Biodiversity conservation values of fragmented communally reserved forests, managed by indigenous people, in a human-modified landscape in Borneo
Biodiversity conservation values of fragmented communally reserved forests, managed by indigenous people, in a human- modified landscape in Borneo
Yayoi Takeuchi 0 1 2
Ryoji Soda 0 2
Bibian Diway 0 2
Tinjan ak. Kuda 0 2
Michiko Nakagawa 0 2
Hidetoshi Nagamasu 0 2
Tohru Nakashizuka 0 2
0 a Current address: International Tropical Timber Organization, Forest Department HQ, Wisma Sumber Alam , Petra Jaya, Kuching, Sarawak , Malaysia ¤b Current address: Research Institute for Humanity and Nature , Kamigamo-Motoyama, Kyoto , Japan
1 Center for Environmental Biology and Ecosystem Studies, National Institute for Environmental Studies , Onogawa, Tsukuba , Japan , 2 Faculty of Literature and Human Sciences, Osaka City University , Sugimoto, Sumiyoshi, Osaka , Japan , 3 Botanical Research Centre Semenggoh, Sarawak Forestry Corporation , Kuching, Sarawak , Malaysia , 4 Graduate School of Bioagricultural Sciences, Nagoya University , Nagoya , Japan , 5 The Kyoto University Museum, Kyoto University , Sakyo-ku, Kyoto , Japan , 6 Graduate School of Life Sciences, Tohoku University , Sendai , Japan
2 Editor: RunGuo Zang, Chinese Academy of Forestry , CHINA
Data Availability Statement: All relevant data are
within the paper and its Supporting Information
vation target into all CRFs.
Biodiversity has been declining because of forest loss and degradation by human developments
and activities [
], particularly in the tropical regions [2±5]. Globally, much attention is paid to
conservation strategies that integrate traditional indigenous practice, as observed in Article 8
(j) of the Convention of Biological Diversity [
]. It has been acknowledged that traditional and
local knowledge and practices contribute to biodiversity conservation [7±10]. In Asia,
traditional forest management systems can be commonly found, such as ªculturally protected
forestsº in China [
], ªcommunity forestsº in Nepal [
], and ªsacred forest groovesº in India
]. These forests provide essential ecosystem services, such as drinking water, area for graves,
recreation, hunting, plant gathering, and ritual/spiritual use, to local people. However, these
traditional uses and customs are threatened because of urbanization and development [
Thus, conservation strategies that incorporate traditional practice can function as a safety net
to minimize the loss of traditional knowledge and practice in the region as well as biodiversity.
In rural areas in Borneo, extensive logging started since the 1970s, and most forests have been
logged at least once. In the current landscape, forested areas have transformed into plantations
for oil palm and acacia. Only small patches of forest remain that the local indigenous Iban
communities deliberately preserve within their area of shifting cultivation [
]. We define this
traditionally managed forest as communally reserved forests (CRFs), which are customarily reserved
forests at a community level for cultural and practical use (i.e., provisioning and cultural service).
A CRF is called a ªpulauº in Iban language, which literally means ªisland,º because CRFs are
unevenly distributed and surrounded by fallow or secondary forests. It was from these reserves
that villagers obtained various kinds of natural resources, such as wood for construction of
houses and boats, and canes [
]. CRFs are generally supposed to be untouched timber sources,
with few trees having been harvested from most CRFs [
], except for an emergency such as
fire. Therefore, they can have a primary forest-based biodiversity and function as reservoirs of
biodiversity in the region.
However, in the current landscape, CRFs are fragmented and isolated from other
primary forests. Forest fragmentation leads to a decline in local and regional diversity,
particularly the loss of rare and endangered species, because of edge and isolation effects [17±19]
and a subsequent homogenization of the species composition [
]. To demonstrate that
CRFs are adequate targets for regional biodiversity conservation, both 1) alpha diversity of
each CRF, including the existence of rare species, and 2) beta diversity, which is a key
component of regional (gamma) diversity that accumulates inter-site differences between local
species assemblages (alpha diversity) need to be assessed. In particular, beta diversity can
directly assist conservation planning because it represents underlying ecological processes
of diversity maintenance of the biological species assemblage [
]. For example, directional
changes of species composition along a spatial or environmental gradient (i.e., the turnover
or distance-decay of similarities) will indicate if multiple forest patches with such a
variation would be necessary. In addition, the nestedness of the species composition or high
richness differences among patches imply that conservation efforts should focus on sites with a
high diversity, rather than species-poor sites [
]. The beta diversity index consist of two
components, species replacement and richness difference [
]. This approach enables us to
understand the relative importance of the mechanisms that influence the beta diversity and
gives us suggestions for conservation strategies.
This study focused on CRFs and explored the conservation values of CRFs that have been
managed by local communities in Sarawak, Malaysia, in terms of their alpha and beta diversity.
First, we investigated the alpha diversity of each CRF in terms of their endangered species and
species richness (S). We also investigated whether multiple CRFs contribute to the regional
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species diversity index. Furthermore, we investigated the relative contributions of replacement
and richness, by dividing the beta diversity index into these components and characterizing
their relative importance in conserving the species diversity in this region. Finally, we discuss
if CRFs retain a conservation value in the region, including the social aspects of conservation.
Materials and methods
This study was conducted in the central part of the Jelalong River basin, Sarawak, Malaysia
(Fig 1). The area comprises various types of landscapes, such as primary mixed dipterocarp
forest (MDF), kerangas forest with nutrient-poor soils (podzol), logged forest, fallow forest,
paddy fields, and acacia or oil palm plantations. The forest (primary and logged forest) cover
in the area (ca. 700km2) in 2015 has been estimated to be approximately 50% (Takeuchi et al.,
unpublished data). The main driving force of land use change here is oil palm plantations.
This mixed landscape was considered appropriate for examining the conservation value of
remnant CRFs in the developing area. The average annual rainfall during 2006±2012 in Tubau
(3Ê90N, 113Ê420E), which is located approximately 5 km from the study area, was 4,556 mm.
The mean air temperature during 2006±2012 at Bintulu airport (3Ê70N, 113Ê10E, approximately
85 km from the study area) was 26.8ÊC. The elevation in the study area ranges from 30 to 200
m above sea level. The research was conducted under the permit issued by Forest Department
Sarawak. We also got permit to conduct the research from the headmen of local villages in the
The study area comprises six villages with local Iban and Penan people. Traditionally, they
have been engaged in slash-and-burn rice cultivation and rubber tapping since the 1960s.
More recently, they have begun to plant oil palms on a small scale as new cash crops. Five out
of these six villages have at least one CRF, and in five villages, there are ten CRFs in total. In
this study, we investigated eight out of these ten CRFs because one was supposed to be
transformed into an oil palm plantation, whereas another was hard to access. The most important
factor for villages that possessed at least one CRF was a water catchment forest, from which
water pipes were laid to the settlements (longhouse). CRFs used as a drinking water resource
are called pulau paip (pipe) or pulau ai (water) in Iban language. Although a CRF is supposed
to be an intact or untouched forest [
], recent CRFs in this area contain rather disturbed
forest patches. Six out of the eight CRFs experienced selective logging at least once in the past
although it was not clear cut (Table 1). All CRFs are used by villagers for hunting and for
collecting non-timber forest products, such as fruits, vegetables, mushrooms, bamboo, rattan,
resin, and wild rubber. Most of those products from CRFs are used for consumption.
However, sometimes villagers gain cash income by selling these products, such as rattan baskets
The study area is approximately 100 km from the Lambir Hills National Park, Miri,
Sarawak (LHNP, 4Ê080±4Ê120N, 114Ê000±114Ê070E, 20±220 m above sea level, Fig 1), which
contains a typical primary lowland MDF. We used data obtained in 2000 from two permanent
vegetation plots in LHNP (4 and 8 ha, respectively) as the control plots of primary forest.
Biodiversity assessment of CRFs
Tree census. In October 2013 and February 2014, we established 16 plots of 50 m × 50 m
each (0.25 ha) in the eight CRFs (Fig 1). Six CRFs had been logged approximately 30 years
before (Table 1). In each plot, all tree stems with a diameter at breast height (DBH, at 1.3 m
above ground) > 10 cm were tagged, identified to species level based on vegetative samples,
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Fig 1. Map of the targeted study area in jelalong. The letters indicate the targeted villages except for F, where does not have a CRF. Village C was
moving to their longhouse into the location C (new). The numbers indicate the communally reserved forests (CRFs), and the open circles in CRFs are the
studied plots and the closed ones are villages. The location of the Lambir Hills National Park (LHNP) is shown in the lower map.
and their DBH measured. Voucher specimens were stored in the Botanical Research Centre
Data analysis±alpha diversity and community structure. To evaluate the alpha diversity
in each CRF, the number of species (S) and Shannon diversity index (H) were calculated. In
addition, the rarefaction curves (i.e., the expected S in random subsamples of a given sample
size from the focal community in a fixed area) were determined for the number of trees in
each plot. This was performed to determine the sample size or area effect of each forest, using
the function ªrarefyº, which provides rarefaction of species richness in each sample size, from
the package vegan in R [
]. To standardize the plot sizes, 1000-times re-sampled 0.25-ha
areas within the plots in LHNP were averaged to describe the rarefaction curves. We also
averaged the result for three plots in CRFs 1±4. We used LHNP data to compare CRF values with
primary forest values. Because we used 4- and 8-ha plot data from LHNP, we standardized the
plot area. To determine the rarefaction curve, we randomly re-sampled a 0.25-ha area for 1000
iterations and calculated the 95% confidence intervals. The similarity in species community
composition between the forests was illustrated by a non-metric multidimensional scaling
]). NMDS calculates an ordination based on a similarity matrix, using Bray±Curtis
distances. We compared data from 16 plots of eight CRFs in the Jelalong area with two plots
from LHNP. Here, we used all data of the LHNP plots as standardization would result in poor
performance of the NMDS probably because of the smaller sample size. NMDS was calculated
with the function metaMDS in the R package ªveganº using species level data.
Data analysis±beta diversity. First, the cumulative species±area curves were produced, to
examine differences in the contribution to regional diversity between smaller and larger CRFs
]. We plotted the cumulative number of species against the number of plots added and
the cumulative area of CRFs by sorting the patches from small to large and from large to small.
Second, two dissimilarity indices, the abundance-based (Bray-Curtis index, DB) and
presence-absence index (Jaccard index, DJ), were calculated for all paired comparisons of CRFs.
84.4 ± 18.4
4.1 ± 0.3
²The CRF is established to be used as a water catchment forest for the new longhouse of the village.
*Proportion followed by the same letter is not significantly different at a level of significance of 0.05 by pairwise Fisher's test adjusted using false discovery
rate (Benjamini & Hochberg, 1995, J R Stat Soc Series B Stat Methodol, 57(1):289±300.).
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Correlations between dissimilarity and geographic distances were examined with a Mantel
tests (using the R package ªecodistº). Furthermore, to investigate whether variations in beta
diversity were caused by S differences among CRFs or by species replacement (turnover), we
employed the method of Legendre [
]. The total beta diversity (BDTotal) is calculated as
Xn 1 Xn
h1 ih1 n
, where Dhi represents the dissimilarity between sites h and i. As Dhi can be decomposed into
two factors, replacement (Replhi) and richness difference (RichDiffhi), the relationship can be
written as follows:
, where ReplTotal
Pn 1 Pn Replhi
h1 ih1 n
This relationship allows us to calculate the proportion of BDTotal accounted for by the
replacement and richness difference fractions as follows:
BDTotal ReplTotal RichDiffTotal
Pn 1Pn RichDiffhi :
h1 ih1 n
ReplProp ReplTotal and
We subsequently produced the triangular graphs to represent the pairwise indices 1 − Dhi,
Replhi, and RichDiffhi which also followed the method of Legendre [
Tree species composition and diversity
We identified 2548 trees, which comprised 67 families, 183 genera, and 543 species in total (S1
Table, S2 Table). There were 14 trees which could not identify species, and we excluded them
from further analysis. Tree communities in the Jelalong CRFs were mainly dominated by
Dipterocarpaceae and Euphorbiaceae families (S2 Table), similar to those in LHNP (S3 Table).
The lowest S (43) was observed in the mixed kerangas and peat swamp forest (CRF 1). S ranged
from 74 to 97 in lowland or hill MDFs, which was equivalent to that of LHNP (Table 1). H was
also the lowest in CRF 1 (approximately 3), whereas in the other forests it ranged from 3.9 to
4.2, which was similar to values of LHNP (Table 1). The rarefaction curves comparing CRFs
and LHNP indicate that all CRFs had species diversity levels similar to the primary forest (Fig
2A). NMDS showed three clear clusters according to the region or soil type: LHNP, kerangas/
peat swamp forest, and other MDFs in Jelalong (Fig 2B). In fact, 79% of species in CRF 1 are
specific for this forest because this is the only kerangas/peat swamp forest among the target
CRFs (S1 Table). In addition, 44% of the species in CRF 2 are also site-specific (S1 Table),
which was the highest uniqueness among the MDF forests. There was no significant
relationship between the S, H, or Simpson's diversity index and the area of CRFs (generalized linear
models, p > 0.10).
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Fig 2. Alpha-diversity and composition of tree species communities in CRFs. (a) Sampling-standardized species richness within
a 0.25-ha plot. Averaged rarefaction curves of eight CRFs are shown. The colored area indicates the 95% CI of LHNP. (b) NMDS
ordination of tree species composition among 16 plots of eight CRFs and 8- and 4-ha plots in LHNP. Circles indicate the forests
disturbed in the past. Plot replicates are linked with the lines.
The cumulative S increased linearly as the plots were added, and the pattern was not very
different whether the smallest or largest CRFs were added first (Fig 3A). The cumulative S
against the cumulative area of CRFs increased largely when the smallest CRFs were added first
than when the largest ones were added first (Fig 3B).
We found a marginally significant negative geographic distance decay of similarity (1-DB;
Mantel r = −0.29, p < 0.09) (Fig 4A). The triangle graph shows the similarity among CRFs and
the components of replacement and richness difference (Fig 4B). The difference of tree species
community was mostly because of replacement, which accounts for 65% of total beta diversity.
Using DJ, a similar tendency was observed (S1 Fig).
The size structure of the trees in Jelalong was different among CRFs (Table 1, S2 Fig). The
percentage of trees with a DBH > 50 cm was > 6.5% in CRFs 1±3, which is almost equivalent to
that in LHNP. Maximum values of DBH were also higher in those CRFs (> 90 cm). On the
other hand, in the other CRFs, relatively small trees were predominant. In CRF 7, the mean
DBH was significantly smaller than that in CRFs 1±3. Furthermore, CRF 7 contained smaller
sized trees in a high density, which may be because this CRF experienced more intensive
disturbance in the past compared with other disturbed CRFs.
Fig 3. Species-area curve. Cumulative number of tree species sampled in 0.25-ha plots against (a) cumulative plot number and (b) CRF area
added. The plots or CRFs were added from smallest to largest (black circle) or largest to smallest (blank square), respectively. The bigger
symbols indicate that a CRF has three plots, i.e., three plots were added at once.
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Geographic distance (m)
Fig 4. Beta-diversity of tree species communities in CRFs. (a) Distance-decay in the similarity (1-DB) of
tree community composition among CRFs. The fitted model from a generalized linear model is shown in
black. (b) Triangular graph of the relationship among 1-DB (similarity), Repl (replacement), and RichDiff
(richness difference). The large central dot is the centroid of the points, and the smaller dots represent the
mean values of 1- DB, Repl, and RichDiff components. The fractions of replacement and richness difference to
the total beta diversity are ReplProp = 0.66 and RichDiffProp = 0.34, respectively.
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1: IUCN Red List criteria: CRÐCritically endangered, ENÐEndangered, VU Vulnerable.
2: Sarawak protected species includes the species in the CITES list.
Species richness of endangered species
All CRFs contained endangered species according to the IUCN Red List [
] and Sarawak
protected species [
] (Table 2). In total, 54 endangered or protected species were found in CRF
plots. The number of endangered or protected species observed per CRF ranged from 5 to 24,
and CRF 2±4 included > 17 species. We found no significant differences in the proportion of
endangered species among CRFs (Fisher's exact test, p > 0.05).
Our results showed that all CRFs harbor a high alpha and beta diversities, which suggests
that all CRFs have a high conservation value. Although most CRFs experienced logging in
the past, those CRFs had S and composition comparable to those of intact forests. This
suggests that after disturbance, tree species diversity can recover because of seed dispersal from
surrounding secondary forests. A previous study by Arroyo-Rodriguez, Pineda [
that fragmented forests tend to have a higher species diversity if they have a high proportion
of forest cover than those with a lower forest cover. Even if species diversity was decreased
by human disturbance, immigration could compensate for the species loss. This could
occur most effectively in landscapes with a higher forest cover. However, the size structure
was different among disturbed and intact CRFs; disturbed CRFs still consist of relatively
smaller trees. This suggests that biomass recovers more slowly than species diversity. These
results are consistent with a previous study in Indonesian Borneo, which reported that
conservative logging reduced the stem density, whereas S was equivalent with that of unlogged
As for beta diversity, we found a marginally significant similarity in distance-decay, which
could be caused by dispersal limitation or environmental heterogeneity, or both [
]. We also
found a high beta diversity derived from a high turnover rate of species composition, not
richness differences, among the sites. Thus, nestedness among CRFs is small, and it implies that all
CRFs can be conservation targets. A high beta diversity has been reported in the region, which
increases the regional diversity.
We also found that CRFs included a total of 54 species from the IUCN Red List species,
Sarawak protected plant, or both. This indicates that CRFs in this small area (4 ha in total)
could cover 17% of the IUCN Red List of Threatened species [categories of critically
endangered (CR), endangered (EN), and vulnerable (VU)] among dicots (Magnoliopsida) occurring
in Sarawak. Therefore, CRFs contribute to the conservation of endangered species. For
example, endangered species, such as ramin (Gonystylus spp. Thymelaeaceae) and gaharu (Aquilaria
spp., Thymelaeaceae), were found in CRFs. Ramin is a light hardwood, and it is a very valuable
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timber in the global market, whereas gaharu is used as an incense and in traditional medicines.
As a high demand for both species in the global market has caused a reduction in their
populations, they are now classified as VU in the IUCN Red List. Furthermore, timber export is
restricted by CITES (listed in Appendix II) [
]. Even though ramin is valuable in the global
market, local people seldom use these species by themselves. Because ramin contains an itchy
resin, it is not a good timber for local use. Furthermore, local people used to use gaharu as
medicines, but recently they prefer buying medicines from a drug store. Thus, villagers
consume few ramin and gaharu specimens from CRFs, and therefore, CRFs could function as
insitu effective conservation spots for these species.
The high species diversity in CRFs maintained in Jelalong is probably owing to several
specific reasons as big trees have rarely been cut down here in a long period at least 70 years after
settlement of the longhouses. First, CRFs were traditionally considered as the timber stock for
longhouse construction [
]. Second, accessing some CRFs was considered as a ªtabooº
because of spiritual beliefs [
]. Third, to maintain a constant supply and good quality of
drinking water, CRFs that have a water catchment function are not supposed to be disturbed;
however, this is a more recent trend. These customs may limit the disturbance of CRFs,
resulting in a high biodiversity within the forests. A fourth reason could be that logging was not that
intensive in the past, particularly in the steep terrain area. Furthermore, an ecological reason
could be that CRFs are surrounded by old secondary forest (usually at least 25±40 years old
after disturbance), which also functions as a species source. It has been previously argued that
one of the important roles of small but intact forests in a fragmented landscape is to provide a
seed source for surrounding degraded forests [
]. The existence of these highly diverse
forests can compensate for the species loss in degraded forests through seed dispersal . The
surrounding degraded forests can rehabilitate faster because of a constant seed input from
small but intact forests, such as CRFs. Eventually, these forests will become a source of species
for CRFs as well. Thus, if we can conserve the traditional mosaic landscape structure in the
rural areas of Borneo, they might contribute to maintaining the species diversity at a regional
]. Future work might consider a comprehensive conservation of biodiversity, i.e.,
corridors between CRFs, particularly for vertebrate movement, which was also recommended by
CRFs can be a plausible biodiversity conservation target for the local government in the
fragmented landscape of the Sarawak lowland area with respect to both alpha and beta diversity.
Our results indicate that the traditional land use practice in indigenous communities, (i.e.,
CRFs) can be useful for biodiversity conservation, at least in the current situation.
Furthermore, designing CRFs as a conservation target can be suitable for the maintenance of regional
species diversity, including endangered species. However, long-term effective conservation
might not be achieved without considering three points. First, the ecological and
environmental factors that affect biodiversity in the long term are still unknown. Biodiversity dynamically
changes in space and time in response to the physical environment, migration, and
deterministic processes in plant demography [
] as well as the surrounding land-use patterns [
]. Second, local demand for CRFs, e.g., how much local people depend on products in CRFs
and how people regard CRF functions, should be quantitatively evaluated in multiple aspects
]). Third, CRFs are prone to development under the pressure of economic incentives
provided by the state and local governments and current trends in the global market. For
example, one CRF in a village was partly opened by the villagers to plant oil palms because
they believed that if they left their forest ªunused,º the government or plantation companies
11 / 14
may take the land. Consequently, CRFs have been decreasing in number and area because of
socio-economic pressures, even though people have recently recognized their value.
Biodiversity conservation using CRFs cannot be achieved without reducing the pressure of land
development. Thus, it is essential that local communities, companies, and policy makers are
together engaged in implementing a conservation strategy that is integrated with their
S1 Table. Number of taxonomic classification of tree species community in each CRF.
S2 Table. Taxonomic classification, abundance and conservation status of tree species
community in each CRF.
S3 Table. Taxonomic classification, abundance of tree species community in 4ha (2000)
and 8ha (1997) plots in Lambir Hills National Park.
S1 Fig. Beta-diversity of tree species communities in CRFs. (a) Distance-decay in the
similarity (1-DJ) of tree community composition among CRFs. The fitted model from a generalized
linear model is shown in black. (b) Triangular graph of the relationship among 1-DJ
(similarity), Repl (replacement), and RichDiff (richness difference). The large central dot is the
centroid of the points, and the smaller dots represent the mean values of 1- DJ, Repl, and RichDiff
components. The fractions of replacement and richness difference to the total beta diversity
are ReplProp = 0.62 and RichDiffProp = 0.26, respectively.
S2 Fig. DBH size frequency of each CRF in jalalong. Means followed by the same letter are
not significantly different at the 0.05 level by pairwise t test adjusted using false discovery rate.
The authors thank Mrs. Engkamat anak Lading (Sarawak Forest Department) and Julaihi
Abdullah (Sarawak Forestry Corporation) for their permission for and assistance with work in
Sarawak, Malaysia. We also thank the staff of Sarawak Forestry Corporation for their field
assistance in this study.
Conceptualization: Yayoi Takeuchi.
Data curation: Yayoi Takeuchi, Tinjan ak. Kuda, Michiko Nakagawa, Hidetoshi Nagamasu,
Formal analysis: Yayoi Takeuchi.
Funding acquisition: Yayoi Takeuchi.
Investigation: Yayoi Takeuchi, Ryoji Soda, Bibian Diway, Tinjan ak. Kuda.
Methodology: Yayoi Takeuchi.
Project administration: Yayoi Takeuchi, Bibian Diway.
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Writing ± original draft: Yayoi Takeuchi.
Writing ± review & editing: Yayoi Takeuchi, Ryoji Soda.
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