Ecosystem Services and Biodiversity of Rubber Plantationsã¢â‚¬â€a Systematic Review

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Open Access

Peer-reviewed

Research Article

Ecosystem Services and Biodiversity in a Rapidly Transforming Mural in Northern Borneo

• Nicolas Labrière,
• Yves Laumonier,
• Bruno Locatelli,
• Ghislain Vieilledent,
• Marion Comptour

x

• Published: October 14, 2015
• https://doi.org/10.1371/journal.pone.0140423

Figures

Abstract

Because industrial agronomics keeps expanding in Southeast Asia at the expense of natural forests and traditional swidden systems, comparing biodiversity and ecosystem services in the traditional forest–swidden agriculture system vs. monocultures is needed to guide decision making on land-use planning. Focusing on tree variety, soil erosion control, and climate change mitigation through carbon storage, we surveyed vegetation and monitored soil loss in various land-utilize areas in a northern Bornean agricultural landscape shaped by swidden agriculture, rubber tapping, and logging, where various levels and types of disturbance have created a fine mosaic of vegetation from food crop fields to natural forest. Tree species diversity and ecosystem service production were highest in natural forests. Logged-over forests produced services similar to those of natural forests. Country uses related to the swidden agronomics system largely outperformed oil palm or rubber monocultures in terms of tree species multifariousness and service production. Natural and logged-over forests should be maintained or managed equally integral parts of the swidden system, and landscape multifunctionality should exist sustained. Considering natural forests host a unique diversity of trees and produce high levels of ecosystem services, targeting carbon stock protection, e.chiliad. through financial mechanisms such as Reducing Emissions from Deforestation and Forest Degradation (REDD+), volition synergistically provide benefits for biodiversity and a wide range of other services. However, the manner such mechanisms could benefit communities must be carefully evaluated to counter the high opportunity toll of conversion to monocultures that might generate greater income, but would be detrimental to the production of multiple ecosystem services.

Citation: Labrière Northward, Laumonier Y, Locatelli B, Vieilledent Thousand, Comptour M (2015) Ecosystem Services and Biodiversity in a Speedily Transforming Landscape in Northern Borneo. PLoS 1 ten(10): e0140423. https://doi.org/10.1371/journal.pone.0140423

Editor: Edward Webb, National Academy of Singapore, SINGAPORE

Received: February 19, 2015; Accepted: September 26, 2015; Published: October 14, 2015

Copyright: © 2015 Labrière et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted utilize, distribution, and reproduction in any medium, provided the original author and source are credited

Information Availability: All relevant data are inside the paper and its Supporting Information files.

Funding: This research received financial back up from CoLUPSIA (EU Financed Project - DCI), AusAid (Agreement 63650 with Center for International Forestry Research), CIRAD, CRP-FTA (CGIAR Research Program on Forests, Trees, and Agroforestry) and ABIES (Ecole Doctorale Agriculture, Alimentation, Biologie, Environnements et Santé).

Competing interests: The authors take alleged that no competing interests exist.

Introduction

Desperate land-use transformations have occurred in the tropical forest landscapes of Southeast Asia in the by decades, leading to the disappearance of natural forests and the replacement of traditional land-use systems with monoculture plantations. On the island of Borneo, the lowland rainforests are at the crossroads of multiple and divergent interests. While these rainforests are hotspots of biological diversity with a loftier charge per unit of endemism and hold important carbon stocks, they are also a major source of valuable timber, and are situated on lands that are very suitable for conversion to oil palm or other big industrial plantations [i–3].

Since the late 1960s, logging has affected most of the lowland forests [4]. Post-obit the boom era that lasted roughly until the 2000s, large areas of logged-over forest were left unmanaged. Although several studies demonstrated the of import role that these forests play in supporting biodiversity and maintaining multiple ecosystem services [v–8], they were slowly depleted through illegal logging and finally converted to oil palm plantations [9]. The detrimental effect of such large-scale land clearing on biodiversity and other services is an accepted premise [ten–13]. At the same fourth dimension, as the extent of industrial agricultural areas keeps increasing, the part of traditional agronomical systems (swidden i.eastward., slash-and-burn down and rotational fallow farming, and smallholder agroforestry systems) vs. alternative agricultural systems in providing goods and services has received much attention [14–17]. To date, however, there has been footling consensus about their part in supporting biodiversity and producing ecosystem services.

Since negative correlations commonly exist between goods and services (due east.k. [18,19]), homo-modified land-use areas would not be expected to produce levels of services like to those of natural forests. Yet, in Sumatra, under depression management intensity weather, mature safety gardens were plant to have a plant species richness like to that of nearby natural or secondary forests and to store substantial amounts of carbon in aboveground biomass [15,20]. Swidden fallows were also shown to reduce soil erosion and contribute to soil nutrient cycling to levels similar to those constitute in natural forests [21–23]. In contrast, studies in West Kalimantan found that an increasing number of shifting tillage cycles naturally led to a subtract in tree species richness and important tree limerick changes [24]. Some argue that such human-modified country use volition non allow whatsoever long-term conservation goal to be fulfilled, partly because maintaining tree diversity might hinder rubber garden productivity [25]. Overall, despite electric current debates about the capacity of man-modified landscapes to protect biodiversity and support ecosystem services, these landscapes are getting increasing attention for their contribution to biodiversity conservation in the global context of vanishing natural habitats [26,27].

Research gaps concerning the event of state-utilise changes on the ecosystem services produced by swidden systems have been identified through a systematic review currently nether progress that aims to bring unbiased evidence to the debate [28]. While need for food and goods is growing worldwide, and biodiversity and services are being lost [29], such data is essential to building sound land management strategies and guiding decision making on land-use planning.

In this study, we address the following question: What level of biodiversity and ecosystem services are found in the different land uses related to the traditional forest–swidden agriculture organisation? We conducted a instance study from a northern Bornean agronomical landscape where nosotros quantitatively estimated the contribution of diverse land uses to: (1) climate change mitigation through carbon storage in live aboveground biomass and topsoil, (2) tree species diversity, and (3) soil erosion control. The two services were chosen because of their relevance for multiple beneficiaries at different scales (local to regional for soil erosion control, and global for climate change mitigation). Tree species diverseness, which we did not consider every bit an ecosystem service, was chosen because of its cross-cut and cross-scale nature, every bit it jointly influences the delivery of goods (e.m. food, raw material, fruit, and timber for local people) and services (e.g. water regulation at the regional scale) [30].

Materials and Methods

Ideals statement

This study strictly complied with Indonesian laws. Authorizations to carry out enquiry activities were obtained from advisable sources both at national (Ministry of Forestry and Ministry of State for Research and Technology) and local level (Head of Kapuas Hulu regency). Permissions from local owners to work on their lands were obtained prior to any action. Sending soil and herbarium samples from the field site to laboratories in Java for further analysis was done after authorization blessing. We did non collect endangered plants or any animals.

Report site and plot selection

Field work was carried out in the surroundings of Keluin (ane°08'57" N, 112°15'37" E), a village located in the district of Batang Lupar, Kapuas Hulu regency, Westward Borneo province, Indonesia (Fig 1). This village is located most a river flowing directly toward the Danau Sentarum National Park, a very complex hydrological system that regulates the hydrological regime of the Kapuas River (the longest river in Kalimantan, which supplies water to the Due west Borneo capital letter urban center of Pontianak) [31]. Altitude in the study area ranges from 50 to 450 yard higher up body of water level [32]. Soils accept adult over sedimentary rocks [33] and vest mostly to the Ultisols order [34]. Mean annual rainfall is 3300 mm (WorldClim data, interpolated judge for the 1950−2000 period with a 30 arc-second resolution [35]). The study area has a tropical rainforest climate with a drier period from June to August, but monthly rainfall is highly variable throughout the yr.

Fig 1. Plot location within the study area.

The study area is located on the isle of Borneo (top left panel), in the Indonesian province of West Borneo, in the regency of Kapuas Hulu (bottom left panel). In the main console, plot location and broad state-employ types (LUT) are displayed forth with sometime logging roads (red) and rivers (blue). The blackness square indicates the location of the village.

https://doi.org/10.1371/periodical.pone.0140423.g001

This site was chosen because of the diversity of land uses representative of northern Bornean traditional agricultural systems that were establish inside a limited perimeter (ca. two km W–East by 5 km Northward–Southward). Traditionally, the primary crop, rice, is cultivated along with other annual crops (such as cassava, maize, etc.) in swiddens from either primary or secondary forest immigration earlier the plot is abandoned afterwards 1−2 years of tillage. Rubber seedlings and saplings, which are planted in some crop fields during the tillage phase or simply subsequently plot abandonment, somewhen lead to condom-based secondary forests (as well called "jungle rubber" gardens) as a result of plant succession. By and current uses of state by the local community (swidden agriculture arrangement mixed with safe gardens) and past logging activities take created a mosaic of vegetation reflecting diverse disturbance types, ages and intensities in the Keluin surface area.

We divers 7 land-utilise types in the written report area: (1) food ingather fields where the master crop, rice (Oryza sativa L.), is planted after using the slash-and-burn down method on the initial vegetation (natural wood or secondary vegetation), (2) young secondary regrowth following field abandonment after crops have been cultivated for ane or two years, (three) old secondary regrowth forests further into the process of vegetation succession following field abandonment, (4) immature prophylactic gardens resulting from the planting of prophylactic seedlings and saplings (Hevea brasiliensis (Willd. ex A.Juss.) Müll.Arg.) in some young fallows, (5) old rubber gardens with complex stand construction, (half-dozen) logged-over woods that was selectively logged from 1997 to 2005, and (vii) natural forest with very little human disturbance.

Two distinct sets of vegetation and erosion plots were established based on a multi-stratified sampling first across land-use type and 2d across disturbance age for stands regenerating after slash and burn (see S1 Tabular array). For the purpose of this study, young and erstwhile stands (≤ xx years and > twenty years following disturbance, respectively) were distinguished from each other because stand construction becomes more than complex xx years later on initial disturbance [36,37]. Plots for the vegetation sampling were scattered across the study area to embrace the variability of topographical situation (ridge, gradient, valley lesser) and slope steepness (from flat to very steep) nowadays in this depression-elevation hilly mural. Plots for the erosion protocol were also scattered across the study area, with the additional constraint of having a homogenous slope of ca. 40% (ca. 22°). Nosotros chose relatively steep slopes (compared with the standard gradient, i.e. nine%, of a typical erosion monitoring method such every bit the Wischmeier plot [38]), every bit erosion hardly occurs on not-blank slopes of low steepness in the study region [22].

Vegetation plots: estimating aboveground carbon stocks and tree species diversity

For immature and one-time stands in both secondary regrowth areas and rubber gardens, 12 plots each of twenty × 20 m were randomly selected (for a total surveyed area of 0.48 ha for each of the four country-use types) to capture the variability of vegetation structure and composition within each state-use type (Fig ane and S1 Table). For natural and logged-over forests, we surveyed a total surface area ca. twice as large as that of secondary regrowth areas and condom gardens to encompass an even much higher variability of vegetation structure and composition: five rectangular plots each of 20 × 100 1000 (longer dimension along the contour line; i ha each forest blazon) were selected. Plots were contiguous but staggered down the slope for natural forest (all plumbing equipment in a 100 × 400 m area). For logged-over forest, they were scattered on either side of a former logging road built on a ridge, ca. 20 m downslope from the road.

All trees with diameter at breast meridian (DBH, i.3 m) ≥ 5 cm were measured, tagged and mapped, and their height estimated, following standard procedures [39]. Leaf samples were collected at least in one case for each colloquial proper noun (consistently given past the same group of highly knowledgeable local people using the Iban linguistic communication) for both immature and sometime secondary regrowth areas and rubber gardens, and for every individual tree for natural and logged-over forests. Identification of the herbarium vouchers were carried out at the Herbarium Bogoriense in Bogor, Republic of indonesia.

We used three different indices to characterize tree species multifariousness at the plot level: species richness, Berger–Parker index, and Fisher'due south α. Species richness is the simplest measure of species diversity merely does not have into business relationship community evenness. Conversely, the Berger–Parker index (defined as the inverse of the proportion of individuals of the most mutual species in the customs) depends just on evenness, and is sensitive to the authorization of a few species. Fisher's α is mathematically unrelated to the first 2 indices, is relatively independent of sample size, and is insensitive to the presence of rare species [40].

Nosotros used the generic Chave et al. allometric equation for tropical forests [41] to calculate tree dry out biomass. Forest specific gravity, a multiplier included in the aforementioned equation, was obtained from the Global Wood Density Database [42,43]. When species were non found in the database, the genus-level boilerplate wood density was used instead. Aboveground biomass (AGB) was split into four fractions (according to tree DBH; 5–10 cm, ten–30 cm, 30–50 cm, and > 50 cm) of which relative proportions were computed with no other belittling purpose than to identify the lowest and highest contributing fractions to total aboveground carbon stocks. Those were calculated from biomass values past application of the standard 0.47 conversion cistron [44].

Because of differences in sampling design (inter-plot distance ranged from twenty to 4650 m), we could not employ tree diversity values aggregated over the full surveyed area (0.48 ha each for secondary regrowth areas and rubber gardens, 1 ha each for natural and logged-over woods) to compare the unlike land-use types (see S1 Fig). Instead, we computed private values–for tree diversity and aboveground carbon–for each 20 × twenty thou plot (12 plots each for young and old secondary regrowth areas and prophylactic gardens, and 25 each for natural and logged-over forests; 98 plots in full) and used resulting hateful values to characterize each land-apply type. All details about individual plot coordinates, stand historic period (whenever relevant) and indicator–aboveground carbon and tree diverseness–values can exist found in S2 Table.

Erosion plots: soil loss monitoring and topsoil carbon stock estimation

Silt fences (made from a nonwoven polyester geotextile) were used to measure hillslope erosion. Following guidelines from Robichaud and Brown [45], 4-meter-wide fences were gear up across the slope, and heavy logs were positioned xv thousand upslope from the fences to form the upper boundaries of laterally unbounded plots of ca. 60 chiliad² contributing areas. Fences from 35 plots in full (five replicates for each of the seven land-use types) were cleaned monthly during xv continuous months (from June 2012 to September 2013), and the nerveless textile was stale, sieved (with a ane mm sieve) and the weight of the resulting fine mineral fraction was recorded. Composite soil samples from 4 sampling points per plot (close to each plot corner) were taken for topsoils (0−20 cm). Stale samples (drying temperature T = 105°C) were analyzed for carbon content (Walkley and Black method, [46]). In addition, for each plot, one sample of topsoil (using a 100 cm³ ring) was taken at mid-slope and dry bulk density (in g cm^–3) was measured. Topsoil carbon stocks were then calculated using carbon content and dry majority density. All details most individual plot coordinates, stand age (whenever relevant) and indicator–topsoil carbon and annual soil loss–values can be found in S3 Table.

Statistical analysis

All statistical analyses were done using R 3.1.ii [47]. Analyses were done on original values in case of normal data distribution and log_x-transformed values if transformation led to normal distributions. For each of the six indicators we studied (aboveground carbon, topsoil carbon, annual soil loss, tree species richness, Fisher'due south α and Berger-Parker index), we tested for spatial autocorrelation on both initial values and residuals of a linear model against land-utilize blazon using Moran's I. In case residuals were still spatially correlated, we used the Lagrange Multiplier diagnostics for spatial dependence to determine the structure of the appropriate spatial regression model (i.e., spatial error model that accounts for error term correlation vs. spatial lag model that accounts for non-independence between observations; [48]) using various functions from the spdep packet [49,50]. Nosotros tested for differences (at p < 0.01) in indicator values depending on land-use type using analysis of variance (ANOVA) followed past Tukey'south honest pregnant departure (HSD) test on either (1) uncorrected values in case indicators or linear model residuals were not-spatially autocorrelated (which was the instance for topsoil carbon, almanac soil loss and Berger-Parker index), or (2) values corrected from spatial auto-correlation (past subtracting the "point" term originating from spatial regression to the uncorrected value; [48]). Values of all statistical tests can be institute in S4 Table.

A nonmetric multidimensional scaling (NMDS) analysis was performed to illustrate plot similarity in terms of tree species composition (using the metaMDS function; see [51]). NMDS analysis is an ordination technique aiming at iteratively collapsing multidimensional information (in this example, plot species composition) into an optimal—lower—number of dimensions while conserving the rank lodge of distances [52]. The closer the points in the initial and resulting spaces, the more similar are the tree species compositions of the respective plots. Using Spearman's rank-order correlation, nosotros tested for correlations betwixt plot distance in the field and in the NMDS plot to assess to what extent spatial autocorrelation influenced results from the NMDS assay.

Results

Tree species diversity and limerick

The three species multifariousness indices were highest in natural forests (Fig 2). However, differences in mean species richness and hateful Fisher'southward α between natural and logged-over forests were not significant. Only Berger–Parker index values (exclusively dependent on community evenness) were significantly different between these two land-use types. Similarly, natural and logged-over forests had ca. lx% more species than practice quondam secondary regrowth forests (next most species-rich state-use blazon).

Fig 2. Tree species diversity indices depending on state-use blazon: (a) species richness; (b) Fischer's α; (c) Berger–Parker index.

Indices were computed for each 20 × twenty chiliad plot before being averaged by country-use type (over 25 plots for logged-over and natural forest, and 12 otherwise). Mean values with the same letter are not significantly different (Tukey'south HSD test on uncorrected values in case no spatial autocorrelation was detected and corrected values otherwise, p < 0.01).

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Older stands (for safe gardens and secondary regrowth forest) consistently showed college index values compared with young ones, but the divergence was only significant for mean Fisher's α. For similar time intervals since terminal disturbance, all the diverseness indices were consistently higher in secondary regrowth areas compared with rubber gardens, but the difference was not significant.

In the two dimensions of the NMDS plot (Fig 3), tree species composition was markedly different in natural forest plots compared with other plots. Logged-over forests had the nigh like tree species composition to natural forests. Tree species composition was highly variable among secondary regrowth areas and rubber gardens (both young and one-time). We found a moderate positive correlation between plot distance in the field and in the NMDS plot (Pearson's r = 0.58; p < 0.001). Even though signal clustering for logged-over and natural wood might therefore outcome in role from the sampling design (spatial autocorrelation), a conscientious inspection of the species present in the different land-use types (see S5 Table) strongly supports our finding that natural forest species are highly specific and dissimilar to all other land-utilise types.

Carbon storage

Aboveground carbon stock levels were significantly higher in natural forests than in any other country-use types (Fig 4). Unsurprisingly, the lowest values were constitute in young stands (rubber gardens or secondary regrowth areas). Even old safety gardens, erstwhile secondary regrowth forests, and logged-over forests had aboveground carbon stocks at levels one-half of those of natural forests.

Fig 4. Mean carbon stocks (+ i SD) in topsoil (0–20 cm) and aboveground biomass.

Means were computed over 12 to 25 replicates per land-use type for aboveground biomass, and over 5 replicates per land-use type for topsoil. Aboveground biomass (AGB) was split into four fractions according to tree diameter at breast tiptop (Ø). Hateful values with the same letter (lowercase for aboveground biomass, uppercase for topsoil) are not significantly different (Tukey's HSD test on uncorrected values in case no spatial autocorrelation was detected and corrected values otherwise, p < 0.01).

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For all types of state utilise, the highest proportions of aboveground carbon were contained in trees with DBH = x−30 cm, while the lowest non-zippo proportions were contained in trees with DBH = 5−10 cm. Yet, for recently disturbed stands such as those in young secondary regrowth areas, small-scale trees (those with DBH = 5−ten cm) could represent up to ca. 25% of aboveground carbon.

Although natural forests stored on average twice as much carbon in topsoils as other land-utilise types, significant differences were observed just between natural forests and secondary regrowth areas (both immature and former) or old prophylactic gardens due to loftier variability within land-use types (for logged-over and natural forests, especially).

Relationship between aboveground carbon stocks and species richness

The greater the aboveground carbon stocks, the greater the species richness in all country-use types, with the noticeable exception of natural forests for which the relationship is negative (cf. regression lines; Fig 5). Almost all plots with high tree multifariousness (richness college than median) and low carbon (aboveground carbon stock below median) belonged to logged-over forests. The vast majority of young secondary regrowth areas and rubber garden plots had low multifariousness and depression carbon. In contrast, all (but one corresponding to a tree-fall gap) natural forest plots showed high diversity and high carbon.

Fig five. Species richness against aboveground carbon stocks.

Each dot (98 in total) represents a 20 × xx g plot. Horizontal and vertical dashed lines represent median values of species richness (n = 25) and carbon stocks in aboveground biomass (68 Mg C ha-ane), respectively. Regression lines (along with standard mistake) are computed independently for each country-employ type. A 2nd-order regression model (best-fit significant model selected amidst polynomial models with degrees 0 to iii) over the whole information fix is also displayed (in black).

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Soil erosion

Almanac soil loss values ranged from 0.8 to 2.2 grand m^–2 yr^–one, with individual plot values varying from 0.5 to ii.seven chiliad grand^-ii yr^-i (run into S3 Tabular array). Annual soil loss was significantly lower in natural forests and young safe gardens compared with food crop fields (Fig half dozen). Other differences in annual soil loss between land-utilise types were not meaning.

Fig vi. Mean almanac soil loss (+ 1 SD) depending on land-utilize type.

Information are averaged over the monitoring period (June 2012 to September 2013) and over the different replicates for each land-use type. Values from three replicates (one in young secondary regrowth area, one in young rubber garden, one in logged-over wood) were discarded because they were abnormally loftier (> 2 times mean value of the corresponding land-use type). Mean values with the same letter of the alphabet are non significantly different (Tukey'south HSD exam on uncorrected values in case no spatial autocorrelation was detected and corrected values otherwise, p < 0.01).

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Discussion

Service production is highest in natural forest

As expected, service product was highest in natural forests (Fig 7). Natural wood plots conspicuously had high levels of both aboveground carbon stocks and tree species richness (summit right corner, Fig v), even though lower tree species richness was observed for the highest values of aboveground carbon stocks. This negative trend might be explained in light of Connell's intermediate disturbance hypothesis [53]. According to this hypothesis, an intermediate level of disturbance is required for a given tree community to reach maximum species richness [53]. Natural wood succession will lead to the competitive exclusion of early on- and mid-successional species, therefore reducing overall species variety. Our results corroborate this hypothesis because aboveground carbon stocks were positively correlated to disturbance historic period [54].

Fig 7. Spider chart of normalized service indicators for different land-use types.

Indicators are normalized and so that the minimum possible value of an indicator is at the center of the radial plot and the maximum observed values are on the outer circles (for the service of soil erosion command, the indicator is the changed of the measured soil loss).Service indicators: Ct = carbon stocks in topsoil; Cb = carbon stocks in aboveground biomass; Sr = tree species richness; Fi = Fisher's α; Bp = Berger–Parker alphabetize; Ec = soil erosion control.

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Aboveground carbon stocks in human-modified land-utilise types did not achieve half those of natural forests. Logged-over forests, agroforests and secondary regrowth areas had topsoil carbon stocks xl–60% lower than those of natural forests. This contrasts with results from Kessler et al. who found no significant reduction in soil carbon stocks betwixt natural forests and cocoa agroforests in Sulawesi, Republic of indonesia [55]. This might in part exist due to the fact that cocoa agroforests in their study region are obtained through gradual thinning of the natural wood with minimum bear upon on the root system [55], while transitions related to practices in our study area (logging, slash and burn down) are more precipitous and therefore potentially more than agonizing for topsoil.

Regarding soil erosion command, fifty-fifty if soil loss was everyman in natural forests and differed significantly between some pairs of land-apply types, low accented values of annual soil loss (2−three orders of magnitude lower than the tolerable soil erosion rate [56]) propose that the service of soil erosion control is delivered equally long equally soils are protected by vegetation cover, as exemplified in a review for the boiling tropics [57]. However, it cannot be asserted that soil erosion is consistently negligible across the landscape and throughout fourth dimension. Nosotros did not monitor soil loss on blank soil elements created by logging activities (e.1000. dirt roads, landslides) or related to safety tapping (e.g. walking tracks) that are known to contribute to erosion at the landscape scale unduly compared to their geographically restricted areas [58,59]. Nor did we monitor soil loss immediately later a major disturbance (east.g. burning or opening of logging tracks). Since extreme rainfall events that occur while soil is temporarily bare can pb to dramatic soil loss, soil loss monitoring before, during and after disturbance is required to follow soil erosion control during land-use modify [sixty].

Our results on tree species multifariousness show that some areas of human-modified land-use types host high tree species richness (eastward.g. logged-over forests and old secondary regrowth forest). This has already been shown for various taxa and is a widely accepted phenomenon [6,8,54,61]. However, we too show that the tree species composition of natural forest is highly specific (cf. Fig 3), which strengthens the exclamation that "primary forests are irreplaceable for sustaining tropical biodiversity" due to habitat restrictions of some highly sensitive or specialist species to such natural habitats [62,63].

Overall, in our report site, natural forests produce the highest levels of services across the mural and this would lend support to land management strategies that promote their strict protection [64]. Schemes and fiscal mechanisms in this surface area that conserve one of these services (e.g. carbon with REDD+, a fiscal mechanism aiming at Reducing Emissions from Deforestation and Woods Degradation) would synergistically benefit the others, therefore increasing the effectiveness of natural forest protection. But correlations between services depend on the spatial resolution and the scope of a study [65–67]. Therefore, more primary data are needed for inferring that mechanisms targeting carbon conservation would necessarily maximize benefits for biodiversity and other ecosystem services at the regional scale.

Logged-over forests and swidden agriculture organization outperform monocultures in terms of service production

In addition to the demand to preserve natural forests, another challenge is to maximize service product in homo-modified land-utilise areas. With the noticeable exception of tree species richness and tree species composition, our data did not testify significant differences in service product between logged-over forests, old safe gardens and old secondary regrowth forests. Tree species richness is high in logged-over forests (one plot tin simultaneously host a mixture of old growth and secondary species), only in such forests, aboveground carbon stocks are low. In contrast, aboveground carbon stocks can be large in some old safe gardens and secondary regrowth forests, merely tree species richness is low. Beyond the diversity of products from these land-use types, there is a complementarity in services produced by such human being-modified landscapes. Despite continuous changes in country use and management, the diversification of human activities—farming, rubber tapping, and logging—ensures the sustained commitment of multiple services.

As anticipated, comparing our results with those in the literature emphasized that a mosaic of state uses produces far more services than do safety or oil palm monocultures: biodiversity is greater [13], erosion is lower (particularly when plantations are prepare on steep slopes), and aboveground carbon stocks are more than twice as peachy [68].

Our results support the finding that logged-over forests in the study area are better than monocultures in terms of biodiversity conservation and ecosystem service production. Hopefully, the strong case made by this study and many others (east.g. [5,8]) will somewhen raise awareness among determination-makers and land-use planners that logged-over forests are non just worth beingness converted only should be sustainably managed.

Is the swidden organisation in Keluin close to a sustainability threshold?

We establish that carbon storage and tree diversity increased forth a successional recovery of the forest later initial clearance: levels of service production were lowest in food crop fields, intermediate in young safe gardens and secondary regrowth areas, and highest in old safety gardens and secondary regrowth forests. More than striking was no trend for carbon storage in topsoil and the slow recovery of different ecosystem services, either in old rubber gardens or secondary regrowth forests. Mean time since terminal disturbance for our old secondary regrowth forest plots was 47 years, and yet species richness was still significantly lower than for natural forests. Similarly, we constitute depression similarity in tree species composition between old secondary regrowth forest and natural forest plots.

From a meta-analysis of the recovery of plant biodiversity and carbon stocks in secondary forests, 50 years are plenty for species richness to reach natural forest levels, but with only a very low proportion of native forest species (hateful value: 26%), fifty-fifty in old stands [54]. The aboveground carbon stocks we institute in onetime secondary regrowth forests (ca. half those of natural forests) are consistent with the literature only lay in the lower part of the range compiled past the meta-analysis that reports aboveground carbon stock of 50–70% pre-disturbance levels after ca. 50 years of forest recovery [54]. Onetime rubber gardens also showed lower values of aboveground carbon stocks than those institute in the literature [69].

Nosotros found topsoil carbon stocks for nutrient crop fields to be half those of natural forest. Our results are consequent with those of a meta-analysis that also showed that soil carbon stocks will somewhen fully recover as croplands are immune to revert to secondary forests [seventy]. Another report estimated that 40−50 years are needed for secondary forest soil carbon stocks to accomplish pre-disturbance levels [71]. Despite the mean time since concluding disturbance (42 years) being inside this range, topsoil carbon in onetime secondary regrowth forests was far beneath the pre-disturbance levels in our study site.

One written report that was also carried out in West Kalimantan institute that an increasing number of cycles of cultivation and forest regrowth did non pb to total phosphorus decline, simply had detrimental consequences for aboveground carbon sequestration [72,73]. The capacity of soils to recover carbon content later disturbances might also be reduced in plots where numerous rotations have already been done. The whole swidden agriculture arrangement is sustainable if the condition that sufficient fourth dimension is allowed for soil and vegetation to recover is met. Soil impoverishment related to reduction in rotation length is a serious threat likely to jeopardize the production of goods and services in the long-term from the traditional swidden system in the Keluin area.

Conclusion

In such a speedily transforming traditional rural landscape in northern Bornean, natural forests host highly unique tree species diversity, have the everyman erosion rate, and store significantly more carbon (in aboveground biomass and topsoil) than do whatsoever other country-use type. Logged-over forests provide services similar to natural forest, except for soil erosion control, which is jeopardized past the presence of the remaining decaying route network that leads to soil loss at the landscape level.

All country uses related to the swidden agriculture organization largely outperform oil palm or rubber monocultures in terms of tree diversity, carbon storage, and soil erosion control. Natural and logged-over forests should be maintained or managed as an integral part of the swidden organization, and landscape multifunctionality should be sustained every bit a safety net against the toll volatility of traded goods (e.k. safety, palm oil, timber, tengkawang oil), upon which the economy of monocrop systems is much more dependent.

Considering of the congruence of services in natural forest, protection of their carbon stocks, for example through financial mechanisms such equally REDD+, will synergistically do good biodiversity and a broad range of other services provided to communities in this area. However, how such mechanisms could benefit communities must exist advisedly evaluated to counter the loftier opportunity cost of conversion to monocultures; these may generate greater income, but may also be more detrimental to the production of multiple ecosystem services.

Ecosystem service recovery fourth dimension following initial slash-and-burn practices on the vegetation is longer in the written report area than has been reported in the literature for similar study situations. As rotation length appears to be a key factor in the sustainability of swidden systems, it is critical to understand the socio-cultural and economic drivers of the reduction in rotation length and the potential feedback of this reduction on social–ecological systems. In the rapidly transforming socio-environmental context of this region, questions remain about the long-term persistence of the swidden agriculture system.

Supporting Information

S1 Fig. Individual-based rarefaction curves for every land-use type.

Rarefaction level was the number of individuals surveyed in erstwhile condom gardens (n = 449). Twelve plots (0.48 ha in full) were surveyed for fallows and condom gardens (both young and old), and 25 plots (one ha in total) for logged-over and natural forest.

https://doi.org/10.1371/journal.pone.0140423.s001

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S1 Table. Sampling blueprint for vegetation and erosion plots.

No vegetation plot was selected in food crop fields under the assumption that tree diverseness and aboveground carbon would be nothing. The beginning plot size dimension is the dimension forth the slope.

https://doi.org/10.1371/journal.pone.0140423.s002

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S2 Table. Vegetation plot features.

Longitude and latitude of each plot are provided in decimal degrees (WSG84 datum). Plot mean diameter at chest tiptop (DBH), height, forest specific gravity (WSG) and aboveground carbon (AGC) are besides provided.

https://doi.org/ten.1371/journal.pone.0140423.s003

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S3 Table. Erosion plot features.

Longitude and latitude of each plot are provided in decimal degrees (WSG84 datum). Plot annual soil loss (ASL) and topsoil carbon (TSC) are also provided. ASL values in gray-tinted cells were discarded for analyses.

https://doi.org/10.1371/periodical.pone.0140423.s004

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S4 Tabular array. Statistical analyses on ecosystem service and tree variety indicators.

We used original indicator values when the distribution was normal and log₁₀-transformed values otherwise. The vegetation set did not include food crop field plots under the assumption that tree diversity and aboveground carbon would be null. Depicted values are either examination statistics (for Moran's I, Lagrange Multiplier and the selected model) or model coefficients, and are presented along with information on statistical significance. For the Berger-Parker index, despite some spatial car-correlation, the spatial dependence coefficient of the spatial fault model was non meaning. We therefore used a regular linear model and acknowledge that results for this indicator might be slightly biased due to spatial auto-correlation.

https://doi.org/10.1371/periodical.pone.0140423.s005

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S5 Table. Species surveyed in each land-use blazon.

Information from plots under the same state-employ type (12 for young and erstwhile rubber gardens and fallows and 25 for logged-over and natural forests) were pooled together. IUCN conservation status is provided for each species (CR = Critically Endangered; EN = Endangered; VU = Vulnerable; LR/cd = Lower Take a chance: Conservation Dependent; LR/nt = Lower Risk: Near Threatened; DD = Data Deficient; LC or LR/lc = Least Concern). In order to be conservative, any species identified to the genus level only (e.chiliad. Aglaia sp.3) or absent from the IUCN Red List was given a "LC" status.

https://doi.org/10.1371/journal.pone.0140423.s006

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Acknowledgments

We thank all the villagers from Keluin for their hospitality, availability, and precious help in data collection. We are peculiarly grateful to Bapak Lasa, Bapak Bandan and Bapak Tinggi for sharing their thorough knowledge on plant denomination and use. We sincerely acknowledge Bapak Engkamat for his unfailing help and support in carrying out field work. Nosotros deeply thank Imam Basuki for his advices on soil erosion monitoring and aid in the field in setting erosion plots. We express gratitude to Bapak Ismail Rachman from the Herbarium Bogoriense for voucher identification. We acknowledge Ervan Rutishauser for his advice on statistical analysis. We are too grateful to Mike Lawes and 2 anonymous reviewers for their insightful comments and suggestions on before versions of the manuscript.

Writer Contributions

Conceived and designed the experiments: NL YL MC. Performed the experiments: NL YL MC. Analyzed the data: NL BL. Contributed reagents/materials/analysis tools: NL YL MC. Wrote the paper: NL YL BL GV MC.

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