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DIVISION S-7—FOREST & RANGE SOILS & SOIL & PLANT ANALYSIS

The Fate of ¹⁵NO^-₂ Tracer in Soils under Different Tree Species of the Catskill Mountains, New York

^a Dep. of Plant Biology, 265 Morrill Hall, Univ. of Illinois, 505 S. Goodwin Ave., Urbana, IL 61801
^b Institute of Ecosystem Studies, Box AB, Millbrook, NY 12545

^* Corresponding author (fitzhugh{at}life.uiuc.edu)

	ABSTRACT

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The incorporation of nitrite (NO^-₂) into soil organic matter (SOM) has received little attention as a mechanism contributing to the retention of atmospherically deposited N in forest ecosystems, despite previous studies in agricultural systems showing that NO^-₂ fixation by SOM is enhanced in soils with high acidity and organic matter content, characteristics commonly found in forest soils. Given previous studies showing that nitrification and nitrate (NO^-₃) leaching may vary significantly in soils under different tree species, the primary objectives of this study were to determine if the incorporation of NO^-₂ into SOM was quantitatively significant and if the incorporation varied among soils under different tree species from the Catskill Mountains in New York State. A pulse-chase laboratory experiment was performed, where ¹⁵NO^-₂ was added to organic soils from three tree species (American beech [Fagus grandifolia], northern red oak [Quercus rubra], sugar maple [Acer saccharum]), and ¹⁵N recoveries were determined in total soil, extractable inorganic, readily mineralizable, microbial biomass, dinitrogen (N₂), and nitrous oxide (N₂O) pools. Results from our experiment demonstrate that the incorporation of NO^-₂ into SOM can occur rapidly, at time scales of 1 d or shorter, and that NO^-₂ incorporation into SOM is the dominant fate of the ¹⁵NO^-₂ tracer, suggesting that the incorporation of NO^-₂ into SOM is a potentially important N sink in forest soils. The incorporation of NO^-₂ into SOM did not vary significantly among tree species. Our results suggest that models of the N cycle in forest ecosystems should include considerations of NO^-₂ incorporation into SOM.

Abbreviations: DON, dissolved organic N • SOM, soil organic matter

	INTRODUCTION

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THE ACCUMULATION of atmospherically deposited N in terrestrial ecosystems can result in N saturation, an excess of N supply over biotic N demand (Aber et al., 1998; Ågren and Bosatta, 1988). Concern about N saturation has prompted recent research on the fate of atmospheric N deposition to forest ecosystems (Magill et al., 1997; Tietema et al., 1998). Nitrogen saturation can adversely affect forest productivity (Fenn et al., 1998), alter competitive interactions among tree species (van Breemen et al., 1997), result in the acidification of soils and drainage waters (Fenn et al., 1996; van Breemen et al., 1987), and contribute to the eutrophication of coastal waters and estuaries (Jaworski et al., 1997). Within the eastern USA, atmospheric N deposition has been implicated as a causative agent of N saturation in spruce forests of the Great Smoky Mountains (Johnson et al., 1991) as well as watersheds of the Appalachian Plateau of West Virginia (Peterjohn et al., 1996) and the Adirondack (Driscoll and Van Dreason, 1993) and Catskill Mountains of New York (Murdoch and Stoddard, 1992; Lovett et al., 2000).

Nitrogen cycling and loss in forest ecosystems can be influenced by a variety of factors, including land-use history (Compton and Boone, 2000), atmospheric inputs (Dise and Wright, 1995), hydrology (Creed et al., 1996), geology (Dahlgren, 1994), climate (Fitzhugh et al., 2001), and tree species (Lovett et al., 2002). Stream NO^-₃ concentrations vary over a 17-fold range among watersheds of the Catskill Mountains (Lovett et al., 2000). Lovett et al. (2002) found that this spatial variability in stream NO^-₃ concentrations within the Catskills was significantly influenced by interwatershed variation in the soil C/N ratio. In turn, soil C/N exhibited a significant positive and negative relationship with the basal area of northern red oak and sugar maple, respectively; thus, spatial variation in NO^-₃ export appears to be related, at least in part, to the composition of tree species in the Catskill Mountains (Lovett et al., 2002).

Tree species may influence N cycling and loss through a variety of processes. Interspecific variation in the chemical composition of leaf litter has been identified as one mechanism by which different tree species can affect N cycling and fluxes (Melillo et al., 1982; Scott and Binkley, 1997). Feedbacks between trees and soils via the quality of leaf litter are believed to contribute to interspecific variation in nitrification (Finzi et al., 1998; Verchot et al., 2001; Ollinger et al., 2002), and thus it is reasonable to hypothesize that NO^-₃ leaching may be influenced by tree species composition.

These tree–soil interactions mediated by litter quality may also affect N sinks within the soil environment. Nitrogen can be retained in a variety of ecosystem pools, including above and belowground biomass as well as SOM. Tracer additions of inorganic N isotopes (¹⁵N) at the plot scale have shown that SOM is an important sink for N additions to forest ecosystems of the eastern USA (Nadelhoffer et al., 1995, 1999; Templer, 2001). Uptake of ¹⁵N by roots and microorganisms can result in the incorporation of ¹⁵N into SOM pools during root and microbial turnover, as well as the decomposition of above and belowground litter inputs. Addition of inorganic ¹⁵N can also be incorporated into SOM via abiotic processes involving the fixation of ammonium (¹⁵NH⁺₄) (Johnson et al., 2000) or nitrite (¹⁵NO^-₂), (Bremner and Fúhr, 1966; Dail et al., 2001).

While the pool of NO^-₂ generally is very small in soils of northern hardwood forests (range 3–11 ng N g^-1; R. Venterea, personal communication, 2002), NO^-₂ is an important intermediate in the nitrification and denitrification processes (Venterea and Rolston, 2000a). Although we were unable to find publications providing rates of atmospheric NO^-₂ deposition, those rates are likely to be negligible relative to atmospheric inputs of NO^-₃ and NH⁺₄. While atmospheric deposition of NO^-₂ likely has an insignificant impact on N cycling in forest ecosystems, the generation of NO^-₂ is the first step in the production of NO^-₃ via autotrophic nitrification, which represents an important flux of N in forest soils. For example, using a mass of 66 Mg ha^-1 for the Oa horizon of a northern hardwood forest (Johnson, 1995) and an average gross nitrification rate of 3 µg N g^-1 d^-1 measured in organic soils of the Catskills (Verchot et al., 2001), the flux of N cycling through the NO^-₂ pool in just the Oa horizon (approximately 70 kg N ha^-1 yr^-1) is approximately 600% of the rate of atmospheric N deposition in the Catskills (approximately 11 kg N ha^-1 yr^-1; Ollinger et al., 1993; Lovett and Rueth, 1999). Reactions involving NO^-₂, therefore, can significantly affect the fate of inorganic N in soils (Venterea and Rolston, 2000b).

The abiotic incorporation of NO^-₂ into SOM has received considerable attention in research on agricultural soils (Azhar et al., 1986a, 1986b; Bremner and Nelson, 1968; Nelson and Bremner, 1969), but has received relatively little study in forest soils. Bremner (1957) first reported that NO^-₂ could be fixed by SOM, presumably via nitrosation reactions, the replacement of a hydrogen atom in a molecule by a nitroso group (Austin, 1961). Nitrite fixation has been found to vary positively with SOM content and inversely with soil pH (Bremner and Fúhr, 1966; Bremner and Nelson, 1968; Nelson and Bremner, 1969). In addition to NO^-₂ fixation by SOM, nitrosation reactions may result in the evolution of a variety of N gases, including N₂ and N₂O (Reuss and Smith, 1965; Smith and Clark, 1960; Stevenson and Swaby, 1964). As the products of NO^-₂ fixation are believed to be relatively recalcitrant to biological mineralization (Bremner and Shaw, 1957; Smith and Chalk, 1979), the incorporation of NO^-₂ into SOM potentially represents a significant, yet little studied, long-term N sink for atmospheric N deposition to forest ecosystems. As soil phenolic compounds are believed to have an important role in NO^-₂ fixation (Azhar et al., 1986b), and litter lignin and tannin concentrations may vary significantly among canopy tree species (Hättenschwiler and Vitousek, 2000; Melillo et al., 1982; Scott and Binkley, 1997), N sinks via NO^-₂ fixation may also vary in soils under different tree species.

To the best of our knowledge, there have been no previous reports on differences among tree species in the recovery of ¹⁵NO^-₂ in SOM. Here we report the results of an experiment where ¹⁵NO^-₂ was added to soils under three tree species (American beech, northern red oak, sugar maple) from the Catskill Mountains in New York state. Previous studies have found that rates of litter decomposition and N cycling can vary significantly among these species, with decomposition rates and nitrification tending to be greatest under maple, intermediate under beech, and lowest under oak (Pastor and Post, 1986; Berg and McClaugherty, 1987; Finzi et al., 1998; Lovett and Rueth, 1999; Verchot et al., 2001). The objectives of this study are to determine the recovery of ¹⁵NO^-₂ after 24 h and 30 d of incubation in the following pools: (i) microbial biomass, (ii) extractable inorganic, (iii) SOM, (iv) readily mineralizable, (v) N₂, and (vi) N₂O, and to compare these recoveries among the three tree species. We hypothesized that: (i) ¹⁵NO^-₂ would move quickly (<1 d) into the SOM pool, (ii) ¹⁵N incorporated into SOM would be relatively recalcitrant to mineralization, (iii) recovery of ¹⁵NO^-₂ in SOM would be greatest under red oak as leaf litter of this species is recalcitrant relative to sugar maple (Pastor and Post, 1986; Berg and McClaugherty, 1987), and thus would be expected to exhibit greater incorporation of NO^-₂ into SOM, and (iv) recovery of ¹⁵N would not be substantial in the microbial biomass or extractable inorganic pools, even after 30 d of incubation.

	MATERIALS AND METHODS

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Site Description
The Catskill Mountains in southeastern New York State comprise an area of approximately 5000 km² and receive among the greatest rates of atmospheric N deposition in the northeastern USA (approximately 11 kg N ha^-1 yr^-1; Ollinger et al., 1993; Lovett and Rueth, 1999). Bedrock consists primarily of flat-lying sandstones, shales, and conglomerates of Devonian age (Stoddard and Murdoch, 1991), and is overlain by glacial till of variable depth (Rich, 1934). Soils of the region are primarily thin inceptisols of moderate to high acidity and are generally stony and well-drained (Lovett et al., 2000; Stoddard and Murdoch, 1991). The climate of the region is characterized by cool summers and cold winters. The Slide Mountain weather station at an elevation of 808 m in the central Catskills has a mean annual temperature of 4.3°C (January mean = -8.5°C, July mean = 16.7°C) and a mean annual precipitation of 153 cm, approximately 20% of which falls as snow. The most dominant tree species in the Catskills are sugar maple, American beech, yellow birch (Betula alleghaniensis), and northern red oak (McIntosh, 1972).

Field Techniques
Plots dominated by sugar maple, American beech, and red oak were selected in the central Catskills. Each plot was 3 m in radius and included 2 or 3 canopy dominant trees of the target species. These small plots were located within a 6-m radius plot of nearly monospecific composition to minimize the edge effects from neighboring trees of other species. For each species, two plots were sampled within each of two watersheds, giving a total of four plots per species. Soils at these watersheds were of the Arnot (loamy-skeletal, mixed, active, mesic Lithic Dystrudepts), Lackawanna (coarse-loamy, mixed, active, mesic Typic Fragiudepts), and Oquaga (loamy-skeletal, mixed, superactive, mesic Typic Dystrudepts) series. Litter (Oi horizon) was removed from the soil surface and then samples of the organic soil in the forest floor (Oe and Oa horizons) were obtained using a tulip bulb corer. The cumulative depth of the Oe and Oa horizons ranged from 1 to 8 cm. Four to five cores were sampled per plot and composited to create one soil sample per plot. Soils were sampled in June of 1999. Soil pH measured in deionized water at a 2:1 ratio (water/soil) varied from 3.3 to 4.7 at our plots, while organic matter contents measured by loss on ignition varied from 31 to 84%.

Laboratory Methods
Soils were passed through an 8-mm sieve and thoroughly homogenized. A subsample was dried in an oven at 60°C to determine the gravimetric soil moisture content and a second subsample was used to determine the field capacity gravimetrically after saturating the sample and allowing it to drain overnight. Each sample was then wetted with deionized water to a moisture content 60% of the field capacity. For each plot, 12 glass Mason jars (946 mL) containing 10 g of wetted soil were covered with an airtight lid fitted with butyl rubber septa (Robertson et al., 1999). Four plastic specimen cups were also set up with 10 g of wetted soil. Six of the glass jars and two specimen cups had no NO^-₂ label added (referred to as controls). To label the other six jars and two specimen cups, a 10-mL syringe fitted with a 2-gauge needle was used. Two milliliters of 1.3 mmol L^-1 Na¹⁵NO^-₂ (99 atom% enriched) was added through the rubber septa into the jars or dispensed directly to the soil in the specimen cups. The lids were then secured on the specimen cups. Three jars and one specimen cup for each of the control and label treatments were incubated for 24 h at room temperature (20°C) and the other set of jars for the control and label treatments were incubated in the dark at 20°C for 30 d.

The quantity of added NO^-₂ was equivalent to 0.26 µmol ¹⁵N/(g wetted soil). Given a range in extractable NO^-₂ concentrations from 0.2 to 0.8 nmol g^-1 in soils of northern hardwood forests (R. Venterea, personal communication, 2002), our addition of ¹⁵NO^-₂ caused a 300- to 1300-fold increase in the extractable NO^-₂ pool. Nelson and Bremner (1969) observed that increasing the amount of NO^-₂ added to soils from 0.7 to 70 mmol g^-1 did not affect the percentage recovery of N in SOM; note, however, that these authors added over three orders of magnitude more NO^-₂ than was added in our study. As we were unable to find any other studies that examined the effects of varying quantities of NO^-₂ addition on N recovery, we are unsure how our perturbation of the NO^-₂ pool affected our results. Bancroft et al. (1979) found that a NO^-₂ addition of 0.07 µmol g^-1 inhibited CO₂ evolution and O₂ utilization for 6 h but that an NO^-₂ addition of 0.36 µmol g^-1, similar to the amount added in our experiment, stimulated CO₂ evolution after 1 d of incubation. It was therefore unclear how or if our NO^-₂ addition affected microbial activity.

Samples for determining the ¹⁵N/¹⁴N ratios of the gases N₂ and N₂O were obtained by taking a 9-mL sample of the headspace in the Mason jars after 24 h and 30 d of incubation and storing the sample in a glass vial. After taking gas samples at 24 h and 30 d, the soils from these same jars were sampled to determine the extractable NH⁺₄ and (NO^-₂ + NO^-₃) concentrations and the ¹⁵N/¹⁴N ratio of the extractable inorganic N pool. Soils were extracted by adding 100 mL of 2 M KCl to the 10-g soil sample, shaking the sample twice during the first hour, allowing it to stand overnight, and then filtering the extract into clean polyethylene bottles through Whatman 41 filter paper (Whatman Ltd., Maidstone, UK). Extractable NH⁺₄ and (NO^-₂ + NO^-₃) concentrations were determined using phenate colorimetry and Cd reduction, respectively, on a Perstorp Analytical Flow Solution 3000 autoanalyzer (Alpkem Corporation, Wilsonville, OR). Another two jars each were used to determine ¹⁵N recovery in microbial biomass following the chloroform fumigation incubation method (Horwath and Paul, 1994). The ¹⁵N recovery in microbial biomass was calculated as the difference in extractable inorganic ¹⁵N between samples that had been fumigated with chloroform, reinoculated, and incubated aerobically for 10 d and samples that had been incubated aerobically for 10 d but were unfumigated. For the unfumigated samples, the production of extractable ¹⁵N during the 10-d incubation was used as an estimate of the readily mineralizable ¹⁵N pool. To determine ¹⁵N levels in the KCl extracts for the extractable inorganic, readily mineralizable, and microbial biomass pools, an N-diffusion technique was used (modified from Stark and Hart [1996] and Brookes et al. [1989]). After 24 h and 30 d of incubation, soils in the specimen cups were oven dried at 60°C for 24 h, ground to a fine powder using a KLECO 4200 pulverizer (Garcia Machine, Visalia, CA), and analyzed for total C and N by dry combustion on a Carlo-Erba NA1500 element analyzer (Carlo-Erba Strumentazione, Milano, Italy). A subsample of the ground soil was used to determine the ¹⁵N/¹⁴N ratio of the soil.

All ¹⁵N analyses were performed at the University of California at Davis under the supervision of D. Harris. Total soil, microbial biomass, and extractable inorganic ¹⁵N/¹⁴N ratios were determined on a Europa Scientific Integra, a continuous flow Isotope Ratio Mass Spectrometer (IRMS) integrated with on-line combustion (PDZ Europa, Cheshire, England). The ratios of ¹⁵N/¹⁴N in N₂ and N₂O were determined on a Europa Scientific Hydra 20/20, a continuous flow IRMS (PDZ Europa, Cheshire, England).

Calculations and Statistical Analyses
Recoveries of ¹⁵N for each of the pools were calculated as the difference in ¹⁵N between the label and control treatments for each replicate. All ¹⁵N recoveries were expressed as percentage of the original quantity of ¹⁵NO^-₂ added. The recovery of ¹⁵N in SOM was calculated as:

[1]

Note that dissolved organic N (DON) will be included in our estimate of ¹⁵N recovery in the SOM pool. Potential net N mineralization was calculated as the difference in the extractable inorganic N concentrations [NH⁺₄ + ] observed at 30 d and 24 h. Potential net nitrification was calculated similarly using extractable (NO^-₂ + NO^-₃) concentrations.

Statistical analyses were performed using SAS software at the = 0.05 level (SAS, 1989). Two-way analysis of variance (ANOVA) was performed using time (24 h and 30 d) and tree species (maple, beech, oak) as factors on ¹⁵N recovery in the following pools: (i) SOM, (ii) extractable inorganic, (iii) microbial biomass, (iv) readily mineralizable, (v) N₂, and (vi) N₂O. Two-way ANOVA using tree species and time as factors was also performed on: (i) extractable soil NH⁺₄ and (NO^-₂ + NO^-₃) concentrations, (ii) total soil C and N concentrations, and (iii) the soil C/N ratio. One-way ANOVA was performed on potential net N mineralization and nitrification using species as a factor. Tukey's honestly significant difference test was used to determine significant differences between species. Pearson correlation coefficients were calculated among the ¹⁵N recovery variables and between the ¹⁵N recovery variables and soil extractable NH⁺₄ and (NO^-₂ + NO^-₃) concentrations, total soil C and N, soil C/N ratio, and potential net N mineralization and nitrification for all data as well as separately for each tree species.

	RESULTS

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The mean total ¹⁵N recovery (sum of ¹⁵N recoveries in the soil, N₂, and N₂O pools) for all data was 70.6% (SE 3.2%), and ranged from 36.3 to 92.3%. For all data, the average recovery of ¹⁵N was greatest for the SOM pool, followed by the extractable inorganic pool (Table 1). Soil organic matter was the dominant fate of the ¹⁵N tracer for 21 of the 24 samples. The minimum recovery of ¹⁵N as SOM (0%; Table 1) occurred for only one outlying sample. If this outlier is excluded, the minimum recovery in SOM was 20%. Mean recoveries in microbial biomass, readily mineralizable, N₂, and N₂O pools were relatively small for all data (Table 1). The average percentage of the readily mineralizable ¹⁵N of the ¹⁵N in the SOM pool was 12.4% (SE 2.4%), ranging from 0 to 57%.

View larger version (27K): [in this window] [in a new window]   Fig. 1. Results of two-way analysis of variance testing the effects of (a) tree species and (b) time of incubation on mean 15NO-2 recoveries in various pools for soils from the Catskill Mountains, New York. Error bars are + one standard error. Bars within a pool with different letters are significantly different as determined by Tukey's honestly significant difference test at = 0.05. Number of observations = 8 for each mean value in panel (a), except N2 and N2O of maple which had seven as the result of sample loss from instrument problems. Number of observations equals 12 for each mean value in panel (b), except N2 and N2O at 24 h which had 11 as the result of sample loss from instrument problems.

For all samples, the ¹⁵N₂ recovery was positively correlated with extractable NH⁺₄ concentrations and negatively correlated with extractable inorganic ¹⁵N recovery (Table 3). For all samples, microbial biomass ¹⁵N recovery was positively related to extractable soil (NO^-₂ + NO^-₃) concentrations as well as potential net nitrification rates, and SOM ¹⁵N recovery was positively correlated with soil total C concentrations and negatively correlated with potential net N mineralization rates (Table 3). For samples from beech stands, extractable inorganic ¹⁵N recovery was negatively correlated with ¹⁵N₂ recovery as well as with extractable soil NH⁺₄ concentrations, and microbial biomass ¹⁵N recovery was negatively correlated with the soil C/N ratio (Table 4). Additionally, for samples from beech stands, ¹⁵N₂ recovery was positively correlated with extractable NH⁺₄, while soil organic matter ¹⁵N recovery was negatively correlated with both potential net N mineralization and nitrification. For samples from maple stands, microbial biomass ¹⁵N recovery was positively related to extractable inorganic ¹⁵N recovery, and ¹⁵N₂ recovery was negatively related to soil C/N ratio (Table 4). For samples from oak stands, microbial biomass ¹⁵N recovery was positively correlated with extractable NH⁺₄ concentrations, and ¹⁵N₂O recovery was positively related to potential net mineralization and nitrification rates. Additionally, for soils from oak stands, extractable inorganic ¹⁵N recovery exhibited a positive relationship with potential net mineralization and nitrification rates, and SOM ¹⁵N recovery was positively related to soil total C concentrations and negatively related to extractable soil (NO^-₂ + NO^-₃) concentrations as well as potential net mineralization and nitrification rates.

	DISCUSSION

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Inefficient measurements of microbial biomass using the chloroform-fumigation technique may have resulted in underestimates of the ¹⁵N recovered in microbial biomass. However, even if our estimate of microbial biomass was only 50% efficient, the average recovery of ¹⁵N in microbial biomass would have increased from 4.2 to 8.4% while the average recovery in SOM would have decreased from 38.9 to 34.7%. Under this scenario, SOM was still the dominant date of the tracer ¹⁵N.

In contrast with our hypothesis, the products of ¹⁵N incorporated into SOM were more labile than native soil organic N. The average recovery of ¹⁵N in the readily mineralizable pool was 12% of the mean recovery of ¹⁵N in SOM, while the potentially mineralizable pool (extractable NH⁺₄ + NO^-₂ + NO^-₃) was 3% of the total soil N. Additionally, our measure of the readily mineralizable pool, being a net rate between gross mineralization and microbial immobilization, likely underestimated the quantity of ¹⁵N mineralized from the ¹⁵N pool in SOM. Our finding that the products of ¹⁵NO^-₂ incorporation were more labile than native soil organic N agreed with the results of Smith and Chalk (1979) who recovered 20 and 10% of fixed ¹⁵NO^-₂ and native soil N, respectively, in the extractable inorganic pool after 70 d of incubation.

Recoveries of ¹⁵NO^-₂ addition in SOM during the current experiment were generally greater than recoveries of ¹⁵NO^-₂ addition in SOM observed in previous experiments using agricultural soils. Nelson and Bremner (1969) recovered between 0 to 8% of ¹⁵NO^-₂ addition in SOM in unsterilized soils after a 24-h incubation. Bremner and Fúhr (1966) and Bremner and Nelson (1968) recovered between 6 and 8% and between 2 and 15%, respectively, in SOM immediately after ¹⁵NO^-₂ addition to unsterilized soils. Smith and Chalk (1979) recovered between 22 and 28% in SOM after ¹⁵NO^-₂ addition to unsterilized soils. Smith and Chalk (1980) recovered between 1 and 30% of ¹⁵NO^-₂ addition in SOM after 24 h of incubation of unsterilized soils. Boudot and Chone (1985) recovered between 56 and 68% of ¹⁵NO^-₂ addition as soil organic N after 2 d of incubation of unsterilized soils. These results demonstrate that the incorporation of NO^-₂ into SOM is as quantitatively significant in organic forest soils from the Catskills as in agricultural soils.

Although considerable research has focused on the capacity of forest soils to retain atmospherically derived N, there has been relatively little study of the role of NO^-₂ fixation in ecosystem N retention or of the role of microbial intermediates, such as NO^-₂, in the internal N cycle of forests. Dail et al. (2001) recovered between approximately 40 to 50% of ¹⁵NO^-₂ addition as insoluble soil organic N in unsterilized O horizon soils and between approximately 10 to 30% as insoluble soil organic N in sterilized O horizons from mixed-hardwood stands at Harvard Forest, Massachusetts, suggesting that the incorporation of NO^-₂ into SOM may occur via both biotic and abiotic processes. Results of the current experiment, coupled with those of Dail et al. (2001), indicated that NO^-₂ fixation into SOM might be an important mechanism in the retention of inorganic N in forest soils that receive elevated inputs of atmospheric N deposition. Nitrite fixation is expected to be most important in soils where the supply of NH⁺₄ exceeds sinks for NH⁺₄ other than oxidation (abiotic fixation, plant and microbial uptake, leaching). These conditions are most likely to be fulfilled in N saturated systems where N supply exceeds biotic N demand. For example, Tietema (1998) found along a gradient of N deposition that gross nitrification was evident in two N saturated ecosystems but not in two N limited systems in Europe. Berntson and Aber (2000) suggested that microbial immobilization of NO^-₃ may be a less significant sink for NO^-₃ in N saturated than in N limited ecosystems, while abiotic sinks may become more important. In N saturated ecosystems where the retention of N via biotic sinks becomes less tight, the fixation of NO^-₂ may restrict the production and leaching of NO^-₃. However, the importance of NO^-₂ fixation as a mechanism of N retention will depend on how well this process competes for other sinks for NO^-₂ (e.g., oxidation to NO^-₃ and dissimilatory reduction).

The unrecovered ¹⁵N (mean 29.4%, range 7.7 to 63.7%) likely reflected production of gases that were not measured in our experiment. These unmeasured gases may have included nitric oxide (NO) and methyl nitrite (Stevenson and Swaby, 1964). For example, Venterea and Rolston (2000a) observed that substantial production of NO in agricultural soils resulted from abiotic reactions involving NO^-₂. Measurement of ¹⁵NO, however, is currently problematic as the result of the high reactivity of this gas (Sich and Russow, 1999). Stevenson et al. (1970) added NO^-₂ to lignin at pH 6 and 7 and found that the average ratio of NO/(N₂O + N₂) produced was 6.7. Multiplying this ratio by the average recovery of ¹⁵N in the (N₂O + N₂) pool for the current experiment gave an estimate of the average recovery for NO of 37%, greater than the mean unrecovered ¹⁵N. Thus, reactions between NO^-₂ and SOM may have accounted for upwards of 70% of the fate of the ¹⁵N tracer. Although soil chemistry differed between our experiment and that of Stevenson et al. (1970), lignin or lignin-like compounds are likely to be a significant component of our organic forest soils. Furthermore, the lower pH of our soils than those of Stevenson would be expected to enhance nitrosation reactions.

Roles of Tree Species in the Fate of ¹⁵NO^-₂ Tracer
Soils under oak had similar rates of potential net N mineralization and concentrations of extractable NH⁺₄ compared with the other species, but soils under oak had significantly lower potential net nitrification rates and extractable (NO^-₂ + NO^-₃) concentrations than maple (Table 2). These patterns indicated that NH⁺₄ was produced readily in soils under oak but some mechanism(s) prevented the oxidation of NH⁺₄ to NO^-₃. The fixation of NO^-₂ onto SOM following the oxidation of NH⁺₄ to NO^-₂ is one mechanism that potentially explains our results. Results from the current experiment, however, did not support our hypothesis that the incorporation of NO^-₂ into SOM would vary significantly among tree species, as ¹⁵N recovery in SOM did not vary significantly among tree species (Table 2). Potential explanations for the greater net nitrification rates under maple than oak include allelopathic inhibition of nitrification via secondary plant compounds and differences in the composition of the microbial population between soils under oak and maple. For example, Lodhi and Killingbeck (1980) found that nitrification was inhibited as the result of toxicity of secondary plant chemical compounds to Nitrosomonas in soils under ponderosa pine in North Dakota. Myers et al. (2001) determined that soil microbial communities under oak species were dominated by fungi, while communities under sugar maple-basswood stands were dominated by bacteria in Michigan. Based on different temporal patterns of microbial uptake of ¹⁵NH₄ in soils under different species from the same plots used in the current experiment, Templer (2001) hypothesized that microbial communities differed in soils between maple and oak stands in the Catskill Mountains. Soil acidity did not appear to be responsible for the variation in nitrification between oak and maple, as the mean soil pH under maple (4.0) was only moderately greater than the mean pH under oak (3.7), while beech had intermediate nitrification rates between oak and maple but had the lowest mean pH (3.5). Verchot et al. (2001) found that rates of gross nitrification were significantly greater in forest floors under maple than oak in the Catskills, whereas there were no significant differences in gross mineralization or in microbial immobilization of NH⁺₄ and NO^-₃ between these species. These results suggest that the low potential net nitrification rates in oak plots resulted from inhibition of nitrification or an inability to nitrify NH⁺₄ as the result of the composition of the microbial community, rather than microbial immobilization of inorganic N.

A recovery of 0% for ¹⁵N in SOM was observed for one of the oak soil samples after a 30-d incubation. This oak soil sample was anomalous in several respects. First, it exhibited a potential net nitrification rate (0.6 µmol g^-1 d^-1) more than an order of magnitude greater than the other three oak samples (mean 0.01 µmol g^-1 d^-1). Second, it had the lowest soil C concentration (25%) of all soils sampled for this experiment (including soils under beech and maple). Third, it exhibited greater recovery of ¹⁵N in the readily mineralizable pool (12.6 ± 2.1%; mean ± 1 SE) than the other oak plots (6.6 ± 1.2%), demonstrating that this one oak plot was responsible for the significantly greater recovery of ¹⁵N in the readily mineralizable pool in oak than the other species (Fig. 1). It is unclear why this oak plot behaves differently in these respects than the other oak plots, but we are currently investigating this irregularity.

The moderate correlation between soil total C and ¹⁵NO^-₂ recovery in SOM for all data (Table 3) was driven by oak as this correlation was evident for soils under oak but not the under the other species (Table 4). This pattern for oak was consistent with previous studies that found that NO^-₂ fixation increases with soil organic matter content (e.g., Nelson and Bremner, 1969; Bremner and Fúhr, 1966). Interestingly, a negative correlation between ¹⁵NO^-₂ recovery in SOM and the concentration of extractable (NO^-₂ + NO^-₃) was observed in soils under oak, but not under the other species (Table 4). Furthermore, ¹⁵NO^-₂ recovery in SOM under oak and beech exhibited significant negative correlations with net N mineralization and nitrification, whereas these correlations were not apparent under maple (Table 4). As soil C, extractable (NO^-₂ + NO^-₃) concentrations, and potential net nitrification rates are indicators of soil quality, these patterns in oak soils, being largely driven by the anomalous plot noted above, suggest an inverse relationship in oak soils between the ¹⁵NO^-₂ recovery in SOM and the quality of the SOM.

While the current experiment demonstrated that the incorporation of NO^-₂ into SOM is relatively rapid, we were unable to determine conclusively if this incorporation occurred via abiotic or biotic processes. Sterilization of soils will be a useful tool for distinguishing between the biotic and abiotic mechanisms of NO^-₂ immobilization. As previous studies have indicated that phenolic compounds have an important role in abiotic NO^-₂ fixation, the sterilization must be performed in a manner that does not change the structure of the phenolic compounds in the soil. Comparison between the incorporation of NO^-₂ into SOM and the incorporation of the other inorganic N species (NH⁺₄, NO^-₃) would be useful in more precisely determining the role of NO^-₂ in the retention of inorganic N. Examination of the turnover of the organic N products of NO^-₂ fixation at time scales of >1 mo would help to better determine the potential for this N retention pathway to be an effective long-term N sink in forest ecosystems. Additionally, competition between NO^-₂ fixation and other fates for NO^-₂ should be explored.

	ACKNOWLEDGMENTS

 
This research was supported by the USDA NRI Competitive Grants program (grant # 96-35101-3126), the National Science Foundation (DEB 9981503) and the A.W. Mellon Foundation. We would like to thank Rod Venterea for helpful discussions on this topic and Michele Casler and Chuck Schirmer for help with field and laboratory work. This is a contribution to the program of the Institute of Ecosystem Studies.

Received for publication March 5, 2002.

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