Land use change effects on trace gas fluxes in the

forest margins of Central Sulawesi, Indonesia

Edzo Veldkamp,1 Joko Purbopuspito,1 Marife D. Corre,1 Rainer Brumme,1

and Daniel Murdiyarso2

Received 12 June 2007; revised 10 September 2007; accepted 29 January 2008; published 2 April 2008.

[1] Land use changes and land use intensification are considered important processescontributing to the increasing concentrations of the greenhouse gases nitrous oxide(N2O) and methane (CH4) and of nitric oxide (NO), a precursor of ozone. Studieson the effects of land use changes and land use intensification on soil trace gasemissions were mostly conducted in Latin America and only very few in Asia.Here we present results from Central Sulawesi where profound changes in landuse and cultivation practices take place: traditional agricultural practices likeshifting cultivation and slash-and-burn agriculture are replaced by permanentcultivation systems and introduction of income-generating cash crops like cacao.Our results showed that N2O emissions were higher from cacao agroforestry(35 ± 10 mg N m�2 h�1) than maize (9 ± 2 mg N m�2 h�1), whereas intermediaterates were observed from secondary forests (25 ± 11 mg N m�2 h�1). NOemissions did not differ among land use systems, ranging from 12 ± 2 mg N m�2 h�1

for cacao agroforestry and secondary forest to 18 ± 2 mg N m�2 h�1 for maize.CH4 uptake was higher for maize (�30 ± 4 mg C m�2 h�1) than cacao agroforestry(�18 ± 2 mg C m�2 h�1) and intermediate rates were measured from secondaryforests (�25 ± 4 mg C m�2 h�1). Combining these data with results from other studies inthis area, we present chronosequence effects of land use change on trace gas emissionsfrom natural forest, through maize cultivation, to cacao agroforestry (with or withoutfertilizer). Compared to the original forests, this typical land use change in thestudy area clearly led to higher N2O emissions and lower CH4 uptake with age ofcacao agroforestry systems. We conclude that this common land use sequence inthe area combined with the increasing use of fertilizer will strongly increase soiltrace gas emissions. We suggest that the future hot spot regions of high N2O(and to a lesser extend NO) emissions in the tropics are those areas where climaticand edaphic conditions allow for intensive agriculture. This scenario is probablypreferable over the alternative of agriculture extensification, which would imply adramatic increase in deforestation rates with accompanying CO2 emissions.

Citation: Veldkamp, E., J. Purbopuspito, M. D. Corre, R. Brumme, and D. Murdiyarso (2008), Land use change effects on trace

gas fluxes in the forest margins of Central Sulawesi, Indonesia, J. Geophys. Res., 113, G02003, doi:10.1029/2007JG000522.

1. Introduction

[2] Land use changes and land use intensification areconsidered important processes contributing to the increasingtrace gas emissions from soils [IPCC, 2001]. The trace gasesnitrous oxide (N2O) and methane (CH4) are importantgreenhouse gases, while nitric oxide (NO) plays an im-portant role in tropospheric chemical reactions includingproduction of ozone, which is also a potent greenhouse gas

[Logan, 1983]. N2O is produced by various sources, butsoils in the humid tropics are considered to be one of themost important contributors [Bouwman, 1998; Brumme etal., 2005; Mosier et al., 1998a]. Although global NOemissions are dominated by fossil fuel emissions ofNOx, the contribution of soils is considerable [Davidsonand Kingerlee, 1997]. Furthermore, NO and N2O emis-sions from soils are often studied together because bothgases are produced by nitrifying and denitrifying bacteriain soils and are affected by the same environmentalcontrols [Davidson et al., 2000]. Upland soils are consid-ered an important sink in the global CH4 budget, contrib-uting about 30 Tg CH4 yr�1, which may be reduced afterforest conversion to agriculture [Keller and Reiners, 1994].[3] Most studies on the effects of land use changes and

land use intensification on N2O, NO and CH4 emissions

JOURNAL OF GEOPHYSICAL RESEARCH, VOL. 113, G02003, doi:10.1029/2007JG000522, 2008

1Buesgen Institute, Soil Science of Tropical and Subtropical Ecosys-tems, Georg-August University of Goettingen, Goettingen, Germany.

2Center for International Forestry Research, Jalan CIFOR, Situgede,Sindangbarang, Bogor, Indonesia.

Copyright 2008 by the American Geophysical Union.0148-0227/08/2007JG000522

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have been conducted in Latin America [e.g., Garcia-Montielet al., 2001; Keller and Reiners, 1994; Keller et al., 2005,1993; Pinto et al., 2006; Reiners et al., 2002; Veldkamp andKeller, 1997; Veldkamp et al., 1998; Verchot et al., 2000,1999; Wick et al., 2005]. In general, conversion of tropicalforests to extensively managed pastures and secondaryforests led to reduced N2O and NO emissions and decreasedCH4 uptake [Keller and Reiners, 1994; Steudler et al., 1996;Verchot et al., 2000; Wick et al., 2005]. Changes to land usesystems where fertilizers were used led to increased N2Oand NO emissions [Matson et al., 1998; Mosier et al.,1998b; Palm et al., 2002; Veldkamp and Keller, 1997;Veldkamp et al., 1998] and reduced CH4 uptake [Palm etal., 2002; Veldkamp et al., 2001]. Agroforestry systemsshowed N2O and CH4 fluxes comparable to secondaryforest [Palm et al., 2002]. In Asia the number of studiesthat analyze the effect of land use and land use changes ontrace gas emissions is much more limited. Conversion oftropical forest to tree plantation in Sumatra, Indonesia led toelevated N2O emissions only for a short period after whichemissions were lower than the original forest [Ishizuka etal., 2002]. Forest clearing for coffee plantation led to astrong increase in N2O emissions in Sumatran Highlands[Verchot et al., 2006]. In southern Kalimantan on peatlands,N2O uptake was measured on all land uses studied (second-ary forest, paddy field, and upland field), and no clear trendwas observed with land use changes [Inubushi et al., 2003].[4] Although large rain forest areas are still intact in

Central Sulawesi, Indonesia, the area of annually clearedforest for agriculture has increased significantly in the lastdecade [Van Rheenen et al., 2004]. Like many rain forestareas in Indonesia, Central Sulawesi is confronted withprofound changes in land use and cultivation practices.Traditional agricultural practices like shifting cultivationand slash-and-burn agriculture are replaced by permanentcultivation systems and introduction of income-generatingcash crops. Farmers mostly plant annual crops (maize) onfreshly opened forest sites, and change to agroforestry afterseveral years of continuous cultivation. In a separate study,it was shown that in maize fields soil organic matterdecreased during continuous cultivation, whereas in agro-forestry soil organic matter levels were stable or had thetendency to increase with time [Dechert et al., 2004]. Thisincrease was probably caused by input of organic materialsfrom the N-fixing shade trees that are commonly used inthese agroforestry systems [Dechert et al., 2005].[5] In the present study, our goal was to analyze the effect

of land use changes on N2O, NO, and CH4 fluxes betweensoil and atmosphere. We measured monthly trace gas fluxeson replicated sites with maize, cacao agroforestry, andsecondary forests during a 6-month period covering thetransition from dry to wet season. In addition, we did a one-time measurement on 50 sites with the same land uses. Weused these data to identify the factors controlling trace gasemissions and to analyze the effects of a common land usechange scenario on trace gas emissions in this region.

2. Materials and Methods

2.1. Study Sites

[6] Our study area was located in the humid tropics ofCentral Sulawesi, Indonesia, at the forest margins of

Lorelindu National Park, south of Palu. The area ismountainous with elevations up to 2300m a.s.l. and issituated about 150 km south of the equator. Large, intactsubmontane and montane rain forests occur in the moun-tains, while valleys and lowland are mostly deforested andused for agriculture. We selected maize, cacao agroforest-ry, and secondary forest sites in three villages (Kaduwaa,Kamarora, and Ranoromba, which are about 30 km fromeach other), resulting in three replicates per land use (thesesites are referred to as ‘permanent sites’). The precipitationrecord collected near Wuasa (about 20 km from Kaduwaa)based on measurements from 1984–1999 showed a weakbi-modal pattern with rainy seasons in February–May andin September–December [BPS, 2000]. Annual rainfall atthis station was 1590 mm and on average no monthreceived less than 100 mm of rain. No long-term rainfallrecords exist for the study sites, but average annual rainfallcollected in 2002 and 2003 was 1856 mm for Kaduwaa,1974 mm for Kamarora, and 1261 mm for Ranoromba.According to the geological map (Sulawesi 2114, 1:250,000)and preliminary surveys, parent rocks in the area mainlyconsist of crystalline and metamorphic rocks (granite, grano-diorite, quarzite, slate and phyllite). All sites were located onthe lower parts of the slopes and in the valleys wherecolluvial, alluvial and lacustrine sediments occur. Soils wereyoung and chemically fertile with only minimal soil chem-ical differences (Table 1). Except for soil bulk density, whichwas higher in the cacao agroforestry (1.25 ± 0.02 g cm�3)followed by maize (1.17 ± 0.03 g cm�3) and secondaryforest (1.05 ± 0.03 g cm�3), there were no significantdifferences in soil properties among the land use types.However, in a study with many more sites in the same area,significant differences were found between soil organicmatter content and ECEC with higher values in secondaryforests compared to maize and agroforestry systems[Dechert et al., 2004]. Management of the different landuses was very diverse (Table 2). Shade trees in the cacaoagroforestry system were legumes (Erythrina spp. andGliricidia sepium). Fertilizer use or rotation with N-fixingcrops like beans was rare on newly cleared maize fields butmore common on maize fields that have been cultivated forprolonged periods. Also in cacao agroforestry systemsfertilizer use was becoming more common, but many cacaoagroforestry sites were not yet fertilized. Because of theweak rainfall seasonality, farmers sow their maize fieldsindependent of the season, so that at any given time maize atdifferent stages of development can be observed. Two of thesecondary forests were heavily logged about 8 years beforemeasurements and one secondary forest contained mainlyplanted trees (Aleurites mollucana, Table 2).[7] Because of social and political unrest in the study

area we were not able to collect more than 6 months of datafrom the permanent sites. Instead, we decided to collectdata in short field campaigns during which the same landuse types were selected in other sites of the same study areaand trace gas fluxes were measured only once (these sitesare referred to as ‘campaign sites’). We sampled in total18 cacao agroforestry sites and 22 maize sites. Only10 secondary forest sites were sampled because secondaryforests are less common in the study area. Fluxes measuredfrom the campaign sites were compared to the fluxes from

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the permanent sites to deduct how well the permanent sitesrepresented the different land use systems.

2.2. Sampling Design and Measurement Period

[8] On each land use type and site, 8 chamber bases(0.35 m diameter; 0.18 m height) were placed in a stratifiedrandom design along 4 parallel 15-m long transects spacedat 5 m apart. Chamber bases were inserted approximately0.05 m deep into the soil an hour before gas sampling andwere removed again after completion of sampling. On thepermanent sites, gas flux measurements were carried outmonthly between June and November 2003. N2O, NO andCH4 fluxes were measured on the same sampling day forthe 3 land uses in each site, and 8 soil samples (taken nearthe chamber bases) were collected from the top 0.1 mdepth for determination of soil moisture and mineral N.Four soil samples were pooled together resulting in 2composite samples. Soil samples were transported on iceand refrigerated in the laboratory in Palu until soil moisturedetermination and mineral N extraction, which were donenormally the day after sampling. For the campaign sites,

one-time gas flux measurements were carried out betweenAugust 2001 and May 2003, and no soil samples werecollected. For each land use type and site, the gas flux wasrepresented by the average of the 8 chamber measurementsper sampling day, and the soil moisture and mineral N bythe mean of the 2 composite soil samples.

2.3. Trace Gas Measurements

[9] We measured N2O and CH4 fluxes using static ventedchambers. Eight gas samples were removed at 5-min inter-vals and stored in 50 mL disposable syringes fitted withpolypropylene stopcocks. We chose this frequent samplingbecause preliminary measurements had shown that fluxes onthe studied sites could be low. Gas samples were transportedto the laboratory in Palu and analyzed within 36 h ofcollection using an automated gas chromatographic system(Shimadzu Scientific Instruments, Baltimore, United States)equipped with an electron capture detector for N2O analysisand a flame ionization detector for CH4 analysis [Loftfield etal., 1997]. Gas fluxes were calculated from linear regressionof concentrations versus time for each chamber. NO was

Table 1. Characteristics of Permanent Sites of Three Land Use Types in the Forest Margins of Central

Sulawesi, Indonesiaa

Locationsy

Kaduwaa Kamarora Ranoromba

Location/ClimateAltitude (m asl) 1156 ± 4a,z 771 ± 45b 454 ± 31c

Approx. coordinates 120�18.270E 1�26.220S 120�09.560E 1�12.060S 119�58.040E 1�04.490SAnnual rainfall (mm) 1856 1974 1261

Soil CharacteristicsBulk density (g cm�3) 1.14 ± 0.11 1.18 ± 0.09 1.16 ± 0.12Ave. soil WFPS (%) 60 ± 16 59 ± 9 49 ± 6Ave. soil Temp. (�C) 23.5 ± 0.6 23.8 ± 2.4 25.9 ± 0.8Soil pH-H2O 6.1 ± 0.4b 6.4 ± 0.4b 7.7 ± 0.3a

Soil pH-KCl 5.3 ± 0.5b 5.4 ± 0.6b 6.9 ± 0.3a

ECEC (mmol(+)kg�1) 131 ± 32 180 ± 74 325 ± 141Base saturation (%) 99.4 ± 0.1 98.9 ± 0.5 99.8 ± 0.1Org. C (mg C g�1 soil) 22.0 ± 3.6 27.5 ± 15.6 24.8 ± 6.9Org. N (mg N g�1 soil) 2.2 ± 0.5 2.4 ± 1.0 2.3 ± 0.5Total P (mg P g�1 soil) 0.58 ± 0.08 0.49 ± 0.05 0.62 ± 0.09

aNotes: y, On each permanent site, three land use types were observed. z, Means (±SD; n = 3 (land uses)) within rowsfollowed by different letter indicate significant difference among sites (one-way ANOVA, Least Significant Difference test atP � 0.05).

Table 2. Management Characteristics in Permanent Sites of the Three Land Use Types in the Forest Margins of

Central Sulawesi, Indonesia

Locations

Kaduwaa Kamarora Ranoromba

Cacao AgroforestryAge of plantation 10 y 23 y 12 yCacao density 3.0 � 3.0 m 2.5 � 2.5 m 3.0 � 3.0 mShade tree density 3.0 � 6.0 m 5.0 � 5.0 m 3.0 � 6.0 mFertilizer use N & P No noApprox. yield (kg ha�1) 700 900 500

MaizeAge of field 8 y 15 y 12 yMaize density 0.5 � 1.1 m 1.1 � 1.2 m 0.8 � 1.0 mFertilizer No rotation with beans NoApprox. yield (ton ha�1) 1.3 1.5 1.0

Secondary ForestTime since logging 8 y 8 y –Time since planting – – 12 y

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measured directly in the field using dynamic chamberswhich were placed on the same chamber bases that wereused for N2O and CH4 sampling. A Scintrex LMA-3chemiluminescence detector (Scintrex, Ontario, Canada)was used to analyze NO after conversion to NO2 by aCrO3 catalyst [Bakwin et al., 1990]. The detector wascalibrated on-site before and after the flux measurementsfrom eight chambers in one site. Detector signal and timewere collected with a Campbell CR 510 data logger(Campbell Scientific, Logan, United States). NO fluxeswere calculated from the linear increase of concentrationsversus time. All calculated fluxes were corrected withmeasured air temperature and air pressure. Zero fluxes(no change in concentration) were included.

2.4. Supporting Parameters

[10] Soil characteristics (Table 1) from the permanentsites were determined at the beginning of the study (2003).Bulk density (for 0–5 cm depth) was measured usingundisturbed soil cores (volume: 250 cm3). Soil samples fordetermination of pH and exchangeable cations were air-dried and passed through a 2-mm sieve. Exchangeablecations were determined by leaching soil samples with100 ml unbuffered 1 M NH4Cl for 4–5 hours. Cations in thepercolates were analyzed using Flame-Atomic AbsorptionSpectrometer (Varian, Darmstadt, Germany). For total organ-ic C, N and P analyses, air-dried and sieved soil samples wereground to <150 mm using a ball mill. Total organic C and Nwere measured using CNS Elemental Analyzer (ElementarVario EL, Hanau, Germany). Total P was determined bydigesting the soil samples under high pressure in concentrat-ed HNO3, and the digests were analyzed using InductivelyCoupled Plasma-Atomic Emission Spectrometer (SpectroAnalytical Instruments, Kleve, Germany).[11] Soil water content and extractable mineral N were

determined from fresh soil samples, which were taken fromthe top 0.10 m of the permanent sites every time gas fluxeswere measured. Soil moisture was determined by oven-drying the samples for 48 h at 105�C, and moisture contentwas expressed in terms of water-filled pore space (WFPS)using the measured bulk densities. For extractable mineralN, 20 g soil was weighed in a 125 mL plastic Nalgenebottle, added with 100 mL 0.5M K2SO4, and filtered afterone hour of agitation. A drop of chloroform was added andthe extracts were frozen and later on transported to theInstitute of Soil Science and Forest Nutrition, Goettingen,Germany for analysis. NO3

� + NO2�, hereafter referred to as

NO3�, and NH4

+ in the extracts were analyzed using standardmethods of continuous flow injection colorimetry (Cenco/Skalar Instruments, Breda, The Netherlands).

2.5. Statistical Analyses

[12] Each site was considered a replicate for a particularland use type, and the gas flux from a site was the mean ofeight chamber measurements per sampling day. Statisticalanalyses were conducted on the mean values of each site andsampling day and not on individual chamber measurements.Tests for normality using Kolmogorov-Smirnov D statisticand for homogeneity of variance using Levene statistic[Sokal and Rohlf, 1981] were conducted for each measuredparameter. The data set showed a nonnormal distributionand nonhomogenous variance, and hence a log transfor-

mation was performed before further analyses. Differencesamong land use types and between seasons were deter-mined from the permanent sites using repeated-measuresanalysis of variance (ANOVA) [Crowder and Hand, 1990],and multiple comparisons were assessed using Least Signif-icant Difference test at P � 0.05. Linear regression wasperformed between trace gas emissions and WFPS usingmean values for each land use type per sampling date. Inaddition, we wanted to know if the differences among landuse types we observed from permanent sites are reflected inthe one-time measurement of the campaign sites. We testedthe differences across land use types and seasons from thecampaign sites using two-way ANOVA with multiple com-parisons using Least Significant Difference test at P � 0.05.We also wanted to test how well our permanent sitesrepresented the land use types in the study area. For thiswe compared the trace gas emissions from the campaignsites and permanent sites. The campaign sites were groupedaccording to the corresponding land use and season of thepermanent sites, and test of differences was carried out usingIndependent T test at P � 0.05.

3. Results

3.1. Land Use and Seasonal Effects on TraceGas Fluxes

[13] From the permanent sites, N2O emissions across sea-sonswere higher in cacao agroforestry (35 ± 10mgNm�2 h�1)than inmaize (9 ± 2mgNm�2 h�1), whereasN2O emissions insecondary forest (25 ± 11 mg N m�2 h�1) did not differ fromother land uses (Figure 1a). On average across seasons, NOemissions ranged from 12 ± 1 mg N m�2 h�1 in cacaoagroforestry and 12 ± 2 mg N m�2 h�1 in secondary forest to18 ± 2 mg N m�2 h�1 in maize but did not differ among landuses (Figure 1b). CH4 uptake across seasons was higher inmaize (�30 ± 4 mg C m�2 h�1) than in cacao agroforestry(�18 ± 2mgCm�2 h�1), while CH4 uptake in secondary forest(�23 ± 4 mg C m�2 h�1) was not different from the other landuses (Figure 1c). N2O fluxes were higher during the dry thanthe wet season only in the cacao agroforestry (Table 3). Wethink, however, that this difference in N2O fluxes was not dueto soil water content as WFPS for a particular land use did notdisplay a clear trend between the wet and dry seasons(Figure 1d). Two of the cacao agroforestry sites had manage-ment activities which probably caused the higher emissionsduring the dry season: in Kaduwaa urea fertilizer was appliedin early June 2003, and inKamarora shade trees were pruned inJuly and August 2003. NO and CH4 fluxes in all land uses didnot differ between the dry and wet season (Table 3).

3.2. Soil Controls on Trace Gas Fluxes

[14] Mineral N was dominated by NO3� in all three land

uses studied. NH4+ and NO3

� did not differ among land usetypes, nor was there any seasonal trend (data not shown).NH4

+, NO3� and (NH4

+ + NO3�) did not correlate to any of the

trace gases measured. The dominance of NO3� in the mineral

N was in contrast to earlier work by our group [Corre et al.,2006] where extractable mineral N measured from intact soilcores was dominated by NH4

+ in similar land use systems.We think that despite our effort to cool the disturbed soilsamples, significant nitrification took place in the samples

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during transport and storage, causing the high NO3� concen-

trations. Thus, we only report total mineral N values.[15] WFPS was higher in cacao agroforestry and sec-

ondary forest than in maize, but there was no differencebetween dry and wet seasons for a particular land use(Figure 1d). This trend in WFPS among land use typesbrought significant negative relationships with CH4 fluxes

and NO/N2O flux ratio when correlating across land usetypes (Figures 2a and 2b).

3.3. Comparison of Fluxes Between Campaignand Permanent Sites

[16] N2O and NO emissions from the campaign sitesfollowed similar trend in differences among land use types

Figure 1. Monthly fluxes (mean ± SE; n = 3 (sites)) of (a) N2O, (b) NO, (c) CH4, and (d) WFPS of thethree land use types from permanent sites in the forest margins of Central Sulawesi, Indonesia (diamond,cacao agroforestry; square, maize; triangle, secondary forest). Shaded area is dry season.

Table 3. Trace Gas Fluxes of the Three Land Use Types During Dry (June–August 2003) and Wet (September–November 2003) Season

From Permanent Sites in the Forest Margins of Central Sulawesi, Indonesiaa

Trace Gases

Land Use Type/Season

Cacao Agroforestry Maize Secondary Forest

Dry Months Wet Months Dry Months Wet Months Dry Months Wet Months

N2O-N (mg N m�2 h�1) 57 ± 16a,y 13 ± 2b 11 ± 2 7 ± 2*,z 41 ± 22 8 ± 3NO-N (mg N m�2 h�1) 13 ± 2 11 ± 2 16 ± 3 21 ± 4* 10 ± 2 13 ± 3CH4-C (mg C m�2 h�1) �15 ± 2* �20 ± 2 �28 ± 5* �33 ± 5* �23 ± 7* �27 ± 5*

aNotes: Measurements were conducted monthly, and each land use type and season had 3 sampling days. y, Means (±SE; n = 3 (sites)) within aland use type followed by a different letter indicate significant difference between seasons (repeated-measures ANOVA, Least Significant Differencetest at P � 0.05). z, Means for a particular land use and season followed by * indicate significant difference from the campaign sites with the sameland use and season (Independent T test at P � 0.05).

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as that from the permanent sites. On average acrossseasons, N2O emissions from the campaign sites werehigher in the cacao agroforestry (61 ± 30 mg N m�2 h�1)than maize (25 ± 11 mg N m�2 h�1) and secondary forest(16 ± 3 mg N m�2 h�1). NO emissions also did not differamong land uses: 12 ± 2 mg N m�2 h�1 in cacao agrofor-estry, 8 ± 2 mg N m�2 h�1 in maize, and 9 ± 3 mg N m�2 h�1

in secondary forest. The campaign sites also showed nodetectable difference in N oxide emissions between the dryand wet season in all land uses (Table 4). For a particularland use and season, the N oxide emissions from thecampaign (Table 4) and permanent (Table 3) sites werecomparable, except in maize during the wet season. For thecampaign sites, average CH4 uptake across seasons washigher in secondary forest (�115 ± 39 mg C m�2 h�1) thanin cacao agroforestry (�18 ± 5 mg C m�2 h�1), while maize(�63 ± 13 mg C m�2 h�1) did not differ with the other land

uses. Comparing the CH4 uptake from campaign andpermanent sites for a particular land use and season, thecampaign sites (Table 4) showed higher CH4 uptake than thepermanent sites (Table 3), and the highest uptake wasobserved in the secondary forest measured during the dryseason.

4. Discussion

4.1. Trace Gas Fluxes in Different Land Use Systems

[17] Information on trace gas emissions from tropicalagricultural systems is presently scarce. Extremely highN2O emissions have been reported from systems that areheavily fertilized and either irrigated or receive a lot ofrainfall [Matson et al., 1998; Reiners et al., 2002; Veldkampand Keller, 1997; Veldkamp et al., 1998]. Relatively lowN2O emissions [Ishizuka et al., 2002; Weitz et al., 1998] or

Table 4. Trace Gas Fluxes of the Three Land Use Types During Dry and Wet Seasons From Campaign Sites in the Forest Margins of

Central Sulawesi, Indonesiaa

Trace Gases

Land Use Type/Season

Cacao Agroforestry Maize Secondary Forest

Dry Months Wet Months Dry Months Wet Months Dry Months Wet Months

N2O-N (mg N m�2 h�1) 28 ± 7ab,y (4) 70 ± 39a (14) 10 ± 4b (5) 29 ± 14ab,z (17)* 19 ± 5ab (5) 13 ± 4ab (5)NO-N (mg N m�2 h�1) 5 ± 2 (3) 14 ± 3 (13) 11 ± 7 (4) 7 ± 2 (11)* 11 ± 7 (3) 7 ± 3 (4)CH4-C (mg C m�2 h�1) �41 ± 12b (4)* �11 ± 4b (13) �82 ± 21b (5)* �57 ± 16b (16)* �175 ± 59a (5)* �55 ± 14b (5)*

aNotes: Measurements were conducted once per site between August 2001 and May 2003, and each sampling date was classified according to season thatthe sampling date belonged. y, Means (±SE; n in brackets is the number of sites) within rows followed by a different letter indicate significant differenceacross land use types and seasons (two-way ANOVA, Least Significant Difference test at P � 0.05). z, Means for a particular land use and season followedby * indicate significant difference from the permanent sites with the same land use and season (Independent T test at P � 0.05).

Figure 2. (a) CH4 fluxes versus water-filled pore space and (b) NO:N2O ratios versus water-filled porespace of the three land use types from permanent sites in the forest margins of Central Sulawesi,Indonesia. Data points are average of 3 sites per sampling date: diamond, cacao agroforestry; square,maize; triangle, secondary forest; open symbols, dry months; filled symbols, wet months. The regressionline in Figure 2a is CH4 flux = �53 + 0.52 * (WFPS); n = 18, R2 = 0.40, P = 0.005. The regression line inFigure 2b is NO/N2O ratio = 8.4 � 0.12 * (WFPS); n = 18, R2 = 0.51, P � 0.001.

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even negative fluxes [Inubushi et al., 2003] have beenreported from unfertilized systems. The N2O emissions thatwe measured from unfertilized maize (permanent sites)were in the same order of magnitude as N2O emissionsfrom unfertilized agriculture in Costa Rica [Weitz et al.,1998], but lower than the emissions reported from afertilized rice-cowpea rotation in tropical Peru [Palm etal., 2002] and from a fertilized maize-groundnut rotation inMalaysia [Khalil et al., 2002]. The cacao agroforestry sitesthat received N fertilizer had the highest N2O and NOemissions in our present study. But also the N2O emissionsfrom the unfertilized cacao agroforestry were higher thanthe original forest in the study area [Purbopuspito et al.,2006]. We attributed these relatively high N2O emissions tothe more rapid N cycling in these agroforestry systems[Corre et al., 2006] which was ascribed to the N input bythe N-fixing shade trees in this land use. In our study area, acomparison of unfertilized cacao agroforestry systems invarious ages showed that the soil organic matter contentwas stable and even had the tendency to increase with age[Dechert et al., 2004]. This, combined with a study onnutrient balance, led to the estimate that legume shade treesfix about 70 kg N ha�1 yr�1 [Dechert et al., 2005]. ElevatedN2O emissions caused by legume trees have also beenobserved in a midsuccessional forest in Puerto Rico [Ericksonet al., 2001]. The N2O emissions we measured from thecacao agroforestry system were higher than N2O emissionsfrom unfertilized multistrata agroforestry systems and peachpalm plantations in Peru [Palm et al., 2002] and fromunfertilized rubber plantations in Sumatra, Indonesia[Ishizuka et al., 2002]. Our results, together with thelimited published N2O and NO data, make clear thatmost published trace gas emissions from tropical agri-culture can be explained with the two levels of controlas hypothesized by the conceptual hole-in-the-pipe (HIP)model [Davidson et al., 2000]. The main level of controlthat influences the magnitude of N2O + NO emissions intropical agriculture is N availability, which is stronglyinfluenced by either N-fixing legumes or N fertilizerapplications. The relative contribution of NO (mainlyproduced by nitrification, an aerobic process) and N2O(mainly produced by denitrification, an anaerobic pro-cess) is mainly controlled by the soil water content(Figure 2b).[18] Until recently, N application in tropical agriculture

was mainly restricted to large scale plantations [Veldkampand Keller, 1997] or rice paddies. However, the use of Nfertilizer is rapidly increasing in tropical areas [Gallowayand Cowling, 2002] and is expected to surpass N applica-tion in temperate areas. An illustration of this is theincreased use of fertilizer in cacao agroforestry systems inour study area; although present rates of N application arestill comparably low (the commonly used rate in lowlandagriculture is 100 kg urea-N ha�1 yr�1, but many farmers ofthis cacao agroforestry system in the study area apply lessthan half of this). It is obvious that these changes will leadto increased N oxide emissions, and future studies should bedirected to investigating how high these increases will beand how to adapt management to control them.[19] The N2O emissions we measured in secondary forests

are within the range of fluxes measured in Costa Rica [Kellerand Reiners, 1994; Reiners et al., 2002; Weitz et al., 1998]

but lower than tree-based systems in Peru [Palm et al., 2002]and Sumatra, Indonesia [Ishizuka et al., 2002]. As secondaryforests are in some stage of succession or recovery afterdisturbance, their biomass in this study area is increasing andthe vegetation and soil act as a sink of N, and hence gaseousN losses are expected to be lower than natural forests. In ourstudy, the average N oxide emissions from both thepermanent and campaign sites were comparable betweenthe secondary forests and the natural forests [Purbopuspitoet al., 2006]. Our secondary forests differed in ages(particularly from the campaign sites) and had manage-ment activities (e.g., cutting of small trees, harvesting ofcandle nuts, etc.), which may have stimulated N cyclingand with that N oxide emissions.[20] CH4 uptake from maize was slightly higher than CH4

uptake from unfertilized maize in Costa Rica [Weitz et al.,1998] and from a low-input maize-legume rotation in Peru[Palm et al., 2002]. Cacao agroforestry had a slightly lowerCH4 uptake than the natural forest at 1200 m elevation inthe same area [Purbopuspito et al., 2006] and an agrofor-estry system in Peru [Palm et al., 2002], but was compa-rable to a rubber plantation in Sumatra [Ishizuka et al.,2002]. Finally, the secondary forest showed slightly lowerCH4 uptake than the older secondary forests in Costa Rica[Keller and Reiners, 1994] and Peru [Palm et al., 2002], butwas comparable to the natural forest at 1200m elevation inthe same area [Purbopuspito et al., 2006] and to a second-ary forest in China [Werner et al., 2006]. Most of thesetrends in CH4 fluxes can be explained with differences ingas diffusivity as a result of compaction: cacao agroforestryhad the highest bulk density, while natural forest and maizedisplayed lower values (Figure 3a). Some studies havefound that high NH4

+ concentrations may inhibit the CH4

oxidation capacity of soils [Steudler et al., 1989; Veldkampet al., 2001] but our study design did not make it possible todeduct possible effects of N fertilizer on CH4 fluxes.[21] The lack of seasonality in trace gas emissions was

possibly a result of the weak and bimodal pattern of wet anddry seasons. Based on the long-term records, the rainyseasons occur from February to May and from Septemberto December. However, interannual variations are large(e.g., in the 15-year rainfall record at Wuasa, annual rainfallvaried between 1036 mm and 2444 mm) and also the timingof the rainy seasons varies considerably between years (inthe Wuasa record, eight different months appear as wettestmonths, four of which also appear as driest month indifferent years). During the 6-month measurement periodin the permanent sites, there was no clear rainy season, asillustrated by the lack of seasonal pattern in WFPS(Figure 1d). The negative correlations of NO/N2O ratioand CH4 with WFPS (Figure 2) were due to the differencesin WFPS among the land uses (Figure 1d). The high WFPSin cacao agroforestry and secondary forest was possibly theeffect of litter cover and shade in these systems, making thesoil less exposed to direct sunlight, whereas the regularweeding in maize sites deprived the soil with cover possiblyresulting to high moisture loss. Correlations of CH4 withWFPS have been observed in other studies in tropical sites[Keller and Reiners, 1994;Weitz et al., 1998]. CH4 uptake issupposed to be limited by the rate at which CH4 can diffuseinto the soil. The direct control of effective gas diffusivity

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by the soil water content explains the negative correlation ofCH4 flux with WFPS.

4.2. How Well Do Measurements From thePermanent Sites Represent the Different Land Uses?

[22] We compared the trace gas emissions between thepermanent and campaign sites to analyze whether the per-manent sites represented the studied land uses in the area. For

N2O and NO emissions, measurements from the permanent(3 sites, each with 6 sampling dates) and campaign sites(3–17 sites, each measured once) were generally compara-ble, indicating that the permanent sites have represented theN oxide emissions. An exception to this was the N trace gasfluxes in maize during the wet season (Tables 3 and 4). Thecampaign maize sites (11–17 sites, each measured once)showed higher N2O fluxes and lower NO fluxes than the

Figure 3. Data from the present study were combined with trace gas emissions measurements and soildata from natural forest sites [Purbopuspito et al., 2006] and other sites of the same land uses in the studyarea [Corre et al., 2006; Dechert et al., 2004, 2005], and were chronologically ordered in such a way thatwe can reconstruct the effects of common land use changes on trace gas emissions in the forest marginsof Central Sulawesi, Indonesia. Farmers usually plant annual crops (maize) on newly opened forest sites,and change to cacao agroforestry after several years of continuous cultivation. The data points for 3-yearold maize are the average of campaign unfertilized maize sites younger than 5 years, and the data pointsfor 5-year old cacao agroforestry are the average of campaign cacao sites younger than 10 years. The datapoints for 8- and 15-year old maize and 10- and 20-year old cacao agroforestry are from permanent sitesin Kaduwaa and Kamarora. (a) bulkdensity, (b) mineral nitrogen, (c) N2O, (d) NO, and (e) CH4. The linesin the figure are our subjective interpretation of the trends with time. The double lines in Figures 3c and3d are our interpretation for unfertilized (lower line) and fertilized (upper line) cacao agroforestry.

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permanent sites. The reason for these differences was thatsome of the campaign maize sites were fertilized during thewet season, while the permanent maize sites were allunfertilized. When considering only the N2O and NOemissions from the campaign fertilized maize, these werehigher than the permanent sites, and N oxide emissionsfrom campaign unfertilized maize were comparable withthe permanent sites.[23] For CH4 fluxes, the trend of differences among land

uses was similar in permanent and campaign sites, but whatdiffered was the magnitude of measured fluxes betweenpermanent and campaign sites. The higher CH4 uptake fromthe campaign sites (4–16 sites, each measured once) thanthe permanent sites (3 sites, each with 6 sampling days)indicated that compared to the N trace gases CH4 was moreaffected by differences in N input and irregularity of seasonsamong the campaign sites. The high CH4 uptake and highvariation (indicated by higher standard error) from thecampaign sites was probably a result of differences in Ninput among the sites measured – e.g., the cacao agrofor-estry sites had different times of N application and pruningof the leguminous shade trees prior to trace gas measure-ments, some of the maize sites were fertilized, and thesecondary forest sites differed in ages. The irregularity ofwet and dry periods between August 2001 and May 2003during which the one-time measurement from these cam-paign sites was conducted may have additionally caused thehigh variation and different CH4 uptake compared to thepermanent sites (measured within the same year, June toNovember 2003).

4.3. Trace Gas Fluxes in a Land Use Change Scenario

[24] In the previous sections we have analyzed the landuse systems as different groups. If we combine these resultswith trace gas measurements and soil data from naturalforest sites [Purbopuspito et al., 2006] and other sites of thesame land uses in the study area [Corre et al., 2006;Dechert et al., 2004] we are able to present a sequence ofsoil conditions and corresponding trace gas fluxes followingdeforestation and successive land use changes for the forestmargins in Central Sulawesi. For this chronosequence wedid not include the results from Ranoromba, because theclimate is drier than the other two sites (Table 1). Thesequence of land use changes that we present starts withnatural forest, which is cleared for maize. After growingmaize for some years, the productivity of maize drops andmaize may be replaced by cacao agroforestry. This land usechange scenario is only one of many different possibilities,but to our observations it is a scenario that has been quitecommon in the study area. In more recent years, clearedforest is more often directly replaced by cacao agroforestrysystems [Dechert et al., 2004; Steffan-Dewenter et al.,2007; Van Rheenen et al., 2004].[25] We observed large changes in soil chemical and

physical properties along the land use chronosequence.After forest clearing, soil bulk density increased, whichcontinued during maize cultivation (Figure 3a). Changing toagroforestry did not revert this process, but actually com-pacted the soil even more, so that on average the soil bulkdensity in the agroforestry systems was about 20% higherthan in the original forest [Dechert et al., 2004]. Comparedto the original forest, mineral nitrogen sharply decreased

after forest clearing and remained stable at low levels insubsequent years of maize cultivation (Figure 3b). Thistrend can be explained by a progressive N limitation duringmaize cultivation which is probably caused by the combineduptake of N by the maize crop and the lack of N replen-ishment in unfertilized maize. In the same study area, it wasshown that although soil fertility was generally high, soilorganic matter stocks declined with duration of maizecultivation, indicating that continuous maize cultivationwas not sustainable [Dechert et al., 2004]. After maizecultivation is replaced by cacao agroforestry, mineral nitro-gen levels tended to increase compared to the low levelsduring maize cultivation, but even after twenty years theydid not return to the levels that were measured in the naturalforest (Figure 3b).[26] These profound changes in soil characteristics along

this land use chronosequence strongly affected the ex-change of trace gases. Immediately following forest clear-ing, N2O emissions increased, but this was only for arelatively short period, until N became strongly limiting[Corre et al., 2006]. N limitation was caused by the com-bined N-uptake by maize and the progressive decompositionof soil organic matter. In addition, the WFPS we measuredin maize was actually lower than in the original forest,which is likely caused by the direct irradiation of the sun.The N2O emissions reacted correspondingly and droppedto levels lower than in the original forest (Figure 3c).After conversion of maize to cacao agroforestry, N2Oemissions tended to increase in the unfertilized systems.This was probably a reaction to increasing N availabilitywith time as a result of N input from the leguminousshade trees [Dechert et al., 2005]. Furthermore, the highbulk density in cacao agroforestry increases the probabilityof anaerobic sites which favor N2O production. In theunfertilized cacao agroforestry system, N2O emissioncould eventually reach a level about twice the N2Oemission from the original forest (Figure 3c). These highemissions are supported by a more rapid N cycling inagroforestry systems as compared to the original forest[Corre et al., 2006]. Increasingly, N fertilizers are appliedto these agroforestry systems and our data showed thatN2O emissions from fertilized agroforestry increased muchmore rapidly than the unfertilized agroforestry systems,eventually reaching levels which were about four timeshigher than the original forest (Figure 3c). NO emissionsreacted differently from N2O emissions. In the maize fields,NO emissions tended to increase with time (Figure 3d),which is probably caused by the drier conditions in the maizefields, favoring a less reduced N oxide gas (NO) than N2O.Even though N availability increased with time in theagroforestry systems, NO emissions did not increase(Figure 3d), which we relate to the high bulk densities andcorrespondingly higher WFPS in these systems. CH4 uptakeshortly increased after forest clearing but further along thechronosequence CH4 uptake decreased with the lowestvalues found in the old agroforestry systems (Figure 3e).This reduction of CH4 uptake with duration of land use isprobably related to the bulk density which also increasedwith time (Figure 3a). A higher bulk density leads to a higherWFPS and correspondingly lower CH4 uptake.[27] Overall, the land use changes that presently occur

(i.e., replacement of forest and maize field with agroforestry

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and the increasing use of N fertilizers in agroforestrysystems) clearly lead to higher N2O emissions and lowerCH4 uptake than the original forest. Expectations are thatfertilizer use will increase in tropical areas, and we thereforeexpect that in the coming decades the contribution of thisand comparable areas to N2O emissions will increasestrongly. The alternative to using N fertilizer would beextensification of agriculture. However, to meet the needsof a growing population, this scenario would require clear-ing more forest for agriculture, which is accompanied with adramatic CO2 loss from deforestation. Such a scenario hashappened in the past decades in the Amazon Basin onheavily weathered soils, where until recently forests havebeen mainly replaced by low-input pastures [Verchot et al.,1999; Wick et al., 2005].[28] We conclude that the future hot spot regions of high

N2O (and to a lesser extend NO) emissions in the tropics arethose areas where climatic and edaphic conditions allow forintensive agriculture. This scenario is probably preferableover the alternative of agriculture extensification, whichwould lead to dramatically higher CO2 emissions fromdeforestation. Reducing N2O and NO emissions from in-tensive tropical agriculture will therefore be one of themajor challenges of the coming decades.

[29] Acknowledgments. The constructive comments of two anonymousreviewers are highly appreciated. The study was funded by DFG (DeutscheForschungsgemeinschaft) as subproject B3 of the collaborative researchprogram ‘‘Stability of rain forest margins’’ (SFB552-STORMA), comanagedby the Universities of Goettingen, Kassel, Bogor and Palu. J.P. held ascholarship from the German Academic Exchange Service (DAAD). We thankthe laboratory staff members of IBW, University of Goettingen, and ofSTORMA, Palu, for their support.

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�����������������������R. Brumme, M. D. Corre, J. Purbopuspito, and E. Veldkamp, Buesgen

Institute, Soil Science of Tropical and Subtropical Ecosystems, Georg-August University of Goettingen, Busgenweg 2, D-37077 Goettingen,Germany. (eveldka@gwdg.de)D. Murdiyarso, Center for International Forestry Research, Jalan CIFOR,

Situgede, Sindangbarang, Bogor 16680, Indonesia.

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