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CONSERVATION BIOGEOGRAPHY OF TERRESTRIAL
MOLLUSCS ON TROPICAL LIMESTONE KARSTS
REUBEN CLEMENTS
(B. Sc.(Hons.), NUS
A THESIS SUBMITTED
FOR THE DEGREE OF MASTER OF SCIENCE
DEPARTMENT OF BIOLOGICAL SCIENCES
NATIONAL UNIVERSITY OF SINGAPORE
i “By great perseverance the snail reached the ark.”
Charles Haddon Spurgeon (1834 - 1892)
ii Acknowledgements
This project was kept afloat by research grants from the Singapore Zoological Gardens, the
National University of Singapore (R-154-000-264-112, R-154-000-222-112), and research permit No. 1773 from the Economic Planning Unit, Prime Minister’s Office, Kuala
Lumpur, Malaysia, which was graciously facilitated by Munirah Abdul Manan. I am very appreciative to Prof. Peter Ng and Prof. Navjot Sodhi for sheltering me in their labs and allowing me to purse my research interest. I am also grateful to Chan Sow Yan for introducing me to limestone hills of Kelantan at the age of 19, Lahiru Widjesa and
Ragothaman Balaji for their invaluable assistance in the field, Tony Whitten for his constructive comments, Elery Hamilton-Smith, Olivier Gargimony and John Sha for granting permission to use their base maps, and Mom & Dad, Charlene Yeong, David
Wilcove, Isvary Sivalingam, Jaap Vermeulen, Kathy Su, Koh Lian Pin, Matthew Lim,
Mary Posa, Rachael Tan, the Ecology and Systematics Lab, and the army of snail sorters for their generous help and support.
iii Table of Contents
Page
Acknowledgements iii
Table of contents iv
Summary vi
General introduction 1
Chapter 1: Limestone karsts: imperiled arks of biodiversity 4
1.1 Biodiversity arks 4
1.1.1. Surface flora 4
1.1.2. Surface fauna 6
1.1.3. Cave fauna 8
1.2. Importance to humanity 10
1.3. Anthropogenic threats 12
Chapter 2: Conservation biogeography of terrestrial molluscs on karsts 15
2.1. Materials and methods 16
2.1.1. Study area 16
2.1.2. Sampling protocol 16
2.1.3. Sorting and identification 17
2.1.4. Statistical analyses 18
2.2. Results 21
2.3. Discussion 23
Chapter 3: Implications and challenges for karst conservation in Southeast Asia 27
3.1. Implications 27
iv 3.2. Challenges 29
3.2.1. Resource shortages 29
3.2.2. Ad-hoc conservation planning 30
3.2.3. Inadequate protection 31
3.2.4. Deficient baseline data 33
General conclusion 35
References 36
Figures 50
Tables 63
Appendix 71
v Summary
In the first chapter, I perform a literature review to show that limestone karsts are considered ‘arks’ of biodiversity and elaborate on their importance to humanity and increasingly threatened status. Although karsts require greater protection due to their high levels of endemism, reserve location is not always performed within a scientific framework. Conservation planners must incorporate biogeographical patterns of karst- endemic species into their decision making processes, but such information is severely lacking. In the second chapter, I identify biogeographical variables (i.e., karst area, isolation, surrounding soil type and geological age) hypothesised to correlate with endemic richness of terrestrial molluscs on karsts, and investigate molluscan species compositional trends across karsts in two different biogeographical regions: Peninsular Malaysia and
Sabah. Generalized linear mixed-effect models revealed an important contribution of karst area and surrounding soil type on molluscan endemic richness, while non-metric multi- dimensional scaling showed that karsts separated by vicariant barriers in different parts of
Peninsular Malaysia and Sabah had distinct malacofaunas. In Malaysia, large karsts surrounded by podzolic soils within biogeographically distinct groups of karsts should therefore be conserved to maximise the protection of endemic molluscs. Having identified karst area as an important predictor of endemic richness, I utilized this information to create irreplaceability and vulnerability maps for karsts in the final chapter. These maps indicated that 10 out of 62 karsts in Peninsular Malaysia should be prioritized for conservation. In addition, I discuss how regional karst conservation initiatives are complicated by issues such as resource shortages, ad-hoc conservation planning, inadequate protective measures and deficient baseline data.
vi General introduction
Humans are extracting natural resources at unprecedented levels. About half the world’s
original forest cover has already been cleared for agriculture and forest products, and
another 30% has subsequently become degraded or fragmented (UNFPA 2004). If the
current pace of habitat loss continues, species extinctions in many areas may reach
catastrophic levels (Sodhi & Brook 2006). To mitigate such a disaster, scientists are
identifying areas within ‘biodiversity hotspots’ (i.e., regions exceptionally rich in
endemic species and facing massive habitat loss; Myers et al. 2000) for priority
conservation. Economically valuable ecosystems within ‘hotspots’, however, may not be
adequately protected due to vested commercial interests, weak legislation and/or deficient
biological data. Limestone karsts are examples of ecosystems in this predicament.
Limestone karsts (hereafter referred to as karsts) are defined as sedimentary rock
outcrops that comprise primarily of calcium carbonate. Most karsts were, in fact, formed millions of years ago by calcium-secreting marine organisms (e.g., corals and brachiopods) before tectonic movements lifted them above the sea level. Over the years, the softer sediments covering these karsts were removed by mechanical and chemical
weathering. This process usually produces ‘tower’ and ‘cockpit’ karst formations in the
tropics. Tower karsts are characterized by tall, precipitous (60° to 90° gradient) cliffs
riddled with caves and sinkholes (Fig. 1a), while cockpit karsts are generally cone-
shaped and have gentle slopes (30° to 40° gradient) (MacKinnon et al. 1996).
In Southeast Asia, karsts cover an area of around 400,000 square kilometers (km2)
with geological ages ranging from the Cambrian to the Quaternary (Day & Urich 2000).
Karsts in this region, which are most extensive in Indonesia, Thailand, and Vietnam (Fig.
1 2), possess impressive geological features such as the world’s largest cave chamber
(Good Luck Cave in Sarawak, Malaysia) and one of the world’s longest underground rivers (St Paul Subterranean River in Palawan, Philippines).
On the highly fragmented Sunda Shelf, karsts have formed ‘islands within islands’ and are considered biodiversity ‘arks’ or reservoirs (Schilthuizen 2004) due to their high levels of species endemism. Despite their importance to humanity (which will be discussed below), karsts in Southeast Asia continue to be negatively impacted by anthropogenic disturbances. Conservation planning for karsts has also been lacking in scientific basis, in part due to the paucity of biogeographical information (e.g., endemic richness patterns) on karst biodiversity. As such, planners are often unable to distinguish karsts that require urgent conservation action.
Terrestrial molluscs are a tractable and highly representative taxon for biogeographical studies given their patterns of high allopatric diversity and endemism
(Solem 1984, Tattersfield 1996, Seddon et al. 2005). Furthermore, the persistence and uniqueness of mollusc shells facilitate relatively easy sampling and identification
(Emberton et al. 1999). Tropical karsts are generally considered evolutionary hotspots for speciation for terrestrial molluscs, (Davison 1991, Schilthuizen 2000). Karsts are also known to support high species densities of molluscs due to the availability of copious quantities of calcium, a mineral essential for their growth and reproduction (Graveland et al. 1994).
I have three main objectives in this thesis. First, I show that karsts are biologically important ‘arks’ under serious threat from human activities. Next, I discuss how I sampled terrestrial molluscs on different karsts to: (1) identify correlates of endemism
2 from a set of important biogeographical factors (i.e., karst area, isolation, surrounding soil type and geological age); and (2) investigate how species compositions vary among different karsts in two biogeographical regions in Malaysia. Finally, I use results from the biogeographical analyses to identify karsts in Peninsular Malaysia for urgent protection in order to maximize the probability of conserving the highest numbers of endemic species. In addition, I will address challenges facing karst conservation within the region and suggest possible mitigation measures.
3 Chapter 1: Limestone karsts: imperiled arks of biodiversity
1.1 Biodiversity arks
High species diversity on karsts can arise from the presence of numerous ecological
niches afforded by complex terrains (e.g., fissured cliffs and extensive caves) and
variable climatic conditions. High species endemism can also occur on karsts with
different tectonic and eustatic histories, degrees of isolation, and incidences of random
events. Karsts can be divided into surface and cave levels, both of which provide ideal
conditions for speciation. On karst surfaces, edaphic (i.e., soil-related) isolation produces
a unique flora that includes many calcicoles (i.e., species adapted to growing on
limestone). At the same time, such vegetation supports animal species somewhat
different from those in non-karstic areas. Due to their poor dispersal capabilities, both
plants and animals such as invertebrates have to adapt to highly alkaline conditions, thin
soil layers, and desiccation on porous limestone bedrock. In caves, animals such as
arthropods and fishes must evolve specializations to cope with fluctuating levels of light,
water quantity, temperature, humidity, gas concentrations, and organic material (Culver
et al. 2000). Examples of karst-associated taxa and their levels of richness and endemism
are discussed below.
1.1.1. Surface flora
The presence of a variety of karst microhabitats can support high floral diversity. For
example, the slopes and gullies of some karsts have greater soil depths that sustain large
trees such as dipterocarps, while rock faces and summits with thinner soil layers are usually colonized by herbaceous species (e.g., aroids, balsams, begonias [Fig. 3a],
4 gesneriads, pandans, and slipper orchids) and bryophytes (Kiew 2001). Abiotic factors
also exert strong influences on the composition of karst vegetation. In Sarawak, karsts in
high precipitation zones are usually covered by acidic peat soils that support plants unlike
those typically associated with limestone substrates (e.g., casuarinas and pitcher plants),
while cool temperatures at high-altitude karsts (e.g., the Api and Benarat karsts of around
1700 m) can support submontane species dissimilar from those found on karsts at lower
altitude (Kiew 1991). High floral richness has been recorded from karsts in Southeast
Asia. In Peninsular Malaysia, around 1216 angiosperm species or 14% of the total
Malayan flora can be found on karsts (Chin 1977). The karsts of the Bau district in
Sarawak also contain a large proportion (15% to 60%; Fig. 4) of regional limestone plant, moss, and orchid species (see Yong et al. 2004). Current figures of karst floral richness,
however, may be underestimated due to the difficulty of sampling inaccessible areas such
as cliff faces and summits. Using data sets of understory flora and summit trees from 20
karsts in Bau (see Yong et al. 2004), I showed that numerous species remain
undiscovered even after 30 months of sampling, as observed and estimated species for
both plant groups were still rising and showed no sign of converging (Fig. 5). Isolation
within edaphically unusual karsts also exerts strong selective forces, which may lead to
the evolution of endemic plant species (Kruckeberg & Rabinowitz 1985). Numerous
species of bryophytes (Mohamed et al. 2005) and vascular plants (Kiew 1991,
MacKinnon et al. 1996, IUCN 2000, Kiew 2001) are restricted to karsts in Southeast
Asia. In Peninsular Malaysia, 21% of 1216 karst-associated plant species are endemic to
the peninsula and 11% are strictly confined to karsts (Chin 1977). Proctor et al. (1982)
have also shown the floral composition of karsts to be quite unique; 60% of the 73 plant
5 species recorded from the Mulu karsts in Sarawak could not be found in other lowland forest types. Botanical expeditions to remote karst areas continue to uncover endemic plants new to science. In Vietnam, biologists recently described a critically endangered genus of conifer (Xanthocyparis vietnamensis) that appears confined to karsts (Farjon et al. 2002).
1.1.2. Surface fauna
Invertebrate groups on karst surfaces can be very speciose. A recent survey showed that a significant proportion (19% to 40%; Fig. 4) of regional butterfly, macromoth, and phasmid species inhabit the Bau karsts of Sarawak (see Yong et al. 2004). Landsnails, in particular, flourish on karsts because the calcium-rich soils favour their growth and reproduction (Graveland et al. 1994). One subgenus (Plectostoma [Fig. 3b]) even shows obligate calcicoly (dependency on calcareous substrates for survival), with all 44 Bornean species recorded only from karsts (Schilthuizen 2004). In Malaysia, around 80% of the total landsnail fauna occur on karsts that comprise less than 1% of the country’s land area
(Schilthuizen 2000). Landsnail endemism peaks on karsts due to their low dispersal capabilities and isolation effects, both of which facilitate radiation at small spatial scales
(Schilthuizen et al. 1999). Among just eight selected landsnail genera, a large number of species (78) were found to be site-endemics (species restricted to single isolated karsts) in
Peninsular Malaysia (Davison 1991). In Borneo, the small (0.2 km2) Sarang karst contains at least six site-endemics, while no less than 50 species are endemic to the large
(15 km2) Subis karst (Vermeulen & Whitten 1999). Other invertebrates such as butterflies also exhibit endemism on karsts, albeit to lesser degrees. For instance, the montane
6 butterfly fauna at the Mulu karsts in Sarawak has more endemic species (possibly due to
specificity for karst-associated host plants) than nearby sandstone outcrops (Holloway
1986).
Vertebrates are relatively well represented around karsts. For example, birds are known to utilize limestone crags for refugia and breeding grounds; high avifaunal richness (129 species from 40 families) was recently recorded from the Bau karsts in
Sarawak (see Yong et al. 2004). Considerable percentages (14% to 22%; Fig. 4) of the total fish, amphibian, snake, and mammal species in Sarawak and Borneo were also found on the same karsts (see Yong et al. 2004). As most vertebrates have high dispersal capabilities, only a few mammals (e.g., François’s leaf monkey [Trachypithecus francoisi] and the Serow [Capricornis sumatraensis]) and birds (e.g., the limestone wren- babbler [Napothera crispifrons]) are believed to be restricted to karsts. Nevertheless, the
potential of discovering new vertebrate taxa at poorly sampled karsts remains quite high.
Recently, the Khammouan karsts in Laos yielded a new mammal family (Laonastidae)
and two new genera of rodents (Laonastes and Saxatilomys), both of which appear
morphologically suited for karstic terrain (Musser et al. 2005). Fishes, on the other hand, are subjected to stronger evolutionary pressures in isolated water bodies. For example, the ichthyofauna of Inlé Lake in Myanmar, which is situated on a limestone plateau 1000 m above sea level, comprises several endemic cyprinid genera (e.g., Inlecypris and
Sawbwa) and species (Annandale 1918).
7 1.1.3. Cave fauna
The relative stability and antiquity of subterranean ecosystems enable relict faunas to
persist (Gibert & Deharveng 2002). In Sarawak, some of the 200 cave species found in
the Mulu karsts belong to ancient animal groups that have mostly disappeared from the
surface (IUCN 2000). On the other hand, the ecotone at the epigean-cave interface can
also generate cave-adapted species (e.g., the endemic landsnail Georissa filiasaulae) that
remain parapatrically (species with contiguous but non-overlapping geographic distributions) connected with their ancestors on the surface (Schilthuizen et al. 2005a).
Invertebrates make up the majority of cave faunas and due to their sheer diversity, surveys consistently yield new genera and species from Southeast Asian karsts (Juberthie
& Decu 2001). In just three hours of sampling a well-documented karst cave in
Peninsular Malaysia, 28% of the 53 invertebrate species collected by Dittmar et al.
(2005) were new records and a further 6% were likely to be new to science. In karst caves, most invertebrates (e.g., flies, cockroaches, and snails) primarily or ultimately depend on guano for food and several arthropods such as glyphiulid millipedes and aderid beetles are even restricted to life on guano piles (Deharveng & Bedos 2000).
Primary consumers such as raphidophorid crickets can reach giant proportions (e.g., in the Mulu karsts; Chapman 1982), which are in turn consumed by larger cave predators
(e.g., centipedes, whip-scorpions, and crabs). Some invertebrates complete their life cycles entirely within caves (troglobites) and most have undergone regressive evolution.
The troglobitic crab, Cancrocaeca xenomorpha (Fig. 3c), from the Maros karsts in
Indonesia are characterized by ocular degeneration, pale coloration and abnormally long appendages after years of isolation in perennial darkness (Ng 1991). Despite the poor
8 sampling effort, troglobitic richness in Southeast Asia (16 to 28 species per cave, n = 4,
Deharveng & Bedos 2000) appears to be higher than in other well-sampled tropical regions (≤ 14 species per cave, n > 100, Central America, Peck & Finston 1993). Surveys of karst caves in Southeast Asia have hinted at high levels of troglobitic endemism, particularly among isopods, diplopods, and collembolids from the genus Trogolopedetes, which has around 12 species restricted to the caves of western Thailand (Deharveng &
Bedos 2000). Crabs of the genus Orcovita are also known to be endemic to anchialine
(marine or brackish water bodies lacking surface connection to the sea) karst caves in countries such as the Philippines (Ng et al. 1996).
Bats are probably the most conspicuous cave-dwelling vertebrates, as they prefer caves to other roosting habitats (Hutson et al. 2001). The Mulu karsts have one of the region’s richest bat faunas (28 species) and more than a million wrinkle-lipped bats
(Chaerephon plicata) occupy a single cave alone (IUCN 2000). Swiftlets roosting in caves can also reach staggering numbers, with around 300,000 individuals occurring at the Niah karsts (Lim & Cranbrook 2002). Due to their isolation from surface streams, fishes are probably the only vertebrates truly endemic to karst caves and many species possess bizarre morphological and behavioral adaptations. Since 1988, 13 cave-restricted fishes have been described from the karsts of five Southeast Asian countries, including a highly depigmented and blind cave loach (Cryptotora thamicola) from Thailand that climbs onto rocks using its large lateral fins (Kottelat 1988). Apart from several reptilian taxa (e.g., geckos, skinks, and snakes), other vertebrates found exclusively in karst caves include the world’s smallest mammal (the bumblebee bat [Craseonycteris thonglongyai]),
9 which has a skull size of only 11 mm and inhabits a few karsts in Kanchanaburi, Thailand
(Hill 1974).
1.2. Importance to humanity
Karsts are mainly exploited for limestone, an important mineral with over 100 industrial
uses (see Davison 2001) that include the production of cement and marble products.
Several karst species are commercially valuable as well. Rare slipper orchids are often
sold or hybridized on a large scale in the billion-dollar orchid industry, while endemic cycads, palms and various herbaceous plants (e.g., Chirita and Paraboea) are sought- after by horticulturalists (Kiew 1991). Nests built by swiftlets (e.g., Collocalia
fuciphagus and C. maximus) on karst cave walls are highly prized in Asian culinary
delicacies. At 15 caves in the Gomantong karsts of Sabah, nest yields of around five tons
can fetch more than US$2.5 million annually (Lim & Cranbrook 2002). Guano deposited
by bats and swiftlets onto cave floors are also harvested for fertilizer. At the Niah karsts,
for example, the Sarawak Museum operates a cooperative to sell guano to local black
pepper fields (MacKinnon et al. 1996).
Services provided by karsts and their biodiversity are less tangible but significant
nonetheless. Karsts readily store rain and apart from maintaining the hydrological
integrity of a watershed (MacKinnon et al. 1996), they also serve as sources of
groundwater for consumption and irrigation. In Indonesia, quarrying caused water
shortages in human settlements because rain flowed directly into underground streams
that emptied into the sea (Bambang & Utomo 2003). Animals in karst caves are known to
perform valuable ecosystem services. Bats pollinate and disperse the seeds of many
10 economically important plants. In the Niah karsts, resident populations of cave nectar
bats (Eonycteris spelaea) are vital pollinators of the durian tree (Durio), which has a
yearly market of around US$1.5 billion in East Asia (Ross 1997). Around karsts,
insectivorous bats such as the Diadem round leaf bat (Hipposideros diadema; Fig. 3d) and swiftlets also help to control agricultural pests; both these animal groups respectively consume up to 7.5 and 11 tons of insects at the Niah karsts each day (Vermeulen &
Whitten 1999).
Besides serving as natural laboratories for biogeographical, ecological, evolutionary, and taxonomic research (Ng 1991, Schilthuizen et al. 1999, Schilthuizen et
al. 2005b), karsts also have huge potential for archaeological and paleontological
discoveries (e.g., fossils of the dwarf hominid [Homo floresiensis] were recently
excavated from a karst cave in Indonesia: Morwood et al. 2004). Karsts feature
prominently in several cultures and religions as well. For example, people have used
caves as places of worship (e.g., by the Buddhists and Hindus; Fig. 1c) or burial sites
(e.g., by the Dayak people in Borneo) for several centuries. The economies of countries
such as Malaysia and Thailand ultimately benefit from cultural and religion-based
tourism, especially during important festivals held at karst temples. Similarly, many
countries have profited from tourism at karsts of high aesthetic value (e.g., the sea-
flooded karst towers of Ha Long Bay, Vietnam). By protecting and maintaining the
natural states of Niah and Mulu karsts, the state of Sarawak obtains US$80,000 from eco-
and geotourism each year (see Yong et al. 2004).
11 1.3. Anthropogenic threats
Karsts are increasingly being threatened by modern destructive practices. Large-scale
operations involving the mining of limestone (Fig. 1b) primarily threaten karst biotas
because they cause irreversible ecosystem damage (Vermeulen 1994). To estimate the
magnitude of limestone quarrying activities in the tropics, I compiled mineral statistics
over a five-year period (1999-2003) for four regions. Southeast Asia appears to have
greater mean annual increases in limestone quarrying rates (5.7% year-1; Fig. 6a) and
significantly higher (χ2 = 16.9, p = 0.001, degree of freedom = 3, Kruskal-Wallis test,
SPSS 11.5 [SPSS Inc. 2002]) mean annual limestone quarrying rates (178 million tons year-1; Fig. 6b) when compared to larger tropical regions such as Africa, South America,
and Central America (including the Caribbean). Furthermore, quarrying rates for each region are likely to be underestimates because they do not include statistics from village-
level quarries. The gravity of these figures, however, will only become clear once
remaining limestone resources for the whole of Southeast Asia have been quantified.
Nevertheless, unregulated limestone quarrying will certainly exacerbate the biodiversity
crisis in Southeast Asia, a megadiverse region that has the highest rate of natural habitat
loss among the tropics (Sodhi & Brook 2006). Site-endemic species face the greatest
extinction risk when a karst is completely quarried. Extinctions of at least 18 karst plant
species have already been documented in Peninsular Malaysia (Kiew 1991). Molluscs are particularly extinction-prone due to their poor tolerance for desiccation, low vagility, and high degrees of site-endemism (Schilthuizen 2004). In Sabah, two site-endemic landsnail species (i.e., Opisthostoma otostoma and O. decrespignyi) are presumed extinct because the karsts where they were found were demolished for an airstrip (Vermeulen 1994).
12 Land clearing for development is another major threat to karst biota. Logging
activities around karsts: (1) reduces shade and humidity and endanger sensitive plants
(Kiew 1991); (2) drives away cave-visiting animals such as mammals and arthropods that
supply organic matter to guano communities (Culver et al. 2000); (3) pollutes cave
streams and kill resident fauna; and (4) diminishes bat populations that depend heavily on
surrounding forests for foraging (Robinson & Webber 2000). The land surrounding karsts
are sometimes burnt to facilitate crop cultivation (e.g., for federal agricultural land
schemes in Malaysia; Davison 2001), but the fires resulting from such activities can
easily sweep up karst slopes. Burnt karsts subsequently experience prolonged desiccation due to higher solar radiation and are more susceptible to further fires (Schilthuizen et al.
2005b). The resulting depauperate secondary vegetation that grows on burnt karsts not only takes decades to recover (Kiew 1991, 2001), but also results in population declines in taxa sensitive to disturbance (Schilthuizen et al. 2005b).
Unsustainable collections of endemic plants of medicinal and ornamental value can also result in population extinctions, while the indiscriminate harvesting of swiftlet nests in Borneo has reduced swiftlet populations (Lim & Cranbrook 2002). Excessive nest harvesting activities may have indirectly contributed to the decline of bat populations as well; the abundance of Naked Bats (Cheiromeles torquatus) at the Niah karsts in
Sarawak fell from 30,000 to around 1000 over a 42-year period (Hutson et al. 2001).
Hunting pressure can also deplete populations of certain karst-associated animals if they
continue unregulated. Bats from karst caves are sold for consumption in the markets of
Thailand and Indonesia, while horn trophies of the threatened Serow (C. sumatraensis) can be purchased from the markets in Laos (Vermeulen & Whitten 1999). Other threats
13 to karst species include the quarrying of speleothems, insecticide use, flooding due to the
damming of nearby rivers, treasure hunting, and spelunking (see Kiew 1991, Davison
2001).
Greater protection clearly needs to be afforded to these arks of biodiversity, but conservation planning for karsts often fails to consider their biological importance. For
example, numerous karsts have been designated for quarrying based solely on their
accessibility and/or economic viability, while a few remain protected only because they
are too remote or lie deep within forest reserves. Ideally, conservation plans for karsts
should account for biogeographical patterns to prevent the over-exploitation of karsts
with potentially high numbers of endemic species.
14 Chapter 2: Conservation biogeography of terrestrial molluscs on karsts
There is a paucity of information on biogeographical patterns of karst biodiversity in
general. For example, the effects of karst area and isolation on endemism have yet to be
quantified. Schilthuizen (2004) proposed that large karsts in different areas should be
preserved to achieve greater representativeness of regional diversity, while Vermeulen
and Whitten (1999) suggested that groups of small and isolated karsts should be protected because species on such outcrops are more prone to extinction. However, these divergent opinions lack supporting evidence, so the quantification of endemism and species richness patterns among karsts is still required. The identification of the determinants of karst diversity can therefore be used to identify karsts harbouring the greatest
biodiversity. In addition, we do not know how species compositions vary across karsts at
the regional scale. Understanding such biogeographical patterns can also help reduce bias
in the location and selection of karst reserves because basing reserve design on only species richness or endemism alone does not necessarily result in the most efficient biodiversity preservation policy (Born et al., 2007).
With more than 800 limestone outcrops scattered across its landscape (Lim &
Kiew 1997, Price 2001), Malaysia is a suitable area for biogeographical studies on karst biodiversity. Most of these outcrops are de facto habitat islands because they are isolated from one other by non-calcareous substrates (Paton 1961). This spatial structure restricts gene flow between isolated karsts, with the result that certain taxonomic groups exhibit high endemicity via allopatric (van Benthem-Jutting 1958, Tweedie 1961) and/or parapatric (Schilthuizen et al. 2002) modes of speciation. We considered a species to be
15 ‘endemic’ if its range is restricted to a single karst, or a group of karsts from the same or
adjacent bodies of limestone bedrock within a particular biogeographical region (e.g.,
Peninsular Malaysia).
2.1. Materials and methods
2.1.1. Study area
I sampled 16 karsts in Peninsular Malaysia (between longitudes 100° 52' E and 102° 28'
E, and between latitudes 3° 18' N and 5° 40' N; Fig. 7; see Appendix 1) and utilized
sampling data from Menno Schilthuizen (MS), who surveyed 27 karsts in Sabah
(between 116° 10' E and 118° 44' E, and between 4° 38' N and 7° 13' N; Fig. 7; see
Appendix 2). The climate in Malaysia is typical of equatorial countries, with continuous
warm temperatures (mean annual temperature around 27°C) and high rainfall (annual
rainfall between 1400 and 4000 mm) that vary with the arrival of the northeast
(November to March) and southwest monsoons (May to September) (Framji et al. 1981).
Limestone vegetation is considered an edaphic climax formation (Symington 1943) and the canopy typically consists of trees such as Vitex, Memecylon and Garcinia, while rock exposures near the base are dominated by bryophytes, shrubs and herbs such as Begonia,
Monophyllaea and Paraboea (Crowther 1982).
2.1.2. Sampling protocol
In Peninsular Malaysia, I sampled 16 karsts during the dry southeast monsoon in July
2005 and 2006. Due to the patchy distribution of terrestrial molluscs, systematic sampling
was preferred in lieu of random sampling to achieve spatial interspersion and reduce bias
16 from segregated replicates (Hurlbert 1984, Cameron & Pokryszko 2005). At the base of each karst face, six replicate plots (4 × 2 m) were located at least 5 m apart. A plot was
located more than 5 m away from the previously sampled plot if the terrain was
unsuitable (e.g., presence of caves or cliff edges) or if it showed signs of artificial habitat
modification. Sampling involved the collection of 4 L of topsoil from the upper 5 cm
layer with a spade and a plastic measuring cup from suitable microhabitats (e.g., rock
crevices or between tree roots) within the plot. Soil samples were always collected in the
karst forest environment and never in caves. In Sabah, MS sampled 27 karsts between
March 2000 and December 2005, irrespective of the season. Sampling on these karsts
derived from a mixture of systematic and random searches done primarily for other
research projects, but sampling effort (i.e., number and size of plots) in each locality was
approximately equivalent.
2.1.3. Sorting and identification
Shells were extracted using a combination of floatation and sieving. Although this
method yielded mostly empty shells that could have belonged to individuals from
previous years (Schilthuizen et al. 2005b), these essentially provided a temporal record of
a karst’s endemic richness. Shells from Peninsular Malaysia were identified to species by
RC, while those from Sabah were identified by MS. Nomenclature follow van Benthem-
Jutting (1950, 1954b, 1954a, 1961b, 1961a) and Vermeulen & Whitten (1998).
Additional verifications were made with type specimens from the Musée National
d’Histoire Naturelle (Paris) and the Natural History Museum (London). Voucher
specimens were deposited in the Raffles Museum of Biodiversity Research (Singapore)
17 and the Universiti Malaysia Sabah’s “Borneensis” collection (Sabah). As endemism can be an artefact of under-sampling of neighbouring karsts, I sought to reduce this potential
bias by determining endemic richness of genera known for their restricted ranges
according to Tweedie (1961), Maassen (2001) and J.J Vermeulen et al. (in preparation):
Diplommatina, Opisthostoma, Gyliotrachela, Boysidia, Paraboysidia, Hypselostoma,
Alycaeus, Chamalycaeus, Rhiostoma, Sinoennea, Discartemon, Haplotychius, Arinia,
Georissa, Everettia, Atopos and Japonia.
2.1.4. Statistical analyses
Based on completeness ratios (i.e., no. of observed species/estimated species:
Soberón et al. 2000), sampling saturation was calculated for karsts in Peninsular
Malaysia, but not for those in Sabah due to the nature of the sampling design. For each
karst, expected species accumulation curves (i.e., sampled-based rarefaction curves) were
first computed based on equations derived by Colwell et al. (2004) and extrapolated to
obtain estimated species richness (to calculate completeness ratios) using the incidence-
based coverage estimator (Colwell & Coddington 1994). All curves and estimators were
computed using EstimateS Version 7.5 (Robert K. Colwell, Connecticut, USA). I
investigated the effects of area and isolation on endemic richness for karsts in Peninsular
Malaysia since sampling completeness ratios were only available for that region. I fitted
generalized linear mixed-effect models (GLMM) to the data using the lmer function
implemented in the R Package (R Development Core Team, Vienna, Austria). For each
GLMM, I coded the number of endemic species per karst as a Poisson-distributed
response variable and karst area (90 m digital elevation model from the Shuttle Radar
18 Topography Mission viewed on ArcGIS 9; ESRI, Redlands, USA), degree of karst isolation (1:25000, topographical maps, series DNMM6102), soil type surrounding karsts
(1:800000 Generalized Soil Map, Peninsular Malaysia, 1970) and karst geological age
(1:500000 Geological Survey of Malaysia, 1985) as linear predictors (fixed effects – see below), assigning each model a Poisson error distribution and a log link function.
Isolation was estimated using two metrics: either (a) the minimum straight-line distance to the nearest adjacent karst, or (b) the number of karsts within a 10-km radius of the focal karst. Area and isolation were treated as covariates, and soil type and geological age as categorical factors. Plots were replicates within a karst, so the term ‘karst’ was included as a random effect to control for repeated sampling of the same statistical unit; ; this effectively reduces the degrees of freedom to the number of karsts. Random effects models are particularly useful here because they control for spatial pseudoreplication and potential autocorrelation (Crawley, 2005). Coding the ‘isolation’ term explicitly as fixed covariate essentially accounts for spatial autocorrelation by examining the relative importance of distance among karsts on endemism patterns.
Given the relatively small number of karsts sampled (n = 16) and replicates (n =
96), I restricted our a priori model set to include only seven models that represented major thematic hypotheses to test (Table 1). These models represented particular combinations of the terms of interest, with karst area considered as a control variable in all models. I did not include the total number of species as a control variable given the expected positive relationship between karst area and total species richness (i.e., classic species-area relationships: Preston 1948, 1960, Diamond 1969, MacArthur 1972).
Furthermore, there was a rather strong univariate log-linear relationship between total
19 species richness and karst area (r2 = 0.44; ignoring the karst random effect). As such, it made little sense to include both of these highly correlated terms in each model as control variables.
An index of Kullback-Leibler (K-L) information loss was used to assign relative strengths of evidence to the different competing models and Akaike’s Information
Criterion (AICc) was used to compare relative model support given that it corrects for small sample sizes (Burnham & Anderson 2002). One could also employ other methods to compare models such as the dimension-consistent Bayesian Information Criterion
(BIC); however, BIC may only be preferable when sample sizes are large (Burnham &
Anderson 2004, Link & Barker 2006). The relative likelihoods of candidate models were calculated using AICc (Burnham & Anderson 2002), with the weight (wAICc) of any particular model varying from 0 (no support) to 1 (complete support) relative to the entire model set. For each model considered, I also calculated the percentage deviance explained (%DE) as a measure of goodness-of-fit, and compared each model’s %DE to that of the control model to examine what proportion of the variance in the response was attributable to individual terms considered.
Compositional trends of mollusc communities across karsts in two different biogeographical regions were investigated using non-metric multi-dimensional scaling
(NMDS: Kruskal 1964) on a species presence/absence data matrix using PC-ORD
Version 4.14 (MjM Software, Oregon, USA). NMDS is a distance-based ordination analysis that searches for the best positions of n entities (samples) on k dimensions (axes) that minimize the departure from monotonicity in the relationship between the original dissimilarity data of the n samples and the reduced k-dimensional ordination space of
20 these samples. NMDS is considered the most effective ordination method for ecological community data because it does not assume linear relationships and reveals the environment the way the biotic community interprets it (McCune & Grace 2002).
Ordination was done using karst species data from Peninsular Malaysia and Sabah. As some species with pan- and paleotropical distributions could have been introduced, they were excluded from both ordinations to reflect differences based only on native malacofauna. After doing an outlier analysis (Tabachnik & Fidell 1989), NMDS was run in the ‘autopilot (slow and thorough)’ mode with random starting configurations and
Sorensen (Bray-Curtis) distance as the dissimilarity measure. A Monte Carlo permutation test was done on the resulting ordinations to evaluate whether NMDS was extracting stronger axes than expected by chance. Multi-response permutation procedures (MRPP:
Mielke Jr. & Berry, 2001) were also performed to provide a non-parametric test of differences between resulting clusters from each ordination.
2.2. Results
Sampling from 16 karsts in Peninsular Malaysia yielded a total of 198 terrestrial mollusc species from 49 genera and 19 families (see Appendix 3), while 173 species from 64 genera and 23 families were sampled from 27 karsts in Sabah (see Appendix 4). Based on the completeness ratios (0.83 to 0.98; Fig. 8), sampling saturation was relatively high for each karst in Peninsular Malaysia. The two model sets using the two different measures of karst isolation (total straight-line distance to the nearest karst and number of karsts within a 10-km radius) revealed nearly identical model rankings and %DE explained, so I only reported the results using total minimum straight-line distance to the nearest karst as
21 the isolation measure. The contrasted generalized linear mixed-effects models (GLMM) revealed an important contribution of karst area (Table 2; Fig. 9) and surrounding soil type on the effect of endemic richness. The most parsimonious model had 65.6% of the
AICc weight and explained over 18% of the deviance in the total number of endemic
species per karst (of which 9.3% was explained by surrounding soil type and 8.8% by
area; Table 2; Fig. 10). Karsts with yellow-grey podzols had the highest predicted
number of endemic species, with red-yellow podzolic karsts having a neutral effect and
karsts made up of other soil types the lowest levels of endemicity (Fig. 10). Although the
next highest-ranked model contained the isolation term (wAICc = 25.7%), its addition
only accounted for another 0.4 % of the deviance explained (Table 2). All other models
had weak support (wAICc < 3.5%).
For karsts in Peninsular Malaysia, NMDS yielded a final optimum three- dimensional ordination space that collectively explained 81% of the variance in the species data. The Monte Carlo test of 400 iterations with randomized data indicated the minimum stress of the solution was lower than would be expected by chance (p < 0.05).
The final solution had a stress value of 8.79, which was considered a good ordination with no real risk of drawing false inferences (McCune & Grace 2002). Sample scores
(i.e., 16 karsts) were plotted in species space (i.e., 189 species after omitting non-native species) on the second and third axes (Fig. 11a), which represented 46 and 26% of the variance, respectively. The ordination for Peninsular Malaysia showed that karsts in the east and west regions were distinct (MRPP multiple pairwise comparison tests; p < 0.001) from each other based on their species compositions (Fig. 11a). A graphical overlay of endemic species scores on the ordination did not reveal any clear associations
22 with any group of karsts (Fig. 11b). For karsts in Sabah, sample scores (i.e., 27 karsts)
were plotted in species space (i.e., 161 species after omitting non-native species) on two
axes that explained 31 and 56% of the variance, respectively (Fig. 11c). The Monte Carlo
test indicated the minimum stress of the solution was lower than would be expected by
chance (p < 0.05). Based on this ordination, the karsts off Sabah, and karsts in the east
and west regions were also different (MRPP multiple pairwise comparison tests;
p < 0.001) from one another based on their species compositions (Fig. 11c). The overlay
of endemic species scores did not show any associations with any group of karsts (Fig.
11d).
2.3. Discussion
As predicted from studies involving species-area (Preston 1948, 1960, Diamond 1969,
MacArthur 1972, Rosenzweig 1995) and endemic species-area relationships (Hubbell
2001), area is an important determinant of both molluscan richness and endemicity on karsts. Indeed, area has been shown to be the most important factor determining terrestrial molluscan species richness on other island systems (Welter-Schultes &
Williams 1999), but my results also indicate its positive effect on endemic richness. For other taxa such as fish and orchids, area predicts both species richness and endemism as well (Ackerman et al., 2007, De Silva et al., 2007). Larger areas are believed to support
higher numbers of endemic species in other taxa (Roos et al. 2004), in part due to their
greater habitat diversity which promotes higher speciation rates (Losos & Schluter 2000).
Another aspect of the relative importance of area and isolation on mollusc endemism
23 could be investigated by comparing trends among small karsts adjacent to large karsts
versus small karsts situated far from any other karst.
The type of soil surrounding karsts appears to have an important influence on
molluscan endemic richness as well. Several studies have documented the impact of soil
qualities (e.g., pH and moisture) on molluscan abundance, densities and species richness
(Graveland et al. 1994, Graveland & van der Wal 1996, Schilthuizen et al. 2003, Martin
& Sommer 2004), but none thus far have quantified their effects on mollusc endemic
richness. In Malaysia, podzolic soils are generally acidic (Andriesse 1968); such
conditions may have promoted speciation as they would have created formidable barriers
to the dispersal of terrestrial molluscs away from karsts, especially among groups that exhibit obligate calcicoly (e.g., species from the subgenus Plectostoma). My measures of isolation and geological age, however, did not appear to affect endemic richness.
Isolation is not always a question of distance (Whittaker 1998) and so its effect on endemic richness might not have been detected using these metrics. Although geological history can determine the degree to which mollusc communities are isolated (van
Benthem-Jutting 1958, Welter-Schultes & Williams 1999), such factors are dynamic and sometimes hard to differentiate accurately for karsts (Chin 1977).
I have demonstrated quantitatively that groups of karsts in different parts of a region support unique malacofaunas. Other studies have reported on the influence of geography on molluscan diversity as well (Nekola 2003, Kiss et al. 2004). In Peninsular
Malaysia, the Titiwangsa Mountain range transverses the middle of the region and effectively separates the eastern part from the west (Fig. 7). Indeed, the karsts situated to the east and west of the mountain range appear to contain different mollusc communities.
24 Vicariant processes probably began when the once-continuous karst region was bisected
by the mountain’s intrusion during the Mesozoic era (van Benthem-Jutting 1958). In the
Amazon, geographical barriers such as ridges are known to have shaped the
phylogeographic relationships of various taxa (Lougheed et al. 1999).
In Sabah, my results indicated that the molluscan communities on karsts offshore
(Fig. 7) are dissimilar to those on the mainland. Radiation of island molluscs can be attributed to their limited dispersal abilities over oceanic barriers and relatively low natural immigration and colonization rates (Cowie 1995, Welter-Schultes & Williams
1999). On mainland Sabah, the karsts situated in the eastern and western parts of Sabah contain distinct malacofaunas that were possibly influenced by the vicariant effects of
major rivers (i.e., Kinabatangan, Segama and Padas Rivers; Fig. 7). With regards to
limestone flora, karsts situated along each of those rivers have been recognized as
separate phytogeographic regions (Kiew 2001). Several karsts in each of the same three
areas of Sabah (i.e., offshore, east and west) have also been regarded as centres of plant
diversity (Davis et al. 1995). In the Neotropics, riverine barriers were believed to play an
important role in shaping present-day species distributions within other taxonomic groups
(Gascon et al. 2000, Hall & Harvey 2002).
Malaysian conservation planners should therefore focus on preserving a few large karsts (i.e., > 1 km2) surrounded by podzols because they potentially contain higher
numbers of endemic mollusc species. Given the observed faunistic turnovers of mollusc
communities across groups of karsts separated by vicariant barriers (e.g., mountains and
rivers), large karsts within such groups should also be conserved to maximise protection
of endemic malacofaunas. In most circumstances, fewer larger reserves are more feasible
25 from biogeographical, financial and political perspectives (Diamond & May 1981,
Whittaker 1998). However, the practicality of conserving extensive karsts more than 100 km2 should be re-evaluated because endemic richness in extremely large areas may be asymptotic (e.g., if species-area curves follow logistic models: He & Legendre 2003).
26 Chapter 3: Implications and challenges for karst conservation in Southeast Asia
3.1. Implications
There is a pressing need to develop scientifically-sound criteria for the location of karst
reserves. Having identified karst area as an important biogeographical variable, I incorporated this factor into irreplaceability versus vulnerability maps (modified from
Margules & Pressey 2000) for 62 karsts (Table 3) in Peninsular Malaysia to single out those that require immediate conservation action. Despite its importance, surrounding soil type was not utilized due to insufficient data for all 62 karsts.
Since irreplaceable habitats can be quantified by their levels of species endemism
(Mittermeier et al. 2003), we used area as a measure of irreplaceability as larger karsts probably contain high endemic richness according to my GLMM results. Irreplaceability scores were also adjusted to account for the vicariant effects on species compositions in eastern and western regions based on my NMDS results. Karst vulnerability was measured by the number and degree of disturbances recorded by Price (2001). According to my criteria, karsts in forest reserves are considered the least vulnerable due to the presence of legislative measures, while undisturbed karsts within forests or around human settlements are slightly more vulnerable due to absence of protective legislation. Karsts designated as temples or parks are likely to be managed, but resident organisms may still experience disturbances from human traffic (Kiew 2001), recreational activities
(McMillan & Larson 2002, McMillan et al. 2003) and thermal radiation emissions from
buildings (Baur & Baur 1993). Karsts affected by agricultural development are highly
threatened because the surrounding vegetation has to be cleared to facilitate crop
27 cultivation (MacKinnon et al. 1996). Quarried karsts are the most vulnerable because limestone blasting is known to cause the extinction of site endemic species (Vermeulen
1994).
The irreplaceability versus vulnerability map was divided into four quadrants (Q) that require specific actions from planners (Margules & Pressey, 2000): (Q1) karsts most likely to be lost with few replacements, protection is urgent; (Q2) karsts with adequate replacements despite their vulnerability, holding measures are required; (Q3) karsts that face low risk from transformation but have high irreplaceability, acquisition for reserves are feasible; and (Q4) karsts that require least intervention, monitoring is still advisable.
Ten karsts in Peninsular Malaysia in (Q1) require urgent protection in decreasing order of priority: Serdam, Gelanggi, Datuk, Rapat, Lanno, Pondok, Kanthan, Batu Caves and
Lang. However, their protection might be difficult due to vested commercial interests from mining companies. For these karsts, feasibility assessments should also be conducted on the ground and those with inadequate forest buffers should be excluded or relegated down the priority list. Due to their position in Q3, three karsts that have yet to received protected status should be considered for preservation in decreasing order of priority: Jaya, Panjang and Hill 001. These karsts are suitable for reserves, in part due to their lower risk of transformation and (possibly) lower costs of land acquisition
(Margules & Pressey 2000). Additional reserves may be identified once the remaining karsts in Malaysia are similarly evaluated.
For karsts in other parts of Southeast Asia, measures for irreplaceability and vulnerability may require modification depending on the prevailing karst physiognomy
(e.g., presence of vicariant barriers) and disturbance types. For example, landscape-scale
28 conservation plans have proven to be effective in regions with extensive karst ecosystems
(e.g., Pu Luong-Cuc Phuong karst conservation project in Vietnam: GEF 2001).
Countries such as Malaysia, however, posses highly fragmented karst landscapes that fall under the jurisdiction of different state governments. In such a scenario, targeting specific karsts for preservation may be more feasible than a regional conservation approach.
However, such conservation strategies will not work as long as political will is lacking.
For example in Malaysia, several karsts that were identified for preservation due to their biological importance decades ago have not received any form of protection
(Molesworth-Allen 1961, Davison 1991, Kiew 1991). Several challenges facing karst conservation initiatives in Malaysia and the rest of the region will be elaborated on below.
3.2. Challenges
3.2.1. Resource shortages
Poverty of communities around karsts will continue to marginalize karst conservation issues. Concepts of population extinctions and unsustainable extractions are usually of little concern to the poor. In Sarawak, a survey of 198 low-income households around the
Bau karsts revealed that a sizeable percentage (54%) were dependent on karst resources for subsistence and around 33% were unwilling to accept conservation measures restricting their customary land rights (see Yong et al. 2004). For cash-strapped governments, royalties from cement manufacture are so substantial that policies for sustainable limestone quarrying are generally overlooked. The regency administration of
Gunungkidul, which presides over one of the poorest areas in Indonesia with a per capita
29 income of approximately US$153, issued quarrying permits to 13 mining companies in
the past decade to revive its ailing economy (Bambang & Utomo 2003). To alleviate poverty and resource overexploitation in karst areas, landuse planning must be improved
(using a landscape-scale conservation approach) to consider the welfare of poorer communities. For example, the managing agencies of the Pu Luong-Cuc Phuong karst conservation project in Vietnam allocated land to locals for sustainable agroforestry and involved them in ecotourism projects to generate income (GEF 2001). Government officials in Gunungkidul are equally concerned that karst quarries will ruin the landscape and affect tourism, which generated US$57,000 more than quarrying in 2002 (Bambang
& Utomo 2003). In Malaysia, karsts that were preserved as aesthetic backdrops for a resort township (Fig. 1d) has not only attracted multi-million dollar investments, but also opened up job opportunities for local residents.
3.2.2. Ad-hoc conservation planning
In most countries, karsts have been preserved based on anthropocentric criteria (e.g.,
karsts with high tourist potential or those that are inaccessible to mining companies).
While such an approach may seem pragmatic to conservation planners, the distinctiveness of its biodiversity and geomorphology must not be neglected. To ensure both these elements are considered during future environmental impact assessments
(EIAs) of karsts, ‘terms of reference’ were drawn up by The World Bank for consultants to follow (Vermeulen & Whitten 1999). During karst EIAs, high species richness or the presence of IUCN (The World Conservation Union) threatened species may only function as secondary indicators; the former does not reflect species rarity and the latter
30 often excludes uncharismatic organisms. Instead, endemism levels of range restricted taxa (e.g., plants, landsnails, and cave animals) could be used as the primary barometer for setting conservation priorities at karsts. If governments deem limestone quarrying to be necessary, groups of small and isolated karsts should not be selected because these are more likely to harbour high numbers of endemic species; larger and more extensive karsts may instead be made open to quarrying prospects (Vermeulen & Whitten 1999).
3.2.3. Inadequate protection
In Southeast Asia, current laws that protect karsts and their biodiversity appear ineffective or are simply non-existent. For example, many karsts in Malaysia receive protection by virtue of being located within the boundaries of national parks (Kiew
1991). In Borneo, agricultural activities often proceed unchecked towards the bases of protected karsts, while localized bans on swiftlet nest harvesting have only served to divert poachers to other unprotected karsts (MacKinnon et al. 1996). Laws to protect karst species are severely lacking (Kiew 2001, Lim & Cranbrook 2002); the only known example is a cave fish from central Java, Indonesia (Vermeulen & Whitten 1999).
Moreover, mining companies often exploit the uncertain demarcation of legal authority arising from the involvement of too many agencies. In Indonesia, laws that necessitate
EIAs prior to quarrying are often circumvented (Bambang & Utomo 2003). Evidently, additional legislative measures have to be formulated. For example, the retention of forested buffer zones around karsts (to prevent fires and maintain habitat integrity) should be made compulsory, while mining companies should be prohibited from starting small- scale operations elsewhere if the karsts allocated to them have not been completely
31 quarried. To curb unnecessary limestone quarrying (e.g., an excess of 14 million tons of
cement was produced in Malaysia during one year; Lock 1998), quarrying rates could
perhaps be monitored and made more transparent. Existing wildlife laws must also be
amended to protect certain keystone species that can umbrella the entire karst community
(Vermeulen & Whitten 1999). For the abovementioned laws and policies to work,
however, governments must clamp down on corruption, resolve conflicting jurisdictions
and provide administrators with greater incentives (e.g., income from geotourism and
fines from offences) to ensure better enforcement and accountability.
Around 13% of the region’s karst area has been nominally protected (Day &
Ulrich, 2000); this level of protection appears satisfactory given the goal of conservation
scientists to protect 10% of all habitat types globally. However, such percentages do not
necessarily correspond to species representation (Rodrigues et al., 2004) and protected
habitats may not be properly managed due to insufficient resources (‘paper parks’). As
karst protection in some countries are still absent or lacking (e.g., in Cambodia and
Myanmar; Table 4), regional governments and international agencies are still working to
increase the percentage of protected karst area in the region. For example, the state
government of Sarawak has extended the coverage of the Gunung Mulu National Park by
250 km2 to include other karsts (IUCN 2000), while organizations such as The World
Bank and The Nature Conservancy have helped protect karst landscapes in Vietnam (e.g.,
Pu Luong-Cuc Phuong karsts) and Indonesia (e.g., Sangkulirang karsts) respectively. The
IUCN has also set up a task force (Working Group on Cave and Karst Protection) to highlight additional karsts for protection. In 2001, the Asian Pacific Forum on Karst
Ecosystems and World Heritage identified several karsts in this region for inscription into
32 the World Heritage list. Karsts can now be found in eight of the 12 World Heritage
natural sites in Southeast Asia (UNESCO 2005). The impressive biodiversity at some of
these sites (Table 5) suggests that PAs containing karsts may help reduce the number of
gap species (species with distributions not covered by PAs; Rodrigues et al. 2004)
worldwide.
3.2.4. Deficient baseline data
The paucity of biological information on karsts and their threatened biodiversity ultimately weakens justifications for their conservation in the long run. For example, threatened karst species, particularly uncharismatic taxa such as cave invertebrates, appear to be severely underrepresented in lists of endangered species. Using the IUCN
Red List search engine, I compiled the total number of threatened species known from karstic habitats listed by the as critically endangered, endangered, and vulnerable. My findings showed that 143 karst-associated species are globally threatened and of these, 31 occur in Southeast Asia (Table 6). These figures, however, appear geographically skewed
and not representative of the true threatened status of karst species worldwide; more than
50% of globally threatened karst plants and molluscs were highlighted from just one country.
To support the argument that there is a lack of karst research worldwide, I screened internationally peer-reviewed articles from the Biological Abstracts® database for biodiversity-related articles over a 20-year period (1985-2004). I found that karsts contribute to just 1% of global and regional biodiversity research output relative to other terrestrial and freshwater ecosystems (Fig. 13). Given that karsts cover around 10% of the
33 land area in Southeast Asia (Day & Urich 2000), more studies need to be devoted to these
ecosystems. For example, the paper by Chapman (1982) is the only known ecological
study of karst caves from the region thus far (Deharveng & Bedos 2000). To promote
research on karsts, governments must commit more funds for capacity building in
biodiversity research and regional institutions should form collaborative efforts with
international scientific agencies. The ASEAN Regional Centre for Biodiversity
Conservation (ARCBC), which facilitates institutional linkages between regional and
European Union organizations, has already implemented eight karst-related research projects in six different Southeast Asian countries (Table 7; ARCBC 2004). It is encouraging that community based educational programmes and workshops on karsts have been carried out with ARCBC and other conservation initiatives (e.g., at the Pu
Luong-Cuc Phuong karsts; GEF 2001), but public awareness of karst conservation still needs to be increased throughout the region.
34 General conclusion
I have shown that karsts are major foci for speciation and important biodiversity arks.
Considering the immense financial returns from cement manufacturing, exploitation of
karsts for limestone cannot be stopped. In Southeast Asia, karsts warrant greater
conservation attention given the higher limestone quarrying rates relative to other tropical
regions. Analyses of biogeographical variables indicate that karsts probably have higher
numbers of endemic mollusc species when they are large and surrounded by podzolic
soils, and support distinct mollusc species compositions when isolated by vicariant
barriers. Large karsts (> 1 km2) surrounded by podzolic soils within biogeographically
distinct groups of karsts should therefore be conserved to maximise the protection of endemic molluscs. Although molluscs can function as biodiversity indicators (e.g., for plants but not birds: Groombridge 1992), other surrogate species should also be assessed because governments are unlikely to conserve karsts solely for such non-charismatic organisms. Ultimately, the conservation strategies outlined in this study will be effective once people begin to recognize the importance of karsts. For example, the economic importance of intact karsts must be conveyed to governments, possibly through further research on the benefit flows between intact and converted versions of karst (e.g., benefit- cost ratios: Balmford et al. 2002). The question now is this – can habitat loss at karsts be slowed down long enough for scientists to get a better grip on the challenges ahead?
Given that Southeast Asia is expected to lose 42% of its biodiversity by the year 2100
(Sodhi & Brook 2006), this is a conservation battle we may well stand to lose.
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49 Figures
Fig. 1. Examples of land uses around karsts. (a) A pristine tower karst in Sarawak, Malaysia. (b) Karst quarried for limestone in Perak, Malaysia. (c) Karst utilized as a Hindu temple in Selangor, Malaysia. (d) Karst used as an aesthetic backdrop for a resort in Perak, Malaysia. Photographs: Reuben Clements.
50
Fig. 2. Distribution of karsts (in black) throughout Southeast Asia (excluding Myanmar) modified from map courtesy of Elery Hamilton-Smith.
51
Fig. 3. Examples of karst biodiversity. (a) Site-endemic begonia, Begonia amphioxus, from Sabah, Malaysia. (b) Site-endemic prosobranch landsnail, Opisthostoma (Plectostoma) obliquedentatum, from Sabah, Malaysia. (c) Blind troglobitic crab, Cancrocaeca, from Sulawesi, Indonesia. (d) Cave-dwelling insectivorous bat, Hipposideros diadema, from Sarawak, Malaysia. Photographs: Menno Schilthuizen (a-b), Louis Deharveng (c) and Kelvin K. P. Lim (d).
52
Fig. 4. Percentages of total flora and fauna (selected taxa) from Sarawak (a) and Borneo (b) recorded on the Bau karsts. These percentages show that karst landscapes can harbor significant proportions of a region’s biodiversity. Data are from Yong et al. (2004).
53
Fig. 5. Observed (Sobs) and estimated (SICE) species of understory flora (a) and summit trees (b), as a function of sampled karsts in Bau, Sarawak. The lack of convergence between Sobs and SICE curves indicates that sampling saturation has not been reached despite 30 months of sampling. Data are from Yong et al. (2004) and curves were generated with presence/absence data using EstimateS (Colwell 2005). Abbreviation: ICE, incidence-based coverage estimator.
54
Fig. 6. Scale of limestone quarrying in terms of: (a) mean annual percentage change in quarrying rates; and (b) mean (± SE) annual quarrying rates for four major tropical regions over a five year-period (1999-2003). Quarrying rates in Southeast Asia appear to be the highest relative to other regions. Calculations excluded countries with incomplete statistics for all five years. Data are from the United States Geological Survey, Minerals information, (http://minerals.usgs.gov/minerals).
55
Fig. 7. Distribution of 16 sampled karsts in Peninsular Malaysia, 27 sampled karsts in Sabah, and major geographical features (i.e., Titiwangsa Mountain Range, Kinabatangan River, Padas River, Segama River). See Appendix 1 for corresponding karst names.
56 70 60 a. Panjang (0.91) 50 b. Baling (0.98) 40 30 c. Bercham (0.83)
No. species of 20 10 0 0123456 No. of quadrats
Fig. 8. Expected species accumulation curves for karsts in Peninsular Malaysia with the: (a) highest species richness; (b) highest completeness ratio; and (c) lowest completeness ratio.
57
58 Fig. 9. Univariate relationships between (A) number of endemic species and total species richness, (B) the complementary log-log transformation of the proportion of species that are endemic and log10 karst area, and (C) the total number of endemic species and log10 karst area.
Fig. 10. Predicted number of endemic species per soil type: yellow-grey (Y-G) podzols, red-yellow (R-W) podzols and all ‘other’ soils. The observed 95 % confidence interval of the number of endemic species per karst (dotted horizontal lines) was determined by a 10,000 iteration bootstrap of the probabilities predicted by the model EN~AR+SL. Changes to the predicted number of endemic species relative to each soil type level were calculated by adjusting the original dataset so that all karsts were given the same soil type (each soil type in turn), keeping the ‘area’ term in the model as in the original dataset. Error bars represent the 10,000 iteration bootstrapped upper 95 % confidence limits.
59 2 2 (a) (c)
1 1
0 0
-1 -1
-2 -2 -2-1012-2-1012
2 2 (b) (d)
1 1
0 0
-1 -1
-2 -2 -2-1012-2-1012
Fig. 11. Non-metric multidimensional scaling joint plot of: (a) 16 karst scores and (b) 189 species scores for Peninsular Malaysia; and (c) 27 karst scores and (d) 131 species scores for Sabah ‘■’ and ‘▬’ respectively represent karsts in the western and eastern regions of Peninsular Malaysia, while ‘▲’, ‘□’, and ‘♦’ respectively represent karsts on islands off Sabah, West Sabah and East Sabah. Only site- and local endemic species are shown and they are indicated by ‘●’ and ‘○’ respectively. The distances between each score reflect their relative dissimilarity.
60
100
75 y
ilit (Q3) (Q1) 50 aceab
Irrepl (Q4) (Q2) 25
0 0 25 50 75 100 Vulnerability
Fig. 12. Irreplaceability and vulnerability scores from 62 different karsts in Peninsular Malaysia (Table 3) were plotted along two axes on a graph, which was divided into four quadrants that require specific actions from planners (Margules & Pressey, 2000): (Q1) karsts most likely to be lost with few replacements, protection is urgent; (Q2) karsts with adequate replacements despite their vulnerability, holding measures are required; (Q3) karsts that face low risk from transformation but have high irreplaceability, acquisition for reserves are feasible; and (Q4) karsts that require least intervention, monitoring is still advisable. ‘●’ and ‘○’ respectively indicate karsts already designated as reserves and those yet to receive any form of protection. Ten karsts in Peninsular Malaysia in (Q1) require urgent protection in decreasing order of priority: Serdam, Gelanggi, Datuk, Rapat, Lanno, Pondok, Kanthan, Batu Caves and Lang. Due to their position in Q3, three karsts that have yet to received protected status should be considered for reserves in decreasing order of priority: Jaya, Panjang and Hill 001.
61
Fig. 13. Percentage of global (black bars) and Southeast Asian (grey bars) biodiversity research conducted in major terrestrial and freshwater ecosystems over a 20-year period (1985-2004). These percentages suggest a paucity of biological information on karsts relative to other ecosystems. Data was obtained from article searches within the abstract, title and keywords of citations in the Biological Abstracts® database using hierarchically nested combinations of relevant keywords and wildcards (available from the author on request).
62 Tables
Table 1. The a priori model set used to examine the relationship between the number of endemic species and biogeographical variables using generalized linear mixed-effects modelling for 16 karsts in Peninsular Malaysia. Shown are the term abbreviations (EN = number of endemic species, AR = karst area, IS = isolation index (minimum straight-line distance to nearest karst or number of karsts within 10 km radius), GA = geological age (Permian & Lower Triassic, Carboniferous or Palaeozoic), and SL = major soil type (yellow-grey podzols, red-yellow podzols or ‘other’), as well as the major analytical (hypothesis) theme represented by each model.
Model No. Model Analytical Theme
1 EN~AR+IS area + isolation 2 EN~AR+IS+AR*IS area + isolation + their interaction 3 EN~AR area only 4 EN~AR+GA area + geological age 5 EN~AR+SL area + soil type 6 EN~AR+IS+GA area + isolation + geological age 7 EN~AR+IS+SL area + isolation + soil type
63 Table 2. Information-theoretic ranking of the generalized linear mixed-effects models investigating the correlates of endemic species richness for 16 karsts in Peninsular Malaysia according to Akaike’s Information Criterion corrected for small sample size (AICc). Terms shown are EN = number of endemic species, RC = total species richness, AR = karst area, IS = isolation index (minimum straight-line distance to nearest karst), GA = geological age (Permian & Lower Triassic, Carboniferous or Palaeozoic), and SL = major soil type (yellow-grey podzols, red-yellow podzols or ‘other’). Also shown is the number of parameters (k), the negative log-likelihood (-LL), the difference in AICc for each model from the most parsimonious model (ΔAICc), AICc weight (wAICc), and the per cent deviance (%DE) explained in the response variable by the model under consideration.
Model k -LL ΔAICc wAICc %DE Δ%DE
EN~AR+SL 6 -45.682 0 0.656 18.1 9.3 EN~AR+IS+SL 7 -45.455 1.874 0.257 18.5 0.4 EN~AR 4 -50.858 5.848 0.035 8.8 - EN~AR+GA 6 -49.000 6.635 0.024 12.1 3.3 EN~AR+IS 5 -50.837 8.032 0.012 8.8 < 0.1 EN~AR+IS+GA 7 -48.889 8.741 0.008 12.3 3.5 EN~AR+IS+AR*IS 6 -50.034 8.704 0.008 10.3 1.5
64 Table 3. Irreplaceability and vulnerability scores for 62 karsts in Peninsular Malaysia
Karst name Area (km2) Region Irreplaceability Disturbance Vulnerability
K001 0.02 WM 20 A 60 Bercham 0.06 WM 21 H,P 30 Tasek 0.06 WM 22 H,P,Q 100 Takun 0.06 WM 23 R 1 Cheroh 0.08 WM 24 H,P,Q 100 Kalong 0.08 WM 25 H 10 Chondong 0.10 WM 36 H 10 Keteri 0.11 WM 37 H,Q 90 Tambun 0.15 WM 38 H 10 Jerneh 0.17 WM 39 H 10 Kandu 0.26 WM 40 H,P 30 Meusah 0.27 WM 41 H,P 30 Gua Harimau 0.33 WM 42 H 10 Kemuning 0.33 WM 43 A 60 Batu Kurau 0.41 WM 44 H 10 Kaplu 0.55 WM 45 H,P 30 Chuping 0.59 WM 46 H,P 90 Keriang 0.60 WM 47 H 10 Layang Layang 0.60 WM 48 H,P 30 Lagi 0.67 WM 49 H,P 90 Badak 0.78 WM 50 H 10 Lang 1.03 WM 66 H,P,Q 100 Batu Caves 1.28 WM 67 H,P,Q 100 Kanthan 1.54 WM 68 H,P,Q 100 Terendum 3.15 WM 69 Q 80 Pondok 4.16 WM 70 H,Q 90 Lanno 4.95 WM 71 H,P,Q 100 Rapat 5.01 WM 72 H,P,Q 100 Baling 5.20 WM 73 H,Q 90 Datuk 7.53 WM 74 H,P,Q 100 Tempurung 7.53 WM 75 H,R 11 Tapah 0.01 EM 16 U 5 Ikan 0.03 EM 17 P 20 Hendrik 0.05 EM 18 U 10 Ciku 5 0.05 EM 19 A 60 Pulau Raba 0.06 EM 20 U 5 Reng 0.06 EM 21 H,P 30
65 Ciku 7 0.06 EM 22 A 60 Sai 0.06 EM 23 H,P 90 Siput 0.07 EM 24 R 1 Tenggek 0.08 EM 25 H,P 90 Cintamanis 0.11 EM 38 H 10 Madu 0.12 EM 39 H,P 30 Senarip 0.14 EM 40 U 5 Tongkat 0.16 EM 41 U 5 Bama 0.19 EM 42 H,P 30 Pasuk 0.21 EM 43 U 5 Charas 0.25 EM 44 H,P 30 Setir 0.25 EM 45 U 5 Musang 0.30 EM 46 H 10 Gagak 0.32 EM 47 H 10 Renayang 0.34 EM 48 H 10 Cenarut 0.59 EM 49 U 5 Sagu 0.81 EM 50 H,Q 90 Jeboh Puyoh 1.04 EM 70 R 1 Gelanggi 1.21 EM 71 H,P,Q 100 Serdam 1.34 EM 72 H,Q 90 H001 1.65 EM 73 U 5 Ciku 4 1.91 EM 74 A 60 Senyum 2.31 EM 75 H,R 11 Panjang 17.51 EM 99 H 10 Jaya 19.02 EM 100 U 5
Irreplaceability scores for 62 karsts in Peninsular Malaysia were calculated based on their area: 0.01 to 0.09 km2 – 25; 0.1 to 0.9 km2 – 50; 1.0 to 9.9 km2 – 75; ≥ 10.0 km2 – 100. To account for the distinct species compositions on karsts in eastern (EM) and western (WM), we first allocated the highest score to the largest karst of a particular size range in EM or WM. Subsequently, we deducted the scores of consecutively smaller karsts within the same size range and region by a value of 1. Vulnerability scores were assigned to karsts with increasing magnitudes of disturbance: karsts in forest reserves (R) – 1; karsts unaffected by human disturbances (U) - 5; karsts affected by human disturbances from nearby settlements (H) – 10; karsts designated as places of worship or recreation (P) – 20; karsts affected by agricultural development (A) – 60; karsts that were previously or are currently being quarried (Q) – 80. Accumulated disturbance scores that exceeded 100 were capped at this value.
66 Table 4. Protected status of karst areas in Southeast Asia.
Country Karst area (Km2) Protected karst area (Km2) Karst protected (%)
Cambodia 20,000 0 0
Indonesia 145,000 22,000 15
Laos 30,000 3000 10
Malaysia 18,000 8000 44
Myanmar 80,000 650 1
Philippines 35,000 10,000 29
Thailand 20,000 5000 25
Vietnam 60,000 4000 7
Total 408,000 52,650 13
Figures should be treated cautiously as they include information from protected areas that do not conform to United Nations recognition criteria. Modified from Day & Ulrich (2000).
67 Table 5. Taxonomic breakdown of species recorded in four of the eight World Heritage natural sites that contain karsts in Southeast Asia (UNESCO, 2005).
Name Country Plants Mammals Herptiles Birds Fishes
Phong Nha-Ke Bang Vietnam 876 113 81 302 72
Dong Phayayen-Khao Yai Thailand 2500 112 200 392 N.A.
Thungyai-Huai Kha Khaeng Thailand N.A. 120 139 400 113
Gunung Mulu Malaysia 3500 81 131 270 48
68 Table 6. Taxonomic breakdown of IUCN threatened species.
Group Habitats worldwide Karsts worldwide Karsts in Southeast Asia
Molluscs 974 20* 18*
Insects 559 0 0
Fishes 800 2* 0
Amphibia 1770 27 4
Reptiles 304 4 0
Birds 1213 0 0
Mammals 1101 2 1*
Plants 8321 88* 8*
Total 15042 143 31
Taxa with more than 50% of the species highlighted from just one country are denoted with *. For information on karst-associated species, three ‘habitat’ categories (i.e., karst and other subterranean hydrological systems; rocky areas, caves and subterranean habitats) and one ‘threat’ category (i.e., mining) were searched using the expert search engine in the 2004 IUCN Red List of Threatened Species (http:\\www.iucnredlist.org).
69 Table 7. Description of eight karst-related research projects funded by ARCBC in six
Southeast Asian countries (ARCBC, 2004).
Karst study area Country Budget (€) Duration (months) Research theme
Maros Indonesia 115,102 24 Biological uses and values
Luangprabang Laos 20,000 15 Biological uses and values
Sarawak Malaysia 99,320 30 Biological uses and values
Southwestern Negros Philippines 48,125 24 Ecological reconstruction
Northwest Panay Philippines 100,000 36 Ecological reconstruction
Phang Nga Bay Thailand 115,102 24 Biological uses and values
Ha Long Bay Vietnam 58,605 24 Biological uses and values
Phong Nha-Ke Bang Vietnam 94,500 24 Biological uses and values
70 Appendix
Appendix 1. Summary information of 16 karsts sampled in Peninsular Malaysia. ‘■’ and ‘▬’ represent karsts in the western and eastern regions respectively. Codes for soil type are as follows: yellow grey podzols – 1; red-yellow podzols – 2; and others (i.e., lithosols on limestone crags, alluvial and gley soils, reddish brown lateritic soils) – 3. Codes for geological age are as follows: Permian & Lower Triassic – 1, Carboniferous – 2; and Palaeozoic – 3. Geographical Area Isolation - straight-line Isolation - no. of karsts No. Karst name Region Coordinates (km2) Soil type Geological age distance to nearest karst (km) within 10 km 1 Baling ■ 5°40'N 100°53'E 5.20 2 3 57.7 0 2 Pondok ■ 4°48'N 100°52'E 4.16 2 2 12.42 0 3 KE 001 ■ 4°51'N 101°07'E 0.02 3 3 0.45 5 4 Datok ■ 4°36'N 101°09'E 7.53 2 3 1.34 33 5 Tasek ■ 4°38'N 101°05'E 0.06 2 3 3.91 24 6 Bercham ■ 4°38'N 101°08'E 0.06 2 3 1.24 24 7 Rapat ■ 4°33'N 101°07'E 5.01 2 3 1.69 37 8 Takun ■ 3°18'N 101°38'E 0.06 2 2 8.66 1 9 Cintamanis ▬ 3°26'N 102°00'E 0.10 2 3 43.56 0 10 Senyum ▬ 3°42'N 102°26'E 2.31 1 1 18.80 0 11 Gelanggi ▬ 3°53'N 102°28'E 1.21 1 1 18.80 0 12 Sai ▬ 4°12'N 101°59'E 0.06 3 1 3.69 1 13 Panjang ▬ 4°48'N 101°59'E 17.51 1 1 2.92 42 14 Ciku 7 ▬ 5°04'N 102°08'E 0.06 1 1 5.02 15 15 Hill 001 ▬ 5°00'N 101°58'E 1.65 3 1 7.81 45 16 Ikan ▬ 5°21'N 102°01'E 0.03 1 1 3.29 22
71 Appendix 2. Summary information of 27 karsts sampled in Sabah, Malaysian Borneo. ‘▲’, ‘□’, and ‘♦’ represent karsts on islands off Sabah, West Sabah and East Sabah respectively. No. Karst name Region Geographical Coordinates 17 Temurung □ 4°43'N 116°24'E 18 Tinahas □ 4°38'N 116°37'E 19 Punggul □ 4°38'N 116°37'E 20 Pungiton □ 4°42'N 116°36'E 21 Sinobang □ 4°48'N 116°38'E 22 Sanaron □ 4°42'N 116°36'E 23 Lian □ 5°29'N 116°10'E 24 Danum ♦ 4°48'N 117°48'E 25 Tomanggong Besar ♦ 5°30'N 118°18'E 26 Tabin ♦ 5°18'N 118°44'E 27 Tomanggong Kecil ♦ 5°30'N 118°17'E 28 Tomanggong 2 ♦ 5°31'N 118°18'E 29 Sungai Resang ♦ 5°31'N 118°21'E 30 Batu Tai ♦ 5°32'N 118°10'E 31 Pangi ♦ 5°31'N 118°18'E 32 Mawas ♦ 5°27'N 118°08'E 33 Materis ♦ 5°31'N 118°01'E 34 Keruak ♦ 5°31'N 118°17'E 35 Kampung ♦ 5°30'N 118°17'E 36 Gomantong ♦ 5°31'N 118°04'E 37 Bod Tai ♦ 5°31'N 118°13'E 38 Baturong ♦ 4°41'N 118°00'E 39 Mantanani Besar ▲ 6°42'N 116°20'E 40 Mantanani Kecil ▲ 6°42'N 116°20'E 41 Balambangan (Bt. Sireh) ▲ 7°12'N 116°51'E 42 Balambangan (Kok Simpul) ▲ 7°13'N 116°53'E 43 Banggi (Karakit) ▲ 7°06'N 117°05'E
72 Appendix 3. Species list of 198 species sampled from 16 karsts in Peninsular Malaysia.
Family Genus Species Ariophantidae Achatina fulica Ariophantidae Dyakia salangana Ariophantidae Hemiplecta cymatium Ariophantidae Hemiplecta humphreysiana Ariophantidae Hemiplecta gemina Ariophantidae Macrochlamys resplendens Ariophantidae Macrochlamys tersa Ariophantidae Microcystina striatula Ariophantidae Microcystina sp.1 to 7 Ariophantidae Pseudoplecta bijuga Ariophantidae Quantula striata Assimineidae Cyclotropis bedaliensis Camaenidae Amphidromus atricallosus Camaenidae Chloritis penangensis Camaenidae Chloritis sp.1 to 2 Camaenidae Landouria sp.1 Camaenidae Trachia gabata Charopidae Charopa sp.1 to 3 Clausiliidae Phaedusa filicostata Cyclophoridae Alycaeus balingensis Cyclophoridae Alycaeus gibbosulus Cyclophoridae Alycaeus kelantanensis Cyclophoridae Alycaeus liratulus Cyclophoridae Alycaeus perakensis Cyclophoridae Alycaeus perakensis var. minor Cyclophoridae Alycaeus thieroti Cyclophoridae Chamalycaeus diplochilus Cyclophoridae Chamalycaeus jousseaumei Cyclophoridae Chamalycaeus microconus Cyclophoridae Chamalycaeus microdiscus Cyclophoridae Chamalycaeus mixtus Cyclophoridae Chamalycaeus oligopleuris Cyclophoridae Chamalycaeus parvulus Cyclophoridae Chamalycaeus sp.1 to 6 Cyclophoridae Cyclophorus malayanus Cyclophoridae Cyclophorus semisulcatus Cyclophoridae Cyclophorus zebrinus Cyclophoridae Cyclophorus perdix
73 Cyclophoridae Cyclotus penangensis Cyclophoridae Cyclotus setosus Cyclophoridae Cyclotus solutus Cyclophoridae Cyclotus sp.1 to 3 Cyclophoridae Geotrochus sp.1 Cyclophoridae Lagochilus townsendi Cyclophoridae Leptopoma perlucidum Cyclophoridae Platyraphe lowi Cyclophoridae Rhiostoma asiphon Cyclophoridae Rhiostoma jousseaumei Cyclophoridae Rhiostoma speleotes Diplommatinidae Diplommatina canaliculata Diplommatinidae Diplommatina crosseana crosseana Diplommatinidae Diplommatina demorgani Diplommatinidae Diplommatina diminuta Diplommatinidae Diplommatina laidlawi Diplommatinidae Diplommatina maduana Diplommatinidae Diplommatina nelvilli Diplommatinidae Diplommatina pentaechma Diplommatinidae Diplommatina sinistra Diplommatinidae Diplommatina sp.1 Diplommatinidae Diplommatina streptophora Diplommatinidae Diplommatina superba Diplommatinidae Diplommatina superba brevior Diplommatinidae Diplommatina tweediei Diplommatinidae Diplommatina ventriculus Diplommatinidae Opisthostoma tenuicostatum Diplommatinidae Opisthostoma coronatum Diplommatinidae Opisthostoma crassipupa Diplommatinidae Opisthostoma hypermicrum Diplommatinidae Opisthostoma megalomphalum Diplommatinidae Opisthostoma michaelis Diplommatinidae Opisthostoma micridium Diplommatinidae Opisthostoma paranomon Diplommatinidae Opisthostoma paulucciae Diplommatinidae Opisthostoma plagiostomum Diplommatinidae Opisthostoma retrovertens Diplommatinidae Opisthostoma sinyumensis Diplommatinidae Opisthostoma sp.1 to 17 Diplommatinidae Opisthostoma umbilicatum Endodontidae Philalanka kusana
74 Endodontidae Philalanka sp.1 to 3 Enidae Ena sp.1 to 6 Euconulidae Coneuplecta microconus Euconulidae Coneuplecta olivacea Euconulidae Liardetia angigyra Euconulidae Liardetia doliolum Euconulidae Liardetia sp.1 to 5 Euconulidae Queridomus fimbriosus Euconulidae Queridomus sp.1 Ferussaciidae Cecilioides caledonica Helicarionidae Geotrochus sp.1 Hydrocenidae Georissa monterosatiana Hydrocenidae Georissa semisculpta Hydrocenidae Acmella sp.1 to 2 Hydrocenidae Hydrocena sp.1 to 3 Pupinidae Pupina arula Pupinidae Pupina excisa Pupinidae Pupina sp.1 to 2 Streptaxidae Discartemon collingei Streptaxidae Discartemon leptoglyphus Streptaxidae Discartemon platymorphus Streptaxidae Discartemon plussensis Streptaxidae Gullela bicolor Streptaxidae Haplotychius atopospria Streptaxidae Haplotychius balingensis Streptaxidae Haplotychius eutropha Streptaxidae Sinoennea apicata Streptaxidae Sinoennea attenuata Streptaxidae Sinoennea baculum Streptaxidae Sinoennea butleri Streptaxidae Sinoennea callizonus Streptaxidae Sinoennea chintamanensis Streptaxidae Sinoennea crumenilla Streptaxidae Sinoennea hungerfordiana Streptaxidae Sinoennea lepida Streptaxidae Sinoennea perakensis Streptaxidae Sinoennea sp.1 to 3 Streptaxidae Sinoennea subcylindrica Streptaxidae Sinoennea tiarella Streptaxidae Sinoennea tweediei Subulinidae Allopeas clavulinum
75 Subulinidae Allopeas gracile Subulinidae Prosopeas tchehelense Subulinidae Subulina octana Trochomorphidae Videna sp.1 to 2 Trochomorphidae Vitrinopsis sp.1 Valloniidae Pupisoma sp.1 to 3 Vertiginidae Boysidia sp.1 Vertiginidae Gyliotrachela depresspira Vertiginidae Gyliotrachela hungerfordiana Vertiginidae Gyliotrachela sp.1 to 7 Vertiginidae Hypselostoma perigyra Vertiginidae Hypselostoma sp.1 to 3 Vertiginidae Hypselostoma terae Vertiginidae Paraboysidia serpa Vertiginidae Paraboysidia sp.1 to 3
76 Appendix 4. Species list of 173 species sampled from 27 karsts in Sabah, Malaysia.
Family Genus Species Achatinellidae Achatinellid sp.1 Achatinellidae Elasmias globulosum Achatinidae Achatina fulica Ariophantidae Dyakia hugonis Ariophantidae Everettia sp.1 to 4 Ariophantidae Hemiplecta humphreysiana Ariophantidae Kalamantania whiteheadi Ariophantidae Macrochlamys indica Ariophantidae Macrochlamys tersa Ariophantidae Microcystina callifera Ariophantidae Microcystina lissa Ariophantidae Microcystina microrhynchus Ariophantidae Microcystina muscorum Ariophantidae Microcystina physotrochus Ariophantidae Microcystina sinica Ariophantidae Microcystina striatula Ariophantidae Parmarion sp.1 Ariophantidae Vitrinula descrepignyi Assimineidae Acmella cyrtoglyphe Assimineidae Acmella nana Assimineidae Acmella ovoidea Assimineidae Acmella polita Assimineidae Acmella striata Assimineidae Acmella umbilicata Bradybaena Bradybaena similaris Bradybaena Cochlostyla trailii Camaenidae Amphidromus adamsi Camaenidae Amphidromus martensi Camaenidae Chloritis kinibalensis Camaenidae Chloritis plena Camaenidae Chloritis sibutuensis Camaenidae Chloritis sp.1 Camaenidae Ganesella acris Camaenidae Trachia pudica Charopidae Beilania philippinensis Charopidae Charopa argos Charopidae Charopa infrastriata Charopidae Charopa jugalis
77 Charopidae Charopa lissobasis Charopidae Discocharopa aperta Charopidae Pilsbrycharopa kobelti Clausiliidae Phaedusa filicostata filialis Cyclophoridae Alycaeus jagori Cyclophoridae Chamalycaeus everetti Cyclophoridae Chamalycaeus sp.1 Cyclophoridae Chamalycaeus specus Cyclophoridae Cyclophorus kinabaluensis Cyclophoridae Ditropopsis constricta Cyclophoridae Japonia anceps Cyclophoridae Japonia balabacensis Cyclophoridae Japonia compressa Cyclophoridae Japonia janus Cyclophoridae Japonia jucunda Cyclophoridae Japonia keppeli Cyclophoridae Japonia smithi Cyclophoridae Japonia kinabaluensis Cyclophoridae Leptopoma pellucidum Cyclophoridae Leptopoma sericatum Cyclophoridae Leptopoma undatum Cyclophoridae Opisthoporus birostris Cyclophoridae Opisthoporus iris Cyclophoridae Platyraphe bongaoensis Cyclophoridae Platyraphe linitus Cyclophoridae Pterocyclos tenuilabiatus Cyclophoridae Pterocyclos trusanensis Diplommatinidae Arinia biplicata Diplommatinidae Arinia boreoborneensis Diplommatinidae Arinia borneensis Diplommatinidae Arinia brevispira brevispira Diplommatinidae Arinia brevispira orientalis Diplommatinidae Arinia clausa Diplommatinidae Arinia cylindrica cylindrica Diplommatinidae Arinia paricostata Diplommatinidae Arinia pertusa Diplommatinidae Arinia simplex Diplommatinidae Arinia sp.1 Diplommatinidae Arinia stenotrochus pachystoma Diplommatinidae Arinia stenotrochus strenotrochus Diplommatinidae Arinia turgida
78 Diplommatinidae Diplommatina antheae Diplommatinidae Diplommatina asynaimos Diplommatinidae Diplommatina calvula Diplommatinidae Diplommatina centralis Diplommatinidae Diplommatina cyrtorhitis Diplommatinidae Diplommatina gomantongensis Diplommatinidae Diplommatina isseli Diplommatinidae Diplommatina oedogaster Diplommatinidae Diplommatina recta Diplommatinidae Diplommatina rubicunda Diplommatinidae Diplommatina soror Diplommatinidae Diplommatina sykesi Diplommatinidae Diplommatina whiteheadi Diplommatinidae Opisthostoma brevituba Diplommatinidae Opisthostoma concinnum Diplommatinidae Opisthostoma cyrtopleuron Diplommatinidae Opisthostoma dormani Diplommatinidae Opisthostoma fraternum Diplommatinidae Opisthostoma hailei Diplommatinidae Opisthostoma javanicum Diplommatinidae Opisthostoma jucundum Diplommatinidae Opisthostoma mirabile Diplommatinidae Opisthostoma obliquedentatum Diplommatinidae Opisthostoma perspectivum Diplommatinidae Opisthostoma simplex Diplommatinidae Opisthostoma sp.1 Diplommatinidae Opisthostoma telestoma Diplommatinidae Opisthostoma brachyacrum lambii Diplommatinidae Opisthostoma lissopleuron Endodontidae Philalanka kusana Endodontidae Philalanka moluensis Endodontidae Philalanka obscura Endodontidae Stenopylis coarctata Euconulidae Kaliella accepta Euconulidae Kaliella angulata Euconulidae Kaliella barrakporensis Euconulidae Kaliella calculosa Euconulidae Kaliella dendrophila Euconulidae Kaliella doliolum Euconulidae Kaliella microconus Euconulidae Kaliella punctata
79 Euconulidae Kaliella scandens Euconulidae Queridomus conulus Euconulidae Rahula sp.1 Ferussaciidae Cecilioides caledonica Helicarionidae Atopos sp.1 Helicinidae Aphanoconia usukanensis Helicinidae Geophorus agglutinans Helicinidae Sulfurina euchromia Helicinidae Sulfurina martensi Hydrocenidae Georissa bangueyensis Hydrocenidae Georissa borneensis Hydrocenidae Georissa filiasaulae Hydrocenidae Georissa gomantongensis Hydrocenidae Georissa saulae Hydrocenidae Georissa scalinella Hydrocenidae Georissa similis Hydrocenidae Georissa sp.1 to 3 Hydrocenidae Georissa williamsi Pupinidae Pupina hosei Rhytididae Macrocycloides sp.1 Streptaxidae Diaphera wilfordii ectyphus Streptaxidae Diaphera wilfordii wilfordii Streptaxidae Huttonella bicolor Subulinidae Allopeas clavulinum Subulinidae Allopeas gracile Subulinidae Borneopeas sp.1 Subulinidae Opeas hannense Subulinidae Paropeas achatinaceum Subulinidae Subulina octona Trochomorphidae Bertia brookei Trochomorphidae Geotrochus bongaoensis Trochomorphidae Geotrochus labuanensis Trochomorphidae Geotrochus meristotrochus Trochomorphidae Geotrochus whiteheadi Trochomorphidae Videna bicolor Trochomorphidae Videna froggatti Trochomorphidae Videna metcalfei Trochomorphidae Videna repanda Trochomorphidae Videna timorensis Valloniidae Pupisoma pulvisculum Vertiginidae Boysidia salpinx
80 Vertiginidae Gastrocopta avanica Vertiginidae Gastrocopta pediculus Vertiginidae Gastrocopta recondita Vertiginidae Nesopupa malayana Vertiginidae Nesopupa moreleti Vertiginidae Ptychopatula orcella Vertiginidae Ptychopatula orcula
81