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Ecology |
Department of Botany and Plant Sciences, University of California, Riverside, California 92521-0124 USA
Received for publication June 13, 2000. Accepted for publication February 9, 2001.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Key Words: arbuscular mycorrhizae • Artemisia californica • Bromus madritensis ssp. rubens • coastal sage scrub • nitrogen deposition
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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; Vitousek et al., 1997
; Bobbink, Horning, and Roelofs, 1998
), but the mechanisms of vegetation change are not always clear. In this study we examined the effects of arbuscular mycorrhizal fungi (AMF) on uptake of soil NO3– vs. NH4+. Elevated NH4+ occurs predominantly in agricultural regions, such as The Netherlands where up to 90 kg N · ha–1 · yr–1 are deposited (Heil et al., 1988
), while NO3– originates from automobile exhaust, as in southern California with a high of 45 kg N · ha–1 · yr–1 (Lents and Kelly, 1993
; Fenn and Bytnerowicz, 1997
; Fenn et al., 1998
). Originally mycorrhizal fungi were shown to be more important in NH4+ assimilation, a result that was explained by its relatively low solubility compared to NO3– (Ames et al., 1983
; Smith et al., 1985
). More recent studies have shown mycorrhizae may also assimilate NO3– (Azcón, Gomez, and Tobar, 1992
; Johansen, Jakobson, and Jensen, 1993
; Cuenca and Azcón, 1994
; Azcón and Tobar, 1998
). The plant response to N deposition will depend upon the form of N and the ability of the plant and mycorrhizal fungi to take up different N forms. We describe a greenhouse study using plants and soil from a southern California shrubland where NO3– is the predominant form of deposition (Padgett et al., 1999
). We examined whether the presence of mycorrhizae in the local vegetation was exacerbating the uptake of deposited NO3– or whether the mycorrhizae were having little effect on NO3– uptake, as hypothesized earlier by Ames et al. (1983)
.
A major mechanism of vegetation change under N deposition is the enhanced growth of some species compared to others. Studies in a European heathland that has converted to grassland indicate that the competitive ability of the grass Brachypodium pinnatum (L) Beauv. was increased by NH4+ deposition (van Dam et al., 1990
). Mediterranean annual grasses have been replacing coastal sage scrub (CSS) vegetation in southern California over the last few decades (Freudenberger, Fish, and Keeley, 1987
; O'Leary, 1995
; Minnich and Dezzani, 1998
). A number of causes have been hypothesized, including frequent fire and grazing, but N deposition has only recently been considered (Allen et al., 1998, 2000
). In areas where exotic grasses have replaced native shrubs, excessive N deposition may maintain grass dominance. Extractable soil N up to 87 µg/g have been observed in southern California, about two-thirds as NO3– (Allen et al., 1998
; Padgett et al., 1999
). Plants show great variation in their ability to use either NH4+, NO3–, or both (Haynes and Goh, 1978
; Falkengren-Grerup, 1995
). Native shrubs and invasive annuals of CSS had plastic responses to both elevated NO3– and NH4+ in the greenhouse (Padgett and Allen, 1999
), but these experiments were done in sterile soil and were not designed to test a mycorrhizal effect.
Different species of AMF can also show preference for uptake of NH4+ vs. NO3– as shown by isotope applications to plants combined with hyphal transport (Azcón, Gomez, and Tobar, 1992
; Vaast and Zasoski, 1992
; Johansen, Jakobsen, and Jensen, 1993
; Tobar, Azcón, and Barea, 1994
; George, Marschner, and Jakobsen, 1995
). Absorption of different forms of N would be promoted by mycorrhizal associations with multiple species of fungi (Chapin, 1980
), as occurs in CSS vegetation. In a recent study on a N deposition gradient in southern California, AMF spore diversity and abundance were reduced in regions with high N deposition (Egerton-Warburton and Allen, 2000)
. Large-spored AMF species declined in high N soils, while many small-spored species became more abundant (Johnson et al., 1991
; Egerton-Warburton and Allen, 2000
). Four of the species found in some of the sites of the gradient study, Glomus etunicatum (Becker & Gerdemann), G. mosseae (Nicolson & Gerdemann) Gerdemann & Trappe, G. macrocarpum (Tul. & Tul.), and G. fasciculatum (Thaxter sensu Gerdemann) Gerdemann & Trappe, are known to assimilate NO3–, NH4+, or both (Ho and Trappe, 1975
; Smith et al., 1985
; Cuenca and Azcón, 1994
; Azcón and Tobar, 1998
). Nitrate reductase, the enzyme critical for the first step in NO3– assimilation, was detected in AMF spores of Glomus mosseae, indicating a role of AMF in N uptake (Ho and Trappe, 1975
). Enzymes involved in NH4+ assimilation have also been isolated in AMF (Smith et al., 1985
).
Since AMF may differ in uptake of NH4+ and NO3–, any change in soil N levels or form resulting from increased N deposition may lead to a change in the behavior of mycorrhizal systems. The objective of the study was to determine (1) growth response to NO3– and NH4+ by a dominant native shrub, Artemisia californica Less. (California sagebrush), and an abundant invasive annual grass, Bromus madritensis L. ssp. rubens (foxtail chess), and (2) how AMF influence growth response to NO3– and NH4+ in these two species.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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; Padgett et al., 1999
). The inoculum was sieved through a 1-mm screen, thoroughly mixed, sealed, placed in a freezer at –12°C, and used within 4 mo. Spore extraction was done by sucrose flotation (Allen et al., 1979
), and spores were collected with a Buchner funnel and 0.45-µm mesh membrane filter (GN-6 Grid, Gelman Sciences, Ann Arbor, Michigan, USA). The spores were counted with a dissecting microscope, and the inoculum contained >200 mycorrhizal spores per gram of sieved soil.
Soil and potting
Native soil was also collected in the Multispecies Reserve for the greenhouse experiment. Before the experiment, the soil cation exchange capacity was 7.4 µmol/100 g (SE = 1.4, N = 5). P concentration (bicarbonate extractable) was 28.8 (2.7) µg/g. Mean KCl-extractable N was 14.5 µg/g NH4+ and 0.8 µg/g NO3– while total Kjeldahl N was 396 (9.9) µg/g.
The soil was sieved through a 1-cm2 wire sieve and mixed with 50% sterile sand, placed in autoclave bags, and steam-sterilized for at least 2 h at 82°C. Two days later, the steaming process was repeated to kill potential germinating spores. Inoculum (5 g) was buried 4 cm deep in pots (6.4 x 25 cm "Deepots," Steuwe and Sons, Corvallis, Oregon, USA) containing 830 g soil mix. Sterile inoculum was added to controls. A sievate (45-µm mesh) from 5 g soil per pot was added to replace microbial populations in controls. Twenty-five milliliters of a specially formulated nutrient solution (described below) and 10 mL of N treatment were added to pots before the seeds were sown into the pots. Ten replicates per treatment were used in this factorial study resulting in a total of 120 plants (two plant species x two mycorrhizal treatments x three N treatments). To assess AMF colonization sequentially, a preliminary experiment was done using the soils and inoculum described above.
Seeds and planting conditions
Seeds of B. madritensis and A. californica were collected from the Motte Rimrock Reserve, 
15 km northwest of Lake Skinner and stored dry at room temperature until planting. Three B. madritensis and ten A. californica seeds were sown into each pot with a thin soil cover. After germination, the seedlings were thinned to one plant per pot, watered as needed, and maintained in a greenhouse at 21°C from March to May, 1997.
Fertilization and harvesting
All of the plants were fertilized with a specially formulated nutrient solution (minus P and N) based on analyses of native soil (Padgett and Allen, 1999
). The seedlings initially received 50 mL of one of three N solutions (control, 10 µg/g N from NH4NO3; high NO3– treatment, 50 µg/g NO3– from Ca(NO3)2; high NH4+ treatment, 50 µg/g NH4+ from NH4Cl) at the beginning of the experiment. An additional 50 mL of N solution was added approximately every 2 wk to maintain high N levels in the N treatments, but none to the controls. Five-gram soil samples were collected in the top 5 cm of the pot of A. californica and analyzed for NH4+ and NO3– concentrations by KCl extraction. During the course of the experiment, the soil N levels in the controls were <20 µg/g NH4+ and NO3–. Soil N levels in the NO3– treatment rose to 160 µg/g at harvest, while those in the NH4+ treatment remained between 100 and 120 µg/g. Electrical conductivity was 0.16 dS/m in the control, 0.22 in NO3– treatment, and 0.59 in the NH4+ treatment at harvest. The pH varied from 6.5 to 7.0 but was not significantly different among treatments. Beginning 5 wk after germination, and weekly thereafter, plant height (A. californica and B. madritensis) and width (A. californica only) and numbers of leaves and tillers (B. madritensis only) were recorded.
Bromus madritensis and A. californica were harvested 7 and 8 wk after germination, respectively. Bromus madritensis was harvested 1 wk earlier before it began to fill seeds, as we did not wish to assess reproductive effort in this study. Shoot and root tissue were separated. Roots were washed, and tissue was oven dried at 60°C for 72 h and weighed. A subsample of the roots was prepared for mycorrhizal staining with trypan blue (Koske and Gemma, 1989
). Percentage root colonization was determined by microscopically examining 100 root intercepts per sample. In addition, three replicates of each species were harvested at 2-wk intervals from control pots in a preliminary experiment to determine dynamics of AMF over time (in the preliminary experiment both plant species were maintained for 8 wk).
Nutrient analyses
Shoot tissue was ground with liquid nitrogen and %N was determined by flash combustion chromatography (Carlo Erba Instruments, Fisons, Dearborn, Michigan, USA). The shoot tissue was prepared for P analysis by microwave digestion (Miller and Sah, 1992
). P concentration was determined spectrophotometrically with the malachite green method (Ohno and Zibilske, 1991
).
Statistical analyses
The growth data were analyzed by factorial analysis of variance followed by LSD0.05 (least significant difference). Growth data over time were analyzed by performing a repeated-measures analysis of variance across all three N treatments. Repeated-measures ANOVA was also performed on each individual N treatment to assess the influence of mycorrhizae on nondestructive measures of plant growth (height, volume, and number of leaves) within each treatment. Plant biomass data were (1 + ln)-transformed to reduce kurtosis and subjected to a two-way factorial ANOVA (nitrogen x mycorrhizal treatment). Roots, shoots, and total biomass were analyzed separately.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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6 wk following germination (Fig. 1). However, mycorrhizal colonization was very low in the main study (0–6% arbuscules, 0–2% hyphae, 0–4% vesicles) in all treatments in both A. californica and B. madritensis at the time of harvest. Mycorrhizal spores, vesicles, and hyphae were observed on a low percentage of the roots. The uninoculated plants were not mycorrhizal, nor was there evidence of pathogens in the roots.
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Biomass
NH4+-treated plants of both species had a positive total biomass (shoot plus root) response to mycorrhizal inoculum, but inoculum did not cause a significant change in biomass of NO3– treated plants of either species (Fig. 4A, B, Table 1). Mycorrhizae were so important for an NH4+ growth response of A. californica that the nonmycorrhizal NH4+-treated plants were as small as the nonmycorrhizal controls. Control plants of B. madritensis had increased total mass with inoculum compared to uninoculated control plants, but control plants of A. californica were not significantly affected by inoculum. Consequently, there was a significant N x mycorrhizae interaction for the total mass in A. californica with P = 0.006 while for B. madritensis the interaction P = 0.077.
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For B. madritensis only, the NH4+-treated mycorrhizal plants had both higher shoot and root mass than any of the other treatments. The mean r : s was 1.26, also without significant differences among mycorrhiza and N treatments.
An overall ANOVA comparing the total biomass of the two plant species (not shown) was not significantly different (i.e., they had similar overall mean biomass values), nor were there significant species x N treatment or species x mycorrhizal treatment interactions. In this ANOVA there was only a significant overall N x mycorrhiza interaction (P < 0.001).
Nutrients
Shoot N concentration varied between species. In A. californica, N concentration did not differ greatly (Fig. 5A), except in the NH4+ treatments where the mycorrhizal plants had significantly lower N in their tissues than did the nonmycorrhizal plants. The N concentrations in control plants were not significantly different from the N in NH4+ and NO3– treatments. In B. madritensis (Fig. 5B), control plants contained significantly less N in their tissues (1% N) than either of the N-treated plants (3.4–4.2% N). Mycorrhizal colonization did not have any significant effect on shoot N content. Shoot P content in B. madritensis was greater (0.49–0.68%) than A. californica (0.25–0.44%). While there were some significant differences in %P between N treatments in A. californica, there were no differences between mycorrhizal treatments within the N treatments in either A. californica or B. madritensis.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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; Vaast and Zasoski, 1992
). The natural soils where A. californica occurs in this region are slightly acidic with pH 6.0–6.5 and tend to be dominated by NH4+. Soils with low N deposition had a seasonal maximum of 9–17 µg/g NH4+ and 2–7 µg/g NO3– (Padgett et al., 1999
). Thus, mycorrhizal A. californica is well adapted to growth in these soils, and the invasive B. madritensis also responded well to NH4+ with inoculum.
Other studies showed that mycorrhizal hyphae may transport NO3– and thereby improve its uptake by the plant (Azcón, Gomez, and Tobar, 1992
; Johansen, Jakobsen, and Jensen, 1993
; Cuenca and Azcón, 1994
), but there was no mycorrhizal response to NO3– by either of our species. The plants were taking up both forms of N, as tissue N increased under fertilization. For B. madritensis, the increase in leaf N was a large 1.2% in controls to 4.2% with NO3–, although leaf N was not as plastic for A. californica. These ranges of tissue N concentrations have been observed in other field and greenhouse studies (Mooney et al., 1977
; Garnier et al., 1997
; Padgett and Allen, 1999
). The lack of growth response by mycorrhizal NO3–- treated plants could be readily explained if these plants had lower mycorrhizal colonization, because plants with sufficient nutrients can reject mycorrhizal fungi. For instance, lower mycorrhizal colonization was observed for A. californica and annual grasses under high NO3– deposition in the field (Egerton-Warburton and Allen, 2000)
. However, further detailed analyses of colonization rates over time coupled with carbon balance of N-fertilized plants need to be undertaken.
Although mycorrhizal colonization was low, the results of the preliminary sequential harvest indicated that by 6 wk 15% of A. californica and B. madritensis roots became colonized with arbuscules. This percentage of arbuscules may be sufficient to colonize all the actively growing root tips and cause a beneficial mycorrhizal response (Allen, 2001)
. Mycorrhizal colonization was likely highest at 6 wk and had declined by the time plants were harvested at 7–8 wk. Mycorrhizal structures such as arbuscules are short-lived and can be expected to turn over in 1–2 wk (Smith and Read, 1997
). Although soil P levels were relatively high (28 µg/g) and plants might not be expected to respond to inoculum, the NH4+-amended plants still had a high response to mycorrhizae. The soils of this region are generally high in P (Padgett et al., 1999
), so these results reflect normal field soil conditions. Low colonization of 10–20% were typical for both these species in the greenhouse (Yoshida, 1999
; Sigüenza, 2000
), yet colonization levels up to 40–80% have been reported in the field for mature A. californica (Egerton-Warburton and Allen, 2000; Sigüenza, 2000)
. Soil disturbance during potting disrupted the network of external mycorrhizal hyphae and would have reduced the fungal infectivity of the soil (Jasper, Abbott, and Robson, 1989
). However, seedlings of A. californica in a restored field plot with minimum soil disturbance had only 22% colonization after 2 yr (Sigüenza, 2000
). The results of this study can be extrapolated to establishing seedlings, but the mycorrhizal response to N may be greater in a mature CSS community with higher levels of colonization.
These two plant species have different life forms, but both had somewhat similar patterns of NO3– and NH4+ growth response with and without mycorrhizae. One difference in N response was that nonmycorrhizal A. californica had growth with NO3– as large as the mycorrhizal NH4+-treated plants, while B. madritensis treated with NO3– were significantly smaller than mycorrhizal NH4+-treated plants. The other difference in response was that the mycorrhizal controls of B. madritensis had higher biomass and were taller with more tillers than nonmycorrhizal controls, while controls of A. californica did not respond significantly to inoculum. Overall, later-successional and woody plants tend to be responsive to mycorrhizae, while early-successional plants tend to be less responsive (Corkidi and Rincon, 1997
). However, if anything, B. madritensis was slightly more responsive than the shrub because both the control and the NH4+-treated B. madritensis responded to mycorrhizae. With regard to N uptake, there is variance in whether plant species prefer NH4+ or NO3–, and life form need not be a factor in preference (Wallace et al., 1978
; Smirnoff and Stewart, 1985
). It was not possible from these two plant species to predict NH4+ and NO3– uptake or mycorrhizal response based on life form. Artemisia californica and B. madritensis may be considered members of the same successional stage, because the invasive species has stabilized in CSS communities. The similar responses to mycorrhizae and N may be reflective of adaptation to the same environmental conditions.
The spore species of mycorrhizal fungi are reduced in diversity and density in NO3–-affected soils in southern California (Egerton-Warburton and Allen, 2000)
, which may cause a further feedback on plant growth. For instance, plant growth was reduced by inoculum from N-fertilized soils in Minnesota, as AMF that are poor mutualists became dominant in eutrophied soils (Johnson, 1993
). In our study, we used only inoculum from a soil unaffected by N deposition, so the results are relevant to a situation where the full complement of spore species is present. If the AMF adapted to high N soils are poorer mutualists (Johnson, 1993
), then poor plant performance with N-affected inoculum may be an additional stress on plants. This will be the subject of a separate study.
The mycorrhizal growth responses alone do not explain the poor performance of A. californica in declining shrublands of southern California. A longer term experiment under elevated NH4NO3 gave a different result, where soil N levels of 50 µg/g caused mortality of A. californica after 6–9 mo, even though it grew very large in this experiment (Allen et al., 1998
). Bromus madritensis completes its life cycle and produces seeds within the short Mediterranean growing season (2–3 mo), so it escapes the potential negative effects of high soil N. N levels in the surface of eutrophied soil may be up to 87 µg/g, although we have not verified N-induced shrub mortality in the field. Additional life history traits of B. madritensis and A. californica may also explain shrub decline. For instance, B. madritensis has rapid germination with the first winter rains, prolific seed production, and high densities and competitive ability compared to A. californica (Eliason and Allen, 1997
; Stylinski and Allen, 1999
). Mycorrhizae would likely be more important to growth of these two plant species under NH4+ deposition. The eutrophication of a soil with moderate levels of NH4+ to a soil with high NO3– means that the functioning of mycorrhizae will change from a beneficial response to a less important role for promoting plant growth.
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FOOTNOTES |
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2 Author for reprint requests, current address: School of Biological Sciences, 419 Steinhaus Hall, University of California, Irvine, California 92697-2527 USA (FAX: 949-824-6599; lyoshida{at}uci.edu
).
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