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A gap analysis of Southeast Asian mammals based


on habitat suitability models

Gianluca Catulloa, Monica Masia, Alessandra Falcuccib, Luigi Maioranob,*,


Carlo Rondininib, Luigi Boitanib
a
Istituto di Ecologia Applicata, via Bartolomeo Eustachio 10, 00161 Rome, Italy
b
Department of Animal and Human Biology, Sapienza Università di Roma, Viale dell’Università 32, 00185 Rome, Italy

A R T I C L E I N F O A B S T R A C T

Article history: Southeast Asia is one of the richest reservoirs of biodiversity on earth and home to one of
Received 9 November 2007 the highest concentrations of endemic species. Many protected areas (PA) have been estab-
Received in revised form lished across the region, but to date no systematic evaluation of their efficacy has been
7 August 2008 published because no comprehensive dataset was available which could be fed into an
Accepted 11 August 2008 analysis of conservation gaps. We collected the geographic range for 1086 mammal species
Available online 23 September 2008 of Southeast Asia and we built species-specific habitat suitability models for 901 of them.
We performed two gap analyses (one based on a combination of distribution models and
Keywords: distribution ranges and one based on distribution ranges only) for each mammalian spe-
Southeast Asian mammal databank cies, to evaluate the effectiveness of the existing network of PA and to identify priority
Gap analysis regions and priority species for expanding and consolidating the network. Our results indi-
Protected areas cate that 7.5–8.2% of species are not covered by any PA, and 51.6–59.1% are covered only
Distribution models partially. These species are distributed throughout the entire study area and their conser-
Mammal distribution ranges vation requires the creation of new PA that can help fill this existing conservation gap. This
Threatened species would be particularly important for species which are endemic of small islands, where
species survival is often threatened by the presence of introduced species and habitat con-
version. Yet PAs cannot be considered as the ending point of a conservation strategy,
because overall, 34% of the species we analyzed (many of which already covered by exist-
ing PAs) were at risk of extinction when considering the IUCN red-list criteria. PAs should
therefore be considered in a broader framework of all local ecological and socio-economic
trends, including the growing human population, growing economy and infrastructure
development.
Ó 2008 Elsevier Ltd. All rights reserved.

1 Introduction country system composed by Indonesia, Malaysia and the


Philippines (McNeely et al., 1990). This extraordinary species
Southeast Asia is one of the richest reservoirs of biodiversity richness encompasses all taxa, and mammals are no excep-
on earth and home to one of the highest concentrations of en- tion (Brooks et al., 1999; Sodhi and Brook, 2006). In fact, roughly
demic species (Sodhi et al., 2006a). The region encompasses one quarter of the mammal species of the world occurs in the
four hotspots (Myers et al., 2000), several of the most valuable area, with many new families and species which have been
eco-regions (Olson and Dinerstein, 1998), and a megadiversity discovered recently (Jenkins et al., 2005; Musser et al., 2005).

* Corresponding author: Tel.: +39 0649694262; fax: +39 06491135.


E-mail addresses: g.catullo@ieaitaly.org (G. Catullo), m.masi@ieaitaly.org (M. Masi), alessandra.falcucci@uniroma1.it (A. Falcucci),
luigi.maiorano@uniroma1.it (L. Maiorano), carlo.rondinini@uniroma1.it (C. Rondinini), luigi.boitani@uniroma1.it (L. Boitani).
0006-3207/$ - see front matter Ó 2008 Elsevier Ltd. All rights reserved.
doi:10.1016/j.biocon.2008.08.019
B I O L O G I C A L C O N S E RVAT I O N 1 4 1 ( 2 0 0 8 ) 2 7 3 0 –2 7 4 4 2731

The rapid and extensive destruction of habitats occurring under analysis (Rondinini et al., 2006b). However, we per-
worldwide across the tropical belt has not spared Southeast formed our analyses also considering geographic ranges to
Asia, which indeed has one of the highest relative rates of obtain a range of reasonable estimates for gap species. Our
deforestation among the major tropical regions (Laurance, analysis is unique in providing indications of conservation
1999). Its native biota is seriously threatened by forest conver- status for a large study area and at a scale that is useful for
sion, forest fires, unsustainable subsistence hunting and conservation planning purposes.
wildlife trade (Sodhi et al., 2004a). In this context, protected
areas (PAs) constitute a valuable tool for assuring the conser- 2. Materials and methods
vation of viable populations within natural ecosystems (Bru-
ner et al., 2001; Redford and Richter, 1999; Groves, 2003; Our study area encompasses the entire Southeast Asia,
Rosenzweig, 2003; Cardillo et al., 2006; Lee et al., 2007). Over including all countries south of China and east of India: Bru-
the years, Southeast Asian countries have established nei Darussalam, Cambodia, Indonesia, Lao PDR, Malaysia,
(though at different paces) national PA systems. However, Myanmar, Papua New Guinea, The Philippines, Singapore,
PAs are often not completely representative of the biodiver- Thailand, and Viet Nam.
sity of a region (Pressey et al., 1993; Scott et al., 1993; Rodri- We characterized the landscape of the study area consider-
gues et al., 1999; Margules and Pressey, 2000; Rondinini ing datasets from different sources and covering: (a) land-cov-
et al., 2005) as their location and design is frequently based er (Global Land Cover 2000 [GLC2000]; European Commission,
on socio-economic, aesthetic and political values rather than Joint Research Center, 2003; http://www-gvm.jrc.it/glc2000);
biological criteria. Consequently, unrepresentative sites of (b) elevation (Hastings et al., 1999; http://www.ngdc.noaa.-
lesser conservation value may be set aside for conservation gov/mgg/topo/globe.html); (c) hydrology (Digital Chart of the
while sites of the higher value remain unprotected. World; ESRI, 1993); (d) human settlements (Digital Chart of
Gap analysis (assessing to what extent animal and plant the World; ESRI, 1993); (e) administrative boundaries (Digital
species are being protected) is a powerful approach to explore Chart of the World; ESRI, 1993); (f) PAs (World Database on
the effectiveness of a PA system in representing local biodi- Protected Areas [WDPA] Consortium, 2006; http://maps.geo-
versity (Scott et al., 1993). Gap analysis has been applied to g.umd.edu/WDPA/WDPA_info/English/index.html). All layers
various taxa globally (Rodrigues et al., 2004a), at continental were re-sampled for the analyses using a common origin
level, and in many countries worldwide (Scott et al., 1993, and a 1-km cell size. From the WDPA, we selected 1635 PAs
2001; Fearnside and Ferraz, 1995; Ramesh et al., 1997; Rodri- presently mapped for SE Asia, irrespective of their IUCN clas-
gues et al., 1999; Powell et al., 2000; De Klerk et al., 2004; Fjeld- sification (IUCN, 1994). From analyses, we excluded 90 PAs for
sa et al., 2004; Oldfield et al., 2004; Yip et al., 2004; Dietz and which no information was available on their boundaries and/
Czech, 2005; Maiorano et al., 2006, 2007; Rondinini et al., or on their area. Of the 1635 PAs, 1088 had information on
2006a), but so far it has never been applied to PAs of Southeast their geographical boundaries, while 547 had the coordinates
Asia because no comprehensive dataset has been available of their geographical center and the information on the size
which could be fed into the GAP process. of the PA. In order to merge all PAs into a single layer, we built
Rodrigues et al. (2004b) and Brooks et al. (2004) suggested circular buffers of the same size as the PA around these cen-
the necessity of fine scale mapping works that, starting from tral points.
the results of the global gap analysis, provide the local context We compiled a geographical database (freely available
that is necessary for conservation. The Southeast Asian Mam- through SAMD’s website) covering the entire study area with
mal Databank project (SAMD – a joint effort between Istituto information on 1086 mammal species, belonging to 17 orders
di Ecologia Applicata, European Commission and IUCN) for (Table 1).
the first time provides a comprehensive, fine-grained, and For each species, we collected from the scientific literature
large scale biodiversity dataset, consisting of extent of occur- all available information on the species–habitat relationships,
rence maps, species–habitat relationships and habitat suit- the elevation range, and the Extent of Occurrence (EOO; the
ability models for all mammals of the region. The dataset full list of papers is available from the authors upon request).
was compiled in 2002–2006 in close collaboration with the Species–habitat relationships (sensu Corsi et al., 2000) fol-
IUCN Global Mammal Assessment process and it is freely lowed the GLC2000 land-cover classes, and each class was
available at SAMD’s website (http://www.ieaitaly.org/samd/). classified as suitable (main or preferred habitats) or unsuit-
In this paper we present the SAMD dataset and provide an able (secondary and unsuitable habitats). Elevation was clas-
assessment of the effectiveness of the existing PAs for the sified according to two classes: inside known elevation
conservation of terrestrial mammals in Southeast Asia. While range, outside known elevation range.
geographic ranges grossly overestimate species distribution All the information collected was reviewed, discussed, and
(conditional on species range size as suggested by Jetz et al., integrated during five dedicated workshops which involved a
2008), thus hiding a number of gap species that overlap PAs selection of the most eminent local and international experts
only in unsuitable portions of their range (Rondinini et al., on various taxa. Each workshop involved from 21 to 48 ex-
2005), distribution models may potentially underestimate perts for 3–5 days of intensive analysis and updating of the
species distribution, providing an overly restrictive picture available data (Mammals of Southeast Asia – Thailand, May
of the current conservation status. As suggested by Rodrigues 2004; Mammals of the Philippines – Philippines, April 2006;
et al. (2004b) and by Brooks et al. (2004), we focused on the Bats and Large Mammals of Southeast Asia – Indonesia,
overlap of PAs with estimated (and validated) suitable areas May 2006; Small Carnivores of Southeast Asia – Vietnam, July
for species, because these are more likely to host the species 2006; Primates of Southeast Asia – Cambodia, September
2732 B I O L O G I C A L C O N S E RVAT I O N 1 4 1 ( 2 0 0 8 ) 2 7 3 0 –2 7 4 4

Table 1 – Orders and number of species included in the Table 2 – Overlay of environmental layers
Southeast Asian Databank
Land-covera Elevationb Suitability score
Order All species Threatened species
1 1 Suitable
Monotremata 4 3 1 2 Not-suitable
Dasyuromorphia 16 3 2 1 Not-suitable
Peramelemorphia 12 2 2 2 Not-suitable
Diprotodontia 58 30
a Suitability scores for land-cover as defined in the method sec-
Proboscidea 1 1
tion: 1 = suitable; 2 = unsuitable.
Scandentia 17 11
b Suitability scores for elevation as defined in the method section:
Dermoptera 2 1
1 = inside known elevation range; 2 = outside known elevation
Primates 76 62
range.
Rodentia 388 114
Lagomorpha 6 1
Erinaceomorpha 7 1 area of potential species presence. The complete species list is
Soricomorpha 56 5 available at SAMD’s website (http://www.ieaitaly.org/samd).
Chiroptera 328 73
Pholidota 3 3
Carnivora 54 24
2.2. Validation
Perissodactyla 3 3
Artiodactyla 52 34 To test the predictive power of the DMs, we measured the per-
Total 1086 371 formance of the models in predicting species potential pres-
Threatened species include critically endangered, endangered, ence. In particular, we measured the agreement between
vulnerable, and near threatened. each DM and a set of points of presence which were indepen-
dently collected in the field. We also measured the agreement
between each DM and a set of random points and we com-
pared the results using a permutation test.
2006). Our dataset was also integrated with the information We obtained point data on species presence gathering the
gathered during two additional workshops run by IUCN in available published and unpublished datasets, consisting
the framework of the Global Mammal Assessment project mainly in observations and captures. In particular, we ob-
(Mammals of Australia and Papua New Guinea – Australia, tained data for Chiroptera, Rodentia, Artiodactyla, Carnivora,
August 2005; Rodents of Southeast Asia - United States, May Primates and Scandentia covering Laos, Thailand, Malaysia,
2006). During these workshops, species conservation status Brunei, Vietnam, Cambodia and Indonesia (Kalimantan).
was reviewed in accordance to the IUCN red-list criteria ver- The datasets covered a total of 351 species and were kindly
sion 3.1 (Table 1; IUCN, 2001). provided by C. Francis (unpublished data), R. Steinmetz
(unpublished data), R. Boonratana (unpublished data), G.
2.1. Distribution models Csorba (unpublished data), J. MacKinnon (unpublished data),
D. Lunde (Lunde et al., 2003), E. Meijaard (unpublished data),
We considered 1077 species (99.2% of the total 1086 species in and J. Walston (unpublished data).
the database) in all the subsequent analyses. We excluded We integrated these existing datasets with point data on
four introduced species and five species with no reliable infor- species presence directly collected in the field in Indonesia,
mation on their distribution. For 901 species, we built deduc- The Philippines and Vietnam. We selected these three coun-
tive distribution models (DM; sensu Corsi et al., 2000) using the tries for several reasons including available logistic support,
available species–habitat relationships and environmental political stability, security for the field crew, cost of expedition
layers. First of all, land-cover and elevation were reclassified and permission to conduct research activities. The field crews
following the available suitability scores (see paragraph above were composed by two researchers from the Institute of Ap-
for more details on the definition of the scores). Then, for plied Ecology (IEA) and by two zoologist from the Indonesian
each species we combined the suitability scores of the two Institute of Sciences for Indonesia, by one researcher from
layers into a synthetic suitability index (Table 2). IEA and by two zoologist from the Institute of Biology of the
For four strictly water dependent species (Aonyx cinerea, Lu- University of the Philippines–Diliman for the Philippines, by
tra lutra, Lutra sumatrana, Lutrogale perspicillata) the habitat two researchers from IEA and by two zoologists from the
suitability scores were computed inside a 3-km buffer around Institute of Ecology and Biological Resources of the Vietnam-
water bodies and courses. For 63 species no information on ese Academy of Science and Technology in Vietnam. In each
the elevation range was available; in this case the suitability country, we followed a systematic random sampling design
was calculated considering only land-cover. to select 100 points (for a total of 300 points). The field crews
We defined as area of potential species presence the area reached the village that was closest to each random point and
inside the EOO that was classified as highly suitable by the conducted a direct and standardized interview (Boitani et al.,
DM. We did not build a DM for 144 species with EOO < 1000 km2 1999) with local hunters and/or villagers (1–5 villagers/hunt-
(too small an extent compared with the extent of our study ers actively participating in the interviews) aimed at collect-
area) and for other 32 species that had unreliable species– ing information on the current presence of 148 species of
habitat relationships (i.e. species whose ecology was not medium and large sized mammals (we considered species
known). For these 176 species, we used their entire EOO as the easier to recognize and of greater economic value for the local
B I O L O G I C A L C O N S E RVAT I O N 1 4 1 ( 2 0 0 8 ) 2 7 3 0 –2 7 4 4 2733

populations) in the immediate neighborhood of the point. of threatened species, we built a map of potential species
Interviews were conducted in the local language with support richness for threatened species considering only those spe-
of pictures of the species; the ability of the interviewees in cies classified as critically endangered, endangered, vulnera-
recognizing species was tested using dummy pictures of com- ble, or near threatened following the IUCN red-list criteria
parable European and/or African species. Only (subjectively version 3.1. The same maps of potential species richness were
judged) reliable information was retained. Not all 300 points calculated considering the EOOs only for all 1077 species.
were reached by the field crews because of logistic reasons:
70 out of the original 100 points were sampled in Indonesia 2.4. Gap analysis
and in the Philippines, 80 out of the original 100 points were
sampled in Vietnam, for a total of 220 sampled points freely We performed two gap analyses: one considering a combina-
accessible through SAMD’s website. tion of the 901 DMs and 176 EOOs, and one considering EOOs
Merging all datasets, we obtained points of presence for only. Gap analysis requires the identification of a representa-
399 species. To decrease spatial dependence, we removed all tion target (Scott et al., 1993). We used a species-specific repre-
locations closer than 5 km one from each other from each sentation target depending on the area of potential presence
species dataset. Moreover, we excluded all species with less for each species. We performed our analyses following the
than five presence points from the validation analyses, representation target defined in the ‘‘global gap’’ project
obtaining a final list of 190 species (21% of all the DMs) for (Rodrigues et al., 2004a): species with a narrow distribution
which model validation was possible. (area of potential presence smaller than 1000 km2) should be
To account for possible location errors and the spatial protected in 100% of the area of potential presence; wide-
uncertainty naturally associated with each point of presence, spread species (area of potential presence greater than
we built a circular buffer (1.5 km radius) around each point of 250,000 km2) should be protected in 10% of the area of poten-
presence (thus a total of nine grid cells was considered for tial presence; species with area of potential presence greater
each point). A point of presence and the corresponding DMs than 1000 km2 and smaller than 250,000 km2 have a represen-
were considered to agree if at least one of the nine cells was tation target that is obtained interpolating between the two
classified as highly suitable. In this way, for each species we extremes using a linear regression on the log-transformed
calculated the percentage of presence points that agreed with area of potential presence.
the DM. A species not represented at all in any PA was considered a
To test the significance of the agreement between points of total gap, a species whose representation target is only par-
presence and the DMs, we used a permutation test following tially met was considered a partial gap, and a species whose
Maiorano et al. (2007). We compared the percentage of agree- representation target is met was considered covered.
ment calculated for the points of presence with that obtained
with 1000 sets of random points sharing the same character- 3. Results
istics as the set of points of presence (same number of points,
distance among points equal or greater than 5 km). If the per- PAs do not cover the countries in the study area with similar
centage of agreement calculated for the points of presence proportions (Table 3). For example, more than 44% of Brunei
was in the top 5% of the agreements obtained from the 1000 Darussalam and less than 6% of Singapore is protected. PAs
random samples, the model was considered validated. cover a disproportionate percentage of mountainous area,
To test whether the 190 species for which the points of the median elevation inside PAs being 438 m (interquartile
presence were available were representative of the ecology range = 753 m) while the median elevation inside the study
of all 901 species with a DM, we compared the distribution area is 190 m (interquartile range = 516 m).
of the suitability scores among the two groups. In particular,
for each land-cover class, we calculated the percentage of 3.1. Validation
the 190 species for which the class represented a suitable
habitat; we calculated the same percentage for the 711 spe- The 190 species that we considered in the validation proce-
cies with a DM but without validation points, and we com- dure were representative of the distribution patterns of all
pared the two distributions using a Kolmogorov–Smirnov test. species. We found no significant difference (p = 0.95) between
the distribution of the high suitability scores for the 190 spe-
2.3. Potential species richness cies and those for the 711 species that were not processed for
validation (Fig. 1). The main difference (although not statisti-
We used the 901 DMs and the 176 EOOs to build a map of po- cally significant) was for the land-cover class ‘‘Tree Cover,
tential species richness, calculated as the sum of all the spe- Regularly Flooded, Fresh Water’’, for which the 190 species
cies’ areas of potential presence (i.e. for species with a DM the with validation show a higher percentage of high suitability
areas inside the EOO classified as suitable, or the entire EOO scores compared to the entire species dataset.
for species without a DM as defined in the Distribution models On average, 32 presence points (median = 20) were avail-
section above). Moreover, to highlight the areas with a high able for the 190 species with a maximum of 233 points for Par-
concentration of endemic or restricted-range species, we also adoxurus hermaphroditus and a minimum of five points for
built a map of potential species richness in which each spe- nine species (Babyrousa babyrussa, Sus cebifrons, Hipposideros
cies was weighted according to the inverse of its area of po- rotalis, Myotis annectans, Phoniscus atrox, Presbytis chrysomelas,
tential presence (hereafter called potential weighted Pygathrix nigripes, Hylobates agilis, Hylopetes nigripes). For 140
richness). To highlight the areas with a high concentration out of 190 species (73.7%), the DMs gave positive validation re-
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Table 3 – Country area, percentage being protected, and number of protected areas in each Southeast Asian country
Country Country area (km2) % In protected areas Number of protected areas

Brunei Darussalam 5898 44.25 44


Cambodia 182,062 24.02 30
Indonesia 1,911,253 14.10 431
Lao PDR 230,662 16.22 25
Malaysia 331,165 16.88 516
Myanmar 669,660 6.31 48
Papua New Guinea 397,160 11.43 35
Philippines 296,940 10.81 198
Singapore 592 5.57 6
Thailand 516,906 20.04 203
Viet Nam 328,809 5.96 99

Fig. 1 – Distribution of the high suitability scores for the species with a distribution model. Land-cover class: 1 – Tree Cover,
Broadleaved, Evergreen; 2 – Tree Cover, Broadleaved, Deciduous, Closed; 3 – Tree Cover, Needle-Leaved, Evergreen; 4 – Tree
Cover, Regularly Flooded, Fresh Water; 5 – Tree Cover, Regularly Flooded, Saline Water; 6 – Mosaic: Tree Cover/Other Natural
Vegetation; 7 – Shrub Cover, Closed-Open, Evergreen; 8 – Shrub Cover, Closed-Open, Deciduous; 9 – Herbaceous Cover,
Closed-Open; 10 – Sparse Herbaceous Or Sparse Shrub Cover; 11 – Cultivated and Managed Areas; 12 – Mosaic: Cropland/Tree
Cover/Other Natural Vegetation; 13 – Mosaic: Cropland/Shrub and/Or Grass Cover; 14 – Bare Areas; 15 – Water Bodies; 16 –
Artificial Surfaces.

sults, which were statistically significant for 46 species ness maps estimated using both EOOs and DMs, and point
(24.2%) at the a = 0.05 level, and for 77 species (40.6%) at the out noteworthy differences with the maps calculated using
a = 0.1 level. For 50 species (26.3%), the percentage of agree- only EOOs. All potential species richness maps calculated
ment among DMs and points of presence was lower than using the EOOs only are available in Appendix 1 online.
the agreement obtained with 1000 sets of random points, Considering potential species richness, the richest areas
but only for eight species (4.2%) the difference was signifi- (Fig. 2a) are found in Borneo (mainly Sarawak and Sabah),
cantly lower (p < 0.05). We found no taxonomic bias in the Western Sumatra, Annamites mountains, and Malay Penin-
validation results, with the exception of Chiroptera and Pri- sula (Malaysia). Other important areas of high potential spe-
mates. Considering the proportion of Chiroptera species over cies richness were also found in the Cardamom mountains
the total sample of species with validation points, we found a in Cambodia and Myanmar, along the mountain ranges of Pa-
percentage of positively validated species greater than ex- pua New Guinea, and in Sulawesi. The relative importance of
pected. On the contrary the validation results for Primates Papua New Guinea and of Sulawesi was lower if considering
showed a percentage of species with a negative validation potential species richness calculated with EOOs only (Fig. 1a
that was greater than expected. in Appendix 1).
The map of potential weighted richness (Figs. 1b and 2b in
3.2. Potential species richness Appendix 1) showed a different pattern, with higher values
being concentrated mainly along mountain ranges (rough-
In general, the richness maps estimated using only EOOs were ly > 500 m a.s.l.) and in small islands. In particular, the richest
similar to those estimated using both EOOs and DMs, although areas were found in the Annamite mountains (Vietnam and
the former maps depicted a much coarser spatial pattern. The Laos) and in the far north of Myanmar, which was the most
paragraphs below focus on describing potential species rich- important area for weighted species richness in Indochina.
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Fig. 2 – (a) Potential species richness calculated as the sum of each species’ area of potential presence (EOO or DM); (b)
potential weighted species richness calculated as the sum of each species’ area of potential presence (EOO or DM): each
species is weighted according to the inverse of its area of potential presence; (c) potential threatened species richness
calculated as the sum of each species’ area of potential presence (EOO or DM) considering only critically endangered,
endangered, vulnerable or near threatened species. All maps are represented using a histogram equalize stretch in ArcGis;
the legends of (a) and (c) report the actual ranges of potential richness values, the legend of (b) reports percentages.
2736 B I O L O G I C A L C O N S E RVAT I O N 1 4 1 ( 2 0 0 8 ) 2 7 3 0 –2 7 4 4

Fig. 2 (continued)

The Malay peninsula (Malaysia) was also a very important Considering a combination of EOOs and DMs, more than
area, as well as the Philippines (especially Palawan, Mindoro, 59% of all the species (636 species) were partial gap species
and Luzon), Sulawesi, New Guinea and a number of small is- and 33% (352) were fully covered (Table 4). The taxa with the
lands (Moluccas, Singapore, Natuna Besar, Mentawai, Engg- highest percentages of partial gap species were Soricomor-
ano, Simeleu, Sangihe, Talaud, Peleng, Waigeo, and Geelvink pha, Rodentia, Diprotodontia, Lagomorpha and Primates,
Bay islands). but many other taxa showed high numbers of partial gap spe-
The map of potential richness for threatened species (Figs. cies (Table 4). Considering EOOs only, 51.6% of all the species
1c and 2c in Appendix 1) clearly shows the importance for con- (556 species) were partial gap species and 41% (440) were fully
servation of areas like the Annamite mountains, Borneo (Sara- covered (Table 4). Once more, Soricomorpha, Rodentia, Diprot-
wak in particular), Western Sumatra and peninsular Malaysia. odontia, Lagomorpha and Primates, although with different
percentages, were the taxa with the highest percentage of
3.3. Gap analysis partial gap species. The complete list of total and partial
gap species is available in Appendix 2 available online.
Considering a combination of DMs (901 species) and EOOs Considering threatened species (i.e. those species classi-
(176 species), only 88 species (8.2%) of the Southeast Asian fied as critically endangered, endangered, vulnerable, or near
mammals that we considered were total gap. This number re- threatened according to the IUCN criteria), from 73.9% (EOOs
mained almost unchanged considering EOOs only, with 81 plus DMs) to 68.2% (EOOs only) are classified as total or partial
species (7.5%) being considered total gap (as it was expected gap (Table 4), with Dasyuromorphia (only when considering
given that 72% of the 88 total gap species above do not have EOOs plus DMs), Diprotodontia and Rodentia being the taxa
a distribution model). Considering both EOOs and DMs, the with the highest percentages of threatened species not cov-
orders with the highest numbers of total gap species were ered by any PA, and Erinaceomorpha, Peramelemorphia, and
the Rodentia (37 species) and the Chiroptera (28 species). Per- Soricomorpha being the taxa with the highest percentages
amelemorphia, Dasyuromorphia, and Artiodactyla showed of threatened species only partially covered by PAs. Notable
relatively low numbers of total gap species (respectively are also the cases of the Dermoptera, Lagomorpha and Probo-
two, two, and six species), but extremely high percentages, scidea that, considering threatened species, are completely
with Peramelemorphia being the order with the highest per- covered by existing PAs (Table 4).
centage of total gap species (Table 4). Considering EOOs only, The areas with the highest numbers of total and partial
the results were almost unchanged, with the exception of gap species (Fig. 3a) are Sulawesi, Papua New Guinea, and
Dasyuromorphia (for which no species was classified as total Mentawai islands, together with many mountainous areas
gap according to the EOO only analyses) and Artiodactyla (Annamite mountains at the boundaries between Laos and
(that passed from five total gap species considering EOOs Vietnam, peninsular Malaysia, North Myanmar, Luzon in
and DMs to three species with EOOs only). the Philippines, and northern Borneo). The same distribution
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Table 4 – Percentage of total gap species, partial gap species, and covered species for each order calculated using a
combination of DMs and EOOs

Order Total gap species (%) Partial gap species (%) Covered species (%)
All species Threatened species All species Threatened species All species Threatened species

Artiodactyla 9.6 (5.8) 3.8 (0.0) 51.9 (51.9) 63.8 (61.8) 38.5 (42.3) 32.4 (38.2)
Carnivora 1.9 (1.9) 0.0 (0.0) 29.6 (18.5) 20.8 (16.7) 68.5 (79.6) 79.2 (83.3)
Chiroptera 8.5 (7.9) 4.1 (4.1) 57.9 (48.8) 79.5 (72.6) 33.5 (43.3) 16.4 (23.3)
Dasyuromorphia 12.5 (0.0) 33.3 (0.0) 50.0 (50.0) 33.3 (66.7) 37.5 (50.0) 33.3 (33.3)
Dermoptera 0.0 (0.0) 0.0 (0.0) 50.0 (50.0) 0.0 (0.0) 50.0 (50.0) 100.0 (100.0)
Diprotodontia 6.9 (6.9) 13.3 (13.3) 67.2 (55.2) 76.7 (70.0) 25.9 (37.9) 10.0 (16.7)
Erinaceomorpha 0.0 (0.0) 0.0 (0.0) 57.1 (57.1) 100.0 (100.0) 42.9 (42.9) 0.0 (0.0)
Lagomorpha 0.0 (0.0) 0.0 (0.0) 66.7 (66.7) 0.0 (0.0) 33.3 (33.3) 100.0 (100.0)
Monotremata 0.0 (0.0) 0.0 (0.0) 50.0 (50.0) 33.3 (33.3) 50.0 (50.0) 66.7 (66.7)
Peramelemorphia 16.7 (16.7) 0.0 (0.0) 50.0 (41.7) 100.0 (100.0) 33.3 (41.7) 0.0 (0.0)
Perissodactyla 0.0 (0.0) 0.0 (0.0) 33.3 (33.3) 33.3 (33.3) 66.7 (66.7) 66.7 (66.7)
Pholidota 0.0 (0.0) 0.0 (0.0) 33.3 (33.3) 33.3 (33.3) 66.7 (66.7) 66.7 (66.7)
Primates 6.6 (6.6) 8.1 (8.1) 63.2 (52.6) 66.1 (54.8) 30.3 (40.8) 25.8 (37.1)
Proboscidea 0.0 (0.0) 0.0 (0.0) 0.0 (0.0) 0.0 (0.0) 100.0 (100.0) 100.0 (100.0)
Rodentia 9.7 (9.4) 13.2 (12.3) 63.1 (57.9) 69.3 (68.4) 27.2 (32.7) 17.5 (19.3)
Scandentia 5.9 (5.9) 9.1 (9.1) 35.3 (23.5) 36.4 (18.2) 58.8 (70.6) 54.5 (72.7)
Soricomorpha 5.4 (5.4) 0.0 (0.0) 76.8 (64.3) 100.0 (100.0) 17.9 (30.4) 0.0 (0.0)
All orders 8.2 (7.5) 8.1 (7.3) 59.1 (51.6) 65.8 (60.9) 32.7 (40.9) 26.1 (31.8)

Results obtained considering EOOs only are given in parenthesis. Threatened species include critically endangered, endangered, vulnerable,
and near threatened. The percentages are calculated considering the number of species in Table 1.

pattern was found considering total and partial gap species 4. Discussion
potential richness calculated using EOOs only (Fig. 2a in the
Appendix 1), with the exceptions of North Vietnam and Min- Our study represents an important contribution to mammal
danao (Philippines), whose potential species richness was conservation in Southeast Asia. It provides a new and com-
higher. plete dataset on all mammal species of the region and pre-
Total gap species were distributed throughout the study sents a synthetic view of the conservation status in relation
area (Fig 3b), from the extreme north of Myanmar to the SE to the network of existing PAs. Several multi-species gap anal-
coast of Papua New Guinea. Many small islands (among yses have been carried out globally (e.g. Rodrigues et al.,
which Tawitawi, Dinagat, and Camiguin in the Philippines, 2004a) or on a sub-continental scale (e.g. Fjeldså et al., 2004;
Natuna Besar, Simeleu, Sangir, and Peleng in Indonesia, Obi, De Klerk et al., 2004) but no comprehensive gap analysis has
Kai, and Aru among the Moluccas) hosted total gap species. ever been performed for the Southeast Asian region. More-
A particularly important case is in the Mentawai archipelagos over, extensive modeling of species distribution has been ap-
(particularly Sipura and North Pagai), west of Sumatra, where plied at national level (e.g. Maiorano et al., 2006) or for other
the highest number of total gap species (five species) was continents (e.g. Rondinini et al., 2005), but no systematic ef-
found. Considering total gap species richness calculated fort has ever been applied to the Southeast Asian region.
using EOOs only (Fig. 2b in Appendix 1), the general pattern Many international conservation efforts have considered our
is almost the same, with the main exceptions of Central Prov- study area (McNeely et al., 1990; Olson and Dinerstein, 1998;
ince in Papua New Guinea and of the mountain range be- Myers et al., 2000; Wikramanayake et al., 2002) and many dif-
tween Irian Jaya and Papua New Guinea where no total gap ferent PAs have been established (currently more than 1700
species was present. according to the WPDA, 2006). Although the effectiveness of
The areas with the highest number of partial and total gap networks of PAs in protecting biodiversity is often debated
species classified as threatened (Fig. 3c) are mainly located in and different studies have produced different results (e.g.
Sulawesi, in Malaysian Borneo, and in the Mentawai islands. Bruner et al., 2001 vs. Sodhi et al., 2004a), in Southeast Asia
Considering mainland Southeast Asia, the Annamite Moun- the contribution of PAs to conservation of an important taxo-
tains and the Malay Peninsula (Malaysia) have a particularly nomic group such as mammals has never been tested. Our
important role. Also in this case, the potential richness pat- analysis clearly indicates that the existing PAs are inadequate
tern obtained considering EOOs only was almost the same in assuring the conservation of mammals across the region.
(Fig. 2c in Appendix 1), with higher richness values in West We based our results both on deductive distribution mod-
Java and in Mindanao, Negros and Mindoro (Philippines). els and on extents of occurrence, with a few discrepancies
Most of the species whose conservation target was com- among the two analyses as already discussed in Rondinini
pletely met have a relatively large distribution range (Fig. 4a). et al. (2005) and Loiselle et al. (2003). Deductive distribution
On the contrary, total gap species (Fig. 4b) have a small to models have been successfully used elsewhere (Rondinini
medium distribution range, a distribution which is similar to et al., 2005; Maiorano et al., 2006, 2007) reducing the level of
that of the species completely enclosed in PAs (Fig. 4d). commission errors that is naturally present in species distri-
2738 B I O L O G I C A L C O N S E RVAT I O N 1 4 1 ( 2 0 0 8 ) 2 7 3 0 –2 7 4 4

Fig. 3 – (a) Potential gap species richness calculated as the sum of each species’ area of potential presence (EOO or DM)
considering only total and partial gap species; (b) potential presence of total gap species (EOO or DM); (c) potential threatened
gap species richness calculated as the sum of each species’ area of potential presence (EOO or DM) considering only total and
partial gap species that were classified as critically endangered, endangered, vulnerable or near threatened. Maps a and c are
represented using a histogram equalize stretch in ArcGIS and report the actual ranges of potential richness values. The list of
total and partial gap species can be found in the Appendix 2 available online.
B I O L O G I C A L C O N S E RVAT I O N 1 4 1 ( 2 0 0 8 ) 2 7 3 0 –2 7 4 4 2739

Fig. 3 (continued)

bution maps (Guisan and Zimmermann, 2000; Scott et al., We found no particular bias in the validation results with
2002; Loiselle et al., 2003; see Jetz et al. 2008 for an analysis reference to the different taxonomic groups. The only excep-
of the ecological correlates). However, there is no inherent tion were the Chiroptera, for which we obtained better valida-
assurance that a distribution model portrays reality (Guisan tions than expected, and the Primates for which the
and Zimmermann, 2000; Johnson and Gillingham, 2004) and proportion of validated species was lower than expected.
a model that poorly represents the presence of a species Clearly, the positive results obtained for Chiroptera are linked
may result in harmful conservation and management actions to the higher quality of the validation points; for almost all
(Loiselle et al., 2003; Wilson et al., 2005). Therefore, model val- the species of Chiroptera considered for validation, we ob-
idation is an essential step in any application of models to tained presence locations from data collected in the field
conservation, and it is an important component of our study. (mainly captures and scientific observations). Considering
We were able to perform a validation analysis for only 21% of Primates, most of the validation points were of lower quality
all the distribution models that we developed (190 out of 901 (if compared with those available for Chiroptera), being col-
distribution models), but we were able to cover a wide taxo- lected mainly through interviews and often located close to
nomic range (12 out of 17 orders), a wide geographic range small patches of suitable habitat (observed directly in the
(from Thailand to Philippines/Sulawesi), and we represented field) that are almost invisible at the scale of our distribution
the distribution patterns of all mammal species. Moreover, model.
the results of the validation process can be considered to be We have provided no measure of commission or omission
positive. The distribution models predicted potential pres- error associated to our distribution models. Both types of er-
ence significantly better than random at the a = 0.05 for rors are important in any conservation planning exercise,
22.2% of the species, and for only 4.2% of the species were with omission errors that affect the comprehensiveness of a
the models significantly worse than random at the same level network of PAs, and commission errors that affect represen-
of significance. For all other distribution models, no statisti- tativeness and adequacy of a reserve network (Rondinini
cally significant result was found, either for the large percent- et al. 2006a). No direct measure of the commission error rate
age of suitable areas in the models or the low number of was possible with out dataset, and yet it has been argued that
available points of presence. conservation decision makers should prefer models that min-
However, raising the significance level to a = 0.1, the per- imize commission errors because such errors lead to the
centage of distribution models which portray species distri- selection of reserves that do not actually contain the target
bution worse than random was almost stable (6.3%), while species (Loiselle et al. 2003; Rondinini et al. 2005; Jetz et al.
almost 41% of the models can be considered to be signifi- (2008)) have demonstrated that EOOs can overestimate the
cantly better than random. We can conclude that our models real range occupancy (conditional on EOO size) with propor-
represent a reasonable baseline for conservation planning at tions going from 0% to 91%, with an average of 39%. However,
the scale of our study area. Jetz et al. (2008) performed their analyses on birds in North
2740 B I O L O G I C A L C O N S E RVAT I O N 1 4 1 ( 2 0 0 8 ) 2 7 3 0 –2 7 4 4

(a) area of potential presence x protection error rate cannot be considered negligible and that it may
100

10 have relevant consequences in gap analyses (Rondinini et


partial gap
covered al., 2006). However, we used two general approaches to esti-
80

mate the frequency of gap, partial gap, and covered species,


% protected

one using EOOs only and the other using a combination of


60

DMs and EOOs. The results of these two approaches should


40

5 provide a range of reasonable estimates that likely brackets


20 12 the true value of the parameter of interest. In fact, while
0
20

90
60
estimates based on EOOs only should minimize omission er-
10
5 rors at the cost of potentially high commission errors, esti-
30 30 20 10 5
0

1 2 3 4 5 6 7 mates based on a combination of DMs and EOOs should


log area of potential presence (km2) reduce commission errors at the expenses of higher omis-
sion errors.
number of species

(b) 0% protected
A further point regarding our distribution models and ex-
tents of occurrence calls for caution in the interpretation of
0 15

our results. We have produced (validated) estimates of habitat


1 2 3 4 5 6 7 suitability and reliable maps of distribution ranges but we do
log area of potential presence (km2) not have any insurance that the species are effectively pres-
ent in their entire EOO or even in the suitable part of their
number of species

(c) 20% protected


EOO only. This is the well-known problem of the ‘‘empty for-
0 75 150

est syndrome’’, with large animals (mainly primates, carni-


vores and ungulates) that are extinct in vast areas of their
former EOO because of commercial hunting, even if the vege-
1 2 3 4 5 6 7
log area of potential presence (km2) tation is still intact (Redford, 1992; Milner-Gulland et al., 2003;
Corlett, 2007). This can have profound influences on our re-
number of species

(d) 100% protected


sults, as it can be demonstrated considering the case of the
0 10 20

banteng (Bos javanicus) and of the Hose’s lead monkey (Presby-


tis hosei). According to our results (see the Appendix 2 and
consider the distribution model) the representation target
1 2 3 4 5 6 7
log area of potential presence (km2) for the banteng is more than met (123% of the representation
target is covered by PAs). However, the species is gone from
Fig. 4 – (a) Number of species for each class of range size and most of the highly suitable areas (even though Java still repre-
for each class of proportion of area of potential presence sent one of the species’ stronghold), mainly because of illegal
inside protected areas (EOOs plus DMs). The grey area hunting for the trade in horns (Hedges, 2000; Steinmetz, 2004).
represents the protection target we set for species. Isolines In the case of the Hoses’s leaf monkey the representation tar-
enclose areas with equal numbers of species (dotted lines get is almost completely met (87% according to our results)
620 species, continuous lines >20 species). (b) Number of but a recent report (Nijman, 2005) outlines that hunting for
total gap species for each range size class. (c) Number of medicinal bezoar stones have produced local extinction of
species for each range size class with 20% of their area of the species even in highly suitable areas as the huge and re-
potential presence protected. This graph corresponds to the mote Kayan Mentarang National Park in Indonesia. However,
peak number of species in (a). (d) Number of species for each our results are still extremely important, because we provide
range size class with 100% of their area of potential at least an estimate of how much suitable habitat remains in
presence protected. Same results (not shown) were obtained relation to the existing PAs, an estimate that suffers with low-
for EOOs only. er commission errors if compared to the original EOO (the
representation target met as measured using the EOOs is
180% for the banteng and 130% for the Hoses’s leaf monkey)
America, South Africa and Australia. We performed our anal- and that is important for planning from the standpoint of po-
yses on mammals in South East Asia, with a much smaller le- tential recovery for populations.
vel of knowledge on species ecology and distribution, As in any gap analysis, our results heavily depend on the
particularly for Rodentia, Soricomorpha, and Chiroptera that dataset and on the pre-determined representation targets.
make up 71% of our sample. Thus we can assume that the In particular, even though we applied a representation target
commission error associated with the distribution models is that has been used in the previous studies, we are not explic-
much smaller if compared to the commission error associated itly accounting for species viability (Svancara et al., 2005).
to the available EOOs, probably with a proportion that is Even considering all the inherent limitations and uncer-
greater than that measured by Jetz et al. (2008). tainties that characterize analyses on a large scale and our
The omission error rate can be easily obtained from the dataset, our results give a clear indication of important pat-
percentages of agreement that we calculated during the val- terns in the current distribution of mammals in Southeast
idation procedure. In particular, an average 32% (standard Asia. The analysis of potential species richness demonstrates
deviation = 21%) of the occurrence points were not covered that many large areas are still potentially occupied by a high
by suitable areas in the DMs. We recognize that the omission number of species, even though many of the flat areas, where
B I O L O G I C A L C O N S E RVAT I O N 1 4 1 ( 2 0 0 8 ) 2 7 3 0 –2 7 4 4 2741

most of the human pressure is concentrated, are relatively 34% of the species were partial gap, while we found that
poor in mammal species. Particular caution is necessary in 52–59% of the species were partial gap. Our results were ob-
considering the results on potential weighted species rich- tained using both distribution models and EOOs, while
ness. In fact, the areas of high species richness located at Rodrigues et al. (2004a), besides considering a different study
the boundaries of our study area are probably influenced by area and working on a different scale, used species’ EOOs
the presence of species that have a much wider distribution only, introducing a greater proportion of commission errors
outside of our study area but that seem to have a small range in their analyses (Rondinini et al., 2005). This difference
when considering only the zone within our study area. For clearly explains the smaller percentage of partial gap species
example, this is the case of the tufted deer (Elaphodus cephalo- (Loiselle et al., 2003; Rondinini et al., 2005) and provides an
phus), a total gap species, and of the red panda (Ailurus ful- indication that our results might be more reliable for conser-
gens): both species occupy a tiny range in northern vation applications.
Myanmar, but outside of our study area the first is distributed The results we obtained for partial gap species are obvi-
throughout central and southern China and the latter occurs ously important for the identification of areas in need of fur-
in Nepal, India, Bhutan, and South China. However, the areas ther attention from the conservation community, but the
with high potential weighted richness in the smaller islands results we obtained for total gap species are particularly
and in the central parts of our study area are clearly an indi- important. In fact, we found a relatively low number of spe-
cation of important centers of restricted species ranges. For cies that are total gaps (8.2–7.5% of the species). Yet a con-
example, at least 15 endemic species are present in the Men- siderably higher number of mammal species of the region
tawai archipelago, with one Chiroptera species (classified as are classified as threatened according to the IUCN red-list
data deficient) that is total gap, five threatened and gap Pri- criteria. In fact, 34% of all 1086 species considered in the
mates species (among which the total gap and critically SAMD database are listed in the IUCN red-list categories as
endangered Macaca pagensis and the partial gap and critically critically endangered, endangered, vulnerable, or near threa-
endangered Simia concolor), eight threatened and gap Rodentia tened, while 45% are classified as least concern and 21% as
species (among which the total gap and endangered Hylopetes data deficient or not evaluated, thus being potential candi-
sipora), and the endangered and total gap Tupaia chrysogaster. dates for a threatened category (red-list category assess-
We have also shown that an important number of species ments reviewed during the five workshops; note that not
are not covered by any PAs. These species are distributed all the species assessments have already been officially con-
throughout the entire study area and their conservation calls firmed by IUCN).
for the creation of new PAs that can contribute to filling the This is clearly an indication that PAs cannot be considered
existing conservation gap. This would be particularly impor- as the ending point of our conservation strategies. Defining
tant for total gap species over small islands, where species PAs is an option that can be pursued relatively easily in many
survival is often endangered by the presence of introduced situations. However, managing effective PAs for conservation
species as well as habitat vulnerability and other factors (Pur- is much more difficult and expensive than just establishing
vis et al., 2000; Sodhi et al., 2004b). them and different studies have indicated that PAs in the tro-
Considering gap species, many small semi-natural areas pics usually act as ‘‘paper parks’’ (Schwartzman et al., 2000;
surrounded by cultivated areas, both in the mainland and in Curran et al., 2004; Fuller et al., 2004; Sigel et al., 2006; Sodhi
the larger islands, should be considered for the establishment et al., 2006b; Verburg et al., 2006; Gaveau et al., 2007; but see
of new PAs or, better, for the implementation of effective Bruner et al., 2001; Nagendra et al., 2004; Nepstad et al., 2006).
management plans, but clearly Papua New Guinea (where Moreover, for a number of species PAs do not ensure prop-
many total gap species occur), Sulawesi, and the internal er conservation (Corlett, 2007). Notable examples can be
mountainous areas represent the areas with the highest con- found among many different taxa, going from the Asian ele-
servation priority (Fig. 3). Particular attention should be phant (Elephas maximus), to rhinos (Dicerorhinus sumatrensis
placed towards species like the saola (Pseudoryx nghetinhensis), and Rhinoceros sondaicus), orangutans (Pongo pygmaeus and
a highly distinctive monotypic genus first described 15 years Pongo abelii), pangolins (Manis spp.) to many other taxa (Cor-
ago (Dung et al., 1993) that is highly endangered because of lett, 2007) for which PAs have not been able to stop population
habitat loss and hunting (Timmins et al., 2007): almost half declines.
of its range is covered by PAs but all the necessary efforts In this context, it is clear that the role of existing PAs, as
should be made to extend protection to the entire range of well as the establishment of new PAs, should be considered
the species along the Annamite mountains (Vietnam–Laos in a broader framework of all local ecological and socio-eco-
borders) where the last know populations of the species occur nomic trends, including the growing human population,
at extremely low densities. growing economy and infrastructure development. PAs alone
Our results are comparable in some ways to those ob- cannot be the solution to all conservation problems. In fact,
tained by Rodrigues et al. (2004a), who identified some of we should also focus on off-reserve management and the
the most important areas for the conservation of mammals preservation of natural processes.
in Southeast Asia. Rodrigues et al. (2004a) developed two
possible global scenarios and found that 5.5–11% of all mam-
mal species were not covered by any PA, a percentage that is Acknowledgements
similar to our 8.2–7.5% of total gap species. However, for par-
tial gap species, our results are different: using the same A great number of people and organizations supported the
representation target, Rodrigues et al. (2004a) found that project throughout its implementation. It is impossible to list
2742 B I O L O G I C A L C O N S E RVAT I O N 1 4 1 ( 2 0 0 8 ) 2 7 3 0 –2 7 4 4

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