Trace gas responses of tropical forest and pasture soils to N and P fertilization

Trace gas responses of tropical forest and pasture soils to

N and P fertilization

Paul A. Steudler,1 Diana C. Garcia-Montiel,1 Marisa C. Piccolo,2 Christopher Neill,1

Jerry M. Melillo,1 Brigitte J. Feigl,2 and Carlos C. Cerri2

Received 31 January 2001; revised 7 December 2001; accepted 10 December 2001; published 24 May 2002.

[1] We measured the responses of nitric oxide (NO), nitrous oxide (N2O) and carbon dioxide(CO2) to nitrogen (N) and/or phosphorus (P) fertilization in a mature moist tropical forest and an11-year-old pasture in the Brazilian Amazon. Nitrogen was applied in two forms, ammonium(NH4

+) and nitrate (NO3�). In the forest, NO emissions increased by 4 to 9 times the controls in the

NH4+ amended plots. Nitrous oxide emissions showed a small response only in the NH4

+ amendedplots. In the pasture, NO emissions during the first 7 days after fertilization with either form of Nwere about twice those in the control plots. Nitrous oxide emissions increased more than 18 timesthe controls in the NO3

� amended plots 1 day after fertilization. The estimated yields of totalnitrogen oxide loss from the forest were between 0.2 and 1.6% of the applied nitrogen,predominately as NO. Pasture yields were greater, up to 2.8% of the applied nitrogen,predominately as N2O. In the context of Rondonia and other regions in the Amazon Basin, pasturemanagement practices are changing to include increased use of fertilizer, particularly in olderpastures that have lower NO and N2O emissions than the original intact forests. This may lead tolarge short-term releases of N2O and alter the future N2O emissions from the Basin. INDEXTERMS: 0315 Atmospheric Composition and Structure: Biosphere/atmosphere interactions; 0322Atmospheric Composition and Structure: Constituent sources and sinks; 1615 Global Change:Biogeochemical processes (4805); KEYWORDS: Nitric oxide, Nitrous oxide, Carbon dioxide,tropical forest, tropical pasture, N and P fertilization

1. Introduction

[2] Nitrogen oxide gases such as nitric oxide (NO) and nitrousoxide (N2O) are important gases that affect the radiative forcing ofthe planet and the chemical reactivity of the atmosphere [Pratheret al., 1995]. The production of these gases from terrestrialecosystems has a large biological component that is sensitive tohuman perturbations. Global inventories of NO and N2O sourcesand sinks suggest that tropical regions are important sources ofthese gases. The magnitude of this tropical source is believed to beincreasing because of changes in land use, increased nitrogendeposition, and use of nitrogen-containing fertilizers [Davidsonand Kingerlee, 1997; Kroeze et al., 1999; Matson et al., 1999;Breuer et al., 2000].Galloway et al. [1995] estimated that in Centraland South America, nitrogen deposition is expected to increase byfourfold and nitrogen fertilizer usage is projected to double by 2020.[3] It is widely recognized that increased use of nitrogen

fertilizers in agricultural systems enhances the emissions of thesenitrogen oxide gases [Eichner, 1990; Cole et al., 1996; Mosieret al., 1998]. Most observations of this enhancement are fromtemperate systems, but a small set of measurements exist fromtropical agricultural systems planted in corn, bananas, and com-mercially valuable tree plantations [Davidson et al., 1996; Matsonet al., 1996; Veldkamp and Keller, 1997; Veldkamp et al., 1998,1999; Weitz et al., 1999; Crill et al., 2000].

[4] One of the largest tropical regions experiencing rapidchanges in forest conversion to agriculture is in the Amazon Basin[Skole and Tucker, 1993; Instituto Nacional de Pesquisas Espa-ciais, 1999, 2000]. Much of the deforested area in the BrazilianAmazon Basin is converted to cattle pasture [Serrao, 1992].Management of these existing pastures is changing rapidly. Asthese pastures grow older, their productivity declines. Many of theregimes aimed at maintaining or raising pasture productivityinvolve the use of nitrogen and phosphorus fertilizers [Nepstadet al., 1991]. Information on how older pastures respond to N andP fertilization is essential for estimating what the future effects willbe on N oxide releases from this region.[5] The objectives of this research were to (1) measure the short-,

intermediate-, and long-term changes in emissions of NO, N2O, andCO2 from forest and pasture soils following fertilization with nitro-gen and/or phosphorus, (2) investigate which microbial processeswere involved in the production of these gases, and (3) estimate thepercentage of the N applied that was lost as N oxide gases.

2. Materials and Methods

2.1. Sites

[6] This research was conducted in a mature forest stand and apasture created in 1987 at Fazenda Nova Vida at km 472 onhighway BR-364, in central Rondonia, Brazil. The climate ishumid tropical with an annual mean temperature of 25.5�C, annualrainfall of 2200 mm, and a dry season from May to September[Bastos and Diniz, 1982]. Soils are Kandiudults with surface soilclay contents of 23–29%.[7] We have been working at this ranch for more than 8 years in

two sequences consisting of a mature forest and pastures of variousages [Neill et al., 1995]. Forest vegetation was typical of the open,

GLOBAL BIOGEOCHEMICAL CYCLES, VOL. 16, NO. 2, 1023, 10.1029/2001GB001394, 2002

1The Ecosystems Center, Marine Biological Laboratory, Woods Hole,Massachusetts, USA.

2Centro de Energia Nuclear na Agricultura, Piracicaba, Sao Paulo,Brazil.

Copyright 2002 by the American Geophysical Union.0886-6236/02/2001GB001394

7 - 1

humid tropical forests of this region with a large number of palms.The forest had been selectively logged between 1982 and 1992with the removal of 1 to 3 trees ha�1. We studied a pasture that was11 years old at the beginning of the experiment. Pastures of this agehave much slower rates of net N mineralization and net nitrificationthan younger pastures [Neill et al., 1995], so that we expecteddifferences between fertilized and nonfertilized treatments to belarge. For management purposes, pastures of this age are beingselected by ranch owners for reformation and fertilization toenhance grass productivity.

2.2. Fertilizer Experiment

[8] To assess the effects of N and P additions on soil NO, N2O,and CO2 fluxes, six different fertilization treatments were appliedin a complete randomized block design. We established a total ofthree blocks per site (forest or pasture), and within each block thesix treatments were randomly assigned to 3 � 3 m plots for a totalof three replicates by treatment, or 18 plots per site. The sixfertilization treatments were ammonium, nitrate, ammonium +phosphate, nitrate + phosphate, phosphate, and control. Ammo-nium was applied as NH4Cl at 100 kg N ha�1 yr�1 and nitrate asNaNO3 at the same annual rate as ammonium. Phosphate wasapplied as Na2HPO4 at 40 kg P ha�1 yr�1. Fertilizer was applied inthree equal amounts spaced throughout the year (March, August,and November 1998). At each application fertilizer was mixed with150 g of acid-washed dry sand so it could be distributed evenly inthe plots.[9] Measurements were conducted 2 or 3 days before and 1, 7,

and 14, 180 (6 months) and 390 days (13 months) after fertilizationto examine the short-, intermediate-, and long-term responses. Wemeasured the gas fluxes and the soil properties, shaded air, and soiltemperatures (surface and 2, 5, and 10 cm depths), soil moistures,net N mineralization, and net nitrification rates and N pools at eachsampling date. Resin P pools were measured prefertilization and at7 and 14 days after fertilization. Measurements were made usingthe following procedure. Fertilizer was applied dry to one block inthe forest and pasture and the next rain event was allowed to washthe fertilizer into the soil. Measurements were then begun 18 to 24hours after the rain ceased. The other two blocks were fertilizedand measured sequentially in the same manner over the next 7 days.Measurement of one block in the forest and pasture required 1 day.The short-term measurements were made during the wet season,and the intermediate-term measurements at 6 months after fertil-ization were made during the dry season. To examine the longer-term responses, we also measured the same variables 13 monthsafter the initial fertilization (wet season) but after two additionalfertilizations in August and November.

2.3. Measurement of Gas Fluxes

[10] Soil fluxes of NO, N2O, and CO2 were measured simulta-neously using a recirculating chamber design similar to the systemsdeveloped by Davidson et al. [1991], Sundquist et al. [1992] andVerchot et al. [1999]. We used a modified two-piece chamberdesign [Bowden et al., 1990] where the lower portion of the PVCchamber (anchor) was inserted into the soil several days in advanceof the first measurement and left in place for the duration of theexperiment to allow repeated sampling at the same locations. Oneanchor was located in the central area of each plot. This effectivelyleft a 0.5-m buffer zone along the plot edges to avoid any edgeeffects. During each flux measurement the chamber top (8.38 L or5.94 L) was placed on the anchor and the changes in headspace-gasconcentrations were measured over a 15- to 20-min incubationtime. The chamber top was also equipped with a luer lock samplingport for collecting headspace-gas samples for N2O analysis. Gasfluxes and soil parameters were measured in the forest between0900 and 1100 LT and in the pasture between 1200 and 1500 LT.

[11] We used a Unisearch Associates LMA-4 NO2 analyzer tomeasure NO concentrations and a LICOR model 6252 infrared gasanalyzer (IRGA) to measure CO2 concentrations. Our design usedthe LICOR pumping system to circulate air at 1 L min�1 through1/4-inch Teflon lines connected to the chamber top. The internalNO analyzer pump subsampled this airflow at about 400 ml min�1

and returned the air to circulating sample stream. A Campbell datalogger was used to record the outputs from the NO and CO2

analyzers at 5-s intervals. Incubations were initiated by collectingambient air concentration data for at least 1 min prior to placing thechamber top on the anchor to ensure initial conditions were stableand representative.[12] The Unisearch NO2 analyzer determines NO concentrations

using a Luminol chemiluminescent technique with a CrO3 con-verter to oxidize NO to NO2. We modified the analyzer to increasethe efficiency of water removal from the analyzer sample air streamby increasing the pressure differential across the stock Nafion dryerand by connecting an inline silica gel drying tube to the outer shellof the drier. This modification resulted in stable converter efficien-cies for at least 50 hours of use under 25–30�C temperature and�90% relative humidity conditions. We also added a 1/4-inchTeflon line to return the exhaust from the analyzer air pump back tothe circulating sample air stream.[13] For NO flux calculation we used data collected 2 min after

chamber closure. This procedure allowed deposition of ambientNO2 and O3 to the soil surface [Davidson et al., 1991]. When wemeasured a very rapid increase in NO concentration, such as in theNH4

+-containing fertilized plots, the deposition period was reducedto about 1 min. A 1.032 ppmv NO standard in O2-free N2 (Scott-Marrin, Riverside, California) was diluted with NO/NO2-free air toproduce a number of NO calibration standards, usually 49.2 ppbv.Ambient air was passed sequentially through scrubbers containingdrierite and ascarite to produce NO/NO2-free air (<0.06 ppbv NO).The analyzer was calibrated before and after each daily fieldsampling and varied by less than ±10 between calibrations.[14] A certified standard of 826 ppmv CO2 in air from Scott

Specialty Gases of was used to calibrate the IRGA. CO2 emissionswere calculated using the steepest portion of the concentration dataagainst incubation time from the first 2–4 min after the chamberwas closed. The analyzer was calibrated before and after each dailyfield sampling and varied by less than ±1% between calibrations.[15] Headspace-gas samples were collected using 10-ml Becton

Dickinson syringes equipped with stopcocks for determination ofN2O concentrations at the beginning and at 2 or 3 times during the15-min chamber incubation. Nitrous oxide concentrations weredetermined using electron capture gas chromatography with adetector temperature of 310�C [Bowden et al., 1990]. Gas sampleswere analyzed on site within 12 hours of collection. A Scott-certified standard of 0.985 ppmv N2O in N2 was used forcalibration. Prior calibrations with multiple standards showed thatthe detector response was linear from 0.310 ppmv (ambient) to atleast 1.00 ppmv. Nitrous oxide fluxes were calculated using thelinear change in N2O concentration against incubation time.

2.4. Ancillary Measurements

[16] At the same time that gas measurements were conducted,we also collected three 2.5-cm-diameter soil cores from the 0–5and 5–10 cm depths in each plot and then composited these bydepth. These samples were used for determinations of gravimetricsoil moisture, inorganic N and P pools, and net rates of Nmineralization and nitrification in each plot. Ammonium andNO3

� pools were measured by extraction with 2 N KCl. Net N min-eralization and net nitrification rates were measured with 7-dayaerobic laboratory incubation [Neill et al., 1995]. Soil P pools weredetermined only in the 0–5 cm of soil depth by the resin-extractable P method used in the first step of the sequential P

7 - 2 STEUDLER ET AL.: TRACE GAS RESPONSES OF SOILS TO N AND P FERTILIZATION

fractionation procedure described by Tiessen and Moir [1993].Resin-extractable P was determined by placing 1 g of air-dry soilinto 50-ml polypropylene centrifuge tube and shaking for 16 hourswith two anion resin strips (9 � 62 mm strip�1) in 30 ml ofdeionized water. The anion exchange resin was then removed byshaking for 1 hr in 30 ml of 0.5 mol L�1 HCL solution that wasthen used for P determinations. Phosphorus concentrations weremeasured by the colorimetric procedure of Murphy and Riley[1962] after pH of the final extracted solution was adjusted. Soilmoisture content was converted to percent water-filled pore space(WFPS) using soil porosity for these sites [Steudler et al., 1996].

2.5. Statistical Analyses

[17] The effects of different forms of N and P fertilization wereevaluated with one- and two-way analysis of variance (ANOVA)using the General Lineal Model of SYSTATA 9.0 program (SPSSInc., 1997). One-way ANOVAs were used to evaluate the effects ofN and P treatments on NO, N2O, and CO2 fluxes at each time afterfertilization. Two-way ANOVAs were used to evaluate the inter-action between treatment and time after fertilization on NO, N2O,and CO2 fluxes. All ANOVAs were performed as n = 3 for the sixtreatments. We used individual single-degree-of-freedom compar-isons from the General Lineal Model of SYSTATA 9.0 program totest for planned comparisons between treatments at each fertiliza-tion measurement time. Data were well transformed when require-ments of normality and homocedasticity were not met. Results ofthe ANOVAs were considered significant when p � 0.05.

3. Results

3.1. Temperature

[18] Forest, air, and surface soil (0–2 cm) temperatures variedlittle during the first 2 weeks of the experiment, where the mean airtemperature was 24.8� ± 0.13�C and the mean surface soil temper-ature was 24.5� ± 0.07�C. There were only small differences inmean air (25.7� ± 0.08�C) and surface soil (23.7� ± 0.25�C)temperatures in the forest 6 and 13 months after fertilizationcompared with the first 2 weeks.[19] Pasture air and surface soil temperatures were much higher

than in the forest during the first two weeks, with means of 30.9� ±0.49�C and 27.7� ± 0.21�C, respectively. Pasture soil temperatureshad a much greater range (25.5� to 36.5�C) than the forest.Temperatures in the pasture six months after fertilization werebetween 6� and 10�C higher than in the forest, with mean air andsurface soil temperatures of 36.0� ± 1.17�C and 29.0� ± 0.42�C,respectively. Temperatures in the pasture 13 months after fertiliza-tion were similar to those measured during the first 2 weeks. Theincreased temperatures and variability in the pasture likely reflectsthe large differences between the canopy cover of the forestcompared with the pasture.

3.2. Soil Moisture

[20] In the forest the pretreatment soil WFPS was 36.1 ± 0.64%at 0–5 cm and 45.1 ± 0.45% at 5–10 cm (Table 1). These appearto be typical wet-season values. One day after fertilization, andimmediately following a rain, WFPS values increased only slightly,by about 2% WFPS at 0–5 cm and about 1% WFPS at 5–10 cm.Water-filled pore space was about 40% lower at both depths 6months after fertilization, during the dry season. Thirteen monthsafter the start of the study, we again measured percent WFPSduring the wet season and observed values that were similar to thepretreatment values also measured in the wet season.[21] Pretreatment soil moistures in the pasture were much higher

than in the forest at both depths (Table 1). The WFPS at 0–5 cmwas 74.3 ± 1.5%, more than double the forest, while the WFPS at5–10 cm was about 10% greater than the forest (56.2 ± 0.73%).

One day after fertilization the pasture WFPS was slightly lower,72.4 ± 2.21% and 55.2 ± 0.63% at 0–5 and 5–10 cm, respectively.Percent WFPS in the pasture was much lower by about one half atthe 0–5 cm and 35% at 5–10 cm 6 months postfertilization, duringthe dry season, but returned to values similar to the pretreatmentvalues 13 months after fertilization.

3.3. Nitrogen Pools and Rates

[22] In both the forest and the pasture, there were no consistentdifferences in NH4

+ or NO3� pools or net N mineralization and net

nitrification rates among the six treatments before the beginning ofthe application of the fertilizer (Table 1). This was true at both the0–5 cm and 5–10 cm depths. The highest NH4

+ pools weremeasured in the pasture NH4

+ treatment even before the applica-tion of the fertilizer. The NH4

+ and NO3� pools at 5–10 cm were

typically lower than pools at 0–5 cm.[23] In the forest, application of NH4

+ more than tripled the soilNH4

+ pools at 0–5 cm depth 1 day after fertilization (Table 1).This effect was very short-lived and disappeared 7 days afterfertilization. Application of NO3

� in the forest nearly tripled thesoil NO3

� pools at 0–5 cm depth (Table 1). This effect wasalso short-lived and disappeared 7 days after fertilization. Noeffects of fertilization were evident at 5–10 cm depth (Table 1).Six months after fertilization, NH4

+ pools were generally largerthan the pretreatment values, especially in the P treatments at5–10 depth. Nitrate pools were also much larger in all plotscompared with the pretreatment values at both depths, buttreatments did not affect NO3

� pool sizes. Thirteen monthsafter fertilization both NH4

+ and NO3� pools were similar to

pretreatment values.[24] In the pasture, application of NH4

+ increased the NH4+ pool

at 0–5 cm depth by a very small amount (Table 1). There was noeffect of NH4

+ addition on NH4+ pools at 5–10 cm depth (Table 1).

Application of NO3� in the pasture did not effect soil NO3

� poolsat either depth. Six months after fertilization, NH4

+ pools wereabout 1.5 times larger in the PO4

�3 treatment at 0–5cm depthcompared with the pretreatment values. Nitrate pools were about10 times lower compared with the pretreatment values 6 monthsafter fertilization. Thirteen months after fertilization, both NH4

+

and NO3� pools were similar to pretreatment values.

[25] We did not observe any effects of the fertilization treat-ments on rates of net N mineralization or net nitrification for theforest or pasture at either depth over the 13 month measurementperiod (Table 1).

3.4. Resin P Pools

[26] In both the forest and pasture, there were no consistentdifferences in resin P pools among the six treatments before thebeginning of the fertilizer treatments (Table 1). Fertilization with Pdid not increase P pools in the forest and were only elevated in thePO4

�3 treatment in pasture 14 days after fertilization.

3.5. Trace Gas Fluxes: Pretreatment

[27] Pretreatment NO, N2O, and CO2 fluxes from the forestwere always significantly (p < 0.05) greater than from the pasture(Figure 1). Prefertilization mean forest gas emissions were 26.2 mgNO-N m�2 hr�1, 38.7 mg N2O-N m�2 hr�1, and 351 mg CO2-Cm�2 hr�1 and showed significant variability between plots( p < 0.05). Variability in the mean flux per treatment was greaterin the forest relative to the pasture.[28] Pretreatment mean emissions in the pasture were 4.0 mg

NO-N m�2 hr�1, 11.7 N2O-N mg N m�2 hr�1, and 186 mg CO2-Cm�2 hr�1 and ranged from more than 6 to 2 times less than theforest (Figure 1). The variability in the mean flux per treatment inthe pasture was lower than in the forest, suggesting that the soil inthe pasture site was more homogeneous.

STEUDLER ET AL.: TRACE GAS RESPONSES OF SOILS TO N AND P FERTILIZATION 7 - 3

Table1.SoilMoisture,Rates

OfNetNMineralization,NetNitrification,NH4+,NO3�,andResin

PPoolsin

ForestandPasture

PlotsFertilizedWithDifferentCombinationsofNitrogen

andPhosphorusa

Treatment

Fertilization

Tim

eWater-Filled

Pore

Space,

%N

Mineralization

Rate,

mgGDS�1d�1

Nitrification

Rate,

mgGDS�1d�1

NH4+Pool,

mgGDS�1

NO3�Pool,

mgGDS�1

Resin

P,b,c

mgGDS�1

0–5cm

Depth,Forest

Control

Before

35.76

(0.95)

0.96

(0.49)

1.08

(0.62)

4.22

(0.75)

4.84

(1.75)

6.03

(0.65)

NH4+

37.53

(1.78)

1.50

(0.85)

3.10

(0.71)

3.08

(0.22)

4.62

(0.89)

5.52

(0.82)

NH4++PO4�3

36.88

(2.88)

4.05

(2.01)

3.45

(1.20)

3.44

(0.98)

4.02

(0.76)

7.02

(0.65)

NO3�

36.26

(0.25)

1.01

(0.18)

1.21

(0.20)

4.48

(1.39)

4.22

(0.75)

4.83

(0.95)

NO3�+PO4�3

34.61

(0.80)

1.80

(0.48)

1.61

(0.35)

6.23

(0.98)

3.08

(0.22)

5.32

(0.91)

PO4�3

35.61

(2.31)

1.06

(0.50)

1.16

(0.52)

4.98

(0.36)

3.44

(0.98)

5.54

(0.29)

Control

1day

after

38.39

(0.86)

2.12

(0.39)

2.59

(0.51)

14.17

(9.87)

4.48

(1.39)

ND

NH4+

37.21

(0.86)

1.59

(0.46)

3.79

(0.15)

10.40

(8.07)

6.23

(0.98)

ND

NH4++PO4�3

36.83

(0.40)

1.62

(1.00)

3.85

(0.38)

3.93

(0.92)

4.98

(0.36)

ND

NO3�

37.66

(1.68)

3.68

(0.85)

3.23

(0.50)

3.80

(0.56)

14.17

(9.87)

ND

NO3�+PO4�3

39.34

(0.26)

1.65

(0.52)

2.20

(0.73)

6.22

(1.26)

10.40

(8.07)

ND

PO4�3

40.29

(2.30)

2.40

(1.16)

2.19

(0.69)

7.52

(2.69)

3.93

(0.92)

ND

Control

7daysafter

32.76

(3.24)

0.75

(0.96)

0.93

(0.82)

6.88

(3.49)

3.80

(0.56)

6.33

(0.97)

NH4+

34.24

(2.07)

1.30

(1.07)

1.64

(1.04)

3.48

(0.92)

6.22

(1.26)

4.02

(0.12)

NH4++PO4�3

34.22

(0.46)

1.64

(0.46)

2.66

(0.29)

7.35

(4.04)

7.52

(2.69)

6.88

(1.57)

NO3�

35.54

(1.67)

2.03

(0.62)

2.40

(0.78)

5.11

(1.14)

6.88

(3.49)

5.18

(1.14)

NO3�+PO4�3

34.38

(2.48)

1.68

(0.19)

2.16

(0.11)

4.93

(0.87)

3.48

(0.92)

7.42

(0.96)

PO4�3

37.83

(2.11)

1.24

(0.09)

1.46

(0.10)

4.36

(1.55)

7.35

(4.04)

4.70

(0.66)

Control

14daysafter

36.98

(0.41)

1.85

(0.30)

2.01

(0.34)

2.11

(0.74)

5.11

(1.14)

5.41

(0.80)

NH4+

38.98

(0.96)

2.78

(0.02)

2.84

(0.09)

4.19

(0.42)

4.93

(0.87)

5.68

(0.69)

NH4++PO4�3

37.05

(2.29)

3.19

(1.55)

2.64

(1.01)

4.49

(3.01)

4.36

(1.55)

11.61

(5.17)

NO3�

37.81

(2.02)

1.32

(0.19)

1.32

(0.19)

11.0

(2.06)

2.11

(0.74)

9.07

(5.29)

NO3�+PO4�3

38.22

(0.80)

1.58

(0.36)

1.83

(0.45)

11.6

(1.86)

4.19

(0.42)

8.55

(2.34)

PO4�3

41.62

(2.80)

2.48

(1.51)

2.82

(1.85)

7.50

(0.49)

4.49

(3.01)

9.65

(0.99)

Control

6monthsafter

19.94

(0.47)

1.16

(0.52)

1.24

(0.52

6.51

(0.53)

11.0

(2.06)

ND

NH4+

21.94

(0.68)

1.52

(0.22)

1.54

(0.20)

4.87

(1.48)

11.6

(1.86)

ND

NH4++PO4�3

19.87

(1.00)

1.53

(0.25)

1.76

(0.25)

8.57

(2.77)

7.50

(0.49)

ND

NO3�

19.87

(1.26)

1.24

(0.04)

1.28

(0.06)

4.60

(0.75)

6.51

(0.53)

ND

NO3�+PO4�3

19.66

(0.26)

2.52

(0.52)

2.50

(0.47)

4.89

(0.81)

4.87

(1.48)

ND

PO4�3

21.08

(2.21)

3.51

(0.18)

2.93

(0.41)

4.12

(0.76)

8.57

(2.77)

ND

Control

13monthsafter

33.12

(1.62)

2.05

(0.41)

1.77

(0.45)

4.63

(0.40)

4.60

(0.75)

ND

NH4+

36.13

(1.96)

1.25

(0.17)

1.14

(0.23)

3.96

(1.82)

4.89

(0.81)

ND

NH4++PO4�3

35.20

(0.40)

1.54

(0.36)

1.40

(0.09)

6.20

(1.78)

4.12

(0.76)

ND

NO3�

37.88

(0.42)

1.65

(0.34)

1.55

(0.31)

1.92

(0.36)

4.63

(0.40)

ND

NO3�+PO4�3

37.58

(2.16)

3.27

(1.96)

2.64

(1.15)

7.30

(2.60)

3.96

(1.82)

ND

PO4�3

38.97

(1.02)

4.84

(2.95)

2.45

(0.82)

5.22

(2.83)

6.20

(1.78)

ND


Treatment

Fertilization

Tim

eWater-Filled

Pore

Space,

%N

Mineralization

Rate,

mgGDS�1d�1

Nitrification

Rate,

mgGDS�1d�1

NH4+Pool,

mgGDS�1

NO3�Pool,

mgGDS�1

Resin

P,b,c

mgGDS�1

0–5cm

Depth,Pasture

Control

Before

70.43

(2.73)

0.32

(1.00)

0.04

(0.10)

7.72

(2.62)

0.89

(0.50)

5.67

(0.90)

NH4+

72.15

(3.25)

0.63

(0.26)

0.02

(0.03)

7.70

(0.74)

1.15

(0.18)

7.47

(2.77)

NH4++PO4�3

73.18

(3.37)

0.86

(0.51)

0.01

(0.03)

9.02

(2.84)

0.91

(0.25)

5.42

(0.73)

NO3�

73.68

(5.00)

0.90

(1.14)

0.08

(0.04)

3.64

(1.26)

0.66

(0.08)

7.32

(0.51)

NO3�+PO4�3

77.77

(5.81)

0.97

(0.49)

0.02

(0.02)

9.85

(3.43)

0.70

(0.15)

6.22

(1.29)

PO4�3

78.41

(1.95)

0.70

(0.31)

0.09

(0.09)

7.03

(1.85)

1.51

(0.46)

5.08

(0.77)

Control

1day

after

69.52

(6.06)

0.55

(0.15)

0.01

(0.02)

5.26

(0.37)

0.50

(0.21)

ND

NH4+

73.50

(4.72)

2.48

(0.99)

0.00

(0.09)

19.13

(8.17)

0.64

(0.41)

ND

NH4++PO4�3

67.73

(3.88)

2.22

(0.31)

0.04

(0.02)

17.69

(2.13)

0.48

(0.15)

ND

NO3�

73.40

(4.15)

1.37

(0.26)

0.00

(0.01)

11.98

(1.80)

0.61

(0.26)

ND

NO3�+PO4�3

73.45

(4.84)

1.63

(0.17)

0.02

(0.07)

14.31

(1.37)

0.73

(0.17)

ND

PO4�3

76.81

(10.4)

0.22

(0.70)

0.07

(0.05)

8.48

(1.03)

0.38

(0.14)

ND

Control

7daysafter

68.91

(3.57)

0.97

(0.37)

0.08

(0.03)

6.60

(2.33)

0.79

(0.20)

15.86

(10.12)

NH4+

74.08

(9.00)

0.56

(0.13)

0.04

(0.03)

7.45

(0.81)

0.52

(0.21)

14.83

(7.31)

NH4++PO4�3

62.42

(3.50)

0.70

(0.07)

0.06

(0.03)

5.73

(0.16)

0.37

(0.11)

4.86

(0.24)

NO3�

71.87

(3.19)

0.52

(0.06)

0.03

(0.01)

6.79

(1.41)

0.71

(0.16)

6.38

(0.98)

NO3�+PO4�3

77.11

(0.42)

0.75

(0.08)

0.00

(0.01)

5.71

(0.82)

0.45

(0.04)

7.48

(1.72)

PO4�3

73.11

(2.10)

1.00

(0.38)

0.02

(0.02)

7.85

(3.33)

0.53

(0.15)

7.23

(0.49)

Control

14daysafter

70.19

(8.71)

0.53

(0.19)

0.00

(0.02)

4.53

(1.17)

0.45

(0.08)

8.25

(0.72)

NH4+

67.56

(5.15)

0.44

(0.32)

0.00

(0.03)

4.23

(1.55)

0.50

(0.12)

11.28

(6.21)

NH4++PO4�3

67.58

(9.17)

0.34

(0.20)

0.01

(0.04)

4.57

(1.93)

0.32

(0.10)

6.39

(1.77)

NO3�

70.39

(7.29)

0.54

(0.18)

0.05

(0.03)

6.24

(1.01)

0.24

(0.09)

3.77

(0.80)

NO3�+PO4�3

81.73

(4.52)

0.45

(0.44)

0.04

(0.01)

3.94

(2.73)

0.16

(0.08)

7.04

(2.61)

PO4�3

79.89

(4.93)

0.50

(0.25)

0.02

(0.01)

4.83

(1.24)

0.35

(0.06)

21.22

(6.38)

Control

6monthsafter

36.74

(1.62)

0.15

(0.04)

0.15

(0.04)

6.37

(0.58)

0.15

(0.15)

ND

NH4+

39.11

(0.85)

0.05

(0.02)

0.10

(0.02)

9.32

(2.79)

0.08

(0.06)

ND

NH4++PO4�3

33.65

(1.55)

0.12

(0.04)

0.13

(0.03)

4.56

(1.56)

0.07

(0.07)

ND

NO3�

32.40

(1.56)

0.13

(0.10)

0.09

(0.02)

5.13

(1.40)

0.23

(0.06)

ND

NO3�+PO4�3

37.16

(1.95)

0.04

(0.02)

0.06

(0.02)

6.25

(1.05)

0.27

(0.17)

ND

PO4�3

35.49

(2.02)

0.16

(0.07)

0.06

(0.08)

12.74

(3.66)

0.11

(0.11)

ND

Control

13monthsafter

71.56

(2.26)

0.04

(0.32)

0.03

(0.08)

4.49

(1.28)

0.80

(0.29)

ND

NH4+

69.95

(10.8)

2.41

(2.48)

0.49

(0.50)

17.24

(10.6)

4.13

(3.05)

ND

NH4++PO4�3

71.94

(4.21)

0.01

(0.23)

0.04

(0.10)

3.47

(0.31)

1.15

(0.32)

ND

NO3�

76.53

(4.77)

0.66

(0.61)

0.20

(0.22)

9.54

(5.10)

0.70

(0.20)

ND

NO3�+PO4�3

76.57

(2.30)

0.00

(0.27)

0.04

(0.07)

6.56

(1.36)

0.87

(0.19)

ND

PO4�3

76.92

(4.46)

0.72

(0.22)

0.11

(0.13)

5.60

(0.23)

1.45

(0.59)

ND

Table

1.(continued)


Treatment

Fertilization

Tim

eWater-Filled

Pore

Space,

%N

Mineralization

Rate,

mgGDS�1d�1

Nitrification

Rate,

mgGDS�1d�1

NH4+Pool,

mgGDS�1

NO3�Pool,

mgGDS�1

Resin

P,b,c

mgGDS�1

5–10cm

Depth,Forest

Control

Before

44.36

(0.63)

0.47

(0.09)

0.54

(0.12)

0.48

(0.24)

2.90

(0.46)

NH4+

44.83

(0.99)

0.91

(1.42)

0.65

(0.12)

10.96

(10.72)

2.87

(0.07)

NH4++PO4�3

45.94

(0.88)

1.27

(0.54)

1.28

(0.56)

0.64

(0.44)

4.11

(0.52)

NO3�

43.69

(0.88)

0.58

(0.16)

0.59

(0.17)

0.06

(0.06)

2.31

(0.31)

NO3�+PO4�3

45.85

(2.29)

0.21

(0.38)

0.23

(0.35)

0.37

(0.19)

2.83

(0.16)

PO4�3

45.89

(0.44)

0.47

(0.15)

0.52

(0.17)

0.33

(0.16)

3.21

(0.45)

CONTROL

1day

after

45.85

(1.14)

0.87

(0.19)

0.96

(0.27)

0.59

(0.59)

3.52

(0.96)

NH4+

45.94

(1.31)

0.67

(0.29)

1.83

(0.17)

8.15

(2.61)

4.79

(0.60)

NH4++PO4�3

47.72

(1.32)

1.27

(0.27)

1.50

(0.08)

16.19

(13.81)

3.24

(1.28)

NO3�

46.74

(0.64)

0.81

(0.19)

0.92

(0.23)

0.78

(0.47)

14.98

(6.28)

NO3�+PO4�3

44.39

(0.69)

0.66

(0.18)

0.68

(0.19)

0.12

(0.12)

10.14

(4.02)

PO4�3

47.76

(2.17)

0.64

(0.08)

0.67

(0.11)

0.19

(0.19)

1.98

(0.51)

CONTROL

7daysafter

40.05

(1.82)

0.55

(0.10)

0.61

(0.07)

0.36

(0.36)

2.94

(0.70)

NH4+

44.37

(2.90)

1.29

(0.21)

1.43

(0.29)

0.96

(0.55)

6.78

(1.77)

NH4++PO4�3

45.16

(1.21)

0.21

(0.95)

0.82

(0.84)

4.22

(2.11)

6.60

(2.51)

NO3�

46.79

(1.11)

0.78

(0.43)

0.80

(0.42)

0.14

(0.14)

6.92

(2.93)

NO3�+PO4�3

37.13

(3.34)

0.77

(0.32)

0.83

(0.30)

0.43

(0.43)

4.53

(0.65)

PO4�3

45.74

(2.18)

1.56

(1.06)

1.62

(1.09)

0.39

(0.22)

3.13

(0.87)

Control

14daysafter

45.02

(0.55)

0.93

(0.03)

0.93

(0.03)

0.00

(0.00)

2.62

(0.77)

NH4+

45.36

(1.88)

1.41

(0.74)

1.41

(0.74)

0.00

(0.00)

4.90

(0.89)

NH4++PO4�3

44.94

(1.65)

1.17

(0.32)

1.28

(0.42)

0.77

(0.77)

3.71

(0.59)

NO3�

46.42

(1.13)

0.50

(0.06)

0.50

(0.06)

0.00

(0.00)

2.94

(0.08)

NO3�+PO4�3

44.16

(0.14)

0.58

(0.06)

0.58

(0.06)

0.00

(0.00)

2.44

(0.43)

PO4�3

46.36

(2.18)

1.06

(0.49)

1.06

(0.49)

0.00

(0.00)

2.81

(1.21)

Control

6monthsafter

29.96

(0.48)

1.20

(0.22)

1.21

(0.19)

1.29

(0.21)

7.39

(1.23)

NH4+

24.79

(5.33)

1.26

(0.30)

1.30

(0.33)

1.56

(1.27)

7.96

(3.13)

NH4++PO4�3

28.02

(1.08)

1.31

(0.08)

1.36

(0.08)

1.92

(0.21)

4.71

(0.93)

NO3�

30.96

(0.82)

1.46

(0.28)

1.49

(0.28)

0.92

(0.18)

3.93

(0.48)

NO3�+PO4�3

28.10

(0.92)

1.38

(0.42)

1.48

(0.44)

4.62

(1.44)

5.06

(0.99)

PO4�3

32.18

(2.43)

1.06

(0.25)

1.24

(0.15)

7.08

(5.26)

5.90

(1.34)

Control

13monthsafter

43.37

(0.21)

0.37

(0.09)

0.27

(0.08)

0.48

(0.24)

3.91

(0.71)

NH4+

43.31

(0.45)

0.80

(0.11)

0.83

(0.39)

1.43

(1.19)

4.38

(1.50)

NH4++PO4�3

48.32

(2.47)

0.62

(0.16)

0.49

(0.08)

0.25

(0.16)

3.72

(0.54)

NO3�

46.23

(1.61)

0.52

(0.27)

0.39

(0.19)

0.30

(0.03)

3.46

(0.44)

NO3�+PO4�3

43.75

(0.81)

0.74

(0.08)

0.62

(0.12)

0.91

(0.06)

3.98

(0.43)

PO4�3

46.63

(0.77)

0.71

(0.32)

0.86

(0.23)

2.46

(1.72)

5.77

(1.62)

Table

1.(continued)


Treatment

Fertilization

Tim

eWater-Filled

Pore

Space,

%N

Mineralization

Rate,

mgGDS�1d�1

Nitrification

Rate,

mgGDS�1d�1

NH4+Pool,

mgGDS�1

NO3�Pool,

mgGDS�1

Resin

P,b,c

mgGDS�1

5–10cm

Depth,Pasture

Control

Before

57.40

(1.64)

0.08

(0.06)

0.04

(0.06)

1.04

(0.30)

0.89

(0.15)

NH4+

54.41

(1.29)

0.15

(0.14)

0.02

(0.07)

1.28

(0.54)

1.07

(0.24)

NH4++PO4�3

57.23

(1.82)

0.03

(0.15)

0.03

(0.02)

2.52

(0.86)

1.03

(0.09)

NO3�

58.15

(1.45)

0.22

(0.05)

0.04

(0.02)

1.47

(0.13)

1.12

(0.24)

NO3�+PO4�3

53.20

(0.73)

0.29

(0.15)

0.02

(0.04)

1.95

(0.96)

0.99

(0.18)

PO4�3

56.61

(1.69)

0.15

(0.05)

0.00

(0.05)

1.08

(0.18)

0.90

(0.31)

Control

1day

after

56.70

(1.42)

0.28

(0.04)

0.04

(0.03)

2.27

(0.39)

0.39

(0.10)

NH4+

53.54

(1.63)

0.35

(0.02)

0.07

(0.04)

2.95

(0.34)

0.31

(0.21)

NH4++PO4�3

55.58

(1.20)

0.37

(0.13)

0.03

(0.02)

2.81

(0.93)

0.30

(0.07)

NO3�

56.32

(1.56)

0.21

(0.12)

0.01

(0.02)

2.29

(0.09)

0.55

(0.05)

NO3�+PO4�3

55.22

(1.36)

0.53

(0.15)

0.03

(0.04)

3.50

(1.00)

0.76

(0.14)

PO4�3

53.59

(2.28)

0.08

(0.29)

0.05

(0.01)

1.71

(0.18)

0.54

(0.09)

Control

7daysafter

53.79

(2.43)

0.45

(0.12)

0.01

(0.06)

3.23

(1.23)

0.57

(0.08)

NH4+

58.64

(7.17)

0.54

(0.21)

0.01

(0.01)

3.67

(1.46)

0.73

(0.24)

NH4++PO4�3

51.53

(1.72)

0.10

(0.04)

0.06

(0.03)

1.10

(0.24)

0.34

(0.17)

NO3�

50.93

(1.27)

0.18

(0.08)

0.00

(0.03)

1.23

(0.72)

0.36

(0.18)

NO3�+PO4�3

51.85

(2.65)

0.53

(0.34)

0.03

(0.04)

4.46

(3.18)

0.35

(0.04)

PO4�3

57.78

(2.33)

0.53

(0.12)

0.03

(0.02)

3.49

(0.95)

0.67

(0.12)

Control

14daysafter

54.73

(3.73)

0.14

(0.14)

0.01

(0.01)

1.08

(0.88)

0.36

(0.05)

NH4+

56.26

(4.15)

0.16

(0.14)

0.00

(0.02)

1.10

(0.83)

0.58

(0.21)

NH4++PO4�3

40.16

(15.9)

0.04

(0.06)

0.00

(0.03)

0.30

(0.30)

0.41

(0.16)

NO3�+PO4�3

53.61

(1.86)

0.11

(0.23)

0.00

(0.02)

0.69

(0.49)

0.36

(0.09)

PO4�3

56.01

(1.82)

0.08

(0.09)

0.02

(0.02)

0.75

(0.69)

0.32

(0.16)

Control

6monthsafter

37.57

(0.45)

0.11

(0.06)

0.16

(0.05)

4.44

(1.57)

0.25

(0.13)

NH4+

36.79

(1.30)

0.27

(0.14)

0.09

(0.04)

2.74

(0.78)

0.09

(0.09)

NH4++PO4�3

35.62

(1.30)

0.03

(0.02)

0.03

(0.02)

2.94

(1.09)

0.26

(0.20)

NO3�

35.19

(0.22)

0.03

(0.07)

0.07

(0.08)

2.29

(0.36)

0.39

(0.20)

NO3�+PO4�3

37.13

(1.60)

0.06

(0.05)

0.06

(0.04)

2.54

(0.84)

0.16

(0.09)

PO4�3

36.51

(0.39)

0.06

(0.06)

0.11

(0.05)

4.13

(1.29)

0.21

(0.19)

Control

13monthsafter

55.91

(2.43)

0.12

(0.17)

0.02

(0.07)

2.41

(0.65)

0.73

(0.13)

NH4+

67.47

(12.20)

0.07

(0.19)

0.01

(0.08)

2.38

(0.36)

1.10

(0.42)

NH4++PO4�3

54.90

(1.79)

0.36

(0.28)

0.02

(0.10)

2.27

(0.45)

0.94

(0.21)

NO3�

54.60

(3.10)

0.69

(0.45)

0.05

(0.13)

6.96

(4.18)

1.34

(0.39)

NO3�+PO4�3

53.04

(4.15)

0.46

(0.64)

0.53

(0.64)

2.40

(0.86)

1.07

(0.22)

PO4�3

37.80

(19.00)

0.01

(0.68)

0.48

(0.50)

4.56

(1.49)

1.21

(0.65)

aDataarepresentedas

means(n

=3),andstandarderrors

arein

parentheses.GDSisgramsdry

soil.

bResin

Ppoolsweremeasuredonly

at0–5cm

depth.

cND

isnotdetermined.

Table

1.(continued)


3.6. Trace Gas Fluxes After Fertilization: Forest

[29] In the forest, the short-term NO emissions increased in theN-fertilized plots during the first 14 days compared with thecontrols (Figure 2). Nitric oxide emissions were significantlygreater (p = 0.05) in the NH4

+ and NH4+ + PO4

�3 amended plots,increasing by 4 to 9 times that of the controls. Nitric oxide releasescontinued to be greater in the N amended plots 6 months afterfertilization. Thirteen months after fertilization, NO emissions werethe same as the controls.[30] The short-term releases of N2O showed a bimodal response

with an increase in the NH4+ + PO4

�3 amended plots 1 day afterfertilization, while the N2O emissions from the other treatmentswere similar to the controls (Figure 2). A second smaller N2O peakwas measured on day 14 in the NO3

�, NH4+ + PO4

�3, and PO4�3

amended plots. This smaller N2O peak was coincident with a neardoubling in the NH4

+ pools in these treatments (Table 1), suggest-ing fertilization had enhanced organic matter decomposition andincreased NH4

+ pools. Emissions were very low during the dryseason (6 months) with a small amount of uptake measured in anumber of the treated plots. Thirteen months after fertilization,there were no differences in N2O releases in the fertilized plotscompared with the controls.[31] Carbon dioxide releases were variable and did not show

a clear response to fertilization except in the NH4+ + PO4

�3

amended plots, where a small increase was measured 7 daysafter fertilization (Figure 2). There was no difference in the CO2

emissions compared with the controls at 6 and 13 months afterfertilization.

3.7. Trace Gas Fluxes After Fertilization: Pasture

[32] In the pasture, plots fertilized with NH4+ + PO4

�3 andNO3

� + PO4�3 showed the greatest NO emissions 1 day after

fertilization, while those amended with NH4+ and NO3

� showedthe greatest NO emissions at 7 days postfertilization (Figure 3).Nitric oxide releases during the first 7 days were about twice thecontrol plots. A small increase in NO emission was measured in theNO3

� treatment 6 months after fertilization, but there were nodifferences after 13 months.

[33] Nitrous oxide emissions showed a dramatic increase 1 dayafter fertilization with NO3

� or NO3� + PO4

�3 (Figure 3). Thisincrease was more than 18 times greater than the emissions fromthe control plots (p = 0.005). However, at 6 and 13 months afterfertilization, there were no differences in the N2O emissions fromany of the N and/or P fertilized plots.[34] Similar to the forest, CO2 emissions from the pasture did

not show a clear response to fertilization (Figure 3). The largestincrease in CO2 emitted was measured from the NO3

� amendedplots 7 days postfertilization. There were no differences in the CO2

emissions compared with the controls at 6 and 13 months post-fertilization.

4. Discussion

4.1. Pretreatment Trace Gas Fluxes

[35] Our pretreatment N oxide emissions are consistent with alimited number of measurements from wet tropical forests andpastures [Luizao et al., 1989; Keller et al., 1993; Coolman, 1994;Keller and Reiners, 1994; Veldkamp et al., 1999; Verchot et al.,1999; Breuer et al., 2000; Davidson et al., 2000; Erickson et al.,2001; Garcia-Montiel et al., 2001; Melillo et al., 2001]. A numberof these studies have shown that forest NO and N2O emissionswere greater than from older pastures. Reduced N oxide emissionsfrom the pasture soils are the result of differences in the N cycles ofthe two ecosystems. Larger emissions of NO and N2O from theforest soils are associated with higher rates of net N mineralizationand net nitrification than in the pasture soils [Neill et al., 1995,1997; Verchot et al., 1999; Garcia-Montiel et al., 2001; Melilloet al., 2001].

4.2. Forest and Pasture Responses to Fertilization

[36] Our results suggest there are different controls on NO andN2O emissions from tropical forests compared with other studiesthat have measured the response of nitrogen oxide emissions to Nand/or P amendments [Kaplan et al., 1988; Keller et al., 1988;Bakwin et al., 1990; Parsons et al., 1993; Serca et al., 1994;Parsons and Keller, 1995; Hall and Matson, 1999]. Our study

Figure 1. Pretreatment mean (n = 18) emissions of NO, N2O, and CO2 from the forest and pasture sites. Error barsrepresent ±1 standard error. Symbols a and b indicate significant differences (t test, p � 0.05) between the forest andpasture means by gas.


suggests that nitrification was the dominant process for NOproduction in the forest soil because the largest enhancements inNO emissions were from the NH4

+ treatments. This is in contrast tothe results of Kaplan et al. [1988], who, in the forest ReservaDucke in Amazonas, Brazil, measured a threefold to fourfoldincrease in NO emissions from NO3

� fertilized sites comparedwith untreated controls. Bakwin et al. [1990], in the same forest,also found that fertilization with NO3

� enhanced NO emissions byfivefold to 150-fold, while NH4

+ treated plots produced on averagevery little increase. From the NO response to the different forms ofN fertilizer both of these studies suggested that denitrification was

primarily responsible for NO production. However, our results areconsistent with two more-recent studies [Serca et al., 1994;Parsons and Keller, 1995] that suggested the NO emission fromthese studied soils seem to be derived from nitrification.[37] We measured only a doubling of N2O emissions from the

forest with N additions compared with the controls. Our resultscontrast other studies that have measured up to 20-fold increaseafter fertilization [Keller et al., 1988]. These investigators proposedthat microbial reduction of NO3

� was the major process forproduction of N2O. Hall and Matson [1999] investigated theresponse of N oxide gas emissions to N fertilization of N- and

Figure 2. Forest fluxes of NO, N2O, and CO2 by treatment over the 13 months fertilization period. Data arepresented as mean (n = 3) and error bars represent ±1 standard error.


P-limited tropical forests in Hawaii and found variable responsesthat were related to whether the forest was N or P limited. In anN-limited forest, N additions did not markedly enhance N2Oemissions. There are several possible explanations for our results.First, plants may have been better competitors for NH4

+ and NO3�.

Second, we added a small amount of N (3.33 g N m2 perfertilization) compared with other studies. Third, the range ofWFPS of 37 to 46% we measured was well below the optimumof 60–70% WFPS for maximal denitrification [Davidson, 1991,1993; Garcia-Montiel et al., 2001]. In fact, the low soil moisturesmeasured in the forest were conducive for increased releases of NOfrom nitrification, and this is what we observed.

[38] Tropical agricultural systems such as sugar cane, corn,banana, wheat, papaya, and balsa tree plantations have shownenhanced emissions of N oxide gases with N fertilization [David-son et al., 1996; Matson et al., 1996; Veldkamp and Keller, 1997;Matson et al., 1998; Veldkamp et al., 1998; Veldkamp et al., 1999;Weitz et al., 1999; Crill et al., 2000]. However, results fromN-fertilized tropical pastures are sparse [Parsons et al., 1993;Parsons and Keller, 1995; Veldkamp et al., 1998]. The resultsfrom all the above studies were conducted on fertile volcanicallyderived andic soils with high organic matter content. The exper-imental sites at Nova Vida are on less fertile, more weathered soils.Our observations of little change in NO emissions and large

Figure 3. Pasture fluxes of NO, N2O, and CO2 by treatment over the 13 months fertilization period. Data arepresented as mean (n = 3) and error bars represent ±1 standard error.


increases N2O emissions from the pasture following fertilizationwere consistent with those of Parsons et al. [1993] and Parsonsand Keller [1995]. We also found, similar to Parsons et al. [1993]and Parsons and Keller [1995], that NO3

� or NO3� + PO4

�3

elicited the greatest N2O response. This indicates that denitrifica-tion was the most important process regulating N2O production.Soil moisture in the pasture surface soils were approximately 74%WFPS, which is near optimum for denitrification [Davidson, 1991,1993]. Our results contrast those of Veldkamp et al. [1998], whofound that the form of N applied did not affect the magnitude of theN2O or NO emissions.

4.3. Controls on N Gas Emissions

[39] We found that the controls on NO and N2O emissions inforest and pasture were very different. This difference appears to bea function of the differences in both the rates of N cycling and therange of soil moistures that occur in these different land covers.Forest soils have higher rates of net N mineralization and netnitrification than the pasture. This rate of N cycling determines anupper boundary for the amount of N oxide gas that can be lost fromeach ecosystem under optimal conditions [Davidson, 1991]. Fur-ther, the percentages of WFPS we measured in the forest andpasture lie on different ends of the range of soil moisture that istypically associated with nitrification and denitrification [David-son, 1991]. The optimal rate of nitrification and production of NOoccur in drier soils within a range of 20–50% WFPS, while themaximal rate of denitrification and production of N2O occur atabout 60% WFPS. Low soil moisture, related to the sandy soiltexture and high rates of evapotranspiration in the forest, favorsnitrification resulting in nearly equal NO and N2O emissions. Thatnitrification is the process controlling the releases of these gases isfurther supported by the increased emissions of NO and N2O withNH4

+ fertilization.[40] The pasture, however, has a more compacted surface soil

layer and lower rates of evapotranspiration, which lead to highersoil moisture and favors denitrification and greater N2O over NOemissions. That denitrification is the process controlling thereleases of these gases is supported by the large increase in N2Oemissions with addition of NO3

� fertilizer.[41] Veldkamp et al. [1998] concluded that environmental

factors, in particular percent WFPS, were the major controllersof nitrogen oxide gas emissions from pastures. Our resultssuggest that nitrogen form and quantity are more importantparameters than WFPS in controlling NO and N2O emissionsfrom tropical pastures. This interpretation is supported by thework of Garcia-Montiel et al. [2001], who studied the seasonalpatterns of NO and N2O fluxes from the same forest and pasturechronosequence and also found that soil N availability was theprimary controller and percent WFPS was the secondary con-troller of N oxide fluxes.

4.4. Estimates of N Yields

[42] We estimated N yields by interpolation of the N gas ratesfrom the fertilized plots minus the controls over the appropriatetime intervals. We found that in the forest, more of the N appliedwas lost as NO than N2O. We estimated that NO-N emissionsaccounted for 0.47, 1.05, and 1.43% of the N applied from NO3

� +PO4

�3, NH4+, and NH4

+ + PO4�3 treatments, respectively. We

found that between 0.06 and 0.20% of the N applied as NO3� and

0.18% of the N applied as NH4+ was lost from the forest as N2O-N

over 2 weeks postapplication. Total nitrogen oxide losses werefrom 0.20 to 1.62% of the N applied, depending on the N form ofthe fertilizer used. Our results were are similar to those of Kelleret al. [1988], who calculated for Amazonian forest that 0.50% ofthe NO3

�-N or 0.1% NH4+-N was lost as N2O-N within two weeks

after application. Hall and Matson [1999] observed that only 0.6%

of the NH4NO3 fertilizer applied was lost as N2O + NO after 7 daysfrom an N-limited tropical forest in Hawaii.[43] In contrast to the forest, more N was lost as N2O from the

pasture, and the maximum total N gas loss was greater than fromthe forest. Approximately 0.03 to 0.05% of the NH4

+-N and 0.03 to0.02% of the NO3

�-N applied to the pasture was released as NO-Nover the first 14 days of the experiment. We estimated thatapproximately 0.40% of the NO3

� -N applied to the pasture wasreleased as N2O-N in the first day following fertilization, and anaverage of 2.75% was lost over the 2 weeks. Total nitrogen oxidelosses were from 0.04 to 2.82% of the N applied, depending on theN form of the fertilizer used. Our estimates of the amounts offertilizer N lost may be conservative because we did not measurethe emissions within in the first few hours after the rain washed thefertilizer into the soil.[44] Nitrogen fertilization of a tropical pasture in Costa Rica

increased annual NO emissions by more than 5 times and N2Oemissions by nearly 10 times [Veldkamp et al., 1998]. These annuallosses from a fertilized pasture constituted 1.3 and 6.8% of the300 kg N ha�1 applied as NO-N and N2O-N, respectively. Thisstudy measured even greater short-term N fertilizer losses than weobserved. Losses were up to 4.6% for NO-N and 28% for N2O-Nwhen environmental conditions were optimal. These yields may behigh because of the large amount of N applied (300 kg N ha�1 yr�1)and the frequency (every 23 days) of the amendments.

5. Summary

[45] We find that nitrogen form and quantity as well as environ-mental factors including percent WFPS are important parameterscontrolling NO and N2O emissions from tropical forests andpastures. We also conclude that deforestation for pasture, thedominant change in land cover in the Amazon, changes not onlythe form of N gas emission but also the processes that control theiremissions from soil. Understanding the role of these controls willbe important for predicting the consequences of future pasturemanagement and land use conversion in the region.[46] In the context of Rondonia and other regions in the Amazon

Basin, pasture management practices are changing to includeincreased use of fertilizer [Nepstad et al., 1991], particularly inolder pastures that have lower NO and N2O emissions than theoriginal intact forests. This may lead to large short-term releases ofN2O. Moreover, there is recent evidence of a trend in Rondonia toconvert pastures to fertilized row-crop agriculture such as corn orsoybean production. If this is done at a large scale, we can expectincreases in NO and N2O fluxes from the region.

[47] Acknowledgments. This research was supported by the NASATerrestrial Ecology Program grant NAG5-3859. We thank Joao Arantes Jr.for his generosity in allowing us to work at Fazenda Nova Vida and JoseCardozo for providing logistical assistance. We thank Sandra Nicoletti,Kathy Newkirk, Chris Catricala, and Keri Holland for their assistance.

ReferencesBakwin, P. S., S. C. Wofsy, S.-M. Fan, M. Keller, S. E. Trumbore, andJ. M. da Costa, Emission of nitric oxide (NO) from tropical forest soilsand exchange of NO between the forest canopy and atmosphericboundary layers, J. Geophys. Res., 95, 16,755–16,764, 1990.

Bastos, T. X., and T. D. de A. S. Diniz, Avaliacao do clima do Estado deRondonia para desenvolvimento agrıcola, Boletim Pesqui. 44, EmpresaBras. de Pesqui. Agropecuaria-Cent. de Pesqui. Agroflor. da AmazoniaOriental, Belem, Brazil, 1982.

Bowden, R. D., P. A. Steudler, J. M. Melillo, and J. D. Aber, Annual nitrousoxide fluxes from temperate forest soils in the northeastern United States,J. Geophys. Res., 95, 13,997–14,005, 1990.

Breuer, L., H. Papen, and K. Butterbach-Bahl, N2O emissions from tropicalforest soils of Australia, J. Geophys. Res., 105, 26,353–26,367, 2000.

Cole, V., et al., Agricultural options for mitigation of greenhouse gas emis-


sions, in Climate Change 1995, Impacts, Adaptations and Mitigation ofClimate Change: Scientific-Technical Analyses, edited by R. T. Watson,M. C. Zinyowera, and R. H. Moss, pp. 745–771, Cambridge Univ.Press, New York, 1996.

Coolman, R. M., Nitrous oxide emissions from Amazonian ecosystems,Ph.D dissertation, N. C. State Univ., Raleigh, 1994.

Crill, P. M., M. Keller, A. M. Weitz, W. T. Grauel, and E. Veldkamp,Intensive field measurements of nitrous oxide emissions from tropicalagricultural soils, Global Biogeochem. Cycles, 14, 85–95, 2000.

Davidson, E. A., Fluxes of nitrous oxide and nitric oxide from terrestrialecosystems, in Microbial Production and Consumption of GreenhouseGases: Methane, Nitrogen Oxides, and Halomethanes, edited by J. E.Rogers and W. B. Whitman, pp. 219–235, Am. Soc. for Microbiol.,Washington, D. C., 1991.

Davidson, E. A., Soil water content and the ratio of nitrous oxide to nitricoxide emitted from soil, in Biogeochemistry of Global Change: Radia-tively Active Gases, edited by R.S. Oremland, pp. 369–386, Chapmanand Hall, New York, 1993.

Davidson, E. A., and W. Kingerlee, A global inventory of nitric oxideemissions from soils, Nutrient Cycl. Agroecosyst., 48, 37–50, 1997.

Davidson, E. A., P. M. Vitousek, P. A. Matson, R. Riley, G. Garcia-Mendez,and J. M. Maass, Soil emissions of nitric oxide in a seasonally drytropical forest of Mexico, J. Geophys. Res., 96, 15,439–15,445, 1991.

Davidson, E. A., P. A. Matson, and P. D. Brooks, Nitrous oxide emissionscontrols and inorganic nitrogen dynamics in fertilized tropical agriculturalsoils, Soil Sci. Soc, Am. J., 60, 1145–1152, 1996.

Davidson, E. A., M. Keller, H. E. Erickson, L. V. Verchot, and E. Veld-kamp, Testing a conceptual model of soil emissions of nitrous and nitricoxides, Bioscience, 50, 667–680, 2000.

Eichner, M. J., Nitrous oxide emissions from fertilized soils: Summary ofavailable data, J. Environ. Qual., 19, 272–280, 1990.

Erickson, H. E., M. Keller, and E. A. Davidson, Nitrogen oxide fluxes andnutrient cycling during post-agricultural succession and forest fertiliza-tion in the humid tropics, Ecosystems, 4, 67–84, 2001.

Galloway, J. N., W. H. Schlesinger, H. L. Levy II, A. Michaels, and J. L.Schnoor, Nitrogen fixation: Anthropogenic enhancement-environmentalresponse, Global Biogeochem. Cycles, 9(2), 235–252, 1995.

Garcia-Montiel, D. C., P. A Steudler, C. Neill, J. M. Melillo, M. C. Piccolo,and C. C. Cerri, Controls on soil nitrogen oxide emissions from forest andpastures in the Brazilian Amazon, Global Biogeochem. Cycles, 15(4),1021–1030, 2001.

Hall, S. J., and P. A. Matson, Nitrogen oxide emissions after nitrogenadditions in tropical forests, Nature, 400, 152–155, 1999.

Instituto Nacional de Pesquisas Espaciais, Desflorestamento Amazonia1995–1997, report, Sao Jose dos Campos, Sao Paulo, Brazil, 1999.

Instituto Nacional de Pesquisas Espaciais, Monitoramento da Floresta Ama-zonia Brasileira por Satelite 1999–2000, report, Sao Jose dos Campos,Sao Paulo, Brazil, 2000. (Available at http://www.inpe.br/Informacoes_Eventos/amz1999_2000/Prodes/index.htm)

Kaplan, W. A., S. C. Wofsy, M. Keller, and J. Maria Da Costa, Emission ofNO and deposition of O3 in a tropical forest, J. Geophys. Res., 93, 1389–1395, 1988.

Keller, M., and W. A. Reiners, Soil-atmosphere exchange of nitrous oxide,nitric oxide, and methane under secondary succession of pasture to forestin the Atlantic lowlands of Costa Rica, Global Biogeochem. Cycles, 8,399–409, 1994.

Keller, M., W. A. Kaplan, S. C. Wofsy, and J. Maria Da Costa, Emissions ofN2O from tropical forest soils: Response to fertilization with NH4

+, NO3�

and PO4�3, J. Geophys. Res., 93, 1600–1604, 1988.

Keller, M., E. Veldkamp, A. M. Weitz, and W. A. Reiners, Effect of pastureage on soil trace-gas emissions form a deforested area of Costa Rica,Nature, 365, 244–246, 1993.

Kroeze, C., A. Mosier, and L. Bouwman, Closing the global N2O budget: Aretrospective analysis 1500–1994, Global Biogeochem. Cycles, 13, 1–8,1999.

Luizao, F. P., P. Matson, G. Livingston, R. Luizao, and P. Vitousek, Nitrousoxide flux following tropical land clearing, Global Biogeochem. Cycles,3, 281–285, 1989.

Matson, P. A., C. Billow, S. Hall, and J. Zachariessen, Fertilization practicesand soil variations control nitrogen oxide emissions from tropical sugarcane, J. Geophys. Res., 100, 25,913–25,922, 1996.

Matson, P. A., R. Naylor, and I. Ortz-Monasterio, Integration of environ-mental, agronomic, and economic aspects of fertilizer management,Science, 280, 112–115, 1998.

Matson, P. A., W. H. McDowell, A. R. Townsend, and P. M. Vitousek, Theglobalization of N deposition: Ecosystem consequences in tropical envir-onments, Biogeochemistry, 46, 67–83, 1999.

Melillo, J. M., P. A. Steudler, B. J. Feigl, C. Neill, D. Garcia-Montiel, M. C.

Piccolo, C. C. Cerri, and H. Tian, Nitrous oxide emissions from forestand pastures of various ages in the Brazilian Amazon, J. Geophys. Res.,106(D24), 34,179–34,188, 2001.

Mosier, A., C. Kroeze, C. Nevison, O. Oenema, S. Seitzinger, and O. VanCleemput, Closing the global atmospheric N2O budget: Nitrous oxideemissions through the agricultural nitrogen cycle, Nutrient CyclingAgroecosyst., 52, 225–248, 1998.

Murphy, J., and J. P. Riley, A modified single solution method for thedetermination of phosphate in natural waters, Anal. Chim. Acta, 27,31–36, 1962.

Neill, C., M. C. Piccolo, P. A. Steudler, J. M. Melillo, B. Feigl, and C. C.Cerri, Nitrogen dynamics in soils of forests and active pastures in thewestern Brazilian Amazon Basin, Soil Biol. Biochem., 27, 1167–1175,1995.

Neill, C., M. C. Piccolo, C. C. Cerri, P. A. Steudler, J. M. Melillo, andM. Brito, Net nitrogen mineralization and net nitrification rates insoils following deforestation for pasture across the southwestern Brazi-lian Amazon Basin Landscape, Oecologia, 110, 243–252, 1997.

Nepstad, D. C., C. Uhl, and E. A. S. Serrao, Recuperation of a degradedAmazon landscape: Forest recovery and agricultural restoration, Ambio,20, 248–255, 1991.

Parsons, W. F. J., and M. Keller, Controls on nitric oxide emissions fromtropical pasture and rain forest soils, Biol. Fertil. Soils, 20, 151–156,1995.

Parsons, W. F. J., M. E. Mitre, M. Keller, and W. A. Reiners, Nitratelimitation of N2O production and denitrification from tropical pastureand rain forest soils, Biogeochemistry, 22, 179–193, 1993.

Prather, M., R. Derwent, D. Ehhalt, P. Fraser, E. Sanhueza, and X. Zhou,Other trace gases and atmospheric chemistry, in Climate Change 1994:Radiative Forcing of Climate Change and an Evaluation of the IPCCIS92 Emission Scenarios, edited by J. T. Houghton et al., pp. 77–126,Cambridge Univ. Press, New York, 1995.

Serca, D., R. Delmas, C. Jambert, and L. Labrouse, Emissions of nitrogenoxides from the equatorial rain forest in central Africa: Origin and reg-ulation of NO emissions from soils, Tellus, Ser. B, 46, 243–254, 1994.

Serrao, E. A., Alternative models for sustainable cattle ranching on alreadydeforested lands in the Amazon, Ann. Acad. Bras. Cienc., 97–104, 1992.

Skole, D. S., and C. Tucker, Tropical deforestation and habitat fragmenta-tion in the Amazon: Satellite data from 1978 to 1988, Science, 260,1904–1910, 1993.

Steudler, P. A., J. M. Melillo,B. J. Feigl, C. Neill, M. C. Piccolo, and C. C.Cerri, Consequence of forest-to-pasture conversion on CH4 fluxes in theBrazilian Amazon Basin, J. Geophys. Res., 101, 18,547–18,554, 1996.

Sundquist, E. T., A. B. Shortlidge, and G. C. Winston, Diurnal variations insoil CO2 fluxes measured by a non-invasive chamber technique at Slee-pers River, Vermont, Eos Trans. AGU, 73, 186, 1992.

Tiessen, H., and J. O. Moir, Characterization of available P by sequentialextraction, in soil sampling and methods of analysis, in Canadian Societyof Soil Science, edited by M. R. Carter, pp. 5–76, Lewis, Boca Raton,Fla., 1993.

Veldkamp, E., and M. Keller, Nitrogen oxide emissions from a bananaplantation in the humid tropics, J. Geophys. Res., 102, 15,889–15,898,1997.

Veldkamp, E., M. Keller, and M. Nunez, Effects of pasture management onN2O and NO emissions from soils in the humid tropics of Costa Rica,Global Biogeochem. Cycles, 12, 71–79, 1998.

Veldkamp, E., E. Davidson, H. Erickson, M. Keller, and A. Weitz, Soilnitrogen cycling and nitrogen oxide emissions along a pasture chronose-quence in the humid tropics of Costa Rica, Soil Biol. Biogeochem., 31,387–394, 1999.

Verchot, L. V., E. A. Davidson, J. H. Cattanio, I. L. Ackerman, H. E.Erickson, and M. Keller, Land use change and biogeochemical controlsof nitrogen oxide emissions from soils in eastern Amazonia, GlobalBiogeochem. Cycles., 13, 31–46, 1999.

Weitz, A. M., M. Keller, E. Linder, and P. M. Crill, Spatial and temporalvariability of nitrogen oxide and methane fluxes from a fertilized treeplantation in Costa Rica, J. Geophys. Res., 104, 30,097–30,107, 1999.

��C. C. Cerri, B. J. Feigl, and M. C. Piccolo, Centro de Energia Nuclear na

Agricultura, Avenida Centenario, 303, CEP 13416000, Piracicaba, SP,Brasil. ([email protected]; [email protected]; [email protected])D. C. Garcia-Montiel, J. M. Melillo, C. Neill, and P. A. Steudler, Marine

Biological Laboratory, The Ecosystems Center, 7 Water Street, WoodsHole, MA 02543-1015, USA. ([email protected]; [email protected];[email protected]; [email protected])


Trace gas responses of tropical forest and pasture soils to N and P fertilization

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