize new roots primarily by infective hyphae or from previously mycorrhizal roots also may decrease as increased N supply can decrease the production of external mycelium by EM fungi (Nilsson and Wallenda 2003) and alter the production of EM host roots (Avis 2003).
This study examined the effect of increased N supply on the inoculum of EM fungi of an oak savanna and was conducted parallel to a study of the EM sporocarp and root colonization responses at the same site (Avis et al 2003). Inoculum was measured with greenhouse bioassays of oak seedlings grown in intact soil cores collected from a long-term field fertilization experiment. Intact soil core bioassays provide a measure of inoculum that may come from a range of sources including spores, sclerotia, hyphae of mycelial networks, and previously colonized roots. To identify whether there were EM fungi that produced propagules tolerant to the periodic fires and drought this savanna can experience, we also examined how N supply impacts propagules tolerant of prolonged soil drying (i.e., resistant propagules). Furthermore we tested whether two EM fungi found important in intact soil bioassays could colonize new roots from roots previously colonized by EM fungi. We hypothesized that oak seedling root colonization in the bioassays should be lower where N supply is high because N increase can decrease the sources of inoculum (sporocarps, soil hyphae and mycorrhizal roots). This hypothesis also predicts that fewer species should be found colonizing roots of bioassay seedlings because lower numbers of EM fungal species produce inoculum under high N conditions.
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METHODS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONLITERATURE CITED |
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). The oaks are interspersed by tall-grass prairie grasses and herbs and, in some locations, by a third EM host plant, Corylus americana Walter. At this study site the savanna is maintained by prescribed burns two of every three y (Reich et al 2001). The bur oaks are approximately 50–150 y old, but the pin oaks are generally younger, 35–70 y old. Mean annual temperature is 6 C and mean annual precipitation 79 cm with the majority occurring from May to September. The average annual inorganic N wet deposition 1999–2001 was 0.53 g m–2 (National Atmospheric Deposition Program 2003).
In this oak savanna, soils and inoculum were collected from within treatment plots of a long-term fertilization experiment that began in 1983 (Tilman 1987). Nine plots 20 m wide and 50 m long were placed across this savanna and randomly assigned to one of two fertilizer treatments or unfertilized control. Unfertilized 1 m boundary areas separated adjacent plots. The fertilizer treatments include two levels of nitrogen: 5.4 and 17.0 g N m–2 y–1 added as NH4NO3 (commercial 34–0–0) "slow release" pellets. To offset indirect effects of N addition, each fertilization treatment also received equal background levels of P, K, Ca, Mg, S and citrate-chelated trace metals applied in these forms and rates: P2O5, 20.0 g m–2 y–1 (as commercial 0–46–0 fertilizer); K2O, 20.0 g m–2 y–1 (commercial 0–0–61); CaCO3, 40.0 g m–2 y–1 (as fine-ground commercial lime); MgSO4, 30.0 g m–2 y–1 (U.S. Pure Epsom salts); CuSO4, 18.0 µg m–2y–1; ZnSO4, 37.7 µg m–2 y–1; CoCO2, 15.3 µg m–2 y–1; MnCl2, 322.0 µg m–2 y–1; NaMoO4, 15.1 µg m–2 y–1; and H3BO3, 12.0 µg m–2 y–1 (Tilman 1987). Control plots remained unfertilized. Fertilization occurred twice annually in early May and in late June. After 16 y of fertilization, net N mineralization increased 20–40% but the ratio of N to other nutrients did not change significantly and pH did not decrease (Avis et al 2003).
Intact soil core bioassays.— –
Before collection of soil samples, black 5
inch standard pots (Belden Plastics, St Paul, Minnesota) were surface sterilized in a 10% bleach solution for 10 min. Polyester fiberfill was placed in the base of each pot to prevent loss of soil. Pots were sealed in plastic bags and transported to the sampling site.
On a single day during the first week of November 2000 and 2001 intact soil cores were taken from eight previously established, randomly placed sampling points within the nine treatment plots. At each sampling point, one soil core (approximately 12.5 cm diam and 12.5 cm deep) was excavated intact with a shovel and carefully placed in a pot so as not to disturb the intact structure of the core (method adapted after Brundrett et al 1996). The shovel was cleaned with 10% bleach and wiped clean between each sampling point. Potted cores were then placed in plastic bags, sealed and transported to a room at 4 C for 2 wk. Additional soil also was collected at this time and steam sterilized to serve as a check on contamination during setup and bioassay growth in the greenhouse. After cold storage, the potted cores were transported to a greenhouse and placed on saucers on greenhouse benches. Steam-sterilized (100 C for 1 h and repeated after 24 h) soil to check for contamination was placed in pots at the same time. Bur oak acorns previously were surface sterilized in 10% bleach solution for 5 min and germinated in moist sterile towels. One acorn exhibiting radicle emergence then was placed on top of each potted core or steam-sterile soil pot in a small furrow made in the center of each core such that the acorn was placed just under the surface of the soil. The tool used for making the furrow was soaked in a 10% bleach solution between each sample. All germinating acorns that did not grow after 2 wk were replaced with new acorns in the manner described above. All containers were weeded of any plants except the oak seedlings. Approximately 100 mL of water was added to the saucers twice per week. Bioassays were maintained for 16 wk at ~25 C with 14 h daylight under high intensity discharge lamps in the greenhouse.
Resistant propagule bioassays.— –
To examine which EM fungi produced resistant propagules (e.g., spores resistant to drying, adapted after Taylor and Bruns 1999) a subset of additional cores were taken adjacent to where intact cores were sampled in 2001. Four cores were taken from one plot of each fertilization treatment and unfertilized control. These soil samples were collected with a shovel and put in plastic bags without attempting to keep the core intact. The size of the core was approximately the same as those in the intact soil bioassay. These samples were mixed in the bag by hand and then enclosed in large paper bags and placed in a forced air dryer at ~32 C for 1 wk. Afterward these soils were sieved to remove large roots. Sterilized, black eight-inch standard pots (Belden Plastics, St Paul, Minnesota) were filled to the top with this soil, seeded with surface-sterilized acorns and maintained as described for the intact core bioassays. Seedlings were watered as needed and harvested after 16 wk.
Ectomycorrhizal fungal colonization of intact core and resistant propagules bioassays.— –
Morphological and molecular tools were used to assess EM fungal colonization. Colonization was examined morphologically in 2000 on 100 root tips for intact soil core bioassays and in 2001 on 200 tips for intact soil core and the resistant propagules bioassays. Colonization was determined primarily by examining the size, color and morphology of fungal structures (mantle type and extra-radical hyphae) found on root surfaces (Agerer 1987–1996, Goodman et al 1996). Descriptions of morphotypes are located in Avis (2003). In most cases, identity of the EM fungi that composed these morphotypes was established by molecular methods in a previous study (Avis et al 2003). Several morphotypes not encountered in the field study were examined further with molecular analysis. Following Avis et al (2003), DNA from single lyophilized tips of previously unidentified morphotypes was extracted, ITS regions amplified and digested with restriction enzymes. If restriction patterns did not match any pattern in a database of patterns from Cedar Creek EM fungi, ITS DNA from these morphotypes was sequenced. BLAST searches were used to assign a tentative phylogenetic relationship.
Mycorrhizal root bioassays.— – We examined whether two dominant EM fungi could colonize new oak roots from previously mycorrhizal roots. On 23 Aug 2002 oak roots colonized by Russula-like and Cortinarius-like morphotypes were collected near select focal trees in the fertilization treatments. Soil was turned with a shovel and ectomycorrhizal oak roots were extracted, put in plastic bags and stored at 4 C.
Before collection of roots from the savanna, bur oak acorns collected from under a single bur oak at Cedar Creek were surface sterilized and germinated on moist paper towels. After radicle emergence, acorns were transferred to steam-sterilized quartz sand and grown several more days until roots were 2–5 cm long.
On 28 Aug 2002 select sets of field-collected roots were transferred to young oak seedling root systems. Roots to serve as mycorrhizal root inoculum sources were selected with a dissecting microscope, and two dominant types of EM fungi were selected. These included Russula-like morphotypes that were orange to gold and often had a distinctive layer of cystidia covering the EM mantle and Cortinarius-like morphotypes having abundant tufts of white hyphae extending from roots (Agerer 1987–1996). Previous experience indicated that selection of these morphotypes based on these morphological criteria consistently yielded the target genera when analyzed by molecular analysis (Avis et al 2003). These two types of EM fungi often colonized large numbers of adjacent root tips and can be the only EM fungi in a continuous segment of root up to 3 cm long. Selection of these tips targeted these monotypic regions of root thereby minimizing the amount of nontarget EM fungi included as inoculum. Selected mycorrhizal roots were rinsed in water and most attached debris removed. No attempt was made to surface sterilize these roots and therefore other soil microbes and nontarget propagules (e.g., spores attached to root surfaces) might have been transferred along with the mycorrhizal roots.
In most cases the amount of mycorrhizal root inoculum applied was enough to cover the length of the emerging oak seedling root system. Typically by this time these root systems had developed many laterals. The seedling root system plus mycorrhizal root inoculum then were set together in a small amount of quartz sand and wrapped in moist paper towels in a "symbiosis packet" so that seedling root growth would come in direct contact with the mycorrhizal root inoculum (modified after the "rag-doll" method for seed germination, Association of Official Seed Analysts 1980). These systems were grown 6 d and transferred to a pot containing steam-sterilized soil collected from this site. This transfer involved unrolling the paper towel without spilling the contents and then gently sliding the symbiosis packet in a premade hole in the sterile soil. Upon visual inspection of the packets during the transfer the seedling roots had grown through and entwined with the mycorrhizal root inoculum indicating that physical contact of new roots to mycorrhizal root inoculum occurred. Soil was gently pushed to close the hole around the symbiosis packet, and a second layer of sterile soil was added on top to level the soil with the root collar. These cultures then were watered and placed on a greenhouse bench. No external lights were used in the greenhouse until late September, and the air temperature was maintained at ~25 C.
Seedlings were harvested 30 Dec 2002. Root systems were washed and examined microscopically. Each root system was rated as follows for the quantity of Russula-like, Cortinarius-like or other fungi present on the oak seedling root system: none (no colonization), low (<10%), moderate (10–50%), or high (>50%) colonization of root tips.
To test if the mycorrhizal root bioassay was a robust method, we examined whether the colonized roots of oak seedlings developed during the initial mycorrhizal root bioassay could serve as mycorrhizal root inoculum for symbiosis packets in subsequent mycorrhizal root bioassays. Two oak seedling root systems highly colonized by Russula-like ectomycorrhizas were rinsed free of any adhering roots from the previous addition of mycorrhizal roots. Only EM roots connected to the central taproot of the oak seedling were transferred. Each seedling root system was divided in three equal sections and each applied to one germinated acorn and rolled in symbiosis packets as above. These seedlings were grown until 12 May 2003 and harvested and examined as above.
Statistical analysis.— –
For intact soil core bioassays, total percent root colonization (total number of EM colonized root tips/total number of root tips counted, *100%), species richness (the number of distinct morphotypes, RFLP types and/or sequence types) and dominant EM fungi abundance (number of EM colonized root tips/total number of root tips counted, *100%) and frequency (presence in a bioassay) from each treatment plot were averaged and examined as a completely randomized design with three treatments and three replicates per treatment. The effect of N treatment, year and treatment-year interaction were compared by two-way ANOVA with Tukey-Kramer HSD for multiple comparisons and assumptions of normality tested using JMP software version 4.0 (SAS Institute Inc., Cary, North Carolina). For the resistant propagules bioassay, one-way ANOVA with Tukey-Kramer HSD for multiple comparisons and chi-squared analysis was conducted to examine the effect of fertilization on root tip colonization and the number of seedlings on which particular morphotypes were found, respectively. In the chi-squared analysis, a two-dimensional contingency table (morphotype presence x fertilization treatment) was used (Zar 1999).
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RESULTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONLITERATURE CITED |
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The number of morphotypes found in the intact core bioassays was not statistically different among soil N levels (F2,2 = 0.77, p = 0.49) or year (F1,1 = 2.21, p = 0.16) and was not affected by the interaction of these factors (F2,2 = 1.63, p = 0.24). Morphotype richness in 2000 was 4.1, 3.6 and 3.3 and in 2001 was 3.3, 3.3, and 3.5 in the 0, 5.4, and 17 g N m–2 y–1 treatments, respectively, with 14 morphotypes found in intact soil core bioassays overall (TABLE I).
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), was one of the most dominant EM fungi in intact soil bioassays colonizing 
10% or more of the roots in all treatments. This morphotype was significantly more abundant and tended to colonize more seedlings in 17 g N m–2 y–1 treatments in both years examined (FIG. 1). However, this Russula morphotype was not found in the resistant propagule bioassay (TABLE II). In contrast Cenococcum geophilum was not affected by fertilization, year or their interaction (FIG. 1). Cenococcum generally colonized fewer roots (
10%) than other dominant EM fungi although it was found on many seedling roots. In resistant propagule bioassays Cenococcum was significantly more abundant in 5.4 g N m–2 y–1 soil and was one of the most commonly found types in resistant propagules bioassays (Table II). Cortinarius morphotypes as measured by percent root tip colonization and frequency were significantly affected by the interaction of N treatment and year (FIG. 1). Cortinarius morphotypes produced resistant propagules in unfertilized soils but not in any of the fertilized soils tested (TABLE II).
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. Because these types were abundant, it was not feasible to sort all tips and we felt more confident pooling the results from each. Together these two types were dominant EM fungi in the intact-core bioassays although in soil of increased N supply they tended to be less abundant (mean percent root tip colonization ± sem: 23.2 ± 2.9, 18.1 ± 5.4, and 14.7 ± 5.2 at 0, 5.4 and 17 g N m–2 y–1, respectively; one-way ANOVA not significant, p = 0.47) and to colonize fewer seedlings (mean number of seedlings colonized ± sem: 5.3 ± 1.2, 4.0 ± 0.6, and 3.7 ± 0.3 at 0, 5.4 and 17 g N m–2 y–1, respectively; one-way ANOVA, not significant, p = 0.36). However in resistant propagule bioassays, these two types colonized more oak seedling roots in 17 g N m–2 y–1 soil (TABLE II
). In the mycorrhizal root bioassays Cortinarius morphotypes successfully colonized four of 12 total cultures with colonization rated as "moderate" on most seedlings. Russula II3 morphotypes successfully colonized six of nine total cultures with colonization rated as "high" on most seedlings. When these Russula II3 colonized roots were transferred to other oak seedlings Russula II3 colonized five of eight cultures. However most colonization was restricted to the upper half of the root systems where the mycorrhizal root inoculum was placed indicating that the spread rate of Russula II3 lagged bur oak seedling root growth.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONLITERATURE CITED |
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) was similar to the response of EM sporocarps and root colonization in the savanna. Avis et al (2003) showed that increased N supply shifted the species composition of EM fungi above- and belowground at this site such that the abundance of Cortinarius spp. declined but that of Russula spp., in particular Russula aff. amoenolens, increased with higher levels of soil N. The generally parallel response between EM inoculum and sporocarp and root colonization suggests that inoculum levels depend on the ability of EM fungi to tolerate N increase across several stages of life history. However we do not know how total colonization in bioassays relates to numbers of infective propagules in a soil because in these bioassays secondary colonization might have occurred by spread of fungi from locations of initial colonization. Therefore the N treatment differences in colonization might indicate either different amounts of inoculum or that N differentially affects the ability of fungi to colonize and spread along bioassay seedling root systems. Secondary colonization also might explain why increased N supply did not affect total percent root colonization in the bioassays. Although our results suggest N fertilization did not reduce the production of inoculum overall, different levels of inoculum could produce similar levels of root colonization if bioassay containers limit maximum root colonization and certain species can spread rapidly from relatively few propagules. The results from our mycorrhizal root bioassays lend support to this idea because they indicate that the Russula spp. dominant at high N supply are capable of effective secondary colonization.
Although the numbers of morphotypes did not differ between N supply levels, we believe our estimates of morphotype richness underestimated species richness to a large extent. Morphotypes are convenient categories that facilitate efficient and rapid organization of large and diverse samples of EM roots but often contain multiple species (Horton and Bruns 2002, Taylor and Bruns 1999). For example in this study the Cortinarius morphotypes included a species-rich group, C. subg. Telamonia. By a conservative estimate, this group contains six species at Cedar Creek and requires intensive molecular analysis to estimate the number of species more accurately (Avis et al 2003). As a result we cannot state with certainty that N increase does not influence the number of species producing inoculum in this study.
Inoculum ecology of dominant EM fungi.— –
Cenococcum geophilum is globally abundant (LoBruglio 1999) and is a major species of the EM community of this oak savanna. Our study illustrates two important aspects of its ecology. First, the inoculum of C. geophilum was not affected by N addition or year and this was similar to its root colonization response measured in the field (Avis et al 2003). The lack of response by C. geophilum to increased N at this site is consistent with the response of C. geophilum in experimentally fertilized conifer forests ( Jonsson et al 2000, Fransson et al 2001). This information suggests that the factors that determine the abundance of C. geophilum and its inoculum are not related to soil N supply. Second, although C. geophilum was found on many seedlings in the bioassays, it colonized roots to a lesser extent than other dominant EM fungi. This suggests that C. geophilum is less competitive under the confined environment of the bioassay pots and might be a poor competitor when close to other species, as has been suggested by others (Dickie et al 2002). Its abundance and success colonizing roots in natural conditions therefore might be due to a widely distributed inoculum although the mechanisms of how its asexually produced sclerotia disperse remain unknown (Fries 1987, Miller et al 1994).
This study provides essential information on the inoculum and dispersal traits of the dominant EM fungus, Russula aff. amoenolens. As mentioned above, this species was stimulated by an increase in N supply to produce more sporocarps and to colonize relatively more roots (Avis et al 2003). In the current study the Russula II3 morphotype, composed primarily of R. aff. amoenolens, was a strong competitor for roots in the intact soil core bioassays especially in 17 g N m–2 y–1 treatments where each year it was more abundant than in other treatments. This might be due to its ability to colonize roots from previously mycorrhizal roots as shown by its success in the mycorrhizal root bioassays. However the lack of any resistant propagules despite a tremendous increase in sporocarp production in 17 g N m–2 y–1 plots (Avis et al 2003) is intriguing and suggests spores produced in these sporocarps might not serve a role in long-term dispersal. However, considering several recent population analyses of Russula spp. wherein numerous, small genets were found in mature communities (Redecker et al 2001, Bergmann and Miller 2002, Liang et al 2004), the absence of resistant propagules as measured in this study might indicate instead the limitations of bioassay and culturing techniques in providing the specific requirements necessary for the germination of some EM fungal spores (Fries 1987).
In 2001 the combined morphotypes of Thelephoroid I6 and Ascomycete I7 (Wilcoxina-like) were dominant in intact soil bioassays but were lower with increased N supply as the abundance of Russula II3 increased. However in resistant propagule assays where Russula II3 was absent this trend was reversed. Of note, these morphotypes were not common in field-collected roots (Avis et al 2003). Their increase in heavily fertilized resistant propagule bioassays in the absence of Russula II3 propagules indicates their propagules tolerate high N supply but do not compete well in established EM communities. Thelephora americana and Wilcoxina spp. have responded in similar ways when grown on ectomycorrhizal conifer seedlings grown in containers and fertilized (Kernahagan et al 2002). Baar et al (1999) also showed that Wilcoxina spp. were abundant in bioassays of postfire collected soil but were not abundant on roots collected from the field suggesting that inoculum of these species is long-lived but requires specific conditions to colonize roots. Although low-intensity fires burn this savanna at Cedar Creek every two out of three y (Reich et al 2001), no fires occurred in 2001 suggesting the response of these EM fungi was not directly related to fire.
The utility of bioassays.— –
The dominant EM fungi found in the intact soil cores were similar to those found colonizing the roots of mature trees in the field (Avis et al 2003). Thus, despite the general observation that seedlings in potted soils are usually colonized by EM fungi that are different than those found in mature EM communities (Taylor and Bruns 1999), the intact core method served as a reasonable surrogate measure of the dominant EM fungi in the oak savanna and might do so elsewhere when field bioassays are not feasible (Hagerman et al 1999). Furthermore studies examining the consequences of shifts in EM fungal community composition might use techniques such as the mycorrhizal root bioassays, which can allow the isolation and manipulation of important EM fungal species and their functional differences.
Conclusion.— – This study indicates that N supply can affect the reproductive propagules of EM fungi differentially. Although the mechanisms by which N increase affects the amount of inoculum and/or the ability of EM fungi to grow from inoculum to colonize roots remain uncertain, it is clear that EM fungi exhibit a range of responses. In regions affected by elevated atmospheric N deposition, these responses might be important factors to include in predictions of how terrestrial ecosystems respond to such perturbation.
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ACKNOWLEDGMENTS |
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FOOTNOTES |
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1 Corresponding author: pavis{at}fieldmuseum.org
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