Effects of tropical forest conversion into oil palm plantations on nitrous oxide emissions: A meta-analysis

Oil palm plantations have dramatically expanded in tropical Asia over the past decades. Although their establishment has been projected to increase nitrous oxide (N2O) emissions, earlier reports have shown inconsistent results. This study analyzed these previously published data to compare N2O emissions in oil palm plantations to reference forests. A linear mixed-effects model was used to examine the significance of the effect of establishing oil palm plantations on N2O emissions, rather than to calculate mean effect sizes because of limitations in the data structure. The results indicated that N2O emissions were significantly greater from oil palm plantations than from reference forests, as expected. This is the first study to report the effect of oil palm plantations on N2O emissions by synthesizing previously published data. To quantify the size of this effect, additional studies with frequent and long-term monitoring data are needed.


Introduction
Oil palm (Elaeis guineensis Jacq.) plantations in tropical Asia have expanded dramatically in the past decades and has contributed to a significant decline in natural forests (Gaveau et al. 2016). According to the FAO (FAOSTAT 2021), the harvested area of oil palm fruit increased from 3.6 million ha in 1961 to 28.3 million ha in 2019; approximately 70% was in Indonesia and Malaysia. The rapid and large expansion of oil palm plantations causes loss of species richness and functional diversity (Koh and Wilcove 2008;Edwards et al. 2014).
Expansion of oil palm plantations has attracted global attention, not only due to the loss of biodiversity but also to enhanced nitrous oxide (N 2 O) emissions (Kaupper et al. 2020;Skiba et al. 2020). N 2 O is mainly produced by soil microbial processes such as nitrification and denitrification (Davidson et al. 2000). Because nitrogen (N) is the main source of N 2 O production, increased N input into soils, including the deposition of atmospheric N (Zhang et al. 2008;Wang et al. 2014), nitrogen-rich litter inputs (Arai et al. 2008;Ishizuka et al. 2021a, b), and chemical fertilization (Liu and Greaver 2009), stimulates N 2 O emissions. Because N fertilization is a common practice for oil palm plantations, the conversion of forests to oil palm plantations is generally projected to increase N 2 O emissions (Kaupper et al. 2020;Skiba et al. 2020). Several studies have reported greater N 2 O emissions from oil palm plantations than from forests in the same region (Melling et al. 2007;Hewitt et al. 2009;Drewer et al. 2021). Nitrogen fertilization resulted in greater N 2 O emissions in multiple oil palm plantations (Aini Abstract Oil palm plantations have dramatically expanded in tropical Asia over the past decades. Although their establishment has been projected to increase nitrous oxide (N 2 O) emissions, earlier reports have shown inconsistent results. This study analyzed these previously published data to compare N 2 O emissions in oil palm plantations to reference forests. A linear mixed-effects model was used to examine the significance of the effect of establishing oil palm plantations on N 2 O emissions, rather than to calculate mean effect sizes because of limitations in the data structure. The results indicated that N 2 O emissions were significantly greater from oil palm plantations than from reference forests, as expected. This is the first study to report the effect of oil palm plantations on N 2 O emissions by synthesizing previously published data. To quantify the size of this effect, additional studies with frequent and long-term monitoring data are needed. 866 T. Mori et al. 2015;Hassler et al. 2017;Oktarita et al. 2017;Rahman et al. 2019), although special (fertilized vs unfertilized areas) and temporal (short vs long period after fertilization) heterogeneity of the effects of fertilization is very large (Fowler et al. 2011;Aini et al. 2015).
However, several studies have reported only slight differences in N 2 O emissions between oil palm plantations and reference forests (Ishizuka et al. 2005;Swails et al. 2021). Even smaller amounts of N 2 O emissions have been reported on oil palm plantations (Yashiro et al. 2007). These inconsistent results could be partly due to insufficient monitoring to detect any fertilization effects (Yashiro et al. 2007;Aini et al. 2015). Hassler et al. (2017) discovered that largescale plantations emit greater levels of N 2 O than forests, but emissions from smallholder plantations did not differ significantly from forest emissions. Thus, previous results have been inconsistent. A larger-scale analysis synthesizing published data is necessary to evaluate the effects on N 2 O emissions of tropical forest conversion to oil palm plantations.

Data collection
Studies reporting N 2 O fluxes from oil palm plantations and forests in the same region were collected using the ISI Web of Science database and the following combinations of keywords: [N 2 O OR "nitrous oxide"] AND ["oil palm"] AND [soil]. The final search was completed on August 23, 2021. Only field-based studies reporting N 2 O fluxes from both oil palm plantations and reference forests were selected for data extraction; incubation experiments were excluded because the environmental conditions varied substantially. Primary, secondary, or disturbed forests were selected as reference forests. A total of 49 papers were identified through the search, however, only eight met the above criteria. The cumulative or average N 2 O emissions were extracted. Cumulative N 2 O emissions were converted into fluxes (µg N m -2 h -1 ). Vegetation type (oil palm vs reference forest), soil type, mean temperature, and annual precipitation were recorded. Google Scholar was used to complement the literature search, and three additional papers were added to the database. Finally, 69 N 2 O flux data from 63 study sites in 10 regions were extracted from the 11 papers (Table S1). Two datasets were prepared. The first was a "full dataset" consisting of all data obtained and containing short-term observations such as single-time measurements. The second was a "long-term frequent monitoring dataset," which consisted of monitoring data with a frequency of every ≤ 2 months and a period of ≥ 1 year.

Analysis
Previous meta-analyses generally used effect sizes (i.e., log-transformed values of N 2 O emissions from post landuse change sites divided by those from reference sites) to evaluate the effects of land-use changes on N 2 O emissions (Hergoualc'h and Verchot, 2014;Van Lent et al. 2015;McDaniel et al. 2019). However, pairwise observations have been uncommon in previous studies (Table S1). In addition, the standard deviation data needed for this approach have been occasionally unavailable. Therefore, in the present study, the effect of establishing an oil palm plantation on N 2 O emissions was evaluated using a linear mixed-effects model. The model was constructed with vegetation type (oil palm plantation vs. reference forest) as a fixed effect, and the study region and study site (Table S1) as random effects. The N 2 O flux data were natural log-transformed before analysis. Since a N 2 O flux datum was smaller than zero, it was replaced with one-half (0.57 µg N 2 O-N m -2 h -1 ) of the minimum gas flux in the dataset (1.14 µg N 2 O-N m -2 h -1 ) (Mori et al. 2016). Statistical analyses were performed using R, version 4.1.1 (The R Foundation for Statistical Computing, Vienna, Austria) and the lme4 and lmerTest packages (R Core Team 2021).

Results and discussion
Linear mixed-effects model analysis demonstrated that N 2 O emissions were significantly greater from oil palm plantations than from reference forests (Fig. 1, Table 1), which is in agreement with the commonly accepted view (Kaupper et al. 2020;Skiba et al. 2020). This result was obtained using both the full dataset (Fig. 1a, Table 1) and the frequent long-term monitoring dataset (Fig. 1b, Table 1). As suggested previously, N fertilization is probably the most important contributing factor in these increased N 2 O emissions (Hassler et al. 2017). Drainage may cause greater N 2 O emissions from peat soils because denitrification, which reduces N 2 O to N 2 under flooded conditions, may be inhibited by reduced water content (Murdiyarso et al. 2010).
Thus, the present study demonstrated the enhancing effect of establishing oil palm plantations on N 2 O emissions, but this meta-analysis also has limitations. First, the sample size is insufficiently robust to quantify the effect on N 2 O emissions and to estimate its impact on global warming (Skiba et al. 2020), although the linear mixed-effects model showed that tropical forest conversion into oil palm plantations elevated ln(N 2 O emissions) by 0.7 to 0.85 (µg N 2 O-N m -2 h -1 ) ( Table 1). More longterm and frequent monitoring data are required. The collected dataset included 29 oil palm plantations and 34 reference forests, among which only a third (11 oil palm plantations and 12 reference forests) had data collected via long-term and frequent monitoring (i.e., with a frequency of every ≤ 2 months and a period of ≥ 1 year). These long-term and frequent monitoring-based data are particularly important because rare or short-term gas flux measurements may fail to detect the fertilization-derived hotspots of N 2 O fluxes (Yashiro et al. 2007;Aini et al. 2015), which would lead to an underestimate of the effect of oil palm plantations on N 2 O emissions. Secondly, the relative importance of factors contributing the higher N 2 O emissions in oil palm plantations, (such as N fertilization or drainage of peatlands) were not determined, also due to the insufficient sample size. For constructing models to estimate the impact of oil palm plantations on N 2 O emissions, additional data are necessary.
Despite these limitations, this paper has shown the enhancing effect of establishing oil palm plantations on N 2 O emissions by synthesizing previously published data. This meta-analysis provides a data-driven basis for the general projection that tropical forest conversion enhances N 2 O emissions (Kaupper et al. 2020;Skiba et al. 2020) and underscores a need for oil palm management practices that mitigate N 2 O emissions.
Funding This study was supported by the Japan Society for the Promotion of Science (JSPS) KAKENHI Grant No 19H03008.
Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http:// creat iveco mmons. org/ licen ses/ by/4. 0/. Fig. 1 N 2 O emissions in reference forests vs. oil palm plantations; a full dataset consisted of all obtained data, b long-term frequent monitoring dataset consisted of monitoring data with a frequency of every ≤ 2 months and a period of ≥ 1 year. Number of observations was 63 and 29 in (a) and (b), respectively Table 1 Results of linear mixed-effects model analysis to estimate the natural log-transformed N 2 O fluxes That a single N 2 O flux datum was replaced with one-half (0.57 µg N 2 O-N m -2 h -1 ) of the minimum gas flux in the dataset (1.14 µg N 2 O-N m -2 h -1 ) before natural log-transformation because it was ˂ 0