High heterotrophic CO2 emissions from a Malaysian oil palm plantations during dry-season

High heterotrophic CO2 emissions from a Malaysian oil palm plantations during dry-season Wetlands Ecol Manage (2018) 26:415–424 https://doi.org/10.1007/s11273-017-9583-6 ORIGINAL PAPER High heterotrophic CO emissions from a Malaysian oil palm plantations during dry-season . . . Magdalena Matysek Stephanie Evers Marshall Kana Samuel Sofie Sjogersten Received: 13 February 2017 / Accepted: 14 October 2017 / Published online: 1 December 2017 The Author(s) 2017. This article is an open access publication Abstract Tropical peatlands are currently being temperature and moisture at site and also accompanied rapidly cleared and drained for the establishment of by depth profiles assessing peat C and bulk density. oil palm plantations, which threatens their globally The soil respiration decreased exponentially with significant carbon sequestration capacity. Large-scale distance from the palm trunks with the sharpest land conversion of tropical peatlands is important in decline found for the plantation with the younger the context of greenhouse gas emission factors and palms with overall fluxes of 1341 and 988 mg CO -2 -1 sustainable land management. At present, quantifica- m h , respectively, at the 2000 and 2006 planta- tion of carbon dioxide losses from tropical peatlands is tions, respectively. The mean heterotrophic flux was -2 -1 limited by our understanding of the relative contribu- 909 ± SE 136 and 716 ± SE 201 mg m h at the tion of heterotrophic and autotrophic respiration to net 2000 and 2006 plantations, respectively. Autotrophic peat surface CO emissions. In this study we separated emissions adjacent to the palm trunks were 845 ± SE -2 -1 heterotrophic and autotrophic components of peat CO 135 and 1558 ± SE 341 mg m h at the 2000 and losses from two oil palm plantations (one established 2006 plantations, respectively. Heterotrophic CO flux in ‘2000’ and the other in 1978, then replanted in was positively related to peat soil moisture, but not -2 ‘2006’) using chamber-based emissions sampling temperature. Total peat C stocks were 60 kg m along a transect from the rooting to non-rooting zones (down to 1 m depth) and did not vary among on a peatland in Selangor, Peninsular Malaysia over plantations of different ages but SOC concentrations the course of 3 months (June–August, 2014). Collar declined significantly with depth at both plantations CO measurements were compared with soil M. Matysek  S. Evers  M. K. Samuel M. Matysek (&)  S. Sjogersten School of Biosciences, University of Nottingham, School of Biosciences, University of Nottingham, Collage Malaysia Campus, Jalan Broga, 43500 Semenyih, Road, Sutton Bonington, Selangor Darul Ehsan, Malaysia Loughborough LE12 5RE, UK e-mail: 0805090m@gmail.com S. Evers Tropical Catchment Research Initiative (TROCARI), M. Matysek Kuala Lumpur, Malaysia Department of Animal and Plant Sciences, University of Sheffield, Alfred Denny Building, Sheffield S102TN, UK M. K. Samuel Climate Change Programme, Malaysian Agricultural S. Evers Research and Development Institute (MARDI) Serdang, School of Natural Sciences and Psychology, Liverpool Selangor, Malaysia John Moores University, Liverpool L3 3AF, UK 123 416 Wetlands Ecol Manage (2018) 26:415–424 but the decline was sharper in the second generation respiration encompasses root growth and maintenance 2006 plantation. The CO flux values reported in this respiration of living roots, as well as emissions from study suggest a potential for very high carbon (C) loss mycorrhizal fungi (Epron 2009). A major limitation of from drained tropical peats during the dry season. This our ability to understand the consequences of land use is particularly concerning given that more intense dry change on decomposition processes and CO losses periods related to climate change are predicted for SE from tropical peatlands, including oil palm planta- Asia. Taken together, this study highlights the need for tions, is the lack of separation of autotrophic and careful management of tropical peatlands, and the heterotrophic respiration components in the majority vulnerability of their carbon storage capability under of studies (Couwenberg et al. 2010). Consequently, a conditions of drainage. comparison of loses of C between forests and lands utilised in agriculture is often impossible. Addition- ally, studies which provide estimates of CO emis- sions from roots on plantations established on tropical Introduction peats are sparse. Jauhiainen et al. (2012) estimated that autotrophic fluxes on an Acacia plantation on peat -2 -1 Tropical peatlands are estimated to occupy range between 115 and 630 mg CO m h consti- 441,025 km globally, with more than half of the tuting 9–26% of total CO emissions, which compares total area (247,778 km ) being located in South-East to findings from oil palm plantations in Indonesia Asia (Page et al. 2011a), and provide the largest long- where the autotrophic component was between 15 and term sink of terrestrial carbon (Page et al. 2011b). The 30% of total CO emissions (Dariah et al. 2014). In substantial amount of carbon (C) present in peatlands contrast, Melling et al. (2013) attributed 60% of total of the region has been sequestered over millennia. soil respiration to autotrophic respiration based on a Nevertheless, recent developments which lead to trenching experiment. Hergoualc’h and Verchot deforestation and drainage of wetlands, for instance (2014) estimate autotrophic emissions from oil palm for the purpose of establishment of plantations, may be planted on tropical peat to be around -1 -1 rapidly turning tropical peat environments into the 0.9 ± 2.7 Mg C ha year . world’s largest sources of carbon emissions (Hoijer It is possible that differences in autotrophic respi- et al. 2012; Tonks et al. 2017). The growing world ration among plantation are in part related to the age of demand for palm oil has driven the extensive conver- plantations. Indeed, Dariah et al. (2014) found com- sion of peat into agricultural plantations, with 3.1 parable heterotrophic respiration rates between plan- million ha of peatlands in the region drained for the tations of 6 and 15 years while net and autotropic CO establishment of plantations, primarily of oil palm and emissions were considerably higher in the more Acacia (Lo and Parish 2013). Peatlands are especially productive older plantation. Another uncertainty attractive as areas for plantation establishment due to regarding how land use type influences CO soil flux the capacity for water retention of organic soils and stems from how the lability of the peat material high nutrient release from decomposing drained peat impacts emissions. It is plausible that surface peat soils (Corley and Tinker 2003). However, since oil consisting of less decomposed organic matter is the palm trees do not grow well on waterlogged soil due to largest contributor to soil CO fluxes as deeper peat poor anchorage and anoxic conditions, the establish- may be more degraded and therefore produce less CO ment of oil palm plantation requires drainage of peat. due to the recalcitrant nature of the remaining This greatly increases the risk of high levels of organic material. Indeed, a relationship between CO emis- matter decomposition, as the presence of oxygen sions and peat functional organic chemistry has been enables the activity of aerobic microorganisms (Hus- shown from undisturbed tropical peatlands (Wright nain et al. 2014). et al. 2013). However, the variation in peat quality Total soil respiration (R ) consists of the auto- with depth and its role in CO emissions from drained s 2 trophic (root-derived; R ) and heterotrophic (non-root peatlands, including oil palm plantations, remains derived; R ) components. Heterotrophic respiration h unclear. involves only the microbial decomposition of soil In addition to plantation age and peat quality, the organic matter (SOM), whereas autotrophic CO flux from tropical peats can be influenced by a 123 Wetlands Ecol Manage (2018) 26:415–424 417 range of other environmental factors. For example, Selangor of c. 670 km . Within this, approximately Melling et al. (2005) found CO emissions under 48 km remains as peat swamp forest (albeit highly different land uses were regulated by different envi- disturbed). Average annual rainfall in the area is ronmental factors: relative humidity in secondary 2419 mm with the dry season normally occurring from forest, soil temperature for sago plantations, and size May to September (with rainfall dipping to c. of water-filled pore spaces for oil palm plantations. 100–150 mm per month) and, to a lesser extent, also CO flux was also influenced by long-term water December to February. The examined sites were a table depth on an Acacia plantation (Jauhiainnen et al. first-generation oil palm plantation, established in 2012). The association between peat temperature and 2000, replacing secondary forest and a second gener- heterotrophic respiration is driven by an exponential ation plantation, established in 2006 (original conver- increase in enzymatic activity in response to higher sion from secondary forest in 1978). Immediately temperatures up to c. 45 C (Luo and Zhou 2006). prior to plantation establishment, the forest would Waterlogged conditions of peatlands may limit CO have been cleared and ditches dug (to a depth of emissions by generating anaerobiosis which reduces approximately 1.5–2 m) to drain the peatland resulting peat oxygenation, while very dry conditions and water in a lower water table. These are then retained for the deficit may also restrain microbial respiration (Jauhi- plantation growth. The peat depth at the time of anien et al. 2005; Marwanto and Agus 2014). How- sampling ranged between 1.5 and 2.1 m. On both ever, to date neither peat temperature nor moisture plantations, four replicate sites were allocated for CO controls of CO emissions from oil palm plantations efflux measurements and six for soil sampling. Soil are well understood, particularly in the context of samples were taken at the four CO measurement sites in situ fluxes separated into autotropic and hetero- plus at two extra sites. In both plantation generations, trophic components of emissions (Couwenberg et al. oil palm trees were positioned in the standard planting 2010). configuration, in a triangular pattern with the distance Given the knowledge gaps around the impact of oil between tree trunks being approximately 9 m. Each palm plantations on C storage and losses, this study row of trees was arranged with frond piles between aims to determine the relative contribution and rows (where oil palm leaves are discarded) and open controls of autotrophic and heterotrophic respiration harvesting path walkways between trees. The under- in two oil palm plantations of different ages. This will storey surrounding frond piles consisted mostly of be achieved by answering the following specific ferns with less aboveground biomass in general at the research questions: (i) what is the relative contribution 2006 plantation as compared with the 2000 plantation. of autotrophic and heterotrophic respiration to net CO However, the sampling areas themselves, within the effluxes from an oil palm plantation on tropical peat? harvesting path locations had bare soil, with no (ii) How do peat C stocks, soil moisture and temper- understory vegetation. The distance between the two ature control heterotrophic and autotropic CO flux of plantations was approximately 1 km. tropical peatlands utilised as oil palm plantations? Measurement campaign Methods This study was conducted over a 5-month period in 2014, with soil samples taken in April and measure- Research sites ments of CO flux, soil temperature and moisture conducted during the dry season, in the months of The study was conducted on an oil palm plantation June, July and August, over the course of 2–3 days cultivated on a peatland located in South Selangor, each month. The soil pH was measured only once, in Peninsular Malaysia. The oil palm plantation from June or July. which samples were taken containing totalled 43 km and is within the vicinity of Kuala Lumpur Interna- Soil CO flux 0 00 0 00 tional airport (244 25.58 , 10140 29.08 ) and South Langat Forest Reserve. This plantation is situated on a Within each plantation, four replicate sites c. 50 m much larger peat soil area of mixed land use in South apart were selected at random. At each site, a palm tree 123 418 Wetlands Ecol Manage (2018) 26:415–424 Soil Organic Carbon measurement was selected at random. At each tree, seven collars were placed in a straight line at 0.5 m intervals away Six soil sampling points were randomly allocated at from the tree trunk, the first one being located 0.5 m and the last one 3.5 m away from the tree. Surface CO each plantation, each being within a 10 m radius from the collar transects. Soil samples were extracted with a measurements across the transect were made to quantify net soil CO fluxes (R ). Since the majority Russian peat corer (50 cm barrel length, 5.2 cm inner 2 s diameter, Eijkelkamp, the Netherlands) at 20 cm of oil palm root biomass is estimated to be limited to the zone within a 2 m radius to the tree trunk, the CO intervals down to 1 m. The samples were collected fluxes at the 3.5 m collar were assumed to be in air-tight plastic bags and placed in a refrigerator on predominately heterotrophic (R ) i.e. with negligible the day of sampling. The storage temperature was contribution of root respiration to the net soil CO between 3 and 6 C and the samples were kept for a efflux (Dariah et al. 2014). The assumption of no roots period of maximum 1 month. The samples were at the 3.5 m distance was tested by digging soil pits at subsequently oven-dried at 70 C to a constant weight and sieved through a 2 mm sieve. Since it was not the study sites. This verified that there were no oil palm roots at the 3.5 distance supporting the assump- possible to separate the dead and the living biomass in the peat, plant parts were not removed from the sieved tion of no autotrophic contribution from oil palm to soil fluxes at this distance. Furthermore, sampling samples, with the exception of large root fragments. Soil Organic Carbon (SOC) content was measured points were selected in areas with no understory vegetation to prevent roots from affecting autotrophic via loss on ignition (LOI). Around 4–10 g (depending respiration. The autotrophic CO emissions (R ) were on the sample) of dried soil was placed in a ceramic 2 a calculated by subtracting the flux measured at the crucible, weighed and put in the furnace set at 550 C 3.5 m collar from the soil respiration (R ) measured at for 4 h, upon which the sample weight was measured again. The obtained weights of oven-dried and burnt the distances closer to the trunk, following the approach used by Jauhianen et al. (2012)inan Acacia samples were thereafter used for estimation of SOM and SOC content according to the Eq. 1 (Farmer et al. plantation on peat soil. The CO fluxes were measured with a Li-Cor LI- 2014): 8100A. At sample locations, round plastic collars cut p ¼ M =M  100 ash ds ash from PVC pipes of the same diameter as the Li-Cor ð1Þ C ¼ðÞ 100  p =R org OM:C ash chamber were inserted (c. 4 cm deep) into the peat c. 24 h before measurements. The Li-Cor soil flux where M sample dry weight, M ash weight after ds ash chamber was placed onto the collars to collect the combustion, P sample ash content, C SOC ash org CO flux data. The distance from the peat surface to content (%), R conversion factor. OM:C the collar top was taken from inside the collar before The value of 1.878 was used as the R factor for OM:C each measurement and the corrections in the gas accurate estimation of SOC content in tropical peats as volume within the chamber were made accordingly. recommended by Farmer et al. (2014). One measurement per collar was made every month and each of these lasted 1 min and 30 s. Bulk density In parallel with each CO flux measurement, we monitored soil temperature, moisture and water Concurrently, peat dry bulk density (BD) was sampled table depth. Moisture and temperature were measured separately. The samples were collected using fabri- at a depth of around 5–8 cm immediately adjacent to cated aluminium soil tube samplers (3.5 cm radius and each collar with a Decagon 5TM moisture probe at the 4.5 cm height), with lid covers. Each sampler was pre- time when measurements of CO fluxes were taken. weighed to determine the weight without soil. For pH values were measured for each collar with an HI sampling, a soil pit of 100 cm depth was dug and 991001 pH probe (Hanna Instruments). Each mea- samples were taken from the pit wall wall every surement was taken in close proximity to a collar. The 20 cm. Soil in the sampler was trimmed to size then depth of the water table was obtained manually from closed with lid covers prior to transfer to the laboratory dipwells which were located at a distance no greater refrigerator. In the laboratory, fresh weight of samples than 10 m from the CO measurement points. 123 Wetlands Ecol Manage (2018) 26:415–424 419 (a) (b) (c) 500 10 01234 01234 01234 Distance (m) Distance (m) Distance (m) Fig. 1 a Net CO flux (R ), b Autotrophic (Ra) CO flux and c relative contribution of R to R along a transect from the palm trunk to 2 s 2 a s outside the canopy at the 2000 and 2006 plantations. Mean ± SE are shown; n = 84 Results was taken before oven-drying. The BD cores were placed in the oven at 105 C for 1–3 days until a constant weight was achieved. BD values were CO fluxes calculated following Eq. 2 (Dariah et al. 2014): At both the 2000 and the 2006 plantation R was Bulk density ðgcm Þ¼ m= V ð2Þ highest adjactent to the palm trunks with Rs being -2 -1 1754 ± SE 173 and 2274 ± SE 233 mg m h at where m mass of dry soil sample (g), V volume of the 2000 and 2006 plantations, respectively. Fluxes sample (cm ). decreased significantly with increasing distance from the tree trunk at both plantations but the decline was Statistical analysis and data presentation sharper at the 2006 plantation (distance 9 plantation interaction: F = 3.13, P \ 0.01; Fig. 1a). The All statistical analyses were performed in GenStat (6,167) decline in the R with distance was described by highly version 17. General Linear Models (GLMs) were used s significant exponential decay models (F = 16.09; to test if CO fluxes (Rs, Ra and the Ra/Rs ratio), pH, (3,13) P \ 0.001; Fig. 1a). The overall mean soil respiration soil temperature and soil moisture varied with distance (R ) at each of the2000 and 2006 plantations of was from the trunk, months and plantations of different -2 -1 1341 and 988 mg CO m h , respectively, when ages using plot as the block effect. Exponential decay 2 scaled to the relative area equating to the specific functions was used to model the decline in Rs, Ra and distances along the measurement transect. the Ra/Rs ratio with distance from the trunk. Soil As expected R declined away from the trunk respiration was scaled to the appropriate zone (i.e. a (F = 3.26, P \ 0.01; Fig. 1b) and in parallel areas associated with increasing distance from the (6,167) with R the decline was sharper at the more recently trunk) using the exponential decay functions. s, re-planted 2006 plantation and followed an exponen- Linear regression was used to assess environmental tial decay model (F = 16.60; P \ 0.001; conditions (soil temperature and water content, pH, (3,13) Fig. 1b). Autotrophic emissions adjacent to the palm water table level and SOC content) and was related to trunks were 845 ± SE 135 and 1558 ± SE autotrophic and heterotrophic CO emissions. The -2 -1 341 mg m h at the 2000 and 2006 plantations, relationship between the heterotrophic CO flux and respectively. The relative contribution of R to R was water table depth was tested using GLMs with the a s 50% at 0.5 m away from the trunk and declined water table depth as the explanatory variable. The data exponentially to 25% 2 m away from the trunk with no was visually examined in GenStat for adherence to the significant difference between the 2000 and 2006 normality assumption of GLMs. plantations (F = 5.12; P \ 0.05; Fig. 1c). The (3,13) -2 -1 mg CO m h % 420 Wetlands Ecol Manage (2018) 26:415–424 limited. At the 2000 plantation, which had higher CO emissions overall, there was no clear link between the respiration rates and soil moisture con- tent. The autotrophic flux did not depend on the level of soil moisture (F = 1.04, P = 0.32) (Fig. 4b). (1,20) The water table depth (WTD) was measured at four points on the 2000 plantation and at two points on the 2006 age class. At all measurement points, WTD was well below the peat surface and well below Malaysian recommended annual average maxima of -40 cm (Evers et al. 2017) during the entire measurement 2000 2006 period, varying between 70 and 120 cm in June and Planting Year August, which reflected the dry weather conditions that were present during these two months as well as Fig. 2 Heterotrophic CO fluxes at two oil palm plantations of the artificially managed drainage extent. The flux did different generations. Mean ± SE are shown; n = 24 not depend on the water table level (F = 0.83, (1,8) P = 0.390, r = 0.09). The water table was measured heterotrophic CO losses measured at 3.5 m distance -2 -1 from the trunk were 909 ± SE 136 mg m h at the in June and August and, consequently, the CO flux data that was used in this particular analysis came from 2000 first generation plantation and were higher than June and August only. WTD had no effect on either from the more recently replanted 2nd generation 2006 -2 -1 surface CO fluxes or peat moisture content of the site where R were 716 ± SE 201 mg m h but h 2 topsoil during the sampling period (F = 0.05, this difference was not statistically significant (1,8) (F P = 0.82). = 0.31, P = 0.60; Fig. 2). (1,23) Neither heterotrophic nor autotrophic respiration The mean soil heterotrophic respiration (Rh) across the measurement transect (F = 3.09, P = 0.08) was influenced by soil temperature (F = 2.75, (1,44) (2, 23) P = 0.11; F = 0.84, P = 0.37). There was no was lowest in August, the month with the lowest soil (1,20) temperatures (Fig. 3a–c), while R (F = 4.82, interaction between soil temperature and site (F (1,44)= a (2,167) 2.03, P = 0.161). Furthermore, there was no signifi- P \ 0.01) fluxes was lowest in July which was the cant relationship between pH and the spatial variation month with the lowest soil moisture content (Fig. 3a, in the heterotrophic CO emissions averaged by month b, d). (F = 0.23, P = 0.639) at either of the sites. (1, 12) Environmental controls of CO emissions Soil organic carbon content and C stock At the 2000 and 2006 plantations, soil moisture varied Bulk densities were highest at the peat surface apart significantly between months (F(2,165) = 40.81, P \ 0.001) and so did temperature from at the deepest layer in the 2006 plantation, which was collected from the base of the remaining peat (F(2,165) = 32.05, P\ 0.001) (Fig. 3b, d). The aver- age volumetric soil moisture content was similar layer (depth 9 plantation interaction: F = 4.31; (3,47) 3 -3 P \ 0.05; Fig. 5a). As expected SOC concentrations between the two plantations: 0.20 and 0.20 m m at the 2000 and 2006 plantations, respectively. Some of declined significantly with depth at both plantations but the decline was sharper in the second generation the variation in the peat moisture content between 2006 plantation (depth 9 plantation: F = 6.07; months may be explained by the fact that the August (3,47) P \ 0.05; Fig. 5b). Overall SOC concentrations were measurements, unlike those of June and July, were higher in the 2000 that the 2006 plantation at 50 and conducted following a rain event. A significant interaction between the soil moisture 37%, respectively. Total peat C stocks were -2 60 kg m (down to 1 m depth) and did not vary content and site (i.e. 2000 or 2006) (F = 4.47, (1,44) P = 0.04) (Fig. 4a) suggested that heterotrophic CO significantly among the two plantations (F = 0.68; P = 0.4; Fig. 5c). emissions at the 2006 plantation were moisture- (1,11) -2 -1 mg CO m h 2 Wetlands Ecol Manage (2018) 26:415–424 421 Fig. 3 Monthly 1500 (a) (c) heterotrophic and autotrophic CO fluxes at the a 2000 and b 2006 oil palm plantations. The heterotrophic flux 34 corresponds to CO fluxes measured at 3.5 m distance from the trunk. The autotrophic fluxes shown are means across the 0.5–3.0 m Rh measurement transect i.e. Ra 28 does not account for the 2000 exponential decay in fluxes with distance and should therefore not be used for comparisons to other sites. (b) (d) 1500 0.3 Monthly c peat temperature and d moisture data are shown for the 2000 and 2006 plantations. Mean ± SE are shown 0.2 Rh Ra 0 0.1 June July August June July August Month Month (a) (b) 0 0.1 0.2 0.3 0.4 00.1 0.2 0.3 0.4 -500 3 -3 Soil water content (m m ) -1000 3 -3 Soil water content (m m ) Fig. 4 Relationship between a heterotrophic and b autotrophic corresponds to CO fluxes measured at 3.5 m distance from the CO flux with soil water content at 2000 and 2006 plantations; trunk. The autotrophic fluxes shown are from 0.5 m distance significant regression lines are shown. The heterotrophic flux from the trunk Discussion higher range of what is reported in the literature for plantations on tropical peat (Jauhianen et al. 2012; The R from both plantations of 117 and 86 Mg CO Dariah et al. 2014; Husnain et al. 2014). Indeed, our R s 2 -1 -1 -2 -1 ha year for 2000 and 2006 respectively, are at the measured close to the trunks (c. 2000 mg m h ) -2 -1 CO flux (mg m h ) -1 -1 -2 -2 mg CO h mg CO h m m 2 3 -3 Moisture (m m ) o Temperature ( C) 422 Wetlands Ecol Manage (2018) 26:415–424 (a) (b) (c) 0.5 m distance 2000 80 3.5 m distance 100 0 2000 2006 0.0 0.1 0.2 0.3 0.4 10 20 30 40 50 60 70 Bulk density (g cm-3) SOC (%) Planting Year Fig. 5 a Soil organic carbon (SOC) content in the peat profile at respectively] n = for each variable. Mean ± SE are shown; the 2000 and 2006 oil palm plantations (0.5 and 3.5 m subsites) and b Carbon stock at the 2000 and 2006 oil palm plantations from depth profiles [0–40 (n = 6) and 60–100 (n = 9), (0.5 and 3.5 m sub-sites); n = 15 for each subsite represent some of the highest reported in the literature Tonks et al. (2017). However, this did not translate (Couwenberg et al. 2010). The high emissions are in into differences in C stocks between the two planta- part likely to be due to our measurements being from tions possibly due the higher bulk densities in the day time during the dry season with prevailing high second-generation 2006 plantation. The more dense temperatures. To enable comparison with other studies soil may be due to both mechanical compaction from we used our dry season measurement to calculate machinery (Melling et al. 2009) but may also be due to annual heterotrophic fluxes from our study sites, enhanced decomposition as higher bulk densities has -1 -1 which were 79 and 65 Mg CO ha year for the been found previously following conversion of peat 2000 and 2006 plantation respectively. This is on the swamp forest to oil palm plantations (Tonks et al. higher side of many values previously reported for oil 2017). -1 palm plantations on peat e.g. c. 35 Mg CO ha The high contribution of autotrophic respiration to -1 -1 -1 year (Dariah et al. 2014), 41 Mg CO ha year net CO effluxes; 24 and 72% adjacent to the trunk 2 2 -1 (Melling et al. 2007), 19.3 ± 16.6 Mg CO ha (0.5 m distance) at the 2000 and 2006 plantations, -1 -1 -1 year (Agus et al. 2010), 7 Mg CO ha year respectively, highlights that it is critical to account for (Melling et al. 2013). Our annual heterotrophic root respiration when estimating C losses from emissions factors are comparable with those of the peatlands (Fig. 1). This is particularly important when US Environment Protection Agency, which use an comparing plantations of different ages, as the relative -1 -1 emission factor of 95 Mg CO ha year , based on contribution of autotrophic CO fluxes to net emis- 2 2 Hooijer et al. (2012) subsidence assessments. How- sions varied considerably among the two plantations ever, care needs to be taken when interpreting the as well as spatially with distance from the trunk annual fluxes as we expect CO emissions to vary (Fig. 1; Dariah et al. 2014). The sharp decline with between the wet and the dry season. The CO flux distance from the trunk in the 2006 plantation is likely values reported in this study suggest a potential for due to a less extensive root system indicating a lower very high C loss from drained tropical peats during the overall contribution of autotrophic respiration to net dry period. This is particularly concerning given that emissions at the 2006 plantation. The higher auto- part of the climate projections for SE Asia is more trophic flux found close to the younger palms in the intense dry periods (IPCC 2014) which may further 2006 plantation (i.e. 0.5 m distance) was unexpected, increase CO emissions from drained peatlands. given that older oil palms have greater root biomass It is likely that the lower overall SOC (both at the (Jourdan and Rey 1997; Smith et al. 2012). We surface and through the peat profile) in the 2006 speculate that this might be linked to greater NPP and plantation was caused by long-term high heterotrophic more active root growth in young palm plants or C losses depleting the SOC (Figs. 2, 5b) in line with decomposition of old root material from the previous Depth (cm) -2 C stock (kg m ) Wetlands Ecol Manage (2018) 26:415–424 423 plantation cycle contributing to the near-palm emis- table depth would not a reliable predictor of CO sions. The autotropic respiration was not related to soil emissions during long periods of drought. moisture or temperature, even though the values of In conclusion, we have identified high hetero- both variables varied substantially between months. trophic CO losses from drained tropical peatlands This suggests that neither soil moisture nor high planted with oil palm. Such high emissions are likely temperature limited root respiration. to be sustained as long as the drained conditions are Moisture was a stronger driver of heterotrophic maintained. The low SOC in the second generation oil CO losses than temperature during the measurement palm plantation suggests that repetitive plantation period, however, only at the 2006 plantation. This is in cycles and associated soil modification has led to C line with findings from drained oil palm plantations in loss throughout the peat profile. Given the large C Indonesia (Jauhiainen et al. 2005; Marwanto and Agus deposits in tropical peatlands and the rapid conversion 2014). Within the range of moisture contents found at of tropical peatlands to oil palm plantations, these high the 2006 sites (around 20% volumetric moisture emissions and changed to C stocks suggests that oil content), greater soil water content increased CO palm plantations can act as hot spots of CO emissions. 2 2 emissions suggesting moisture limitation of decom- Acknowledgements We are grateful to the TROCARI position. This may, in part, explain why higher (Tropical Catchment Research Initiative) team and temperatures did not substantially increase emissions, specifically, Dr Rory Padfield, Siti Noor Fitriah Azizan, as in contrast to finding on Kalimantan, where peat Huynh Minh Nhat, Stephane´ Arul Mariampillai, Tan Jia Min with moisture contents of 70–80% responded strongly and Loo Yen Yi for their help in collecting water table depth values and assisting with other elements of data collection to higher temperatures (Jauhiainen et al. 2014). during the sampling period. Reviewed by Nick Girkin Although the average soil moisture content did not (University of Nottingham). vary between the two plantations, the short duration of sampling (2–3 days each month) does not represent Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http:// long-term moisture values, which are likely to be creativecommons.org/licenses/by/4.0/), which permits unre- influenced by the variations in canopy coverage and stricted use, distribution, and reproduction in any medium, evaporation rates between the old and the new tree provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Com- stands. mons license, and indicate if changes were made. The depth of the water table is considered to affect respiration rates via effects on the water content of the top soil where the SOC mineralisation rate is expected to be the highest (Hirano et al. 2009). In contrast, in References this study the water table depth did not impact on the surface peat moisture content or affect the rate of Agus F, Handayani E, van Noordwijk M, Idris K, Sabiham S heterotrophic respiration suggesting that the relation- (2010) Root respiration interferes with peat CO emission ship between the water table depth and the microbial measurement. In: 19th World Congress of soil science, soil solutions for a changing world, Brisbane, Australia respiration was not constant along the whole soil Chimner RA, Cooper DJ (2003) Influence of water table levels profile or was prevalent to a certain depth only, as has on CO emissions in a Colorado subalpine fen: an in situ previously been found in temperature and boreal microcosm study. Soil Biol Biochem 35:345–351 wetlands (Chimner and Cooper 2003;Ma¨kiranta et al. Corley RHV, Tinker PB (2003) The oil palm. Blackwell, Oxford Couwenberg J, Domain R, Joosten H (2010) Greenhouse gas 2009). However, over long time-scales, a relationship fluxes from tropical peatlands in south-east Asia. Glob between the water table depth and CO emissions is Change Biol 16:1715–1732 more likely to be present (Hooijer et al. 2012) and the Dariah A, Marwanto S, Agus F (2014) Root- and peat-based short duration of this measurement campaign might CO emissions from oil palm plantations. Mitig Adapt Strateg Glob Change 19:831–843 have prevented the appearance of a clear pattern Epron D (2009) Separating autotrophic and heterotrophic between the position of the water table and CO components of soil respiration: lessons learned from emissions. It is plausible that the disconnect between trenching and related root-exclusion experiments. In: heterotrophic CO emissions and the water table depth Kutsch WL, Bahn M, Heinemeyer A (eds) Soil carbon dynamics: an integrated methodology, pp. 157–168. shown here, reflects the strong water table draw-down Cambridge University Press, Cambridge occurring during the dry season. In this case, water 123 424 Wetlands Ecol Manage (2018) 26:415–424 Evers S, Yule CM, Padfield R, O’Reilly P, Varkkey H (2017) Luo Y, Zhou X (2006) Soil respiration and the environment. Keep wetlands wet: the myth of sustainable development Academic Press, London of tropical peatlands–implications for policies and man- Ma¨kiranta P, Laiho R, Fritze H, Hyto¨nen J, Laine J, Minkkinen agement. Glob Change Biol 23(2):534–549 K (2009) Indirect regulation of heterotrophic peat soil Farmer J, Matthews R, Smith P, Langan C, Hergoualc’H K, respiration by water level via microbial community struc- Verchot L, Smith JU (2014) Comparison of methods for ture and temperature sensitivity. Soil Biol Biochem quantifying soil carbon in tropical peats. Geoderma 41:695–703 214–215:177–183 Marwanto S, Agus F (2014) Is CO flux from oil palm planta- Hergoualc’h K, Verchot LV (2014) Greenhouse gas emission tions on peatland controlled by soil moisture and/or soil factors for land use and land-use change in Southeast Asian and air temperatures? Mitig Adapt Strateg Glob Change peatlands. Mitig Adapt Strateg Glob Change 19:789–807 19:809–819 Hirano T, Jauhiainen J, Inoue T, Takahashi H (2009) Controls Melling L, Hatano R, Goh KJ (2005) Soil CO flux from three on the carbon balance of tropical peatlands. Ecosystems ecosystems in tropical peatland of Sarawak, Malaysia. 12:873–887 Tellus 57B:1–11 Hooijer A, Page S, Jauhiainen J, Lee WA, Lu XX, Idris A, Melling L, Goh KJ, Beauvais C, Hatano R (2007) Carbon flow Anshari G (2012) Subsidence and carbon loss in drained and budget in a young mature oil palm agroecosystem on tropical peatlands. Biogeoscience 9:1053–1071 deep tropical peat. In: Rieley JO, Banks CJ, Radjagukguk B Husnain H, Wigena IGP, Dariah A, Marwanto S, Setyanto P, (ed) Proceedings of the international symposium and Agus F (2014) CO emissions from tropical drained peat in workshop on tropical peatland, Yogyakarta, Indonesia Sumatra, Indonesia. Mitig Adapt Strateg Glob Change Melling L, Chua K, Lim K (2009) Managing peat soils under oil 19:845–862 palm. http://tropicalpeat.sarawak.gov.my/modules/web/ IPCC, 2014: Summary for policymakers. In: Field CB, Barros pages.php?mod=download&id=Publication&menu_id= VR, Dokken DJ, Mach KJ, Mastrandrea MD, Bilir TE, 0&sub_id=111. Accessed 19 Sept 2017 Chatterjee M, Ebi KL, Estrada YO, Genova RC, Girma B, Melling L, Tan SY, Goh KJ, Hatano R (2013) Soil microbial and Kissel ES, Levy AN, MacCracken S, Mastrandrea PR, root respirations from three ecosystems in tropical peatland White LL (eds) Climate change 2014: impacts, adaptation, of Sarawak, Malaysia. J Oil Palm Res 25:44–57 and vulnerability. Part A: global and sectoral aspects. Page SE, Rieley JO, Banks HJ (2011a) Global and regional Contribution of Working Group II to the Fifth Assessment importance of the tropical peatland carbon pool. Glob Report of the Intergovernmental Panel on Climate Change. Change Biol 17:798–818 Cambridge University Press, Cambridge, United Kingdom Page SE, Morrison R, Malins C, Hooijer A, Rieley JO, Jauhi- and New York, NY, USA, pp 1–32 ainen J (2011b) Effects of peat surface greenhouse gas Jauhiainen J, Takahashi H, Heikkinen JE, Martikainen PJ, emissions from oil palm plantations in Southeast Asia. Vassanders H (2005) Carbon fluxes from a tropical peat White Paper Number 15. Indirect Effects of Biofuel Pro- swamp forest floor. Glob Change Biol 11:1788–1797 duction Series. International Council on Clean Trans- Jauhiainen J, Hooijer A, Page SE (2012) Carbon dioxide portation, Washington emissions from an Acacia plantation on peatland in Smith DR, Townsend TJ, Choy AWK, Hardy ICW, Sjo¨gersten S Sumatra, Indonesia. Biogeosciences 9:617–630 (2012) Short-term soil carbon sink potential of oil palm Jauhiainen J, Kerojoki O, Silvennoinen H, Suwido L, Vasander plantations. GCB Bioenerg 4(5):588–596 H (2014) Heterotrophic respiration in drained tropical peat Tonks AJ, Aplin P, Beriro DJ, Cooper H, Evers S, Vane CH, is greatly affected by temperature—a passive ecosystem Sjogersten S (2017) Impacts of conversion of tropical peat cooling experiment. Environ Res Lett 9:105013 swamp forest to oil palm plantation on peat organic Jourdan C, Rey H (1997) Architecture and development of the chemistry, physical properties and carbon stocks. Geo- oil-palm (Elaeis guineensis Jacq.) root system. Plant Soil derma 289:36–45 189:33–48 Wright EL, Black CR, Cheesman AW, Turner BL, Sjo¨gersten S Lo J, Parish F (2013) Peatlands and climate change in Southeast (2013) Impact of simulated changes in water table depth on Asia. ASEAN Peatland Forests Project and Sustainable ex situ decomposition of leaf litter from a neotropical Management of Peatland Forests Project, ASEAN Secre- peatland. Wetlands 33:217–226 tariat and Global Environment Centre, Jakarta http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Wetlands Ecology and Management Springer Journals

High heterotrophic CO2 emissions from a Malaysian oil palm plantations during dry-season

Free
10 pages
Loading next page...
 
/lp/springer_journal/high-heterotrophic-co2-emissions-from-a-malaysian-oil-palm-plantations-KvjqlF0AsH
Publisher
Springer Netherlands
Copyright
Copyright © 2017 by The Author(s)
Subject
Life Sciences; Freshwater & Marine Ecology; Conservation Biology/Ecology; Environmental Law/Policy/Ecojustice; Marine & Freshwater Sciences; Hydrology/Water Resources; Water Quality/Water Pollution
ISSN
0923-4861
eISSN
1572-9834
D.O.I.
10.1007/s11273-017-9583-6
Publisher site
See Article on Publisher Site

Abstract

Wetlands Ecol Manage (2018) 26:415–424 https://doi.org/10.1007/s11273-017-9583-6 ORIGINAL PAPER High heterotrophic CO emissions from a Malaysian oil palm plantations during dry-season . . . Magdalena Matysek Stephanie Evers Marshall Kana Samuel Sofie Sjogersten Received: 13 February 2017 / Accepted: 14 October 2017 / Published online: 1 December 2017 The Author(s) 2017. This article is an open access publication Abstract Tropical peatlands are currently being temperature and moisture at site and also accompanied rapidly cleared and drained for the establishment of by depth profiles assessing peat C and bulk density. oil palm plantations, which threatens their globally The soil respiration decreased exponentially with significant carbon sequestration capacity. Large-scale distance from the palm trunks with the sharpest land conversion of tropical peatlands is important in decline found for the plantation with the younger the context of greenhouse gas emission factors and palms with overall fluxes of 1341 and 988 mg CO -2 -1 sustainable land management. At present, quantifica- m h , respectively, at the 2000 and 2006 planta- tion of carbon dioxide losses from tropical peatlands is tions, respectively. The mean heterotrophic flux was -2 -1 limited by our understanding of the relative contribu- 909 ± SE 136 and 716 ± SE 201 mg m h at the tion of heterotrophic and autotrophic respiration to net 2000 and 2006 plantations, respectively. Autotrophic peat surface CO emissions. In this study we separated emissions adjacent to the palm trunks were 845 ± SE -2 -1 heterotrophic and autotrophic components of peat CO 135 and 1558 ± SE 341 mg m h at the 2000 and losses from two oil palm plantations (one established 2006 plantations, respectively. Heterotrophic CO flux in ‘2000’ and the other in 1978, then replanted in was positively related to peat soil moisture, but not -2 ‘2006’) using chamber-based emissions sampling temperature. Total peat C stocks were 60 kg m along a transect from the rooting to non-rooting zones (down to 1 m depth) and did not vary among on a peatland in Selangor, Peninsular Malaysia over plantations of different ages but SOC concentrations the course of 3 months (June–August, 2014). Collar declined significantly with depth at both plantations CO measurements were compared with soil M. Matysek  S. Evers  M. K. Samuel M. Matysek (&)  S. Sjogersten School of Biosciences, University of Nottingham, School of Biosciences, University of Nottingham, Collage Malaysia Campus, Jalan Broga, 43500 Semenyih, Road, Sutton Bonington, Selangor Darul Ehsan, Malaysia Loughborough LE12 5RE, UK e-mail: 0805090m@gmail.com S. Evers Tropical Catchment Research Initiative (TROCARI), M. Matysek Kuala Lumpur, Malaysia Department of Animal and Plant Sciences, University of Sheffield, Alfred Denny Building, Sheffield S102TN, UK M. K. Samuel Climate Change Programme, Malaysian Agricultural S. Evers Research and Development Institute (MARDI) Serdang, School of Natural Sciences and Psychology, Liverpool Selangor, Malaysia John Moores University, Liverpool L3 3AF, UK 123 416 Wetlands Ecol Manage (2018) 26:415–424 but the decline was sharper in the second generation respiration encompasses root growth and maintenance 2006 plantation. The CO flux values reported in this respiration of living roots, as well as emissions from study suggest a potential for very high carbon (C) loss mycorrhizal fungi (Epron 2009). A major limitation of from drained tropical peats during the dry season. This our ability to understand the consequences of land use is particularly concerning given that more intense dry change on decomposition processes and CO losses periods related to climate change are predicted for SE from tropical peatlands, including oil palm planta- Asia. Taken together, this study highlights the need for tions, is the lack of separation of autotrophic and careful management of tropical peatlands, and the heterotrophic respiration components in the majority vulnerability of their carbon storage capability under of studies (Couwenberg et al. 2010). Consequently, a conditions of drainage. comparison of loses of C between forests and lands utilised in agriculture is often impossible. Addition- ally, studies which provide estimates of CO emis- sions from roots on plantations established on tropical Introduction peats are sparse. Jauhiainen et al. (2012) estimated that autotrophic fluxes on an Acacia plantation on peat -2 -1 Tropical peatlands are estimated to occupy range between 115 and 630 mg CO m h consti- 441,025 km globally, with more than half of the tuting 9–26% of total CO emissions, which compares total area (247,778 km ) being located in South-East to findings from oil palm plantations in Indonesia Asia (Page et al. 2011a), and provide the largest long- where the autotrophic component was between 15 and term sink of terrestrial carbon (Page et al. 2011b). The 30% of total CO emissions (Dariah et al. 2014). In substantial amount of carbon (C) present in peatlands contrast, Melling et al. (2013) attributed 60% of total of the region has been sequestered over millennia. soil respiration to autotrophic respiration based on a Nevertheless, recent developments which lead to trenching experiment. Hergoualc’h and Verchot deforestation and drainage of wetlands, for instance (2014) estimate autotrophic emissions from oil palm for the purpose of establishment of plantations, may be planted on tropical peat to be around -1 -1 rapidly turning tropical peat environments into the 0.9 ± 2.7 Mg C ha year . world’s largest sources of carbon emissions (Hoijer It is possible that differences in autotrophic respi- et al. 2012; Tonks et al. 2017). The growing world ration among plantation are in part related to the age of demand for palm oil has driven the extensive conver- plantations. Indeed, Dariah et al. (2014) found com- sion of peat into agricultural plantations, with 3.1 parable heterotrophic respiration rates between plan- million ha of peatlands in the region drained for the tations of 6 and 15 years while net and autotropic CO establishment of plantations, primarily of oil palm and emissions were considerably higher in the more Acacia (Lo and Parish 2013). Peatlands are especially productive older plantation. Another uncertainty attractive as areas for plantation establishment due to regarding how land use type influences CO soil flux the capacity for water retention of organic soils and stems from how the lability of the peat material high nutrient release from decomposing drained peat impacts emissions. It is plausible that surface peat soils (Corley and Tinker 2003). However, since oil consisting of less decomposed organic matter is the palm trees do not grow well on waterlogged soil due to largest contributor to soil CO fluxes as deeper peat poor anchorage and anoxic conditions, the establish- may be more degraded and therefore produce less CO ment of oil palm plantation requires drainage of peat. due to the recalcitrant nature of the remaining This greatly increases the risk of high levels of organic material. Indeed, a relationship between CO emis- matter decomposition, as the presence of oxygen sions and peat functional organic chemistry has been enables the activity of aerobic microorganisms (Hus- shown from undisturbed tropical peatlands (Wright nain et al. 2014). et al. 2013). However, the variation in peat quality Total soil respiration (R ) consists of the auto- with depth and its role in CO emissions from drained s 2 trophic (root-derived; R ) and heterotrophic (non-root peatlands, including oil palm plantations, remains derived; R ) components. Heterotrophic respiration h unclear. involves only the microbial decomposition of soil In addition to plantation age and peat quality, the organic matter (SOM), whereas autotrophic CO flux from tropical peats can be influenced by a 123 Wetlands Ecol Manage (2018) 26:415–424 417 range of other environmental factors. For example, Selangor of c. 670 km . Within this, approximately Melling et al. (2005) found CO emissions under 48 km remains as peat swamp forest (albeit highly different land uses were regulated by different envi- disturbed). Average annual rainfall in the area is ronmental factors: relative humidity in secondary 2419 mm with the dry season normally occurring from forest, soil temperature for sago plantations, and size May to September (with rainfall dipping to c. of water-filled pore spaces for oil palm plantations. 100–150 mm per month) and, to a lesser extent, also CO flux was also influenced by long-term water December to February. The examined sites were a table depth on an Acacia plantation (Jauhiainnen et al. first-generation oil palm plantation, established in 2012). The association between peat temperature and 2000, replacing secondary forest and a second gener- heterotrophic respiration is driven by an exponential ation plantation, established in 2006 (original conver- increase in enzymatic activity in response to higher sion from secondary forest in 1978). Immediately temperatures up to c. 45 C (Luo and Zhou 2006). prior to plantation establishment, the forest would Waterlogged conditions of peatlands may limit CO have been cleared and ditches dug (to a depth of emissions by generating anaerobiosis which reduces approximately 1.5–2 m) to drain the peatland resulting peat oxygenation, while very dry conditions and water in a lower water table. These are then retained for the deficit may also restrain microbial respiration (Jauhi- plantation growth. The peat depth at the time of anien et al. 2005; Marwanto and Agus 2014). How- sampling ranged between 1.5 and 2.1 m. On both ever, to date neither peat temperature nor moisture plantations, four replicate sites were allocated for CO controls of CO emissions from oil palm plantations efflux measurements and six for soil sampling. Soil are well understood, particularly in the context of samples were taken at the four CO measurement sites in situ fluxes separated into autotropic and hetero- plus at two extra sites. In both plantation generations, trophic components of emissions (Couwenberg et al. oil palm trees were positioned in the standard planting 2010). configuration, in a triangular pattern with the distance Given the knowledge gaps around the impact of oil between tree trunks being approximately 9 m. Each palm plantations on C storage and losses, this study row of trees was arranged with frond piles between aims to determine the relative contribution and rows (where oil palm leaves are discarded) and open controls of autotrophic and heterotrophic respiration harvesting path walkways between trees. The under- in two oil palm plantations of different ages. This will storey surrounding frond piles consisted mostly of be achieved by answering the following specific ferns with less aboveground biomass in general at the research questions: (i) what is the relative contribution 2006 plantation as compared with the 2000 plantation. of autotrophic and heterotrophic respiration to net CO However, the sampling areas themselves, within the effluxes from an oil palm plantation on tropical peat? harvesting path locations had bare soil, with no (ii) How do peat C stocks, soil moisture and temper- understory vegetation. The distance between the two ature control heterotrophic and autotropic CO flux of plantations was approximately 1 km. tropical peatlands utilised as oil palm plantations? Measurement campaign Methods This study was conducted over a 5-month period in 2014, with soil samples taken in April and measure- Research sites ments of CO flux, soil temperature and moisture conducted during the dry season, in the months of The study was conducted on an oil palm plantation June, July and August, over the course of 2–3 days cultivated on a peatland located in South Selangor, each month. The soil pH was measured only once, in Peninsular Malaysia. The oil palm plantation from June or July. which samples were taken containing totalled 43 km and is within the vicinity of Kuala Lumpur Interna- Soil CO flux 0 00 0 00 tional airport (244 25.58 , 10140 29.08 ) and South Langat Forest Reserve. This plantation is situated on a Within each plantation, four replicate sites c. 50 m much larger peat soil area of mixed land use in South apart were selected at random. At each site, a palm tree 123 418 Wetlands Ecol Manage (2018) 26:415–424 Soil Organic Carbon measurement was selected at random. At each tree, seven collars were placed in a straight line at 0.5 m intervals away Six soil sampling points were randomly allocated at from the tree trunk, the first one being located 0.5 m and the last one 3.5 m away from the tree. Surface CO each plantation, each being within a 10 m radius from the collar transects. Soil samples were extracted with a measurements across the transect were made to quantify net soil CO fluxes (R ). Since the majority Russian peat corer (50 cm barrel length, 5.2 cm inner 2 s diameter, Eijkelkamp, the Netherlands) at 20 cm of oil palm root biomass is estimated to be limited to the zone within a 2 m radius to the tree trunk, the CO intervals down to 1 m. The samples were collected fluxes at the 3.5 m collar were assumed to be in air-tight plastic bags and placed in a refrigerator on predominately heterotrophic (R ) i.e. with negligible the day of sampling. The storage temperature was contribution of root respiration to the net soil CO between 3 and 6 C and the samples were kept for a efflux (Dariah et al. 2014). The assumption of no roots period of maximum 1 month. The samples were at the 3.5 m distance was tested by digging soil pits at subsequently oven-dried at 70 C to a constant weight and sieved through a 2 mm sieve. Since it was not the study sites. This verified that there were no oil palm roots at the 3.5 distance supporting the assump- possible to separate the dead and the living biomass in the peat, plant parts were not removed from the sieved tion of no autotrophic contribution from oil palm to soil fluxes at this distance. Furthermore, sampling samples, with the exception of large root fragments. Soil Organic Carbon (SOC) content was measured points were selected in areas with no understory vegetation to prevent roots from affecting autotrophic via loss on ignition (LOI). Around 4–10 g (depending respiration. The autotrophic CO emissions (R ) were on the sample) of dried soil was placed in a ceramic 2 a calculated by subtracting the flux measured at the crucible, weighed and put in the furnace set at 550 C 3.5 m collar from the soil respiration (R ) measured at for 4 h, upon which the sample weight was measured again. The obtained weights of oven-dried and burnt the distances closer to the trunk, following the approach used by Jauhianen et al. (2012)inan Acacia samples were thereafter used for estimation of SOM and SOC content according to the Eq. 1 (Farmer et al. plantation on peat soil. The CO fluxes were measured with a Li-Cor LI- 2014): 8100A. At sample locations, round plastic collars cut p ¼ M =M  100 ash ds ash from PVC pipes of the same diameter as the Li-Cor ð1Þ C ¼ðÞ 100  p =R org OM:C ash chamber were inserted (c. 4 cm deep) into the peat c. 24 h before measurements. The Li-Cor soil flux where M sample dry weight, M ash weight after ds ash chamber was placed onto the collars to collect the combustion, P sample ash content, C SOC ash org CO flux data. The distance from the peat surface to content (%), R conversion factor. OM:C the collar top was taken from inside the collar before The value of 1.878 was used as the R factor for OM:C each measurement and the corrections in the gas accurate estimation of SOC content in tropical peats as volume within the chamber were made accordingly. recommended by Farmer et al. (2014). One measurement per collar was made every month and each of these lasted 1 min and 30 s. Bulk density In parallel with each CO flux measurement, we monitored soil temperature, moisture and water Concurrently, peat dry bulk density (BD) was sampled table depth. Moisture and temperature were measured separately. The samples were collected using fabri- at a depth of around 5–8 cm immediately adjacent to cated aluminium soil tube samplers (3.5 cm radius and each collar with a Decagon 5TM moisture probe at the 4.5 cm height), with lid covers. Each sampler was pre- time when measurements of CO fluxes were taken. weighed to determine the weight without soil. For pH values were measured for each collar with an HI sampling, a soil pit of 100 cm depth was dug and 991001 pH probe (Hanna Instruments). Each mea- samples were taken from the pit wall wall every surement was taken in close proximity to a collar. The 20 cm. Soil in the sampler was trimmed to size then depth of the water table was obtained manually from closed with lid covers prior to transfer to the laboratory dipwells which were located at a distance no greater refrigerator. In the laboratory, fresh weight of samples than 10 m from the CO measurement points. 123 Wetlands Ecol Manage (2018) 26:415–424 419 (a) (b) (c) 500 10 01234 01234 01234 Distance (m) Distance (m) Distance (m) Fig. 1 a Net CO flux (R ), b Autotrophic (Ra) CO flux and c relative contribution of R to R along a transect from the palm trunk to 2 s 2 a s outside the canopy at the 2000 and 2006 plantations. Mean ± SE are shown; n = 84 Results was taken before oven-drying. The BD cores were placed in the oven at 105 C for 1–3 days until a constant weight was achieved. BD values were CO fluxes calculated following Eq. 2 (Dariah et al. 2014): At both the 2000 and the 2006 plantation R was Bulk density ðgcm Þ¼ m= V ð2Þ highest adjactent to the palm trunks with Rs being -2 -1 1754 ± SE 173 and 2274 ± SE 233 mg m h at where m mass of dry soil sample (g), V volume of the 2000 and 2006 plantations, respectively. Fluxes sample (cm ). decreased significantly with increasing distance from the tree trunk at both plantations but the decline was Statistical analysis and data presentation sharper at the 2006 plantation (distance 9 plantation interaction: F = 3.13, P \ 0.01; Fig. 1a). The All statistical analyses were performed in GenStat (6,167) decline in the R with distance was described by highly version 17. General Linear Models (GLMs) were used s significant exponential decay models (F = 16.09; to test if CO fluxes (Rs, Ra and the Ra/Rs ratio), pH, (3,13) P \ 0.001; Fig. 1a). The overall mean soil respiration soil temperature and soil moisture varied with distance (R ) at each of the2000 and 2006 plantations of was from the trunk, months and plantations of different -2 -1 1341 and 988 mg CO m h , respectively, when ages using plot as the block effect. Exponential decay 2 scaled to the relative area equating to the specific functions was used to model the decline in Rs, Ra and distances along the measurement transect. the Ra/Rs ratio with distance from the trunk. Soil As expected R declined away from the trunk respiration was scaled to the appropriate zone (i.e. a (F = 3.26, P \ 0.01; Fig. 1b) and in parallel areas associated with increasing distance from the (6,167) with R the decline was sharper at the more recently trunk) using the exponential decay functions. s, re-planted 2006 plantation and followed an exponen- Linear regression was used to assess environmental tial decay model (F = 16.60; P \ 0.001; conditions (soil temperature and water content, pH, (3,13) Fig. 1b). Autotrophic emissions adjacent to the palm water table level and SOC content) and was related to trunks were 845 ± SE 135 and 1558 ± SE autotrophic and heterotrophic CO emissions. The -2 -1 341 mg m h at the 2000 and 2006 plantations, relationship between the heterotrophic CO flux and respectively. The relative contribution of R to R was water table depth was tested using GLMs with the a s 50% at 0.5 m away from the trunk and declined water table depth as the explanatory variable. The data exponentially to 25% 2 m away from the trunk with no was visually examined in GenStat for adherence to the significant difference between the 2000 and 2006 normality assumption of GLMs. plantations (F = 5.12; P \ 0.05; Fig. 1c). The (3,13) -2 -1 mg CO m h % 420 Wetlands Ecol Manage (2018) 26:415–424 limited. At the 2000 plantation, which had higher CO emissions overall, there was no clear link between the respiration rates and soil moisture con- tent. The autotrophic flux did not depend on the level of soil moisture (F = 1.04, P = 0.32) (Fig. 4b). (1,20) The water table depth (WTD) was measured at four points on the 2000 plantation and at two points on the 2006 age class. At all measurement points, WTD was well below the peat surface and well below Malaysian recommended annual average maxima of -40 cm (Evers et al. 2017) during the entire measurement 2000 2006 period, varying between 70 and 120 cm in June and Planting Year August, which reflected the dry weather conditions that were present during these two months as well as Fig. 2 Heterotrophic CO fluxes at two oil palm plantations of the artificially managed drainage extent. The flux did different generations. Mean ± SE are shown; n = 24 not depend on the water table level (F = 0.83, (1,8) P = 0.390, r = 0.09). The water table was measured heterotrophic CO losses measured at 3.5 m distance -2 -1 from the trunk were 909 ± SE 136 mg m h at the in June and August and, consequently, the CO flux data that was used in this particular analysis came from 2000 first generation plantation and were higher than June and August only. WTD had no effect on either from the more recently replanted 2nd generation 2006 -2 -1 surface CO fluxes or peat moisture content of the site where R were 716 ± SE 201 mg m h but h 2 topsoil during the sampling period (F = 0.05, this difference was not statistically significant (1,8) (F P = 0.82). = 0.31, P = 0.60; Fig. 2). (1,23) Neither heterotrophic nor autotrophic respiration The mean soil heterotrophic respiration (Rh) across the measurement transect (F = 3.09, P = 0.08) was influenced by soil temperature (F = 2.75, (1,44) (2, 23) P = 0.11; F = 0.84, P = 0.37). There was no was lowest in August, the month with the lowest soil (1,20) temperatures (Fig. 3a–c), while R (F = 4.82, interaction between soil temperature and site (F (1,44)= a (2,167) 2.03, P = 0.161). Furthermore, there was no signifi- P \ 0.01) fluxes was lowest in July which was the cant relationship between pH and the spatial variation month with the lowest soil moisture content (Fig. 3a, in the heterotrophic CO emissions averaged by month b, d). (F = 0.23, P = 0.639) at either of the sites. (1, 12) Environmental controls of CO emissions Soil organic carbon content and C stock At the 2000 and 2006 plantations, soil moisture varied Bulk densities were highest at the peat surface apart significantly between months (F(2,165) = 40.81, P \ 0.001) and so did temperature from at the deepest layer in the 2006 plantation, which was collected from the base of the remaining peat (F(2,165) = 32.05, P\ 0.001) (Fig. 3b, d). The aver- age volumetric soil moisture content was similar layer (depth 9 plantation interaction: F = 4.31; (3,47) 3 -3 P \ 0.05; Fig. 5a). As expected SOC concentrations between the two plantations: 0.20 and 0.20 m m at the 2000 and 2006 plantations, respectively. Some of declined significantly with depth at both plantations but the decline was sharper in the second generation the variation in the peat moisture content between 2006 plantation (depth 9 plantation: F = 6.07; months may be explained by the fact that the August (3,47) P \ 0.05; Fig. 5b). Overall SOC concentrations were measurements, unlike those of June and July, were higher in the 2000 that the 2006 plantation at 50 and conducted following a rain event. A significant interaction between the soil moisture 37%, respectively. Total peat C stocks were -2 60 kg m (down to 1 m depth) and did not vary content and site (i.e. 2000 or 2006) (F = 4.47, (1,44) P = 0.04) (Fig. 4a) suggested that heterotrophic CO significantly among the two plantations (F = 0.68; P = 0.4; Fig. 5c). emissions at the 2006 plantation were moisture- (1,11) -2 -1 mg CO m h 2 Wetlands Ecol Manage (2018) 26:415–424 421 Fig. 3 Monthly 1500 (a) (c) heterotrophic and autotrophic CO fluxes at the a 2000 and b 2006 oil palm plantations. The heterotrophic flux 34 corresponds to CO fluxes measured at 3.5 m distance from the trunk. The autotrophic fluxes shown are means across the 0.5–3.0 m Rh measurement transect i.e. Ra 28 does not account for the 2000 exponential decay in fluxes with distance and should therefore not be used for comparisons to other sites. (b) (d) 1500 0.3 Monthly c peat temperature and d moisture data are shown for the 2000 and 2006 plantations. Mean ± SE are shown 0.2 Rh Ra 0 0.1 June July August June July August Month Month (a) (b) 0 0.1 0.2 0.3 0.4 00.1 0.2 0.3 0.4 -500 3 -3 Soil water content (m m ) -1000 3 -3 Soil water content (m m ) Fig. 4 Relationship between a heterotrophic and b autotrophic corresponds to CO fluxes measured at 3.5 m distance from the CO flux with soil water content at 2000 and 2006 plantations; trunk. The autotrophic fluxes shown are from 0.5 m distance significant regression lines are shown. The heterotrophic flux from the trunk Discussion higher range of what is reported in the literature for plantations on tropical peat (Jauhianen et al. 2012; The R from both plantations of 117 and 86 Mg CO Dariah et al. 2014; Husnain et al. 2014). Indeed, our R s 2 -1 -1 -2 -1 ha year for 2000 and 2006 respectively, are at the measured close to the trunks (c. 2000 mg m h ) -2 -1 CO flux (mg m h ) -1 -1 -2 -2 mg CO h mg CO h m m 2 3 -3 Moisture (m m ) o Temperature ( C) 422 Wetlands Ecol Manage (2018) 26:415–424 (a) (b) (c) 0.5 m distance 2000 80 3.5 m distance 100 0 2000 2006 0.0 0.1 0.2 0.3 0.4 10 20 30 40 50 60 70 Bulk density (g cm-3) SOC (%) Planting Year Fig. 5 a Soil organic carbon (SOC) content in the peat profile at respectively] n = for each variable. Mean ± SE are shown; the 2000 and 2006 oil palm plantations (0.5 and 3.5 m subsites) and b Carbon stock at the 2000 and 2006 oil palm plantations from depth profiles [0–40 (n = 6) and 60–100 (n = 9), (0.5 and 3.5 m sub-sites); n = 15 for each subsite represent some of the highest reported in the literature Tonks et al. (2017). However, this did not translate (Couwenberg et al. 2010). The high emissions are in into differences in C stocks between the two planta- part likely to be due to our measurements being from tions possibly due the higher bulk densities in the day time during the dry season with prevailing high second-generation 2006 plantation. The more dense temperatures. To enable comparison with other studies soil may be due to both mechanical compaction from we used our dry season measurement to calculate machinery (Melling et al. 2009) but may also be due to annual heterotrophic fluxes from our study sites, enhanced decomposition as higher bulk densities has -1 -1 which were 79 and 65 Mg CO ha year for the been found previously following conversion of peat 2000 and 2006 plantation respectively. This is on the swamp forest to oil palm plantations (Tonks et al. higher side of many values previously reported for oil 2017). -1 palm plantations on peat e.g. c. 35 Mg CO ha The high contribution of autotrophic respiration to -1 -1 -1 year (Dariah et al. 2014), 41 Mg CO ha year net CO effluxes; 24 and 72% adjacent to the trunk 2 2 -1 (Melling et al. 2007), 19.3 ± 16.6 Mg CO ha (0.5 m distance) at the 2000 and 2006 plantations, -1 -1 -1 year (Agus et al. 2010), 7 Mg CO ha year respectively, highlights that it is critical to account for (Melling et al. 2013). Our annual heterotrophic root respiration when estimating C losses from emissions factors are comparable with those of the peatlands (Fig. 1). This is particularly important when US Environment Protection Agency, which use an comparing plantations of different ages, as the relative -1 -1 emission factor of 95 Mg CO ha year , based on contribution of autotrophic CO fluxes to net emis- 2 2 Hooijer et al. (2012) subsidence assessments. How- sions varied considerably among the two plantations ever, care needs to be taken when interpreting the as well as spatially with distance from the trunk annual fluxes as we expect CO emissions to vary (Fig. 1; Dariah et al. 2014). The sharp decline with between the wet and the dry season. The CO flux distance from the trunk in the 2006 plantation is likely values reported in this study suggest a potential for due to a less extensive root system indicating a lower very high C loss from drained tropical peats during the overall contribution of autotrophic respiration to net dry period. This is particularly concerning given that emissions at the 2006 plantation. The higher auto- part of the climate projections for SE Asia is more trophic flux found close to the younger palms in the intense dry periods (IPCC 2014) which may further 2006 plantation (i.e. 0.5 m distance) was unexpected, increase CO emissions from drained peatlands. given that older oil palms have greater root biomass It is likely that the lower overall SOC (both at the (Jourdan and Rey 1997; Smith et al. 2012). We surface and through the peat profile) in the 2006 speculate that this might be linked to greater NPP and plantation was caused by long-term high heterotrophic more active root growth in young palm plants or C losses depleting the SOC (Figs. 2, 5b) in line with decomposition of old root material from the previous Depth (cm) -2 C stock (kg m ) Wetlands Ecol Manage (2018) 26:415–424 423 plantation cycle contributing to the near-palm emis- table depth would not a reliable predictor of CO sions. The autotropic respiration was not related to soil emissions during long periods of drought. moisture or temperature, even though the values of In conclusion, we have identified high hetero- both variables varied substantially between months. trophic CO losses from drained tropical peatlands This suggests that neither soil moisture nor high planted with oil palm. Such high emissions are likely temperature limited root respiration. to be sustained as long as the drained conditions are Moisture was a stronger driver of heterotrophic maintained. The low SOC in the second generation oil CO losses than temperature during the measurement palm plantation suggests that repetitive plantation period, however, only at the 2006 plantation. This is in cycles and associated soil modification has led to C line with findings from drained oil palm plantations in loss throughout the peat profile. Given the large C Indonesia (Jauhiainen et al. 2005; Marwanto and Agus deposits in tropical peatlands and the rapid conversion 2014). Within the range of moisture contents found at of tropical peatlands to oil palm plantations, these high the 2006 sites (around 20% volumetric moisture emissions and changed to C stocks suggests that oil content), greater soil water content increased CO palm plantations can act as hot spots of CO emissions. 2 2 emissions suggesting moisture limitation of decom- Acknowledgements We are grateful to the TROCARI position. This may, in part, explain why higher (Tropical Catchment Research Initiative) team and temperatures did not substantially increase emissions, specifically, Dr Rory Padfield, Siti Noor Fitriah Azizan, as in contrast to finding on Kalimantan, where peat Huynh Minh Nhat, Stephane´ Arul Mariampillai, Tan Jia Min with moisture contents of 70–80% responded strongly and Loo Yen Yi for their help in collecting water table depth values and assisting with other elements of data collection to higher temperatures (Jauhiainen et al. 2014). during the sampling period. Reviewed by Nick Girkin Although the average soil moisture content did not (University of Nottingham). vary between the two plantations, the short duration of sampling (2–3 days each month) does not represent Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http:// long-term moisture values, which are likely to be creativecommons.org/licenses/by/4.0/), which permits unre- influenced by the variations in canopy coverage and stricted use, distribution, and reproduction in any medium, evaporation rates between the old and the new tree provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Com- stands. mons license, and indicate if changes were made. The depth of the water table is considered to affect respiration rates via effects on the water content of the top soil where the SOC mineralisation rate is expected to be the highest (Hirano et al. 2009). In contrast, in References this study the water table depth did not impact on the surface peat moisture content or affect the rate of Agus F, Handayani E, van Noordwijk M, Idris K, Sabiham S heterotrophic respiration suggesting that the relation- (2010) Root respiration interferes with peat CO emission ship between the water table depth and the microbial measurement. In: 19th World Congress of soil science, soil solutions for a changing world, Brisbane, Australia respiration was not constant along the whole soil Chimner RA, Cooper DJ (2003) Influence of water table levels profile or was prevalent to a certain depth only, as has on CO emissions in a Colorado subalpine fen: an in situ previously been found in temperature and boreal microcosm study. Soil Biol Biochem 35:345–351 wetlands (Chimner and Cooper 2003;Ma¨kiranta et al. Corley RHV, Tinker PB (2003) The oil palm. Blackwell, Oxford Couwenberg J, Domain R, Joosten H (2010) Greenhouse gas 2009). However, over long time-scales, a relationship fluxes from tropical peatlands in south-east Asia. Glob between the water table depth and CO emissions is Change Biol 16:1715–1732 more likely to be present (Hooijer et al. 2012) and the Dariah A, Marwanto S, Agus F (2014) Root- and peat-based short duration of this measurement campaign might CO emissions from oil palm plantations. Mitig Adapt Strateg Glob Change 19:831–843 have prevented the appearance of a clear pattern Epron D (2009) Separating autotrophic and heterotrophic between the position of the water table and CO components of soil respiration: lessons learned from emissions. It is plausible that the disconnect between trenching and related root-exclusion experiments. In: heterotrophic CO emissions and the water table depth Kutsch WL, Bahn M, Heinemeyer A (eds) Soil carbon dynamics: an integrated methodology, pp. 157–168. shown here, reflects the strong water table draw-down Cambridge University Press, Cambridge occurring during the dry season. In this case, water 123 424 Wetlands Ecol Manage (2018) 26:415–424 Evers S, Yule CM, Padfield R, O’Reilly P, Varkkey H (2017) Luo Y, Zhou X (2006) Soil respiration and the environment. Keep wetlands wet: the myth of sustainable development Academic Press, London of tropical peatlands–implications for policies and man- Ma¨kiranta P, Laiho R, Fritze H, Hyto¨nen J, Laine J, Minkkinen agement. Glob Change Biol 23(2):534–549 K (2009) Indirect regulation of heterotrophic peat soil Farmer J, Matthews R, Smith P, Langan C, Hergoualc’H K, respiration by water level via microbial community struc- Verchot L, Smith JU (2014) Comparison of methods for ture and temperature sensitivity. Soil Biol Biochem quantifying soil carbon in tropical peats. Geoderma 41:695–703 214–215:177–183 Marwanto S, Agus F (2014) Is CO flux from oil palm planta- Hergoualc’h K, Verchot LV (2014) Greenhouse gas emission tions on peatland controlled by soil moisture and/or soil factors for land use and land-use change in Southeast Asian and air temperatures? Mitig Adapt Strateg Glob Change peatlands. Mitig Adapt Strateg Glob Change 19:789–807 19:809–819 Hirano T, Jauhiainen J, Inoue T, Takahashi H (2009) Controls Melling L, Hatano R, Goh KJ (2005) Soil CO flux from three on the carbon balance of tropical peatlands. Ecosystems ecosystems in tropical peatland of Sarawak, Malaysia. 12:873–887 Tellus 57B:1–11 Hooijer A, Page S, Jauhiainen J, Lee WA, Lu XX, Idris A, Melling L, Goh KJ, Beauvais C, Hatano R (2007) Carbon flow Anshari G (2012) Subsidence and carbon loss in drained and budget in a young mature oil palm agroecosystem on tropical peatlands. Biogeoscience 9:1053–1071 deep tropical peat. In: Rieley JO, Banks CJ, Radjagukguk B Husnain H, Wigena IGP, Dariah A, Marwanto S, Setyanto P, (ed) Proceedings of the international symposium and Agus F (2014) CO emissions from tropical drained peat in workshop on tropical peatland, Yogyakarta, Indonesia Sumatra, Indonesia. Mitig Adapt Strateg Glob Change Melling L, Chua K, Lim K (2009) Managing peat soils under oil 19:845–862 palm. http://tropicalpeat.sarawak.gov.my/modules/web/ IPCC, 2014: Summary for policymakers. In: Field CB, Barros pages.php?mod=download&id=Publication&menu_id= VR, Dokken DJ, Mach KJ, Mastrandrea MD, Bilir TE, 0&sub_id=111. Accessed 19 Sept 2017 Chatterjee M, Ebi KL, Estrada YO, Genova RC, Girma B, Melling L, Tan SY, Goh KJ, Hatano R (2013) Soil microbial and Kissel ES, Levy AN, MacCracken S, Mastrandrea PR, root respirations from three ecosystems in tropical peatland White LL (eds) Climate change 2014: impacts, adaptation, of Sarawak, Malaysia. J Oil Palm Res 25:44–57 and vulnerability. Part A: global and sectoral aspects. Page SE, Rieley JO, Banks HJ (2011a) Global and regional Contribution of Working Group II to the Fifth Assessment importance of the tropical peatland carbon pool. Glob Report of the Intergovernmental Panel on Climate Change. Change Biol 17:798–818 Cambridge University Press, Cambridge, United Kingdom Page SE, Morrison R, Malins C, Hooijer A, Rieley JO, Jauhi- and New York, NY, USA, pp 1–32 ainen J (2011b) Effects of peat surface greenhouse gas Jauhiainen J, Takahashi H, Heikkinen JE, Martikainen PJ, emissions from oil palm plantations in Southeast Asia. Vassanders H (2005) Carbon fluxes from a tropical peat White Paper Number 15. Indirect Effects of Biofuel Pro- swamp forest floor. Glob Change Biol 11:1788–1797 duction Series. International Council on Clean Trans- Jauhiainen J, Hooijer A, Page SE (2012) Carbon dioxide portation, Washington emissions from an Acacia plantation on peatland in Smith DR, Townsend TJ, Choy AWK, Hardy ICW, Sjo¨gersten S Sumatra, Indonesia. Biogeosciences 9:617–630 (2012) Short-term soil carbon sink potential of oil palm Jauhiainen J, Kerojoki O, Silvennoinen H, Suwido L, Vasander plantations. GCB Bioenerg 4(5):588–596 H (2014) Heterotrophic respiration in drained tropical peat Tonks AJ, Aplin P, Beriro DJ, Cooper H, Evers S, Vane CH, is greatly affected by temperature—a passive ecosystem Sjogersten S (2017) Impacts of conversion of tropical peat cooling experiment. Environ Res Lett 9:105013 swamp forest to oil palm plantation on peat organic Jourdan C, Rey H (1997) Architecture and development of the chemistry, physical properties and carbon stocks. Geo- oil-palm (Elaeis guineensis Jacq.) root system. Plant Soil derma 289:36–45 189:33–48 Wright EL, Black CR, Cheesman AW, Turner BL, Sjo¨gersten S Lo J, Parish F (2013) Peatlands and climate change in Southeast (2013) Impact of simulated changes in water table depth on Asia. ASEAN Peatland Forests Project and Sustainable ex situ decomposition of leaf litter from a neotropical Management of Peatland Forests Project, ASEAN Secre- peatland. Wetlands 33:217–226 tariat and Global Environment Centre, Jakarta

Journal

Wetlands Ecology and ManagementSpringer Journals

Published: Dec 1, 2017

References

You’re reading a free preview. Subscribe to read the entire article.


DeepDyve is your
personal research library

It’s your single place to instantly
discover and read the research
that matters to you.

Enjoy affordable access to
over 18 million articles from more than
15,000 peer-reviewed journals.

All for just $49/month

Explore the DeepDyve Library

Search

Query the DeepDyve database, plus search all of PubMed and Google Scholar seamlessly

Organize

Save any article or search result from DeepDyve, PubMed, and Google Scholar... all in one place.

Access

Get unlimited, online access to over 18 million full-text articles from more than 15,000 scientific journals.

Your journals are on DeepDyve

Read from thousands of the leading scholarly journals from SpringerNature, Elsevier, Wiley-Blackwell, Oxford University Press and more.

All the latest content is available, no embargo periods.

See the journals in your area

DeepDyve

Freelancer

DeepDyve

Pro

Price

FREE

$49/month
$360/year

Save searches from
Google Scholar,
PubMed

Create lists to
organize your research

Export lists, citations

Read DeepDyve articles

Abstract access only

Unlimited access to over
18 million full-text articles

Print

20 pages / month

PDF Discount

20% off