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Status of Biological Diversity in Malaysia<br />

and<br />

Threat Assessment of Plant Species in Malaysia<br />

Proceedings of the Seminar and Workshop<br />

28 30 June 2005


THE STATUS OF MAMMALIAN BIODIVERSITY IN MALAYSIA<br />

1. Macaca nemestrina (Cercopithecidae) Photo courtesy L.G. Saw<br />

2. Rhacophorus bipunctatus (Rhacophoridae). Photo courtesy Elango Velautham<br />

3. Cyrtodactylus cavernicolus (Gekkonidae). Photo courtesy Indraneil Das<br />

4. Panthera tigris (Felidae). Photo courtesy L.G. Saw<br />

5. Cervus unicolor (Cervidae). Photo courtesy G.W.H. Davison<br />

6. Calliophis bivirgata (Elapidae). Photo courtesy Jeet Sukumaran<br />

7. Amyda cartilaginea (Trionychidae). Photo courtesy Indraneil Das<br />

8. Bufo parvus (Bufonidae). Photo courtesy Norsham Yaakob<br />

9. Riverine vegetation in a Malaysian lowland dipterocarp forest. Photo<br />

courtesy L.G. Saw<br />

2


G.W.H. DAVISON & ZUBAID AKBAR (2007)<br />

STATUS OF BIOLOGICAL DIVERSITY IN MALAYSIA &<br />

THREAT ASSESSMENT OF PLANT SPECIES IN MALAYSIA<br />

THE STATUS OF MAMMALIAN BIODIVERSITY<br />

IN MALAYSIA<br />

1<br />

G.W.H. Davison & 2 Zubaid Akbar<br />

ABSTRACT<br />

There are approximately 298 valid named species of non-marine mammals within the political<br />

borders of Malaysia. This total includes 229 species in Peninsular Malaysia, and 221 species<br />

in East Malaysia (Sabah and Sarawak), of which 152 species are shared. Over the past 22<br />

years the list for Peninsular Malaysia has expanded by 22, and over the past 25 years the list<br />

for East Malaysia has expanded by 30. Most of the additions are bats. Two genera of mammals<br />

(Pithecheirops, Diplogale) and 30 species are endemic to Malaysia, so far as records now<br />

show. Biodiversity questions range from historical uncertainty, to the definition of geographical<br />

limits, continued survival, synonymy, species already described elsewhere but newly recorded<br />

(various examples) and taxonomy of cryptic species. Since these questions are so varied in<br />

type, scattered across a range of taxa, and each involve few species, it will be inefficient to<br />

focus research effort on a major untargetted build-up of museum specimens. Two important<br />

fields to concentrate on are genetic diversity/biosystematics (including within-species<br />

diversity), and conservation (population dynamics, habitat availability, community structure).<br />

These will be important for retaining the genetic viability of increasingly fragmented<br />

populations of forest mammals, and can only be effective if adequate resources are available<br />

to support research as well as management posts with associated capacity-building.<br />

INTRODUCTION<br />

The status of the biodiversity of mammals, like that of other biological groups, can be divided<br />

into two main themes: first, the description of the diversity that exists at the various genetic,<br />

population and species levels of taxonomy; and second, documenting the changes in numbers<br />

of each species in the wild, as a response to development and other pressures.<br />

Knowledge about the total number of mammal species that occur in Malaysia is still increasing<br />

rapidly, and there are still several taxonomically difficult groups (for example Cynopterus;<br />

Crocidura; Myotis; Haeromys; Petaurillus; Glyphotes). There are approximately 298 valid<br />

named species of non-marine mammals within the political borders of Malaysia (Table 1;<br />

1<br />

National Parks Board, Singapore Botanic Gardens, 1 Cluny Road, Singapore 259569;<br />

Geoffrey_Davison@NParks.gov.sg<br />

2<br />

School of Environmental and Natural Resource Sciences, Universiti Kebangsaan Malaysia, 43600 Bangi, Selangor;<br />

zubaid@pkrisc.cc.ukm.my<br />

3


THE STATUS OF MAMMALIAN BIODIVERSITY IN MALAYSIA<br />

Appendix), and perhaps another four known but unnamed species. This total includes 229<br />

species in Peninsular Malaysia, and 221 species in East Malaysia (Sabah and Sarawak), of<br />

which 152 species are shared. This means that 77 of the species in Peninsular Malaysia have<br />

not been found in Sabah or Sarawak, and for 68 species the reverse is true. Over the past 22<br />

years there have been 23 additions and one deletion (a mongoose) from the list for Peninsular<br />

Malaysia. One species (Javan Rhino Rhinoceros sondaicus) has become locally extinct there<br />

in historical time. Over the past 25 years there have been 31 additions and one deletion (the<br />

squirrel Glyphotes canalvus, sunk in the synonymy of Callosciurus orestes) to the list in East<br />

Malaysia. Nearly all of the additions are of bats.<br />

Table 1. Diversity of mammals in the three major political divisions of Malaysia*.<br />

Peninsular Sarawak Sabah Sabah &<br />

Malaysia<br />

Sarawak<br />

Total species 229 180 203 221<br />

recorded<br />

Total genera 108 98 104 105<br />

recorded<br />

Total families 32 30 31 31<br />

recorded<br />

Non-bats 123 118 120 129<br />

Most speciose Bats (106), Bats (62), Bats (83), Bats (92),<br />

orders Rodents (55) Rodents (56) Rodents (58) Rodents (62)<br />

Most speciose Rhinolophus (18), Rhinolophus (8), Myotis (10), Hipposideros<br />

(11),<br />

genera Hipposideros (18), Hipposideros (8), Rhinolophus (8) Rhinolophu (10),<br />

Myotis (9) Tupaia (8), Tupaia (8) Myotis (10)<br />

No. of genera 63 58 61 61<br />

with 1 species<br />

No. of families 9 12 (2†) 13 13<br />

with 1 species<br />

No. of orders 3 2 3 3<br />

with 1 species<br />

* Compiled after various authors.<br />

† The two families that were each represented by a single species, now locally extinct, in Sarawak are<br />

Bovidae (Bos javanicus) and Rhinocerotidae (Dicerorhinus sumatrensis)<br />

Of 128 bats recorded from Malaysia, 106 are known from Peninsular Malaysia and 92 from<br />

Sabah and Sarawak. Of 178 non-flying terrestrial mammals recorded from ‘Malaysia, 123<br />

are known from the Peninsula and 129 from Sabah and Sarawak. Thus only 22 (24%) of the<br />

bats known from Sabah and Sarawak are not shared with the Peninsula, whereas 55 (42.6%)<br />

of the non-flying mammals from Sabah and Sarawak are not shared. There is greater similarity<br />

between the bat faunas of these geographically separate areas than between their non-bat<br />

faunas.<br />

Two genera (Pithecheirops, Diplogale) and 30 species are known only from records within<br />

the political boundaries of Malaysia, and for the time being they can be considered endemic<br />

(Table 2). There is obviously a strong possibility that species known from Peninsular Malaysia<br />

and lowland Sabah/Sarawak may also occur in Kalimantan, Sumatra and/or Brunei.<br />

4


G.W.H. DAVISON & ZUBAID AKBAR (2007)<br />

Table 2. Mammals so far known only from specimens and sightings within the political<br />

boundaries of Malaysia<br />

Suncus ater Sabah (Kinabalu) Montane<br />

Crocidura baluensis Sabah (Kinabalu) Montane<br />

Tupaia montana Sarawak, Sabah Montane<br />

Rhinolophus convexus Peninsular Malaysia Montane<br />

Rhinolophus chiewkweeae Peninsular Malaysia Lowland<br />

Hipposideros ‘bicolor’ 142 kHz Peninsular Malaysia Lowland<br />

Hipposideros coxi SW Sarawak Lowland<br />

Hipposideros nequam Peninsular Malaysia Lowland<br />

Myotis ridleyi Peninsular Malaysia, Sabah Lowland<br />

Myotis gomantongensis Sabah Lowland<br />

Pipistrellus cuprosus Sabah Lowland<br />

Pipistrellus societatis Peninsular Malaysia Lowland<br />

Hesperoptenus doriae Peninsular Malaysia, Sarawak Lowland<br />

Hesperoptenus tomesi Peninsular Malaysia, Sabah Lowland<br />

Murina aenea Peninsular Malaysia, Sabah Lowland<br />

Murina rozendaali Peninsular Malaysia, Sabah Lowland<br />

Kerivoula sp. nov. Peninsular Malaysia Lowland<br />

Callosciurus (Glyphotes) simus Sabah, Sarawak Montane<br />

Lariscus hosei Sabah, Sarawak Largely montane<br />

Dremomys everetti Sabah, Sarawak Montane<br />

Petaurillus emiliae Sarawak Lowland<br />

Maxomys alticola Sabah Montane<br />

Maxomys baeodon Sabah, Sarawak Montane<br />

Maxomys inas Peninsular Malaysia Montane<br />

Lenothrix malaisia Peninsular Malaysia, Sabah, Sarawak Lowland<br />

Pithecheirops otion Sabah Lowland<br />

Chiropodomys major Sabah, Sarawak Lowland and submontane<br />

Melogale everetti Sabah Montane<br />

Diplogale hosei Sabah, Sarawak Montane<br />

Herpestes hosei Sarawak Unknown<br />

Endemic to PM 7 (Lowland 5; Montane 2)<br />

Endemic to Sabah 7 (Lowland 3; Montane 4)<br />

Endemic to Sarawak 3 (Lowland 2; Unknown 1)<br />

Endemic to Sabah + Sarawak 7 (Lowland 1; Montane 6)<br />

Endemic to PM + Sabah and/or Sarawak 6 (Lowland 6)<br />

Total endemic to Malaysia 30 (Lowland 17; Montane 12; Unknown 1)<br />

Several species can be considered near-endemic, that is, they have been recorded from within<br />

and also from just beyond the borders of Malaysia, or almost certainly occur beyond Malaysia<br />

based on habitat requirements (Table 3). The number of endemics and near-endemics is<br />

uncertain for two main reasons: some species (especially bats) are known from only a handful<br />

of specimens, so they could easily turn up elsewhere; and suitable habitat in adjacent territories<br />

(e.g., Kalimantan) may have been insufficiently studied. A couple of montane forms in<br />

Peninsular Malaysia, otherwise endemic, might extend just across the border into Thailand.<br />

One bat, Myotis oreias, is known from only a single specimen from Singapore, where later<br />

surveys have failed to find it; if the species is valid, it might still survive in Malaysia or<br />

elsewhere in the region.<br />

5


THE STATUS OF MAMMALIAN BIODIVERSITY IN MALAYSIA<br />

Table 3. Species of mammals known predominantly from within the political boundaries of<br />

Malaysia, but which are either known or almost certainly occur in similar habitats in adjacent<br />

territories.<br />

Tupaia longipes*<br />

Sabah and Sarawak, southwards into East Kalimantan<br />

Dendrogale melanura<br />

Mountains of north & central Borneo – under-recorded Kalimantan?<br />

Hipposideros ridleyi<br />

Extinct in Singapore, otherwise only known within Malaysia<br />

Callosciurus baluensis Mountains of north & central Borneo –<br />

under-recorded Kalimantan?<br />

Callosciurus adamsi<br />

Not recorded yet from Kalimantan?<br />

Callosciurus orestes<br />

Mountains of north & central Borneo – under-recorded Kalimantan?<br />

Petaurillus hosei / kinlochi* Peninsular Malaysia, Sabah, Sarawak; known from Brunei<br />

*Taxonomic status uncertain<br />

In addition to endemics and near-endemics, Malaysia possesses some mammal populations<br />

of major significance; either they represent a significant proportion of the whole species, or<br />

they are genetically distinctive. Bennett (1991) estimated about 2000 to 3000 Proboscis<br />

monkeys Nasalis larvatus in Sabah, and fewer than 1000 in Sarawak. Numbers in Kalimantan<br />

are not known, but the Malaysian population might be one quarter or one third of the world<br />

population. There are about 11,000 Orang-utans Pongo pygmaeus morio in Sabah, and perhaps<br />

500 Pongo pygmaeus pygmaeus in Sarawak. The Sabah population is one of the largest in<br />

the world, with tremendous conservation importance. The Sabah population of the Asian<br />

Elephant Elephas maximus, which just extends into East Kalimantan, may amount to 1600<br />

individuals. Not only is this a relatively large proportion of the whole species (about 5%), but<br />

the population is genetically distinctive, and therefore it is also internationally important<br />

(Fernando et al., 2003). These are just three examples of mammals for which Malaysia has<br />

special conservation responsibilities.<br />

Around 87 out of the total number of Malaysian mammals (about 292, according to the<br />

splitting taxonomy adopted by IUCN 2004) have been given some sort of conservation risk<br />

status (Table 4). They include six Critically Endangered, 15 Endangered, 24 Vulnerable, 33<br />

Lower Risk, and nine Data Deficient species. They represent about 30% of Malaysia’s<br />

mammals. Of the 30 Malaysian endemics, 3 are Critically Endangered, 4 Endangered, 5<br />

Vulnerable, 2 Lower Risk and 3 Data Deficient, making 17 or 57% of the endemics under<br />

some degree of threat, as far as they have been assessed. IUCN (2004) in fact lists 111 species<br />

at risk, but their total includes 18 marine mammals not considered here—for some of these,<br />

occurrence is anecdotal—and three terrestrial species that have not in fact occurred in Malaysia<br />

(Macaca leonina, Prionailurus viverrinus (possible), and Ursus thibetanus).<br />

Pangolin, elephant and flying lemur are the three mammalian orders with only one local<br />

representative each. Loss of genetic diversity in any of these could be ranked as a more<br />

serious national loss than, say, the loss of genetic diversity in a family or genus with many<br />

representatives.<br />

Since the last edition of the most recent taxonomic summaries (Medway 1983; Payne et al.<br />

1985) there has been one significant change at family level (Herpestidae is often now<br />

recognized as separate from Viverridae); nine changes at generic level (a new genus<br />

Pithecheirops; generic splits e.g. Arielulus, Hypsugo, etc.), and about 23 changes at species<br />

level (truly new discoveries; taxonomic splits; sunk as synonyms; name changes).<br />

6


G.W.H. DAVISON & ZUBAID AKBAR (2007)<br />

Table 4. List of threatened terrestrial mammals in Malaysia (listing and taxonomy follow<br />

IUCN, 2004).<br />

CR = Critically Endangered (6 species)<br />

EN = Endangered (15 species)<br />

VU = Vulnerable (24 species)<br />

LR/nt = Lower Risk/near-threatened (33 species)<br />

DD = Data Deficient (10 species)<br />

Species Category Criteria (IUCN 2004)<br />

Chimarrogale hantu CR B1+2c (= C. phaeura part)<br />

Dicerorhinus sumatrensis CR A1bcd; C2a<br />

Hipposideros nequam CR B1+2c<br />

Rhinoceros sondaicus CR C2a Now extinct within<br />

Malaysia Rhinolophus convexus CR D<br />

Suncus ater CR B1+2c<br />

Bos javanicus EN A1cd + 2cd; C1+<br />

Catopuma badia EN C2a(ii)<br />

Chimarrogale phaeura EN B1+2c<br />

Crocidura malayana EN B1+2c<br />

Cuon alpinus EN C2a(i)<br />

Cynogale bennetti EN A1ce; C2a<br />

Elephas maximus EN A1cd<br />

Hesperoptenus doriae EN B1+2c<br />

Maxomys alticola EN C2a<br />

Maxomys baeodon EN C2a<br />

Nasalis larvatus EN A2c; C1+2a<br />

Panthera tigris EN C2a(i)<br />

Pongo pygmaeus EN A2cd<br />

Rattus baluensis EN B1+2c<br />

Tupaia longipes EN B1+2c (= Tupaia glis?)<br />

Pipistrellus cuprosus VU A2c<br />

Bos gaurus VU A1cd + 2cd; C1+<br />

Capricornis sumatraensis VU A2cd<br />

Catopuma temminckii VU C2a(i)<br />

Dendrogale melanura VU B1+2c<br />

Diplogale hosei VU B1+2c<br />

Haeromys margarettae VU A1c; B1+2c<br />

Haeromys pusillus VU A1c<br />

Hipposideros coxi VU D2<br />

Hipposideros ridleyi VU B1+2c<br />

Hystrix brachyura VU A1d<br />

Lariscus hosei VU B1+2c<br />

Lutra perspicillata VU A2acd<br />

Macaca arctoides VU A1cd<br />

Macaca nemestrina VU A1cd<br />

Melogale everetti VU B1+2c<br />

Neofelis nebulosa VU C2a(i)<br />

Pardofelis marmorata VU C2a(i)<br />

Prionailurus planiceps VU C2a(i)<br />

[Prionailurus viverrinus] VU C2a(i) (Doubtful record)<br />

Rousettus spinalatus VU C2a<br />

7


THE STATUS OF MAMMALIAN BIODIVERSITY IN MALAYSIA<br />

Suncus hosei VU B1+2c<br />

Sundasciurus jentinki VU B1+2c<br />

Tapirus indicus VU A2c+3c+4c<br />

Aethalops alecto<br />

Aonyx cinereus<br />

Chaerephon johorensis<br />

Cheiromeles torquatus<br />

Chiropodomys muroides<br />

Coelops robinsoni<br />

Dyacopterus spadiceus<br />

Hapalomys longicaudatus<br />

Harpiocephalus mordax<br />

Hipposideros lekaguli<br />

Hipposideros lylei<br />

Hylobates agilis<br />

Hylobates lar<br />

Hylobates muelleri<br />

Hystrix crassispinis<br />

Kerivoula intermedia<br />

Kerivoula minuta<br />

Macaca fascicularis<br />

Manis javanica<br />

Murina aenea<br />

Murina huttoni<br />

Murina rozendaali<br />

Myotis macrotarsus<br />

Myotis montivagus<br />

Myotis ridleyi<br />

Pipistrellus kitcheneri<br />

Presbytis femoralis<br />

Pteromyscus pulverulentus<br />

Rhinolophus creaghi<br />

Rhinolophus marshalli<br />

Rhinolophus philippinensis<br />

Sundasciurus brookei<br />

Symphalangus syndactylus<br />

LR/nt<br />

NT<br />

LR/nt<br />

LR/nt<br />

LR/nt<br />

LR/nt<br />

LR/nt<br />

LR/nt<br />

LR/nt<br />

LR/nt<br />

LR/nt<br />

LR/nt<br />

LR/nt<br />

LR/nt<br />

LR/nt<br />

LR/nt<br />

LR/nt<br />

LR/nt<br />

LR/nt<br />

LR/nt<br />

LR/nt<br />

LR/nt<br />

LR/nt<br />

LR/nt<br />

LR/nt<br />

LR/nt<br />

LR/nt<br />

LR/nt<br />

LR/nt<br />

LR/nt<br />

LR/nt<br />

LR/nt<br />

LR/nt<br />

Pipistrellus societatis<br />

DD<br />

Helarctos malayanus<br />

DD<br />

Hipposideros doriae DD (= H. sabanus)<br />

Lutra sumatrana<br />

DD<br />

Myotis gomantongensis<br />

DD<br />

Presbytis frontata<br />

DD<br />

Presbytis hosei<br />

DD<br />

Suncus malayanus<br />

DD<br />

[Trachypithecus villosus] DD (= Presbytis cristata part)<br />

Apparently rare but not yet assessed:<br />

Hipposideros orbicularis ?<br />

Rhinolophus chiewkweeae ?<br />

Kerivoula sp. nov. ?<br />

8


G.W.H. DAVISON & ZUBAID AKBAR (2007)<br />

LITERATURE REVIEW<br />

The basis for an understanding of mammal diversity in Peninsular Malaysia was set in place<br />

by the work of H.C. Robinson, C.B. Kloss and F.N. Chasen, in the period from 1902 until<br />

1941. Their work was primarily taxonomic and geographical, sampling and listing, describing<br />

species and subspecies, especially island races, of nearly all mammals. They deposited their<br />

collections in the Federated Malay States Museums and/or the Raffles Museum Singapore,<br />

with duplicates going largely to the British Museum (Natural History). Chasen (1940)<br />

published the definitive Handlist that summarises all of the earlier literature. Between them<br />

these three scientists produced nearly 200 publications on mammals of the region, including<br />

38 by Chasen (Tweedie 1948) and a massive 86 by Kloss (Banks 1951), mostly concerning<br />

Peninsular Malaysia but extending as far as India, Vietnam, Hainan and Java.<br />

In Sarawak, an equivalent process was undertaken first by A.H. Everett (1893), who collected<br />

natural history specimens and published a first list of mammals for Borneo, and then by the<br />

directors of the Sarawak Museum. Sarawak and Sabah received some attention from the<br />

Federated Malay States Museums (e.g., Chasen & Kloss 1931), while Hill (1960) provided a<br />

long publication on the Robinson Collection of mammals in the British Museum (Natural<br />

History) that included Bornean as well as Malay Peninsula material. Knowledge about the<br />

mammals of Sabah was added to by Davis (1962) and by Harrison (1964).<br />

Beginning at a slightly later period, agencies such as the Institute for Medical Research, the<br />

Department of Wildlife & National Parks, related institutions such as the Malaysian<br />

Agricultural Research and Development Institute (MARDI) and the Palm Oil Research<br />

Institute Malaysia (PORIM and its successors), as well as Malaysian universities have<br />

contributed to a wide array of mammalian studies. Thus, while the main taxonomic collections<br />

were museum-based and dated largely from the colonial era, more specialized collections for<br />

particular research purposes were also developed on a smaller scale within local institutions.<br />

The range of taxonomic methods applied has become highly sophisticated, including DNA<br />

hybridization (e.g., Han et al. 2000), gene sequencing (e.g., Fernando et al. 2003), and<br />

analysis of ultrasound (e.g., Kingston et al. 2001) and audible sound (Ross 2004). The emphasis<br />

of recent taxonomic work has been on cryptic species within traditionally difficult taxa,<br />

using a combination of new and classical morphometric techniques to separate out the species,<br />

e.g. by Ruedi (1995, 1996). The following paragraphs touch on some main areas of work, but<br />

are far from complete; many other studies of equal interest could be mentioned. Many relevant<br />

papers have appeared in the Journal of Wildlife & Parks, the Malayan Nature Journal and the<br />

Sarawak Museum Journal.<br />

Bio-medical studies, especially of mammal-borne zoonoses, have been the province of the<br />

Institute for Medical Research (e.g., Lim 1973; Lim et al. 1977). There has been a very<br />

strong emphasis on small mammals such as rats and squirrels, but a liberal research policy<br />

has led to publications on many species of mammals large and small, and on community<br />

ecology, altitudinal zonation and other topics. As vectors of economically and socially<br />

important diseases, the parasites of Malaysian mammals have come under scrutiny for many<br />

years (e.g. Mullin et al. 1972; Zunika et al. 2002). Escalante et al. (2005) have recently<br />

shown that South-east Asia—rather than Africa, as previously thought—may be the origin<br />

of the human-infecting Plasmodium vivax, now existing nearly worldwide. Furthermore, the<br />

dependence of endoparasites and ectoparasites (e.g., Fain et al. 1984) on mammalian (and,<br />

9


THE STATUS OF MAMMALIAN BIODIVERSITY IN MALAYSIA<br />

of course, many other) hosts adds a level of meta-diversity to the diversity of the hosts<br />

themselves. If a species of mammal declines or disappears, it sets in progress a whole train of<br />

other extinctions.<br />

Physiological studies have been rather limited, but examples include, e.g., Pevet & Yadav<br />

(1980), Rudd (1965), Medway (1971), Whittow & Gould (1976), Whittow et al. (1977a,<br />

1977b). This still leaves great scope for investigating the potential range of diversity in<br />

physiological mechanisms and responses, seasonality and environmental cues, unusual<br />

digestive physiology, responses to lunar cycles, and other features that might be expected in<br />

a tropical forest fauna with high species diversity and many behavioural specializations.<br />

Zoogeographical studies (e.g., Chasen 1940, Raven 1935, Shukor 1996, Meijaard 2003)<br />

and taxonomic studies have been the staple of Malaysian-based and foreign-based research,<br />

at least until the advent of single-species ecological research projects in the 1960s. Of many<br />

possible examples, the more genetically-based studies include those by Medway & Yong<br />

(1976), Yong (1970, 1975, 1982) and Yong & Dhaliwal (1972) on rodents. A detailed genetic<br />

analysis of 200 individual orang-utans Pongo pygmaeus by Goossens et al. (2005) is not only<br />

one of the most intensive DNA samplings of any wild primate, but has practical implications<br />

in demonstrating bottlenecks and in recommending the maintenance of forest corridors between<br />

isolated groups.<br />

Synecological studies have been carried out to a rather limited extent, examining niche<br />

differentiation between species in small groups such as primates (e.g., MacKinnon &<br />

MacKinnon in Chivers 1981); squirrels (Payne 1979); and other rodents including flying<br />

squirrels (Muul & Lim 1978). Barrett (1984) studied the community ecology of nocturnal<br />

mammals; Johns (e.g., 1986, 1992) examined the effects of logging; and Jephte (1996) has<br />

looked at some impacts of hunting.<br />

It has been shown that forest over alluvial ground in the extreme lowlands at Kuala Lompat,<br />

Krau Game Reserve, has the richest species composition of bats in the world (Kingston et al.<br />

2003). The much smaller community of small carnivores in lowland forest has also been<br />

looked at (e.g., Rajaratnam 2001, Heydon & Bulloh 1996). Emmons (2000) was able to<br />

complete an intensive study of treeshrews, including both diurnal and nocturnal species, and<br />

to demonstrate their extraordinary maternal physiology. Community structure, representing<br />

the ecological basis of biodiversity, has been described by Harrison (1962) and by Wells et al.<br />

(2004). Camera trapping has emerged as a significant research tool (Miura et al. 1997;<br />

Kawanishi 2002; Azlan & Sharma 2003; Numata et al. 2005).<br />

Autecological studies, detailed species-by-species investigations, have been conducted on<br />

about 7% of Malaysian mammals (about 11% of the non-bats). Not a single one of Malaysia’s<br />

endemic mammals has been the subject of an autecological study, but admittedly they tend to<br />

be small, less charismatic species that do not play a key ecological role (compared, for instance,<br />

with widespread key species like elephant or tiger). Table 5 lists many of the species for<br />

which there have been such studies, together with some indication of the duration of the<br />

study (as a rough guide to the intensity of the research); but this does not pretend to be a<br />

complete list. About 17 species have been the subject of detailed studies in Peninsular Malaysia,<br />

and about 8 species in Sabah and Sarawak (excluding the treeshrews). There have been fewer<br />

single-species studies in Sarawak than elsewhere (e.g., red banded langur Presbytis melalophos<br />

cruciger at Maludam; proboscis monkey Nasalis larvatus; flying fox Pteropus vampyrus) but<br />

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G.W.H. DAVISON & ZUBAID AKBAR (2007)<br />

Table 5. Partial list (for additions and improvements) of single-species ecological studies,<br />

with a rough indication of the length of studies and names of researchers or institutions.<br />

Many shorter studies, and mixed field and laboratory studies, could be added to this list,<br />

which emphasizes graduate-level field research. DWNP = Dept. of Wildlife & National Parks.<br />

Tiger >5 years (Kawanishi; DWNP; WWF)<br />

Siamang >5 years (Chivers; Raemaekers)<br />

White-handed Gibbon >5 years (Chivers; Raemaekers; Vellayan)<br />

Orang-utan >5 years (MacKinnon, Ancrenaz, short studies)<br />

Elephant >5 years (Olivier, Mohd Khan, DWNP)<br />

Long-tailed Macaque >3 years (Aldrich-Blake; Mah)<br />

Pig-tailed Macaque 3 years (Caldecott)<br />

Banded Langur 3 years (Bennett; Curtin; Ahmad)<br />

Dusky Langur 3 years (Hardy; Curtin)<br />

Maroon Langur 3 years (Davies)<br />

Proboscis Monkey >3 years (Boonratana, Bennett et al.)<br />

Tapir 3 years (Williams, DWNP)<br />

Seladang >3 years (Conry, DWNP)<br />

Wild Boar 3 years (Ickes, Diong)<br />

Sumatran Rhino >3 years (Flynn, Tajuddin, DWNP)<br />

Flying Fox 3 years (Gumal)<br />

Spotted-winged Fruit-bat 3 years (Hodgkison)<br />

Sun Bear 3 years (Wong Siew Te)<br />

Agile Gibbon 2 years (Gittins)<br />

Plantain Squirrel 2 years (Hafidzi)<br />

Slow loris 2 years (Barrett)<br />

Rusa Intermittent (DWNP)<br />

Serow Intermittent (DWNP)<br />

more emphasis on single-issue studies such as the effects of hunting, fire, and logging.<br />

From the earliest days there have been site-specific expeditions, to investigate places where<br />

taxonomic novelties were expected, and to fill in gaps of geographical coverage. Early examples<br />

were the expeditions led by the Federated Malay States Museums to Gunung Tahan and<br />

Gunung Kinabalu. Later examples have included Gunung Benom (Medway 1972), Pulau<br />

Tioman, Gunung Lawit (no consolidated publication), Danum Valley (Kiew 1977), Gunung<br />

Mulu (Anderson et al. 1979), and Lambir Hills (Soepadmo 1984). Furthermore, important<br />

series of papers on the conservation of mammalian diversity have been published by Wyatt-<br />

Smith & Wycherley (1961), and by Bennett (1991), Payne & Andau (1991), Ratnam et al.<br />

(1991) and Zaaba et al. (1991).<br />

AVAILABLE CHECKLISTS AND REVISIONS<br />

Checklists and revisions have formed the basis for all of the medical-related, physiological,<br />

synecological and autecological work mentioned above. There are formal checklists as well<br />

as field guides for all parts of Malaysia. The essential lists for Peninsular Malaysia were<br />

given by Medway (1969, 1978, 1983), and the relevant field guide is by Francis (2001). The<br />

11


THE STATUS OF MAMMALIAN BIODIVERSITY IN MALAYSIA<br />

list for Borneo was compiled by Medway (1965, 1977), and the relevant field guide with<br />

additions to the list is by Payne et al. (1985). Corbet & Hill (1992) provide the authoritative<br />

regional taxonomic work.<br />

There have been several revisions by group. Hill (1963) revised the genus Hipposideros,<br />

Jenkins & Hill (1981) revised the Hipposideros cervinus/galeritus complex, and Hill & Francis<br />

(1984) have made contributions on the distribution of bats generally. Zubaid (e.g., 1994),<br />

Francis (e.g., 1995), Abdullah (e.g., 2003) and their co-workers have added many records.<br />

Mongooses, a small but difficult group because of sexual dimorphism in skull size, were<br />

revised by Wells (1989). Other workers who have revised particular groups include Medway<br />

& Yong (1976) on rats; Brandon-Jones (1984) on colobines; Jenkins (1982), Davison (1984)<br />

and Ruedi (1995, 1996) on shrews; Meijaard & Groves (2004) on mouse-deer; Fernando et<br />

al. (2003) on elephants; and Han et al. (2000) on tree-shrews.<br />

SPECIMENS – WHERE ARE THEY HELD?<br />

The largest collections of relevant skins, skeletons and spirit-preserved material are in the<br />

Natural History Museum (BMNH), London; the American Museum of Natural History<br />

(AMNH), New York; the Field Museum of Natural History in Chicago; the United States<br />

National Museum in Washington; Naturalis in Leiden; the Raffles Museum of Biodiversity<br />

Research in Singapore; and in the Sarawak Museum and Sabah Museum.<br />

There are also important collections within Malaysia at the Institute for Medical Research<br />

(IMR), the Department of Wildlife & National Parks, and at Universiti Malaya and other<br />

institutions of higher learning. These tend to have enhanced value in cases where they are<br />

linked to related studies (e.g., the link between medical studies, parasite collections and<br />

mammalian host collections in IMR), and where the collections are specialized (e.g., skeleton<br />

collections at Universiti Malaya).<br />

SPECIALISTS AND THE NEED FOR ASSISTANCE<br />

Many possible taxonomic and systematic questions could be posed for which information is<br />

needed. For example, are Petaurillus hosei and P. kinlochi conspecific? Is the highland form<br />

of Rhinolophus trifoliatus, known from one specimen from Sabah and one from Kalimantan,<br />

a full species? What are the systematics of the Hipposideros bicolor group (including<br />

H. dyacorum, H. pomona, H. ater and H. cineraceus)? Such questions generally involve a<br />

few species, scattered across many taxonomic groups. These are not the sort of questions that<br />

occupy a taxonomist full time, but often arise as adjuncts to other related studies.<br />

Although checklists are fun to compile, and can encourage the search for rare or seldomfound<br />

species, their value is strictly limited unless they are directed towards a particular<br />

purpose. Such a purpose could include a distribution atlas, follow-up investigations of<br />

community ecology, or looking at the impacts of development activities. Further knowledge<br />

of numbers, population dynamics, sustainability, and management for conservation would<br />

all be worthy targets that can build on checklists only if they are followed by intensive research.<br />

12


G.W.H. DAVISON & ZUBAID AKBAR (2007)<br />

Aquatic mammals (cetaceans, dugong) are very poorly known, from every aspect of their<br />

biology. A small research group has been established in Universiti Malaysia Sabah.<br />

The only reasonably detailed distribution maps for mammals in Peninsular Malaysia are for<br />

primates (compiled and summarized by Marsh & Wilson 1981), and in Sabah for a selection<br />

of larger mammals (Davies & Payne 1982). A database of distribution records, which must<br />

have a high degree of taxonomic reliability, would be an important aim.<br />

There are sometimes differences in the presence/absence of species between sites, even in<br />

contiguous forests a few kilometers apart, in apparently homogenous habitat. The ecological<br />

requirements of mammals are not sufficiently known to be sure of the reasons. They need<br />

study.<br />

Rates of food intake, energetics, and even the diets of most Peninsular Malaysian mammals<br />

are very poorly known (e.g., the proportion of different prey species in the diet of predators,<br />

or of food-plants in the diet of herbivores).<br />

Various species have been labelled as pollinators, seed dispersers or seed predators, or as<br />

destroyers of seedlings, but the detailed information base for this is limited primarily to<br />

squirrels (e.g., Payne 1979), primates (e.g., Chivers 1980) and bats (e.g., Hodgkison et al.<br />

2003); hence the relevance of wildlife to land management practices such as forestry is hard<br />

to demonstrate.<br />

Breeding seasonality, reproductive rates, survival rates and lifespan are poorly studied and<br />

documented, and unknown for many species of wildlife.<br />

Not a single formalized, mathematical model for a Population and Habitat Viability Analysis<br />

exists for any Peninsular Malaysian animal (although the Peninsular Malaysian component<br />

of the populations of some species such as Asian elephant, Sumatran rhino, and tiger have<br />

been considered in less mathematically rigorous viability assessments, resulting in species<br />

action plans). One detailed study exists for one population of orangutans in Sabah (Goossens<br />

et al. 2005).<br />

Virtually no information is available on the population densities of even common species<br />

such as mousedeer and wild pigs (but see Diong 1973 and Ickes 2001).<br />

Thus, the biological basis for advising on the management of wildlife is extremely sketchy.<br />

Advice often has to rely on extrapolating from the same or similar species in other countries,<br />

common sense and guesswork.<br />

INTERNATIONAL, REGIONAL OR NATIONAL<br />

PROJECTS THAT CAN HELP<br />

Various cooperative ventures exist, in which Malaysia already participates, or could participate,<br />

to enhance knowledge of the diversity of mammals.<br />

There are examples related to particular groups of mammals, such as bats. The Malaysian<br />

13


THE STATUS OF MAMMALIAN BIODIVERSITY IN MALAYSIA<br />

Bat Research Group has been very active since the mid 1990s, with a long record of<br />

publications. Successful initiatives of this type deserve local support, in order to sustain<br />

output. They can serve as models for other research programmes, for example on rodents or<br />

on small carnivores, or on other vertebrate groups. Recent interest in bats has had spin-offs<br />

such as Bat Education workshops for children, and has spread from Malaysia to Singapore<br />

through a network of non-governmental organizations.<br />

GenBank is an international cooperative web-based catalogue of available genome sequences.<br />

Participation in this network is up to the individual scientist, and at first sight it is most<br />

useful as a source of information. It is less obvious but just as valuable as a repository to<br />

upload information. This announces what a researcher is working on, provides a fuller range<br />

of data, acts as a form of citation in a similar way to publishing, and ultimately enhances<br />

reputation.<br />

Suggestions to establish tissue banks have emerged from university research groups. If these<br />

are simply collections of tissue from road-kills, or untargeted trapping, tissue banks will be<br />

slow to develop to a point where any single collection can form a basis for research projects.<br />

The concept needs to be turned round, so that intensive research projects become a source of<br />

tissue samples, in specialized areas such as particular taxa, or to demonstrate inter- and<br />

intra-population variability.<br />

Scientists in the Philippines and Brunei Museum have research programmes on cetaceans.<br />

Information from aircraft pilots has been collated (e.g., in Brunei) to document aerial sightings<br />

that supplement data from beached animals. There is plenty of scope in the region to expand<br />

observation networks of pilots, fishing crews, divers and photographers, and their observations<br />

can provide information not only about cetaceans but also about whale-sharks, sea-snakes,<br />

sea-birds, migratory birds at oil rigs, and turtles.<br />

The IUCN Red Lists provide information about the conservation status of many species.<br />

Categorisation, species by species, is a cooperative venture that usually depends on scientists<br />

and conservationists from many countries because knowledge is dispersed, and because most<br />

species occur in more than one country. Malaysian mammalogists have a lot to contribute if<br />

the categories are to be realistic.<br />

A spin-off use of these categories is as biodiversity indicators that measure Malaysia’s progress<br />

towards the target of the Convention on Biological Diversity, to reduce the rate of biodiversity<br />

loss by 2010. Statistical methods are under development, and being applied group by group<br />

to the better-assessed taxa such as birds and amphibians. The turn of mammals will soon<br />

come, and Malaysian scientists can participate to refine both methodology and data.<br />

CAN THIS WORK BE DONE IN MALAYSIA?<br />

IF SO, WHAT IS REQUIRED?<br />

It is relatively straightforward to maintain species lists, although a level of uncertainty must<br />

always be accepted in defining species limits (Appendix). The uncertainty need not be an<br />

obstacle, even to researchers in fields other than taxonomy, even though they may express<br />

frustration at the ‘failure’ of classical taxonomy to settle names (Dayrat 2005). On the contrary,<br />

uncertainties about species boundaries are signposts to fruitful areas for research on physiology,<br />

14


G.W.H. DAVISON & ZUBAID AKBAR (2007)<br />

genetics and behaviour. ‘Official’ lists of taxa will be supported if they prove useful, which<br />

means they must be flexible, accessible, and based on a broad range of taxonomists’ views.<br />

A database of what has been done could be useful, but a database of scientists can only<br />

provide a minimum list. It cannot include every individual with an interest in mammals who<br />

is potentially a contributor to knowledge, and it is not very clear who would use a list of<br />

scientists, since each scientist should know all others within his or her research field. Possibly<br />

databases should be in the form of bibliographies and library resources, rather than lists of<br />

projects or individuals. Library resources would be useful to everyone, and bibliographies are<br />

in themselves databases about which researchers are active on what topics.<br />

Better information flow should encourage the standardisation of field methods. There was a<br />

period in the 1960s and 1970s when it appeared that small-mammal trapping techniques<br />

were becoming well standardized (groups of three traps at 30 or 50 m intervals, one on the<br />

ground, one on a log, one in a tree). In the 1970s and 1980s similar uniformity was developed<br />

for census walks for primates and squirrels. This facilitated comparison between studies, and<br />

encouraged quantification. The use of mistnets, harp traps, radio telemetry and other techniques<br />

also require standardization.<br />

The limited funding needs to be targetted – but how to target? Rather than judging taxonomic<br />

projects on their potential for commercial application, it might be possible to assign funds to<br />

improving equipment capabilities / techniques, e.g. investment in electron microscopy, facilities<br />

for DNA analysis, and cryopreservation of tissues. Such facilities could be used by many<br />

scientists, and would enable them to compete in the international science arena. Funding for<br />

postgraduate research would encourage intensive research on single topics for several years,<br />

which is the route to in-depth understanding and international publications. Investment is<br />

needed in developing career structures and training for taxonomy. Investment is also required<br />

in conservation management training, to ensure that the diversity of mammals persists.<br />

A natural history museum, like tissue banks, will probably be effective only if collections are<br />

targeted. It must not be an excuse for indiscriminate collecting, but it could be a boon when<br />

populations of plants and animals are doomed by land conversion. Sharing on-line specimen<br />

data between museums, just as botanists have BRAHMS (Botanical Research and Herbarium<br />

Management System), is sorely needed.<br />

Collecting specimens of all Malaysian mammals will not resolve all questions, because<br />

comparison is necessary, often with extra-limital material. On-site work such as that by<br />

Kingston et al. (2001) can only reveal a new species by a combination of field and lab work.<br />

Taxonomic work by Kawada et al. (2003), Meijaard & Groves (2004), Gorog et al. (2004)<br />

and Olson et al. (2004) continues to show that regional comparisons are needed. Even name<br />

changes (e.g., Tragulus javanicus back to T. kanchil; Talpa micrura to Talpa klossii to<br />

Euroscaptor micrura) are not just name changes, but result from splits within wider<br />

populations, over broad geographical areas. Malaysian taxonomists cannot afford to specialize<br />

in taxonomy within Malaysia’s borders, but need the ambition, academic friendships and<br />

access to regional research material that will enable them to place Malaysia’s mammals in a<br />

regional and international context. For example, the species status of Tupaia glis cannot be<br />

resolved without access to Thai, Burmese and Chinese T. berlangeri. The subspecies status<br />

of orang-utans in Sarawak and Sabah, and the viability of their populations, cannot be judged<br />

without reference to those in Kalimantan. The Red List status of Rhinolophus creaghi cannot<br />

be reliably decided until it is known that it also occurs in Palawan. Taxonomy needs a regional<br />

approach, sometimes even a global approach, and this means that international collaborations<br />

15


THE STATUS OF MAMMALIAN BIODIVERSITY IN MALAYSIA<br />

with colleagues and institutions elsewhere are essential. Museum collections in other countries<br />

will still be essential points of reference, even if large series of all Malaysian taxa are available<br />

within Malaysia.<br />

Malaysian mammalogists need to participate in revision of the IUCN Red Lists. The current<br />

list includes Macaca fascicularis and Coelops robinsoni as both Lower Risk/near-threatened<br />

(LR/nt). It includes Pipistrellus cuprosus and Bos gaurus as both Vulnerable. Such contrasts<br />

make it clear that defining rigid one-word categories of status are just a first step. Much more<br />

crucial is the collection of information on their population biology and their response to<br />

pressures, because the conservation methodologies to be applied will be drastically different<br />

in each case.<br />

REFERENCES<br />

ABDULLAH, M.T., JUB, N. & JALAWEH, N. 2003. First record of Hipposideros ater in<br />

Sarawak, Malaysian Borneo. Sarawak Museum Journal 79: 271–274.<br />

ANDERSON, J.A.R., CRANBROOK, EARL OF, & JERMY, C.A. 1979. Management Plan<br />

for Gunung Mulu National Park. Sarawak Forestry Department and Royal Geographical<br />

Society.<br />

AZLAN, J.M. & SHARMA, D.S.K. 2003. Camera trapping the Indochinese tiger, Panthera<br />

tigris corbetti, in a secondary forest in Peninsular Malaysia. Raffles Bulletin of Zoology<br />

51(2): 421–428.<br />

BANKS, E. 1951. Obituary: Cecil Boden Kloss. Bulletin of the Raffles Museum 23: 336–<br />

346.<br />

BARRETT, E.B.M. 1984. The ecology of some nocturnal mammals in the rain forest of<br />

Peninsular Malaysia. Ph.D. thesis, University of Cambridge.<br />

BENNETT, E.L. 1991. Diurnal primates. Pp. 150–172. In: Kiew, R. (ed.), The State of Nature<br />

Conservation in Malaysia. Malayan Nature Society, Kuala Lumpur.<br />

BRANDON-JONES, D. 1984. Colobus and leaf monkeys. Pp. 398–408. In: Macdonald, D.<br />

(ed.). The Encyclopedia of Mammals. Vol. 1. Allen & Unwin, London.<br />

CHASEN, F.N. 1940. A handlist of Malaysian mammals. Bulletin of the Raffles Museum 15:<br />

xx + 209.<br />

CHASEN, F.N. & KLOSS, C.B. 1931. On a collection of mammals from the lowlands and<br />

islands of North Borneo. Bulletin of the Raffles Museum 6: 1–82.<br />

CHIVERS, D.J. 1981. Malayan Forest Primates. Pergamon Press, Oxford.<br />

CORBET, G.B. & HILL, J.E. 1992. The mammals of the Indomalayan region: a systematic<br />

review. Oxford University Press, Oxford and London.<br />

DAVIES, A.G. & PAYNE, J.B. 1982. A Faunal Survey of Sabah. WWF Malaysia and Game<br />

Branch, Sabah Forestry Department.<br />

DAVIS, D.D. 1962. Mammals of the lowland rain-forest of North Borneo. Bulletin of National<br />

Museum, Singapore 31: 1–130.<br />

DAVISON, G.W.H. 1984. New records of Peninsular Malayan and Thai shrews. Malayan<br />

Nature Journal 36: 211–215.<br />

DAYRAT, B. 2005. Towards integrative taxonomy. Biological Journal of the Linnean Society<br />

85: 407–415.<br />

DIONG, C.H. 1973. Studies of the Malayan wild pig in Perak and Johor. Malayan Nature<br />

Journal 26: 120–151.<br />

EMMONS, L.H. 2000. Tupai: a field study of Bornean treeshrews. University of California<br />

16


G.W.H. DAVISON & ZUBAID AKBAR (2007)<br />

Press, Berkeley.<br />

ESCALENTE, A.A., CORNEJO, O.E., FREELAND, D.E., POE, A.C., CURREGO, E.,<br />

COLLINS, W.E. & LAL, A.A. 2005. A monkey’s tale: the origin of Plasmodium vivax<br />

as a human malaria parasite. Proceedings of the National Academy of Sciences, USA<br />

102: 1980–1985.<br />

EVERETT, A.H. 1893. A nominal list of the mammals inhabiting the Bornean group of<br />

islands. Proceedings of Zoological Society of London 1893: 492–496.<br />

FAIN, A., NADCHATRAM, M. & LUKOSCHUS, F.S. 1984. Fur mites of the family Myobiidae<br />

(Acari: Prostigmata) parasitic on bats in Peninsular Malaysia. Malayan Nature Journal<br />

37: 175–183.<br />

FERNANDO, P., VIDYA T.N.C., PAYNE J., STUEWE M., DAVISON G., ALFRED R.J.,<br />

ANDAU P., BOSI E., KILBOURN A. & MELNICK D.J.. 2003. DNA analysis indicates<br />

that Asian elephants are native to Borneo and are therefore a high priority for conservation.<br />

PLOS Biology 1: 110–115.<br />

FRANCIS, C.M. 1995. First records for Peninsular Malaysia of two species of spectacular<br />

orange bats from Temengor, Hulu Perak, Malaysia. Malayan Nature Journal 48: 397–<br />

401.<br />

FRANCIS, C.M. 2001. A Photographic Guide to the Mammals of South-East Asia. New<br />

Holland, London.<br />

GOOSSENS, B., CHIKHI, L., JALIL, M.F., ANCRENAZ, M., LACKMAN-ANCRENAZ,<br />

I., MOHAMED, M., ANDAU, P. & BRUFORD, M.W. 2005. Patterns of genetic diversity<br />

and migration in increasingly fragmented and declining orang-utan (Pongo pygmaeus)<br />

populations from Sabah, Malaysia. Molecular Ecology, 14(2): 441–456.<br />

GOROG, A.J., SINAGA, M.H. & ENGSTROM, M.D. 2004. Vicariance or dispersal?<br />

Historical biogeography of three Sunda shelf murine rodents (Maxomys surifer,<br />

Leopoldamys sabanus and Maxomys whiteheadi). Biological Journal of Linnean Society<br />

81: 91–109.<br />

HAN, K.H., SHELDON, F. & STUEBING, R. 2000. Interspecific relationships and<br />

biogeography of some Bornean tree shrews (Tupaiidae: Tupaia), based on DNA<br />

hybridization and morphometric comparisons. Biological Journal of Linnean Society<br />

70: 1–14.<br />

HARRISON, J.L. 1962. The distribution of feeding habits among animals in a tropical rain<br />

forest. Journal of Animal Ecology 31: 53–63.<br />

HARRISON, J.L. 1964. Introduction to the Mammals of Sabah. Sabah Society, Kota Kinabalu.<br />

HEYDON, M. & BULLOH, P. 1996. The impact of selective logging on sympatric civet<br />

species in Borneo. Oryx 30: 31–36.<br />

HILL, J.E. 1960. The Robinson collection of Malaysian mammals. Bulletin of Raffles Museum<br />

29: 1–112.<br />

HILL, J.E. 1963. A revision of the genus Hipposideros. Bulletin of the British Museum<br />

(Natural History) Zoology 11: 1–129.<br />

HILL, J.E. & FRANCIS, C.M. 1984. New bats (Mammalia: Chiroptera) recorded from Borneo<br />

and Malaya. Bulletin of the British Museum (Natural History) Zoology 47: 305–329.<br />

HODGKISON, R., BALDING, S., AKBAR, Z. & KUNZ, T.H. 2003. Fruit bats (Chiroptera:<br />

Pteropodidae) as seed dispersers and pollinators in a lowland Malaysian rain forest.<br />

Biotropica 35(4): 491–502.<br />

ICKES, K. 2001. Hyper-abundance of native wild pigs (Sus scrofa) in a lowland Dipterocarp<br />

rain forest of Peninsular Malaysia. Biotropica 33: 682–690.<br />

IUCN. 2004. The IUCN Red List of Threatened Species. IUCN World Conservation Union,<br />

17


THE STATUS OF MAMMALIAN BIODIVERSITY IN MALAYSIA<br />

Gland, Switzerland.<br />

JENKINS, P.D. 1982. A discussion of Malayan and Indonesian shrews of the genus Crocidura<br />

(Insectivora: Soricidae). Zoologische Mededelingen 56: 267–279.<br />

JENKINS, P.D. & HILL, J.E. 1981. The status of Hipposideros galeritus Cantor, 1846 and<br />

Hipposideros cervinus (Gould, 1854) (Chiroptera: Hipposideridae). Bulletin of the British<br />

Museum (Natural History) Zoology 41: 279–294.<br />

JEPHTE, S. 1996. Calling adaptations by primates, hornbills and argus pheasants to hunting<br />

in Sabah and Sarawak. M.Sc. thesis, Universiti Kebangsaan Malaysia, Bangi.<br />

JOHNS, A.D. 1986. Effects of selective logging on the behavioural ecology of West Malaysian<br />

primates. Ecology 67: 684–694.<br />

JOHNS, A.D. 1992. Vertebrate responses to selective logging: implications for the design of<br />

logging systems. Philosophical Transactions of Royal Society, London 335: 437–442.<br />

KAWADA, S., SHINOHARA, A., YASUDA, M., ODA, S. & LIM, B.L. 2003. The mole of<br />

Peninsular Malaysia: notes on its identification and ecology. Mammal Study 28: 73–77.<br />

KAWANISHI, K. 2002. Population status of tigers (Panthera tigris) in a primary rainforest<br />

of Peninsular Malaysia. Ph.D. thesis, University of Florida, Gainesville.<br />

KIEW, B.H. (ed.). 1977. A survey of the proposed Sungei Danum National Park, Sabah.<br />

WWF Malaysia, Kuala Lumpur.<br />

KINGSTON, T., FRANCIS, C.M., AKBAR, Z. & KUNZ, T.H. 2003. Species richness in an<br />

insectivorous bat assemblage from Malaysia. Journal of Tropical Ecology 19: 67–79.<br />

KINGSTON, T., LARA, M.C., JONES, G., AKBAR, Z., KUNZ, T.H. & SCHNEIDER, C.J.<br />

2001. Acoustic divergence in two cryptic Hipposideros species: a role for social selection?<br />

Proceedings of Royal Society, London, Biological Sciences 268 (1474): 1381–1386.<br />

LIM, B.L. 1973. Preliminary survey of some Malaysian wild mammals as potential laboratory<br />

experimental animals. Jikken Dobutsu 22 (Supplement): 195–199.<br />

LIM, B.L., MUUL, I. & CHAI, K.S. 1977. Zoonotic studies of small animals in the canopy<br />

transect at Bukit Lanjan Forest Reserve, Selangor, Malaysia. Malayan Nature Journal<br />

31: 127–140.<br />

MARSH, C.W. & WILSON, W.L. 1981. Survey of Primates in Peninsular Malaysian Forests.<br />

University of Cambridge and Universiti Malaysia Kebangsaan.<br />

MEDWAY, LORD. 1965. Mammals of Borneo; field keys and an annotated checklist. Journal<br />

of Malayan Branch, Royal Asiatic Society 36(3): xiv + 193.<br />

MEDWAY, LORD. 1969. The wild mammals of Malaya and Singapore. Oxford University<br />

Press, Kuala Lumpur.<br />

MEDWAY, LORD. 1971. Observations on the social and reproductive biology of the bentwinged<br />

bat Miniopterus australis in northern Borneo. Journal of Zoology, London 165:<br />

261–273.<br />

MEDWAY, LORD. 1972. The Gunong Benom Expedition 1967. 6. The distribution and<br />

altitudinal zonation of birds and mammals on Gunong Benom. Bulletin of the British<br />

Museum (Natural History) Zoology 23: 103–154.<br />

MEDWAY, LORD. 1977. Mammals of Borneo, 2 nd edition. Monographs of the Malaysian<br />

Branch, Royal Asiatic Society, No. 7. Kuala Lumpur.<br />

MEDWAY, LORD. 1978. The wild mammals of Malaya (Peninsular Malaysia) and Singapore.<br />

2 nd edition. Oxford University Press, Kuala Lumpur.<br />

MEDWAY, LORD. 1983. The wild mammals of Malaya (Peninsular Malaysia) and Singapore.<br />

2 nd edition, with corrections. Oxford University Press, Kuala Lumpur.<br />

MEDWAY, LORD & YONG, H.S. 1976. Problems in the systematics of the rats (Muridae) of<br />

Peninsular Malaysia. Malaysian Journal of Science 4: 43–53.<br />

18


G.W.H. DAVISON & ZUBAID AKBAR (2007)<br />

MEIJAARD, E. 2003. Mammals of south-east Asian islands and their Late Pleistocene<br />

environments. Journal of Biogeography 30: 1245–1257.<br />

MEIJAARD, E. & GROVES, C.P. 2004. A taxonomic revision of the Tragulus mouse-deer<br />

(Artiodactyla). Zoological Journal of Linnean Society 140: 63–102.<br />

MIURA, S., YASUDA, M. & RATNAM, L. 1997. Who steals the fruits? Monitoring frugivory<br />

of mammals in a tropical rain forest. Malayan Nature Journal 50: 183–191.<br />

MULLIN, S.W., COLLEY, F.C. & STEVENS, G.S. 1972. Coccidia of Malaysian mammals:<br />

new host records and descriptions of three new species of Eimeria. Journal of Protozoology<br />

19: 260–263.<br />

MUUL, I. & LIM, B.L. 1978. Comparative morphology, food habits and ecology of some<br />

Malaysian arboreal rodents. Pp. 361–368. In: Montgomery, G.G. (ed.), The Ecology of<br />

Arboreal Folivores. Smithsonian Institution Press, Washington, D.C.<br />

NUMATA, S., OKUDA, T., SUGIMOTO, T., NISHIMURA, S., YOSHIDA, K., QUAH,<br />

E.S., YASUDA, M., MUANGKHUM, K. & NUR SUPARDI, M.N. 2005. Camera<br />

trapping: a non-invasive approach as an additional tool in the study of mammals in<br />

Pasoh Forest Reserve and adjacent fragmented areas in Peninsular Malaysia. Malayan<br />

Nature Journal 57: 29–45.<br />

OLSON, L.E., SARGIS, E.J. & MARTIN, R.D. 2004. Phylogenetic relationships among<br />

treeshrews (Scandentia): a review and critique of the morphological evidence. Journal<br />

of Mammalian Evolution 11: 49–71.<br />

PAYNE, J. 1979. Synecology of Malayan tree squirrels, with special reference to the genus<br />

Ratufa. Ph.D. thesis, University of Cambridge.<br />

PAYNE, J. & ANDAU, M. 1991. Large mammals in Sabah. Pp. 177–183. In: Kiew, R. (ed.),<br />

The State of Nature Conservation in Malaysia. Malayan Nature Society, Kuala Lumpur.<br />

PAYNE, J., FRANCIS, C.M. & PHILLIPPS, K. 1985. Field Guide to the Mammals of Borneo.<br />

Sabah Society, Kota Kinabalu and WWF Malaysia, Kuala Lumpur.<br />

PEVET, P. & YADAV, M. 1980. The pineal gland of equatorial mammals. I. The pinealocytes<br />

of the Malaysian rat (Rattus sabanus). Cell Tissue Research 210: 417–433.<br />

RAJARATNAM, R. 2001. The ecology of small carnivores in Tabin Wildlife Reserve, Sabah,<br />

Malaysia. Ph.D. thesis, University of Armidale, New England, Australia.<br />

RATNAM, L., NOR AZMAN HUSSEIN & LIM, B.L. 1991. Small mammals in Peninsular<br />

Malaysia. Pp. 143–149. In: Kiew, R. (ed.), The State of Nature Conservation in Malaysia.<br />

Malayan Nature Society, Kuala Lumpur.<br />

RAVEN, H.C. 1935. Wallace’s line and the distribution of Indo-Australian mammals. Bulletin<br />

of the American Museum of Natural History 68: 179–293.<br />

ROSS, M.D. 2004. The Long Calls of wild male Orangutans: a phylogenetic approach.<br />

Diploma Thesis, University of Hanover, Germany.<br />

RUDD, R.L. 1965. Weight and growth in Malaysian rain forest mammals. Journal of<br />

Mammalogy 46: 588–594.<br />

RUEDI, M. 1995. Taxonomic revision of shrews in the genus Crocidura from the Sunda<br />

Shelf and Sulawesi, with description of two new species (Mammalia: Soricidae).<br />

Zoological Journal of Linnean Society 115: 211–265.<br />

RUEDI, M. 1996. Phylogenetic evolution and biogeography of Southeast Asian shrews (genus<br />

Crocidura: Soricidae). Biological Journal of Linnean Society 58: 197–219.<br />

SHUKOR MD. NOR. 1996. The mammalian fauna on the islands at the tip of Sabah, Borneo.<br />

Fieldana, Zoology, new series, 83: 1–51.<br />

SOEPADMO, E. (ed.). 1984. An ecological survey of Lambir Hills National Park, Sarawak.<br />

WWF Project No. 44/81. WWF Malaysia, Kuala Lumpur.<br />

TWEEDIE, M.W.F. 1948. Obituary: Frederick Nutter Chasen. Bulletin of the Raffles Museum<br />

19


THE STATUS OF MAMMALIAN BIODIVERSITY IN MALAYSIA<br />

18: 170–176.<br />

WELLS, D.R. 1989. Notes on the distribution and taxonomy of Peninsular Malaysian<br />

mongooses (Herpestes). Natural History Bulletin of the Siam Society 37: 87–97.<br />

WELLS, K., PFEIFFER, M., MAKLARIN, L. & LINSENMAIR, K.E. 2004. Use of arboreal<br />

and terrestrial space by a small mammal community in a tropical rain forest in Borneo,<br />

Malaysia. Journal of Biogeography 31: 641–652.<br />

WHITTOW, G.C. & GOULD, E. 1976. Body temperature and oxygen consumption of the<br />

pentail tree shrew (Ptilocercus lowii). Journal of Mammalogy 57: 754–756.<br />

WHITTOW, G.C., SCAMMELL, C., LEONG, M. & R &, D. 1977a. Temperature regulation<br />

in the smallest ungulate, the Lesser Mousedeer (Tragulus javanicus). Comparative<br />

Biochemistry & Physiology A, 56 (1A): 23–26.<br />

WHITTOW, G.C., SCAMMELL, C., MANUEL, J.K., R &, D. & LEONG, M. 1977b.<br />

Temperature regulation in a hypometabolic primate, the slow loris (Nycticebus coucang).<br />

Archives Internationale du Physiologie et Biochimie 85: 139–151.<br />

WYATT-SMITH, J. & WYCHERLEY, P.R. (eds.). 1961. Nature Conservation in Western<br />

Malaysia, 1961. Malayan Nature Journal, 21 st Anniversary Special Issue. Kuala Lumpur.<br />

YONG, H.S. 1970. A Malayan view of Rattus edwardsi and R. sabanus. Zoological Journal<br />

of the Linnean Society 40: 359–370.<br />

YONG, H.S. 1975. Karyotypes of four species of Callosciurus from Peninsular Malaysia.<br />

Malaysian Journal of Science 3: 1–5.<br />

YONG, H.S. 1982. Karyotypes of Hapalomys and Pithecheir from Peninsular Malaya.<br />

Cytologia 47: 535–538.<br />

YONG, H.S. & DHALIWAL, S.S. 1972. Supernumerary (B-) chromosomes in the Malayan<br />

house rat, Rattus rattus diardi. Chromosoma 36: 256–262.<br />

ZAABA, Z.A., MOHD TAJUDDIN, A., MUSTAFA, A.R. & EBIL, Y. 1991. Large mammals<br />

in Peninsular Malaysia. Pp. 173–176. In: Kiew, R. (ed.), The State of Nature Conservation<br />

in Malaysia. Malayan Nature Society, Kuala Lumpur.<br />

ZUBAID, A. 1994. Bornean Horseshe Bat Rhinolophus borneensis newly recorded in<br />

Peninsular Malaysia. Malayan Nature Journal 48: 37–38.<br />

20


G.W.H. DAVISON & ZUBAID AKBAR (2007)<br />

ZUNIKA, A., IBRAHIM, S.F., CUSHION, M.T. & SASTERHENN, T.M. 2002. Detection of<br />

Pneumocystis carinii in lungs of wild mammals from Crocker Range Park by PCR<br />

amplification. ASEAN Review of Biodiversity and Environmental Conservation online<br />

http://www.arbec.com.my/<strong>pdf</strong>/art20julysep02.<strong>pdf</strong><br />

APPENDIX<br />

Checklist of Mammals from Malaysia<br />

Moonrat Echinosorex gymnurus PM Srk Sab<br />

Lesser Gymnure Hylomys suillus PM Srk Sab<br />

Short-tailed Mole Euroscaptor micrura PM<br />

House Shrew Suncus murinus PM Srk Sab<br />

Black Shrew Suncus ater Sab<br />

Malayan Pygmy Shrew Suncus (etruscus) malayanus PM Srk Sab<br />

Crocidura malayana<br />

PM<br />

SEA White-toothed Shrew Crocidura fuliginosa PM Srk Sab<br />

Kinabalu White-toothed Shrew Crocidura baluensis Sab<br />

Crocidura negligens<br />

PM<br />

Crocidura attenuata<br />

PM<br />

Sunda Shrew Crocidura monticola PM Srk Sab<br />

Sunda Water Shrew Chimarrogale phaeura PM Srk Sab<br />

Flying Lemur Cynocephalus variegatus PM Srk Sab<br />

Geoffroy’s Rousette Rousettus amplexicaudatus PM Srk Sab<br />

Rousettus leschenaultii<br />

PM<br />

Bare-backed Rousette Rousettus spinalatus Srk Sab<br />

Malayan Flying Fox Pteropus vampyrus PM Srk Sab<br />

Island Flying Fox Pteropus hypomelanus PM Sab<br />

Malaysian Fruit Bat Cynopterus ‘brachyotis’ open-country taxon PM Srk Sab<br />

Cynopterus ‘brachyotis’ forest taxon PM Srk Sab<br />

Horsfield’s Fruit Bat Cynopterus horsfieldi PM Srk Sab<br />

Short-nosed Fruit Bat Cynopterus sphinx PM<br />

Dusky Fruit Bat Penthetor lucasi PM Srk Sab<br />

Dayak Fruit Bat Dyacopterus spadiceus PM Srk Sab<br />

Spotted-winged Fruit Bat Balionycteris maculata PM Srk Sab<br />

Black-capped Fruit Bat Chironax melanocephalus PM Sab<br />

Grey Fruit Bat Aethalops alecto PM<br />

Aethalops aequalis Srk Sab<br />

Tailless Fruit Bat Megaerops ecaudatus PM Srk Sab<br />

Wetmore’s Fruit Bat Megaerops wetmorei PM ?<br />

Cave Fruit Bat Eonycteris spelaea PM Srk Sab<br />

Greater Nectar Bat Eonycteris major Srk Sab<br />

Common Long-tongued Fruit Bat Macroglossus minimus PM Srk Sab<br />

Hill Long-tongued Fruit Bat Macroglossus sobrinus PM<br />

Greater Sheath-tailed Bat Emballonura alecto Srk Sab<br />

Lesser Sheath-tailed Bat Emballonura monticola PM Srk Sab<br />

Black-bearded Tomb Bat Taphozous melanopogon PM Srk Sab<br />

21


THE STATUS OF MAMMALIAN BIODIVERSITY IN MALAYSIA<br />

Long-winged Tomb Bat Taphozous longimanus PM Srk Sab<br />

Pouch-bearing Bat Taphozous (Saccolaimus) saccolaimus PM Srk Sab<br />

Hollow-faced Bat Nycteris javanica PM Srk Sab<br />

Malayan False Vampire Megaderma spasma PM Srk Sab<br />

Indian False Vampire Megaderma lyra PM<br />

Intermediate Horseshoe Bat Rhinolophus affinis PM Srk<br />

Lesser Brown Horseshoe Bat Rhinolophus stheno PM<br />

Peninsular Horseshoe Bat Rhinolophus robinsoni PM<br />

Glossy Horseshoe Bat Rhinolophus refulgens PM<br />

Least Horseshoe Bat Rhinolophus pusillus PM<br />

N. Malayan Horseshoe Bat Rhinolophus malayanus PM<br />

Acuminate Horseshoe Bat Rhinolophus acuminatus PM Sab<br />

Big-eared Horseshoe Bat Rhinolophus macrotis PM<br />

Lesser Woolly Horseshoe Bat Rhinolophus sedulus PM Srk Sab<br />

Trefoil Horseshoe Bat Rhinolophus trifoliatus PM Srk Sab<br />

Hill Trefoil Horseshoe Bat Rhinolophus sp. (undescribed) Sab<br />

Woolly Horseshoe Bat Rhinolophus luctus PM Srk Sab<br />

Croslet Horseshoe Bat Rhinolophus coelophyllus PM<br />

Marshall’s Horseshoe Bat Rhinolophus marshalli PM<br />

Pearson’s Horseshoe Bat Rhinolophus pearsonii PM<br />

Shamel’s Horseshoe Bat Rhinolophus shameli PM<br />

Rhinolophus convexus<br />

PM<br />

Chiew Kwee’s Horseshoe Bat Rhinolophus chiewkweeae PM<br />

Bornean Horseshoe Bat Rhinolophus borneensis PM Srk Sab<br />

Arcuate Horseshoe Bat Rhinolophus arcuatus Srk<br />

Creagh’s Horseshoe Bat Rhinolophus creaghi Srk Sab<br />

Philippine Horseshoe Bat Rhinolophus philippinensis Srk Sab<br />

Bicolour Roundleaf Horseshoe Bat Hipposideros ‘bicolor’ 131kHz taxon PM Srk Sab<br />

Bicolour Roundleaf Horseshoe Bat Hipposideros ‘bicolor’ 142 kHz taxon PM Srk? Sab?<br />

Hipposideros pomona<br />

PM<br />

Malayan Roundleaf Horseshoe Bat Hipposideros nequam<br />

PM<br />

Dusky Roundleaf Horseshoe Bat Hipposideros ater PM Sab<br />

Dayak Roundleaf Horseshoe Bat Hipposideros dyacorum PM Srk Sab<br />

Lawas Roundleaf Horseshoe Bat Hipposideros sabanus PM Srk Sab<br />

Least Roundleaf Horseshoe Bat Hipposideros cineraceus PM Sab<br />

Singapore Roundleaf Hipposideros ridleyi PM Sab<br />

Horseshoe Bat<br />

Hipposideros orbicularis<br />

PM<br />

Common Roundleaf Hipposideros cervinus PM Srk Sab<br />

Horseshoe Bat<br />

Cantor’s Roundleaf Hipposideros galeritus PM Srk Sab<br />

Horseshoe Bat<br />

Cox’s Roundleaf Horseshoe Bat Hipposideros coxi Srk<br />

Shield-faced Bat Hipposideros lylei PM<br />

Lekagul’s Roundleaf Hipposideros lekaguli PM<br />

Horseshoe Bat<br />

Great Roundleaf Horseshoe Bat Hipposideros armiger PM<br />

Large Roundleaf Horseshoe Bat Hipposideros larvatus PM Srk<br />

Pratt’s Roundleaf Horseshoe Bat Hipposideros pratti PM<br />

Diadem Roundleaf Horseshoe Bat Hipposideros diadema PM Srk Sab<br />

Trident Horseshoe Bat Aselliscus stoliczkanus PM<br />

22


G.W.H. DAVISON & ZUBAID AKBAR (2007)<br />

Malayan Tailless Horseshoe Bat Coelops robinsoni PM Srk<br />

East Asian Tailless Horseshoe Bat Coelops frithii<br />

PM<br />

Whiskered Bat Myotis (mystacinus) muricola PM Srk Sab<br />

Burmese Whiskered Bat Myotis montivagus PM Sab<br />

Gomantong Whiskered Bat Myotis gomantongensis Sab<br />

Himalayan Whiskered Bat Myotis siligorensis Sab<br />

Horsfield’s Bat Myotis horsfieldii PM Srk Sab<br />

Lesser Large-footed Bat Myotis hasseltii PM Srk Sab?<br />

Myotis (formosus) hermani<br />

PM<br />

Myotis (ater) rozendaali PM Srk Sab<br />

Grey Large-footed Bat Myotis adversus PM Sab<br />

Pallid Large-footed Bat Myotis macrotarsus Srk Sab<br />

Ridley’s Bat Myotis ridleyi PM<br />

House Bat Scotophilus kuhlii PM Sab<br />

New Guinea Brown Bat Philetor brachypterus PM Srk Sab<br />

Lesser Flat-headed Bat Tylonycteris pachypus PM Srk Sab<br />

Greater Flat-headed Bat Tylonycteris robustula PM Srk Sab<br />

Large False Serotine Hesperoptenus tomesi PM Sab<br />

Blanford’s False Serotine Hesperoptenus blanfordi PM Sab<br />

Doria’s False Serotine Hesperoptenus doriae PM Srk<br />

Noctule Nyctalus noctula PM<br />

Malaysian Noctule Pipistrellus stenopterus PM Srk Sab<br />

Woolly Pipistrelle Pipistrellus petersi Sab<br />

Brown Pipistrelle Pipistrellus (Hypsugo) macrotis PM<br />

Brown Pipistrelle Pipistrellus (Hypsugo) imbricatus Srk<br />

White-winged Pipistrelle Pipistrellus (Hypsugo) vordermanni Srk<br />

May be conspecific with P. (H.) imbricatus<br />

Red-brown Pipistrelle Pipistrellus (Hypsugo) kitcheneri Sab<br />

Coppery Pipistrelle Pipistrellus (Arielulus) cuprosus Sab<br />

Gilded Black Pipistrelle Pipistrellus (Arielulus) circumdatus PM<br />

Benom Pipistrelle Pipistrellus (Arielulus) societatis PM<br />

Javan Pipistrelle Pipistrellus javanicus PM Sab<br />

Least Pipistrelle Pipistrellus tenuis PM Sab<br />

Dark Brown Pipistrelle Pipistrellus ceylonicus Sab<br />

Thick-thumbed Pipistrelle Glischropus tylopus PM Srk Sab<br />

Large Bent-winged Bat Miniopterus magnater Srk? Sab<br />

SEAsian Bent-winged Bat Miniopterus medius PM Sab<br />

Schreibers’s Bat Miniopterus schreibersii PM Srk? Sab<br />

Lesser Bent-winged Bat Miniopterus australis Srk Sab<br />

Brown Tube-nosed Bat Murina suilla PM Srk Sab<br />

Round-eared Tube-nosed Bat Murina cyclotis PM Srk Sab<br />

Hutton’s Tube-nosed Bat Murina huttoni PM<br />

Bronzed Tube-nosed Bat Murina aenea PM Sab<br />

Gilded Tube-nosed Bat Murina rozendaali Sab<br />

Hairy-winged Bat Harpiocephalus harpia Sab<br />

Harpiocephalus mordax PM Sab?<br />

Papillose Bat Kerivoula papillosa PM Srk Sab<br />

Hardwicke’s Forest Bat Kerivoula hardwickii PM Srk Sab<br />

Flores Woolly Bat Kerivoula flora Sab<br />

Clear-winged Bat Kerivoula pellucida PM Srk Sab<br />

Small Woolly Bat Kerivoula intermedia PM? Sab<br />

Least Forest Bat Kerivoula minuta PM Sab<br />

Painted Bat Kerivoula picta PM<br />

23


THE STATUS OF MAMMALIAN BIODIVERSITY IN MALAYSIA<br />

Whitehead’s Woolly Bat Kerivoula whiteheadi Srk Sab<br />

Kerivoula sp. nov.<br />

PM<br />

Groove-toothed Bat Phoniscus atrox PM Sab<br />

Frosted Groove-toothed Bat Phoniscus jagori PM<br />

Free-tailed Bat Mops mops PM Srk<br />

Wrinkled-lipped Bat Chaerephon plicata PM Srk Sab<br />

Dato Meldrum’s Bat Chaerephon johorensis PM<br />

Hairless Bat Cheiromeles torquatus PM Srk Sab<br />

Common Treeshrew Tupaia glis PM Srk<br />

Tupaia ‘longipes’ Srk Sab<br />

Mountain Treeshrew Tupaia montana Srk Sab<br />

Lesser Treeshrew Tupaia minor PM Srk Sab<br />

Slender Treeshrew Tupaia gracilis Srk Sab<br />

Painted Treeshrew Tupaia picta Srk<br />

Striped Treeshrew Tupaia dorsalis Srk Sab<br />

Large Treeshrew Tupaia tana Srk Sab<br />

Pentailed Treeshrew Ptilocercus lowii PM Srk Sab<br />

Smooth-tailed Treeshrew Dendrogale melanura Srk Sab<br />

Slow Loris Nycticebus coucang PM Srk Sab<br />

Western Tarsier Tarsius bancanus Srk Sab<br />

Silvered Leaf Monkey Presbytis cristata PM Srk Sab<br />

Dusky Leaf Monkey Presbytis obscura PM<br />

Banded Leaf Monkey Presbytis melalophos PM Srk<br />

Grey Leaf Monkey Presbytis hosei Srk Sab<br />

Maroon Leaf Monkey Presbytis rubicunda Srk Sab<br />

White-fronted Leaf Monkey Presbytis frontata Srk<br />

Proboscis Monkey Nasalis larvatus Srk Sab<br />

Long-tailed Macaque Macaca fascicularis PM Srk Sab<br />

Pig-tailed Macaque Macaca nemestrina PM Srk Sab<br />

Stump-tailed Macaque Macaca arctoides PM<br />

White-handed Gibbon Hylobates lar PM<br />

Agile Gibbon Hylobates agilis PM<br />

Bornean Gibbon Hylobates muelleri Srk Sab<br />

Siamang Hylobates syndactylus PM<br />

Bornean Orang-utan Pongo pygmaeus Srk Sab<br />

Malayan Pangolin Manis javanica PM Srk Sab<br />

Black Giant Squirrel Ratufa bicolor PM<br />

Cream-coloured Giant Squirrel Ratufa affinis PM Srk Sab<br />

Plantain Squirrel Callosciurus notatus PM Srk Sab<br />

Belly-banded Squirrel Callosciurus flavimanus PM<br />

Prevost’s Squirrel Callosciurus prevostii PM Srk Sab<br />

(Variable Squirrel) Callosciurus finlaysoni Feral<br />

Black-banded Squirrel Callosciurus nigrovittatus PM<br />

Kinabalu Squirrel Callosciurus baluensis Srk Sab<br />

Ear-spot Squirrel Callosciurus adamsi Srk Sab<br />

24


G.W.H. DAVISON & ZUBAID AKBAR (2007)<br />

Bornean Black-banded Squirrel Callosciurus orestes Srk Sab<br />

Red-bellied Sculptor Squirrel Callosciurus (Glyphotes) simus Srk Sab<br />

Horse-tailed Squirrel Sundasciurus hippurus PM Srk Sab<br />

Slender Squirrel Sundasciurus tenuis PM Srk Sab<br />

Low’s Squirrel Sundasciurus lowii PM Srk Sab<br />

Jentink’s Squirrel Sundasciurus jentinki Srk Sab<br />

Brooke’s Squirrel Sundasciurus brookei Srk Sab<br />

Himalayan Striped Squirrel Tamiops macclellandii PM<br />

Three-striped Ground Squirrel Lariscus insignis PM Srk<br />

Four-striped Ground Squirrel Lariscus hosei Srk Sab<br />

Shrew-faced Ground Squirrel Rhinosciurus laticaudatus PM Srk Sab<br />

Bornean Mountain Dremomys everetti Srk Sab<br />

Ground Squirrel<br />

Red-cheeked Ground Squirrel Dremomys rufigenis PM<br />

Black-eared Pygmy Squirrel Nannosciurus melanotis Srk<br />

Plain Pygmy Squirrel Exilisciurus exilis Srk Sab<br />

Whitehead’s Pygmy Squirrel Exilisciurus whiteheadi Srk Sab<br />

Tufted Ground Squirrel Rheithrosciurus macrotis Srk Sab<br />

Selangor Pygmy Flying Squirrel Petaurillus kinlochii PM<br />

Hose’s Pygmy Flying Squirrel Petaurillus hosei Srk Sab<br />

Lesser Pygmy Flying Squirrel Petaurillus emiliae Srk<br />

Red-cheeked Flying Squirrel Hylopetes spadiceus PM Srk Sab<br />

Grey-cheeked Flying Squirrel Hylopetes lepidus PM Srk Sab<br />

Whiskered Flying Squirrel Petinomys genibarbis PM Srk Sab<br />

White-bellied Flying Squirrel Petinomys setosus PM Srk Sab<br />

Vordermann’s Flying Squirrel Petinomys vordermanni PM Srk?<br />

Horsfield’s Flying Squirrel Iomys horsfieldii PM Srk Sab<br />

Smoky Flying Squirrel Pteromyscus pulverulentus PM Srk Sab<br />

Large Black Flying Squirrel Aeromys tephromelas PM Srk Sab<br />

Thomas’s Flying Squirrel Aeromys thomasi Srk Sab<br />

Red Giant Flying Squirrel Petaurista petaurista PM Srk Sab<br />

Spotted Giant Flying Squirrel Petaurista elegans PM Srk Sab<br />

Large Bamboo Rat Rhizomys sumatrensis PM<br />

Hoary Bamboo Rat Rhizomys pruinosus PM<br />

Pencil-tailed Tree-mouse Chiropodomys gliroides PM Srk Sab<br />

Large Pencil-tailed Tree-mouse Chiropodomys major Srk Sab<br />

Grey-bellied Pencil-tailed Chiropodomys muroides Sab<br />

Tree-mouse<br />

Marmoset Rat<br />

Hapalomys longicaudatus<br />

Monkey-footed Rat Pithecheir melanurus PM<br />

Pithecheirops otion<br />

Sab<br />

Ranee Mouse Haeromys margarettae Srk Sab<br />

Lesser Ranee Mouse Haeromys pusillus Srk Sab<br />

Asian House Mouse Mus castaneus PM Srk Sab<br />

Ricefield Mouse Mus caroli PM Sab?<br />

House Rat Rattus rattus PM Srk Sab<br />

Malaysian Wood Rat Rattus tiomanicus PM Srk Sab<br />

Ricefield Rat Rattus argentiventer PM Srk Sab<br />

Summit Rat Rattus baluensis Sab<br />

Polynesian Rat Rattus exulans PM Srk Sab<br />

Annandale’s Rat Rattus annandalei PM<br />

Brown Rat Rattus norvegicus PM Srk Sab<br />

25


THE STATUS OF MAMMALIAN BIODIVERSITY IN MALAYSIA<br />

Muller’s Rat Sundamys muelleri PM Srk Sab<br />

Mountain Giant Rat Sundamys infraluteus Srk Sab<br />

Bowers’s Rat Sundamys bowersii PM<br />

Dark-tailed Tree Rat Niviventer cremoriventer PM Srk Sab<br />

Long-tailed Mountain Rat Niviventer rapit PM Srk Sab<br />

White-bellied Rat Niviventer bukit PM<br />

Red Spiny Rat Maxomys surifer PM Srk Sab<br />

Brown Spiny Rat Maxomys rajah PM Srk Sab<br />

Mountain Spiny Rat Maxomys alticola Sab<br />

Malayan Mountain Spiny Rat Maxomys inas PM<br />

Chestnut-bellied Spiny Rat Maxomys ochraceiventer Srk Sab<br />

Small Spiny Rat Maxomys baeodon Srk Sab<br />

Whitehead’s Rat Maxomys whiteheadi PM Srk Sab<br />

Grey Tree Rat Lenothrix malaisia PM Srk Sab<br />

Long-tailed Giant Rat Leopoldamys sabanus PM Srk Sab<br />

Edwards’ Rat Leopoldamys edwardsi PM<br />

Large Bandicoot Rat Bandicota indica PM<br />

Lesser Bandicoot Rat Bandicota bengalensis PM<br />

Malayan Porcupine Hystrix brachyura PM Srk Sab<br />

Thick-spined Porcupine Hystrix crassispinis Srk Sab<br />

Brush-tailed Porcupine Thecurus macrourus PM<br />

Long-tailed Porcupine Trichys fasciculata PM Srk Sab<br />

Wild Dog Cuon alpinus PM<br />

Malayan Sun Bear Helarctos malayanus PM Srk Sab<br />

Yellow-throated Marten Martes flavigula PM Srk Sab<br />

Malay Weasel Mustela nudipes PM Srk Sab<br />

Ferret-badger Melogale everetti Sab<br />

Teledu Mydaus javanensis Srk Sab<br />

Small-clawed Otter Aonyx cinerea PM Srk Sab<br />

Hairy-nosed Otter Lutra sumatrana PM Srk Sab<br />

Common Otter Lutra lutra PM<br />

Smooth-coated Otter Lutra perspicillata PM Srk Sab<br />

Malay Civet Viverra tangalunga PM Srk Sab<br />

Large Indian Civet Viverra zibetha PM<br />

Large Spotted Civet Viverra megaspila PM<br />

Little Civet Viverricula malaccensis PM<br />

Banded Linsang Prionodon linsang PM Srk Sab<br />

Common Palm Civet Paradoxurus hermaphroditus PM Srk Sab<br />

Masked Palm Civet Paguma larvata PM Srk Sab<br />

Binturong Arctitis binturong PM Srk Sab<br />

Small-toothed Palm Civet Arctogalidia trivirgata PM Srk Sab<br />

Banded Palm Civet Hemigalus derbyanus PM Srk Sab<br />

Hose’s Palm Civet Diplogale hosei Srk Sab<br />

Otter Civet Cynogale bennettii PM Srk Sab<br />

Short-tailed Mongoose Herpestes brachyurus PM Srk Sab<br />

Indian Grey Mongoose Herpestes edwardsii PM (feral, extinct)<br />

Hose’s Mongoose Herpestes hosei Srk<br />

Javan Mongoose Herpestes javanicus PM<br />

26


G.W.H. DAVISON & ZUBAID AKBAR (2007)<br />

Collared Mongoose Herpestes semitorquatus Srk Sab<br />

Crab-eating Mongoose Herpestes urva PM<br />

Tiger Panthera tigris PM<br />

Leopard Panthera pardus PM<br />

Clouded Leopard Neofelis nebulosa PM Srk Sab<br />

Golden Cat Catopuma temminckii PM<br />

Bay Cat Catopuma badia Srk Sab<br />

Leopard Cat Prionailurus bengalensis PM Srk Sab<br />

Flat-headed Cat Prionailurus planiceps PM Srk Sab<br />

(Fishing Cat<br />

Prionailurus viverrina) Old skin, Tasik Bera (doubtful record)<br />

Marbled Cat Felis marmorata PM Srk Sab<br />

Asian Elephant Elephas maximus PM Sab<br />

Malayan Tapir Tapirus indicus PM<br />

Javan Rhinoceros Rhinoceros sondaicus PM (extinct)<br />

Sumatran Rhinoceros Dicerorhinus sumatrensis PM Srk Sab<br />

(extinct)<br />

Wild Pig Sus scrofa PM<br />

Bearded Pig Sus barbatus PM Srk Sab<br />

Lesser Mouse-deer Tragulus kanchil PM Srk Sab<br />

Greater Mouse-deer Tragulus napu PM Srk Sab<br />

Barking Deer Muntiacus muntjak PM Srk Sab<br />

Yellow Muntjak Muntiacus atherodes Srk Sab<br />

Sambar Cervus unicolor PM Srk Sab<br />

Gaur Bos gaurus PM<br />

Banteng Bos javanicus PM Srk Sab<br />

Serow Capricornis sumatraensis PM<br />

PM = Peninsular Malaysia; Srk = Sarawak; Sab = Sabah<br />

SEA = South East Asia<br />

27


ALLEN JEYARAJASINGAM (2007)<br />

STATUS OF BIOLOGICAL DIVERSITY IN MALAYSIA &<br />

THREAT ASSESSMENT OF PLANT SPECIES IN MALAYSIA<br />

AN ASSESSMENT OF THE CURRENT<br />

KNOWLEDGE OF MALAYSIA’S AVIFAUNA<br />

Allen Jeyarajasingam<br />

ABSTRACT<br />

A total of 742 species of birds belonging to 85 families has been recorded within the political<br />

boundaries of Malaysia. Of these 43 are endemics, distributed between Peninsular Malaysia<br />

and the Bornean states of Sarawak and Sabah. This paper serves to assess and highlight the<br />

current state of knowledge of Malaysia’s birds with special emphasis on status, distribution,<br />

breeding biology and conservation. Although a common checklist is maintained for the country,<br />

the gathering and processing of scientific information have to be separate between Peninsular<br />

Malaysia, Sarawak, and Sabah, because the latter are disjunct territories, separated by sea.<br />

High species diversity still remains in the rainforest, both lowland and montane with over 395<br />

species or 53%. Despite nearly 150 years of specimen collection, field observations by both<br />

professional and amateur naturalists as well as other field and laboratory work, current<br />

knowledge remains relatively low, especially in Sarawak and Sabah. Most type specimens<br />

collected in the country by foreign collectors and scientists are currently deposited in museums<br />

abroad. Large gaps in the breeding biology of most resident species, together with knowledge<br />

of habits and conservation status exist. These can be eventually filled in if there is close cooperation<br />

and information sharing between government agencies, local universities and nongovernmental<br />

organizations in establishing and effectively coordinating a systematic network<br />

in order to build up an easily accessible and user friendly database for the realization of<br />

conservation goals.<br />

Sekolah Menengah Sains Alam Shah, Jalan Yaakob Latif, Bandar Tun Razak, 56000 Kuala Lumpur, Tel: 03–9131 5014,<br />

Fax: 03–9131 8119; allenj1959@yahoo.com<br />

29


INDRANEIL DAS & NORSHAM YAAKOB (2007)<br />

STATUS OF BIOLOGICAL DIVERSITY IN MALAYSIA &<br />

THREAT ASSESSMENT OF PLANT SPECIES IN MALAYSIA<br />

STATUS OF KNOWLEDGE OF THE<br />

MALAYSIAN HERPETOFAUNA<br />

1<br />

Indraneil Das & 2 Norsham Yaakob<br />

ABSTRACT<br />

Altogether, 203 species of amphibians and 397 species of reptiles are now known from<br />

Peninsular Malaysia and its offshore islands, and from East Malaysia (Sabah and Sarawak,<br />

and associated islands, on Borneo). Although a total of 600 herpetofaunal species seems a<br />

large figure in comparison to other landmasses of similar size regionally, a number of species<br />

have been discovered or recognized as new only in the last half a decade. Most of the new<br />

discoveries have been made from montane regions and offshore islands, but important findings<br />

have also been made not too far from the urban areas. Identification resources for the fauna<br />

specific to Peninsular Malaysia are relatively few, although recent field guides exist for all<br />

groups of taxa (except caecilians) for Borneo. No major systematic institutions exist within<br />

Malaysia for either type material or recent voucher specimens of herpetofaunal species, the<br />

Sarawak Museum in Kuching being repository of a small collection of mainly secondary<br />

types and older general collections from this state; the Selangor Museum in Kuala Lumpur<br />

was destroyed in the bombing of the city during World War II. Besides a concerted effort to<br />

continue inventories of Malaysia’s herpetofauna, urgently needed are the development of<br />

herpetology as a distinct discipline within the biological sciences of the university curriculum,<br />

and training of a generation of young biologists in relevant fields of systematics, ecology,<br />

genetics, biogeography, anatomy and morphology, in curatorship and an appreciation of the<br />

great outdoors.<br />

INTRODUCTION<br />

Malaysia supports a high species richness and endemicity in herpetofauna (Yong 1998), with<br />

203 described species of amphibians and 397 described species of reptiles (Tables 1 & 2).<br />

This diversity is unequally distributed across the country, the majority occurring in the<br />

highlands, which support a disproportionately large area of primary forest, compared to the<br />

lowlands. Altogether, these species represent a panoply of evolutionary history and diversity,<br />

from ancient groups that may had been restricted to mountain-tops due to climatic variation<br />

during the Pleistocene, to modern ones represented by diverse lineages. The underpinning<br />

reasons for the high levels of herpetological diversity of the Malaysian herpetofauna are:<br />

1<br />

Institute of Biodiversity & Environmental Conservation, Universiti Malaysia Sarawak, 94300 Kota Samarahan,<br />

Sarawak, Malaysia; idas@ibec.unimas.my<br />

2<br />

Forest Research Institute Malaysia, 52109 Kepong, Selangor, Malaysia; norsham@frim.gov.my<br />

31


STATUS OF KNOWLEDGE OF THE MALAYSIAN HERPETOFAUNA<br />

Table 1. Composition of amphibian fauna in Malaysia. The listing includes introduced species<br />

Family<br />

Number of species<br />

Bufonidae 35<br />

Megophryidae 28<br />

Microhylidae 34<br />

Ranidae 51<br />

Rhacophoridae 48<br />

Ichthyophiidae 7<br />

Total 203<br />

Table 2. Composition of the reptile fauna in Malaysia. The listing includes introduced species<br />

Family<br />

Number of species<br />

Acrochordidae 2<br />

Anomochilidae 2<br />

Boidae 4<br />

Colubridae 144<br />

Cylindrophiidae 3<br />

Elapidae 10<br />

Hydrophiidae 21<br />

Typhlopidae 5<br />

Viperidae 12<br />

Xenopeltidae 1<br />

Xenophidiidae 2<br />

Agamidae 37<br />

Anguidae 1<br />

Eublepharidae 1<br />

Dibamidae 5<br />

Gekkonidae 46<br />

Lacertidae 1<br />

Lanthanotidae 1<br />

Scincidae 61<br />

Uromastycidae 2<br />

Varanidae 4<br />

Crocodylidae 4<br />

Cheloniidae 4<br />

Dermochelyidae 1<br />

Emydidae 1<br />

Geoemydidae 12<br />

Testudinidae 3<br />

Trionychidae 5<br />

Total 397<br />

32


INDRANEIL DAS & NORSHAM YAAKOB (2007)<br />

i) parts of south-east Asia were not glaciated and were refuges during the height of the<br />

Pleistocene glaciation (see Heaney 1991, for a review);<br />

ii) the region has a complex history of sea-level fluctuations that attached and detached<br />

islands to the Asian mainland, joining and severing populations in the process;<br />

iii) the region shows a high diversity of geology and climate, and therefore, supports diverse<br />

ecological conditions; and<br />

iv) the area still is clothed in relatively large unbroken tracts of primary forests, such as<br />

tropical rainforests and montane forests.<br />

This paper presents a history and inventory of the herpetofauna of Malaysia, conducts an<br />

analysis of trends in research and provides some suggestions for the future.<br />

THE ROLE OF HERPETOFAUNA<br />

Amphibians and reptiles often constitute significant biomass, exceeding that of all other<br />

vertebrates (Burton & Likens 1975; Iverson 1982), form important linkages in the ecosystem<br />

by providing dispersal mechanisms for plants (Moll 1980; Vogt & Guzman 1988; Varela &<br />

Bucher 2002; Liu et al. 2004; Rick & Bowman 1961; Moll & Jansen 1995; Fialho 1990;<br />

Iverson 1985), form an important link in the trophic structure through predation, sometimes<br />

of much larger animals (Singh 2000), scavenging (Furbank 1996); Spencer et al. 1998; Esque<br />

& Peters 1994), and form a potential prey-base themselves (Ernst et al. 1994; Souza & Abe<br />

2000; Martuscelli 1995; Rhodin et al. 1993), contribute to environmental heterogeneity (Kaczor<br />

& Harnett 1990), have keystone functions in maintaining ecosystem structure (Thorbjarnarson<br />

1992; Ross 1998) and foster important symbiotic associations with an array of organisms<br />

(Lago 1991; Witz et al. 1991). Several species of turtles regularly eat water hyacinths,<br />

Eichhornia, presumably helping to control this water weed (Davenport et al. 1992; Varghese<br />

& Tonapi 1986; Fachin-Terán et al. 1995). Population data on herpetofaunal species have<br />

been used for constructive predictive models of abundance of target taxa (Clawson et al.<br />

1984).<br />

Amphibians and reptiles are known to be important predators of insect (Bhanotar & Bhatnagar<br />

1976; Gans 1994) and rodent (Lim 1974; Whitaker & Advani 1983) pests in agricultural<br />

ecosystems, and support a thriving trade based on export of froglegs (Niekisch 1986). Snake<br />

venom is used in medical research, for the production of life-saving drugs (Lim et al. 1977a;<br />

1977b; Reid 1968; Stocker 1990) and over 500 alkaloids of 22 different structural classes<br />

have been found in skin extracts of amphibians (Daly et al. 2002), many with potential<br />

pharmaceutical value. Amphibians and reptiles are used in biomedical research, such as in<br />

transplant immunology, the culture of cells and tissues for studies of cell growth and association<br />

(Wake et al. 1975). In Malaysia, several species have high commercial value. Larger frogs,<br />

including Limnonectes blythi, Fejervarya cancrivora and F. limnocharis, are eaten including<br />

some large lizards, particularly Varanus salvator and V. nebulosus (see Khan 1969) and many<br />

turtle and tortoise species (Kiew 1984f; Lim & Das 1999). Several species of snakes, such as<br />

Python reticulatus, Naja sumatrana, Ophiophagus hannah and Acrochordus javanicus are<br />

prized for their meat and medicine (Lim 1961) as are crocodilians (Tweedie & Harrison 1970;<br />

Anonymous 1983). Finally, amphibians and reptiles, on account of their typically small body<br />

size, high species diversity and widespread distribution, poikilothermy and lack of parental<br />

care have been considered model organisms for the study of vertebrate life (Pianka 1986).<br />

33


STATUS OF KNOWLEDGE OF THE MALAYSIAN HERPETOFAUNA<br />

Little is known of the parasitic fauna of amphibians and reptiles in Malaysia. The few studies<br />

carried out by Lim et al. (1990), Lim & Shabrina Mohd. Sharif (1998), Ambu et al. (1982),<br />

Stiller et al. (1977) & Nadchatram (1979) reveal that some of the endoparasites are of medical<br />

and public health importance. Some of the helminthic parasites, such as the pentastomids are<br />

pathogenic to man. These group of parasites are fairly prevalent among pythons, elapid and<br />

viperid snakes. Ecto- and endoparasites of any animal taxa provide ecological labeling of the<br />

host species, as they are associated with the food habits in relation with the environment. To<br />

date, knowledge of the host-parasite relationship of amphibians and reptiles (viruses, bacteria,<br />

protozoa, helminthes and arthropods) is in its infancy, and this comprises another gap in the<br />

study of biological associations.<br />

Peninsular Malaysia<br />

HISTORICAL ACCOUNT OF STUDIES<br />

Early herpetological collections in the Malay Peninsula were made by Cantor (1847) and<br />

Stoliczka (1870a, 1870b, 1870c; 1873), not surprisingly, focussing on former centres of<br />

European trade, including Penang, Malacca and Singapore. Biographies of these early explorers<br />

are in Kolmaš (1982) and Smith (1931b). Unusual for his time, Theodore Edward Cantor<br />

(1809–1860), Danish surgeon-naturalist with the English East India Company, included details<br />

of colouration and natural history. He observed that the now rare estuarine trionychid turtle,<br />

Pelochelys cantorii was commonly caught in fishing stakes. Cantor’s material is at present in<br />

the Natural History Museum, London, with the painting of the species, and serves as iconotypes,<br />

being preserved at the Bodleian Library of Oxford University. Ferdinand Stoliczka (1838–<br />

1874), a member of the Asiatic Society of Bengal and palaeontologist of the Geological Survey<br />

of India, the ‘high-altitude explorer’ (sensu Kolmaš 1982), collected on Penang’s highest<br />

mountain–Great Hill or Bukit Bendera, describing numerous new taxa, including the bufonid<br />

genus Ansonia, named after the Lieutenant-Governor of Penang, Major General Archibald<br />

Edward Harbord Anson (1826–1925) at the time of Stoliczka’s visit.<br />

Significant collections of amphibians and reptiles from the Malay Peninsula at the end of the<br />

Nineteenth Century were made by Major Stanley Smyth Flower (Flower 1896, 1899), of the<br />

Northumberland Fusiliers (obituary in Smith 1946). Flower also sent specimens to London<br />

(Boulenger 1896b). Early checklists of the amphibians of Peninsular Malaysia in 1902 and<br />

1904 were compiled by Arthur Lennox Butler (1873–1939), Curator of the Selangor State<br />

Museum, who subsequently became Superintendent of the Sudan Game Preservation<br />

Department, and show 58 species. Herbert Christopher Robinson (1905) added additional<br />

species to the list, counting 63 nominal species, plus an “Ixalus”. Local administrators (such<br />

as Dudley Francis Amelius Hervey, 1849–1911, of the Malayan Civil Service) sent material<br />

to George Albert Boulenger (1858–1937) at the British Museum (Natural History), London,<br />

who described new species (e.g., Boulenger 1887a). Butler too deferred to Boulenger for<br />

taxonomic opinion on the fauna, and sent specimens to London, eventually to be described by<br />

the latter (e.g., Boulenger 1900b; 1900c; 1900d; 1905).<br />

The first public museum in Peninsular Malaysia was established at Taiping in 1883, with<br />

Leonard Wray (1852–1942), formerly an engineer with the Public Works Department of the<br />

Perak Civil Service, as the Curator (biography in Burkill 1927). The Selangor Museum opened<br />

34


INDRANEIL DAS & NORSHAM YAAKOB (2007)<br />

to the public in 1888, Wray holding charge as Curator. The main museum building was<br />

completed in 1907, and in 1940, the Perak Museum and Selangor Museum were amalgamated<br />

to form the Federated Malay States Museum. Herpetological (and other zoological) surveys<br />

were carried out by the Selangor Museum throughout the Malay Peninsula, and reported in<br />

the Journal of the Museum. Following the government’s programme of decentralisation in the<br />

1930s, the two museums were again separated, and became state institutions. Museum staff<br />

continued to publish in the Federated Malay States Museums Journal, which issued 19 volumes<br />

between 1905 and 1939 (terminating with World War II). A misdirected load of bombs from<br />

an American B29 bomber landed on Selangor Museum on 10 March 1945. The collections<br />

were destroyed, and parts of the salvaged material were eventually transferred to the Perak<br />

Museum, Taiping in January 1946. In May 1949, the office of the Director of Museums moved<br />

from Kuala Lumpur to Taiping.<br />

The most important collection of regional herpetological (and indeed, zoological) materials<br />

lies in the Raffles Museum of Biodiversity Research, National University of Singapore. The<br />

Museum’s earliest collection originates from the 1840s, and contains much valuable material<br />

acquired by a succession of field-oriented curators, some of whom also acquired specimens<br />

through exchange programmes with other museums. In 1888, field collectors were hired and<br />

collections took place mainly from the region of the border between Selangor and Pahang.<br />

The following year, collectors were sent to Johor and Jelebu in Negeri Sembilan.<br />

Compared to Borneo, there were fewer foreign expeditions in the Malay Peninsula in the<br />

Nineteenth and Twentieth Centuries. In 1899–1900, English biologists, together with students<br />

from the universities of Cambridge and Oxford conducted the Skeat Expedition, organised by<br />

Walter William Skeat (1866–1953), British ethnographer and member of the Malayan Civil<br />

Service (Skeat 1900). Its objective was to collect data on ethnology, zoology, botany and<br />

geology of the Pattani States of Siam (now Thailand), adjacent portions of northern Malaysian<br />

states, including Terengganu and Kelantan (sites listed in Skeat 1901), then under Siamese<br />

sovereign. The acquired herpetological materials were studied by Frank Fortescue Laidlaw<br />

(1876–1963) (Laidlaw 1900, 1901a, 1901b), a student of Trinity College, Cambridge, who<br />

was to later become an authority of the Odonata.<br />

A second collection from the northern Malay Peninsula was made by Thomas Nelson Annandale<br />

(1876–1924), a student of Balliol College, Oxford, who was to later join the Indian Museum,<br />

and Herbert Christopher Robinson (1874–1929), who was appointed Curator of the Selangor<br />

Museum, between 1901 and 1902. Boulenger (1903) provided an extended account of the<br />

fauna in a special volume edited by Annandale and Robinson. In the species accounts were<br />

extensive ecological notes made by Annandale. New herpetological taxa described were named<br />

for the leaders of the expedition, include the rare rhacophorid, Rhacophorus robinsonii, for<br />

Robinson and Cyclemys annandalii (presently Heosemys annandalii), for Annandale.<br />

An important collector was Count Nils Gyldenstolpe (1886–1961), ‘Lord of the Bedchamber’<br />

to King Gustav V of Sweden, who was primarily interested in ornithological taxonomy (see<br />

Curry-Lindahl 1961), but also made significant herpetological collections in Thailand (1911–<br />

1912) and the Malay Peninsula (1914–1915). His material were described by Einar Lönnberg<br />

(1865–1942), professor in charge of vertebrates at Naturhistoriska Riksmuseet, Stockholm,<br />

Sweden (Lonnberg 1916), his assistant, Lars Gabriel Andersson (1868-1951) Swedish zoologist<br />

and for a while, a member of staff of the Museum (Andersson 1916), and by Gyldenstolpe<br />

35


STATUS OF KNOWLEDGE OF THE MALAYSIAN HERPETOFAUNA<br />

(1916) himself. One of Lonnberg’s species, Elachyglossa gyldenstolpei, named for the leader<br />

of the expedition, was recently included in the genus Limnonectes by Ohler and Dubois (1999).<br />

The German-born zoologist, Karl Richard Hanitsch (1860–1940), while primarily a specialist<br />

of the Blattidae, was hired as the Raffles Museum’s first Curator (1895–1919). During this<br />

time, apart from donations from expatriates, the herpetological collection grew through<br />

expeditions organised by Hanitsch. In 1898, Hanitsch prepared a catalogue of herpetofauna<br />

of the Malay Peninsula and archipelago. Formerly of the Sarawak Museum, Major John Coney<br />

Moulton (1886–1926), was to succeed Hanitsch as the second Director of the Raffles Museum<br />

(1919–1923). Also primarily interested in entomology (especially the Rhopalocera and the<br />

Cicadidae), Moulton collected locally, as well as in Borneo. Between 1923 and 1932, Cecil<br />

Boden Kloss (1877–1949) was Director of the Raffles Museum. Boden-Kloss, with Museum<br />

Curator, Frederick Nutter Chasen (1897–1942), conducted a joint expedition with the Federated<br />

Malay States Museum to Cameron Highlands in Peninsular Malaysia, in addition to collecting<br />

in Gunung Angsi in Negri Sembilan. In 1927, Smedley made herpetological collections on<br />

Pulau Aur and Pulau Tioman, islands off the east coast. In 1929, the Raffles Museum<br />

commenced publication of its journal, the Bulletin of the Raffles Museum, since renamed the<br />

Raffles Bulletin of Zoology, and now in its 54th volume. Some of the herpetological material<br />

acquired by local collectors and expatriates were made available to Malcolm Arthur Smith<br />

(1875–1958; obituary in Tenison 1959), physician at the Royal Court of Siam (see Smith<br />

1957), who published descriptions and faunal lists (Smith 1924, 1925c, 1935, 1940).<br />

Another famous Curator of the Raffles Museum was Michael Willmer Forbes Tweedie (1907–<br />

1993), who was Assistant Curator in 1932 and Curator between 1932 and 1941, and Director<br />

between 1946 and 1957 (biography in Ng 1995). While primarily a carcinologist, he published<br />

a number of valuable herpetological papers, including the book, The Snakes of Malaya, first<br />

published in 1953, with subsequent editions in 1954, 1957, 1961 and 1983. In the post World<br />

War II era, the Raffles Museum received material from Lim Boo Liat (from throughout<br />

Peninsular Malaysia), Hugh Alistair Reid (Penang) and E.N.W. Oliver (Bukit Larut). Reid<br />

(1913–1983) was associated with the Penang General Hospital, and made observations on sea<br />

snake poisoning, and in 1961, founded the Penang Institute of Snake and Venom Research<br />

(Hawgood 1998).<br />

In the decades before the closing of the last century, two substantial monographic inventories<br />

were published – those of Grandison (1972: reporting the Gunung Benom Expedition) and<br />

Dring (1979), presenting an inventory of Gunung Lawit in northern Terengganu). Lim Boo<br />

Liat (1926–), formerly with the Institute of Medical Research, Kuala Lumpur, and currently<br />

associated with the Department of Wildlife and National Parks, published extensively on the<br />

herpetofauna, especially snakes, covering locality inventories, food behaviour studies and<br />

captive behaviour including epidemiology of snake bites (e.g., Lim 1955; 1963b; 1967; Lim<br />

& Kamarudin 1975), produced a guide to the venomous snakes (Lim 1979, revised editions in<br />

1982 and 1991) and described two new species of the genus Macrocalamus (see Lim 1963a;<br />

Norsham & Lim 2003).<br />

A number of papers specific to amphibians of the region were published in the second half of<br />

the 20th Century, culminating in the book on the fauna by Berry (1975). At about the same<br />

period, a number of papers of systematic and ecological value, by a large number of local<br />

university and research institutes, noteworthy amongst these being inventories and the<br />

36


INDRANEIL DAS & NORSHAM YAAKOB (2007)<br />

description of a number of new amphibian species by Kiew (1972; 1984a; 1984b; 1984c;<br />

1987); Yong’s (1977) rediscovery of Rhacophorus robinsoni in Peninsular Malaysia; Berry<br />

and Hendrickson’s (1963) description of Leptobrachium nigrops; sea snake inventories by<br />

Lim and Balasingam (1969); Hendrickson’s (1966) account of the herpetofauna of Pulau<br />

Tioman; Yong et al.’s (1988) report of direct development in the frog genus Philautus; Denzer<br />

& Manthey’s (1991) checklist of the lizards of Peninsular Malaysia and Singapore, to mention<br />

a few. Toward the end of the decade, a fine introductory work to the fauna of southeast Asia<br />

was published by Manthey & Grossmann (1997). With German text and richly illustrated<br />

with colour photos, the volume has a comprehensive species listing covering Sundaland (the<br />

Malay Peninsula, Borneo, Sumatra, Java, Bali and associated islands), and descriptions of<br />

representatives from every genera of amphibians and reptiles.<br />

Ecological research on turtles has been conducted by a number of colleagues in Peninsular<br />

Malaysia. After the early observations on the natural history of the now endangered river<br />

terrapin, Batagur baska, by Khan (1964), intensive studies, involving radio telemetry, were<br />

conducted by Edward Owen Moll (1939–) of Eastern Illinois University (Moll 1980). The<br />

same worker also reported on natural history and exploitation of other non-marine turtles of<br />

West Malaysia (Dunson & Moll 1980; Moll 1976; 1978), and wrote a status paper on the<br />

estuarine and marine turtles of Peninsular Malaysia (Siow & Moll 1981). In the wake of Moll,<br />

studies on estuarine turtles, especially the painted terrapin, Callagur borneoensis, was<br />

conducted as part of a doctoral thesis by Dionysius Shankar Kumar Sharma, staff of World<br />

Wide Fund for Nature Malaysia—apart from internal reports, the results are not publicly<br />

available. A valuable report by Sharma (1999) is available on the trade in tortoises and<br />

freshwater turtles. Marine turtles of Peninsular Malaysia have been the subjects of intensive<br />

studies in comparison, primarily by Chan Eng Heng, Professor of Zoology at Kolej Universiti<br />

Sains dan Teknologi Malaysia. A number of scientific papers have resulted from these studies<br />

(Chan & Liew 1996); 1999; Liew & Chan 2002; Tan et al. 2000).<br />

Starting in 2001, Larry Lee Grismer (1955–) and collaborators, including the authors of this<br />

essay, inventoried the Seribuat Archipelago, including its most famous island, Pulau Tioman,<br />

producing island lists, new species descriptions and biogeographic analyses (Grismer 2005;<br />

Grismer et al. 2006; Grismer & Das 2005; Grismer et al. 2003; Grismer et al. 2004a; Grismer<br />

et al. 2004b; Grismer et al. 2004c; Grismer & Leong 2005; Grismer et al. 2002a; Grismer et<br />

al. 2002b; Diaz et al. 2004; Grismer et al. 2006; Youmans & Grismer 2006). These studies are<br />

on going, and have in recent years, been extended to the Malay Peninsula and Pulau Langkawi,<br />

on the west coast (Grismer et al. 2006). Other important works from this century include<br />

Vogel et al. (2004), who revised the pit vipers previously referred to Trimeresurus popeiorum<br />

(at present, Popeia popeiorum), recognising several species within the group, David & Pauwels<br />

(2004) and Norsham & Lim (2003), described new species of Macrocalamus. Another<br />

colleague who made important contributions to regional herpetology is Tzi-Ming Leong (1972–<br />

), formerly a graduate student with the National University of Singapore, and currently with<br />

Singapore National Parks, who published extensively on the herpetofauna of the Malay<br />

Peninsula and adjacent areas (e.g., Grismer & Leong 2005; Leong 2000; Leong & Grismer<br />

2004; Leong & Lim 2003b; Leong et al. 2003), and especially on amphibians and their larvae<br />

(e.g., Leong 2002; 2004; Leong & Lim 2003a; 2003c; Leong & Norsham 2002), as part of a<br />

recent doctoral thesis. Jeet Sukumaran (1971–), formerly with World Wide Fund for Nature-<br />

Malaysia and Universiti Malaya, and currently a graduate student at the University of Kansas,<br />

produced several site inventories (Sukumaran 2003; Sukumaran et al. 2006), an as yet<br />

37


STATUS OF KNOWLEDGE OF THE MALAYSIAN HERPETOFAUNA<br />

unpublished thesis on amphibian distribution on Gunung Jerai, in addition to popular writing<br />

(Sukumaran 2002a; 2002b). He also maintains the website, Frogs of the Malay Peninsula (see<br />

Appendix III).<br />

The work of the present authors (Das, born 1964; Norsham, born 1972) in Peninsular Malaysia<br />

includes surveys of montane and other highland environments, which have resulted in the<br />

discovery of a number of species new to science (e.g., Das 2005; Das & Haas 2005a; Das &<br />

Norsham 2003; Das et al. 2004; Norsham 2003; Norsham & Abdul 2000). The collection of<br />

the Raffles Museum was also examined, and the discovery of new species resulted (Das &<br />

Lim 2000; Das & Lim 2001a), apart from the herpetological type catalogue of the collection<br />

(Das & Lim 2001b), all undertaken with the collaboration of its Curator, Kelvin Kok Peng<br />

Lim (1966–).<br />

Two recent works in popular format exist for the herpetofauna of Peninsular Malaysia: Chanard<br />

et al. (1999) published an innovative pictorial checklist for the area (including Thailand),<br />

updating the species list of both amphibians and reptiles. The field guide to the reptiles of the<br />

same region by Cox et al. (1998) covers the more common or interesting species. These help<br />

update the fauna, last treated to a monographic review by Boulenger (1912: A vertebrate<br />

fauna of the Malay Peninsula from the Isthmus of Kra to Singapore including the adjacent<br />

islands. Reptilia and Batrachia), with an update by Smith (1930).<br />

Sarawak<br />

The earliest herpetological specimens from Borneo were collected during the voyage of H.M.S.<br />

Sulphur, commanded by Captain (later Admiral) Edward Belcher (1799–1877). An account<br />

of the voyage to the Far East was written by Belcher (1843), where he described the ship as<br />

weighing 380 tons and had a crew of 109 men. Materials from this expedition, organised<br />

primarily to suppress piracy in the Malay Archipelago and other parts of south-east Asia, are<br />

extant in The Natural History Museum, London include (species marked with asterisk were<br />

described as new based on this collection) Takydromus sexlineatus, Tropidophorus brookei,<br />

Mabuya multifasciata, Hemidactylus brookii*, Hemidactylus frenatus, Cosymbotus platyurus,<br />

Cnemaspis kendallii* and Gekko monarchus, Tropidolaemus wagleri (see Gray 1845). Also<br />

collected were Tarentola borneensis* and Euprepis belcheri*, at present synonymous with<br />

Mabuia delalandei Duméril & Bibron, 1839, both known to be endemic to Cape Verde Islands.<br />

Apart from these erroneous records, the Belcher collections indicated that only the lowland<br />

fauna was sampled.<br />

The first checklist of the herpetofauna of Borneo was compiled in 1848 by the Scottish botanist,<br />

Hugh Low (1824–1905), a self-described admirer of Rajah Brooke (see below) of Sarawak<br />

(biography in Cowan 1968) and author of a book on Sarawak at the time of the First Rajah<br />

Brooke (Low 1848), entitled, ‘Sarawak. Its inhabitants and productions being notes during a<br />

residence in that country with His Excellency Mr. Brooke’. It listed a mere 19 species of<br />

reptiles and three of amphibians (additional species were mentioned in the text itself, including<br />

unspecified “land tortoises” of two species and flying lizards). Some of the early zoological<br />

specimens in western museums originate from collections made by European residents of<br />

Sarawak. Lewis Llewellyn Dillwyn (1814–1892) and James Motley (1814–1892) wrote a<br />

book on the natural history of Labuan, an island off Borneo and now Federal Territory of<br />

Malaysia (Motley & Dillwyn 1855) and sent collections in 1864 to the British Museum (Natural<br />

38


INDRANEIL DAS & NORSHAM YAAKOB (2007)<br />

History), London (now, The Natural History Museum, London), which, in 1872 and 1893–<br />

1894, purchased a collection made by Alfred Hart Everett (Günther 1872; Boulenger 1895a;<br />

1896a; 1906).<br />

Sarawak was a hive of activity, both scientific and ethnographic, at that time. Two other<br />

Europeans, the Italian nobleman Marquis Giacomo Doria of Genoa (1840–1913) and botanist<br />

Odoardo Beccari (1843–1920) landed on the shores of Borneo in June 1865. The latter was to<br />

become famous for his botanical collections (biographies in Cranbrook 1986; Saint 1987),<br />

remained till 1868, and made some significant collections of amphibians and reptiles (see<br />

Shelford 1905b). Beccari’s adventures were recounted in popular vein, initially in his native<br />

Italian (Beccari 1902), the work subsequently translated into English in 1904. The collections<br />

were described by Wilhelm Carl Hartwig Peters (1815–1883), of the Zoologisches Museum<br />

für Naturkunde, in Berlin (Peters 1861, 1862, 1871, 1872), and one in collaboration with<br />

Doria himself (Peters & Doria 1878). Another famous collector from the period was Alfred<br />

Russel Wallace (1823–1913), cofounder, with Charles Robert Darwin (1809–1882), of the<br />

theory of evolution through natural selection. Wallace’s collections on Borneo were along the<br />

Simunjan and Sadong Rivers of Sarawak (see Bastin 1986; field sites listed in Baker 2001).<br />

Apart from his herpetological collections (listed by Cranbrook et al. 2005), Wallace influenced<br />

the then Rajah of Sarawak, James Brooke (1803–1868) to establish the Sarawak Museum<br />

(Banks 1983; Leh 1993), in 1886. A recent biography of Wallace was authored by his great<br />

nephew, Wilson (2000), and Wallace himself had described his time in Sarawak and other<br />

parts of south-east Asia in his entertaining memoir, entitled ‘The Malay Archipelago: the land<br />

of the orangutan and the bird of paradise’ (Wallace 1869).<br />

A series of professional curators, hired from Europe, was behind the success of the Sarawak<br />

Museum. The results of their researches were to be published in the scientific organ of this<br />

institution, the Sarawak Museum Journal. The first Curator of the Museum was John E.A.<br />

Lewis, appointed in 1888 (Harrisson 1961a). He was succeeded by George Darby Haviland<br />

(1857–1901) who served between 1893 and 1895. Herpetological research by the first two<br />

Curators were restricted to collections. The first Curator to collect and publish extensively<br />

was Edward Bartlett (ca. 1836–1908; see Das 2000, for a biography), who was associated<br />

with the Museum, between 1895 and 1897. Among Bartlett’s largest work is a 24 page paper<br />

on the crocodiles and lizards of Borneo that were represented in the Sarawak Museum, including<br />

the description of eight new species of lizards (Bartlett 1895e). Additionally, he wrote a series<br />

of papers in The Sarawak Gazette, the monthly official gazette for the staff of the Sarawak<br />

Civil Service, on turtles and tortoises (1894a, 1895a, 1895b, 1896b), amphibians (1894b) and<br />

snakes (1895c, 1895d, 1896a, 1896c). These were reprinted in a book edited by Bartlett (1896d).<br />

In the late 19th Century, two officers in the pay of the Sarawak Civil Service, Charles Hose<br />

(1863–1929) and Alfred Hart Everett (1849–1898), made extensive zoological (and other)<br />

collections in Sarawak, that, via sale, made their way to European and American museums, to<br />

be described by curators there (e.g., Boulenger 1892; 1893; 1895a; 1895b; 1896a). Biographies<br />

and obituaries of Hose are in Nuttall (1927) and Durrans (1993), while those of Everett are in<br />

Anonymous (1898) and Sharpe (1898).<br />

Arguably, the most famous curator the Sarawak Museum had was Robert Walter Campbell<br />

Shelford (1872–1912; see Poulton 1916 for a biography), between 1898 and 1905. Although<br />

primarily interested in entomology, he wrote two taxonomic papers on herpetological subjects<br />

(Shelford 1901b; 1905a; 1906), as well as a checklist of the reptiles of Borneo (Shelford<br />

39


STATUS OF KNOWLEDGE OF THE MALAYSIAN HERPETOFAUNA<br />

1901, with an addenda and corrigenda in 1902) and an incomplete account of his time in<br />

Sarawak (Shelford 1916), interrupted by his untimely death. A total of 212 species was listed<br />

as occurring (deleting erroneous records and including new reports in Shelford’s 1902 note),<br />

and localities were provided for the species listed. Shelford continued the tradition of sending<br />

specimens to the British Museum, which were worked on by Boulenger, who described new<br />

species, including Lygosoma shelfordi Boulenger (1900a) honouring its collector.<br />

Shelford was succeeded by John Coney Moulton (1886–1926), between 1908 and 1915.<br />

Although Moulton wrote no major herpetological papers during his time the Museum building<br />

was enlarged. Moulton was succeeded by Eric Georg Mjöberg (1882–1938, born Hallands<br />

Ian) for a couple of years (1922–1924). Nonetheless, his collections were from some of the<br />

remotest regions of Sarawak–Gunung Murud, Gunung Penrissen and Gunung Pueh, including<br />

the adjacent Gunung Beremput), and yielded many novelties, that were described by Smith<br />

(1925a; 1925b). Mjöberg wrote a popular account of his various expeditions in Borneo and<br />

Sumatra, originally in Swedish, entitled ‘Tropikermas villande urskogar’ (Mjöberg 1928).<br />

Mjöberg was succeeded by Edward Banks (1903–1988) in 1925, and his emphasis being on<br />

mammals, and apart from a 1931 paper on crocodiles and a 1937 paper on sea turtles, did not<br />

publish on herpetology. In the aftermath of World War II, in 1947, Tom Harnett Harrisson<br />

(1911–1976; obituaries and biographied in Smythies 1975; Medway 1976; Heimann 1997)<br />

was hired as Government Ethnologist and Curator of the Sarawak Museum. Apart from his<br />

ecclectic natural history and ethnographic interests, Harrisson wrote extensively on<br />

herpetological topics, notably a series of sea turtle papers in 18 parts in the Sarawak Museum<br />

Journal (Harrisson 1951; 1954; 1955; 1956a; 1956b; 1958a; 1958b; 1959; 1961b; 1962; 1963b;<br />

1964; 1965; 1966; 1967) and also, papers reporting the rediscovery of Lanthanotus borneensis<br />

were published in notes authored by his then wife, Barbara Brünig Harrisson née Guttler<br />

(1922–) and a colleague, Neville Seymour Haile (1928–2004) (B. Harrisson 1961, 1962);<br />

T. Harrisson 1963a; Harrisson & Haile 1961a; 1961b). Haile (1958) also published a checklist<br />

of the snakes of Borneo. Harrisson also made the first herpetological collection from the<br />

remote Kelabit Highlands of Sarawak, incidental to his work on mammals there, which was<br />

described by Tweedie (1949).<br />

Closer to the present time, several foreign contributors have dealt with the local herpetofauna<br />

(see below). During the Gunung Mulu Expedition in 1977–1978, organised by the Sarawak<br />

Government and the Royal Geographical Society, Julian Christopher Mark Dring (1951–)<br />

collected herpetofauna from this site, revising several amphibian groups and describing new<br />

species (e.g., Dring 1983a; 1983b; 1987).<br />

Sabah<br />

Known historically as British North Borneo during most of the Nineteenth Century, Sabah<br />

has had its fair share of explorers. Predictably, its highest mountain, Gunung Kinabalu, was<br />

subject to intense botanical and zoological interest. Between 1887 and 1888, John Whitehead<br />

(1860–1899), an ornithologist, organised expeditions to Gunung Kinabalu (described in his<br />

folio-format work entitled ‘The exploration of Mount Kina Balu’; Whitehead 1893). His<br />

herpetological specimens were donated to the British Museum (Natural History), London and<br />

the Muséum National d’Histoire Naturelle, Paris, and were described, sometimes<br />

simultaneously, by Boulenger (1887b) at the former collection, and Mocquard (1890) at the<br />

40


INDRANEIL DAS & NORSHAM YAAKOB (2007)<br />

latter. Mocquard’s paper presented an updated list of herpetofauna of Borneo, with 204 species,<br />

comprising 49 amphibians and 155 reptiles.<br />

Another noteworthy expedition to this mountain was led in 1899 by Karl Richard Hanitsch<br />

(1860–1940), of the Raffles Museum, Singapore. The expedition was described by Hanitsch<br />

(1900), and Boulenger in London identified the herpetological specimens, in the process<br />

describing Leptobrachium baluensis, Gecko rhacophorus (at present Ptychozoon rhacophorus),<br />

Stoliczkia borneensis and Oreocalamus hanitschi. Two field associates of the Raffles Museum<br />

in Singapore, Frederick Nutter Chasen (1897–1942) and Henry Maurice Pendlebury (?–1945)<br />

collected on Kinabalu between April and May 1929 (Pendlebury & Chasen 1932), making<br />

their herpetological material available to Malcolm Smith, who wrote an account based on a<br />

collection of some 600 specimens, that are mostly extant in the Raffles Museum of Biodiversity<br />

Research, National University of Singapore (Smith 1931a). Boden Kloss’s 1928 visit to Gunung<br />

Kinabalu was to select collecting stations for a survey of this mountainous area the following<br />

year, when the Kampung (= village) Kiau approach was taken. Consequently, it bears the<br />

label of a great many specimens, including a number of types.<br />

Malaysia<br />

Robert Frederick Inger (1920–) of the Field Museum of Natural History, Chicago, has been<br />

the most famous of the living scholars of Bornean herpetology. His contributions include<br />

monographs on systematics, field guides, papers on systematics, ecology and biogeography<br />

(e.g., Inger 1954; 1956; 1957; 1958a; 1958b; 1964; 1966; 1967; 1989; Inger & Frogner 1980;<br />

Inger & Gritis 1983; Inger & Haile 1959; Inger & Leviton 1961; Inger & Stuebing 1989;<br />

1991; 1996); 1997; Inger et al. 1995; 1996); 2001; Inger & Tan 1996); Inger & Voris 2001),<br />

which continue to inspire the public, a most interesting tropical fauna. A second staff of the<br />

same institution, Harold Knight Voris (1940–), studied marine and freshwater snakes of the<br />

region, publishing ecological and taxonomic studies (e.g., Han et al. 1991; Voris 1964; 1985;<br />

Voris & Karns 1996). A collaborator of Inger and Voris is Robert Butler Stuebing (1946–)<br />

who conducted research on sea snakes and crocodilians (Engkamat et al. 1991; Stuebing<br />

1985; Stuebing et al. 1985; Stuebing & Voris 1990; Stuebing et al. 2006), and also produced<br />

important accounts of several sites, new species descriptions (Stuebing 1994; Stuebing &<br />

Wong 2000) and an updated checklist of the snakes of Borneo (Stuebing 1991, with an update<br />

in 1994), culminating in a field guide to the snakes of Borneo, coauthored with Inger (Stuebing<br />

& Inger 1999). He also made a passionate plea for the continuation of systematic research in<br />

the region, and pointed out the need for continuing with systematic collections (Stuebing<br />

1998). A number of Japanese colleagues have contributed to our knowledge of the Bornean<br />

herpetofauna. Foremost, for the study of the Amphibia, is Masafumi Matsui (1950–), who<br />

conducted field work in Sabah and Sarawak, describing new species as well as aspects of<br />

distribution and biology, especially acoustics (Matsui 1983; 1986; 1996); Matsui et al. 1985;<br />

1996). His co-workers published significant works on reptiles–Tsutomu Hikida (1951–) and<br />

Hidetoshi Ota (1959–) published a number of papers on the distribution, genetics and<br />

systematics of lizards (e.g., Hikida 1979; 1980; 1982; 1990; Ota & Hikida 1988; 1989; 1991;<br />

1996); Ota et al. 1989; 1990; 1991; 1992; 1996a; 1996b) The German contribution to the<br />

knowledge of Bornean herpetofauna have been significant, including the work of Rudolph<br />

Malkmus and Ulrich Manthey (1946–) throughout Borneo, and especially in Gunung Kinabalu,<br />

culminating in a volume on the herpetofauna of that massif (Malkmus et al. 2002).<br />

41


STATUS OF KNOWLEDGE OF THE MALAYSIAN HERPETOFAUNA<br />

Marine turtles of Malaysian Borneo have received attention in recent times by several workers.<br />

Nicolas James Pilcher (1965–) published on the situation in Sarawak and Sabah (Pilcher &<br />

Basintal 2000; Pilcher et al. 2000; Pilcher & Ali 1999; 2000), besides co-editing a book on<br />

sea turtle biology and conservation (Pilcher & Ismail 2000). G. Stanley de Silva (?–) an early<br />

staff member of Sabah Parks, contributed a number of papers on marine turtles of Sabah,<br />

addressing conservation issues (de Silva 1969a; 1969b; 1971; 1978; 1980). Ritchie & Jong<br />

(1993) published a popular account of man-eating crocodiles of the Batang Lupar region of<br />

central Sarawak, which was recently updated (Ritchie & Jong 2002).<br />

A number of local herpetologists have commenced publication of research papers and notes,<br />

all useful for increasing our overall knowledge of the distribution and biology of a fascinating<br />

fauna, including Norhayati Ahmed (1968–) of Universiti Kebangsaan Malaysia, who has<br />

published regional checklists and inventories (e.g., Norhayati et al. 2004; 2005a; 2005b).<br />

The work of the first author of this paper included the addition of a number of species to the<br />

Bornean fauna (e.g., Das & Bauer 1998; Das & Lim 2003) and of Peninsular Malaysia (e.g.<br />

Das & Lim 2000; Das & Norsham 2003), a historical account of herpetofaunal researches and<br />

explorations on Borneo (Das 2004b) and most recently, authored a book on the reptiles of<br />

Borneo (Das 2006). Collaboration with Alexander Haas (1964–) of Biozentrum Grindel und<br />

Zoologisches Museum, Universität Hamburg, on a project on the systematics and<br />

ecomorphology of amphibian larvae in Borneo is ongoing, and has resulted in several papers<br />

(e.g., Das & Haas 2005b; Haas et al. 2006). The second author contributed to the literature of<br />

Peninsular Malaysia, such as papers on distributional records, inventories and new species<br />

descriptions (e.g., Norsham & Abdul 2000; Norsham 2003; Norsham & Lim 2003).<br />

TRENDS IN RESEARCH<br />

Figures 1 and 2 present the rate of description of species of amphibians and reptiles known to<br />

occur in Malaysia to date. Analyses of the discoveries of the two groups are interesting. For<br />

amphibians, most new species were discovered in the 1890–1900s decade, coinciding with<br />

Boulenger, especially his British Museum catalogues, and also the various papers he wrote at<br />

the time based on material originating from the Malay Peninsula. Two other spikes are evident–<br />

the 1960–1970s and 1980–1990s decades, when a number of new species were described<br />

from Borneo by Inger and co-workers. A slump in species descriptions is evident thereafter.<br />

The most productive phase of discovery amongst the reptiles of Malaysia occurred in the<br />

1830–1840s decade. Major monographs were published at this time from the museums of<br />

Paris and London, based on materials received from Malaysia and elsewhere, important<br />

contributors being John Edward Gray (1800–1875), Hermann Schlegel (1804–1884), Theodore<br />

Edward Cantor (1809–1860), André-Marie-Constant Duméril (1774–1860), Auguste-Henri-<br />

André Duméril (1812–1870) and Gabriel Bibron (1806–1848). The description of a large<br />

number of species since the beginning of the 21st Century thus heralds a new age of discovery<br />

of an interesting fauna.<br />

The herpetofauna of Malaysia thus continues to be poorly known, as a result of incomplete<br />

sampling of the fauna. Much of the data available at present result from limited sampling done<br />

a century ago, and many species have not been collected since the original description. The<br />

42


INDRANEIL DAS & NORSHAM YAAKOB (2007)<br />

40<br />

Number of species<br />

30<br />

20<br />

10<br />

0<br />

1760 1770 1780 1790 1800 1810<br />

1820 1830 1840 1850 1860 1870 1880 1890 1900 1910 1920 1930 1940 1950 1960 1970 1980 1990 2000<br />

Decade of description<br />

Fig. 1. Description of currently valid species of amphibians known from Malaysia, in 10<br />

years interval.<br />

50<br />

40<br />

Number of species<br />

30<br />

20<br />

10<br />

0<br />

1750 1760 1770 1780 1790 1800 1810<br />

1820 1830 1840 1850 1860 1870 1880 1890 1900 1910 1920 1930 1940 1950 1960 1970 1980 1990 2000<br />

Decade of description<br />

Fig. 2. Description of currently valid species of reptiles known from Malaysia, in 10 years<br />

interval.<br />

43


STATUS OF KNOWLEDGE OF THE MALAYSIAN HERPETOFAUNA<br />

most recent compilation on the amphibian fauna of Peninsular Malaysia, that of Berry (1975),<br />

and of snakes by Tweedie (1983), are in need of revision, and carry no colour illustrations.<br />

There has been no modern synthesis of the rich lizard fauna, nor the crocodilians of Peninsular<br />

Malaysia. Lim & Das (1999) published a field guide to the turtles of Peninsular Malaysia (as<br />

well as Borneo). On the other hand, the herpetofauna of Borneo, is much better known, thanks<br />

to long-term researches conducted by Inger and his associates, resulting in field guides to<br />

anuran amphibians (Inger & Stuebing 1989; 1997 – reprinted 2005) and snakes (Stuebing &<br />

Inger 1999). A volume on lizards by the same publisher is available (Das 2004a), and most<br />

recently, a volume on the reptiles of the island (Das 2006). Given the relatively solid basis of<br />

systematics of the herpetofauna of Borneo (from where, nonetheless, new species continue to<br />

be described), an ecological and systematic comparison of the faunas of Peninsular Malaysia<br />

and Borneo is proposed. Because there have been little direct comparisons of the fauna of<br />

Peninsular Malaysia, with that of the much better known eastern part (Sarawak and Sabah in<br />

Borneo), several species at present thought to be conspecific are likely to be vicars or even<br />

possibly unrelated, as some research now underway with specific species complexes (e.g.,<br />

Rana chalconota, Limnonectes macrodon, Fejervarya limnocharis, Cosymbotus platyurus<br />

and Ophiophagus hannah) suggest. Many of the new species discovered are cryptic species,<br />

which are very similar to known species, hence simply not recognised until a thorough revision<br />

of the entire group is undertaken, sometimes utilizing modern laboratory (including gene<br />

sequencing) and field (ecological and behavioural) methods. Hanken (1999) described the<br />

process of amphibian discovery in the recent past, attributing this to not only inventories of<br />

poorly known regions but also the use of genetic tools. Nonetheless, the new species discoveries<br />

for Malaysia are at present the result of relatively ‘coarse-screening’, suggesting that additional<br />

species that are taxonomically cryptic will be discovered in the future, with the use of DNA<br />

and other techniques.<br />

Cryptic species are frequently localized, some restricted to patches of forests a few dozen<br />

hectares in extent or to one or two adjacent hill streams, making their discovery difficult,<br />

unless a concerted effort is made to conduct an exhaustive inventory. Non-recognition of<br />

cryptic species is known to have lead to their extinction (Daugherty et al. 1990). Other species<br />

may show populations with disjunctions, and structured into well defined phylogenetic<br />

assemblages or metapopulations, some with significant genetic variants, all requiring careful<br />

consideration for identification and conservation (see Sites & Crandall 1997). Supplying names<br />

to these “hidden” species, thus, is the first step towards their universal recognition and protection<br />

(Longino 1993; Wheeler 1995). True, the recognition of cryptic species is increasing the<br />

conservation burden; it also emphasizes the importance of moving away from taxon-based<br />

conservation to that emphasizing protection of the environment at the level of landscapes and<br />

ecosystems (Lovich & Gibbons 1997; Das 2002). Despite this knowledge, systematic research<br />

in the country is rather limited, and systematic collection small and scattered. The most<br />

significant one in Sarawak, the Sarawak Museum, has a small type collection (Das & Leh<br />

2005), and none of historical significance exists elsewhere. New collections have now started<br />

in the Forest Research Institute Malaysia, Kepong, by the second author, at Universiti<br />

Kebangsaan Malaysia and Universiti Malaya, in Kuala Lumpur, and in Sabah, at the campus<br />

of Universiti Malaysia Sabah, Kota Kinabalu (the Borneensis collection), the Sabah State<br />

Museum, also at Kota Kinabalu, and at the Sabah Parks, Gunung Kinabalu National Park<br />

Headquarters.<br />

44


INDRANEIL DAS & NORSHAM YAAKOB (2007)<br />

CONSERVATION ISSUES AND THE FUTURE<br />

Human impact on the rainforests in Malaysia predates 600 years before present (Maloney<br />

1985). However, since the 1970s, large-scale conversion of forest areas for agricultural use<br />

has put great stress on the remaining tropical forests of the country (Aiken & Moss 1975;<br />

Appanah 1998). West Malaysia, on account of its peninsular geometry and faunal similarity<br />

to other large Sundaic islands, has an insular quality (Heaney 1991), potentially making species<br />

more vulnerable to extinction than in typical continental situations. The forests of Borneo are<br />

threatened primarily through conversion of forests to plantations and timber extraction (Primack<br />

& Hall 1992).<br />

As a megadiversity country, much of Malaysia’s biological diversity remains intimately<br />

associated with her tropical rainforests. However, regions of exceptional concentration of<br />

species within biodiversity hotspots are in montane regions, which are thus of great conservation<br />

importance in supporting species with small geographic ranges, including rare and endemic<br />

species. Other areas include poorly explored offshore islands, many of which continue to<br />

have unexplored biological diversity. Protection of small areas may be a relatively more efficient<br />

and cost-effective method for protecting regional biodiversity. A recent study in Amazonia,<br />

comparing collection-based data and those on qualitative study of regional biodiversity show<br />

little correspondence, emphasizing the need for more rigorous data collection and analysis to<br />

identify and subsequently protect biodiversity hotspot areas.<br />

Besides overt threats to the fauna, caused by changing land-use patterns and habitat destruction,<br />

faunal decline in other parts of the world has also been reported from causes not completely<br />

understood at present, and may stem from a combination of factors, including ozone layer<br />

depletion, infection by virulent microorganisms, use of organochlorine pesticides and herbicides<br />

and habitat fragmentation. Lack of data on abundance make estimates of levels of imperilment<br />

of the Malaysian herpetofauna impossible, and serious attempts to remedy this may be needed<br />

to understand factors that potentially threaten species and populations. This gap is suspected<br />

to be a serious impediment to the conservation and management of an important component<br />

of the country’s biodiversity.<br />

The use of amphibians and reptiles to understand human impact on the environment is an<br />

active area of study (review in Parent 1992; see also Bury et al. 1980), although there has been<br />

little work done in tropical Asia. The systematic basis of these researches is of fundamental<br />

importance, and much work has been conducted in adjacent regions, such as Thailand, and in<br />

other Asian countries, such as Singapore, India, Sri Lanka and most recently, Vietnam. The<br />

work in Sri Lanka is particularly significant, in leading to the increase of the amphibian fauna<br />

from 53 to over 250 species (Pethiyagoda & Manamendra-Arachchi 1998; see also<br />

Manamendra-Arachchi & Pethiyagoda 2005; Meegaskumbura & Manamendra-Arachchi 2005).<br />

As many cryptic species have small ranges, non-detection of unique species has been linked<br />

to their extinctions (see Daugherty et al. 1990).<br />

Nearly 600 species of amphibians and reptiles have been recorded from Malaysia, although<br />

this fauna is unequally distributed. An important challenge is to identify, at various spatial<br />

scales, areas of exceptional concentrations of species, or so-called “hotspots” of biodiversity<br />

of the herpetofauna (sensu Myers 1988; 1990). Important montane regions that hold promise<br />

include the Titiwangsa (or Main) Range of Peninsular Malaysia, that comprises Gunung Noring<br />

45


STATUS OF KNOWLEDGE OF THE MALAYSIAN HERPETOFAUNA<br />

(1,889 m), Gunung Chamah (2,171 m), Gunung Batu Putih (2,132 m), Cameron Highlands<br />

(1628 m) and Fraser’s Hill (1,524 m), besides limestone areas of Gua Musang, Kelantan and<br />

the Kinta Valley area, Perak. Within Borneo, important montane regions requiring additional<br />

work include Gunung Mulu (2,377 m), Gunung Murud (2,423 m), Gunung Kinabalu (4,101<br />

m) and Gunung Dulit (1,311 m). Specific ecological habitats inadequately sampled include<br />

peat swamps and kerangas.<br />

One of the main goals of these studies should be to develop aid to the identification of the<br />

fauna, leading to a comprehensive (i.e., covering all nominal species and subspecies)<br />

monographs, field keys and field guides for the identification of amphibians and reptiles of<br />

Malaysia. Field guides are important in promoting conservation awareness and action, assisting<br />

capacity building, supporting environmental assessments (such as monitoring and evaluation)<br />

of development projects, encouraging ecotourism, building biodiversity databases, land-use<br />

planning through GIS applications and the production of regional and international Red Data<br />

Books of Threatened Species (Whitten 1996).<br />

Contemporary conservation programmes derive substantial inputs from scientific databases<br />

on the distribution, ecology and systematics of regional biodiversity. Identification of hotspots,<br />

be these centres of high diversity or endemicity is critical for reserve selection and design<br />

(Lovich 1994), helping focus scarce conservation money on the areas with the highest priority.<br />

Myers (1988, 1990), utilizing plants as indicators, identified 18 areas of the Earth that support<br />

species disproportionately high for their combined area. Fortuitously, there is a concordence<br />

with the distribution of other taxa as well, and at least 19% of the world’s herpetofauna are<br />

found in Myers’ hotspots (Mittermeier et al. 1992). Biodiversity awareness is generating an<br />

increasing demand for basic information which systematics can provide (see Kottelat 1995).<br />

A priority of the systematist, in the face of rapid loss of habitats, has become the development<br />

of identification tools, critical for promoting environmental awareness and conservation,<br />

supporting environmental impact analyses and for other biodiversity studies.<br />

The information base for amphibian and reptile systematics, taxonomy and field identification<br />

for Peninsular Malaysia continues to be the work of Boulenger (1912), with a substantial<br />

supplement by Smith (1930). The amphibian fauna of Borneo is somewhat better, with field<br />

guides available for the turtles, frogs and snakes (e.g., Inger 1966; Inger & Stuebing 1997;<br />

Stuebing & Inger 1999; Lim & Das 1999). Nonetheless, most of the field guides are not<br />

comprehensive in coverage. Several factors are responsible–the discovery of new species,<br />

reallocation of species to genera other than the ones originally allocated to, and in some<br />

instances, to different families, the synonymy of some names and the revival from synonymy<br />

of others, in addition to new distributional and natural history information. Monographs<br />

prepared in the early part of the last century contain terse descriptions, that would equally fit<br />

several closely related species (or “shoe-horning”), thereby potentially causing serious<br />

underestimation of biodiversity if assessments are made using these resources. Additionally,<br />

neither of the works mentioned carry colour photographs, often critical for field identification.<br />

Work conducted regionally, including in adjacent countries, has lead to a dramatic increase in<br />

the local fauna. For instance, fieldwork conducted in recent years in Vietnam has increased<br />

the number of known species of anuran amphibians by 40 species (N. B. Ananjeva, pers.<br />

comm. 1999).<br />

We conclude by emphasizing the importance of basic sciences for both conservation biology<br />

and biotechnology. Herpetology as an integral part of biodiversity science needs to be<br />

46


INDRANEIL DAS & NORSHAM YAAKOB (2007)<br />

incorporated into the curricula of local schools and universities, in which students are exposed<br />

to the essentials of systematics, ecology, genetics, biogeography, anatomy and morphology,<br />

in training in field studies, acquisition and curation of biological specimens. And above all,<br />

what is needed is an encouragement of the appreciation of the great outdoors.<br />

We summarise the primary activities for enhancing herpetological conservation as discussed<br />

above:<br />

• Continue herpetofaunal inventories, particularly in species-rich zones and ecosystems,<br />

such as montane regions, lowland rainforests and offshore islands;<br />

• Examine anthropogenic effects on the herpetofauna, including the role of land-use patterns,<br />

habitat fragmentation and destruction, use of organochlorine pesticides and herbicides;<br />

• Establish and support systematic research, in addition to research on ecology, conservation<br />

biology, genetics, and related topics;<br />

• Develop identification resources tools, such as monographs, field keys and field guides<br />

to the fauna;<br />

• Promote local capacity building;<br />

• Prioritize conservation action, through regional Red Data Books, etc;<br />

• Promote conservation efforts that focus on the herpetofauna; and<br />

• Include herpetology and herpetological field techniques in the curricula of local schools<br />

and universities.<br />

ACKNOWLEDGEMENTS<br />

We dedicate this paper to Lim Boo Liat, who supported our early efforts to study the Malaysian<br />

herpetofauna, and continue to encourage and guide us. In the field, we received assistance and<br />

advice from a large number of friends, Datuk Chan Chew Lun, Lord Cranbrook, L. Lee Grismer,<br />

Alexander Haas, Robert F. Inger, Alexander Haas, Maklarin Lakim, Tzi-Ming Leong, Kelvin<br />

K. P. Lim, Peter K. L. Ng, Robert B. Stuebing, Jeet Sukumaran, Tan Heok Hui, Paul Yambun<br />

and Dennis Yong.<br />

We are also thankful to the following additional colleagues for various courtesies: Aaron<br />

Matthew Bauer, Villanova University, Villanova; Chris Austin, Lousiana, Lousiana State<br />

University, Baton Rouge; Colin John McCarthy and David Gower, The Natural History<br />

Museum, London; Robert Frederick Inger and Harold Knight Voris, Field Museum of Natural<br />

History, Chicago; the late Ernst Williams, Jim Hanken, José Rosado and Van Wallach, Museum<br />

of Comparative Zoology, Cambridge, MA; Patrick David and Ivan Ineich, Muséum National<br />

d’Histoire Naturelle, Paris; Marinus Charles Hoogmoed, Nationaal Natuurhistorisch Museum,<br />

Leiden; Ulrich Manthey, Society for Southeast Asian Herpetology, Berlin; Charles Leh Moi<br />

Ung, Sarawak Museum, Kuching; Kelvin Kok Peng Lim, Tan Heok Hui and Peter Kee Lin<br />

Ng, Raffles Museum of Biodiversity Research, National University of Singapore; Ronald Ian<br />

Crombie and George Robert Zug, National Museum of Natural History, Smithsonian Institution,<br />

Washington, D.C.; and Miguel Vences and Leobertus van Tuijl, Zoological Museum,<br />

Amsterdam.<br />

Our researches on the herpetofauna of Malaysia as well as manuscript preparation were<br />

supported by grants from Universiti Malaysia Sarawak and Forest Research Institute Malaysia.<br />

Finally, we are grateful to Kraig Adler, Aaron Bauer, Patrick David, Genevieve V. A. Gee,<br />

Lim Boo Liat and Robert Stuebing for reading and commenting on the manuscript.<br />

47


STATUS OF KNOWLEDGE OF THE MALAYSIAN HERPETOFAUNA<br />

REFERENCES<br />

AIKEN, S.R. & MOSS, M.R. 1975. Man’s impact on the tropical rainforest of Peninsular<br />

Malaysia: a review. Biological Conservation 8: 213–229.<br />

AMBU, S., KRISHNANSAMY, M., DE WITT, G. F., RAHMAN, A. & HALIM, S. 1982.<br />

Study of helminthic infection of some snakes in northern Peninsular Malaysia. Pp. 1–4 in<br />

Proceeding of IUCN/SSC snake group, First Meeting. 8–12 November 1982.<br />

APPANAH, S. 1998. Forest management. Pp. 94–95 in S. Sani (ed.) The Encyclopedia of<br />

Malaysia. Volume 1. The environment. Archipelago Press, Singapore.<br />

ANDERSSON, L. 1916. Zoological results of the Swedish zoological expeditions to Siam<br />

1911–12 and 1914. 3. Batrachians. Kungliga Svenska Vetenskapsakademiens Handlingar<br />

4 (3–4): 13–17.<br />

ANONYMOUS. 1898. Death of Mr. Alfred Hart Everett. Sarawak Gazette July 1898: 136–<br />

137.<br />

ANONYMOUS. 1983. Cobra meat in demand. Malayan Naturalist 37(2): 11.<br />

BANKS, E. 1931. Some measurements of the estuary crocodile (Crocodylus porosus) from<br />

Sarawak. Journal of the Bombay Natural History Society 33: 1086–1088.<br />

BANKS, E. 1937. The breeding of the edible turtle (Chelonia mydas). Sarawak Museum<br />

Journal 4: 523–532.<br />

BANKS, E. 1983. Reminiscence of a Curator. Sarawak Museum Journal, New Series 32: 59–<br />

60.<br />

BARTLETT, E. 1894a. Notes on the chelonians: tortoises and turtles, found in Borneo and the<br />

adjacent islands. Sarawak Gazette 24: 187–188.<br />

BARTLETT, E. 1894b. Notes on the batrachians, or frogs and toads of Borneo and the adjacent<br />

islands. Sarawak Gazette 24: 202–204.<br />

BARTLETT, E. 1895a. Notes on tortoises. No. 2. Sarawak Gazette 25: 29–30.<br />

BARTLETT, E. 1895b. Notes on tortoises. No. 3. Sarawak Gazette 25: 83–84.<br />

BARTLETT, E. 1895c. Notes on the snakes of Borneo and the adjacent islands. Sarawak<br />

Gazette 25: 160–162.<br />

BARTLETT, E. 1895d. Notes on the snakes of Borneo and the adjacent islands. Part II. Sarawak<br />

Gazette 25: 182–184.<br />

BARTLETT, E. 1895e. The crocodiles and lizards of Borneo in the Sarawak Museum, with<br />

descriptions of supposed new species, and the variation of colours in the several species<br />

during life. Journal of the Straits Branch of the Royal Asiatic Society 1895(28): 73–96.<br />

BARTLETT, E. 1896a. Notes on the snakes of Borneo and the adjacent islands. Part III.<br />

Sarawak Gazette 26: 153–157.<br />

BARTLETT, E. 1896b. Notes on tortoises. No. 4. Sarawak Gazette 26: 113.<br />

BARTLETT, E. 1896c. Notes on the snakes. Part IV. Sarawak Gazette 26: 241.<br />

BARTLETT, E. 1896d. The ethnological, zoological, and botanical note book of Sarawak.<br />

Domingo J. J. Rodrigues.for Government Printer, Kuching. 238 pp.<br />

BASTIN, J. 1986. Introduction. In: The Malay Archipelago. The land of the orang-utan and<br />

the bird of paradise. pp:vii–xxvii. A. R. Wallace (author). Oxford University Press, Kuala<br />

Lumpur.<br />

BAKER, D.B. 2001. Alfred Russel Wallace’s record of his consignments to Samuel Stevens,<br />

1854–1861. Zoologisches Mededelingen 75(16): 251–341.<br />

BECCARI, O. 1902. Nelle foreste di Borneo: viaggi e ricerche di un naturalista. Tipografia<br />

di Salvador Landi, Firenze. xvi + 667 pp, 13 pls., 4 maps. (Reprinted 1921, Fratelli Alinari<br />

Societá Anonima, Instituto di Edizioni Artistische, Firenze. xvi + 469 pp, 70 pls.; English<br />

48


INDRANEIL DAS & NORSHAM YAAKOB (2007)<br />

translation by E. H. Gigliolo, edited by F. H. H. Guillemard, 1904, Wanderings in the<br />

great forests of Borneo. Travels and researches of a naturalist in Sarawak. Archibald<br />

Constable & Co. Ltd., London. vxxiv + 424. Reprinted, 1986, 1989, Oxford University<br />

Press, Singapore).<br />

BELCHER, E. 1843. Narrative of a voyage round the world, performed in Her Majesty’s ship<br />

Sulphur, during the years 1836–1841, including details of the naval operations in China,<br />

from December 1840 to November 1841. 2 volumes. Henry Colburn, London.<br />

BERRY, P.Y. 1975. The amphibian fauna of Peninsular Malaysia. Tropical Press, Kuala<br />

Lumpur.<br />

BERRY, P.Y. & HENDRICKSON, J.R. 1963. Leptobrachium nigrops, a new pelobatid frog<br />

from the Malay Peninsula, with remarks on the genus Leptobrachium in southeast Asia.<br />

Copeia 1963(4): 643–648.<br />

BHANOTAR, R.K. & BHATNAGAR, R.K. 1976. Reptile predators of the desert locust.<br />

Journal of the Bombay Natural History Society 73: 311–313.<br />

BOULENGER, G.A. 1882. Catalogue of the Batrachia Salientia s. Ecaudata in the collection<br />

of the British Museum. Taylor & Francis, London.<br />

BOULENGER, G.A. 1887a. On new batrachians from Malacca. Annals and Magazine of<br />

Natural History Series 5, 19: 345–348.<br />

BOULENGER, G.A. 1887b. On new reptiles and batrachians from North Borneo. Annals and<br />

Magazine of Natural History, Series 5, 20: 95–97.<br />

BOULENGER, G.A. 1891. Remarks on the herpetological fauna of Mount Kina Baloo, North<br />

Borneo. Annals and Magazine of Natural History (6)7: 341–345.<br />

BOULENGER, G.A. 1892. An account of the reptiles and batrachians collected by Mr. C.<br />

Hose on Mt. Dulit, Borneo. Proceedings of the Zoological Society of London 1892: 505–<br />

508.<br />

BOULENGER, G.A. 1893. Descriptions of new reptiles and batrachians obtained in Borneo<br />

by Mr. A. Everett and Mr. C. Hose. Proceedings of the Zoological Society of London<br />

1893: 522–528.<br />

BOULENGER, G.A. 1895a. Descriptions of two new snakes of the genus Calamaria. Annals<br />

and Magazine of Natural History (6)16: 481.<br />

BOULENGER, G.A. 1895b. Descriptions of four new batrachians discovered by Mr. Charles<br />

Hose in Borneo. Annals and Magazine of Natural History (6)16: 169–171.<br />

BOULENGER, G.A. 1896a. Descriptions of two new batrachians obtained by Mr. A. Everett<br />

on Mount Kina Balu, North Borneo. Annals and Magazine of Natural History (6)17:<br />

449–450.<br />

BOULENGER, G.A. 1896b. On a new gecko from Penang. Proceedings of the Zoological<br />

Society of London 1896: 767–768.<br />

BOULENGER, G.A. 1899. Descriptions of three new reptiles and a new batrachian from<br />

Mount Kina Balu, North Borneo. Annals and Magazine of Natural History (7)4: 451–<br />

454.<br />

BOULENGER, G.A, 1900a. Descriptions of new reptiles and batrachians from Borneo.<br />

Proceedings of the Zoological Society of London 1900: 182–187.<br />

BOULENGER, G.A. 1900b. Descriptions of new batrachians and reptiles from the Larut<br />

Hills, Perak. Annals and Magazine of Natural History (32)6: 186–193.<br />

BOULENGER, G.A. 1900c. Descriptions of two new lizards from Selangor. Journal of the<br />

Bombay Natural History Society 13: 333–334.<br />

BOULENGER, G.A. 1900d. Descriptions of a new lizard from Batu Caves, Selangor. Journal<br />

of the Bombay Natural History Society 13: 335.<br />

49


STATUS OF KNOWLEDGE OF THE MALAYSIAN HERPETOFAUNA<br />

BOULENGER, G.A. 1903. Report on the batrachians and reptiles. Pp. 131–176 in Fasciculii<br />

Malayenses. Anthropological and zoological results of an expedition to Perak and the<br />

Siamese Malay States 1901–1902, undertaken by Nelson Annandale and Herbert C.<br />

Robinson. Vol. 1. Zoology. University Press, Liverpool.<br />

BOULENGER, G.A. 1905. Descriptions of a new frog of the genus Ixalus from Selangor.<br />

Journal of the Federated Malay States Museum 2(1): 1.<br />

BOULENGER, G.A. 1906. Reptiles and batrachians. Pp. 517–531 in The history of the<br />

collections contained in the Natural History Departments of the British Museum. Vol. II.<br />

Separate historical accounts of the several collections included in the Departments of<br />

Zoology. British Museum, London.<br />

BOULENGER, G.A. 1912. A vertebrate fauna of the Malay Peninsula from the Isthmus of<br />

Kra to Singapore including the adjacent islands. Reptilia and Batrachia. Taylor & Francis,<br />

London. xiii + 294 pp.<br />

BURKILL, I.H. 1927. Botanical collectors, collections and collecting places in the Malay<br />

Peninsula. A review of the work so far done towards a knowledge of the plant-geography<br />

of Malaya. The Gardens’ Bulletin 4(4&5): 112–202.<br />

BURTON, T.M. & LIKENS, G.E. 1975. Salamander populations and biomass in the Hubbard<br />

Brook Experimental Forest, New Hampshire. Copeia 1975: 541–546.<br />

BURY, R.B.,CAMPBELL, H.W. & SCOTT, N.J. 1980. Role and importance of nongame<br />

wildlife. Transactions of the North American Wildlife & Natural Resources Conference<br />

45: 197–207.<br />

BUTLER, A.L. 1902. On recent additions to the batrachian fauna of the Malay Peninsula.<br />

Proceedings of the Zoological Society of London 1902(2): 188–190.<br />

BUTLER, A.L. 1904. A list of the batrachians known to inhabit the Malay Peninsula, with<br />

some remarks on their habits, distribution, & c. Journal of the Bombay Natural History<br />

Society 15: 193–205 and 387–402.<br />

CANTOR, T.E. 1847. Catalogue of reptiles inhabiting the Malayan Peninsula and islands,<br />

collected or observed by Theodore Cantor, Esq., M.D. Bengal Medical Service. Journal<br />

of the Asiatic Society of Bengal 16: 607–656, 897–952, 1026–1078. (Reprinted 1966,<br />

A.Asher, Amsterdam, and 1981, as T.H. Canton, Catalogue of reptiles inhabiting the<br />

Asian continent. Cosmo Publications, New Delhi.)<br />

CHAN, E.H. & LIEW, H.C. 1996). Decline of the leatherback population in Terengganu,<br />

Malaysia, 1956–1995. Chelonian Conservation and Biology 2(2): 196–203.<br />

CHAN, E.H. & LIEW, H.C. 1999. Hawksbill turtles, Eretmochelys imbricata nesting on Redang<br />

Island, Terengganu, Malaysia from 1993 to 1997. Chelonian Conservation and Biology<br />

3(2): 326–329.<br />

CHAN-ARD, T., GROSSMANN, W., GUMPRECHT, A. & SCHULZ, K.D. 1999. Amphibians<br />

and reptiles of Peninsular Malaysia and Thailand: an illustrated checklist. Bushmaster<br />

Publications, Würselen. 240 pp.<br />

CLAWSON, M.E., BASKETT, T.S. & ARMBRUSTER, M.J. 1984. An approach to habitat<br />

modeling for herpetofauna. Wildlife Society Bulletin 12: 61–69.<br />

COWAN, C.F. 1968. Sir Hugh Low, G.C.M.G. (1824–1905). Journal of the Society for the<br />

Bibliography of Natural History 4(7): 327–343.<br />

COX, M.J., VAN DIJK, P.P., NABHITABHATA, J. & THIRAKHUPT, K. 1998. A photographic<br />

guide to snakes and other reptiles of Peninsular Malaysia, Singapore and Thailand. New<br />

Holland Publishers (UK) Ltd., London. 144 pp.<br />

CRANBROOK, LORD. 1986. Introduction. Pp. v–ix in O. Beccari (author) Wanderings in<br />

the great forests of Borneo. Reprinted 1993. Oxford University Press, Singapore, Oxford<br />

and New York.<br />

50


INDRANEIL DAS & NORSHAM YAAKOB (2007)<br />

CRANBROOK, EARL OF, HILLS, D.M., McCARTHY, C.J. & PRvS-JONES, R. 2005.<br />

A.R. Wallace, collector: Tracing his vertebrate specimens. Part I. Pp. 8–34 in Tuen, A.A.<br />

& Das, I. (eds) Wallace in Sarawak – 150 years later. An International Conference on<br />

Biogeography and Biodiversity. Institute of Biodiversity & Environmental Conservation,<br />

Universiti Malaysia Sarawak, Kota Samarahan.<br />

CURRY-LINDAHL, K. 1961. Obituary. Nils Gyldenstolpe. Ibis 103: 627.<br />

DALY, J.W., KANEKO, T., WILHAM, J., GARRAFFO, H.M., SPANDE, T.S., ESPINOSA,<br />

A. & DONNELLY, M.A. 2002. Bioactive alkaloids of frog skin: combinatorial<br />

bioprospecting reveals that pumiliotoxins have an arthropod source. Proceedings of the<br />

National Academy of Sciences, U.S.A. 99(22): 13996–14001.<br />

DAS, I. 2000. Herpetological contributions of Edward Bartlett (ca. 1836–1908), pioneering<br />

herpetologist in Borneo. Newsletter and Bulletin of the International Society for the History<br />

and Bibliography of Herpetology 2(1): 17–19.<br />

DAS, I. 2002. Amphibians of the Indo–Pacific region: conservation of neglected biodiversity.<br />

Pp. 47–49 in Wikramanayake, E., Dinerstein, E., Loucks, C., Olson, D.M., Morrisson, J.,<br />

Lamoreux, J., McKnight, M. & Hedao, P. (eds) Terrestrial ecoregions of the Indo–Pacific.<br />

A conservation assessment. Island Press, Washington, D.C.<br />

DAS, I. 2004a. A pocket guide: Lizards of Borneo. Natural History Publications (Borneo),<br />

Kota Kinabalu.<br />

DAS, I. 2004b. Collecting in the “Land below the Wind”: herpetological explorations of Borneo.<br />

In: Herpetological expeditions and voyages. A. M. Bauer (ed.). Bonner Zoologische<br />

Beiträge 52(2): 231–243.<br />

DAS, I. 2005. A new species of Polypedates (Amphibia: Anura: Rhacophoridae) from Gunung<br />

Murud, Sarawak (Borneo). Raffles Bulletin of Zoology 53(2): 265–270.<br />

DAS, I. 2006. A photographic guide to the snakes and other reptiles of Borneo. New Holland<br />

Publishers (UK), Ltd., London. 144 pp.<br />

DAS, I. & BAUER, A.M. 1998. Systematics and biogeography of Bornean geckos of the<br />

genus Cnemaspis Strauch, 1887 (Sauria: Gekkonidae), with the description of a new<br />

species. Raffles Bulletin of Zoology 46(1): 11–28.<br />

DAS, I. & GRISMER, L.L. 2003. Two new species of Cnemaspis Strauch, 1887 (Sauria:<br />

Gekkonidae) from the Seribuat Archipelago, Pahang and Johor States, West Malaysia.<br />

Herpetologica 59(4): 546–554.<br />

DAS, I. & HAAS, A. 2003. A new species of Kalophrynus (Anura: Microhylidae) from the<br />

highlands of north-central Borneo. Raffles Bulletin of Zoology 51(1): 109–113.<br />

DAS, I. & HAAS, A. 2005a. A new species of Rhacophorus (Anura: Rhacophoridae) from<br />

Gunung Gading, Sarawak. Raffles Bulletin of Zoology 53(2): 257–263.<br />

DAS, I. & HAAS, A. 2005b. Sources of larval identities for amphibians from Borneo.<br />

Herpetological Review 36(4): 375–382.<br />

DAS, I. & LEH, C. 2005. A legacy of Wallace: Sarawak Museum and the history of<br />

herpetological research in Sarawak. Pp 57–65 in Tuen, A.A. & Das, I. (eds) Wallace in<br />

Sarawak – 150 years later. Proceedings of an International Conference on Biogeography<br />

and Biodiversity. Institute of Biodiversity and Environmental Conservation, Universiti<br />

Malaysia Sarawak, Kota Samarahan.<br />

DAS, I. & LIM, L.J. 2000. A new species of Cyrtodactylus (Sauria: Gekkonidae) from Pulau<br />

Tioman, Malaysia. Raffles Bulletin of Zoology 48(2): 223–231.<br />

DAS, I. & LIM, K.K.P. 2001a. A new Bufo (Anura: Bufonidae) from the peat swamps of<br />

Selangor, West Malaysia. Raffles Bulletin of Zoology 49(1): 1–6.<br />

51


STATUS OF KNOWLEDGE OF THE MALAYSIAN HERPETOFAUNA<br />

DAS, I. & LIM, K.K.P. 2001b. Catalogue of herpetological types in the collection of the<br />

Raffles Museum of Biodiversity Research, National University of Singapore. Raffles<br />

Bulletin of Zoology 49(1): 7–11.<br />

DAS, I. & LIM, K.K.P. 2003. Two new species of Dibamus (Squamata: Dibamidae) from<br />

Borneo. Raffles Bulletin of Zoology 51(1): 137–141.<br />

DAS, I. & NORSHAM, Y. 2003. A new species of Dibamus (Squamata: Dibamidae) from<br />

Peninsular Malaysia. Raffles Bulletin of Zoology 51(1): 143–147.<br />

DAS, I., NORSHAM, Y. & LIM, B.L. 2004. A new species of Calluella Stoliczka, 1872<br />

(Anura: Microhylidae) from Taman Negara, Pahang State, Peninsular Malaysia. Raffles<br />

Bulletin of Zoology 52(1): 257–260.<br />

DAUGHERTY, C.H., CREE, A., HAY, J.M. & THOMPSON, M.B. 1990. Neglected taxonomy<br />

and continuing extinctions of tuatara (Sphenodon). Nature 347: 177–179.<br />

DAVENPORT, J., WONG, T.M. & EAST, J. 1992. Feeding and digestion in the omnivorous<br />

estuarine turtle Batagur baska (Gray). Herpetological Journal 2: 133–139.<br />

DAVID, P. & PAUWELS, O.S.G. 2004. A re-evaluation of the taxonomy of Macrocalamus<br />

lateralis Günther, 1864 (Serpentes, Colubridae), with the description of two new species.<br />

Raffles Bulletin of Zoology 52(2): 635–645.<br />

DENZER, W. & MANTHEY, U. 1991. A nominal checklist of the lizards inhabiting Peninsular<br />

Malaysia and Singapore. Raffles Bulletin of Zoology 39(2): 309–322.<br />

DE SILVA, G.S. 1969a. Turtle conservation in Sabah. Sabah Society Journal 5: 6–26.<br />

DE SILVA, G.S. 1969. Marine turtle conservation in Sabah. Annual Report of the Research<br />

Board Forest Department, Sabah. Pp. 124–135.<br />

DE SILVA, G.S. 1971. Marine turtles in the State of Sabah, Malaysia. IUCN New Series,<br />

Supplement Paper 31: 47–52.<br />

DE SILVA, G.S. 1978. Turtle notes (sightings of Dermochelys in Sabah waters). Borneo<br />

Research Bulletin 10(1): 23–24.<br />

DE SILVA, G.S. 1980. The status of sea turtle populations in East Malaysia and the South<br />

China Sea. Pp. 327–337 in Bjorndal, K.A. (ed.) Biology and conservation of sea turtles.<br />

Smithsonian Institution Press, Washington, D.C.<br />

DIAZ, R.E., LEONG, T.M., GRISMER, L.L. & NORSHAM, Y. 2004. A new species of<br />

Dibamus (Squamata: Dibamidae) from West Malaysia. Asiatic Herpetological Research<br />

10: 1–7.<br />

DRING, J.C.M. 1979. Amphibians and reptiles from northern Trengganu, Malaysia, with<br />

descriptions of two new geckos: Cnemaspis and Cyrtodactylus. Bulletin of the British<br />

Museum of Natural History (Zoology) 34: 181–241.<br />

DRING, J.C.M. 1983a. Some frogs from Sarawak. Amphibia-Reptilia 4: 103–115.<br />

DRING, J.C.M. 1983b. Frogs of the genus Leptobrachella (Pelobatidae). Amphibia-Reptilia<br />

4: 89–102.<br />

DRING, J.C.M. 1987. Bornean treefrogs of the genus Philautus (Rhacophoridae). Amphibia-<br />

Reptilia 8: 19–47.<br />

DUNSON, W.A. & MOLL, E.O. 1980. Osmoregulation in sea water of hatchling emydid<br />

turtles, Callagur borneoensis, from a Malaysian sea beach. Journal of Herpetology 14(1):<br />

31–36.<br />

DURRANS, B. 1993. Introduction. In: The pagan tribes of Borneo. Volume One. pp: viii–xli.<br />

C. Hose & W. McDougall (authors). Oxford University Press, Singapore. (Reprint of the<br />

original 1912 edition).<br />

ENGKAMAT, L.A., STUEBING, R.B. & VORIS, H.K. 1991. A population size estimate of<br />

the yellow-lipped sea krait, Laticauda colubrina, on Kalampunian Damit Island, Sabah,<br />

Malaysia. Copeia 1991(4): 1139–1142.<br />

52


INDRANEIL DAS & NORSHAM YAAKOB (2007)<br />

ERNST, C.H., LOVICH, J.E. & BARBOUR, R.W. 1994. Turtles of the United States and<br />

Canada. Second edition. Smithsonian Institution Press, Washington, D.C. 578 pp.<br />

ESQUE, T.C. & PETERS, E.L. 1994. Ingestion of bones, stones, and soil by desert tortoises.<br />

Pp. 105–111 in Bury, R.B & Germano, D.J. (eds.) Biology of North American tortoises.<br />

USDI National Biological Survey, Washington, D.C.<br />

FACHIN-TERÁN, A., VOGT, R.C. & GOMEZ, M.D.S. 1995. Food habits of an assemblage<br />

of five species of turtles in the Rio Guapore, Rondonia, Brazil. Journal of Herpetology<br />

29: 536–547.<br />

FIALHO, R.F. 1990. Seed dispersal by a lizard and a treefrog—effect of dispersal site on seed<br />

survivorship. Biotropica 22: 423–424.<br />

FLOWER, S.S. 1896. Notes on a collection of reptiles and batrachian made in the Malay<br />

Peninsula in 1895–96, with a list of the species recorded from that region. Proc. Zool.<br />

Soc. London 1896: 856–914.<br />

FLOWER, S.S. 1899. Notes on a second collection of batrachians made in the Malay Peninsula<br />

and Siam, from November 1896 to September 1898, with a list of the species recorded<br />

from those countries. Proc. Zool. Soc. London 1899: 600–697.<br />

FURBANK, M. 1996). Road kill predation by the long-necked turtle Chelodina longicollis<br />

(Shaw). Herpetofauna 26(1): 49–50.<br />

GANS, C. 1994. Frogs and paddy: Problems of management. Journal of the Bombay Natural<br />

History Society 91: 29–36.<br />

GRANDISON, A.G.C. 1972. The Gunong Benom Expedition 1967. 5. Reptiles and amphibians<br />

of Gunong Benom with a description of a new species of Macrocalamus. Bulletin of the<br />

British Museum (Natural History) Zoology 23(4): 45–101.<br />

GRAY, J.E. 1845. Catalogue of the specimens of lizards in the collection of the British Museum.<br />

British Museum (Natural History), London. xxviii + 289 pp.<br />

GRISMER, L.L. 2005. Tioman Archipelago. Evolution’s laboratory. Malaysian Naturalist<br />

59(2): 12–23.<br />

GRISMER, J.L., GRISMER, L.L., DAS, I., NORSHAM, Y., LIM, B.L., LEONG, T.M.,<br />

YOUMANS, T.Y. & KAISER, H. 2004c. Species diversity and a checklist of the<br />

herpetofauna of Pulau Tioman, Peninsular Malaysia, with a preliminary overview of habitat<br />

utilisation. Asiatic Herpetological Research 10: 247–279.<br />

GRISMER, J.L., LEONG, T.M. & NORSHAM, Y. 2003. Two new southeast Asian skinks of<br />

the genus Larutia and intrageneric phylogenetic relationships. Herpetologica 59(4): 552–<br />

564.<br />

GRISMER, L.L. 2006. Two new species of skinks (genus Sphenomorphus Fitzinger 1843)<br />

from the Seribuat Archipelago, West Malaysia. Herpetological Natural History 9(2): 151–<br />

162.<br />

GRISMER, L.L. & DAS, I. 2005. A new species of gekkonid lizard of the genus Cnemaspis<br />

Strauch, 1887 from Pulau Pemanggil, Johor, West Malaysia. Herpetological Natural<br />

History 10(1): 1–7.<br />

GRISMER, L.L., DAS, I. & LEONG, T.M. 2003. A new species of Gongylosoma (Squamata:<br />

Colubridae) from Pulau Tioman, West Malaysia. Herpetologica 59(4): 567–574.<br />

GRISMER, L.L., GRISMER, J.L. & YOUMANS, T.M. 2004a. A new species of Leptolalax<br />

(Anura: Megophryidae) from Pulau Tioman, West Malaysia. Asiatic Herpetological<br />

Research 10: 8–11.<br />

GRISMER, L.L., KAISER, H. & NORSHAM, Y. 2004b. A new species of reed snake of the<br />

genus Calamaria H. Boie, 1827, from Pulau Tioman, Pahang, West Malaysia. Hamadryad<br />

28(1 & 2): 1–6.<br />

53


STATUS OF KNOWLEDGE OF THE MALAYSIAN HERPETOFAUNA<br />

GRISMER, L.L. & LEONG, T.M. 2005. New species of Cyrtodactylus (Squamata: Gekkonidae)<br />

from southern Peninsular Malaysia. Journal of Herpetology 39(4): 584–591.<br />

GRISMER, L.L., NORSHAM, Y., LIM, L.B., LEONG, T.M., DAS, I., SOSA, R.A., GRISMER,<br />

J.L., CRANE, K.M., DIAZ, R.E., FIGUEROA, S.V., LEDBETTER, C.A., NEWBOLD,<br />

S.C., NEWBOLD, S.R., PATEL, C.P., CASTRO, J., ESCOBAR, III, R.A., GUERRERO,<br />

S., PINEDO, J.W., TRUJILLO, J.D. & KAISER, H. 2002a. First report on the herpetofauna<br />

of Pulau Aur, Johor, West Malaysia. Hamadryad 26(2): 350–353.<br />

GRISMER, L.L., NORSHAM, Y., LIM, L.B., LEONG, T.M., DAS, I., SOSA, R.A., GRISMER,<br />

J.L., CRANE, K.M., DIAZ, R.E., FIGUEROA, S.V., LEDBETTER, C.A., NEWBOLD,<br />

S.C., NEWBOLD, S.R., PATEL, C.P., CASTRO, J., ESCOBAR, III, R.A., GUERRERO,<br />

S., PINEDO, J.W., JONES, P.A. & KAISER, H. 2002b. Report on the herpetofauna of<br />

Pulau Tulai, Malaysia. Hamadryad 26(2): 369–371.<br />

GRISMER, L.L., YOUMANS, T.M., WOOD, P.L., JR. & GRISMER, J.L. 2006. Checklist of<br />

the herpetofauna of the Seribuat Archipelago, West Malaysia with comments on<br />

biogeography, natural history, and adaptive types. Raffles Bulletin of Zoology 54(1): 157–<br />

180.<br />

GRISMER, L.L., YOUMANS, T.M., WOOD, P.L., JR., PONCE, A., WRIGHT, S.B., JONES,<br />

B.S., JOHNSON, R., SANDERS, K.L., GOWER, D.J., NORSHAM, Y. & LIM, K.K.P.<br />

2006. Checklist of the herpetofauna of Pulau Langkawi, Malaysia, with comments on<br />

taxonomy. Hamadryad 30(1&2): 58–71.<br />

GÜNTHER, A.C.L. 1872. On the reptiles and amphibians of Borneo. Proceedings of the<br />

Zoological Society of London 1872: 586–600.<br />

GYLDENSTOLPE, N. 1916. Zoological results of the Swedish Zoological Expeditions to<br />

Siam, 1911–1912 and 1914–1915.– II. Snakes. Kungliga Svenska Vetenskapsakademiens<br />

Handlingar 55(3): 1–28.<br />

HAAS, A., HERTWEG, S. & DAS, I. 2006. Extreme tadpoles: the morphology of the fossorial<br />

megophryid larva, Leptobrachella mjobergi. Zoology 109(1): 26–42.<br />

HAILE, N.S. 1958. The snakes of Borneo, with a key to the species. Sarawak Museum Journal,<br />

New Series 8: 743–771.<br />

HAN, K.H., STUEBING, R.B. & VORIS, H.K. 1991. Population structure and reproduction<br />

in the marine snake, Lapemis hardwickii Gray, from the west coast of Sabah. Sarawak<br />

Museum Journal, New Series 42(63): 463–475.<br />

HANITSCH, R. 1900. An expedition to Mount Kinabalu, British North Borneo. Journal of<br />

the Straits Branch of the Royal Asiatic Society 34: 49–88.<br />

HANKEN, J. 1999. Why are there so many new amphibian species when amphibians are<br />

declining? Trends in Ecology and Evolution 14(1): 7–8.<br />

HARRISSON, B. 1961. Lanthanotus borneensis – habits and observations. Sarawak Museum<br />

Journal, New Series 10: 17–18.<br />

HARRISSON, B. 1962. Beobachtungen am lebenden Taubwaran Lanthanotus borneensis.<br />

Natur und Museum 92(2): 38–45.<br />

HARRISSON, T. 1951. The edible turtle (Chelonia mydas) in Borneo. 1. Breeeding season.<br />

Sarawak Museum Journal, New Series 3: 593–596.<br />

HARRISSON, T. 1954. The edible turtle (Chelonia mydas) in Borneo. 2. Copulation. Sarawak<br />

Museum Journal, New Series 6: 126–128.<br />

HARRISSON, T. 1955. The edible turtle (Chelonia mydas) in Borneo. 3. Young turtles (in<br />

captivity). Sarawak Museum Journal, New Series 6: 633–640.<br />

HARRISSON, T. 1956a. The edible turtle (Chelonia mydas) in Borneo. 4. Growing turtles<br />

and growing problems. Sarawak Museum Journal, New Series 7: 233–239.<br />

54


INDRANEIL DAS & NORSHAM YAAKOB (2007)<br />

HARRISSON, T. 1956b. The edible turtle (Chelonia mydas) in Borneo. 5. Tagging turtles<br />

(and why). Sarawak Museum Journal, New Series 7: 504–515.<br />

HARRISSON, T. 1958a. Notes on the edible turtle (Chelonia mydas). 6. Semah ceremonies,<br />

1949–1958. Sarawak Museum Journal, New Series 8: 482–486.<br />

HARRISSON, T. 1958b. Notes on the edible turtle (Chelonia mydas). 7. Long-term tagging<br />

returns, 1952–1958. Sarawak Museum Journal, New Series 8: 772–774.<br />

HARRISSON, T. 1959. Notes on the edible turtle (Chelonia mydas). 8. First tag returns outside<br />

Sarawak. Sarawak Museum Journal, New Series 9: 277–278.<br />

HARRISSON, T. 1961a. Second to none: our first Curator (and others). Sarawak Museum<br />

Journal, New Series 10: 17–29.<br />

HARRISSON, T. 1961b. Notes on the green turtle (Chelonia mydas). 9. Some new hatching<br />

observations. Sarawak Museum Journal, New Series 10: 293–299.<br />

HARRISSON, T. 1962. Notes on the green turtle (Chelonia mydas). 10. Some emergence<br />

variations. 11. West Borneo numbers, the downward trend. 12. Monthly laying cycles.<br />

Sarawak Museum Journal, New Series 10: 610–630.<br />

HARRISSON, T. 1963a. Lanthanotus borneensis: the first 30 live ones. Sarawak Museum<br />

Journal, New Series 11: 299–301.<br />

HARRISSON, T. 1963b. Notes on marine turtles. 13. Growth rate of the hawksbill. 14. Albino<br />

green turtles and sacred ones. Sarawak Museum Journal, New Series 11: 302–306.<br />

HARRISSON, T. 1964. Notes on marine turtles. 15. Sabah’s turtle islands. Sarawak Museum<br />

Journal, New Series 11: 624–627.<br />

HARRISSON, T. 1965. Notes on marine turtles. 16. Some loggerhead and hawksbill<br />

comparisons with the green turtle. Sarawak Museum Journal, New Series 12: 419–422.<br />

HARRISSON, T. 1966. Notes on marine turtles. 17. Sabah and Sarawak islands compared.<br />

Sarawak Museum Journal, New Series 14: 335–340.<br />

HARRISSON, T. 1967. Notes on marine turtles. 18. A report on the Sarawak turtle industry<br />

(1966) with recommendations for the future. Sarawak Museum Journal, New Series 15:<br />

424–436.<br />

HARRISSON, T. & HAILE, N.S. 1961a. A rare earless monitor lizard from Borneo. Nature<br />

190(4782): 1213.<br />

HARRISSON, T. & HAILE, N.S. 1961b. Notes on a living specimen of earless monitor lizard,<br />

Lanthonotus borneensis. Journal of the Ohio Herpetological Society 3(2): 13–16.<br />

HAWGOOD, B.J. 1998. Hugh Alistair Reid OBE MD: investigation and treatment of snake<br />

bite. Toxicon 36(3): 431–446.<br />

HEANEY, L.R. 1991. A synopsis of climatic and vegetational change in southeast Asia. Climate<br />

Change 19: 53–61.<br />

HEIMANN, J.M. 1997. The most offending soul alive. Tom Harrisson and his remarkable<br />

life. University of Hawai’i Press, Honolulu. 468 pp.<br />

HENDRICKSON, J.R. 1966. Observations on the fauna of Pulau Tioman and Pulau Tulai. 5.<br />

The reptiles. Bulletin of the National Museum, Singapore 34: 53–71.<br />

HIKIDA, T. 1979. (Notes on the Bornean arboreal skink, Apterygodon vittatus.) Japanese<br />

Journal of Herpetology 8: 68–69. (In Japanese.)<br />

HIKIDA, T. 1980. Lizards of Borneo. Acta Phytotaxonomica et Geobotanica 31: (1–3): 97–<br />

102. (In Japanese)<br />

HIKIDA, T. 1982. A new limbless Brachymeles (Sauria: Scincidae) from Mt. Kinabalu, North<br />

Borneo. Copeia 1982: 840–844.<br />

HIKIDA, T. 1990. Bornean gekkonid lizards of the genus Cyrtodactylus (Lacertilia:<br />

Gekkonidae) with descriptions of three new species. Japanese Journal of Herpetology<br />

13: 91–107.<br />

55


STATUS OF KNOWLEDGE OF THE MALAYSIAN HERPETOFAUNA<br />

INGER, R.F. 1954. On a collection of amphibians from Mount Kina Balu, North Borneo.<br />

Journal of the Washington Academy of Sciences 44(8): 250–251.<br />

INGER, R.F. 1956. Some amphibians from the lowlands of north Borneo. Fieldiana Zoology<br />

34(36): 389–424.<br />

INGER, R.F. 1957. A new gecko of the genus Cyrtodactylus with a key to the species from<br />

Borneo and the Philippines islands. Sarawak Museum Journal, New Series 8: 261–264.<br />

INGER, R.F. 1958a. A new toad from Sarawak. Sarawak Museum Journal, New Series 8:<br />

476–478.<br />

INGER, R.F. 1958b. Three new species related to Sphenomorphus variegatus (Peters).<br />

Fieldiana Zoology 39: 257–268.<br />

INGER, R.F. 1964. Two new species of frogs from Borneo. Fieldiana Zoology 44(20): 151–<br />

159.<br />

INGER, R.F., 1966. The systematics and zoogeography of the Amphibia of Borneo. Fieldiana<br />

Zoology 52: 1–402.<br />

INGER, R.F. 1967. A new colubrid snake of the genus Stegonotus from Borneo. Fieldiana<br />

Zoology 51(5): 77–83.<br />

INGER, R.F. 1989. Four new species of frogs from Borneo. Malayan Nature Journal 42:<br />

229–243.<br />

INGER, R.F., BOEADI & TAUFIK, A. 1996). New species of ranid frogs (Amphibia: Anura)<br />

from Central Kalimantan, Borneo. Raffles Bulletin of Zoology 44(2): 363–369.<br />

INGER, R.F. & FROGNER, K.J. 1980. New species of narrow-mouth frogs (genus Microhyla)<br />

from Borneo. Sarawak Museum Journal, New Series 27: 311–322.<br />

INGER, R.F. & GRITIS, P.A. 1983. Variation in Bornean frogs of the Amolops jerboa species<br />

group, with description of two new species. Fieldiana Zoology 19: 1–13.<br />

INGER, R.F. & HAILE, N.S. 1959. Two new frogs from Sarawak. Sarawak Museum Journal,<br />

New Series 9: 270–276.<br />

INGER, R.F. & LEVITON, A.E. 1961. A new colubrid snake of the genus Pseudorabdion<br />

from Sumatra. Fieldiana Zoology 44: 45–57.<br />

INGER, R.F. & STUEBING, R.B. 1989. Frogs of Sabah. Sabah Parks Trustees, Kota Kinabalu.<br />

133 pp.<br />

INGER, R.F. & STUEBING, R.B. 1991. A new species of frog of the genus Leptobrachella<br />

Smith (Anura: Pelobatidae) with a key to the species from Borneo. Raffles Bulletin of<br />

Zoology 39: 99–103.<br />

INGER, R.F. & STUEBING, R.B. 1994. First record of the lizard genus Pseudocalotes<br />

(Lacertilia; Agamidae) in Borneo, with description of a new species. Raffles Bulletin of<br />

Zoology 42: 961–965.<br />

INGER, R.F. & STUEBING, R.B. 1996). Two new species of frogs from southeastern Sarawak.<br />

Raffles Bulletin of Zoology 44: 543–549.<br />

INGER, R.F. & STUEBING, R.B. 1997. A field guide to the frogs of Borneo. Natural History<br />

Publications (Borneo) Sdn. Bhd., Kota Kinabalu. 205 pp.<br />

INGER, R.F., STUEBING, R.B. & TAN, F.L. 1995. New species and new records of anurans<br />

from Borneo. Raffles Bulletin of Zoology 43: 115–131.<br />

INGER, R.F. & TAN, F.L. 1996. Checklist of the frogs of Borneo. Raffles Bulletin of Zoology<br />

44(2): 551–574.<br />

INGER, R.F., TAN, F.L., LAKIM, M. & YAMBUN, P. 2001. New species of the lizard genus<br />

Sphenomorphus (Lacertilia: Scincidae), with notes on ecological and geographic<br />

distribution of species in Sabah, Malaysia. Raffles Bulletin of Zoology 49(2): 181–189.<br />

INGER, R.F., TAN, F.L. & YAMBUN, P. 2001. A new species of toad of the genus Ansonia<br />

(Anura: Bufonidae) from Borneo. Raffles Bulletin of Zoology 49(1): 35–37.<br />

56


INDRANEIL DAS & NORSHAM YAAKOB (2007)<br />

INGER, R.F. & VORIS, H.K. 2001. The biogeographical relations of the frogs and snakes of<br />

Sundaland. Journal of Biogeography 28: 863–891.<br />

IVERSON, J.B. 1982. Biomass of turtle populations: a neglected subject. Oecologia 55: 69–<br />

76.<br />

IVERSON, J.B. 1985. Lizards as seed dispersers? Journal of Herpetology 19: 292–293.<br />

IVERSON, J.B. 1992. Species richness maps of the freshwater and terrestrial turtles of the<br />

world. Smithsonian Herpetological Information Service 88: 1–18.<br />

KACZOR, S.A. & HARNETT, D.C. 1990. Gopher tortoise (Gopherus polyphemus) effects<br />

on soils and vegetation in a Florida Sandhill community. American Midland Naturalist<br />

123: 100–111.<br />

KHAN, M.K.M.K. 1964. A note on Batagur baska (the river terrapin or tuntong). Malayan<br />

Nature Journal 18: 184–189.<br />

KHAN, M.K.M.K. 1969. A preliminary study of the Water Monitor, Varanus salvator. Malayan<br />

Nature Journal 22: 64–68.<br />

KIEW, B.H. 1972. The frogs of Tasek Bera. Malayan Nature Journal 25: 130–134.<br />

KIEW, B.H. 1984a. A new species of sticky frog (Kalophrynus palmatissimus n. sp.) from<br />

Peninsular Malaysia. Malayan Nature Journal 37: 145–152.<br />

KIEW, B.H. 1984b. Rana malesiana, a new frog from the Sunda region. Malayan Nature<br />

Journal 37: 153–161.<br />

KIEW, B.H. 1984c. A new species of frog (Kalophrynus baluensis n. sp.) from Mount Kinabalu,<br />

Sabah, Malaysia. Malayan Nature Journal 38: 151–156.<br />

KIEW, B.H. 1984d. A new species of burrowing frog (Calluella flava sp. nov.) from Borneo.<br />

Malayan Nature Journal 37: 163–166.<br />

KIEW, B.H. 1984e. A new species of frog (Kalophrynus baluensis n. sp.) from Mount Kinabalu,<br />

Sabah, Malaysia. Malayan Nature Journal 38: 151–156.<br />

KIEW, B.H. 1984f. Conservation status of the Malaysian fauna. III. Amphibians. Malayan<br />

Naturalist 37(4): 6–10.<br />

KIEW, B.H. 1987. An annotated checklist of the herpetofauna of Ulu Endau, Johore, Malaysia.<br />

Malayan Nature Journal 41: 413–423.<br />

KOLMAŠ, J. 1982. Ferdinand Stoliczka (1838–1874): the life and work of the Czech explorer<br />

in India and High Asia. Wiener Studien zur Tibetologie und Buddhiskunde. Heft 9.<br />

Universitat Wien, Wien/Vienna. 58 pp.<br />

KOTTELAT, M. 1995. Systematic studies and biodiversity: the need for a pragmatic approach.<br />

Journal of Natural History 29: 565–569.<br />

LAGO, P.K. 1991. A survey of arthropod associated with gopher tortoise burrows in<br />

Mississippi. Entomological News 102: 1–13.<br />

LAIDLAW, F.F. 1900. On the frogs collected during the “Skeat Expedition” to the Malay<br />

Peninsula, 1899–1900. Proceedings of the Zoological Society of London 1900(3): 883–<br />

890.<br />

LAIDLAW, F.F. 1901a. List of a collection of snakes, crocodiles, and chelonians from the<br />

Malay Peninsula, made by members of the “Skeat Expedition,” 1899–1900. Proceedings<br />

of the Zoological Society of London 1901(2): 575–586.<br />

LAIDLAW, F.F. 1901b. On a collection of lizards the Malay Peninsula, made by members of<br />

the “Skeat Expedition,” 1899–1900. Proceedings of the Zoological Society of London<br />

1901(3): 301–311.<br />

LEH, C. 1993. Development of the Sarawak Museum 1886–1993. Sarawak Gazette 70: 16–<br />

20.<br />

LEONG, T.M. 2000. Amphibian tales. Nature Watch, Singapore 8(4): 2–8.<br />

57


STATUS OF KNOWLEDGE OF THE MALAYSIAN HERPETOFAUNA<br />

LEONG, T.M. 2002. Status of larval identities among the Peninsular Malaysian Anura.<br />

Herpetological Review 33(3): 171–174.<br />

LEONG, T.M. 2003. Larval descriptions of some poorly known tadpoles from Peninsular<br />

Malaysia (Amphibia: Anura). Raffles Bulletin of Zoology 52(2): 609–620.<br />

LEONG, T.M. & GRISMER, L.L. 2004. A new species of kukri snake, Oligodon (Colubridae),<br />

from Pulau Tioman, West Malaysia. Asiatic Herpetological Research 10: 12–16.<br />

LEONG, T.M. & LIM, B.L. 2003a. A new species of Rana (Amphibia: Anura: Ranidae) from<br />

the highlands of the Malay Peninsula, with diagnostic larval descriptions. Raffles Bulletin<br />

of Zoology 51(1): 115–122.<br />

LEONG, T.M. & LIM, K.K.P. 2003b. Herpetofaunal records from Fraser’s Hill, Peninsular<br />

Malaysia, with larval descriptions of Limnonectes nitidus and Theloderma asperum<br />

(Amphibia: Ranidae and Rhacophoridae). Raffles Bulletin of Zoology 51(1): 123–136.<br />

LEONG, T.M. & LIM, C.F. 2003c. The tadpole of Rana miopus Boulenger, 1918 from<br />

Peninsular Malaysia. Hamadryad 27(2): 175–178.<br />

LEONG, T.M., MATSUI, M., YONG, H.S. & HAMID, A.A. 2003. Revalidation of Rana<br />

laterimaculata Barbour et Noble, 1916 from the synonymy of Rana baramica Boettger,<br />

1901. Current Herpetology 22(1): 17–27.<br />

LEONG, T.M. & NORSHAM, Y. 2002. Tadpole of the Peninsular Malaysian ranid Limnonectes<br />

tweediei (Smith, 1935). Hamadryad 27(1): 78–82.<br />

LIEW, H.C. & CHAN, E.H. 2002. An analysis of tagging data on the green turtles of Redang<br />

Island, Malaysia. Pp. 135–136 in Mosier, A., Foley, A. & Brost, B. (compiled) Proceedings<br />

of the 20th Annual Symposium on Sea Turtle Biology and Conservation. NOAA Tech.<br />

Memo. NMFS–SEFSC–477.<br />

LIU, H., PLATT, S.G. & BORG, C. K. 2004. Seed dispersal by the Florida box turtle (Terrapene<br />

carolina bauri) in pine rockland forests of the lower Florida Keys, United States. Oecologia<br />

138: 539–546.<br />

LIM, B.L. 1955. Snakes collected near Kuala Lumpur. Malayan Nature Journal 9: 122–125.<br />

LIM, B.L. 1961. The role of snakes in the balance of nature. In: Nature conservation in western<br />

Malaysia, 1961. J. Wyatt-Smith & P. R. Wycherley (eds). Malayan Nature Journal 21st<br />

Anniversary Special Issue: 211–213.<br />

LIM, B.L. 1963a. Macrocalamus tweediei, a new species of reed snake from Malaya. Bulletin<br />

of the National Museum, Singapore 32: 99–102; Pl. 2.<br />

LIM, B.L. 1963b. Comments on some rare snakes. Federated Museums Journal, Singapore 8:<br />

60–64.<br />

LIM, B.L. 1979. Poisonous snakes of Peninsular Malaysia. Malayan Nature Society, Kuala<br />

Lumpur. 61 pp. Second edition 1982; Third edition 1991. vi + 74 pp.<br />

LIM, B.L. 1967. Further comments on rare snakes. Federated Museums Journal, Singapore<br />

12: 123–126.<br />

LIM, B.L. 1974. Snakes as natural predators of rats in an oil palm estate. Malayan Nature<br />

Journal 27: 114–117.<br />

LIM, B.L. & BALASINGAM, E. 1969. A collection of sea snakes from Port Swettenham,<br />

Selangor and Tumpat, Kelantan. Federation Museums Journal, New Series 14: 123–126.<br />

LIM, B.L. & DAS, I. 1999. Turtles of Borneo and Peninsular Malaysia. Natural History<br />

Publications (Borneo) Sdn Bhd., Kota Kinabalu. 151 pp.<br />

LIM, B.L. & KAMARUDIN, M.S. 1975. Notes on new locality records of some rare snakes<br />

in Peninsular Malaysia. Malayan Nature Journal 29: 23–27.<br />

LIM, B.L. & SHABRINA MOHD. SHARIF. 1998. Parasites of some reptile species. Journal<br />

of Wildlife and National Park 16: 51–55.<br />

58


INDRANEIL DAS & NORSHAM YAAKOB (2007)<br />

LIM, B.L., DE WIT, G.F. & LIM, T.W. 1977a. Extraction of raw venom from the common<br />

cobra, Naja naja kaouthia and the Malaysian pit viper, Ancistrodon rhodostoma. The<br />

Snake 9: 8–10.<br />

LIM, B.L., LING, A.E. & DE WITT, G.F. 1977b. Comparative studies on the dry weight of<br />

venoms from the Malaysian Pit Viper (Agkistrodon rhodostroma). The Snake 9: 11–13.<br />

LIM, B.L., RATNAM, L. & ANAN, S. 1990. A study on the collection of snakes from Taman<br />

Negara, Malaysia. Journal of Wildife and Parks 10: 116–134.<br />

LONGINO, J.T. 1993. Scientific naming. National Geographic Research & Explorations 9(1):<br />

80–85.<br />

LONNBERG, E. 1916. Zoological results of the Swedish Zoological Expedition to Siam,<br />

1911–1912 and 1914–1915. II. Lizards. Kungliga Svenska Vetenskapsakademiens<br />

Handlingar 55(4): 1–12.<br />

LOVICH, J.E. 1994. Biodiversity and zoogeography of non-marine turtles in southeast Asia.<br />

Pp. 380–391 in Majumdar, S.K., Brenner, F.J., Lovich, J.E., Schalles, J.F. & Miller, E.E.<br />

(eds). Biological diversity: problems and challenges. The Pennsylvania Academy of<br />

Science, Philadelphia.<br />

LOVICH, J.E. & GIBBONS, J.W. 1997. Conservation of covert species: protecting species<br />

we don’t even know. Pp. 426–429 in Abbema, J. van (ed.) Proceedings: Conservation,<br />

restoration and management of turtles and tortoises–An international conference. State<br />

University of New York, Purchase.<br />

LOW, H. 1848. Sarawak. Its inhabitants and productions being notes during a residence in<br />

that country with His Excellency Mr. Brooke. Richard Bentley, London. 416 pp.<br />

MALKMUS, R. 1992. Leptolalax pictus sp.n. (Anura: Pelobatidae) vom Mount Kinabalu/<br />

Nord-Borneo. Sauria 14(3): 3–6.<br />

MALKMUS, R. 1996. Leptobrachium gunungensis sp. nov. (Anura: Pelobatidae) vom Mount<br />

Kinabalu, Nord-Borneo. Mitteilungen aus dem Zoologischen Museum 72: 297–301.<br />

MALKMUS, R., MANTHEY, U., VOGEL, G., HOFFMANN, P. & KOSUCH, J. 2002.<br />

Amphibians & reptiles of Mount Kinabalu (North Borneo). Koeltz Scientific Books,<br />

Königstein. 424 pp.<br />

MALKMUS, R. & MATSUI, M. 1997. Megophrys kobayashii, ein neuer pelobatider Frosch<br />

vom Mount Kinabalu. Sauria 19(1): 31–37.<br />

MALKMUS, R. & RIEDE, K. 1996. Die Baumfrösche der Gattung Philautus vom Mount<br />

Kinabalu – Teil I: Überblick und die aurifasciatus-Gruppe mit Beschreibung einer neuen<br />

Art (Philautus saueri n. sp.). Sauria 18(1): 27–37.<br />

MALONEY, B.K. 1985. Man’s impact on the rainforests of West Malaysia: the palynological<br />

record. Journal of Biogeography 12: 537–558.<br />

MANAMENDRA-ARACHCHI, K. & PETHIYAGODA, R. 2005. The Sri Lankan shrubfrogs<br />

of the genus Philautus Gistel, 1848 (Ranidae: Rhacophorinae), with description of<br />

27 new species. Raffles Bulletin of Zoology Supplement 12: 163–303.<br />

MANTHEY, U. & GROSSMANN, W. 1997. Amphibien & Reptilien Südostasiens. Natur<br />

und Tier, Münster. 512 pp.<br />

MANTHEY, U. & STEIOF, C. 1998. Rhacophorus cyanopunctatus sp. n. (Anura:<br />

Rhacophoridae), ein neuer Flugfrosch von der Malaiischen Halbinsel, Sumatra und Borneo.<br />

Sauria 20(3): 37–42.<br />

MARTUSCELLI, P. 1995. Hydromedusa tectifera (South American snake-necked turtle).<br />

Predation. Herpetological Review 26: 34–35.<br />

MATSUI, M. 1983. Amphibians from Sabah. II. Acoustic characteristics of three common<br />

anuran species. Contributions of the Biology Laboratory of Kyoto University 26: 123–<br />

129.<br />

59


STATUS OF KNOWLEDGE OF THE MALAYSIAN HERPETOFAUNA<br />

MATSUI, M. 1986. Three new species of Amolops from Borneo (Amphibia: Anura, Ranidae).<br />

Copeia 1986(3): 623–630.<br />

MATSUI, M. 1996. Call characteristics and systematic relationships of a Malayan treefrog<br />

Nyctixalus pictus (Anura, Rhacophoridae). Herpetological Journal 6(2): 62–64.<br />

MATSUI, M., HIKIDA, T. & NAMBU, H. 1985. The amphibians and reptiles collected from<br />

Borneo, Malaysia. Bulletin of Toyama Science Museum 8: 151–159.<br />

MATSUI, M., YONG, H.S., ARAYA, K. & HAMID, A.A. 1996. Acoustic characteristics and<br />

systematic relationships of arboreal microhylid frogs of the genus Metaphrynella from<br />

Malaysia. Journal of Herpetology 30(3): 424–427.<br />

MEDWAY, LORD. 1976. Tom Harrisson the ornithologist, and Bornean ornithology. Borneo<br />

Research Bulletin 8(2): 69–73.<br />

MEEGASKUMBURA, M. & MANAMENDRA-ARACHCHI, K. 2005. Description of eight<br />

new species of shrub-frogs (Ranidae: Rhacophorinae: Philautus) from Sri Lanka. Raffles<br />

Bulletin of Zoology Supplement 12: 305–338.<br />

MITTERMEIER, R.A., CARR, J.L., SWINGLAND, I.R., WERNER, T.B. & MAST, R.B.<br />

1992. Conservation of amphibians and reptiles. Pp. 59–80 in Adler, K. (ed.) Herpetology:<br />

current research on the biology of amphibians and reptiles. Society for the Study of<br />

Amphibians and Reptiles, Oxford, Ohio.<br />

MJÖBERG, E. 1928. I Tropikermas villande urskogar. Bokförlaget Natur och Kultur,<br />

Stockholm. 212 pp. English translation by Barwell, A. 1930. Forest life and adventures<br />

in the Malay Archipelago. George Allen & Unwin Ltd., London. 201 pp.<br />

MOCQUARD, F. 1890. Recherches sur la faune herpétologique des Iles de Bornéo et de<br />

Palawan. Nouvelles Archives du Muséum National d’Histoire Naturelle (Série 3), 2: 115–<br />

168.<br />

MOLL, D. & JANSEN, K.P. 1995. Evidence for a role in seed dispersal by two tropical<br />

herbivorous turtles. Biotropica 27: 121–127.<br />

MOLL, E.O. 1976. West Malaysian turtles: utilisation and conservation. Herpetological Review<br />

7: 163–166.<br />

MOLL, E. O. 1978. Drumming along the Perak. Natural History 87(5): 36–43.<br />

MOLL, E.O. 1980. Natural history of the river terrapin, Batagur baska (Gray), in Malaysia<br />

(Testudines: Emydidae). Malaysian Journal of Science 6(A): 23–62.<br />

MOTLEY, J. & DILLWYN, L.L. 1855. Contributions to the natural history of Labuan and<br />

adjacent coasts of Borneo. John van Voorst, London. 62 pp., 12 pls.<br />

MYERS, N. 1988. Threatened biotas: “hotspots” in tropical forests. Environmentalist 8: 187–<br />

208.<br />

MYERS, N. 1990. The biodiversity challenge: expanded hot-spot analysis. Environmentalist<br />

10: 243–256.<br />

NADCHATRAM, M. 1979. Ectoparisites of Malayan snakes. Malayan Nature Journal 33:<br />

75–78.<br />

NG, P.K.L. 1995. Obituary. Michael Wilmer (sic) Forbes Tweedie (1907–1993). Crustaceana<br />

68(1): 111–115.<br />

NIEKISCH, M. 1986. The international trade in frogs’ legs. Traffic Bulletin 8(1): 7–8.<br />

NORHAYATI A., JULIANA, S. & LIM, B.L. 2004. A photographic guide to amphibians of<br />

Endau Rompin State Park. Forestry Department of Peninsular Malaysia, Kuala Lumpur.<br />

59 pp.<br />

NORHAYATI A., JULIANA, S. & LIM, B.L. 2005a. A pocket guide: Amphibians of Ulu<br />

Muda Forest Reserve. Forestry Department of Peninsular Malaysia, Kuala Lumpur. 120<br />

pp.<br />

60


INDRANEIL DAS & NORSHAM YAAKOB (2007)<br />

NORHAYATI, A., JULIANA, S., SHARMA, D.S.K. & ZAFIR, Z.W. 2005b. A survey of<br />

amphibians at Sungai Bebar, Pekan Forest Reserve. Pp. 149–152 in Latiff, A., Hamzah,<br />

K.A., Ahmed, N., Said, M.N.M., Nee, T.A. & Gill, S.K. (eds) Biodiversity expedition.<br />

Sungai Bebar, Pekan, Pahang. UNDP / GEF Peat Swamp Forest Project, Technical Series<br />

No. 4.<br />

NORSHAM, Y. 2003. A record of Anomochilus leonardi Smith, 1940 (Anomochilidae) from<br />

Peninsular Malaysia. Hamadryad 27(2): 285–286.<br />

NORSHAM, Y. & ABDUL, J. 2000. Terrestrial herpetofauna. Journal of Wildlife and Parks,<br />

18: 21–28.<br />

NORSHAM, Y. & LIM, B.L. 2003. A new species of mountain reed snake, Macrocalamus<br />

gentingensis, from Genting Highlands, Pahang, Peninsular Malaysia. Hamadryad 27(1):<br />

83–89.<br />

NUTTALL, G.H.F. 1927. The contributions to science of Charles Hose, Hon. Sc. D. (Cantab.)<br />

(1887–1927). Pp. 272–287 in C. Hose. Fifty years of romance and research or a junglewallah<br />

at large. Hutchinson & Co. (Publishers) Ltd., London.<br />

OHLER, A.M. & DUBOIS, A. 1999. The identity of Elachyglossa gyldenstolpei Andersson,<br />

1916 (Amphibia: Ranidae) with a discussion of some aspects of statistical support to<br />

taxonomy. Zoologica Scripta 28: 269–279.<br />

OTA, H. & HIKIDA, T. 1988. A new species of Lepidodactylus (Sauria: Gekkonidae) from<br />

Sabah, Malaysia. Copeia 1988(3): 616–621.<br />

OTA, H. & HIKIDA, T. 1989. Karyotypes of three species of the genus Draco (Agamidae:<br />

Lacertilia) from Sabah, Malaysia. Japanese Journal of Herpetology 13(1): 1–6.<br />

OTA, H. & HIKIDA, T. 1991. Taxonomic review of the lizards of the genus Calotes Cuvier<br />

1817 (Agamidae: Squamata) from Sabah, Malaysia. Tropical Zoology 4: 179–192.<br />

OTA, H. & HIKIDA, T. 1996. The second specimen of Calotes kinabaluensis de Grijs<br />

(Squamata: Agamidae) from Sabah, Malaysia, with comments on the taxonomic status of<br />

the species. Journal of Herpetology 30(2): 288–291.<br />

OTA, H., HIKIDA, T., HASEGAWA, M., LABANG, D. & NABHITABHATA, J. 1996a.<br />

Chromosomal variation in the scincid genus Mabuya and its arboreal relatives (Reptilia:<br />

Squamata). Genetica 98: 87–94.<br />

OTA, H., HIKIDA, T., KON, M. & HIDAKA, T. 1989. Unusual nest site of a scincid lizard<br />

Sphenomorphus kinabaluensis from Sabah, Malaysia. Herpetological Review 20(2): 38–<br />

39.<br />

OTA, H., HIKIDA, T., MATSUI, M. & MORI, A. 1990. Karyotype of Gekko monarchus<br />

(Squamata: Gekkonidae) from Sarawak, Malaysia. Japanese Journal of Herpetology 13(4):<br />

136–138.<br />

OTA, H., HIKIDA, T., MATSUI, M. & MORI, A. 1991. Karyotypes of two water skinks of<br />

the genus Tropidophorus (Reptilia: Squamata) from Borneo. Journal of Herpetology 25(4):<br />

488–490.<br />

OTA, H., HIKIDA, T., MATSUI, M. & MORI, A. 1992. Karyotypes of two species of the<br />

genus Cyrtodactylus (Squamata: Gekkonidae) from Sarawak, Malaysia. Caryologia 45(1):<br />

43–49.<br />

OTA, H., SENGOKU, S. & HIKIDA, T. 1996b. Two new species of Luperosaurus (Reptilia:<br />

Gekkonidae) from Borneo. Copeia 1996): 433–439.<br />

PARENT, G.H. 1992. L’utilisation des batraciens et reptiles comme bio-indicateurs. Les<br />

Naturalistes Belges 73(2): 33–63.<br />

PENDLEBURY, H.M. & CHASEN, F.N. 1932. A zoological expedition to Mt. Kinabalu,<br />

British North Borneo (1929). Journal of the Federated Malay States Museum 17: 1–38.<br />

61


STATUS OF KNOWLEDGE OF THE MALAYSIAN HERPETOFAUNA<br />

PETERS, W.C.H. 1861. Eine zweite Übersicht (vergl. Monatsberichte 1859 p. 269) der von<br />

Hrn. F. Jagor auf Malacca, Java, Borneo und den Philippinen gesammelten und dem Kgl.<br />

zoologischen Museum übersandten Schlangen. Monatsberichte der Königlich Akademie<br />

der Wissenschaften zu Berlin 1861: 683–691.<br />

PETERS, W.C.H. 1862. Präparate vor zur craniologischen Unterscheidung der<br />

Schlangengattung Elaps und über eine neue Art der Gattung Simotes, S. semicinctus.<br />

Monatsberichte der Königlich Akademie der Wissenschaften zu Berlin 1862: 635–638.<br />

PETERS, W.C.H. 1871. Über neue Reptilien aus Ostafrica und Sarawak (Borneo), vorzüglich<br />

aus der Sammlung des Hern. Marquis J. Doria zu Genua. Monatsberichte der Königlich<br />

Akademie der Wissenschaften zu Berlin 1871: 566–581.<br />

PETERS, W.C.H. 1872. Übersicht der von den Herren M. G. Doria und D. O. Beccari in<br />

Sarawak auf Borneo von 1865 bis 1868 gesammelten Amphibien. Annali del Museo Civico<br />

di Storia Naturale di Genova 3: 27–45.<br />

PETERS, W.C.H. & DORIA, G. 1878. Catalogo dei rettili e dei batraci raccolti da O. Beccari,<br />

L. M. D’Albertis e A. A. Bruijn nella sotto-regione Austro-Malese. Annali del Museo<br />

Civico di Storia Naturale di Genova 13: 323–450.<br />

PETHIYAGODA, R. & MANAMENDRA-ARACHCHI, K. 1998. Evaluation of Sri Lanka’s<br />

amphibian diversity. Occasional Papers of the Wildlife Heritage Trust of Sri Lanka 2: 1–<br />

12.<br />

PIANKA, E.R. 1986. Ecology and natural history of desert lizards. Analysis of the ecological<br />

niche and community structure. Princeton University Press, Princeton. 208 pp.<br />

PILCHER, N.J. & ALI, L. 1999. Reproductive biology of the hawksbill turtle Eretmochelys<br />

imbricata in Sabah, Malaysia. Chelonian Conservation & Biology 3(2): 330–336.<br />

PILCHER, N.J. & ALI, L. 2000. Malaysia’s Turtle Islands Park: nesting trends and their<br />

implications for management. In: Proceedings of the 18th Annual Sea Turtle Symposium.<br />

Abreu-Grobois, F.A., Briseño-Dueñas, R., Márquez, R. & Sarti, L. (Compilers). NOAA<br />

Tech. Mem. MFS–SEFSC–436: 288–289.<br />

PILCHER, N.J. & BASINTAL, P. 2000. Reproductive biology of the green turtle Chelonia<br />

mydas in Sabah, Malaysia. Asian Journal of Tropical Biology 4(1): 59–66.<br />

PILCHER, N.J. & ISMAIL, G. (eds). 2000. Sea turtles of the Indo Pacific: research,<br />

conservation and management. ASEAN Academic Press, London. 361 pp.<br />

PILCHER, N.J., ENDERBY, S., STRINGELL, T. & BATEMAN, L. 2000. Nearshore turtle<br />

hatchling distribution and predation. Pp. 151–166 in Pilcher, N.J. & Ismail, G. (eds) Sea<br />

turtles of the Indo-Pacific. ASEAN Academic Press, London.<br />

POULTON, E.B. 1916. Editor’s introduction—biographical and general. Pp. xiii–xxii in<br />

Shelford, R.W.C. (author) A Naturalist in Borneo. T. Fisher Unwin Ltd., London. 331 pp.<br />

PRIMACK, R.D. & HALL, P. 1992. Biodiversity and forest change in Malaysian Borneo.<br />

BioScience 42(11): 829–837.<br />

REID, H.A. 1968. The paradox of therapeutic defibrination. The Lancet 1968: 485–486.<br />

RHODIN, A.G.J., MITTERMEIER, R.A. & HALL, P.M. 1993. Distribution, osteology, and<br />

natural history of the Asian giant softshell turtle, Pelochelys bibroni, in Papua New Guinea.<br />

Chelonian Conservation and Biology 1: 19–30.<br />

RICK, C.M. &BOWMAN, R. 1961. Galapagos tomatoes and tortoises. Evolution 15: 407–<br />

417.<br />

RITCHIE, J. & JONG, J. 1993. Bujang Senang. Terror of Batang Lupar. Samasa Press, Kuching.<br />

134 pp.<br />

RITCHIE, J. & JONG, J. 2002. Man-eating crocodiles of Borneo. With chapters, “The natural<br />

history of crocodiles” (pp. 1–4) and “A bibliography of the crocodiles of Borneo” (pp.<br />

62


INDRANEIL DAS & NORSHAM YAAKOB (2007)<br />

112–117) by I. Das. Natural History Publications (Borneo), Sdn. Bhd., Kota Kinabalu.<br />

118 pp.<br />

ROBINSON, H.C. 1905. Further additions to the batrachian fauna of the Malay Peninsula<br />

with a list of the species at present known to occur therein. Journal of the Federated<br />

Malay States Museum 1(1): 19–24.<br />

ROSS, J.P. (ed.). 1998. Crocodiles. Status survey and conservation Action Plan. Second edition.<br />

IUCN/SSC Crocodile Specialist Group, Gland and Gainesville. 96 pp.<br />

SAINT, M. 1987. Wallace, Becarri (sic) and Bishop McDougall. Sarawak Gazette 113: 30–<br />

31.<br />

SHARMA, D.S.K. 1999. Tortoises and freshwater turtle trade and utilisation in Peninsular<br />

Malaysia. TRAFFIC Southeast Asia, Kuala Lumpur. 39 pp.<br />

SHARPE, R.B. 1898. Obituary of Everett. Ibis 1898: 627.<br />

SHELFORD, R.W.C. 1901a. A list of the reptiles of Borneo. Journal of the Straits Branch of<br />

the Royal Asiatic Society 35: 43–68.<br />

SHELFORD, R.W.C. 1901b. On two new snakes from Borneo. Annals and Magazine of Natural<br />

History 7(8): 516–517.<br />

SHELFORD, R.W.C. 1902. A list of the reptiles of Borneo – Addenda et corrigenda. Journal<br />

of the Straits Branch of the Royal Asiatic Society 38: 133–135.<br />

SHELFORD, R.W.C. 1905a. A new lizard and a new frog from Borneo. Annals and Magazine<br />

of Natural History (7)15: 208–210.<br />

SHELFORD, R.W.C. 1905b. “Wanderings in the great forests of Borneo” by Odardo Beccari.<br />

Sc. D., F.L.M.S., C.M.Z.S. etc. Sarawak Gazette July: 160–161.<br />

SHELFORD, R.W.C. 1906. A note on “flying” snakes. Proceedings of the Zoological Society<br />

of London 1906: 227–230.<br />

SHELFORD, R.W.C. 1916. A naturalist in Borneo. T. Fisher Unwin Ltd., London. 331 pp.<br />

Reprinted 1999 Natural History Publications (Borneo) Sdn. Bhd., Kota Kinabalu.<br />

SINGH, G.R. 2000. Ganges soft-shell turtle Aspideretus gangeticus predating on Nilgai<br />

Boselaphus tragocamelus in Keoladeo National Park, Bharatpus, Rajasthan. Journal of<br />

the Bombay Natural History Society 97: 285.<br />

SIOW, K.T. & MOLL, E.O. 1981. Status and conservation of estuarine and sea turtles in West<br />

Malaysian waters. Pp. 339–347 in Bjorndal, K.A. (ed.) Biology and conservation of sea<br />

turtles. Smithsonian Institution Press, Washington, D.C.<br />

SITES, J., JR. & CRANDALL, K. 1997. Testing species boundaries in biodiversity studies.<br />

Conservation Biology 11(6): 1289–1297.<br />

SKEAT, W.W. 1900. Report on Cambridge Exploring Expedition to the Malay Provinces of<br />

Lower Siam. Journal of the Anthropological Institute of Great Britain and Ireland 30:<br />

73–77.<br />

SKEAT, W.W. 1901. Appendix. List of place-names in the Siamese Malay States visited by<br />

Members of the “Skeat Expedition”. Pp. 583–586 in Laidlaw, F.F. (author) List of a<br />

collection of snakes, crocodiles, and chelonians from the Malay Peninsula, made by<br />

members of the “Skeat Expedition,” 1899–1900. Proceedings of the Zoological Society<br />

of London 1901(2): 575–586.<br />

SMITH, M.A. 1921. Two new batrachians and a new snake from Borneo and the Malay<br />

Peninsula. Journal of the Federated Malay States Museum 10: 197–199.<br />

SMITH, M.A. 1922. On a collection of reptiles and batrachians from the mountains of Pahang,<br />

Malay Peninsula. Journal of the Federated Malay States Museum 10: 263–282.<br />

SMITH, M.A. 1924. Two new lizards and a new tree frog from the Malay Peninsula. Journal<br />

of the Federated Malay States Museum 11(3 & 4): 183–186.<br />

63


STATUS OF KNOWLEDGE OF THE MALAYSIAN HERPETOFAUNA<br />

SMITH, M.A. 1925a. On a collection of reptiles and amphibians from Mt. Murud, Borneo.<br />

Sarawak Museum Journal 3(1): 5–14.<br />

SMITH, M.A. 1925b. Contribution to the herpetology of Borneo. Sarawak Museum Journal<br />

3(8): 15–34.<br />

SMITH, M.A. 1925c. A new ground-gecko (Gymnodactylus) from the Malay Peninsula.<br />

Journal of the Malay Branch of the Royal Asiatic Society 3(1): 87.<br />

SMITH, M.A. 1930. The Reptilia and Amphibia of the Malay Peninsula from the Isthmus of<br />

Kra to Singapore including the adjacent islands. Bulletin of the Raffles Museum 3: 1–149.<br />

SMITH, M.A. 1931a. The herpetology of Mt. Kinabalu, North Borneo, 13,455 ft. Bulletin of<br />

the Raffles Museum 5(1): 3–32.<br />

SMITH, M.A. 1931b. The fauna of British India, including Ceylon and Burma. Vol. I. Loricata,<br />

Testudines. (Taylor and Francis, London. 185 pp. Reprinted in 1970 by Ralph Curtis<br />

Books, Hollywood, Florida and in 1980 by Today and Tomorrow’s Publishers, Dehradun.<br />

SMITH, M.A. 1935. On a collection of reptiles and amphibians from Perak, Malay Peninsula.<br />

Bulletin of the Raffles Museum (10): 61–63.<br />

SMITH, M.A. 1940. A new snake of the genus Anomochilus from the Malay Peninsula. Annals<br />

and Magazines of Natural History Series 11, 6(35): 447–449.<br />

SMITH, M.A. 1946. Stanley Smyth Flower 1871–1946. Copeia 1946(4): 185–187.<br />

SMITH, M.A. 1957. A physician at the Court of Siam. Country Life Ltd., London. 164 pp.<br />

Reprinted 1982, 1985, 1986, Oxford University Press, Singapore, Oxford and New York.<br />

SMYTHIES, B.E. 1975. Obituary (of Tom Harrisson). Sarawak Museum Journal, New Series<br />

23: 311–312.<br />

SOUZA, F.L. & ABE, A.S. 2000. Feeding ecology, density and biomass of the freshwater<br />

turtle, Phrynops geoffroanus, inhabiting a polluted urban river in south-eastern Brazil.<br />

Journal of the Zoology 252: 437–446.<br />

SPENCER, R.J., THOMPSON, M.B. & HUME, I.D. 1998. The diet and digestive energetics<br />

of an Australian short-necked turtle, Emydura macquarii. Comparative Biochemistry and<br />

Physiology 121: 341–349.<br />

STILLER, D., LIM, B.L. & NADCHANTRAM, M. 1977. Entonyssus asiaticus Fain, 1960<br />

(Acari: Entonyssidae), a lung parasite of Malaysian snakes with notes on the immature<br />

stages. Southeast Asian Journal of Tropical Medicine and Public Health 1: 129–130.<br />

STOCKER, K. F. 1990. Medical use of snake venom proteins. CRC Press, Boston. 280 pp.<br />

STOLICZKA, F. 1870a. Observations on some Indian and Malayan Amphibia and Reptilia.<br />

Proceedings of the Asiatic Society of Bengal 1870(4): 103–108.<br />

STOLICZKA, F. 1870b. Observations on some Indian and Malayan Amphibia and Reptilia.<br />

Journal of the Asiatic Society of Bengal 39(2): 134–157.<br />

STOLICZKA, F. 1870c. Observations on some Indian and Malayan Amphibia and Reptilia.<br />

Journal of the Asiatic Society of Bengal 39(3): 159–228.<br />

STOLICZKA, F. 1873. Notes on some species of Malayan Amphibia and Reptilia. Journal of<br />

the Asiatic Society of Bengal 42(2): 111–126.<br />

STUEBING, R.B. 1985. Batang Lupar crocodiles: happy bachelors, lovesick behemoths, or<br />

nasty brutes? Malayan Naturalist 39(1/2): 43–46.<br />

STUEBING, R.B. 1991. A checklist of the snakes of Borneo. Raffles Bulletin of Zoology 39:<br />

323–362.<br />

STUEBING, R.B. 1994. A checklist of the snakes of Borneo: addenda and corrigenda. Raffles<br />

Bulletin of Zoology 42(4): 931–936.<br />

STUEBING, R.B. 1994. A new species of Cylindrophis (Serpentes: Cylindrophiidae) from<br />

Sarawak, western Borneo. Raffles Bulletin of Zoology 42: 967–973.<br />

64


INDRANEIL DAS & NORSHAM YAAKOB (2007)<br />

STUEBING, R.B. 1998. Faunal collecting in southeast Asia: fundamental need or blood sport?<br />

Raffles Bulletin of Zoology 46(1): 1–10.<br />

STEUBING, R.B., BEZUIJEN, M.R., AULIYA, M. & VORIS, H.K. 2006. The current and<br />

historic distribution of Tomistoma schlegelii (the false gharial) (Müller, 1838) (Crocodylia,<br />

Reptilia). Raffles Bulletin of Zoology 54(1): 181–197.<br />

STUEBING, R.B. & INGER, R.F. 1999. A field guide to the snakes of Borneo. Natural History<br />

Publications (Borneo) Sdn Bhd., Kota Kinabalu. 254 pp.<br />

STUEBING, R.B., ISMAIL, G. & SALLIH, K. 1985. On the possible causes of crocodile<br />

attacks in Batang Lupar, Sarawak. Report to the Faculty of Science and Natural Resources,<br />

Universiti Kebangsaan Malaysia– Sabah Campus, Kota Kinabalu. 45 pp.<br />

STUEBING, R.B. & VORIS, H.K. 1990. Relative abundance of marine snakes on the west<br />

coast of Sabah, Malaysia. Journal of Herpetology 24(2): 201–202.<br />

STUEBING, R.B. & WONG, A. 2000. A new species of frog, Philautus erythrophthalmus<br />

(Rhacophoridae) from southwestern Sabah, Malaysia. Raffles Bulletin of Zoology 48:<br />

293–296.<br />

SUKUMARAN, J. 2002a. Frogs and toads in Malaysia. Tam Tam (February–March 2002): 4–<br />

15.<br />

SUKUMARAN, J. 2002b. Snaking out. The fear factor. Malaysian Naturalist 56(2): 22–25.<br />

SUKUMARAN, J. 2003. The amphibian fauna of a forested area in Temengor, Perak, Malaysia,<br />

with the first record of Philautus parvulus (Boulenger, 1893) in the Malay Peninsula.<br />

Hamadryad 27(1): 1–10.<br />

SUKUMARAN, J., NORSHAM, Y. & YONG, D. 2006. The herpetofauna of the southeast<br />

Pahang peat swamp forest. Hamadryad 30(1&2): 74–90.<br />

TAN, S.G., NG, W.K., JOSEPH, J. & CHAN, E.H. 2000. Genetic variation in hawksbill turtle<br />

(Eretmochelys imbricata) from Malaysia using RAPD markers. Pp. 261–266 in Shariff,<br />

M., Yusoff, F.M., Gopinath, N., Ibrahim, H.M. & Nik Mustapha, R.A. (eds) Towards<br />

sustainable management of the Straits of Malacca. MASDEC, Universiti Putra Malaysia,<br />

Serdang, Malaysia.<br />

TENISON, W.P.C. 1959. Dr. Malcolm Arthur Smith, F.L.S., F.Z.S. British Journal of<br />

Herpetology 2(8): 136–137.<br />

THORBJARNARSON, J. 1992. Crocodiles: an Action Plan for their conservation. IUCN,<br />

Gland. 136 pp.<br />

TWEEDIE, M.W.F. 1949. Reptiles of the Kelabit Plateau. Sarawak Museum Journal 5: 154–<br />

155.<br />

TWEEDIE, M.W.F. 1953. The snakes of Malaya. Government Printing Office, Singapore.<br />

139 pp. Second edition, 1961. 143 pp.; third edition, 1983. Singapore National Printers<br />

(Pte) Ltd., Singapore. 167 pp.<br />

TWEEDIE, M.W.F. & HARRISON, J.L. 1970. Malayan animal life. Third edition. Longmans,<br />

Green and Co., London and Longman Malaysia Bhd., Kuala Lumpur. Note: Reprinted<br />

1977, 1981 and 1988. 237 pp.<br />

VARELA, R.O. & BUCHER, E.H. 2002. Seed dispersal by Chelonoidis chilensis in the Chaco<br />

dry woodland of Argentina. Journal of Herpetology 36: 137–140.<br />

VARGHESE, G. & TONAPI, G.T. 1986. Observations on the identity of some Indian freshwater<br />

turtles and their feeding habits. Biological Conservation 37: 87–92.<br />

VOGEL, G., DAVID, P. & PAUWELS, O.S.G. 2004. A review of morphological variation in<br />

Trimeresurus popeiorum (Serpentes: Viperidae: Crotalinae), with the description of two<br />

new species. Zootaxa 727: 1–63.<br />

VOGT, R.C. & GUZMAN-GUZMAN, S. 1988. Food partitioning in a Neotropical freshwater<br />

turtle community. Copeia 1988: 37–47.<br />

65


STATUS OF KNOWLEDGE OF THE MALAYSIAN HERPETOFAUNA<br />

VORIS, H.K. 1964. Notes on the sea snakes of Sabah. Sabah Society Journal 2(3): 138–141.<br />

VORIS, H.K. 1985. Population size estimates for a marine snake (Enhydrina schistosa) in<br />

Malaysia. Copeia 1985(4): 955–961.<br />

VORIS, H.K. & KARNS, D.R. 1996. Habitat utilization, movements, and activity patterns of<br />

Enhydris plumbea (Serpentes: Homalopsinae) in a rice paddy wetland in Borneo.<br />

Herpetological Natural History 4(2): 111–126.<br />

WAKE, D.B., ZWEIFEL, R.G., DESSAUER, H.C., PIANKA, E.R., RABB, G.B., RUIBAL,<br />

R., WRIGHT, J.W. & ZUG, G.R. 1975. Report of the Committee of Resources in<br />

Herpetology. Copeia 1975: 391–404.<br />

WALLACE, A.R. 1869. The Malay Archipelago: the land of the orangutan and the bird of<br />

paradise. Macmillan and Co., London. 638 pp. Reprinted several times.<br />

WHEELER, O.D. 1995. Systematics, the scientific basis for inventories of biodiversity.<br />

Biodiversity & Conservation 4: 476–489.<br />

WHITAKER, R. & ADVANI, R. 1983. Preliminary field study on snakes as agents of<br />

management of rodent populations. Indian Forester 109: 417–419.<br />

WHITEHEAD, J. 1893. The exploration of Mount Kina Balu. Gurney & Jackson, London.<br />

317 pp. Reprinted 1991, Yayasan Sabah, Kota Kinabalu, 317 pp., and 1992, with an<br />

introduction by Bernard Harrison, Graham Brash Publishers, Singapore.<br />

WHITTEN, T. 1996. Field guides: useful tools in environmental planning and management.<br />

Environmental Department Dissemination Notes 51: 1–4.<br />

WILSON, J.G. 2000. The forgotten naturalist. In search of Alfred Russel Wallace. Arcadia<br />

Scholarly Publishing Pty Ltd, Kew, Victoria. 263 pp.<br />

WITZ, B.W., WILSON, D.S. & PALMER, M.D. 1991. Distribution of Gopherus polyphemus<br />

and its vertebrate symbionts in three burrow categories. American Midland Naturalist<br />

126: 152–158.<br />

YONG, H.S. 1977. Rediscovery of Rhacophorus robinsoni, an Asian-frog in Peninsular<br />

Malaysia. Malayan Nature Journal 30(1): 59–61.<br />

YONG, H.S. 1998. Reptiles and amphibians. Pp. 62 in Yong, H.S. (ed.) The Encyclopedia<br />

Malaysia. Volume 3. Animals. Archipelago Press, Singapore.<br />

YONG, H.S., NG, C.K. & ISMAIL, R. 1988. Conquest of the land: direct development in a<br />

Malaysian Philautus tree frog. Nature Malaysiana 13(4): 5–7.<br />

YOUMANS, T.M. & GRISMER, L.L. 2006. A new species of Cyrtodactylus (Reptilia:<br />

Squamata: Gekkonidae) from the Seribuat Archipelago, West Malaysia. Hepertological<br />

Natural History 10(1): 61–70.<br />

66


INDRANEIL DAS & NORSHAM YAAKOB (2007)<br />

APPENDIX 1<br />

Checklist of Amphibian Species of Malaysia<br />

Peninsular Sabah Sarawak<br />

Malaysia<br />

Bufonidae<br />

Ansonia albomaculata Inger 1960<br />

•<br />

Ansonia anotis Inger Tan & Yambun 2001<br />

•<br />

Ansonia fuliginea (Mocquard 1890)<br />

•<br />

Ansonia guibei Inger 1966<br />

•<br />

Ansonia hanitschi Inger 1960 • •<br />

Ansonia leptopus (Günther 1872) • •<br />

Ansonia longidigita Inger 1960 • •<br />

Ansonia malayanus Inger 1960<br />

•<br />

Ansonia minuta Inger 1960<br />

•<br />

Ansonia penangensis Stoliczka 1870<br />

•<br />

Ansonia platysoma Inger 1960 • •<br />

Ansonia spinulifer (Mocquard 1890) • •<br />

Ansonia tiomanicus Hendrickson 1966<br />

•<br />

Ansonia torrentis Dring 1984<br />

•<br />

Bufo asper Gravenhorst 1829 • • •<br />

Bufo divergens Peters 1871 • •<br />

Bufo juxtasper Inger 1964 • •<br />

Bufo kumquat Das & Lim 2001<br />

•<br />

Bufo macrotis Boulenger 1887<br />

•<br />

Bufo melanostictus Schneider 1799 • • •<br />

Bufo parvus Boulenger 1887<br />

•<br />

Bufo quadriporcatus Boulenger 1887 • • •<br />

Leptophryne borbonica (Tschudi 1839) • • •<br />

Pedostibes everetti (Boulenger 1896)<br />

•<br />

Pedostibes hosii (Boulenger 1892) • • •<br />

Pedostibes maculatus (Mocquard 1890)<br />

•<br />

Pedostibes rugosus Inger 1958 • •<br />

Pelophryne api Dring 1984<br />

•<br />

Pelophryne exigua (Boettger 1901)<br />

•<br />

Pelophryne guentheri (Boulenger 1882)<br />

•<br />

Pelophryne macrotis (Boulenger 1895)<br />

•<br />

Pelophryne misera (Mocquard 1890)<br />

•<br />

Pelophryne rhopophilus Inger & Stuebing 1996<br />

•<br />

Pelophryne signata (Boulenger 1895) • •<br />

Pseudobufo subasper Tschudi 1839<br />

•<br />

Megophryidae<br />

Leptobrachella baluensis Smith 1931 • •<br />

Leptobrachella brevicrus Dring 1984<br />

•<br />

Leptobrachella mjobergi Smith 1925<br />

•<br />

Leptobrachella palmata Inger & Stuebing 1991<br />

•<br />

Leptobrachella parva Dring 1984 • •<br />

Leptobrachella sarasinae Dring 1984<br />

•<br />

67


STATUS OF KNOWLEDGE OF THE MALAYSIAN HERPETOFAUNA<br />

Leptobrachium abbotti (Cochran 1926) • •<br />

Leptobrachium gunungense Malkmus 1996<br />

•<br />

Leptobrachium hendricksoni Taylor 1962 • •<br />

Leptobrachium montanum Fischer 1885 • •<br />

Leptobrachium nigrops Berry & Hendrickson 1963 • •<br />

Leptobrachium smithi Matsui et al. 1998<br />

•<br />

Leptolalax arayai Matsui 1997<br />

•<br />

Leptolalax dringi Dubois 1987 • •<br />

Leptolalax gracilis (Günther 1872)<br />

•<br />

Leptolalax hamidi Matsui 1997<br />

•<br />

Leptolalax heteropus Boulenger 1900<br />

•<br />

Leptolalax kajangensis Grismer et al. 2004<br />

•<br />

Leptolalax maurus Inger et al.1997<br />

•<br />

Leptolalax pelodytoides (Boulenger 1893)<br />

•<br />

Leptolalax pictus Malkmus 1992<br />

•<br />

Megophrys baluensis (Boulenger 1899)<br />

•<br />

Megophrys edwardinae Inger 1989 • •<br />

Megophrys kobayashii Malkmus & Matsui 1997<br />

•<br />

Megophrys nasuta (Schlegel 1858) • • •<br />

Xenophrys aceras (Boulenger 1903)<br />

•<br />

Xenophrys dringi (Inger, Stuebing & Tan 1995)<br />

•<br />

Xenophrys longipes (Boulenger 1885)<br />

•<br />

Microhylidae<br />

Calluella brooksi (Boulenger 1904)<br />

•<br />

Calluella flava Kiew 1984<br />

•<br />

Calluella guttulata (Blyth 1856)<br />

•<br />

Calluella minuta Das & Norsham 2004<br />

•<br />

Calluella smithi (Barbour & Noble 1916) • •<br />

Chaperina fusca Mocquard 1892 • • •<br />

Gastrophrynoides borneensis (Boulenger 1890)<br />

•<br />

Kalophrynus baluensis Kiew 1984<br />

•<br />

Kalophrynus eok Das & Haas 2003<br />

•<br />

Kalophrynus heterochirus Boulenger 1900 • •<br />

Kalophrynus intermedius Inger 1966<br />

•<br />

Kalophrynus nubicolus Dring 1984<br />

•<br />

Kalophrynus palmatissimus Kiew 1984<br />

•<br />

Kalophrynus pleurostigma Tschudi 1838 • • •<br />

Kalophrynus punctatus Peters 1871<br />

•<br />

Kalophrynus robinsoni Smith 1922<br />

•<br />

Kalophrynus subterrestris Inger 1966 • •<br />

Kaloula baleata (Müller 1836) • • •<br />

Kaloula pulchra Gray 1831 • •<br />

Metaphrynella pollicaris (Boulenger 1890)<br />

•<br />

Metaphrynella sundana (Peters 1867) • •<br />

Microhyla annectans Boulenger 1900<br />

•<br />

Microhyla berdmorei (Blyth 1856) • • •<br />

Microhyla borneensis Parker 1926 • •<br />

Microhyla butleri Boulenger 1900<br />

•<br />

Microhyla fissipes Boulenger 1884<br />

•<br />

Microhyla heymonsi Vogt 1911<br />

•<br />

Microhyla maculifera Inger 1989<br />

•<br />

Microhyla palmipes Boulenger 1897<br />

•<br />

68


INDRANEIL DAS & NORSHAM YAAKOB (2007)<br />

Microhyla perparva Inger & Frogner 1979 • •<br />

Microhyla petrigena Inger & Frogner 1979 • •<br />

Microhyla superciliaris Parker 1928<br />

•<br />

Micryletta inornata (Boulenger 1890)<br />

•<br />

Phrynella pulchra Boulenger 1887<br />

•<br />

Ranidae<br />

Amolops larutensis (Boulenger 1899)<br />

•<br />

Fejerarya cancrivora (Gravenhorst 1829) • • •<br />

Fejervarya limnocharis (Gravenhorst 1829) • • •<br />

Fejervarya raja (Smith 1930)<br />

•<br />

*Hoplobatrachus chinensis (Osbeck 1765)<br />

•<br />

Huia cavitympanum (Boulenger 1893) • •<br />

Ingerana baluensis (Boulenger 1896) • •<br />

Ingerana tenasserimensis (Sclater 1892)<br />

•<br />

Limnonectes blythi (Boulenger 1920)<br />

•<br />

Limnonectes finchi (Inger 1966)<br />

•<br />

Limnonectes ibanorum (Inger 1964)<br />

•<br />

Limnonectes ingeri (Kiew 1978) • •<br />

Limnonectes kenepaiensis (Inger 1966)<br />

•<br />

Limnonectes kuhlii (Tschudi 1838) • • •<br />

Limnonectes laticeps (Boulenger 1882) • •<br />

Limnonectes leporinus (Andersson 1923) • •<br />

Limnonectes macrognathus (Boulenger 1917) •<br />

Limnonectes malesianus (Kiew 1984) • •<br />

Limnonectes nitidus (Smedley 1931)<br />

•<br />

Limnonectes palavanensis (Boulenger 1894) • •<br />

Limnonectes paramacrodon (Inger 1966) • •<br />

Limnonectes pileatus (Boulenger 1916)<br />

•<br />

Limnonectes plicatellus (Stoliczka 1873)<br />

•<br />

Limnonectes tweediei (Smith 1935)<br />

•<br />

Meristogenys amoropalmus (Matsui 1986) • •<br />

Meristogenys jerboa (Günther 1872)<br />

•<br />

Meristogenys kinabaluensis (Inger 1966) • •<br />

Meristogenys macrophthalmus (Matsui 1986)<br />

•<br />

Meristogenys orphocnemis (Matsui 1986)<br />

•<br />

Meristogenys phaeomerus (Inger & Gritis 1983)<br />

•<br />

Meristogenys poecilus (Inger & Gritis 1983)<br />

•<br />

Meristogenys whiteheadi (Boulenger 1887)<br />

•<br />

Occidozyga baluensis (Boulenger 1896) • •<br />

Occidozyga laevis (Günther 1858) • • •<br />

Occidozyga lima (Gravenhorst 1829)<br />

•<br />

Rana banjarana Leong & Lim 2003<br />

•<br />

Rana baramica Boettger 1901 • • •<br />

Rana erythraea (Schlegel 1837) • • •<br />

Rana glandulosa Boulenger 1882 • • •<br />

Rana hosii Boulenger 1891 • • •<br />

Rana laterimaculata Barbour & Noble 1916 • •<br />

Rana luctuosa (Peters 1871) • • •<br />

Rana miopus Boulenger 1918<br />

•<br />

Rana nicobariensis (Stoliczka 1870) • • •<br />

Rana nigrovittata (Blyth 1856)<br />

•<br />

Rana picturata Boulenger 1920 • •<br />

69


STATUS OF KNOWLEDGE OF THE MALAYSIAN HERPETOFAUNA<br />

Rana raniceps (Peters 1871) • • •<br />

Rana signata (Günther 1872) • • •<br />

Staurois guttatus (Günther 1859) • •<br />

Staurois latopalmatus (Boulenger 1887) • •<br />

Staurois tuberilinguis Boulenger 1918 • •<br />

Taylorana hascheana (Stoliczka 1870)<br />

•<br />

Rhacophoridae<br />

Chirixalus nongkhorensis (Cochran 1927)<br />

•<br />

Nyctixalus pictus (Peters 1871) • • •<br />

Philautus acutus Dring 1987<br />

•<br />

Philautus amoeanus Smith 1931<br />

•<br />

Philautus aurantium Inger 1989<br />

•<br />

Philautus bunitus Inger et al. 1995<br />

•<br />

Philautus disgregus Inger 1989<br />

•<br />

Philautus erythropththalmus Stuebing & Wong 2000<br />

•<br />

Philautus gunungensis Malkmus & Riede 1996<br />

•<br />

Philautus hosii (Boulenger 1895) • •<br />

Philautus ingeri Dring 1987 • •<br />

Philautus kerangae Dring 1987<br />

•<br />

Philautus longicrus (Boulenger 1894) • •<br />

Philautus mjobergi Smith 1925 • •<br />

Philautus parvulus (Boulenger 1893)<br />

•<br />

Philautus petersi (Boulenger 1900) • • •<br />

Philautus refugii Inger & Stuebing 1996<br />

•<br />

Philautus saueri Malkmus & Reide 1996<br />

•<br />

Philautus tectus Dring 1987 • •<br />

Philautus umbra Dring 1987<br />

•<br />

Philautus vermiculatus (Boulenger 1900)<br />

•<br />

Polypedates chlorophthalmus Das 2005<br />

•<br />

Polypedates colletti (Boulenger 1890) • • •<br />

Polypedates leucomystax Gravenhorst 1829 • • •<br />

Polypedates macrotis (Boulenger 1894) • • •<br />

Polypedates otilophus Boulenger 1893 • •<br />

Rhacophorus angulirostris Ahl 1927 • •<br />

Rhacophorus appendiculatus (Günther 1859) • • •<br />

Rhacophorus baluensis Inger 1954 • •<br />

Rhacophorus bipunctatus Ahl 1927<br />

•<br />

Rhacophorus cyanopunctatus Manthey & Steioff 1998 • • •<br />

Rhacophorus dulitensis Boulenger 1892 • •<br />

Rhacophorus everetti Boulenger 1894 • •<br />

Rhacophorus fasciatus Boulenger 1895<br />

•<br />

Rhacophorus gadingensis Das & Haas 2005<br />

•<br />

Rhacophorus gauni Inger 1966 • •<br />

Rhacophorus harrissoni Inger & Haile 1959 • • •<br />

Rhacophorus kajau Dring 1984 • •<br />

Rhacophorus nigropalmatus Boulenger 1895 • •<br />

Rhacophorus pardalis Günther 1858 • • •<br />

Rhacophorus prominanus Smith 1924<br />

•<br />

Rhacophorus reinwardtii (Schlegel 1840) • • •<br />

Rhacophorus robinsoni Boulenger 1903<br />

•<br />

Rhacophorus rufipes Inger 1966 • •<br />

Rhacophorus tunkui Kiew 1987<br />

•<br />

70


INDRANEIL DAS & NORSHAM YAAKOB (2007)<br />

Theloderma asper (Boulenger 1886)<br />

•<br />

Theloderma horridum (Boulenger 1903) • •<br />

Theloderma leprosa (Tschudi 1838)<br />

•<br />

Ichthyophiidae<br />

Caudacaecilia asplenia (Taylor 1965)<br />

Caudacaecilia larutensis (Taylor 1960)<br />

Caudacaecilia nigroflava (Taylor 1960)<br />

Ichthyophis biangularis Taylor 1965<br />

Ichthyophis dulitensis Taylor 1960<br />

Ichthyophis monochrous Bleeker 1858<br />

Ichthyophis singaporensis Taylor 1960<br />

* introduced species.<br />

Checklist of 15 April 2006.<br />

•<br />

•<br />

•<br />

•<br />

•<br />

•<br />

•<br />

71


STATUS OF KNOWLEDGE OF THE MALAYSIAN HERPETOFAUNA<br />

Checklist of Reptile Species of Malaysia<br />

APPENDIX II<br />

Peninsular Sabah Sarawak<br />

Malaysia<br />

Acrochordidae<br />

Acrochordus granulatus (Schneider 1799) • • •<br />

Acrochordus javanicus Hornstedt 1787 • •<br />

Anomochilidae<br />

Anomochilus leonardi Smith 1940 • •<br />

Anomochilus weberi van Lidth de Jeude 1890<br />

•<br />

Boidae<br />

Python breitensteini Steindachner 1881 • •<br />

Python brongersmai Stull 1938<br />

•<br />

Python molurus (Linnaeus 1758)<br />

•<br />

Python reticulatus (Schneider 1801) • • •<br />

Colubridae<br />

Ahaetulla fasciolata (Fischer 1885) • •<br />

Ahaetulla mycterizans (Linnaeus 1758)<br />

•<br />

Ahaetulla prasina (Boie 1827) • • •<br />

Amphiesma flavifrons (Boulenger 1887) • •<br />

Amphiesma frenatum (Dunn 1923)<br />

•<br />

Amphiesma inas (Laidlaw 1901)<br />

•<br />

Amphiesma petersii (Boulenger 1893) • • •<br />

Amphiesma sanguineum (Smedley 1931)<br />

•<br />

Amphiesma saravacense (Günther 1872) • • •<br />

Aplopeltura boa (Boie 1828) • • •<br />

Asthenodipsas laevis (Boie 1827) • • •<br />

Asthenodipsas malaccanus Peters 1864 • • •<br />

Bitia hydroides Gray 1842<br />

•<br />

Boiga cyanea (Duméril et al. 1854)<br />

•<br />

Boiga cynodon (Boie 1827) • • •<br />

Boiga dendrophila (Boie 1827) • • •<br />

Boiga drapiezii (Boie 1827) • • •<br />

Boiga jaspidea (Duméril et al. 1854) • • •<br />

Boiga multomaculata (Boie 1827)<br />

•<br />

Boiga nigriceps (Günther 1863) • • •<br />

Calamaria albiventer (Gray 1835)<br />

•<br />

Calamaria bicolor Duméril et al. 1854 • •<br />

Calamaria borneensis (Bleeker 1860) • •<br />

Calamaria everetti Boulenger 1893 • •<br />

Calamaria gervaisii Duméril et al. 1854<br />

•<br />

Calamaria grabowskyi Fischer 1885 • •<br />

Calamaria gracillima Günther 1872<br />

•<br />

Calamaria griswoldi Loveridge 1938<br />

•<br />

Calamaria hilleniuisi Inger & Marx 1965 • •<br />

72


INDRANEIL DAS & NORSHAM YAAKOB (2007)<br />

Calamaria ingeri Grismer et al. 2004<br />

•<br />

Calamaria lateralis Mocquard 1890<br />

•<br />

Calamaria leucogaster Bleeker 1860 • •<br />

Calamaria lovii Boulenger 1887 • • •<br />

Calamaria lumbricoidea Boie 1827 • • •<br />

Calamaria melanota Jan 1862<br />

•<br />

Calamaria modesta Duméril et al. 1854<br />

•<br />

Calamaria pavimentata Duméril et al. 1854<br />

•<br />

Calamaria prakkei van Lidth de Jeude 1893<br />

•<br />

Calamaria schlegeli Duméril et al. 1854 • • •<br />

Calamaria schmidti Marx & Inger 1955<br />

•<br />

Calamaria suluensis Taylor 1922 • •<br />

Calamaria virgulata Boie 1827 • •<br />

Cantoria violacea Girard 1857<br />

•<br />

Cerberus rynchops (Schneider 1799) • • •<br />

Chrysopelea ornata (Shaw 1802)<br />

•<br />

Chrysopelea paradisi Boie 1827 • • •<br />

Chrysopelea pelias (Linnaeus 1758) • • •<br />

Coelognathus erythrurus (Duméril et al. 1854)<br />

•<br />

Coelognathus flavolineatus (Schlegel 1837) • • •<br />

Coelognathus radiatus (Boie 1827)<br />

•<br />

Collorhabdium williamsoni Smedley 1931<br />

•<br />

Dendrelaphis caudolineatus (Gray 1834) • • •<br />

Dendrelaphis cyanochloris (Wall 1921)<br />

•<br />

Dendrelaphis formosus (Boie 1827) • • •<br />

Dendrelaphis pictus (Gmelin 1789) • • •<br />

Dendrelaphis striatus (Cohn 1905) • •<br />

Dryocalamus subannulatus (Duméril et al. 1854) • •<br />

Dryocalamus tristrigatus (Günther 1858) • •<br />

Dryophiops rubescens (Gray 1834) • • •<br />

Elaphe prasina (Blyth 1854)<br />

•<br />

Elapoidis fuscus Boie 1827<br />

•<br />

Enhydris alternans (Reuss 1834)<br />

•<br />

Enhydris bocourti (Jan 1865)<br />

•<br />

Enhydris doriae (Peters 1871) • •<br />

Enhydris enhydris (Schneider 1799) • •<br />

Enhydris indica (Gray 1842)<br />

•<br />

Enhydris pahangensis Tweedie 1946<br />

•<br />

Enhydris plumbea (Boie 1827) • •<br />

Enhydris punctata (Gray 1849)<br />

•<br />

Fordonia leucobalia (Schlegel 1837) • •<br />

Gerarda prevostiana (Eydoux & Gervais 1837) •<br />

Gongylosoma balodeirum (Boie 1827) • • •<br />

Gongylosoma longicauda (Peters 1871) • • •<br />

Gongylosoma mukutense Grismer et al. 2003<br />

•<br />

Gonyophis margaritatus (Peters 1871) • • •<br />

Gonyosoma oxycephalum (Boie 1827) • • •<br />

Homalopsis buccata (Linnaeus 1758) • • •<br />

Hydrablabes periops (Günther 1872) • •<br />

Hydrablabes praefrontalis (Mocquard 1890)<br />

•<br />

Lepturophis borneensis Boulenger 1900 • • •<br />

Liopeltis tricolor (Schlegel 1837) • • •<br />

Lycodon albofuscus (Duméril et al. 1854) • • •<br />

73


STATUS OF KNOWLEDGE OF THE MALAYSIAN HERPETOFAUNA<br />

Lycodon butleri Boulenger 1900<br />

•<br />

Lycodon capucinus Boie 1827 • •<br />

Lycodon effraenis Cantor 1847 • •<br />

Lycodon laoensis Günther 1864<br />

•<br />

Lycodon subcinctus Boie 1827 • • •<br />

Macrocalamus chanardi David & Pauwels 2004 •<br />

Macrocalamus gentingensis Norsham & Lim 2003 •<br />

Macrocalamus jasoni Grandison 1972<br />

•<br />

Macrocalamus lateralis Günther 1864<br />

•<br />

Macrocalamus schulzi Vogel & David 1999<br />

•<br />

Macrocalamus smithi David & Pauwels, 2004 •<br />

Macrocalamus tweediei Lim 1963<br />

•<br />

Macrocalamus vogeli David & Pauwels 2004<br />

•<br />

Macropisthodon flaviceps (Duméril et al. 1854) • •<br />

Macropisthodon rhodomelas (Boie 1827) • • •<br />

Oligodon annulifer Boulenger 1893<br />

•<br />

Oligodon booliati Leong & Grismer 2004<br />

•<br />

Oligodon cf. cinereus (Günther 1864)<br />

•<br />

Oligodon everetti Boulenger 1893<br />

•<br />

Oligodon meyerinkii (Steindachner 1891)<br />

•<br />

Oligodon octolineatus (Schneider 1801) • • •<br />

Oligodon purpurascens (Schlegel 1837) • • •<br />

Oligodon semicinctus (Peters 1862) ? ?<br />

Oligodon subcarinatus (Günther 1872) • •<br />

Oligodon vertebralis (Günther 1865)<br />

•<br />

Opisthotropis typica (Mocquard 1890)<br />

•<br />

Oreocalamus hanitschi Boulenger 1899 • • •<br />

Oreophis porphyraceus (Cantor 1839)<br />

•<br />

Orthriophis taeniurus (Cope 1861) • • •<br />

Pareas carinatus (Boie 1828) • •<br />

Pareas macularius Blyth in: Theobald 1868<br />

•<br />

Pareas margaritophorus Jan in: Bocourt 1866 •<br />

Pareas nuchalis (Boulenger 1900) • •<br />

Pareas vertebralis (Boulenger 1890) • •<br />

Psammodynastes pictus Günther 1858 • • •<br />

Psammodynastes pulverulentus (Boie 1827) • • •<br />

Pseudorabdion albonuchalis (Günther 1896) • •<br />

Pseudorabdion collaris (Mocquard 1892) • •<br />

Pseudorabdion longiceps (Cantor 1847) • •<br />

Pseudorabdion saravacensis (Shelford 1901)<br />

•<br />

Pseudoxenodon baramensis (Smith 1921)<br />

•<br />

Pseudoxenodon macrops (Blyth 1855)<br />

•<br />

Ptyas carinata (Günther 1858) • • •<br />

Ptyas fusca (Günther 1858) • • •<br />

Ptyas korros (Schlegel 1837) • •<br />

Ptyas mucosa (Linnaeus 1758)<br />

•<br />

Rhabdophis chrysargos (Schlegel 1837) • • •<br />

Rhabdophis conspicillatus (Günther 1872) • • •<br />

Rhabdophis murudensis (Smith 1925) • •<br />

Rhabdophis subminiatus (Schlegel 1837)<br />

•<br />

Sibynophis collaris (Gray 1853)<br />

•<br />

Sibynophis geminatus (Boie 1826)<br />

•<br />

Sibynophis melanocephalus (Gray 1835) • • •<br />

74


INDRANEIL DAS & NORSHAM YAAKOB (2007)<br />

Stegonotus borneensis Boulenger 1899<br />

•<br />

Stoliczkia borneensis Boulenger 1899 • •<br />

Xenelaphis ellipsifer Boulenger 1900 • • •<br />

Xenelaphis hexagonotus (Cantor 1847) • • •<br />

Xenochrophis flavipunctatus (Hallowell 1860)<br />

•<br />

Xenochrophis maculatus (Edeling 1864) • •<br />

Xenochrophis trianguligerus (Boie 1827) • • •<br />

Xenochrophis vittatus (Linnaeus 1758)<br />

•<br />

Xenodermus javanicus Reinhardt 1836 • • •<br />

Cylindrophiidae<br />

Cylindrophis engkariensis Stuebing 1994<br />

•<br />

Cylindrophis lineatus Blanford 1881<br />

•<br />

Cylindrophis ruffus (Laurenti 1768) • •<br />

Elapidae<br />

Bungarus candidus (Linnaeus 1758)<br />

•<br />

Bungarus fasciatus (Schneider 1801) • • •<br />

Bungarus flaviceps Reinhardt 1843 • • •<br />

Calliophis bivirgata (Boie 1827) • • •<br />

Calliophis gracilis Gray 1835<br />

•<br />

Calliophis intestinalis (Laurenti 1768) • • •<br />

Calliophis maculiceps (Günther 1858)<br />

•<br />

Naja kaouthia Lesson 1831<br />

•<br />

Naja sumatrana Müller 1887 • • •<br />

Ophiophagus hannah (Cantor 1836) • • •<br />

Hydrophiidae<br />

Aipysurus eydouxii (Gray 1849) • •<br />

Astrotia stokesii (Gray in: Stokes 1846)<br />

•<br />

Enhydrina schistosa (Daudin 1803) • • •<br />

Hydrophis brookii Günther 1872 • •<br />

Hydrophis caerulescens (Shaw 1802) • • •<br />

Hydrophis cyanocinctus (Daudin 1803) • • •<br />

Hydrophis fasciatus (Schneider 1799) • • •<br />

Hydrophis gracilis (Shaw 1802) • ? ?<br />

Hydrophis klossi Boulenger 1912 • •<br />

Hydrophis melanosoma Günther 1864 • •<br />

Hydrophis ornatus (Gray 1842) • •<br />

Hydrophis spiralis (Shaw 1802) • • •<br />

Hydrophis torquatus Günther 1864<br />

•<br />

Kerilia jerdoni Gray 1849 • •<br />

Kolpophis annandalei Laidlaw 1901<br />

•<br />

Lapemis curtus Shaw 1802 • • •<br />

Laticauda colubrina (Schneider 1799) • • •<br />

Laticauda laticaudata (Linnaeus 1758)<br />

•<br />

Pelamis platyura (Linnaeus 1766) • • •<br />

Praescutata viperina (Schmidt 1852) • •<br />

Thalassophis anomalus Schmidt 1852 • • •<br />

Typhlopidae<br />

Ramphotyphlops albiceps (Boulenger 1898)<br />

•<br />

Ramphotyphlops braminus (Daudin 1803) • • •<br />

75


STATUS OF KNOWLEDGE OF THE MALAYSIAN HERPETOFAUNA<br />

Ramphotyphlops lineatus (Schlegel 1839) • • •<br />

Ramphotyphlops olivaceus (Gray 1845)<br />

•<br />

Typhlops muelleri Schlegel 1839<br />

•<br />

Viperidae<br />

Calloselasma rhodostoma (Boie 1827)<br />

•<br />

Cryptelytrops purpureomaculatus (Gray 1832) •<br />

Garthius chaseni (Smith 1931)<br />

•<br />

Ovophis convictus (Stoliczka 1870)<br />

•<br />

Parias hageni (van Lidth de Jeude 1886)<br />

•<br />

Parias malcolmi (Loveridge 1938)<br />

•<br />

Parias sumatranus (Boie 1827) • • •<br />

Popeia fucata (Vogel, David & Pauwels 2004) •<br />

Popeia nebularis (Vogel, David & Pauwels, 2004) •<br />

Popeia sabahi (Regenass & Kramer 1981) • •<br />

Trimeresurus borneensis (Peters 1871) • • •<br />

Tropidolaemus wagleri (Boie 1827) • • •<br />

Xenopeltidae<br />

Xenopeltis unicolor Reinwardt 1827 • • •<br />

Xenophidiidae<br />

Xenophidion acanthognathus Günther & Manthey 1995<br />

Xenophidion schaeferi Günther & Manthey 1995<br />

•<br />

•<br />

Agamidae<br />

Acanthosaura armata (Hardwicke & Gray 1827) •<br />

Acanthosaura crucigera Boulenger 1885<br />

•<br />

Aphaniotis fusca (Peters 1864) • •<br />

Aphaniotis ornata (van Lidth de Jeude 1893)<br />

•<br />

Bronchocela cristatella (Kuhl 1820) • • •<br />

Calotes emma Gray 1845<br />

•<br />

Calotes versicolor (Daudin 1802)<br />

•<br />

Complicitus nigrigularis (Ota & Hikida 1991)<br />

•<br />

Draco blanfordii Boulenger 1885<br />

•<br />

Draco cornutus Günther 1864 • •<br />

Draco cristatellus Günther 1872 • • •<br />

Draco fimbriatus Kuhl 1820 • • •<br />

Draco haematopogon Boie in: Gray 1831 • • •<br />

Draco maculatus (Gray 1845)<br />

•<br />

Draco maximus Boulenger 1893 • • •<br />

Draco melanopogon Boulenger 1887 • • •<br />

Draco obscurus Boulenger 1887 • • •<br />

Draco quinquefasciatus Hardwicke & Gray 1827 • • •<br />

Draco sumatranus Schlegel 1844 • • •<br />

Gonocephalus belli (Duméril & Bibron 1837) •<br />

Gonocephalus bornensis (Schlegel 1848) • •<br />

Gonocephalus chamaeleontinus (Laurenti 1768) •<br />

Gonocephalus doriae (Peters 1871) • •<br />

Gonocephalus grandis (Gray 1845) • • •<br />

Gonocephalus liogaster (Günther 1872) • •<br />

Gonocephalus mjobergi Smith 1925<br />

•<br />

Gonocephalus robinsoni Boulenger 1908<br />

•<br />

76


INDRANEIL DAS & NORSHAM YAAKOB (2007)<br />

Harpesaurus borneensis (Mertens 1924)<br />

•<br />

Hypsicalotes kinabaluensis (de Grijs 1937)<br />

•<br />

Phoxophrys borneensis Inger 1960 • •<br />

Phoxophrys cephalum (Mocquard 1890) • •<br />

Phoxophrys nigrilabris (Peters 1864)<br />

•<br />

Phoxophrys spiniceps Smith 1925 • •<br />

Pseudocalotes dringi Hallermann & Böhme 2000 •<br />

Pseudocalotes flavigula (Smith 1924)<br />

•<br />

Pseudocalotes larutensis Hallerman & McGuire 2001 •<br />

Pseudocalotes sarawacensis Inger & Stuebing 1994<br />

•<br />

Anguidae<br />

Ophisaurus buettikoferi van Lidth de Jeude 1905 • •<br />

Eublepharidae<br />

Aeluroscalabotes felinus (Günther 1864) • • •<br />

Dibamidae<br />

Dibamus booliati Das & Norsham 2003<br />

Dibamus ingeri Das & Lim 2003<br />

Dibamus leucurus (Bleeker 1860)<br />

Dibamus tiomanensis Diaz et al. 2004<br />

Dibamus vorisi Das & Lim 2003<br />

•<br />

•<br />

•<br />

•<br />

•<br />

Gekkonidae<br />

Cnemaspis affinis (Stoliczka 1870)<br />

•<br />

Cnemaspis argus Dring 1979<br />

•<br />

Cnemaspis baueri Das & Grismer 2003<br />

•<br />

Cnemaspis dringi Das & Bauer 1998<br />

•<br />

Cnemaspis flavolineata (Nicholls 1949)<br />

•<br />

Cnemaspis kendallii (Gray 1845) • •<br />

Cnemaspis kumpoli Taylor 1963<br />

•<br />

Cnemaspis limi Das & Grismer 2003<br />

•<br />

Cnemaspis nigridia (Smith 1925)<br />

•<br />

Cosymbotus craspedotus (Mocquard 1890) • • •<br />

Cosymbotus platyurus (Schneider 1792) • • •<br />

Cyrtodactylus aurensis Grismer 2005<br />

•<br />

Cyrtodactylus baluensis (Mocquard 1890) • •<br />

Cyrtodactylus brevipalmatus (Smith 1923)<br />

•<br />

Cyrtodactylus cavernicolus Inger & King 1961<br />

•<br />

Cyrtodactylus consobrinus (Peters 1871) • • •<br />

Cyrtodactylus elok Dring 1979<br />

•<br />

Cyrtodactylus ingeri Hikida 1990<br />

•<br />

Cyrtodactylus malayanus (De Rooij 1915)<br />

•<br />

Cyrtodactylus matsuii Hikida 1990<br />

•<br />

Cyrtodactylus peguensis (Boulenger 1893)<br />

•<br />

Cyrtodactylus pubisulcus Inger 1957 • •<br />

Cyrtodactylus pulchellus Gray 1827<br />

•<br />

Cyrtodactylus quadrivirgatus Taylor 1962 • •<br />

Cyrtodactylus semenanjungensis Grismer & Leong 2005 •<br />

Cyrtodactylus seribuatensis Youmans & Grismer 2005 •<br />

Cyrtodactylus sworderi (Smith 1925)<br />

•<br />

Cyrtodactylus tiomanensis Das & Lim 2000<br />

•<br />

77


STATUS OF KNOWLEDGE OF THE MALAYSIAN HERPETOFAUNA<br />

Cyrtodactylus yoshii Hikida 1990<br />

•<br />

Gehyra butleri Boulenger 1900<br />

•<br />

Gehyra mutilata (Wiegmann 1834) • • •<br />

Gekko gecko Linnaeus 1758 • • ?<br />

Gekko monarchus (Duméril & Bibron 1836) • • •<br />

Gekko smithii (Gray 1842) • • •<br />

Hemidactylus brookii Gray 1845 • •<br />

Hemidactylus frenatus Duméril & Bibron 1836 • • •<br />

Hemidactylus garnotii Duméril & Bibron 1836<br />

•<br />

Hemiphyllodactylus harterti (Werner 1900)<br />

•<br />

Hemiphyllodactylus typus Bleeker 1860 • • •<br />

Lepidodactylus lugubris (Duméril & Bibron 1836)<br />

•<br />

Lepidodactylus ranauensis Ota & Hikida 1988<br />

•<br />

Luperosaurus browni Russell 1979 • •<br />

Ptychozoon horsfieldii (Gray 1827) • •<br />

Ptychozoon kuhli Stejneger 1902 • • •<br />

Ptychozoon lionotum Annandale 1905<br />

•<br />

Ptychozoon rhacophorus (Boulenger 1899)<br />

•<br />

Lacertidae<br />

Takydromus sexlineatus Daudin 1802 • •<br />

Lanthanotidae<br />

Lanthanotus borneensis Steindachner 1877<br />

•<br />

Scincidae<br />

Apterygodon vittatum Edeling 1864 • •<br />

Brachymeles apus Hikida 1982 • •<br />

Dasia grisea (Gray 1845) • •<br />

Dasia olivacea Gray 1839 • • •<br />

Dasia semicincta (Peters 1867)<br />

•<br />

Emoia atrocostata (Lesson 1830) • • •<br />

Emoia caeruleocauda (De Vis 1892)<br />

•<br />

Lamprolepis nieuwenhuisii (van Lidth de Jeude 1905) • •<br />

Lamprolepis vyneri (Shelford 1905)<br />

•<br />

Larutia larutensis (Boulenger 1900)<br />

•<br />

Larutia miodactyla (Boulenger 1903)<br />

•<br />

Larutia puehensis Grismer et al. 2003<br />

•<br />

Larutia seribuatensis Grismer et al. 2003<br />

•<br />

Larutia trifasciata (Tweedie 1940)<br />

•<br />

Lipinia nitens (Peters 1871)<br />

•<br />

Lipinia surda (Boulenger 1900)<br />

•<br />

Lipinia vittigera (Boulenger 1894) • • •<br />

Lygosoma albopunctata Gray 1846<br />

•<br />

Lygosoma bampfyldei Bartlett 1895 • • •<br />

Lygosoma bowringii (Günther 1864) • • •<br />

Lygosoma quadrupes (Linnaeus 1766)<br />

•<br />

Mabuya indeprensa (Brown & Alcala 1980)<br />

•<br />

Mabuya longicauda (Hallowell 1856)<br />

•<br />

Mabuya macularia (Blyth 1853)<br />

•<br />

Mabuya multifasciata (Kuhl 1820) • • •<br />

Mabuya rudis Boulenger 1887 • •<br />

Mabuya rugifera (Stoliczka 1870) • • •<br />

78


INDRANEIL DAS & NORSHAM YAAKOB (2007)<br />

Sphenomorphus aesculeticola Inger et al. 2002<br />

•<br />

Sphenomorphus alfredi (Boulenger 1898)<br />

•<br />

Sphenomorphus anomalopus (Boulenger 1890) •<br />

Sphenomorphus butleri (Boulenger 1912)<br />

•<br />

Sphenomorphus cameronicus Smith 1924<br />

•<br />

Sphenomorphus cophias (Boulenger 1908)<br />

•<br />

Sphenomorphus crassa Inger et al. 2002<br />

•<br />

Sphenomorphus cyanolaemus Inger & Hosmer 1965 • •<br />

Sphenomorphus haasi Inger & Hosmer 1965 • •<br />

Sphenomorphus hallieri (van Lidth de Jeude 1905)<br />

•<br />

Sphenomorphus indicus (Gray 1853)<br />

•<br />

Sphenomorphus ishaki Grismer 2006<br />

•<br />

Sphenomorphus kinabaluensis (Bartlett 1895)<br />

•<br />

Sphenomorphus maculatus (Blyth 1845)<br />

•<br />

Sphenomorphus maculicollus Bacon 1967 • •<br />

Sphenomorphus malayanus (Doria 1888)<br />

•<br />

Sphenomorphus multisquamatus Inger 1958 • •<br />

Sphenomorphus murudensis Smith 1925<br />

•<br />

Sphenomorphus praesignis (Boulenger 1900)<br />

•<br />

Sphenomorphus sabanus Inger 1958<br />

•<br />

Sphenomorphus sanctus (Duméril & Bibron 1839) •<br />

Sphenomorphus scotophilus (Boulenger 1900) •<br />

Sphenomorphus shelfordi (Boulenger 1900)<br />

•<br />

Sphenomorphus sibuensis Grismer 2006<br />

•<br />

Sphenomorphus stellatus (Boulenger 1900) • •?<br />

Sphenomorphus tanahtinggi Inger et al. 2002<br />

•<br />

Sphenomorphus tenuiculum (Mocquard 1890)<br />

•<br />

Sphenomorphus tersus (Smith 1916)<br />

•<br />

Tropidophorus beccarii Peters 1871 • •<br />

Tropidophorus brookei (Gray 1845) • •<br />

Tropidophorus micropus an Lidth de Jeude 1905<br />

•<br />

Tropidophorus mocquardii Boulenger 1894<br />

•<br />

Tropidophorus perplexus Barbour 1921<br />

•<br />

Uromastycidae<br />

Leiolepis belliana (Hardwicke & Gray 1827)<br />

Leiolepis triploida Peters 1971<br />

•<br />

•<br />

Varanidae<br />

Varanus dumerilii (Schlegel 1839) • • •<br />

Varanus nebulosus (Gray 1831)<br />

•<br />

Varanus rudicollis Gray 1845 • • •<br />

Varanus salvator (Laurenti 1768) • • •<br />

Crocodylidae<br />

Crocodylus porosus Schneider 1801 • • •<br />

Crocodylus raninus Müller & Schlegel 1844<br />

•<br />

Crocodylus siamensis Schneider 1801<br />

•?<br />

Tomistoma schlegelii (Müller 1838) • • •<br />

Dermochelyidae<br />

Dermochelys coriacea (Vandelli 1761) • • •<br />

79


STATUS OF KNOWLEDGE OF THE MALAYSIAN HERPETOFAUNA<br />

Cheloniidae<br />

Caretta caretta (Linnaeus 1758)<br />

•?<br />

Chelonia mydas (Linnaeus 1758) • •<br />

Eretmochelys imbricata (Linnaeus 1766) • •<br />

Lepidochelys olivacea (Eschscholtz 1829)<br />

•<br />

Trionychidae<br />

Amyda cartilaginea (Boddaert 1770) • • •<br />

Chitra chitra Nutphand 1979<br />

•<br />

Dogania subplana (Geoffroy Saint-Hillaire 1809) • • •<br />

Pelochelys cantorii Gray 1864 • •<br />

*Pelodiscus sinensis (Wiegmann 1834) • •<br />

Geoemydidae<br />

Batagur baska (Gray 1831)<br />

•<br />

Callagur borneoensis (Schlegel & Müller 1844) • •<br />

Cuora amboinensis (Daudin 1801) • • •<br />

Cyclemys dentata (Gray 1831) • •<br />

Cyclemys oldhami Gray 1863<br />

Heosemys annandalei (Boulenger 1903)<br />

•<br />

Heosemys grandis (Gray 1860)<br />

•<br />

Heosemys spinosa (Gray 1831) • •<br />

Malayemys macrocephala (Gray 1859)<br />

•<br />

Notochelys platynota (Gray 1834) • • •<br />

Orlitia borneensis Gray 1873 • •<br />

Siebenrockiella crassicollis (Gray 1831) • •<br />

Emydidae<br />

*Trachemys scripta (Schoepff 1792) • • •<br />

Testudinidae<br />

Indotestudo elongata (Blyth 1853)<br />

•<br />

Manouria emys (Schlegel & Müller in: Temminck 1844) • • •<br />

Manouria impressa (Günther 1882)<br />

•<br />

* refers to introduced species.<br />

Checklist of 15 April 2006.<br />

80


INDRANEIL DAS & NORSHAM YAAKOB (2007)<br />

APPENDIX III<br />

Websites Relevant to Malaysian Herpetology<br />

1. Amphibian Species of the World (Second Edition) by D. R. Frost, American Museum of Natural<br />

History (www.research.amnh.org/herpetology/amphibia/index/html)<br />

2. Reptile Species of the World by P. Uetz, European Molecular Biology Laboratory (www.emblheidelberg.de-uetz/db-info/related.html).<br />

3. Frogs of the Malay Peninsula by J. Sukumaran, University of Kansas (www.frogweb.org)<br />

4. Lizards of Borneo by I. Das & G. Ismail, Universiti Malaysia Sarawak (www.arbec.com.my/lizards.)<br />

5. Turtles and Crocodiles of Borneo by I. Das, Universiti Malaysia Sarawak (www.arbec.com.my/<br />

crocodilesturtles)<br />

6. Amphibia Web, University of California (http://www.amphibiaweb.org)<br />

7. Amphibia Tree (http://texas.amphibiatree.org)<br />

8. HerpNET (http://herpnet.org)<br />

9. Aquatic Snakes of Southeast Asia by Harold Voris, Field Museum of Natural History (http://<br />

www.fieldmuseum.org/aquaticsnakes)<br />

10. Bibliomania by Breck Bartholomew (http://www.herplit.com). Includes a database of approximately<br />

50,000 citations.<br />

81


A. AHMAD & A.R. KHAIRUL-ADHA (2007)<br />

STATUS OF BIOLOGICAL DIVERSITY IN MALAYSIA &<br />

THREAT ASSESSMENT OF PLANT SPECIES IN MALAYSIA<br />

STATE OF KNOWLEDGE ON FRESHWATER<br />

FISHES OF MALAYSIA<br />

1<br />

A. Ahmad & 2 A.R. Khairul-Adha<br />

ABSTRACT<br />

Freshwater fishes of Malaysia are diverse and inhabit a great variety of habitats ranging from<br />

small torrential streams to estuarine, highly acidic ecosystems and alkaline waters. Several<br />

species are endemic. Currently, there are about 280 species of freshwater fishes in Peninsular<br />

Malaysia, with more than 100 and 200 species reported from Sabah and Sarawak, respectively.<br />

The figures for Sabah and Sarawak are believed to be underestimates as the two states are<br />

poorly inventoried. In Peninsular Malaysia research on freshwater fishes is already established<br />

while in Sabah and Sarawak, the research is actively picking up in pace. Unlike Sabah, the<br />

fishes of Sarawak have never been the subject of any major research endeavor. Focus was<br />

given to major rivers in the state and many isolated and inland water bodies were left unexplored.<br />

In general, the fish diversity reported from Peninsular Malaysia reflects the peninsula’s close<br />

similarity with mainland Asiatic icthyofauna and the Sundaic component. The lack of research<br />

coordination, funding and local variations in regulation hamper efforts to bring together all<br />

collections into one repository centre. This issue requires urgent attention.<br />

INTRODUCTION<br />

Land development has altered the landscape as well as the aquatic ecosystems in many parts<br />

of Malaysia. Conversion of an intact forest has resulted in a loss of fish habitats in the country.<br />

These losses are almost always permanent and recovery, if taking place, will probably take<br />

many years and even so, does not restore the original diversity. Freshwater fishes of Malaysia<br />

are diverse and interesting but the knowledge is rather unsatisfactory and varies greatly in<br />

Peninsular Malaysia, Sabah and Sarawak.<br />

Freshwater fishes inhabit a great variety of habitats ranging from small torrential streams to<br />

estuarine habitats, with several species flourishing in highly acidic ecosystems of peat swamps<br />

and acid-water freshwater swamps. There are some species that thrive in both acidic and<br />

alkaline waters. Several species are endemic and their distribution are restricted to small areas,<br />

1<br />

Freshwater Ecosystem Research Unit (UPEAT), Department of Biological Sciences, Faculty of Science and<br />

Technology, University College of Science and Technology Malaysia (KUSTEM), 21030 Kuala Terengganu,<br />

Terengganu; amirrudin@kustem.edu.my<br />

2<br />

Faculty of Resources Science & Technology, Universiti Malaysia Sarawak, Dept. of Aquatic Sciences, 94300 Kota<br />

Samarahan, Sarawak; akhairul@frst.unimas.my<br />

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STATE OF KNOWLEDGE ON FRESHWATER FISHES OF MALAYSIA<br />

or confined to a particular drainage system, or if widely distributed, confined to an island or to<br />

a few localities.<br />

The diversity of freshwater fishes in Peninsular Malaysia reflects a close similarity with<br />

mainland Asiatic icthyofauna and others are from Sundaic origin. These overlaps have been<br />

recognized by many researchers (e.g., Mohsin & Ambak 1983, Zakaria-Ismail, 1994). In<br />

Malaysia, there are various institutions engaged in the study of freshwater fish diversity.<br />

However, much of the research is driven on individual basis, rather than on a collective or<br />

collaborative effort, and this leads to a loss in information when focus and funding change<br />

directions. The lack of research coordination and local variation in enforcement hamper efforts<br />

to bring together all known specimens freshwater fishes of Malaysia into one holding institution.<br />

The objective of this paper is to present the state of knowledge on the freshwater fish diversity<br />

in Malaysia. This information is gathered from past and recent publications. The need for a<br />

repository center is briefly discussed here. Brief information about the specialists and people<br />

working in the conservation and management of freshwater fishes as well as the possibilities<br />

for international collaboration are highlighted.<br />

FRESHWATER FISHES OF PENINSULAR MALAYSIA<br />

Freshwater fishes of Peninsular Malaysia have been receiving attention since 1800s. However,<br />

post-1990s may be regarded as the period where studies on the freshwater fishes are at its<br />

peak. Numerous works were published, particularly for Peninsular Malaysia (for details account<br />

of references, see Lim & Tan 2002). For the past 15 years, research on the freshwater fishes<br />

in Peninsular Malaysia has increased steadily and many new species and new records were<br />

reported. These were made possible by the surveys and inventories conducted in areas<br />

previously inaccessible and areas that were believed to harbor a lower diversity.<br />

As of 2002, at least 278 species are recognized as native with at least 24 species introduced<br />

(Lim & Tan 2002). This number, at present, is around 290. Since 1990, 50 more native species<br />

have been added to the list and more than half are new to science (Lim & Tan 2002). To date,<br />

Peninsular Malaysia has probably one of the most extensively studied ichthyofauna diversity<br />

in the Southeast Asia region. This is due to the easy access to various inland habitats. Mohsin<br />

& Ambak (1983)’s publication on the diversity of freshwater fishes of Peninsular Malaysia is<br />

very extensive and considered a “classic” but, typically, it contains numerous nomenclature<br />

errors. In 1989, M. Zakaria-Ismail completed his doctorate on the systematics, zoogeography<br />

and conservation of freshwater fishes of Peninsular Malaysia (Zakaria-Ismail 1989). In his<br />

dissertation, he listed many species as new records. This list is now no longer the most updated<br />

checklist and furthermore, his dissertation is not widely available. Many new species have<br />

been subsequently added to the list, arising from inventories done at other areas such as the<br />

North Selangor Peat Swamp Forest (NSPSF) (Ng et al. 1992). The inventories, which began<br />

in 1989, resulted in the discovery and documentation of 65 species of fish. Following this,<br />

several other reports on the freshwater fish diversity are being prepared (Ahmad & Lim in<br />

prep). The species diversity in Peninsular Malaysia may not exceed 300 unless major taxonomic<br />

revisions on certain groups are dealt with, supplemented with the use of molecular approaches.<br />

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A. AHMAD & A.R. KHAIRUL-ADHA (2007)<br />

FRESHWATER FISHES OF SABAH AND SARAWAK<br />

Sabah and Sarawak has perhaps over 100 and 200 species, respectively. It is difficult to<br />

provide a close estimate of the diversity as many studies are still in progress or about to begin.<br />

Therefore, the figures currently available for Sabah and Sarawak are poor estimates. The two<br />

states are believed to harbor more than what we currently know of their ichthyofauna diversity.<br />

This low number merely reflects the lack of inventory studies. For Sabah, Chin (1990) listed<br />

the number of freshwater fish species ca. 155, including 12 exotic species. Martin-Smith &<br />

Tan (1998) acknowledged that the true number of freshwater fishes in Sabah is probably<br />

much higher.<br />

Sabah is probably better known for its freshwater fish diversity based on the work of Robert<br />

F. Inger & P. K. Chin, the Freshwater Fishes of North Borneo (1962) and a subsequent<br />

supplementary chapter in 1990 (Inger & Chin 1990). Apart from this, there were no other<br />

major taxonomical studies/revisions nor were there many comprehensive collections made—<br />

much of the research in the state were ecological in approach. Specialist collections at localized<br />

areas however, yielded interesting results (Chin & Samat 1992, Chin & Samat 1995). Work<br />

by Martin-Smith & Tan (1998) has significantly contributed to the understanding of<br />

ichthyofauna in eastern Sabah. Two new species of the genus Gastromyzon had been described<br />

recently (Tan & Martin-Smith 1998).<br />

Unlike Sabah, the freshwater fishes of Sarawak have never been the subject of any major<br />

research endeavor. Scattered studies were conducted mainly on documenting the fish fauna<br />

that were affected by development as part of the requirement of Environmental Impact<br />

Assessment (EIA). Again, focus was given to major rivers in the state and many isolated and<br />

inland water bodies were left unexplored. Watson & Balon (1984) conducted a survey along<br />

the Baram River but much of the associated taxonomic work was ignored. The listing of<br />

species that occurred in the River drainage, including those that occurred in Brunei, can be<br />

found in Kottelat & Lim (1995). This listing is probably the only major publication for the<br />

state of Sarawak. Several new species including a Rasbora, a freshwater puffer fish and an<br />

anabantoids fish had been described in the last decade from the state.<br />

AREAS WITH KNOWN DIVERSITY<br />

Previous studies on the freshwater fishes of Peninsular Malaysia were mainly conducted at<br />

Taman Negara (King Edward’s National Park) (Zakaria-Ismail 1984, Tan & Hamzah 1990).<br />

Following this, at least four major rivers were surveyed and among them, only Sungai Pahang<br />

can be regarded as being thoroughly surveyed (Khan et al. 1996) and the fish collection properly<br />

catalogued and identified to the taxon level!<br />

Fish survey along a tributary of Sungai Terengganu was made prior to the construction of the<br />

Kenyir hydroelectric dam more than two decades ago. Cramphorn (1983) visited several sites<br />

and the materials collected might be available elsewhere. The fish diversity along Sungai<br />

Perak and Sungai Kelantan have been documented by T.I. Kvernevik but these are not complete.<br />

A major gap is recognized and a more thorough survey is urgently required.<br />

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STATE OF KNOWLEDGE ON FRESHWATER FISHES OF MALAYSIA<br />

As for Tasik Bera and Tasik Chini, the ichthyofauna diversity and it contributions to fisheries<br />

have been documented by Mizuno & Furtado (1982). This was followed ten years later by the<br />

study on the swamp ichthyofauna of North Selangor Peat Swamp Forest (NSPSF) (Ng et al.<br />

1992, 1994). The study marks the beginning of a fresh era for the freshwater fish research in<br />

Malaysia, particularly for Peninsular Malaysia.<br />

In the late 1990s, a study was initiated to document the fish diversity of a small pocket of peat<br />

and freshwater swamp forest in the Pondok Tanjung Forest Reserve, Perak. In the five months<br />

of short-period samplings (December 1997 to April 1998), 42 fish species were recorded<br />

(Mansor et al. 1999) and the number has now increased to 50 species (A. Ahmad unpubl.).<br />

More focus was given to document the freshwater fish fauna of peat swamp related ecosystems.<br />

Zakaria-Ismail (1999) reported about 33 species of freshwater fish in Nenasi Forest Reserve,<br />

Pahang. Another study recorded 46 species in Southeast Pahang Peat Swamp Forest (SEPPSF).<br />

The most recent survey in SEPPSF, conducted along Sungai Bebar and Sungai Serai, yielded<br />

approximately 58 species, thus bringing the total fish species known to SEPPSF to 65 species<br />

(Ahmad et al. 2005).<br />

Studies on the freshwater fish species in several major islands in Peninsular Malaysia yielded<br />

surprising results. Penang Island’s ichthyofauna was documented by Alfred (1963) in which<br />

Neolissocheilus hendersoni (previously known as Acrossocheilus hendersoni Herre) was<br />

described. The species is endemic to Penang and Langkawi Islands. The Tioman Island’s<br />

ichthyofauna has been surveyed by several researchers and the latest results were published<br />

by Ng et al. (1999). Fourteen species were reported to inhabit the many streams and creeks on<br />

the island. Despite its relatively low diversity, two species occurring there: Sundoreonectes<br />

tiomanensis (loach) and Clarias batu (catfish) are not found elsewhere. While Clarias batu is<br />

common along streams (Lim & Ng 1999), the loach is confined to a single cave situated in the<br />

island’s interior.<br />

In 2002, Malayan Nature Society (MNS) together with several other institutions organized a<br />

scientific and heritage expedition to the island of Langkawi. Together with previous collections,<br />

a checklist of the freshwater fish was prepared. At least 24 species were recorded, while three<br />

others are additional to the ones already known for Peninsular Malaysia (Ahmad & Lim in<br />

prep).<br />

Inventory studies were also conducted in states parks such as Endau-Rompin (Zakaria-Ismali<br />

1987, Ng & Tan 1999), Perlis State Park (Ahmad et al. 2001, Samat et al. 2002, Ahmad &<br />

Samat 2005), Penang National Park (Ahmad et al. 2002, Ahmad et al. 2004), small streams<br />

and headwaters in Pahang (Zakaria-Ismail 1993) and Johor (Lim et al. 1990), small isolated<br />

swamps in Terengganu (Kottelat et al. 1992). Ng & Tan (1999) recorded two new catfish<br />

species from Sungai Kahang while several new species were described from the freshwater<br />

swamps at Kuala Berang, Terengganu (Kottelat & Lim 1993).<br />

In Sabah, there were no other major studies except for the work of Inger & Chin (1962).<br />

Localised surveys were conducted while others were more ecological in approach. Samat &<br />

Chin (1996) produced a checklist of the balitorid fishes, comprising 19 species and briefly<br />

discussed the biogeography, taxonomy, species composition and ecomorphology. A study on<br />

the balitorid loach, Gastromyzon is currently on-going (K.K.P. Lim, pers. comm.). Studies<br />

conducted at Danum Valley (Martin-Smith 1998, Martin-Smith & Tan 1998) yielded several<br />

86


A. AHMAD & A.R. KHAIRUL-ADHA (2007)<br />

new species (Tan & Martin-Smith 1998). Inventories were also conducted at Sungai Segama<br />

in the Tabin Wildlfe Reserve, Crocker Range, Maliau Basin and Kinabalu Park (Goose 1972,<br />

Samat 1990).<br />

In Sarawak, apart from the work of Watson & Balon (1984) and the compilation of a fish<br />

checklist by Kottelat & Lim (1995), several other studies were conducted, mainly focusing on<br />

small areas and lacking major taxonomic work. Inventories were conducted along the Rajang<br />

River, Lambir and Gunung Mulu National Parks, Batang Ai and Bario areas. Large areas of<br />

the peat swamp forest in the state are yet to be explored. A small pocket of peat swamp forest<br />

near University Malaysia Sarawak (UNIMAS) has about 16 species of freshwater fish (Khairul-<br />

Adha & Yuzine in press). Surveys in other areas were conducted but the results are preliminary<br />

(Ahmad & Khairul-Adha in prep.).<br />

REPOSITORY CENTER<br />

Malaysia does not have a national repository centre (Ng 2000). The collections in Peninsular<br />

Malaysia are currently deposited in the respective institutions where the research is conducted.<br />

The need for a national repository centre is necessary but until this is created, universities,<br />

research institutions and government agencies will continue to keep their respective collections.<br />

At present, the collection at University Malaya (BIRCUM) is probably the only one being<br />

actively used by researchers and taxonomists alike. The University College of Science and<br />

Technology Malaysia (KUSTEM), Kuala Terengganu and University Kebangsaan Malaysia<br />

(UKM), Bangi each holds a good collection of freshwater fishes. The collections at KUSTEM<br />

are mainly new collections and this does not include collections reported by Mohsin & Ambak<br />

(1983). Fisheries Research Institute (FRI), Malacca, holds a significant number of collections<br />

that includes materials from Sungai Pahang. Many of these collections may not have been<br />

accurately curated.<br />

In Sabah and Sarawak, both the State Museums play a significant role in holding a large<br />

collection of fishes found in the states. Apart from that, University Malaysia Sabah (UMS),<br />

Kota Kinabalu and UNIMAS have their own collections. The number of collections may not<br />

be as great compared to the Museums’ collections, but they are still considered significant<br />

from the viewpoint of research.<br />

LOCAL EXPERTISE<br />

Ng (2000) stated that taxonomic expertise is a greatly misused word. In Malaysia, the number<br />

of practising taxonomists is scarce. Many taxonomists are trained in the field of research but<br />

unfortunately, do not eventually practice active taxonomic research. The establishment of the<br />

national repository center may not materialize if there is insufficient number of taxonomists,<br />

ecologists and biologists. In addition, it is becoming increasingly difficult to encourage the<br />

younger generation to be involved in the research and development of freshwater fishes.<br />

Kottelat & Whitten (1996) and Ng (2000) commented on the pathetic number of practising<br />

taxonomists in Asia. In Malaysia, the figure (Table 2 in Ng 2000) showed that only a few are<br />

involved in this field, but the actual number practicing might be even less than what is reported!<br />

In addition, many senior researchers are not actively publishing their results. The collaboration<br />

87


STATE OF KNOWLEDGE ON FRESHWATER FISHES OF MALAYSIA<br />

between Malaysia and other external agencies such as the Raffles Museum of Biodiversity<br />

Research (RMBR), Singapore, plays a significant role in enhancing knowledge on the country’s<br />

freshwater fishes.<br />

External collaboration is needed but more importantly, the availability of sufficient research<br />

funding is crucial to enable inventory work and systematic research. The involvement of<br />

organisations such as the United Nation Development Program, (UNDP) through the Global<br />

Environmental Facility (GEF) in the research on the peat swamp forests in Southeast Pahang,<br />

Sarawak and Sabah is significant in contributing to the habitat conservation. Notwithstanding<br />

this, it is crucial that local researchers play a more active role to the research and conservation<br />

of these precious natural resources.<br />

ACKNOWLEDGEMENTS<br />

Special thanks to Prof. Dr. A. Ambak (KUSTEM), Assoc. Prof. Dr. Peter K.L. Ng (ZRC),<br />

Kelvin K.P. Lim (ZRC), Assoc. Prof. Dr. Lee Nyanti (UNIMAS) and Patrick K.Y. Lee (UM)<br />

for valuable discussion on this paper. The first author is also grateful to Siti Ariza Aripin for<br />

gathering the materials for this manuscript.<br />

REFERENCES<br />

AHMAD, A., ALI, A.B. & MANSOR, M. 2001. Freshwater fishes of Wang Kelian, Perlis<br />

State Park. Pp. 111–121 in Faridah-Hanum, I., Osman, K. & Latiff A. (eds.) Kepelbagaian<br />

Biologi dan Pengurusan Taman Negeri Perlis: Persekitaran Fizikal dan Biologi Wang<br />

Kelian. Jabatan Perhutanan Perlis.<br />

AHMAD, A., YUSRI, Y., SITI AZIZAH, M.N. & ALI, A.B. 2002. The fish fauna of Pantai<br />

Acheh Park, Penang, Malaysia. Journal of Bioscience 13(2): 35–41.<br />

AHMAD, A., YUSRI, Y., SITI AZIZAH, M.N. & ALI, A.B. 2004. The fish fauna of Pantai<br />

Acheh Forest Reserve in Penang, Malaysia: species composition, local distribution and<br />

inter-site relationship. Journal of Bioscience 15(1): 49–61.<br />

AHMAD, A. & SAMAT, A. 2005. Additional records of the freshwater fishes of Perlis State<br />

Park, Peninsular Malaysia. Malayan Nature Journal 57(3): 327–343.<br />

AHMAD, A., MAZLAN, A.G., SYED AHMAD RIZAL, T.N., ABD. RAHMAN, A.R.,<br />

JAMIL, M., JACQUELINE, L., & ABDULLAH, S. 2005. Freshwater fishes of Sungai<br />

Bebar and adjacent areas. Pp. 145–148 in Summary Findings PSF Technical Series No. 4.<br />

Peat Swamp Forest Project. UNDP, GEF, Pahang Forestry Department & Universiti<br />

Kebangsaan Malaysia.<br />

ALFRED, E.R. 1963. Notes on a collection of freshwater fishes from Penang. Bulletin of the<br />

National Museum 32: 143–156.<br />

CHIN, P.K. 1990. The freshwater fishes of North Borneo. 47 pp. in Inger, R.F. & Chin, P.K.<br />

The Freshwater Fishes of North Borneo. Sabah Zoological Society, Sabah.<br />

CHIN, P.K. & SAMAT, A. 1992. A new species of loach, Nemacheilus elegentissimus (family<br />

Balitoridae, subfamily Nemacheilinae) from Danum Valley, Sabah. Malay. Nat. J. 46:<br />

25–33.<br />

CHIN, P.K. & SAMAT, A. 1995. Freshwater fishes of Danum Valley, Sabah. Sabah Soc. J.<br />

12: 17–46.<br />

88


A. AHMAD & A.R. KHAIRUL-ADHA (2007)<br />

CRAMPHORN, J. 1983. Sungai Terengganu fish survey, 1980. Malay. Nat. 36(4): 16–20.<br />

GOOSE, J.P. 1972. Fishes of Kinabalu National Park (North Borneo). Biologie 48(3): 1–5.<br />

INGER, R.F. & CHIN, P.K. 1962. The Freshwater Fishes of North Borneo. Fieldiana Zool.<br />

45: 1–268.<br />

INGER, R.F. & CHIN, P.K. 1990. The Freshwater Fishes of North Borneo. Fieldiana Zool.<br />

45: 1–268. Revised edition. Lun Hing Trading, Kota Kinabalu.<br />

KHAIRUL-ADHA, A.R. & YUZINE, E. (in press). The fish fauna. Biodiversity of a peat<br />

swamp forest at Kota Samarahan. Institute of Biodiversity and Environmental<br />

Conservation, University Malaysia Sarawak, Kota Samarahan.<br />

KHAN, M.S., LEE, P.K.Y., CRAMPHORN, J. & ZAKARIA-ISMAIL, M. 1996. Freshwater<br />

fishes of the Pahang River basin, Malaysia. Wetlands International – Asia Pacific<br />

Publication No. 112. 82 pp.<br />

KOTTELAT, M. & LIM, K.K.P. 1993. A review of the eel-loaches of the genus Pangio<br />

(Teleostei: Cobitidae) from the Malay Peninsula, with descriptions of six new species.<br />

The Raffles Bulletin of Zoology 41(2): 203–249.<br />

KOTTELAT, M. & LIM, K.K.P. 1995. Freshwater fishes of Sarawak and Brunei Darussalam:<br />

a preliminary annotated checklist. The Sarawak Museum Journal XLVIII 69 (new series):<br />

228–256.<br />

KOTTELAT, M. & WHITTEN, T. 1996. Freshwater biodiversity in Asia with special reference<br />

to fish. World Bank Technical Paper No. 343. 59 pp. World Bank, Washongton D.C.<br />

KOTTELAT, M., NG, P. & LIM, K. 1992. Recent collections of freshwater fish from<br />

Terengganu, Peninsular Malaysia. Malayan Naturalist 46(2): 7–12.<br />

LIM, K.K.P. & NG, H.H. 1999. Clarias batu, a new species of catfish (Teleostei: Clariidae)<br />

from Pulau Tioman, Peninsular Malaysia. The Raffles Bulletin of Zoology, Supplement<br />

No. 6: 157–167.<br />

LIM, K.K.P. & TAN, H.H. 2002. Freshwater fish diversity in Peninsula Malaysia: A review<br />

of recent findings. In: A. Ali et al. (eds.) The Asian wetlands: bringing partnership into<br />

good wetland practices. Penerbit Universiti Sains Malaysia, Penang. In CD form.<br />

LIM, K.K.P., NG, P.K.L. & KOTTELAT, M. 1990. On a collection of freshwater fishes from<br />

Endau-Rompin, Pahang-Johore, Peninsular Malaysia. The Raffles Bulletin of Zoology<br />

38(1): 31–54.<br />

MANSOR, M., ALI, A.B. & AHMAD, A. 1999. Pondok Tanjung: a unique blackwater swamp<br />

in Malaysia. Pp. 110–120 in M.R. Che Salmah & A.B. Ali (eds.) Proceedings of the Joint<br />

USM-RCJ-NHK Education Corporation Workshop on Public Awareness of Wetlands and<br />

Role of Ramsar Convention on Wetland Conservation and Wise Use, Penerbit Universiti<br />

Sains Malaysia, Penang.<br />

MARTIN-SMITH, K.M. 1998. Relationship between fishes and habitat in rainforest streams<br />

in Sabah, Malaysia. Journal of Fish Biology 52: 458–482.<br />

MARTIN-SMITH, K.M. & TAN, H.H. 1998. Diversity of freshwater fishes from eastern<br />

Sabah: an annotated checklist from Danum Valley and a consideration of inter- and intracatchment<br />

variability. The Raffles Bulletin of Zoology 46(2): 573–604.<br />

MIZUNO, N. & FURTADO, J.I. 1982. Ecological notes on fishes. Pp. 321–349 in Furtado,<br />

J.I. & Mori, S. (eds.) Tasek Bera. The Ecology of a Freshwater Swamp. Dr. W. Junk<br />

Publishers, The Hague.<br />

MOHSIN, A.K.M. & AMBAK, A. 1983. Freshwater Fishes of Peninsular Malaysia. Universiti<br />

Pertanian Malaysia, Selangor. 284 pp.<br />

NG, H.H. & TAN, H.H. 1999. The fishes of the Endau drainage, Peninsular Malaysia with<br />

descriptions of two new species of catfishes (Teleostei: Akysidae, Bagridae). Zoological<br />

Studies (Taiwan) 38(3): 350–366.<br />

89


STATE OF KNOWLEDGE ON FRESHWATER FISHES OF MALAYSIA<br />

NG, H.H., TAN, H.H. & LIM, K.K.P. 1999. The inland fishes of Pulau Tioman, Peninsular<br />

Malaysia. The Raffles Bulletin of Zoology, Supplement No. 6: 169–187.<br />

NG, P.K.L. 2000. Development and future direction of biodiversity collections in Southeast<br />

Asia. Pp. 49–65 in Proceeding of the International Conference on In-situ & Ex-situ<br />

Biodiversity Conservation in the New Millennium, 20–22 June 2000, Kota Kinabalu, Sabah.<br />

NG, P.K.L., TAY, J.B., LIM, K.K.P. & YANG, C.M. 1992. The conservation of the fish and<br />

other aquatic fauna of the North Selangor Peat Swamp Forest and adjacent areas. Asian<br />

Wetland Bureau Publication No. 81. 90 pp.<br />

NG, P.K.L., TAY, J.B. & LIM, K.K.P. 1994. Diversity and conservation of blackwater fishes<br />

in Peninsular Malaysia, particularly in the North Selangor peat swamp forest.<br />

Hydrobiologia 285: 203–218.<br />

SAMAT, A. 1990. Taburan dan populasi ikan air tawar di beberapa altitud di Taman Kinabalu,<br />

Sabah. Pertanika 13(13): 341–348.<br />

SAMAT, A. & CHIN, P.K. 1996. The balitorid fish of Sabah. The Sarawak Museum<br />

Journal L(71) (new series): 87–92.<br />

SAMAT, A., AHMAD, A., USUP, G. & MAIMON, A. 2002. Fishes of Perlis State Park with<br />

reference to its habitat environment and conservation. Pp. 135–147 in Latiff, A., Osman,<br />

K., Faridah-Hanum, I. & A. Rahman, Y. (eds.) Kepelbagaian Biologi dan Pengurusan<br />

Taman Negeri Perlis: Persekitaran Fizikal dan Biologi dan Sosio-ekonomi Wang Mu.<br />

Taman Negeri Perlis & Jabatan Perhutanan Perlis.<br />

TAN, E.S.P. & HAMZAH, J. 1990. Game fishes of Taman Negara. J. Wildlife and Parks 10:<br />

78–93.<br />

TAN, H.H & MARTIN-SMITH, K.M. 1998. Two new species of Gastromyzon (Teleostei:<br />

Balitoridae) from the Kuamut headwaters, Kinabatangan Basin, Sabah, Malaysia. Raffles<br />

Bulletin of Zoology 46(2): 361–371.<br />

WATSON, D.J. & BALON, E.K. 1984. Structure and production of fish communities in tropical<br />

rain forest streams of northern Borneo. Can. J. Zool. 62: 927–940.<br />

ZAKARIA-ISMAIL, M. 1984. Checklist of fishes of Taman Negara. Malayan Naturalist 37:<br />

21–26.<br />

ZAKARIA-ISMAIL, M. 1987. The fish fauna of the Ulu Endau river system, Johore, Malaysia.<br />

Malayan Nature Journal 41: 403–411.<br />

ZAKARIA-ISMAIL, M. 1989. Systematics, zoogeography and conservation of the freshwater<br />

fishes of Peninsular Malaysia. Unpublished PhD. dissertation, Colorado State University,<br />

USA. 473 pp.<br />

ZAKARIA-ISMAIL, M. 1993. The fish fauna of the Sungai Teris and Sungai Rengit, Krau<br />

Game Reserve, Pahang, Malaysia. Malayan Nature Journal 46: 201–228.<br />

ZAKARIA-ISMAIL, M. 1994. Zoogeography and biodiversity of the freshwater fishes of<br />

Southeast Asia. Hydrobiologia 285: 41–48.<br />

ZAKARIA-ISMAIL, M. 1999. Survey of fish diversity in peat swamp forest. Pp. 173–198 in<br />

Chin T.Y. & Havmoller, P. (eds.) Sustainable management of Peat Swamp Forest in<br />

Peninsular Malaysia, Vol. 1: Resource and Environment. Forestry Department Peninsular<br />

Malaysia, Kuala Lumpur.<br />

90


MD. AKHIR ARSHAD & PADILAH BAKAR (2007)<br />

STATUS OF BIOLOGICAL DIVERSITY IN MALAYSIA &<br />

THREAT ASSESSMENT OF PLANT SPECIES IN MALAYSIA<br />

Commercial and Exotic Fish Diversity in<br />

Marine Parks in the Straits of Malacca and<br />

South China Sea<br />

1<br />

Md. Akhir Arshad & 2 Padilah Bakar<br />

ABSTRACT<br />

Inventory of species diversity in different marine ecosystems has been conducted in Peninsular<br />

Malaysia, Sabah and Sarawak since early 1900’s. Much of the work in taxonomic identifications<br />

was made possible through integrated effort ranging from periodic national fish resource surveys<br />

initiated as early as 1926, fishing trials and statistical data collected at various landing points.<br />

These efforts were strengthened by regional cooperation mechanisms, international research<br />

initiatives and grants. These have contributed, directly and indirectly, to an increase in<br />

information on marine fish diversity. At present, there are 1751 species of marine and brackish<br />

water fish recorded in Malaysia. More than 400 species recorded in the coastal areas and river<br />

estuaries and more than 450 species recorded offshore in East Malaysia alone. The diversity<br />

in the coastal areas, estuaries and offshore for Peninsular Malaysia is lower.<br />

Improvements in diving and photographic-videographic equipments have provided a superb<br />

documentation of information of biodiversity at specific sites especially in marine park islands<br />

for both coastal and offshore areas. The interest in underwater photography and videography<br />

has enhanced the work significantly. Significant findings on fish biodiversity in marine park<br />

islands especially on rare and exotic species have increased tremendously.<br />

This paper provides an overall picture of the Global Taxonomic Initiative (GTI) in Malaysia’s<br />

marine fish environment based on the information gathered through individual research and<br />

institutional efforts, including published and unpublished reports. Information specific to Pulau<br />

Payar in the Straits of Malacca, Pulau Redang Islands in Terengganu, Tioman Islands in Pahang<br />

and Tinggi Islands in Johor are selected for the review since extensive research and surveys<br />

had been conducted on these islands.<br />

The paper also discusses issues and obstacles experienced in undertaking the Global Taxonomic<br />

Initiative and provide recommendations for more effective GTI efforts including repository<br />

and management of specific marine ecosystems and corridors.<br />

Fisheries Research Institute, 11960 Batu Maung, Penang, Tel: 04–626 3925, Fax: 04–626 2210; 1 akhir38@yahoo.com;<br />

2<br />

padilahbakar@yahoo.com<br />

91


1. Cucurlionidae. Photo courtesy Shawn Cheng<br />

2. Hospitalitermes sp. (Termitidae) Photo courtesy Shawn Cheng<br />

3. Danaus affinis (Nymphalidae). Photo courtesy L.G. Kirton<br />

4. Drupadia ravindra moorei (Lycaenidae). Photo courtesy L.G. Kirton<br />

5. Junonia orithya wallacei (Nymphalidae). Photo courtesy L.G. Kirton<br />

6. Johora grallator (Potamidae). Photo courtesy Lim Cheng Puay<br />

7. Geosesarma gracillimum (Grapsidae). Photo courtesy P.K.L. Ng<br />

8. Odontolabis femoralis (Lucanidae). Photo courtesy L.G. Kirton<br />

9. Riverine vegetation in a tropical lowland dipterocarp forest. Photo<br />

courtesy L.G. Saw


STATUS OF BIOLOGICAL DIVERSITY IN MALAYSIA &<br />

THREAT ASSESSMENT OF PLANT SPECIES IN MALAYSIA<br />

MALAYSIAN FRESHWATER CRABS:<br />

CONSERVATION PROSPECTS AND<br />

CHALLENGES<br />

1<br />

Peter K. L. Ng & 2 Darren C. J. Yeo<br />

ABSTRACT<br />

Of the over 150 species of true freshwater crab species now known from Sundaic Southeast<br />

Asia, more than half occur in Malaysia. Currently, 24 genera and 102 described species from<br />

four families; Potamidae, Gecarcinucidae, Parathelphusidae and Sesarmidae, are known. Many<br />

species of freshwater crabs, however, have very restricted geographic ranges, a consequence<br />

of their relative low fecundity cum direct development, poor dispersal abilities, and nichespecialisation.<br />

This makes freshwater crabs highly susceptible to anthropogenic activities.<br />

While there is no clear evidence that any one species has been made extinct as a result, the<br />

threats facing many known species are critical. The conservation status of Malaysian freshwater<br />

crabs are reviewed and assessed using the criteria established by the IUCN (2001), and the<br />

problems and challenges associated with these discussed. The report serves as a starting point<br />

for determining appropriate conservation strategies for these animals.<br />

INTRODUCTION<br />

Of the estimated 6,500 known species of brachyuran crabs, over 1,000 are known to be wholly<br />

freshwater in habit. Freshwater crabs are one of the most important organisms inhabiting<br />

Southeast Asian freshwaters, but are relatively poorly known because of their secretive habits.<br />

They are present in almost all clean freshwater bodies, from lowlands to high mountains.<br />

Some species have also become terrestrial and semi-terrestrial, moving about or burrowing<br />

into the forest floor. Their direct development and freshwater habit have resulted in rampant<br />

speciation, with a large number of species occurring in this part of the world. Malaysia alone<br />

has one of the highest densities of freshwater crab diversity in the world, with 24 genera and<br />

102 known species from four families (Potamidae: 41 species; Parathelphusidae: 40 species;<br />

Gecarcinucidae: 3 species; and Sesarmidae: 18 species), many of them endemic, and more<br />

than half of them described between 1990 and 2000 (Ng 1988, 1990a, 2004; Cranbrook &<br />

Furtado 1988; Ng & Ambu 1998).<br />

Department of Biological Sciences, National University of Singapore, Kent Ridge, Singapore 119260, Republic of<br />

Singapore; 1 dbsngkl@nus.edu.sg; 2 darrenyeo@nus.edu.sg<br />

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MALAYSIAN FRESHWATER CRABS: CONSERVATION PROSPECTS AND CHALLENGES<br />

Much of this diversity and endemism is owed to the complicated topography and equally<br />

diverse and heterogeneous habitats found in much of the country, ranging from rugged montane<br />

habitats with waterfalls and torrential streams to moist lowland forests to subterranean<br />

freshwaters; in both continental as well as insular landmasses. These provide plenty of<br />

opportunities not only for allopatric speciation to occur by geographic isolation, but also for<br />

sympatric speciation through niche specialization in the many ecological niches available.<br />

Naturally, these are coupled with the freshwater crab characteristics of possessing low fecundity,<br />

direct development and limited dispersal abilities.<br />

The species distributions cover a wide gamut, from point endemics such as Johora johorensis<br />

(Gunung Pulai, Johor) to localized taxa like Geosesarma nemesis (Gunung Pulai and Gunung<br />

Panti, Johor, and Singapore) to wide ranging species such as Parathelphusa maculata<br />

(throughout Peninsular Malaysia, southernmost Thailand, Singapore and southern half of<br />

Sumatra).<br />

The present paper aims to assess and discuss the conservation status of the 102 freshwater<br />

crab species now known from Malaysia.<br />

MATERIALS AND METHODS<br />

For purposes of reference and discussion, certain geographical terms have been used in this<br />

paper. These are defined below:<br />

Sundaland/Sundaic - refers to the continental land masses and islands of the Sunda Shelf, i.e.,<br />

Malay Peninsula, Borneo, Sumatra, Java and Lesser Sunda Islands. Palawan (including<br />

Balabac) is included but Sulawesi and the southern islands of the Philippines (e.g.,<br />

Mindanao and Mindoro) are excluded.<br />

Malay/Malayan - pertaining to Peninsular Malaysia, inclusive of southernmost Thailand (south<br />

of the Isthmus of Kra), and Singapore.<br />

The terminology for morphological structure follows essentially that used by Ng (1988). Several<br />

genera and species are in the process of being described or the descriptions are in press. In<br />

such instances, no name has been applied. In this paper, the abbreviations G1 and G2 are used<br />

for the male first and second pleopods, respectively.<br />

Although Ng (1988) previously recognised the taxon of subspecies, a reconsideration of the<br />

state of brachyuran systematics suggests that such a fine division is neither useful nor realistic,<br />

especially considering the poor understanding we have of their mechanisms of speciation.<br />

The phylogenetic species concept is utilised here as far as possible. Under this framework, all<br />

taxa previously regarded as subspecies are recognised here as species.<br />

With regards to the threat status, the most recent (IUCN 2001) guidelines (Red List Categories<br />

& Criteria, version 3.1) were adopted for use in assessing the threat-levels of the various<br />

freshwater crab species considered. These categories are: Critically Endangered (CR),<br />

Endangered (EN), Vulnerable (VU), Near Threatened (NT), Least Concern (LC), or Data<br />

Deficient (DD).<br />

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PETER K. L. NG & DARREN C. J. YEO (2007)<br />

Although the criterion of population size is an important consideration in ascertaining a species’<br />

threat level, this is almost impossible to determine for the freshwater crab species treated here.<br />

The necessary quantifications simply have not been done. Many species are also very secretive<br />

in habits, and several have not been rediscovered since they were first collected. In particular,<br />

species, which are obligate cave dwellers, deep forest terrestrial species, tree-climbers or that<br />

otherwise have very specialised niches, cannot be effectively sampled. As such, the only<br />

objective data-sets of use are of the presence/absence type. Even so, when a species is<br />

supposedly absent from an area, this observation must be considered with regards to its known<br />

habits and behaviour. In many cases, the habitats and habits of a species can be predicted on<br />

the basis of its carapace physiognomy, leg structure and proportions, eye form as well as<br />

colour.<br />

Nevertheless, in general, the presence/absence criterion at least allows the geographic range<br />

to be predicted using either the Extent of Occurrence (i.e. area contained within the shortest<br />

continuous imaginary boundary encompassing known sites of occurrence), or the Area of<br />

Occupancy (i.e. the area within its Extent of Occurrence which is actually occupied by the<br />

taxon). Given that most tropical habitats are very heterogeneous in structure, and aquatic<br />

habitats (including swamp forest structure and underground water-tables) fluctuate substantially<br />

depending on the time of the year; and that some species have small and highly localised<br />

populations; the Area of Occupancy (i.e. the available aquatic habitat particular to the species)<br />

criterion is too subjective to be very useful. The Extent of Occurrence is thus the preferred<br />

criterion for estimates used here for geographic range.<br />

As such, the CR, EN and VU outcomes resulted from evaluation against criteria B1(a) and<br />

(b)(iii) in those categories. Continuing decline in Extent of Occurrence and/or quality of habitat<br />

was inferred if the habitat was not a protected area, or if it was a protected area subject to<br />

anthropogenic impacts such as pollution or encroachment.<br />

A taxon is CR if its Extent of Occurrence is estimated to be less than 100 km 2 (B1) and its<br />

habitat is severely fragmented or it is known to exist at only one location (B1(a)); and there is<br />

a continuing decline in the area, extent and/or quality of its habitat (b)(iii).<br />

It is EN if its Extent of Occurrence is estimated to be less than 5,000 km 2 (B1) and its habitat<br />

is severely fragmented or it is known to exist at no more than five locations (B1(a)); and there<br />

is a continuing decline in the area, extent and/or quality of its habitat (b)(iii).<br />

It is VU if its Extent of Occurrence is estimated to be less than 20,000 km 2 (B1) and its habitat<br />

is severely fragmented or it is known to exist at no more than 10 locations (B1(a)); and there<br />

is a continuing decline in the area, extent and/or quality of its habitat (b)(iii). VU status was<br />

also applied to taxa that have an Area of Occupancy estimated to be less than 20 km 2 ; and are<br />

known from only a single population which is at least partly in a protected area, but is “prone<br />

to the effects of human activities or stochastic events within a very short time period in an<br />

uncertain future, and is thus capable of becoming Critically Endangered or even Extinct in a<br />

very short time period” (D2).<br />

NT status was awarded to taxa that were evaluated against the criteria but did not qualify for<br />

CR, EN or VU at present, but likely to qualify for such a category in the near future.<br />

97


MALAYSIAN FRESHWATER CRABS: CONSERVATION PROSPECTS AND CHALLENGES<br />

LC status was awarded to taxa that were evaluated against the criteria and did not qualify for<br />

CR, EN, VU or NT; in general, these taxa are widespread (Extent of Occurrence greater than<br />

20,000 km 2 ) and abundant.<br />

RESULTS<br />

The results are presented in Table 1, which is a checklist of the freshwater crabs of Malaysia,<br />

showing available data relevant to the IUCN (2001) Red List criteria together with the<br />

conservation outcomes. The assessment shows that of the 102 Malaysian species known, 16<br />

taxa are Critically Endangered, 46 Endangered, 28 Vulnerable, 10 of Least Concern and 2 are<br />

Data Deficient. None of the species evaluated here qualified for the Near Threatened category<br />

as defined above.<br />

DISCUSSION<br />

Based on the conservation status assigned to the Malaysian freshwater crabs in the present<br />

study, a few patterns have emerged that should be noted. The restricted distributions of most<br />

of the freshwater crab species in Malaysia pose serious problems for conservation. It is<br />

somewhat fortunate that the species with the most restricted distributions are those which<br />

inhabit offshore islands or mountains (see later, however). These areas are generally less<br />

disturbed or not scheduled for development, at least for the moment. The serious loss of<br />

natural forest as a result of land development and agriculture has generally affected the lowlands<br />

more severely. The species which do occur in lowlands, e.g., Parathelphusa maculata and<br />

Sayamia sexpunctata, are still common in relatively unpolluted plantation waterways and<br />

ricefields. These lowland species also have relatively much wider distributions, and are least<br />

at risk. Ten species (e.g., Perithelphusa borneensis) reported here with an Extent of Occurrence<br />

of approximately 1,500 to 2,000 km 2 are categorized as Least Concern. Aquatic species (e.g.,<br />

Isolapotamon collinsi and Thelphusula baramensis) in general appear to be faring better than<br />

their terrestrial kin, as only 22 out of 51 primarily aquatic species (43%) are categorized under<br />

Critically Endangered or Endangered. On the other hand, terrestrial or semi-terrestrial species<br />

like Geosesarma katibas and Thelphusula granosa seem to be under much greater threat, with<br />

36 out of 47 such species (77%) being regarded as Critically Endangered or Endangered.<br />

Perhaps not surprisingly, the results also indicate that specialist species, e.g., the obligate<br />

cave-dwelling crab, Cerberusa caeca, are also more threatened, with most such taxa being<br />

Critically Endangered or Endangered. Interestingly, highland taxa, despite their relative<br />

inaccessibility, seem to also be at higher risk, with all 10 highland species in Peninsular Malaysia<br />

(e.g., Johora grallator) being Critically Endangered or Endangered. Many of the potamids<br />

and smaller parathelphusids are especially vulnerable to development and pollution. The limited<br />

distribution of most of these species with very restricted ranges is not an anomaly. Johora<br />

johorensis for example, is only known from Gunung Pulai, and despite much collecting around<br />

the hill and other areas, has not been recorded elsewhere. In neighbouring hills, it is replaced<br />

by two very different taxa: J. intermedia to the north and J. murphyi to the east. Any<br />

development of Gunung Pulai would thus have dire consequences for J. johorensis. Finally,<br />

the isolated nature of small islands also appears to put the island endemic species at a<br />

disadvantage, as illustrated by the eight species (five Johora, one Parathelphusa, two<br />

Geosesarma) known only from Pulau Tioman, all of which are regarded as Endangered.<br />

98


Table 1. Checklist of the freshwater crabs of Malaysia (Potamidae, Parathelphusidae, Gecarcinucidae, Sesarmidae)<br />

Species Status No. of Extent of Range Habitat/Ecology Threats Conservation measures<br />

sites Occurrence<br />

Johora aipooae EN 1


Species Status No. of Extent of Range Habitat/Ecology Threats Conservation measures<br />

sites Occurrence<br />

Johora gua EN 1


Species Status No. of Extent of Range Habitat/Ecology Threats Conservation measures<br />

sites Occurrence<br />

Johora intermedia LC >20


Species Status No. of Extent of Range Habitat/Ecology Threats Conservation measures<br />

sites Occurrence<br />

Johora tahanensis VU 3


Species Status No. of Extent of Range Habitat/Ecology Threats Conservation measures<br />

sites Occurrence<br />

Stoliczia CR 1


Species Status No. of Extent of Range Habitat/Ecology Threats Conservation measures<br />

sites Occurrence<br />

Stoliczia CR 1


Species Status No. of Extent of Range Habitat/Ecology Threats Conservation measures<br />

sites Occurrence<br />

Stoliczia tweediei CR 1


Species Status No. of Extent of Range Habitat/Ecology Threats Conservation measures<br />

sites Occurrence<br />

Isolapotamon VU 4


Species Status No. of Extent of Range Habitat/Ecology Threats Conservation measures<br />

sites Occurrence<br />

Isolapotamon VU 3


Species Status No. of Extent of Range Habitat/Ecology Threats Conservation measures<br />

sites Occurrence<br />

Phricotelphusa CR 1


Species Status No. of Extent of Range Habitat/Ecology Threats Conservation measures<br />

sites Occurrence<br />

Thelphusula VU 2


Species Status No. of Extent of Range Habitat/Ecology Threats Conservation measures<br />

sites Occurrence<br />

Thelphusula EN 1


Species Status No. of Extent of Range Habitat/Ecology Threats Conservation measures<br />

sites Occurrence<br />

Stygothelphusa CR 1


Species Status No. of Extent of Range Habitat/Ecology Threats Conservation measures<br />

sites Occurrence<br />

Sundathelphusa EN 1 2,000 km 2 Widespread throughout Primarily aquatic. Living in No immediate threat, The retention of<br />

maculata De Man, Peninsular Malaysia. Also slow-flowing lowland streams especially to populations designated protected<br />

1879 found in Singapore and under rocks, vegetation, leaf within protected areas areas.<br />

southern half of Sumatra. litter and debris. Also dig deep throughout its range.<br />

burrows in stream banks. High<br />

tolerance for anoxic water<br />

conditions.<br />

Parathelphusa VU 5


Species Status No. of Extent of Range Habitat/Ecology Threats Conservation measures<br />

sites Occurrence<br />

Parathelphusa EN 1


Species Status No. of Extent of Range Habitat/Ecology Threats Conservation measures<br />

sites Occurrence<br />

Salangathelphusa VU 2


Species Status No. of Extent of Range Habitat/Ecology Threats Conservation measures<br />

sites Occurrence<br />

Geosesarma EN 1


Species Status No. of Extent of Range Habitat/Ecology Threats Conservation measures<br />

sites Occurrence<br />

Geosesarma LC 6


Species Status No. of Extent of Range Habitat/Ecology Threats Conservation measures<br />

sites Occurrence<br />

Geosesarma EN 1


MALAYSIAN FRESHWATER CRABS: CONSERVATION PROSPECTS AND CHALLENGES<br />

The conservation of freshwater crabs hinges almost entirely on preserving patches of natural<br />

forest large enough to maintain the good water quality of the original streams. Potamids are<br />

extremely sensitive to polluted or silted waters, and will not survive when exposed to these<br />

factors. In Singapore for example, the small patch of primary forest of Bukit Timah Hill (ca.<br />

70 hectares) is quite sufficient to maintain a small but thriving population of the potamid<br />

Johora singaporensis. This species is known from only one other area in Singapore, which is<br />

threatened with development, and Bukit Timah is probably its last refuge (see Ng 1988, 1989,<br />

1990b). The same is true for Parathelphusa reticulata, which is known to occur only in a<br />

small remnant patch of peat swamp forest patch of less than 50 hectares in the Central Catchment<br />

Area of Singapore (Ng 1989, 1990a, b). Similar patterns have been recorded for the freshwater<br />

crabs of Sri Lanka (Bahir et al. 2005).<br />

Development, agriculture and exploitation of forest products probably cannot be halted, but<br />

compromises will have to be made if many freshwater crab species are not to be extirpated. It<br />

is likely that some species have already become extinct through extensive developments in<br />

some areas before their taxonomy can be better understood. Judicious and careful exploitation<br />

(e.g., controlled logging) is unlikely to cause extinctions as long as the water drainages are not<br />

polluted or redirected and the forest cover not completely stripped away. The recolonisation<br />

of many lowland plantations and estates by more adaptable species like Parathelphusa maculata<br />

is encouraging. How more montane taxa like potamids will cope is not known, but considering<br />

their fastidious habitat requirements, most species will not be able to adapt as readily as<br />

parathelphusids.<br />

The subjectivity of threat levels assigned here must be emphasised, as some of the limitations<br />

of this study echo the challenges faced in conservation. Conservation challenges are often<br />

associated with the amount of knowledge available on the species. The freshwater crabs of<br />

Singapore and southern Peninsular Malaysia are better known, and their biology and distribution<br />

better understood, as are the potential threats. This, of course, stems from an inherent bias for<br />

conservation efforts to target the better studied species, which are better known simply because<br />

they are more easily caught by workers in more accessible areas, e.g., Johora tiomanensis, a<br />

large, locally common aquatic species found in the lower stretches of the forest streams of the<br />

southern half of Pulau Tioman, which are mostly in close proximity to villages. Conversely,<br />

hard-to-find species tend to be neglected as we simply do not know enough to initiate directed<br />

conservation efforts, e.g., Geosesarma tiomanicum, a tiny terrestrial species that dwells among<br />

the leaf litter of the forest floor in the rugged, hilly parts of Pulau Tioman, often some distance<br />

away from water sources – encountering this species in the middle of the forest is purely a<br />

matter of chance, subject to weather, seasons, and their own fluctuating populations (Ng 1988;<br />

Yeo et al. 1999).<br />

Another aspect of our limited knowledge of some freshwater crabs that proves challenging<br />

for conservation, is the evolving taxonomy of some taxa. Some wide-ranging “species” that<br />

we might try to conserve (or worse, not see the need to conserve, presuming that they are<br />

widespread and common enough) may actually prove to be complexes of several distinct<br />

cryptic taxa, which could differ in various ways such as diets, habits, microhabitat preferences,<br />

ecological niches, local distribution, etc. One such possibility is Johora intermedia, which is<br />

here assigned the status of “Least Concern” primarily because it has been recorded from more<br />

than 20 sites throughout the lower half of the Main Range of Peninsular Malaysia (Selangor,<br />

Pahang, Negri Sembilan and northwestern Johor) in an estimated Extent of Occurrence of<br />

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PETER K. L. NG & DARREN C. J. YEO (2007)<br />

some 1,500 km 2 . However, while the area it is known from appears to be relatively extensive,<br />

it must be noted that the distribution consists of many pockets of populations, and this species<br />

is known to show the greatest variation among the Johora species, facts that point to it probably<br />

being a species complex (Ng 1988). Another probable species complex is the troglophilic<br />

crab, Stygothelphusa bidiensis, which has an unlikely distribution of two disjunct cave systems<br />

in Sarawak (Bau and Gua Serian). The available evidence suggests that the populations in the<br />

two cave systems actually belong to two separate species (unpublished data). The same situation<br />

is true of Lepidothelphusa cognetti, which occurs in the sandstone streams of Bau and Penrissen.<br />

Another point to consider is that for freshwater crabs in developing countries, the line separating<br />

a vulnerable or endangered species is a very fine one. This is mainly because of the very<br />

restricted distributions of many species and the speed of development projects; the time lapse<br />

between project conception and implementation, even for large scale ones, can be as short as<br />

a year.<br />

Using Peninsular Malaysia and Singapore as an example, 42 species of potamids and<br />

parathelphusids are known at present. All the potamids (27 taxa) are found only in Peninsular<br />

Malaysia and Singapore. Of the 15 parathelphusids, 10 are endemic to Peninsular Malaysia<br />

and Singapore, the other five species also occurring in Sumatra or southern Thailand. The<br />

endemic taxa are almost always highland species, or occur on isolated islands. The conservation<br />

of this remarkable diversity is imperative (see also Ng 1988). There is thus, more than ever, a<br />

need to establish more nature reserves and national parks. And careful planning, co-ordination<br />

and supervision to minimise its destructive effects must temper development, inevitable though<br />

it may be. At the same time, other broader, long term issues, those of water-shed conservation,<br />

sufficient size of protected areas, and forest conditions (primary or secondary or disturbed)<br />

must be given due consideration. Such matters if dealt with properly would not just be for the<br />

benefit of freshwater crab diversity, but for the overall ecosystem as well.<br />

ACKNOWLEDGEMENTS<br />

The authors thank the organisers of the workshop for inviting this paper from them, in particular,<br />

Saw Leng Guan, the chair of the organising committee.<br />

REFERENCES<br />

BAHIR, M.M., NG, P.K.L., CRANDALL, K. & PETHIYAGODA, R. 2005. A conservation<br />

assessment of the freshwater crabs of Sri Lanka. Raffles Bulletin of Zoology Supplement<br />

12: 121–126.<br />

CRANBROOK, EARL OF, & FURTADO, J.L. 1988. Freshwaters–Decapod Crustacea. Pp.<br />

225–250 in Earl of Cranbrook (ed.) Key Environments: Malaysia. Pergamon Press, Oxford.<br />

IUCN (International Union for the Conservation of Nature and Natural Resources), 2001. The<br />

IUCN Red List of Threatened Species: 2001 Categories & Criteria. Version 3.1. http://<br />

www.redlist.org/info/categories_criteria2001.html [accessed 01.01.2004].<br />

NG, P.K.L. 1988. The Freshwater Crabs of Peninsular Malaysia and Singapore. Department<br />

of Zoology, National University of Singapore. Shinglee Press, Singapore.<br />

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MALAYSIAN FRESHWATER CRABS: CONSERVATION PROSPECTS AND CHALLENGES<br />

NG, P.K.L. 1989. Endemic freshwater crabs in Singapore: Discovery, Speciation and<br />

Conservation. Singapore Institute of Biology Bulletin 13(2/3): 45–51.<br />

NG, P.K.L. 1990a. Parathelphusa reticulata spec. nov., a new species of freshwater crab from<br />

blackwater swamps in Singapore (Crustacea: Decapoda: Brachyura: Gecarcinucoidea).<br />

Zoologische Mededelingen 63: 241–254.<br />

NG, P.K.L. 1990b. The Freshwater Crabs and Prawns of Singapore. Pp. 189–204 in Chou,<br />

L.M. & Ng, P.K.L.(eds.) Essays in Zoology. Department of Zoology, National University<br />

of Singapore.<br />

NG, P.K.L. 2004. Crustacea: Decapoda, Brachyura. Pp. 311–336 in Yule, C.M. & Yong, H.S.<br />

(eds.) Freshwater invertebrates of the Malaysian region. Academy of Sciences Malaysia.<br />

NG, P.K.L. & AMBU, S. 1998. Freshwater crabs, prawns and snails. Pp. 86–87 in Yong, H.S.<br />

(ed.) Encyclopedia of Malaysia, Volume 3: Animals, Didier Millet Editions, Kuala Lumpur,<br />

Malaysia.<br />

YEO, D.C.J., CAI Y.-X. & NG, P.K.L. 1999. The freshwater and terrestrial decapod crustacea<br />

of Pulau Tioman, Peninsular Malaysia. In: Sodhi, N.S., Yong H.S. & Ng, P.K.L.(eds.)<br />

The Biodiversity of Pulau Tioman, Peninsular Malaysia. Raffles Bulletin of Zoology,<br />

Supplement 6: 197–244.<br />

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STATUS OF BIOLOGICAL DIVERSITY IN MALAYSIA &<br />

THREAT ASSESSMENT OF PLANT SPECIES IN MALAYSIA<br />

OVERVIEW OF INSECT BIODIVERSITY<br />

RESEARCH IN PENINSULAR MALAYSIA<br />

1<br />

Shawn Cheng & 2 Laurence G. Kirton<br />

ABSTRACT<br />

Malaysia’s commitment to implement the Convention on Biological Diversity has provided<br />

fresh impetus for the documentation of the country’s flora and fauna. Insects greatly outnumber<br />

other major lifegroups in terms of diversity and numbers, but an assessment of the degree to<br />

which the biodiversity and taxonomy of insects have been researched in Malaysia indicates<br />

that there are still great needs. In a survey of institutions in the vicinity of the capital city of<br />

Malaysia, 25% of 387 entomology dissertations and articles written over the last decade were<br />

on the subject of insect diversity, with many of the studies being of the numerical kind, while<br />

only 4% were on taxonomy and systematics – the science of describing biological diversity.<br />

In addition, the taxonomy and diversity of only a few major insect orders, such as Lepidoptera<br />

(butterflies and moths), Isoptera (termites) and Phasmida (stick insects), have been relatively<br />

well studied in Malaysia. Little is known of other important insect orders, such as Coleoptera<br />

(beetles), Hymenoptera (bees, wasps and ants), Diptera (flies) and Hemiptera (bugs). We argue<br />

that if any effective inventory of Malaysia’s insect fauna is to take place, sustained interest<br />

and funding needs to be devoted to the study of their diversity and taxonomy.<br />

INTRODUCTION<br />

Biodiversity is often broadly defined as the different forms of plants, animals and<br />

microorganisms that exist, the levels at which they occur (e.g., species, population and<br />

ecosystem levels) and the different ways in which organisms, climate and geology combine to<br />

form functioning ecosystems. Approximately 1.8 million living species have been named and<br />

described and, of these, one million are insects (May 2002). It has also been estimated that<br />

invertebrates represent more than 90% of the planet’s 10 million or so animal species (Erwin<br />

1983, Wilson 1992).<br />

Insects are ubiquitous in the environment and play important roles in maintaining the stability<br />

of ecosystems by being part of the food chain, mediating decomposition processes and through<br />

various ecological interactions, such as pollination, predation and herbivory. Large-scale<br />

anthropogenic activities such as forest clear-cutting extirpate insect species and destroy<br />

ecosystem dynamics and interactions that have been in place for millennia.<br />

Forest Research Institute Malaysia, 52109 Kepong, Selangor, Malaysia. 1 shawn@frim.gov.my; 2 laurence@frim.gov.my<br />

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OVERVIEW OF INSECT BIODIVERSITY RESEARCH IN PENINSULAR MALAYSIA<br />

In view of the rapid decline of forested areas in the world, world leaders agreed to promote the<br />

sustainable use and conservation of natural resources, at the United Nations Conference on<br />

Environment and Development held in Rio de Janeiro in 1992. The Biodiversity Treaty, an<br />

important document stemming from the conference in Rio, emphasised the importance of<br />

countries accepting the responsibility for conserving biological diversity and promoting their<br />

use in a sustainable manner. Malaysia ratified the treaty in 1994, a year after the Treaty came<br />

into force. At the international conference, “Biodiversity: Science and Governance,” held in<br />

Paris in 2005, the Malaysian premier, Dato Seri’ Abdullah Ahmad Badawi, highlighted the<br />

government’s efforts to protect and conserve the environment through the actions and<br />

coordination of the National Council on Biodiversity and Technology and the Natural Resources<br />

and Environment Ministry. A current project, initiated by the Prime Minister, aims to document<br />

Malaysia’s biodiversity with the objective of producing a national ‘red data book’ on endangered<br />

animal and plant species in the country, their distributions and the levels of threat they face<br />

(Koh 2005; Cyranoski 2005).<br />

In view of this plan to document Malaysia’s biodiversity, there is a need to assess the current<br />

status of insect diversity research and the level of information available on major insect groups<br />

in Peninsular Malaysia. In this paper, we examine current trends in entomological research by<br />

analysing the undergraduate and postgraduate dissertation topics of students over the last<br />

decade in a few universities in and around the Klang Valley of Peninsular Malaysia, namely,<br />

University of Malaya, Universiti Kebangsaan Malaysia and Universiti Putra Malaysia. In<br />

addition, we examined both entomological dissertations and articles stemming from research<br />

by the Forest Research Institute Malaysia (FRIM) in the Pasoh Field Station from 1964 to<br />

1999. FRIM was included in the survey because it is the primary research institution that<br />

conducts research on diversity and conservation in Peninsular Malaysia. Although there are<br />

limitations to the data obtained – for example, not all Malaysian universities or all years were<br />

included in the census – the results of this survey are still expected to give a good indication<br />

of the pattern of entomological research in Peninsular Malaysia. In addition to conducting this<br />

survey, we also examined the availability of taxonomic information on several well-known<br />

insect orders in Peninsular Malaysia.<br />

TRENDS IN RELATION TO FIELDS OF RESEARCH<br />

The number of entomological dissertations and articles from each of the institutions surveyed,<br />

and the number on insect diversity, is shown in Table 1. A total of 387 entomology dissertations<br />

and articles were examined. About 25% of these were on the subject of insect diversity; with<br />

Universiti Kebangsaan Malaysia contributing 75% of all studies on insect diversity.<br />

Figure 1 shows the frequency of dissertations and articles on different topics of entomological<br />

research for the combined dataset of the survey, some of which covered more than one research<br />

area. Insect control was the most heavily researched area, and accounted for 31% of all<br />

entomological research. Insect diversity was the next most studied subject and accounted for<br />

close to 26% of all reported entomological work. Biological and ecological research, which<br />

was a popular area of research among undergraduates, contributed 37% of all documented<br />

work. Insect taxonomy, accounted for a mere 4% of all entomological studies. Although the<br />

survey did not cover taxonomic work published in local and international journals by staff of<br />

the various universities surveyed, this low figure is probably still reflective of the shortage of<br />

taxonomic research on insects in Malaysia.<br />

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SHAWN CHENG & LAURENCE G. KIRTON (2007)<br />

Table 1. Numbers of research dissertations and articles on entomology and insect diversity (in<br />

parentheses) in the institutions surveyed.<br />

Institutions Faculties Years No. of<br />

examined dissertations /<br />

articles<br />

*<br />

Universities:<br />

Universiti Malaya Institute of Biological Science 1995-2004 83 (21)<br />

Universiti Putra Forestry & Agriculture 1991-2001 144 (2)<br />

Malaysia<br />

Faculties<br />

Universiti Kebangsaan School of Bioscience 1995-2004 128 (75)<br />

Malaysia<br />

Institutes:<br />

Forest Research Institute – 1964-1999 32 (2)<br />

Malaysia † Total 387 (100)<br />

*<br />

All counts for universities were based on dissertations. † For the Forest Research Institute Malaysia,<br />

counts were based on both dissertations and scientific articles from projects conducted in the Pasoh<br />

Field Station’s 50-hectare plot (Soepadmo et al. 2000).<br />

Control<br />

Diversity<br />

Biology<br />

Field of study<br />

Ecology<br />

Taxonomy<br />

Environmental monitoring<br />

Bioinformatics<br />

Forensics<br />

Biochemistry<br />

0 20 40 60 80 100 120 140<br />

Num ber of dissertations / articles<br />

Fig. 1. Numbers of dissertations/articles written on different entomological research areas in<br />

the institutions surveyed.<br />

In addition to the areas of entomological research mentioned above, there are also new and<br />

emerging areas of entomological research, such as environmental monitoring using insects as<br />

indicator species, bioinformatics, forensics and insect biochemistry. Together, they contributed<br />

to a very small number (eight) of the 387 dissertations, reports and articles written, among the<br />

four institutions surveyed.<br />

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OVERVIEW OF INSECT BIODIVERSITY RESEARCH IN PENINSULAR MALAYSIA<br />

TRENDS IN RELATION TO INSECT ORDERS STUDIED<br />

Figure 2 shows the number of dissertations/articles written on the different insect groups in<br />

the four institutions surveyed. About 15 insect orders have been the subject of studies. They<br />

represent slightly less than half of all recognised insect orders. The most researched insect<br />

order was Lepidoptera (butterflies and moths), while Neuroptera, Plecoptera, Thysanura and<br />

Collembola were the least studied groups. Other orders that were the focus of much<br />

entomological research were Coleoptera, Hymenoptera, Homoptera, Diptera, Hemiptera,<br />

Orthoptera and Isoptera, in decreasing frequency. To some extent, the level of research on the<br />

different orders reflects the size of the order, for example, Coleoptera and Hymenoptera are<br />

the largest and second largest insect orders, respectively. It also reflects their economic<br />

importance in agriculture and forestry, as pests (e.g., many Coleoptera and Hemiptera) or as<br />

beneficial insects (e.g., Hymenoptera). There were also many entomological dissertations /<br />

articles written that were not on any specific insect order; many were comparative studies on<br />

the composition of invertebrate communities in natural and disturbed environments.<br />

General<br />

Lepidoptera<br />

Coleoptera<br />

Hymenoptera<br />

Hom optera<br />

Insect order<br />

Diptera<br />

Hemiptera<br />

Orthoptera<br />

Isoptera<br />

Odonata<br />

Neuroptera<br />

Plecoptera<br />

Collembola<br />

Acarina<br />

0 10 20 30 40 50 60 70 80 90 100<br />

No. of dissertations / articles<br />

Fig. 2. Numbers of dissertations / articles written on different insect orders in the institutions<br />

surveyed. The category, ‘General,’ refers to dissertations / articles that did not specify a specific<br />

insect order, or that were about invertebrate or insect communities in general. Dissertations /<br />

articles on Acarina (mites) are included for comparison.<br />

AVAILABILITY OF TAXONOMIC INFORMATION ON THE<br />

DIFFERENT INSECT ORDERS<br />

The level of taxonomic information available on several insect orders in Peninsular Malaysia<br />

is compared against the size of the different orders in Table 2. The order Coleoptera (beetles)<br />

is well-known as the most diverse and numerous in the animal kingdom. However, there is a<br />

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SHAWN CHENG & LAURENCE G. KIRTON (2007)<br />

great void of information on Coleoptera in Malaysia. Although some groups have been relatively<br />

well-studied (e.g., Chrysomelidae), on the whole there is very little documentation of the<br />

taxonomy of most groups of beetles. Lepidoptera (butterflies and moths) is another vastly<br />

diverse group, but it has been relatively well-studied in Peninsular Malaysia. Moths are much<br />

more diverse than butterflies, and although there are several good monographs on them, much<br />

more work is needed to document their diversity in Peninsular Malaysia as well as in Sabah<br />

and Sarawak. The Isoptera (termites) and Phasmida (stick insects) are two other relatively<br />

well-studied groups in Peninsular Malaysia, although many unresolved taxonomic problems<br />

are recognised to exist the Isoptera (Tho 1992).<br />

Table 2. Comparison of relative species diversity and the level of taxonomic information<br />

available for some insect orders occurring in Peninsular Malaysia.<br />

Order Relative size * Availability of Monographs available<br />

taxonomic information<br />

1. Coleoptera * * * * * * * * * * Very low -<br />

2. Lepidoptera * * * * * * * * High Butterflies: Fleming (1983),<br />

Corbet & Pendlebury (1992);<br />

Moths: Holloway (1976) † ,<br />

Barlow (1982)<br />

3. Hymenoptera * * * * * * Very low -<br />

4. Diptera * * * * * Very low -<br />

5. Hemiptera * * * * Very low -<br />

6. Homoptera * * * Very low -<br />

7. Orthoptera * * * Very low -<br />

8. Collembola * * Very low -<br />

9. Isoptera * * Moderate Tho (1992)<br />

10. Phasmida * High Brock (1999), Seow-Choen<br />

(2000)<br />

11. Thysanura * Very low -<br />

*<br />

Relative size of the order is based on figures given in Romoser & Stoffolano (1998).<br />

†<br />

In addition, there is a further series of publications on the moths of Borneo by Holloway (1983, 1985,<br />

1986, 1987, 1988, 1993, 1996, 1997, 1998, 1999, 2001). Many parts of this series are also available on<br />

the World Wide Web (http://www.mothsofborneo.com). Although based on specimens from Borneo,<br />

Holloway’s work is a useful reference for Peninsular Malaysia as well.<br />

Orders that have been relatively well studied are, to some extent, those that have attractive<br />

species (e.g., butterflies, moths and stick insects) or that have some importance in agriculture<br />

and forestry (e.g., termites). It is also worth noting that a number of monographs were authored<br />

by individuals who were not entomologists by profession, but who pursued the study of insects<br />

privately (e.g., the monographs on butterflies and stick insects).<br />

In spite of its large number of species, many of which are beneficial insects, taxonomic<br />

information on the Hymenoptera (bees, wasps and ants) in Peninsular Malaysia is still very<br />

lacking. Other relatively large groups that have been little studied are the Diptera, Hemiptera,<br />

Homoptera, and Orthoptera. Many groups of insects for which taxonomic information is still<br />

lacking are important in ecosystem functions such as pollination, predation, phytophagy and<br />

the promotion of soil stability.<br />

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OVERVIEW OF INSECT BIODIVERSITY RESEARCH IN PENINSULAR MALAYSIA<br />

CURRENT AND FUTURE NEEDS FOR INSECT DIVERSITY<br />

RESEARCH IN MALAYSIA<br />

As in most other countries, economically important insect pest species have been an important<br />

area of research in Malaysia. Research has often been driven by the need to develop management<br />

strategies for such pest species, thus, studies on insect control were highest in frequency in the<br />

institutions surveyed. Insect diversity studies ranked second in number. However, many utilised<br />

indices of diversity (e.g., Simpson’s D & E and the Shannon diversity index) to measure<br />

biodiversity richness (or poorness). In many such studies, specimens are sorted based on<br />

phenotypes (termed “recognisable taxonomic units”) to obtain diversity indices for different<br />

study areas. While this method allows for the comparison of animal or plant richness, it does<br />

little to enable the understanding of biological and ecological systems.<br />

At the heart of understanding biological and ecological systems in an ecosystem is the<br />

understanding of the species that make up the diversity of the ecosystem, and the interactions<br />

of these species with other each other and with their environment. Such an understanding is<br />

only made possible through taxonomic work that enables us to identify species and provides<br />

a foundation upon which we can build on our knowledge of their biology, behaviour and<br />

ecological functions. In spite of this, taxonomic studies were poorly represented in the<br />

institutions surveyed, ranking last in number among mainstream areas of research such as<br />

diversity, ecology and biology.<br />

The few studies on insect taxonomy that have been conducted in the country have primarily<br />

been on specific insect groups. Many insect groups have been poorly researched. The<br />

Hymenoptera, Diptera and Hemiptera, to name a few, are taxonomically diverse groups, yet<br />

there are no monographs on these insect groups in Malaysia. The Collembola and Thysanura<br />

are also poorly researched insect groups. Although small and rarely noticed, they are important<br />

in terrestrial ecosystems. Collembolans, for example, help in decomposition and nutrient cycling<br />

in the soil, while thrips are thought to be important pollinators of dipterocarp trees.<br />

Taxonomists shoulder the responsibility of documenting organic diversity, and their skills are<br />

also needed in many ecological studies. In addition to their role in documenting species,<br />

taxonomists also usually ensure the proper curation and maintenance of valuable reference<br />

collections, as well as work on the systematics of the groups of organisms they study. The<br />

field of systematics, which is an extension of taxonomy, analyses relationships between<br />

organisms and discusses origins or causes of diversity. Research on systematics can often<br />

indirectly provide more information on the biological and ecological interactions of species<br />

than studies on diversity, yet it has rarely been pursued as a subject of research in the institutions<br />

surveyed. The dearth of taxonomic or systematic studies on insects is a serious cause for<br />

worry; our limited capacity to identify insects inadvertently limits our capacity to document at<br />

least three quarters of our country’s biological diversity.<br />

CONCLUSION<br />

The dearth of taxonomic information on the majority of insect orders in Peninsular Malaysia<br />

is a matter of great concern, because one of the prerequisites in any effort to conserve species<br />

is that they need to be identified and described. Most insect orders remain poorly studied in<br />

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SHAWN CHENG & LAURENCE G. KIRTON (2007)<br />

Peninsular Malaysia. There is a great need for taxonomic and systematic studies on insects in<br />

Malaysia, especially on many of the less popular insect groups. In addition, taxonomists and<br />

systematists need to be provided with adequate funds and incentives that will enable them to<br />

conduct their research, purchase relevant equipment and discuss and present their work. At<br />

the administrative and political level, there needs to be sustained interest and commitment to<br />

funding to ensure that insect diversity is properly documented and described. The success of<br />

Malaysia’s initiative to inventorise its biodiversity greatly depends on sustained political will.<br />

ACKNOWLEDGEMENTS<br />

We wish to thank Ms. Sheena Jeremiah and Mr. Jeyakumar for their assistance in data collection.<br />

Our thanks also go to the custodians of the various resource centres at Universiti Malaya,<br />

Universiti Kebangsaan Malaysia and Universiti Pertanian Malaysia for permission to use their<br />

reference libraries.<br />

REFERENCES<br />

BARLOW, H.S. 1982. An Introduction to the Moths of South East Asia. Malayan Nature<br />

Society, Kuala Lumpur. 305 pp.<br />

BROCK, P.D. 1999. Stick and Leaf insects of Peninsular Malaysia and Singapore. Malayan<br />

Nature Society, Kuala Lumpur. 222 pp.<br />

CORBET, S.A. & PENDLEBURY, H.M. 1992. The Butterflies of the Malay Peninsula. 4th<br />

edition. Revised by Eliot, J.N. Malayan Nature Society, Kuala Lumpur. 595 pp.<br />

CYRANOSKI, D. 2005. Malaysia plans ‘red book’ in its attempt to go green. Nature 436:<br />

313.<br />

ERWIN, T.L. 1983. Tropical forest canopies: the last biotic frontier. Bulletin of the<br />

Entomological Society of America 29: 14–19.<br />

FLEMING, W.A. 1983. Butterflies of West Malaysia and Singapore. 2 nd edition. Revised by<br />

McCartney, A. Longman Malaysia, Kuala Lumpur. 148 pp.<br />

HOLLOWAY, J.D. 1976. Moths of Borneo with Special Reference to Mount Kinabalu. Malayan<br />

Nature Society, Kuala Lumpur. 264 pp.<br />

HOLLOWAY, J.D. 1983. The moths of Borneo: family Notodontidae. Malayan Nature Journal<br />

37: 1–107.<br />

HOLLOWAY, J.D. 1985. The moths of Borneo: family Noctuidae: subfamilies Euteliinae,<br />

Stictopterinae, Plusiinae, Pantheinae. Malayan Nature Journal 38: 157–317.<br />

HOLLOWAY, J.D. 1986. The moths of Borneo: key to families; families Cossidae,<br />

Metarbelidae, Ratardidae, Dudgeoneidae, Epipyropidae and Limacodidae. Malayan Nature<br />

Journal 40: 1–165.<br />

HOLLOWAY, J.D. 1987. The Moths of Borneo, part 3. Southdene Sdn. Bhd., Kuala Lumpur.<br />

199 pp.<br />

HOLLOWAY, J.D. 1988. The Moths of Borneo, part 6. Southdene Sdn. Bhd., Kuala Lumpur.<br />

101 pp.<br />

HOLLOWAY, J.D. 1993. The moths of Borneo: family Geometridae, subfamily Ennominae.<br />

Malayan Nature Journal 47: 1–309.<br />

HOLLOWAY, J.D. 1996. The moths of Borneo: family Geometridae, subfamilies Oenochrominae,<br />

Desmobathrinae and Geometrinae. Malayan Nature Journal 49: 147–326.<br />

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OVERVIEW OF INSECT BIODIVERSITY RESEARCH IN PENINSULAR MALAYSIA<br />

HOLLOWAY, J.D. 1997. The moths of Borneo: family Geometridae, subfamilies Sterrhinae<br />

and Larentiinae. Malayan Nature Journal 51: 1–242.<br />

HOLLOWAY, J.D. 1998. The moths of Borneo: families Castniidae, Callidulidae, Drepanidae<br />

and Uraniidae. Malayan Nature Journal 52: 1–155.<br />

HOLLOWAY, J.D. 1999. The moths of Borneo: Lymantriidae. Malayan Nature Journal 53:<br />

1–188.<br />

HOLLOWAY, J.D. 2001. The moths of Borneo: family Artiidae, subfamily Lithosiinae.<br />

Malayan Nature Journal 55: 279–486.<br />

KOH, L.C. 2005. Malaysia to prepare inventory of ecosystem this year. The New Straits<br />

Times, 24 January 2005. p. 2.<br />

MAY, R. 2002. Biological Diversity in a Crowded World: Past, Present and Likely Future.<br />

Essay. . February 2002.<br />

MAYR, E. & ASHLOCK, P.D. 1991. Principles of Systematic Zoology. McGraw-Hill, New<br />

York. 475 pp.<br />

ROMOSER, W.S. & STOFFALANO, J.G., JR. 1998. The Science of Entomology. 4 th edition.<br />

McGraw-Hill, Singapore. 605 pp.<br />

SEOW-CHOEN, F. 2000. An Illustrated Guide to the Stick and Leaf Insects of Peninsular<br />

Malaysia and Singapore. Natural History Publications (Borneo), Kota Kinabalu. 173 pp.<br />

SOEPADMO, E., MANOKARAN, N., NOORSIHA, A., JULIA, S., QUAH, E.S. & CHUNG,<br />

R.C.K. 2000. Ecological Studies in Pasoh Forest Reserve, Negeri Sembilan, Peninsular<br />

Malaysia (1964-1999). Forest Research Institute Malaysia, Kuala Lumpur (unpublished<br />

booklet). 32 pp.<br />

THO,Y.P. 1992. Termites of Peninsular Malaysia. Kirton, L.G. (ed.). Forest Research Institute<br />

Malaysia, Kuala Lumpur. 224 pp.<br />

WILSON, E.O. 1992. The Diversity of Life. Harvard University Press, Cambridge,<br />

Massachusetts. 413 pp.<br />

128


CHEY VUN KHEN (2007)<br />

STATUS OF BIOLOGICAL DIVERSITY IN MALAYSIA &<br />

THREAT ASSESSMENT OF PLANT SPECIES IN MALAYSIA<br />

RESEARCH ON THE DIVERSITY OF MOTHS AND<br />

BUTTERFLIES IN MALAYSIA AND THEIR USE AS<br />

BIODIVERSITY INDICATORS<br />

Chey Vun Khen<br />

ABSTRACT<br />

The two geographical regions of Malaysia namely the Malay Peninsula and Sabah and Sarawak<br />

in Borneo, share a large proportion of their biodiversity including many moth and butterfly<br />

species. There are about 4,000 species of larger moths and 936 species of butterflies in Borneo.<br />

The Malay Peninsula has 1,031 species of butterflies, about 88 % of which are also found in<br />

Borneo. Their suitability as indicators of biodiversity is discussed: moths and butterflies are<br />

better known taxonomically in Malaysia, they respond rapidly to habitat change, their<br />

caterpillars being mainly phytophagous reflect the vegetation type being sampled, and moths<br />

especially are more speciose and easily sampled using a light-trap, which facilitates data<br />

analysis. The main biodiversity indices used are explained: for moth samples, Williams Alpha<br />

based on the log series is most appropriate, and for butterflies, which normally have smaller<br />

samples, non-parametric indices–e.g., the Shannon and Simpson indices – are commonly used.<br />

Research work on the diversity of moths and butterflies in Malaysia is also reviewed.<br />

INTRODUCTION<br />

Malaysia comprises two regions in Sundaland separated by the South China Sea, namely the<br />

Malay Peninsula and Sabah and Sarawak in the island of Borneo. Despite the geographical<br />

separation, the two regions share a large proportion of their biodiversity, including many<br />

species of moths and butterflies (Insecta: Lepidoptera), as they were joined by land when sea<br />

levels were lower in the last ice age.<br />

Butterflies are the most glamorous insects, and they have been better studied worldwide<br />

compared to all other insect groups. In the Malay Peninsula, there are 1,031 species, with 21<br />

endemics (Corbet & Pendlebury 1992), while the number of species is lower in the island of<br />

Borneo (936) but with a much higher number of endemics (94) (Ohtsuka 1996). About 88 %<br />

of the species in the Malay Peninsula are also found in Borneo. However, most of them occur<br />

as different subspecies in the two different regions. Half of the species are distributed in the<br />

Forest Research Centre (Sepilok), Sabah Forestry Department, P.O. Box 1407, 90715 Sandakan, Sabah. Malaysia.<br />

Fax: 089-531068. Email: VunKhen.Chey@sabah.gov.my<br />

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BIODIVERSITY INDICATORS<br />

lowlands below 750 m, and one-seventh of the species occur in the highlands. The rest are<br />

found in habitats at both elevations.<br />

Moths are more speciose than butterflies, and taxonomically they have been better studied in<br />

Borneo than in the Malay Peninsula. They are commonly divided into the bigger macromoths<br />

and the smaller micromoths. According to Holloway (pers. comm.), there are just over 4,000<br />

species of macromoths in Borneo. Most of them are also found in the Malay Peninsula. Robinson<br />

& Tuck (1993) estimated the number of species of the lesser-studied micromoths in South-<br />

East Asia to be more than 6,000, with most of the species occurring in Malaysia. Moths are<br />

more diverse between 500 metres and 1,000 metres above sea level (Chey 1998), where there<br />

is an overlap of both lowland and montane elements.<br />

THREATENED SPECIES<br />

CITES (2001) includes all the birdwing butterflies (Troides spp.) in Appendix II. This also<br />

covers the exceedingly beautiful Rajah Brooke’s Birdwing, Troides (Trogonoptera) brookiana,<br />

found in Malaysia. In the IUCN Red Data Book on threatened swallowtail butterflies of the<br />

world (Collins & Morris 1985), three endemic species found in Malaysian Borneo are listed<br />

in the threatened categories, namely Papilio acheron, Graphium procles, and Troides<br />

andromache. They are mainly montane species. Another two species, Papilio mahadeva (in<br />

the Malay Peninsula) and Papilio karna (in Borneo), were said to require further monitoring<br />

and research. However, it is not only the sought-after, showy butterflies, which are threatened.<br />

As more lowland forests are being cleared, the families with a high proportion of lowland<br />

endemics with forest-restricted distribution, such as the lasiocampid and limacodid moths<br />

(Holloway & Barlow 1992) and the satyrid and amathusiid butterflies (Hamer et al. 2003), are<br />

losing much of their habitat. Paradoxically some species of limacodids may be able to persist<br />

(a few with pest status) in palm plantations such as oil palm and coconut.<br />

TAXONOMY<br />

The main taxonomic monograph on butterflies in the Malay Peninsula was written by Corbet<br />

& Pendlebury (4 th edition, 1992, revised and enlarged by J.N. Eliot). Volumes written by<br />

Otsuka (1988) on the bigger butterflies (Papilionidae, Pieridae and Nymphalidae), Seki et al.<br />

(1991) on the Lycaenidae and Maruyama (1991) on the Hesperiidae form the primary<br />

monograph in Borneo. Revisions of some groups are also being carried out, e.g., the rattanfeeding<br />

hesperiid genus, Zela (Kirton & Eliot 2004). Abang et al. (2004) described 11 new<br />

subspecies of butterflies of the families Pieridae, Nymphalidae, and Lycaenidae found in<br />

Balambangan island, Borneo.<br />

For moths, introductory monographs have been published by Barlow (1982), focusing mainly<br />

on macromoths, and Robinson et al. (1994), focusing on micromoths. A major taxonomic<br />

work on the macros is being published in the “Moths of Borneo” series by Holloway (1983,<br />

1985, 1986, 1987, 1988, 1989a, 1993, 1996, 1997, 1998, 1999, 2001, 2003). A further volume,<br />

consisting of two more parts, is about to go to press at the time of writing.<br />

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CHEY VUN KHEN (2007)<br />

Local collections of Lepidoptera are kept mainly in the forest research institutions of Peninsular<br />

Malaysia, Sabah and Sarawak. The Sabah Forest Insect Museum in Sepilok, for example,<br />

houses more than 2,400 species of macromoths with 18,000 pinned specimens. Various other<br />

collections are also maintained by universities and other research institutions. In addition,<br />

there are privately owned collections, such as that of Dato’ Henry Barlow, who keeps an<br />

excellent collection of moths in his residence in Genting Sempah. By and large most of the<br />

collections with type specimens are housed in the major museums in developed countries, for<br />

example, the Natural History Museum in London.<br />

INDICATORS OF BIODIVERSITY<br />

Biodiversity on a global scale is estimated to be about 10 million species, and over 60 % are<br />

insects (Speight et al. 1999). Since the insect fauna is a major proportion of the biodiversity in<br />

a terrestrial ecosystem such as the tropical rain forest, human disturbance such as forest<br />

conversion will have a telling effect on it. The insect group that fulfils most criteria as effective<br />

indicators of changes in biodiversity is moths (Holloway & Stork 1991).<br />

Taxonomy is the foundation of biodiversity, and its importance is underlined when insect<br />

groups are being used as bioindicators. To avoid confusion such as pooling of sibling species,<br />

which would adversely affect data, insect groups with better known taxonomy are preferred.<br />

Compared to other insect groups, moths (especially the macromoths) are the best known<br />

taxonomically after butterflies. Butterflies, however, are fewer in species and less readily<br />

sampled, which makes data analysis more difficult. Moths are easily sampled using a lighttrap<br />

at night and, being more speciose, they provide a larger data set that is easier to analyse.<br />

Compared to vertebrates such as mammals or birds, which are less readily observed or sampled,<br />

moths, for the afore-mentioned reasons, are relatively easily sampled.<br />

In their larval stage, moths and butterflies are mainly phytophagous leaf-feeders (Holloway et<br />

al. 2001; Robinson et al. 2001), but the caterpillars of some species of moths belong to other<br />

guilds such as detrivores of plant and animal material, flower, fruit, and seed predators, stem<br />

borers, lichen and algal browsers, fungal feeders and insectivores (Holloway & Stork 1991).<br />

Some of them are stenotopic species restricted to a certain habitat, some are specialists with<br />

limited ecological tolerance or are host-plant specific, while others are generalists indicative<br />

of disturbed habitat. Moths of the Lophoptera lineage (Noctuidae: Stictopterinae) have<br />

caterpillars that are known to be leaf-feeders of Dipterocarpaceae, and species in this group<br />

are likely to be absent in highly degraded forest sites (Chey 2002). Thus, abundance or absence<br />

of the moths will reflect on the composition of the vegetation in the area being sampled.<br />

Rapid and sensitive response to environmental disturbance is a prerequisite for a bioindicator.<br />

Moths and butterflies generally have short life cycles and respond rapidly to changes in the<br />

environment. Species with limited ecological tolerance can only thrive in an undisturbed forest<br />

environment and will be the first to disappear after human disturbance. Most generalists or r-<br />

strategists, on the other hand, are opportunists distributed over a wide range of ecological<br />

gradients, and they rapidly increase in abundance as a result of disturbance. They particularly<br />

favour early successional stages in ecological regeneration, and many are pests of crops.<br />

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BIODIVERSITY INDICATORS<br />

BIODIVERSITY INDICES<br />

Species abundance models are commonly used to indicate the level of biodiversity in a habitat,<br />

with the log normal and the log series being the main models. They are based on an assumption<br />

that for a very large sample that closely reflects the population structure, it will result in a bellshaped<br />

log normal curve. But a typical smaller annual sample is one-tailed and usually fits<br />

equally well to the log series and the log normal, with the rarer species having been missed.<br />

Species abundance curves usually have the log abundance plotted against species rank. A<br />

shallower curve means higher diversity while a steeper curve means lower diversity.<br />

Moth samples are usually annual samples, which fit into the log series. Based on the log<br />

series, a diversity index known as Williams Alpha is derived (Fisher et al. 1943). This index<br />

is independent of sample size, which allows cross-comparison of most samples. The log series<br />

gives a diversity value less subject to the vagaries of the non-resident species, and is more<br />

dependent on the mid-range species resident at the site, and hence more representative (Taylor<br />

1978). For these reasons, most moth samples are compared using Williams Alpha. A higher<br />

value means higher diversity.<br />

For butterfly samples, which are normally smaller, non-parametric indices with no assumption<br />

on the underlying species abundance distribution are commonly used. These include the popular<br />

Shannon index, as well as Simpson’s index (Magurran 1988). They are diversity indices based<br />

on the proportional abundances of species.<br />

SIMILARITY COEFFICIENTS<br />

Biodiversity indices alone may tell us the levels of diversity but they don’t show the composition<br />

of the underlying species assemblages. The ‘coefficient of association’ is a R-mode measure<br />

of percentage dissimilarity showing the pattern in species distributions and, hence, species<br />

associations, among the sampling sites. Based on the percentage dissimilarity, numerical singlelink<br />

dendrograms as well as linkage diagrams can be drawn in which species indicative of a<br />

habitat are clustered together. This technique has been applied in biodiversity studies in<br />

Malaysia, for example, by Chey (1994).<br />

Similarity coefficients can also be used in the R-mode to identify associations of species of<br />

moths that show correlations with particular vegetation zones and altitude zones (e.g., Holloway<br />

1989b; Chey et al. 1997; Intachat et al. 2005). These associations offer particularly good<br />

suites of indicator species.<br />

Preston’s coefficient of faunal resemblance (1962), a simpler Q-mode measure of similarity<br />

based on presence or absence of species, is commonly used. The number of species present in<br />

each of any two sites and the number of shared species between them are used to calculate the<br />

Preston’s coefficient. Based on the coefficient values, single-link dendrograms can be drawn<br />

clustering similar sites together.<br />

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CHEY VUN KHEN (2007)<br />

RESEARCH REVIEW<br />

Apart from the taxonomic work mentioned earlier, most of the research work on diversity of<br />

moths and butterflies in Malaysia has focused on their use as bioindicators of habitat quality<br />

and habitat change.<br />

The specialist of Bornean macromoths, Dr. Jeremy Holloway in London, started his association<br />

with Borneo back in 1965 when a Cambridge expedition to Mount Kinabalu was organised. A<br />

paper giving a numerical analysis of the Kinabalu moth samples was published (Holloway<br />

1970), as well as a taxonomic monograph on the moths of Mount Kinabalu (Holloway 1976).<br />

Thereafter, he has been consistently publishing taxonomic monographs in his “Moths of<br />

Borneo” series. Apart from that, he also publishes papers on moth ecology, particularly on the<br />

use of moths as indicators in comparing forest habitats in Malaysia. His papers include one on<br />

the larger moths of Gunung Mulu in Sarawak (Holloway 1984), and the response of moths to<br />

forest conversion in Sabah (Holloway et al. 1992).<br />

Dr. Holloway also trained up two Malaysian entomologists working on moths. One is the<br />

present author who used moths to compare the biodiversity between plantation and natural<br />

forests in Sabah (Chey 1994; Chey et al. 1997), and who later studied the moth diversity of<br />

Lanjak-Entimau in Sarawak (Chey 2000a; 2000b). Another is Dr. Jurie Intachat of FRIM,<br />

who assessed moth diversity in natural and managed forests in Peninsular Malaysia (Intachat<br />

1995; Intachat et al. 1999a; 1999b; 2005). Chey worked on the whole spectrum of macromoths<br />

to inventory biodiversity, while Intachat focused on the geometroid moths specifically to<br />

monitor change.<br />

Others who have worked on moth diversity in Borneo include the German researchers Schulze<br />

& Fiedler (1996, 1997) and Beck et al. (2002).<br />

Research on butterflies as indicators of forest disturbance in Sabah has been carried out since<br />

the mid 1990s by Dr. Jane Hill of the UK and her colleagues. Their papers include species<br />

abundance models (Hill & Hamer 1998), comparison of butterflies in rain forest gaps and<br />

closed-canopy forests (Hill et al. 2001) as well as in natural and selectively logged forests<br />

(Hamer et al. 2003), and the effects of rainfall as opposed to logging on the abundance of a<br />

selected butterfly species (Hill et al. 2003). They used fruit-baited traps, which were also used<br />

to study vertical stratification of activity (Tangah et al. 2004), as well as walk-and-count<br />

ground-based surveys.<br />

In addition to these studies, a lot of general information on moths and butterflies in Malaysia<br />

is provided in the handbook by Holloway et al. (2001) and in the hostplant book by Robinson<br />

et al. (2001).<br />

ACKNOWLEDGEMENT<br />

Dr. J.D. Holloway of the Natural History Museum in London kindly commented on the<br />

manuscript.<br />

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BIODIVERSITY INDICATORS<br />

REFERENCES<br />

ABANG, F., TREADAWAY, C.G. & SCHROEDER, H.G. 2004. A contribution to the butterfly<br />

fauna of the island of Balambangan (Malaysia, Sabah). Futao No. 47: 1–13.<br />

BARLOW, H.S. 1982. An Introduction to the Moths of South East Asia. With plates by B.<br />

D’Abrera. Malayan Nature Society, Kuala Lumpur. 305 pp.<br />

BECK, J., SCHULZE, C.H., LINSENMAIR, K.E. & FIEDLER, K. 2002. From forest to<br />

farmland: diversity of geometrid moths along two habitat gradients on Borneo. Journal<br />

of Tropical Ecology 18: 33–51.<br />

CHEY, V.K. 1994. Comparison of biodiversity between plantation and natural forests in Sabah<br />

using moths as indicators. D.Phil. thesis, Oxford University. 284 pp.<br />

CHEY, V.K. 1998. Butterflies and moths. Pp. 102–103 in Yong, H.S. (ed.) The Encyclopedia<br />

of Malaysia, Volume 3: Animals. Archipelago Press, Editions Didier Millet, Singapore.<br />

CHEY, V.K. 2000a. Insects. Pp. 93–105 in Soepadmo, E. & Chai, P.P.K. (eds.) Development<br />

of Lanjak-Entimau Wildlife Sanctuary as a Totally Protected Area. Phase I & Phase II.<br />

1993–1999. Scientific Report. ITTO, Yokohama & Sarawak Forest Department, Kuching.<br />

CHEY, V.K. 2000b. Moth diversity in the tropical rain forest of Lanjak-Entimau, Sarawak,<br />

Malaysia. Malayan Nat. J. 54(4): 305–318.<br />

CHEY, V.K. 2002. Comparison of moth diversity between lightly and heavily logged sites in<br />

a tropical rain forest. Malayan Nat. J. 56(1): 23–41.<br />

CHEY, V.K., HOLLOWAY, J.D. & SPEIGHT, M.R. 1997. Diversity of moths in forest<br />

plantations and natural forests in Sabah. Bulletin of Entomological Research 87: 371–<br />

385.<br />

CITES. 2001. CITES Handbook. CITES Secretariat, Switzerland.<br />

COLLINS, N.M. & MORRIS, M.G. 1985. Threatened Swallowtail Butterflies of the World.<br />

The IUCN Red Data Book. IUCN, Gland & Cambridge, UK. 401 pp.<br />

CORBET, A.S. & PENDLEBURY, H.M. 1992. The Butterflies of the Malay Peninsula. 4 th ed.<br />

rev. J.N. Eliot with plates by B. D’Abrera. Malaysian Nature Society, Kuala Lumpur. 595<br />

pp.<br />

FISHER, R.A., CORBET, A.S. & WILLIAMS, C.B. 1943. The relation between the number<br />

of species and the number of individuals in a random sample of an animal population. J.<br />

Anim. Ecol. 12: 42–58.<br />

HAMER, K.C., HILL, J.K., BENEDICK, S., MUSTAFFA, N., SHERRATT, T.N., MARYATI,<br />

M. & CHEY, V.K. 2003. Ecology of butterflies in natural and selectively logged forests<br />

of northern Borneo: the importance of habitat heterogeneity. Journal of Applied Ecology<br />

40: 150–162.<br />

HILL, J.K. & HAMER, K.C. 1998. Using species abundance models as indicators of habitat<br />

disturbance in tropical forests. Journal of Applied Ecology 35: 458–460.<br />

HILL, J.K., HAMER, K.C., TANGAH, J. & DAWOOD, M. 2001. Ecology of tropical<br />

butterflies in rainforest gaps. Oecologia 128: 294–302.<br />

HILL, J.K., HAMER, K.C., DAWOOD, M.M., TANGAH, J. & CHEY, V.K. 2003. Rainfall<br />

but not selective logging affect changes in abundance of a tropical forest butterfly in<br />

Sabah, Borneo. Journal of Tropical Ecology 19: 35–42.<br />

HOLLOWAY, J.D. 1970. The biogeographical analysis of a transect sample of the moth fauna<br />

of Mt. Kinabalu, Sabah, using numerical methods. Biol. J. Linn. Soc. 2: 259–286.<br />

HOLLOWAY, J.D. 1976. Moths of Borneo with special reference to Mount Kinabalu. Malayan<br />

Nature Society & Sabah Foundation. 264 pp.<br />

134


CHEY VUN KHEN (2007)<br />

HOLLOWAY, J. D. 1983. The moths of Borneo: family Notodontidae. Malayan Nat. J. 37: 1–<br />

107.<br />

HOLLOWAY, J.D. 1984. The larger moths of the Gunung Mulu National Park: a preliminary<br />

assessment of their distribution, ecology, and potential as environmental indicators. Pp.<br />

149–190 in Jermy, A.C. & Kavanagh, K.P. (eds.) Gunung Mulu National Park, Sarawak,<br />

Part II. Sarawak Museum Journal 30. Special Issue 2.<br />

HOLLOWAY, J.D. 1985. The moths of Borneo: family Noctuidae: subfamilies Euteliinae,<br />

Stictopterinae, Plusiinae, Pantheinae. Malayan Nat. J. 38: 157–317.<br />

HOLLOWAY, J.D. 1986. The moths of Borneo: key to families; families Cossidae,<br />

Metarbelidae, Ratardidae, Dudgeoneidae, Epipyropidae, Limacodidae. Malayan Nat. J.<br />

40: 1–166.<br />

HOLLOWAY, J.D. 1987. The moths of Borneo: superfamily Bombycoidea: families<br />

Lasiocampidae, Eupterotidae, Bombycidae, Brahmaeidae, Saturniidae, Sphingidae.<br />

Southdene, Kuala Lumpur. 199 pp.<br />

HOLLOWAY, J.D. 1988. The moths of Borneo: family Arctiidae, subfamilies Syntomiinae,<br />

Euchromiinae, Arctiinae; Noctuidae misplaced in Arctiidae (Camptoloma, Aganainae).<br />

Southdene, Kuala Lumpur. 101 pp.<br />

HOLLOWAY, J.D. 1989a. The moths of Borneo: family Noctuidae, trifine subfamilies:<br />

Noctuinae, Heliothinae, Hadeninae, Acronictinae, Amphipyrinae, Agaristinae. Malayan<br />

Nat. J. 42: 57–226.<br />

HOLLOWAY, J.D. 1989b. Moths. Pp. 437–453 in Lieth, H. & Werger, M.J.A. (eds.) Tropical<br />

Rain Forest Ecosystems. Elsevier Science Publishers, Amsterdam.<br />

HOLLOWAY, J.D. 1993. The moths of Borneo: family Geometridae, subfamily Ennominae.<br />

Malayan Nat. J. 47: 1–309.<br />

HOLLOWAY, J.D. 1996. The moths of Borneo: family Geometridae, subfamilies<br />

Oenochrominae, Desmobathrinae, Geometrinae. Malayan Nat. J. 49: 147–326.<br />

HOLLOWAY, J.D. 1997. The moths of Borneo: family Geometridae, subfamilies Sterrhinae,<br />

Larentiinae. Malayan Nat. J. 51: 1–242.<br />

HOLLOWAY, J.D. 1998. The moths of Borneo: families Castniidae, Callidulidae, Drepanidae<br />

and Uraniidae. Malayan Nat. J. 52: 1–155.<br />

HOLLOWAY, J.D. 1999. The moths of Borneo: family Lymantriidae. Malayan Nat. J. 53: 1–<br />

188.<br />

HOLLOWAY, J.D. 2001. The moths of Borneo: family Arctiidae, subfamily Lithosiinae.<br />

Malayan Nat. J. 55: 279–486.<br />

HOLLOWAY, J.D. 2003. The moths of Borneo: family Nolidae. Southdene, Kuala Lumpur.<br />

279 pp.<br />

HOLLOWAY, J.D. & BARLOW, H.S. 1992. Potential for loss of biodiversity in Malaysia,<br />

illustrated by the moth fauna. Pp. 293–311 in Abdul Aziz S.A. Kadir & Barlow, H.S.<br />

(eds.) Pest Management and the Environment in 2000. CAB International & Agricultural<br />

Institute of Malaysia.<br />

HOLLOWAY, J.D. & STORK, N.E. 1991. The dimensions of biodiversity: the use of<br />

invertebrates as indicators of human impact. Pp. 37–61 in Hawksworth, D.L. (ed.) The<br />

Biodiversity of Microorganisms and Invertebrates: Its Role in Sustainable Agriculture.<br />

CAB International.<br />

HOLLOWAY, J.D., KIRK-SPRIGGS, A.H. & CHEY, V.K. 1992. The response of some rain<br />

forest insect groups to logging and conversion to plantation. Phil. Trans. R. Soc. Lond. B<br />

335: 425–436.<br />

135


RESEARCH ON THE DIVERSITY OF MOTHS AND BUTTERFLIES IN MALAYSIA AND THEIR USE AS<br />

BIODIVERSITY INDICATORS<br />

HOLLOWAY, J.D., KIBBY, G. & PEGGIE, D. 2001. The Families of Malesian Moths and<br />

Butterflies (Fauna Malesiana Handbooks, Vol. 3). Brill Academic Publishers, Leiden.<br />

456 pp.<br />

INTACHAT, J. 1995. Assessment of moth diversity in natural and managed forests in Peninsular<br />

Malaysia. D.Phil. thesis. Oxford University. 156 pp.<br />

INTACHAT, J., HOLLOWAY, J.D. & SPEIGHT, M.R. 1999a. The impact of logging on<br />

geometroid moth populations and their diversity in lowland forests of Peninsular Malaysia.<br />

Journal of Tropical Forest Science 11(1): 61–78.<br />

INTACHAT, J., CHEY, V.K., HOLLOWAY, J.D. & SPEIGHT, M.R. 1999b. The impact of<br />

forest plantation development on the population and diversity of geometrid moths<br />

(Lepidoptera: Geometridae) in Malaysia. Journal of Tropical Forest Science 11(2): 329–<br />

336.<br />

INTACHAT, J., HOLLOWAY, J.D. & SPEIGHT, M.R. 2005. A preliminary assessment of the<br />

diversity of geometroid moths within different types of forests in Peninsular Malaysia.<br />

Malayan Nat. J. 57(1): 1–28.<br />

KIRTON, L.G. & ELIOT, J.N. 2004. A revision of the rattan-feeding skipper genus, Zela de<br />

Niceville (Lepidoptera: Hesperiidae). Malayan Nat. J. 56(4): 317–367.<br />

MAGURRAN, A.E. 1988. Ecological Diversity and Its Measurement. Croom Helm, London.<br />

179 pp.<br />

MARUYAMA, K. 1991. Butterflies of Borneo Vol. 2 No. 2. Hesperiidae. Tobishima<br />

Corporation, Tokyo. 83 pp.<br />

OHTSUKA, K. 1996. Bornean butterflies examined through distribution. Fujimura Girls’<br />

High School, Tokyo. 52 pp.<br />

OTSUKA, K. 1988. Butterflies of Borneo Vol. 1. Tobishima Corporation, Tokyo. 61 pp.<br />

PRESTON, F.W. 1962. The canonical distribution of commonness and rarity. Ecology 43:<br />

185–215, 410–432.<br />

ROBINSON, G.S. & TUCK, K.R. 1993. Diversity and faunistics of small moths<br />

(Microlepidoptera) in Bornean rainforest. Ecological Entomology 18: 385–393.<br />

ROBINSON, G.S., TUCK, K.R. & SHAFFER, M. 1994. A Field Guide to the Smaller Moths<br />

of South-East Asia. With illustrations by K. Cook. The Natural History Museum, London<br />

& Malaysian Nature Society, Kuala Lumpur. 309 pp.<br />

ROBINSON, G.S., ACKERY, P.R., KITCHING, I.J., BECCALONI, G.W. & HERNANDEZ,<br />

L.M. 2001. Hostplants of the Moth and Butterfly Caterpillars of the Oriental Region. The<br />

Natural History Museum, London & Southdene, Kuala Lumpur. 744 pp.<br />

SCHULZE, C.H. & FIEDLER, K. 1996. First record of the family Dudgeoneidae (Lepidoptera,<br />

Ditrysia) from Borneo. Tinea 15: 74–77.<br />

SCHULZE, C.H. & FIEDLER, K. 1997. Patterns of diversity and vertical stratification in<br />

hawkmoths (Lepidoptera: Sphingidae) of a Bornean rain forest. Mitteilungen der Deutschen<br />

Gesellschaft für allgemeine und angewandte Entomologie 11: 767–770.<br />

SEKI, Y., TAKANAMI, Y. & OTSUKA, K. 1991. Butterflies of Borneo, Vol. 2 No. 1<br />

Lycaenidae. Tobishima Corporation, Tokyo. 113 pp.<br />

SPEIGHT, M.R., HUNTER, M.D. & WATT, A.D. 1999. Ecology of Insects. Concepts and<br />

Applications. Blackwell Science, Oxford.<br />

TANGAH, J., HILL, J.K., HAMER, K.C. & DAWOOD, M.M. 2004. Vertical distribution of<br />

fruit-feeding butterflies in Sabah, Borneo. Sepilok Bulletin 1: 15–25.<br />

TAYLOR, L.R. 1978. Bates, Williams, Hutchinson – a variety of diversities. Pp. 1-18 in Mound,<br />

L.A. & Waloff, N. (eds.) R.E.S. Symposium 9. Diversity of Insect Faunas. Blackwell.<br />

136


ARTHUR Y.C. CHUNG (2007)<br />

STATUS OF BIOLOGICAL DIVERSITY IN MALAYSIA &<br />

THREAT ASSESSMENT OF PLANT SPECIES IN MALAYSIA<br />

AN OVERVIEW OF RESEARCH ON BEETLE<br />

DIVERSITY & TAXONOMY IN MALAYSIA<br />

Arthur Y.C. Chung<br />

ABSTRACT<br />

Beetles form the most diverse insect order, with an estimated 400,000 species worldwide<br />

representing two-fifths of all insect species. Although some research has been carried out on<br />

beetle diversity in Malaysia, because of their high diversity, our understanding of their<br />

taxonomy, diversity, species assemblages and ecology is still far from adequate. Even at the<br />

family level, there are 166 families worldwide, more than half of which are recorded in Malaysia.<br />

Diversity in the beetle order is not only observed in numbers. Size, shape, colour and occurrence<br />

in various habitat types are also diverse in beetles. The smallest, biggest and bulkiest insects<br />

are beetles. Many small beetles are found in leaf litter and soil, and these are relatively difficult<br />

to extract and study. Different methods have to be used to conduct a comprehensive survey of<br />

beetles because of their occurrence in various types of habitats. The number of researchers<br />

who are working on beetle diversity, however, is very low, making it difficult to achieve an<br />

adequate knowledge of this insect group. Basic information on beetle diversity is very important,<br />

as this can contribute valuable information that can guide the formulation of conservation<br />

measures. In addition, many beetles are essential from an ecological and economic point of<br />

view. For example, the pollinating weevil, Elaeidobius kamerunicus, has contributed<br />

significantly to increased yields in the palm oil industry in Malaysia. In view of this, there is<br />

a need to encourage more researchers to work on beetles, such as through the provision of<br />

adequate funding. Having good and well-managed collections of beetles is crucial in facilitating<br />

research on beetle diversity and taxonomy. In addition to this, the use of information technology,<br />

such as databasing and electronic imaging, will enhance such efforts. There is also a need for<br />

networking and collaboration within agencies in Malaysia, as well as with foreign institutions,<br />

as a platform for the sharing and exchange of information that will further contribute to our<br />

understanding of beetle diversity at the local, regional and global level.<br />

INTRODUCTION<br />

Biodiversity has emerged at the centre of one of the most contentious global debates of this<br />

century. The debate often focuses on tropical rainforests, which are extremely diverse. Insects<br />

are one of the most important and dominant inhabitants of the rainforest. Approximately threequarters<br />

of all species worldwide are insects, and more than half are found in tropical rainforests.<br />

Forest Research Centre, Forest Department, P.O. Box 1407, 90715 Sandakan, Sabah; Tel: 089-537886; Fax: 089-<br />

531068; Arthur.Chung@sabah.gov.my<br />

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AN OVERVIEW OF RESEARCH ON BEETLE DIVERSITY & TAXONOMY IN MALAYSIA<br />

To date, a substantial amount of research has been carried out to investigate insect diversity in<br />

the tropics (e.g. Stork 1991; Davis et al. 1997; Chung 1999). However, the current level of<br />

understanding of the diversity of many insect groups is still deficient. The importance of good<br />

local species-richness data for a wide range of questions posed by evolutionary biology in<br />

general and ecology in particular, is evident (Hammond 1990). To assess habitats for their<br />

relevance for conservation, ecological and diversity inventories provide an essential tool for<br />

environmental management, and insects are a major component in every terrestrial habitat.<br />

Beetles are extremely diverse and abundant (Stork 1991; Chung et al. 2000a), and they<br />

participate in a great variety of interactions with other organisms. This makes them an important<br />

group to study if we are to understand the assemblage structure and diversity of the insect<br />

fauna in various tropical habitats.<br />

BASIC INFORMATION OF BEETLES<br />

Beetles belong to the insect order Coleoptera, which is characterized by a pair of sheath wings<br />

known as elytra. This is believed to be the most important factor that has contributed to the<br />

evolutionary success of the beetles (Evans 1977). The body and the elytra (forewings) are<br />

usually heavily sclerotized, giving the beetle an armoured appearance, which also protect it<br />

from dehydration and ultraviolet radiation. The cuticle (outer skin and skeleton) consists of<br />

chitin and protein, which is tough and protects the soft, inner organs. Another typical<br />

characteristic feature of this group is the biting mouthparts, giving them great adaptability.<br />

The word ‘beetle’ actually comes from the Middle English word ‘bityl’ or ‘betyll’ and the Old<br />

English ‘bitula’ meaning ‘little biter’ (Lawrence & Britton 1994). Beetles are an endopterygote<br />

group, that is they exhibit complete metamorphosis (holometabolous development), with<br />

distinct larval and pupal stages. Other detailed characteristic features of beetles are explained<br />

in standard taxonomical and ecological references of this group, for example, Evans (1977),<br />

Lawrence and Britton (1994) and Crowson (1981).<br />

Beetles are probably related to soft-bodied, weakly flying insects such as alder flies<br />

(Megaloptera) and lacewings (Neuroptera) (Evans 1977; Lawrence & Newton 1982). The<br />

ancestors of beetles probably evolved about 300 million years ago during the Upper<br />

Carboniferous or Lower Permian periods (Evans 1977). There are fossils showing that the<br />

primitive Coleoptera had megalopteran-like venation on the elytra. Some other fossils have<br />

been found in the Ural mountains, Russia and in Czechoslovakia, showing marked similarities<br />

to the recent archostematan Ommadidae (a primitive Coleoptera family). The evolutionary<br />

history and phylogeny of beetles are discussed in Crowson (1981), and Lawrence and Newton<br />

(1982).<br />

DIVERSITY AND TAXONOMIC CLASSIFICATION OF BEETLES<br />

With an estimated 400,000 species, beetles form the most diverse insect order, outnumbering<br />

the Lepidoptera and Hymenoptera (Hammond 1992; 1995). They encompass two-fifths of all<br />

insect species. In comparison, there are about 45,000 species of vertebrates and 250,000 species<br />

of plants. Beetles are not only diverse in species but also in structure and size: the largest of<br />

them (the cerambycids Titanus giganteus from South America and Xixuthrus heros from Fiji)<br />

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ARTHUR Y.C. CHUNG (2007)<br />

attain a length of 200 mm, almost 800 times greater than that of the smallest ones (Nanosella<br />

and related genera in the family Ptiliidae), which fall well within the size range of larger<br />

protozoans, such as Paramecium (Lawrence & Britton 1994).<br />

There are a few beetle classifications used worldwide (e.g. Crowson 1981; Lawrence 1982;<br />

1991; Paulian 1988) since the first appearance of Crowson’s major work in 1955. One of the<br />

latest and widely used was compiled by Lawrence and Newton (1995), in accordance to the<br />

International Code of Zoological Nomenclature (ICZN 1985). This classification listed 166<br />

families, 453 subfamilies and approximately 3,300 genera placed within four suborders<br />

(Table 1).<br />

The largest suborder of Coleoptera is Polyphaga, which is divided into five series and 16<br />

superfamilies, covering more than 90% of all beetle species. Within the Polyphaga, the<br />

superfamilies Chrysomeloidea, Curculionoidea and Staphylinoidea are the most successful<br />

groups (Lawrence & Newton 1982). The Chrysomeloidea (Chrysomelidae-Bruchidae-<br />

Cerambycidae) and Curculionoidea (Anthribidae-Attelabidae-Brentidae-Apionidae-<br />

Curculionidae-Scolytidae-Platypodidae) are predominantly herbivorous with 70,000 and<br />

60,000 described species, respectively. The superfamily Staphylinoidea (c. 40,000 described<br />

species) contains the predominantly predacious and saprophagous Staphylinidae (c. 30,000<br />

described species), Pselaphidae, Scydmaenidae, Leodidae and Ptiliidae.<br />

Table 1. The suborders of Coleoptera<br />

Suborder<br />

Archostemata<br />

Myxophaga<br />

Adephaga<br />

Polyphaga<br />

Remarks<br />

3 families, rare and primitive beetles, several fossils up to 280 million<br />

years old.<br />

4 families, small and uncommon beetles, feeding on algae.<br />

8 families including Carabidae and Cicindelidae, mainly carnivorous<br />

beetles.<br />

Majority of the families, vary greatly in form and habits, feeding on<br />

various types of food.<br />

Taxonomic classification within the order is rather complicated, and it is important to realize<br />

that the higher level classification of Coleoptera is not stable. Some suborders and many<br />

families probably do not represent monophyletic groups. Cladistic hypotheses for the<br />

classification of the Coleoptera are, therefore, lacking (Mawdsley 1994; Gullan & Cranston<br />

1998; Chung 2003). A comprehensive bibliography on beetle families can be obtained through<br />

the internet (Lawrence et al. 2005).<br />

IMPORTANCE OF BEETLES IN THE TROPICAL ECOSYSTEM<br />

Because of their high diversity, beetles are suitable insects to use as indicators of environmental<br />

change. They are found in numbers in most vegetation types and can be easily sampled using<br />

various techniques (Chung et al. 2000b). Beetles are widely used in studies on diversity and<br />

ecology (e.g. Davis et al. 1997; Chung 2004). Documentation of diverse and ecologically<br />

important insect groups, such as assemblages of beetles, can provide qualitative and quantitative<br />

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AN OVERVIEW OF RESEARCH ON BEETLE DIVERSITY & TAXONOMY IN MALAYSIA<br />

measures of biodiversity that provide a basis for decision making in relation to conservation<br />

(Harper & Hawksworth 1995).<br />

Many beetles attack living trees and, thus, reduce the commercial value of their timber (Booth<br />

et al. 1990). They also sometimes cause the death of the trees, either directly or by transmitting<br />

pathogens. Some scarab beetles attack and cause severe damage to oil palm (Wood 1968) and<br />

rattans (Chung 1995). The gold dust weevil, Hypomeces squamosus, is one of the commonest<br />

defoliators that attacks many tree species, including dipterocarps and fast-growing exotic tree<br />

species (Chey 1996). Many cerambycids beetles are stem-borers: their larvae can severely<br />

damage trees, resulting in devaluation of timber and, sometimes, tree mortality. Thapa (1974)<br />

reported attack by the cerambycid borer, Cyriopalus wallacei, on dipterocarps in Sabah.<br />

Ambrosia beetles (Scolytidae and Platypodidae) also cause damage to many species of forest<br />

trees and rattans (Anzai 1991; Chung 1995; Chey 1996).<br />

Some beetles are beneficial to humans. The discovery of a weevil pollinator had a dramatic<br />

effect on production in Malaysian oil palm plantations. The weevil, Elaeidobius kamerunicus,<br />

was introduced into Malaysia in 1981 to replace the practice of assisted pollination (Syed et<br />

al. 1982; Yee et al. 1984). Sakai et al. (1997) also reported that beetles of the families<br />

Chrysomelidae and Curculionidae contributed to the pollination of Shorea parvifolia in<br />

Sarawak. In addition, dung beetles (Scarabaeidae) are important decomposers and nutrient<br />

recyclers in the rainforest.<br />

More research needs to be carried out on beetles because, in spite of their economic importance,<br />

there is still a lack of taxonomic and ecological information on the order in South-east Asia.<br />

For example, Hammond (1990; 1992) estimated that about 75% of the 6,000 species of beetles<br />

collected from a lowland forest in Sulawesi were undescribed, and Mohamedsaid (1990, 1993a;<br />

1993b, 1994, 1996a) described numerous new species of leaf beetles in Malaysia within a<br />

short period of time.<br />

STUDIES ON BEETLE DIVERSITY AND TAXONOMY IN<br />

MALAYSIA & ADJACENT COUNTRIES<br />

Chung (2003) recorded 106 families of beetles in Borneo, mainly from Sabah (Appendix 1).<br />

This number, however, does not include all the families known to occur in Borneo. In Peninsular<br />

Malaysia, at least 93 beetle families are known to occur (Tung 1983), this number being based<br />

on the beetle family list issued by the Commonwealth Institute of Entomology in England.<br />

A few recent studies on beetle diversity have been conducted in Malaysia. Chung (1999) and<br />

Chung et al. (2000a & b) compared the beetle diversity in various habitat types in Sabah, that<br />

is, primary forest, logged-over forest, forest plantations and oil palm plantations. In Peninsular<br />

Malaysia, Fauziah (2003a; 2003b) conducted beetle surveys in Langkawi and Johore. Abang<br />

and Norashikin (submitted) investigated the diversity and distribution of night flying beetles<br />

in a lowland mixed dipterocarp forest site in Sabah using modified Pennsylvanian light traps.<br />

Burghouts et al. (1992) also compared Coleoptera with other invertebrates in their study on<br />

leaf-litter decomposition and litter invertebrates, in a Sabah lowland rainforest. A project on<br />

“Tools for monitoring soil biodiversity in the ASEAN Region,” with funding from the Darwin<br />

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ARTHUR Y.C. CHUNG (2007)<br />

Initiative, UK, was conducted in Sabah between the years 2000-2003, involving researchers<br />

from the Natural History Museum (London), Universiti Malaysia Sabah and the Sabah Forestry<br />

Department. One of the focal study groups was soil and leaf-litter inhabiting beetles, which<br />

have been little studied.<br />

In the adjacent country of Brunei, Mawdsley (1994) investigated the spatial structure of the<br />

Coleoptera assemblage in the rainforest and explored ways in which biologists can scale up<br />

estimates of species richness from a local to a regional scale. He used a wide range of collecting<br />

methods to sample from ground to canopy levels and compared the importance of each sampling<br />

method. Stork (1987a; 1987b, 1991) studied the arthropod fauna of lowland rainforest trees,<br />

in the same area as Mawdsley, wherein he emphasized the composition, guild structure and<br />

faunal similarity between Coleoptera and other insect groups.<br />

Other research on Coleoptera has focused on certain beetle groups, emphasizing their taxonomy<br />

or ecology. Much of the research has been conducted by foreign researchers. Abang (2001)<br />

provided a list of publications on insect taxonomy (including beetles) authored by foreign<br />

scientists in Malaysia. Despite high diversity in the order, only 11 papers were published on<br />

beetles in the Malayan Nature Journal and the Malayan Naturalist from 1940 to 1990 (Kiew &<br />

Lyons 1992). Mohamed Salleh Mohamedsaid is one of the very few Malaysian beetle<br />

taxonomists. His work focuses on the taxonomy of leaf beetles, Chrysomelidae (e.g.,<br />

Mohamedsaid 1996a; 1997). A total of 1,073 species and 215 genera from 13 subfamilies<br />

were recorded in Malaysia and Borneo (Mohamedsaid 2004). In addition, Fatimah Abang of<br />

Universiti Malaysia Sarawak (UNIMAS) works on longhorn beetles (e.g. Abang & Vives<br />

2004, Abang 2003, Vives & Abang 2003) and weevils (pers. comm.).<br />

Davis (1993) and Davis et al. (1997) investigated the ecology and behaviour of rainforest<br />

dung beetles in south-eastern Sabah. Hammond (1984) published a checklist of Staphylinidae<br />

occurring in Borneo, but emphasized that this list is conservative and that the actual number<br />

of staphylinids could be many times more than the figure in the list. Stork (1986) published an<br />

inventory of the Carabidae from Borneo. Hlavac and Maruyama (2004) worked on<br />

Staphylinidae that exhibit mutualistic relationships with ants in Peninsular Malaysia. Fireflies<br />

were studied by Ballantyne and Menayah (2000), and Mahadimenakbar et al. (2003). The<br />

Forest Research Institure Malaysia (FRIM) has also conducted some ecological research on<br />

fireflies (Krishnakumari 2002) and has on-going research on their biology and habitat<br />

requirements (L.G. Kirton, pers. comm.).<br />

Japanese researchers have also contributed significantly to research on beetle diversity and<br />

taxonomy in Malaysia. Mizunuma and Nagai (1994) published a comprehensive, illustrated<br />

account of the world’s lucanids, and many of the species featured are found in this region,<br />

including Malaysia. Ohara et al. (2001) worked on Histeridae, Ochi and Kon (1994) on dung<br />

beetles, and Kon et al. (1995) on Passalidae, while Araya (1994) and Araya et al. (1994)<br />

worked on Lucanidae. Makihara (1999) studied the Cerambycidae of Kalimantan, and his<br />

illustrated publication is often used as a reference in Sabah and Sarawak because,<br />

biogeographically, they share a lot of similarities with Kalimantan. The on-going Bornean<br />

Biodiversity and Ecosystem Conservation (BBEC) Programme has provided opportunities<br />

for Japanese researchers to work on beetles in Malaysia, particularly in Sabah (Mustafa &<br />

Kusano 2004).<br />

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Much of the research work in the past focused only on certain beetle taxa and not on Coleoptera<br />

as a whole. It is important that more research is conducted to study and understand beetles as<br />

a group, in order to gain a more comprehensive picture of this order collectively.<br />

BEETLE REFERENCE COLLECTIONS IN MALAYSIA<br />

As with all animal or plant groups, a reference collection of beetles is important for the study<br />

of their systematics as well as their diversity and, ultimately, forms the basis for their<br />

conservation. It provides basic, salient information, and the primary evidence for existence of<br />

species. Besides being indispensable to taxonomic work, a good beetle collection is part of<br />

the local, national, regional and international natural heritage (Abang & Ghazally 2001, Chung<br />

& Chey 2001). Beetle collections are usually an integral part of insect collections in general,<br />

which are often housed by museums, Federal or State Departments of Forestry and Agriculture,<br />

research institutions and universities. A list of the depositories that house existing insect<br />

collections in Malaysia has been provided by Abang and Ghazally (2001).<br />

To date, there are approximately 1,700 species of beetles from 89 families in the Coleoptera<br />

collection of the Forest Research Centre in Sepilok, Sandakan. Although some are<br />

morphospecies – that is, they are recognised as having different morphology even though it is<br />

uncertain if they are different species – this number still probably reflects a very high number<br />

of true species. At the Sarawak Forest Research Centre in Kuching, more than 350,000<br />

specimens from 31 families have been recorded, but only about 10% are identified to genus<br />

level (Lucy Chong, pers. comm.). There is also a good collection of beetles at Universiti<br />

Kebangsaan Malaysia in Bangi, with more than 600 identified beetle species, mainly from the<br />

family Chrysomelidae (Anon. 1996, Mohamedsaid 1996b). However, after the retirement of<br />

Prof. Mohamed Salleh Mohamedsaid, there is no other beetle specialist working on this group<br />

(Azman S., pers. comm.). A total of 61 families have been recorded at the Forest Research<br />

Institute Malaysia (FRIM) in Kepong (S. Cheng, pers. comm.). Other prominent beetle<br />

collections are in the Sarawak Museum and Universiti Malaysia Sarawak (Abang et al., 1996),<br />

Universiti Malaya and Universiti Malaysia Sabah.<br />

THE NEED FOR COOPERATION IN RESEARCH ON BEETLE<br />

DIVERSITY AND TAXONOMY IN MALAYSIA<br />

The high diversity of beetles in Malaysia practically guarantees that one will always be<br />

encountering beetles that have never been collected before, thus, classifying and identifying<br />

them can be a daunting task. Unlike many other insect orders, the taxonomy of beetles is<br />

difficult and unstable. The status of some families is very uncertain, while the classification of<br />

some obscure families varies, subject to the different views of different beetle taxonomists.<br />

Many of the characters used to delineate families are very general, being applicable to various<br />

beetle families. Being very diverse, there are many exceptions in the characters used. For<br />

example, some tenebrionids look almost identical to erotylids or coccinellids. In view of these<br />

difficulties, experience, skill and time are important when working on beetle diversity. It is<br />

also essential for beetle specialists to cooperate and share information, in order to be more<br />

effective in advancing our understanding of beetle taxonomy and diversity.<br />

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ARTHUR Y.C. CHUNG (2007)<br />

There are very few researchers that work on beetles in Malaysia and it is, therefore, difficult to<br />

achieve an adequate knowledge of this insect group. Abang and Ghazally (2001) noted that<br />

there were only about 17 insect taxonomists in the entire country, a number that is far too<br />

small to provide the substantial effort needed to alleviate the problem of a shortage of taxonomic<br />

information on insects. Basic information on beetle taxonomy and diversity is very important,<br />

as this can contribute valuable information that can guide the formulation of measures to<br />

ensure sustainable environmental management. Furthermore, many beetles are important from<br />

an ecological and economic perspective. For example, the pollinating weevil, Elaeidobius<br />

kamerunicus, has contributed significantly to the palm oil industry in Malaysia.<br />

In view of the immensity and importance of the task, there is a need to encourage more<br />

researchers to work on beetles. Adequate funds need to be channeled towards such research to<br />

encourage more work on beetle diversity and taxonomy. Having good and well-managed<br />

collections of beetles is crucial in enabling research on beetle diversity and taxonomy. In<br />

addition to this, the use of information technology, such as databasing and imaging (e.g.,<br />

digital images of specimens), will enhance such efforts. There is also a need for networking<br />

and collaboration within agencies in Malaysia, as well as with foreign institutions, as a platform<br />

for the sharing and exchange of information that will further contribute to our understanding<br />

of beetle diversity at the local, regional and global level. Since many of the good collections<br />

of beetles are in the developed countries, it is important for local scientists to liaise with<br />

foreign counterparts and work together with them. ANeT, established under the DIWPA network<br />

for social insect collections, is a good example of networking of researchers who are working<br />

on ants, through meetings, seminars and via the Internet.<br />

In summary, my recommendations to enhance research on beetle diversity in Malaysia are<br />

similar to those highlighted for the roles of collections in biodiversity conservation (Abang &<br />

Ghazally 2001, Chey 2001), and they can be summarized as follows:<br />

• Increase the number of beetle specialists in Malaysia;<br />

• Provide training on beetle diversity and taxonomy for inexperienced curators and auxiliary<br />

staff;<br />

• Provide funding and other incentives to encourage research on beetle diversity and<br />

taxonomy;<br />

• Encourage beetle specialists to publish identification manuals and monographs to benefit<br />

more para-taxonomists and students;<br />

• Increase the use of information technology to enhance research on beetle diversity and<br />

taxonomy;<br />

• Establish networking and collaborative work; and<br />

• Establish a directory for researchers working on beetles in this region.<br />

ACKNOWLEDGEMENTS<br />

The author would like to thank Dr. Chey Vun Khen (Sabah Forestry Department), Lucy Chong<br />

& Paulus Meleng (Sarawak Forestry Corporation), Prof. Fatimah Abang (UNIMAS), Dr. Rosli<br />

Hashim (UM), Prof. Zaidi Mohd. Isa & Azman Sulaiman (UKM), Dr. Laurence Kirton &<br />

Shawn Cheng (FRIM) for providing information regarding collections in their respective<br />

institutions.<br />

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REFERENCES<br />

ABANG, F. & GHAZALLY, I. 2001. The role of entomological collections in research and<br />

education: a case for Malaysia. Sabah Museum Monograph 6: 31–48.<br />

ABANG, F. 2003. A checklist of the longhorn beetles from Sarawak. Serangga 8(1&2): 24–<br />

30.<br />

ABANG, F. & MOHD. FAUZI, N. (submitted). Diversity and vertical distribution of night<br />

flying beetles (Coleoptera) in a Bornean lowland mixed dipterocarp forest. Sarawak<br />

Museum Journal.<br />

ABANG, F., SULAIMAN, H. & MUNEY, S. 1996. Systematic entomology in Sarawak: a<br />

preview. Serangga 1(2): 63–73.<br />

ABANG, F. & VIVES, E. 2004. Two new species of Callichromatini from Sarawak, Southwestern<br />

Borneo (Coleoptera: Cerambycidae). Lambillionea CIV: 233–237.<br />

ANON. 1996. Pusat Sistematik Serangga, Universiti Kebangsaan Malaysia. Serangga 1(1):<br />

1–6.<br />

ARAYA, K. 1994. Discovery of a flightless Aegus (Coloptera, Lucanidae) in Borneo. Elytra<br />

22: 271–280.<br />

ARAYA, K., KIKUTA, T. & OKUMA, T. 1994. The genus Penichrolucanus (Coleoptera,<br />

Lucanidae) new to the fauna of Borneo. Elytra 22: 151–152.<br />

ANZAI, M. 1991. Attraction of beetles (in particular ambrosia beetles) to freshly felled logs<br />

of plantation species. Sabah Forestry Department Report. 52 pp.<br />

BALLANTYNE, L.A. & MENAYAH, R. 2000. Redescription of synchronous firefly, Pteroptyx<br />

tener Olivier (Coleoptera: Lampyridae), of Kampung Kuantan, Selangor. Malayan Nature<br />

Journal 54(4): 323–328.<br />

BOOTH, R.G., COX, M.L. & MADGE, R.B. 1990. IIE Guides to Insects of Importance to<br />

Man— Coleoptera. International Institute of Entomology & The Natural History Museum,<br />

London. 384 pp.<br />

BURGHOUTS, T., ERNSTING, G., KORTHALS, G. & VRIES, T.D. 1992. Litterfall, leaf<br />

litter decomposition and litter invertebrates in primary and selectively logged dipterocarp<br />

forest in Sabah, Malaysia. Philosophical Transactions of the Royal Society, Series B 335:<br />

407–416.<br />

CHEY, V.K. 1996. Forest Pest Insects in Sabah. Sabah Forest Record No. 15, Sabah Forest<br />

Department. 111 pp.<br />

CHEY, V.K. 2001. Local insect collections: problems and challenges. Sabah Museum<br />

Monograph 6: 27–30.<br />

CHUNG, A.Y.C. 1995. Insect pests of rattans in Sabah. The Planter 71(827): 55–66.<br />

CHUNG, A.Y.C. 1999. The Diversity of Coleoptera Assemblages in Different Habitat Types<br />

in Sabah, Malaysia with Special Reference to Herbivory. D.Phil. thesis, Oxford University,<br />

U.K. 307 pp.<br />

CHUNG, A.Y.C., EGGLETON, P., SPEIGHT, M.R., HAMMOND, P.M. & CHEY, V.K. 2000a.<br />

The diversity of beetle (Coleoptera) assemblages in different habitat types in Sabah,<br />

Malaysia. Bulletin of Entomological Research 90(6): 475–496.<br />

CHUNG, A.Y.C., EGGLETON, P., SPEIGHT, M.R., HAMMOND, P.M. & CHEY, V.K. 2000b.<br />

Beetle (Coleoptera) sampling with the Winkler method, flight-interception-trapping and<br />

mist-blowing in Sabah, Malaysia. Sabah Parks Nature Journal 3: 63–78.<br />

CHUNG, A.Y.C. 2003. Manual for Bornean beetle (Coleoptera) family identification. Prepared<br />

for Course on Tools for Monitoring Soil Biodiversity in the ASEAN Region, Universiti<br />

Malaysia Sabah, Kota Kinabalu, 12-26 October 2003. (Unpublished).<br />

144


ARTHUR Y.C. CHUNG (2007)<br />

CHUNG, A.Y.C. 2004. Vertical stratification of beetles (Coleoptera) using flight intercept<br />

traps in a lowland rainforest of Sabah, Malaysia. Sepilok Bulletin 1: 27–39.<br />

CHUNG, A.Y.C. & CHEY, V.K. 2001. The importance of the forest insect collection in Sabah.<br />

Pp. 179–183 in Zahra Y., Moo-Tan, S. & Yorath, S. (eds.) Proceedings of the International<br />

Conference on In-Situ & Ex-Situ Biodiversity Conservation in the New Millennium. 20-<br />

22 June 2000. Yayasan Sabah & Sabah Museum, Kota Kinabalu.<br />

CROWSON, R.A. 1955. The natural classification of the families of Coleoptera. Nathaniel<br />

Lloyd, London. 187 pp.<br />

CROWSON, R.A. 1981. The biology of the Coleoptera. Academic Press, London. 802 pp.<br />

DAVIS, A.J. 1993. The ecology and behaviour of rainforest dung beetles in northern Borneo.<br />

Ph.D. Thesis, Leeds University, U.K. 280 pp.<br />

DAVIS, A.J., HUIJBREGTS, J., KIRK-SPRIGGS, A.H., KRIKKEN, J. & SUTTON, S.L.<br />

1997. The ecology and behaviour of arboreal dung beetles in Borneo. Pp. 417–432 in<br />

Stork, N.E., Adis, J. & Didham, R.K. (eds.) Canopy arthropods. Chapman & Hall, London.<br />

EVANS, G. 1977. The life of beetles. George Allen & Unwin Ltd., London. 232 pp.<br />

FAUZIAH, A. 2003a. Diversity of Coleoptera in Endau Rompin. In: The Proceedings of the<br />

Seminar on Ecological Studies in Tropical Rainforests. 19-20 August, 2003. FRIM,<br />

Kepong.<br />

FAUZIAH, A. 2003b. Beetle diversity on Langkawi Islands. In: The Proceedings of the Seminar<br />

on the findings of the Scientific & Heritage Expedition 2003 – Langkawi Islands. 20-21<br />

October, 2003. Langkawi, Kedah Darul Aman.<br />

GULLAN, P.J. & CRANSTON, P.S. 1998. The insects: an outline of entomology. Chapman &<br />

Hall, London. 470 pp.<br />

HAMMOND, P.M. 1984. An annotated check-list of Staphylinidae (Insecta: Coleoptera)<br />

recorded from Borneo. Sarawak Museum Journal 33(54): 187–218.<br />

HAMMOND, P.M. 1990. Insect abundance and diversity in the Dumago-Bone National Park,<br />

North Sulawesi, with special reference to the beetle fauna of lowland rainforest in the<br />

Toraut region. Pp. 197–254 in Knight, W.J. & Holloway, J.D. (eds.) Insects and the<br />

rainforests of South East Asia (Wallacea). The Royal Entomological Society of London.<br />

HAMMOND, P.M. 1992. Species inventory. Pp. 17–39 in Groombridge, B. (ed.) Global<br />

biodiversity–status of the earth’s living resources. WCMC, Chapman & Hall, London.<br />

HAMMOND, P.M. 1995. The current magnitude of biodiversity. Pp. 113–138 in Heywood,<br />

V.H. & Watson, R.T. (eds.) Global biodiversity assessment. Cambridge University Press,<br />

Cambridge.<br />

HARPER, J.L. & HAWKSWORTH, D.L. 1995. Preface. Pp. 5–12 in Hawksworth, D.L. (ed.)<br />

Biodiversity – measurement and estimation. Chapman & Hall, London.<br />

HLAVAC, P. & MARUYAMA, M. 2004. A new genus and species of the myrmecophilus<br />

tribe Sahlbergiini from Malaysia (Coleoptera: Staphylinidae: Aleocharinae)<br />

Koleopterologische Rundschau 74: 191–199.<br />

ICZN. 1985. International Code of Zoological Nomenclature, adopted by the XV International<br />

Congress of Zoology. International Trust for Zoological Nomenclature, London. 338 pp.<br />

KIEW, R. & LYONS, K. 1992. Annotated bibliography: Malayan Nature Journal (1940-1990),<br />

Malayan Naturalist (1974-1990). Malayan Nature Journal 44(3&4): 123–479.<br />

KON, M., UEDA, A. & JOHKI, Y. 1995. Two new species of Aceraius (Coleoptera, Passalidae)<br />

from Sabah, Borneo. Japanese Journal of Systematic Entomology 1: 99–104.<br />

KRISHNAKUMARI, A.N. 2002. Management and Conservation of Fireflies in Peninsular<br />

Malaysia. PhD Thesis. University of London, Imperial College of Science, Technology<br />

and Medicine, 216 pp.<br />

145


AN OVERVIEW OF RESEARCH ON BEETLE DIVERSITY & TAXONOMY IN MALAYSIA<br />

LAWRENCE, J.F. 1982. Coleoptera. Pp. 482–553 in Parker S.P. (ed.) Synopsis and<br />

classification of living organisms. McGraw-Hill Book Co., London.<br />

LAWRENCE J.F. 1991. Order Coleoptera. Pp. 144–658 in Stehr, F.W. (ed.) Immature insects<br />

vol. 2. Kendall/Hunt Publ. Co., Dubuque, Iowa.<br />

LAWRENCE, J.F. & BRITTON, E.B. 1994. The beetles of Australia. CSIRO, Melbourne<br />

University Press, Victoria. 192 pp.<br />

LAWRENCE, J.F., HASTINGS, A.M., DALLWITZ, M.J., PAINE, T.A. & ZURCHER, E.J.<br />

2005. General bibliography: beetles of the world.<br />

http://biodiversity.uno.edu/delta/elateria/www/genbibl.htm (Date accessed: 15 June, 2005)<br />

LAWRENCE, J.F. & NEWTON, A.F.Jr. 1982. Evolution and classification of beetles. Annual<br />

Review of Ecology and Systematics 13: 261–290.<br />

LAWRENCE, J.F. & NEWTON, A.F. Jr. 1995. Families and subfamilies of Coleoptera (with<br />

selected genera, notes, references and data on family-group names). Pp. 779–1092 in<br />

Pakaluk, J. & Slipinski, S.A. (eds.) Biology, phylogeny, and classification of Coleoptera:<br />

papers celebrating the 80 th birthday of Roy A. Crowson. Muzeum i Instytut Zoologii<br />

PAN, Warszawa.<br />

MAHADIMENAKBAR, M.D., SCHILTHUIZEN, M. & ZULHAZMAN, H. 2003. Preliminary<br />

survey of fireflies (Coleoptera: Lampyridae) in Lower Kinabatangan, Sabah. Pp. 27–36<br />

in Maryati M., Atsuko T., Goossens, B. & Indran, R. (eds.) Lower Kinabatangan Scientific<br />

Expedition 2002. Universiti Malaysia Sabah.<br />

MAKIHARA, H. 1999. Atlas of longicorn beetles in Bukit Soeharto Education Forest,<br />

Mulawarman University, East Kalimantan, Indonesia. PUSREHUT Special Publication<br />

No. 7. Mulawarman University & JICA. 140 pp.<br />

MAWDSLEY, N.A. 1994. Community structure of Coleoptera assemblage in a Bornean<br />

tropical forest. Ph.D. thesis, University of London. 307 pp.<br />

MIZUNUMA, T. & NAGAI, S. 1994. The lucanid beetles of the world. Mushi-sha, Tokyo,<br />

Japan. 340 pp.<br />

MOHAMEDSAID, M.S. 1990. A new species of Lilioceris from Sabah, Malaysia<br />

(Chrysomelidae: Criocerinae). Entomological Review of Japan XLV(2): 93–95.<br />

MOHAMEDSAID, M.S. 1993a. A new species of Monolepta Chevrolat from Borneo<br />

(Coleoptera, Chrysomelidae, Galerucinae). Entomological Review of Japan XLIII(1):<br />

1–9.<br />

MOHAMEDSAID, M.S. 1993b. An interesting new species of Liroetiella from Sabah, Malaysia<br />

(Coleoptera, Chrysomelidae, Galerucinae). Entomological Review of Japan XLIII(1):<br />

45–46.<br />

MOHAMEDSAID, M.S. 1994. New species of Aulacophora from Sabah, Malaysia<br />

(Coleoptera, Chrysomelidae, Galerucinae). Treubia 31(1): 1–9.<br />

MOHAMEDSAID, M.S. 1996a. A new genus and two new species of Galerucinae from<br />

Malaysia (Coleoptera: Chrysomelidae). Serangga 1(2): 79–89.<br />

MOHAMEDSAID, M.S. 1996b. Spesimen holotip Chrysomelidae (Insecta: Coleoptera) dalam<br />

repository Pusat Sistematik Serangga, Universiti Kebangsaan Malaysia. Serangga 1(1):<br />

23–27. (in Malay).<br />

MOHAMEDSAID, M.S. 1997. Nota mengenai kumbang daun subfamili Chrysomelinae dari<br />

Semenanjung Malaysia (Coleoptera: Chrysomelidae). Serangga 2(1): 119–124. (in Malay).<br />

MOHAMEDSAID, M.S. 2004. Catalogue of the Malaysian Chrysomelidae (Insecta:<br />

Coleoptera). Pensoft, Bulgaria. 239 pp.<br />

MUSTAFA, K.Y. & KUSANO, T. 2004. Working together towards nature conservation for<br />

our future. Mid term progress report of BBEC programme (February 2002–November<br />

2004). BBEC Publication No. 34. JICA, Sabah State Government & UMS. 65 pp.<br />

146


ARTHUR Y.C. CHUNG (2007)<br />

OCHI, T. & KON, M. 1994. Dung beetles (Coleoptera, Scarabaeidae) collected from Sabah,<br />

Borneo (I). Elytra 22: 281–298.<br />

OHARA, M., MAZUR, S., MIZOTA, K. & MOHAMED, M. 2001. Records of the histerid<br />

beetles (Coleoptera: Histeridae) at the Crocker Range Park, Sabah, East Malaysia–A report<br />

of the Scientific Expedition to the Crocker Range, Sabah, Malayasia (Crocker XPDC<br />

’99). Nature and Human Activities 6: 59–63.<br />

PAULIAN, R. 1988. Biologie des Coleopteres. Lechevalier, Paris. 719 pp. (in French)<br />

SAKAI, S., MOMOSE, K., YUMOTO, T., KATO, M. & INOUE, T. 1997. Beetle pollination<br />

of Shorea parvifolia (section Mutica, Dipterocarpaceae) in general flowering period in<br />

Sarawak, Malaysia. Pp. 169–179 in Inoue, T. & Hamid, A.A. (eds.) General flowering of<br />

tropical rainforests in Sarawak. Canopy Biology Program in Sarawak: Series II.<br />

STORK, N.E. 1986. An annotated checklist of the Carabidae (including Cicindelinae,<br />

Rhysodinae and Paussinae) recorded from Borneo. Department of Entomology, Natural<br />

History Museum, London. 24 pp.<br />

STORK, N.E. 1987a. Guild structure of arthropods from Bornean rainforest trees. Ecological<br />

Entomology 12: 69–80.<br />

STORK, N.E. 1987b. Arthropod faunal similarity of Bornean rainforest trees. Ecological<br />

Entomology 12: 219–226.<br />

STORK, N.E. 1991. The composition of the arthropod fauna of Bornean lowland rainforest<br />

trees. Journal of Tropical Ecology 7:161–180.<br />

SYED, R.A., LAW, I.H. & CORLEY, R.H.V. 1982. Insect pollination of oil palm: introduction,<br />

establishment and pollinating efficiency of Elaeidobius kamerunicus in Malaysia. The<br />

Planter 58: 547–561.<br />

THAPA, R.S. 1974. The biology and ecology of the borer Cyriopalus wallacei Pasc. Sabah<br />

Forest Record No. 11, Sabah Forest Department. 33 pp.<br />

TUNG, V.W.Y. 1983. Common Malaysian Beetles. Longman, Malaysia. 142 pp.<br />

VIVES, E. & ABANG, F. 2003. Notes on the Lepturinae (Coleoptera: Cerambycidae) of the<br />

Sarawak Museum insect collection. The Sarawak Museum Journal LVIII(79): 245–250.<br />

WOOD, B.J. 1968. Pests of oil palms in Malaysia and their control. The Incorporated Society<br />

of Planters, Kuala Lumpur. 204 pp.<br />

YEE, C.B., LIM, K.C., ONG, F.C. & CHAN, K.W. 1984. The effects of Elaeidobius<br />

kamerunicus Faust. on bunch components of Elaeis guineensis Jacq. Pp. 129–139 in<br />

Proceedings of the Symposium on Impact of the Pollinating Weevil on the Malaysia Oil<br />

Palm Industry. 21-22 February 1984, Kuala Lumpur.<br />

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APPENDIX 1<br />

A list of beetle families, based on Chung (2003)<br />

1 Acanthoceridae 43 Geotrupidae 85 Ptiliidae<br />

2 Aderidae 44 Gyrinidae 86 Ptilodactylidae<br />

3 Anobiidae 45 Histeridae 87 Ptinidae<br />

4 Anthicidae 46 Hybosoridae 88 Rhipiceridae<br />

5 Anthribidae 47 Hydraenidae 89 Rhipiphoridae<br />

6 Apionidae 48 Hydrophilidae 90 Rhizophagidae<br />

7 Attelabidae 49 Inopeplidae 91 Rhysodidae<br />

8 Biphyllidae 50 Jacobsoniidae 92 Salpingidae<br />

9 Bostrychidae 51 Laemophloeidae 93 Scaphidiidae<br />

10 Bothrideridae 52 Lagriidae 94 Scarabaeidae<br />

11 Brentidae 53 Lampyridae 95 Scirtidae<br />

12 Bruchidae 54 Languriidae 96 Scolytidae<br />

13 Buprestidae 55 Lathridiidae 97 Scraptiidae<br />

14 Cantharidae 56 Leiodidae 98 Scydmaenidae<br />

15 Carabidae 57 Limnichidae 99 Silphidae<br />

16 Cebrionidae 58 Lophocateridae 100 Silvanidae<br />

17 Cerambycidae 59 Lucanidae 101 Sphindidae<br />

18 Cerylonidae 60 Lycidae 102 Staphylinidae<br />

19 Chelonariidae 61 Lyctidae 103 Tenebrionidae<br />

20 Chrysomelidae 62 Lymexylidae 104 Throscidae<br />

21 Cicindelidae 63 Melandryidae 105 Trogidae<br />

22 Cisidae 64 Meloidae 106 Trogositidae<br />

23 Clambidae 65 Melyridae<br />

24 Cleridae 66 Mordellidae<br />

25 Coccinellidae 67 Mycetophagidae<br />

26 Colydiidae 68 Mycteridae<br />

27 Corylophidae 69 Nitidulidae<br />

28 Crytophagidae 70 Nosodendridae<br />

29 Cucujidae 71 Noteridae<br />

30 Curculionidae 72 Oedemeridae<br />

31 Dermestidae 73 Othniidae<br />

32 Discolomidae 74 Passalidae<br />

33 Dryopidae 75 Passandridae<br />

34 Dytiscidae 76 Paussidae<br />

35 Elateridae 77 Pedilidae<br />

36 Elmidae 78 Phalacridae<br />

37 Endomychidae 79 Phengodidae<br />

38 Erotylidae 80 Platypodidae<br />

39 Eucinetidae 81 Propalticidae<br />

40 Eucnemidae 82 Pselaphidae<br />

41 Eulichadidae 83 Psephenidae<br />

42 Georissidae 84 Pterogeniidae<br />

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STATUS OF BIOLOGICAL DIVERSITY IN MALAYSIA &<br />

THREAT ASSESSMENT OF PLANT SPECIES IN MALAYSIA<br />

THE STATUS OF RESEARCH ON HYMENOPTERA<br />

IN MALAYSIA, WITH SPECIAL EMPHASIS ON<br />

ICHNEUMONIDAE<br />

Idris A.B.<br />

ABSTRACT<br />

The insect order Hymenoptera (wasps, ants and bees) is the second most speciose and diverse<br />

order on earth after beetles. They are extremely important as biological control agents of<br />

insect pests. The number of species is unknown but more than 115,000 species have been<br />

described and 5 to 10 times more await discovery. Problems faced by researchers working on<br />

Hymenoptera include poor inventory data, unavailability of up-to-date identification keys,<br />

checklists, databases, reference books and catalogues, and the lack of taxonomic revision.<br />

The number of researchers working on Hymenoptera worldwide is declining at an alarming<br />

rate. To date, 1,200 ant species have been recorded in Malaysia while more than 20,000<br />

ichneumonid specimens have been collected, viz., up from 300 specimens eight years ago.<br />

Many species have been recorded from Malaysia for the first time, and many new species<br />

have been identified. Research is being conducted on ant and ichneumonid wasp systematics,<br />

as well as on their diversity and ecology, particularly in relation to habitat change. Generally,<br />

ants and ichneumonids were negatively affected by habitat (forest) change and could be used<br />

as bioindicators of habitat disturbance. Few revisions and catalogues are available, and there<br />

are no checklists. Specimens are housed in museums and insect collection centers throughout<br />

the world. Major collection centres in Malaysia include the Center for Insect Systematics<br />

(UKM) and Institute for Tropical Biology and Conservation (ITBC) (UMS).<br />

INTRODUCTION<br />

Hymenoptera is derived from the Greek words hymen, which means ‘membrane’ (or Hymeno,<br />

the Greek god of marriage), and ptera, which means ‘wing’ (LaSalle & Gauld 1993). The<br />

order comprises two suborders—Symphyta and Apocrita. The Symphyta, or sawflies, are<br />

more primitive. They have complete wing venation and do not have the constricted ‘wasp’swaist’<br />

seen in the rest of the order (LaSalle & Gauld 1993). Most species have phytophagous<br />

larvae that resemble those of Lepidoptera in both appearance and behaviour. Sawflies are a<br />

relatively small group consisting of 14 families, which contain just over 5% of described<br />

species of Hymenoptera, with the majority in the family Tenthredinidae (Gaston 1993).<br />

Center for Insect Systematics, School of Environmental and Natural Resource Sciences, Faculty of Science &<br />

Technology, Universiti Kebangsaan Malaysia; idrisgh@pkrisc.cc.ukm.my<br />

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THE STATUS OF RESEARCH ON HYMENOPTERA IN MALAYSIA<br />

The suborder Apocrita contains the vast majority of species of Hymenoptera. It is divided into<br />

two groups, the Parasitica and Aculeata. The aculeates represent the most diverse group of<br />

Hymenoptera, in which the ovipositor structure has been modified into a sting. This group<br />

contains the groups of Hymenoptera known to most people, such as bees, wasps, hornets and<br />

ants. Some species are quite large in size, having a wing span of up to 10 cm (eg. the Spider<br />

wasps, Pompilidae). The majority of species are predatory (eg. wasps and hornets) or pollen<br />

feeding (eg. bees), but parasitism is common, particularly in the lower aculeates (Chrysidoidea).<br />

There are 19 families in Aculeata, and together they account for over 45% of described<br />

Hymenoptera species (Gaston 1993), with the families Apidae (bees), Formicidae (ants) and<br />

Sphecidae containing the most species.<br />

The Parasitica is the largest group of Hymenoptera, and includes all non-aculeate Apocrita.<br />

Members have a constricted waist, but in which the ovipositor has not been developed into a<br />

sting. The vast majority of the species are parasitoids. However, there are species which are<br />

phytophagous, gall-forming, or predatory. The Parasitica contains 48 families in 10<br />

superfamilies, and encompasses almost half the described species of Hymenoptera, with most<br />

of the species in superfamilies Ichneumoniodea and Chalcidoidea (Gaston 1993). The majority<br />

of the species, especially the Chalcidoidea, are very small (eg. 0.18 mm in length for some<br />

species in the family Trichogrammatidae), and most people are not even aware of their existence<br />

and role.<br />

The insect order Hymenoptera is one of the dominant life forms on earth, both in terms of the<br />

number of species as well as in the diversity of life styles that have evolved within the group.<br />

The Hymenoptera contain the vast majority of socially organized insects and parasitoids, as<br />

well as a great variety of specialist predators and herbivores. They have emerged as the most<br />

speciose group in many studies on terrestrial biodiversity and they are pre-eminent as biological<br />

control agents of insect pest species.<br />

The number of species of Hymenoptera is unknown and, at present, is almost impossible to<br />

estimate with any accuracy. Even the number of described species has not been accurately<br />

documented, given that there are many families for which there are no checklists or catalogues<br />

available. Some good checklists or catalogues are those of Johnson (1992), Bolton (1995),<br />

Noyes (1998), Townes (1983), van Achterberg (1983, 1988, 1997), Quicke (1987) and Sharkey<br />

(1988). La Salle and Gauld (1993) and Gaston (1993) have estimated the number of described<br />

species of Hymenoptera at more than 115,000 species. However, the total number (including<br />

undescribed and uncollected species) could be 5–10 times more, given that this is often the<br />

proportion of new species that are discovered following taxonomic revision of highly speciose<br />

families (Austin 1999). Determining the number of species for the ‘megadiverse’ regions of<br />

the world is a major problem. These areas include tropical or subtropical countries such as<br />

Australia, India, Malaysia, Indonesia, China, Brazil, Equador, Peru, Columbia, Mexico, Zaire<br />

and Madagascar; with a few exceptions, they have generally been poorly surveyed (McNeely<br />

et al. 1990). The hymenopteran fauna of Costa Rica is particularly well-studied (Hanson &<br />

Gauld 1995), and this work serves as a useful foundation for future research on the fauna of<br />

Costa Rica itself, and for other regions. The extent of species richness and biological complexity<br />

within the Hymenoptera dictates that the group should be at the center of studies assessing<br />

arthropod diversity. The full extent of their diversity will only be revealed when detailed<br />

studies similar to those in Costa Rica are undertaken for other species-rich regions of the<br />

world. Limiting factors common to many countries are the unavailability of up-to-date<br />

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IDRIS A.B. (2007)<br />

identification keys, taxonomic revisions, checklists, databases and catalogues (these are either<br />

lacking, difficult to get or very expensive to buy), the lack of taxonomists, poor financial<br />

support and a lack of research facilities and training programs.<br />

STUDIES ON HYMENOPTERA IN MALAYSIA<br />

Out of 100 families of Hymenoptera listed in Goulet and Huber (1993), there are only four<br />

groups, namely the Formicidae (true ants), Apidae (bees) and two parasitic wasp families<br />

(Ichneumonidae and Braconidae) that have been given more attention by local entomologists.<br />

Unfortunately, none of the present-day local entomologists undertake full-time taxonomic<br />

research, and this has a negative impact on efforts to advance our knowledge of the taxonomy<br />

and diversity of even these better-studied groups of Hymenoptera.<br />

A. Ants (Formicidae)<br />

Ants are important decomposers of organic matter, and contribute to nutrient cycling and soil<br />

enrichment. They have a well-earned title as ‘ecological engineers’ in terrestrial ecosystems<br />

(LaSalle & Gauld 1993)—they serve as food for other animals, have roles to play in seed<br />

dispersal, are able to control parasitism and predation, and some species have evolved<br />

mutualistic relationships with plants and other insects. In view of this, studies on this particular<br />

group of insects are vital.<br />

There are no checklists available for ants in Malaysia, but Bolton (1995) has catalogued the<br />

ants of the world. According to Maryati (pers. comm.), there are currently 1,200 species of<br />

ants recorded from Malaysia, an increase of 300 over the number of species reported 10 years<br />

ago (Maryati 1995). This increase in the number of species recorded is mainly a result of<br />

intensive study by her research team, supported by external grants, in collaboration with<br />

scientists from the United Kingdom (Natural History Museum), Japan, USA, and Europe. The<br />

interesting geological and evolutionary history of Borneo, and its high biodiversity, attracts<br />

research collaboration between local and foreign entomologists. Although most of the ant<br />

collections are kept at the Natural History Museum (NHM), London, some are also deposited<br />

at the new ‘Borneonsis’ Collection Center in the Institute for Tropical Biology and Conservation<br />

(ITBC) located in Universiti Malaysia Sabah (UMS), or in other museums or national<br />

collections in Japan, the United Kingdom and USA. A number of publications that are useful<br />

references for researchers working on ants, some of which are revisions or catalogues, are<br />

listed in Table 1.<br />

Malaysian entomologists currently working on ants are Datin Professor Dr. Maryati Mohamed<br />

of Universiti Malaysia Sabah (UMS), Professor Dr. Ahmad Said Sajap of Universiti Putra<br />

Malaysia (UPM) and the author, Associate Professor Dr. Idris Abd. Ghani of Universiti<br />

Kebangsaan Malaysia (UKM). Foreign entomologists actively involved in ant research in<br />

Malaysia are Professor Dr. Kazuo Ogata (Osaka University), Professor Dr. Seiki Yamane<br />

(Kagoshima University), Dr. Y. Hashimoto (attached to University Malaysia Sabah) and Dr.<br />

Barry Bolton (Natural History Museum, London). Japanese researchers are currently involved<br />

in a project on ‘Insect Inventory in Tropical Asia’, funded the JSPS (Japan Society for the<br />

Promotion of Science).<br />

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Table 1. Selected Publications Dealing with Ants in Malaysia.<br />

No Title Authors & Year<br />

1 The Role of Three Insect Groups (Ants, Dung beetles and Bakhtiar 2000<br />

Geometrid Moths) as Biological Indicators in Three Type of<br />

Habitats (Primary, Secondary & Oil Palms). MSc Thesis,<br />

Universiti Malaysia Sabah.<br />

2 A revision of the Australian ant genus Notoncus Emery, with Bolton 1955<br />

note on the genera of Melophorini.<br />

3 The ant tribe Tetramoriini. The genus Myr in the Oriental and<br />

Indo-Australian Regions, and in Australia. Bolton 1977<br />

4 A New General Catalogue of the Ants of the World Bolton 1995<br />

5 A preliminary analysis of the ants of Pasoh Forest Reserve Bolton 1996<br />

6 Identification Guide to the Ant Genera of the World Bolton 1997<br />

7 Stratification of ants in a primary rainforest in Sabah, Borneo Bruhl et al. 1998<br />

8 Leaf litter ant communities in tropical lowland rainforest Bruhl 2001<br />

in Sabah, Malaysia: Effect of forest disturbance and fragmentation<br />

9 Fauna semut di Hutan Hujan Tropika (Primer Sekunder) Chung 1993<br />

di Lembah Danum<br />

10 Common Lowland Forest Ants of Sabah. Forest Department Sabah. Chung 1995<br />

11 The ants of Tabin Wildlife Reserve, Sabah Hashimoto et al. 1999<br />

12 Diversity of Ants along an Urbanisational Gradient. MSc. Thesis.<br />

Universiti Malaysia Sabah Jimbau 2004<br />

13 Semut, UBTP, Universiti Malaysia Sabah Maryati 1995<br />

14 Terrestrial Ants of Poring, Kinabalu Park, Sabah Maryati et al. 1996<br />

15 Terrestrial Ants of Sayap, Kinabalu Park, Sabah Maryati 1998<br />

16 Taburan Semut Mengikut Altitude di Gunung Kinabalu. MSc thesis. Norhasiah 2000<br />

Universiti Malaysia Sabah.<br />

17 Comparison of Ant & Termite Diversity Between Regenerating & Noel 2004<br />

Primary Forest in Danum Valley & their Relationship with Physical,<br />

Climatic and Biological Factors. MSc. Thesis. Universiti Malaysia<br />

Sabah.<br />

18 Ant composition along an elevation gradient in Mount Kinabalu, Shanmuga 1996<br />

Sabah, Malaysia<br />

19 Canopy ants diversity assessment in the fragmented rainforest Widodo et al. 2001<br />

of Sabah<br />

20 Ground ant fauna in a Bornean Dipterocarp Forest Yamane et al. 1996<br />

B. Bees (Apidae)<br />

1. Honey bee group<br />

Apart from providing us with honey, pollen and resin, honey bees are vitally important as<br />

pollinators. Seven species have, so far, been recorded in Malaysia. They are Apis dorsata<br />

(giant honey bee, believed to be native to Malaysia), A. cerana (oriental honey bee), A. florea<br />

(dwarf honey bee), A. nuluensis and A. koschevnikovi (two bee species that nest in cavities),<br />

A. mellifera (common honey bee, introduced from Australia for the bee keeping industry) and<br />

A. andreniformis (recently described from Tenum, Sabah).<br />

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IDRIS A.B. (2007)<br />

There are few Malaysian entomologists working on bees; they are Prof. Dr. Mahadzir Mardan<br />

(Universiti Putra Malaysia), Mr. Hussan Abdul Kadir (Malaysian Agriculture Research and<br />

Development Institute) and Mr. Salim Tingek in the Tenom Agricultural Research Station,<br />

Sabah (TARSS). These entomologists are studying bee behavior, pollination or<br />

thermoregulation. TARSS is quickly becoming a center dedicated to research on bees. Bee<br />

specimens are kept at various academic institutions such as UKM, UM, UPM and UMS and<br />

government agencies such as MARDI and the Department of Agriculture (Crop Protection<br />

Division).<br />

2. Stingless bee group<br />

Like honey bees, the stingless bees also play an important role in pollination (e.g., Trigonia<br />

thoracica, the pollinator for starfruit), Stingless bees however, are not an important source of<br />

honey and they are not kept commercially in hives. Very little is known about these bees.<br />

To date, there are no Malaysian entomologists actively working on this group, nor are there<br />

any international or regional funds to support such research. However, Dr. Khoo Soo Ghee<br />

(retired lecturer of the University of Malaya) had recorded at least 35 species of Trigona from<br />

Malaysia, and this confirms Malaysia’s status as being the country with the highest diversity<br />

of Trigona species in tropical Asia (S.G. Khoo, pers. comm.). Much of the material stemming<br />

from his research (identification keys, checklists, literature and specimens) are currently kept<br />

at the Insect Collection of University of Malaya or in Dr. Khoo’s personal collection.<br />

Identification keys for both honey bees and stingless bees are available at University of Malaya,<br />

TARSS and UPM, as well as from related websites, e.g., Taxacom Listserv Archive for 1996<br />

or http://www.taxapad.com.<br />

C. Parasitic Wasps, with special emphasis on Ichneumoidea (Ichnemonidae<br />

and Braconidae)<br />

The parasitic wasps (Parasitica; refer above) is the largest group of Hymenoptera, the two<br />

largest families, Ichneumonidae and Braconidae, respectively having 35 and 28 subfamilies<br />

worldwide (Goulet & Huber 1993). These two subfamilies have been studied more than the<br />

other families. In nature, these parasitic wasps, also known as parasitoids, regulate herbivore<br />

populations, thereby reducing damage to the leaves, stems, flowers, fruits and roots of plants.<br />

In view of this, Altieri & Nicholls (2004) suggested that these wasps indirectly promote global<br />

floral and faunal diversity. However, highly disturbed habitats such as agricultural ecosystems<br />

do not favor parasitoid survival.<br />

1. Braconidae<br />

The braconids of the Old World Tropics, in particular the Indo-Australian and Oriental species,<br />

have been studied primarily by Drs. C. van Achterberg (Leiden Museum), D.L.J. Quicke<br />

(Imperial College, London) and A.B. Idris (UKM, Malaysia). At least three recent revisions<br />

have been published (Quicke 1997, Simboloti & van Achterberg 1990a, 1990b). In addition,<br />

one illustrated book to the subfamilies was published in 1996 (van Achterberg 1996), and<br />

another publication, “Keys to the Genera of Braconidae of the World,” is in press (van<br />

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THE STATUS OF RESEARCH ON HYMENOPTERA IN MALAYSIA<br />

Achterberg, pers. comm.). In Malaysia, inventory work has just begun on braconids and, to<br />

date, there are c. 7,000 braconid specimens from 22 subfamilies in the collection of the Centre<br />

for Insect Systematics (CIS), UKM. Postgraduate collaboration with the Natural History<br />

Museum in Leiden, Holland and the University of Leiden, is on-going.<br />

2. Ichneumonidae<br />

Ichneumonidae is the largest family in the order Hymenoptera and the second largest family<br />

in the Animal kingdom. The number of species in the family exceeds the total number of<br />

vertebrate species and is greater than the number of species from any other insect family, with<br />

the exception of the Cucurlionidae (weevils), which is the most speciose insect family in the<br />

world (LaSalle & Gauld 1993, Romoser & Stoffolano 1998). It is estimated that Ichneumonidae<br />

comprises 5–8% of the total number of described insect species on earth (Gaston 1993). In<br />

1969, Townes reported that 16,032 ichneumonid species had been described worldwide and<br />

that, of these, 2,579 species were from the Indo-Australian region. Based on this, he estimated<br />

that the total number of ichneumonid species worldwide could be more than 60,464.<br />

a. Systematics and Taxonomic Studies<br />

The earliest studies on Ichneumonidae were conducted by Gravenhost in 1829. In Malaysia,<br />

studies were initiated by Smith (1858), who first described Pimpla punctata (Pimplinae),<br />

Sketia croceipes (Cryptinae) and Enicospilus giganteus (Ophininae) from Sarawak (East<br />

Malaysia). In 1903, Cameron (1903) described Camptotypus rugosus (Pimplinae) from<br />

Peninsular Malaysia. Since then, many species have been described or recorded from Malaysia.<br />

Despite this, there have been no concerted efforts to collect and inventorise or to work on the<br />

taxonomy, systematics, zoogeographical distribution and phylogenetic relationships of<br />

Malaysian ichneumonids. In view of this, a study on Malaysian ichneumonids was initiated<br />

by the author in late 1997. To begin with, the genera Goryphus (Cryptinae) and Xanthopimpla<br />

(Pimplinae) were extensively studied. New species were described and new records made.<br />

Xanthopimpla is a very large tropicopolitan genus, with most species occurring in the Indo-<br />

Papuan archipelago, while the genus Goryphus is one of the commonest genera of Cryptinae<br />

and is highly abundant in the tropical and subtropical parts of the Old World. Both groups are<br />

poorly known. Studies on the genera Theronia (Pimplinae) and Enicospilus (Ophininae) have<br />

just begun in early 2005.<br />

Eight years ago, the CIS had about 300 specimens of Ichneumonidae. Today it has over 20,000<br />

specimens, accumulated over a period of seven to eight years of study. Of these, 20 specimens<br />

are types or paratypes. A total of 28 out of the 35 ichneumonid subfamilies world-wide, and<br />

21 out of the 22 ichneumonid subfamilies in the Indo-Australian region (Yu & Horstmann<br />

1997a, 1997b, Goulet & Huber 1993), have been collected. Among the subfamilies collected<br />

were Agriotypinae, Tersilochinae, Cylloceriinae, Micropleptinae, Orthopelmatinae and<br />

Tatogastrinae, which are new records for tropical Asia. A total of 140 genera were identified<br />

and, of these, at least 20 genera were new records for Malaysia. For Goryphus (Cryptinae), 20<br />

species were recorded for Malaysia (up from only 8 prior to this study), including six new<br />

records and five new species (Yu & Horstmann 1997a). A total of 58 species of the genus<br />

Xanthopimpla were also recorded, of which five species were new to science and nine species<br />

were new records for Malaysia. This represents a 40% increase in the number of species<br />

recorded from Malaysia. To date we have already successfully identified one species of<br />

Enicospilus, that is, E. lietincki, as a new record for Malaysia.<br />

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IDRIS A.B. (2007)<br />

Molecular phylogenetic studies using 28S rRNA and CO1 genes are in progress. Our<br />

preliminary results indicate that the use of CO1 genes gives better resolution compared to 28S<br />

genes. In addition, phylogenies derived from molecular classification agreed with those derived<br />

from morphology, at the genus level (Idris et al. 2005).<br />

b. Ecological Studies<br />

Results from an ecological study conducted in several localities in Peninsular Malaysia, that<br />

is, Taman Negara Merapoh (TNM), Pasoh Forest Reserve (PFR), Kuala Lompat Forest Reserve<br />

(KLFR) in the Krau Wildlife Reserve, Bangi Forest Reserve (UKMFR), Kuala Langat South<br />

Forest (HKLS) and Kuala Langat North Forest (HKLU), showed that the abundance of<br />

Xanthopimpla spp. (Hymenoptera: Ichneumonidae) were significantly different between<br />

localities. Table 2 shows the ichneumonid species diversity (Shannon-Weiner diversity index,<br />

H’) in the six different forest localities. The ichneumonid abundance in TNM, a primary<br />

forest, was not significantly different from that in HKLU, a forest that had been logged five<br />

years ago. In fact, both forests had somewhat similar species richness indices (Margalef’s<br />

richness index, R’) and evenness indices (Shannon-Weiner evenness index, E’). Interestingly,<br />

only 48% of species were common to both forests. The primary forest conditions of TNM<br />

help equilibrate the population of Xanthopimpla species within the resources available. HKLU,<br />

even though highly fragmented, has a high number of individuals and high species diversity.<br />

This suggests that H’ will be high, irrespective of the degree of habitat disturbance, as long as<br />

the number of species (richness, R’) and number of individuals of a species (evenness, E’) are<br />

high (Magurran 1988). Disturbed forest fragments result in an increase in the abundance and<br />

diversity of arthropod species (Samways, 1994). Although some species may be lost as a<br />

result of disturbances, others may benefit from these same disturbances. The abundance and<br />

diversity of wasps in HKLU could be attributed to the EL-Nino effects or a difference in<br />

forest type. It could also be due to the heterogeneity of HKLU as compared to other forests as<br />

suggested by the habitat heterogeneity hypothesis (Price 1984, Gauld 1987, Huston 1994). In<br />

comparison with other forest fragments, HKLU is considerably more dynamic, as it was logged<br />

in 1993 and constitutes vegetation still under succession. HKLS was last logged in 1976,<br />

while PFR and KLFR were logged more than 50 years ago and would have achieved greater<br />

climax equilibrium. PFR is considered less disturbed (FRIM, 1995), while Kuala Lompat is<br />

adjacent to a large area of pristine forest. HKLS, Pasoh and Kuala Lompat had low wasp<br />

abundance and diversity and this is probably due to competitive equilibrium resulting from<br />

Table 2. Shanon diversity indices (H’), evenness indices (E’) and Margalef’s indices (richness<br />

indices, R’) for Xanthopimpla species in six different forest localities in Peninsular Malaysia.<br />

Forests 1<br />

H’ E’ R’<br />

Hutan Kuala Langat Utara (HKLU) 2 2.62 a 0.95 4.93<br />

Taman Negara, Merapoh (TNM) 2.55 a 0.94 4.47<br />

Pasoh Forest Reserve (PFR) 1.99 b 0.96 2.73<br />

Kuala Lompat Forest Reserve (KLFR) 1.98 b 0.95 2.82<br />

Bangi Forest Reserve (UKMFR) 1.89 b 0.91 2.92<br />

Hutan Kuala Langat Selatan (HKLS) 2 1.70 b 0.95 2.17<br />

1<br />

Values of H’ with similar alphabets were not significantly different at p < 0.05 (paired t-test).<br />

2<br />

HKLU and HKLS are peat swamp forests; the others are lowland dipterocarp forests.<br />

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THE STATUS OF RESEARCH ON HYMENOPTERA IN MALAYSIA<br />

competitive exclusion (Huston, 1994; Cox & Moore, 1993). For Bangi FR, the low wasp<br />

abundance and diversity are probably due to its isolated location and small fragment size (it is<br />

only 105 ha). Huston (1994) pointed out that in smaller areas, competition is high and this<br />

results in equilibrium between extinction and immigration; such areas are likely to have lower<br />

diversity compared with larger areas.<br />

The study also showed that ichneumonid diversity was significantly higher in the understorey<br />

than in the middle-storey or canopy of the forest, based on traps placed on a canopy tower at<br />

0 m, 8 m and 15 m above ground level. Species richness and species evenness followed the<br />

same trend (Idris & Kee 2002). These results agree with that of Gonzaga & Idris (2004), who<br />

studied the vertical abundance of Xanthopimpla species (Ichneumonidae) in Pasoh Forest<br />

Reserve. Idris & Kee (2002) found that ichneumonid diversity tended to increase from the<br />

forest fringe into the interior, but only up to between 400 to 600 m into the interior of the<br />

forest (Table 3). This indicates that there are more ichneumonid species in the interior of the<br />

forest than in the fringe, and that species that inhabit the interior of the forest may be sensitive<br />

to disturbance. However, this was not the case for some species of genus Xanthopimpla such<br />

as X. gampsura, X.elegans elegans and X. stemator, as their abundance and diversity tended<br />

to be higher in the fringe than in the interior of the forest (Gonzaga & Idris 2004). The percent<br />

species similarity between all ground level samples and the ground level samples at the base<br />

of the canopy tower was higher than the percent species similarity between ground level traps<br />

and traps placed at a height of 15 m on the canopy tower (Table 4).<br />

In 1998, a series of studies were conducted at the Bangi Forest Reserve to compare the<br />

effectiveness of various collecting methods. Malaise traps, pitfall traps, yellow pan traps,<br />

light traps and sweep nets were used. The results indicated that Malaise traps were more<br />

effective. In Sulawesi, Indonesia, Noyes (1989) found that yellow pan traps and sweep nets<br />

Table 3. Shannon diversity index (H’), species evenness (E), and species richness (R) for<br />

Ichneumonidae collected at the Sungkai Wildlife Forest Reserve, Perak, Malaysia from July<br />

till October 2000.<br />

Shannon’s<br />

Trap location Diversity Shannon’s Margalef’s index<br />

Index (H’) 1 Evenness (E) (Richness, R)<br />

Horizontal distance<br />

from forest edge (m) 2<br />

0 2.76 b 0.89 5.91<br />

100 3.50 c 0.94 10.23<br />

200 4.30 d 0.99 16.96<br />

400 4.53 d 0.97 16.87<br />

600 4.49 d 0.95 16.90<br />

Vertical Height (m) 3<br />

0 3.68 b 0.95 9.19<br />

15 0.35 a 1.52 1.68<br />

1<br />

Values of H’ with the same alphabet were not significantly different at alpha = 0.05.<br />

2<br />

Malaise traps were installed on the ground or forest floor.<br />

3<br />

Malaise traps were installed at the top and bottom of a canopy tower 400 m from the forest edge.<br />

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IDRIS A.B. (2007)<br />

Table 4. Percent species similarity of Ichneumonid species between ground level and canopy<br />

samples at Sungkai Wildlife Forest Reserve, Perak, Malaysia (July to October 2000).<br />

Species similarity (%)<br />

Sampling location Horizontal Horizontal Bottom of Top of<br />

(total) (400 m) tower tower<br />

Horizontal (total) 1 100 - - -<br />

Horizontal (400 m) 2 75.4 100 - -<br />

Bottom of tower 3 50 98.7 100 38.1<br />

Top of tower 3 33.3 45.4 38.1 100<br />

1<br />

All species from all sites in the horizontal sampling with ground-level Malaise traps, viz. 0, 100, 200, 400 and 600<br />

m from the forest edge.<br />

2<br />

Data for horizontal sampling with ground-level Malaise traps at 400 m from the forest edge.<br />

3<br />

Data for the canopy tower, 400 m from the forest edge (bottom = 0 m, top = 15 m from forest floor).<br />

sometimes collected more ichneumonids in areas that are undulating. Although the Bangi<br />

forest is also undulating, the mean numbers of ichneumonids caught in yellow pan traps and<br />

sweep nets were significantly lower than in Malaise traps. However, for the nocturnal<br />

ichneumonid subfamily Ophioninae, light traps were more effective.<br />

A study on the flight phenology of ichneumonids in the primary and regenerating forests of<br />

Pasoh F.R. was conducted from April 2002 to March 2003. Generally, in both forests, there were<br />

two peaks flight activities, viz., June-July and October-December 2002, with the highest activity<br />

recorded in July 2002. Based on the flight phenology of the different genera, parasitoids could<br />

be categorized into genera that (1) peaked twice a year, (2) peaked only in June-July, (3) peaked<br />

only in October-December and (4) peaked in March. However, the flight activity of most genera<br />

varied with locality. The results also showed that seasonal new leaf flushes of trees may influence<br />

flight activity of ichneumonids. More ichneumonids were caught during the dry season of May<br />

to August 2002 than during the wet season of October to December 2002. Additionally, the<br />

optimum number of samples needed to yield maximum species diversity (the asymptote or<br />

threshold level) was higher in primary forests than in secondary or disturbed forests.<br />

c. Zoogeographical Distribution<br />

A study on the zoogeographical distribution of the genus Xanthopimpla and Goryphus recorded<br />

58 species and three subspecies of Xanthopimpla in Malaysia (Idris et al. 2005). Of these, 53<br />

and 34 were from Malay Peninsular and East Malaysia (Sabah and Sarawak), respectively.<br />

Only 20 species of Goryphus have been recorded in Malaysia: 12 species from the Peninsula<br />

and eight species from Sabah (no species have been recorded from Sarawak yet). The lower<br />

number of species recorded from East Malaysia is due to lower sampling intensity as a<br />

consequence of a limited budget. Zoogeographical maps showing the distribution of each<br />

species in Peninsular Malaysia, Sabah and Sarawak are available (Idris et al. 2005).<br />

d. Potential Biological Indicators<br />

There was a significant difference between disturbed and undisturbed habitats in relation to<br />

body size class distribution of Xanthopimpla species (Table 5). Although medium- and smallsized<br />

Xanthopimpla species dominated both habitats, populations of larger-sized species<br />

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THE STATUS OF RESEARCH ON HYMENOPTERA IN MALAYSIA<br />

(approximately 12 mm body length or larger) tended to be higher in disturbed areas. This<br />

could be an example of competitive exclusion, in which certain species are prevented from<br />

occupying an area by the presence of other species (Cox & Moore, 1993). Xanthopimpla<br />

species, as examples of pimpline wasps, lay eggs in suitable hosts, and larger species select<br />

hosts that enable the development of a larger wasp. (Gauld, 1984). Disturbed habitats may<br />

favor the existence of suitable hosts for large Xanthopimpla species, which compete with<br />

smaller species for the limited resources available. Certain large species like X. gampsura<br />

were abundant in disturbed habitats, while X. nigritarsis nigritarsis was found only in pristine<br />

habitats. Although the finding is preliminary and needs to be verified by replication at other<br />

locations, these two species of Xanthopimpla may have the potential to be used as biological<br />

indicators for habitat disturbance.<br />

Table 5. Contingency table 1 for the body length of Xanthopimpla species collected in<br />

undisturbed and disturbed habitats.<br />

Body length (mm) Undisturbed Disturbed<br />

Small (5.30 - 8.66) 16 20<br />

Medium (8.67 - 12.03) 30 11<br />

Large (12.04 - 15.4) 2 11<br />

Total 48 42<br />

1<br />

Chi Square (2 degrees of freedom) = 15.15, p < 0.001.<br />

PUBLICATIONS AND OTHER SOURCES OF INFORMATION ON<br />

ICHNEUMONIDAE AND OTHER PARASITIC HYMENOPTERA<br />

There are many ways to access information on Hymenoptera, in particular the Ichneumonidae<br />

and other parasitic hymenopterans. Provided below is a list of relevant references, revisions,<br />

catalogues, CD-ROMs and electronic information-sources (websites, etc). Useful books for<br />

beginners are those written by LaSalle & Gauld (1993), Gauld & Bolton (1996), Austin &<br />

Dowton (2000), Quicke (1987), Morley (1913) and Goulet & Huber (1993). Books or<br />

catalogues specifically on Braconidae (braconid wasps) and Formicidae (ants) have been written<br />

by van Achterberg (1996), Shenefelt (1975), van der Vecht & Shenefelt (1969) and Bolton<br />

(1997). Many other books or catalogues provide information on Ichneumonid wasps<br />

(Hymenoptera: Ichneumonidae) but these are too numerous to list here. To date, few revisions<br />

on Ichneumonidae and Braconidae have been published; these are Townes (1983), Quicke<br />

(1997) and Simboloti & van Achterberg (1990a & 1990b). Bouèek (1988) and Huang &<br />

Noyes (1994) provide good revisions for Chalcidoidea and Encyrtidae, respectively.<br />

There are several journals that frequently publish or are devoted to research on Hymenoptera<br />

(Table 7). The Oriental Insects Monograph, Pacific Insect Monograph and Ichneumonologia<br />

Orientalis commonly publish articles on Ichneumonidae and Braconidae of the Indo-Australian<br />

and Oriental Regions, while the Zoologische Mededelingen Leiden and Zoologische<br />

Verhandelingen usually publish articles on braconids. The Journal of Hymenoptera Research<br />

publishes research on any aspect of Hymenoptera. Other articles on Hymenoptera diversity<br />

and taxonomy can also sometimes be found in Serangga, Bulletin of Entomological Research,<br />

Biocontrol and various other entomological journals.<br />

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IDRIS A.B. (2007)<br />

At least one Interactive Catalogue of World Ichneumonidae called ‘Taxapad 1998’ is available<br />

in the form of CD-ROM (Table 7). (http:/www.taxapad.com) The CD is available for purchase<br />

at over RM 2,000/-, inclusive of a guide book. A CD-ROM identification guide to the genera<br />

of Braconidae is almost ready (van Achterberg, pers. comm.). Information on Chalcidoidea is<br />

also available online (http://www.nhm.ac.uk/entomology/chalcidoids) and ‘A Universal<br />

Chalcidoidea Database’ on CD ROM is also available for purchase (RM 4,000/- each) (John<br />

Noyes, pers. comm.). The proceedings of the ‘International Symposium on biological control<br />

of arthropods’ is also available on CD ROM (van Driesche, pers. comm.).<br />

Table 6. List of publications related to Ichneumonidae and other parasitic Hymenoptera<br />

Type of References and Titles<br />

Author (s) and Year<br />

Books/Revisions/Catalogues<br />

1. Hymenoptera & Biodiversity LaSalle & Gauld 1993<br />

2. The Hymenoptera Gauld & Bolton 1996<br />

3. Hymenoptera: Evolution, Biodiversity & Biological Control Austin & Dowton 2000<br />

4. Parasitic wasps Quicke 1997<br />

5. Hymenoptera of the World: Identification to Subfamilies Goulet & Huber 1993<br />

6. Illustrated Key to Subfamilies Braconidae (Hymenoptera: van Achterberg 1996<br />

Ichneumonoidea)<br />

7. Identification Guide to the Ant Genera of the World Bolton 1997<br />

8. Fauna of British India. Vol 3: Hymenoptera Morley 1913<br />

9. Australasian Chalcidoidea Bouèek 1988<br />

10. An Introduction to the Ichneumonidae of Australia Gauld 1984a<br />

11. The Pimplinae, Xoridinae, Acaenitinae and Lycorininae Gauld 1984b<br />

(Hymenoptera: Ichneumonidae) of Australia<br />

12. The taxonomy, distribution & host preferences of African Gauld & Mitchell 1978<br />

Parasitic Wasps of the Subfamily Ophioninae<br />

13. The taxonomy, distribution & host preferences of Indo-Papuan Gauld & Mitchell 1981<br />

Parasitic Wasps of the Subfamily Ophioninae (Hymenoptera:<br />

Ichneumonidae)<br />

14. Studies on the Hymenoptera. A collection of articles on Gupta 1993<br />

Hymenoptera commemorating the 70 th Birthday of Henry<br />

Townes<br />

15. Revision of genera Gelini (Ichneumonidae). Townes 1983<br />

16. A Catalogue and Reclassification of the Indo-Australian Townes et al. 1961<br />

Ichneumoidae<br />

17. A Catalogue of World Ichneumonidae (Parts 1 & 2) Yu & Horstmann<br />

1997a,1997b<br />

18. The Indo-Australian species of Xanthopimpla (Ichneumonidae) Townes & Chiu 1970a<br />

1970b<br />

19. Genera of Ichneumonidae, Part I Townes 1969<br />

20. A revision of the Indo-Pacific Species of Ooencyrtus Huang & Noyes 1994<br />

(Hymenoptera: Encyrtidae)<br />

21. Revision of the Euagathis species (Hymenoptera: Braconidae) Simboloti & van<br />

from Sulawesi<br />

Achterberg 1990a<br />

22. Revision of the Euagathis species (Hymenoptera: Braconidae) Simboloti & van<br />

from the Sundaland<br />

Achterberg 1990b<br />

23. Hymenopterorum Catalogus: Braconidae 8 Shenefelt 1975<br />

24. Hymenoptera Catalogus: Braconidae 1 van der Vecht &<br />

Shenefelt 1969<br />

25. The Old World Genera of Braconine Wasps Quicke 1987<br />

(Hymenoptera: Braconidae)<br />

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THE STATUS OF RESEARCH ON HYMENOPTERA IN MALAYSIA<br />

Researchers working on Hymenoptera can stay in touch with each other by registering<br />

themselves in a discussion group (parahym@)nhm.ac.uk). Registration can be done online or<br />

by contacting John Noyes at the NHM (j.noyes@nhm.ac.uk). The ‘International Hymenoptera<br />

Conference’ is held every four years and enables researchers to present their research findings.<br />

Table 7. Examples of some Journals, CD-ROM/VCD, Websites and Researchers Working on<br />

Hymenoptera Parasitica.<br />

Journals<br />

1. Journal of Hymenoptera Research<br />

2. Journal Natural History<br />

3. Zoologische Mededelingen Leiden.<br />

4. Zoologische Verhandelingen.<br />

5. Serangga<br />

6. Oriental Insects Monograph<br />

7. Pacific Insect Monograph<br />

8. Ichneumonologia Orientalis<br />

9. Bulletin Entomological Research<br />

(Devoted to only systematics articles except for no.7 and 9)<br />

CD-ROM/VCD<br />

1. Interactive Catalogue of World Ichneumonidae. 1998.<br />

(Taxapad 1999) by Dicky, S. Yu. 1998.<br />

http://www.taxapad.com<br />

2. Universal Chalcidoidea Database : CD-ROM by Noyes (1998).<br />

http://www.nhm.ac.uk/entomology/chalcidoids<br />

3. International Symposium on biological control of arthropods.<br />

CD-ROM Delta-interkey CSIRO, Australia.<br />

Available Websites<br />

http:/www.nhm.ac.uk/entomology/chalcidoids<br />

http://www.nhm.ac.uk/entomolgy/hymcours<br />

http://www.insectconsultancy.nl<br />

http://www.sfu.ca/~carmean/tig/<br />

http://www.tolweb.org<br />

http://www.zoo.bio.ufpr.br/hymenoptera<br />

http://www.hymenoptera.tamu.edu/<br />

http://hymenoptera.tamu.edu/ish/<br />

http://www.discoverlife.org<br />

http://www.royensoc.co.uk<br />

hymenopterans<br />

hymenopterans<br />

stingless bees<br />

Apocrita<br />

hymenopoterans<br />

hymenopterans<br />

chalcids<br />

especially ants<br />

insect parasitoids<br />

RESEARCHERS<br />

Currently, few researchers work on hymenopterans, and many of those that do work on this<br />

order work on bees, ants and larger-sized wasps (e.g., vespids and specids), which are not as<br />

diverse as ichneumonids, braconids and chalcids (Goulet & Huber 1993). Table 8 lists the<br />

researchers working on parasitic Hymenoptera.<br />

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IDRIS A.B. (2007)<br />

Table 8. List of Researchers working on the specific groups of Hymenoptera, and Institution<br />

in which they are attached.<br />

Hymenoptera Group Researchers Institute(s)<br />

Ichneumonids M. Fitton & I. D. Gauld Natural History Museum,<br />

London<br />

V.K Gupta<br />

University of Florida/<br />

American Institute of<br />

Entomology, Florida<br />

D.K. Yu<br />

Agriculture & Agri-Food<br />

Canada Research Center,<br />

Alberta, Canada<br />

D. Wahl American Entomological<br />

Institute, Gainesville, Florida,<br />

USA<br />

K. Horstmann Biozentrum, Zoologie III, Am<br />

Hubland, Germany<br />

H. Goulet, J.T Huber Center for Land & Biological<br />

& M.J Sharkey<br />

Resources Research Ottawa,<br />

Canada<br />

Braconids D.L. Quicke Imperial College of Science,<br />

Technology and Medicine,<br />

University of London<br />

C. van Achterberg The Natural History Museum,<br />

Leiden, Holland<br />

A.D Austin<br />

R.A.Wharton<br />

J.B. Whittfield<br />

University of Adelaide,<br />

Australia<br />

Department of Entomology,<br />

Texas A & M University,<br />

Texas, USA<br />

University of Illinois at<br />

Urbana Champaign, USA<br />

Chalcids J. Heraty University of California,<br />

Riverside<br />

J. Noyes Natural History Museum,<br />

London<br />

J. LaSalle CSIRO, Australia<br />

SOURCES OF FUNDS<br />

Funds to conduct research on Hymenoptera can be sourced from the ASEAN Regional Centre<br />

for Biodiversity Conservation, the Japanese International Cooperation Agency (JICA), the<br />

Darwin Initiative, Asia-Link Projects (supported by the European Union) and the Japan Society<br />

for the Promotion of Science (JSPS). Locally, government and semi-government agencies<br />

such as the Ministry of Science, Technology and Innovation (under the Intensification of<br />

Research Priority Areas or IRPA grant system), Federal Land Development Authority (FELDA)<br />

and the Johor State Park are primary sources of funding. With sufficient funds, inventories<br />

and research into the taxonomy, and ecology of Malaysian Hymenoptera can be conducted.<br />

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THE STATUS OF RESEARCH ON HYMENOPTERA IN MALAYSIA<br />

Overseas funding agencies are also open avenues for collaboration between local taxonomists<br />

and foreign researchers.<br />

DEPOSITORIES OF COLLECTIONS<br />

Many collections of Hymenoptera are housed in various institutes of higher learning and<br />

museums overseas. The largest collections, with many type specimens, are in the Natural<br />

History Museum (United Kingdom), Oxford University Museum (United Kingdom), National<br />

Museum of Natural History (Leiden, Netherlands), American Institute of Entomology Insect<br />

Collection (Florida, USA) and other museums in Europe, Japan and the USA. The American<br />

Institute of Entomology Insect Collection in Florida has c. 800,000 of ichneumonid specimens.<br />

Museums and insect collection centers that have Malaysian specimens include:<br />

• Bishop Museum, 1525 Bernice Street, Honolulu, HI 69817-0916 USA.<br />

• Deutsches Entomologisches Institut Schicklerstrasse 5D-16225 Eberswalde, Germany.<br />

• Hope Entomological Collections, The University Museum, Parks Road, Oxford OX1<br />

3PW United Kingdom.<br />

• Institut Royal des Sciences Naturelles de Belgique, Département d’Entomologie, Rue<br />

Vautier 29, B-1000 Bruxelles, Belgique.<br />

• Muséum National d’Histoire, Laboratoire d’Entomologie, 45 rue de Buffon, F-75005<br />

Paris, France.<br />

• Museum Victoria Science Program, GPO BOX 666E, Melbourne, Victoria 3001 Australia.<br />

• National Museum of Natural History, Naturalis, P.O. Box 9517, 2300 RA Leiden, The<br />

Netherlands.<br />

• Naturhistorisches Museum Wien, Burgring 7, A-1014 Wien, Austria.<br />

• Systematic Entomology, Faculty of Agriculture, Hokkaido University, 060-8589, Japan.<br />

• The Natural History Museum, Cromwell Road, London SW7 5BD, United Kingdom.<br />

• Universiteit van Amsterdam, Zoölogisch Museum Amsterdam, Afdeling Entomologie,<br />

Plantage Middenlaan 64, 1018 DH Amsterdam, the Netherland.<br />

• Zoological Museum, University of Copenhagen, Universitetsparken 15 DK-2100<br />

Copenhagen, Denmark.<br />

• Zoologisches Museum an der Humboldt-Universität zu Berlin, 10115 Berlin,<br />

Invalidenstrae 43, Germany.<br />

• American Institute of Entomology Insect Collection, University of Florida, USA.<br />

CONCLUSION<br />

Hymenopterans are an important component of our national biodiversity heritage, and play a<br />

significant role in maintaining ecological balance in many natural and man-made ecosystems.<br />

Only two Malaysian researchers are currently working on the taxonomic diversity and species<br />

abundance of Hymenoptera in relation to habitat change. The difficulties in getting grants and<br />

reference materials and the lack of job vacancies for students trained in taxonomic research<br />

contribute to the dearth of researchers. Only few institutes have specimen holdings i.e., the<br />

Center for Insect Systematics of UKM, Borneansis Collection (University Malaysia Sabah),<br />

Forest Research Institute Malaysia (FRIM) and Sabah Forest Research Center (FRC). It would<br />

be very difficult to develop checklists, revisions or catalogues on Hymenoptera if the basic<br />

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IDRIS A.B. (2007)<br />

need for local expertise and resources are not met. While Malaysia may have adequate facilities<br />

for such research, a further problem is the insufficiency of annual funds to curate specimens<br />

on a long term basis.<br />

ACKNOWLEDGEMENTS<br />

We thank the CIS staff who were involved in the studies. The studies were funded by IRPA<br />

09-02-02-0022, 09-02-02-0170 and 09-02-02-0017-EA072 under the auspices of the Ministry<br />

of Science, Technology and Innovation (MOSTI).<br />

REFERENCES<br />

ALTIERI, M.A. & NICHOLLS, C.I. 2004. Biodiversity and Pest Management in<br />

Agroecosystems. 2 nd Edition. Food Products Press. An Imprint of The Haworth Press,<br />

Inc., New York.<br />

AUSTIN, A.D. & DOWTON, M. 2000. Hymenoptera: Evolution, Biodiversity and Biological<br />

Control. CSIRO Publishing, Australia. 467 pp.<br />

AUSTIN, A.D. 1999. The role of species in biodiversity research–lessons from the parasitic<br />

Hymenoptera. Pp. 159–165 in W. Ponder & D. Lunney (eds.). The Conservation and<br />

Biodiversity of Invertebrates. Royal Society of New South Wales, Sydney.<br />

BAKHTIAR, E.Y. 2000. The role of three insect groups (ants, dung beetles and geomerid<br />

moths) as biological indicator in three habitat types (primary forest, secondary forest<br />

and oil palm plantation) at Tabin, Lahad Datu, Sabah. MSc Thesis. Universiti Malaysia<br />

Sabah. 196 pp.<br />

BOLTON, B. 1955. A New Genera Catalogue of the Ants of the World. Harvard University<br />

Press, Cambridge, Massachusetts.<br />

BOLTON, B. 1977. The ant tribe Terramoriini. The genus Tetramorium Mayr in the Oriental<br />

and Indo-Australian regions, and in Australia. Bulletin of the British Museum (Natural<br />

History) (Entomology) 36: 67–151.<br />

BOLTON, B. 1997. Identification Guide to the Ant Genera of the World. Harvard University<br />

Press, Cambridge, London. 222 pp.<br />

BOUEK, Z. 1988. Australasian Chalcidoidea (Hymenoptera): A Biosystematic Revision of<br />

Genera of Fourteen Families, with a Reclassification of Species. CAB International, UK.<br />

832 pp.<br />

BRUHL, C.A. 2001. Leaf litter ant communities in tropical lowland rainforest in Sabah,<br />

Malaysia. Effects of forest disturbance and fragmentation. PhD Thesis. Universiti Malaysia<br />

Sabah. 230 pp.<br />

BRUHL, C.A., GUNSALAM, G. & LINSENMAIR, K.E. 1998. Stratification of ants<br />

(Hymenoptera: Formicidae) in a primary rainforest in Sabah, Borneo. Journal of Tropical<br />

Ecology 14: 285–297.<br />

CAMERON, P. 1903. Description of new genera and species of Hymenoptera taken by Robert<br />

Sheford at Sarawak, Borneo. Journal of the Straits Branch of the Royal Asiatic Society<br />

39: 101–153.<br />

CHUNG, A.Y.C. 1993. Kajian fauna semut (Hymenootera: Formicidae) di Hutan Hujan<br />

Tropika (Promer dan Sekunder) di Lembah Danun, Sabah. BSc Thesis, Universiti<br />

Kebangsaan Malaysia. 108 pp.<br />

163


THE STATUS OF RESEARCH ON HYMENOPTERA IN MALAYSIA<br />

CHUNG, A.Y.C. 1995. Common lowland rainforest ants of Sabah. The Borneo Nature Series<br />

No. 1: Sabah. 59 pp<br />

COX, B.C. & MOORE, P.D. 1993. Biogeography: An Ecological and Evolutionary Approach.<br />

5 th edition. Blackwell Scientific Publications. Oxford.<br />

GASTON, K.J. 1993. Spatial patterns in the description and richness of the Hymenoptera. Pp.<br />

277–293 in LaSalle, J. & Gauld, I.D. (eds.). Hymenoptera and Biodiversity. CABI,<br />

Wallingford.<br />

GAULD, I. & BOLTON, B. (eds.). 1996. The Hymenoptera. 2 nd Edition. Oxford University<br />

Press, Oxford and The Natural History Museum, London.<br />

GAULD, I.D. & MITCHELL, P.A. 1978. The taxonomy, distribution & host preferences of<br />

African Parasitic Wasps of the Subfamily Ophioninae. CAB & CIE, England.<br />

GAULD, I.D. & MITCHELL, P.A. 1981. The taxonomy, distribution & host preferences of<br />

Indo-Papuan Parasitic Wasps of the Subfamily Ophioninae. CAB & CIE, England.<br />

GAULD, I.D. 1984a. An Introduction to the Ichneumonidae of Australia with a contribution<br />

on Metopiinae by M.G. Fitton. British Museum of Natural History, London.<br />

GAULD, I.D. 1984b. The Pimplinae, Xoridinae, Acaenitinae and Lycorininae (Hymenoptera:<br />

Ichneumonidae) of Australia. Bull. Brit. Mus. Nat. Hist. (Ent.) 49(4): 235–339.<br />

GAULD, I.D. 1987. Some factors affecting the composition of tropical ichneumonid faunas.<br />

Biol. J. Linn. Soc. 30: 299–312.<br />

GAULD, I.D. 1991. The Ichneumonidae of Costa Rica. Memoirs of the American<br />

Entomological Institute Volume 47.<br />

GONZAGA, A.D. & IDRIS, A.B. 2004. Horizontal and Vertical Distribution of Genus<br />

Xanthopimpla (Hymenoptera: Ichneumonidae) in an Ecological Plot of Pasoh Forest<br />

Reserve, Malaysia. J. Asia-Pacific Entomology 7(2): 221–225.<br />

GOULET, H. & HUBER, J.T. 1993. Hymenoptera of the world. An Identification Guide to<br />

Subfamilies. Research Branch, Agriculture Canada, Publication 1894/E. 668 pp.<br />

GUPTA, V. K. (ed.) 1993. Studies on the Hymenoptera. A collection of articles on Hymenoptera<br />

Commemorating the 70 th Birthday of Henry Townes. Contributions of the American<br />

Entomological Institute, Vol. 20.<br />

GUPTA, V.K. 1987. Catalogue of the Indo-Austarlian Ichneumonidae. Memoirs of the American<br />

Entomological Institute 41: 17–237.<br />

HANSON, P. E. & GAULD, I.D. (eds.) 1995. The Hymenoptera of Costa Rica. Oxford<br />

University Press, Oxford and The Natural History Museum, London.<br />

HUANG, D.W. & NOYES, J.S. 1994. A revision of the Indo-Pacific species of Ooencyrtus<br />

(Hymenoptera: Encyrtidae), parasitoids of the immature stages of economically important<br />

insect species. Bull. Br. Mus. Nat. Hist. 63(1): 1–136.<br />

HUSTON, M.A. 1994. Biological Diversity: The Coexistence of Species on Changing<br />

Landscapes. Cambridge University Press. Great Britain.<br />

IDRIS, A.B. & KEE, S.S. 2002. Horizontal and vertical diversity of Ichneumonid wasps<br />

(Hymenoptera: Ichneumonidae) in the Sungkai Wildlife Forest Reserve in Perak, Malaysia.<br />

J. Asia-Pacific Entomol. 5: 85–89.<br />

IDRIS, A.B., NUR AZURA, A., GONZAGA, A.D. NG, Y.F. & SUHANA, Y. 2005. Current<br />

study on Ichneumonid of Malaysia. Report of Insect Inventory Project in Tropic Asia<br />

(TAIIV): 71–81.<br />

JOHNSON, N.F. 1992. Catalogue of World Species of Proctotrupoidea. Exclusive of<br />

Palatygastridae (Hymenoptera). The American Entomological Institute, Gainsesville.<br />

JONATHAN, J.K. & GUPTA, V. K. 1973. Ichneumonologia Orientalis: Part III. The Goryphus-<br />

Complex (Hymenoptera: Ichneumonidae). The Association for the Study of Oriental<br />

Insects, Dept. of Zoology, University of New Delhi, India.<br />

164


IDRIS A.B. (2007)<br />

LASALLE, J. & GAULD, I.D. 1993. Hymenoptera and Biodiversity. CABI, Wellingford.<br />

348 pp.<br />

MAGURRAN, A.E. 1988. Ecological Diversity and its Measurement. Chapman & Hall.<br />

New York.<br />

MARYATI, M. 1995. Semut, UBTP: Universiti Malaysia Sabah. Dewan Bahasa dan Pustaka.<br />

53 pp.<br />

MARYATI, M. 1998. Terresterial Ants (Formicidae: Hymenoptera) of Sayap-Kinabalu Park,<br />

Sabah. ASEAN Review of Biodiversity and Environmental Conservation (ARBEC).<br />

15 pp.<br />

MARYATI, M., AZIZAH, H. & ARBAIN, K. 1996. Terrestrial ants (Hymenoptera: Formicidae)<br />

of Poring, Kinabalu Park, Sabah. Pp 117-123. In Tropical rainforest research–current<br />

issues, Monographiae biologicae, Edward, D.S., Booth, W.T. & Choy, S.C. (Eds.). Kluwer<br />

Academic Publisher, London.<br />

MCNEELY, J.A., MILLER, K.A., REID, W.V., MITTERMEIR, R.A. & WERNER, T.B. 1990.<br />

Conserving the World’s Biological Diversity. IUCN, Gland, Switzerland; WRI, CI, WWF-<br />

US and the World Bank, Washington, DC.<br />

MORLEY, C. 1913. The Fauna of British India. Hymenoptera, Vol. III. Tylor & Francis.<br />

London.<br />

NOEL, B.T. 2004. Comparison on ant and termite diversity between regenerating and primary<br />

forest in Danum Valley and their relationship with physical, climatic and biological factors.<br />

MSc Thesis, Universiti Malaysia Sabah. 78 pp.<br />

NORHASILAH, M.Y 2000. Taburan semut (Hymenoptera: Formicidae) mengikut altitude di<br />

Gunung Kinabalu. BSc Thesis, Universiti Malaysia Sabah. 70 pp.<br />

NOYES, J.S. 1989. The diversity of Hymenoptera in the tropics with special references to<br />

Parasitica in Sulawesi. Ecological Entomology 14: 197–207.<br />

NOYES, J.S. 1998. Catalogue of the Chalcidoidea of the World. Biodiversity Catalogue<br />

Database and Image Library CDROM Series. ETI Biodiversity Center, Amsterdam.<br />

PRICE, P.W. 1984. Insect Ecology. John Wiley & Sons, Toronto. 300 pp.<br />

QUICKE, D.L.J. 1987. The old world genera of braconine wasps (Hymenoptera: Braconidae).<br />

J. Nat. Hist. 21: 43–157.<br />

QUICKE, D.L.J. 1997. Parasitic Wasps. Chapman & Hall, London. 470 pp.<br />

ROMOSER, W.S. & STOFFALANO. J.G., JR. 1998. The Science of Entomology. 4 th edition.<br />

Mc Graw Hill, Washington DC. 605 pp.<br />

SAMWAYS, M.J. 1994. Insect Conservation Biology. Chapman & Hall, London. 274 pp.<br />

SHANMUGA, S. 1996. Ant composition (Hymenoptera) along an elevation gradient in Mount<br />

Kinabalu, Sabah. MSc Thesis, Universiti Malaysia Sabah. 110 pp.<br />

SHARKEY, M.J. 1988. A taxonomic Revision of Alabagrus (Hymenoptera: Braconidae).<br />

Bull. Br. Mus. Nat. Hist. 57(2): 31–437.<br />

SHENEFELT, R.D. 1975. Hymenopterorum Catalogus. Braconidae 8. Uitgeverij Dr. W. Junk<br />

B.V. 230 pp.<br />

SIMBOLOTI, S. & VAN ACHTERBERG, C. 1990a. Revision of the Euagathis species<br />

(Hymenoptera: Braconidae) from Sulawesi. Zool Ver.Nat. Hist. Mus., Leiden.<br />

SIMBOLOTI, S. & VAN ACHTERBERG, C. 1990b. Revision of the Euagathis species<br />

(Hymenoptera: Braconidae) from the Sundaland. Zool Verh. Nat. Hist. Mus, Leiden.<br />

SMITH, F. 1858. Catalogue of Hymenopterous insects collected at Sarawak, Borneo ; Mt<br />

Ophir, Malacca and at Singapore by A.R. Wallace. Journal of the Proceedings of the<br />

Linnaean Society of London. Zoology 2: 42–130.<br />

TOWNES, H. 1969. The genera of Ichneumonidae, Part 1. Memoirs of the American<br />

Entomological Institute 11: 1–300.<br />

165


THE STATUS OF RESEARCH ON HYMENOPTERA IN MALAYSIA<br />

TOWNES, H. 1983. Revision of Genera of Gelini (Ichneumonidae). Memoirs of the American<br />

Entomological Institute 35: 281 pp.<br />

TOWNES, H. & CHIU, S.C. 1970a. The Indo-Australian species of Xanthopimpla<br />

(Ichneumonidae). Memoirs of the American Entomological Institute 14: 1–36.<br />

TOWNES, H. & CHIU, S.C. 1970b. The Indo-Australian Species of Xanthopimpla<br />

(Ichneumonidae). Memoirs of the American Entomological Instititue 14: 193–194.<br />

TOWNES, H., TOWNES, M. & GUPTA, V.K. 1961. A Catalogue and Reclassification of the<br />

Indo-Australian Ichneumoidae. Memoirs of the American Entomological Instititue 1:<br />

1–522.<br />

VAN ACHTERBERG, C. 1996. Illustrated Key to Subfamilies Braconidae (Hymenoptera:<br />

Ichneumonoidea). Zoologische Verhandelingen. The National Natuurhistorisch Museum,<br />

Leiden.<br />

VAN ACHTERBERG, C. 1983. Revision notes on the genera Dapsilarthra Aut. And Mesocrine<br />

Foester (Hymenoptera, Braconidae, Alysinae). Tijdschrift Voor Entomologie 126(1-2):<br />

1–24.<br />

VAN ACHTERBERG, C. 1988. Revision of the subfamily Blacinae Foster (Hymenoptera,<br />

Braconidae). Zoologische Verhandelingen 249: 1–324.<br />

VAN ACHTERBERG, C. 1997. Revision of the Haliday collection of Braconidae<br />

(Hymenoptera). Zoologische Verhandelingen 314: 1–115.<br />

VAN DER VECHT, C.H. & SHENEFELT, R.D. 1969. Hymenoptera Catalogus: Braconidae<br />

1. Uitgeverij, Netherland.<br />

WAHL, D.B. & SHARKEY, J.S. 1993. Superfamily Ichneumonoidea. Pp 358–449 in Goulet,<br />

H. & Huber, J.T. (eds.). Hymenoptera of the World: An Identification Guide to Families.<br />

Research Branch, Agriculture Canada, Publication 194/E.<br />

WAHL, D.B. 1993. Family Ichneumonidae. Pp. 395–442 in Goulet, H. & Huber, J.T. (eds.).<br />

Hymenoptera of the World: An Identification Guide to the Families. Canada<br />

Communication Group Publishing, Canada.<br />

WIDODO, E.S., MARYATI, M. & HASHIMOTO, Y. 2001. Canopy and diversity assessment<br />

in the fragmented rainforest of Sabah, East Malaysia. Nature and Human Activities 6:<br />

13–23.<br />

YAMANE, S.K., ITINO, T. & ABD. RAHMAN, N. 1996. Ground ant fauna in a Bornean<br />

Dipterocarp Forest. The Raffles Bulletin of Zoology 44(1): 253–262.<br />

YU, D.S. & HORSTMANN, K. 1997a. A Catalogue of World Ichneumonidae (Hymenoptera).<br />

Mem. Am. Entomol. Inst. 58 (Part 1): 1–790.<br />

YU, D.S. & HORSTMANN, K. 1997b. A Catalogue of World Ichneumonidae (Hymenoptera).<br />

Mem. Am. Entomol. Inst. 58 (Part 2): 791–876.<br />

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1. Pisolithus aurantioscabrosus (Pisolithaceae). Photo courtesy Lee S.S.<br />

2. Cantharellus sp. (Cantharellaceae). Photo courtesy Lee S.S.<br />

3. Panus giganteus (Polyporaceae). Photo courtesy Lee S.S.<br />

4. Amanita tjibodensis (Amanitaceae). Photo courtesy Lee S.S.<br />

5. Russula sp. (Russulaceae). Photo courtesy Lee S.S.<br />

6. Thelephora sp. (Thelephoraceae). Photo courtesy Lee S.S.<br />

7. Stereum sp. (Stereaceae). Photo courtesy Lee S.S.<br />

8. Dictyophora indusiata (Phallaceae). Photo courtesy Lee S.S.<br />

9. Canopy of a Malaysian lowland dipterocarp forest. Photo courtesy L.G. Saw<br />

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STATUS OF BIOLOGICAL DIVERSITY IN MALAYSIA &<br />

THREAT ASSESSMENT OF PLANT SPECIES IN MALAYSIA<br />

MACROFUNGAL DIVERSITY IN MALAYSIA<br />

1<br />

Lee Su See & 2, 3 Roy Watling<br />

ABSTRACT<br />

Macrofungi, also known as macromycetes or larger fungi, are fungi, which possess large<br />

(macroscopic) sporocarps or fruiting bodies. Many macrofungi are important as sources of<br />

food and medicine; some are symbionts in ectomycorrhizal associations with trees while others<br />

cause diseases and decay. It is estimated that up to about 70% of the fungi in Malaysia have<br />

yet to be discovered. This paper discusses the status of macrofungal diversity in Malaysia and<br />

shows that the existing figures for the number of species of Malaysian fungi are grossly<br />

underestimated. Much research still needs to be done before a clearer understanding of the<br />

status of macrofungal (and total fungal) diversity in Malaysia can be obtained and the resources<br />

needed for such an undertaking are discussed in the paper.<br />

INTRODUCTION<br />

Malaysia, one of the world’s 12 most biologically diverse countries, is known to possess over<br />

15,000 species of flowering plants, 286 species of mammals, more than 150,000 species of<br />

invertebrates, over 1,000 species of butterflies, 12,000 moth species, and more than 4,000<br />

species of marine fishes (WCMC 1994). Yet amazingly, according to the Assessment of<br />

Biological Diversity in Malaysia (Anonymous 1997), there are only 400 species of fungi in<br />

the peninsula and 300 species in East Malaysia. The report does not mention whether any<br />

species are common to the two regions.<br />

An assessment of all the fungi known to occur in Malaysia would be a monumental and time<br />

consuming task requiring access to numerous libraries and fungal collections around the world.<br />

As the time given for preparation of this paper was rather short, we restrict ourselves to a<br />

discussion of the diversity of only the basidiomycete macrofungi here, which still is a<br />

considerable task.<br />

Macrofungi, also known as macromycetes or larger fungi, are fungi which possess large<br />

(macroscopic) sporocarps or fruiting bodies (Hawksworth et al. 1995) visible to the naked<br />

eye as opposed to the microfungi or micromycetes which possess microscopic sporomes. For<br />

the purpose of this paper Singapore is geographically considered part of Malaysia, thus reports<br />

1<br />

Forest Research Institute Malaysia, Kepong, 52109 Selangor, Malaysia; leess@frim.gov.my<br />

2<br />

Caledonian Mycological Enterprises, 26 Blinkbonny Avenue, Edinburgh EH4 3HU, U.K.<br />

3<br />

Royal Botanic Garden Edinburgh, EH3 5LR, U.K.<br />

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of macrofungi from the former are also included as those being from Malaysia. Many<br />

macrofungi are important as sources of food and medicine, some are symbionts in<br />

ectomycorrhizal associations with trees while others cause diseases and decay.<br />

A recent study of putative ectomycorrhizal fungi in a lowland rain forest at Pasoh, Malaysia<br />

clearly illustrates the large number of tropical fungi yet to be discovered (Lee et al. 2003). Of<br />

the 296 taxa of putative ectomycorrhizal fungi recorded, 66% are undescribed, reflecting the<br />

poor knowledge of macrofungi in the tropics. In another study also conducted at Pasoh, more<br />

than 200 species of polypores were found from a relatively small area of about 4 ha and along<br />

adjacent trails (Hattori & Lee 2003). The authors of this last study estimate that about 300<br />

species of polypores might be expected from this single research site compared to only about<br />

330 species recorded for the whole of Europe where most of the species have already been<br />

listed (Ryvarden & Gilbertson 1993, 1994). These examples are from only a few studies in<br />

Malaysia re-emphasising the late Prof. E.J.H. Corner’s estimate that up to 70% of the fungi in<br />

Malaysia had yet to be discovered. From information obtained through personal communication,<br />

Jones and Hyde (2004) estimated that there are over 2,000 documented fungi in Malaysia. It<br />

would be safe to say that this figure is still an underestimate of the fungal diversity of Malaysia.<br />

LITERATURE REVIEW<br />

The first attempt to list Malayan fungi was made by Bancroft in 1913 (cited in Chipp 1921) in<br />

his “List of fungi identified in the Federated Malay States” in which 105 species were<br />

mentioned. An additional five species were listed by Sharples later that same year (Chipp<br />

1921) and this was followed by a brief but important contribution on 16 boletes five years<br />

later by Patouillard and Baker (1918) (see Watling 2000). Subsequently, a general list of fungi<br />

for the Malay Peninsula was published by Chipp (1921) who, however, did not attempt to<br />

give a total number of species as many synonyms were evident and many of the early<br />

determinations still needed checking. Basidiomycetes make up the bulk of the collections<br />

described by Chipp (1921), with the earliest records being the collections of Beccari between<br />

1865 and 1879 on his way to Sarawak and those of Rev. Father Scortechini in 1885. Other<br />

early collectors included Kunstler but the majority of the collections were the result of work<br />

by Ridley and Mrs. E. Burkill (Chipp 1921). The data contained in these early reports are now<br />

long out of date and the taxonomy considerably changed but there has been no other general<br />

listing of the fungi for the peninsula or Malaysia since. This lack of information was evident<br />

in Lim’s (1972) short illustrated report on the more common macrofungi of Malaysia and<br />

Singapore, where the majority of the fungi were identified to genus level only and where<br />

surprisingly only one of the ten references listed was directly concerned with Malaysian fungi,<br />

despite extensive monographic work in the area.<br />

Unlike other tropical countries, Malaysia and Singapore have been very well served for the<br />

macrofungi as many world monographs have been published centred around the macrofungi<br />

species found in the Malay Peninsula. This has been a result largely of the efforts and<br />

contributions of the late Prof. E.J.H. Corner who undoubtedly was the most prolific and<br />

authoritative mycologist in Malaysia (Watling 2001a). Of his 141 publications produced<br />

between 1929 until his death in 1996 (Watling 2001a), 97 concerned mycological topics,<br />

nearly all of them dealing with the macrofungi. His monographic treatments of the Boletaceae,<br />

Cantharellaceae, Clavariaceae, Thelephoraceae, Tricholomataceae and Polyporaceae are used<br />

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LEE SU SEE & ROY WATLING (2007)<br />

worldwide and are highly significant contributions to the fungal flora of Malaysia. In 15<br />

monographs covering just eight basidiomycete groupings, Corner described 621 new taxa of<br />

Malaysian fungi (Table 1). These new discoveries mainly resulted from his collecting trips to<br />

selected locations in the forests of Singapore, parts of Johor, Negeri Sembilan, Pahang and<br />

Mt. Kinabalu in Sabah. No doubt many more new taxa would have been discovered had the<br />

collecting trips been extended to more areas in each location and to other locations in the<br />

country. Considering that macrofungi are found in over 140 families in the basidiomycetes<br />

(and this excludes the many larger Ascomycota), it is quite awe-inspiring to imagine the numbers<br />

of new taxa that await discovery.<br />

In addition to the monumental work of Corner, there are various publications on the macrofungal<br />

diversity of specific localities in Malaysia, such as Pulau Langkawi (Kuthubutheen 1981), the<br />

grounds of the Forest Research Institute Malaysia (FRIM), Kepong (Watling & Lee 1995,<br />

1998), Sabah (Pegler 1997), selected forest reserves in Peninsular Malaysia (Lee et al. 1995,<br />

Watling & Lee 1999, Salmiah et al. 2002), and Pasoh Forest Reserve, Negeri Sembilan (Hattori<br />

& Lee 2003, Lee et al. 2002, 2003). There are also several publications on ascomycetes from<br />

Malaysia (e.g., Spooner 1991, Whalley 1993, Whalley et al. 1996, 1999) but these are not<br />

considered in the present paper.<br />

Table 1. New taxa of Malaysian macrofungi described in selected monographs of the late<br />

Prof. E.J.H. Corner<br />

Fungus Group No. new taxa Reference(s)<br />

Amanita 30 Corner & Bas (1962)<br />

Boletes 105 Corner (1972)<br />

Cantharelloid fungi 24 Corner (1966)<br />

Clavarioid fungi 9 Corner (1970)<br />

Pleurotoid polypores 15 Corner (1981)<br />

Polypores 172 Corner (1983, 1984a, 1984b,<br />

1987, 1989a, 1989b, 1991a)<br />

Thelephora and allies 18 Corner (1968)<br />

Tricholomataceous agarics:<br />

Mycenoid and tricholomatoid 103 Corner (1994)<br />

components<br />

Marasmioid components 93 Corner (1996)<br />

Trogia 52 Corner (1991b)<br />

Note: several species have varieties, which are not included here.<br />

A recent study of polypores in East and South-East Asia (Hattori 2004) found that South-East<br />

Asia possesses a rich diversity of polypore fungi, many of which are possibly endemic. South-<br />

East Asia is considered a refugia during the Pleistocene and is the centre of distribution for<br />

several species (Table 2). Of the 208 species of polypore fungi found in Pasoh, Negeri Sembilan<br />

between 1992 and 1999, seven were temperate species, 33 pantropical, 24 paleotropical and<br />

144 found only in South-East Asia showing that many were probably endemic (Hattori 2004).<br />

Data on macrofungal diversity may also be obtained from publications dealing with other<br />

aspects of macrofungi, for example, those dealing with utilization, e.g., Burkill (1966), Sather<br />

(1978), Chin (1981, 1988) and Christensen (2002). However, data from some of the older<br />

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MACROFUNGAL DIVERSITY IN MALAYSIA<br />

Table 2. Polypore fungi whose centre of distribution is considered to be in South-East Asia<br />

Antrodiella aurantilaeta (Corner) T. Hatt. & Ryv.<br />

Antrodiella brunneimontana (Corner) T. Hatt.<br />

Elmerina holophaea Pat.<br />

Elmerina ungulata Corner<br />

Inonotus scaurus (Lloyd) T. Hatt.<br />

Protodaedalea hispida Imazeki<br />

Tyromyces incarnatus Imazeki<br />

Source: Hattori 2004<br />

publications need to be reexamined or re-evaluated and the fungal identifications confirmed<br />

but this may be impossible to carry out in the absence of voucher specimens. Information may<br />

also be obtained from assorted publications on macrofungal taxonomy from Malaysia (e.g.,<br />

Baroni & Watling 1999; Hattori & Lee 1999; Pegler & VanHaecke 1994; Sims et al. 1995;<br />

Watling et al. 1995; Watling & Hollands 1990; Watling 1993a, 1993b, 1994a, 1997; Watling<br />

& Sims 2004; Turnbull 1995; Turnbull & Watling 1999) or South-East Asia (e.g., Jülich<br />

1980, 1982, 1984a, 1984b; Watling 1994b, 1998, 2001b); ecology (e.g., Hong et al. 1984)<br />

and plant pathology (e.g., Hilton 1959, Singh 1973, Lee 1993, Lee & Noraini Sikin 1999).<br />

Although a listing of Malaysian macrofungi may be compiled by going through all the published<br />

literature, the veracity of much of the data cannot be confirmed unless voucher specimens<br />

exist.<br />

SPECIMEN COLLECTIONS<br />

Information on specimen collections of Malaysian fungi is scattered and not easily accessible.<br />

Fungal collections made before 1912 were sent to the Royal Botanic Gardens, Kew (Chipp<br />

1921) with a small amount kept for comparison at the Singapore Botanic Gardens (SING).<br />

Collections made during the British colonial era in Malaya, including those from forestry and<br />

agriculture were also sent to Kew (K) for identification. Collections made by the Rev. M.J.<br />

Berkeley which were originally housed at the British Museum were transferred to Kew in<br />

1979 under the Morton Agreement and material collected from Malaya and Singapore sent to<br />

the well known mycologists G.E. Massee, M.C. Cooke, E.M. Wakefield and R.W.G. Dennis<br />

were all deposited and available for examination at Kew. Some of the material collected on<br />

more recent expeditions to Borneo, e.g., to Mulu, are housed both at the Royal Botanic Garden<br />

Edinburgh (E) and at Kew (see Watling & Hollands 1990). Prof. Corner’s extensive collection<br />

of Malaysian specimens, except those monographed before 1972, are now held in the Edinburgh<br />

Botanic Garden library and herbarium. Other materials are in the Botany School, Cambridge<br />

(CGE), although it is hoped that in the future these specimens will also be transferred to join<br />

the Edinburgh holdings. Some, many in rather poor condition, are held in the Singapore Botanic<br />

Gardens. Presently when time permits Evelyn Turnbull in Edinburgh is gradually databasing<br />

Corner’s collections but this is a slow activity. However, many of the collections so-far<br />

catalogued have been examined and where necessary revised by visiting scientists, e.g., C.<br />

deCock, T. Hattori, U. Koljag, Y. Ota, E. Horak, S. Miller and R. Garcia-Sandoz. Other Corner’s<br />

collections can also be found in the US Department of Agriculture’s collections at Beltsville,<br />

Maryland, U.S.A. (BPI) as demonstrated on its website, whilst many of the collections of W.<br />

Jülich would most probably be deposited at the Rijksherbarium, Leiden, Netherlands (L).<br />

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LEE SU SEE & ROY WATLING (2007)<br />

Some collections of specific groups are also housed in Zurich, Switzerland (ZT) and Innsbruck,<br />

Austria resulting from collections made by Swiss and Austrian mycologists who visited<br />

Malaysia and South-East Asia in the 1970s and 1980s and exchange of specimens with Corner.<br />

None of these materials is supported by voucher cultures. Recent collections made by R.<br />

Watling & E. Turnbull of the Royal Botanic Garden Edinburgh under the auspices of<br />

collaborative projects with FRIM and featured in their papers noted above are deposited in the<br />

Edinburgh herbarium.<br />

Several institutions in Malaysia maintain culture collections of macrofungi for research,<br />

teaching and commercial purposes. Apart from those at FRIM, most of the cultures are of<br />

non-indigenous species, comprising macrofungi cultivated in the country for food or medicinal<br />

purposes and whose original sources are largely undetermined (Tan & Lee 1999). However,<br />

specimen collections of macrofungi are rarer. Some universities such as Universiti Malaya<br />

(UM), Universiti Putra Malaysia (UPM) and Universiti Malaysia Sarawak (UNIMAS), hold<br />

some macrofungal collections, but information on the status and condition of the collections<br />

is not available. FRIM has a small collection of macrofungal specimens, mainly focused on<br />

the ectomycorrhizal and wood-inhabiting taxa. In order to obtain up-to-date information on<br />

the fungi of Malaysia, a survey of fungal collections, both of cultures and herbarium specimens<br />

held by both local and overseas institutions, needs to be carried out.<br />

Early drawings of Malaysian macrofungi collected in Singapore made by C. de Alwis and<br />

Mrs. Burkill have been transferred from Edinburgh, where they formed part of the Corner<br />

bequest, to Singapore while Corner’s field notes, commentaries and keys, line-drawings and<br />

numerous water colours accompany his material in Edinburgh.<br />

SPECIALISTS/RESEARCHERS<br />

In the early 1900s, specific scientists were assigned to study or specialize in particular fungal<br />

groups, for example, ascomycetes were under the purview of C.F. Baker who was a staff<br />

member of the Singapore Botanic Gardens in 1917, while the myxomycetes were the specialty<br />

of A.R. Sanderson (Chipp 1921). Corner’s brief when he was appointed Assistant Director in<br />

Singapore included overseeing mycology and this led to him becoming involved in the study<br />

of butt-rot fungi of rubber, which in its turn led to the development of the mitic hyphal system<br />

for the classification of polypores. This tradition of specialization was upheld until very recently<br />

in most institutions dealing with fungal taxonomy, e.g., the International Mycological Institute<br />

in the U.K., the Rijksherbarium, Leiden, but unfortunately this practice ceased in the 1990s<br />

due to budget constraints. Several British experts well versed with the Malaysian mycota such<br />

as D.N. Pegler and R. Watling have retired and as a result of changing priorities in parallel<br />

with many countries in the western world, have not been replaced. However, there is hope yet<br />

in Japan and China where there are several young mycologists including fungal taxonomists<br />

who are interested in tropical fungal diversity. There has also been an upsurge of interest in<br />

the study of mycodiversity in neighbouring Thailand where many young researchers are being<br />

trained both locally and abroad in mycology and fungal taxonomy. Locally, researchers who<br />

work with Malaysian macrofungi are usually not trained as mycologists or taxonomists, their<br />

knowledge of macrofungal taxonomy being acquired through personal interest or necessity<br />

while working on plant pathology or other disciplines involving fungi. As in the west, mycology<br />

and fungal taxonomy are given little attention if any, in local university curricula as attention<br />

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is focused more on the more glamorous and current topics of biotechnology and applied<br />

microbiology. The reasons for this are best discussed at another forum. There is a need to<br />

identify local researchers who are able to contribute the expertise needed to fully evaluate the<br />

fungal diversity of Malaysia.<br />

Public appreciation of the fungi and their diversity needs to be encouraged through the<br />

organisation of interesting educational talks and regular fungal forays but the lack of sufficient<br />

experienced and knowledgeable leaders is a major stumbling block. One way to overcome<br />

this lack of expertise would be to invite some of the retired, experienced mycologists to conduct<br />

hands-on training courses and workshops on fungal taxonomy for local students, scientists<br />

and researchers. These experts could also be appointed visiting/honorary lecturers or professors<br />

at local universities to help strengthen the teaching of mycology and taxonomy as well as to<br />

assist in the supervision of student projects. Such experts could also be invited to participate<br />

in expeditions and other interdisciplinary projects where a fungal component exists, thereby<br />

in the process contributing to the evaluation and enumeration of our fungal diversity.<br />

RELATED PROJECTS<br />

At FRIM and other local educational and research institutions, various studies concerning<br />

macrofungi are being carried out, e.g., projects on selected plant pathogens, fungi utilized for<br />

food, medicine and industrial purposes, and those involved in ectomycorrhizal associations.<br />

However, there are few projects aimed directly at evaluating the macrofungal diversity of the<br />

country. One post-graduate project currently being undertaken at a local university aims to<br />

evaluate the biodiversity of polypore fungi using both classical and molecular techniques for<br />

ex-situ germplasm conservation and cultivation. A collaborative project between Universiti<br />

Sains Malaysia and some Japanese researchers has been underway for the last two years in the<br />

north of the country but details are sketchy. Between 1992 and 1998, FRIM collaborated with<br />

mycologists from the U.K. and Japan on the macrofungi of Pasoh Forest Reserve, Negeri<br />

Sembilan and this has resulted in the publication of several research papers, the discovery of<br />

many undescribed fungi of which some have already been published as new (Watling et al.<br />

1995; Hattori & Lee 1999). Many of the collections made during the duration of these two<br />

projects still await further study and it is likely that several more new species, particularly in<br />

the Russulaceae and hypogeous fungi will be described when the taxonomists find the time to<br />

work on the collections. It is only through the joint efforts of such collaborative projects and<br />

with the help of foreign experts that we can hope to have a better understanding of our<br />

macrofungal diversity.<br />

In the U.K. the British Mycological Society has been at the forefront of British mycology and<br />

its members have actively played a role in the enumeration of the British fungal flora. There is<br />

no equivalent organization in Malaysia but non-governmental organisations such as the<br />

Malaysian Nature Society (MNS), Worldwide Fund for Nature (WWF) and other organisations<br />

involved in nature conservation and education could assist in the evaluation of the Malaysian<br />

macrofungal diversity if such a project were to be implemented. Many members of the MNS<br />

are keen and expert nature photographers and have submitted photos of assorted fungi for<br />

identification. With a little education, interested members could be trained to properly collect<br />

and document the details of the fungi for further identification by the experts. This is where<br />

the stumbling block lies—there is a dearth of local expertise in the identification of the<br />

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macrofungi. Some of the measures mentioned in the previous section could hopefully be<br />

implemented to overcome this problem.<br />

RESOURCES REQUIRED<br />

Information on macrofungal diversity in Malaysia is still far from satisfactory. As a first step,<br />

a thorough review of the literature on the topic needs to be conducted together with an<br />

assessment of the collections available not only in Malaysia but worldwide. This requires<br />

time, manpower and funding. Secondly, manpower and funding are needed for field visits to<br />

collect macrofungi from various locations and habitats throughout the country. This is a daunting<br />

and time consuming task as the collecting trips should coincide with the fungal fruiting seasons<br />

of the various locations. To ensure a proper representation of the flora of a particular area,<br />

collections need to be made over a continuous period of several years. Suitably trained<br />

manpower is needed not only to make the collections but also to describe and identify them.<br />

For the short-term, this could best be achieved either by inviting foreign experts to lead such<br />

collecting trips whilst providing on-the-job training to young, local researchers who could<br />

then continue the work later on, or by suitable candidates training with a mentor in Europe or<br />

North America, and in the case of Edinburgh, working with Corner’s collections as the senior<br />

author and Tham Foong Yee from Singapore have been able to do. More importantly,<br />

researchers who have been trained in fungal taxonomy and inventory should continue to work<br />

in those fields and not be assigned to other projects so as not to lose the impetus gained from<br />

that training. Dedicated positions or time available in a particular job for macrofungal taxonomy<br />

must be assured. Otherwise, the benefits from the training would not be realized and no further<br />

progress would be made in macrofungal taxonomy. Facilities to store the specimens, such as<br />

proper storage cabinets and a herbarium are also needed, as are suitably trained curators for<br />

the collections. Molecular techniques are now routinely used for fungal identification; therefore<br />

equipment for such methods should also be available.<br />

CONCLUSION<br />

An up-to-date and accurate listing of the macrofungal diversity of Malaysia is a huge challenge<br />

that requires time, manpower, funding and expertise, not all of which are in place at the moment.<br />

Given the proper resources, dedication and commitment, it can be achieved, thereby not only<br />

providing us with a knowledge of our rich natural heritage but also open the doors for<br />

exploration and sustainable utilisation of our natural wealth for the welfare and benefit of<br />

humankind.<br />

REFERENCES<br />

ANONYMOUS. 1997. Malaysia: Country Study on Biological Diversity. Assessment of<br />

Biological Diversity in Malaysia. Ministry of Science, Technology and the Environment,<br />

Malaysia. 186 pp.<br />

BARONI, T. & WATLING, R. 1999. Taxonomic and mycogeographic notes on some Malaysian<br />

fungi IV. Notes on Clitopilus and Rhodocybe. Mycotaxon LXXII: 57–72.<br />

175


MACROFUNGAL DIVERSITY IN MALAYSIA<br />

BURKILL, I.H. 1966. A Dictionary of the Economic Products of the Malay Peninsula. Vol. 1<br />

& II. Ministry of Agriculture and Cooperatives, Kuala Lumpur, Malaysia. 2443 pp.<br />

CHIN, F.H. 1981. Edible and poisonous fungi from the forests of Sarawak. Part 1. The Sarawak<br />

Museum Journal 29: 211–225.<br />

CHIN, F.H. 1988. Edible and poisonous fungi from the forests of Sarawak. Part II. The Sarawak<br />

Museum Journal 60 (New Series): 195–201.<br />

CHIPP, T.F. 1921. A list of the fungi of the Malay Peninsula. The Gardens’ Bulletin, Straits<br />

Settlements II (9, 10, 11): 311–418.<br />

CHRISTENSEN, H. 2002. Ethnobotany of the Iban and Kelabit. A joint publication of the<br />

Forest Department Sarawak; NEPCon, Denmark; and University of Aarhus, Denmark.<br />

384 pp.<br />

CORNER, E.J.H. & BAS, C. 1962. The genus Amanita in Singapore and Malaya. Persoonia<br />

2: 241–304.<br />

CORNER, E.J.H. 1966. A Monograph of Cantharelloid Fungi. Oxford University Press.<br />

255 pp.<br />

CORNER, E.J.H. 1968. A monograph of Thelephora (Basidiomycetes). Beih. Nova Hedwigia<br />

27: 1–110.<br />

CORNER, E.J.H. 1970. Supplement to “A monograph of Clavaria and allied genera”. Beih.<br />

Nova Hedwigia 33: 1–299.<br />

CORNER, E.J.H. 1972. Boletus in Malaysia. Government Printing Office, Singapore.<br />

263 pp.<br />

CORNER, E.J.H. 1981. The agaric genera Lentinus, Panus and Pleurotus with particular<br />

reference to Malaysian species. Beih. Nova Hedwigia 69: 1–169.<br />

CORNER, E.J.H. 1983. Ad Polyporaceas I. Amauroderma and Ganoderma. Beih. Nova<br />

Hedwigia 75: 1–182.<br />

CORNER, E.J.H. 1984a. Ad Polyporaceas II. Polyporus, Mycobonia and Echinochaete. Beih.<br />

Nova Hedwigia 78: 1–129.<br />

CORNER, E.J.H. 1984b. Ad Polyporaceas III. Piptoporus, Buglossoporus, Laetiporus,<br />

Meripilus and Bondarzewia. Beih. Nova Hedwigia 78: 133–222.<br />

CORNER, E.J.H. 1987. Ad Polyporaceas IV. The genera Daedalea, Flavodon, Gloeophyllum,<br />

Heteroporus, Irpex, Lenzites, Microporellus, Nigrofomes, Nigroporus, Oxyporus,<br />

Paratrichaptum, Rigidoporus, Scenidium, Trichaptum, Vandebylia and Steccherinum. Beih.<br />

Nova Hedwigia 86: 1–265.<br />

CORNER, E.J.H. 1989a. Ad Polyporaceas V. The genera Albatrellus, Boletopsis, Coriolopsis<br />

(dimitic), Cristelloporia, Diacanthodes, Elmeria, Fomitopsis (dimitic), Gloeosporus,<br />

Grifola, Hapalopilus, Heterobasidion, Hydnopolyporus, Ischnoderma, Loweporus,<br />

Parmastomyces, Perenniporia, Pyrofomes, Stecchericium, Trechispora, Truncospora and<br />

Tyromyces. Beih. Nova Hedwigia 96: 1–218.<br />

CORNER, E.J.H. 1989b. Ad Polyporaceas VI. The genus Trametes. Beih. Nova Hedwigia 97:<br />

1–197.<br />

CORNER, E.J.H. 1991a. Ad Polyporaceas VII. The Xanthochroic Polypores. Beih. Nova<br />

Hedwigia 101: 1–175.<br />

CORNER, E.J.H. 1991b. Trogia (Basidiomycetes). Gardens’ Bulletin Singapore, Supplement<br />

2: 1–97.<br />

CORNER, E.J.H. 1994. Agarics in Malesia: I Tricholomatoid, II Mycenoid. Beih. Nova<br />

Hedwigia 109: 1–271.<br />

CORNER, E.J.H. 1996. The Agaric genera Marasmius, Chaetocalathus, Crinipellis,<br />

Heimiomyces, Resupinatus, Xerula and Xerulina in Malesia. Beih. Nova Hedwigia 111:<br />

1–175.<br />

176


LEE SU SEE & ROY WATLING (2007)<br />

HAWKSWORTH, G.C., KIRK, P.M., SUTTON, B.C. & PEGLER, D.N. 1995. Ainsworth &<br />

Bisby’s Dictionary of the Fungi. 8 th edition. CAB International, Wallingford, U.K.<br />

616 pp.<br />

HATTORI, T., & LEE, S.S. 1999. Two new species of Perenniporia described from a lowland<br />

rainforest of Malaysia. Mycologia 91(3): 525–531.<br />

HATTORI, T. & LEE, S.S. 2003. Community structure of wood-decaying basidiomycetes in<br />

Pasoh. Pp. 161–170 in Okuda, T., Manokaran, N., Matsumoto, Y., Niiyama K., Thomas<br />

S.C. & Ashton P.S. (eds.) Pasoh. Ecology of a Lowland Rain Forest in Southeast Asia.<br />

Springer, Tokyo.<br />

HATTORI, T. 2004. Diversity and distribution patterns of East and Southeast Asian polypores.<br />

Paper presented at the IV Asia-Pacific Mycological Congress, 14–19 November 2004,<br />

Chiangmai, Thailand.<br />

HILTON, R.N. 1959. Maladies of Hevea in Malaya. Rubber Research Institute, Malaya.<br />

101 pp.<br />

HONG, L.T., THILLAINATHAN, P. & ARSHAD, O. 1984. Observations on the fruiting and<br />

growth of some agarics in a dipterocarp stand. Malayan Nature Journal 38: 81–88.<br />

JONES, E.B.G. & HYDE, K.D. 2004 Introduction to Thai fungal diversity. Pp. 7–35 in Jones,<br />

E.B.G., Tanticharoen, M. & Hyde, K.D. (eds.) Thai Fungal Diversity. National Center for<br />

Genetic Engineering and Biotechnology (BIOTEC), Thailand.<br />

JÜLICH, W. 1980. (3) Basidiomycetes: Phanerochaete Karst. In: Jermy, A.C. (ed.) Notulae et<br />

novitiates Muluenses. Bot. J. Linn. Soc. 81: 43–46.<br />

JÜLICH, W. 1982. Basidiomycetes of South-East Asia. 1. The genus Paraphelaria<br />

(Auriculariales). Persoonia 11(4): 397–406.<br />

JÜLICH, W. 1984a. Basidiomycetes of South-East Asia. 2. on Scenedium apiarum, with a<br />

discussion of the nomenclatural status of the genus Hexagonia Pollini (Hexagona Fr.).<br />

Persoonia 12(2): 107–117.<br />

JÜLICH, W. 1984b. Basidiomycetes of South-East Asia. 3. On Flabellophora Cunn., the<br />

pancake fungus. Int. J. Myc. Lich. 1(3): 319–325.<br />

KUTHUBUTHEEN, A.J. 1981. Notes on the macrofungi of Langkawi. The Malayan Nature<br />

Journal 34(3): 123–130.<br />

LEE, S.S. 1993. Diseases. Pp. 203–223 in Awang, K. & Taylor, D. (eds.) Acacia mangium<br />

Growing and Utilization. MPTS Monograph Series No. 3. Bangkok, Thailand: Winrock<br />

International and FAO.<br />

LEE, S.S. & NORAINI SIKIN, Y. 1999. Fungi associated with heart rot of Acacia mangium<br />

trees in Peninsular Malaysia and East Kalimantan. Journal of Tropical Forest Science 11:<br />

240–254.<br />

LEE, S.S., BESL, H. & SALMIAH, U. 1995. Some fungi of the Sungai Halong and surrounding<br />

areas, Temengor Forest Reserve, Hulu Perak, Malaysia. Malayan Nature Journal 48:<br />

147–155.<br />

LEE, S.S., WATLING, R. & NORAINI SIKIN, Y. 2002. Ectomycorrhizal basidiomata fruiting<br />

in lowland rain forests of Peninsular Malaysia. Bois et Forêts des Tropiques 274(4):<br />

33–43.<br />

LEE, S.S., WATLING, R. & TURNBULL, E. 2003. Diversity of putative ectomycorrhizal<br />

fungi in Pasoh Forest Reserve. Pp. 149–159 in Okuda, T., Manokaran, N., Matsumoto,<br />

Y., Niiyama, K., Thomas, S.C. & Ashton, P.S. (eds.) Pasoh. Ecology of a Lowland Rain<br />

Forest in Southeast Asia. Springer, Tokyo.<br />

LIM, G. 1972. Some common large fungi in Malaysia and Singapore. The Malayan Nature<br />

Journal 25: 84–89.<br />

177


MACROFUNGAL DIVERSITY IN MALAYSIA<br />

PATOUILLARD, N. & BAKER, C.F. 1918. Some Singapore Boletinae. Journal of the Straits<br />

Branch of the Royal Asiatic Society 78: 67–72.<br />

PEGLER, D.N. 1997. The Larger Fungi of Borneo. Natural History Publications, Kota<br />

Kinabalu. 95 pp.<br />

PEGLER, D.N. & VANHAECKE, M. 1994. Termitomyces of Southeast Asia. Kew Bulletin<br />

49(4): 717–736.<br />

RYVARDEN, L. & GILBERTSON, R.L. 1993. European Polypores Part 1: 1–393. Fungiflora,<br />

Oslo.<br />

RYVARDEN, L. & GILBERTSON, R.L. 1994. European Polypores Part 2: 394–743.<br />

Fungiflora, Oslo.<br />

SALMIAH, U., JONES, E.B.G. & WATLING, R. 2002. The distribution of wood-inhabiting<br />

fungi in Peninsular Malaysia. Journal of Tropical Forest Science 14(4): 433–440.<br />

SATHER, C. 1978. Iban folk mycology. The Sarawak Museum Journal 47: 81–102.<br />

SIMS, K., WATLING, R. & JEFFRIES, P. 1995. A revised key to the genus Scleroderma.<br />

Mycotaxon LVI: 4.3–420.<br />

SINGH, K.G. 1973. A Check-list of Host and Diseases in Peninsular Malaysia. Bulletin No.<br />

132. Ministry of Agriculture and Fisheries Malaysia. Kuala Lumpur.189 pp.<br />

SPOONER, B.M. 1991. Lophodermium and Hypoderma from Mt. Kinabalu, Sabah, Kew<br />

Bulletin 46: 73–100<br />

TAN, Y.H. & LEE, S.S. 1999. Mushroom genetic resources in Malaysia. Pp. 28–37 in<br />

Broderick, A. & Nair, T. (eds.) Proceedings Mushroom Biology and Mushroom Products,<br />

Vol. II. Sydney, Australia.<br />

TURNBULL, E. 1995. Inocybe in Peninsular Malaysia. Edinburgh Journal of Botany. 52(3):<br />

351–359.<br />

TURNBULL, E. & WATLING, R. 1999. Taxonomic and floristic notes on Malaysian larger<br />

fungi III. Malayan Nature Journal 53 (3): 189–200.<br />

WATLING, R. 1993a. A remarkable bolete: validation of Boletus peltatus. Edinburgh Journal<br />

of Botany 50(2): 237–240.<br />

WATLING, R. 1993b. Observations on Malaysian Bolbitiaceae with records from Solomon<br />

Islands. Gardens Bulletin, Singapore 45(2): 359–381.<br />

WATLING, R. 1994a. Taxonomic and floristic notes on some Malaysian larger fungi–1.<br />

Malayan Nature Journal 48: 67–78.<br />

WATLING, R. 1994b. Ectomycorrhizal fungi in the Paleotropics. Mycologia Helvetica 2:<br />

129–138.<br />

WATLING, R. 1997. Tricholosporum superbum: a new Malesian agaric. Bolletino del Gruppo<br />

Micologico G. Bresadola – Nuova Serie BGMB 40(2-3): 485–490.<br />

WATLING, R. 1998. Heinemannomyces: a new lazuline-spored agaric genus from South<br />

East Asia. Belgian Journal of Botany 131(2): 133–138.<br />

WATLING, R. 2000. Bresadola, Cesati and Patouillard’s old world Boletes. Pp. 577–590 in<br />

Papetti, C. (ed.) Micologia Duemila. Associazione Micologica Bresadola, Trento, Italy.<br />

WATLING, R. 2001a. John Corner’s contribution to tropical mycology. Pp. 33–40 in L.G.<br />

Saw, L.S.L. Chua & K.C. Khoo (eds.) Taxonomy: the Cornerstone of Biodiversity.<br />

Proceedings of the Fourth International Flora Malesiana Symposium 1998. Forest Research<br />

Institute Malaysia, Kepong.<br />

WATLING, R. 2001b. The relationships and possible distributional patterns of boletes in<br />

south-east Asia. Mycological Research 105(12): 1440–1448.<br />

WATLING, R. & HOLLANDS, R. 1990. Boletus from Sarawak. Notes from the Royal Botanic<br />

Garden Edinburgh 46: 405–422.<br />

178


LEE SU SEE & ROY WATLING (2007)<br />

WATLING, R. & LEE, S.S. 1995. Ectomycorrhizal fungi associated with members of the<br />

Dipterocarpaceae in Peninsular Malaysia–I. Journal of Tropical Forest Science 7(4): 657–<br />

669.<br />

WATLING, R. & LEE, S.S. 1998. Ectomycorrhizal fungi associated with members of the<br />

Dipterocarpaceae in Peninsular Malaysia–II. Journal of Tropical Forest Science 10(4):<br />

421–430.<br />

WATLING, R. & LEE, S.S. 1999. Some larger fungi of Semangkok Forest Reserve, Selangor.<br />

Malayan Nature Journal 53(4): 315–322.<br />

WATLING, R. & SIMS, K. 2004. Taxonomic and floristic notes on some larger Malaysian<br />

fungi. IV Scleroderma. Pp. 93–96 in Cripps, C. (ed.) Fungi in Forest Ecosystems:<br />

Systematics, Diversity & Ecology. New York Botanic Garden, New York.<br />

WATLING, R., TAYLOR, A., LEE, S.S., SIMS, K. & ALEXANDER, I. 1995. A rainforest<br />

Pisolithus; its taxonomy and ecology. Nova Hedwigia 61 (3-4): 417–429.<br />

WHALLEY, A.J.S. 1993. Tropical Xylariaceae; their distribution and ecological situation. Pp<br />

113–119 in Isaac, S., Frankland, J., Watling, R. & Whalley, A.J.S. (eds.) Aspects of Tropical<br />

Mycology, Cambridge.<br />

WHALLEY, M., WHALLEY, A.J.S., THIENHIRUN, S. & SIHANONTH, P. 1999. Camillea<br />

malaysianensis sp. nov. and the distribution in SE Asia. Kew Bulletin 54: 715–722.<br />

WHALLEY, M., WHALLEY, A.J.S. & JONES, E.B.G. 1996. Camillea selangorensis sp.<br />

nov. from Malaysia. Sydowia 48: 145–151.<br />

WORLD CONSERVATION MONITORING CENTRe (WCMC) (1994) Species database.<br />

Downloaded from info@WCMC.org.uk<br />

179


SITI AISYAH ALIAS (2007)<br />

STATUS OF BIOLOGICAL DIVERSITY IN MALAYSIA &<br />

THREAT ASSESSMENT OF PLANT SPECIES IN MALAYSIA<br />

A CHECKLIST OF MANGLICOLOUS<br />

MARINE FUNGI FROM MALAYSIA<br />

Siti Aisyah Alias<br />

ABSTRACT<br />

Mangrove forests occur in muddy shores, lagoons and estuaries of tidal rivers and provide a<br />

very unique habitat to many organisms including manglicolous marine fungi. Submerged<br />

parts of aerial roots, pneumatophores, subterranean roots, rhizomes, overhanging branches<br />

and twigs of mangrove trees and driftwood are the most common niches for marine fungi. The<br />

number of higher marine fungi species recorded from the mangrove areas has increased in<br />

recent years. Studies revealed that mangrove fungi are the second largest group among the<br />

marine fungi. A checklist of Malaysian higher marine fungi from the mangrove ecosystem is<br />

presented in this paper. The total number of fungi species recorded in Malaysia is 302 of<br />

which 234 species are identified and 68 species unidentified. The total number of species<br />

recorded in Malaysia is relatively high when compared to the total number of species recorded<br />

worldwide (444 species). The Ascomycota was the largest group encountered (275 species),<br />

followed by Deuteromycota (23 species) and Basidiomycota (2 species). The most commonly<br />

occurring species were Lignincola leaves (17.87%), followed by Verruculina enalia (13.92%),<br />

Trichocladium achrasporum (12.88%), Savoryella lignincola (12.35%), Dictyosporum<br />

pelagicum (11.86%), Lulworthia grandispora (11.53%), Halocyphina villosa (11.55%),<br />

Periconia prolifica (10.10%), Leptosphaeria australiensis (9.32%), Halosarpheia marina<br />

(8.93%), Halosarpheia retorquens (8.22%), Lignincola longirostris (8.16%), Halosarpheia<br />

ratnagierensis (7.40%), Kallicroma tethys (7.30%), Dactylospora heliotrepha (5.81%),<br />

Trichocladium alopallonellum (5.73%), Trichocladium linderi (5.40%), Cirrenalia pygmea<br />

(5.38%), Savoryella paucispora (5.36%) and Marinosphaeria sp. (5.07%). Percentage<br />

colonization was 84.8% and the average number of fungi per sample was 2.93.<br />

Institute of Biological Sciences, University Malaya, 50603 Kuala Lumpur. Tel: 03–7967 4387, Fax: 03–7967 4178;<br />

siti_aisyah_2000@yahoo.com<br />

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SEAWEED DIVERSITY IN MALAYSIA<br />

1. Halymenia sp. (Rhodophyta). Photo courtesy S.M. Phang.<br />

2. A mixture of Phaeophyta. Photo courtesy S.M. Phang.<br />

3. Arytera littoralis (Sapindaceae). Photo courtesy L.G. Saw.<br />

4. Etlingera elatior (Zingiberaceae). Photo courtesy L.G. Saw.<br />

5. Nepenthes rajah (Nepenthaceae). Photo courtesy L.G. Saw.<br />

6. Pinanga disticha (Palmae). Photo courtesy L.G. Saw.<br />

7. Etlingera metriocheilos (Zingiberaceae). Photo courtesy L.G. Saw.<br />

8. Rafflesia cantleyi (Rafflesiaceae). Photo courtesy L.G. Saw.<br />

9. Alpinia malaccensis (Zingiberaceae). Photo courtesy L.G. Saw.<br />

184


PHANG et al (2007)<br />

STATUS OF BIOLOGICAL DIVERSITY IN MALAYSIA &<br />

THREAT ASSESSMENT OF PLANT SPECIES IN MALAYSIA<br />

SEAWEED DIVERSITY IN MALAYSIA<br />

S. M. Phang, C. L. Wong, P. E. Lim, J. L. S. Ooi, S. Y. Gan, Melor Ismail,<br />

H. Y. Yeong & Emienour Muzalina Mustafa<br />

ABSTRACT<br />

Malaysia has an extensive coastline totaling 3432 km with 418,000 km 2 of continental shelf.<br />

Numerous islands form clusters along the coastlines. Rocky shores and sandy bays alternate<br />

with mudflats, while coral reefs fringe most islands. All these harbour niches for the variety of<br />

seaweed species found in Malaysian waters. The first checklist of the marine benthic algae in<br />

Malaysia was published in 1991 by Phang and Wee, together with a historical account of<br />

phycological research in this region. In 1998 Phang updated the checklist, including the first<br />

Malaysian new species (Sargassum stolonifolium Phang et Yoshida) published in the ‘Seaweeds<br />

Resources of the World’ by Critchley and Ohno. The present tally includes 386 taxa comprising<br />

Chlorophyta (13 families, 102 taxa), Rhodophyta (27 families, 182 taxa), Phaeophyta (8<br />

families, 85 taxa) and Cyanophyta (8 families, 17 taxa). Many of the seaweeds have potential<br />

for commercialisation based on a variety of products and uses. The seaweed resources have<br />

to be protected against biodiversity losses due to habitat destruction, pollution, over-harvesting<br />

and biopiracy. The inventory of Malaysian seaweeds must continue together with more focused<br />

ecological studies. Biomass assessments of natural seaweed areas, productivity determination<br />

and phenological studies of important species, should be encouraged. Only then can the<br />

status of the seaweed flora of Malaysia be assessed and threatened species and habitats<br />

identified.<br />

INTRODUCTION<br />

Malaysia lies within the Indo-Malay-Philippine archipelago, which is part of the Indo-West<br />

Pacific region. With its extensive coastline totaling 4675 km with 418 000 km 2 of continental<br />

shelf, there exists high marine biodiversity as well as bioproductivity. Of the marine<br />

bioresources, the marine algae find niches in the various marine habitats (Phang, 1998). Algae<br />

are non-flowering photosynthetic organisms ranging from the microscopic phytoplankton to<br />

the macroscopic marine algae or seaweeds. In the present classification system, members of<br />

the Algae Kingdom are separately placed into three different phyla. The prokaryotic bluegreen<br />

algae belong to the Prokaryota; the unicellular eukaryotic algae are placed in the Protista;<br />

while the macroscopic eukaryotic algae are placed in the Plantae. The seaweeds are thus part<br />

of the Plantae and may be grouped into three divisions namely the Chlorophyta (green<br />

Institute of Biological Sciences & University of Malaya Maritime Research Centre, University Malaya, 50603 Kuala<br />

Lumpur, Malaysia; Tel: 03-79674610, Fax: 03-79674699; phang@um.edu.my<br />

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SEAWEED DIVERSITY IN MALAYSIA<br />

seaweeds), Rhodophyta (red seaweeds) and the Phaeophyta (brown seaweeds). In this paper,<br />

the filamentous marine blue green algae (Cyanophyta) will also be considered seaweeds, as<br />

many of these species have both ecological and commercial importance just like the other<br />

seaweeds.<br />

In Malaysia, these tropical seaweeds are subjected to the equatorial climate dominated by<br />

monsoon wind systems, with the Northeast Monsoon blowing between November and March,<br />

while the Southwest Monsoon brings rain from May to September (Phang 1998). Mangrove<br />

swamps dominate the west coast Peninsular Malaysia which is sheltered by Sumatra, Indonesia.<br />

On the east coast, rocky shores of post-Triassic granite are found in the north and Triassic<br />

quartzite and shale towards the south. Sandy and rocky beaches with coral reefs characterise<br />

the coastlines of Sabah and Sarawak. The salinity of Malaysian waters range between 28 and<br />

34 ppt, while surface water temperature range between 27 and 29°C. Semi-diurnal tides occur<br />

on the west coast Peninsular Malaysia, while the east coast has a mixed tidal system. Mixed<br />

tidal regimes occur in Sabah and Sarawak.<br />

SURVEY AND DOCUMENTATION OF SEAWEED<br />

RESOURCES IN MALAYSIA<br />

The early records of seaweeds in the Southeast Asian region were contributed through the<br />

Preussische Expedition nach Ost-Asien (1860–1863) (Martens, 1866) and the Siboga<br />

Expedition (1899 – 1900) (Gepp & Gepp, 1911). Teo & Wee (1983) published the first guide<br />

to the seaweeds of Singapore. Seaweed research in Malaysia started in the 1980’s when Phang<br />

(1984) published the first account of the seaweed resources of Malaysia. Using sources of<br />

information like Burkill’s (1966) ‘A Dictionary of the Economic Products of the Malay<br />

Peninsula’ and publications without verification from deposited specimens, a list of Malaysian<br />

seaweeds and their uses was compiled. In 1991, Phang and Wee published the first checklist<br />

of the marine benthic algae in Malaysia together with a historical account of the study of<br />

marine algae in this region (Phang & Wee 1991). In 1998, Phang updated the checklist of<br />

Malaysian marine algae including additions from Phang (1994a, b, 1995) and a new species<br />

Sargassum stolonifolium described from Penang, west coast Peninsular Malaysia (Phang &<br />

Yoshida 1997). This checklist was published as part of the chapter on the seaweed resources<br />

of Malaysia in the ‘Seaweed Resources of the World’ (Critchley & Ohno 1998). Two hundred<br />

and sixty specific and infraspecific taxa (17 Cyanophyta, 92 Chlorophyta, 94 Rhodophyta<br />

and 57 Phaeophyta) were recorded (Phang 1998). Rhodophyta dominated as is expected of<br />

tropical seaweed flora. As we move towards the tropics, the ratio of red to brown seaweeds<br />

increases (Feldmann 1937). Many of the red algae are filamentous comprising mainly epiphytic<br />

species. These two checklists comprise many species that were reported in literature but were<br />

not verified due to absence of deposited material.<br />

A survey conducted from 1995 to1999 by the University of Malaya in collaboration with<br />

Hokkaido University, Japan, resulted in many additions to the checklist and confirmation of<br />

some taxa, especially of the Rhodophyta. Thirty-eight new records (Kawaguchi et al. 2002,<br />

Masuda et al. 1997, 1999, 2000a, 2000b, 2001a, 2001b, 2002, 2003; Tani & Masuda 2003,<br />

Tani et al. 2003, Terada et al. 2000, Yamagishi et al. 2003), including one new species<br />

Lomentaria gracillima Masuda et Kogame were added to the checklist. Further additions<br />

included taxa previously recorded by Zanardini (1872), 35 species of Rhodophyta, 13 species<br />

186


PHANG et al (2007)<br />

of Phaeophyta and 16 species of Chlorophyta recorded by Ahmad Ismail (1995), Ajisaka<br />

(2002), Ajisaka et al. (1999) and Lim et al. (2001). In 2004, two new records of Gracilaria,<br />

Gracilaria articulata and G. manilaensis (Lim & Phang 2004) and 13 new records of Sargassum<br />

(Wong & Phang 2004), were published. Two expeditions to the northeast Langkawi resulted<br />

in a checklist for Langkawi Islands with 84 taxa identified (Phang et al. 2005). The seaweed<br />

flora of Langkawi is quite distinct from that of Peninsular Malaysia and East Malaysia. At the<br />

species level, the Sorenson’s Coefficient of Similarity (S) between flora of Langkawi and<br />

west coast Peninsula Malaysia is 35.21%, although at the genus level, the S= 66.22%. The<br />

tally of Malaysian marine algae now stands at 388 specific and infraspecific taxa (17 taxa of<br />

Cyanophyta, 102 Chlorophyta, 182 Rhodophyta and 87 Phaeophyta) (Phang 2006). Table 1<br />

gives the checklist of Malaysian marine algae. Most of the specimens are deposited at the<br />

Seaweeds and Seagrasses Herbarium established at the Institute of Biological Sciences, Faculty<br />

of Science, University of Malaya, which presently houses more than 7000 numbers of herbarium<br />

specimens collected from Malaysia, and the Herbarium of the Graduate School of Science,<br />

Hokkaido University, Japan.<br />

Of the marine blue-green algae or Cyanophyta, species of Oscillatoria and Lyngbya dominate<br />

the mudflats while Brachytrichia grow abundantly over intertidal rocks and the sandy seabed.<br />

The Chlorophyta consists of the second highest number of taxa in Malaysian waters. Twelve<br />

species of Caulerpa have been recorded, mainly in coral reefs. Recent collections indicate<br />

that eight of these, namely C. lentillifera, C. peltata, C. racemosa, C. scalpelliformis, C.<br />

serrulata, C. sertulariodes, C. taxifolia and C. verticillata are still commonly found. The<br />

coral reefs are also dominated by species of Halimeda (H. discoidea, H. opuntia, H. tuna), the<br />

erect coralline algae which contribute towards reef building with the calcium carbonate retained<br />

in their cell walls. Several species of Enteromorpha and Ulva are found in the nutrient-rich<br />

shores and mudflats. Enteromorpha intestinalis, E. chlathrata, Ulva lactuca and U. fasciata<br />

are commonly seen covering small rocks, stones, driftwood and sandy patches along beaches.<br />

Many of these species are eaten by the coastal communities of the region.<br />

The red seaweeds or Rhodophyta comprise the highest number of taxa. Species of Halymenia<br />

dominate the subtidal bedrock areas, while Laurencia and Hypnea species inhabit the bedrocks<br />

at the intertidal regions. These grow mainly in the cleaner deep waters. Four species of<br />

Eucheuma and two species of Kappaphycus, sources of carrageenan, have been collected<br />

from lower intertidal to upper sub-tidal areas in Sabah and around islands in Peninsular<br />

Malaysia. Except for the cultivated Kappaphycus, many of the Eucheuma species seem to<br />

have disappeared from Peninsular Malaysia. Twenty-two species of the agarophytic genus<br />

Gracilaria have been reported, many of which inhabit mangroves, sandy-mudflats and rocky<br />

shores. Erect coralline (Amphiroa, Jania) as well as crustose coralline (Lithothamnion,<br />

Peyssonnelia) Rhodophytes are commonly found in the coral reefs especially in the cleaner<br />

deep waters around the islands. In the mangroves small tufted thalli of Bostrychia, Laurencia<br />

microcladia, Caloglossa adnata, Catenella grow commonly with the green filaments of<br />

Chaetomorpha linum and Cladophora. Common epiphytic taxa include Champia parvula,<br />

Centroceras, Ceramium, Spyridia, Polysiphonia, Heterosiphonia, Herposiphonia and<br />

Tolypiocladia glomerulata (Phang 1989). Thirty-eight new records including one new species,<br />

were reported from the Malaysian-Japanese collaboration from 1995.<br />

The brown seaweeds or Phaeophyta contribute high algal biomass (Phang & Maheswary 1989)<br />

on reefs. While Sargassum and Dictyota dominate in terms of species number, Padina are the<br />

most frequently found species. They inhabit a variety of substratum including mangroves,<br />

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Table 1. Checklist of Malaysian Marine Algae<br />

TAXA DISTRIBUTION HABITAT<br />

Division Cyanophyta<br />

Order Chroococcales<br />

Family Microcystaceae<br />

Merismopedia thermalis Kutzing [Syn: Agmenellum thermale (Kutzing) Drouet & Daily] Sn M<br />

Microcystis zanardii (Hauck) P. Silva comb. nov [Syn: Anacystis aeruginosa (Zanardini) Drouet & Daily] Sn R, E<br />

Family Entophysalidaceae<br />

Entophysalis Kutzing Sn Mg<br />

Order Oscillatoriales<br />

Family Nostocaceae<br />

Anabaena licheniformis Bory de Saint-Vincent Sn E<br />

Calothrix C. Agardh E R<br />

Calothrix crustacea Schousboe & Thuret W C<br />

Nostoc commune Vaucher Sn R, P<br />

Family Scytonemataceae<br />

Scytonema hofman-bangii C. Agardh [Scytonema hofmannii C. Agardh nom. illeg.] Sn P<br />

Family Oscillatoriaceae<br />

Lyngbya majuscula (Dillwyn) Harvey W M<br />

Oscillatoria lutea C. Agardh Sn E<br />

Family Phormidiaceae<br />

Pelagothrix clevei J. Schmidt W R<br />

Spirulina subsalsa (Oersted)<br />

Family Schizotrichaceae<br />

Schizothrix arenaria (Berkeley) Gomont Sn E<br />

Schizothrix calcicola (C. Agardh) Gomont Sn S, M<br />

Schizothrix mexicana Gomont Sn R, C, S, M, E<br />

188


Order Stigonematales<br />

Family Mastigocladaceae<br />

Brachytrichia quoyi (C. Agardh) Bornet & Flahault W R, C<br />

Mastigocladus Cohn Sn Mg<br />

Division Chlorophyta<br />

Order Ulvales<br />

Family Ulvaceae<br />

Enteromorpha clathrata (Roth) Greville E, Sn C, R, M, E<br />

Enteromorpha compressa (Linnaeus) Nees W -<br />

Enteromorpha flexuosa (Wulfen) J. Agardh W -<br />

Enteromorpha flexuosa (Wulfen) J. Agardh subsp. flexuosa [Syn: Enteromorpha prolifera (O.F. Muller)<br />

J. Agardh var. tubulosa (Kutzing)] P -<br />

Enteromorpha flexuosa (Wulfen) J. Agardh subsp. flexuosa [Syn: Enteromorpha tubulosa (Kutzing)<br />

Kutzing] Sn R<br />

Enteromorpha flexuosa (Wulfen) J. Agardh subsp. paradoxa (C. Agardh) Blidin Sn S<br />

Enteromorpha intestinalis (Linnaeus) Nees W, E, P R, S<br />

Enteromorpha ovata Thivy & Visalaksmi ex H. Joshi & V. Krishnamurthy Sn W<br />

Ulva beytensis Thivy & Sharma Sn C<br />

Ulva conglobata Kjellman W R<br />

Ulva fasciata Delile E, Sb, Sn E, D, M, S<br />

Ulva lactuca Linnaeus W, Sn D<br />

Ulva latissima Linnaeus P -<br />

Ulva pertusa Kjellman P, Sn D<br />

Ulva reticulata Forsskaal P, W, Sn D<br />

Family Sphaeropleaceae<br />

Sphaeroplea C. Agardh Sn M, S<br />

Order Cladophorales<br />

Family Anadyomenaceae<br />

Anadyomene plicata C. Agardh W, E, Sk R, C, S<br />

Anadyomene stellata (Wulfen) C. Agardh Sb -<br />

189


Family Siphonocladaceae<br />

Boergesenia forbesii (Harvey) J. Feldmann E C, E, R<br />

Boodlea coacta (Dickie) G. Murray & De Toni E S<br />

Boodlea composita (Harvey) Brand [Syn: Cladophora composita Harvey] W, E -<br />

Boodlea montagnei (Harvey ex J. Gray) Egerod [Syn: Microdictyon montagnei Harvey ex J. Gray] W, Sn C, E<br />

Boodlea struveoides Howe E -<br />

Cladophoropsis herpestica (Montagne) Howe W -<br />

Cladophoropsis javanica (Kutzing) P. Silva comb. nov. [Cladophoropsis zollingeri (Kutzing) Reinbold] Sn C<br />

Cladophoropsis membranaceae (Hofman Bang ex C. Agardh) Børgesen E, Sn E, M<br />

Cladophoropsis sundanensis Reinbold W, Sn R<br />

Dictyosphaeria cavernosa (Forsskal) Bøergesen [Syn: Dictyosphaeria favulosa (C. Agardh) Decaisne<br />

ex Endlicher] W, E, Sn C, R<br />

Struvea anastomosans (Harvey) Piccone et Grunow ex Piccone [Syn: Struvea deliculata Kutzing] W, E C, E, R<br />

Struvea ramosa Dickie E C, R<br />

Family Valoniaceae<br />

Valonia aegagropila C. Agardh W, E C, R<br />

Valonia fastigiata Harvey ex J. Agardh W, P R<br />

Valonia utricularis (Roth) C. Agardh W, E C, R<br />

Valoniopsis pachynema (G. Martens) Børgesen W R<br />

Family Cladophoraceae<br />

Chaetomorpha aerea (Dillwyn) Kutzing E -<br />

Chaetomorpha antennina (Bory de Saint-Vincent) Kutzing W R<br />

Chaetomorpha crassa (C. Agardh) Kutzing Sn M<br />

Chaetomorpha gracilis Kutzing Sn M<br />

Chaetomorpha gracilis Kutzing [Syn: Lola gracilis (Kutzing) V. Chapman] Sn Mg<br />

Chaetomorpha linum (O.F. Muller) Kutzing W, E, Sn C, E, M, R, S<br />

Chaetomorpha minima Collins & Hervey W, E E<br />

Chaetomorpha spiralis Okamura W -<br />

Cladophora catenata (Linnaeus) Kutzing E C, E, R<br />

Cladophora coelothrix Kutzing [Syn: Cladophora repens Harvey] E -<br />

Cladophora forsskali (Kutzing) Bornet ex De Toni [Syn: Siphonocladus forsskalii (Kutzing) Bornet<br />

ex De Toni] Sk -<br />

190


Cladophora inserta Dickie forma inserta [Syn: Cladophora inserta Dickie] W S<br />

Cladophora patentiramea (Montagne) Kutzing Sn M<br />

Cladophora prolifera (Roth) Kutzing W S<br />

Cladophora prolifera (Roth) Kutzing [Syn: Cladophora rugolosa G. Martens] W S<br />

Cladophora sericea (Hudson) Kutzing [Syn: Cladophora nitida Kutzing] Sn Mg<br />

Cladophora stimpsonii Harvey E C<br />

Cladophora vagabunda (Linnaeus) van den Hoek E E<br />

Cladophora vagabunda (Linnaeus) van den Hoek [Syn: Cladophora fascicularis (Mertens<br />

ex C. Agardh) Kutzing] W C, R<br />

Cladophora vagabunda (Linnaeus) van den Hoek [Syn: Cladophora mauritiana Kutzing] Sn E<br />

Cladophoropsis javanica (Kutzing) P. Silva, comb. nov. [Rhizoclonium grande Børgesen] W, Sn R<br />

Rhizoclonium hookeri Kutzing [Syn: Rhizoclonium africanum Kutzing] E -<br />

Ventricaria ventricosa (J. Agardh) Olsen & J. West [Valonia ventricosa J. Agardh] E, P C<br />

Order Bryopsidales<br />

Family Bryopsidaceae<br />

Bryopsis corymbosa J. Agardh W, E, Sn C, E, R<br />

Bryopsis hypnoides Lamouroux E F<br />

Bryopsis indica A.Gepp & E. Gepp E, Sn C, E<br />

Bryopsis pennata Lamouroux W, E C, R<br />

Bryopsis pennata Lamouroux var. leprieurii (Kutzing) Collins & Harvey Sn C, R, E<br />

Bryopsis pennata Lamouroux var. secunda (Harvey) Collins & Hervey Sn C, R<br />

Bryopsis plumosa (Hudson) C. Agardh E, Sn C, R<br />

Derbesia fastigiata W. R. Taylor Sn Mg<br />

Derbesia prolifica W. R. Taylor E C<br />

Family Caulerpaceae<br />

Caulerpa fergusonii G. Murray W R<br />

Caulerpa lentillifera J. Agardh W, E, Sb, P, Sn C, D, M, R, S<br />

Caulerpa mexicana Sonder ex Kutzing [Syn: Caulerpa crassifolia (C. Agardh) J. Agardh] P -<br />

Caulerpa microphysa (Weber van Bosse) J. Feldmann W, E R<br />

Caulerpa peltata Lamouroux W, E, Sn C, R, S<br />

Caulerpa peltata Lamouroux [Syn: Caulerpa racemosa (Forsskaal) J. Agardh var. clavifera<br />

(Turner) Weber-van Bosse] P, Sn C<br />

191


Caulerpa peltata Lamouroux [Syn: Caulerpa racemosa (Forsskaal) J. Agardh var. peltata<br />

(Lamouroux) Eubank] E C<br />

Caulerpa prolifera (Forsskaal) Lamouroux forma zosterifolium Børgesen W C<br />

Caulerpa racemosa (Forsskaal) J. Agardh W, E, Sb, Sn C, M, S<br />

Caulerpa racemosa (Forsskaal) J. Agardh var. laetevirens (Montagne) Weber-van Bosse W R<br />

Caulerpa racemosa (Forsskaal) J. Agardh var. macrophysa (Sonder ex Kutzing) W. R. Taylor W, E R, S<br />

Caulerpa racemosa (Forsskaal) J. Agardh var. turbinata (J. Agardh) Eubank Sn C<br />

Caulerpa racemosa (Forsskaal) J. Agardh var. turbinata (J. Agardh) Eubank [Syn: Caulerpa<br />

chemnitzia (Esper) Lamouroux] P -<br />

Caulerpa scalpelliformis (R. Brown ex Turner) C. Agardh P -<br />

Caulerpa serrulata (Forsskaal) J. Agardh W, E, Sb, Sn C<br />

Caulerpa serrulata (Forsskaal) J. Agardh var. pectinata Kutzing W R, S<br />

Caulerpa sertulariodes (S. Gmelin) Howe W, Sb, Sn C, D, S<br />

Caulerpa sertulariodes(S. Gmelin) Howe forma longiseta (Bory de Saint-Vincent) Svedelius W S<br />

Caulerpa taxifolia (Vahl) C. Agardh W, E, P, Sb, Sn C, D, R<br />

Caulerpa verticillata J. Agardh W, E, Sb, Sn C, R, E<br />

Family Codiaceae<br />

Codium arabicum Kutzing W, Sn D<br />

Codium geppiorum O. Schmidt W, E, Sn C, E, S<br />

Codium tomentosum Stackhouse E, P C, R<br />

Family Halimedaceae<br />

Halimeda discoidea Decaisne Sb R, S<br />

Halimeda macroloba Decaisne W, E C, S<br />

Halimeda opuntia (Linnaeus) Lamouroux W, E, Sb, Sn C, S<br />

Halimeda opuntia (Linnaeus) Lamouroux var. minor Vickers E C, S<br />

Halimeda simulans Howe W, E S<br />

Halimeda tuna (Ellis & Solander) Lamouroux W, E, Sb, Sn C, S<br />

Family Udoteaceae<br />

Avrainvillea erecta (Berkeley) A. Gepp & E. Gepp W, E, Sn C, E, S<br />

Avrainvillea longicaulis (Kutzing) G. Murray & Boodle W, E C<br />

Avrainvillea obscura (C. Agardh) J. Agardh E C, S<br />

192


Tydemannia expeditionis Weber-van Bosse E R, S<br />

Udotea argentea Zanardini var. spumosa A. Gepp & E. Gepp W C, S<br />

Udotea cyathiformis Decaisne (Syn.: Udotea sublittoralis Taylor) E -<br />

Udotea flabellum (Ellis & Solander) Howe W S<br />

Rhipidosiphon javensis Montagne [Syn: Udotea javensis (Montagne) A. Gepp & E.Gepp] W, E, Sn C, S<br />

Order Dasycladales<br />

Family Dasycladaceae<br />

Bornetella Munier-Chalmas Sn C<br />

Neomeris annulata Dickie P, E, Sn C, R<br />

Family Polyphysaceae<br />

Acetabularia acetabulum (Linnaeus) P. Silva [Acetabularia mediterranea Lamouroux nom. illeg.] P -<br />

Acetabularia crenulata Lamouroux Sb -<br />

Acetabularia major G. Martens P -<br />

Acetabularia parvula Solms-Laubach E C<br />

Acetabularia pusilla (Howe) Collins E -<br />

Division Rhodophyta<br />

Order Erythropeltidales<br />

Family Erythrotrichiaceae<br />

Erythrotrichia carnea (Dillwyn) J. Agardh Sn E<br />

Order Acrochaetiales<br />

Family Acrochaetiaceae<br />

Acrochaetium Nageli E C<br />

Order Nemaliales<br />

Family Galaxauraceae<br />

Galaxaura rugosa (Ellis & Solander) Lamouroux [Syn: Galaxaura squalida Kjellman] Sb -<br />

Tricleocarpa cylindrica (Ellis & Solander) Huisman & Borowitzka [Syn: Galaxaura cylindrica<br />

(Ellis & Solander) Lamouroux] Sb -<br />

193


Family Liagoraceae<br />

Liagora ceranoides Lamouroux [Syn: Liagora leprosa J. Agardh] E -<br />

Order Gelidiales<br />

Family Gelidiaceae<br />

Gelidium amansii Lamouroux W R<br />

Gelidium pusillum (Stackhouse) Le Jolis W R<br />

Gelidium spinosum (S. Gmelin) P. Silva, comb nov. [Syn: Gelidium latifolium Bornet ex Hauck] P -<br />

Pterocladia caerulescens (Kutzing) Santelices W C, S<br />

Pterocladia caloglossoides (Howe) Dawson [Syn: Pterocladia parva Dawson] E C, R<br />

Family Gelidiellaceae<br />

Gelidiella acerosa (Forsskal) J. Feldmann & G. Hamel [Syn: Gelidiopsis rigida (C. Agardh)<br />

Weber-van Bosse] E, P C, R<br />

Gelidiella lubria (Kutzing) J. Feldmann & G. Hamel [Syn: Gelidiella bornetii (Weber van Bosse)<br />

J. Feldmann & G. Hamel]<br />

Gelidiella pannosa (Feldmann) Feldmann et G. Hamel W R<br />

Order Gracilariales<br />

Family Gracilariaceae<br />

Gracilaria articulata Chang et Xia P M<br />

Gracilaria canaliculata Sonder P C, M, S<br />

Gracilaria blodgetti Harvey [Syn: Gracilaria cylindrica Børgesen] W M<br />

Gracilaria cacalia (J. Agardh) Dawson Sn C<br />

Gracilaria changii (Xia et Abbott) Abbott, Zhang et Xia W, E Mg, M, R, S<br />

Gracilaria coronopifolia J. Agardh W, E, Sn C, M<br />

Gracilaria crassa Harvey ex J. Agardh Sb, Sn D<br />

Gracilaria dura (C. Agardh) J. Agardh Sb -<br />

Gracilaria edulis (G. Gmelin) P. Silva W R, S, M<br />

Gracilaria edulis (S. Gmelin) P. Silva [Gracilaria lichenoides Greville nom. illeg.] W, Sk, Sn R<br />

Gracilaria eucheumoides Harvey P -<br />

Gracilaria firma Chang et Xia W, Sb R<br />

Gracilaria foliifera (Forskaal) Børgesen W R<br />

Gracilaria lichenoides Greville forma taenoides (J. Agardh) V. Hay [Syn: Gracilaria taenoides J. Agardh] P -<br />

194


Gracilaria manilaensis Yamamoto et Trono P, W M<br />

Gracilaria minor (Sonder) Durairatnam P -<br />

Gracilaria multifurcata Børgesen W C, R<br />

Gracilaria salicornia (C. Agardh) Dawson W, E, Sb Mg, M, R, S<br />

Gracilaria subtilis (Xia et Abbott) Xia et Abbott W S, M<br />

Gracilaria tenuistipitata Zhang et Xia W R<br />

Gracilaria textorii (Suringar) De Toni W R<br />

Gracilaria urvillei (Montagne) Abbott, Zhang et Xia W, Sb, Sn S, M<br />

Gracilaria verrucosa (Hudson) Papenfuss [Gracilaria confervoides Greville nom. illeg.] P, Sb -<br />

Gracilariopsis bailiniae Zhang et Xia W, Sb R<br />

Order Bonnemaisoniales<br />

Family Pterocladiophilaceae<br />

Asparagopsis taxiformis (Delile) Trevisan E R, C, S<br />

Family Halymeniaceae<br />

Cryptonemia crenulata (J. Agardh) J. Agardh Sb R<br />

Cryptonemia yendoi Weber van Bosse W R<br />

Grateloupia filicina (Lamouroux) C. Agardh W, Sb R, F<br />

Halymenia dilatata Zanardini E, Sb C, R<br />

Halymenia durvillei Bory de Saint-Vincent W, E, Sb, P C, R<br />

Halymenia floresia (Clemente y Rubio) C. Agardh E, Sn C, R, S<br />

Halymenia formosa Harvey ex Kutzing E, Sn C<br />

Halymenia maculata J. Agardh W, E, Sb, Sk C, R<br />

Halymenia microcarpa (Montagne) P. Silva [Syn: Halymenia durvillei Bory de Saint-Vincent var. Sn C<br />

ceylanica Kutzing (Harvey ex Kutzing)]<br />

Family Kallymeniaceae<br />

Callophyllis heanophylla Setchell E R<br />

Family Peyssonneliaceae<br />

Peyssonnelia inamoena Pilger E C, F<br />

Family Rhizophyllidaceae<br />

Portieria hornemannii (Lyngbye) P. Silva E C<br />

195


Order Hildenbrandiales<br />

Family Hildenbrandiaceae<br />

Hildenbrandia rubra (Sommerfelt) Meneghini W R<br />

Order Corallinales<br />

Family Corallinaceae<br />

Amphiroa anceps (Lamarck) Decaisne E C, R<br />

Amphiroa foliaceae Lamouroux W, E, Sb C, R<br />

Amphiroa fragilissima (Linnaeus) Lamouroux W, E, Sb, P, Sn E<br />

Amphiroa rigida Lamouroux W, E, Sn C, E, R<br />

Amphiroa tribulus (Ellis et Solander) Lamouroux E, Sb -<br />

Corallina Linnaeus W, Sb -<br />

Fosliella dispar Foslie E -<br />

Jania adhaerens Lamouroux E -<br />

Jania capillacea Harvey E -<br />

Jania decussate-dichotoma (Yendo) Yendo E C<br />

Jania rubens (Linnaeus) Lamouroux W, Sb E<br />

Melobesia membranacea (Esper) Lamouroux Sk, P E<br />

Mesophyllum erubescens (Foslie) Lemoine [Lithothamnion erubescens Foslie] W R<br />

Mesophyllum simulans (Foslie) Lemoine [Lithothamnion simulans (Foslie) Foslie] W R<br />

Family Caulacanthaceae<br />

Catenella impudica (Montagne) J. Agardh Sn Mg<br />

Catenella nipae Zanardini W, Sk, Sn Mg<br />

Caulacanthus ustulatus (Turner) Kutzing W, Sk R<br />

Order Gigartinales<br />

Family Gigartinaceae<br />

Chondracanthus acicularis (Roth) Fredericq [Gigartina acicularis (Roth) Lamouroux] W C<br />

Chondracanthus intermedius (Suringar) Hommersand W R<br />

Family Hypneaceae<br />

Hypnea charoides Lamouroux W R<br />

Hypnea cenomyce J. Agardh Borneo -<br />

196


Hypnea cornuta (Kutzing) J. Agardh W S, M<br />

Hypnea esperi Grunow Sn C, E<br />

Hypnea flexicaulis Yamagishi et Masuda Sb E<br />

Hypnea musciformis (Wulfen) Lamouroux P -<br />

Hypnea pannosa J. Agardh W, E C, R<br />

Hypnea spinella (C. Agardh) Kutzing E, Sn C, E, R<br />

Hypnea spinella (C. Agardh) Kutzing [Syn: Hypnea cervicornis J. Agardh] E, Sb, Sn C<br />

Hypnea stellulifera (J. Agardh) Yamagishi et Masuda W, Sb F, M, R<br />

Family Sarcodiaceae<br />

Sarcodia J. Agardh W R<br />

Family Schizymeniaceae<br />

Titanophora (J. Agardh) J. Feldmann W C<br />

Family Solieriaceae<br />

Agardhiella subulata (C. Agardh) Kraft & Wynne [Syn: Agardhiella tenera (J. Agardh) Schmitz] P -<br />

Eucheuma serra (J. Agardh) J. Agardh P -<br />

Eucheuma arnoldii Weber van-Bosse [Syn: Eucheuma cuppressoideum Weber-van Bosse] P, Sn -<br />

Eucheuma denticulatum (Burman) Collins & Harvey [Syn: Eucheuma muricatum (S. Gmelin)<br />

Weber-van Bosse] P -<br />

Eucheuma denticulatum (Burman) Collins & Harvey [Syn: Eucheuma spinosum J. Agardh] P -<br />

Eucheuma horridum J. Agardh P -<br />

Kappaphycus alvarezii (Doty) Doty ex P. Silva, comb. nov Sb S<br />

Kappaphycus cottonii (Weber-van Bosse) Doty ex P. Silva Sb C, R<br />

Solieria anastomosa P. Gabrielson et Kraft Sb C, R<br />

Solieria robusta Greville (Kylin) Sn -<br />

Order Rhodymeniales<br />

Family Champiaceae<br />

Champia compressa Harvey E C, F, R<br />

Champia parvula (C. Agardh) Harvey W, E E<br />

Champia vieillardii Kutzing E C<br />

Gastroclonium compressum (Hollenberg) Chang & Xia E -<br />

197


Family Lomentariaceae<br />

Lomentaria gracillima Masuda et Kogame Sb E<br />

Lomentaria monochlamydea (J. Agardh) Kylin E C<br />

Family Rhodymeniaceae<br />

Botryocladia leptopoda (J. Agardh) Kylin W Mn, C, S<br />

Ceratodictyon spongiosum Zanardini W, Sb C, R<br />

Chamaebotrys boergesenii (Weber-van Bosse) Huisman E C, E<br />

Chrysymenia J. Agardh Sb -<br />

Coelarthrum Børgesen Sb R<br />

Gelidiopsis intricata (C. Agardh) Vickers E C<br />

Order Ceramiales<br />

Family Ceramiaceae<br />

Anotrichium tenue (C. Agardh) Nageli (Syn: Griffithsia tenuis C. Agardh) W, E, Sb C, E, R<br />

Antithamnionella elegans (Berthold) J. Price & D. John [Syn: Antithamnionella breviramosa (Dawson)<br />

Wallaston in Wolmsley & Bailey] E E<br />

Callithamnion fellipponei Howe E -<br />

Centroceras clavulatum(C. Agardh) Montagne Sb -<br />

Centroceras minutum Yamada E C<br />

Ceramium corniculatum Montagne E -<br />

Ceramium diaphanum (Lightfoot) Roth [Ceramium tenuissimum (Roth) Areschoug nom. illeg.] W, E E<br />

Ceramium fimbriatum Setchell & Gardner [Syn: Ceramium gracillimum (Kutzing) Griffiths & Harvey] E E<br />

Ceramium flaccidum (Kutzing) Ardissone E E<br />

Corrallophila huysmansii (Weber-van Bosse) R. Norris [Syn: Ceramium huysmansii Weber-van Bosse] Sn R<br />

Griffithsia schousboei Montagne W E, R<br />

Ptilothamnion codicolum (Dawson) Abbott E E<br />

Spyridia filamentosa (Wulfen) Harvey W, E C, E, R, S,<br />

Wrangelia argus (Monatgne) Montagne E E<br />

Wrangelia bicuspidata Børgesen W, E Mn, C, S<br />

Family Dasyaceae<br />

Dasya iyengarii Børgesen W, E, Sb, Sk E, F<br />

Dasya longifila Masuda et Uwai Sb E<br />

Dasya malaccensis Masuda et Uwai W F<br />

198


Dasya pilosa (Weber-van Bosse) Millar E, Sb R<br />

Heterosiphonia crispella (C. Agardh) Wynne W, E, Sb, Sk E, F<br />

Heterosiphonia Montagne W E<br />

Family Delesseriaceae<br />

Caloglossa adhaerens King & Puttock [Syn: Caloglossa adnata (Zanardini) De Toni] Sk -<br />

Delesseria adnata Zanardini [Syn: Caloglossa bengalensis (Martens) King & Pullock] Sk -<br />

Delesseria beccarii Zanardini [Syn: Caloglossa beccarii (Zanardini) De Toni] Sk -<br />

Hypoglossum caloglossoides Wynne et Kraft E C, E<br />

Hypoglossum rhizophorum Ballantine et Wynne E C<br />

Hypoglossum simulans Wynne, I. Price & Ballantine W C<br />

Martensia australis Harvey Sb E, R<br />

Martensia fragilis Harvey W, E C, E, R<br />

Taenioma dotyi Hollenberg W R<br />

Taenioma perpusillum (J. Agardh) J. Agardh Sb, Sk E<br />

Zellera tawallina Martens Sb R<br />

Family Rhodomelaceae<br />

Acanthophora muscoides (Linnaeus) Bory de Saint-Vincent Sn C<br />

Acanthophora spicifera (Vahl) Børgesen W, E, Sn, P C, D, R, S<br />

Acanthophora spicifera (Vahl) Børgesen [Syn: Acanthophora orientalis J. Agardh] W, Sn C, E<br />

Acanthophora spicifera (Vahl) Børgesen [Syn: Acanthophora thierryi Lamouroux] Sk -<br />

Amansia rhodantha (Harvey) J. Agardh Sb R<br />

Bostrychia moritziana (Sonder ex Kutzing) J.Agardh Sn Mg<br />

Bostrychia tenella (Lamouroux) J. Agardh W Mg<br />

Bostrychia tenella (Lamouroux) J. Agardh [Syn: Bostrychia binderi Harvey] Sn R<br />

Chondria armata (Kutzing) Okamura E, P R<br />

Chondria decidua Tani et Masuda Sb E<br />

Chondria econstricta Tani & Masuda Sb E<br />

Chondria xishaensis Zhang (Chang) & Xia Sb E<br />

Herposiphonia pacifica Hollenberg W, E F, R<br />

Herposiphonia secunda (C. Agardh) Ambronn E -<br />

Herposiphonia vietnamica Pham Sb E<br />

Laurencia articulata Tseng E C, R<br />

Laurencia botryoides (C. Agardh) Gaillon P -<br />

199


Laurencia caduciramulosa Masuda et Kawaguchi E R<br />

Laurencia calliclada Masuda E R<br />

Laurencia concreta Crib W, Sb C<br />

Laurencia corymbosa J. Agardh W, E C, R<br />

Laurencia decumbens Kutzing [Syn: Laurencia pygmaea Weber-van Bosse] W R<br />

Laurencia flexilis Setchell Sk R<br />

Laurencia glandulifera (Kutzing) Kutzing W R<br />

Laurencia implicata J. Agardh E -<br />

Laurencia intricata Lamouroux W, E -<br />

Laurencia lageniformis Masuda Sb, Sk R<br />

Laurencia majuscula (Harvey) Lucas E, Sb, Sk C, R<br />

Laurencia microcladia Kutzing Sn Mg<br />

Laurencia nangii Masuda Sb C, E<br />

Laurencia obtusa (Hudson) Lamouroux W C<br />

Laurencia pannosa Zanardini Sk -<br />

Laurencia papillosa (C. Agardh) Greville, Setchell et Gardner W, E, Sb, Sk C, R, S<br />

Laurencia parvipapillata Tseng E C<br />

Laurencia perforata (Bory de Saint-Vincent) Montagne E C<br />

Laurencia pinnata Yamada W R<br />

Laurencia similis Nam et Saito Sb C, R<br />

Leveillea junggermanniodes (Herling & G. Martens) Harvey W, Sn E, C<br />

Murrayellopsis dawsonii Post E R<br />

Neosiphonia apiculata (Hollenberg) Masuda et Kogame E, Sb E<br />

Neosiphonia flaccidissima (Hollenberg) M.S.Kim et I.K.Lee W E<br />

Neosiphonia savatieri (Hariot) M.S.Kim et I.K.Lee E, Sb E<br />

Polysiphonia coacta Tseng E C, R<br />

Polysiphonia decussata Hollenberg E E<br />

Polysiphonia ferulaceae Suhr ex J. Agardh Sn E<br />

Polysiphonia fucoides (Hudson) Greville [Syn: Polysiphonia nigrescens (Hudson) Greville in W. Hooker] W, E E, R<br />

Polysiphonia platycarpa Børgesen Sn E<br />

Polysiphonia scopulorum Harvey W, E C, E, F, R<br />

Polysiphonia subtillisima Montagne E E, C<br />

Polysiphonia violaceae Greville E E, R<br />

Tolypiocladia calodictyon (Harvey ex Kutzing) P. Silva E E<br />

Tolypiocladia glomerulata (C. Agardh) Schmitz W, E E<br />

200


Division Phaeophyta<br />

Order Ectocarpales<br />

Family Ectocarpaceae<br />

Ectocarpus siliculosus (Dillwyn) Lyngbye [Misapplied name: Ectocarpus confervoides (Roth) Le Jolis] W -<br />

Ectocarpus variabilis Vickers W -<br />

Feldmannia enhali Hamel W, E E<br />

Feldmannia indica (Sonder) Wolmsley & Bailey W, E D, E<br />

Feldmannia simplex (Crouan & Crouan) Hamel [Syn.: Ectocarpus cylindricus Saunders] E -<br />

Family Ralfsiaceae<br />

Ralfsia Berkeley Sb -<br />

Order Sphacelariales<br />

Family Sphacelariaceae<br />

Sphacelaria caespitula Lyngbye Sk, Sn -<br />

Sphacelaria rigidula Kutzing [Syn: Sphacelaria furcigera Kutzing] W, Sb R<br />

Order Dictyotales<br />

Family Dictyoceae<br />

Dictyopteris acrostichoides (J. Agardh) Bornet W C, S<br />

Dictyopteris deliculata Lamouroux E E<br />

Dictyopteris woodwardia (R. Brown ex Turner) [Syn: Haliseris woodwardia (R. Brown ex Turner) Sk -<br />

C. Agardh]<br />

Dictyota bartayresiana Lamouroux W, E, Sn C, R<br />

Dictyota beccariana Zanardini Sk, P -<br />

Dictyota cervicornis Kutzing Sn M<br />

Dictyota cervicornis Kutzing [Syn: Dictyota indica Sonder ex Kutzing] E, Sn C<br />

Dictyota cervicornis Kutzing [Syn: Dictyota pardalis Kutzing] P -<br />

Dictyota cervicornis Kutzing forma spiralis Taylor E R<br />

Dictyota ciliolata Kutzing Sn C<br />

Dictyota dentata Lamouroux Sb -<br />

Dictyota dichotoma (Hudson) Lamouroux W, E, P, Sb, Sk R<br />

Dictyota dichotoma (Hudson) Lamouroux [Syn: Dictyota apiculata J. Agardh] P -<br />

Dictyota divaricata Lamouroux E -<br />

Dictyota friabilis Setchell W, E C, Mn, M, R<br />

201


Dictyota hauckiana Nizamuddin [Syn: Dictyota atomaria Hauck] Sb -<br />

Dictyota jamaicensis Taylor E S<br />

Dictyota linearis (C. Agardh) Greville W -<br />

Dictyota maxima Zanardini Sk -<br />

Dictyota mertensii (Martius) Kutzing [Syn: D. dentata Lamouroux] E S<br />

Dictyota submaritima Va Pham Hoang E R<br />

Lobophora variegata (Lamouroux) Wolmsley ex Oliveira (Syn.: Pocockiella variegata (Lamouroux)<br />

Papenfuss) W, E, Sb C, S<br />

Padina australis Hauck W, E C, R<br />

Padina boergesenii Allender & Kraft W, E C<br />

Padina boryana Thivy [Syn: P. commersonii Bory de Saint-Vincent] W, E, Sn R, C<br />

Padina caulescens Thivy E -<br />

Padina gymnospora (Kutzing) Sonder Sb, Sn C, S<br />

Padina minor Yamada E C, S<br />

Padina pavonia Lamouroux Sk -<br />

Padina tetrastromatica Hauck W, E, Sn C, R<br />

Spatoglossum vietnamense Pham Sb C<br />

Stypopodium zonale (Lamouroux) Papenfuss Sn C<br />

Order Scytosiphonales<br />

Family Chnoosporaceae<br />

Chnoospora minima (Hering) Papenfuss W R<br />

Family Scytosiphonaceae<br />

Colpomenia sinuosa (Mertens ex Roth) Derbes & Solier W, Sb E, R<br />

Hydroclathrus clathratus (C. Agardh) Howe [Syn: Asperococcus clathratus (C. Agardh) J. Agardh] W, P, Sb C, S<br />

Rosenvingea fastigiata (Zanardini) Børgesen [Syn.: Asperococcus fastigiatus Zanardini] Sk -<br />

Rosenvingea orientalis (J. Agardh) Børgesen W C, S<br />

Order Fucales<br />

Family Cystoseiraceae<br />

Cystoseira trinodis (Forsskal) C. Agardh E C, R<br />

Hormophysa cuneiformis (J. Gmelin) P. Silva W, E, Sb C, D, R<br />

Hormophysa cuneiformis (J. Gmelin) P. Silva [Syn: Cystoseira prolifera J. Agardh] W, Sk, Sn C, D<br />

Hormophysa cuneiformis (J. Gmelin) P. Silva [Syn: Cystoseira triquetra C. Agardh] Sb, Sn C<br />

202


Family Sargassaceae<br />

Sargassum abbottiae Trono W C<br />

Sargassum acutifolium Greville W, Sk C<br />

Sargassum angustifolium C. Agardh Sk, Sn -<br />

Sargassum aquifolium (Turner) C. Agardh Sn -<br />

Sargassum asperifolium Hering & G. Martens ex J. Agardh Sn D<br />

Sargassum baccularia (Mertens) C. Agardh W C<br />

Sargassum balingasayense Trono Sb C<br />

Sargassum binderi Sonder ex J. Agardh W C<br />

Sargassum cervicorne Greville E C<br />

Sargassum cinereum J. Agardh E, Sb, Sn D<br />

Sargassum crassifolium J. Agardh [Syn: Sargassum feldmanii Pham]<br />

Sargassum cristaefolium C. Agardh W, E C, R<br />

Sargassum dotyi Trono W C, R<br />

Sargassum duplicatum (J. Agardh) J. Agardh Sb, Sn R<br />

Sargassum erumpens Tseng et Lu E C<br />

Sargassum filipendula C. Agardh Sb -<br />

Sargassum granuliferum C. Agardh W, P C<br />

Sargassum grevillei J. Agardh W C<br />

Sargassum heterocystum (kuetzing) Montagne E C, R<br />

Sargassum hornschuchii C. Agardh Sb C<br />

Sargassum ilicifolium (Turner) C. Agardh W, E, Sn R, C<br />

Sargassum ilicifolium (Turner) C. Agardh [Syn: Sargassum sandei Reinbold] W R<br />

Sargassum illicifolium (Turner) C. Agardh var conduplicatum Grunow E R<br />

Sargassum laxifoliumTseng et Lu Sb C, R<br />

Sargassum microcystum J. Agardh Sb C, R<br />

Sargassum myriocystum J. Agardh W, Sn C<br />

Sargassum oligocystum Montagne Sb R<br />

Sargassum polycystum C. Agardh W, E, Sb, Sn D, C, R, S<br />

Sargassum siliculosoides Tseng et Lu E C, R<br />

Sargassum siliquosum J. Agardh W, P, Sb, Sn R<br />

Sargassum spathulaefolium J. Agardh W, Sn D<br />

Sargassum squarrosum Greville W C, R<br />

Sargassum stolonifoium Phang et Yoshida W R<br />

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Sargassum swartzii C. Agardh W C<br />

Sargassum tenerrimum J. Agardh Sb -<br />

Sargassum torvum J. Agardh Sn R<br />

Sargassum virgatum C. Agardh W, Sn C<br />

Sargassum vulgare C. Agardh Sb C<br />

Sargassum wightii Greville W C<br />

Turbinaria conoides (J. Agardh) Kutzing W, E, P, Sb, Sn C, D, R<br />

Turbinaria deccurrens Bory de Saint-Vincent W, E R<br />

Turbinaria ornata (Turner) J. Agardh W, E, P, Sn C, S<br />

Turbinaria ornata (Turner) J. Agardh var. serrata Jaasund Sn C<br />

Turbinaria tricostata Barton E -<br />

Abbreviation<br />

Distribution:<br />

P: Peninsular Malaysia; Sb: Sabah; Sk: Sarawak; Sn: Singapore; E: East Coast Peninsular Malaysia; W: West Coast Peninsular Malaysia<br />

Habitat:<br />

C: Coral; D: Driftweed; E: Epiphyte; M: Mud; Mg: Mangrove; P: Planktonic; R: Rock, Bedrock, Stones; S: Sand; W: Wood; F: Fish cage, fishing line<br />

and fish net<br />

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PHANG et al (2007)<br />

sandy areas, mudflats, coral reefs and rocky shores. Turbinaria and the encrusting Lobophora<br />

variegata often accompany the Padina on the intertidal coral reefs. The new species Sargassum<br />

stolonifolium Phang and Yoshida described from Penang Island, is the first in the genus to<br />

exhibit the phenomena of new plantlets derived from the first leaves (Phang & Yoshida 1997).<br />

ECONOMIC IMPORTANCE OF SEAWEEDS IN MALAYSIA<br />

Early records show that several seaweeds were utilised in Malaysia for food, animal feed,<br />

fertiliser and traditional medicine (Burkill 1966, Hooper 1960, Zaneveld 1959, Phang 1984).<br />

Seaweeds like Gracilaria changii, G. edulis, G. salicornia, G. tenuispitata and Gelidium spp.<br />

are used as salads and for the preparation of desserts such as agar-agar. Sarer which is a<br />

species of Gracilaria forms part of the food for the ‘buka puasa’ during the fasting months,<br />

especially along the east coast. In Sabah Eucheuma and Caulerpa are collected and eaten<br />

either raw or blanched in salads. In the Chinese medicine shops one can buy dried Sargassum,<br />

Turbinaria and Ulva of unknown origin, which is popularly used by the Chinese in a soup<br />

considered as a rich source of iodine and which ‘cools’ the body system. The nutritional value<br />

of Malaysian seaweeds is not known except for a short study reporting on the lipid and fattyacid<br />

content of selected seaweeds (Norazmi 2001). Nine species of seaweeds were analysed<br />

for fatty acid composition, and Dictyota dichotoma was found to contain the highest (17.6%<br />

ash-free dry wt) amount of lipids. All the seaweeds contained eicosapentaenoic acid ranging<br />

from 2.4 to 10.7% total fatty acid, with Gracilaria edulis having the highest content.<br />

Of the Malaysian seaweeds, only Eucheuma (Kappaphycus) is presently cultivated for the<br />

commercial production of carrageenan chips as well as semi-refined carrageenan in Tawau,<br />

Sabah. Fishing families around Semporna, east coast Sabah, are involved in the mariculture<br />

of the Eucheuma using the monofilament techniques in the reefs fringing the islands near<br />

Semporna. The average cultivation period is 45 days and continues for eight months of the<br />

year. The monthly production from Semporna was around 60 to 100 tonnes dry wt per month<br />

(Phang 1998). The harvested seaweed is sun dried on the platforms of houses built on the<br />

reefs and sold at RM 1.10 (US$1 = RM3.8) per kg dry wt (moisture content of 32 to 35%) to<br />

the carrageenan producers. There are three semi-refined carrageenan factories in Tawau.<br />

Gracilaria changii, a good source of high quality agar and agarose (Phang 1994b) has also<br />

been experimentally cultivated in shrimp ponds, mangrove ponds and irrigation canals (Phang<br />

et al. 1996). Unlike Eucheuma, Gracilaria farming has not gone large-scale, probably because<br />

there are no large agar factories in the region.<br />

The search for novel bioactive compounds from marine algae has revealed tropical seaweeds<br />

to be a potentially important source (Masuda et al. 2002, Varaippan et al. 2004). Bioactive<br />

properties of seaweeds range from antiviral to antioxidant, immunostimulatory, anti-coagulant,<br />

anti-thrombic and anti-inflammatory. Traditionally coralline algae like Corallina and Amphiroa<br />

are crushed and fed to children to expel worms. Halimeda opuntia, Acanthophora spicifera,<br />

Laurencia, Eucheuma spinosum, Gracilaria sp., Hypnea musciformis, Dictyopteris sp., and<br />

Sargassum spp. contain antibiotic compounds.<br />

These tropical seaweed resources have great potential for development as food, feed and<br />

sources of biopharmaceutical products in addition to industrial colloids. A potentially good<br />

culture system would be the integrated culture with shrimp, fish or abalone farming. Gracilaria<br />

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SEAWEED DIVERSITY IN MALAYSIA<br />

can be cultured in shrimp ponds, where the seaweed removes dissolved nutrients from the<br />

excess feed of the shrimps, thereby cleaning up the water, and produce a useful biomass for<br />

extraction of agar and agarose or any other useful biochemicals (Phang et al. 1996). The<br />

seaweeds can also be used to feed aquaculture species like abalone. The young larvae find<br />

protection amongst the seaweeds from predators and the seaweeds also produce oxygen and<br />

remove carbon dioxide, thereby contributing to reduction in global warming simultaneously.<br />

THREATS TO SEAWEED RESOURCES<br />

There is little information on the ecology and biology of tropical seaweeds, more so of the<br />

Malaysian species (Phang 1988, 1989, 1995; Wong & Phang 2004). Information on standing<br />

biomass and productivity of natural populations is scarce, while none on the harvesting from<br />

any natural seaweed populations is available.<br />

Threats to seaweed resources include land reclamation, construction of jetties, bridges and<br />

marinas, pollution, trawlers, destructive fishing methods, sand mining, overharvesting of<br />

commercial species, introduction of alien and invasive species, illegal bioprospecting and<br />

also natural phenomena like tropical storms, typhoons and global warming. Of these threats,<br />

development of islands and coastal areas into resorts and marinas is the greatest. Natural<br />

sandy habitats and fringing coral reefs have been silted over by clearing of mangroves (Phang<br />

1988, 1995) as well as beach areas, for aquaculture and construction. Increased marine traffic<br />

adds oil and grease to the waters, while untreated discharges from sewage facilities, rubber<br />

and palm oil mills, electronic and electro-plating industries, bring organic and inorganic<br />

pollutants to the marine ecosystem (Ramachandran et al. 1995).<br />

MANAGEMENT OF SEAWEED RESOURCES<br />

Habitat destruction is an important issue related to the management of the seaweeds. Continued<br />

population concentration in coastal areas will lead to increased user conflicts, competition for<br />

ocean resources and habitat destruction. Aquaculture may replace wild fishing, resulting in<br />

impacts on the habitats of the seaweeds in the form of pollution and also habitat destruction.<br />

This issue may hopefully be addressed with the implementation of the National Coastal Zone<br />

Management Plan. The increase in bioprospecting would require laws to prevent biopiracy.<br />

Presently there are no specific legislations or policies to safeguard the seaweed resources.<br />

Marine Parks serve as refuges for seaweeds, but without increased manpower, funding and<br />

authority, even seaweed habitats in protected areas may be threatened. While about 14 ministries<br />

and 23 government agencies perform ocean related functions, there is no clear Federal-State<br />

relationship regarding biodiversity management. There is also lack of coordinated gathering,<br />

processing, storage and dissemination of biodiversity information. Recently the Marine Parks<br />

Division has been entrusted the task of documenting the marine resources of Malaysia. There<br />

is a lack of skilled human resources in implementing agencies as well as research institutions<br />

and universities for managing the resources, especially in the form of taxonomists. The<br />

important contribution of the general public to marine biodiversity conservation and<br />

management must not be neglected. Non-governmental organisations like the Malaysian Nature<br />

Society and the Malaysian Society of Marine Sciences regularly organise community awareness<br />

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PHANG et al (2007)<br />

programmes to enlist public assistance in the protection of natural resources. An Environmental<br />

Education Curriculum should be introduced to schools to inculcate awareness in the younger<br />

population.<br />

Strategies for the protection of seaweeds and other natural resources include the establishment<br />

of a National Biodiversity Directorate, National Ocean Council, National Biodiversity Database<br />

and more Marine Protected Areas. The practice of sustainable fisheries, sustainable mariculture<br />

and the control of invasive alien species must be enforced. Integrated marine and coastal area<br />

management should be practiced. Alternative livelihoods could be introduced for poverty<br />

alleviation in coastal communities. There should be increased funding for research in areas of<br />

distribution, abundance and ecology of seaweed resources, thus enabling the proper assessment<br />

of the sustainability of the seaweed resources in Malaysia.<br />

CONCLUDING REMARKS<br />

The last two decades have seen an increase in seaweeds as a potential economic resource in<br />

the Asia-Pacific region, including Malaysia. Two genera, Eucheuma (Kappaphycus) and<br />

Gracilaria were targeted for development in Malaysia. However Gracilaria cultivation has<br />

not gone beyond the experimental stage. Eucheuma culture in Sabah continues with the fishing<br />

community around Semporna and has spread to the Kudat area through initiatives from the<br />

state government. These resources cannot meet the demands of the three carrageenan factories.<br />

Gracilaria on the other hand does not demand clean waters as Eucheuma, and should in fact<br />

grow well in Peninsular Malaysian waters. Agar processing requires simpler technology than<br />

carrageenan, and in fact has a high domestic demand (Jahara & Phang 1990). Of the other<br />

seaweeds, Caulerpa species are easy to culture but would require good marketing to sell its<br />

use as a delicacy in restaurants. Acanthophora, Gracilaria and Hypnea can be grown as feed<br />

for abalone.<br />

The inventory of Malaysian seaweeds continues. Presently 386 taxa are recorded. Many<br />

scientifically interesting as well as commercially important species have been identified.<br />

Ecological information is scarce. Biomass assessments of natural seaweed areas, productivity<br />

determination and phenological studies of important species, should be encouraged. Only<br />

then can the status of the seaweed flora of Malaysia be assessed, and threatened species and<br />

habitats identified. The use of new approaches like molecular taxonomy should be encouraged<br />

to enhance species identification and possibly provide a fingerprinting technique to monitor<br />

and prevent biodiversity loss.<br />

ACKNOWLEDGEMENTS<br />

Acknowledgements are due to Professor Michio Masuda, University of Hokkaido, whose<br />

expertise made a worthy checklist possible, Professors Shigeru Kawaguchi, Tetsuro Ajisaka,<br />

K. Kogame, Misni Surif and all the expedition members, especially my students Wong Ching<br />

Lee, Melor Ismail and Murugadas T. Loganathan, who contributed towards the wonderful<br />

collections. We are grateful to the Fisheries Departments, Marine Parks and Fisheries Research<br />

Institutes, throughout the Malaysian states, which have always been very generous with their<br />

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assistance during our fieldwork. Generous research grants from the IRPA Grants No.09-02-<br />

03-222 and 09-02-03-788, MOSTE, Malaysia and Ministry of Education, Science, Sports and<br />

Culture, Japan, are gratefully acknowledged.<br />

REFERENCES<br />

AHMAD ISMAIL 1995. Rumpai Laut Malaysia. (Seaweeds of Malaysia). Dewan Bahasa<br />

dan Pustaka, Malaysia. (In Bahasa Malaysia).<br />

AJISAKA, T. 2002. Sargassum specimens from Singapore and Malaysia in the Herbarium of<br />

the Bishop Museum. Pp. 77–88 in Abbott, I.A. & McDermid, K. (eds.) Taxonomy of<br />

Economic Seaweeds. With reference to some Pacific species. Vol. VIII. California Sea<br />

Grant Programme.<br />

AJISAKA, T., PHANG, S.M. & YOSHIDA, T. 1999. Preliminary report of Sargassum species<br />

collected from Malaysian coasts. Pp. 23–42 in Abbott, I.A. (ed.) Taxonomy of Economic<br />

Seaweeds. With reference to some Pacific species. Vol. VII. California Sea Grant<br />

Programme.<br />

BURKILL, I.H. 1966. A Dictionary of the Economic Products of the Malay Peninsula. 2 vols.<br />

Ministry of Agriculture and Cooperatives, Kuala Lumpur, Malaysia.<br />

CRITCHLEY, A.T. & OHNO, M. 1998. Seaweed Resources of the World. Japan International<br />

Cooperation Agency.<br />

FELDMANN, J. 1937. Recherches sur la vegetation marine de la Mediterranee. La cote des<br />

Alberes. Rev. Algol. 10: 1–339.<br />

GEPP, A. & GEPP, E.S. 1911. The Codiaceae of the Siboga Expedition including a monograph<br />

of Flabellariaceae and Udoteaceae. Siboga-Expedite Monographie 62.<br />

HOOPER, D. 1960. On Chinese Medicine: Drugs of Chinese Pharmacies in Malaya. The<br />

Garden’s Bulletin Straits Settlements VII(1-15): 1–57.<br />

JAHARA, J. & PHANG, S.M. 1990. Seaweed Marketing and Agar Industries in Malaysia.<br />

Pp. 75–86 in BOBP, Gracilaria production and utilization in the Bay of Bengal. BOBP/<br />

REP/45. Bay of Bengal Programme.<br />

KAWAGUCHI, S., KATO, A., MASUDA, M., KOGAME, K. & PHANG, S.M. 2002.<br />

Taxonomic Notes on the Marine Algae of Malaysia. VII. Five Species of Rhodophyceae,<br />

with the Description of Lomentaria gracillima sp. nov. Botanica Marina 45: 536–547.<br />

LIM, P.E. & PHANG, S.M. 2004. Gracilaria species (Gracilariales, Rhodophyta) of Malaysia<br />

including two new records. Mal. J. Sci. 23(2): 71–80.<br />

LIM, P.E., THONG, K.L. & PHANG, S.M. 2001. Molecular differentiation of two<br />

morphological variants of Gracilaria salicornia. J. Appl. Phycol. 13: 335–342.<br />

MARTENS, G. VON. 1866. In Die Preussische Expedition nach Ost-Asien; nach amlitchen<br />

quellen: Botanischer Theil, Berlin.<br />

MASUDA, M., ABE, T., KAWAGUCHI, S. & PHANG, S.M. 1999. Taxonomic Notes on<br />

Marine Algae from Malaysia. I. Six Species of Rhodophyceae. Botanica Marina 42:<br />

449–458.<br />

MASUDA, M., ABE, T., KAWAGUCHI, S. & PHANG, S.M. 2001b. Taxonomic Notes on<br />

Marine Algae from Malaysia. VI. Five Species of Ceramiales (Rhodophyceae). Botanica<br />

Marina 44: 467–477.<br />

MASUDA, M., ABE, T., KOGEAME, K., KAWAGUCHI, S., PHANG, S.M., DAITOH, T.,<br />

SAKAI, Y. & SUZUKI, M. 2002. Taxonomic Notes on the Marine Algae of Malaysia.<br />

VIII. Three species of Laurencia (Rhodophyceae). Botanica Marina 45: 571–579.<br />

208


PHANG et al (2007)<br />

MASUDA, M., KAWAGUCHI, S. & PHANG, S.M.1997. Taxonomic Notes on Laurencia<br />

similis and L. papillosa (Ceramiales, Rhodophyta) from the Western Pacific. Botanica<br />

Marina 40: 229–239.<br />

MASUDA, M., KATO, A., AHIMADA, S., KAWAGUCHI, S. & PHANG, S.M. 2000a.<br />

Taxonomic Notes on Marine Algae from Malaysia. II. Seven Species of Rhodophyceae.<br />

Botanica Marina 43: 181–190.<br />

MASUDA, M., KOGAME, K., KAWAGUCHI, S. & PHANG S.M. 2000b. Taxonomic Notes<br />

on Marine Algae from Malaysia. IV. Six Species of Ceramiales (Rhodophyceae). Botanica<br />

Marina 43: 569–579.<br />

MASUDA, M., KOGANE, K., KAWAGUCHI, S. & PHANG, S.M. 2001a. Taxonomic Notes<br />

on Marine Algae from Malaysia. V. Five Species of Rhodymeniales (Rhodophyceae).<br />

Botanica Marina 44: 81–88.<br />

MASUDA, M., UWAI, S., KOGAME, K., KAWAGUCHI, S. & PHANG, S.M. 2003.<br />

Taxonomic Notes on Marine Algae from Malaysia. X. Four Species of Dasya<br />

(Rhodophyceae), with the Descriptions of Dasya longifila sp. nov and D. malaccensis sp.<br />

nov. Botanica Marina 46: 243–255.<br />

NORAZMI MOHAMED 2001. Fatty-acid Composition of Some Malaysian Seaweeds.<br />

Unpublished B.Sc. Thesis, Institute of Biological Sciences, University of Malaya.<br />

PHANG, S.M. 1984. Seaweed Resources of Malaysia. Wallaceana W38: 3–8.<br />

PHANG, S.M. 1988. The Effect of Siltation on Algal Biomass Production at a Fringing Coral<br />

Reef Flat, Port Dickson, Peninsular Malaysia. Wallaceana 51: 3–5.<br />

PHANG, S.M. 1989. Notes on the Ecology of Some Marine Epiphytic Rhodophytes at Cape<br />

Rachado, Peninsular Malaysia. Malayan Nature Journal 43: 84–95.<br />

PHANG, S.M. 1994a. New Records of Malaysian Marine Algae. Hydrobiologia 285: 123–129.<br />

PHANG, S.M.1994b. Some Species of Gracilaria from Peninsular Malaysia and Singapore.<br />

Pp. 125–134 in Abbott, I.A. (ed.) Taxonomy of Economic Seaweeds. With reference to<br />

some Pacific species, Vol. IV. California Sea Grant College.<br />

PHANG, S.M.1995. Distribution and abundance of marine algae on the coral reef flats at<br />

Cape Rachado, Port Dickson, Peninsular Malaysia. Malaysian J. Science 16A: 23–32.<br />

PHANG, S.M. 1998. The Seaweed Resources of Malaysia. Pp. 79–91 in Critchley, A.T. &<br />

Ohno, M. (eds.) Seaweed Resources of the World, Japan International Cooperation Agency.<br />

PHANG, S.M. 2006. Seaweed resources in Malaysia: current status and future prospects.<br />

Aquatic Ecosystem Health & Management 9(2): 185–202.<br />

PHANG, S.M. & MAHESWARY, V. 1989. Phycocolloid Content of Some Malaysian<br />

Seaweeds. Pp. 65–77 in Proceedings Twelfth Annual Seminar Malaysian Society of Marine<br />

Sciences. Kuala Lumpur.<br />

PHANG, S.M. & YOSHIDA, T. 1997. Sargassum stolonifolium Phang et Yoshida sp. nov.<br />

from Penang Island, Peninsular Malaysia. Pp. 61–73 in Abbott, I.A. (ed.) Taxonomy of<br />

Economic Seaweeds. With reference to some Pacific and Caribbean species. Vol. VI.<br />

California Sea Grant College.<br />

PHANG, S.M. & WEE, Y.C. 1991. Benthic Marine Algae. Pp. 51–61 in Kiew, R. (ed.) The<br />

State of Nature Conservation in Malaysia. Malayan Nature Society.<br />

PHANG, S.M., SHAFEEI SHAHARUDDIN, HASHIM NORAISHAH & SASEKUMAR,<br />

A. 1996. Studies on Gracilaria changii (Gracilariales, Rhodophyta) from Malaysian<br />

Mangroves. Hydrobiologia 326/327: 347–352.<br />

PHANG, S.M., WONG, C.L., LIM, P.E., YEONG, H.Y. & CHAN, C.X. 2005. Seaweed<br />

Diversity of Langkawi with emphasis on Northeast Langkawi. Malaysian J. Science 24:<br />

77–94.<br />

209


SEAWEED DIVERSITY IN MALAYSIA<br />

RAMACHANDRAN, S.D., MURUGADAS, T.L., TONG, S.L. & PHANG, S.M. 1995. Heavy<br />

metal accumulation in Malaysian seaweeds. Pp. 240–245 in Watson, D., Ong, K.S. &<br />

Vugers, G. (eds.) ASEAN Criteria and Monitoring. Advances in Marine Environmental<br />

Management and Human Health Protection. EVS Environmental Consultants, Vancouver<br />

and National Science and Technology Board, Singapore.<br />

TANI, M. & MASUDA, M. 2003. A Taxonomic Study of Two Minute Species of Chondria<br />

(Ceramiales, Rhodophyta) from the North-Western Pacific, with the Description of<br />

Chondria econstricta sp. nov. Phycologia 42(3): 220–231.<br />

TANI, M., YAMAGISHI, Y., MASUDA, M., KOGAME, K., KAWAGUCHI, S. & PHANG,<br />

S.M. 2003. Taxonomic Notes on Marine Algae from Malaysia. IX. Four Species of<br />

Rhodophyceae, with the Description of Chondria decidua sp. nov. Botanica Marina 46:<br />

24–35.<br />

TEO, L.W. & WEE, Y.C. 1983. Seaweeds of Singapore. Singapore University Press, Singapore.<br />

TERADA, R., KAWAGUCHI, S., MASUDA, M., KAWAGUCHI, S. & PHANG, S.M. 2000.<br />

Taxonomic Notes on Marine Algae from Malaysia. III. Seven Species of Rhodophyceae.<br />

Botanica Marina 43: 347–357.<br />

WONG, C.L. & PHANG, S.M. 2004. Biomass Production of Two Sargassum Species at Cape<br />

Rachado, Malaysia. Hydrobiologia 512: 79–88.<br />

WONG, C.L. & PHANG, SM. 2004. Diversity and Distribution of Malaysian Sargassum<br />

species. Pp. 23–46 in Phang S.M., Chong, V.C., Ho, S.C., Noraieni, M., Jillian, O.L.S.<br />

(eds). Marine Science into the New Millennium: New Perspectives & Challenges.<br />

University of Malaya Maritime Research Centre, Kuala Lumpur, Malaysia.<br />

VARAIPPAN, C. S., ANG, M.Y., ONG, C.Y. & PHANG, S.M. 2004. Biologically active<br />

polybrominated indoles in the red alga Laurencia similis from the coastal waters of Sbah<br />

(Rhodomelaceae, Ceramiales). Malaysian J. Sci. 23(2): 119–126.<br />

YAMAGISHI,, Y., MASUDA, M., ABE, T., UWAI, S., KOGAME, K., KAWAGUCHI, S. &<br />

PHANG, S.M. 2003. Taxonomic Notes on Marine Algae from Malaysia. XI. Four Species<br />

of Rhodophyceae. Botanica Marina 46: 534–547.<br />

ZANARDINI, G. 1872. Phycearum indicarum pugillus a CL. Eduardo Beccari ad Borneum,<br />

Singapore et Ceylanum annis. MDCCCLXV-VI-VII cellectarum. Mem. Reale Istituto<br />

Veneto Sci. Let. Art. 17: 129–170.<br />

ZANEVELD, J.S. 1959. The Utilization of Marine Algae in Tropical South and East Asia.<br />

Economic Bot. 13: 89–131.<br />

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STATUS OF BIOLOGICAL DIVERSITY IN MALAYSIA &<br />

THREAT ASSESSMENT OF PLANT SPECIES IN MALAYSIA<br />

TOWARDS THE FLORA OF MALAYSIA<br />

1<br />

L. G. Saw & 2 R. C. K. Chung<br />

ABSTRACT<br />

Malaysia has an estimated 15,000 species of vascular plants (angiosperms, gymnosperms and<br />

pteridophytes). Although located in the Malesian region, its affinity is Sundaic, having common<br />

elements with Sumatra, Java and Palawan. The two halves of Malaysia, Peninsular Malaysia<br />

extending from mainland Asia and East Malaysian states of Sabah and Sarawak on the island<br />

of Borneo have their own distinct floristic components. Peninsular Malaysia has about 8,300<br />

species of vascular plants and Sabah and Sarawak have an estimated 12,000 species. The<br />

Flora of Sabah and Sarawak is generally richer than that of Peninsular Malaysia. For trees, on<br />

the average, Sabah and Sarawak have about 44% more species than Peninsular Malaysia. The<br />

flora of Peninsular Malaysia is better documented that of Sabah and Sarawak. The Flora of<br />

Malaysia project is planned in a phased approach, the approach is taken due to historical<br />

reasons, the different flora affinities between Peninsular Malaysia and Sabah and Sarawak<br />

and perceived resources available for such an endeavour. Peninsular Malaysia has recent<br />

revisions on a number of large families and families of tree species. Until recently, Sabah and<br />

Sarawak do not have specific accounts for the region. The Tree Flora of Sabah and Sarawak<br />

project, initiated in 1991, represents the first systematic modern attempt to document some of<br />

the important plant families of these two states. This project is expected to continue for another<br />

10 years to complete the revision of about 4,000 estimated tree species found in the two states.<br />

The Flora of Peninsular Malaysia project began in 2005 with initial funds from the Malaysian<br />

government for at least the next five years. Upon completion of the Tree Flora of Sabah and<br />

Sarawak project, it is envisage the Flora of Sabah and Sarawak project will only start in about<br />

2015. It is estimated that the Flora of Peninsular Malaysia project will take at least 20 years to<br />

complete (at revision rates of about 400-500 species a year). To achieve such rates, there must<br />

be substantial increase in manpower involvement and fund allocation.<br />

INTRODUCTION<br />

The two geographical halves of Malaysia pose interesting challenges towards documenting<br />

the flora of Malaysia. Peninsular Malaysia or the Malay Peninsula (here includes Singapore<br />

and Peninsular Thailand) contains the floristic elements of the Sunda Self and also of the<br />

mainland Asiatic species from seasonal climates (Wong 1998). Borneo, with its greater isolation<br />

from Malaya, has a flora of Sundaic element; however its flora is quite distinct. Historically,<br />

Forest Research Institute Malaysia, 52109 Kepong, Selangor, Malaysia; 1 sawlg@frim.gov.my; 2 richard@frim.gov.my<br />

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TOWARDS THE FLORA OF MALAYSIA<br />

the two regions followed quite different botanical past. A very brief historical perspective is<br />

provided here, highlighting only the major works that are significance to the flora of these two<br />

regions. A more detail account of the historical works relating to the flora of both Borneo and<br />

Malaya can be obtained from the introductory volumes of the Flora Malesiana volumes (de<br />

Wit 1949, van Steenis-Kruseman 1950, van Steenis 1955). Wong (1987, 1995a) and Soepadmo<br />

(1999) also provided reviews with additional updates from de Wit, van Steenis and van Steenis-<br />

Kruseman of the botanical collection and documentation of the flora of both Peninsular Malaysia<br />

and Borneo.<br />

BOTANICAL HISTORY OF PENINSULAR MALAYSIA<br />

Botanical Collections<br />

Peninsular Malaysia with a more direct former British Colonial rule had a longer and more<br />

sustained period of botanical exploration and enumeration. Its botanical history dates back to<br />

the first British settlement in the early 1800’s in the Malay Peninsula in Penang where the<br />

island was important for the spice trade. Among the very important collectors during this<br />

period include that of N. Wallich whose collection, arranged in a catalogue (Wallich’s<br />

catalogue), included contributions from G. Porter, W. Jack and G. Finlayson. Numbering<br />

about 8,000 species, Wallich’s catalogue became the basis of many plant names for Penang<br />

and Singapore in Malaya, and India. W. Griffith, Wallich’s predecessor, collected large numbers<br />

of specimens particularly from Malacca also form the basis of the foundation of botanical<br />

work in Malaya. Many collectors followed included L. Wray Jr., Father Scortechini, H. Kunstler<br />

(often labelled as King’s Collector), A.C. Maingay, C. Curtis, C.B. Kloss, R. Derry, T. Oxley,<br />

J.S. Goodenough, I.H. Burkill, Mohamad Haniff, N. Cantley, F.W. Foxworthy and etc. A full<br />

listing of these collectors has been summarised by Burkill (1927) with some details of their<br />

background and their collection itineraries can be obtained from van Steenis-Kruseman (1950).<br />

H.N. Ridley’s arrival into Malaya is very significant to Malayan botany. Between 1888 and<br />

1900, he was appointed as Director of Gardens and Forests, Straits Settlements and in 1901-<br />

1912, Director of Gardens, Singapore. Ridley was a man of great ability and he contributed<br />

most significantly towards the botany of Peninsular Malaysia. In his career, he described over<br />

4,200 plant species. He amassed a huge collection amounting to about 50,000 numbers, of<br />

which the main set is in Kew with duplicates in Singapore and other herbaria (van Steenis-<br />

Kruseman 1950). No other collector has amassed such a size of collection for Malaya since.<br />

Subsequent directors and curators of the herbarium at Singapore Botanic Gardens continued<br />

to build upon the foundation set up by Ridley. Of particular importance were the contributions<br />

from I.H. Burkill, M.R Henderson, E.H.J. Corner, R.E. Holttum and C.X. Furtado. All of<br />

them had contributed in exploration, collections and publications, giving us a better<br />

understanding of the flora of Peninsular Malaysia.<br />

At the turn of the twentieth century, A.M. Burn-Murdoch set up a forest herbarium in Kuala<br />

Lumpur, with the aim of producing an account of the commercially important tree species of<br />

Malay Peninsula (Wong 1987). The specimens were collected as reference specimens and<br />

duplicates were submitted to H.N. Ridley for identification. The small herbarium was at the<br />

office of the Conservator of Forests, Strait Settlements and Federated Malay States. His<br />

successor, G.E.S. Cubitt continued with the collection although at a slower rate. In 1916, the<br />

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L.G. SAW & R.C.K. CHUNG (2007)<br />

Wray Herbarium of the Agriculture Department was transferred to the Forest Department in<br />

Kuala Lumpur (Cubitt 1919). In 1918, Cubitt secured the services of F.W. Foxworthy, as the<br />

first Forest Research Officer of the Federated Malay States and Straits Settlements. Under<br />

Foxworthy the herbarium grew quickly. By the end of 1920, the herbarium contained over<br />

6000 numbers (Wong 1987). With the decision to form a Forest Research Institute (FRI), an<br />

area of about 800 acres was acquired at Kepong in 1926 and the main office building was<br />

constructed in 1929 with the herbarium moving into the east wing of the building. C.F.<br />

Symington joined FRI in 1929 and began to assist the running of the herbarium. He contributed<br />

a large collection to the Kepong herbarium in particular the family Dipterocarpaceae on which<br />

he was preparing a foresters’ manual of the important timber family. By the time World War II<br />

broke out in Malaya with J.G. Watson having succeeded Foxworthy, the herbarium had about<br />

43,000 specimens. Unfortunately, during the war many of the specimens were badly damaged<br />

when looters plundered the herbarium. With the internment of the British officers, V.L. Bain,<br />

a Eurasian being exempted from detention was appointed the acting State Forest Officer of<br />

Selangor. He was able to reappoint several local staff members at Kepong. Aziz Budin went<br />

on to restore the damaged collection and attempted to replace some of the lost specimens<br />

either by duplicates or by new collections.<br />

After the war, J. Wyatt-Smith took charged of the herbarium and collection gained momentum.<br />

With the formation of the Federation of Malaya in 1957 and subsequently the Federation of<br />

Malaysia in 1963, the transition towards Malayanisation came into being. K.M. Kochummen<br />

who joined FRI as Assistant Botanist in 1953 subsequently took charge of the herbarium in<br />

1960. In 1964, F.S.P. Ng was recruited as Forest Botanist. By 1965, the collection at FRI<br />

numbered over 74,000 specimens (Wong 1987). In 1965, T.C. Whitmore was engaged under<br />

the Colombo Plan to lead the Tree Flora of Malaya project (Whitmore 1972). In the years<br />

following, Whitmore conducted large collecting expeditions into many parts of Peninsular<br />

Malaysia, many places not collected previously. The Tree Flora project completed its last<br />

volume with the publication of Volume 4 in 1989. By then the herbarium has accumulated<br />

about 130,000 specimens. In 1980, K.M. Wong joined Kochummen managing the FRI<br />

collection. L.G. Saw joined the institute in 1982 as Hill Forest Silviculturist, later in 1985<br />

joined the herbarium to understudy Kochummen as he was to retire. In 1985, the Forest Research<br />

Institute Malaysia (FRIM) was formed as a statutory body from FRI and in the years following;<br />

the mandate of FRIM was to expand beyond forestry related flora research it traditionally<br />

worked on and have now included the study of the total flora of Malaysia. In this much<br />

summarised survey of collections, we have not included many collectors which should be a<br />

subject of much wider review. Later botanists to join the much expanded role of FRIM included<br />

Farah Ghani (deceased), Idris Mohd. Said (have since left), L.S.L. Chua, R.C.K. Chung, Y.Y.<br />

Sam, E. Soepadmo and more recently Ruth Kiew.<br />

Bibliography of the Flora of Peninsular Malaysia<br />

In the following account, we have restricted the discussion to the main floristic publications<br />

that pertain to the flora of the Malay Peninsula. Other incidental accounts of local checklists<br />

and revisions of genera can be obtained from the bibliography found in the general chapter of<br />

Flora Malesiana Volume 5 (van Steenis 1955) and Turner (1997). The Flora of British India<br />

was the first major account covering all the families of Malay Peninsula. The scope of the<br />

volumes was to include plants within the British territories of India, together with those of<br />

Kashmir and Western Tibet, and Malaya (Hooker & Thomson, 1872-1897 in 7 volumes) as<br />

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TOWARDS THE FLORA OF MALAYSIA<br />

part of the British colony. Plants from Borneo however, were not included in the revisions.<br />

Although the Flora of India included treatment of the Flora of Malay Peninsula, it became<br />

apparent that it was not warranted from a phytogeography perspective and the manner of<br />

treatment produced from limited data available at the time had produced an unsatisfactory<br />

revision (de Wit 1949). As a result, G. King (1889), working from the Calcutta Herbarium,<br />

initiated the series Materials for a Flora of the Malayan Peninsula. The revisions, written by<br />

various authors, were originally published as separate papers in the Journal of the Asiatic<br />

Society of Bengal. King and Gamble subsequently compiled these instalments into 4 volumes.<br />

King died after completion of Volume 4 and the work of editorship was passed on to J.S.<br />

Gamble who continued the series to instalment 26 which were compiled into Vol. 5 with the<br />

last instalment published in 1936 (Ng & Jacobs 1983). These volumes however, covered only<br />

the dicotyledonous families and even so, the Urticales viz. Cannabinaceae, Moraceae, Ulmaceae,<br />

Urticaceae and most of the Euphorbiaceae never appeared in print (Ng & Jacobs 1983). H.N.<br />

Ridley (1907) published separately in Singapore in three parts of the Materials for a Flora of<br />

the Malayan Peninsula completing the monocotyledons. These publications were very important<br />

ground-breaking work and they become the basis for subsequent work on the Flora of the<br />

Malayan Peninsula. Using the Materials as foundation for the Flora of the Malay Peninsula,<br />

Ridley upon his retirement completed the Flora of Malay Peninsula and published them in 5<br />

volumes between 1922 and 1925 (Ridley 1922-1925) for the angiosperms and a separate final<br />

fern instalment in 1926 (Ridley 1926).<br />

Following Ridley’s publication of the Flora of Malay Peninsula, botanical work continued in<br />

more detail and from different perspectives. I.H. Burkill (1935), succeeding Ridley,<br />

subsequently produced two volumes of A Dictionary of the Economic Products of the Malay<br />

Peninsula. Other important publications from Singapore included E.H.J. Corner’s (1940)<br />

Wayside Trees of Malaya, M.R. Henderson’s (1959, 1974) Malayan Wild Flowers. By the<br />

1950s, a revised Flora of Malaya was initiated as knowledge of the Malayan flora improved<br />

with more explorations and collections. A number of publications followed, mainly by Holttum<br />

(Zingiberaceae (1950), Marantaceae (1951), bamboos (1958), orchids (1964) and ferns (1968)).<br />

The volume on grasses was published by Gilliland (1971). With the move of interest away<br />

from floristic work in the 1970s in Malaysia and Singapore, the revised Flora of Malaya was<br />

more or less discontinued. Piggott (1988) produced a popular photographic account for ferns.<br />

The orchid flora was again subjected to another revision in 1992 by Seidenfaden & Wood.<br />

Turner (1997) collated a checklist of Peninsular Malaysian flora based on literature. More<br />

recently, Clarke (2001) published the Nepenthes of Sumatra and Peninsular Malaysia and<br />

Kiew (2005) revised the Begonias of Peninsular Malaysia in richly illustrated volumes.<br />

At the Forest Research Institute at Kepong, interest was towards tree species and identification<br />

manuals for foresters for the more important timber tree families and other minor forest products.<br />

Burn-Murdoch (1911, 1912) initiated the first publications of such foresters’ manual with the<br />

publication of the Trees and Timbers of the Malay Peninsula. The Malayan Forest Records<br />

series was started and Foxworthy published a number of volumes on commercial timbers and<br />

minor forest products (Foxworthy 1921, 1922, 1932). In 1934, C.F. Symington was appointed<br />

the first Forest Botanist and he envisaged producing a foresters’ tree manual comprising all<br />

the Malayan timber-producing families. However, it was obvious that much research was still<br />

required and that a great deal of instability still existed in the botanical nomenclature. He then<br />

concentrated on the most important timber family, the Dipterocarpaceae, which he completed<br />

in 1940 and was published as the Foresters’ Manual of Dipterocarps in 1943 in his absence<br />

(Symington 1943).<br />

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L.G. SAW & R.C.K. CHUNG (2007)<br />

After the War, John Wyatt-Smith served as Forest Botanist. Wyatt-Smith also saw the<br />

importance of Symington’s work and the need to document similar information on timber<br />

trees of other families. However, it became evident also that the botanical knowledge of the<br />

many non-Dipterocarps was inadequate for a similar treatment. In the interim, Wyatt-Smith<br />

(1952) produced a booklet listing out the more common timber species found in Malaya that<br />

is used by staff of the Forest Department as an identification tool for the common timber<br />

species (Pocket Check List of Timber Trees). K.M. Kochummen subsequently revised this<br />

“Pocket Check List” three times to include new information. The Pocket Check List has now<br />

become an important identification reference for students of the common Peninsular Malaysian<br />

timber species. Wyatt-Smith also produced a series of other more taxonomic publications on<br />

some of the important timber families (e.g., Burseraceae (Wyatt-Smith 1953a), Leguminosae<br />

(Wyatt-Smith 1953b), Myristicaceae (Wyatt-Smith 1953c), Sapotaceae (Wyatt-Smith 1954a),<br />

Lauraceae (Wyatt-Smith 1954b) and Sapindaceae (Wyatt-Smith 1954c), and the genus<br />

Calophyllum (Guttiferae) (Henderson & Wyatt-Smith 1956)).<br />

The Tree Flora of Malaya project under T.C. Whitmore as editor published two volumes<br />

(Whitmore 1972, 1973) followed by another two volumes with F.S.P. Ng (1978, 1989) as<br />

editor. The final four volumes covered over 2,800 species of trees found in Malaya. Interests<br />

in the non-timber but commercially important groups resulted in the production of J.<br />

Dransfield’s (1979) A manual of the rattans of the Malay Peninsula and K.M. Wong’s (1995b)<br />

The bamboos of Peninsular Malaysia.<br />

BOTANICAL HISTORY OF SABAH AND SARAWAK<br />

(AND BORNEO)<br />

Sabah and Sarawak lack the collection intensity of Malaya in the early years. However, in<br />

recent years both herbaria at the Forest Research Centres of Sandakan and Kuching have<br />

added much to their collections. Wong (1995a) has amply summarised the collection history<br />

and bibliography of Bornean flora in the introductory chapters of the Tree Flora of Sabah and<br />

Sarawak Volume 1. We shall not elaborate further here. Suffice to add since that review, the<br />

Tree Flora of Sabah and Sarawak has since published five volumes (Soepadmo & Wong<br />

1995, Soepadmo et al. 1996, Soepadmo & Saw 2000, Soepadmo et al. 2002, 2004). The<br />

Plants of Kinabalu project led by Beaman and his collaborators completed the project with the<br />

publication of five volumes of the series (Parris et al. 1992, Wood et al. 1993, Beaman &<br />

Beaman 1998, Beaman et al. 2001, Beaman & Anderson 2004). Modern identification manuals,<br />

amounting to floristic enumerations, of the rattans of Sabah and Sarawak (J. Dransfield 1984,<br />

1992), and the bamboos of Sabah (S. Dransfield 1992) have been published. More charismatic<br />

groups such as orchids and Nepenthes continue to attract interest with a checklist of the Orchids<br />

of Borneo (Wood & Cribb 1994), Slipper Orchids of Borneo (Cribb 1997) and the Orchids of<br />

Borneo (Beaman et al. 2001), and Nepenthes of Borneo (Clarke 1997) produced. A richly<br />

illustrated Etlingera (Zingiberaceae) of Borneo was also recently published (Poulsen 2006).<br />

THE FLORA OF MALAYSIA – WHAT DO WE KNOW?<br />

Currently there is no comprehensive checklist for the flora of Malaysia. A number of checklists<br />

exist as a result of the different botanical history of the two main regions of Malaysia. For<br />

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TOWARDS THE FLORA OF MALAYSIA<br />

Peninsular Malaysia, the work of Ridley (1922-1926) provided the first complete enumeration<br />

of the vascular plants of the Flora of Malay Peninsula; the angiosperms were published in the<br />

five volumes between 1922 and 1925. Subsequently, Ridley published a separate checklist of<br />

the ferns (Ridley 1926). Ridley’s enumeration by now has become outdated; Turner’s (1997)<br />

publication of “A Catalogue of the Vascular Plants of Malaya” serves as the most recent<br />

checklist based on existing literature survey. In this catalogue Turner enumerated 8,198 species<br />

(Table 1). Parris & Latiff (1997) published a further update on the ferns and fern allies with<br />

some additions and nomenclatural changes to the group (Table 2). In this checklist, ferns and<br />

fern allies of Sabah and Sarawak were included to provide the first complete checklist of the<br />

group for Malaysia.<br />

Table 1. Summary of the checklist of the flora of Peninsular Malaysia comparing Ridley’s<br />

(1922-1925, 1926) enumeration and Turner’s (1997) catalogue<br />

Enumeration Groups Families Genera Species<br />

Ridley (1922-1925, 1926) Ferns 16 86 417<br />

Gymnosperms 3 5 23<br />

Dicots 132 1,048 5,009<br />

Monocots 31 354 1,734<br />

Total 182 1,493 7,183<br />

Turner (1997) Ferns & fern allies 34 133 632<br />

Gymnosperms 4 8 27<br />

Dicots 165 1,092 5,529<br />

Monocots 45 418 2,010<br />

Total 248 1,651 8,198<br />

Table 2. Ferns and fern allies checklist enumerated in 1997 (Parris & Latiff 1997)<br />

Region<br />

Species Total<br />

Malay Peninsula 647<br />

Sabah 750<br />

Sarawak 615<br />

Total 1,165<br />

For Sabah and Sarawak, no checklist exists but two important compilations were made for<br />

Borneo (Merrill 1921, Masamune 1942, 1945). Masamune’s compilations provided a more<br />

critical checklist and in that enumeration, 8,164 species of Bornean vascular plants were listed<br />

(Table 3). Other and more current accounts for flora of Borneo were mostly foresters’ manuals<br />

and checklists often on selected groups in the region or states of Brunei, Kalimantan, Sabah<br />

and Sarawak (e.g. Anderson 1980, Argent et al. 1997, Ashton 1964, 1968, 1988, Browne<br />

1955, Burgess 1966, Cockburn 1976, 1980, Hasan & Ashton 1964, Keith 1947, Kessler &<br />

Sidiyasa 1994, Newman et al. 1996, Primack 1983, Smythies 1965, Whitmore et al. 1990a,<br />

1990b, 1990c, Wood & Agama 1956, Wood & Meijer 1964). The other checklists and revisions<br />

have been reviewed in the previous section. The launch of the Tree Flora of Sabah and Sarawak<br />

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L.G. SAW & R.C.K. CHUNG (2007)<br />

Table 3. Summary of the flora of Borneo based on Masamune’s checklist<br />

Checklists Groups Families Genera Species<br />

Masamune (1945) Ferns & fern allies 118 963<br />

Masamune (1942) Gymnosperms 5 7 34<br />

Dicots 133 996 4,997<br />

Monocots 29 307 2,170<br />

Total 167 1,428 8,164<br />

in 1991 was very significant as it was for the first time, a modern floristic approach was used<br />

in a systematic fashion to enumerate the trees species (Soepadmo & Wong 1995). Apart from<br />

these enumerations, the other sources of information on the flora of Malaysia are from the<br />

Flora Malesiana Series I & II for seed plants and ferns and other scattered publications.<br />

Based upon the above discussion, the flora for Peninsular Malaysia now stands over 8,300<br />

species with recent updates from Turner (1997) (e.g., Turner 2000, Latiff & Turner 2001a,<br />

2001b, 2001c, 2001d, 2002a, 2002b, 2003, Kamarudin & Turner 2004). This is a relatively<br />

accurate estimate and provides a relatively good understanding of the actual flora for Peninsular<br />

Malaysia. For Sabah and Sarawak, however, it is more difficult to arrive at an accurate figure.<br />

Most estimates are for Borneo (e.g. Merrill (1921) estimated about 9,000 species, Masamune<br />

(1942, 1945) enumerated about 8,200 species and more recently Wong (1995a) estimated a<br />

flora of between Merrill’s 9,000 and 15,000 species). Kiew (1984) stressed the urgency for<br />

the Bornean flora where at the time of her review, no singular project has been initiated for<br />

Borneo. As mentioned earlier, the Tree Flora of Sabah and Sarawak is the most important<br />

modern taxonomic project for Borneo. Since its inception in 1991, five volumes have been<br />

published and the estimation based on the revision from volumes 1 to 5 provides an indication<br />

of the diversity of the Bornean flora. Table 4 provides a comparison of the Tree Flora of Sabah<br />

and Sarawak with the Flora of Malaya comparing similar families and their enumeration.<br />

Table 4. Comparing revisions of similar families of the Tree Flora of Sabah and Sarawak with<br />

the Tree Flora of Malaya (figures for Tree Flora of Sabah and Sarawak were extracted from<br />

volumes 1–5 included 2 single-species families not found in the Tree Flora of Malaya; figures<br />

for Tree Flora of Malaya volumes 1-4 with updates from Turner (1997))<br />

TFSS Tree Flora of Sabah & Tree Flora of Malaya Species<br />

Volumes Sarawak common to<br />

Families Genera Species Families Genera Species both regions<br />

1 31 99 312 31 91 227 152<br />

2 23 75 247 21 63 186 116<br />

3 4 29 358 4 27 246 139<br />

4 6 21 292 6 21 202 106<br />

5 4 25 361 4 27 225 132<br />

Total 68 249 1,570 66 229 1,086 645<br />

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TOWARDS THE FLORA OF MALAYSIA<br />

On the average, the Tree Flora of Sabah and Sarawak contained about 44.5% more species<br />

than the Tree Flora of Malaya. If this proportion is maintained for the rest of the tree flora,<br />

then with the Tree Flora of Malaya having 2,830 species (Ng et al. 1990), it is estimated that<br />

the Tree Flora of Sabah and Sarawak will contain just over 4,000 species. Based upon this<br />

estimation also, with about 8,300 species of vascular plants in Peninsular Malaysia, it is<br />

estimated that the Flora of Sabah and Sarawak will contain about 12,000 species. In the table<br />

above, we have also included in the count, 645 species in the revisions that are common to<br />

both Sabah and Sarawak, and Peninsular Malaysia, i.e., 59.4% overlap. Based upon this overlap<br />

and using the estimated ratios we have worked out earlier, the total tree flora of Malaysia<br />

should be just over 5,200 species and estimated total flora of vascular plants of Malaysia will<br />

be just over 15,300 species.<br />

HERBARIA, COLLECTIONS AND SPECIMENS<br />

Specimens are essential in the documentation of the flora of Malaysia. Today, the collection at<br />

the herbarium of Forest Research Institute Malaysia (KEP) stands about 300,000 specimens.<br />

The other large herbarium holdings include the Forest Research Centre at Sandakan (SAN)<br />

with 253,725 specimens and the Forest Research Centre at Kuching (SAR) with about 250,000<br />

specimens (Table 5). Other important Malaysian collections are found at the herbaria at<br />

Universiti Malaya (KLU) and Universiti Kebangsaan Malaysia (UKMB). The herbarium at<br />

the Singapore Botanic Gardens (SING) is particularly very important for the Peninsular<br />

Malaysian flora. Many type specimens for plants described from Peninsular Malaysia are<br />

found there. It has about 650,000 specimens. Other important collections for the Malaysian<br />

flora include The Forest Herbarium (BKF), Bangkok, Thailand, National Herbarium of<br />

Netherlands, Leiden (L), Royal Botanic Gardens, Kew (K), Royal Botanic Gardens, Edinburgh<br />

(E), UK, Arnold Arboretum (A), Harvard University, USA, and Central National Herbarium<br />

(CAL), Calcutta, India. For Sabah and Sarawak, the Herbarium Beccarianum (FI-B), Florence,<br />

Italy is particularly important for Beccari’s collection and the herbarium of Brunei Forest<br />

Department (BRUN).<br />

Table 5. Important herbarium holdings for Malaysia and Singapore<br />

Country Institutions Specimens<br />

Malaysia Forest Research Institute Malaysia 300,000<br />

Forest Research Centre, Sandakan, Sabah 253,725<br />

Forest Research Centre, Kuching, Sarawak 250,000<br />

Universiti Malaya 65,000<br />

Universiti Kebangsaan Malaysia 72,000<br />

Singapore Singapore Botanic Gardens 650,000<br />

STATE OF KNOWLEDGE FOR A FLORA OF MALAYSIA<br />

Among the key resources to speeding up the documentation of a flora of Malaysia is the<br />

availability of recent revisions that may set the foundation for the flora writing. The vascular<br />

flora of Malaysia will include 250 families in Peninsular Malaysia and 253 families in Sabah<br />

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L.G. SAW & R.C.K. CHUNG (2007)<br />

and Sarawak. In working towards the flora of Malaysia, we have continued to separate the<br />

two regions for the purpose of further analysis, simply out of convenience from the historical<br />

perspective and also a general tendency in many revisions to maintain the two regions as<br />

separate. We have compiled a review of recently published revisions against these families<br />

that included the floras of Peninsular Malaysia (Malaya) and of Sabah and Sarawak (Borneo).<br />

The recent revisions include publications from the Flora Malesiana series, Tree Flora of Malaya,<br />

the revised Flora of Malaya, Tree Flora of Sabah and Sarawak, and other journal articles or<br />

series covering revisions of the whole family in the list. In the analysis, out of the 250 families<br />

occurring in Peninsular Malaysia, 207 families (83%) have recent revisions. This is a very<br />

good coverage. For Sabah and Sarawak or Borneo, the coverage is much lower, 164 families<br />

out of 253 occurring there or about 64%. In recent years, world checklists are being generated<br />

and these are being made available in the internet, for example, the checklists available from<br />

Royal Botanic Gardens, Kew (www.kew.org/wcb/), where the monocots are now available<br />

for downloading. Such checklists can certainly provide an initial update especially for Borneo<br />

where existing list by Masamune (1942, 1945) has long become obsolete.<br />

TOWARDS A FLORA OF MALAYSIA<br />

In the last decade and half, Malaysia has been very fortunate in terms of the resources available<br />

to document its floristic diversity. The Tree Flora of Malaya published its final volume in<br />

1989 (Ng 1989). In 1990, it became apparent that the botanical work of documenting the flora<br />

of Malaysia should continue and it was an obvious decision to continue the well tested formula<br />

of the Tree Flora of Malaya to be extended to Sabah and Sarawak. The first author was then<br />

delegated to prepare proposals for funding towards a Tree Flora of Sabah and Sarawak project.<br />

The project was launched in 1991 for first five years with funding from the Malaysian<br />

Government, the Overseas Development Administration (ODA) of the United Kingdom and<br />

the International Tropical Timber Organisation (ITTO). It was originally estimated that the<br />

project will run for ten years to cover about 3,000 species (Soepadmo 1995) in eight volumes.<br />

Having completed five volumes of the tree flora, with the current estimate of about 4,000<br />

species of trees, we envisage that the Tree Flora of Sabah and Sarawak will need at least<br />

another ten years to complete the remaining estimated 2,500 species at a revision rate of about<br />

250 species per year using present resources.<br />

In realising the Flora of Malaysia, a pragmatic approach is to review our existing commitment<br />

towards the Tree Flora of Sabah and Sarawak project and how else can we extend into a full<br />

national flora project. The institutions currently engaged in the Tree Flora of Sabah and Sarawak,<br />

i.e. the Forest Research Institute Malaysia, and the Forest Departments of Sabah and Sarawak<br />

would want to complete the Tree Flora project. The review of species distribution and literature<br />

provided above also provide an indication that the Flora of Malaysia can be completed in a<br />

phase approach. In this pragmatic approach, the Flora of Malaysia can be tackled as two<br />

regional projects, revisions for Peninsular Malaysia and for Sabah and Sarawak. And it is this<br />

approach that we have taken towards plans to realise the Flora of Malaysia. In April 2004, the<br />

Ministry of Natural Resources and Environment was formed. With the creation of the ministry,<br />

it became of national priority that the government was committed to document the biodiversity<br />

of the country. The work of documenting the flora of Malaysia became very quickly a national<br />

need and no more an academic wish-list for botanists in Malaysia. For the immediate use, the<br />

country requires a checklist of its flora, as Peninsular Malaysia has already a checklist; the<br />

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TOWARDS THE FLORA OF MALAYSIA<br />

immediate need was for Sabah and Sarawak to have an updated list. Under the Ninth Malaysian<br />

Plan, a project was prepared just to meet this need.<br />

In 2005, plans were drawn for a Flora of Peninsular Malaysia project. It was thought that the<br />

time was ripe for the project. The Tree Flora of Sabah and Sarawak has already been running<br />

well for about 15 years and Peninsular Malaysia since the Tree Flora of Sabah and Sarawak<br />

project started has been relatively neglected. Furthermore, as explained earlier, a phase approach<br />

to realise the Flora of Malaysia was a very viable option for Malaysia. Following the proposal,<br />

the Flora of Peninsular Malaysia received funding at the end of 2005 for the next five years.<br />

For Sabah and Sarawak, we reckon when the Tree Flora of Sabah and Sarawak project is<br />

completed, attempts will be made to start the Flora of Sabah and Sarawak project.<br />

COLLABORATIONS, CONTRIBUTORS AND RATES OF REVISION<br />

Flora projects are always collaborative involving both local and foreign experts. The<br />

experiences from both the Tree Flora of Malaya and Tree Flora of Sabah and Sarawak projects<br />

have shown that contributions from experts are essential to their success. Experts often produce<br />

revisions at much faster pace. At the same time, local botanists must be trained to form expertise<br />

that can continue with the work within the country. Such strategy must be used for a Flora of<br />

Malaysia. Currently, Tree Flora of Sabah and Sarawak and the new Flora of Peninsular Malaysia<br />

are also using such strategy. Collaborations are at different levels, at institutional level, our<br />

traditional partners include local partners such as Forest Research Centre, Sandakan, Forest<br />

Research Centre, Kuching, Universiti Malaya, Universiti Kebangsaan Malaysia, Universiti<br />

Malaysia Sarawak, Universiti Malaysia Sabah; regional herbaria include Singapore Botanic<br />

Gardens and the Royal Forest Herbarium, Bangkok; internationally the Royal Botanic Gardens<br />

Kew, Royal Botanic Gardens Edinburgh, Natural History Museum, London, National<br />

Herbarium of Netherlands, Leiden, and Arnold Arboretum, Harvard University, USA. The<br />

collaborating institutes are important to support herbarium specimen loans, sourcing of<br />

literature, provide base for specimen consultations and taxonomic expertise. From these<br />

institutions, the current projects have over 25 collaborators promising to contribute to the<br />

revisions of the families.<br />

To develop and build local expertise, two essential elements must be in place; opportunities to<br />

build careers in botanical sciences and availability of training regimes for those interested.<br />

The Flora of Peninsular Malaysia project when it was mooted included these elements. We are<br />

also very fortunate that in the last few years, the Forest Research Institute Malaysia has<br />

committed to increase the number of botanists to do floristic work. In the last two years,<br />

FRIM has recruited five new botanists and took in eight contract researchers for the two<br />

projects. Together with existing staff, FRIM now has 18 botanists working on both these<br />

projects. Training of these new and aspiring botanists have become a very important element<br />

of the projects together with getting the revisions done. We are confident if the current<br />

institutional and financial supports are maintained, both the Tree Flora of Sabah and Sarawak<br />

and the Flora of Peninsular Malaysia projects will be successful and will produce not just the<br />

revisions that contributes towards a Flora of Malaysia but also ensure that Malaysia will<br />

maintain a pool of botanists trained in understanding the local flora.<br />

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L.G. SAW & R.C.K. CHUNG (2007)<br />

How many years will it take for the current flora projects to complete? It is very important that<br />

in planning towards a Flora of Malaysia, we have realistic estimation and projection of<br />

manpower and financial layout. The Tree Flora of Malaya took 24 years to complete. Kiew<br />

(1984) made some projections on the rate of revisions botanists takes in producing the different<br />

types of floras (identification and information floras) based from past flora projects. They<br />

ranged from 250 species per taxonomist per year to 20-30 per year. Based upon our experience<br />

with the Tree Flora of Sabah and Sarawak, we have estimated the rate of revision using a fulltime<br />

experienced botanist as an example. We have taken the example of the late Mr. K.M.<br />

Kochummen who worked with the Tree Flora of Sabah and Sarawak project. During his tenure<br />

with the project, Kochummen revised five families covering 375 species (Table 6) from 1992<br />

to March 1999. This gave a rate of about 54 species per year for the seven years he was with<br />

the project.<br />

Table 6. Families revised by K.M. Kochummen (1992–March 1999) during his tenure with<br />

the Tree Flora of Sabah and Sarawak project<br />

Families Genera Species<br />

Anacardiaceae 17 92<br />

Burseraceae 8 59<br />

Celestraceae 10 44<br />

Moraceae 5 173<br />

Ochnaceae 5 7<br />

Total 45 375<br />

For the Flora of Peninsular Malaysia, Table 7 provides the different rates of revision against<br />

the number of full-time staff working on the flora revisions. The matrix estimates the number<br />

of years needed to complete the Flora of Peninsular Malaysia with the estimated flora of 8,300<br />

species. Using the example of Kochummen, we estimated that for a budding botanist, it would<br />

be very difficult to maintain a revision of over 50 species per year. A more realistic figure of<br />

about 40 species may be feasible for a relatively grounded botanist. If our current manpower<br />

strength is maintained with about 10 full-time botanists working for the project, we envisage<br />

that it will take just over twenty years to complete the Flora of Peninsular Malaysia. This<br />

estimate ignores the contributions from other collaborators.<br />

Table 7. Rate of revision based on about 8,300 species of vascular for the Flora of Peninsular<br />

Malaysia<br />

Number of Full-time Staff<br />

5 10 15 20<br />

Revision 20 83 42 28 21<br />

Rates/ 30 55 28 18 14<br />

Staff/ 40 42 21 14 10<br />

Year 50 33 17 11 8.3<br />

60 28 14 9.2 6.9<br />

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For the Tree Flora of Sabah and Sarawak we have also worked out the rates using similar<br />

formulation (Table 8). The project with 5 full-time staff will take over twelve years to complete.<br />

Table 8. Revision rates based on about 2,500 species of tree species for the Tree Flora of<br />

Sabah and Sarawak<br />

Number of Full-time Staff<br />

5 10 15 20<br />

Revision 20 25 12.5 8.3 6.3<br />

Rates/ 30 16.7 8.3 5.6 4.2<br />

Staff/ 40 12.5 6.3 4.2 3.1<br />

Year 50 10 5 3.3 2.5<br />

60 8.3 4.2 2.8 2.1<br />

FINANCES AND INSTITUTIONAL COMMITMENT<br />

One of the constant challenges in any flora project is to ensure long-term commitment and<br />

sustainability in funding for the continuity of project. Projects are financed in fixed timeframe,<br />

e.g., it is fortunate that we have funding for 5 years for the Flora of Peninsular Malaysia.<br />

Following which it is often difficult to obtain extension. The Tree Flora of Sabah and Sarawak<br />

project went through a number of funding changes over the last 15 years — ODA, ITTO,<br />

Government of Malaysia until 2006 (Intensification of Research and Development Priority<br />

Areas (IRPA) funding), the IRPA funding ceased in 2006 and from then on, the project is<br />

dependent on research development fund from the Ninth Malaysian Plan for the next five<br />

years. In future, we are not certain how we can continue but it is up to the project to develop<br />

different ways to maintain the funding continuity. It is therefore important that such a project<br />

must have strong institutional commitment, failing which it would be almost impossible to<br />

secure continuity in finances and manpower commitment. Similarly, we expect the Flora of<br />

Peninsular Malaysia to go through different funding challenges as the project develops. We<br />

are fortunate that for the first five years we have quite generous funding coming from IRPA.<br />

It is essential funding bodies would want to see good products from the project. There is a<br />

need to be creative in selling the products from the project outside the standard flora volumes<br />

which projects like this deliver. More innovative methods must be used to make the results of<br />

the projects become pertinent or relevant to both national and scientific needs.<br />

The Tree Flora of Sabah and Sarawak now has produced five volumes, FRIM is currently<br />

making information from the project available in the internet thus disseminating the results of<br />

the project to the wider public. The Flora of Peninsular Malaysia is being implemented together<br />

with a conservation project of threatened plants of Peninsular Malaysia, thus extending the<br />

taxon information with distribution to be used in conservation.<br />

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L.G. SAW & R.C.K. CHUNG (2007)<br />

CONCLUSION<br />

Based upon the discussion above, the phase approach towards a Flora of Malaysia and the<br />

following points are reiterated.<br />

• The inventory for a Flora of Malaysia can be done with resources in Malaysia and<br />

collaboration with our traditional partners;<br />

• Based on current Tree Flora of Sabah and Sarawak and the Flora of Peninsular Malaysia<br />

projects, the Flora of Malaysia to continue with the geographical division of Peninsular<br />

Malaysia and Sabah & Sarawak;<br />

• The project to be phased into the immediate short-term needs (checklists) and revisions<br />

of the two geographical floras; and<br />

• Project must be seen as long-term and requires long-term institutional and financial<br />

commitments.<br />

REFERENCES<br />

ANDERSON, J.A.R. 1980. A Checklist of the Trees of Sarawak. Forest Department, Sarawak.<br />

364 pp.<br />

ARGENT, G., CAMPBELL, E.J.F. & WILKIE, P. (eds.). 1997. Manual of the Larger and<br />

More Important Non-Dipterocarp Trees of Central Kalimantan, Indonesia. Volumes 1 &<br />

2. Forest Research Institute, Samarinda, Indonesia. 685 pp.<br />

ASHTON, P.S. 1964. Manual of Dipterocarp Trees of Brunei State. Oxford University Press,<br />

London. 242 pp.<br />

ASHTON, P.S. 1968. A Manual of the Dipterocarp Trees of Brunei State and of Sarawak.<br />

Borneo Literature Bureau for Sarawak Forest Department, Kuching. 129 pp.<br />

ASHTON, P.S. 1988. Manual of the Non-Dipterocarp Trees of Sarawak. Volume 2. Dewan<br />

Bahasa dan Pustaka for Forest Department Sarawak, Kuching. 490 pp.<br />

BEAMAN, J.H. & ANDERSON, C. 2004. The Plants of Mount Kinabalu 5. Dicotyledon<br />

Families Magnoliaceae to Winteraceae. Natural History Publications (Borneo) in<br />

association with Royal Botanic Gardens, Kew. 609 pp.<br />

BEAMAN, J.H. & BEAMAN, R.S. 1998. The Plants of Mount Kinabalu 3. Gymnosperm and<br />

Non-Orchid Monocotyledons. Natural History Publications (Borneo) in association with<br />

Royal Botanic Gardens, Kew. 220 pp.<br />

BEAMAN, J.H., ANDERSON, C. & BEAMAN, R.S. 2001. The Plants of Mount Kinabalu 4.<br />

Dicotyledon Families Acanthaceae to Lythraceae. Natural History Publications (Borneo)<br />

in association with Royal Botanic Gardens, Kew. 570 pp.<br />

BEAMAN, T.E., WOOD, J.J., BEAMAN, R.S. & BEAMAN, J.H. 2001. Orchids of Borneo.<br />

Natural History Publications (Borneo) in association with Royal Botanic Gardens, Kew.<br />

584 pp.<br />

BROWNE, F.G. 1955. Forest trees of Sarawak and Brunei. Government Press, Sarawak. 369<br />

pp.<br />

BURN-MURDOCH, A.M. 1911. Trees and timbers of the Malay Peninsula, Part 1. F.M.S.<br />

Government Press. Kuala Lumpur.<br />

BURN-MURDOCH, A.M. 1912. Trees and timbers of the Malay Peninsula, Part 2. F.M.S.<br />

Government Press. Kuala Lumpur.<br />

223


TOWARDS THE FLORA OF MALAYSIA<br />

BURGESS, P.F. 1966. Timbers of Sabah. Sabah Forest Records No. 6. Forest Department,<br />

Sabah. 511 pp.<br />

BURKILL, I.H. 1927. Botanical collectors, collections and collecting places in the Malay<br />

Peninsula. The Gardens’ Bulletin, Straits Settlements 4 (4 & 5): 113–202.<br />

BURKILL, I.H. 1935. A dictionary of the economic products of the Malay Peninsula. Vols. 1<br />

& 2. Governments of the Straits Settlements and Federated Malay States.<br />

CLARKE, C.C. 1997. Nepenthes of Borneo. Natural History Publications, Kota Kinabalu and<br />

Science and Technology Unit, Sabah. 209 pp.<br />

CLARKE, C.C. 2001. Nepenthes of Sumatra and Peninsular Malaysia. Natural History<br />

Publications (Borneo). 329 pp.<br />

COCKBURN, P.F. 1976. Trees of Sabah. Volume 1. Sabah Forest Records No. 10. Forest<br />

Department Sabah. 261 pp.<br />

COCKBURN, P.F. 1980. Trees of Sabah. Volume 2. Sabah Forest Records No. 10. Forest<br />

Department Sabah. 124 pp.<br />

CORNER, E.J.H. 1940. Wayside Trees of Malaya. 2 Volumes United Selangor Press, Kuala<br />

Lumpur.<br />

CUBITT, G.E.S. 1919. Report on forest administration for the year 1918. Federated Malay<br />

States. F.M.S. Government Press. Kuala Lumpur.<br />

CRIBB, P.J. 1997. Slipper orchids of Borneo. Natural History Publications, Kota Kinabalu.<br />

DE WIT, H.C.D. 1949. History of Malaysian phytography. Flora Malesiana I(4): LXXI-CLXI.<br />

DRANSFIELD, J. 1979. A manual of the rattans of the Malay Peninsula. Malayan Forest<br />

Records 29. Forest Department, West Malaysia. 270 pp.<br />

DRANSFIELD, J. 1984. The rattans of Sabah. Sabah Forest Records 13. Forest Department<br />

Sabah. 87 pp.<br />

DRANSFIELD, J. 1992. The rattans of Sarawak. Royal Botanic Gardens, Kew & Sarawak<br />

Forest Department. 233 pp.<br />

DRANSFIELD, S. 1992. The bamboos of Sabah. Sabah Forest Records No. 14. Royal Botanic<br />

Gardens, Kew & Forestry Department Sabah. 94 pp.<br />

FOXWORTHY, F.W. 1921. The commercial woods of the Malay Peninsula. Malayan Forest<br />

Records 1. Forest Department, Federated Malay States Government.<br />

FOXWORTHY, F.W. 1922. Minor forest products of the Malay Peninsula. Malayan Forest<br />

Records 2. Forest Department, Federated Malay States Government.<br />

FOXWORTHY, F.W. 1932. Dipterocarpaceae of the Malay Peninsula. Malayan Forest Records<br />

10. Federated Malay States Government.<br />

GILLILAND, H.B. 1971. A revised flora of Malaya. Volume 3. Grasses of Malaya. Botanic<br />

Gardens, Singapore. 319 pp.<br />

HASAN, P. & ASHTON. P.S. 1964. A checklist of Brunei trees. 132 pp.<br />

HENDERSON, M.R. 1959. Malayan Wild Flowers, Dicotyledons. Caxton Press Ltd., Kuala<br />

Lumpur.<br />

HENDERSON, M.R. 1974. Malayan Wild Flowers, Monocotyledons. Art Printing Works,<br />

Kuala Lumpur.<br />

HENDERSON, M.R. & WYATT-SMITH, J. 1956. Calophyllum Linn. The Gardens’ Bulletin<br />

Singapore 15: 375.<br />

HOLTTUM, R.E. 1950. The Zingiberaceae of the Malay Peninsula. The Gardens’ Bulletin<br />

Singapore 13: 1–250.<br />

HOLTTUM, R.E. 1951. The Marantaceae of Malaya. The Gardens’ Bulletin, Singapore 13:<br />

254–296.<br />

224


L.G. SAW & R.C.K. CHUNG (2007)<br />

HOLTTUM, R.E. 1958. The bamboos of the Malay Peninsula. The Gardens’ Bulletin Singapore<br />

16: 1–135.<br />

HOLTTUM, R.E. 1964. A revised flora of Malaya. Volume 1. Orchids of Malaya. Botanic<br />

Gardens, Singapore. 759 pp.<br />

HOLTTUM, R.E. 1968. A revised flora of Malaya. Volume 2. Ferns of Malaya. Botanic Gardens,<br />

Singapore. 653 p.<br />

HOOKER & THOMSON. 1872–1897. Flora of India. Volumes 1–7.<br />

KAMARUDIN, M.S. & TURNER, I.M. 2004. Quarterly notes: New taxa and records of<br />

Malaysian vascular plants. Folia malaysiana 5(1): 65–68.<br />

KESSLER, P.J.A. & SIDIYASA, K. 1994. Trees of the Balikpapan-Samarinda area, East<br />

Kalimantan, Indonesia. Tropenbos Series 7. The Tropenbos Foundation, Wageningen,<br />

The Netherlands. 446 pp.<br />

KIETH, H.G. 1947. The timbers of North Borneo. North Borneo Forest Records No. 3.<br />

Government of the Colony of North Borneo. 154 pp.<br />

KIEW, R. 1984. Towards a flora of Borneo. Pp. 73–80 in Ismail Sahid et al. (eds.), Research<br />

Priorities in Malaysian Biology. Universiti Kebangsaan Malaysia.<br />

KIEW, R. 2005. Begonias of Peninsular Malaysia. Natural History Publications (Borneo),<br />

Kota Kinabalu. 308 pp.<br />

KING, G. 1889. Materials for a Flora of the Malayan Peninsula. Journal of the Asiatic Society<br />

of Bengal 58: 359–408.<br />

LATIFF, A. & TURNER, I.M. 2001a. Quarterly notes: New taxa and records of Malaysian<br />

vascular plants. Folia malaysiana 2(1): 54–56.<br />

LATIFF, A. & TURNER, I.M. 2001b. Quarterly notes: New taxa and records of Malaysian<br />

vascular plants. Folia malaysiana 2(2): 127–128.<br />

LATIFF, A. & TURNER, I.M. 2001c. Quarterly notes: New taxa and records of Malaysian<br />

vascular plants. Folia malaysiana 2(3): 203–206.<br />

LATIFF, A. & TURNER, I.M. 2001d. Quarterly notes: New taxa and records of Malaysian<br />

vascular plants. Folia malaysiana 2(4): 283–284<br />

LATIFF, A. & TURNER, I.M. 2002a. Quarterly notes: New taxa and records of Malaysian<br />

vascular plants. Folia malaysiana 3(1): 67–68.<br />

LATIFF, A. & TURNER, I.M. 2002b. Quarterly notes: New taxa and records of Malaysian<br />

vascular plants. Folia malaysiana 4(2): 129–132<br />

LATIFF, A. & TURNER, I.M. 2003. Quarterly notes: New taxa and records of Malaysian<br />

vascular plants. Folia malaysiana 4(3 & 4): 227–230.<br />

MASAMUNE, G. 1942. Enumeratio Phanerogamarum Bornearum. Taihoku. 739 pp.<br />

MASAMUNE, G. 1945. Enumeratio Pteridophytarum Bornearum. 124 pp.<br />

MERRILL, E.D. 1921. A bibliographic enumeration of Bornean plants. Journal of Straits<br />

Branch Royal Asiatic Society, Special Number. 637 pp.<br />

NEWMAN, M.F., BURGESS, P.F. & WHITMORE, T.C. 1996. Manuals of Dipterocarps for<br />

Foresters: Borneo Island Light Hardwoods. Royal Botanic Gardens Edinburgh & CIFOR.<br />

275 pp.<br />

NG, F.S.P. & JACOBS, M. 1983. A guide to King’s “Materials for a flora of the Malayan<br />

Peninsula”. The Gardens’ Bulletin Singapore 36: 177–185.<br />

NG, F.S.P. (ed.) 1978. Tree Flora of Malaya. Volume 3. Malayan Forest Records 26. Forest<br />

Department, West Malaysia. 339 pp.<br />

NG, F.S.P. (ed.) 1989. Tree Flora of Malaya. Volume 4. Malayan Forest Records 26. Forest<br />

Department, West Malaysia. 549 pp.<br />

225


TOWARDS THE FLORA OF MALAYSIA<br />

NG, F.S.P., LOW, C.M. & MAT ASRI, N.S. 1990. Endemic trees of the Malay Peninsula.<br />

Research Pamphlet 106. Forest Research Institute Malaysia, Kuala Lumpur. 118 pp.<br />

PARRIS, B.S. & LATIFF, A. 1997. Towards a Pteridophyte flora of Malaysia: A provisional<br />

checklist of taxa. Malayan Nature Journal 50: 235–280.<br />

PARRIS, B.S., BEAMAN, R.S. & BEAMAN, J.H. 1992. The Plants of Mount Kinabalu 2.<br />

Ferns. Royal Botanic Gardens, Kew. 165 pp.<br />

PIGGOTT, A.G. 1988. Ferns of Malaya in colour. Tropical Press Sdn. Bhd. Kuala Lumpur,<br />

Malaysia. 458 pp.<br />

POULSEN, A.D. 2006. Etlingera of Borneo. Natural History Publications (Borneo) in<br />

association with Royal Botanic Garden Edinburgh. 263 pp.<br />

PRIMACK, R.B. 1983. Forester’s guide to the Moraceae of Sarawak. Forest Department<br />

Sarawak, Kuching. 140 pp.<br />

RIDLEY, H.N. 1907. Materials for a Flora of the Malayan Peninsula. 3 Parts. Methodist<br />

Publishing House. Part 1, 233 pp.; Part 2, 235 pp.; Part 3, 197 pp.<br />

RIDLEY, H.N. 1922–1925. The flora of the Malay Peninsula. Volume 1-5. L. Reeve & Co.,<br />

Ltd. London.<br />

RIDLEY, H.N. 1926. The ferns of the Malay Peninsula. Journal of the Malayan Branch,<br />

Royal Asiatic Society 4: 1–121.<br />

SEIDENFADEN, G. & WOOD, J.J. 1992. The orchids of Peninsular Malaysia and Singapore.<br />

Olsen & Olsen, Fredensborg. 779 pp.<br />

SMYTHIES, B.E. 1965. Common Sarawak trees. Borneo Literature Bureau, Sarawak. 153 p.<br />

SOEPADMO, E. 1995. Background to the Tree Flora of Sabah and Sarawak Project. Pp.<br />

XIII–XIX in Soepadmo, E. & Wong, K.M. (eds.) Tree Flora of Sabah and Sarawak.<br />

Volume One. Forest Research Institute Malaysia, Kuala Lumpur, Sabah Forestry<br />

Department, Sandakan & Sarawak Forestry Department, Kuching.<br />

SOEPADMO, E. 1999. Botanical study of Malaysian medicinal plants–an appraisal. In A.<br />

Manaf Ali et al. (eds.) Phytochemical and biopharmaceutins from the Malaysian rain<br />

forest. FRIM & PSSM, Kuala Lumpur.<br />

SOEPADMO, E., SAW, L.G. & CHUNG, R.C.K. (eds.) 2002. Tree Flora of Sabah and Sarawak,<br />

Vol. 4. Forest Research Institute Malaysia, Kuala Lumpur, Sabah Forestry Department,<br />

Sandakan & Sarawak Forestry Department, Kuching. 388 pp.<br />

SOEPADMO, E., SAW, L.G. & CHUNG, R.C.K. (eds.) 2004. Tree Flora of Sabah and<br />

Sarawak, Vol. 5. Forest Research Institute Malaysia, Kuala Lumpur, Sabah Forestry<br />

Department, Sandakan & Sarawak Forestry Department, Kuching. 528 pp.<br />

SOEPADMO, E. & WONG, K.M. (eds.) 1995. Tree Flora of Sabah and Sarawak. Vol. 1.<br />

Forest Research Institute Malaysia, Kuala Lumpur, Sabah Forestry Department, Sandakan<br />

& Sarawak Forestry Department, Kuching. 513 pp.<br />

SOEPADMO, E. & SAW, L.G. (eds.) 2000. Tree Flora of Sabah and Sarawak. Vol. 3. Forest<br />

Research Institute Malaysia, Kuala Lumpur, Sabah Forestry Department, Sandakan &<br />

Sarawak Forestry Department, Kuching. 511 pp.<br />

SOEPADMO, E., WONG, K.M. & SAW, L.G. (eds.) 1996. Tree Flora of Sabah and Sarawak.<br />

Vol. 2. Forest Research Institute Malaysia, Kuala Lumpur, Sabah Forestry Department,<br />

Sandakan & Sarawak Forestry Department, Kuching. 443 pp.<br />

SYMINGTON, C.F. 1943. Foresters’ manual of Dipterocarps. Malayan Forest Records No.<br />

16. Syonan-Hakubutukan, Kuala Lumpur, Malaya. 244 pp.<br />

TURNER, I.M. 1997 (‘1995’). A catalogue of the vascular plants of Malaya. The Gardens’<br />

Bulletin Singapore 47: 1–757.<br />

TURNER, I.M. 2000. The taxonomy of Malaysian vascular plants: New taxa (1996–2000)<br />

and endemic genera. Folia malaysiana 2: 41–82.<br />

226


L.G. SAW & R.C.K. CHUNG (2007)<br />

VAN STEENIS, G.G.G.J. 1955. Annotated selected bibliography. Flora Malesiana Series I.<br />

Volume 5. P. Noordhoff Ltd.<br />

VAN STEENIS-KRUSEMAN, M.J. 1950. Cyclopaedia of collectors. Flora Malesiana Series<br />

I. Volume 1. P. Noordhoff Ltd.<br />

WHITMORE, T.C. (ed.) 1972. Tree Flora of Malaya. Volume 1. Malayan Forest Records 26.<br />

Forest Department, West Malaysia. 471 pp.<br />

WHITMORE, T.C. (ed.) 1973. Tree Flora of Malaya. Volume 2. Malayan Forest Records 26.<br />

Forest Department, West Malaysia. 444 pp.<br />

WHITMORE, T.C., TANTRA, I.G.M. & SUTISNA, U. 1990a. Tree Flora of Indonesia. Check<br />

list of Kalimantan. Part I. Forest Research and Development Centre. Bogor. Pp. 1–181.<br />

WHITMORE, T.C., I.G.M. & SUTISNA, U. 1990b. Tree Flora of Indonesia. Check list of<br />

Kalimantan. Part II. 1. Forest Research and Development Centre. Bogor. Pp. 181–429.<br />

WHITMORE, T.C., I.G.M. & SUTISNA, U. 1990c. Tree Flora of Indonesia. Check list of<br />

Kalimantan. Part II. 2. Forest Research and Development Centre. Bogor. Pp. 431–620.<br />

WONG, K.M. 1987. The herbarium and arboretum of the Forest Research Institute of Malaysia<br />

at Kepong–a historical perspective. The Gardens’ Bulletin Singapore 40: 15–30.<br />

WONG, K.M. 1995a. A brief history of botanical collecting and documentation in Borneo.<br />

Pp. XXI-XLI in Soepadmo, E. & Wong, K.M. (eds.). Tree Flora of Sabah and Sarawak.<br />

Volume 1. Forest Research Institute Malaysia, Kuala Lumpur, Sabah Forestry Department,<br />

Sandakan & Sarawak Forestry Department, Kuching. 513 pp.<br />

WONG, K.M. 1995b. The Bamboos of Peninsular Malaysia. Malayan Forest Records No. 41.<br />

Forest Research Institute Malaysia, Kepong.<br />

WONG, K.M. 1998. Patterns of plant endemism and rarity in Borneo and the Malay Peninsula.<br />

In Peng, C.-I. & Lowry II, P.P. (eds.). Rare, threatened, and endangered floras of Asia and<br />

the Pacific Rim. Academia Sinica Monograph Series No. 16: 139–169.<br />

WOOD, G.H.S. & AGAMA, J. 1956. Check list of forest flora of North Borneo. North Borneo<br />

Forest Records No. 6.<br />

WOOD, G.H.S. & MEIJER, W. 1964. Dipterocarps of Sabah (North Borneo). Sabah Forest<br />

Records No. 5.<br />

WOOD, J.J., BEAMAN, R.S. & BEAMAN, J.H. 1993. The Plants of Mount Kinabalu 2.<br />

Orchids. Royal Botanic Gardens, Kew. 411 pp.<br />

WOOD, J.J. & CRIBB, P.J. 1994. A checklist of orchids of Borneo. Royal Botanic Gardens,<br />

Kew.<br />

WYATT-SMITH, J. 1952. Pocket check list of timber trees. Malayan Forest Records No. 17.<br />

Forest Department, Kuala Lumpur.<br />

WYATT-SMITH, J. 1953a. Manual of Malayan timber trees. Burseraceae. F.R.I. Research<br />

Pamphlet No. 1. Forest Research Institute, Kepong.<br />

WYATT-SMITH, J. 1953b. Manual of Malayan timber trees. Leguminosae. F.R.I. Research<br />

Pamphlet No. 2. Forest Research Institute, Kepong.<br />

WYATT-SMITH, J. 1953c. Manual of Malayan timber trees. Myristicaceae. F.R.I. Research<br />

Pamphlet No. 3. Forest Research Institute, Kepong.<br />

WYATT-SMITH, J. 1954a. Manual of Malayan timber trees. Sapotaceae. F.R.I. Research<br />

Pamphlet No. 4. Forest Research Institute, Kepong.<br />

WYATT-SMITH, J. 1954b. Manual of Malayan timber trees. Lauraceae. F.R.I. Research<br />

Pamphlet No. 5. Forest Research Institute, Kepong.<br />

WYATT-SMITH, J. 1954c. Manual of Malayan timber trees. Sapindaceae. F.R.I. Research<br />

Pamphlet No. 6. Forest Research Institute, Kepong.<br />

227


NAZIR KHAN NIZAM KHAN & MOHD YUNUS ZAKARIA (2007)<br />

STATUS OF BIOLOGICAL DIVERSITY IN MALAYSIA &<br />

THREAT ASSESSMENT OF PLANT SPECIES IN MALAYSIA<br />

FOREST RESOURCES TREND AND<br />

SUSTAINABLE FOREST MANAGEMENT IN<br />

PENINSULAR MALAYSIA<br />

1<br />

Nazir Khan Nizam Khan & 2 Mohd Yunus Zakaria<br />

ABSTRACT<br />

Malaysia is well endowed with some of the world’s richest forests, a richness not only in<br />

terms of numbers and uniqueness of species but also diversity of habitats and ecosystems. The<br />

total forested area in Peninsular Malaysia is about 44.7% (5.88 million hectares) of its land<br />

area. Of this total, some 35.7% (4.70 million hectares) are within Permanent Reserved Forests<br />

(PRFs). PRFs are legally gazetted Forest Reserves, managed sustainably for economic, social<br />

and environmental values. During the implementation of the New Economic Policy in 1970,<br />

the need to eradicate poverty and distribute wealth among the various communities saw the<br />

massive development of large-scale agriculture, particularly in the rural areas. This has resulted<br />

in the conversion of forest areas to plantation crops such as oil palm and rubber. Although<br />

large forest areas were cleared for this purpose, at the same time, there was a significant<br />

increase in the gazettement of PRFs. In 1970, the total forested areas was approximately 8.0<br />

million ha and this dropped to 5.87 million ha in 2003 or a decrease of 27%. During the same<br />

period, the area gazetted as PRFs was 3.3 million ha in 1970 and it was increased to 4.7<br />

million ha or an increase of 42% in 2003.<br />

In an attempt to conserve the species and genetic resources in various forest and ecological<br />

types, the Forestry Department has also set aside pockets of virgin forests known as Virgin<br />

Jungle Reserve (VJR) and has taken actions to classify relevant areas of the PRFs into eleven<br />

different functional classes. Efforts are also being taken by the Department to ensure in situ<br />

conservation of biodiversity during forest harvesting in the PRFs. The Forestry Department is<br />

committed to forest conservation and protection of the environment, where PRF areas open<br />

for harvesting are subjected to forest management certification processes and the acreage of<br />

the PFR areas opened for harvesting are regulated and controlled. From another perspective,<br />

the Forestry Department had, to date, organised eight scientific biodiversity expeditions.<br />

INTRODUCTION<br />

The tropical rainforest has long been valued as a source for food, fuel, medicine and materials,<br />

for shelter and livelihood. It will continue to play an important role in the country’s socioeconomic<br />

development and environmental conservation.<br />

Forest Department Peninsular Malaysia, Jalan Sultan Salahuddin, 50660 Kuala Lumpur; 1 nazir@forestry.gov.my;<br />

2<br />

yunus@forestry.gov.my<br />

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FOREST RESOURCES TREND AND SUSTAINABLE FOREST MANAGEMENT IN PENINSULAR MALAYSIA<br />

The economic contributions of the forest are well recognized particularly to the wood and<br />

non-wood based industry and trade. This is reflected by the fact that the country has emerged<br />

as one of the main supplier of the world’s tropical hardwood products. In 2003, the forestry<br />

sector contributed RM 16.3 billion, which is 4.3 percent of the total export earnings, of which<br />

Peninsular Malaysia contributed RM 8.13 billion. The forestry sector also provided employment<br />

opportunities for over 330,000 people in Malaysia. In Peninsular Malaysia, the sector provided<br />

direct employment to 87,000 people. Forest revenue collected by various states in Peninsular<br />

Malaysia amounted to RM 335 million in 2003.<br />

Although not easily translated into financial values, the roles of forests in watershed protection,<br />

conservation of soil and water resources, conservation of flora and fauna, conservation of<br />

genetic resources and support for agricultural and environmental conservation have long been<br />

recognized by forest managers. To meet the environmental as well as socio-economic needs,<br />

Permanent Reserved Forest (PRF) areas, wildlife reserves and water catchment areas were<br />

established.<br />

This paper highlights the trends and current status of forest resources. It also elaborates on the<br />

forest management practices and biodiversity conservation in Peninsular Malaysia and the<br />

various initiatives and actions undertaken to achieve sustainable forest management. Forest<br />

coverage and timber production are briefly discussed here.<br />

SUSTAINABLE FOREST MANAGEMENT<br />

The World Conservation Strategy, which was initiated by the United Nations Environmental<br />

Program (UNEP), defines conservation as follows (IUCN 1980):<br />

All human lives depend on the natural environment for survival and long-term well-being.<br />

Hence for any economic development to be sustainable, it must first be ecologically sustainable,<br />

and must satisfy three conditions:<br />

• Ecological integrity of the ecosystem must be maintained;<br />

• Renewable resources must be used sustainably; and<br />

• Biological diversity must be maintained.<br />

Article 2 of the Convention of Biological Diversity defines ‘sustainable use’ as the use of<br />

components of biological diversity in a way and at a rate that does not lead to the long-term<br />

decline of biological diversity, thereby maintaining its potential to meet the needs and aspirations<br />

of present and future generation (Anonymous 2005).<br />

The sustainable forest management concept in Malaysia is in line with the conservation and<br />

sustainable use definitions outlined by the World Conservation Strategy and Convention of<br />

Biological Diversity respectively. The definition adopted by Malaysia and the International<br />

Tropical Timber Council is “Sustainable forest management is the process of managing<br />

permanent forest land, to achieve one or more clearly specified objectives of management<br />

with regard to continuous flow of desired forest products and services, without undue reduction<br />

in its inherent values and future productivity and without undesirable effects in the physical<br />

and social environment” (Mohd Yunus et al. 2003).<br />

230


NAZIR KHAN NIZAM KHAN & MOHD YUNUS ZAKARIA (2007)<br />

Malaysia is committed to manage its natural forest in a sustainable manner; to ensure continuous<br />

timber production, maintain multiple functions of the forests, conserve biodiversity and control<br />

environmental impact (Mohd Yunus 1993, Anonymous 1996). The following are the objectives<br />

of the National Forest Policy 1978 (revised 1992) (Anonymous 1995):<br />

• To conserve and manage the nation’s forest, based on the principles of sustainable<br />

management<br />

• To protect the environment and to conserve the forest biological diversity, genetic resources,<br />

and to enhance research and education<br />

CONSTITUTIONAL PROVISIONS, POLICY AND LEGISLATIONS<br />

Under Article 74(2) of the Malaysian Constitution, forestry comes under the jurisdiction of<br />

the respective State Governments. As such, each state is empowered to enact laws on forestry<br />

and to formulate forest policy independently. The executive authority of the Federal Government<br />

only extends to the provision of the maintenance of the experimental and demonstration stations,<br />

training and in the conduct of research.<br />

In order to facilitate the adoption of a coordinated and common approach to forestry, the<br />

National Land Council (NLC) established the National Forestry Council (NFC) in December<br />

20, 1971. The NLC is empowered under the Malaysian Constitution to formulate a national<br />

policy for the promotion and control of the utilization of land for mining, agriculture and<br />

forestry. The NFC serves as a forum for the Federal and the State Governments to discuss and<br />

resolve common issues relating to forestry policy, administration and management. The<br />

responsibility for implementing the decisions of the NFC lies with State Governments unless<br />

it is within the authority of the Federal Government.<br />

In 1977, the National Forestry Policy was accepted by the National Forestry Council and later<br />

endorsed by the National Land Council on April 19, 1978. This policy was revised in November<br />

1992 to take cognizance of the current concern expressed by the world community on the<br />

importance of biological diversity conservation and the sustainable utilization of the genetic<br />

resources, as well as the role of local communities in forest development.<br />

STATUS OF PENINSULAR MALAYSIA’S FOREST RESOURCES<br />

Forested Areas<br />

During the implementation of the New Economic Policy in 1970, particularly with two prime<br />

objectives, i.e. eradication of poverty and distribution of wealth among the races, one of the<br />

strategies was the development of large-scale agricultural development, particularly in rural<br />

areas. The development of forest areas into palm oil and rubber plantations in tandem causes<br />

reduction of forested areas in Peninsular Malaysia. However, there was a significant increase<br />

in the gazettement of permanent reserved forest (PRF). In 1970, the total forested areas was<br />

approximately 8.0 million ha and this has dropped to 5.87 million ha in 2003, a decrease of 27<br />

%. During the same period, the area gazetted as PRF was 3.3 million hectares and this was<br />

increased to 4.7 million ha or an increase of 42 % in 2003. Table 1 illustrates the trend.<br />

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FOREST RESOURCES TREND AND SUSTAINABLE FOREST MANAGEMENT IN PENINSULAR MALAYSIA<br />

In 2003, natural forest cover in Peninsular Malaysia was 5.88 million ha or 44.7 % of the total<br />

land area of Peninsular (Abdul Rashid, 2005). The bulk of these forested areas comprised the<br />

Dry Inland Forest (5.4 million ha), followed by Peat Swamp Forest (0.30 million ha), Mangrove<br />

Forest (0.10 million ha) and Planted Forest (0.08 million ha).<br />

Permanent Reserved Forest and Protected Areas in Peninsular Malaysia<br />

Out of the 5.88 million ha, 4.70 million ha or 35.7% of the total land area had been designated<br />

as the Permanent Reserved Forest (PRF) to be managed sustainably for the benefit of the<br />

present and future generations (Abdul Rashid, 2005).<br />

Of the total PRF, approximately 3.18 million ha (24.2% of the total land area) are classified as<br />

production forest with the remaining 1.52 million ha (11.6 % of the total land area) being<br />

classified as protection forest (Abdul Rashid, 2005). Based on the National Forestry Policy,<br />

the role of the production forest is to ensure the supply in perpetuity, at reasonable levels, of<br />

all forms of forest produce that can be economically produced within the country. On the<br />

other hand, the role of the protection forest is to ensure favourable climatic and physical<br />

conditions of the country, the safeguarding of water resources, soil fertility, environmental<br />

quality, conservation of biological diversity and the minimization of damage by floods and<br />

erosion to rivers and agricultural lands.<br />

Apart from the protection forests within the PRF, other protected areas, which had been gazetted<br />

as national parks, wildlife and bird sanctuaries amounted to 0.89 million ha (6.8% of the total<br />

land area) (Abdul Rashid, 2005). Of this total, 0.58 million ha are designated as National and<br />

State Parks, while 0.31 million ha are wildlife and bird sanctuaries. A total of 0.12 million ha<br />

(0.9% of the total land area) of the wildlife and bird sanctuary areas are located within the PRF.<br />

Table 1. Forested Area and Permanent Reserved Forests (PRF) in Peninsular Malaysia (1970 to 2003)<br />

Year PRF (ha) Forested Year PRF (ha) Forested<br />

Area (ha)<br />

Area (ha)<br />

1970 3,337,708 8,009,000 1987 4,288,408 6,348,000<br />

1971 3,307,770 7,875,000 1988 4,928,646 6,288,000<br />

1972 3,434,326 7,583,000 1989 4,866,201 6,320,000<br />

1973 3,412,113 7,450,000 1990 4,866,470 6,270,000<br />

1974 3,412,113 7,319,000 1991 4,748,057 6,111,000<br />

1975 3,448,007 7,290,000 1992 4,675,021 6,042,000<br />

1976 3,448,007 7,199,000 1993 4,698,459 6,024,008<br />

1977 3,164,439 6,968,000 1994 4,687,463 6,003,000<br />

1978 2,948,351 6,839,000 1995 4,684,904 5,991,000<br />

1979 2,932,943 6,588,000 1996 4,684,094 5,820,547<br />

1980 3,124,045 6,505,000 1997 4,731,927 5,852,869<br />

1981 3,083,103 6,438,000 1998 4,730,216 5,838,860<br />

1982 3,064,837 6,378,000 1999 4,853,646 5,938,068<br />

1983 3,064,837 6,373,000 2000 4,837,500 5,979,649<br />

1984 2,999,655 6,353,000 2001 4,840,431 5,924,407<br />

1985 3,274,008 6,353,000 2002 4,701,858 5,892,901<br />

1986 4,617,010 6,455,000 2003 4,696,211 5,879,723<br />

232


NAZIR KHAN NIZAM KHAN & MOHD YUNUS ZAKARIA (2007)<br />

Forest Plantations<br />

To relieve the pressures on natural forests as well as to supplement future wood supply of the<br />

country, forest plantations, which are capable of yielding a high volume of timber per unit<br />

area within a shorter rotation, are being established. The species planted include tropical pines<br />

such as Pinus caribaea, P. merkusii and Araucaria species, as well as fast-growing hardwood<br />

species, such as Acacia mangium, Gmelina arborea, and Paraserianthes falcataria. Other<br />

species planted include Tectona grandis, Shorea macrophylla and Durio zibethinus. By the<br />

end of 2003, 0.08 million ha of plantation areas were established in Peninsular Malaysia.<br />

In view of the growing importance of forest plantation and to encourage greater private sector<br />

investment, a National Committee on Forest Plantation Development with full participation<br />

from the private sector had been formed. The Committee’s main role is to formulate a national<br />

strategy and action plan for the promotion and effective implementation of forest plantation<br />

programs. As forest plantation projects are being viewed as strategic projects of national interest,<br />

the Government of Malaysia provides fiscal incentives, as well as full tax exemption under<br />

the Pioneer Status for ten (10) years or 100% tax exemption under the Investment Tax<br />

Allowance for five (5) years, effective from 1993.<br />

FOREST MANAGEMENT PRACTICES<br />

Forest management in Peninsular Malaysia has a long history; it goes back to nearly a century<br />

ago when the first Chief Forest Officer was appointed in 1901. The forest management practices<br />

are being developed and revised to meet fluctuating market, supply and demand situations, as<br />

well as advancement made in ecological, industrial, and harvesting technologies.<br />

Functional Classes<br />

Section 10 of National Forestry Act 1984 required PRF areas to be classified and gazetted into<br />

eleven functional classes. Except for the first functional class (3.18 million ha), which is for<br />

timber production under sustainable management, all the remaining ten functional classes<br />

(1.52 million ha) are for purposes of conservation and protection and are as follows:<br />

Hectares (approximate)<br />

Production forest 3,000,000<br />

Soil protection forest 300,000<br />

Soil reclamation forest 6,000<br />

Flood control forest 6,000<br />

Water catchment forest 800,000<br />

Forest sanctuary for wildlife 100,000<br />

Virgin Jungle Reserved forest 20,000<br />

Amenity forest 70,000<br />

Education forest 50,000<br />

Research forest 30,000<br />

Forest for federal purposes 20,000<br />

233


FOREST RESOURCES TREND AND SUSTAINABLE FOREST MANAGEMENT IN PENINSULAR MALAYSIA<br />

The classification of the above functional classes is by no means exclusive. An area of the<br />

PRF can be classified under more than one functional class provided their uses are not<br />

contradictory. For example, forest trekking, camping, picnicking and bird watching activities<br />

should not pose problems in the catchment areas provided these are done in low densities.<br />

There is a need to formulate specific management practices for each of the functional classes.<br />

One of the aims of classifying the forest into different functions is to ensure that the forest is<br />

used and managed within its capacity. Over-use and inappropriate management result in forest<br />

health degradation that could change the forest ecosystem. The drastic changes in the ecosystem<br />

will negatively impact human welfare, health and food production.<br />

Selective Management System (SMS)<br />

Currently, the production forests are managed under Selective Management System. The system<br />

advocates the selection of a cutting regime based on diameter limits and species composition<br />

of the standing trees. In Peninsular Malaysia, the implementation of the SMS involves<br />

conducting forest activities that could be distinctly categorized into three stages, namely preharvesting,<br />

during harvesting and post-harvesting activities. The pre-harvesting activities<br />

include pre-felling forest inventory, cutting limit prescription and timber tagging. During<br />

harvesting, activities include directional felling and forest road construction while post harvest<br />

activities include forest survey, post-felling forest inventory and prescription of silvicultural<br />

treatments. Some of the activities are further elaborated below.<br />

The SMS is designed to achieve sustainability of the forest with management objectives of<br />

economic and efficient harvesting under prevailing conditions. It requires the selection of<br />

management (cutting) regimes based on inventory data, which will be equitable to logger and<br />

forest owner, as well as ensuring ecological balance and environmental quality.<br />

Pre-Harvesting Activities<br />

Cutting Limits Prescription<br />

The cutting limits prescription is based on the stand and stock information obtained from the<br />

pre-felling forest inventory, together with other relevant information needed to determine the<br />

optimal cutting regimes (diameter limits) for the forest area. Under SMS, the next cut is expected<br />

to be between 30-55 years and with an estimated net economic outturn of 30–40 cubic meters<br />

per hectare. The criteria for cutting limits prescription are as follows:<br />

• The cutting limit prescribed for the group of dipterocarp species should not be less than<br />

50 cm dbh, except for Neobalanocarpus heimii (Chengal) where the cutting limit prescribed<br />

should not be less than 60 cm dbh.<br />

• The cutting limit prescribed for the group of non-dipterocarp species should not be less<br />

than 45 cm dbh.<br />

• The residual stocking should have at least 32 sound commercial trees per ha from the<br />

diameter class 30–45 cm or its equivalence.<br />

• The difference in the cutting limits prescribed between the dipterocarp and that of the<br />

non-dipterocarp species should be at least 5 cm.<br />

• The percentage of dipterocarp species in the residual stand for trees having 30 cm dbh<br />

and above should not be less than that in the original stand.<br />

234


NAZIR KHAN NIZAM KHAN & MOHD YUNUS ZAKARIA (2007)<br />

Timber Tagging<br />

Subsequently, timber tagging is carried out where harvestable trees are marked. This activity<br />

is carried out to ensure that only marked trees are felled, as well as to control the amount of<br />

timber output from the forest. The timber tagging system has proven to be an efficient<br />

mechanism in controlling and tracking the movement and removal of logs from the forest.<br />

During Harvesting Activities<br />

During harvesting, prescribed forestry activities would have to be conducted in accordance<br />

with rules and regulations as stipulated in the logging license issued by the State Forestry<br />

Department. Among others, matters given due consideration during forest harvesting include:<br />

• directional felling to ensure minimal damage to residual stand;<br />

• construction of forest roads, skid trails and log landings according to prescribed standards<br />

to ensure minimal adverse environmental impact; and<br />

• demarcation of adequate buffer zones along rivers and streams to mitigate soil erosion.<br />

Post-Harvesting Activities<br />

Forest Survey<br />

Immediately after harvesting, a forest survey is carried out to check on felled and un-felled<br />

trees and compliance to license conditions.<br />

Post-Felling Forest Inventory<br />

Normally, at two to five years after harvesting, a post-felling forest inventory is conducted to<br />

assess the status of the residual stand, as well as to determine any appropriate silvicultural<br />

treatments to be carried out.<br />

A similar inventory is conducted at year 10 to assess the status of the regenerated forest. The<br />

sequence of operations under SMS is shown in Table 2.<br />

Annual Harvesting Coupe<br />

The annual harvesting coupe for the natural forests is determined for a period of five years,<br />

which follows the Malaysia Plan. For the Eighth Malaysia Plan (2001–2005), the annual<br />

harvesting coupe is 42,870 ha. This is expected to provide an annual yield of 3.43 million<br />

meter cubic (Abdul Rashid, 2005). Table 3 shows the trend of annual harvesting coupe from<br />

1994 to 2003. Table 4 shows the log consumption by the sawmill and plywood/veneer industries.<br />

Based on the current production capacity of the forest, acreage of PRF and current log<br />

consumption, it is concluded that log supply from the PRF (natural forests) will not be able to<br />

meet the industry’s demand and this supply will continue to decline further in the long term.<br />

In terms of resource sustainability, current forest planning and integrated operational studies<br />

have shown that, with average growth rates of trees over 30 cm dbh of 0.8–1.0 cm per year in<br />

diameter and 2.0–2.5 cubic meters per hectare per year in commercial gross volume, the hill<br />

forests in Peninsular Malaysia are capable of producing every 25–55 years of at least 45–85<br />

net cubic meters per hectare.<br />

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FOREST RESOURCES TREND AND SUSTAINABLE FOREST MANAGEMENT IN PENINSULAR MALAYSIA<br />

Table 2. Sequence of Operations under the SMS<br />

Year<br />

Activities<br />

n-2 to n-1 Pre-felling forest inventory of 10% sampling intensity using<br />

systematic-line plots to determine appropriate cutting regimes (limits).<br />

n-1 to n Tree marking incorporating directional felling.<br />

N<br />

Felling all marked trees.<br />

n + 1 / 4<br />

to n + 1 / 2<br />

Forest survey to determine fines on trees unfelled, royalty on short<br />

logs and tops, and damage to residuals.<br />

n + 2 to n + 5<br />

Post-felling forest inventory of 10% inventory using systematic-lineplots<br />

to determine residual stocking and appropriate silvicultural<br />

treatments.<br />

n +10<br />

Forest inventory of regenerated forest to determine status of the forest.<br />

Table 3. Annual Harvesting Coupe<br />

Year Approved Annual Annual Coupe<br />

Coupe (ha)<br />

Logged (ha)<br />

1994 52,250 37,725<br />

1995 52,250 33,246<br />

1996 46,040 37,587<br />

1997 46,040 34,410<br />

1998 46,040 30,408<br />

1999 46,040 41,527<br />

2000 46,040 30,366<br />

2001 42,870 26,711<br />

2002 42,780 26,482<br />

2003 42,780 27,714<br />

Source: Forestry Statistics Peninsular Malaysia 2003<br />

Table 4. Log Consumption By Sawmill and Plywood/Veneer Mills (Meter Cubic)<br />

Year Sawmill Plywood/Veneer Total<br />

1994 9,196,184 1,993,797 11,189,981<br />

1995 10,046,496 1,450,941 11,497,437<br />

1996 9,173,683 1,606,582 10,780,265<br />

1997 9,172,923 1,599,376 10,772,299<br />

1998 5,532,675 1,023,785 6,556,460<br />

1999 6,348,688 1,080,691 7,429,379<br />

2000 6,092,286 9,524,26 7,044,712<br />

2001 5,443,689 7,977,05 6,241,394<br />

2002 5,425,635 7,952,38 6,220,873<br />

2003 6,279,228 7,600,45 7,039,273<br />

Source: Forestry Statistics Peninsular Malaysia 2003<br />

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NAZIR KHAN NIZAM KHAN & MOHD YUNUS ZAKARIA (2007)<br />

The size of forest area opened for harvesting is regulated and controlled through the National<br />

Forestry Council (NFC). To enhance regulation on harvesting operations, the NFC has decided<br />

to set output cap per unit area, at 85 meter cubic per ha. With this output cap, the damages to<br />

the forest stand is expected to be lower and will ensure sufficient trees left for regeneration<br />

and future harvesting.<br />

Technology Development<br />

Environmentally, socially and economically sound timber harvesting is a fundamental aspect<br />

of wise forest use. In recent years, research into reduced impact logging (RIL) and low impact<br />

logging (LIL) harvesting technologies as a systematic approach to planning, implementing,<br />

monitoring and evaluating forest harvesting has been intensified. The principal aim of the<br />

new technologies is to improve forest management by minimizing the negative impacts of<br />

forest harvesting on the residual stand and the environment.<br />

Reduced impact logging can be described as the implementation of an intensively planned<br />

and controlled set of forest harvesting guidelines, which results in low level of damage to<br />

residual trees, soil and water so that the productive capacity of the forest after logging is<br />

sustained together with its ecological functions.<br />

The essential components of RIL operation generally comprise pre- harvest forest inventory<br />

of individual trees, pre-harvest planning of roads and skid trails‘ direction of felling‘ efficient<br />

utilization of felled trees, minimum ground disturbances and effective field supervision. Besides<br />

the government’s efforts, the private sector has also contributed to the improvement of forest<br />

harvesting technologies. For example, Kumpulan Perkayuan Kelantan (KPK) has initiated<br />

the building of crusher-run all-weather forest roads in its concession areas, while KPKKT<br />

(Kumpulan Pengurusan Kayu Kayan Terengganu Sdn Bhd) has modified an excavator for log<br />

extraction that was found to reduce the amount of logging damage substantially when compared<br />

to the conventional method. In addition, a local company has built a modified excavator known<br />

as RIMBAKA for the purpose of log extraction.<br />

FOREST MANAGEMENT CERTIFICATION<br />

From the Malaysian perspective, forest management certification entails an independent<br />

assessment of a forest management operation, according to specific economic, social,<br />

environmental and ecological criteria, indicators, activities and management specifications.<br />

This forest assessment typically includes an evaluation of the economic viability of the<br />

operation, the social and environmental impact of the forest management activities and the<br />

ecological health of the forest. It covers forest inventory, management planning, silviculture,<br />

harvesting, computation and control of the annual allowable cut, road construction and other<br />

related forest management activities.<br />

Since its establishment, the Malaysia Timber Certification Council (MTCC) has been involved<br />

in a number of internal consultative processes to formulate and revise the Malaysian Criteria<br />

& Indicators (MC&I). It involved government departments and agencies, environmental nongovernmental<br />

organisations (NGOs), forest licensees, manufacturers of wood and panel<br />

products, and trade unions.<br />

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FOREST RESOURCES TREND AND SUSTAINABLE FOREST MANAGEMENT IN PENINSULAR MALAYSIA<br />

A total of 29 indicators, 87 activities and 49 standards of performance under 6 criteria of the<br />

MC&I were used to assess forest management practices in 8 states in Peninsular Malaysia;<br />

Pahang, Selangor, Terengganu, Johor, Kedah, Perak, Negeri Sembilan and Kelantan. To date,<br />

a total of 4.68 million ha of PRF covering the eight State Forest Management Units (FMUs)<br />

had been given MTCC’s Certificate for Forest Management.<br />

MS ISO 9002<br />

The MS ISO 9000, in brief, is a series of standards for quality management and quality assurance<br />

system. The adoption of MS ISO 9000 series will ensure the establishment of quality systems,<br />

products and services. The MS ISO 9000 processes can help to attain sustainable forest<br />

management because the processes will ensure activities are carried out according to the<br />

standards.<br />

The core process identified for the Forestry Department was sustainable timber production<br />

from the PRF while the major activities identified to ensure the achievement of this core<br />

process are forest boundary demarcation, pre-felling forest inventory, timber tagging, forest<br />

harvesting, post-felling forest inventory and silvicultural treatments.<br />

The Forestry Department Headquarters, and eight State Forestry Departments namely, Johor,<br />

Kedah, Pahang, Selangor, Kelantan, Negeri Sembilan, Perak and Terengganu have been<br />

awarded the MS ISO 9002 certificates.<br />

FOREST BIOLOGICAL DIVERSITY CONSERVATION<br />

The tropical rainforest of Malaysia is one of the most complex and rich ecosystems in the world.<br />

The forest has long been recognized as a repository of genetic resources for both flora and<br />

fauna. As one of the 12 mega-diverse countries in the world, the forests are home to at least<br />

14,500 species of flowering plants and trees, 600 species of birds, 286 species of mammals, 140<br />

species of snakes and 80 species of lizards (Zul Mukhshar, 2000, Mohd Yunus & Mangsor<br />

2002). In an attempt to diversify and expand the conservation of genetic resources of various<br />

forest and ecological types in their original conditions, the Forestry Department has also set<br />

aside pockets of Virgin Jungle Reserves (VJRs). A total of 87 VJRs covering 23,002 hectares<br />

were established throughout Peninsular Malaysia. These VJRs represent samples of the many<br />

forest types found in the PRFs. Represented forest types include Mangrove Forest, Heath Forest,<br />

Peat Swamp Forest, Lowland Dipterocarp Forest, Hill Dipterocarp Forest, Upper Dipterocarp<br />

Forest and Montane Forest (there are no VJRs in the upper hill and montane forests). These<br />

VJRs are unique and represent an integral part of sustainable management practice in Peninsular<br />

Malaysia. Besides VJRs, there are other protection areas under different functional classes. There<br />

is 0.12 million ha of protected areas in the PRF or 2.5% of the PRF area.<br />

Efforts are also being taken by the Forestry Department to ensure in situ conservation of<br />

biodiversity during forest harvesting in the production forests of the PRFs. In this context,<br />

even though the prescribed minimum cutting limit for the Dipterocarp species in Peninsular<br />

Malaysia is 50 cm dbh; for the species Neobalanocarpus heimii (Chengal), the minimum<br />

cutting limit has been raised to 60 cm so as to better conserve populations of this species. In<br />

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NAZIR KHAN NIZAM KHAN & MOHD YUNUS ZAKARIA (2007)<br />

addition, other measures for environmental protection and biological conservation have been<br />

taken into consideration during harvesting: retention of mother trees and fruits trees; retention<br />

tree for protection; buffer zone along rivers and streams; timber tagging and directional felling;<br />

construction of forest roads; and skid trails and log landings according to prescribed standards<br />

approved by the Forestry Department. Seed Production Areas (SPA) have also been established<br />

in natural stands for indigenous species such as Shorea leprosula, S. parvifolia, S. acuminata<br />

and Eurycoma longifolia.<br />

The Forestry Department together with the Forest Research Institute Malaysia (FRIM) is<br />

undertaking a project to locate and survey threatened tree species. A number of species have<br />

already been identified and the Department is taking the necessary steps to conserve areas<br />

where the populations occur.<br />

FOREST BIODIVERSITY EXPEDITIONS<br />

The Forestry Department is committed to forest conservation and protection of the environment.<br />

A number of projects with greater emphasis on forest bio-diversity is being implemented in<br />

the Eighth Malaysia Plan and these are expected to continue into the Ninth Malaysia Plan.<br />

To date, the Forestry Department has organised several scientific biodiversity expeditions.<br />

The first expedition was held at the Perlis State Park, Perlis (28 September to 4 October<br />

1999). This was then followed by the Endau Rompin State Park, Pahang (16-22 June 2002),<br />

Matang Mangroves, Perak (20-25 October 2002), Ulu Muda Forest Reserve, Kedah (23-29<br />

March 2003), Gunung Stong Forest Reserve, Kelantan (24-29 May 2003), the Royal Belum<br />

State Park, Perak (25 July–1 August 2003), Gunung Mandi Angin, Terengganu (5-10 June<br />

2004) and Forest Park Kenong, Pahang (16-21 August 2004). In all the expeditions, the<br />

department had the fullest cooperation and active participation from scientists from Universiti<br />

Kebangsaan Malaysia (UKM), Universiti Putra Malaysia, Universiti Sains Malaysia (USM),<br />

Universiti Malaya (UM), World Wide Fund for Nature, Malaysia (WWF), Malaysian Nature<br />

Society (MNS), SIRIM, Forest Research Institute Malaysia (FRIM), Institute of Medical<br />

Research (IMR) and other related government agencies. In addition, the Forestry Department<br />

also participated in scientific expedition organized by other organization, namely LADA and<br />

MNS for the Scientific and Heritage Expedition of Langkawi Islands from 10-19 April 2003,<br />

with UKM in the Scientific Expedition of Tasik Chini, Pahang from 22-27 May 2004 and with<br />

FRIM during the Scientific Expedition of Gunung Aais, Pahang from 3-10 July 2004.<br />

The Forestry Department had also organised a series of seminars to disseminate the results of<br />

the expeditions. To date, three seminars had been organised, namely Endau-Rompin, Pahang<br />

(5–6 May 2003), Ulu Muda, Kedah (14–16 February, 2004) and Gunung Stong, Kelantan<br />

(20–22 April, 2004). In addition a National Conference on Sustainable Management of Matang<br />

Mangroves, Perak was held from 5 – 8 October 2004.<br />

CONCLUSION<br />

The need for effective forest management and conservation must be given priority, not only to<br />

ensure a sustained supply of wood and non-wood forest products but also to maintain forest<br />

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FOREST RESOURCES TREND AND SUSTAINABLE FOREST MANAGEMENT IN PENINSULAR MALAYSIA<br />

health for environmental stability, to provide sanctuary for wildlife and to serve as an invaluable<br />

storehouse of genetic resources useful for indigenous tree species, agricultural crops and<br />

livestock. This renewal asset will continue to be managed in accordance with national objectives<br />

and priorities so that the country will continue to enjoy the benefits generated from the forests<br />

and forest industries.<br />

Malaysia’s commitment to sustainable forest management is best reflected through her<br />

achievements in the formulation of the comprehensive National Forestry Policy and the National<br />

Forestry Act, the establishment and gazettement of PRF and a network of conservation areas,<br />

and the marked progress made in forestry research and development. It is further attested by<br />

the operationalisation and implementation of the Malaysian Criteria, Indicators and Activities<br />

for Assessing Sustainable Forest Management based on the elaboration of the ITTO Criteria<br />

and Indicators for Sustainable Management of Natural Tropical Forest, and the allocation of<br />

financial resources to carry out forest development activities, as well as projects and studies<br />

related to sustainable management.<br />

Sustainable forest management is the principle of the forest management practices in Malaysia<br />

and the Forestry Department will continue to enhance and improve its management practices<br />

in the light of new research findings, innovative technologies, better skills and knowledge.<br />

Thus, it will demand conscientious effort, a lot of hard work and a strong commitment,<br />

determination and collaboration from the government, private sectors and non-governmental<br />

organizations (NGOs).<br />

REFERENCES<br />

ABDUL RASHID, M.A. 2005. Forest Management In Malaysia. Paper presented during the<br />

Malaysian Timber Mission to Australia & New Zealand, 7–11 April 2005. Forestry<br />

Department Peninsular Malaysia, Kuala Lumpur.<br />

ANONYMOUS. 1993. Final project reports Project PD10/87 (F) – Forest Management of<br />

Natural Forest In Malaysia. Report presented to the International Tropical Timber<br />

Organisation (ITTO). Forestry Department Peninsular Malaysia, Kuala Lumpur, Malaysia.<br />

ANONYMOUS. 1995. National Forestry Policy 1978 (Revised 1992). Forestry Department<br />

Peninsular Malaysia, Kuala Lumpur, Malaysia.<br />

ANONYMOUS. 1996. Forestry In Peninsular Malaysia. Forestry Department Peninsular<br />

Malaysia, Kuala Lumpur, Malaysia.<br />

ANONYMOUS. 2004. Forestry Statistics Peninsular Malaysia 2003. Forestry Department<br />

Peninsular Malaysia. Kuala Lumpur, Malaysia.<br />

ANONYMOUS. 2005. Convention On Biological Diversity Handbook. Secretariat of the<br />

Convention on Biological Diversity. Montreal, Canada.<br />

IUCN/UNEP/WWF. 1980. World Conservation Strategy. IUCN, Gland, Switzerland.<br />

MOHD YUNUS, Z. 1993. Determination Of The Optimum Cut and Rotation In Malaysian<br />

Production Forests: An Economic Approach. MPhill. Dissertation, University Of Wales,<br />

Bangor, UK.<br />

MOHD YUNUS, Z. & MANGSOR, M.Y. 2002. Telok Bahang Forest Trails An Oldest Tropical<br />

Rainforest In The City’s Vicinity, Penang Malaysia. Penang State Forestry Department,<br />

Penang, Malaysia. Pp. 6 & 7.<br />

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MOHD YUNUS, Z., MANGSOR, M.Y., SHEIKH ABU BAKAR & A. YUSOF, S. 2003.<br />

Commercialise: Forest Knowledge and Beauty. Paper presented at the KUSTEM 2 nd Annual<br />

Seminar On Sustainability Science and Management. Kolej Universiti Sains & Teknologi<br />

Malaysia, Terengganu, Malaysia.<br />

ZUL MUKHSHAR, M.S. 2000. The Role Of Forestry Department Peninsular Malaysia In<br />

The Management And Conservation Of Protected Areas. Paper presented at the Workshop<br />

on the Management And Conservation of Protected Area: Administrative and Legislative<br />

Issues. Forestry Department Peninsular Malaysia, Kuala Lumpur, Malaysia.<br />

241


WONG KHOON MENG (2007)<br />

STATUS OF BIOLOGICAL DIVERSITY IN MALAYSIA &<br />

THREAT ASSESSMENT OF PLANT SPECIES IN MALAYSIA<br />

PLANT BIOGEOGRAPHY OF THE<br />

MALAYSIAN REGION<br />

Wong Khoon Meng<br />

ABSTRACT<br />

The major characteristics of Malaysia’s rich plant diversity are explored. Basic ideas in plant<br />

geography are recapitulated, outlining the interest and significance of studying plant<br />

distributions. The biogeography of the Malaysian region focuses on two principal components:<br />

the distribution of taxa within the region, which identify the Riau Pocket and other<br />

biogeographical elements, and affinities between geographical areas, such as the Malesian<br />

and Australasian floras. Aspects of historical biogeography, pertaining to changes in distribution<br />

with reference to earth history, i.e., geological processes and changes through geologic time<br />

(including plate tectonics, continental drift and “interplate dispersal” of plants, and climatic<br />

change), and ecological biogeography, addressing patterns of distribution in relation to<br />

prevailing environmental conditions (such as the Malesian demarcation knots and local<br />

edaphically controlled floristic differences), are dealt with. The biogeographical setting of the<br />

Malaysian region is summarized in terms of the biogeographical units recognized via repeated<br />

floristic patterns (the Malay Peninsula, Perak, the Riau Pocket and NW Borneo hotspot, the<br />

Kapuas-Lupar region, the East Coast Sabah subprovince, and seasonal Asiatic intrusions);<br />

sharp ecological definitions and isolated environments (high mountains, limestone hills,<br />

ultramafic sites, kerangas-peat swamp complexes) and the apparently high speciation rates in<br />

lowland rain forests.<br />

Rimba Ilmu Botanic Garden, Institute of Biological Sciences, University of Malaya, 50603 Kuala Lumpur,<br />

Tel: 03–7967 4685; Fax: 03–7967 6150; wong@um.edu.my<br />

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J. GREGSON, R. DE KOK, J. MOAT & S. BACHMAN (2007)<br />

STATUS OF BIOLOGICAL DIVERSITY IN MALAYSIA &<br />

THREAT ASSESSMENT OF PLANT SPECIES IN MALAYSIA<br />

APPLICATION OF GIS TO CONSERVATION<br />

ASSESSMENTS AT THE ROYAL BOTANIC<br />

GARDENS, KEW<br />

J. Gregson, R. de Kok, J. Moat & S. Bachman<br />

ABSTRACT<br />

As part of its conservation work in areas such as Madagascar and Cameroon, the GIS unit at<br />

the Royal Botanic Gardens, Kew has developed the use of Geographical Information Systems<br />

(GIS) in making rapid conservation assessments. These applications assist Kew staff to make<br />

better informed species conservation status assessments, such as International Union for<br />

Conservation of Nature and Natural Resources (IUCN) ratings, based not only on herbarium<br />

and field data, but also on up to date vegetation maps, physical and climatic conditions and<br />

known threats. This article gives an overview of the work of the South-East Asia Section at<br />

Kew, and reviews the algorithms used by the GIS unit which are relevant to the Malaysian<br />

Plant Red Data Project.<br />

INTRODUCTION<br />

The Royal Botanic Gardens, Kew has been at the forefront of plant taxonomy research for<br />

over 150 years, and has a long history of research and collaboration in South-East Asia. As<br />

scientists have become more aware of the worldwide threat to biodiversity, the focus of Kew’s<br />

work has moved in recent years towards plant conservation and sustainable use of plants. A<br />

variety of work is being undertaken in these areas: baseline biodiversity research (producing<br />

inventories and check-lists); production of support materials, such as field-guides; seed-banking<br />

and development of specialised horticultural techniques with a view to future re-introductions<br />

and forest restoration; research into sustainable use of plants; and vegetation mapping and<br />

conservation assessments using Geographic Information Systems (GIS). This work is carried<br />

out in collaboration with local institutions, with an emphasis on training and capacity-building.<br />

Baseline biodiversity research is being undertaken with contributions to regional floras such<br />

as Flora Malesiana (Chrysobalanaceae (Prance 1989), Nepenthaceae (Cheek & Jebb 2001))<br />

and the Tree Flora of Sabah and Sarawak (Aquifoliaceae (Andrews 2002), Chrysobalanaceae<br />

(Prance 1995), Dipterocarpaceae (Ashton 2004)). Inventories and check-lists are also being<br />

produced, for regions including Mt Kinabalu (Beaman 1992-2004), Brunei (Coode et al. 1996),<br />

Department of Botany, Natural History Museum, Cromwell Road, London SW7 5BD, U.K. Tel: +44(0)20 7942<br />

5349; j.gregson@nhm.ac.uk<br />

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APPLICATION OF GIS TO CONSERVATION ASSESSMENTS AT THE ROYAL BOTANIC GARDENS, KEW<br />

Mt Jaya and Vogelkop (New Guinea), and the Maliau Basin, Danum Valley and Imbak Valley<br />

in Sabah. Kew is also working on World Checklists of various groups: Monocots, Labiates,<br />

Euphorbiaceae, Rubiaceae, Conifers, Araliaceae, Sapotaceae, Fagales and Magnoliaceae have<br />

been completed to date.<br />

Kew is also active in bioinformatics, and several computer-based interactive keys have been<br />

produced or are being worked on, including Rattans of Borneo, Rattans of Laos and an<br />

interactive key to the families of the Flora Malesiana region (Malesian Key Group 2004).<br />

Projects can include the production of field guides, which are an invaluable identification aid<br />

and educational tool: current projects include the production of a Field Guide to the Forest<br />

Trees of Southern Thailand, and a project to assess and conserve plant diversity in commercially<br />

managed tropical rainforests in eastern Sabah, both with funding from the UK Darwin Initiative.<br />

Kew offers a wide range of training opportunities, from informal courses and support to<br />

international courses in Herbarium Techniques, Botanic Garden Management, Plant<br />

Conservation Strategies and Tropical Plant Identification.<br />

The herbarium at Kew also contains a dedicated GIS unit, which provides GIS and Remote<br />

Sensing support for Kew, and works on various projects around the world. GIS is a useful tool<br />

for speeding up conservation assessments, by automating initial IUCN ratings based on<br />

herbarium specimen data, and by using analysis of plant distribution patterns combined with<br />

other geographical data to inform conservation planning. This paper looks at some of the<br />

ways in which GIS has been used to help with conservation assessments, looking at examples<br />

of past and current projects the unit is working on.<br />

Geographical Information Systems (GIS) is a more powerful version of a conventional printed<br />

map, with the advantage that different sets of information can be extracted from the map, as<br />

required. In addition, databases can be linked to the geographical information stored in the<br />

map, and this data can be analyzed and modeled spatially using computer software. GIS has<br />

many applications, and can be put to use in the field of plant conservation in two main ways:<br />

using herbarium specimen data, and vegetation mapping using data from remote sensing.<br />

Point Distribution Maps<br />

GIS AND HERBARIUM SPECIMEN DATA<br />

The information contained in herbarium specimen labels provides a large and useful database,<br />

which includes spatial data (locality information) and temporal data (collection dates), which<br />

is ideal for analysis by GIS. Research into plant taxonomy at Kew has generated a large body<br />

of information in plant systematics as well as accumulating one of the largest and most complete<br />

herbarium collections in the world. This information, especially when combined with data<br />

from other herbaria, can be put to use developing advice for biodiversity conservation planning<br />

(e.g., Schatz 2002).<br />

Many families with particular expertise at Kew, for example Palms and Rubiaceae, have been<br />

studied in depth and large databases have been created for these families using data from the<br />

Kew Herbarium and other herbaria around the world; the locality information recorded on<br />

these specimens has been looked up in atlases and gazetteers and translated into numerical<br />

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J. GREGSON, R. DE KOK, J. MOAT & S. BACHMAN (2007)<br />

coordinates (georeferencing) suitable for analysis by GIS. Although the data originates from<br />

different eras and is of varying accuracy, the accuracy of herbarium specimen records can be<br />

weighted, to take into account imprecise locality data from older specimens. A series of inhouse<br />

tools have been developed to aid georeferencing of Kew’s herbarium specimens including<br />

converting co-ordinates from different projections e.g. UTM and taking bearings from a known<br />

locality e.g. ‘20 miles north of Gaborone’.<br />

The software used by the GIS unit includes all ESRI products (previously ArcView and now<br />

ArcGIS 9) and ERDAS primarily for remote sensing work. The Digital Chart of the World<br />

can be used as a standard base map for plotting species point distribution maps. Additional<br />

maps (called layers) can then be added and queries between the map layers are possible.<br />

Standard GIS techniques and algorithms have been used in a variety of ways and are continually<br />

being developed for novel applications.<br />

A simple example (Fig. 1) shows a point distribution map combined with a map of geological<br />

substrate. A histogram can be quickly plotted showing how the distribution of different species<br />

varies with geological substrate. By combining point distribution maps with other types of<br />

map, histograms can be produced to show the range of substrates, vegetation types or altitudes<br />

which a particular species prefers – this information can be used in conservation planning,<br />

Fig. 1. Analysis of distribution in relation to geological substrate.<br />

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APPLICATION OF GIS TO CONSERVATION ASSESSMENTS AT THE ROYAL BOTANIC GARDENS, KEW<br />

also to locate where a species may occur and has not been collected or even for the reintroduction<br />

of a species.<br />

A revision of the Leguminosae of Madagascar (Du Puy et al. 2001) has provided the basis for<br />

applying GIS to the investigation of ecological parameters which determine the extent of<br />

species distributions. The revision produced a database of Papilionoid Legumes in Madagascar,<br />

giving the co-ordinates of each collection locality, which could be used to make a point<br />

distribution map. The species distribution map was then compared with other map layers in<br />

the system, such as altitude, substrate, climate or vegetation type and the results gave much<br />

greater precision of altitudinal ranges, substrate preferences (both difficult to determine<br />

accurately in the field, leading to inaccurate data on specimen labels) and data on other<br />

ecological parameters which dictate the distribution patterns of the species.<br />

This data on ecological parameter preferences of species, combined with map layers, can be<br />

used to predict the full possible distribution of a species, filling in the apparent gaps caused by<br />

under-collection in certain areas: a technique called gap analysis (Scott et al. 1993). Point<br />

distribution maps only show where species have been collected, and not necessarily the whole<br />

range of a species: the points are often concentrated along roads and rivers or other easily<br />

accessible areas. However, by applying this technique, the full distribution of a species can be<br />

predicted from incomplete point distribution maps.<br />

Other techniques have also been developed from this project, and are discussed below.<br />

GIS AND IUCN RATINGS<br />

One of the primary targets agreed under the Global Strategy for Plant Conservation (Anon.<br />

2002) is “A preliminary assessment of the conservation status of all known plant species, at<br />

national regional and international levels” (Target (a) (ii)) – to be achieved by 2010. However,<br />

currently less than 3% of vascular plants have a global conservation status using the IUCN<br />

criteria, and between 2003 and 2004, the number of species evaluated and published was<br />

similar to the number of new species described during that period. The rate at which IUCN<br />

ratings can be assigned and published therefore needs to be dramatically increased if this<br />

target is to be met, and if IUCN ratings are to be of use in conserving plant biodiversity.<br />

GIS can be used as a tool for applying IUCN ratings as certain parameters used in IUCN Red<br />

List criteria can be quickly calculated from databased and georeferenced species. Using<br />

herbarium datasets, scripts have been developed in Avenue (ArcView’s programming language)<br />

to automate the calculation of Extent of Occurrence (EOO), Area of Occupancy (AOO),<br />

estimates of the number of subpopulations as well as the number of collections and number of<br />

unique localities. Willis et al. (2003) used herbarium data in Red List assessments of<br />

Plectranthus from eastern and southern tropical Africa, and describe the GIS techniques used.<br />

Extent of occurrence (EOO)<br />

The spatial distribution (range) of a species can be used in assessing its conservation status, as<br />

a species with a small distribution, or a distribution fragmented in few locations, is likely to be<br />

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J. GREGSON, R. DE KOK, J. MOAT & S. BACHMAN (2007)<br />

more threatened than a species which is continuously distributed over a large geographical<br />

area. Distribution is also the parameter which is most suitable for GIS analysis.<br />

IUCN criteria recognise two types of range-related attributes of a species: extent of occurrence”<br />

(EOO) is the area that includes all sites of occurrence of a species (Fig. 2a), and “area of<br />

occupancy” (AOO, discussed below) is the area within a species’ extent of occurrence which<br />

is currently occupied by the species (Fig. 2b).<br />

In order to assign a category of threat to a species, five quantitative criteria are defined (criteria<br />

A-F), and at least one needs to be met for a species to qualify as threatened, but a species<br />

should be tested against all criteria where possible. Various parameters are used in each criterion<br />

and extent of occurrence is used in Criteria A (declining population) and B (geographical<br />

range size, and fragmentation, decline or fluctuations).<br />

IUCN defines the extent of occurrence as “the area contained within the shortest continuous<br />

imaginary boundary which can be drawn to encompass all the known, inferred or projected<br />

sites of present occurrence of a taxon…EOO can often be measured by a minimum convex<br />

polygon (the smallest polygon in which no internal angle exceeds 180 degrees and which<br />

contains all the sites of occurrence).” (IUCN 2001).<br />

Extent of occurrence can be calculated within a GIS by:<br />

1. importing georeferenced data<br />

2. plotting a point distribution map<br />

3. generating a polygon enclosing the points<br />

4. calculating the area of the shape<br />

An algorithm should be used to ensure the shape is drawn in the same way each time (Willis<br />

et al. 2003). In addition it should be noted that the EOO calculation can only be made when<br />

there are at least three unique localities.<br />

IUCN (2001) recommend that EOO is calculated using a minimum convex polygon (also<br />

called a convex hull), (see above). However, Burgman & Fox (2003) showed that estimates<br />

based on minimum convex polygons are often biased, affected by the spatial arrangement of<br />

the habitat, the sample size and the spatial and temporal distribution of the sampling. The use<br />

of Alpha hulls is recommended for estimating EOO as this method can reduce (but not eliminate)<br />

these errors.<br />

Scripts have been developed for automating EOO calculations in ArcGIS using Alpha-hulls.<br />

Problems may arise when trying to define the value of alpha (). IUCN (2005) suggest a<br />

value of 2 as ‘a good starting point, but no further information is available.<br />

Area of occupancy (AOO)<br />

IUCN defines area of occupancy as “the area with its ‘extent of occurrence’ which is occupied<br />

by a taxon” (IUCN 2001). This definition reflects the fact that a species will not usually occur<br />

throughout the area of its extent of occurrence, which may contain unsuitable or unoccupied<br />

habitats. AOO is used in Criteria A (declining population), B (geographical range size, and<br />

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APPLICATION OF GIS TO CONSERVATION ASSESSMENTS AT THE ROYAL BOTANIC GARDENS, KEW<br />

fragmentation, decline or fluctuations). and D (very small population or very restricted<br />

distribution).<br />

IUCN recommends obtaining estimates by counting the number of occupied cells in a uniform<br />

grid that covers the entire range of a taxon, then tallying the total area of all occupied cells<br />

(Fig. 2b). This is a calculation that can be easily automated within a GIS.<br />

One problem which arises with area of occupancy calculations is that the results of this method<br />

are highly influenced by the placement of the grid. For example, if an organism is found at<br />

four localities that are less distant from each other than the distance across a grid cell, the<br />

calculated area of occupancy can vary by a factor of four (White 2004). This problem can be<br />

reduced by searching for a grid position which minimizes the area of occupancy. White (2004)<br />

describes a method for automating this procedure within ArcView and concludes that “the<br />

arbitrary nature of using fixed grid methods should be avoided”. Using an automated method<br />

has the advantage that it results in a consistent grid placement, ensuring consistent results if<br />

the procedure is replicated (Willis et al. 2003).<br />

However, another problem arises with calculating AOO because the “size of the area of<br />

occupancy will be a function of the scale at which is measured, and should be at a scale<br />

appropriate to relevant biological aspects of the taxon, the nature of the threats and the available<br />

data” (IUCN 2001). For example if a species has been rarely sampled, then the distance between<br />

observed locations might reflect a lack of observations rather than a lack of occupied habitat<br />

and a coarser grid may therefore be more appropriate. It is therefore not appropriate to use one<br />

set cell size for a wide range of taxa, but what is an appropriate grid size to use when automating<br />

AOO calculations?<br />

The guidelines for using the IUCN criteria (IUCN 2005) recommend a grid size of 2 km,<br />

recognising that for intensely sampled species, a finer grid of 1 km may be more appropriate,<br />

and for sparsely sampled species, a coarser grid. Grid sizes of more than 3.2 km are not<br />

recommended as they preclude the listing of species as Critically Endangered (CR) because<br />

the AOO threshold for CR is 10 km 2 . A method is described of standardising AOO estimates<br />

by scaling the AOO estimate up or down to the reference scale (a 2 km grid size).<br />

Willis et al. (2003) suggest that a suitable grid cell width/height is one tenth of the maximum<br />

distance between any two points on the extent of occurrence polygon. This effectively scales<br />

AOO to the EOO measurement and has given good results so far. Calculations of AOO using<br />

this ‘sliding scale’ grid width/height are currently adopted by the GIS unit at Kew, although<br />

the grid cell size can be manually set by the user within the application. AOO can also be<br />

calculated when there are only two unique localities; the ‘sliding scale’ technique can be used<br />

where grid cell width/height is one tenth of the distance between the two points.<br />

Number of Sub-populations<br />

IUCN defines sub-populations as “geographically or otherwise distinct groups in the population<br />

between which there is little demographic or genetic exchange” (IUCN 2001). Subpopulations<br />

are used in Criteria B (geographical range size, and fragmentation, decline or fluctuations)<br />

and C (small population size and fragmentation, decline or fluctuations). Two techniques for<br />

estimating the number of subpopulations of a species have been developed: the cell adjacency<br />

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J. GREGSON, R. DE KOK, J. MOAT & S. BACHMAN (2007)<br />

method (Schatz 2002) and Rapoport’s mean propinquity method (Willis et al. 2003), (Fig. 2c).<br />

The cell adjacency method considers all contiguous grid cells from the AOO calculations to be<br />

a single subpopulation. Rapoport’s mean propinquity technique is based on the mean line<br />

length of a minimum spanning tree (a set of lines that connect all points in the minimum<br />

possible distance). Subpopulations are separated where the limb (line) distance is greater than<br />

twice the mean limb distance (Willis et al. 2003).<br />

Other parameters<br />

The above three parameters have the advantage that they can be calculated quickly, easily and<br />

automatically from georeferenced data sets, and can be used to assign preliminary conservation<br />

ratings to species using IUCN Criteria. For taxa that are threatened, a more detailed ‘desktop’<br />

conservation assessment may be required and GIS can be of use here too. Habitat level data<br />

can be used to infer declines at the species level. Remote sensing imagery including aerial<br />

photographs and satellite images were used to see how forest cover changed over time at<br />

Mount Oku and Ijim Ridge in Cameroon (Baena 2005).<br />

A B C D<br />

Fig. 2. Examples of EOO, AOO and subpopulations calculations using GIS. From Willis et al.<br />

(2003).<br />

Habitat fragmentation for each species distribution can also be calculated: the preferred habitat<br />

of the species is first identified from the label, and species distributions compared to habitat<br />

datasets. Fragmentation of habitats can be calculated using Fragstats program and Patch Analyst<br />

in ArcView. Consideration needs to be made as to which metric of fragmentation is used;<br />

again there may not be a ‘one size fits all’ solution. It may also be possible to develop indices<br />

of fragmentation based on the subpopulation techniques as discussed above. Biological meaning<br />

can be added to the distances between subpopulations, i.e., by considering dispersal ability so<br />

that a more realistic measure of fragmentation can be obtained.<br />

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GIS AND VEGETATION MAPPING<br />

As noted above, currently only c. 3% of vascular plants have a global conservation status<br />

using the IUCN criteria, and so in some areas, much more rapid methods of conservation<br />

assessment may be required.<br />

Analysis of vegetation maps in GIS can be a powerful tool for rapid conservation prioritization.<br />

GIS analyses provide solid scientific data, which can be used for planning and management of<br />

biodiversity conservation. This technique produces relatively rapid biodiversity assessments,<br />

and so is particularly suited to conservation hotspots where information on the distribution<br />

and rarity of the vast majority of plant species is scarce, and habitats are being destroyed<br />

faster than individual species distribution data is being compiled.<br />

Madagascar is one such conservation hotspot with high biodiversity and a high level of<br />

endemism, which is under threat from habitat degradation and destruction. At Kew, the methods<br />

described below have been used successfully in Madagascar to identify conservation priorities,<br />

and similar techniques may be applicable in other conservation hotspot areas such as South-<br />

East Asia.<br />

Case study: vegetation mapping in Madagascar<br />

Du Puy & Moat (1998) used the Papilionoid Legume specimen database to demonstrate that<br />

certain parameters such as seasonality and substrate (underlying rock type) have an effect on<br />

species distribution (see discussion above). Distinct preferences can be demonstrated for many<br />

species, such as exclusive occurrence in seasonally dry or perennially humid habitats, on a<br />

certain geological type such as limestones, quartzites or sand (Du Puy & Moat 1998). A more<br />

informative vegetation map can therefore be made by dividing the broad vegetation zones<br />

into narrow vegetation types based on rock type, which reflect the distribution of individual<br />

species, so that each type of vegetation contains its own distinctive range of species. This<br />

subdivision of vegetation zones based on underlying rock types is therefore a way of rapidly<br />

estimating patterns of individual species distributions. If as many vegetation types as possible<br />

are included in reserves, the resulting network of protected areas will contain as large a diversity<br />

as possible. This technique has been successfully applied to conservation and planning and<br />

management of protected areas in Madagascar (Du Puy & Moat 1996).<br />

Initially, a map of remaining primary vegetation in Madagascar was derived from satellite<br />

imagery. Classification and mapping was done by remote sensing techniques, using Landsat<br />

and Spot data (Faramalala 1988).<br />

In the next step, a geological map was digitised and simplified to rock types affecting vegetation<br />

(e.g. limestone, lavas etc). A composite map was then produced, of vegetation zones and rock<br />

types, showing patterns of variation within vegetation zones (Fig. 3). Each vegetation zone<br />

subdivision (vegetation type) will contain a different suite of species, so the maximum number<br />

of species can be preserved by conserving as many of the vegetation zone subdivisions as<br />

possible.<br />

The current degrees of protection for each vegetation type were quantified, by overlaying a<br />

map of protected areas onto the vegetation types map. Amounts of protection for each type<br />

252


J. GREGSON, R. DE KOK, J. MOAT & S. BACHMAN (2007)<br />

Fig. 3 (From Du Puy & Moat 1998)<br />

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APPLICATION OF GIS TO CONSERVATION ASSESSMENTS AT THE ROYAL BOTANIC GARDENS, KEW<br />

were automatically calculated in ArcView, and the results displayed on histograms (Fig. 4),<br />

enabling poorly protected areas to be identified.<br />

This technique enables plant diversity assessments of hotspot areas to be compiled relatively<br />

rapidly, which can then be used to identify conservation priorities, so that new reserves can be<br />

targeted to conserve the greatest possible diversity of species.<br />

Fig. 4. (From Du Puy & Moat 1998).<br />

FUTURE WORK<br />

The GIS unit at RBG Kew is continuing to develop techniques to aid conservation efforts, in<br />

particular through improving automated conservation assessments based on IUCN Categories<br />

and Criteria. Ecological niche modelling has been investigated as a potential tool for estimating<br />

species range size and may be useful in delimiting isolated populations, therefore informing<br />

studies of fragmentation. Lack of data may be the biggest problem for these techniques as<br />

large numbers of data points (i.e. unique localities) are often needed to a) run the algorithms<br />

and b) validate the final models. As previously mentioned an index for fragmentation based<br />

on Rapoport’s mean propinquity method and dispersal ability is also being investigated. The<br />

algorithms for the methods as outlined above are available from the GIS unit upon request.<br />

This initial work on the Madagascar Vegetation is being updated using remote sensing<br />

techniques for the year 2000/1/2 (Anon. 2005) This uses MODIS imagery, which separates<br />

vegetation classes with a single-date surface reflectance image combined with entire year<br />

vegetation greenness data. Composite images of Landsat ETM imagery were used to eliminate<br />

cloud cover. An initial classification separated 11 land cover classes, and then a higher resolution<br />

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J. GREGSON, R. DE KOK, J. MOAT & S. BACHMAN (2007)<br />

subsequently (from 250 metres to 30 metres) obtained, using Landsat ETM (enhanced thematic<br />

mapper) on board Landsat 7.<br />

CONCLUSION<br />

Recent advances in information technology have led to the development of computer based<br />

methods in conservation biology, and GIS is a particularly useful tool for plant conservation.<br />

Target 2 of the Global Strategy for Plant Conservation aims for “a preliminary assessment of<br />

the conservation status of all known plant species, at national, regional and international levels”<br />

(Anon. 2002) but at current rates, this target will take a long time to reach. GIS can speed up<br />

this process by providing a means to automate the preliminary assessment of the conservation<br />

status of a particular species based upon specimen information present within existing major<br />

collections.<br />

The application of these methods is limited by the availability of data and the uncertainties in<br />

the available data. These GIS techniques require large amounts of georeferenced specimen<br />

data, and such databases are often the product of taxonomic work. However, new technologies<br />

facilitating data transfer and electronic publication now make it possible for data held within<br />

institutions to be shared and analysed collaboratively.<br />

ACKNOWLEDGEMENTS<br />

We thank the following members of staff at the Royal Botanic Gardens, Kew for their<br />

contributions to this paper: Sharon Balding, Stuart Cable, Colin Clubbe, Robyn Cowan,<br />

Matthew Daws, Michael Fay, Roger Joiner, Eimear Nic Lughadha, Simon Owens, Hugh<br />

Pritchard, Margaret Ramsay, Moctar Sacandé, Vincent Sarasan, Paul Smith, Roger Smith,<br />

Nigel Taylor, Clare Tenner and Christopher Wood.<br />

REFERENCES<br />

ANDREWS, S. 2002. Aquifoliaceae. Pp. 1–28 in Soepadmo, E., Saw, L.G. & Chung, R.C.K.<br />

(eds) Tree Flora of Sabah and Sarawak. Vol. 4. Forest Research Institute Malaysia, Kuala<br />

Lumpur.<br />

ANON., 2002. Global Strategy for Plant Conservation. Published by the Secretariat of the<br />

Convention on Biological Diversity, Quebec.<br />

ANON., 2005. CEPF Madagascar Vegetation Mapping Project. Availabe at http://<br />

www.vegmad.org/<br />

ASHTON, P.S. 2004. Dipterocarpaceae. Pp. 63–388 in Soepadmo, E., Saw, L.G. & Chung,<br />

R.C.K. (eds) Tree Flora of Sabah and Sarawak. Vol. 5. Forest Research Institute Malaysia,<br />

Kuala Lumpur.<br />

BAENA, S. 2005. Monitoring vegetation cover changes in Mount Oku and the Ijim Ridge<br />

(Cameroon) using satellite and aerial sensor detection. Available at http://www.kew.org/<br />

gis/projects/oku_cameroon/index.html<br />

BEAMAN, J.H. 1992–2004. The Plants of Mount Kinabalu. 5 volumes. Royal Botanic Gardens,<br />

Kew.<br />

255


APPLICATION OF GIS TO CONSERVATION ASSESSMENTS AT THE ROYAL BOTANIC GARDENS, KEW<br />

BURGMAN, M. & FOX, C. 2003. Bias in species range estimates from minimum convex polygons:<br />

implications for conservation and options for improved planning. Animal Conservation 6:<br />

19–28.<br />

CHEEK, M. & JEBB, M. 2001. Nepenthaceae. Flora Malesiana 15, Ser. I: Vol. 15. Nationaal<br />

Herbarium Nederland, Leiden. 164 pp.<br />

COODE, M., DRANSFIELD, J., FORMAN, L., KIRKUP, L. & SAID, I. (eds.) 1996. A checklist<br />

of the flowering plants and gymnosperms of Brunei Darussalam. Ministry of Industry<br />

and Primary Resources, Brunei Darussalam. 494 pp.<br />

DU PUY, D.J. & MOAT, J.F. 1996. A refined classification of the primary vegetation of<br />

Madagascar based on the underlying geology: using GIS to map its distribution and to<br />

assess its conservation status. Pp. 205–218 in Lourenço W.R. (ed.) Proceedings of the<br />

International Symposium on the Biogeography of Madagascar. Editions de l’ORSTROM,<br />

Paris.<br />

DU PUY, D.J. & MOAT, J.F. 1998. Vegetation mapping and classification in Madagascar<br />

(using GIS): implications and recommendations for the conservation of biodiversity. Pp.<br />

97–117 in Huxley, C.R., Lock, J.M. & Cutler, D.F. (eds.) Chorology, taxonomy and<br />

ecology of the Floras of African and Madagascar. Royal Botanic Gardens, Kew.<br />

DU PUY, D.J., BOSSER, J., RABEVOHITRA, R., VILLIERS, J., LABAT, J. & MOAT, J.F.<br />

2001. The Leguminosae of Madagascar. Royal Botanic Gardens, Kew. 720 pp.<br />

FARAMALALA, M.H. 1988. Etude de la Végétation de Madagascar à l’aide des Données<br />

spatiales. Doctoral Thesis, Univ. Paul Sabatier, Toulouse. 167 pp.<br />

IUCN 2001. IUCN Red List Categories and Criteria. Version 3.1. IUCN Species Survival<br />

Commission. IUCN, Gland, Swizerland and Cambridge, UK.<br />

IUCN 2005. Guidelines for Using the IUCN Red List Categories and Criteria. IUCN Species<br />

Survival Commission. IUCN, Gland, Swizerland and Cambridge, UK.<br />

PRANCE, G.T. 1989. Chrysobalanaceae. Flora Malesiana 10, Ser. I: 635–678.<br />

PRANCE, G.T. 1995. Chrysobalanaceae. Pp. 155–180 in Soepadmo, E. & Wong, K.M. (eds.)<br />

Tree Flora of Sabah and Sarawak, Vol. 1. Forest Research Institute Malaysia, Kuala<br />

Lumpur.<br />

SCHATZ, G. 2002. Taxonomy and Herbaria in Service of Plant Conservation: Lessons from<br />

Madagascar’s Endemic Families. Annals of the Missouri Botanic Gardens 89(2):<br />

145–152.<br />

SCOTT, J.M., DAVIS, F., CSUTI, B., NOSS, K., BUTTERFIELD, B., GROVES, C.,<br />

ANDERSON, H., CAICCO, S., D’ERCHIA, F., EDWARDS, T.C. Jr, ULLIMAN, J. &<br />

WRIGHT, R. 1993. Gap Analysis: A geographic approach to protection of biological<br />

diversity. Wildlife Monograph 123. 41 pp.<br />

The Malesian Key Group 2004. An Interactive Key to Malesian Seed Plants Version 1.0. The<br />

Nationaal Herbarium Nederland, Leiden & The Royal Botanic Gardens, Kew. Available<br />

at http://www.rbgkew.org.uk/herbarium/keys/fm/<br />

WHITE, J. 2004. Range size, error rates and the geometry of rare species distributions. In<br />

Brooks, M., Carothers, S. & La Banca, T. (eds.) The Ecology and Management of Rare<br />

Plants of Northwestern California: Proceedings from a 2002 Symposium of the North<br />

Coast Chapter of the California Native Plant Society. CNPS Press, Sacramento, CA.<br />

226 pp.<br />

WILLIS, F., MOAT, J. & PATON, A. 2003. Defining a role for herbarium data in Red List<br />

assessments: a case study of Plectranthus from eastern and southern tropical Africa.<br />

Biodiversity and Conservation 12: 1537–1552.<br />

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C. LUSTY, W.A.N.AMARAL, W. D.HAWTHORNE, L.T. HONG & S. OLDFIELD (2007)<br />

STATUS OF BIOLOGICAL DIVERSITY IN MALAYSIA &<br />

THREAT ASSESSMENT OF PLANT SPECIES IN MALAYSIA<br />

APPLYING THE IUCN RED LIST CATEGORIES<br />

IN A FOREST SETTING<br />

1<br />

C. Lusty, 2 W. A. N. Amaral, 3 W. D. Hawthorne,<br />

4<br />

L. T. Hong & 5 S. Oldfield<br />

ABSTRACT<br />

The IUCN-The World Conservation Union Red List categories provide a globally-accepted<br />

framework for classifying animal and plant taxa according to their risk of extinction. Different<br />

versions of the categories have been in use for forty years. Their present form, version 3.1<br />

published in 2001, demands a quantitative assessment of species status, and has been carefully<br />

designed to accommodate the spectrum of case-studies from large mammals to mosses or<br />

commercially-exploited trees to poorly-known insects. Consequently, the categories are<br />

assigned by the use of any one of five major criteria that infer either past or potential species<br />

population declines, or habitat declines, restriction in geographical distribution or population<br />

numbers. For the uninitiated assessors of forest species, the categories may present a daunting<br />

need for largely unavailable data. In this paper, we would like to demonstrate that the categories<br />

can be applied through the use of available forest management data, biological inventory<br />

datasets and/or proxy information on habitats, as well as a certain amount of inference or<br />

extrapolation. Developing standards for using the criteria at a national level promotes<br />

consistency, replicability and a shared understanding of the categories. Furthermore, shared<br />

standards can be developed and applied across regions through forest genetic resource networks<br />

and species specialist networks (e.g. APFORGEN and the IUCN Species Survival Commission<br />

(SSC) Global Tree Specialist Group), and contribute to global indicators of biodiversity loss<br />

relevant to the Global Strategy on Plant Conservation and the Convention on Biological<br />

Diversity’s 2010 target.<br />

1<br />

International Plant Genetic Resources Institute (IPGRI), INIBAP, Parc Scientific Agropolis II, 34397 Montpellier –<br />

Cedex 5, France; Fax: +33 467 610334; c.lusty@cgiar.org<br />

2<br />

International Plant Genetic Resources Institute (IPGRI), Via dei Tre Denari 472/a, 00057 Maccarese (Fumicino),<br />

Rome, Italy; Fax: +39 06 61979661;<br />

3<br />

Department of Plant Sciences, University of Oxford, South Parks Road, Oxford, OX1 3RB, UK;<br />

Fax: +44 1865 275074; william.hawthorne@plant-sciences.oxford.ac.uk<br />

4<br />

IPGRI Regional office for Asia, Pacific and Oceania, c/o Stesen Kuarantin Lepas Masuk, Jabatan Pertanian Bangunan<br />

JKR (P) 1746, P.O. Box 236 UPM Post Office, 434 Serdang, Selangor Darul Ehsan Malaysia, +60 3 948 7655;<br />

l.hong@cgiar.org<br />

5<br />

Botanic Gardens Conservation International (BGCI), Descanso House, 199 Kew Road, Richmond, Surrey,<br />

TW9 3BW UK; Fax: +44 208 3325956; sara.oldfield@bgci.org<br />

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INTRODUCTION<br />

In 2002, the Conference of the Parties to the Convention on Biological Diversity (CBD) and<br />

world leaders at the World Summit on Sustainable Development endorsed a commitment to<br />

reduce biodiversity loss by 2010. Among the indicators of biodiversity loss that are being<br />

adopted by the CBD are the IUCN Red List categories. Red List categories and Red Data<br />

books, over the past four decades of use, have become widely recognised as an international<br />

standard and reference for species conservation status. However, only 2.5% of the estimated<br />

number of extant (and recently extinct) species has been assessed; the comprehensively covered<br />

groups being mammals, amphibians, birds, conifers and cycads (Baillie et al. 2004).<br />

Furthermore, at a national or local level, conservation action continues to be geared towards<br />

species that are economically, ecologically or aesthetically attractive at a local level, rather<br />

than to the species which are listed ‘top of the league’ in Red Lists.<br />

It has been the expressed intention of the IUCN Red List categories not to prioritize species<br />

but to provide an objective indicator of extinction risk, which might be used as an initial step<br />

in the conservation prioritization process. In reality, throughout much of the developing world<br />

resource managers carrying out conservation on the ground do not apply or refer to the Red<br />

List categories for multiple reasons. This divorce between the processes of defining<br />

conservation priorities at a local level and global level could give reason to be sceptical of the<br />

2010 targets being monitored appropriately, let alone achieved. However, the Workshop on<br />

Threat Assessment of Plant Species in Malaysia, organized by the Forest Research Institute<br />

Malaysia (FRIM) represents a national level initiative to bring together conservation<br />

practitioners, taxonomists and Red List assessors to provide coherence to the Red List process.<br />

This paper is not an overview of the guidelines for the Red List categories (please see the<br />

official guidelines prepared by the IUCN SSC Red List Programme) but explores their<br />

application when assessors only have access to limited datasets. It also briefly examines the<br />

Red Listing process in comparison to a conservation prioritization process, which might be<br />

adopted by a forest resource manager, and suggests mechanisms by which Red Listing might<br />

be better aligned to conservation action on the ground.<br />

THE EVOLUTION OF THE IUCN RED LISTING SYSTEM<br />

Before 1994, the IUCN proposed a mechanism for Red Listing species that was based entirely<br />

on subjective judgement of experts. Species were categorized according to an increasing order<br />

of extinction risk: from ‘Endangered’, ‘Vulnerable’ to ‘Rare’, and ‘Indeterminate’ for those<br />

species which were threatened to an unknown degree. Responding to recommendations for<br />

the development of a system to promote transparency, objectivity and replicability, several<br />

new versions of the categories were drafted and tested in consultation with experts of different<br />

taxonomic fields over a five-year period. The agreed system, version 2.3, was published in<br />

1994 (IUCN 1994) and presented a quantitative framework for the application of categories<br />

very similar to the present version (3.1). Different animal and plant groups were evaluated<br />

using version 2.3 categories and a number of issues arose, most publicly a controversy on the<br />

listing of commercially-exploited fish species. A Criteria Review Working Group was brought<br />

together to recommend revisions to the system. As a result of their discussions some small but<br />

significant changes were made and version 3.1 was published in 2001 (IUCN 2001; see box<br />

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C. LUSTY, W.A.N.AMARAL, W. D.HAWTHORNE, L.T. HONG & S. OLDFIELD (2007)<br />

entitled “Main differences between versions 2.3 and 3.1.”). A system for the application of<br />

categories at a regional level was also devised and published in 2003 (IUCN 2003).<br />

In version 2.3 and 3.1 the IUCN have striven to develop a scientifically thorough and robust<br />

evaluation system to represent as accurately as possible the risk of species extinction. The<br />

system is impressively flexible in being applicable to a wide range of life forms under very<br />

different types of threat, everything from corals, colonial ants, obscure mosses known only<br />

from one location, ancient redwoods, elephants and commercially-exploited fish species.<br />

Such broad applicability has been achieved through the use of a range of criteria, of which<br />

only one need apply for the allocation of a threat category:<br />

A. Population reduction (past, present or future)<br />

B. Limited geographic range, fragmented, declining or fluctuating<br />

C. Small population size and fragmented, declining or fluctuating<br />

D. Very small population or restricted distribution<br />

E. Quantitative analysis of extinction risk<br />

Each criterion has three quantitative thresholds corresponding to increasing extinction risk:<br />

‘Critically Endangered’, ‘Endangered’ or ‘Vulnerable’. Species that do not meet any thresholds<br />

are considered either to be ‘Near Threatened’, ‘Least Concern’, ‘Data Deficient’ or ‘Not<br />

evaluated’. The thresholds are arbitrary but appear to be generally applicable to a wide range<br />

of threatened taxa. For any one species, the thresholds of some criteria may be inappropriate<br />

but at least one alternative criterion should be applicable. The spirit in which the system was<br />

devised encourages the user to examine each species profile against all five criteria so that the<br />

most relevant and precautionary assessment is attained. For more details you are directed to<br />

the red list categories and guidelines (IUCN 2001; IUCN 2005; http://www.iucnredlist.org/<br />

info/programme.html).<br />

Main differences between versions 2.3 and 3.1 of the IUCN Red List Categories<br />

• New A subcriterion with a more challenging threshold (reductions of at least 50% as<br />

opposed to 20%) for species which are subject to population declines because of known<br />

and reversible threats. This provides leeway for species undergoing a controllable<br />

decline (e.g. commercial exploitation) to avoid classification as threatened until a<br />

more serious population decline has taken place;<br />

• The threshold for species classified under VU A have risen from a 20% population<br />

decline to 30%;<br />

• Allowance of population declines within a ‘moving window’ of the past or future in<br />

A4<br />

• Maximum time cap for derived future declines of 100 years;<br />

• Addition of subcriterion on extreme fluctuations under C2;<br />

• VU D2 guidelines for restricted area of occupancy reduced from 100km 2 to 20km 2<br />

• Loss of ‘Lower Risk - Conservation Dependent’*<br />

• Some important changes in definitions have taken place<br />

• National and regional level assessments possible<br />

* this affects the evaluation of 20% of Peninsular Malaysian tree species which were assessed<br />

against version 3.0 categories – the most appropriate category for these species is now ‘Near<br />

Threatened’<br />

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APPLYING THE IUCN RED LIST CATEGORIES IN A FOREST SETTING<br />

The present version is not expected to be updated in the foreseeable future. A comprehensive<br />

set of guidelines (IUCN 2005) and a documentation format have also been produced. Evaluated<br />

species must now follow a submission system, involving the completion of a four-page<br />

information sheet with a 15-page annex to capture information on habitat, threat, conservation<br />

measures, use and trade. Forms are submitted to the Red List Secretariat and evaluated by the<br />

appropriate Red List Authority. Depending on the approval of the assessment the species will<br />

be published in the next edition of the IUCN Red List of Threatened Species TM .<br />

A QUANTITATIVE ASSESSMENT WHERE FEW<br />

QUANTITATIVE DATA EXIST<br />

All numerical data, as well as less quantitative information, are uncertain to some extent and<br />

most of the difficulty of using the red list categories is related to uncertainty of various kinds<br />

(Akçakaya et al. 2000). Estimating population sizes and declines for individual species depends,<br />

at best, on the use of statistical distributions that are subject to environmental influences, intra<br />

and inter-population variation, or, at worse, on circumstantial information, inferences from<br />

related taxa or trends in the species’ habitat.<br />

The way in which uncertainty within the data is handled has a significant influence on the<br />

outcome of the assessment. Perversely, the more data available on a species the greater the<br />

number of options available to carry out the categorization, and as a consequence additional<br />

uncertainties creep into the assessment and the need for detail in the guidelines increases. An<br />

illustration of this paradox is the category ‘data deficient’, which is intended for both species<br />

that are “well-studied, with biology well known, but where appropriate data on abundance<br />

and/or distribution are lacking”; and for species known from type specimens for which there<br />

are no available data at all.<br />

Data uncertainty is recognized to be a result of either measurement error or natural variation<br />

or semantic vagueness (Akçakaya et al. 2000)—the latter being the payback for designing a<br />

system that has to limit explicitness in order to conserve its general applicability. The authors<br />

of the guidelines and criteria make a considerable effort to describe how assessors deal with<br />

data paucity and uncertainty. Specific methods for dealing with different forms of uncertainty<br />

are developed using fuzzy numbers (Akçakaya et al, 2000). Assessors are suggested to provide<br />

range values and best estimates and describe the means through which these were attained—<br />

through confidence limits or expert opinion etc. They are also advised to be explicit about<br />

their attitude to risk and dispute, both of which influence the interpretation of data and the<br />

management of uncertainty. The qualification of individual species under a range of categories<br />

to reflect data uncertainty is acceptable—although only one category will be published in a<br />

red listing.<br />

Fuzzy numbers are most effective when datasets are relatively rich and measurement error is<br />

the greatest constraint. Where data are poor, the assessor is faced with the quandary of using<br />

estimation, inference and even suspicion in what appears to be a well-defined quantitative<br />

framework. In these cases, where qualitative data are used to answer a quantitative question<br />

the possibilities for interpretational and semantic errors become more significant. For example,<br />

a ‘subpopulation’, which is used in criteria B and C, is defined by rates of genetic exchange<br />

(“typically one successful migrant individual per year or less”). Taking tree species as an<br />

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C. LUSTY, W.A.N.AMARAL, W. D.HAWTHORNE, L.T. HONG & S. OLDFIELD (2007)<br />

example, this knowledge is confidently or partly known for perhaps 100 or so tropical trees in<br />

total, which have been the focus of detailed studies—for lesser known species defining<br />

subpopulations remains highly assumptive, based less on measurement and more on the<br />

assessors willingness to make a judgement based on general ecological knowledge of the<br />

taxonomic group and the presumed extent and distribution of subpopulations. Similarly putting<br />

an estimate on the age of ‘mature individuals’, as a basis for estimates of population size, or<br />

the ‘average age of parents’, the unit for estimating the timeframe within which population<br />

reductions are measured, are challenging for the vast majority of tropical plant species,<br />

especially as these values may not be constant throughout the range of a species.<br />

There are some criteria that are more lenient than others at allowing the use of inference or<br />

proxy data. There are defined terms of assessment based on an increasing degree of assumption:<br />

• Observed is based on firm data.<br />

• Estimated is based on data with an allowance of statistical estimation or assumptions<br />

about observed variables (e.g. indices of abundance) and the measure variable (number<br />

of mature individuals). Estimations are also projected into the future.<br />

• Inferred is a calculation based on indirect evidence but at least within the same units of<br />

measurement (e.g. population declines based on rate of habitat loss). Inferences may also<br />

be made when imposing trends from certain subpopulations to infer the status of lesser<br />

known subpopulations and the global population as a whole.<br />

• Suspected is a type of inference that is based on indirect evidence concerned with another<br />

unit of measurement (e.g. population declines based on changes in habitat quality).<br />

A first step to approaching the Red Listing process might be to realize the potential of the<br />

available dataset and work with the criteria that are suited to the levels of assumption that are<br />

required. For criteria C1 and for D (categories of ‘Endangered’ and ‘Critically Endangered’)<br />

population size must be estimated, whereas criterion A allows the use of proxy data to infer<br />

population reductions.<br />

RULES OF THUMB AND USING PROXY DATA<br />

Rules of thumb can help to tighten the definitions for defined groups of species or geographical<br />

areas so that assessments can be made using a common understanding. Rules of thumb are<br />

“rules of general guidance that are based on experience or practice rather than theory”. They<br />

represent a pragmatic approach to dealing with limited information or circumstances. In the<br />

case of the Red List categories they potentially help to improve replicability, consistency and<br />

Ways of dealing with lack of data:<br />

• estimations, projections, inferences, and suspected trends, including:<br />

– the use of proxy data<br />

– extrapolation from known subpopulations to less well-known subpopulations<br />

– ecological inference from close relatives to less well-known species<br />

• using criteria which are more accepting of qualitative data e.g. A & B<br />

• describing range values and giving best estimates<br />

• establishing rules of thumb<br />

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transparency and introduce some certainty about how the evaluation took place. The guidelines<br />

are full of rules of thumb that are applicable at a general level. However, more specific rules<br />

of thumb may be defined for groups of related taxa or unrelated taxa either with shared life<br />

forms, biological or ecological traits, habitat preferences or geographical ranges.<br />

There are numerous points in the Red List process where decisions on interpretation make a<br />

considerable difference to the assessment and where rules of thumb may be particularly useful;<br />

the interpretation of the main definitions in particular:<br />

1. Generation length/Mature individuals – estimating the average age of parents and when<br />

age at effective reproductive maturity is particularly influential for species exhibiting<br />

wide ranging values (e.g. for trees between 100 years). The interpretation of<br />

these definitions influence estimated population size and the estimated timeframe by which<br />

population declines are judged (Criteria A, B, C & D).<br />

2. Location/Subpopulation/Severely fragmented – defining subpopulations that exist in<br />

almost complete isolation from incoming genetic influence or locations that may be<br />

potentially influenced by a single event is a relatively subjective judgement, especially<br />

for lesser known species. These definitions influence population status estimates (Criteria<br />

B, C & D).<br />

3. Extent of occurrence (EOO)/Area of occupancy (AOO) – measuring EOO and AOO<br />

is entirely subject to the scale of measurement and influence distribution estimates (Criteria<br />

A & B). The guidelines recognise that the scale used should be appropriate to the biological<br />

aspects of the taxon, the nature of threats and available data. Clearly rules of thumb are<br />

called for here.<br />

4. Population reduction/Continuing decline/Extreme fluctuations – depend on<br />

judgements as to whether a decline is part of a natural fluctuation or a more serious<br />

extinction process (Criteria A, B & C). Assessors also must consider whether the trend<br />

will continue.<br />

Developing a common understanding of the spirit of the definitions and how they should be<br />

interpreted or defining rules of thumb within a group of assessors or a network may significantly<br />

speed up and simplify the evaluation process. Using proxy data provides a special case. Where<br />

specific habitat types harbour a number of endemic species, it may be possible to share estimates<br />

of habitat loss among relevant species. Inferences of decreasing habitat extent or quality are<br />

acceptable for criteria A and B. Quantifying the reduction of specific habitat types at a national<br />

level through a consensual approach may facilitate the assessment of diverse species. However,<br />

careful attention should be paid to assessing the habitat-specificity of the species in question<br />

and the impact of forest loss and fragmentation on those species, as well as whether other<br />

criteria may apply. Proxy data should not be used to carry out bulk assessments of large<br />

numbers of species without giving thought in each individual case to whether the species<br />

might be more or less prone to extinction and deserve more detailed assessment.<br />

The other alternative is to give species a category of ‘data deficient’. The problem with this<br />

category is that it is a hold-all for assessments suffering diverse data limitations and has no<br />

application in conservation prioritization. More compelling support for pursuing a path of<br />

assigning threat categories wherever possible is provided by the hundreds of resource managers,<br />

who are making decisions on conservation priorities every day.<br />

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THE CASE OF TREE SPECIES<br />

Between 1995 and 1998 a Dutch Government-funded project undertaken by the World<br />

Conservation Monitoring Centre and the IUCN SSC assessed 10,000 tree species according<br />

to the 2.3 version of the IUCN categories, of which 5999 were threatened and documented in<br />

the World List of Threatened Trees (Oldfield et al. 1998). As part of the project William<br />

Hawthorne reviewed the 2.3 version of the IUCN categories and suggested several rules of<br />

thumb for the application of the criteria and associated definitions; many of which were taken<br />

up and presented as guidelines to the several hundred assessors involved. One of the main<br />

recommendations that arose from his review was that assessing tropical tree species according<br />

to their distribution (i.e. criterion B) is the most appropriate and practical way of optimizing<br />

use of available data; by contrast “approaches via notions of population size or change are<br />

likely to be unreliable or untenable” (Hawthorne 1995).<br />

Examples of rules of thumb used in the assessment of trees include:<br />

– defining mature individuals as those which have reached potential according to their<br />

ecological niche – canopy species which have reached the canopy etc.;<br />

– estimating generation length to be 10–20 years for medium-large pioneer trees, 50 years<br />

for most tropical species and 100 years for slow-growing species;<br />

– measuring EOO for tropical species using degree squares (i.e. slightly more than 100 km<br />

square) and a finer resolution for higher threat categories<br />

More than half the assessments of threatened tree species fulfilled the B criterion and were<br />

assigned the ‘Vulnerable’ category (Table 1). Many of these assessments were ‘inferred’ from<br />

declines in habitat. These are tree species usually from restricted areas of forest type habitats,<br />

which have declined by at least 20% in the past 100 years (i.e., approximately 2–3 tree<br />

generations). The lack of data may have precluded more severe threat categories from being<br />

assigned; available data to estimate population size were very rare and those species that were<br />

assessed using the C criterion were usually highly specified or confined to islands or mountains.<br />

Very few classifications were listed under more than one criterion.<br />

Table 1. The assessment of tree species using the 2.3 version of the IUCN categories<br />

A criterion B criterion C criterion D criterion Total<br />

Declining Population Less than 10,000 Population<br />

population of at confined to individuals and confined to 100<br />

least 20% 20,000km 2 and declining km 2 or 5<br />

declining<br />

locations<br />

% tree species 22% 56% 6% 16%<br />

assessed<br />

Number of 1320 3359 360 960 5999<br />

tree species<br />

assessed<br />

Ex CR EN VU DD<br />

% tree species 2% 16% 22% 60% 5%<br />

assessed<br />

Number of tree 95 976 1,319 3,609 375<br />

species assessed<br />

Source: Oldfield & Lusty (1998)<br />

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APPLYING THE IUCN RED LIST CATEGORIES IN A FOREST SETTING<br />

CONSERVATION PRIORITIZATION PROCESSES<br />

An unsurprising but nonetheless striking insight provided by William Hawthorne’s study is<br />

that conservation prioritization processes for forest resource management use much the same<br />

datasets as might be used in the assignment of a Red List category. Graudal et al. (2004)<br />

propose that resource conservation assessments should consider past and present geographical<br />

distribution, prevailing utilization patterns in terms of direct use or indirect land-use, occurrence<br />

in protected areas – i.e. data types that would feed directly into an A or B criterion Red List<br />

assessment. However, as a rule, Red List categories are not used or applied in the resource<br />

management setting, except in various developed countries where resource management and<br />

nature conservation are more effectively linked.<br />

Evidently there are often substantial differences between typical national conservation<br />

prioritization processes and Red Listing, not least the scale at which either is carried out: Red<br />

Listing categories were designed for use at the species or global level; conservation prioritization<br />

is applied at a local level and is frequently customised to the local conditions and situations,<br />

although they often respect global distribution patterns. Furthermore, the main criterion for<br />

including species in some forest conservation programmes is their present and possible future<br />

value (Graudal et al. 2004, although not for example Hawthorne and Abu Juam 1995). Resource<br />

managers place emphasis on a wider range of factors, including costs of intervention, potential<br />

success, legal issues and particularly on species’ value in phylogenetic, economic, ecological<br />

or cultural terms. Assessments may be based on qualitative data, soliciting different stakeholders<br />

to provide a subjective score for each variable. Weightings and judgement values may also be<br />

used. For example, a multistakeholder group, comprising scientists, researchers, farmers, local<br />

peasants, and business people, scored forest tree species for their ‘utility’, ‘ecological value’<br />

and ‘threat’ in Sao Paulo State, Brazil (Koshy et al. 2002).<br />

The Ghana Forestry Department uses the “Star system” (Hawthorne & Abu Juam 1995,<br />

Hawthorne 1996, 2001), which aims to define plant species priority for conservation on the<br />

basis primarily of species’ global distribution. Aspects of a species’ biology, economic and<br />

ecological value have a minor influence on the categorization. Black, Gold, Blue, Scarlet,<br />

Red, Pink and Green stars are assigned in order of declining conservation priority. Species<br />

that are extremely rare on a global scale automatically attain a high significance (Black Star)<br />

without regard for other species or data attributes. Other species might have been sampled in<br />

more degree squares, but are estimated to be sparser or more ecologically sensitive and so<br />

may also earn high significance despite their wider range. Common and widespread but heavily<br />

exploited species earn a reddish (Scarlet, Red or Pink) Star according to degree of exploitation<br />

in proportion to inventories of standing crop. One of the main applications of Stars is in a<br />

weighted average score of rarity for the plant community (a Genetic Heat Index), and for this<br />

purpose, the weight is approximately in inverse proportion to the numbers of degree squares<br />

occupied for a subsample of species in each of the Stars. Stars have also been useful in Ghana<br />

to frame management regulations – e.g. allowable cut in logging operations is reduced for<br />

Scarlet Star species, and Black Star species are to be protected wherever they occur; and to<br />

justify patterns of uneven apportionment of global funds to local conservation initiatives<br />

(Hawthorne et al. 1998). Similar Star categorisations have been applied in Mexico and<br />

Honduras, Cameroon and Malaysia (see Chua et al. 1998; Gordon et al. 2004)<br />

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As a rule conservation prioritization processes—and there many types, often very divergent<br />

from each other—do not necessarily register changes in threat but are more clearly aimed to<br />

provide managers or policy makers an indication of which species are worth conserving at<br />

any one time. The change in priorities over the years may not necessarily be linked to changes<br />

in extinction risk, especially where assessments are based on subjective judgements of ad hoc<br />

groups of stakeholders. The conservation prioritization process, therefore, may not provide a<br />

reliable monitoring tool. Assessments in the Red List system should hypothetically be<br />

comparable over time, although it is too early to judge whether this proves to be correct,<br />

especially for the more subjective assessments.<br />

Numerous other differences between the two systems exist, including the following:<br />

• IUCN Red List system offers the option of classifying species according to just one<br />

dimension or parameter of the current status or trends of their population. In this way it<br />

encourages a precautionary approach. A conservation prioritization approach would<br />

usually be more holistic, taking account of all available data.<br />

• Conservation prioritization occurs at a local scale and may not be applicable at a global<br />

level. The Red List system was designed for global level assessments and works best at<br />

this level.<br />

• Conservation prioritizations are undertaken by resource managers and stakeholders. IUCN<br />

Red List assessments are most often carried out by taxonomists and as a result are frequently<br />

considered to be ‘top down’ and academic, but that is not to say they would not benefit<br />

from more local inputs.<br />

• Resource managers are obliged to make further within species assessments about which<br />

populations or gene pools are a priority for conservation.<br />

However, the similarities between the two scales of approach are fundamental. The baseline<br />

data are often the same. The Red List categories depend on a much broader use of ecological,<br />

biological and utilization aspects of species than is immediately obvious when first discovering<br />

the criteria. The two systems can share the following data types:<br />

– geographical distribution<br />

– number of individuals<br />

– regeneration rates and population trends<br />

– threats and sustainable use considerations<br />

– ecological specificity<br />

– levels of protection or conservation measures<br />

The effectiveness of both systems is underpinned by reliable taxonomy and nomenclature,<br />

and, obviously, both are constrained by the lack of information. Conservation prioritization is<br />

constrained by the availability of data on species occurrence, frequency, ecology and status<br />

(Amaral et al. 2004). Basic surveys are needed to locate populations, estimate population<br />

numbers, study population dynamics and monitor threats. Both assessments, therefore, share<br />

the challenge of dealing with data uncertainty and different attitudes to risk and both would<br />

potentially be advanced by the pooling of expert opinion and developing a consensual or<br />

synergistic approach.<br />

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APPLYING THE IUCN RED LIST CATEGORIES IN A FOREST SETTING<br />

MECHANISMS FOR SHARING INFORMATION AND<br />

METHODOLOGIES<br />

The Red List workshop held in Kuala Lumpur, Malaysia, brought together nearly 200 people<br />

from around 50 different institutes, including national and state forest departments, the national<br />

forestry research institute, environmental and conservation organizations, botanic gardens<br />

and universities. The workshop represented a first step towards the development of a national<br />

Red Data book of plants and focused on familiarizing participants with the Red List categories.<br />

Some dissatisfaction had previously been expressed by Malaysian scientists and resource<br />

managers with the way certain published Red Data assessments had been derived mainly<br />

through remote desk work with insufficient reference to details on the ground (Chen, 2004).<br />

Red List assessments, furthermore, are perceived by some to play an important role in<br />

determining both government and international trade policy concerning commercial species<br />

and, therefore, are treated with political interest (despite the expressed intentions of the IUCN<br />

for the Red List categories not to be used for prioritization without the consideration of multiple<br />

additional factors). Given this context the workshop played a pivotal role in developing a<br />

common understanding of the Red List system among a diverse group of stakeholders and<br />

allowed taxonomists and researchers to benefit from the insights of resource managers and for<br />

the latter to contribute directly to the assigning of Red List categories.<br />

One of the main challenges in both resource management and Red List assessments is to<br />

ensure that the species of concern out of the thousands of described species are the focus of<br />

attention. The highly rare species are well-known by the taxonomist but possibly not by the<br />

resource manager. From the latter’s perspective rare species may be overlooked if their use<br />

and value are not considered to be significant, or they may simply be unrecognised. However,<br />

mutual territory of appreciation to both taxonomists and resource managers exists in the form<br />

of species that are locally widespread (and hence appear in forest inventories) but suffering<br />

(or have suffered) significant declines either through habitat decline or direct exploitation.<br />

These species potentially may be considered threatened through the use of criterion A or B.<br />

These are the same criteria that allow the use of inference and are more open to interpretation.<br />

The Malaysian workshop allowed resource managers and researchers to air their different<br />

views on and discuss the impact of past, continuing or future habitat declines on species<br />

extinction rates. In the future, such a group could come to an agreement on the estimated<br />

decline in specific habitat types and how species might be consistently assessed using criteria<br />

A and B. Fortunately, the Malaysian Red Listing process has only just begun and according to<br />

the project manager will involve a number of follow-up workshops to achieve this kind of<br />

consensus (Saw L.G. pers. comm.).<br />

There are further existing mechanisms for facilitating more informed assessments, including<br />

networks, databases and electronic conference groups. Numerous forest genetic resources<br />

(FGR) or forestry networks are already functioning and these are viable and valuable channels<br />

for facilitating, enhancing awareness and also assisting in informed assessments across the<br />

region as well as nationally. Examples of networks associated with IPGRI include the South<br />

Pacific Regional Initiative on Forest Genetic Resources (SPRIG), which has coordinated work<br />

in five south pacific island nations, the Central Asian and Transcaucasian Network on Plant<br />

Genetic Resources (CATCN-PGR) in the central Asian sub-region, the Sub-Saharan African<br />

Programme of Forest Genetic Resources (SAFORGEN) coordinating work in sub-Saharan<br />

countries and the Asia Pacific Forest Genetic Resources Programme (APFORGEN). Such<br />

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C. LUSTY, W.A.N.AMARAL, W. D.HAWTHORNE, L.T. HONG & S. OLDFIELD (2007)<br />

networks could provide the channels for introducing and discussing the Red List categories<br />

and carrying out joint assessments.<br />

The IUCN/SSC Global Tree Specialist Group (GTSG) was established in 2003 with two specific<br />

aims. The first is to act in an advisory capacity to the action-based Global Trees Campaign<br />

which is run by UNEP/World Conservation Monitoring Centre and Fauna and Flora<br />

International and aims to conserve the world’s most threatened plant species. The second is to<br />

promote and implement Red Listing for trees. The GTSG takes a pragmatic approach to red<br />

listing, attempting to use all available information to evaluate species in priority regions and<br />

taxonomic groups. The intention is to provide evaluations which can be used as part of<br />

conservation planning for tree species where possible using evaluation workshops as a means<br />

to determine conservation priorities. In its first year of operation (2004) the GTSG contributed<br />

to the evaluation of over 1200 tree species using various approaches including desk studies,<br />

correspondence with experts, workshops and liaison with other IUCN/SSC plant specialist<br />

groups. The GTSG also evaluated several major commercial timber species and in doing so<br />

sought input from a wide range of stakeholders in an attempt to develop a robust evaluation<br />

model.<br />

CONCLUSIONS<br />

Despite its quantitative framework, the IUCN Red List categorisation inevitably demands<br />

varying degrees of subjective judgement. It is a well-matured system, in the sense that the<br />

rules have evolved through more than a decade of use and feedback, but is somewhat<br />

complicated and time-consuming to absorb and use. The risk that such a system presents is<br />

that while a few relatively well-known groups may be intensively assessed by well-versed<br />

assessors the vast majority of threatened species remain either unevaluated or their assessment<br />

is unrecognised. A small percentage (3%) of described plant species has been assessed using<br />

versions 3.0 or 3.1 Red List categories. Whereas, an exercise to approximate for missing data<br />

carried out by Pitman & Jørgensen (2002), using proxies of endemic species and threatened<br />

species for different combinations of countries, hotspots, tropical and temperate zones, suggest<br />

that somewhere between 22% and 47% of described plant species are likely to be threatened.<br />

It is widely recognised that global-level biodiversity monitoring needs to address a far broader<br />

range of species and means should be sought to increase the involvement of a wider group of<br />

stakeholders, the use of local calibration, ground-truthing and locally collected data (Balmford<br />

et al. 2005).<br />

The feasibility, therefore, of assessing plants using the IUCN Red List system may be brought<br />

into question. However, the knowledge that resource managers and policy makers are obliged<br />

to make daily decisions about genetic resources and that species-level information and indicators<br />

are increasingly sought in international and national policy-making should encourage us to<br />

maximise on the strong points of the Red List system and on all information and expertise<br />

available to accelerate the application of the Red List categories. We are advocating that this<br />

process might be better facilitated through the use of rules of thumb and coordinated through<br />

joint initiatives between taxonomists, conservationists and resource managers typified by the<br />

Workshop on threat assessment of plant species in Malaysia. In addition, some of the raw data<br />

used to categorise the species (e.g. degree square distribution data; estimates of population<br />

size) could also be used to frame local systems (focused initially through the Red List priorities<br />

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themselves), and can be checked and updated periodically as a means of monitoring<br />

conservation status and Red List categorization. While there is a place for more informed Red<br />

List assessments, involving experts and resource managers on the ground, the application of<br />

the Red List categories in conservation prioritization processes is less clear and not seriously<br />

explored here. This is an area that should be more formally reviewed and studied.<br />

REFERENCES<br />

AKÇAKAYA, H.R., FERSON, S., BURGMAN, M., KEITH, D.A., MACE, G.M. & TODD,<br />

C.R. 2000. Making consistent IUCN classifications under uncertainty. Conservation<br />

Biology 14: 1001–1013.<br />

AMARAL, W.A.N., KJAER, E., YANCHUK, A & GRAUDAL, L. 2004. Research needs.<br />

Pp. 37–48 in FAO, FLD, IPGRI. Forest Genetic Resources Conservation and Management.<br />

Vol. 1: Overview, concepts and some systematic approaches. International Plant Genetic<br />

Resources Institute, Rome, Italy.<br />

BAILLIE, J.E.M., HILTON-TAYLOR, C., STUART, S.N. (eds.). 2004. 2004 IUCN Red List<br />

of threatened species. A global species assessment. IUCN Species Survival Commission.<br />

IUCN, Gland, Switzerland and Cambridge, UK. 191 pp.<br />

BALMFORD, A., CRANE, P., DOBSON, A., GREEN, R.E., & MACE, G.E. 2005. The 2010<br />

challenge: data availability, information needs and extraterrestrial insights. Phil. Trans.<br />

R. Soc. B 360: 221–228.<br />

CHEN, H.K. 2004. A Malaysian assessment of the World List of Threatened Trees. Traffic,<br />

Southeast Asia, Selangor, Malaysia. 48 pp.<br />

CHUA, L.S.L., HAWTHORNE, W.D., SAW, L.G.& QUAH, E.S. 1998. Biodiversity database<br />

and assessment of logging impacts. Pp. 30–41 in Lee, S.S., Dan, Y.M., Gauld, I.D. &<br />

J.Bishop (eds.) Conservation, management and development of forest resources.<br />

Proceedings of the Malaysia-United Kingdom Programme Workshop, 21-24 October,<br />

1996, Kuala Lumpur. Forest Research Institute, Malaysia.<br />

GORDON, J.E., HAWTHORNE, W. D., REYES-GARCY´, A., SANDOVAL, G., &<br />

BARRANCE, A.J. 2004. Assessing landscapes: a case study of tree and shrub diversity<br />

in the seasonally dry tropical forests of Oaxaca, Mexico and southern Honduras. Biological<br />

Conservation 117: 429–442.<br />

GRAUDAL, L., YANCHUK, A. & KJAER, E. 2004. National planning. Pp. 25–36 in FAO,<br />

FLD, IPGRI. Forest Genetic Resources Conservation and Management. Vol. 1: Overview,<br />

concepts and some systematic approaches. International Plant Genetic Resources Institute,<br />

Rome, Italy.<br />

HAWTHORNE, W.D. & ABU-JUAM, M. 1995. Forest protection in Ghana. IUCN, Gland,<br />

Switzerland and Cambridge, UK. 203 pp.<br />

HAWTHORNE, W.D. 1995. Categories of conservation priority and Ghanaian tree species -<br />

A comparison of IUCN red book categories and Ghanaian ‘Star’ values. Unpublished<br />

report commissioned by the World Conservation Monitoring Centre.<br />

HAWTHORNE, W.D. 1996. Holes and the sums of parts in Ghanaian forest: Regeneration,<br />

scale and sustainable use. In: Swaine, M.D., Alexander, I.J., & Watling, R. (eds.). Studies<br />

in Guinea-Congo rain forest. Proceedings of the Royal Society, Edinburgh 104(b): 75–<br />

176.<br />

268


C. LUSTY, W.A.N.AMARAL, W. D.HAWTHORNE, L.T. HONG & S. OLDFIELD (2007)<br />

HAWTHORNE, W.D. 2001. Forest conservation in Ghana: forestry, dragons, genetic heat.<br />

In: Weber, W., White, L.J., Vedder, A., & Naughton-Treves, L. (eds) African rain forest<br />

ecology and conservation. An interdisciplinary perspective. Yale University Press.<br />

HAWTHORNE, W.D., GRUT, M. & ABU-JUAM, M. 1998. Forest production and biodiversity<br />

conservation in Ghana, and proposed international support of biodiversity conservation.<br />

CSERGE working paper, GEC 98-18.<br />

IUCN. 1994. IUCN red list categories: Version 3.0. Prepared by the IUCN Species Survival<br />

Commission. 21 pp.<br />

IUCN. 2001. IUCN red list categories. Version 3.1. IUCN Species Survival Commission.<br />

IUCN, Gland, Switzerland and Cambridge, UK. 30 pp.<br />

IUCN. 2003. Guidelines for application of IUCN Red List criteria at regional levels: version<br />

3.0. IUCN Species Survival Commission. IUCN, Gland, Switzerland and Cambridge,<br />

UK. 26 pp.<br />

IUCN. 2005. Guidelines for using the IUCN red list categories and criteria. Prepared by the<br />

Standards and Petitions Subcommittee of the IUCN SSC Red List Programme Committee.<br />

52 pp.<br />

KOSHY, M.P., NAMKOONG, G., KAGEYAMA, P., STELLA, A., GANDARA, F. &<br />

AMARAL, W.A.N. 2002. Decision-making strategies for conservation and use of forest<br />

genetic resources. Unpublished report.<br />

OLDFIELD, S. & LUSTY, C.1998. Conservation and sustainable management of trees (with<br />

CD-Rom) World Conservation Press. 32 pp.<br />

OLDFIELD, S. LUSTY, C. & MACKINVEN, A. 1998. The World List of Threatened Trees.<br />

World Conservation Press. 650 pp.<br />

PITMAN, N.C.A. & JØRGENSEN, P.M. 2002. Estimating the size of the world’s threatened<br />

flora. Science 298: p. 989.<br />

269


STATUS OF BIOLOGICAL DIVERSITY IN MALAYSIA &<br />

THREAT ASSESSMENT OF PLANT SPECIES IN MALAYSIA<br />

LEE et al (2007)<br />

CONSERVATION STRATEGIES OF SHOREA<br />

LUMUTENSIS (DIPTEROCARPACEAE) IN<br />

PENINSULAR MALAYSIA<br />

1,4<br />

S. L. Lee, 1 K. K. S. Ng, 1 L. G. Saw, 1 C. T. Lee, 1 M. Norwati, 2 N. Tani,<br />

2<br />

Y. Tsumura & 3 J. Koskela<br />

ABSTRACT<br />

To conserve a rare plant, conservation programs must be guided by the biological attributes of<br />

the species. Shorea lumutensis is a rare and endemic dipterocarp in Peninsular Malaysia. A<br />

comprehensive research study was initiated to assess the population ecology and population<br />

genetics of S. lumutensis to elucidate specific ecological and genetic requirements and<br />

subsequently to recommend conservation strategies. This paper is apparently the first attempt<br />

at applying both the ecological and genetic approaches into conservation management of a rare<br />

dipterocarp. This paper also attempts to link the gaps between conservation research and<br />

conservation management in a realistic approach. It is our hope that this study will serve as a<br />

model for the other studies related to conservation of rare dipterocarps.<br />

INTRODUCTION<br />

In Peninsular Malaysia, the family Dipterocarpaceae comprises 155 species (Ashton 1982). In<br />

the past, conservation of the dipterocarps was not an important issue as the family was seen as<br />

common and none of the species were presumably threatened. However, a recent study by Saw<br />

& Sam (2000) indicates that over 57% of the species have distribution patterns restricted to<br />

specific zones. There are also 30 species that are endemic to Peninsular Malaysia, and out of<br />

these, 12 species are considered rare. Many rare plants are endangered in part because their<br />

populations are small. Small and isolated populations are inherently more vulnerable to natural<br />

catastrophes, demographic and environmental stochasticity (Shaffer 1981, Lande 1998,<br />

Holsinger 2000). They are also threatened by genetic stochasticity such as loss of genetic diversity<br />

by drift and inbreeding (Keller & Waller 2002). In addition, plants with narrow habitat specificity<br />

and limited dispersal potential are at particular risk for global extinction, as landscapes become<br />

mosaics due to anthropogenic activities.<br />

1<br />

Forest Research Institute Malaysia, Kepong, 52109 Selangor Darul Ehsan, Malaysia<br />

2<br />

Forestry and Forest Products Research Institute, Tsukuba, Ibaraki 305-8687, Japan<br />

3<br />

International Plant Genetic Resources Institute, Regional Office for Europe, Via dei Tre Denari 472/a, 00057 Maccarese<br />

(fiumicino), Rome, Italy<br />

4<br />

Correspondence: Soon Leong LEE, leesl@frim.gov.my<br />

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CONSERVATION STRATEGIES OF SHOREA LUMUTENSIS (DIPTEROCARPACEAE) IN PENINSULAR MALAYSIA<br />

Shorea lumutensis is one of the rare and endemic dipterocarps in Peninsular Malaysia. It was<br />

assigned as critically endangered according to IUCN (1994) version 2.3 criteria (CR A1cd,<br />

C2a) due to suspected population reduction of at least 80% over the last 10 years and the<br />

population estimated to number less than 250 mature individuals. Taxonomic characteristics of<br />

S. lumutensis have been described by Symington (1943) and Ashton (1982). It is a mediumsized<br />

to large tree with irregular longitudinally fissured bark and short buttress (Fig. 1). The<br />

leaves are leathery and oblong-elliptic in shape and have about 14 pairs of nerves, prominent<br />

beneath and usually markedly glaucous on the undersurface. The species produces hermaphrodite<br />

flowers (about 9 mm long, petals linear and pale yellow in color with 20-25 stamens) and<br />

subsessile fruits with three outer and two inner wings. Locally known as balau putih (putih in<br />

Malay means white, referring to the leaf undersurface), it is reported to be restricted to the<br />

western part of Peninsular Malaysia.<br />

Very little is known about the biology of S. lumutensis. Consequently, we do not know how to<br />

address specific conservation problems and how to set conservation strategies and priorities.<br />

This research was aimed to assess the population ecology and population genetics of<br />

Fig. 1. Morphological characteristics of S. lumutensis.<br />

272


LEE et al (2007)<br />

S. lumutensis to elucidate specific ecological and genetic requirements for the species’ existence.<br />

The specific objectives were: (1) to generate information on the population status, habitat<br />

association, spatial distribution, demographic structure, population dynamics, flowering and<br />

fruiting biology, and germination and seedling behaviour of S. lumutensis; (2) to generate<br />

information on the levels of genetic diversity, spatial genetic structure, population genetic<br />

structure, inbreeding, mating system, gene flow, minimum population size and breeding unit<br />

size for conservation; and (3) to integrate the outputs to recommend management prescriptions<br />

and conservation priorities for the species and its habitats.<br />

Population Survey<br />

MATERIALS AND METHODS<br />

Since S. lumutensis is reported to be restricted to the western part of Peninsular Malaysia, a<br />

forest survey was conducted in seven forest reserves, i.e., Segari Melintang, Tanjung Hantu,<br />

Lumut, Teluk Muroh, Pangkor Utara, Sungai Pinang, and Pangkor Selatan in the Manjung<br />

District. For these reserves, the major threats to the existence of the species were identified.<br />

Study Plot<br />

For the purpose of ecological studies, an 8-ha study plot (200 400 m) across an elevation<br />

gradient of 65-125 m, in Compartment 5, Sungai Pinang Forest Reserve, was demarcated for<br />

the study. The plot was subdivided into 400 subplots, each of 10 20 m. Within the study plot,<br />

all S. lumutensis individuals >1 cm dbh were mapped and their diameters recorded.<br />

Topography and Spatial Distribution<br />

Influence of topography on its spatial distribution was examined by their relative abundance in<br />

four different elevation classes, i.e., valley ranging 65–80 m above sea level (asl), lower and<br />

upper slopes ranging 81–95 m asl, 96–110 m asl respectively, and ridge ranging 111–125 m asl.<br />

The subplots were assigned to their respective elevation classes, taking the elevation at the<br />

center of the subplots as the mean.<br />

Spatial Distribution Analysis<br />

Diameter sizes were defined into four classes: large trees (BIG) >25.0 cm, pole trees (POL) 4.0-<br />

25.0 cm, saplings (SAP) 2.0–2.5 cm, and seedlings (SEE) 1.0–1.1 cm. Five continuous distance<br />

classes, each of 20 m, were considered, from 0–20 m to 80–100 m. The spatial distribution of<br />

each stem diameter class was tested using the Ripley’s (1976) K-function. Confidence limits were<br />

estimated using the bootstrap method; the location of individuals was randomized in 19 Monte<br />

Carlo trials to determine a 95% confidence interval within each 20-m distance class.<br />

Demographic Structure and Short-term Population Dynamics<br />

The demographic structure of the species was examined by assigning individuals to one of five<br />

size classes (dbh): 1–5 cm, 6–10 cm, 11–20 cm, 21–30 cm, and >31 cm, and fitted to inverse<br />

J-shaped curve (y = ae -bx ), the shape distribution of natural tree populations with abundant<br />

273


CONSERVATION STRATEGIES OF SHOREA LUMUTENSIS (DIPTEROCARPACEAE) IN PENINSULAR MALAYSIA<br />

regeneration (Condit et al. 1998). Short-term population dynamics was derived from the initial<br />

census in September 2001 and a repeat census in August 2004 for growth rates (based on<br />

increase in dbh) and mortality.<br />

Flowering and Fruiting Biology<br />

Phenological observations were carried out using binocular from January 2002 to October<br />

2005. Periodic surveillance was undertaken following Appanah & Chan (1982) to establish<br />

the flowering stages (budding, initial bloom, peak bloom, tail bloom, and termination of bloom),<br />

flowering intensity (intense, moderate, and poor) and fruiting stages (seed development, seed<br />

maturing and seed fall).<br />

Germination and Seedling Studies<br />

Seed collections were conducted in December 2002 for trees B026 and B385, and in January<br />

2003 for trees B004 and B005 within the 8-ha study plot in Sungai Pinang. The seed weight<br />

variation and its effect on germination and speed of germination were tested using binary and<br />

ordinal logistic regression analyses, respectively. The relationship between seed weight and<br />

seedling vigor (seedling height after three months of growth) was tested for y = bx + c, in<br />

which y represents the seedling height, x the seed weight, and a and b are the intercept and the<br />

slope of the curve, respectively.<br />

Development of Microsatellite Loci<br />

The total genomic DNA was extracted from leaf tissues using the procedure described by<br />

Murray & Thompson (1980), with modification, and further purified using CsCl-ethidium<br />

bromide gradient (Sambrook & Russell 2001). The microsatellite library enriched for<br />

dinucleotide (CT) repeats was constructed following Lee et al. (2004). For those loci showing<br />

multiple alleles, low stutter and robustness of interpretation, forward primers labelled with<br />

6-FAM, HEX, or NED fluorescent dyes were synthesized and further used to confirm the polymorphic<br />

loci using 24 large trees of S. lumutensis from Sungai Pinang.<br />

Sample Collection and DNA Extraction<br />

During the mapping process at the 8-ha study plot in Sungai Pinang, leaf or inner bark samples<br />

were collected for individuals >1 cm dbh for genetic studies. In addition, a total of 40–48<br />

representative samples were also collected from Pangkor Selatan, Lumut, Segari Melinting<br />

and Teluk Muroh, using the transect-line sampling method, as explained by Lee et al. (2000).<br />

The 54 individuals of S. lumutensis >20 cm dbh in Sungai Pinang were also used together with<br />

the four half-sib families (B004, B005, B026, and B385) collected within the 8-ha study plot<br />

for mating system and gene flow studies. Genomic DNA was extracted using the procedure<br />

described by Murray & Thompson (1980), with modification.<br />

Microsatellite Analysis<br />

The samples were genotyped for four native microsatellite loci (Slu057, Slu110, Slu124 and<br />

Slu175) and four microsatellite loci developed for S. leprosula (Sle111a, Sle118, Sle267 and<br />

Sle303a; Lee et al. 2004). PCR amplifications and fragment analysis were performed according<br />

274


LEE et al (2007)<br />

to Lee et al. (2004) using a GENEAMP PCR System 9700 (Applied Biosystems) and an ABI<br />

PRISM 377 DNA Sequencer (Applied Biosystems), respectively.<br />

Data Analysis<br />

Allelic frequencies were determined for each locus in each population (individuals with dbh<br />

>25 cm were used to represent the Sungai Pinang population). Based on these data, the following<br />

levels of genetic diversity were estimated: average number of alleles per locus (A a<br />

), allelic<br />

richness (R s<br />

; Petit et al. 1998), gene diversity (H e<br />

; Nei 1987) and fixation index (F is<br />

; Nei 1987).<br />

Spatial genetic structure in the Sungai Pinang was evaluated using Moran’s I coefficient (Moran<br />

1950). An indication of the trends in spatial scale of genetic substructuring was obtained using<br />

correlograms (Sokal & Oden 1978). A permutation procedure using Monte Carlo simulation<br />

was applied to test significant deviation from random distribution of each calculated measure<br />

(Manly 1997). Population genetic structure was quantified using R-statistics (R st<br />

; Slatkin 1995,<br />

Goodman 1997). Relatedness among populations was quantified using D A<br />

genetic distances<br />

(Nei et al. 1983) for pairwise comparison of divergence between populations and cluster analysis<br />

on genetic distances via the neighbor-joining (NJ) method (Saitou & Nei 1987). Relative strength<br />

of the nodes was determined using bootstrapping analysis (1000 replicates). For the direct<br />

estimation of gene flow, parentage was determined by simple exclusion method and likelihoodbased<br />

approach in the program CERVUS 2.0 (Marshall et al. 1998). The breeding unit parameters<br />

were estimated according to Nason et al. (1998). The minimum population size to maintain<br />

current level of genetic diversity was estimated according to Lee et al. (2002).<br />

Ecology<br />

RESULTS<br />

The species was present in five forest reserves, i.e., Sungai Pinang, Pangkor Selatan, Segari<br />

Melintang, Lumut and Teluk Muroh, which were confined to an area of approximately 313<br />

km². As the two island populations (Sungai Pinang and Pangkor Selatan) are separated from<br />

the mainland by the Straits of Dinding, they must have been isolated from mainland populations<br />

many thousand years ago. Among the three mainland populations, no distinctive geographical<br />

barrier divided the Lumut and Teluk Muroh but the Segari Melintang population was separated<br />

by the Manjung River.<br />

Within these reserves, S. lumutensis occurs as small patches in a general matrix of coastal hill<br />

dipterocarp forest, usually at >100 m asl. Isolated individuals are occasionally seen but rare.<br />

The species is most often a subcanopy to emergent tree. Symington (1943) reported that the<br />

species seldom exceeded 50 cm dbh but in Sungai Pinang and Lumut, four trees >100 cm dbh<br />

were encountered. The preferred habitat for these five populations appears to be dry coastal hill<br />

forest on moderate-fertility soils, in microclimates where drainage is good or where high soil<br />

moisture levels cannot be permanently maintained. The number of large trees was estimated to<br />

be less than 500 for these five populations. Although the number of large trees was low in each<br />

of the populations, progressively larger numbers of associated saplings and seedlings were<br />

observed scattered surrounding the large trees in each of these populations. We also identified<br />

the following potentially major threats for population endangerment: logging activities (Segari<br />

Melintang), excavation for stones (quarry) and conversion to oil palm plantations (Lumut and<br />

Teluk Muroh), and land development for tourism (Pangkor Selatan and Sungai Pinang).<br />

275


CONSERVATION STRATEGIES OF SHOREA LUMUTENSIS (DIPTEROCARPACEAE) IN PENINSULAR MALAYSIA<br />

A total of 416 individuals >1 cm dbh were recorded within the 8-ha plot in Sungai Pinang. The<br />

population density of S. lumutensis >30 cm dbh within the plot was 4.4 trees ha -1 . The prominent<br />

associated species within the habitat are two palm species, i.e., Eugeissona tristis and Calamus<br />

castaneus. The study of the relationship between microtopography and spatial distribution<br />

showed that the species distribution was strongly related to topography; prominent on ridges<br />

and upper slopes, and totally absent in the lower slopes and valleys. This was further supported<br />

by spatial distribution analyses, in which significant spatial aggregation was detected at four<br />

size classes (Fig. 2) and the level of aggregation was highest in SEE and SAP, followed by<br />

POL, and then BIG.<br />

Diameter distribution was skewed, with many more small than large individuals being present.<br />

The distribution was significantly fitted to inverse J-shaped curves (y = ae -bx ; a = 154.6; b =<br />

0.6; r² = 0.98, P < 0.01), indicating abundant regeneration. The medium-sized trees (11–20<br />

cm) constituted 1.7% of the total 416 individuals found within the plot, compared with 8.2% in<br />

the largest-sized trees (>31 cm) and 82.2% in the smallest-sized trees (1–5 cm). Short-term<br />

population dynamics derived from the initial census in September 2001 and a repeat census in<br />

August 2004 showed that a total of 75 trees died over the 3-year study period. Mortality was<br />

detected only at the two lowest-sized classes (1–5 cm and 6–10 cm), 22% and 8% respectively<br />

(Table 1). Growth was slow in most of the trees enumerated, at mean rates around<br />

0.3 mm yr -1 (lowest-sized class) to 2.4 mm yr -1 (highest-sized class) and the mean growth rate<br />

increased with increasing size class.<br />

15<br />

BIG<br />

30<br />

25<br />

POL<br />

10<br />

20<br />

Ripley’s K<br />

5<br />

0<br />

Ripley’s K<br />

15<br />

10<br />

5<br />

0<br />

-5<br />

-5<br />

-10<br />

-10<br />

0 1 2 3 4 5<br />

0 1 2 3 4 5<br />

clas s<br />

Distance class<br />

class<br />

Distance class<br />

70<br />

60<br />

SAP<br />

90<br />

80<br />

SEE<br />

70<br />

50<br />

60<br />

Ripley’s K<br />

40<br />

30<br />

20<br />

10<br />

0<br />

-10<br />

0 1 2 3 4 5<br />

Distance clas class s<br />

Ripley’s K<br />

50<br />

40<br />

30<br />

20<br />

10<br />

0<br />

-10<br />

-20<br />

0 1 2 3 4 5<br />

Distance class class<br />

Fig. 2. Spatial distribution analysis using Ripley’s K-function on four diameter classes of<br />

S. lumutensis within an 8-ha (400 200 m) plot: large trees (BIG >25 cm), pole trees (POL<br />

4–25 cm), saplings (SAP 2.0–2.5 cm) and seedlings (SEE 1.0–1.1 cm). Distance classes were<br />

defined at five intervals, each of 20 m, from 0–20 m (class 1) to 80–100 (class 5). Dotted lines<br />

represent 95% confidence limits.<br />

276


LEE et al (2007)<br />

Table 1. Percentages of mortality, mean and maximum growth rates of S. lumutensis at five<br />

diameter size classes in the Sungai Pinang plot between 2001 and 2004. Value in parentheses is<br />

the standard deviation.<br />

Size class/cm No. of trees % Mean growth Max. rate/<br />

mortality rate/mm yr -1 mm yr -1<br />

1–5 342 22 0.3 (0.5) 1.3<br />

6–10 14 8 0.7 (0.7) 2.3<br />

11–20 7 0 1.4 (1.1) 3.7<br />

21–30 19 0 1.6 (1.2) 3.7<br />

>31 34 0 2.4 (1.9) 6.3<br />

Phenological observations within the 8-ha study plot from January 2002 to October 2005 showed<br />

a flowering event in August 2002 on five trees, i.e., B004, B005, B026, B325 and B385. The<br />

budding stage was observed on B026, B325 and B385 on 15 August 2002 and two weeks later<br />

on B004 and B005. The duration of bloom was short, approximately two weeks. The period<br />

from tail flowering to mature fruit fall was approximately 10 weeks and the period from budding<br />

stage to mature fruit fall was approximately 16 weeks. Variation of seed morphology was<br />

obvious among trees; the tree B385 produced the biggest mature seeds with shorter wings.<br />

Fruit predation was extensive; the majority of the fallen mature seeds were consumed by small<br />

mammals (e.g., squirrels and rats).<br />

The distribution of seed size based on 200 individually weighed seeds from four mother trees<br />

was approximately normal (Fig. 3A). The average seed weight was 18.8 mg (SD = 5.5).<br />

Germination study showed that the proportion of seed germinated was 35.5%. All the fertile<br />

seeds germinated within 22 days and more than 50% germinated within nine days (Fig. 3B).<br />

An ordinal logistic regression analysis showed that seed weight did not affect the speed of<br />

germination (z = 0.73, P = 0.465). However, a binary logistic regression analysis on the<br />

probability of seedling emergence vs. seed weight revealed that a significant relationship exists<br />

between these variables (z = 6.23, P < 0.001). Accordingly, seed weight did influence seedling<br />

emergence but did not influence the speed of germination.<br />

There was a weak relationship (seedling height = 0.26 [seed weight] + 3.17; n = 71, r² = 0.19,<br />

P = 0.11) between seedling height (after three months of growth) and seed weight (Fig. 3C);<br />

only 19.1% of the variability among the observed values of seedling height was explained by<br />

the linear relationship between seedling height and seed weight and the remaining 81.9% of the<br />

variation was not explained by this relationship. The germination rate and seedling performance<br />

according to mother tree are shown in Table 2. The germination rate ranged from 6% (B004) to<br />

60% (B385). At the age of two years, the mean seedling height ranged from 23 cm (B005) to 38<br />

cm (B026) and the mean diameter at ground height (dgh) ranged from 3.7 mm (B005) to 5.3<br />

mm (B026). B026 produced small seeds (mean seed weight = 17.8 ± 2.8 mg) with low<br />

germination rate (22%) but had seedlings with the most vigor (mean height and dgh after two<br />

years of growth were 38 ± 12 cm and 5.3 ± 1.2 mm, respectively).<br />

Genetics<br />

From the microsatellite library enriched for dinucleotide (CT) repeats, a total of 336 clones<br />

were sequenced. A high proportion of the clones were identified to contain microsatellite repeat<br />

277


CONSERVATION STRATEGIES OF SHOREA LUMUTENSIS (DIPTEROCARPACEAE) IN PENINSULAR MALAYSIA<br />

25<br />

20<br />

A<br />

Proportion (% )<br />

15<br />

10<br />

5<br />

0<br />

6-8 9-11 12-14 15-17 18-20 21-23 24-26 27-29 30-32 33-35<br />

W e Weight (m(mg)<br />

30<br />

25<br />

B<br />

Proportion (% )<br />

20<br />

15<br />

10<br />

5<br />

0<br />

1-3 4-6 7-9 10-12 13-15 16-18 19-21 22-24<br />

TimTime e of of germination (Day) (Day)<br />

16<br />

14<br />

C<br />

See dling he ight (cm )<br />

12<br />

10<br />

8<br />

6<br />

4<br />

2<br />

0<br />

10 14 18 22 26 30<br />

Seed ed Weight w (mg)<br />

g)<br />

Fig. 3. (A) Distribution of seed sizes (black) and proportions of germinated seed<br />

(grey) based on 200 individually weighed seeds from four mother trees in one population.<br />

(B) Proportions of seeds germinated at three-day intervals within 24 days. (C) Relationship<br />

between seed weight and seedling height (after three months of growth): seedling height<br />

= 0.26 (seed weight) + 3.17 (r² = 0.19, P = 0.11).<br />

(97.9%). However, these microsatellite clones showed high redundancies and only 55.3% were<br />

unique (single copy). For these unique microsatellite clones, 87.3% were CT/GA repeats, 8.3%<br />

were GT/CA repeats, and 4.4% were other repeats (e.g., GT/CA, AAG, and GGA). Screening<br />

of 48 primer pairs of unique microsatellite clones, however, managed only to obtain five<br />

polymorphic loci after screening on 24 large trees from Sungai Pinang (Table 3). The number<br />

of alleles ranged from two (Slu175) to nine (Slu124), and the probability of paternity exclusion<br />

278


LEE et al (2007)<br />

Table 2. Mean seed weights, germination rates and seedling performance after two years of<br />

potting of four mother trees of S. lumutensis. Value in parentheses is the standard deviation.<br />

Tree No.<br />

No. of<br />

seeds<br />

Germination test<br />

Seedling performance<br />

after two years<br />

No. of Mean seed % seed Mean height Mean<br />

seeds weight/mg germinated /cm dgh/mm<br />

004 85 50 12.0 (3.1) 6 - -<br />

B005 190 50 20.5 (2.9) 54 23 (9) 3.7 (1.3)<br />

B026 100 50 17.8 (2.8) 22 38 (12) 5.3 (1.2)<br />

B385 120 50 24.6 (3.7) 60 28 (10) 4.1 (0.8)<br />

Table 3. Locus names, primer sequences, repeat motifs, annealing temperatures (T), numbers<br />

of alleles observed (A) and allele size ranges of microsatellites sequenced from the CT-enriched<br />

genomic library of S. lumutensis. Expected heterozygosity (H e<br />

), polymorphic information content<br />

(PIC) and probability of paternity exclusion (P e<br />

). * indicate a significant departure from Hardy-<br />

Weinberg equilibrium (P < 0.05).<br />

Locus Primer sequence (5’ - 3’) Repeat T A Size H e<br />

PIC P e<br />

Slu 044a F: ACA AAA AGT GGA TGG TGA G (GA) 15<br />

50 3 138-152 0.535* 0.409 0.218<br />

R: TTG TAG TGT TGT CCA GTG TG<br />

Slu 057 F: TTT GTG GTC CCC GCC TTC TG (CT) 12<br />

50 3 109-113 0.525 0.459 0.273<br />

R: ATC AGA CAA TCT TTT TGG AC<br />

Slu 110 F: CAT CCT TAC CTT TGT CAC CC (GA) 21<br />

50 5 216-222 0.649 0.567 0.368<br />

R: TCA GGC TCC ATT CTT CTT TT<br />

Slu 124 F: GCA AAA TAA TAC TCA ATG GG (CA) 12<br />

50 9 130-161 0.759 0.713 0.544<br />

R: TGT CAC ATG GGT AAT AAA CT<br />

Slu 175 F: CAT CAT TAC AAT CAT CCA TC (GA) 15<br />

50 2 217-223 0.294 0.246 0.123<br />

R: CAC TTG CTT CGT CGT CTA CC<br />

ranged from 0.123 (Slu175) to 0.544 (Slu124). A significant departure from Hardy-Weinberg<br />

equilibrium was detected on Slu044a. Linkage disequilibrium was found between Slu044a<br />

and Slu175.<br />

The study revealed high levels of genetic diversity in S. lumutensis (Table 4). The allelic richness<br />

ranged from 5.7 (Lumut) to 6.3 (Segari Melintang) whereas the gene diversity ranged from<br />

0.609 (Sungai Pinang) to 0.673 (Segari Melintang). The study also showed high positive values<br />

of fixation index (F is<br />

> 0.1) in all populations, an indication of an excess of homozygotes. The<br />

spatial distribution of alleles study showed significant spatial genetic structure in SEE, SAP<br />

and BIG but not in POL (Fig. 4). The coefficient of population differentiation quantified using<br />

R-statistics showed that most of the total genetic diversity was partitioned within population.<br />

The proportion of genetic diversity distributed among populations was estimated as 0.058, thus<br />

only 5.8% of the genetic variability was distributed among populations. The cluster analysis<br />

among populations, however, formed three genetic clusters; Lumut/Teluk Muroh, Sungai Pinang/<br />

Pangkor Selatan, with Segari Melintang being the outlier (Fig. 5).<br />

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CONSERVATION STRATEGIES OF SHOREA LUMUTENSIS (DIPTEROCARPACEAE) IN PENINSULAR MALAYSIA<br />

Table 4. Genetic diversity statistics (A a<br />

, R s<br />

and H e<br />

) and fixation indices (F is<br />

) of S. lumutensis<br />

based on eight microsatellite loci. Value in parentheses is the standard deviation.<br />

Population Sample size A a<br />

R s<br />

H e<br />

F is<br />

Sungai Pinang 47 7.4 (1.8) 6.0 (1.4) 0.609 (0.082) 0.130<br />

Pangkor Selatan 48 8.1 (1.7) 6.1 (1.1) 0.663 (0.077) 0.128<br />

Segari Melintang 48 7.9 (1.9) 6.3 (1.3) 0.673 (0.058) 0.109<br />

Lumut 40 6.6 (1.4) 5.7 (1.2) 0.636 (0.074) 0.156<br />

Teluk Muroh 48 7.0 (1.5) 6.0 (1.1) 0.661 (0.052) 0.194<br />

Mean 46 7.4 (0.6) 6.0 (0.2) 0.648 (0.026) 0.143<br />

0.15<br />

0.1<br />

BIG<br />

0.06<br />

0.04<br />

0.02<br />

POL<br />

0.05<br />

0<br />

Moran’s I<br />

0<br />

-0.05<br />

Moran’s I<br />

-0.02<br />

-0.04<br />

-0.06<br />

-0.08<br />

-0.1<br />

-0.1<br />

-0.15<br />

0 1 2 3 4 5<br />

Distance e clas class s<br />

-0.12<br />

0 1 2 3 4 5<br />

Distance class<br />

0.06<br />

0.04<br />

SAP<br />

0.1<br />

SEE<br />

0.02<br />

0.05<br />

Moran’s I<br />

0<br />

-0.02<br />

-0.04<br />

-0.06<br />

-0.08<br />

Moran’s I<br />

0<br />

-0.05<br />

-0.1<br />

-0.1<br />

0 1 2 3 4 5<br />

Distance class<br />

-0.15<br />

0 1 2 3 4 5<br />

class<br />

Distance class<br />

Fig. 4. Correlograms of average Moran’s I coefficients on four diameter classes of S. lumutensis<br />

within an 8-ha (400 200 m) plot: large trees (BIG >25 cm), pole trees (POL 4–25 cm),<br />

saplings (SAP 2.0–2.5 cm) and seedlings (SEE 1.0–1.1 cm). Distance classes were defined at<br />

five intervals, each of 20 m, from 0–20 m (class 1) to 80–100 m (class 5). Dotted lines represent<br />

95% envelopes of average I distribution after 1000 permutations of individual multi-genotypes<br />

within each diameter class.<br />

The phenological observations using binocular showed five flowering trees (B004, B005, B026,<br />

B325 and B385) during the flowering event in August 2002. However, paternity assignment<br />

showed that an addition of seven trees (B003, B011, B012, B023, B030, B349 and B397)<br />

within the 8-ha plot also contributed pollen for the reproduction of the four mother trees. In<br />

other words, these trees might have flowered but at low density which could not be picked up<br />

through binoculars. The dbh of the flowering trees ranged from 31–110 cm and this allowed us<br />

to make the assumption that trees above 30 cm dbh can be considered as reproductively mature.<br />

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LEE et al (2007)<br />

SM<br />

BI<br />

LU<br />

TM<br />

52<br />

SP<br />

PS<br />

Fig. 5. Neighbor-joining (NJ) cluster analysis based on D A<br />

distances (Nei et al. 1983) among<br />

the Sungai Pinang (SP), Lumut (LU), Pangkor Selatan (PS), Segari Melintang (SM) and Teluk<br />

Muroh (TM) populations. The bootstrap values (based on 1000 replications) were generated<br />

by PowerMarker software (Liu & Muse 2005).<br />

The summary results of mating system, paternity assignment and breeding unit parameters are<br />

given in Table 5. Shorea lumutensis can be inferred to follow the mixed-mating model (mean<br />

outcrossing rate = 63.4%), with B004 showing the lowest value of outcrossing rate (22.2%)<br />

and B005 the highest (92.0%). The pollen flow is moderately extensive, in the range of 122.0<br />

m (B004) to 220.3 m (B385) with the mean of 175.2 m, and this allowed us to postulate that<br />

low energy insects might be the main pollinators for S. lumutensis. In comparison with the<br />

germination study, mother trees with higher outcrossing rate and receiving pollen from many<br />

distant paternal trees produced bigger seeds, and bigger seeds have a greater probability to<br />

germinate and establish seedlings. The mean breeding unit size and area were estimated as 52<br />

individuals and 11.8 ha, respectively. The minimum population size to maintain current levels<br />

of genetic diversity (number of alleles) is shown in Fig. 6. The basic relationship between A t<br />

with sample size was logarithmic. To maintain 95% of alleles, 270 individuals are required (in<br />

the range of 200-310 individuals).<br />

Table 5. The summary results of mating system, paternity assignment and breeding unit<br />

parameters of four half-sib families of S. lumutensis in Sungai Pinang. Value in parentheses is<br />

the standard deviation.<br />

Mating system and paternity assignment<br />

% of seed<br />

Mean pollen<br />

% of seed due received<br />

flow<br />

to outcrossing pollen outside<br />

distance/m<br />

plot<br />

Breeding unit parameter<br />

Tree No.<br />

No. of<br />

seeds<br />

Size/individual<br />

Area/ha<br />

B004 38 22.2 11.1 122.0 (0.0) 70 16.0<br />

B005 50 92.0 24.0 220.0 (120.2) 47 10.7<br />

B026 44 61.4 13.6 138.4 (28.3) 45 10.3<br />

B385 50 78.0 16.0 220.3 (78.5) 44 10.1<br />

Mean 45.5 63.4 (15.1) 16.2 (2.8) 175.2 (26.2) 52 (6) 11.8 (1.4)<br />

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CONSERVATION STRATEGIES OF SHOREA LUMUTENSIS (DIPTEROCARPACEAE) IN PENINSULAR MALAYSIA<br />

100<br />

90<br />

80<br />

70<br />

% of alleles<br />

60<br />

50<br />

40<br />

30<br />

20<br />

10<br />

0<br />

10 30 50 70 90 110 130 150 170 190 210 230 250 270 290 310 330<br />

No. of individua ls<br />

Fig. 6. Changes in % of alleles maintained with changes in the number of individuals of S.<br />

lumutensis removed. All values were based on a mean of 1000 resamplings with standard<br />

errors (SE). Dotted lines represent standard errors.<br />

DISCUSSION AND RECOMMENDATIONS<br />

This study showed that S. lumutensis comprises only five populations and perhaps no more<br />

than 500 large individuals; extinction of the species is likely if nothing is done to conserve it.<br />

There are two basic conservation strategies for plants, in situ and ex situ conservation. In situ<br />

conservation involves the designation, management and monitoring of species at the location<br />

where they are currently found, whereas ex situ conservation involves the sampling, transfer<br />

and storage of species away from the original locations where they were found. Conserving S.<br />

lumutensis in its natural habitat is clearly the first step. However, ex situ conservation is also<br />

necessary to provide insurance against catastrophic events and to facilitate the possibility of<br />

future reintroduction into appropriate habitats.<br />

Selection of In situ Conservation Area<br />

Shorea lumutensis has >90% of its total genetic diversity residing within the population and<br />

displays mix-mating system. As the species is endemic to Peninsular Malaysia and comprises<br />

only five populations and perhaps no more than 500 large individuals, the five populations<br />

need to be conserved. The cluster analysis showed that Segari Melintang harbors some unique<br />

genetic characteristics which should receive additional attention for conservation purposes.<br />

The minimum population size needed to maintain 95% of its genetic diversity was estimated as<br />

270 individuals (in the range of 200-310) and the mean breeding unit size was estimated as 52<br />

individuals. When planning a conservation area, however, a minimal population size should be<br />

regarded only as a last resort and an extreme compromise. For added safety, much larger<br />

population or area should constitute units of in situ conservation (Hawkes et al. 1997). However,<br />

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LEE et al (2007)<br />

as the resources available for conservation programs are limited, it is unrealistic simply to<br />

recommend in situ conservation area “as large as possible”. In practice, the size of a conservation<br />

area, rather than the number of trees, is often dictated by the relative concentration of people<br />

and the suitability of the land for human exploitation (agriculture, urbanization, logging, etc).<br />

Therefore, for S. lumutensis, conserving an area no less than 100 ha with at least of 300<br />

individuals >10 cm dbh (including 60 reproductive trees >30 cm dbh) in each population will<br />

be sufficient to maintain maximum levels of genetic diversity to withstand loss of genetic<br />

variability due to drift and should be enough to contain the minimum number of reproductive<br />

individuals to prevent inbreeding.<br />

The areas should be demarcated within the Compartments where S. lumutensis is found, such<br />

as Compartment 5 of Sungai Pinang (N 04º14’32”; E 100º33’33”), Compartments 1 and 2 of<br />

Pangkor Selatan (N 04º12’19”; E 100º34’23”), Compartment 5 of Teluk Muroh (N 04º11’13”;<br />

E 100º37’47”), Compartment 3 of Lumut (N 04º13’38”; E 100º38’26”), and Compartments 41<br />

and 42 of Segari Melintang (N 04º22’36”; E 100º37’13”) (Fig. 7). Extensive surveys should be<br />

carried immediately to enumerate, measure and tag the individuals within these compartments.<br />

The survey should be extended to other compartments if the criterion of conserving 300<br />

individuals cannot be fulfilled. The criterion of at least 100 ha should always be satisfied even<br />

when the number of individuals exceeds 300. There is a possibility that the number of individuals<br />

is less than 300 in Pangkor Selatan; than the population might require re-introduction to increase<br />

its size and gene pool.<br />

For each population of S. lumutensis, the conservation area to be established should have a<br />

central core area, surrounded by a buffer zone and perpheral to this, a transition zone (Fig. 7).<br />

Laidlaw (1994) and Lee et al. (2002) have shown that there is a higher occurrence of deleterious<br />

effects on reserves that are situated at the edge of a forest reserve. The presence of a buffer<br />

zone will protect the core from edge effects and other factors that might threaten the population<br />

viability of S. lumutensis present in the core. The transition zone, however, may be made available<br />

for sustainable harvesting activities.<br />

To ensure these conservation areas are fully protected, legal provisions must be in place at the<br />

State level. The establishment of in situ conservation areas will not only conserve S. lumutensis,<br />

but also help to conserve the forest ecosystem and other important, but non-targeted species,<br />

such as tongkat ali (Eurycoma longifolia, Simaroubaceae) in Sungai Pinang.<br />

Monitoring and Management In situ conservation Area<br />

Monitoring is a quantitative assessment of the status of a population and its component<br />

individuals over time (Tuxill & Nabhan 2001). Monitoring is important both before and after<br />

legal protection of in situ conservation areas. Before protection, monitoring gives a basis for<br />

prediction and allows a critical situation to be identified. During protection, monitoring indicates<br />

the effectiveness of protected areas in preserving and enhancing the species they contain.<br />

Once the conservation areas are demarcated, the areas shall be monitored at frequent intervals<br />

to note disturbances or encroachments. Habitat protection from anthropogenic catastrophes<br />

represents the first and the most important measure for the existence of the species in a natural<br />

habitat. Phenological observations can be initiated during this process to check the reproductive<br />

status and to enable seed collections.<br />

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CONSERVATION STRATEGIES OF SHOREA LUMUTENSIS (DIPTEROCARPACEAE) IN PENINSULAR MALAYSIA<br />

Segari Melintang<br />

Tanjung Hantu<br />

Conservation area design<br />

Core<br />

Pangkor Utara<br />

Buffer zone<br />

Transition zone<br />

Sungai Pinang<br />

Lumut<br />

Pangkor Selatan<br />

Teluk Muroh<br />

Fig. 7. Proposed in situ conservation areas (compartments highlighted in black) and model for<br />

reserve design (inset) of S. lumutensis. Compartments where the survey was conducted are<br />

highlighted in grey. The species is not present in Pangkor Utara and Tanjung Hantu.<br />

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LEE et al (2007)<br />

Even if the habitat remains untouched, all populations face some risk of decline through exposure<br />

to the vagaries of natural temporal and spatial variations, such as environmental and demographic<br />

variations. Hence, monitoring of population size should also be conducted at appropriate intervals<br />

to detect any drastic reduction so that timely management prescriptions can be provided to<br />

ensure their health.<br />

At five-year intervals, the populations should be enumerated to determine its size distribution,<br />

mortality, recruitment, population growth and other demographic variables. The information<br />

generated helps to understand the mechanisms that influence population behavior and can be<br />

used to predict population trends. In addition, genetic assessment should also be conducted to<br />

determine population bottlenecks and inbreeding depression. The 8-ha study plot is already<br />

available for Sungai Pinang and this should be included in the core area. A similar study plot<br />

shall be established in Pangkor Selatan, Segari Melintang, Lumut and Teluk Muroh. Although<br />

monitoring is an expensive process in terms of time and resources, it is the only way to ensure<br />

that S. lumutensis is conserved effectively.<br />

A management plan for the conservation areas must be developed to regulate human intervention<br />

in a manner that ensures the population viability of the target species is maintained or enhanced<br />

(Maxted et al. 1997a). Given the large amount of genetic diversity detected presently,<br />

S. lumutensis should have enough genetic resources necessary for short-term ecological<br />

adaptation and for long-term evolutionary change. However, all the populations exhibited high<br />

positive values of fixation index, an indication of homozygote excess, which might indicate<br />

depression due to inbreeding. In Sungai Pinang, the inbreeding depression can be either due to<br />

high selfing rate or biparental mating. Inbreeding causes the loss of heterozygosity with no<br />

change in allele frequencies, because continuous selfing and mating between relatives will<br />

purge the deleterious recessive alleles and expose them as homozygotes to the environment<br />

(Oostermeijer et al. 2003). It is generally agreed that inbreeding is associated with increased<br />

seed abortion, low germination rates, high seedling mortality, and poor growth and flowering<br />

of the offspring (Dudash & Carr 1998). Thus, if a population consists of less than 60 reproductive<br />

individuals, the priority should be to enlarge the population size to minimize inbreeding<br />

depression due to small population size. If a population consists of a few hundred reproductive<br />

individuals, thinning is required to reduce the degree of spatial genetic structure and thus<br />

minimize the inbreeding depression due to biparental mating.<br />

The direct estimation of gene flow showed that its pollen flow is not extensive, which might<br />

indicate that its pollen do not cross large forest openings. Because the five populations were<br />

isolated from each other due to geographical barrier or fragmentation, if the populations are<br />

allowed to exist in small population sizes for a long period of time, it is expected that the loss<br />

of genetic variation by drift cannot be compensated for by immigration of seeds or pollens<br />

from other populations. This leads to genetic erosion and increased genetic differentiation among<br />

populations. Consequently, low levels of genetic diversity might reduce evolutionary potential<br />

and increase the probability of population extinction. The most effective way to counter genetic<br />

risks is to allow for migration, i.e., the exchange of pollen and seeds with neighbors. The idea<br />

of habitat corridors initially developed for animal conservation (Simberloff & Cox 1987) might<br />

be an option, and provided resources are available, this approach may be applied to bridge the<br />

Sungai Pinang population with that in the Pangkor Selatan, and Teluk Muroh population with<br />

the Lumut population.<br />

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CONSERVATION STRATEGIES OF SHOREA LUMUTENSIS (DIPTEROCARPACEAE) IN PENINSULAR MALAYSIA<br />

In situ conservation areas should be intensively managed to support the natural regeneration of<br />

target species and prevent them from competition with other species that may become dominant<br />

following the rules of natural succession. The demographic study conducted in Sungai Pinang<br />

showed that the population consisted of a low number of medium-sized trees and had high<br />

mortality of seedlings. Thus, silviculture treatments should be designed to encourage seedling<br />

regeneration and enhance sapling growth by selectively eliminating the two prominent associated<br />

palm species (E. tristis and C. castaneus), so as to minimize the space competition and maximize<br />

the sunlight exposure. Nevertheless, as the two island populations were entirely isolated from<br />

mainland populations and the three mainland populations were isolated from each other either<br />

due to geographical barrier or fragmentation, restricted gene flow and contemporary demographic<br />

independence are anticipated. Therefore, the five populations should be considered as distinct<br />

management units, which will require specific management prescriptions. Like monitoring,<br />

management prescription activities are often expensive in time and resources. Hence, active<br />

management should be carried out with decreasing intensity and eventually stops when<br />

monitoring indicates that survival and reproduction, especially the quality of the offspring,<br />

have achieved acceptable levels.<br />

Ex situ Conservation<br />

Ex situ conservation can be divided into several specific techniques, such as seed storage, in<br />

vitro storage, DNA storage, field gene bank and botanical garden. As the species produces<br />

recalcitrant seeds which are extremely short-lived in nature, ex situ conservation based on seed<br />

storage and periodic regeneration appears to be more in principle than in practice. Although in<br />

vitro conservation is seldom useful or economically viable for the conservation of forest trees,<br />

it may be more relevant to S. lumutensis with seed storage problems. The use of DNA storage<br />

method is rapidly increasing in importance. It is now routinely possible to amplify specific<br />

oligonucleotides or genes from the entire mixture of genomic DNA. The advantage of this<br />

technique is that it is efficient, simple and takes up little space but the obvious problem is that<br />

it does not allow the regeneration of entire plants (Maxted et al. 1997b). A better assurance<br />

against possible extinction in its natural habitat is the establishment of the species in ex situ<br />

conservation areas, such as botanical gardens and arboreta. Realistically, however, botanical<br />

gardens and arboreta collections are always limited to a small number of individuals.<br />

Although the establishment of new populations to areas outside their historic range might not<br />

be successful due to genetic and ecological adaptation problems, increased use of S. lumutensis<br />

in terms of planting in forest areas, watersheds and degraded lands or as field gene bank should<br />

be encouraged. The idea is that the cultivation of a valuable but rare tree species can result in<br />

multiplication and distribution of its germplasm. Moreover, when a rare species becomes<br />

common as a result of planting, and its products have economic value, the harvesting pressures<br />

on its natural populations will decrease.<br />

As the species is outcrossed and the majority of its genetic diversity was partitioned within the<br />

population, a minimum of 10 unrelated mother trees per population should be used to establish<br />

a field gene bank. In addition, as the species exhibited significant spatial genetic structure up<br />

to the scale of about 20 m, the selected mother trees for seed collections should be more than 20<br />

m apart. Chances for success are greatest if seeds are drawn from a composite cross among the<br />

available populations so that natural selection will weed out unsuccessful genotypes from among<br />

the segregating progeny of such hybrid populations (Barrett & Kohn 1991). Larger seeds have<br />

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LEE et al (2007)<br />

a greater chance of germination compared to smaller seeds. Using 30 progenies per mother tree<br />

and combining the progenies from five populations would provide a stand of 1500 individuals.<br />

In addition to the genetic considerations, stand sizes should be kept at a manageable level and<br />

that the burden of future management and regeneration is within the capacity of the institution<br />

in charge. A minimum of 10 ha is recommended. Initial planting may want to consider planting<br />

2000 individuals (40 progenies per mother tree) because this number will decrease as a result<br />

of mortality and other factors.<br />

ACKNOWLEDGEMENTS<br />

This report was extracted from the paper, “Linking the gaps between conservation research and<br />

conservation management of rare dipterocarps: A case study of Shorea lumutensis” by the<br />

same authors in Biological Conservation 131(2006): 72–92. The Forest Department of Perak is<br />

acknowledged for granting us permission to access the various forest reserves. We thank the<br />

District Forest Officer of Kinta Manjung and the staff of the Renjer Office in Lumut for their<br />

logistic support during the field work; and Ghazali Jaafar, Yahya Mahani, Ramli Ponyoh, Mariam<br />

Din, Sharifah Talib, the late Baya Busu, Ayau Kanir, Angan Atan and Mustapa Data for their<br />

excellent assistance in the field and laboratory. The Forest Department of Peninsular Malaysia<br />

is acknowledged for providing the digital maps of the forest reserves in Manjung District and<br />

Hamidah Mamat (FRIM) for helping to illustrate Fig. 7. This project was supported in part by<br />

the IRPA research grant (09-04-01-0013-EA001), the Timber Export Levy Fund (A179 QIZZ),<br />

and the International Plant Genetic Resources Institute (IPGRI) Agreement No. APO01/056,<br />

APO02/084 and APO03/094.<br />

REFERENCES<br />

APPANAH, S. & CHAN, H.T. 1982. Methods of studying the reproductive biology of some<br />

Malaysian primary forest trees. Malaysian Forester 45: 10–20.<br />

ASHTON, P.S. 1982. Dipterocarpaceae. Flora Malesiana 9: 237–552.<br />

BARRETT, S.C.H., & KOHN, J.R. 1991. Genetic and evolutionary consequences of a small<br />

population size in plants: implications for conservation. Pp. 3–30 in Falk, D.A. & Holsinger,<br />

K.E. (eds.), Genetics and Conservation of Rare Plants. Oxford University Press, New<br />

York.<br />

BÜCKING, W. 2003. Are there threshold numbers for protected forests? Journal of<br />

Environmental Management 67: 37–45.<br />

CONDIT, R., SUKUMAR, R., HUBBELL, S.P. & FOSTER, R.B. 1998. Predicting population<br />

trends from size distributions: a direct test in tropical tree communities. American Naturalist<br />

152: 495–509.<br />

COX, G.W. 1993. Conservation Ecology. W.C. Brown, Dubugue, IA.<br />

DUDASH, M.R. & CARR, D.E. 1998. Genetics underlying inbreeding depression in Mimulus<br />

with contrasting mating systems. Nature 393: 682–684.<br />

FRANKEL, O.H. & SOULÉ, M.E. 1981. Conservation and Evolution. Cambridge University<br />

Press, Cambridge.<br />

FRANKLIN, I.R. 1980. Evolutionary change in small populations. Pp. 135–150 in Soulé, M.E.<br />

& Wilcox, B.A. (eds.), Conservation Biology: An Evolutionary-Ecological Perspective.<br />

Sinauer Assocs., Sunderland, Massachusetts.<br />

287


CONSERVATION STRATEGIES OF SHOREA LUMUTENSIS (DIPTEROCARPACEAE) IN PENINSULAR MALAYSIA<br />

GOODMAN, S.J. 1997. Rst Calc: a collection of computer programs for calculating estimates<br />

of genetic differentiation from microsatellite data and determining their significance.<br />

Molecular Ecology 6: 881–885.<br />

GRAUDAL, L., KJAER, E.D. & CANGER, S. 1995. A systematic approach to the conservation<br />

of genetic resources of trees and shrubs in Denmark. Forest Ecology and Management 73:<br />

117–134.<br />

GRAUDAL, L., YANCHUK, A. & KJÆR, E. 2004. National planning. Pp. 25–36 in FAO,<br />

DFSC, IPGRI, Forest Genetic Resources Conservation and Management, Vol. 1: Overview,<br />

Concepts and Some Systematic Approaches. International Plant Genetic Resources Institute,<br />

Rome.<br />

HAMRICK, J.L. 1993. Genetic diversity and conservation in tropical forest. Pp. 1–9 in Drysdale,<br />

R.M., John, S.E.T. & Yapa, A.C. (eds.), Proceedings of the ASEAN-Canada Symposium<br />

on Genetic Conservation and Production of Tropical Tree Seed. ASEAN–Canada Forest<br />

Tree Seed Center, Saraburi, Thailand.<br />

HAWKES, J.G. 1991. International workshop on dynamic in situ conservation of wild relatives<br />

of major cultivated plants: summary of final discussion and recommendations. Israel Journal<br />

of Botany 40: 529–536.<br />

HAWKES, J.G., MAXTED, N. & ZOHARY, D. 1997. Reserve design. Pp. 132–143 in Maxted,<br />

N., Ford-Lloyd, B.V. & Hwakes, J.G. (eds.), Plant Genetic Conservation: the In Situ<br />

Approach. Kluwer Academic Publishers, Dordrecht.<br />

HOLSINGER, K.E. 2000. Demography and extinction in small population. Pp. 55–74 in Young,<br />

A.G. & Clarke, G.M. (eds.), Genetics, Demography and Viability of Fragmented<br />

Populations. Cambridge University Press, Cambridge.<br />

IUCN 1994. IUCN Red List Categories and Criteria version 2.3. IUCN, Gland.<br />

KELLER, L.F. & WALLER, D.M. 2002. Inbreeding effects in wild populations. Trends in<br />

Ecology and Evolution 17: 230–241.<br />

KOSKI, V. 1996. Management guidelines for in situ conservation of wind pollinated temperate<br />

conifers. Forest Genetic Resources 24: 1–7.<br />

LAIDLAW, R.K. 1994. The Virgin Jungle Reserves of Peninsular Malaysia: the Ecology and<br />

Dynamics of Small Protected Areas in Managed Forest, Ph.D. dissertation, University of<br />

Cambridge, Cambridge.<br />

LANDE, R.C. 1998. Anthropogenic, ecological and genetic factors in extinction and<br />

conservation. Research on Population Ecology 40: 259–269.<br />

LAWRENCE, M.J. & MARSHALL, D.F. 1997. Plant population genetics. Pp. 99–113 in<br />

Maxted, N., Ford-Lloyd, B.V. & Hwakes, J.G. (eds.), Plant Genetic Conservation: the In<br />

Situ Approach. Kluwer Academic Publishers, Dordrecht.<br />

LEE, S.L. & KRISHNAPILLAY, B. 2004. Status of forest genetic conservation and management<br />

in Malaysia. Pp. 206–228 in Luoma-aho, T., Hong, L.T., Ramanatha Rao, V. & Sim, H.C.<br />

(eds.), Proceedings of the Asia Pacific Forest Genetic Resources Programme (APFORGEN)<br />

Inception Workshop. IPGRI-APO, Serdang, Malaysia.<br />

LEE, S.L., TANI, N., NG, K.K.S. & TSUMURA, Y. 2004. Isolation and characterization of 21<br />

microsatellite loci in an important tropical tree Shorea leprosula and their applicability to<br />

S. parvifolia. Molecular Ecology Notes 4: 222–225.<br />

LEE, S.L., WICKNESWARI, R., MAHANI, M.C. & ZAKRI, A.H. 2000. Genetic diversity of<br />

Shorea leprosula Miq. (Dipterocarpaceae) in Malaysia: Implications for conservation of<br />

genetic resources and tree improvement. Biotropica 32: 213–224.<br />

LEE, S.L., NG, K.K.S., SAW, L.G., NORWATI, A., SITI SALWANA, M.H., LEE, C.T. &<br />

NORWATI, M. 2002. Population genetics of Intsia palembanica (Leguminosae) and genetic<br />

288


LEE et al (2007)<br />

conservation of Virgin Jungle Reserves (VJRs) in Peninsular Malaysia. American Journal<br />

of Botany 89: 447–459.<br />

LIU, K. & MUSE, S.V. 2005. PowerMarker: Integrated analysis environment for genetic marker<br />

data. Bioinformatics 21: 2128–2129.<br />

MANLY, B.F.J. 1997. Randomization, Bootstrap and Monte Carlo Methods in Biology.<br />

Chapman and Hall, London.<br />

MARSHALL, T.C., SLATE, J., KRUUK, L. & PEMBERTON, J.M. 1998. Statistical confidence<br />

for likelihood-based paternity inference in natural populations. Molecular Ecology 7:<br />

639–655.<br />

MAXTED, N., GUARINO, L. & DULLOO, M.E. 1997a. Management and monitoring. Pp.<br />

144–159 in Maxted, N., Ford-Lloyd, B.V. & Hwakes, J.G. (eds.), Plant Genetic<br />

Conservation: the In Situ Approach. Kluwer Academic Publishers, Dordrecht.<br />

MAXTED, N., FORD-LLOYD, B.V. & HWAKES, J.G. 1997b. Complementary conservation<br />

strategies. Pp. 15–39 in Maxted, N., Ford-Lloyd, B.V. & Hwakes, J.G. (eds.), Plant Genetic<br />

Conservation: the In Situ Approach. Kluwer Academic Publishers, Dordrecht.<br />

MENGES, E.S. 1991. The application of minimum viable population theory to plants. Pp. 31–<br />

61 in Falk, D.A. & Holsinger, K. (eds.), Genetic and Conservation of Rare Plants. Oxford<br />

University Press, New York.<br />

MORAN, P.A.P. 1950. Notes on continuous stochastic phenomena. Biometrika 37: 17–23.<br />

MURRAY, M. & THOMPSON, W.F. 1980. Rapid isolation of high molecular weight plant<br />

DNA. Nucleic Acids Research 8: 4321–4325.<br />

NASON, J.D., HERRE, E.A. & HAMRICK, J.L. 1998. The breeding structure of a tropical<br />

keystone plant resource. Nature 391: 685–687.<br />

NEI, M. 1987. Molecular Evolutionary Genetics. Columbia University Press, New York.<br />

NEI, M., TAJIMA, F. & TATENO, Y. 1983. Accuracy of estimated phylogenetic trees from<br />

molecular data. Journal of Molecular Evolution 19: 153–170.<br />

OOSTERMEIJER, J.G.B., LUIJTEN, S.H. & DEN NIJS, J.C.M. 2003. Integrating demographic<br />

and genetic approaches in plant conservation. Biological Conservation 113: 389–398.<br />

PETIT, R.J., EL MOUSADIK, A. & PONS, O. 1998. Identifying population for conservation<br />

on the basis of genetic markers. Conservation Biology 12: 844–855.<br />

RIPLEY, B.D. 1976. The second-order analysis of stationary processes. Journal of Applied<br />

Probability 13: 255–266.<br />

SAITOU, N. & NEI, M. 1987. The neighbor-joining method: a new method for reconstructing<br />

phylogenetic trees. Molecular Biology and Evolution 11: 553–570.<br />

SAMBROOK, J. & RUSSELL, D.W. 2001. Molecular Cloning: A Laboratory Manual, 3rd<br />

edn. Cold Spring Harbor Laboratory Press, New York.<br />

SAW, L.G. & SAM, Y.Y. 2000. Conservation of Dipterocarpaceae in Peninsular Malaysia.<br />

Journal of Tropical Forest Science 12: 593–615.<br />

SHAFFER, M.L. 1981. Minimum population sizes for species conservation. BioScience 31: 131–<br />

134.<br />

SIMBERLOFF, D. & COX, J. 1987. Consequences and costs of conservation corridors.<br />

Conservation Biology 1: 63–71.<br />

SLATKIN, M. 1995. A measure of population subdivision based on microsatellite allele<br />

frequency. Genetics 139: 457–462.<br />

SOKAL, R.R. & ODEN, N.L. 1978. Spatial autocorrelation in biology. I. Methodology.<br />

Biological Journal of Linnean Society 10: 199–228.<br />

SYMINGTON, C.F. 1943. Forester’s Manual of Dipterocarps, Malayan Forest Records No.<br />

16. Forest Research Institute, Kuala Lumpur, Malaysia.<br />

289


CONSERVATION STRATEGIES OF SHOREA LUMUTENSIS (DIPTEROCARPACEAE) IN PENINSULAR MALAYSIA<br />

THEILADE, I., YANCHUK, A. & HALD, S. 2004. Establishment and management of ex situ<br />

conservation stands. Pp. 31–45 in FAO, FLD, IPGRI, Forest Genetic Resources<br />

Conservation and Management. Vol. 3: In Plantations and Genebanks (ex situ). International<br />

Plan Genetic Resources Institute, Rome.<br />

TUXILL, J. & NABHAN, G.P. 2001. People, Plants and Protected Areas: A Guide to In Situ<br />

Management. Earthscan Publications, London.<br />

WYATT-SMITH, J. 1950. Virgin jungle reserves. Malayan Forester 13: 92–94.<br />

290

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