Batu Caves, Selangor (called Gua Batu or Bukit Batu in Malay) is an iconic tower karst limestone hill that dominates the landscape. It lies about 12 km northeast of Kuala Lumpur, the capital city of Malaysia. It covers about 1.1 km² and reaches 329 m at the highest point. It lies 3° north of the Equator. Day length varies just 15 min between June and December. The climate is equatorial with annual temperature variation much smaller than the diurnal variation with highest day and night temperatures of 33 °C and 23 °C, respectively, in April and the lowest temperatures of 31 °C and 22 °C in January. Mean annual rainfall is 2540 mm. June is the driest month with 130 mm of rain in 13 rainy days while November is the wettest month with 24 rainy days and 278 mm of rain. Humidity averages about 80% throughout the year. The karst is covered in limestone forest (Saw 2010).

Batu Caves is not only an outstanding nature monument, known for its unique plant and animal biodiversity and its caves and cave ecosystem, but it is also a site of great cultural and tourist importance. Its majestic Temple Cave houses the Sri Subramaniarswamy Temple that, during the Thaipusam Festival, attracts more than a million devotees and tourists. Formerly, Batu Caves was surrounded by lowland rain forest, but already by the 1890s, when the first scientific study was conducted (Ridley 1898), coffee plantations were beginning to encroach the area. Due to its accessibility to Kuala Lumpur, over the following 120 years, it has been studied by many scientists with different specialities, making Batu Caves the best studied limestone karst in Malaysia and SE Asia (Kiew 2014; Kiew et al. in press). Batu Caves is home to at least 366 plant species (6 lycophytes, 40 ferns, 2 gymnosperms and 318 flowering plant species) representing 30% of Peninsular Malaysia’s limestone flora (Kiew et al. in press).

In 1930, Batu Caves was gazetted as a Public Recreation Area. In the same year, the Sri Subramaniarswamy Temple was placed under the management of the Sri Maha Mariamman Temple. In 2007, the temple complex was designated as a Cultural Heritage Site. In 2016, the entire Batu Caves environmental complex was classified as an Environmentally Sensitive Area. Quarrying on a small scale had already started in 1889. In 1952 and 1959, parts of the Reserve were revoked and quarry licences issued. A third quarry opened in 1972 (Yussof 1997). Quarrying ceased in 1981, but no attempt has been made to rehabilitate the quarry sites and even after 40 years, the cliff faces remain bare and scar the hill. One cave was completely destroyed by quarrying (Lim et al. 2010). The surrounding lowland forest has been progressively cleared and today, there is no longer a buffer zone of trees around the base of the karst. In only a few places does a narrow strip of forest persist. Current major threats include continuing illegal encroachment, increasingly frequent accidental fires and unregulated infrastructure development (Kiew et al. 2019).

In view of these on-going threats, there is an urgent and pressing need to re-evaluate the current status of Batu Caves, particularly its sensitive biodiversity, to assess the impacts of the various threats and uses. In common with all karst sites, Batu Caves is of finite size, so it is imperative to ensure that any change does not impact negatively and cause permanent loss or damage, while, at the same time, enabling Batu Caves to remain accessible to devotees, tourists, scientists, speleologists and rock climbers etc.

To identify species of greatest conservation concern, a novel quantitative method, the CIS, was used, based on weighting a combination of parameters (whether the species is a native species, is from primary vegetation, is restricted to limestone, is endemic and its conservation status, based on IUCN Criteria and Categories). For a karst hill, this enables the assessment of species, microhabitats and sites for their conservation importance and identifies species and microhabitats of high conservation value, irrespective of the number of species present.

Initially, the Conservation Importance Scoring system was trialled in 2016 during the Rapid Biodiversity Assessment of Batu Caves and proved rapid and effective in producing accurate, quantitative reproducible results that identified species, microhabitats and sites with maximum biodiversity. It was not only effective at the species, microhabitats and site levels, but also has potential as a robust methodology that enables comparison between limestone karsts on a scientific basis.

For the CIS to be successfully applied, the first step is to identify the many microhabitats found on a single karst hill. By identifying and surveying all microhabitats, those with unique assemblages of species, particularly of threatened species, can be pinpointed. In this way, most of the rare and threatened species will be captured and, by using CIS, those species and microhabitats most at risk can be identified.

To evaluate the current status of plant diversity on Batu Caves, a Rapid Biodiversity Assessment was initiated in November–December 2016 and carried on throughout the Batu Caves Scientific Expedition between July 2018 and June 2020. The survey covered the entire base of the karst, the steep earth-covered slopes, areas around caves and the summit where it was accessible without climbing equipment (Table 3). Sixteen microhabitats (Table 1) were identified, each characterised by physical factors (topography, substrate, whether they were exposed or shaded) and their particular assemblage of species. Level of disturbance was also recorded.

All microhabitats at twelve sites were surveyed (Table 3, Suppl. material 1: Appendix). Some sites investigated covered a range of microhabitats. Disturbed, as well as undisturbed sites, were included. Three disused quarry sites were also surveyed. All sites were photographed and geographical co-ordinates were recorded using a Garmin Global Positioning System (GPS). Names of the sites/caves follow those of Lim et al. (2010).

Wherever practicable, transects of variable length (their length depending on the terrain), were set up, either along the base of the hill or vertically up steep earth-covered slopes in gullies as high as was possible to scramble without using climbing equipment or on the summit. Transects were 5 m wide, but of variable length and were often discontinuous depending on the diverse nature of the terrain. All plants along the transect were recorded, microhabitats were identified and the types of threats and level of disturbance recorded. For some microhabitats, for example, vertical cliffs or stalactites, transects were not appropriate, so the entire area was surveyed until no additional species were recorded. Plants on cliff faces were identified visually using binoculars. From the surveys, species lists were generated for each site and for each of their microhabitats (Suppl. material 1: Appendix).

For the state of disturbance, sites were assessed visually and by species composition using four categories: more-or-less undisturbed, moderately disturbed, very disturbed and totally disturbed. From a literature search, rare, endemic and threatened species were identified (Kiew 2014) and their habitat gleaned from information on herbarium specimens. These species were specifically searched for and, where found, the current status of their population assessed by counting population size (grouped into: less than 50 individuals, 51–100, 101–250, more than 250) and their life stages (seedling, juvenile and reproductive) were recorded.

Accurate species identification is of paramount importance, particularly where rare and threatened species are involved. To verify identification and to provide a permanent reference, specimens were collected for each species at first encounter. For Critically Endangered species, only a single shoot was collected to verify its identity without reducing the plant population. Plants with flowers and/or fruits were made into herbarium specimens and deposited in the main collection in the Kepong Herbarium (KEP) at the Forest Research Institute Malaysia. Voucher specimens were made for sterile specimens and stored separately at KEP. Photographs were taken for most species. Identification was based on local floras, recent taxonomic revisions, matching with authenticated specimens in KEP and consultation with specialists.

Data were gathered from previous literature on Batu Caves, from herbarium holdings in the Forest Research Institute Malaysia (KEP), University of Malaya (KLU) and Singapore Botanic Garden (SING). The comprehensive recent botanical inventories from the Rapid Biodiversity Assessment in 2016 and Batu Caves Scientific Expedition in 2019 provided up-to-date information on the vascular plant species still surviving on Batu Caves.

To determine the CIS, several criteria were used and scores were assigned (Table 4): provenance (native or alien); whether it is a component of primary or secondary vegetation or is a weed; whether it is restricted to growing on limestone substrates, most frequently grows on limestone or grows on a variety of substrates, i.e. is indifferent to substrate type; and level of endemism, whether it is a site endemic, i.e. known only on Batu Caves or from Batu Caves and a few other sites in the state of Selangor or is endemic in Peninsular Malaysia. Provenance and endemic status were obtained by reference to the species distribution reported in standard floras and Turner (1997) and whether it is restricted to limestone substrates from Chin (1977, 1979, 1983a, b).

Conservation status is important because it indicates the level of threat of extinction of the species. In order to assess the conservation status of Malaysian species, the IUCN Red List Categories and Criteria 3.1 (IUCN 2019) were applied. The IUCN Red List Categories define the extinction risk of the species assessed. A total of nine Red List Categories are used: Extinct (EX), Extinct in the Wild (EW), Critically Endangered (CR), Endangered (EN), Vulnerable (VU), Near Threatened (NT), Least Concern (LC), Data Deficient (DD) and Not Evaluated (NE). Critically Endangered (CR), Endangered (EN) and Vulnerable (VU) species are considered to be threatened with extinction. The conservation status assessment here may be different from those published on the IUCN Red List for plants if a particular taxon is not endemic in Peninsular Malaysia, in which case, it is a regional assessment (Chua and Saw 2006). For species endemic to Peninsular Malaysia, the conservation status is the global status. Extent of Occupancy (EOO) for species restricted to limestone hills is assumed to be same as its Area of Occupancy (AOO) due to substrate restriction. The distributions of all the Batu Caves endangered species fall outside the network of Totally Protected Areas. The comprehensive Taxon Data Information Sheet (TDIS) is used to score each species to produce a relevant conservation status for it in the context of Peninsular Malaysia. The TDIS comprises scientific name, taxonomy details, common names, habitat preferences, geographical range, general distribution pattern, population decline, threats, Red List Categories and Criteria, a rationale for the listing, current conservation measures, utilisation, literature used in assessment, details of assessor(s), date of assessment and names of evaluator.

Figure 1.

Study sites on Batu Caves, a limestone karst in Selangor, Peninsular Malaysia (Google Maps).

From the CIS, species, microhabitats and sites could be compared (Table 4). Species of greatest conservation importance are those that score highest (22), the result of a combination of being a native species of primary vegetation, restricted to limestone habitats, endemic to Batu Caves and Critically Endangered conservation status. Species of no conservation importance with a score of zero are alien weeds that grow on a variety of soil types and have a wide extra-Malaysian distribution and are categorised as Least Concern.

The Rapid Biodiversity Assessment survey collected a total 127 plant species in 101 genera and 53 families (Table 5). This is about 34% of the 366 species recorded from Batu Caves since 1890. However, Kiew et al. (in press) document changes in the flora and note that, for example, half the orchid species (20 species) have not been recently collected and that four species, Polyalthia guabatuensis, Sageretia thea var. malesiana, Sapium insigne and Sauropus macranthus, that grew in the buffer zone that has been almost eliminated, are now probably extinct in Malaysia. The crucial factor, however, is whether species of conservation importance persist on Batu Caves and these were the focus of collecting and most were located (Table 6).

Species of greatest conservation concern are the threatened species. The Flora of Peninsular Malaysia project is in the process of assessing the conservation status of vascular plants and, to date, about 12% of vascular plant species have been assessed. Of those assessed, 23 species recorded from Batu Caves (Table 6) are provisionally assessed as threatened (Rafidah, in press). Six species were assessed as CR, 13 as EN, three as VU and one as DD. Five species are endemic to Batu Caves and three are endemic in the State of Selangor. A further five species are not endemic, but, in Peninsular Malaysia, are known only from Batu Caves. Threatened species with the highest CIS are the Critically Endangered Epithema parvibracteatum and Rhaphidophora burkilliana, both endemic in Batu Caves, which score the maximum CIS of 22. Amongst the other threatened species (assessed as Endangered or Vulnerable) are the species restricted to Selangor limestone, Maxburretia rupicola and Ophiorrhiza fruticosa that score 19 or 21, respectively, while the nine other threatened species score 13–19 (Table 6). The great majority are restricted to limestone and most are endemic in Peninsular Malaysia.

Table 6 illustrates the wide range of microhabitats (exposed cliff face, lower and upper steep earth-covered slopes, screes, cave mouth, rocky summit, summit with peaty soil, doline and shaded vertical cliffs) in which these threatened species occur and the fact that many are confined to a single specific microhabitat. While some threatened species are common in their microhabitat on Batu Caves, like Pararuellia sumatrensis var. ridleyi and Typhonium fultum and have sizable populations of more than 250 individuals and are represented by all life stages; others are of particular conservation concern due to their small population size. Species that grow on the lower levels of the steep earth-covered slopes are particularly vulnerable to habitat disturbance as is illustrated by the decline in populations of Argostemma inaequilaterum and Begonia phoeniogramma. The only known population of Argostemma inaequilaterum has been eliminated (Chin 1980). We were only able to locate a single specimen of A. inaequilaterum in the vicinity of this original population.

The major threat that endangers all these species on Batu Caves is habitat disturbance, whether from encroachment, quarries or fire (Figure 2). The Critically Endangered (CR) species confined to specialised, narrow microhabitats (Table 6) are particularly vulnerable to disturbance. Epithema parvibracteatum (Figure 5) and Rhaphidophora burkilliana grow only in light shade, wet screes of small, fallen boulders, a microhabitat that is only associated with caves. Impatiens ridleyi only grows in light shade on vertical walls of cave mouths or on stalactites that are kept damp by dripping water (Figure 6). In addition, Epithema parvibracteatum and Impatiens ridleyi are particularly vulnerable, being short-lived herbs that depend on stable conditions to enable the next generation to become re-established from seed. However, the fact that the I. ridleyi population has survived at the type site for over a hundred years from its discovery in the 1890s (Ridley 1898) until today in spite of the surrounding anthropogenic activities (Figure 3) indicates that, if a habitat is protected from change, the species can survive indefinitely.

Figure 2.

Aftermath of extensive accidental burning on Batu Caves.

The diversity of microhabitats identified on Batu Caves is illustrated by the 16 microhabitats listed in Tables 1, 2. Characteristic of the limestone flora is the relatively high number of threatened species that occupy specific and often restricted microhabitats (Tables 6, 7). This emphasises that, for any conservation survey of limestone karst hills, a necessary first step is therefore to identify the various microhabitats and their associated species. For the first time, a quantitative method is used that makes it possible to assess the relative conservation importance of each microhabitat, irrespective of the number of species recorded (Suppl. material 1: Appendix). Number of species does not necessarily correlate with the conservation importance of a habitat though this is often used as a criterion in Environmental Impact Assessments (EIA). For example, the cave mouth at Gua Belah (Site 10) supports 10 species which together have a CIS of 111, compared with the secondary vegetation that grows on the lower slope below Gua Belah and has twice the number of species (21 species), but the CIS is only half (63) that of the cave mouth (Table 8).

Figure 3.

The vertical shaded wall microhabitat illustrates high biodiversity of limestone hills.

Amongst these microhabitats, those that stand out as harbouring most species of conservation importance (Table 7) are the steep, shaded earth-covered slopes (microhabitat f), those associated with caves (microhabitats j and k), the craggy summit (microhabitats m and n), the dolines (microhabitat g) and the vertical wet shaded rock faces (microhabitat i). Their high score is a result of the combination of their threatened status, level of endemism and their being restricted to limestone. Even remnants of the buffer zone (microhabitat c) still also harbour plant diversity.

Sites of greatest conservation importance are recognised by their high total CIS (Table 7). Due to the rugged topography of karst hills, several very different microhabitats can be found at a single site. For example, sites with undisturbed caves, such as Gua Belah, have one of the highest CIS (723) because it covers six different microhabitats (Table 8). Using total CIS as a tool to compare sites, in spite of great variation in area, number of species, level of disturbance etc., it is possible to identify those that are of greatest conservation importance (Table 9).

Sites outstanding for their high total CIS (Table 9, Figure 4, Suppl. material 1: Appendix), include those either where species diversity is particularly high (Site 8 Kampung Wira Damai), the only site on Batu Caves where undisturbed limestone forest persists or where several species of high conservation importance occur, like the summit (Site 9 Fig. Tree Cave) or sites that include several different microhabitats, like the sites with caves, such as Site 10 Gua Belah (Table 8) and Site 7 Temple Cave.

Figure 4.

Conservation Importance Score (CIS) and species for all sites on Batu Caves.

Habitat deterioration from anthropogenic activities is the major threat to the biodiversity of Batu Caves and its effect on the flora is brought into focus by comparing their CIS (Table 9). All sites that score less than CIS 100 have been severely disturbed and hardly any or no element of the limestone flora remains. Sites that score between CIS 103–113 are those where, while most of the limestone flora has been eliminated, a few species have managed to survive. Sites with a CIS of more than 180 include microhabitats that still retain their diversity and species of conservation importance. However, the deleterious effect of disturbance can be seen by comparing Site 7 (CIS 329) and Site 10 (CIS 723) that are both cave sites with similar microhabitats. Site 7, that houses the Temple Cave, has been heavily disturbed by infrastructure provided to accommodate many visitors compared with Site 10 Gua Belah, which, apart from clearing the limestone forest from the base and lower slopes, is still relatively undisturbed. The only biodiverse microhabitats to survive are the permanently wet vertical walls and stalagmites and the greatly degraded scree, but even so, small populations of the threatened Begonia phoeniogramma, Epithema parvibracteatum and Impatiens ridleyi are greatly reduced and constantly face extermination by new ‘beautification’ projects.

Figure 5.

Epithema parvibracteatum (Gesneriaceae), endemic to Batu Caves.

Figure 6.

The type locality of Impatiens ridleyi (Balsaminaceae) in danger.

Figure 7.

Paraboea verticillata (Gesneriaceae), one of a very few indigenous species that can colonise quarried rock faces.

The three criteria for identifying IPAs are species richness, presence of threatened species and threatened habitats (Anderson 2002). The criteria were revised for tropics to incorporate new elements to be scientifically robust and applicable globally (Darbyshire et al. 2017). Under the Malaysia National Strategy for Plant Conservation, Malaysia is committed to conserve 50% of IPAs (Saw et al. 2009). As limestone areas are recognised nationally as Environmentally Sensitive Areas (ESA Rank 1), limestone hills automatically qualify as a threatened habitat. On all three criteria, the area of Batu Caves qualifies as an IPA. With 366 species, Batu Caves is more species-rich than any other limestone hill in Peninsular Malaysia (Kiew et al., in press) and it is home to 23 threatened species, of which four are endemic to Batu Caves (Rafidah, in press). However, until today, it still does not have secure legal protection and encroachment continues unabated.

Several state-wide surveys have attempted to rank karst hills by their relative biodiversity importance, based on species lists and identifying rare and threatened species (e.g. for Perak (Malaysian Nature Society 1991); for Kelantan (Davison and Kiew 1990); for Perlis (Kiew 1993)). However, not being quantitative makes comparison of their conservation value between hills difficult when the hills harbour different assemblages of species, different rare and endangered species and different levels of disturbance. Surveying all microhabitats and implementing CIS not only gives weight to threatened species, but also provides a quantitative value for the hill’s overall biodiversity and it immediately distinguishes pristine vegetation from disturbed or secondary vegetation or vegetation comprised of alien or weed species. An additional advantage of the CIS over basing comparison mainly on the presence of rare and threatened species is that it also quantifies biodiverse limestone flora that might not include many rare and threatened species. Once a quantitative method, like the CIS method, is implemented, it provides a scientific basis for identifying hills that are IPAs. It is then possible to compare and so rank the 445 limestone hills in Peninsular Malaysia i.e. those of outstanding conservation value that need to be gazetted as Totally Protected Areas to comprehensively protect Peninsular Malaysia’s limestone flora. Only those with low biodiversity value or are badly degraded can be considered for exploitation. As a single hill protects only a fraction of the limestone flora, state and national networks of limestone hills need to be identified and protected.

In Malaysia, before a mining licence is issued, it is a requirement to carry out a Detailed Environmental Impact Assessment under Environmental Quality (Prescribed Activities) (Environmental Impact Assessment) Order 1987. There are no recommended standard methodologies required. Most frequently, species lists are provided. However, because there is no method to evaluate the conservation importance of species, the lists are often bulked up by listing the scientific names of fruit trees, weeds and other alien species. Indeed, it is not unusual for these lists to include no limestone species at all. The EIAs for mining the Chiku limestone, Kelantan and Gunung Pulai, Kedah, were examples of this practice. That number of species is not a direct indicator of conservation importance of a site is clearly shown at Batu Caves, where disturbed sites can be species-rich with weed species that have no conservation value, whatsoever (compare Site 11 and Site 10.5, for example). Nor is there is any requirement that populations of known narrowly endemic species be located and assessed (Kiew et al. 2019). In a few cases, where results from quadrats and fixed-length transects are included, because of the rugged terrain, they are usually sited in disturbed vegetation around the flat base of the karst (e.g. G. Kanthan, Perak) and so do not capture the diversity of microhabitats and their species. In fact, results from quadrats and fixed-length transects can be positively misleading in providing species lists of abundant and common weed or secondary species, while entirely missing rare site endemics that occupy narrow microhabitats.

Requiring the implementation of the Conservation Importance Scoring in EIAs would provide a robust methodology that would ensure that species and microhabitats with high CIS are relocated and their populations assessed. Data based on (i) identification and survey of all microhabitats, (ii) search for all known rare and threatened species recorded from the particular hill; and (iii) accurately identified plant species, would provide a sound scientific basis to evaluate the biodiversity importance of an individual karst.

As this plant diversity survey of Batu Caves illustrates, implementation of the CIS, involving survey of all microhabitats for maximum species capture, search for known rare and threatened species and accurate identification of species, provides a robust, quantitative methodology for enabling comparison of individual karst hills at the state or national levels so that those with greatest conservation value can be designated as IPAs and form a network of limestone hills that comprehensively cover the diversity of the limestone flora in Peninsular Malaysia.