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Ecology |
2Department of Biology, Duke University, Durham, North Carolina, 27708 USA; 3Department of Crop Science, P.O. Box 7620, North Carolina State University, Raleigh, North Carolina 27695 USA; 4Department of Biology and Division of Environmental Science and Policy, Nicholas School of the Environment & Earth Science, Phytotron Building, Box 90340, Duke University, Durham, North Carolina 27708-0340 USA
Received for publication August 7, 2003. Accepted for publication October 31, 2003.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Key Words: ammonium • CO2 • controlled environments • nitrate • nitrogen metabolism • nitrogen uptake • Prosopis flexuosa • Prosopis glandulosa
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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; Johnson et al., 1998
). For many species grown under elevated CO2, a suite of morphological and physiological responses occur. The most common responses include increased rates of photosynthesis, decreases in leaf nitrogen concentration, increases in total nonstructural carbohydrate concentration, decreases in specific leaf area (leaf area : leaf dry mass), and increases in biomass (see reviews by Lawlor and Mitchell, 1991
; Ceulemans and Mousseau, 1994
; Drake et al., 1997
; Norby et al., 1999
). While these effects are fairly general, there is enormous variation in their magnitude across different species and environmental conditions (Roumet et al., 1999
; Körner, 2000
). In most natural ecosystems, low nitrogen (N) and/or phosphorus (P) impose major constraints upon plant growth (Chapin et al., 1986
, 1987
; Raven et al., 1992
), and it can be expected that these nutrient limitations will affect plant responses to increasing levels of atmospheric CO2 (Bazzaz, 1990
; Jackson et al., 1990
; Berntson et al., 1998
; Körner, 2000
).
The general importance of the N economy of plants in mediating the rates and directions of CO2-induced plant responses is reviewed by McGuire et al. (1995)
and Stitt and Krapp (1999)
. However, many key, specific questions regarding N metabolism and direct and indirect interactions with CO2 remain uncertain (Reeves et al., 1994
; Pritchard et al., 1997
). The growth responses of plants to elevated CO2 are usually diminished or even eliminated when plants are grown at limiting N levels (e.g., Jackson et al., 1990
; McGuire et al., 1995
; Rogers et al., 1996a
, b
; Drake et al., 1997
; Mousseau, 2000
). However, few studies have examined the effect of different N forms on plant responses to varying levels of N under elevated CO2. This is in spite of the fact that it is well known that for vascular plants, N is mainly taken up as NO3 or NH4 ions and that changes in their relative proportion may have differential effects on plant growth and metabolism (Salsac et al., 1987
; Raven et al., 1992
; Falkengren-Grerup, 1995
). In a study of fast- and slow-growing grasses, Bowler and Press (1996)
found that the slow-growing species attained a greater total dry mass and leaf area ratio (LAR; leaf area : plant dry mass) when NH4+ was supplied as the source of N and grown at an elevated level of CO2. The LAR was significantly higher for the fast grower only when NO3 was supplied as the source of N. Elevated CO2 decreased root NO3– uptake capacity by 55% in a desert shrub (BassiriRad et al., 1997b
), but in a species of pine, high CO2 stimulated a shift in preference for NO3-N over NH4-N (BassiriRad et al., 1997a
). Clearly, there is a need to further investigate how the forms of plant-available N influence plant growth responses to elevated CO2.
Geiger et al. (1999)
stressed the importance of examining physiological responses related to N metabolism and plant growth in parallel to distinguish between the direct effects of elevated CO2 and N availability. Evidence is increasing that monitoring the levels of certain metabolites directly involved in the assimilation of NO3– and NH4+ (e.g., amino acids, proteins, organic acids, and free NO3–) may provide more accurate information about the N status of the shoot because they can elicit feedback mechanisms that regulate both N uptake and assimilation pathways (Barneix and Causin, 1996
; Islam et al., 1996
; Schenk, 1996
; Poorter et al., 1997
; Geiger et al., 1999
). Given that the majority of our understanding of plant growth, soil N, and elevated CO2 interactions comes primarily from studies of agronomic species or from mesic temperate ecosystems (Körner, 1996
), this need is paramount for species from nutrient-poor arid and semiarid regions where low soil N poses major constraints (Chapin et al., 1986
) and is likely to play a key role in mediating plant responses to elevated CO2 in these systems (Polley et al., 1995
, 1997a
; Smith et al., 2000
).
In the present study, we examined the growth responses of two species of shrubs (Prosopis) from semiarid ecosystems, grown at either ambient (350 ppm) or elevated CO2 (650 ppm) and with different levels of total soil N, supplied at two NO3– : NH4+ ratios. We also measured several tissue metabolites (e.g., free NO3–, soluble proteins, and organic acids) in an attempt to better understand the physiological basis of the observed responses. Using seedlings grown in the controlled environment facilities of the Duke University Phytotron, we focused on two main questions with regard to the relative responses of these two species: (1) How do differences in N availability (Nlevel) and the ratio of NO3-N to NH4-N externally supplied (Nsource) affect plant growth and biomass allocation responses to elevated CO2 in these species? (2) How do differences in CO2, Nlevel, and Nsource affect N uptake and metabolites related to N assimilation?
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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; Pissani and Distel, 1998
). Prosopis glandulosa is a fast-growing deciduous shrub native to the arid and semiarid regions of southwestern United States (Virginia et al., 1982
). Seeds of P. flexuosa were collected at Estación San Miguel, Quines, San Luis (Argentina) in January 1999; seeds of P. glandulosa were collected in August 1999 at the Jornada Experimental Range near Las Cruces, New Mexico (USA). For both species, seeds from one individual (i.e., half-sib seed families) were used in the experiment.
Experimental design
On 18 April, seeds were mechanically scarified and sown in PVC pots (10.2 cm diameter x 40 cm height, two seeds/pot) containing a mixture of sand : gravel (4 : 1). Pots were placed in a controlled environment greenhouse in the Duke University Phytotron, which was set at 27°/20°C day (15 h)/night temperatures, and watered daily with distilled water until the seeds germinated. By 8 d after sowing (das), a sufficient number of plants had germinated, and 12 pots per species were transferred to each of four walk-in growth chambers to create a 2 (spp.) x 2 (CO2 level) x 2 (N level) x 2 (NO3– : NH4+ ratio) design. Environmental conditions common to all chambers were as follows: temperatures as in the greenhouse, 15-h photoperiod, 900 µmol · m–2 · s–1 light intensity, and 40% relative humidity. Two chambers were maintained at an ambient CO2 concentration (350 ppm, control treatment) and two at high CO2 (650 ppm). Within each chamber, three pots per species were irrigated three times per week with a modified Hoagland's solution representing one of four Nlevel x Nsource ratio treatments. The two Nlevel treatments were high (8.0 mmol/L) and low (0.8 mmol/L) total N concentrations, which were supplied at either 1 : 1 (equal) or 3 : 1 (high nitrate) NO3– : NH4+ ratios. All the solutions were labeled with 5 atom % 15N, obtained by proper mixtures of (NH4)2SO4, Ca(NO3)2, and K15NO3 at 10 atom % (Table 1). Micronutrients were supplied from a Hoagland's stock solution without Fe, which was supplied separately as 330 Fe DTPA (0.03 g/ L). Final solution pH was adjusted to 6.0. During the fertilization period, pots were flushed every 2 wk with distilled water to minimize salt accumulation.
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Chemical analyses
Freeze-dried material was used for analysis of tissue metabolites. Total N and 15N determinations were performed using an SIRA Series II isotope ratio mass spectrometer (VG ISOGAS, Middlewich, Cheshire, UK). The proportion of total N in the plant derived from external NO3– (15NO3-Npl) was calculated based on the proportion of 15N-labeled NO3– in the fertilizer solution:
Specific absorption rate (SAR) for either total N levels or N forms was calculated as:
). Because of sample size and cost considerations, for the remaining analyses samples of roots and leaves from two randomly chosen plants from the same treatment (one plant per chamber) were pooled to create three samples of sufficient size.
Soluble proteins in roots and shoots were extracted with 0.1 N NaOH (40 mg/3.5 mL, 30 min at room temperature) and, after filtration, with the Pierce Coomassie protein assay reagent (Pierce Chemical Co., Rockford, Illinois, USA). The reaction mixture contained 0.2 mL sample + 2.0 mL reagent modified by addition of 5 mg/mL soluble polyvinylpyrrolidone (Sigma-Aldrich, St. Louis, Illinois, USA; pharmaceutical grade, MW [molecular weight] 40 000), which minimized interference due to the formation of brown quinones during the extraction procedure (Jones et al., 1989
). A stock solution of bovine serum albumin (Sigma-Aldrich) in 0.1 N NaOH (1 mg/mL) was used as a standard.
Free nitrate and ammonium concentrations in root and leaf extracts were determined using a continuous flow, rapid diffusion process (Carlson, 1986
). Samples were obtained by extracting 30 mg of finely ground tissue with 6–7 mL distilled H2O for 90 min at 45°C. Extracts were filtered through Whatman #1 filter paper, and 3–4 mL samples of the recovered filtrate were brought up to 8 mL with distilled H2O. Prior to the dilution, leaf extracts were washed with chloroform (0.5 mL/mL, 4 h at 4°C), centrifuged (5 min at 1500 g), and the clear upper aqueous phase used for NO3– and NH4+ determinations.
For organic acid analyses, 25-mg samples were extracted three times at room temperature with 8.0 mL of 80% ethanol solution. During the extraction, samples were placed in a sonicator bath for 5 min. The supernatants were combined and brought up to 25 mL with the same ethanol solution. Aliquots of 5.0 mL were dried overnight in a speedvac (Savant Speedvac Concentrator, Thermo-Savant Company), and the pellet reconstituted in 1.5 mL distilled water. After centrifugation, the clear supernatant was used for organic acid determination. Organic acids were measured by ion chromatography. Separations were done with an AS-11 analytical column equipped with an AG-11 guard column (Dionex Corporation). An anion trap column (ATC-1) was installed between the gradient pump and injection valve to remove anionic contaminants from the eluents. The eluents consisted of high purity water, methanol, 1.0 mmol/L NaOH and 100.0 mmol/L NaOH, which were run in a gradient. Organic acids were detected using suppressed electrical conductivity. Although numerous organic acids can be detected with this procedure, malate was present in the largest amount, followed by citrate; these are the only ones reported here.
N fixation
Our use of seedlings poses no complications with regard to nodulation and fixation. While both species used in this experiment have the potential to symbiotically fix N2, evidence suggests that in warm desert ecosystems mesquite nodulation is most commonly associated with deeper roots on mature plants (Virginia et al., 1986
). For example, Jenkins et al. (1988)
, in an extensive survey of the depth distribution of Prosopis glandulosa root- nodulating bacteria at the Jornada Range, found that surface soils had very low populations of effective rhizobia and root nodules were not seen on seedlings. It is likely that during the initial establishment of mesquite seedlings, nodulation is not prevalent because of low symbiont populations, fluctuating soil moisture conditions, the high availability of surface N (relative to subsurface soils), and because the time required for root infection and the development of an effective symbiosis precludes a symbiotic source of N to very young plants, as used in this experiment. For these reasons, the use of mineral N nutrition in our experiments with seedlings (rather than symbiotic N) is a reasonable approximation of field conditions.
Statistical analyses
All analyses were performed using Data Desk software (Velleman, 1995
). Effects of treatments were analyzed using a nested analysis of variance (ANOVA) model (Potvin and Tardif, 1988
). The model included CO2, species, Nlevel, and Nsource as main effects, with chamber number as a random factor nested within CO2. For measurements in which it was necessary to pool samples, a four-way ANOVA design using the same main effect terms was used.
Histograms and normal probability plots were used to determine whether data required logarithmic (ln), square-root, or arcsine square-root (for ratio data) transformation for satisfactorily normal distributions of residuals and homogeneity of variances. Post-ANOVA comparisons of treatment means were made using Bonferroni's test (Day and Quinn, 1989
).
Differences in whole-plant nitrogen use efficiency (NUE) between CO2 treatments were examined using analysis of covariance to compare the slopes of the relationship between log-transformed plant N content and log-transformed non-N plant dry mass (see Coleman et al., 1993
). Separate analyses were performed for each Nlevel treatment. The model used plant N content as the dependent variable, non-N plant dry mass as the covariate, and CO2 as the independent variable. Differences in slopes between CO2 levels were indicated by a significant non-N plant dry mass x CO2 interaction term. P values given in the text refer to results from ANOVAs unless otherwise indicated.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Several significant differences between species in their growth responses were found. At the initial (pretreatment) harvest, both species had similar shoot biomass and had reached a similar developmental stage; however, average root biomass of P. glandulosa seedlings was about 50% higher than that of P. flexuosa (P < 0.001; data not shown). This difference remained highly significant at the final harvest, which led to greater root : shoot ratios in P. glandulosa than in P. flexuosa in most of our treatment combinations (Fig. 1c, d; species main effect P < 0.001). Prosopis glandulosa also had greater total biomass than P. flexuosa (Fig. 1; species main effect P < 0.001); however, there was a significant species x N interaction, and post-hoc tests indicate that species differences in this trait were significant only for the low N treatment.
Root : shoot ratio was the only growth and allocation trait significantly affected by the N form when considered as the main effect in the ANOVA: it was higher in plants fed with an equal rather than a high NO3– : NH4+ ratio (P < 0.01). However, the significant CO2 level x Nlevel x Nsource interaction for total plant biomass (P < 0.055, Fig. 1) indicated that, at low Nlevel, this trait significantly increased in both species as a response to elevated CO2 when a high NO3– : NH4+ ratio was externally supplied.
Nitrogen uptake and metabolism
Nitrogen uptake was strongly affected by Nlevel, as SAR-N of high Nlevel plants was about four times higher than for plants in the low Nlevel treatment (P < 0.001; Fig. 1e, f). Increasing CO2 did not significantly affect SAR-N of any of our treatment combinations (Fig. 1e, f). Of the two species studied, P. flexuosa had, on average, a higher SAR-N than P. glandulosa in all tested conditions (species main effect P < 0.001).
The proportion of N in the plant derived from uptake of either NO3– or NH4+ varied depending upon the species and total N supply rate, as well as the Nsource considered (Fig. 2). Because the relative proportions of NO3-N to NH4-N in plant tissues differed markedly between the 3 : 1 and the 1 : 1 NO3– : NH4+ treatments, separate analyses were performed for plants in each group. When an equal ratio of NO3– : NH4+ was supplied, the proportion of N derived from NO3– uptake was significantly higher than that from NH4+ uptake in plants from the high Nlevel treatment, regardless of the species or the atmospheric CO2 concentration (Nlevel main effect, P < 0.001). A similar effect was also observed when a 3 : 1 NO3– : NH4+ ratio was supplied. On the other hand, in the 3 : 1 treatment a significant difference between species indicates that P. flexuosa accumulated a higher proportion of tissue N derived from exogenous NO3– than did P. glandulosa (P < 0.001). This trend was particularly accentuated at high N and may be related to the significantly higher SAR-NO3– shown by P. flexuosa than P. glandulosa plants when NO3– was the major N source (data not shown). At low N supply, the relative proportion of NO3-N to NH4-N in plant tissues mostly resembled that of the external solution. Increasing atmospheric CO2 had no significant effects on SAR of either N form.
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The concentration of soluble proteins in plant tissues tended to increase in concert with external N supply, although the responses depended on the organ and the treatment combination considered. Soluble protein concentration in the leaves increased on average by more than 50% when plants were grown at a high N supply (P < 0.001; Fig. 3i, j). Increasing atmospheric CO2 significantly decreased the leaf soluble protein concentration when expressed on a per unit dry mass basis (P < 0.001), but not when expressed on a per unit leaf area basis (data not shown). Moreover, elevated CO2 resulted in a 35% increase (nonsignificant) in leaf soluble protein (area basis) in P. flexuosa plants from the high Nlevel, high nitrate treatment, suggesting that the decrement in leaf protein concentration was probably due to increments in specific leaf mass. Interestingly, root soluble protein levels in the same group of plants nearly doubled (P < 0.001) at elevated as compared to ambient CO2 (Fig. 3k, l). At high N, protein accumulation in both leaves and roots also depended on the Nsource ratio (P < 0.05 and 0.001, respectively, for the Nlevel x Nsource ratio interaction term from ANOVAs) and was significantly higher in plants from the equal Nsource ratio than in those from the high nitrate treatment (P < 0.01 from post-hoc tests). At low Nlevel, P. glandulosa plants accumulated on average 40% more soluble proteins in their roots than P. flexuosa irrespective of the external CO2 level or Nsource.
Effects of the CO2 treatments on NUE were investigated by comparing the slopes of the relationship between total plant N and net biomass accumulation per plant (i.e., total plant biomass – total plant N, see Coleman et al., 1993
) in different CO2 treatments, separately for each species (Fig. 4). Because preliminary analyses indicated that slopes of this relationship did not differ between Nsource ratio treatments, data from both treatments were combined for analysis. Nitrogen use efficiency was unaffected by CO2 at high Nlevel in either species (Fig. 4). At low Nlevel, NUE was unaffected by CO2 in P. glandulosa, but P. flexuosa had significantly lower NUE at elevated than at ambient CO2 (P < 0.05 from ANCOVA).
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Citrate concentrations in the leaves decreased in the high Nlevel treatment and increased in the low Nlevel treatment when plants were grown at elevated CO2 (data not shown). Significant Nlevel x Nsource ratio interaction terms were found for both leaf and root citrate concentrations (P < 0.01 in both cases), which showed a similar pattern of response to those of malate. Likewise, effects of CO2 treatments on root citrate levels mirrored those for malate.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Growth responses at both high CO2 and Nlevel also differed between these species depending on Nsource ratio in the external solution. Larger growth responses to increased atmospheric CO2 were found for P. flexuosa plants in the high nitrate than in the equal Nsource ratio treatment, while the reverse was true for P. glandulosa (e.g., Fig. 1). While our data do not allow us to completely explain the observed pattern, some of our results suggest that elevated CO2 responses in the former species are more dependent on a high relative availability of NO3- N than are those of P. glandulosa. For example, even though P. flexuosa had on average higher SAR-N than P. glandulosa plants (Fig. 1), at a high Nlevel, P. flexuosa plants could maintain a significantly higher SAR of NO3– (and to a lesser extent of NH4+, data not shown) than P. glandulosa only in the 3 : 1 NO3– : NH4+ treatment. Also in these plants (but not in P. glandulosa ones), the concentration of free nitrate in the roots significantly decreased and that of soluble proteins increased with increasing CO2. Because these changes were not accompanied by an increment and a decrement of free NO3– and protein levels, respectively, in the leaves (hence merely reflecting changes in allocation patterns), N assimilation may have been stimulated by high CO2 when P. flexuosa plants were grown with a high rather than an equal NO3– : NH4+ ratio.
Growth responses to elevated CO2 were markedly limited at low N supply, which is consistent with the literature (e.g., Jackson et al., 1990
; McGuire et al., 1995
; Rogers et al., 1996a
, b
; Drake et al., 1997
; Mousseau, 2000
). However, the exact nature of this CO2–N interaction also depended on the Nsource ratio supplied. A high NO3– : NH4+ ratio in the soil significantly stimulated the growth responses of both species to elevated CO2 in the low Nlevel treatment. This suggests that NO3– may be the preferred N source for both species. Edaphic and physiological information support this conclusion: the NO3– : NH4+ ratio in soils where these species grow is usually >10, and values up to 70 have been measured beneath canopies of these plants (Virginia et al., 1982
; Mazzarino et al., 1991a
,b
), although values below 10 can occur in dry seasons (Mazzarino et al., 1991a
). On the other hand we found that, at a high N supply, the concentration of organic acids in the roots of both species was markedly depleted in plants from the equal Nsource ratio treatment as compared to those from the high nitrate treatment, which is a common response among species adapted to use NO3– rather than NH4+ as their primary N source (Salsac et al., 1987
). Clearly, any disruption that affects nitrate availability in ecosystems where these two species occur—such as increases in rainfall (leaching), fire, and N deposition—could have significant implications for seedling growth and/or responses to human disturbance such as elevated atmospheric CO2.
At low N availability P. glandulosa produced more biomass than P. flexuosa regardless of CO2 level (Fig. 1). This difference was mainly due to an increased resource allocation to root tissue. In fact, at both initial (t0) and final harvests, P. glandulosa had higher root biomass and root : shoot ratios than P. flexuosa. This trend was particularly pronounced at low Nlevel and was also accompanied by a significantly higher allocation of the soluble protein N fraction (Fig. 3). Unexpectedly, this increase in resource allocation to roots did not significantly increase their physiological uptake capacity, since at low Nlevel both species have similar SAR of either NO3- or NH4-N, irrespective of the CO2 level. The fact that increasing atmospheric CO2 did not stimulate physiological N-uptake capacity when N was limiting for growth differs from results reported for other species (Chapin et al., 1987
; Jackson et al., 1990
; Jackson and Reynolds, 1996
), but is consistent with the findings of BassiriRad et al. (1997b)
who reported that the rate of NO3– uptake in Prosopis glandulosa plants growing at low N supply was relatively insensitive to CO2 enrichment. They also suggested that nutrient uptake responses under elevated CO2 were quite variable among different species.
In this study, Nlevel, Nsource, and atmospheric CO2 concentration generally had no major effects on NUE in either species. Under constant environmental conditions, NUE is expected to increase up to a maximum value as N supply diminishes and then decline as N supply approaches the minimum amount necessary to sustain plant growth (Bridgham et al., 1995
). It is possible that, in most of our treatment combinations, N supply at high and low Nlevel was above and below the optimum values for NUE, respectively, such that no differences for this trait could be detected between N treatments. Nevertheless, the one case where a significant effect of CO2 on NUE was found—for P. flexuosa plants at low Nlevel—demonstrates that responses to elevated CO2 are not only affected by Nlevel and Nsource but can also differ markedly between closely related species.
Overall, our results indicate that seedlings of both species are highly responsive to N availability. In our experimental conditions, seedling growth of both Prosopis species at a limiting N supply benefited from increases in atmospheric CO2, provided that a high proportion of NO3 to NH4-N was present in the soil solution. This enhancement, in combination with responses that increase N acquisition (e.g., increased resource allocation to the roots) and water use efficiency, suggests that these semiarid species will be better able to cope with both nutrient and water deficits as CO2 levels rise. Given that species of Prosopis are major components of woody shrub encroachment, which in the past 150 years has affected many regions of the globe (Van Auken, 2000
), further research of N metabolism and and plant growth are needed to distinguish between the direct effects of elevated CO2 and N limitations in Prosopis. This is especially germane for better clarifying the effects of increasing CO2 on shrub establishment in arid and semiarid regions of the world (Archer et al., 1995
; Polley et al., 1997b
; Van Auken, 2000
).
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FOOTNOTES |
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5 Present address: Departamento de Biodiversidad y Biología Experimental, F.C.E.y N., Universidad de Buenos Aires, Ciudad Universitaria, 1428 Capital Federal, Argentina
6 E-mail: james.f.reynolds{at}duke.edu
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LITERATURE CITED |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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