Fluxes of CH4, CO2, NO, and N2O in an improved fallow agroforestry system in eastern Amazonia

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Agriculture, Ecosystems and Environment 126 (2008) 113–121 www.elsevier.com/locate/agee

Fluxes of CH4, CO2, NO, and N2O in an improved fallow agroforestry system in eastern Amazonia Louis V. Verchot a,*, Silvio Brienza Ju´niorb, Valdirene Costa de Oliveira c, James K. Mutegi a, J. Henrique Cattaˆnio c, Eric A. Davidson c a

World Agroforestry Centre (ICRAF), P.O. Box 30677, Nairobi, Kenya Embrapa Amazoˆnia Oriental, Cx. Postal 48, 66095-100 Bele´m, Brazil c Woods Hole Research Center, 149 Woods Hole Road, Falmouth, MA 02540-1644, United States b

Available online 21 March 2008

Abstract The objective of this study was to evaluate the effect of leguminous fallows on methane (CH4), carbon dioxide (CO2), N oxides (N2O and NO) fluxes. We measured CH4, N2O, NO, and CO2 fluxes from improved fallows of Inga edulis and Acacia mangium during two successive fallow periods in an old agricultural frontier on sandy soils in eastern Amazonia. Sampling for the first fallow period was done in 1996 and 1997 while that for the second fallow was done in 1999 and 2000. We observed net CH4 uptake during majority of the sampling campaigns. We did not observe any significant difference in CH4 flux between improved fallows and unimproved fallows (control) during either of the sampling periods (P > 0.05). We observed significantly higher uptake during the dry season relative to wet season, indicating the importance of soil water content and gas transport on CH4 fluxes. For both wet and dry seasons, soil respiration rates (CO2), N2O and NO fluxes were similar for improved fallow plots and the control (P > 0.05). We did not observe any significant seasonality in soil respiration or NO fluxes, but there was a significant difference in N2O flux between seasons (P = 0.0638). Contrary to other studies, our observations suggest that improved fallows using N-fixing trees do not appear to decrease the soil CH4 sink and also do not seem to increase CO2 and N-oxide emission in these sandy Amazonian soils. The result for N oxides is particularly pertinent to greenhouse gas (GHG) accounting methods that assess N2O emissions as a fraction of N fixation. # 2008 Elsevier B.V. All rights reserved. Keywords: Trace gases; Land-use change; N oxides; C cycle; N cycle

1. Introduction It has been suggested that agroforestry could have an important role in the mitigation of the accumulation of greenhouse gases in the atmosphere and setting developing countries on a more climate friendly path to agricultural development (Houghton et al., 1993; Unruh et al., 1993; IPCC, 2000; Verchot et al., 2007). But soil emission of nonCO2 trace gases, particularly N oxides could be a spoiler in this scenario. The proposal of agroforestry as a climate friendly approach for intensification of tropical agriculture is based upon the fact that the integration of trees into * Corresponding author. E-mail address: [email protected] (L.V. Verchot). 0167-8809/$ – see front matter # 2008 Elsevier B.V. All rights reserved. doi:10.1016/j.agee.2008.01.012

agricultural landscapes has a high potential for both soil fertility enhancement and carbon sequestration (IPCC, 2000). Leguminous species are used in many agroforestry systems as an alternative source of N to support crop growth. Soils are important sources and sinks of a number of trace gases that are play a role in the enhanced greenhouse effect, notably CO2, N2O, NO and CH4. There are few data on the effects of using leguminous trees in agroforestry systems on the fluxes of these gases between the soil and the atmosphere. The few data that exist suggest that N-fixing trees sometime enhance N-oxide emission and reduce the CH4 sink. For example, Verchot et al. (2006,2007) suggested that agricultural intensification including plantation of N-fixing trees in a shade coffee system in Sumatra led to increased N2O emissions from soils. However, results across

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sites are inconsistent and some systems do not experience significantly elevated emissions. Palm et al. (2002) conducted a study in Yurimaguas, Peru with a shade coffee system that used N-fixing trees to maintain fertility and found that this system had no higher N2O emissions than a comparable secondary forest site. Emissions from the coffee were much lower those from either low or high input fertilized systems. For CH4, both fertilizer and the N-fixing trees weakened the soil CH4 sink and in the case of high N inputs, the soil became a net source. Of all of these gases, we have perhaps the best mechanistic understanding of the N-oxide fluxes and can best predict the likely impact of increasing soil N availability through N-fixing trees on emissions (Davidson et al., 2000; Davidson and Verchot, 2000). N2O emissions from soils are very much dependent on the quality of the plant litter that is produced and incorporated into the soil (Millar, 2002). Greater emissions have been recorded following incorporation of residues with low C:N ratios, such as those of legumes, than have been recorded after incorporation of material with high C:N ratios, such as cereal straw (Kaiser et al., 1998; Baggs et al., 2000). Baggs et al. (2001) showed that N2O production in a controlled environment experiment is influenced by the polyphenol content the organic materials and by their ability to bind proteins. Emissions following incorporation of high quality Gliricidia sepium leaves were significantly higher than those following incorporation of Calliandra calothyrsus or from Peltophorum dasyrrachis leaves, due to the rapid release of N from the G. sepium leaves. C. calothyrsus and G. sepium had similar C:N ratios, but the polyphenol content of C. calothyrsus was three times higher that that of G. sepium and the protein binding capacity was greater by more than an order of magnitude. Improved fallow systems are the agroforestry systems that make perhaps the most intensive use of N-fixing trees. Improved fallow systems consist of a rotation between crops and tree-legume fallow. A legume tree is established and allowed to grow for a short period, usually between 9 months and 4 years, during which all cropping activities cease. The fallow is cut prior to cultivation and leaf biomass of the fallow is incorporated into the soil. The field is then cropped for 1–4 seasons before the fallow is replanted. In field trials in western Kenya, total N2O emissions over 34 days following incorporation of Sesbania sesban residues (2 kg N2O-N ha1), were higher than emissions following the incorporation of Macroptilium atropurpureum and natural fallow residues. A flux of 7.2 g N2O-N t1 ha1 day1 was measured in the S. sesban treatment on the first day after incorporation. This result was attributed to the rapid release of N from this high quality (high N, low lignin) residue (Baggs et al., 2000). Although the data are sparse, there is an emerging consensus that N-fixing trees affect soil–atmosphere gas exchange and that the magnitude of these fluxes suggest that it is necessary to account for these changes when evaluating the potential of agroforestry systems to contribute to climate

change mitigation. In this study we present data from two sampling efforts at different stages of maturity of an improved fallow system in eastern Amazonia. During the first sampling campaign, which was done during the first fallow cycle and began when trees were 1 year old, we measured CH4 and CO2 fluxes. Measurements were made during the second fallow cycle and expanded to include N2O and NO. Our hypotheses were that growing improved fallows of N-fixing trees would reduce CH4 consumption and enhance CO2 and N-oxide production. The enhanced Noxide production should manifest through high NO emissions during the dry season and high N2O emissions during the wet season.

2. Methods 2.1. Site description This study was conducted on a farm near the town of Igarape Ac¸u (18070 4100 latitude south, and 478470 1500 longitude west) in northern Para´ State of Brazil. Mean annual temperature is 26 8C. Average annual rainfall is around 2500 mm year1, and the season is divided into a wet season between January and May and a dry season between June and December. Less than 10% of the annual rainfall generally falls during the dry season. The soil was classified as an Entisol (Psamment), and was deep and well drained. The surface horizon had a sandy texture (86% sand). Basic soil data are presented in Table 1. Annual rainfall in the region ranges from 2000 to 3000 mm, and mean annual temperature is 26 8C. There is a short, but distinct dry season at this site between July and November, where rainfall of <200 mm month1 is recorded. In 1995, an experiment to test improved fallows with different tree species and different inter-tree spacing was established with a randomized complete block design. Five blocks were established for the experiment, but only four of the blocks were measured in this study, as the fifth block was reserved for more destructive sampling during the course of the experiment. The traditional agricultural system in the region was a slash-and-burn system where maize was grown Table 1 Soil chemical characteristics before the start of the experiment (n = 15) (source: Brienza, 1999) Soil characteristics

Depth (cm) 3

Bulk density (g cm ) pH (soil:water 1:2.5) P (mg kg1) a K (cmolc kg1)a Na (cmolc kg1)a Ca (cmolc kg1)b Al (cmolc kg1)b a b

0–5

5–10

10–20

20–30

30–50

1.3 5.6 7.0 36.8 18.5 2.9 0.1

1.3 5.4 3.8 25.0 16.5 1.5 0.3

1.4 5.2 2.3 20.5 13.5 0.8 0.5

1.4 5.2 1.0 15.5 9.8 0.5 0.8

1.5 5.2 1.0 13.5 8.3 0.3 0.9

Mehlich-1 (HCl + H2SO4). 1 M KCl extraction (Guimara˜es et al., 1970).

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for 2–4 years before the land was abandoned for up to 20 years. In our experiment, maize (cultivar BR 106) was planted in January 1995 at 1.0 m  0.5 m spacing and cassava (cultivar ‘‘olho verde’’) was planted in the same plots in February 1995 at 1 m  1 m spacing. The leguminous trees Acacia angustissima Kuntze, Clitoria racemosa G. Don, Sclerolobium paniculatum Vogel, Inga edulis Mart., and Acacia mangium Willd. were planted after maize harvest (June 1995) and four months after cassava had been planted (February 1995). Trees and cassava grew together for eight months until the cassava was harvested (February 1996). After the last cassava weeding (between October–November 1995) the fallow vegetation started to grow as an enriched fallow. For this study, 1 year of cropping was followed by 2.5 years of fallow (Brienza, 1999). The 1999–2000 sampling began after the last cassava harvest and thus corresponds to the second fallow phase. For this study, only the control plots and plots with A. mangium and I. edulis, were measured. We had two major sampling seasons: one in 1996–1997, which was during the first fallow period; one in 1999–2000, which occurred during the first year of the second fallow phase. In the 1996–1997 sampling, CH4 was measured once during the dry season (November 1996), and twice during the wet season (May and June 1997). One block was lost during the June 1997 sampling due to instrument problems. Sampling for CO2 was done three times during the wet season (May 1996 and May and June 1997) and twice during the dry season (August 1996 and November 1996,). These data were collected as part of different studies, which explains why we have only a few coincident measurements of these gases. However, these data compliment the second sampling period and thus we have chosen to include them here. Total aboveground biomass at the end of the first fallow phase (2.5 years) was 30.3 Mg ha1 for I. edulis, 50.2 Mg ha1 for A. mangium, and 24.0 Mg ha1 for the control (Brienza, 1999). For the 1999–2000 season, sampling was done five times during the wet season (April and December 1999, January, February and March 2000) and twice during the dry season (July and November 2000). Four gasses were measured during this season: CO2, CH4, N2O and NO. Due to instrument failure, data for CO2 and NO were not collected in November and December 1999.

using a Nafion gas sample dryer (Perma Pure Inc., Toms River, NJ). NO and CO2 concentrations were recorded at 5 s intervals over a period of 3–4 min using a data logger. Fluxes were calculated from the rate of increase in concentration using the steepest linear portion of the accumulation curve. N2O and CH4 fluxes were measured with a static chamber technique (Verchot et al., 1999; Matson et al., 1990), using the same chamber bases as those used for the NO and CO2 measurements. In each plot, four chambers were measured per sampling. At the time of measurement, a PVC cover (20cm PVC end-cap) was placed over the base making a chamber with a headspace volume of approximately 5.5 L. Four 20 mL headspace samples were withdrawn at 10-min intervals and returned to the laboratory for analysis with gas chromatographs fitted with an electron capture detector, for N2O, and a flame ionization detector for CH4.

2.2. Gas fluxes

We observed uptake (negative fluxes) of CH4 by the soil for all the treatments during the first fallow period (Fig. 1). The differences in CH4 fluxes between treatments were not significant (P = 0.5719), and although we observed higher CH4 uptake during the dry season in comparison to wet season, this difference was not significant (P = 0.1806). There was also no block effect for CH4 fluxes. During most of the flux measurements after the fallow period, we observed uptake of CH4 by soils in both improved fallow and control plots (Fig. 2). The only positive flux (emission) measured was in the A. mangium plots during the March sampling, which is during the wet season. During the second measurement

NO and CO2 fluxes were measured using a dynamic chamber technique (Verchot et al., 1999; Davidson et al., 2000). In each plot, four chambers were measured per sampling. Air was circulated in a closed loop between a Scintrex LMA-3 NO2 analyzer (Scintrex, Inc., Ontario, Canada), a LiCor 6252 infra-red gas analyzer (LiCor, 6252) and the chamber through Teflon tubing using a battery operated pump, at a rate of 0.5 L min1. Because of problems with humidity wetting the CrO3 catalyst in the NO2 analyzer, we dried the air stream entering the analyzer

2.3. Soil inorganic N Soil inorganic N was determined four times during the rainy season in the latter half of the 1999–2000 sampling period. We collected two soil samples to a depth of 10 cm, per site and per sampling date. Samples were transported on ice to the laboratory where they were refrigerated until extraction. After returning to the lab, all soil samples were thoroughly mixed; coarse roots and coarse organic matter were removed by hand. We determined the inorganic N pool sizes by extracting NO3-N and NH4-N from a 25 g subsamples of field-moist soil with 100 mL of 2 M KCl. The soil–KCl solution was shaken for an hour on an orbital shaker and allowed to settle over night. A 20 mL aliquot of the supernatant was removed and frozen for later analysis. Analysis was done on an Alpkem (Wilsonville, Oregon, USA) autoanalyzer using a modified Griess-Illosvay procedure for determination of NO3-N + NO2-N, which was reported as NO3-N (Bundy and Meisinger, 1994) and a salicylate-hypochlorite procedure for NH4-N (Kemper and Zweers, 1986).

3. Results 3.1. CH4 fluxes

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L.V. Verchot et al. / Agriculture, Ecosystems and Environment 126 (2008) 113–121 Table 2 Seasonal summary of methane fluxes (mg CH4 m2 day1) during the each sampling period Treatment

Dry season

Wet season

Annual total

First sampling Control Inga edulis Acacia mangium

1.13 (0.39) 1.40 (0.35) 0.95 (0.28)

0.77 (0.19) 0.96 (0.29) 0.76 (0.20)

3.36 4.18 3.06

Second sampling Control I. edulis A. mangium

0.78 (0.51) 1.15 (0.42) 1.12 (0.29)

0.45 (0.22) 0.47 (0.26) 0.01 (0.58)

2.36 3.16 2.41

Values are mean (S.E.), negative values indicate uptake.

Fig. 1. CH4 and CO2 fuxes during first sampling period. Shaded areas show dry season. Error bars indicate 1S.E.

period, differences in CH4 flux among treatments were significant (P = 0.0521), as were the differences in CH4 fluxes between the dry and wet seasons (P < 0.0001; Table 2). Uptake was greatest during the dry season in comparison to the wet season. Monthly differences during the wet and dry seasons were however, not significant (Fig. 2). We calculated annual totals by stratifying the year into wet season and dry season and calculating the mean flux for each season. The wet season in this region of the Amazon Basin extends for 5 months (July–November). We calculated a weighted average annual flux and then extrapolated to express the flux in terms of CH4 uptake per hectare for the year (Table 2). We recognize that the estimate for the first

fallow period is only indicative, and less well based than the estimate for the second fallow period. Uptake at this site was not affected by treatment and was in the range of 2.5– 4 kg CH4 ha1 year1. Uptake rates were significantly different between the two fallow phases (P = 0.0069) with higher uptake in the first fallow period (Table 2). 3.2. Soil respiration For the first fallow period where trees were in their second year of growth, soil respiration rates were similar between the I. edulis and A. mangium fallows and the control (P = 0.6401 and 0.9531 for dry and wet season, respectively; Table 3). We did observe significant seasonal respiration differences during the second fallow, but not during the first fallow phase (P = 0.4595 during first sampling and P = 0.0689 during second sampling). During the second fallow period we observed significantly higher respiration rate during the month of January (beginning of rainy season) in comparison to all the other months (ANOVA, P < 0.0001) (Fig. 2). The other months exhibited similar respiration rates for all the treatments (P > 0.05). There was also no significant difference between the different types of fallow species (P = 0.4143). We had few measurements during the dry season for this series of measurements due to problems with the gas analyzer. We used the same approach as for CH4 to calculate an annual flux for each sampling period. We acknowledge that without repetition during the dry season this extrapolation is tenuous, but other gases show small degree of intra-seasonal variability, which suggests that this extrapolation at least provides a reasonable indication of the magnitude of the annual flux. We found a significant difference between soil respiration during the first series of measurements and second fallow (P = 0.0475) with higher respiration rates during the second fallow. This difference was due largely to the higher respiration rate in the A. mangium treatment during the second sampling (P = 0.0789). 3.3. N2O and NO fluxes

Fig. 2. CH4 and CO2 fuxes during second sampling period. Shaded areas show dry season. Error bars indicate 1S.E.

We observed production of N2O and NO in the improved fallows and the control for the two seasons (Fig. 2). We did not observe any significant differences in N2O and NO fluxes

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Table 3 Seasonal summary of soil respiration rate during second fallow period (1999 and 2000) Dry season (g C m2 h1)

Wet season (g C m2 h1)

Annual total (Mg C ha1 year1)

First sampling Control I. edulis A. mangium

0.29 (0.05) 0.25 (0.11) 0.23 (0.04)

0.22 (0.02) 0.23 (0.07) 0.23 (0.05)

22.6 21.0 19.7

Second sampling Control I. edulis A. mangium

0.22 (0.02) 0.21 (0.03) 0.23 (0.03)

0.31 (0.06) 0.33 (0.08) 0.36 (0.05)

22.9 22.7 24.9

Treatment

Values are mean (S.E.).

between either the two types of improved fallow or between any of them and the control (P = 0.8247 and 0.9972 for N2O and NO, respectively). The seasonal comparison for NO (Table 4) is tenuous because several measurements were missed due to instrument problems, but based upon the one measurement in the dry season there does not appear to be a seasonal difference (P = 0.8025). There was a significant seasonal effect for N2O (P = 0.0638). There was more temporal variability in the N2O measurements (Fig. 2) than in the NO measurements. Annual fluxes of N oxides accounted for loss of approximately 2 kg N ha1 with slightly higher loss occurring as NO than as N2O. 3.4. Soil inorganic N In all systems NH4-N dominated the soil inorganic-N pool and only a small portion of the soil inorganic-N pool consisted of NO3-N (Table 5). We did not note any increase in soil inorganic N in the fallow plots (P > 0.05). There was a trend of increasing NO3-N over the course of the rainy season, with significantly higher levels in each treatment observed in March (P < 0.05).

4. Discussion 4.1. CH4 fluxes Annual CH4 uptake observed at these sites in Igarape Ac¸u are consistent with other sites in the Amazon, but were not particularly high compared to coarse texture soils elsewhere in the tropics. Others have shown that soil texture greatly affects CH4 consumption rates because gas-phase transport of O2 and CH4 are the most important factors affecting the net

balance of CH4 production and consumption and soil texture strongly affects diffusivity of gases within soils (Striegl, 1993; Verchot et al., 2000; Del Grosso et al., 2000). Fine texture soils in humid tropical forests consume 1.5–2.0 kg ha1 year1, while medium and coarse texture soils consume >4.0 kg ha1 year1 (Verchot et al., 2000). Verchot et al. (2000) reported uptake rates on clay soils in an eastern Amazonian site of 1.3 and 3.1 kg CH4 ha1 year1 in an active and a degraded pasture, respectively. Table 6 presents a summary of CH4 uptake rates at other tropical agricultural sites, where all observations that identified soil texture indicate that measurements were made on medium texture soils. The values observed on our site are consistent with the expectation that coarse texture soils should have higher uptake rates than medium or fine texture soils. The importance of gas-phase transport within the soil is also revealed by the seasonality of CH4 fluxes, where soil water content affects the seasonality of gas diffusion rates. During the wet season, macropores are largely water filled and diffusion from the atmosphere is slowed, compared to the dry season where macropores are largely unfilled. For both the fallow and after fallow phases, soils were stronger sinks during the dry season than during the wet season. Increased N availability has been shown to reduce the soil CH4 sink (Bedard and Knowles, 1989; Hu¨tsch, 1996; Castro et al., 1994; Steudler et al., 1989). Keller et al. (1990) suggested that a pulse of N availability after deforestation could inhibit the CH4 flux. We expected that a similar phenomenon would be observed in improved fallows using N-fixing trees. However, we observed no significant increase in soil inorganic N pools. We found no significant difference in CH4 fluxes between the control plots and the improved fallow plots in either measurement period. Thus, in these coarse texture soils, improved fallows not appear to alter soil

Table 4 Seasonal summary of N2O and NO (ng N cm2 h1) fluxes from improved fallow plots in the years 1999 and 2000 Treatment

N2O Wet season

Dry season

Annual total

Wet season

Dry season

Annual total

Control I. edulis A. mangium

1.44 (0.57) 1.24 (0.38) 1.51 (0.69)

0.80 (0.30) 0.71 (0.50) 0.87 (0.37)

0.93 0.81 1.00

0.99 (0.57) 1.70 (0.56) 2.03 (0.69)

1.58 (1.31) 1.36 (0.54) 1.33 (0.60)

1.08 1.37 1.52

Values are mean (S.E.).

NO

118

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Table 5 Soil inorganic N content (mg g1) during the second fallow phase Month

December 1999 January 2000 February 2000 March 2000

Control

A. mangium

NO3

NH4

0.04 0.02 0.06 0.11

1.87 1.56 1.23 3.41

(0.03) (0.01) (0.03) (0.10)

+

(0.35) (0.34) (0.27) (0.64)

NO3 0.05 0.08 0.06 0.17

inorganic N availability to such an extent that this affects soil CH4 uptake. 4.2. Soil respiration Soil respiration is a good indicator of belowground carbon allocation (Raich and Nadlehoffer, 1989; Salimon et al., 2004). We expected that carbon inputs to the soil would be greater in the improved fallows than in the control fallow treatment and that the CO2 efflux from the soil would be greater as a result. This expectation was based largely on the observations of higher aboveground biomass in the improved fallows; Brienza (1999) found, a total aboveground biomass of 30.3 Mg ha1 for the I. edulis fallow, 50.2 Mg ha1 for the A. mangium fallow, and 24.0 Mg ha1 for a natural fallow after 2.5 years. However, we did not observe a significant treatment effect overall or in any of the individual measurements. This suggests that belowground C allocation and turnover were similar in the different types of fallows. Soil CO2 efflux is often modeled as a Q10 function of temperature (Davidson et al., 2006), but several authors (Davidson et al., 2000, 2006) have shown that soil water content also plays an important controlling role in tropical soils where there is less inter-seasonal variability in temperature. We saw no consistent significant seasonal effect in either measurement period. During the second fallow measurement, we observed high soil respiration rates early in the rainy season (January measurements >0.5 g C m2 h1) relative to all other monthly measurements. These high rates may have been due to wet-up effects following the dry season, which have been demonstrated to produce pulses of microbial activity and CO2 production (Birch, 1958; Bottner, 1985; Kieft et al., 1987; Davidson et al., 2000; Savage and Davidson, 2003). These pulses are often explained as a response of microbial respiration to the release of organic substrates from microbial cells that died during the dry period.



I. eldulis NH4

(0.02) (0.04) (0.04) (0.04)

1.26 2.60 1.48 1.57

+

(0.32) (0.52) (0.35) (0.54)

NO3

NH4+

0.05 0.02 0.06 0.11

1.32 1.44 1.52 3.61

(0.03) (0.00) (0.02) (0.04)

(0.49) (0.31) (0.43) (0.79)

4.3. N oxides Few data exist of N-oxide emission from tropical agricultural systems, and those that exist are primarily N2O data. However, we do understand the underlying mechanisms that govern N-oxide emissions from soils and we can draw some conclusions from the empirical data that support this mechanistic understanding. Thus, agricultural soils often have higher N-oxide emissions than soils under native vegetation. Increased N availability generally leads to increased N-oxide emission (Firestone and Davidson, 1989; Verchot et al., 1999; Davidson et al., 2000) because this stimulates the microbial processes of nitrification and denitrification, which produce the gas fluxes. Goreau and deMello (1988) showed that N fertilization increased N2O emissions fifteen-fold in cowpeas grown in Amazonia. Crill et al. (2000) found that fertilizer applications of 122 kg N ha1 to maize in Costa Rica increased N2O emissions threefold, from 0.5 to 1.8 kg ha1 per season. Thus, N2O losses amounted to 1.4% of the fertilizer application. Weitz et al. (2001) found similar results in fertilized sites in Costa Rica, where N2O-N losses amounted to between 0.2% and 2.3% of N fertilizer applications in a maize system. Increased N2O fluxes following fertilization have been observed in many other systems, including temperate agriculture, fertilized forests, tree plantations, and grasslands. Fertilization also increases soil NO fluxes. Sanhueza (1997) recorded emissions between 3.3 and 3.7 kg-N ha1 year1 in cereal crops in Venezuela. OrtizMonasterio et al. (1996) found that NO emissions increased from 2.7 to 6.3 kg ha1 year1 following fertilization of an irrigated wheat system in Mexico. Observations in temperate systems reinforce the results of these few tropical studies. We expected an increase in N-oxide emission in the fallow treatments both during the fallows and in the cultivation phase after the fallows because we expected

Table 6 Summary of other studies of soil CH4 uptake in agricultural systems Author

Annual flux (kg CH4 ha1)

Annual rainfall

Soil texture

Delmas et al. (1991) MacDonald et al. (1998) Palm et al. (2002) Palm et al. (2002) Delmas et al. (1991) Palm et al. (2002)

1.3 1.5 2.8 1.5 1.0 2.1

1200 1513 2200 2200 1362 2200

– Medium Medium Medium – Medium

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between fallows and the control determined in a laboratory assay (P = 0.4475). Net nitrification rates were also measured during the first fallow phase and they were low in a laboratory assay (0.05–0.50 mgN g-soil1 day1), but slightly higher in control plots (P = 0.0142). Net mineralization and net nitrification data were not available for the second fallow phase. These data suggest that the fallows did not increase N availability in these soils and that the N economy of these soils was largely based on NH4+ rather than NO3. Therefore N fallows using N-fixing trees in this situation are unlikely to increase N emissions to the atmosphere. At the second level of control in the conceptual model, soil water content regulates the proportion of the gaseous products that is emitted from the soil. When the soil is wet, the more reduced gas, N2O, is produced in greater quantity than the more oxidized gas, NO. When the soil is dry, the situation is reversed. In our observations we found a significant seasonal effect on the ratio of N2O to NO (P = 0.0277; Fig. 3).

5. Conclusion

Fig. 3. Total N-oxide emissions from soils in the different treatments and the overall seasonal ratios of N2O to NO. Error bars indicate 1S.E.

increased N inputs into the soil organic-N pool, but we found no increases. While determining the factors that govern the fluxes of N oxides in tropical agricultural systems is beyond the scope of this study, we can use the framework of the hole-in-the-pipe model to understand the spatial and temporal variation of the N-oxide fluxes (Firestone and Davidson, 1989). This model posits two levels of control of N-oxide emission from the soil. The first level is the availability of N in the soil, which controls the total N-oxide flux. In our experiment, we expected that the plots with N-fixing trees would have greater N availability than the control plots. We found no significant difference in the total N-oxide flux between the fallow treatments and the control (P = 0.8253; Fig. 3), which suggests that the N-fixing trees did not increase the N availability in this system. In a separate measurement not associated with the gas measurements, we assessed N availability during the first fallow phase (data not shown). Soil NO3-N levels were below the detection limit in the top 5 cm of the profile in all plots and soil NH4-N levels were very low (0.001–0.008 mgN g-soil1). The data that we presented on soil inorganic N stocks for the second fallow phase show that NH4-N levels were higher, but NO3-N was still very low. For net N mineralization rates measured during the first fallow phase, there was no difference

Our observations suggest that improved fallows using Nfixing trees do not appear to decrease the soil CH4 sink and also do not seem to increase CO2 and N-oxide emission in these sandy Amazonian soils. This experiment was not designed to test hypotheses on the effects of soil texture on gas emissions in fallows. However, we speculate that the reasons that our observations are contrary to observations in similar systems elsewhere are related to the very sandy texture of these soils. We do have a relatively good mechanistic understanding of the processes that regulate the magnitudes of the fluxes of these gases and we also understand the relationship between soil texture and the cycling of C and N in soils. We expect very rapid turnover of both C and N inputs to the soil, with little humification of organic inputs. At the outset of this paper we raised the concern that the effects of non-CO2 greenhouse gases could compromise carbon sequestration schemes based upon agroforestry practices if these practices involved planting of N-fixing trees. This study adds to the data available from which conclusions can be drawn. Previous work has indicated that agroforestry systems with N-fixing trees raise N-oxide emissions and reduce the sink strength of CH4. (Palm et al., 2002; Millar, 2002; Baggs et al., 2000, 2001; Verchot et al., 2006) Our results indicate that this is not always the case and that there are situations where N-fixing trees have no effect on soil trace gas fluxes. This finding has implications for GHG accounting methods and is consistent with recent modifications to the IPCC National GHG Accounting Guidelines (de Klein et al., 2006). In these guidelines, biological N fixation was removed as a direct source of N2O emissions because

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emissions do not arise from the N-fixation process itself (Rochette and Janzen, 2005). Currently accepted accounting systems include accounting procedures for increased emissions due to planting of N-fixing species, which are based on N-fixation rates. These results suggest that it would be better to base accounting systems on the impact of management on N availability and not strictly on N-fixation rates. Further quantification of gas fluxes in systems with Nfixing trees and identification of factors that reduce negative impacts of N-fixing trees will increase the opportunity for agroforestry to contribute to climate change mitigation.

Acknowledgements Partial support for this research was provided by NSF Atmospheric Chemistry Program under NSF Grant ATM9410759 and by the NASA LBA Grant no. NCC5-332. Partial funding was also provided through core funding to ICRAF. Logistical support in Brazil was supplied by the Empresa Brasileira de Pesquisa Agropecua´ria/Centro de ´ mido and the Instituto Pesquisa Agropecua´ria do Tro´pico U ˆ de Pesquisa Ambiental da Amazonia.

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