Biodiversity assessment of Niah National Park. 2008

Mohd Tajuddin Abdullah, PhD, FASc

A transect survey was conducted from 2 6 December 2004 in Niah National Park to estimate species diversity and relative abundance of birds and mammals. This study was conducted in four forest line transects: Madu Trail (TR1), Sungai Tangap (TR2), Niah Great Cave (TR3), Bukit Kasut (TR4), and one river transect along the Niah River (RT). A total of 521 birds representing 59 species from 23 families were recorded. The Black-Nest Swiftlet (Aerodramus maximus) and the Mossy-Nest Swiftlet (Aerodramus salanganus) were the most common species in the park. The family Timaliidae (babblers), with nine species, was recorded as the most diverse family, whereas Strigidae (owls) and Hirundinidae (swallows) were the least diverse families with one species in each. A total of 29 mammalian individuals representing seven species from four families were recorded. The family Sciuridae (squirrels) with three species was recorded as the most diverse family, whereas Cynocephalidae (flying lemurs) and Muridae (rodents) were the least diverse families with one species and one individual each. TR1 was recorded with the highest Shannon-Weiner index (diversity index) of H = 4.75 and H = 2.20 for birds and mammals respectively. The lowest bird H = 3.73 was recorded for TR2, whereas the lowest mammal H = 0 was recorded for TR2 and RT. Although this study does not identify factors that contribute to different species diversity at each transect line, field observations suggest that vegetation and human activities were the major elements that contributed to the observations found at each transect in this study. Studies on the vegetation types and potential disturbances that influence the faunal diversity will provide useful insights in conservation and management planning of this park.

No. 4/2008 ISSN 1823-3902 Research Article Floral survey of Laiban sub-watershed in the Sierra Madre Mountain Range in the Philippines Karl L. VILLEGAS and Filiberto A. POLLISCO ........................................................................ 1 Research Article Diversity of gingers at Serudong, Sabah, Malaysia Januarius GOBILIK .................................................................................................................... 15 23 Research Article Horizontal distribution of intertidal nematode from Sabah, Malaysia SHABDIN Mohd. Long and OTHMAN Haji Ross....................................................................... 39 Research Article Stand structure and tree composition of Timbah Virgin Jungle Reserve, Sabah, Malaysia Januarius GOBILIK .................................................................................................................... 55 Research Article Preliminary molecular phylogeny of Bornean Plagiostachys (Zingiberaceae) based on DNA sequence data of internal transcribed spacer (ITS) Avelinah JULIUS, Monica SULEIMAN and Atsuko TAKANO ................................................... 67 Research Article Bats (chiropteran) recorded with Aspergillus species from Kubah National Park, Sarawak, Malaysia JAYA SEELAN Sathiya Seelan,Faisal Ali ANWARALI KHAN, SEPIAH Muid and M.T. ABDULLAH ......................................................................................... 81 Short Notes Rapid assessment on the abundance of bird species utilising the Kota Kinabalu Wetland Centre Mangroves, Sabah, Malaysia Andy Russel MOJIOL, AFFENDY Hassan, Jocelyn MALUDA and Suzen IMMIT ........................................................................................................................ 99 Short Communication A preliminary study on the morphometrics of the Bornean Elephant NURZHAFARINA Othman, MARYATI Mohamed, Abdul Hamid AHMAD, Senthivel NATHAN, Heather Thomas PIERSON and Benoit GOOSSENS .................................................................. 109 Checklist A preliminary survey on the butterfly fauna of Sungai Imbak Forest Reserve, a remote area at the centre of Sabah, Malaysia Mohd. Fairus JALIL, Hairul Hafiz MAHSOL, Nordin WAHID and Abdul Hamid AHMAD ................................................................................................................ 115 ISSN 1823-3902 http://www.ums.edu.my/penerbit 9 771823 390005 No. 4/2008 Research Article Biodiversity assesment in a Sarawak lowland dipterocarp rainforest of Niah National Park Faisal Ali ANWARALI KHAN, Mohamad Faishal BUJANG, Mohd. Azmin KASSIM, YAP Sheau Yuh, Besar KETOL, Wahap MARNI, Isa SAIT, C.J. LAMAN, Abang Arabi ABG AIMRAN, Zaidi MAWEK, Abang Abdul Mutalib ABG TAJUDIN, Haidar ALI and M.T. ABDULLAH .............................................................................................. Journal of Tropical Biology and Conservation Journal of Tropical Biology and Conservation No. 4/2008 ISSN 1823-3902 A JOURNAL OF THE INSTITUTE FOR TROPICAL BIOLOGY AND CONSERVATION UNIVERSITI MALAYSIA SABAH Instructions for Authors Managing Editors: Monica Suleiman and Henry Bernard, Institute for Tropical Biology and Conservation, Universiti Malaysia Sabah, Locked Bag 2073, 88999, Kota Kinabalu, Sabah, MALAYSIA.Tel: +60-88-320000 ext. 2375/2385; Fax: +60-88-320291. E-mail: monicas@ums.edu.my or hbtiandun@yahoo.com Manuscripts submitted to Journal of Tropical Biology and Conservation should comprise original, unpublished material and should not currently be under consideration for publication elsewhere. A Journal of the Institute for Tropical Biology and Conservation, Universiti Malaysia Sabah Editorial Committee Managing Editors Assoc. Prof. Dr Monica Suleiman Dr Henry Bernard Editorial Board Assoc. Prof. Dr Abdul Hamid Ahmad Dr Bakhtiar Effendi Yahya Assoc. 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All manuscripts are subjected to peer review. Monographs There are no charges for papers published. Very long papers (longer than 25 printed pages), however, are not encouraged. Such papers will be published in monographs series. Payment for excess pages can be arranged. Copyright and Reprints Authors who wish to republish an article or a significant part of it must obtain written permission to reprint the material from the original publisher. Authors will receive 25 free reprints. CONTENTS No. 4/2008 Research Article Floral survey of Laiban sub-watershed in the Sierra Madre Mountain Range in the Philippines Karl L. VILLEGAS and Filiberto A. POLLISCO ....................................................................... 1 Research Article Diversity of gingers at Serudong, Sabah, Malaysia Januarius GOBILIK ....................................................................................................................... 15 Research Article Biodiversity assesment in a Sarawak lowland dipterocarp rainforest of Niah National Park Faisal Ali ANWARALI KHAN, Mohamad Faishal BUJANG, Mohd. Azmin KASSIM, YAP Sheau Yuh, Besar KETOL, Wahap MARNI, Isa SAIT, C.J. LAMAN, Abang Arabi ABG AIMRAN, Zaidi MAWEK, Abang Abdul Mutalib ABG TAJUDIN, Haidar ALI and M.T. ABDULLAH ................................................................................................ 23 Research Article Horinzontal distribution of intertidal nematode from Sabah, Malaysia SHABDIN Mohd. Long and OTHMAN Haji Ross..................................................................... 39 Research Article Stand structure and tree composition of Timbah Virgin Jungle Reserve, Sabah, Malaysia Januarius GOBILIK ....................................................................................................................... 55 Research Article Preliminary molecular phylogeny of Bornean Plagiostachys (Zingiberaceae) based on DNA sequence data of internal transcribed spacer (ITS) Avelinah JULIUS, Monica SULEIMAN and Atsuko TAKANO ............................................... 67 Research Article Bats (chiropteran) recorded with Aspergillus species from Kubah National Park, Sarawak, Malaysian JAYA SEELAN Sathiya Seelan, Faisal Ali ANWARALI KHAN, SEPIAH Muid and M.T. ABDULLAH ....................................................................................... 81 Short Notes Rapid assessment on the abundance of bird species utilising the Kota Kinabalu Wetland Centre Mangroves, Sabah, Malaysia Andy Russel MOJIOL, AFFENDY Hassan, Jocelyn MALUDA and Suzen IMMIT ........................................................................................................................... 99 Short Communication A preliminary study on the morphometrics of the Bornean Elephant NURZHAFARINA Othman, MARYATI Mohamed, Abdul Hamid AHMAD, Senthivel NATHAN, Heather Thomas PIERSON and Benoit GOOSSENS ........................ 109 Checklist A preliminary survey on the butterfly fauna of Sungai Imbak Forest Reserve, a remote area at the centre of Sabah, Malaysia Mohd. Fairus JALIL, Hairul Hafiz MAHSOL, Nordin WAHID and Abdul Hamid AHMAD ............................................................................................................. 115 JOURNAL OF TROPICAL BIOLOGY AND CONSERVATION, 4 (1) : 1 – 14, 2008 Research Article Floral survey of Laiban sub-watershed in the Sierra Madre Mountain Range in the Philippines Karl L. VILLEGAS1, 3 and Filiberto A. POLLISCO 2, 4, Jr. 1 Cagayan Valley Programme on Environment and Development, Isabela State University, Cabagan Isabela 3328, Philippines 2 Environmental Science Institute, Miriam College, Loyola Heights, Quezon City 1101, Philippines 3 Institute of Environmental Sciences, Leiden University, 2300 RA Leiden, The Netherlands 4 ASEAN Centre for Biodiversity, University of the Philippines Los Banos, College, Laguna 4031, Philippines ABSTRACT The Laiban sub-watershed is part of the Kaliwa watershed nestled in the Sierra Madre Mountain Range in Luzon Island, Philippines. The watershed was identified as one of the 14 priority biodiversity conservation sites within the Sierra Madre Biodiversity Corridor. This study presents the results of the vegetation survey, which aimed to characterize various vegetation types and determine species richness and composition. Endangered, rare and endemic species were also identified. Land uses were surveyed and representative vegetation types were selected using patch and quadrat sampling techniques. Existing trail systems served as transect lines in conducting the rapid vegetation assessment during the transect walk. A total of 121 species belonging to 102 genera and 56 families were recorded during the survey. Of the 121 species recorded, 20% of these were endemics. Indigenous species Keywords: Plant Survey, Laiban, Kaliwa Watershed, Sierra Madre comprised about 53% while exotic species was 27%. Many of the abundant and common plants were exotics and indigenous species, which comprised majority of the total species recorded. The endangered species consisted only 4% of the total species recorded. The vegetation types identified were: 1) secondary forests that are scattered in patches along the slopes; 2) grassland, which could be seen with distinct boundaries; 3) plantation forest; and 4) bamboo (Schizostachyum lumampao) that may be the dominant vegetation. The subwatershed is degraded and characterized by the presence of kaingin areas, grasslands, Buho bamboo (S. lumampao) and fragmented patches of secondary forests and brushland mosaics. INTRODUCTION The Philippines is considered as one of the mega-biodiversity hotspots in the world (World Bank, 2004). A biodiversity hotspot is defined as “an area featuring exceptional 2 FLORAL SURVEY OF LAIBAN IN SIERRA MADRE concentrations of endemic species and expressing exceptional loss of habitat” (Myers et al., 2000). In the Philippines, there are over 6,000 endemic species with 80% of forest cover loss over the last century. It is no wonder that the country is a mega-biodiversity hotspot. One of the major biogeographic regions in the country is the Sierra Madre Mountain Range. In the southeastern portion of the range, the Kaliwa Watershed forms part of the Sierra Madre Biodiversity Corridor (SMBC). This watershed including its microbasin, the Laiban sub-watershed, was recently identified as one of the 14 priority biodiversity conservation sites within the SMBC (Miriam College, 2004). On the other end, there has been increasing interest in this sub-watershed as an alternative water source for Metro Manila residents. The Kaliwa Watershed has been widely studied, but previous studies have been devoted mainly in other sites. To date, there has been no documented survey conducted in the Laiban sub-watershed. This study was designed to generate baseline information on the vegetative types and composition of the sub-watershed; and to identify the conservation status of plant species in the area. MATERIALS AND METHODS The study site is the Laiban sub-watershed, which serves as an important microbasin of the bigger Kaliwa Watershed, nestled in the Sierra Madre Mountain Range. It is located in the east of Metro Manila in the district (Barangay) of Laiban, municipality of Tanay in the province of Rizal, the Philippines (Fig. 1). The village Project Site Legend Luzon Island Tree cover broadleaved evergreen Inland water 0 25 50 Figure 1: Location of the study site in Barangay Laiban 100 kilometres 3 KARL L.VILLEGAS & FILIBERTO A. POLLISCO community in the site belongs to the indigenous people called the Dumagats and Remontados. The sub-watershed is a 180 ha area which is generally characterized by mountainous terrain with steep slopes in all sides. This consisted of cultivated land and forested hills with slash and burn cultivation (kaingin) areas present in the cup of the inverted U-shape (Fig. 2) and along the lower slopes of the study site. Some small creeks run through the lower slopes and connect to the main river beyond the village. The Kaliwa Watershed was classified as a forest reserve and a portion of the watershed was declared as a National Park and Wildlife Sanctuary. At present, the Kaliwa Watershed is reclassified as a protected area under the National Integrated Protected Areas System (REECS, 1999 as cited in Miriam College, 2004). However, the area is considered degraded due to anthropogenic pressures. Upland farms or kaingin areas were mainly established by the indigenous people. The vegetation survey of the sub-watershed was conducted from February to May 2005. The Patch Sampling Technique (Ohsawa, 1991; Rice & Lambshead, 1994) was used based on identified land uses and survey objectives. This approach uses the selection of patches as a landscape element to determine the vegetation composition. Nested plots using the Quadrat Sampling Method (QSM) were laid out within patches of vegetation to gather biological data. Sampling plots measuring 20 m × 20 m were established to identify vegetation in the canopy stratum; 5 m × 5 m for the intermediate vegetation; and 1 m × 1 m quadrats for the ground vegetation. The transect walk method was also done for the rapid vegetation assessment using the existing trail system covering most of the area. The sampling plots and transect walk site are as shown in Figure 2. 1 4 Tower 2 3 Transect Walk Site 0 0.25 0.5 1 kilometres Figure 2: Location of sampling plots and transect walk in the sub-watershed 4 The identification of plant species was done through referral to literatures and specimen verification at the herbarium laboratory of the College of Forestry and Natural Resources in University of the Philippines Los Banos. The International Plant Name Index website (www.ipni.org) was consulted in verifying the names of plant taxa. In addition, the 2004 IUCN Red List of Threatened Species (www.iucnredlist.org) also served as an online information database in checking the conservation status of plants. RESULTS AND DISCUSSION A study on floral diversity was previously conducted in other areas of the Kaliwa Watershed (DENR, 2005). This characterized the bigger watershed into various community types such as Imperata stand, Saccharum stand, bamboo thicket and shrubland vegetation. For this study, the vegetation type and composition of the Laiban sub-watershed were surveyed and characterized. The Laiban sub-watershed was degraded and characterized by the presence of kaingin areas, grasslands, Buho bamboo (S. lumampao) and patches consisting of secondary forests and brushlands. The kaingin areas were mostly devoid of trees and made up of agricultural crops such as Manihot esculenta, Arachis hypogaea, Zea mays and Citrus sp. The plants outside the kaingin area were mostly grasses and small shrubs. The vegetation types identified during the survey were: 1) secondary forests that are scattered in patches along the slopes; 2) grassland, which could be seen with distinct boundaries; 3) plantation forest; and 4) bamboo (S. lumampao) that may be the dominant vegetation. The secondary forest is situated on the midslopes of the site just above the kaingin area tilled by the ‘Chieftain’ of the indigenous FLORAL SURVEY OF LAIBAN IN SIERRA MADRE people. The elevation is recorded at 290 m asl along a west-facing slope. Six medium-sized trees were recorded in the canopy vegetation of the sampling plot. These included Ficus gul, Strombosia philippinensis, Ficus nota, Leucaena leucocephala, Artocarpus ovatus and Buchanania nitida. All of these species usually thrive along slopes near tributaries, except for L. leucocephala, which could also persist in the other surrounding habitat types, e.g. brushlands. Ten species were identified in the intermediate vegetation. These were Alphonsea arborea, Myristica philippinensis, S. philippinensis, Bridelia penangiana, Hedyachras philippinensis, Terminalia foetidissima, Pisonia umbellifera, Gomphandra luzoniensis, Dinochloa acutiflora and Leea aculeata. There were only six species recorded at the ground level. These included the Aglaonema sp., Curculigo capitulate, L. aculeata, Centrosema pubescens, Mikania cordata and Donax cannaeformis. Other species were recorded during the transect walk within the secondary forest and brushland mosaic (Table 1). The grassland vegetation (160 m asl) is dominated by the grass species, Imperata cylindrica. The tree species found in the area are sparse. However, there were still three species recorded such as Antidesma ghaesembilia, Bauhinia malabaricum and Gmelina arborea. The former two species are both indigenous and naturally growing in the area. They are quite common in grassland vegetation throughout the Sierra Madre Mountain Range. Gmelira arborea, on the other hand is introduced, as an attempt on reforesting the area. There were six species representing the intermediate stratum as follows: Melastoma malabathricum, Cananga odorata, Cratoxylon formosum, A. ghaesembilia, B. malabaricum and Psidium guajava. The ground vegetation consisted only of two species, I. cylindrica and C. odorata. KARL L.VILLEGAS & FILIBERTO A. POLLISCO At almost 500 m asl, the grassland vegetation in the ridge is slightly different from the grassland found in the lower altitude. Different vegetative composition was observed except for the common presence of I. cylindrica. There were six tree species recorded which were the Ficus septica, Ficus nota, Macaranga tanarius, Cordia dichotoma, F. gul and Acalypha stipulacea. The presence of Ficus trees in this grassland is unusual, however, these species have also been recorded in high elevation mossy forest types in the Bicol Region (Pollisco, 2002). Other species included in the sampling plot were six pioneer species. These were the Lantana camara, D. cannaeformis, C. odorata, Saccharum spontaneum and two vine species. No species were recorded in the ground layer because honey gatherers sporadically burned the area. This demonstrated that anthropogenic pressures are being exerted aside from the kaingin activities found in the lower slopes. At 180 m asl, the plantation forest is characterized by more or less evenly spaced trees. There were only three dominant species of trees, Swietenia macrophylla, Acacia auriculiformes and G. arborea. The intermediate vegetation consisted of mostly indigenous species. These included Buchanania arborescens, Semecarpus cuneiformis, Guioa koelreuteria, Pterospermum celebicum, Pittosporum pentandrum and Hibiscus tiliaceus. In the undergrowth, only four species were recorded. These were the Chromolaena odorata, Lygodium flexuosum, M. malabathricum and Leukosyke capitallata. Chromolaena odorata and M. malabathricum are both exotics. The Buho (S. lumampao) bamboo represents another vegetation type occupying a large portion of the site. On the other hand, they are subjected to the kaingin practice of the local people, hence, most of these are being cut down and burned to make way for cash crops. Being 5 a grass species, the Buho bamboo is able to reestablish during the period when the local people shift to another adjacent area and the cycle starts all over again. A total of 121 species belonging to 102 genera and 56 families were recorded. Table 1 shows the checklist of vegetation found in Laiban sub-watershed. The site harboured about eight plant habits or form. Out of 121 species documented, 69 were tree species, 17 shrubs, nine herbs, seven vines, six grasses, five palms and four species for both bamboo and fern. There were no large trees found in the area, however, there were tree species that belong to the large size category such as the Koordersiodendron pinnatum and Shorea contorta. Another large tree was the Albizzia acle. All of three species belong to the endangered species list under the CITES (PAWB-DENR, 2000) and IUCN (2004), though with varying conservation status. Many of the shrubs were less than a metre tall which occupied the ground stratum. Most of these were found in open areas such as Stachytarpheta jamacaensis, Moghania strobilifera and Mussaenda sp. The fern plants were mostly located in the upper slopes adjacent to water sources or where there is high moisture and shade. Endemicity is defined as the state of having limited geographic range, which could be confined to an area or to a country (Williams et al., 1996). Some species in the watershed were classified as endemics, either within the Sierra Madre Mountain Range or as country endemic. Of the 121 species recorded, 20% or 24 of these were endemics. The proportion of endemics to exotic and indigenous species is shown in Figure 3. Examples of these endemic species were A. acle, Artocarpus blancoi, S. philippinensis and M. philippinensis. 6 Table 1: List of vegetation found during the survey in Laiban sub-watershed SCIENTIFIC NAME PLANT HABIT VEGETATION TYPE ENCOUNTERED ECOLOGICAL CONSERVATION STATUS STATUS Acanthaceae Pachystachys lutea Nees Cordyline fruticosa (L.) A. Chev. shrub plantation forest exotic common shrub plantation forest exotic abundant large tree plantation forest indigenous depleted medium to large tree grassland, plantation forest indigenous depleted small to medium tree small to medium tree indigenous indigenous rare depleted exotic abundant endemic indigenous rare endangered Agavaceae Anacardiaceae Koordersiodendron pinnatum (Blanco) Merr. Buchanania arborescens (Blume) Blume Buchanania nitida Engl. Semecarpus cuneiformis Blanco Mangifera indica L. large tree Annonaceae Platymitra arborea (Blanco) Kesler Cananga odorata (Lamk.) Hook.f. & Thoms. large tree medium tree plantation/secondary forest plantation/secondary forest/brushland mosaic plantation/secondary forest/brushland mosaic secondary forest secondary forest Apocynaceae Alstonia parvifolia Merr. small tree grassland, plantation forest endemic depleted Araceae Aglaonema commutatum Schott Colocasia esculentum (L.) Schott herb herb secondary forest secondary forest indigenous exotic common abundant Araliaceae Polyscias nodosa (Blume) Seem. medium tree plantation/secondary forest/brushland mosaic indigenous depleted Arecaceae Areca catechu L. palm secondary forest/ brushland mosaic endemic common FLORAL SURVEY OF LAIBAN IN SIERRA MADRE FAMILY NAME SCIENTIFIC NAME PLANT HABIT VEGETATION TYPE ENCOUNTERED ECOLOGICAL STATUS CONSERVATION STATUS Arecaceae Arenga pinnata (Wurmb) Merr. palm indigenous common Veitchia merrillii Becc. H.E. Moore Cocos nucifera L. palm palm endemic exotic abundant abundant Calamus merrillii Becc. rattan secondary forest/ brushland mosaic plantation forest plantation/secondary forest brushland mosaic plantation/secondary forest brushland mosaic endemic endangered Aspleniaceae Asplenium musaefolium Mett. fern secondary forest indigenous common Asteraceae Crassocephalum crepidioides (Benth.) S. Moore Chromolaena odorata (L.) R.M. King & M. Robinson Mikania cordata (Burm. f.) B.L. Rob. shrub plantation forest indigenous common shrub exotic common vine grassland/ridge grassland, plantation forest secondary forest exotic common Bombacaceae Ceiba pentandra (L.) Gaertn. large tree ridge grassland exotic common Boraginaceae Cordia dichotoma G. Forst. small tree ridge grassland indigenous depleted Burseraceae Canarium asperum Benth. ssp. asperum var. asperum large tree plantation forest indigenous depleted Clusiaceae Cratoxylum formosum (Jack) Dyer ssp. Formosum small tree grassland, plantation forest indigenous depleted Combretaceae Terminalia foetidissima Griff. large tree plantation/secondary forest endemic depleted Convulvulaceae Ipoemoea batatas (L.) Lamk vine secondary forest indigenous abundant Cyperaceae Cyperus rotundus L. Cyperus sp. sedge sedge plantation forest plantation forest indigenous indigenous common common KARL L.VILLEGAS & FILIBERTO A. POLLISCO FAMILY NAME 7 8 SCIENTIFIC NAME PLANT HABIT VEGETATION TYPE ENCOUNTERED ECOLOGICAL CONSERVATION STATUS STATUS Datiscaceae Octomeles sumatrana Miq. large tree ridge grassland indigenous indeterminate Dipterocarpaceae Shorea contorta Vidal large tree secondary forest/ brushland endemic critically endangered Euphorbiaceae Homonoia riparia Lour. Neotrewia cumingii (Muell.-Arg.) Pax & K. Hoffm. Antidesma ghaesembilla Gaertn. var. ghaesembilla small tree small tree ridge grassland secondary forest indigenous endemic common depleted small tree indigenous common Macaranga tanarius (L.) Muell.-Arg. small tree indigenous abundant Acalypha amentacea Roxb. Manihot esculenta Crantz Macaranga bicolor Muell.-Arg. Aleurites moluccana (L.) Willd. Codiaeum variegatum (L.) Blume Bridelia penangiana Hook. f. small tree shrub small to medium tree large tree small tree small tree grassland, plantation/ secondary forest/ brushland mosaic ridge grassland, secondary forest/brushland mosaic ridge grassland plantation forest secondary forest plantation forest plantation forest secondary forest indigenous exotic endemic exotic exotic indigenous common abundant vulnerable abundant common depleted Bauhinia malabarica Roxb. small tree indigenous abundant Centrosema pubescens Benth. Calopogonium mucunoides Desv. vine vine grassland, secondary forest/brushland mosaic secondary forest plantation forest exotic exotic common common Pterocarpus indicus Willd. Forma indicus large tree plantation forest indigenous endangered Flemingia strobilifera (L.) Roxb. ex W. Aiton Samanea saman (Jacq.) Merr. vine plantation forest indigenous common large tree plantation forest exotic abundant Flacourtiaceae Flacourtia jangomas (Lour.) Raeusch. small tree plantation forest exotic common Heliconiaceae Heliconia psittacorum L.f. herb plantation forest exotic abundant Fabaceae Fabaceae FLORAL SURVEY OF LAIBAN IN SIERRA MADRE FAMILY NAME PLANT HABIT VEGETATION TYPE ENCOUNTERED ECOLOGICAL CONSERVATION STATUS STATUS Hypoxidaceae Curculigo capitulata (Lour.) O. Kuntze herb secondary forest, ridge grassland indigenous common Icacinaceae Gomphandra luzoniensis (Merr.) Merr. medium tree secondary forest endemic indeterminate Leeaceae Leea aculeata Blume ex Spreng. small tree secondary forest/ brushland mosaic indigenous common Malvaceae Hibiscus rosasinensis L. Urena lobota L. Hibiscus tiliaceus L. Rubus sp. small tree shrub small tree small tree plantation forest plantation forest plantation forest ridge grassland exotic exotic indigenous indigenous abundant common common depleted Marantaceae Donax cannaeformis (Forst.) K. Schum herb secondary forest/brushland mosaic, ridge grassland indigenous rare Melastomataceae Melastoma malabathricum L. shrub grassland, plantation forest indigenous common Meliaceae Swietenia mahogani (L.) Jacq. large tree exotic endangered Dysoxylum cumingianum C. DC. small to medium tree plantation/secondary forest/brushland mosaic secondary forest indigenous depleted Albizia acle (Blanco) Merr. medium to large tree Acacia auriculiformis A. Cunn. small to medium tree ex. Benth Leucaena leucocephala (Lam.) de Wit small tree Mimosa pudica L. shrub plantation forest plantation forest endemic exotic depleted abundant secondary forest plantation forest exotic exotic abundant common Artocarpus blancoi (Elmer) Merr. large tree endemic vulnerable Artocarpus ovatus Blanco Ficus gul Laut. et K. Schum. var. gul small tree small tree endemic indigenous abundant depleted Ficus septica Burm. F. var. septica small tree plantation/secondary forest secondary forest secondary forest, ridge grassland secondary forest, ridge grassland indigenous common Mimosaceae Moraceae 9 SCIENTIFIC NAME KARL L.VILLEGAS & FILIBERTO A. POLLISCO FAMILY NAME PLANT HABIT VEGETATION TYPE ENCOUNTERED ECOLOGICAL CONSERVATION STATUS STATUS Moraceae Ficus ulmifolia Lam. Artocarpus heterophyllys Lamk. Ficus congesta Roxb. var. congesta Ficus pseudopalma Blanco Ficus odorata (Blanco) Merr. Artocarpus communis J.R. & G. Forst. Ficus variegata Blume var. variegate Ficus nota (Blanco) Merr. small tree small to medium tree medium tree small tree small to medium tree large tree large tree small tree secondary forest plantation forest plantation forest grassland, secondary forest secondary forest plantation forest plantation forest plantation/secondary forest, ridge grassland endemic exotic indigenous endemic endemic exotic indigenous indigenous vulnerable abundant depleted common depleted common common common Moringaceae Moringa oleifera Lamk. small tree plantation forest exotic abundant Musaceae Musa textiles Nees Musa sapientum L. herb herb secondary forest plantation forest indigenous exotic abundant abundant Myristicaceae Myristica philippinensis Lam. medium tree secondary forest endemic vulnerable Myrsinaceae Ardisia squamulosa Presl small tree plantation/secondary forest endemic vulnerable Myrtaceae Psidium guajava L. Syzygium cumini (L.) Skeels Syzygium calubcob (C.B.Rob) Merr. small tree medium tree medium tree grassland ridge grassland secondary forest/ grassland mosaic exotic indigenous indigenous abundant abundant indeterminate Nyctaginaceae Pisonia umbellifera (Forst.) Seem. small tree secondary forest indigenous indeterminate Olacaceae Strombosia philippinensis (Baill.) Rolfe medium tree secondary forest endemic depleted Passifloraceae Passiflora foetida L. vine ridge grassland exotic common Pittosporaceae Pittosporum pentandrum (Blanco) Merr. small tree plantation/secondary forest/brushland mosaic indigenous indeterminate FLORAL SURVEY OF LAIBAN IN SIERRA MADRE SCIENTIFIC NAME 10 FAMILY NAME SCIENTIFIC NAME PLANT HABIT VEGETATION TYPE ENCOUNTERED ECOLOGICAL CONSERVATION STATUS STATUS Poaceae Dinochloa acutiflora (Munro) S. Dransf. Schizostachyum lumampao (Blanco) Merr. Bambusa merrilliana (Elmer) Rojo & Roxas Imperata cylindrica (L.) Beauv. bamboo secondary forest indigenous common bamboo plantation forest endemic common bamboo secondary forest/ brushland mosaic grassland/ridge grassland, plantation forest indigenous rare indigenous abundant Zea mays L. Saccharum spontaneum L. grass grass plantation forest grassland/ridge grassland exotic indigenous abundant abundant Polygalaceae Xanthophyllum vitellinum (Blume) Dietr. small tree ridge grassland indigenous indeterminate Polypodiaceae Diplazium esculentum (Retz.) Sw. fern indigenous common Nephrolepis sp. fern indigeneous common Rosaceae Prunus grisea (Blume) Kalkm. var. grisea small to medium tree secondary forest, ridge grassland plantation/secondary forest/brushland mosaic, ridge grassland secondary forest indigenous indeterminate Rubiaceae Nauclea orientalis (L.) L. Neonauclea auriculata Quis. & Merr. Mussaenda philippica A. Rich. var. aurorae Sul. medium to large tree plantation forest indigenous depleted small tree plantation forest indigenous common Rubiaceae Psychotria luzoniensis (Cham. & Schlecht.) F. -Vill. small tree secondary forest indigenous common Rutaceae Micromelum inodorum (Blanco) Tan. Micromelum compressum (Blanco) Merr. small tree small tree secondary forest secondary forest/ brushland mosaic indigenous indigenous indeterminate indeterminate grass KARL L.VILLEGAS & FILIBERTO A. POLLISCO FAMILY NAME 11 12 SCIENTIFIC NAME Sapindaceae Guioa koelreuteria (Blanco) Merr. small tree Glenniea philippinensis (Radlk.) Leenh. small to medium tree plantation/secondary forest endemic secondary forest endemic rare rare Sapotaceae Chrysophyllum cainito L. medium tree plantation forest exotic common Schizaeaceae Lygodium japonicum Sw. fern indigenous common Lygodium circinnatum (Burm. f.) Sw. fern secondary forest/ brushland mosaic plantation/secondary forest/brushland mosaic indigenous common Pterospermum niveum Vidal small tree indigenous depleted Pterospermum obliquum Blanco small tree plantation/secondary forest/brushland mosaic secondary forest/ brushland mosaic indigenous depleted Tiliaceae Diplodiscus paniculatus Turcz. medium tree secondary forest endemic vulnerable Ulmaceae Celtis luzonica Warb. large tree secondary forest endemic vulnerable Urticaceae Leucosyke capitellata (Poir.) Wedd. small tree plantation forest indigenous indeterminate Verbenaceae Premna odorata Blanco Gmelina arborea Roxb. Stachytarpheta jamaicensis (L.) Vahl. Lantana camara L. small tree large tree shrub shrub indigenous exotic exotic exotic abundant abundant common common Clerodendrum bethunianum small tree plantation forest grassland, plantation forest plantation forest plantation/secondary forest/brushland mosaic, ridge grassland ridge grassland indigenous common Kolowratia elegans Presl. herb secondary forest, ridge grassland endemic common Sterculiaceae Zingiberaceae PLANT HABIT VEGETATION TYPE ENCOUNTERED ECOLOGICAL CONSERVATION STATUS STATUS FLORAL SURVEY OF LAIBAN IN SIERRA MADRE FAMILY NAME 13 KARL L.VILLEGAS & FILIBERTO A. POLLISCO 20% Indigenous Exotic Endemic 53% 27% Figure 3: Proportion of ecological status of species in the Laiban sub-watershed The endangered species consisted only 4% of the total species listed in the sampling area (Table 2). These endangered species were C. odorata, Pterocarpus indicus, Calamus merrillii, S. contorta and S. macrophylla. Most of these are listed in the IUCN Red List of Threatened Species while the others are listed under the Convention on International Trade of Endangered Species (CITES). The tree, S. macrophylla, though classified as exotic is quite common, but also listed under both CITES and IUCN because of its high value in the international trade. Vulnerable species, on the other hand, comprised 6% of the total species recorded. Some of these were A. blancoi, Diplodiscus paniculatus, Macaranga bicolor, F. ulmifolia, and M. philippinensis. Table 2: Conservation status of plant species Conservation Status Number of Species Percentage (%) Abundant Common Depleted Vulnerable Rare Endangered Indeterminate 27 44 22 7 6 5 10 22 36 18 6 5 4 8 Total 121 100 Many of the abundant and common plants consisted of exotics and indigenous species. This comprised majority of the total species recorded. Men often introduce exotic species due to their aesthetic value, whereas wildlife disperses the indigenous ones. The complete list of the conservation status of species is found in Table 1. ACKNOWLEDGEMENTS We would like to thank our colleagues whom in one way or another, have contributed to the completion of the project, especially Drs. Angelina Galang and Donna Reyes of the Environmental Science Institute of Miriam College. Our sincere gratitude also goes to the local people of Laiban who accompanied us during the fieldwork and accommodated us during our stay in the barangay. Finally, we also would like to acknowledge Dr. Rodel Lasco for commenting on this paper. REFERENCES Department of Environment and Natural Resources (DENR). 2005. Watershed Research and Development Support Project for Kaliwa Watershed. Project Report. University of the Philippines Los Baños Foundation, Inc. College, Laguna. 14 IUCN Red List of Threatened Species. 2004. http://www.iucnredlist.org/ Miriam College. 2004. Comprehensive Plan of the Southern Sierra Madre Wildlife Center Project. (unpublished). Myers, N., R.A. Mittermeier, G.A.B. Da Fonseca and J. Kent. 2000. Biodiversity hotspots for conservation priorities. Nature. 403: 853 – 858. Ohsawa, M. 1991. Structural comparison of tropical montane rainforest along latitudinal and altitudinal gradients in South and East Asia. Vegetation. 97: 1 – 10. PAWB-DENR. 2000. Statistics on Philippine Protected Areas and Wildlife Resources. DENR, Quezon City, Philippines. Pollisco, F.A. Jr. 2002. Biophysical Assessment of the Quinale a river Watershed in Albay, Bicol. Final Report to the DENR Region V and World Bank. Hassalts and Assoc., Inc. (unpublished). FLORAL SURVEY OF LAIBAN IN SIERRA MADRE Rice, A.L. and P.J.D. Lambshead. 1994. Patch dynamics in the deep sea benthos: The role of a heterogeneous supply of organic matter. Pp.469 – 499. In: Giller, P.S., Hildrew, A.G. and D.G. Raffaelli (Eds). Aquatic Ecology: Scale, pattern and process. Proceedings of the 34th Symposium of the British Ecological Society. Oxford: Blackwell Scientific Publications. The International Plant Name Index. 2005. Published on the Internet. http:// www.ipni.org/ (accessed 16 November 2005). Williams, P., D. Gibbons, C. Margules, A. Rebelo, C. Humphries and R. Pressey. 1996. A Comparison of Richness Hotspots, Rarity Hotspots, and Complementary Areas for Conserving Biodiversity of British Birds. Conservation Biology. 10: 155 – 174. World Bank. 2004. Philippines Environment Monitor: Assessing Progress. The World Bank Group. JOURNAL OF TROPICAL BIOLOGY AND CONSERVATION, 4 (1) : 15 – 21, 2008 Research Article Diversity of gingers at Serudong, Sabah, Malaysia Januarius GOBILIK Sabah Forestry Department, Forest Research Centre P.O. Box 1407, Sepilok 90715 Sandakan, Sabah, Malaysia ABSTRACT The species richness and abundance of the Zingiberaceae (hereafter gingers) were studied in five study plots in Serudong and in one study plot in an adjacent area. The study plots were in undisturbed upland kerangas forest (mossy kerangas forest), one in an undisturbed lower montane-kerangas forest, one in disturbed upland mixed dipterocarp forest, and three in upland mixed dipterocarp-kerangas forest (disturbed, partially disturbed and undisturbed, respectively). Thirty-nine species were documented from the general area; eight of which were found outside the plots. Eightyone percents of the species were recorded from the disturbed forest plots. None of the species were recorded from the undisturbed upland kerangas and lower montanekerangas forest plots. Species richness averaged 11 species per hectare. The index of diversity of gingers for the study area was estimated to be 2.0 (Shannon diversity index, H’) and it was highest in the disturbed upland mixed dipterocarp forest plot. At the scale of this study, the diversity of gingers in Serudong is found to be lower than that of many other forest reserves in Sabah. The most novel collection was Geostachys, a genus that was documented in Sabah only recently. Keywords: Gingers, species composition, Borneo This finding was the second for a species of this genus in Sabah. INTRODUCTION The diversity of gingers in Serudong has not been well documented. Therefore, in 2006, a team from the Sabah Forestry Department carried out an expedition to study the density and composition of these plants in this area. The collected information can be used to assess the importance of Serudong as an in-situ conservation area for gingers in Sabah. The results are reported in this paper. METHODS Study Site Serudong is a 123,643 ha forest management unit (FMU25) situated in southern Sabah on the border to Kalimantan (4°12 – 33’N, 117°8 – 32’E; Fig. 1). The elevation is 450 – 1,300 m above sea level but only a few hills rise above 1,000 m (Sabah Forestry Department, 2005). The daily temperature fluctuates from 21°C to 32°C. The annual rainfall is 2,500 – 3,500 mm. The area is characterized by the Kapilit geological formation and Lokan and Crocker are the main soil associations; others are Maliau, Labau, Kalabakan, Serudong and Gomantong associations. Its main soil unit is orthic acrisol, which is sandy and less fertile. 16 DIVERSITY OF GINGERS AT SERUDONG, SABAH Figure 1: Location of Serudong (FMU25) in Sabah (insert picture) and locations of the study plots in FMU (plot 1–5). The control plot (plot 6) was established in Nurod-Urod Forest The natural vegetation of the area is composed of upland mixed dipterocarpkerangas (59.1%); lower montane-kerangas (17.8); lowland mixed dipterocarp-kerangas (7.1); lowland mixed dipterocarp (6.6); upland mixed dipterocarp (4.9); upland kerangas (4.4; mossy kerangas forest sensu Fox, 1972); and lowland kerangas forests (0.1). A large portion of the forest is in secondary and logged-over conditions. Sampling Method Five study plots (1–5) were established in four of the major forest types in Serudong (Table 1). The locations of the plots were preidentified on a satellite image of the study area and were visited on the ground. One control plot (Plot 6) was established in Nurod Urod Forest Reserve, a forest reserve in adjacent area to Serudong. In the plots, gingers were identified and counted. Relative density of the species was calculated as sum of density of the species divided by sum of density of all species and multiplied by 100. From these data, the diversity of the gingers was estimated using PCORD® (McCune & Mefford, 1999; version 4.14). The same software was used to run a cluster analysis to find out the similarity of composition of gingers between the studied forest types (distance measure: Sorensen (Bray-Curtis); linkage: group average). The gingers were also qualitatively surveyed along the trail to the peak of Gunung Maliat (1,300 m), which is situated on the international boundary that separates Sabah and Kalimantan, Indonesia. Voucher specimens were kept at Sandakan Herbarium (SAN). 17 JANUARIUS GOBILIK Table 1: The five plots established at Serudong (plot 1–5) and the one from Nurod Urod (plot 6) and their characteristics Plot 1 2 3 4 5 6 Forest Type Disturbance Size (m 2 ) Upland kerangas Lower montane-kerangas Upland mixed dipterocarp Upland mixed dipterocarp-kerangas Upland mixed dipterocarp-kerangas Upland mixed dipterocarp-kerangas Undisturbed Undisturbed Disturbed Disturbed Partially disturbed Undisturbed 4 4 4 4 4 4 RESULTS No gingers were recorded from the undisturbed upland kerangas forest (Plot 1) and undisturbed lower montane-kerangas forest plots (Plot 2). The remaining plots harboured 31 species (Table 2). Eight additional species were found outside the plots (Burbidgea schizocheila Hackett, Elettariopsis kerbyi R.M. Sm., Etlingera rubromarginata A.D. Poulsen & Mood, Etlingera brachychila var. vinosa A.D. Poulsen, Geocharis fursiformis var. borneensis R.M. Sm., Hedychium cylindricum Ridl., Hedychium sp., and Zingiber argenteum Theilade & Mood). Of these 39 species, eight taxa were identified only to the genus due to the lack of flowers for a thorough identification. Species richness averaged 11 species per hectare (ranged 7–17 per plot). The index of diversity and species evenness of gingers and species evenness in the area were estimated to be 2.0 (Shannon diversity index, H’) and 0.9, respectively (Table 3). Relative density averaged 3(±6) stems per hectare. Index of diversity, species count, relative density and species evenness were highest in the disturbed forest plots. In terms of species composition and relative density, the cluster analysis showed that Plots 3 and 4 × × × × × × 20 50 190 300 400 500 Elevation (m) 770 1300 860 700 720 760 were inseparable from each other and were distinctively dissimilar (100%) from Plots 5 and 6. Plots 5 and 6, on the other hand, were only 57% similar. The most interesting collection was that of Geostachys, a genus that was found occurring in Sabah only recently at Maliau Basin (see Lim & Lau, 2006). Serudong is thus a new locality for its occurrence. The species was represented by 22 clumps in the partially disturbed upland mixed dipterocarpkerangas forest plot (Plot 5). This species has a potential as an ornamental; the leaves were dark green with burgundy underneath and the stem was dark green with reddish base. The old and dried inflorescence was found with old floral bracts congested at its top and the old fruits appear to be oblong; this species is distinct from that described from Maliau Basin. DISCUSSION At the scale of this study, the diversity of gingers in Serudong is found to be lower than that of many other forest reserves in Sabah. There are about 168 species of gingers in Sabah (see: Gobilik & Yusoff, 2005; Gobilik et al., 2005a; Poulsen, 2006; Julius et al., 2007), but only 23% are found at Serudong. The number of species in this area can be ranked as lower than that of Mt. Kinabalu (Gobilik & Yusoff, 2005), Imbak Valley (Gobilik et al., 18 DIVERSITY OF GINGERS AT SERUDONG, SABAH Table 2: List, relative mean density and evenness of ginger species in the study plots No. Species Mean (±SD) Evenness 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 Alpinia ligulata K. Schum. Alpinia nieuwenhuizii Val. Amomum borealiborneense I.M. Turner Amomum coriaceum R.M. Sm. Amomum dimorphum M. Newman Amomum oliganthum K. Schum. Amomum sp. Amomum testaceum Ridl. Amomum uliginosum Koenig Boesenbergia variegata R.M. Sm. Elettaria surculosa (K. Schum.) Burtt & R.M. Sm. Etlingera albolutea A.D. Poulsen Etlingera baculutea A.D. Poulsen Etlingera brevilabrum (Val.) R.M. Sm. Etlingera inundata Sakai & Nagam. Etlingera velutina (Ridl.) R.M. Sm. Geostachys sp. Globba pendula Roxb. Globba propinqua Ridl. Hornstedtia reticulata K. Schum. Hornstedtia sp. Plagiostachys breviramosa Cowley Plagiostachys aff. roseiflora A. Julius & A. Takano Plagiostachys oblanceolata J. Gobilik & A. Lamb Plagiostachys sp. a Plagiostachys sp. b Plagiostachys strobilifera (Bak.) Ridl. Zingiber pseudopungens R.M. Sm. Zingiber sp. a Zingiber sp. b Zingiber viridiflavum Theilade & Mood 5.9 (6.9) 3.2 (6.5) 1.6 (1.9) 4.3 (8.6) 2.2 (2.9) 1.4 (1.7) 3.6 (7.1) 5.6 (11.2) 11.7 (14.8) 1.2 (2.4) 3.6 (5.8) 0.6 (1.2) 0.5 (1.0) 2.7 (4.7) 5.0 (3.6) 1.2 (2.4) 11.2 (22.5) 1.2 (2.4) 0.3 (0.6) 0.5 (1.0) 0.6 (1.2) 1.2 (2.4) 0.3 (0.6) 8.1 (10.6) 1.5 (2.9) 3.1 (6.1) 6.3 (9.7) 2.9 (4.5) 1.1 (1.3) 0.6 (1.2) 0.3 (0.6) 1.0 0.0 0.9 0.0 0.9 0.9 0.0 0.0 0.9 0.0 0.6 0.0 0.0 0.5 1.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.9 0.0 0.0 0.7 0.7 1.0 0.0 0.0 3.0 (4.9) 0.3 Averages: Table 3: Relative mean density, species count (S), evenness (E) and diversity index of gingers in the study plots (H = Shannon’s diversity index; D = Simpson’s diversity index) Plot Mean (±SD) S E H D Forest Condition 3 4 5 6 2.4 3.2 3.2 3.2 (3.5) (4.9) (9.2) (7.8) 17 12 8 7 0.9 0.9 0.7 0.9 2.5 2.4 1.5 1.7 0.9 0.9 0.7 0.8 Disturbed Disturbed Partially disturbed Undisturbed Averages: 3.0 (6.4) 11 0.9 2.0 0.8 JANUARIUS GOBILIK 2005b), Tabin Wildlife Reserve (Gobilik, 2002), Crocker Range Park (Gobilik & Yusoff, 2005), Danum Valley (Magintan, 2000), Maliau Basin, and Tawau Hills Park (Gobilik, 2005; unpublished expedition data). Nevertheless, Serudong harbours more gingers than the Mt. Trus Madi area (Gobilik & Yusoff, 2005), another area in Sabah where the upland mixed dipterocarp forest type is also prominent. The low diversity of gingers in Serudong can be associated with many factors. The most important could be the distribution of kerangas (heath) soil, degrees of forest disturbance, and altitudes in the study area. Kerangas forest is known to be infertile (Newbery, 1991), and this forest will not support many ginger species, which are generally known to grow well only on moist and high-organic-content soils (Larsen et al., 1999). The low species count in the undisturbed upland mixed dipterocarpkerangas forest plots indicates the adverse effect of kerangas soil to recruitment of gingers. Most of the species are even occurring at a very low frequency and abundance as one can interpret from the very low evenness of the species (see Table 2). Gingers are generally non-specialist regarding substrate (Theilade, 1998) especially in kerangas forest, perhaps with the exception of Etlingera dictyota (Poulsen, 2006). Forest destruction reduces plant diversity (Slik et al., 2002), but to a certain degree, it could cause the contrary (Connell, 1978). In Serudong, the latter appears to be case because the disturbed forest plots harbour more species than the undisturbed forest plots (Table 3). Thus it could be that in the forest where the soil is infertile such as in kerangas forest, logging would instead increase soil fertility as well as ginger diversity. It is quite logic to assume that nutrients from the rotting tree branches and stumps are recycled into the soil and are 19 consumed by the gingers. The gingers would then have more energy to reproduce as one can interpret from their slightly higher Simpson’s diversity index from the disturbed forest plots (Table 3; Simpson’s diversity index is reported to be positively dependent on species’ abundance – see Magurran, 1988). This scenario, however, does not imply that the disturbed kerangas forest could facilitate a recruitment of gingers beyond that of forests of fertile soils. Although some gingers are confined in montane forests (Beaman & Beaman, 1998), the richness of ginger species decreases with increasing altitude (Gobilik & Yusoff, 2005). Hence the low diversity of gingers in this study can be associated with the fact that the study plots (all) were established in upland forest, which is occurring just above the so-called lowland forest, a forest where gingers are usually abundant (Gobilik & Yusoff, 2005). As evidence, none of the species were found in the undisturbed lower montane-kerangas forest plot (1,300 m) or along the trail to the peak of the Gunung Maliat (1,000 – 1,300 m). Moreover, gingers have not yet been reported to inhabit mossy forest (>2,300 m elevation), even on large mountains such as Mt. Kinabalu and Mt. Trus Madi (Gobilik & Yusoff, 2005). Therefore, they are not expected to inhabit upland kerangas forest, which is a mossy forest sensu Fox (1972). In Serudong, mossy forest took event at lower altitude (700 m in this study) due to ‘Massenerhebung effect’, a reduction in the lower altitudinal limits of vegetation zones on isolated hills of infertile soils, a common phenomenon which occurs in south-eastern of Sabah (Fox, 1972). Light and precipitation are the other two factors for the higher density and species richness of gingers in the disturbed forest. This is because many gingers are growing well only in open, wet and humid conditions 20 (Larsen et al., 1999; Poulsen, 2006). In other word, the previous logging activities in the study area had opened the forest canopy and facilitated more light to reach the gingers on the ground, and in Serudong, where the precipitation is relatively high (2,500–3,500 mm), water does not limit their survival even after they were being exposed to heavy sunlight by the logging activities. On the other hand, they generate more energy to reproduce, because they receive enough light, water, and nutrient (from the rotting tree stems and branches) to carry out a productive photosynthesis. In other words, the open canopy, high precipitation, and nutrient from the rotting wood debris left by the logging are at least compensating the adverse effect of kerangas soil on ginger’s recruitment in the study area. The present results also underline the importance of gingers as indicators of forest disturbance. The composition of gingers reflects the disturbance level of the forest very well as one can interpret from the Cluster Analysis’s result. Nevertheless, none of the species are confined in either forest condition. Similar results had also been reported from Tabin Wildlife Reserve (Gobilik, 2002). As a summary, 62% of the species in Serudong are widespread gingers in Sabah, 13% are locally abundant at several districts and 5% are locally rare. Of the remaining 21% nonidentified species, only the species of Geostachys may be confined to this area. In addition, this species could be new species since it is distinct from that was described from Maliau Basin. If so, at the scale of this study, the importance of Serudong as an insitu conservation area for gingers can be highlighted only by the occurrence of this species and the 5% locally rare species of DIVERSITY OF GINGERS AT SERUDONG, SABAH the area. Many more special gingers may, however, be found at this area in the future if intensive inventories were to be carried out. ACKNOWLEDGMENTS I would like to thank the Sabah Biodiversity Centre for funding the expedition to Serudong and also to Dr Axel Poulsen for reviewing the early version of this paper. REFERENCES Beaman, J. H. and R. S. Beaman. 1998. The Plants of Mount Kinabalu: Gymnosperms and Non-orchid Monocotyledons. Kota Kinabalu: Natural History Publications (Borneo). Connell, J. H. 1978. Diversity in tropical rain forest and coral reefs. Science. 199: 1302 – 1310. Fox, J. E. D. 1992. The natural vegetation of Sabah and natural regeneration of the dipterocarp forests. PhD thesis. University of Wales (unpublished). Gobilik, J. 2002. Some aspects of abundance and distribution of Zingiberaceae and Costaceae in Tabin Wildlife Reserve, Sabah. MSc thesis. Universiti Malaysia Sabah, Kota Kinabalu, Sabah (unpublished). Gobilik, J. and M. Yusoff. 2005. 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Diversity, abundance and distribution of ground herbs in primary and selectively logged forest of Danum Valley (North Eastern Borneo). MSc thesis. Universiti Malaysia Sabah, Kota Kinabalu (unpublished). Magurran, A. E. 1998. Ecological diversity and its measurement. Cambridge, London: University Press. McCune, B. and M. J. Mefford. 1999. PCORD®. Multivariate Analysis of Ecological Data. Version 4.14. MjM Software Design, Gleneden Beach, Oregon. USA. 21 Newberry, D. M. 1991. Floristic variation within kerangas (heath) forest: Re-evaluation of data from Sarawak and Brunei. Vegetation. 96: 43 – 86. Poulsen, A. D. 2006. Etlingera of Borneo. Kota Kinabalu: Natural History Publications (Borneo). Sabah Forestry Department. 2005. Sustainable Forest Management Plan for Forest Management Unit Serudung, FMU 25. Sabah Forestry Department, Sandakan, Sabah (unpublished). Slik, J. W. F., R. W. Verburg and P. J. A. Keßler. 2002. Effects of fire and selective logging on the tree species compisition of lowland dipterocarp forest in East Kalimantan, Indonesia. Biodiversity and Conservation. 11: 85 – 98. Thelaide, I. 1998. The genus Zingiber in Thailand and Malaysia: Taxonomy, biology and uses. PhD thesis. University of Aarhus, Denmark (unpublished). JOURNAL OF TROPICAL BIOLOGY AND CONSERVATION, 4 (1) : 23 – 37, 2008 Research Article Biodiversity assesment in a Sarawak lowland dipterocarp rainforest of Niah National Park Faisal Ali ANWARALI KHAN1, 2, Mohamad Faishal BUJANG2, Mohd. Azmin KASSIM2, YAP Sheau Yuh2, Besar KETOL2, Wahap MARNI2, Isa SAIT2, C.J. LAMAN2, Abang Arabi ABG AIMRAN3, Zaidi MAWEK3, Abang Abdul Mutalib ABG TAJUDIN3, Haidar ALI3 and M.T. ABDULLAH2 1 Department of Biological Sciences, Texas Tech University, Lubbock, TX 79409-3131, USA 2 Department of Zoology, Faculty of Resource Science and Technology, Universiti Malaysia Sarawak, 94300 Kota Samarahan, Sarawak, Malaysia 3 Sarawak Forestry Corporation, Level 12, Office Tower, Hock Lee Centre, Jalan Datuk Abang Abdul Rahim, 93450 Kuching, Sarawak, Malaysia ABSTRACT A transect survey was conducted from 2 – 6 December 2004 in Niah National Park to estimate species diversity and relative abundance of birds and mammals. This study was conducted in four forest line transects: Madu Trail (TR1), Sungai Tangap (TR2), Niah Great Cave (TR3), Bukit Kasut (TR4), and one river transect along the Niah River (RT). A total of 521 birds representing 59 species from 23 families were recorded. The Black-Nest Swiftlet (Aerodramus maximus) and the Mossy-Nest Swiftlet (Aerodramus salanganus) were the most common species in the park. The family Timaliidae (babblers), with nine species, was recorded as the most diverse family, whereas Strigidae (owls) and Hirundinidae (swallows) were the least diverse families with one species in each. A total of 29 mammalian individuals representing seven species from four families were recorded. The family Sciuridae (squirrels) with three species was recorded as the most diverse family, whereas Cynocephalidae (flying lemurs) and Muridae (rodents) were the least Keywords: Birds, mammals, Niah National Park, relative abundance, species diversity, transect diverse families with one species and one individual each. TR1 was recorded with the highest Shannon-Weiner index (diversity index) of H’ = 4.75 and H’ = 2.20 for birds and mammals respectively. The lowest bird H’ = 3.73 was recorded for TR2, whereas the lowest mammal H’ = 0 was recorded for TR2 and RT. Although this study does not identify factors that contribute to different species diversity at each transect line, field observations suggest that vegetation and human activities were the major elements that contributed to the observations found at each transect in this study. Studies on the vegetation types and potential disturbances that influence the faunal diversity will provide useful insights in conservation and management planning of this park. INTRODUCTION Extended to an area of only 31.4 km sq (3,140 hectares), Niah National Park is one of Sarawak’s smallest National Parks (Bennett, 1992). Its uniqueness for paleontology studies (e.g., Harrisson, 1958, Piper et al., 2007) and diverse ecology has attracted visitors, naturalists and scientists. The park is located 16 km inland, on 24 TRANSECT SURVEY IN NIAH NATIONAL PARK Figure 1: Map showing the locations of sampling areas in Niah National Park (adapted and modified from Hazebroek & Abang Morshidi 2000). All details and symbols were included inside the map. Transects were shaded with different colours as described in the map. Different colours of land cover refer to different elevations in the park. FAISAL ALI ANWARALI KHAN et. al. the northern region of Sarawak (Hazebroek & Abang Morshidi, 2000). It is about 110 kilometres southwest of Miri and located near the Niah River, approximately 3.8 km from the small town of Batu Niah (Bransbury, 1993; Hazebroek & Abang Morshidi, 2000). Niah cave was first established as a National Historic Monument in 1958, and later as national park on 23 November, 1974. It was officially opened to the public on 1 January, 1975. Niah National Park has been proposed as a World Heritage Site by United Nations (UNESCO) owing to the important fact that it holds prehistoric human civilization remains (from 49,000 years ago) in Niah cave (Hazebroek & Abang Morshidi, 2000). Limestone forest, mixed dipterocarp forest, peat swamp forest and regenerated forest are the main vegetations found in this park (Good, 1991; Anderson, 1996). About 60% to 70% of the park is dominated by Gunung Subis (394 m), which is a large and almost vertical limestone structure (Hazebroek & Abang Morshidi, 2000). In terms of the parks biodiversity, previous studies have documented approximately 190 species of birds, 64 species of mammals, 48 species of snakes and 22 species of frogs (Good, 1991). Niah cave serves as the main habitat for thousands of swiftlets and various species of bats (Medway, 1997). Black-Nest Swiftlets (Aerodramus maximus) and Mossy-Nest Swiftlets (Aerodramus salanganus) are the major occupants of this cave. These swiftlets also contribute as the major source of income for the local people (especially those in the Chang longhouse inside the park; Figure 1) that collect swiftlets nests, which are in demand in the market for medical reasons. Although the park harbours diverse wildlife, no studies have been conducted utilizing transect lines to survey, document, or update the current list of fauna with estimated relative abundance and diversity. This technique works best with diurnal animals and is usually biased towards highly social animals. However, there are also 25 several advantages that have made this method a useful tool to measure species diversity. This includes the ability to provide a broader range of species than the trapping method due to the dependency on trapping method’s limitation that it depends on trap numbers, bait types, position of traps and season (dry or monsoon). Therefore studies using transect surveys are able to provide a quick and reliable estimation of species diversity, especially to monitor the trend of faunal diversity in the park as a result of urbanization or disturbances in the surrounding areas. Past logging operations that began in the 1960s have led to the emergence of town like Batu Niah that further explains the forest fragmentation found around Niah National Park. It is estimated that about 40% of Niah River water catchment areas (land cover areas) were transformed into a palm oil plantations in 2002. Only 22% of the forest catchment area from 1972 still remains in 2005 (Hansen, 2005). It was also noted that the native people from the long-house inside the park have started to cultivate inside the park boundary. Shifting cultivation and poaching were practised by the locals threatened the forest ecosystem, and thereby affecting wildlife (Hansen, 2005). In view of these threats, a study was conducted in five transects to document the species diversity, and relative abundance as an estimate of bird and mammal diversity in Niah National Park. This study also was aimed to facilitate park management by providing a list of fauna sighted along the walkways as a reflection of potential attractions. It is expected that this baseline data can be useful for future monitoring, management planning and conservation of wildlife in this park. MATERIALS AND METHODS Study Area Transect line surveys were carried out at five different transect lines. Four of them were 26 conducted along popular visitors trails: Madu Trail, Sungai Tangap Trail, Great Cave Trail and Bukit Kasut Trail in the forest, whereas the last one was along the Niah River, which flows along the national park boundary. The location and the range of each transect is shown in Figure 1. Field Methodology A transect line survey for data collection of birds and mammals was used without disruption on these faunas, as this involves only observations, rather than direct handling of the animals. The survey was conducted in 1 km distance for each transect line and 3.2 km distance for the river transect as illustrated in Figure 1. The presence of birds and mammals in each area was recorded based on direct and indirect observations. Direct observations were conducted by sighting the animals with binoculars whereas indirect observations were conducted based on the presence of signs such as vocalizations, footprints, faeces, feeding marks on fruits, nests and wallows (Mohd. Nor et al., 1992). Birds and mammals found along transects were identified using identification keys by Smythies (1981, 1998, 1999), Payne et al. (1985), Lekagul & Round (1991), Bond (1993), MacKinnon & Philipps (1993), Gregory-Smith (1995), Davison & Chew (1996), Harris et al. (1996), and Francis (1998). Individual bird and mammal surveys were recorded according to the species identifications. Observations were performed by several small groups that collected the data independently to reduce the double counting. Data was frequently compared between groups to avoid any miscalculation or misidentification. In some cases (mainly swiftlets), average record from all the groups was used as the final observation count. Thus, the data presented herein is the best estimate of faunal diversity. Transects Lines Surveys were conducted at four locations as following: transect line one (TR1), transect line TRANSECT SURVEY IN NIAH NATIONAL PARK two (TR2), transect line three (TR3) and transect line four (TR4). Surveys were conducted by groups of 8 to 10 people equipped with binoculars, field identification keys, and inventory lists. First, transects were measured and marked with coloured plastic-flagging tags at each 25 m interval as the observation point along transects. Survey hours were divided into three sessions: morning (from 0600 hours to 1000 hours), evening (1600 hours to 1800 hours), and at night (1930 hours to 2130 hours) to obtain the best estimation of both nocturnal and diurnal animals in the park. Observers walked at a speed of approximately 500 metres per hour and stopped for one minute at each 25 metre mark to observe and listen for any movement, calls, or signs of animals. This was repeated for five days at four different transects simultaneously by five different groups (including those in river transect). Each group was shuffled between transects to randomize observers and reduce observation errors. This method was useful to document diversity for a large area in a short time, as the length of the survey relies mainly on funding and manpower availabilty. River Transect Surveys along the Niah River were conducted by boat from Pangkalan Lobang dock to Bukit Kasut dock in a distance of about 3.2 km. The survey was conducted between 0630 hours to 0700 hours, 1200 hours to 1230 hours, and 1600 hours to 1635 hours. Boat speed was set at approximately 7.1 km per hour. The boat engine will be off to listen to the animals sound. Other surveys methods follow the description in transect line methods above. Data Analysis Observation counts in the transect line study were used to calculate the relative abundance of each species. Species diversity indices were calculated for birds and mammals for each line transect. The Shannon-Wiener Index and Evenness were calculated using the DIVERS FAISAL ALI ANWARALI KHAN et. al. program (Krebs, 1989), which has been modified (methods for data entry and retrieval has been changed) for ease of data input and output (Laman, 2001). Lastly, the diversity indices between transects were statistically compared using pairwise diversity comparisons following t-test method from Zar (1996). RESULTS Bird Species Diversity and Abundance A total of 521 individuals of birds representing 59 species from 23 families were recorded (see Table 1). The family Timaliidae was recorded as the most diverse family with nine species, followed by Cuculidae with six species, and both Nectariniidae and Pycnonotidae with five species. According to Sarawak's legislation (1998), a total of 15 species from eight families are under Part I and Part II Wildlife Protection Ordinance 1998, which are protected in Sarawak. This study has recorded one species, Anthracoceros malayanus (family Bucerotidae; Black Hornbill) that is listed under Part I (Totally Protected Animals) as well as Egretta garzetta (family Ardeidae; Little Egret), Loriculus galgalus (family Psittacidae; Blue-crowned Hanging Parrot), Ninox scutulata (family Strigidae; Brown Hawk-owl), Copsychus malabaricus (family Turdidae; White-rumped Shama), all species of swiftlets (family Apodidae), all species of kingfishers (family Alcedinidae), and all species of woodpeckers (family Picidae) that are listed in Part II (Protected Animals) of Wildlife Protection Ordinance 1998. The avifauna of the park was dominated by the Black-Nest Swiftlet (Aerodramus maximus) with the highest relative abundance at each transect and was followed by Mossy-Nest Swiftlet (Aerodramus salanganus). The family Apodidae recorded the highest relative abundance with 32.1% (or 167 out of 521 individuals). Generally all birds, except for owls, are active during the day. The only nocturnal avian species observed was the Brown Hawk Owl. 27 Table 2 shows the Shannon-Weiner Index for diversity analysis of each transect. Species diversity index was highest at TR1 (4.75), followed by RT (4.26), TR4 (4.07), TR3 (4.03), and finally TR2 (3.73). Zar’s t-test calculation at a = 0.05 indicates that there were significant differences in diversity indices between TR1 vs. TR2, TR1 vs. TR3, and TR1 vs. TR4. In contrast, the result indicates that there were no significant differences between TR2 vs. TR3, TR2 vs. TR4, and TR3 vs. TR4. The analysis did not include the comparison with the river transect as the observations for the river transect were set at 3.2 km whereas the rest of transects were calculated for 1 km range. Mammal Species Diversity and Abundance A total of 29 individuals of mammals representing seven species from four families were recorded (see Table 3). The mammals were recorded using observation and vocalization techniques for the following families: Cynocephalidae, Cercopithecidae, Sciuridae and Muridae. Following Sarawak's legislation (1998), only flying lemurs (family Cynocephalidae) were included in Part II of Wildlife Protection Ordinance. Only the Plaintain Squirrel (Callosciurus notatus) and Prevost’s Squirrel (Callosciurus prevostii) from the family Sciuridae were recorded at RT (two individuals) and TR2 (one individual) respectively. Although this suggests a 100% relative abundance at each transect, they were represented by less than two individuals that may provide a biased estimation of the overall mammals in those transects. Highest relative abundance was followed by the Pig-Tailed Macaque (Macaca nemestrina) and the Plain Pigmy Squirrel (Exilisciurus exilis), with both at 22.2% for TR1 and TR3 respectively. In general, the highest relative abundance for mammals was dominated by the family Sciuridae with 65.5% (19 out of 29 individuals). Table 4 shows the Shannon-Weiner Index for the diversity analysis of each transect. Species’ Family Species and Common Name Total Ardeidae Accipitridae Rallidae Psittacidae Cuculidae Strigidae Apodidae Alcedinidae Picidae Eurylaimidae Hirundinidae Aegithinidae 3 2 12 5 3 6 11 3 1 19 1 103 64 1 1 5 2 16 2 3 5 20 1 2 10 1 2 6 3 Transect 2 3 4 RT Relative Abundance (%) TR1 TR2 TR3 TR4 3 1 1 3 1 5 1 4 1 1 2 2 2 13 10 32 17 3 1 23 17 2 4 3 1 7 1 2 2 9 2 1 8 4 2 5 2 4 1 7 6.0 0.9 0.9 2.8 7 2 2 2 0.9 4.6 2 1 5 29 6 16 4 1 1 3 2 0.9 3.5 0.9 0.9 1.7 1.8 1.7 11.9 9.2 27.8 14.8 2.6 0.9 1 1 5.2 1.8 1.8 1.8 2.7 0.9 20.4 15.0 1.5 3.0 0.8 5.2 21.6 11.9 1.8 3.7 1 5 6.4 0.9 1.8 1.8 8.0 1.8 0.9 7.0 3.5 1.7 4.4 2 1 1 4 4.0 2.0 10.0 12.0 8.0 2.0 2.0 6.0 4.0 0.8 3.7 2.0 0.8 1 2 1 RT 2.0 4.0 0.9 1.7 0.9 0.9 3.0 TRANSECT SURVEY IN NIAH NATIONAL PARK Bucerotidae Megalaimidae Egretta garzetta (Little Egret) Spilornis cheela (Crested Serpent-eagle) Amaurornis phoenicurus (White-breasted Waterhen) Loriculus galgalus (Blue-crowned Hanging Parrot) Cuculus micropterus (Indian Cuckoo) Cacomantis merulinus (Plaintive Cuckoo) Surniculus lugubris (Drongo Cuckoo) Phaenicophaeus chlorophaeus (Raffles’s Malkoha) Phaenicophaeus sumatranus (Chestnut-bellied Malkoha) Centropus sinensis (Greater Coucal) Ninox scutulata (Brown Hawk-owl) Aerodramus maximus (Black-nest Swiftlet) Aerodramus salanganus (Mossy-nest Swiftlet) Actenoides concretus (Rufous-collared Kingfisher) Todirhamphus chloris (White-collared Kingfisher) Halcyon capensis (Stork-billed Kingfisher) Alcedo atthis (Common Kingfisher) Ceyx rufidorsus (Rufous-backed Kingfisher) Anthracoceros malayanus (Black Hornbill) Megalaima rafflesii (Red-crowned Barbet) Megalaima mystacophanos (Red-throated Barbet) Megalaima australis (Little Barbet) Sasia abnormis (Rufous Piculet) Picus puniceus (Crimson-winged Woodpecker) Eurylaimus ochromalus (Black-and-yellow Broadbill) Hirundo tahitica (Pacific Swallow) Aegithina tiphia (Common Iora) Chloropsis cyanopogon (Lesser Green Leafbird) Chloropsis cochinchinensis (Blue-winged Leafbird) 1 28 Table 1: Composition and relative abundance of avifauna recorded in Niah National Park. Total individuals captured and their associated relative abundance are showed according to transect lines (TR = Transect and RT = River Transect) Species and Common Name Total Pycnonotidae Turdidae Timaliidae Sylviidae Muscicapidae Dicaeidae Nectariniidae Sturnidae Dicruridae Pycnonotus goiavier (Yellow-vented Bulbul) Pycnonotus plumosus (Olive-winged Bulbul) Pycnonotus brunneus (Red-eyed Bulbul) Alophoixus bres (Grey-cheeked Bulbul) Alophoixus phaeocephalus (Yellow-bellied Bulbul) Trichixes pyrropyga (Rufous-tailed Shama) Copsychus saularis (Magpie Robin) Copsychus malabaricus (White-rumped Shama) Trichastoma rostratum (White-chested Babbler) Malacocincla malaccensis (Short-tailed Babbler) Malacopteron magnum (Rufous-crowned Babbler) Malacopteron cinereum (Scaly-crowned Babbler) Malacopteron magnirostre (Moustached Babbler) Napothera atrigularis (Black-throated Wren Babbler) Macronous gularis (Striped Tit Babbler) Macronous ptilosus (Fluffy-backed Tit Babbler) Stachyris erythroptera (Chestnut-winged Babbler) Orthotomus sericeus (Rufous-tailed Tailorbird) Rhipidura perlata (Spotted Fantail) Prionochilus maculatus (Yellow-breasted Flowerpecker) Dicaeum trigonostigma (Orange-bellied Flowerpecker) Anthreptes malacensis (Brown-throated Sunbird) Hypogramma hypogrammicum (Purple-naped Sunbird) Nectarinia jugularis (Olive-backed Sunbird) Arachnothera longirostra (Little Spiderhunter) Arachnothera robusta (Long-billed Spiderhunter) Aplonis panayensis (Asian Glossy Starling) Acridotheres tristis (Common Myna) Cracula religiosa (Hill Myna) Dicrurus paradiseus (Greater Racket-tailed Drongo) 4 4 12 1 2 1 6 12 11 1 5 1 3 4 3 1 20 27 4 26 1 7 3 7 19 6 3 2 2 10 Total number of individuals Total number of families Total number of species 521 23 59 1 Transect 2 3 4 RT TR1 Relative Abundance (%) TR2 TR3 TR4 RT 4 2 1 2 1 2 1 1 5 1 4 1 4 5 1 3 3 2 1 2 2 4 3 1 8.0 1.8 0.9 1.8 0.9 2 2 1.8 0.9 0.9 4.6 0.9 3 2 1 1 2 6 4 5 7 7 4 6 7 8 4 7 1 5 9 1 1 2 0.9 3.5 4.4 2.2 1.5 0.9 1.8 1.5 3.0 2.2 2.0 4.0 4.0 2.6 2 2 2 4 6 3.5 0.9 2.7 FAISAL ALI ANWARALI KHAN et. al. Family 4 5 2 7 1 1 1 1 1.8 0.9 0.9 1.8 5.5 3.7 4.6 1.5 1.5 6.1 6.1 3.5 5.3 5.2 6.0 3.5 6.2 0.9 4.4 6.7 0.8 0.8 1.7 3.5 4.4 1.5 5.2 1.8 3.7 5.5 3 2 1 3 2 1 1 109 19 37 115 113 134 5 0 15 17 13 13 23 26 26 4 2.0 2.0 2.0 2.0 6.0 4.0 0.9 2.8 1.7 0.9 0.9 3.0 23 29 30 TRANSECT SURVEY IN NIAH NATIONAL PARK Table 2: Shannon - Weiner Index and evenness of avifauna (above), and comparison of diversity indices between two transects using the Zar t-test (below). The Zar t-test is calculated by comparing each transect line with other transect lines studied here. The river transect was not included for the Zar t-test, as explained in the results section (TR = Transect; RT = River Transect; α = 0.05) TR 1 TR2 TR3 TR4 RT Number of individuals Number of families Number of species Shannon-Weiner Index (H’) Evenness 109 19 37 4.75 0.04 115 15 23 3.73 0.12 113 17 26 4.03 0.09 134 13 26 4.07 0.08 50 13 23 4.26 0.04 Transect t-calculated t-critical Significant/Not significant Transect 1 vs. Transect 2 Transect 1 vs. Transect 3 Transect 1 vs. Transect 4 Transect 2 vs. Transect 3 Transect 2 vs. Transect 4 Transect 3 vs. Transect 4 22.07 17.10 17.56 – 5.19 – 5.28 – 0.74 1.96 1.96 1.96 1.96 1.96 1.96 diversity index was highest at TR1 (2.20) followed by TR3 (1.84), and TR4 (1.75). However, the result of the diversity index for mammals at TR2 and RT was zero. This is due to the small number of individuals at both line transects. The Zar t-test calculations at α = 0.05 showed that there was a significant difference between the diversity indices of TR1 vs. TR3, and TR1 vs. TR4. In contrast, results showed that there was no significant difference between TR3 vs. TR4. DISCUSSION Bird Species Diversity and Abundance Results from this study showed that the avian family Apodidae had the highest relative abundance. This was probably due to high spotting chances compared to other animals, as they fly in a range and become detectable to the naked eye. The occurrence of limestone caves also explains this observation. Both the Black-Nest Swiftlet (A. maximus) and the Significant Significant Significant Not significant Not significant Not significant Mossy-Nest Swiftlet (A. salanganus) were recorded with the highest relative abundance at all transects. According to Rahman & Abdullah (2002), abundance of swiftlets is influenced by the presence of caves and cliffs that serves as their major roosting site. Hazebroek & Abang Morshidi (2000) also reported that the Niah Great Cave is one of the largest limestone caves in Sarawak, with a high number of fauna occupying this habitat. In this cave, swiftlets were estimated to reach a total of 150,000 individuals. Three swiftlet species were found in the park: Black-Nest, Mossy-Nest and White-Bellied Swiftlets. Of these, Black-Nest Swiftlets are the most common found in Borneo and form the main population in the park (Hazebroek & Abang Morshidi, 2000). During this survey, most of the swiftlets were recorded in the morning and evening owing to the fact that they hunt and feed during the daytime. Swiftlets were observed on a regular day leaving their roosting cave as early as 0600 hours and returning as early as 1600 hours (also see Medway, 1997; Lim & Cranbrook, 2002). Family Species Total Cynocephalidae Cercopithecidae Sciuridae Muridae 1 Transect 2 3 Cynocephalus variegatus (Flying Lemur) Macaca fascicularis (Long-tailed Macaque) Macaca nemestrina (Pig-tailed Macaque) Callosciurus prevostii (Prevost’s Squirrel) Callosciurus notatus (Plantain Squirrel) Exilisciurus exilis (Plain Pigmy Squirrel) Sundamys muelleri (Muller’s Rat) 1 2 1 6 13 5 1 1 3 2 1 1 Total number of individuals Total number of families Total number of species 29 4 7 9 3 5 1 1 1 4 RT Relative Abundance (%) TR1 TR2 TR3 TR4 1 RT 12.5 2 22.2 1 2 4 2 2 4 1 2 9 2 4 8 2 4 2 1 1 11.1 33.3 22.2 11.1 100.0 11.1 22.2 44.4 22.2 25.0 50.0 12.5 FAISAL ALI ANWARALI KHAN et. al. Table 3: Composition and relative abundance of mammals recorded in Niah National Park. Total individuals captured and their associated relative abundance are showed according to transect lines (TR = Transect; RT = River Transect) 100. 0 31 32 TRANSECT SURVEY IN NIAH NATIONAL PARK Table 4. Shannon - Weiner Index and evenness of mammals (above), and comparison of diversity indices between two transects using the Zar t-test (below). The Zar t-test was calculated by comparing each transect line with other transect lines studied here. The river transect was not included for the Zar t-test, as explained in the results section (TR = Transect; RT = River Transect; t-critical is at 1.96 at α = 0.05) TR1 TR2 TR3 TR4 RT Number of individuals Number of families Number of species Shannon-Weiner Index (H’) Evenness 9 3 5 2.20 0.16 1 1 1 0.00 0.00 9 2 4 1.84 0.27 8 2 4 1.75 0.30 2 1 1 0.00 Infinite Transect t-calculated t-critical Transect 1 vs. Transect 2 Transect 1 vs. Transect 3 Transect 1 vs. Transect 4 Transect 2 vs. Transect 3 Transect 2 vs. Transect 4 Transect 3 vs. Transect 4 4.06 4.48 0.87 2.57 2.57 2.78 Previous study by Rahman et al. (2004) at Fairy Cave and Wind Cave Bau, have also recorded Mossy-Nest Swiftlet with highest relative abundance: 18.2% (14 individuals). Similarly, Hassin (2004) also indicated that Mossy-Nest Swiftlet was the dominant species in Bau limestone forest with relative abundance of 25.74% (or 26 out of 101 individuals) when using mist-net techniques. Although the current study has reported lower swiftlet abundance compared to those in Bau limestone forests, it indicates nothing more than the difference in techniques used and number of species recorded in each study rather than the diversity of the site. Our study in Niah National park has recorded more than 500 individual of birds compared to those at Bau (Hassin, 2004) which recorded only 101 individuals through trapping techniques. This also indicates that the transect survey is able to cover a broader range of bird species in comparison to trapping techniques that depend on trap efficiency and positioning. Significant/Not significant No comparison Significant Significant No comparison No comparison Not significant Babblers from the family Timaliidae were recorded with the highest number of species. This family was easily identified in the field compared to other families through their conspicuous calls. These species forage at both forest floor and under canopy (Strange & Jeyarajasingam, 1993). They feed on various types of food such as insects, larvae, and worms, and inhabit primary and secondary lowland forest. In Peninsular Malaysia, babblers alone contribute up to 25% of forest community species richness (Madoc, 1992). Cuckoo species from the family Cuculidae were recorded with the second highest number of species. These species were found mainly in open areas and river habitats. Sunbirds and spiderhunters of the family Nectariniidae were recorded with the third highest number of species. These birds were recorded in various types of habitats such as primary forest, secondary forest, gardens, plantations and peat swamp forest. These habitats provide this group of birds with a large FAISAL ALI ANWARALI KHAN et. al. range of food sources, microhabitats, and protection from predators. TR1 was recorded with the highest diversity index followed by TR4. Both areas were categorized as less disturbed, and this may be the reason for their high species diversity. Generally, not many visitors or local commuters pass by this area. TR4 was not open to the public during this study. TR1 consisted of secondary forest, with patches of mixed dipterocarp forest. This type of forest provides variety of food sources such as seeds, fruits, small mammals, insects and larvae. Conversely, TR4 is situated in an area covered by secondary lowland forest, but surrounded by primary forest. This area is less disturbed and appropriate as foraging areas for birds. This study has recorded TR1 (4.75) and TR2 (3.73) diversity indices higher than those by Kon et al. (2004) which used mist-nets at similar transects (TR1 = 3.1 and TR2 = 3.15). Generally, the advantage of a wildlife survey compared to the mist-nets method is the ability to cover a larger sampling area, in both horizontal and vertical space. Transect surveys also enable the observer to cover all forest levels from above canopy, canopy, middle canopy, under canopy and forest floor levels with the aid of binoculars and animal calls. The mistnetting technique is more passive, selective, and is usually designed for capturing avifauna under canopy. Trapping techniques also depend on net position across flyway direction. This will influence the capture rate of the study. The transect survey technique is more general for broader coverage of species diversity. A previous study by Rahman et al. (2004) at Bau limestone forest indicated that less disturbed areas have H’ = 1.03, whereas disturbed areas have H’ = 1.30. In comparison to our study, birds at Niah National Park were more diverse than those from Bau limestone forest. This was mainly due to the differences in level of disturbance, availability of food resources and forest vegetation in both study sites. Results from this study also indicated that 33 the evenness index for all line transects were below 0.50. Low evenness index suggests that the number of individuals from each species were significantly different from each other in this study. This was mainly due to the large gap between high swiftlet count and any other species in this study which recorded observation rates of less than half that of the the swiftlet count. Bird diversity indices showed significant differences in the following transect comparisons: TR1 vs. TR2, TR1 vs. TR3 and TR1 vs. TR4. This may be due to the differences in vegetation types and levels of disturbance at these transects. Secondary forest, with patches of primary mixed dipterocarp forest dominated the TR1 area. Vegetations in primary forest and lowland mixed dipterocarp forest provide a greater variety of fruit compared to those in secondary forests (Smythies & Davison, 1999). Fruits are an important source of food for the majority of bird species. Fewer visitors and reduced local activities, along with food source availability in TR1 were the major factors that resulted in significant differences between these transects. TR2 and TR4 were dominated by secondary forest, whereas TR3 was mainly dominated by limestone vegetation, which is known for lower biodiversity than any other forest types in Borneo (MacKinnon & Phillipps, 1993). Seasonal swamp forest that emerged during the rainy season also may have reduced foraging activities by the birds in TR2 areas throughout this study period. In contrast, results do not show any significant difference in the following diversity indices comparisons; TR2 vs. TR3 and TR2 vs. TR4. Both, TR2 and TR3 can be categorized as disturbed areas, as there was a great amount of human activity, especially due to visitors and local sounds (e.g., walking, talking) that may have reduced bird activity around these areas. Both of these trails are popular trails that lead to the Niah Great Cave and the Long House inside the park. Both of these transects faced 34 similar problems, as they were adjacent to each other in this study. Although fewer visitors and human activities were observed at TR4 than at TR2 and TR3, statistical analysis indicates that there were no significant differences between TR2 vs. TR4 and TR3 vs. TR4. This may be due to the similarity in secondary forest vegetation found in both TR2 and TR4 that subsequently supported similar bird species composition at both of the transects. Although both TR3 and TR4 were observed with different vegetation types and levels of disturbance, and both were situated at a distance from each other, statistical analysis showed no significant difference between TR3 vs. TR4. However, after considering the park boundary, we found that TR4 was adjacent to the cultivated lands and logging camps, whereas TR3 was situated near limestone forest. These separate habitats may have resulted in a similar level of ecology and diversity constraint at both transects that could not be differentiated in statistical analyses. Mammal Species Diversity and Abundance Exilisciurus exilis and C. notatus from the family Sciuridae were common throughout the study. Results indicate that both species were recorded with the highest density and relative abundance. Squirrels are the small mammals that visitors most often encountered in Niah National Park (Hazebroek & Abang Morshidi, 2000). The availability of food sources, such as fruits, seeds, leaves, and other smaller animals might sustain their high population. Sciuridae can also adapt to various types of forest vegetation and is able to partition the space in trees within other species in the family. Plain Pigmy Squirrels (E. exilis) often forage on tree trunks, Plaintain Squirrels (C. notatus) forage on branches and on the ground, whereas Prevost’s Squirrels (C. prevostii) forage in the canopies of high and big tree branches. Fungi that were found in all vegetation types on tree trunks, branches, twigs, left litter, soil and dead plant materials also serve TRANSECT SURVEY IN NIAH NATIONAL PARK as the major source of food for this family (Hazebroek & Abang Morshidi, 2000). Figs, especially Ficus benjamina were identified as an important food resource for all frugivorous animals in the park. This plant can be regarded as the ‘keystone’ species that promotes the diversification of other fauna in the park (sensu Marduka 2001). The Long-Tailed Macaque and the Pig-Tailed Macaque were the only large mammals recorded and representative throughout the study. Most of the large mammals were shy and they usually hide when encountered with humans. Seasonal effect during monsoon season (e.g., seasonal swamp: Karim et al., 2004) and short study period may have influenced the low number of large mammals recorded in this study. Apart from this, hunting pressure by the locals also may have contributed to the reduction of large mammals recorded in the park (Mohd. Nor et al., 1992). Only one individual of Prevost’s Squirrel was recorded at TR2 and two individuals of Plantain Squirrel were recorded at RT in this study. This may be due to the condition of the area which can be categorized as disturbed, with high frequency of visitors and local activity along the transect. The seasonal swamp at TR2 also might have reduced the foraging range of any ground dwelling animal, especially the small mammals in this area. TR1 had the highest diversity index as recorded in birds. Lowland dipterocarp forest was the main factor that contributed to the richness of mammals’ community in the park as it provided optimal food resources for diverse groups of animals (Hazebroek & Abang Morshidi, 2000; Karim et al., 2004). TR2 and RT were recorded with 0.0 diversity index with only one species in both of the survey sites (refer Ludwig & Reynolds, 1988). Previous study by Karim et al. (2004) at Bau limestone area using trapping methods indicated that a total of 42 species from 17 families were recorded. Both Muridae and Sciuridae dominated that area with Muller’s Rat FAISAL ALI ANWARALI KHAN et. al. (Sundamys muelleri) as the most common species there. However current study only recorded 29 individuals representing seven species and four families in Niah National Park. A study by Nyaun et al. (2004) using trapping techniques (cage traps) at Madu Trail showed a higher value of diversity indices compared to those of similar sites in the study. This is mainly due to the baits that were used in traps that made it possible to attract shy animals into the traps. Hence, the probability of documenting small mammals (mostly shy) is higher using traps compared to direct observation, which depends on skill and chance of sighting mammals in the dense tropical rainforest. Therefore, differences in survey method may contribute to the variation between trapping and observation techniques, as traps were found more efficient in documenting, both volant and non-volant small mammals. Previous studies, using traps (e.g., mist-nets, harp traps, cage traps, camera traps) have documented new geographic records for the park and Sarawak (e.g., Hall et al., 2002; Abdullah 2003; Azlan & Sharma, 2006; Jayaraj et al., 2006; Anwarali et al., 2007). A study at Tanjung Berlipat, Niah National Park (north to our study site), was recorded with a total of 35 species from 16 families of mammals. Tanjung Berlipat was reported to have less disturbed vegetation and reduced number of visitors. However, the small mammal species account compiled by the Niah National Park Management for Tanjung Berlipat does not provide details on the field methods and sampling effort used. This may represent a compilation of all other previous surveys performed in the park. An analysis on small mammal diversity showed that there are significant differences between TR1 vs. TR3 and TR1 vs. TR4 diversity indices. This correlates with different forest vegetation and levels of human disturbance found at each transect. The level of disturbance was significant at TR4, as this transect is situated 35 opposite Batu Niah town and exposed to vehicle sounds and boat engines along the nearby river. This may be the major factor that influences the mammals’ species compositions in this area. CONCLUSIONS AND RECOMMENDATIONS Species diversity is a simple measure of community stability and persistence of the ecosystem in the face of disturbances (Hamilton, 2005). The transect line is a useful tool for rapid assessment of the diversity of birds and mammals in a tropical rainforest. However, this method is limited due to the behaviour of the animals, experience of the observer, and visibility of the target taxa in the dense tropical lowland forest. Increased survey period with more replicates to take account of seasonal and habitat differences will provide better estimates of the faunal diversity. This is also important to ensure the consistency of data in providing the best interpretation of diversity, density, and relative abundance of the studied faunas at a particular site. Wildlife surveys also require special skills to enable the observer to identify the birds and mammals from a distance, and possibly from their calls and footprints. The faunal lists compiled in this transect survey can be improved by including trapping techniques that would enable the researcher to overcome some of the disabilities in transect surveys. The amount of line transects can be increased, so that at least 10% of the study is covered to provide a better estimation of diversity. The study should also be conducted away from the park walkways to reduce disturbance on the animals by park visitors when observations are conducted. As this survey was done during monsoon season, seasonal swamp might have influenced animals activity, especially ground dwelling mammals. Therefore, surveys during dry or fruiting season might increase the number of animals observed. 36 ACKNOWLEDGEMENTS We are particularly grateful to Miss Nafisah Tahir and Sabrina Reduan for volunteering in this wildlife survey. We thank Peter A. Larsen, John R. Middleton, Sergio Solari and anonymous JTBC reviewers for constructive comments on the previous draft. We also thank Mary Belden and Nur Qasdina Jeeta Abdullah for proofreading this manuscript. We thank the Sarawak Forestry Corporation (SFC) for permission to conduct wildlife research in Niah National Park, Sarawak. We thank Niah National Park management for providing accommodation and other logistic facilities for our study group during the field expedition. This study would not have been possible if not for the collecting efforts by members of the Zoology Department. FAAK was supported through the length of his study at Texas Tech University with Dr Robert J. Baker by the Higher Education Ministry of Malaysia and UNIMAS. 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Long1 and OTHMAN Haji Ross2 1 Department of Aquatic Science, Faculty of Resource Science and Technology, Universiti Malaysia Sarawak, 94300 Kota Samarahan, Sarawak, Malaysia E-mail: lshabdin@frst.unimas.my 2 School of Environmental and Natural Resources Sciences, Faculty of Science and Technology, Universiti Kebangsaan Malaysia, 43600 UKM Bangi, Selangor, Malaysia ABSTRACT The aim of this study is to determine the horizontal distribution of nematodes species density, species diversity and feeding types on the intertidal area of Lok Kawi beach, Sabah, Malaysia. The approach taken was to sample the nematodes and measured selected parameters of the hole water from high-water to low-water marks. The results show that the nematode feeding type non selective deposit feeders (1B) and epigrowth feeders (2A) groups, species diversity, evenness, species richness and species number increased towards the low tide level. The height of the beach did not clearly show their influence on the horizontal distribution of the nematodes. Pearson correlation coefficient shows that there is a significant correlation (R = 0.64, p < 0.05) between the height of the beach and the species diversity of the nematodes. However, the cluster and factor analysis of the stations did not show clearly about the influence of height of the beach on nematodes densities. Therefore, we conclude that there were no definite and universal causative factors, which controlled the horizontal distribution of nematodes species diversity in the intertidal Keywords: Water parameters, density, diversity, feeding types sandy and muddy habitats of the Lok Kawi beach, Sabah. INTRODUCTION Previous studies on horizontal distribution of nematodes have been carried out along salinity gradients in estuaries (Warwick, 1971), across intertidal sandy habitats (Blome,1983) and with increasing water depth both onto the continental shelf and into the deep sea (Tietjen,1976). Most of the studies were carried out in the temperate countries. Several species groups have been suggested across the sandy intertidal habitats. Firstly, species often restricted to certain zones namely sublittoral fringe guild, secondly, eurytopic species (usually with their distribution centred on the lower shore) and thirdly, species confined to the upper shore (Coull, 1988). Four strata of meiofauna distribution was proposed during low tide on sandy beaches (McLachlan, 1980); namely, (1) a dry sand stratum – near the top of the beach where the upper sand layers are >50% desiccated; (2) a moist sand stratum, which underlies the dry sand stratum and extends seaward. It reaches until the depth of the permanent water table; desiccation is < 50% and oxygen levels are high (>70 % saturation); (3) Water table stratum crossing the beach and 40 lying underneath strata 1 and 2. The sand is always moist and oxygen saturation is 40 to 70%; (4) a low oxygen stratum underneath stratum 3, which may be very deep in high energy beaches, where oxygen tension is < 30% saturated. This pattern can be modified by a variety of factors such as a change in wave action or sediment grain size, change in beach slope, freshwater seepage, tidal amplitude, temperature as it affects desiccation (McLachlan, 1980). Other authors have reported similar patterns from other areas of the world but they use different kind of controlling factors (Pollock & Hummon, 1971). Studies on horizontal distribution of nematode’s community on the intertidal area of Sabah are still limited (Shabdin & Othman, 1999; Shabdin & Othman, 2000; Shabdin & Othman, 2005). Moreover, studies on the ecology of Malaysian freeliving nematodes (to date, have generally) are limited to the higher major taxa (Sasekumar,1994) with the exception for study carried out in Merbok mangrove, Kedah (Somerfield et al.,1998). However, the Merbok mangrove study only examined the community level of nematodes at High Water Neap (HWN) and High Water Spring (HWS). The question of how the distribution of species diversity of freeliving nematodes from high water to low water on the intertidal area of monsoonalmaritime-tropical country like Sabah, Malaysia is still unclear. Therefore the objectives of the present study are; (i) to examine the nematode community structure from Mean High Water Neap (MHWN) to Mean Low Water Neap (MLWN), (ii) to determine the relationship between nematode species diversity, horizontal distribution and physico-chemical parameters of the water in Lok Kawi beach, Kota Kinabalu, Sabah, Malaysia. HORIZONTAL DISTRIBUTION OF INTERTIDAL NEMATODE METHODOLOGY Study Area The general climate of Sabah west coast is monsoonal-maritime-tropical, i.e. generally hot and humid with very heavy rainfall. Seasonal variations in climate and weather are not equated with temperature, as it is relatively high and constant, but due to variations in moisture associated with the northeast and southwest monsoons. The onset and retreat of the monsoons generally follow the same temporal pattern but variations from year to year are not uncommon. The monsoons also vary in strength and constancy from year to year. The northeast monsoon is generally from December and February or early March and southwest monsoon is from late June to early November. There are also successive inter-monsoons from April to May (Meteorological Department Sabah, 1993). Lok Kawi beach was chosen in the present study because of its accessibility from Kota Kinabalu city which is about 6 km to the south. It is located at 5° 52’ N and 116° 2’ E. Two habitats, sandy and muddy substratum existed together and thus it would be logistically easier to carry out sampling process. The beach lies in a southwest to north direction and stretching approximately 4.5 km along the Lok Kawi coastline parallel to the Putatan road. The beach extends about 0.6 km out into the shallow foreshore water of the Lok Kawi coast during low tide (Fig. 1). The northeast of the Lok Kawi beach consists of muddy area. The area is sheltered due to the presence of sandbar in front of it. Scattered patches of the seagrass beds (Enhalus sp.) have been found in the area. The southern part of the muddy area is the sand flats. Small isolated patches of coral reefs mostly covered by patches of dead coral rubbles and sand can be seen at the western part of the beach. SHABDIN MOHD. LONG & OTHMAN HAJI ROSS 41 PHILIPPINES Mangroves Coral remains Quadrat Casuarina Figure 1: Map shows the location of sampling stations at Lok Kawi beach (T1 to T4 – Transect) 42 Meiofauna Sampling and Physico-chemical Parameters Measurement Sampling was carried out on May 1992. Four transects perpendicular to the coastline were set up on the beach during low tide at Lok Kawi beach (Fig. 1). Transect 1 (T1) was in the muddy area (mangrove) while transects 2 (T2), 3 (T3) and 4 (T4) were located on the sandflats. Five quadrats running from Mean High Water Neap (MHWN) to Mean Low Water Neap (MLWN) were located along the transect generally at height intervals of 0.95 metres measured using a standard surveying technique (Moore,1979). One of these stations was then levelled to the nearest standard Chart Datum point, which in every case was a tide gauge. Height of stations relative to Chart Datum and the tidal constant were calculated from data derived from the local chart and by courtesy of the Marine Department of Kota Kinabalu, Sabah. Preliminary meiofauna survey on the Lok Kawi beach shows that the vertical distribution of meiofauna was up to 30 cm depth. In order to minimize sampling error from spatial heterogeneity in species composition and abundance, a subsampling strategy was adopted. At each quadrat, eight 30 cm sediment cores were collected over an area 0.25 metre2 on the beach using the 7.01 cm2 transparent tube. The sediment from these cores were put into separate labelled plastic bags and preserved in 5% neutralized seawater formalin. Variance to mean ratios of faunal counts of the first eight random samples taken at the first sampling was not significant at the 5% level (F test). Hence the samples were homogenous and all samples at each tide level and then subsequent ones were drawn from the same parent population. In the laboratory, meiofauna was extracted from the substrate either by sieving or combination of sieving and centrifuging techniques. HORIZONTAL DISTRIBUTION OF INTERTIDAL NEMATODE Meiofauna samples from sandy habitat were extracted using the sieving method only while samples from muddy habitat were extracted by a combination of sieving and centrifuging techniques (Shabdin, 1985). The materials retained on the 32 µm sieve then washed into 100 ml specimen bottles. Then the eight cores of extracted sediments (meiofauna in the eight specimen bottles) were pooled together into 1 litre measuring cylinder and made up to 1 litre with freshwater to be subsampled. A simple device used for subsampling is called ‘meiofauna subsampler’ (Moore et al., 1987). One subsample of 50 ml will generally yield sufficient nematodes for analysis although several subsamples were taken in case of low density. The subsamples were allowed to pass through a 32 µm sieve and rinsed with freshwater to remove salt. The material retained on the 32 µm sieve (sample from sandy habitat) was made concentrated by washing it to the edge of the sieve and then washed it with water from the wash bottle into a grid Petri dish. The subsampled specimens of the nematodes then were scattered in a grid Petri dish. Next, the total number of nematodes in the grid Petri dish was counted under a SV5 Zeiss stereomicroscope. The numbers of organisms were finally converted to densities in units of individuals/10 cm square. Using a fine end of pipette blocked with cotton wool at the other end and the mouth piece, all the nematodes were sucked and transferred to a glass cavity block containing 5% glycerine: 5% pure ethanol: 90% freshwater by volume and left in desiccator for a few days (Platt & Warwick,1983). This would allow the ethanol and water to evaporate slowly leaving the nematodes in pure glycerine. Finally, the nematodes were transferred to a fresh drop of anhydrous glycerine (phenol added) on a slide and a cover slip added, supported by several small glass blocks at both ends. Glyceel was used as a sealant. The nematodes were identified to the species level under a compound microscope. Illustrations of each nematode SHABDIN MOHD. LONG & OTHMAN HAJI ROSS species were made using a camera lucida and identifications were performed using the key by Platt & Warwick (1983, 1988) and verified by various keys in the literatures. Environmental parameters of the pore water such as temperature, salinity, dissolved oxygen and pH value were measured in situ at each quadrate using Hydrolab Environmental Data System (model SVR-2 – Susonde Unit). For every quadrat, one core of sediment up to 30 cm depth was taken for particle size analysis. A piston-style corer, marked with permanent marker at every 1 cm was used to sample three cores of sediment for chlorophyll a analysis. The sediment for chlorophyll a and phaeopigments analyses were put into the cooler box and brought back to the laboratory for further analysis. The standard methods were followed for the analyses of particle size and chlorophyll a. Clustering of the stations using the cluster neighbour-joining methods and Detrended correspondence analysis (Saitou & Ney,1987) of the stations (quadrats) within four transects at Lok Kawi were based on density of 85 nematodes species and the environmental parameter values such as height above chart datum, temperature, pH, salinity, dissolved oxygen, median particle size, percentage silt and clay, chlorophyll a and pheopigment. RESULTS Environmental Parameters The variations of environmental factors such as intertidal height, temperature, pH, salinity, dissolved oxygen, median particle size, silt and clay, chlorophyll a and pheopigment in Lok Kawi beach are summarized in Table 1. The record of these factors were expressed by following the quadrats sequence from MHWN to MLWN. 43 Intertidal heights of quadrats were plotted in relation to the Chart Datum and the tidal constants in Table 1. Most of the Quadrats 1 within the four transects were closer to the MHWN level and therefore considered as MHWN quadrats. Their heights above Chart Datum were between 4.50 and 4.60 metres. Quadrats 2, 3 and 4 in all transects were in the range of 3.70 to 2.30 metres above Chart Datum and considered as Mid-Tide Level (MTL) quadrats. Quadrats 5 in all transect were located closer to MLWN and ranged in heights above Chart Datum between 1.40 to 1.60 m. There was little variation in pore water temperature at the four transects at Lok Kawi beach, this being not greater than about 2.9°C. Temperatures were generally within the range of 28.5 to 31.4°C (Table 1) and close to the temperature of the sea. In general, the pore water temperature within four transects was quite similar. The pH values of pore water within the four transect were ranged from 7.0 to 8.5 and shows the basic pH. The variation of pH is 1.5. There was a wide variation in pore water salinity at the four transects at Lok Kawi beach but this being not greater than 15.5 Practical Salinity Unit (PSU) (Table 1). The pore water salinity within four transects were ranged from 14.7 to 30.2 PSU. Salinity values at Quadrats 5 and 1, Transect 4 were much lower (14.7 & 17.5 PSU) due to the influence of freshwater intrusion from Desa Cattle drainage after a heavy rainfall in the night before sampling. Both of the quadrates were located close to the Desa Cattle channel on the beach. Similarly, salinity values at Quadrat 1 Transect 2 were also low (16.1 PSU) due to the freshwater seepage from the supralittoral area after a heavy rain in the night before sampling. The salinity at Lok Kawi beach was influenced by freshwater seepage and the salinity values at all transects were found to be lower than the surface sea water adjacent to it. 44 HORIZONTAL DISTRIBUTION OF INTERTIDAL NEMATODE Table 1: Summary of Environmental parameters at Lok Kawi, Sabah (Tran.–transect, TL–tide level, Quadrat, HCD–Height above Chart Datum (m), Tem.–temperature (°C), Sal.–salinity (PSU), DO–dissolved oxygen (mg/l), Med.-median (Ø, particle size), S&C-percentage silt and clay, Chlo.-Chlorophyll a (mg/m3), Pheo–Pheopigment (mg/m3). MHWN – Mean High Water Neap, MTL – Mid-Tide Level and MLWN – Mean Low Water Neap) Tran. TL Q HCD Tem. pH Sal. DO Med. S&C Chlo. Pheo. 1 MHWN MTL 1 2 3 4 5 4.55 3.70 2.95 2.30 1.40 29.5 29.6 30.8 30.3 31.4 7.0 7.0 7.1 7.5 7.6 25.8 29.9 26.1 29.0 25.5 0.3 0.4 0.9 0.2 0.4 2.8 5.2 3.0 2.6 2.7 35.9 69.3 43.9 35.9 36.6 5.02 4.00 3.94 3.50 5.76 3.52 7.87 13.88 10.75 7.69 1 2 3 4 5 4.60 3.65 3.10 2.40 1.60 30.5 30.0 29.4 29.0 30.1 7.8 7.8 8.0 7.9 7.7 16.1 29.7 30.2 29.3 27.7 1.1 1.1 1.6 2.1 0.7 1.5 1.2 0.9 1.1 1.2 7.4 7.2 10.1 9.1 6.5 1.81 5.32 3.44 3.40 2.62 7.69 2.20 0.75 1.12 1.62 1 2 3 4 5 4.60 3.70 3.05 2.30 1.55 30.6 30.0 29.9 29.1 28.9 7.5 7.8 7.8 8.5 8.5 21.9 28.9 27.8 21.1 17.5 1.1 1.6 1.5 0.9 0.6 1.1 1.4 2.2 1.5 2.3 11.3 3.4 4.2 6.2 11.4 2.50 4.60 1.73 2.99 4.01 2.68 2.15 1.36 0.15 5.76 1 2 3 4 5 4.50 3.65 3.00 2.40 1.60 28.5 29.4 29.8 29.8 30.6 7.9 8.0 8.0 8.2 7.9 17.5 27.9 27.8 28.3 14.7 0.8 0.8 0.9 0.9 0.6 1.3 1.1 1.4 1.4 2.0 4.1 4.1 3.6 3.3 4.4 0.94 0.91 4.74 7.61 2.39 0.61 0.40 1.97 2.40 1.00 MLWN 2 MHWN MTL MLWN 3 MHWN MTL MLWN 4 MHWN MTL MLWN Dissolved oxygen values of the pore water are listed in Table 1. On all transects the values were variables ranging from 0.2 (Transect 1) to 2.1 mg/l (Transect 2). The lowest value were recorded along the mangrove transect (Transect 1). The minimum value (0.2 mg/l) was recorded at Quadrat 4 Transect 1. Median particle size in Transect 1 ranged from 2.6 to 5.2 ∅ whereas the values in other transects ranges from 0.9 (Transect 2) to 2.3 ∅ (Transect 3) (Table 1). The silt and clay percentages was higher in Transect 1 compared to the other transects. The lowest value in the mangrove transect (Transect 1) was 35.9% whereas the highest value in the sandy transects was only 11.4% (Transect 3). There was a wide variation in the distribution of chlorophyll a in all transects (Table 1) with no horizontal trends apparent. The mean concentration of the four transects ranged from 3.17 (Transect 3) to 4.44 mg/m3 (Transect 1). The distribution of pheopigment varied along all transects and no horizontal trend was apparent (Table 1). The mean concentration of four transects ranged from 1.28 (Transect 4) to 8.74 mg/m3 (Transect 1). Most of the values in Transect 1 (mangrove area) were either similar or higher (7.69 to 13.88 mg/m3) than the other sandy transects (Transects 2, 3 and 4). Nematode’s Distribution Total density The maximum nematode’s density recorded at Lok Kawi beach was 7,015 (Quadrat 5, Transect 4) and minimum of 413 ind./10 cm square (Quadrat 2, Transect 2) (Table 2). The mean SHABDIN MOHD. LONG & OTHMAN HAJI ROSS nematode’s density ranged from 1,473 (Transect 3) to 3,055 ind./10 cm square (Transect 4). Higher densities of nematodes in the lower half of the beach at Transects 2 to 4. They appeared to be a gradual increase in density from the upper shore towards the lower shore except for Quadrat 1 in Transects 2 and 3 where densities of nematodes were higher than some MTL quadrats. However, no horizontal trend was apparent in Transect 1 (mangrove area). Horizontal distribution of nematode species Considering the horizontal distribution of nematode’s species as a whole within all transects and tide levels at Lok Kawi, beach, five groups of species can be observed (Fig. 2). Firstly, the nematode’s species distributed from MHWN to MLWN. A total of 24 species were included in this group. Five species were distributed from MHWN to MTL only and considered as the second group. The third group which comprised of 19 species was zoned from MTL to MLWN. The fourth group 45 contained 1 species and its distribution was at MHWN and MLWN. The fifth group of nematode species was distributed either at MHWN or MTL or MLWN only and comprised of 34 species (MHWN: 6 species, MTL: 12 species, and MLWN: 16 species). Horizontal distribution of nematode feeding types By considering the horizontal distribution of the nematode feeding type groups as a whole at Lok Kawi beach, four trends can be observed (Fig. 3). The group selective deposit feeders (1A) varied erratically along transect with its density average ranged from 244 to 996 ind./10 cm square. The non-selective deposit feeders (1B) and epigrowth feeders (2A) groups show a clear increase in density towards the lower half of the beach. However, the density of the predators/omnivorous (2B) group seemed to be stable from MHWN to MLWN. Table 2: Total density of the nematodes in all transects at Lok Kawi beach Transect Tide Level Quadrat Density 1 MHWN MTL 1 2 3 4 5 1 2 3 4 5 1 2 3 4 5 1 2 3 4 1846 785 4032 1760 4281 4088 413 447 1181 5494 1113 452 1737 1919 2142 554 1059 2437 4211 5 7015 2 MLWN MHWN MTL 3 MLWN MHWN MTL 4 MLWN MHWN MTL MLWN 46 HORIZONTAL DISTRIBUTION OF INTERTIDAL NEMATODE Desmodora cazca Metacomesoma aequale Maryllynnia gerlachi Theristus pertenuis Gammanema sp.1 Daptonema spirum Viscosia meridionalis Prochromadora sp. Spirinia parasitifera Eleutherolaimus hopperi Daptonema articulatum Ptycholaimellus macrodentatus Oncholaimus oxyuris Stylotheristus mutilus Paradontophora pacifica Metalinhomoeus karachiensis Terschellingia communis Sphaerolaimus penicillus Haliplectus sp. Leptolaimus venustus Leptolaimus luridus Sphaerotheristus macrostoma Ingenia mirabilis Metalinhomoeus insularis Oncholaimus campylocercoides Tripyloides sp. Minolaimus sp. Ironid gen.1 Terschellingia longicaudata Terschellingoides filiformis Halichoanolaimus chordiurus Halalaimus supercirrhatus Cyatholaimid sp.1 Molgolaimus sp. Metacyatholaimus sp. Xyala Metachromadora onyxoides Chromadorella sp.1 Chromadorella sp.2 Chromadorella filiformis Hypodontolaimus pumilio Aegialoalaimus sp.2 Siphonolaimus purpureus Paracomesoma inaequale Trichotheristus sp. Nannolaimoides decoratus Ironid gen.2 Paralinhomoeus conspicuus Daptonema sp. Oncholaimus sp. Steineria ampullacea Richtersia sp. Desmocolex sp. Acanthonchus cobbi Aponema sp. Paracanthoncus sp. Setoplectus sp. Quadricoma sp. Gairleanema sp. Parodontophora sp. Ceramonema filum Chromadorita c.f. luekarti Platycomopsis sp. Gammanema sp.2 Paralongicyatholaimus macramphis Dorylaimopsis turneri Oncholaimus brachycercus Spilophorella sp. Rhynchonema cinctum Rhabdocoma sp. Chromadorita tenuis Conilia sp. Paramesonchium sp. Oxystomina elongata Gammanema kosswigi Neotonchus sp. Nemanema sp. Prooncholaimus sp. Linhomoeus sp. Cyatholaimid sp.2 Trissonchulus sp. Anoplostoma subulatum Daptonema kornoeense Figure 2: Horizontal distribution of nematodes species in Lok Kawi beach, Kota Kinabalu, Sabah, Malaysia * Combination of nematodes distribution in all transects SHABDIN MOHD. LONG & OTHMAN HAJI ROSS 47 Figure 3: Horizontal distribution of nematodes feeding types (mean values for 4 transects) in Lok Kawi beach (Q1: Mean High Water Neap, Q2 to Q4: Mid-Tide Level, Q5: Mean Low Water Neap, 1A: Selective deposit feeders, 1B: Non selective deposit feeders, 2A: Epigrowth feeders and 2B: Predators/Omnivorous) Species diversity of nematodes When considering the horizontal distribution of species number, species diversity, and evenness as a whole at Lok Kawi beach, these values were found to be generally increased towards the low water (Fig. 4). This shows that the nematode parameters decreases as the beach Chart Datum increases except for the species diversity. Species diversity phenomenon is common due to a higher species density at low tide stations leading to the domination of one or two species so that the species diversity become low if we compared with the stations higher on the beach. Statistical Analysis Pearson correlation analysis results shows that there was a significant correlation between the height above Chart Datum and total nematodes, nematode feeding type non-selective deposit feeders (1B), nematode feeding type epigrowth feeders (2A), nematode species diversity, nematode evenness, nematode species richness and number of nematode species (Table 4). Cluster analysis of the stations (quadrats) within four transects at Lok Kawi beach showed at least two major groups of stations are clustered in the dendrogram (Fig. 5). The first cluster included stations from T2Q5 to T1Q1. One station (T4Q5) is separated from the main 2 clusters. The cluster analysis did not show clearly about the influence of height of the beach on meiofaunal densities. Detrended correspondence analysis of the stations also showed similar results (Fig. 6). HORIZONTAL DISTRIBUTION OF INTERTIDAL NEMATODE Species no. Diversity and evenness 48 Quadrate Figure 4: Horizontal distribution (mean values of 4 transects) of Shannon – Weiner diversity index (H’), Pielou’s evenness (J’) and species no. of nematodes (S) (Q1: Mean High Water Neap, Q2 to Q4: Mid-Tide Level, Q5: Mean Low Water Neap) Table 4: Pearson correlation coefficient of nematodes and beach height Nematode parameters Total nematodes Nematodes feeding type non-selective deposit feeders (1B) Nematodes feeding type Epigrowth feeders (2A) Shannon-Wiener diversity Pielou’s evenness Nematodes species number Height above Chart Datum R = -0.55, P<0.05 R = -0.57, P<0.05 R = -0.61, P<0.05 R = 0.64, P<0.05 R = -0.46, P<0.05 R = -0.63, P<0.05 SHABDIN MOHD. LONG & OTHMAN HAJI ROSS 49 2500 Linkage Distance 2000 1500 1000 500 Group 2 Group 1 Factor 2 Figure 5: Dendrogram illustrating the similarity of the stations (quadrats) at Mean High Water Neap (Q1), Mid-Tide Level (Q2 to Q4) and Mean Low Water Neap (Q5) T1 to T4 (Transects) Factor 1 Figure 6: Detrended correspondence analysis of the nematodes species at Mean High Water Neap ( ), Mid-Tide Level ( ) and Mean Low Water Neap ( ) T1Q1 T1Q2 T2Q2 T2Q3 T2Q4 T3Q2 T4Q1 T3Q4 T3Q3 T3Q1 T3Q5 T1Q3 T1Q4 T1Q5 T2Q5 T2Q1 T4Q2 T4Q3 T4Q4 T4Q5 0 50 DISCUSSION The density of nematodes in the mangrove and sandy sediments varied considerably both on a global and local scales (Dye,1983; Hodda & Nicholas, 1985; Alongi, 1987; Olafsson, 1995). This variation is within the recorded range from other intertidal habitat. Several authors have found significant differences in tropical meiofaunal densities among intertidal positions in mangrove and sandy areas with highest abundance at low water stations (Dye, 1983; Hodda & Nicholas, 1985; Alongi, 1990; Sasekumar, 1994) although Dye (1983) found that meiofauna in highest number at mid-water level. The similar result was also known in certain areas (Moore, 1979). Animal tolerant to higher temperatures, lower values of water saturation and oxygen tension, appeared to occupy higher tidal levels (Rao & Misra, 1983). Alongi (1990) concluded that physical factor (temperature, grain size, salinity, infrequent tidal inundation limiting dispersal) accounted for the differences observed rather than biological variables. In the present study, Pearson correlation showed that the species density and diversity of the nematodes were influenced by the height of the beach, however clustering and Detrended correspondence analysis did not clearly show the influences of this factor. Therefore, in this case the conclusion by Coull (1988) that there were no unequivocal and universal causative factors controlling the nematode’s species density on the sandy and muddy intertidal habitats in a tropical country like Malaysia can be supported. The study of nematode species zonation across the intertidal habitat have been conducted both in temperate and tropical regions (Moore, 1979; Coull, et al., 1979; Alongi, 1987). Three groups of species have been suggested across the sandy intertidal habitats. Firstly, the species often restricted themselves to sublittoral fringe guild, secondly, eurytopic species where their distribution are centred on HORIZONTAL DISTRIBUTION OF INTERTIDAL NEMATODE the lower shore and thirdly, the species that confined to the upper shore only (Coull, 1988). The current study found that five groups of nematode’s species were distributed horizontally along the intertidal height. The species distributed from MTL to MLWN or found only at MTL were considered as stenotopic species. These species possibly prefer a more stable condition towards low-tide zone. However, the species that were distributed from MHWN to MLWN were considered as eurytopic and able to tolerate to the changes in the environmental parameters while the species that were restricted in distribution to a certain tide level such as between MHWN and MTL can only tolerate desiccation during exposure on the beach (Tengku Balkis, 2000; Farizah, 2001; Shabdin, 2006). Deposit feeders nematodes usually outnumber other feeding guilds in the Australian mangrove (Hodda & Nicholas, 1986). In Lok Kawi beach, the non-selective deposit feeder (1B) was dominant in both the mangrove (T1) and sandy sediment (T4) transects. The epigrowth feeders (2A) were dominant in other sandy sediment transects (Transects 2 and 3). The current finding is in accordance with the general trend for the proportion of epistrate feeders to be higher in the more sandy sediments and for deposit feeders to dominate in finer sediments (Hodda & Nicholas, 1986; Olafsson, 1995). However, the non-selective deposit feeders were also dominant in one of the sandy transects (Transect 4). This finding had deviated from the general trends. The nonselective deposit feeders (1B) were able to ingest particles of a wider size range including benthic diatoms (Platt & Warwick, 1983). The occurrence of maximum chlorophyll a value recorded at Quadrat 4, Transect 4 explains this situation. Based on several studies in India (Fell et al., 1975; Krishnamurthy et al., 1984) predatory SHABDIN MOHD. LONG & OTHMAN HAJI ROSS nematodes were more abundant in the tropics than in other intertidal areas. The results of this study do not support the generalization that predatory fauna is more abundant in tropical sediments. The deposit feeders were abundance in the mangrove and one of the sandy sediment transects (Transect 4) in Lok Kawi beach. It appears that the proportion of nematodes feeding groups is as variable in the tropical sediments as in other intertidal areas. The nonselective deposit feeders (1B) and epigrowth feeders (2A) groups increased in density towards MLWN. This is possibly due to the more stable condition towards low-tide level (Tietjen, 1977, Shabdin, 2006). When the nematode’s diversity values were compared, one trend is apparent. The diversity, species richness, evenness and number of species increased towards the low-tide level. Pearson correlation coefficient shows that there is a significant correlation between the height of the beach and the species diversity of the nematodes and this is possibly due to the stable condition towards low-tide level. However, the cluster and Detrended correspondence analysis of the stations did not show clearly the influence of height of the beach on meiofaunal densities. The different of results between both analyses were due to the nature of analysis. Cluster and factor analysis of the stations within four transects were based on density of 85 nematodes species and the values of physico-chemical parameters which compared to the Pearson correlation analysis that only calculated based on the total density of nematodes and the physico-chemical parameters values. However, the results of the cluster – factor analysis are more reliable due to the more accurate results obtained as compared to the Pearson correlation analysis (Moore, 1983). Therefore, we conclude that there were no definite and universal causative factors, which controlled horizontal distribution of freeliving 51 nematode in the intertidal sandy and muddy habitats of the Lok Kawi beach. ACKNOWLEDGEMENTS We wish to thank Universiti Malaysia Sarawak (UNIMAS) for their financial support and the Zoology Department, Universiti Kebangsaan Malaysia for the use of their laboratory facilities. We wish to thank Associate Prof. Dr Tajuddin Abdullah, for his comment to improve the manuscript and Prof. Y. Shirayama from Seto Marine Biological Laboratory, Kyoto University, Japan for providing us the nematode’s literature of Prof. S.A. Gerlach collections. REFERENCES Alongi, D.M. 1987. Inter-estuary variation and intertidal zonation of freeliving nematode communities in tropical mangrove systems. Marine Ecology Progress Series. 40: 103 – 114. Alongi, D.M. 1990. Community dynamics of freeliving nematodes in some tropical mangrove and sandflats habitats. 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Final year project report, Department of Aquatic Science, Faculty of Resource Science and Technology, 53 Universiti Malaysia Sarawak. pp 25. Tietjen, J.H. 1976. Distribution and species diversity of deep sea nematodes off North Carolina. Deep Sea Research. 23: 755 – 768. Tietjen, J.H. 1977. Population, distribution and structure of the freeliving nematodes of Long Island Sound. Marine Biology. 43: 123 – 136. Warwick, R.M. 1971. Nematode association in the Exe Estuary. Journal of the Marine Biological Association of the United Kingdom. 51: 439 – 454. JOURNAL OF TROPICAL BIOLOGY AND CONSERVATION, 4 (1) : 55 – 66, 2008 Research Article Stand structure and tree composition of Timbah Virgin Jungle Reserve, Sabah, Malaysia Januarius GOBILIK Sabah Forestry Department, Forest Research Centre P.O. Box 1407, Sepilok 90715 Sandakan, Sabah, Malaysia. ABSTRACT The stand structure and tree composition of Timbah Virgin Jungle Reserve (VGR Timbah) were studied. Three locations in the VJR were selected, and at each location, 1-ha study plot was established. The plots were sub-divided into 10×10 m2 sub-plots, and in each sub-plot, stem diameters of trees > 5 cm diameter-at-breastheight (DBH) were measured. The trees were identified, and their relative density and relative basal area per hectare were calculated. Little difference was found in tree density and basal area per ha between the plots. From the plots, 2,369 trees > 5 cm DBH were enumerated. Total basal area of the trees was 119.5 m2. Stem diameter class distribution of the trees was found to follow the inverse J-shape pattern. Many of the trees had 5 – < 20 cm DBH (75.9 % of the total stem). Only 4.2% had > 60 cm DBH. Total densities of the trees > 5 cm and > 10 cm DBH were 790 and 474 trees ha–1, respectively and total basal areas per ha were 39.8 and 38.4 m2 ha–1, respectively. In this study, 47 tree families, 118 genera and 117 species of trees were identified. Many of the trees were Dipterocarpaceae (20% of the total stems). The most abundant species was Dryobalanops beccarii (4.3% of the total stems; 34 trees ha–1). Keywords: Sabah, Timbah Virgin Jungle Reserve, forest ecology Pioneer and disturbed forest trees were found at a very low density. The results suggest that VJR Timbah's soils are infertile, since D. beccarii, the most abundant species in the plots, prefers leached whitish or yellowish sandy soils. The results also suggest that the VJR had experienced a less significant logging encroachment or invasion of disturbed forest trees. The results imply that VJR Timbah still maintains its undisturbed forest stand structure and tree composition, although it is relatively small in size and surrounded by a large matrix of heavily logged forest. INTRODUCTION Of the many forest enumeration activities in Sabah, only a few are in virgin jungle reserves (VJR). The scenario would be that many foresters and researchers are not interested to study the biological components of VJRs because many of these forests are comparatively small and surrounded by a dense matrix of disturbed forests. To date, little is documented about the stand structure and tree composition of the forests in VJRs. In this paper, the stand structure and tree composition of VJR Timbah are reported. The information would be important to assist in the development of management prescriptions for the VJR or for the logged-over commercial forest surrounding the VJR. STAND STRUCTURE AND TREE COMPOSITION OF TIMBAH VIRGIN JUNGLE RESERVE, SABAH 56 METHODS Study Site VJR Timbah is a 110 ha area situated in compartment 53 of the Tangkulap Forest Reserve (Fig. 1). The general climatic and ecological condition of the VJR have not yet been described. In Tangkulap, the annual rainfall averages 3,000 mm, but it is highly variable (1,777 mm to 3,708 mm), with a major deficit occurs every 6 years (Sabah Forestry Department, 2006). May – August and November – February are the wettest seasons and March – April and September – October are the driest seasons. The daily temperature averages 27°C. The main rock types of the area derived from Kolapis formation and Ultrabasic Igneous. The main soil association is Lokan with orthic acrisol as the main soil unit. The natural vegetation of the area is predominantly lowland mixed dipterocarp forest and is dominated by Shorea johorensis and its associated Dipterocarpus species, or by Dryobalanops beccarii and its associated Shorea species (Sabah Forestry Department, 2006). Vegetation Sampling and Data Analysis The study was carried out in 2004. Three 1-ha plots were established in the VJR at 2 km interval distance: plot 1 (5°26'8.099”N; 117°12'12.036”E), plot 2 (5°26'5.411”N; 117°12'2.793”E) and plot 3 (5°26'2.218”N; 117°11'54.296”E; Figure 1). The plots were sub-divided into 10×10 m2 sub-plots to facilitate the enumeration of trees down to 5 cm stem-diameter at breast-height (DBH). The DBH of the trees was measured and the trees Figure 1: Location of VJR Timbah in Sabah and the three study plots (P1 – P3) in the VJR JANUARIUS GOBILIK 57 were identified. The number of saplings of dipterocarps (< 5 cm DBH to down to 50 cm tall) was also counted. Relative density and basal area per ha were calculated for every species. Relative density (or relative basal area per ha) of species was calculated as sum of density (or sum of relative basal area per ha) of the species divided by sum of density (or sum of relative basal area per ha) of all species. Voucher specimens were kept at Sandakan Herbarium (SAN). Nomenclature in this study follows largely the Tree Flora of Sabah and Sarawak (Soepadmo et al., 1995, 1996, 2000, 2002 & 2004). RESULTS Little difference was found in tree density and basal area per ha between the plots. The three 1-ha study plots included 2,369 trees > 5 cm DBH (average = 790 trees ha–1) and 1,411 trees >10 cm DBH (average = 474 trees ha–1). Many of the trees had 5 < 20 cm DBH (75.9%; Figure 2 and Table 1 – see DBH's mode). Only 4.2% had > 60 cm DBH. Dipterocarps composed 45.0 most of the trees > 60 cm DBH (Appendix 1 – see Maximum DBH). At 180 cm DBH, Dryobalanops beccarii (Dipterocarpaceae) was the largest tree in the plots. Total basal area of the trees > 5 cm DBH was 119.5 m2 (average = 39.8 m2 ha–1). For the trees > 10 cm DBH, it was 115.3 m2 (average = 38.4 m2 ha–1). As was expected, trees > 100 cm DBH had the highest contribution to the total basal area per ha (24.3%; Fig. 2). It was followed by the trees 10 < 30 cm DBH (22%). Stocking of dipterocarp saplings in the plots were 558 saplings ha–1. There were 47 families, 118 genera and 117 species identified from the plots. Most of the species were Dipterocarpaceae (35 species), Euphorbiaceae (20 species), Anacardiaceae (7 species), Sapotaceae (6 species), and Moraceae (5 species; Appendix 1). A small number of the trees (14.4%), however, were unable to be identified to genus or species. The most abundant trees in the plots were Dipterocarpaceae, Euphorbiaceae, Myristicaceae, Myrtaceae and Lauraceae. The relative densities Relative density Relative basal area/ha 40.0 35.0 30.0 25.0 20.0 15.0 10.0 5.0 Size class (DBH, cm) Figure 2: Size class distribution for all trees = 5 cm DBH in the study plots >100 90-<100 80-<90 70-<80 60-<70 50-<60 40-<50 30-<40 20-<30 10-<20 0.0 5-<10 % 58 STAND STRUCTURE AND TREE COMPOSITION OF TIMBAH VIRGIN JUNGLE RESERVE, SABAH of trees from these families were 20%, 10.4%, 8.5%, 7.6% and 4.3% respectively (Table 1). Other important families were Annonaceae, Anacardiaceae, Burseraceae, Clusiaceae, Bombacaceae and Verbenaceae. The relative densities of trees from the latter were 3.5%, 2.7%, 2.6%, 2.5%, 2.4% and 2.4% respectively. Thirteen (29.8%) of the families had <5 individuals (<0.2% relative density). In terms of basal area, Dipterocarpaceae had the highest contribution to the total basal area per ha (55.4%), followed by Myrtaceae (4.5%), Myristicaceae (3.4%), Euphorbiaceae (3%), Sterculiaceae (2.8%), Lauraceae (2.5%) and Bombacaceae (2.2%; Table 1). Other families that had more than 1% contribution to the total basal area per ha were Clusiaceae (1.3%), Fagaceae (1.3%), Anacardiaceae (1.2%), Moraceae (1.2%), Sapotaceae (1.2%), Burseraceae (1.1%), Lecythidaceae (1.1%) and Melastomataceae (1.1%). Of the 117 species known from the plots, only six had more than 1% relative density (>24 trees ha-1), namely, Dryobalanops beccarii (4.3%), Pternandra coerulescens (1.9%), Knema laurina (1.6%), Shorea mecistopteryx (1.5%), Teijsmanniodendron simplicifolium (1.2%) and Durio grandiflorus (1%; Appendix 1). Only 16 species of these 117 species had more than 1% (>1.2 m2 ha–1) contribution to the total basal area per ha. They were mainly dipterocarps (13 species): Dryobalanops beccarii (14%), Shorea mecistopteryx (4.5%), Dipterocarpus stellatus (2.6%), Dipterocarpus pachyphyllus (1.8%), Shorea argentifolia (1.7%), Dryobalanops lanceolata (1.7%), Shorea pauciflora (1.2%), Shorea laevis (1.1%), Shorea hypoleuca (1.1%), Shorea macroptera (1%), Parashorea tomentella (1%) and Dipterocarpus globosus (1%). DISCUSSION The results indicate that much of VJR Timbah's stand structure and tree composition are similar to that of undisturbed mixed dipterocarp forests. Stem diameter class distribution of trees in the VJR follows the inverse J-shape pattern, which is similar to that of lowland primary forest of Danum Valley (Newbery et al., 1992; Newbery et al., 1996) and Segaliud-Lokan (Fox, 1967). The VJR, however, supports a slightly lower density of trees compared with several other undisturbed mixed dipterocarp forests. Its density of trees >10 cm DBH was 474 trees ha–1 compared to 487 – 569 trees ha–1 in Danum Valley (Newbery et al., 1999; Bischoff et al., 2005), 477 trees ha–1 in Sungai Menyala and 546 trees ha–1 in Pasoh (Manokaran & Swaine, 1994). On the other hand, it appears to facilitate many large trees to co-exist compared to the other forests, just as one could imply from its higher total basal area per hectare (38.4 m2 ha–1). In Danum Valley, Sungai Menyala and Pasoh, the average basal areas per ha of trees >10 cm DBH were 30.6, 31.8 and 29.1 m2 ha–1, respectively. It has a closely similar average basal area per ha to Bukit Lagong (41.1 m2 ha–1; Manokaran & Swaine, 1994), a hill mixed dipterocarp forest in Peninsular Malaysia, but again its density of trees >10 cm DBH is lower than that of the latter. Generally, the results imply that VJR Timbah still maintains its undisturbed forest stand structure and tree composition, although it is relatively small and being surrounded by a large matrix of logged forest. The VJR has a closely similar number of families and genera (47 and 118, respectively) to Sungai Menyala (45 and 116, respectively). However, those numbers are lower than that of Danum Valley (59 and 164 respectively) and Bukit Lagong (51 and 139 respectively). It has again a similar number of families to Pasoh (45-48), but its number of genera is lower than that of the latter (125-14). Even so, the top-ten list of family of higher density in the VJR is closely similar to that of Danum Valley, Bukit Lagong, Sungai Menyala and Pasoh. The list differs only in the positions of the families in the ranking. On the top the ranking are Dipterocarpaceae and Euphorbiaceae, and these families are followed by any of these families: Myristicaceae, Myrtaceae, Annonaceae, Anacardiaceae, JANUARIUS GOBILIK 59 Table 1: Family composition, density (D), relative density (Rd) and relative basal area per hectare (Rba/ ha) of trees > 5 cm DBH in the study plots (N = number of individuals; Total = 2,369) Family Alangiaceae Anacardiaceae Annonaceae Apocynaceae Bombacaceae Burseraceae Celastraceae Chrysobalanaceae Combretaceae Crypteroniaceae Dilleniaceae Dipterocarpaceae Ebenaceae Elaeocarpaceae Euphorbiaceae Fagaceae Flacourtiaceae Clusiaceae Hypericaceae Icacinaceae Lauraceae Lecythidaceae Leguminosae Magnoliaceae Melastomataceae Meliaceae Moraceae Myristicaceae Myrsinaceae Myrtaceae Olacaceae Oleaceae Unidentified taxon Polygalaceae Rhamnaceae Rubiaceae Rutaceae Sabiaceae Sapindaceae Sapotaceae Simaroubaceae Sterculiaceae Theaceae Thymelaeaceae Tiliaceae Ulmaceae Verbenaceae N 9 65 82 2 58 61 10 10 4 2 1 473 46 3 247 30 30 59 1 6 103 35 30 4 46 19 28 203 2 181 5 1 227 10 5 47 3 1 16 46 6 38 3 13 39 1 58 D (trees ha –1 ) Rd (%) Rba/ha (%) Maximum DBH (cm) 3 21.7 27.3 0.7 19.3 20.3 3.3 3.3 1.3 0.7 0.3 157.7 15.3 1 82.3 10 10 19.7 0.3 2 34.3 11.7 10 1.3 15.3 6.3 9.3 67.7 0.7 60.3 1.7 0.3 75.7 3.3 1.7 15.7 1 0.3 5.3 15.3 2 12.7 1 4.3 13.0 0.3 19.3 0.4 2.7 3.5 0.1 2.4 2.6 0.4 0.4 0.2 0.1 0.0 20.0 1.9 0.1 10.4 1.3 1.3 2.5 0.0 0.3 4.3 1.4 1.3 0.2 1.9 0.9 1.2 8.5 0.1 7.6 0.2 0.0 9.6 0.4 0.2 2.0 0.1 0.0 0.7 1.9 0.3 1.6 0.1 0.5 1.6 0.0 2.4 0.1 1.2 0.9 0.1 2.2 1.1 0.3 0.1 0.0 0.1 0.0 55.4 0.6 0.0 3.0 1.3 0.9 1.3 0.0 0.1 2.5 1.1 0.7 0.0 1.1 0.4 1.2 3.6 0.0 4.5 0.2 0.0 8.4 0.5 0.3 0.7 0.0 0.0 0.4 1.2 0.1 2.8 0.0 0.1 0.4 0.0 0.9 20.4 39.5 51.6 35.4 125.0 52.5 35.4 24.2 8.0 25.8 14.0 180.0 53.2 15.0 90.0 70.0 80.0 55.4 25.5 15.6 78.0 90.0 69.0 13.4 38.2 44.6 71.0 70.0 8.3 72.0 43.3 7.3 92.0 72.0 46.8 41.4 13.7 6.4 44.9 51.6 27.1 79.3 16.6 29.0 25.8 5.1 36.9 DBH's mode 6.4 7.0 8.9 18.5 5.7 7.2 8.0 7.0 6.1 17.5 14.0 5.4 6.1 10.2 6.4 12.1 10.2 10.2 25.5 8.0 7.3 8.9 5.4 8.9 6.1 22.3 6.4 7.6 8.0 10.2 11.5 7.3 6.1 5.7 20.1 6.1 8.6 6.4 10.2 7.0 4.8 8.9 6.1 5.1 9.6 5.1 11.1 60 STAND STRUCTURE AND TREE COMPOSITION OF TIMBAH VIRGIN JUNGLE RESERVE, SABAH Burseraceae, Lauraceae, Clusiaceae, and Bombacaceae. The position of the families, however, changes with inclusion of trees < 10 cm DBH or < 5 cm DBH in the data analyses. Such inclusion favours families composed mainly by small-sized trees to be on the top of the ranking. The number of known species in the VJR (117 species) is incomparable to that of Danum Valley (307; Bischoff et al., 2005), Bukit Lagong (253), Sungai Menyala (232) and Pasoh (235 – 276). This is because the number of species identified positively in this study is much lower than that of the latter. Notwithstanding, of the known species, the top-ten list of abundant species in the VJR is differing from that of the latter. Of the 10 abundant species in the VJR, none is found in Danum Valley, only one in Bukit Lagong (S. laevis), three in Pasoh (Ochanostachys amentacea, Shorea parvifolia, S. pauciflora), and four in Sungai Menyala (S. macroptera, O. amentacea, S. parvifolia, S. pauciflora). In the VJR, Dryobalanops beccarii, a dipterocarp, was the common species, but in Danum Valley, Bukit Lagong, Sungai Menyala and Pasoh, it was the non-dipterocarps. It was Mallotus wrayi in Danum (Newbery et al., 1992), Hydnocarpus filipes in Bukit Lagong, Santiria laevigata in Sungai Menyala and Xerospermum noronhianum in Pasoh. A strong preference of a few dipterocarp species for certain soil conditions has been reported in Borneo (Palmiotto et al., 2004). In Sabah, D. beccarii was reported to prefer leached whitish or yellowish sandy soils and to occur as a pure stand in areas of such soil condition (Fox, 1972). Thus the latter could explain the above result, although the density of D. beccarii in the VJR appears to be lower than that of found by Fox (1972) in the forest at the mouths of the Segama and Sugut Rivers or that of forest at the upper stream of the Imbak River (personal observation, 2005). The high density of D. beccarii and Shorea mecistopteryx in the study plots suggests that VJR Timbah has a slightly different ecological condition than that of Parashorea tomentellaEusideroxylon zwageri forest type, the forest type of the general area (Tangkulap Forest Reserve) where the VJR is situated. While these two species were found abundantly in the plots, Parashorea tomentella and its three common associated species, Dryobalanops lanceolata, Dipterocarpus caudiferus and Shorea leprosula, occur at very low density. Shorea johorensis and Eusideroxylon zwageri, the other two important species associated with Parashorea tomentella, were also not found in the plots. In other words, Parashorea tomentella and its associated species are very scarce in the plots, although they are markedly abundant in the adjacent forests to the VJR (Fox, 1967; Seino et al., 2005). Therefore, based on Fox's (1972) classification of forest types in Sabah, VJR Timbah's vegetation can be loosely classified as lowland mixed dipterocarp forest of Parashorea tomentella-Eusideroxylon zwageri forest type with a strong influence of inland heath forest of swampy-padang forest type. There are five important points that can be postulated from the results. First, soil characteristics are suspected to be the determining factor for the current tree composition in the VJR. The two abundant trees in the VJR, D. beccarii and S. mecistopteryx, are reported to prefer leached whitish or yellowish sandy soils. Thus only trees that could tolerate such soil condition would successfully populate the VJR. Secondly, there will be other sites in Tangkulap that have similar soil condition to VJR Timbah. Such similarity also means that the sites are infertile. If so, the common and abundant trees in the typical Parashorea tomentella-Eusideroxylon zwageri forest type would not be suitable as planting material to reforest some degraded sites in Tangkulap. The sites could instead be appropriately reforested with D. beccarii, S. mecistopteryx and S. macroptera. Thirdly, the suspicion that many of the small VJRs in Sabah JANUARIUS GOBILIK had experienced heavy logging encroachment may only be half true. This is because a small VJR such as VJR Timbah has still had stand structure and tree composition that are similar to that of undisturbed forests, although it is surrounded by forest that was heavily logged. Fourthly, the invasion of disturbed forest trees into small VJRs is less prominent. As was the scenario in VJR Timbah, pioneer and disturbed forest trees were scarcely found in the study plots, although these trees were predominantly abundant in the adjacent forest to the VJR. Fifthly, as was the scenario in VJR Timbah, many of the small VJRs in Sabah may still maintain their undisturbed forest stand structures and tree compositions. If so, these VJRs still reserve important information on the pre-disturbance stand structures and tree compositions of the disturbed forests in adjacent areas to them. Therefore, future studies on the stand structures and species compositions of the forests in these VJRs are highly encouraged so that this information can be used in the management of the disturbed forests. ACKNOWLEDGEMENTS I would like to thank Prof. Dato' Dr Abdul Latiff Mohamad of Universiti Kebangsaan Malaysia for his constructive suggestions, which have improved this paper significantly. REFERENCES Bischoff, W., D. M. Newbery, M. Lingenfelder, R. Schnaeckel, G. H. Petol, L. Madani and C. E. Ridsdale. 2005. Secondary succession and dipterocarp recruitment in Bornean rain forest after logging. Forest Ecology and Management. 218: 174 – 192. Fox, J. E. D. 1967. An enumeration of lowland dipterocarp forest in Sabah. The Malayan Forester. 30: 263 – 279. Fox, J. E. D. 1972. The natural vegetation of Sabah and natural regeneration of the dipterocarp forests. PhD thesis. University of Wales, Wales. 61 Manokaran, N. and M. D. Swaine. 1994. Population dynamics of trees in dipterocarp forest of Peninsular Malaysia. Malayan Forest Records no. 40, Forest Research Institute Malaysia, Kepong, Kuala Lumpur. Newbery, D. M., D. N. Kennedy, G. H. Petol, L. Madani and C. E. Ridsdale. 1999. Primary forest dynamics in lowland dipterocarp forest at Danum Valley, Sabah, Malaysia and the role of the understorey. Philosophical Transactions of the Royal Society, London (B). 354: 1763 – 1782. Newbery, D. M., E. J. E. Campbell, J. Proctor and M. J. Still. 1996. Primary lowland dipterocarp forest at Danum valley, Sabah, Malaysia: Species composition and patterns in the understorey. Vegetatio. 122: 193 – 220. Newbery, D. M., E. J. F. Campbell, Y. F. Lee, C. E. Ridsdale and M. J. Still. 1992. Primary lowland dipterocarp forest at Danum Valley, Sabah, Malaysia: Structure, relative abundance and family composition. Philosophical Transactions of the Royal Society, London. 354: 1763 – 1782. Palmiotto, P. A., S. J. Davies, K. A. Vogt, M. S. Ashton, D. J. Vogt and P. S. Ashton. 2004. Soil related habitat specialization in dipterocarp rain forest tree species in Borneo. Journal of Ecology. 92: 609 – 623. Sabah Forestry Department. 2006. Forest Management Plan of Tangkulap Forest Reserve for the period 2006 – 2015. Forestry Department of Sabah, Sandakan, Sabah, Malaysia. Seino, T. M., M. Takyu, S. C. Aiba, K. Kitayama and R. C. Ong. 2005. Floristic composition, stand structure and aboveground biomass of the tropical rain forests of Deramakot and Tangkulap Forest Reserve in Malaysia under different forest management. In: Lee, Y. F., A. Y. C. Chunga and K. Kitayama. (Eds.). Proceedings of the Second International Workshop on Synergy between Carbon Management and Biodiversity Conservation in Tropical Rain Forests. Forest Research 62 STAND STRUCTURE AND TREE COMPOSITION OF TIMBAH VIRGIN JUNGLE RESERVE, SABAH Centre, Sabah Forestry Department, Sandakan, Sabah, Malaysia, 30 November – 1 December 2005. pp 29 – 52. Soepadmo, E. and K. M. Wong. (Eds.). 1995. Tree Flora of Sabah and Sarawak. Volume 1. A jointly publication of Forest Research Institute Malaysia, Kuala Lumpur; Forestry Department Sabah, Sandakan and Forestry Department Sarawak, Kuching. Soepadmo, E., K. M. Wong and L. G. Saw. (Eds.). 1996. Tree Flora of Sabah and Sarawak. Volume 2. A jointly publication of Forest Research Institute Malaysia, Kuala Lumpur; Forestry Department Sabah, Sandakan and Forestry Department Sarawak, Kuching. Soepadmo, E. and L. G. Saw. (Eds.). 2000. Tree Flora of Sabah and Sarawak. Volume 3. A jointly publication of Forest Research Institute Malaysia, Kuala Lumpur; Forestry Department Sabah, Sandakan and Forestry Department Sarawak, Kuching. Soepadmo, E., L. G. Saw and R. C. K. Chung. (Eds.). 2002. Tree Flora of Sabah and Sarawak. Volume 4. A jointly publication of Forest Research Institute Malaysia, Kuala Lumpur; Forestry Department Sabah, Sandakan and Forestry Department Sarawak, Kuching. Soepadmo, E., L. G. Saw and R. C. K. Chung. (Eds.). 2002. Tree Flora of Sabah and Sarawak. Volume 5. A jointly publication of Forest Research Institute Malaysia, Kuala Lumpur; Forestry Department Sabah, Sandakan and Forestry Department Sarawak, Kuching. JANUARIUS GOBILIK 63 Appendix 1: Species composition; N = Number of individuals; D = Density (trees ha–1); Rd = Relative density; Rba/ha = Relative basal area per hectare of trees > 5 cm DBH in the study plots; Max DBH = Maximum DBH (cm); Total = 2,369 Species Family N Actinodaphne sp. Adinandra dumosa Aglaia spp, Alangium javanicum Alseodaphne sp. Antidesma leucopodum Aporusa elmerii Aporusa grandistipulata Aporusa spp, Aquilaria malaccensis Archidendron jiringa Ardisia elliptica Artocarpus anisophyllus Artocarpus dadah Artocarpus elasticus Artocarpus kemando Artocarpus spp, Artocarpus tamaran Atuna cordata Atuna sp. Baccaurea latifolia Baccaurea macrocarpa Baccaurea parviflora Baccaurea spp, Barringtonia macrostachya Barringtonia spp, Barringtonia stipulata Beilschmiedia sp. Blumeodendron tokbrai Calophyllum spp, Canarium odontophyllum Canarium sp. Castanopsis motleyana Chionanthus pluriflorus Chisocheton pentandrus Chisocheton sp. Cleistanthus megacarpus Cratoxylum cochinchinense Croton oblongus Crypteronia griffithii Cryptocarya spp, Dacryodes costata Dehassia incrassata Dillenia excelsa Dimocarpus sp. Diospyros discocalyx Diospyros elliptifolia Diospyros spp, Diploknema sebifera Lauraceae Theaceae Meliaceae Alangiaceae Lauraceae Euphorbiaceae Euphorbiaceae Euphorbiaceae Euphorbiaceae Thymelaeaceae Leguminosae Myrsinaceae Moraceae Moraceae Moraceae Moraceae Moraceae Moraceae Chrysobalanaceae Chrysobalanaceae Euphorbiaceae Euphorbiaceae Euphorbiaceae Euphorbiaceae Lecythidaceae Lecythidaceae Lecythidaceae Lauraceae Euphorbiaceae Clusiaceae Burseraceae Burseraceae Fagaceae Oleaceae Meliaceae Meliaceae Euphorbiaceae Hypericaceae Euphorbiaceae Crypteroniaceae Lauraceae Burseraceae Lauraceae Dilleniaceae Sapindaceae Ebenaceae Ebenaceae Ebenaceae Sapotaceae 3 3 12 9 4 2 21 3 10 1 2 2 2 6 1 7 10 1 6 3 5 18 16 26 5 26 3 4 1 29 2 3 15 1 2 3 2 1 1 3 12 3 3 1 6 4 3 38 3 D Rd (%) Rba/ha (%) Max DBH DBH's mode 1 1 4 3 1.3 0.7 7 1 3.3 0.3 0.7 0.7 0.7 2 0.3 2.3 3.3 0.3 2 1 1.7 6 5.3 8.7 1.7 8.7 1 1.3 0.3 9.7 0.7 1 5 0.3 0.7 1 0.7 0.3 0.3 1 4 1 1 0.3 2 1.3 1 12.7 1 0.1 0.1 0.5 0.4 0.2 0.1 0.9 0.1 0.4 0.0 0.1 0.1 0.1 0.3 0.0 0.3 0.4 0.0 0.3 0.1 0.2 0.8 0.7 1.1 0.2 1.1 0.1 0.2 0.0 1.2 0.1 0.1 0.6 0.0 0.1 0.1 0.1 0.0 0.0 0.1 0.5 0.1 0.1 0.0 0.3 0.2 0.1 1.6 0.1 0.1 0.0 0.4 0.1 0.0 0.0 0.2 0.0 0.1 0.1 0.0 0.0 0.3 0.3 0.3 0.2 0.1 0.0 0.1 0.0 0.2 0.4 0.1 0.5 0.1 0.3 0.1 0.3 0.1 0.6 0.0 0.0 0.9 0.0 0.0 0.0 0.0 0.0 0.0 0.1 0.5 0.0 0.0 0.0 0.2 0.0 0.0 0.6 0.0 42.7 16.6 44.6 20.4 17.8 22.0 21.7 10.2 18.8 29.0 9.9 8.3 70.0 45.2 71.0 32.5 33.1 11.8 18.2 13.1 38.2 42.0 13.7 37.3 26.1 29.0 26.8 53.5 32.2 55.4 14.0 9.9 70.0 7.3 11.8 10.8 13.4 25.5 7.6 25.8 59.2 14.0 22.0 14.0 44.9 7.6 17.5 53.2 10.2 6.4 6.1 22.3 6.4 5.4 6.7 8.6 5.7 9.6 29.0 6.4 8.0 7.6 7.0 71.0 7.6 6.4 11.8 8.6 8.3 7.0 7.0 5.7 6.4 10.2 6.7 12.4 12.1 32.2 6.1 9.2 6.7 6.7 7.3 5.4 7.0 10.8 25.5 7.6 17.5 6.1 5.7 8.0 14.0 7.6 5.1 9.2 7.0 6.1 64 STAND STRUCTURE AND TREE COMPOSITION OF TIMBAH VIRGIN JUNGLE RESERVE, SABAH Species Family Dipterocarpus acutangulus Dipterocarpus applanatus Dipterocarpus caudiferus Dipterocarpus confertus Dipterocarpus globosus Dipterocarpus pachyphyllus Dipterocarpus spp, Dipterocarpus stellatus Dryobalanops beccarii Dryobalanops keithii Dryobalanops lanceolata Drypetes longifolia Drypetes sp. Durio grandiflorus Durio spp, Dyera costulata Dysoxylum sp. Elaeocarpus stipularis Elateriospermum tapos Eurycoma longifolia Ficus sp. Fordia splendidissima Ganua kingiana Ganua sarawakensis Garcinia mangostana Garcinia parvifolia Garcinia parvifolia Gironniera nervosa Gluta oba Gluta spp, Gluta swintonia Gonystylus bancanus Gymnacranthera spp, Heritiera spp, Hopea beccariana Hopea nervosa Hopea pentanervia Hydnocarpus borneensis Hydnocarpus woodii Irvingia malayana Knema laurina Koompassia excelsa Koompassia malaccensis Koordersiodendron pinnatum Lansium domesticum Lithocarpus echinifer Lithocarpus spp, Litsea spp, Lophopetalum beccariana Lophopetalum javanicum Lophopetalum sp. Macaranga sp. Macaranga winkleri Dipterocarpaceae Dipterocarpaceae Dipterocarpaceae Dipterocarpaceae Dipterocarpaceae Dipterocarpaceae Dipterocarpaceae Dipterocarpaceae Dipterocarpaceae Dipterocarpaceae Dipterocarpaceae Euphorbiaceae Euphorbiaceae Bombacaceae Bombacaceae Apocynaceae Meliaceae Elaeocarpaceae Euphorbiaceae Simaroubaceae Moraceae Leguminosae Sapotaceae Sapotaceae Clusiaceae Clusiaceae Euphorbiaceae Ulmaceae Anacardiaceae Anacardiaceae Anacardiaceae Thymelaeaceae Myristicaceae Sterculiaceae Dipterocarpaceae Dipterocarpaceae Dipterocarpaceae Flacourtiaceae Flacourtiaceae Simaroubaceae Myristicaceae Leguminosae Leguminosae Anacardiaceae Meliaceae Fagaceae Fagaceae Lauraceae Celastraceae Celastraceae Celastraceae Euphorbiaceae Euphorbiaceae N 5 1 14 4 4 10 43 20 102 1 4 5 6 24 22 2 1 3 5 2 1 19 10 1 3 16 1 1 20 26 4 12 43 32 2 7 1 17 10 4 38 2 3 1 1 1 11 18 1 6 3 1 5 D 1.7 0.3 4.7 1.3 1.3 3.3 14.3 6.7 34 0.3 1.3 1.7 2 8 7.3 0.7 0.3 1 1.7 0.7 0.3 6.3 3.3 0.3 1 5.3 0.3 0.3 6.7 8.7 1.3 4 14.3 10.7 0.7 2.3 0.3 5.7 3.3 1.3 12.7 0.7 1 0.3 0.3 0.3 3.7 6 0.3 2 1 0.3 1.7 Rd (%) 0.2 0.0 0.6 0.2 0.2 0.4 1.8 0.8 4.3 0.0 0.2 0.2 0.3 1.0 0.9 0.1 0.0 0.1 0.2 0.1 0.0 0.8 0.4 0.0 0.1 0.7 0.0 0.0 0.8 1.1 0.2 0.5 1.8 1.4 0.1 0.3 0.0 0.7 0.4 0.2 1.6 0.1 0.1 0.0 0.0 0.0 0.5 0.8 0.0 0.3 0.1 0.0 0.2 Rba/ha (%) 1.6 0.0 0.2 0.0 1.0 1.8 4.5 2.6 14.6 0.0 1.1 0.1 0.1 0.3 1.6 0.1 0.0 0.0 0.0 0.0 0.0 0.0 0.1 0.1 0.1 0.2 0.0 0.0 0.5 0.3 0.1 0.1 0.4 2.4 0.6 0.2 0.0 0.2 0.6 0.1 0.4 0.0 0.5 0.0 0.0 0.0 0.3 0.8 0.0 0.2 0.0 0.0 0.1 Max DBH 109.2 14.6 33.8 10.5 112.0 112.0 125.0 95.9 180.0 17.2 98.0 26.8 25.5 28.0 125.0 35.4 15.0 15.0 10.5 6.7 10.5 10.2 22.0 42.7 26.4 26.1 4.8 5.1 39.5 29.9 34.1 20.1 33.1 79.3 75.0 29.9 5.7 28.3 80.0 27.1 22.3 9.2 69.0 20.1 6.4 20.4 36.3 78.0 22.9 35.4 8.9 5.7 19.1 DBH's mode 38.2 14.6 4.8 9.2 13.4 9.9 6.1 12.4 5.7 17.2 4.8 5.4 6.7 9.6 29.6 18.5 15.0 10.2 6.4 4.8 10.5 5.4 6.4 42.7 12.4 5.4 4.8 5.1 7.0 5.7 5.1 5.1 8.3 8.9 59.2 9.2 5.7 4.8 5.1 9.6 10.2 8.3 24.5 20.1 6.4 20.4 10.2 7.3 22.9 9.9 8.0 5.7 8.9 JANUARIUS GOBILIK 65 Species Family Madhuca sp. Magnolia sp. Mallotus muticus Mallotus pinangensis Mallotus spp, Mallotus stipularis Mallotus wrayi Mangifera pajang Mangifera sp. Melanochyla beccariana Melicope luna-akenda Meliosma sumatrana Memecylon laevigatum Mesua macrantha Microcos crassifolia Microcos spp, Myristica spp, Nauclea sp. Neesia spp, Nephelium lappaceum Ochanostachys amentacea Orophea sp. Palaquium rostratum Parashorea malaanonan Parashorea tomentella Parinari sp. Parishia insignis Payena accuminata Payena macrophylla Peltophorum racemosum Pentace adenophora Pentace laxiflora Pentace sp. Pentaspadon motleyana Pleiocarpidia sandakanica Polyalthia spp, Polyalthia sumatrana Pternandra coerulescens Ryparosa acuminata Santiria sp. Scaphium sp. Scorodocarpus borneensis Shorea accuminatissima Shorea argentifolia Shorea falciferoides Shorea fallax Shorea gibbosa Shorea hypoleuca Shorea laevis Shorea leprosula Shorea macrophylla Shorea macroptera Shorea mecistopteryx Shorea ovalis Sapotaceae Magnoliaceae Euphorbiaceae Euphorbiaceae Euphorbiaceae Euphorbiaceae Euphorbiaceae Anacardiaceae Anacardiaceae Anacardiaceae Rutaceae Sabiaceae Melastomataceae Clusiaceae Tiliaceae Tiliaceae Myristicaceae Rubiaceae Bombacaceae Sapindaceae Olacaceae Annonaceae Sapotaceae Dipterocarpaceae Dipterocarpaceae Chrysobalanaceae Anacardiaceae Sapotaceae Sapotaceae Leguminosae Tiliaceae Tiliaceae Tiliaceae Anacardiaceae Rubiaceae Annonaceae Annonaceae Melastomataceae Flacourtiaceae Burseraceae Sterculiaceae Olacaceae Dipterocarpaceae Dipterocarpaceae Dipterocarpaceae Dipterocarpaceae Dipterocarpaceae Dipterocarpaceae Dipterocarpaceae Dipterocarpaceae Dipterocarpaceae Dipterocarpaceae Dipterocarpaceae Dipterocarpaceae N 1 4 3 6 66 24 14 3 2 4 3 1 1 11 2 21 122 6 12 10 2 7 4 7 5 3 3 3 7 1 10 5 1 2 7 60 16 45 4 4 6 3 3 6 3 17 6 2 2 4 9 20 36 10 D 0.3 1.3 1 2 22 8 4.7 1 0.7 1.3 1 0.3 0.3 3.7 0.7 7 40.7 2 4 3.3 0.7 2.3 1.3 2.3 1.7 1 1 1 2.3 0.3 3.3 1.7 0.3 0.7 2.3 20 5.3 15 1.3 1.3 2 1 1 2 1 5.7 2 0.7 0.7 1.3 3 6.7 12 3.3 Rd (%) 0.0 0.2 0.1 0.3 2.8 1.0 0.6 0.1 0.1 0.2 0.1 0.0 0.0 0.5 0.1 0.9 5.1 0.3 0.5 0.4 0.1 0.3 0.2 0.3 0.2 0.1 0.1 0.1 0.3 0.0 0.4 0.2 0.0 0.1 0.3 2.5 0.7 1.9 0.2 0.2 0.3 0.1 0.1 0.3 0.1 0.7 0.3 0.1 0.1 0.2 0.4 0.8 1.5 0.4 Rba/ha (%) 0.0 0.0 0.1 0.1 0.3 0.1 0.1 0.0 0.0 0.0 0.0 0.0 0.0 0.5 0.0 0.1 2.8 0.1 0.3 0.1 0.0 0.2 0.1 0.5 1.0 0.1 0.0 0.1 0.0 0.0 0.1 0.1 0.0 0.2 0.2 0.6 0.2 1.1 0.1 0.3 0.4 0.2 0.0 1.7 0.2 0.5 0.6 1.1 1.1 0.3 0.3 1.0 4.5 0.1 Max DBH 24.2 13.4 36.0 17.2 14.6 13.7 13.7 18.8 19.4 20.1 13.7 6.4 8.9 37.9 10.5 21.7 70.0 26.1 38.9 31.2 21.3 51.6 30.6 75.0 84.0 24.2 8.3 39.5 15.6 15.9 22.3 25.8 9.9 39.2 41.4 24.2 28.3 38.2 22.9 52.5 64.6 43.3 24.2 89.0 42.0 40.8 90.0 99.0 104.0 68.5 41.4 58.6 170.0 24.5 DBH's mode 24.2 8.9 7.6 4.8 7.6 5.4 4.8 7.0 9.6 7.0 8.6 6.4 8.9 37.9 5.7 9.6 10.8 9.6 7.3 10.2 11.5 5.4 13.4 5.4 11.8 7.0 5.1 9.9 7.0 15.9 12.1 10.2 9.9 28.3 6.1 8.9 8.0 6.1 6.4 5.7 6.7 11.8 5.7 13.4 6.4 7.3 8.9 82.0 75.0 5.4 5.4 12.4 10.5 4.8 66 STAND STRUCTURE AND TREE COMPOSITION OF TIMBAH VIRGIN JUNGLE RESERVE, SABAH Species Family Shorea parvifolia Shorea pauciflora Shorea smithiana Shorea spp, Shorea superba Shorea waltonii Shorea xanthophylla Sindora beccariana Stemonurus scorpioides Syzygium spp, Teijsmanniodendron bogoriensis Teijsmanniodendron holophyllum Teijsmanniodendron pteropodum Teijsmanniodendron simplicifolium Terminalia sp. Trigonobalanus verticillata Trigonopleura malayana Triomma malaccensis Unidentified taxon Unidentified taxon Unidentified taxon Unidentified taxa Urophyllum spp, Vatica dulitensis Vatica oblongifolia Vatica spp, Xanthophyllum ellipticum Zizyphus angustifolius Dipterocarpaceae Dipterocarpaceae Dipterocarpaceae Dipterocarpaceae Dipterocarpaceae Dipterocarpaceae Dipterocarpaceae Leguminosae Icacinaceae Myrtaceae Verbenaceae N D Rd (%) Rba/ha (%) Max DBH DBH's mode 1 2 3 59 5 1 4 4 6 180 1 0.3 0.7 1 19.7 1.7 0.3 1.3 1.3 2 60 0.3 0.0 0.1 0.1 2.5 0.2 0.0 0.2 0.2 0.3 7.6 0.0 0.4 1.2 0.0 11.3 0.1 0.7 0.0 0.7 0.1 4.5 0.0 78.3 135.0 17.2 140.0 29.6 105.0 17.5 90.0 15.6 72.0 14.6 78.3 19.1 6.4 6.4 5.4 105.0 8.0 12.1 8.0 10.2 14.6 Verbenaceae 22 7.3 0.9 0.5 36.9 6.1 Verbenaceae 6 2 0.3 0.1 22.0 11.1 Verbenaceae 29 9.7 1.2 0.4 34.7 5.4 4 3 3 9 40 58 16 227 34 16 11 25 10 5 1.3 1 1 3 13.3 19.3 5.3 75.7 11.3 5.3 3.7 8.3 3.3 1.7 0.2 0.1 0.1 0.4 1.7 2.4 0.7 9.6 1.4 0.7 0.5 1.1 0.4 0.2 0.0 0.1 0.0 0.0 0.7 0.6 0.6 8.4 0.4 0.3 0.2 0.5 0.5 0.3 8.0 25.2 13.4 11.1 41.1 28.7 51.6 92.0 29.9 48.4 25.8 31.8 72.0 46.8 6.1 25.2 9.6 7.0 7.3 5.7 10.2 6.1 7.0 5.4 6.4 9.6 5.7 20.1 Combretaceae Fagaceae Euphorbiaceae Burseraceae Burseraceae Lauraceae Sapotaceae Other trees Rubiaceae Dipterocarpaceae Dipterocarpaceae Dipterocarpaceae Polygalaceae Rhamnaceae JOURNAL OF TROPICAL BIOLOGY AND CONSERVATION, 4 (1) : 67 – 80, 2008 Research Article Preliminary molecular phylogeny of Bornean Plagiostachys (Zingiberaceae) based on DNA sequence data of internal transcribed spacer (ITS) Avelinah JULIUS¹*, Monica SULEIMAN² and Atsuko TAKANO³ ¹Tropical Forest Biodiversity Centre, Forest Research Institute Malaysia, 52109 Kepong, Selangor, Malaysia E-mail: plagiovel80@yahoo.com ²Institute for Tropical Biology and Conservation, Universiti Malaysia Sabah, Locked Bag 2073, 88999 Kota Kinabalu, Sabah, Malaysia ³Museum of Nature and Human Activities Hyogo, 6 Chome, Yayoigaoka, Sanda, Hyogo 669-1546, Japan ABSTRACT A molecular phylogenetic analysis based on DNA sequence data of internal transcribed spacer region (ITS 1, ITS 2) and 5.8S gene and re-evaluation of morphological characters were performed in order to examine the relationships of Plagiostachys and related genera, and to elucidate the previous informal grouping of Bornean Plagiostachys. A total of 111 taxa, including 25 taxa of Plagiostachys were included in the analysis. The strict consensus tree (length = 1094; CI = 0.482; HI = 0.518) showed that Plagiostachys consisted a strong supported (BS = 96%) clade with some Alpinia species that belong to section Alpinia. However, species of Plagiostachys comprised three subclades (A, B and C) and each subclade was moderately to strongly supported with relatively high bootstrap values. The three subclades of Plagiostachys were also recognized morphologically by the combination of inflorescence and capsule characters. Poor resolved tree prevent us to conclude phylogenetic status of the genus Plagiostachys, but at the moment we propose Keywords: Bornean, phylogeny, Plagiostachys, Zingiberaceae this genus remain an independent genus and wait for further analysis. Previous informal grouping of Bornean Plagiostachys was not supported from both molecular and morphological analyses. INTRODUCTION Plagiostachys Ridl., is relatively small but complex genus in Zingiberaceae. It is distributed mainly in the Malesian region with the centre of diversity in Borneo, where currently 10 species of Plagiostachys are known. The genus is distinguished from the other genera in Zingiberaceae by the tightly congested, apparently lateral inflorescence, which is, in fact, terminal on the short stem of the leafy shoots, and usually breaks through the leaf sheaths just above ground level or sometimes in the middle (Smith, 1990). The flower is subtended by a usually tubular bracteole, and the labellum is small and rather fleshy, with diverged venation of petaloid in some species. The bracteoles and flowers are very mucilaginous and tend to decay within one day in some species. Such a mucilaginous nature makes herbarium works difficult, therefore relatively few studies have been done in this genus (Smith, 1985; Cowley, 68 PRELIMINARY MOLECULAR PHYLOGENY OF BORNEAN PLAGIOSTACHYS 1999; Sakai & Nagamasu, 2003; Gobilik et al., 2005). In order to study Plagiostachys, collecting sufficient number of spirit specimens of flowers, inflorescences and observations of morphological characters in the field or a living status are vital. Smith (1985) divided the Bornean Plagiostachys into two informal groups, Group 1 and Group 2 (Table 1). Species belonging to Group 1 have bilobed ligule, mucilaginous inflorescence, distinctly tubular and early decaying bracteoles, yellow and white with some pink flowers, fleshy and soon-decaying calyx, style that adnate to corolla wall, and oblong-pyriforms capsules. On the other hand, species of Group 2 have truncate or emarginate ligule, tubular at base or open bracteoles, pinkish-red with yellow labellum flowers, papery calyx, style that free from the corolla wall, and globose capsules. The grouping was, however, disputed by Cowley (1999) and Sakai & Nagamasu (2003) as the characters used for the grouping did not fit with any species described recently. Cowley (1999) mentioned that the characters of the ligule, style and capsule of P. parva J. Cowley belonged to Smith’s Group 1, whereas characters of the calyx, bracteole and non-mucilaginous nature of the inflorescence belonged to Group 2. Another species, P. breviramosa J. Cowley differed from Smith’s Group 2 by its adnated style to the corolla tube, non-globose capsule and bilobed ligule. Similarly, the species described recently by Gobilik et al. (2005), i.e. P. lasiophylla Gobilik & A. L. Lamb and P. oblanceolata Gobilik & A. L. Lamb also belong to neither Smith’s groups. Although Gobilik et al. (2005) placed their two new species in Smith’s Group 2 on the basis of the not mucilaginous inflorescences, but the characters of the style, capsule shape and ligule Table 1: Characters used for the classification of the genus Plagiostachys (after Smith, 1985) Character Group 1 1. Inflorescence Mucilaginous Group 2 Non-mucilaginous 2. Bracteole Distinctly tubular, early decaying, Tubular at base or open, partially only the very basal part remaining decaying or persistent at fruiting stage 3. Calyx Fleshy, at least decaying in upper part Calyx not fleshy, not decaying 4. Style Sometimes adnate to the wall of the corolla tube above the epigynous glands Usually free from the wall of the corolla-tube at the base 5. Capsule Oblong-pyriform, angled, rarely globose Globose 6. Ligule Bilobed Truncate or emarginate, rarely bilobed 7. Floral colour Yellow and white with some pink Pinkish-red with yellow labellum AVELINAH JULIUS et al. of these two species belong to Smith’s Group 1. Thus, the reliability of Smith’s classification became doubtful. Re-evaluation of these morphological characters used for the informal grouping and grouping itself should be needed. Recent molecular phylogenetic analyses based on DNA sequence data (plastid matK and nuclear rDNA ITS) done by Kress et al. (2002, 2005 & 2007) and Pedersen (2004) confirmed that Plagiostachys and Alpinia were sister group. Kress et al. (2002, 2005 & 2007) also showed that Amomum and Alpinia were polyphyletic groups and Plagiostachys was embedded within Alpinia. Plagiostachys was moderately to strongly supported (BS>70%) as a monophyletic group. Unfortunately only two species of the genus were included in their analyses, making the phylogenetic position of Plagiostachys within Alpinioideae remained inconclusive. In this preliminary study, we examined morphological characters of Plagiostachys used for classification and analyzed DNA sequences of the internal transcribed spacer (ITS) from an expanded taxon sampling of the genus Plagiostachys, together with related genera of the Alpinioideae previously used in the investigation of Kress et al. (2005) in order to (1) resolve the position of Plagiostachys within Alpinioideae, (2) evaluate the informal grouping within Plagiostachys as proposed by Smith (1985) and (3) evaluate the morphological characters used in classification of the genus with respect to our phylogenetic results. MATERIALS AND METHODS Morphological Study Plant collection and observation were mainly made during December 2003 to July 2004, late February to early March and from November to December 2005 in Sabah, Malaysia. These specimens were deposited at BORH, HYO and 69 SAN. Additional materials, i.e. specimens and digital images of specimens of Plagiostachys (including type specimens) from BO, E, Fl, G, IBSC, K, NHM and PR were also consulted. Morphological attributes used in Smith’s informal grouping were examined for the 17 taxa of Plagiostachys: ligule, bracteole, floral colour, calyx, style and capsule. Taxon Sampling The sources of plant material with voucher and accession numbers are represented in Table 2. The 19 taxa of Plagiostachys and three taxa of Alpinia were newly sequenced. The expanded sampling of Bornean Plagiostachys is well represented by both Smith’s Group 1 and Group 2. In addition, 89 accessions including 58 species of Alpinia representing all six major clades of Kress et al. (2005) were downloaded from GenBank. In total 111 taxa were used for the analysis. The tribe Riedelieae represented by four genera (Burbidgea, Pleuranthodium, Riedelia and Siamanthus) and the incertae sedis Siliquamomum were selected as outgroups. Genomic DNA Extraction, PCR Amplification and Sequencing Fresh or silica gel dried leaf tissues were used for total DNA extraction using a modified CTAB (hexadecyltrimethyl-ammonium bromide) method (Doyle & Doyle, 1987; Takano & Okada, 2002). The entire ITS1-5.8S-ITS2 region was amplified via polymerase chain reaction (PCR) using ITS5P (5’-GGAAGGAGAAGTCGTAACAAGG-3’) and ITS8P (5’-CACGCTTCTCCAGACTACA3’) of Möller & Cronk (1997). The thermal cycling parameters were: initial denaturation at 94°C for 30 seconds, primers annealing at 48°C for 2 minutes, and extension at 72°C for 45 seconds. A final extension at 72°C for 7 minutes was done at the end of the amplification. PCR products were then purified by using High Pure PCR Product Purification kit (Roche Diagnostic 70 PRELIMINARY MOLECULAR PHYLOGENY OF BORNEAN PLAGIOSTACHYS Table 2: List of taxa used in this study with information related to taxonomy, collections, vouchers and GenBank accession number. Data are presented in the following sequence: Taxon name, Voucher (if available), Collection site/ Source of DNA (if available) and GenBank accession numbers for ITS1, 5.8S and ITS2. “¯ ” indicates voucher and collection site/ source of DNA is not available. Outgroup: Burbidgea nitida Hook.f., J. Mood 96p81, —, AF414494; B. pauciflora Valeton, S. Sakai 241 KYO, AB097253; B. pubescens Ridl., J. Mood 990, —, AF414495; B. schizocheila Hort., Rangsiruji & M. Newman s.n. E, AY769821; B. stenantha Ridl., —, —, AJ388308; Riedelia sp., —, —, AF478785; Pleuranthodium floccosum (Valeton) R. M. Sm., —, —, AY742333; P. trichocalyx (Valeton) R. M. Sm., —, —, AY742332; Siamanthus siliquosus K. Larsen & J. Mood, Living collection RBGE 20001319 E, Thailand, AY769820; Siliquamomum tonkinense Baill., Kress #006802 US, —, AF478791; Renealmia alpinia (Rottb.) Maas, Kress #99-6407 US, Tropical America, AF478778; R. batternbergiana Bak., Kress #94-5277 US, Tropical Africa, AF478779. Ingroup: Aframomum luteoalbum K. Schum., A. D. Poulsen 708 AAU, Africa, AF414493; Afra. verrucosum J.M. Lock, A. D. Poulsen 771 AAU, Africa, AF414492; Alpinia aenea Argent, G. Argent et al. 0016 E, Indonesia, AY769833; Alp. aquatica (Retz.) Roscoe, —, —, AY742335; Alp. arctiflora (F. Muell.) Benth., —, —, AY742336; Alp. argentea (B. L. Burtt & R. M. Sm.) R. M. Sm., —, Sumatra, AY742337; Alp. bilamellata Makino, —, —, AY742339; Alp. blepharocalyx K. Schum., Kress #98-6136 US, AF478709; Alp. caerulea Benth., —, —, AY742342; Alp. calcarata Roscoe, Kress #94-3675 US, China, AF478710; Alp. carolinensis Koidz., Kress #99-6404 US, Micronesia, AF478711; Alp. conchigera Griff., Kress #00-6706 US, China, AF478712; Alp. cylindrocephala K. Schum., —, —, AY742345; Alp. elegans K. Schum., Kress #99-6412 US, Philippines, AF478713; Alp. eremochlamys K. Schum., —, —, AY742346; Alp. fax B. L. Burtt & R. M. Sm., —, —, AY742348; Alp. formosana K. Schum., —, —, AY742350; Alp. foxworthyi Ridl., Kress #98-6293 US, Philippines, AF478713; Alp. galanga (L.) Willd., Kress #94-5263 US, Ex hort. Hawaii, AF478715; Alp. guangdongensis S. J. Chen & Z. Y. Chen, —, —, AY742352; Alp. haenkei C. Presl, —, —, AY742354; Alp. hainanensis K. Schum., —, —, AY742355; Alp. hansenii R. M. Sm., A. Julius 155 BORH, Sabah, DQ507828; Alp. havilandii K. Schum., Cultivated, Mountain Garden, K. Park, Sabah, DQ507829, Alp. hookeriana Valeton, —, —, AY742356; Alp. intermedia Gagnep., Kress #97-5780 US, Japan, AF478716; Alp. japonica (Thunb.) Miq., ¯ , ¯ , AY742358; Alp. jianganfen T. L. Wu, —, —, AY188289; Alp. ligulata K. Schum., ¯ , Borneo, AY742361; Alp. maclurei Merr., —, —, AY742362; Alp. monopleura K. Schum., —, —, AY742363; Alp. nanchuanensis Z. Y. Zhu, —, — , AY188290; Alp. napoensis H. Dong & G. J. Xu, —, —, AF254466; Alp. nigra (Gaertn.) B. L. Burtt, —, —, AF254459; Alp. nieuwenhuizii Valeton, —, Sabah, DQ507830; Alp. novaepommeraniae K. Schum., —, —, AY742368; Alp. nutans K. Schum., —, —, AY742369; Alp. officinarum Hance, Kress #00-6614 US, China, AF478718; Alp. oxyphylla Miq., —, —, AY742372; Alp. pinetorum Loes. AY742373; Alp. pinnanensis T. L. Wu & Senjen Chen, —, —, AF254470; Alp. polyantha Fang, —, —, AY745692; Alp. pricei Hayata, —, —, AY742374; Alp. pumila Hook “f.”, Kress #976119 US, China, AF478719; Alp. rosea Elmer, —, Philippines, AY742377; Alp. rubricaulis K. Schum., —, Sumatra, AY742378; Alp. rugosa J. -P. Liao ined., —, —, AY742379; Alp. sibuyanensis Elmer, —, Philippines, AY742381; AVELINAH JULIUS et al. 71 Table 2 continues: Alp. species #2, —, —, AY742383; Alp. species #1, —, —, AY742382; Alp. stachyoides Hance, — , —, AY742384; Alp. strobiliformis T. L. Wu & Senjen Chen var. glabra T. L. Wu, —, —, AF254471; Alp. suishaensis Hayata, —, —, AY742385; Alp. tonkinensis Gagnep., —, —, AY742386; Alp. vittata Bull., Kress #99-6415 US, Polynesia, AF478720; Alp. warburgii K. Schum., ¯ , Sumatra, AY742388; Alp. zerumbet (Pers.) B. L. Burtt & R. M. Sm., ¯ , ¯ , AY742389;A. aff. calycodes Baker, W. Baker 1051 K, Indonesia, AY769834; Amomum angustipetalum S. Sakai & Nagam., S. Sakai 389 KYO, Sarawak, AB097245; Amo. calyptratum S. Sakai & Nagam., S. Sakai 363 KYO, Sarawak, AB097239; Amo. dimorphum M. F. Newman, S. Sakai 372 KYO, Sarawak, AB097244; Amo. durum S. Sakai & Nagam., S. Sakai 362 KYO, Sarawak, AB097241; Amo. oliganthum K. Schum., S. Sakai 370 KYO, Sarawak, AB097243; Amo. roseisquamosum Nagam. & S. Sakai, S. Sakai 188 KYO, Sarawak, AB097246, Amo. somniculosum S. Sakai & Nagam., S. Sakai 373 KYO, Sarawak, AB097247; Amo. villosum Lour., Kress #01-6978 US, —, AF478724; Etlingera triorgyalis (Baker) R. M. Sm., L.B. Pedersen & B. Johans. 1065 C, —, AF414475; Etl. yunnanensis (T. L. Wu & Senjen Chen) R. M. Sm., W.J. Kress 95-5511 US, —, AF414468; Hornstedtia gracilis R. M. Sm., J. Mood 996, AF414482; H. hainanensis T. L. Wu & Senjen Chen, Kress #97-5769 US, —, AF478766; Leptosolena haenkei C. Presl, —, —, AY742331; Plagiostachys albiflora Ridl. 1, A. Julius & P. Jimbau 2 BORH, Sabah, DQ507835; P. albiflora Ridl. 2, A. Julius & A. Takano AT34 BORH, HYO, Sabah, DQ507834; P. brevicalcarata Julius & A. Takano, A. Julius & A. Takano AT35 SAN, HYO, Sabah, DQ507839; P. crocydocalyx (K. Schum.) B. L. Burtt & R. M. Sm., A. Julius & A. Takano AT1 SAN, HYO, Sabah, DQ507837; P. glandulosa S. Sakai & Nagam., S. Sakai 374 KYO, Sarawak, AB097251; P. lasiophylla Gobilik & A. L. Lamb, Cultivated. Sandakan, Sepilok, RDC, Evo. Trail, Sabah, DQ507843; P. longicaudata Julius & A. Takano, A. Julius & A. Takano AT76 SAN, HYO, Sabah, DQ507832; P. megacarpa Julius & A. Takano, A. Julius et al. AGS2 SAN, HYO, Sabah, DQ507844; P. mucida Holttum, Khaw Siok Hooi 741 E, KEP, Malay Peninsula, AY769841; P. oblanceolata Gobilik & A. L. Lamb, A. Julius et al. ATW34 BORH, HYO, Sabah, DQ507848; P. breviramosa complex, A. Julius & A. Takano AT63 SAN, HYO, Sabah, DQ507842; P. parva J. Cowley, AMGB 1 BORH, SNP, Sabah, DQ507840; P. roseiflora Julius & A. Takano, A. Julius & A. Takano AT64 SAN, HYO, Sabah, DQ507846; P. strobilifera (Baker) Ridl. 1, A. Julius & A. Takano AT61 BORH, Sabah, DQ507833; P. strobilifera (Baker) Ridl. 2, ¯ , Sabah, DQ507849; P. strobilifera (Baker) Ridl. #3, S. Sakai 361 KYO, Sarawak, AB097252; P. parva complex, A. Julius & A. Takano AT65 SAN, HYO, Sabah, DQ507841; P. viridisepala Julius & A. Takano, A. Julius 198 SAN, HYO, Sabah, DQ507838; P. species 3, Cultivated. Sandakan, Sepilok, RDC, Evo. Trail, Sabah, DQ507836; P. odorata C. K. Lim, Kress #99-6330 US, Thailand, AF478772; P. species #1, Kress #00-6745US, Sabah, AF478773; P. aff. albiflora, Khaw Siok Hooi 745 KEP & E, Peninsular Malaysia, AY769840 P. aff. megacarpa, A. Julius et al., ATS2 BORH, Sabah, DQ507845; P. aff. breviramosa complex, A. Julius & A. Takano AT2 BORH, Sabah, DQ507831. 72 PRELIMINARY MOLECULAR PHYLOGENY OF BORNEAN PLAGIOSTACHYS GmbH, Germany). Automated sequencing was conducted using ABI Prism® BigDyeTM Terminator Ready Cycle Sequencing kits on an Applied Biosystems HITACHI 3100 Genetic Analyzer Automated Sequencer, using both the PCR primers and another two internal primers, ITS2K (5’-GGCACAACTTGCGTTCAAAG-3’) (Rangsiruji et al., 2000) and ITS3P (5’GCATCGATGAAGAACGTA-3’) (Möller & Cronk, 1997). Phylogenetic Analysis Following the published sequence of the 5.8S rDNA gene and the ITS region in P. glandulosa (AB097251), sequence boundaries of 5.8S rDNA gene and both ITS1 and ITS2 regions of the 22 taxa yielded in this study were determined. The aligned matrix was then submitted to the GenBank with accession number from DQ507828 to DQ507849. Clustal X version 1.8 (Thompson et al., 1997) was used for multiple alignment of complete sequences with default settings. Nucleotide composition and G+C content were analyzed using MEGA Ver.3.0 (Kumar et al., 2004). Phylogenetic analysis was performed using PAUP* Version 4.0b8 (Swofford, 2001). Characters were left unordered and equally weighted. Maximum parsimony (MP) analysis of the ITS sequence data was conducted using heuristic search methods (10 Random Addition Replicates) with Tree Bisection Reconnection (TBR) branch swapping to find the most parsimonious trees, COLLAPSE option in effect, MULTREES and steepest descent options were not in effect. In order to evaluate the relative support of the clades, bootstrap analysis was executed using 1000 replicates heuristic with TBR. RESULTS Phylogenetic Analysis Alignment of the sequences yielded a data matrix of 640 total characters, of which 260 were phylogenetically informative. The complete ITS sequences of Plagiostachys varied in length from 542 to 574 bp data matrix (without coded gap). The length of ITS1 ranged from 159 to 164 bp with a GC content of 55.6%, the 5.8S ranged from 183 to 186 bp and GC of 50.1%, while that of ITS2 was greater and ranged from 198 to 226 bp with GC content of 58.6%. The strict consensus of 100 equally parsimonious trees with accompanying bootstrap values were given in Figure 1 (length = 1094; CI = 0.482; RC = 0.389). The homoplasy index (HI) of the data was 0.518. As shown in Figure 2, Plagiostachys made a strongly supported clade (BS = 96%) with some Alpinia species of Smith’s (1990) section Alpinia subsections Cenolophon and Paniculatae. The Plagiostachys can be further subdivided into three major subclades (A, B and C) with moderate to strong support (BS > 70%). Subclade A composed of species found only in Borneo and moderately supported with 76% bootstrap value. Three small groups of species can be found within this first subclade: (i) P. lasiophylla, P. megacarpa Julius & A. Takano, P. aff. megacarpa, P. oblanceolata, P. roseiflora Julius & A. Takano, Plagiostachys sp. 3 (BS = 61%), (ii) three replicates of P. strobilifera (BS = 64%), and (iii) P. parva, P. parva complex and Plagiostachys sp. 2 (BS = 91%). Thirteen taxa of Plagiostachys formed the moderatesupported subclade B with 72% bootstrap value. Species consists within this second subclade can be found in Borneo, Malay Peninsula and Thailand. Three small groups of species are found in Plagiostachys subclade B: i) P. breviramosa complex and P. aff. breviramosa (BS = 78%), ii) P. aff. albiflora and Plagiostachys odorata C. K. Lim (BS=76%), and iii) P. albiflora Ridl., P. brevicalcarata Julius & A. Takano, P. glandulosa S. Sakai & Nagam., P. longicaudata Julius & A. Takano, P. mucida Holttum and Plagiostachys sp. 4 (BS = 75%). The third well-supported subclade C composed of two species, P. crocydocalyx (K. Schum.) B. L. Burtt & R. M. Sm. and P. viridisepala Julius & A. Takano, which are only found in Borneo (BS = 99%). AVELINAH JULIUS et al. 73 Figure 1: Strict consensus tree of 100 equally parsimonious trees with emphasis on the Plagiostachys resulting from the ITS sequence data (length = 1094; CI = 0.483 excluding informative characters; HI=0.517) showing bootstrap values from the parsimony analysis (above the line if > 50 %) (Abbreviation: ITS = Internal Transcribed Spacer; CI = Consistency Index; HI = Heuristic Index) 74 PRELIMINARY MOLECULAR PHYLOGENY OF BORNEAN PLAGIOSTACHYS Figure 2: The Plagiostachys + some species of Alpinia clade resulting from MP analysis (see Fig. 1). The clade contains three subclades of Plagiostachys (subclades A, B and C) and few species of Alpinia from section Alpinia. Bootstrap values for MP is shown above the line (if > 50 %) (Abbreviation: Alp. = Alpinia; Plg. = Plagiostachys) AVELINAH JULIUS et al. 75 MORPHOLOGICAL STUDY DISCUSSION The status of vegetative and floral characters examined was summarized in Table 3. In each character, it is stable within species. Only one species, P. albiflora matched with Smith’s criteria in all morphological status, however, the rest of the species showed mixed character status of groups 1 and 2 as in P. breviramosa and P. parva. Phylogenetic Position of Plagiostachys and its Relationship with Related Genera The present ITS analysis focused on phylogenetic position of Plagiostachys showed that the species of the genus are divided into three major subclades A, B and C with 76%, 72% and 99% bootstrap supports respectively. These subclades consist of strongly supported clade with Alpinia nieuwenhuizii Valeton and A. ligulata K. Schum. (BS = 98%) + A. rubricaulis K. Schum., A. warburgii K. Schum. and A. argentea B. L. Burtt & R. M. Sm (BS = 54%) + A. hansenii R. M. Sm. and A. havilandii K. Schum. (BS = 85%). Our result is basically congruent with Kress et al. (2002, 2005 & 2007), since most of the members of the clade are that of A. glabra clade of Kress et al. (2005), together with A. hansenii and A. havilandii, the newly analyzed taxa. The reason why these two Alpinia were added was because both species have lateral inflorescence as in Plagiostachys. It is interesting both Alpinia also become sisters taxa to Plagiostachys, since it might indicate that the event having lateral inflorescence had happened only in the Plagiostachys + some species of Alpinia clade. However, other Alpinia species in this clade have a terminal inflorescence, and as shown in Figure 2, subclades within the Plagiostachys + some species of Alpinia clade are unresolved, so the phylogenetic relationships among these subclades of Plagiostachys’s and Alpinia’s remain unknown. Therefore, we could not discuss the evolution of lateral inflorescence further. At least we could mention that the species of Plagiostachys and Alpinia do not mix up with each other in these subclades. By adding more data such as extending the taxon sampling on both Plagiostachys and Alpinia, and employing more than one gene markers as others did (e.g. ITS and trnL-F by Ngamriabsakul et al., 2004; ITS and rps16 by Pedersen, 2004; ITS and matK by Xia et al., Figure 3 shows the distribution of morphological character status which was used by Smith (1985) for informal groupings of Plagiostachys. As suggested from this study, Plagiostachys is subdivided into three major subclades (A, B and C) with moderate to strong support (BS > 70%), and each character used by Smith was scattered into these three subclades: not mucilaginous inflorescence was found in the species of subclade A and part of subclade B, and mucilaginous status was found in part of subclade B and subclade C. Both character status of ligule (bilobed vs. truncate), of bracteole (distinctly tubular and early decaying vs. tubular at base or open and persistent), of style (adnate to vs. free from the corolla wall), and of capsule (oblong-ovoid or pyriform vs. globose) are also found in subclades A and B. Instead, the hairiness of capsules seems to be useful character: all species bearing glabrous capsules were gathered in the subclade B, and species with pubescent capsules were in the subclades A and C. Therefore, the combination of those inflorescence and hairiness of capsules could be used to distinguish the three subclades: the species of subclade A has not mucilaginous inflorescence status and pubescent capsules, those of subclade B show not – or mucilaginous inflorescence but glabrous capsules, and those of subclade C has mucilaginous inflorescence but pubescent capsules. 76 Table 3: Comparison of some keys morphological characters for Bornean Plagiostachys PRELIMINARY MOLECULAR PHYLOGENY OF BORNEAN PLAGIOSTACHYS Table 3 Continues: AVELINAH JULIUS et al. 77 78 PRELIMINARY MOLECULAR PHYLOGENY OF BORNEAN PLAGIOSTACHYS 2004), we could obtain more resolved tree and answer how we should treat Plagiostachys in the near future. At the moment, the possibility of monophyly of Plagiostachys is still remain, therefore we suggest to leave Plagiostachys as an independent genus. Evaluation of Smith’s Informal Grouping within Bornean Plagiostachys Our examination of morphological characters used by Smith’s informal grouping (Tables 1 & 3) revealed that only one species could completely satisfy her criteria. Additionally, the molecular phylogenetic analysis showed that Plagiostachys is divided into three subclades with moderate to strong support and not correspond to previous informal grouping (Fig. 3). Therefore, we conclude that Smith’s grouping should no longer be used for Bornean Plagiostachys as Cowley (1999) and Sakai & Nagamasu (2003) suggested. Evaluation of the Morphological Characters Used for Classification in Plagiostachys In molecular phylogenetic analysis, we found three subclades in Plagiostachys: subclades A, B and C (Fig. 2), and among morphological characters examined, the status of ligule, bracteole, floral colour and calyx were scattered into these subclades (Fig. 3). This indicates these characters are useful for species recognition but less significant for infrageneric grouping. On the contrary, combination of those inflorescence (mucilaginous vs. not-mucilaginous) and hairiness of capsules (pubescent vs. glabrous) could be used to recognize the three subclades. Smith (1985) used the shape of the capsule to distinguish between groups 1 and 2, but did not mention the hairiness of capsules. However, as inflorescence character, also it could be a useful character for classification. ACKNOWLEDGEMENTS We thank Januarius Gobilik (Forest Research Centre, Sandakan, Sabah) for providing materials of P. lasiophylla and Plagiostachys sp. 3, Prof. Dr Menno Schilthuizen (National Museum of Natural History ‘Naturalis’, Leiden), Dr Takuji Tachi (Hokkaido University), Mr Liew Thor Seng (UMS), Mrs Lam Nyee Fan (UMS), Mr Freddy Disuk (UMS), Dr Suzan Benedict (UMS) and Dr Nazirah Mustafa (UMS) for technical assistance. We acknowledge Dr Hidetoshi Nagamasu for providing invaluable comments on the manuscript. Part of this study was based on the Master’s thesis of Avelinah Julius, which was submitted to Universiti Malaysia Sabah. REFERENCES Cowley, J. 1999. Two new species of Plagiostachys (Zingiberaceae) from Borneo. Kew Bulletin. 54: 139 – 146. Doyle, J. J. and J. L. Doyle. 1987. A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochemical Bulletin. 19: 11 – 15. Gobilik, J., A. Lamb and M. Y. Mashitah. 2005. Two new species of Plagiostachys (Zingiberaceae) from Sabah, Borneo. Sandakania. 16: 49 – 56. Kress, W. J., L. M. Prince and K. J. Williams. 2002. The phylogeny and a new classification of the gingers (Zingiberaceae): Evidence from molecular and morphological data. American Journal of Botany. 89: 1682 – 1696. Kress, W. J., A. Z. Liu, M. F. Newman and Q. J. Li. 2005. The molecular phylogeny of Alpinia (Zingiberaceae): A complex and polyphyletic genus of gingers. 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JOURNAL OF TROPICAL BIOLOGY AND CONSERVATION, 4 (1) : 81 – 97, 2008 81 Research Article Bats (chiropteran) reported with Aspergillus species from Kubah National Park, Sarawak, Malaysia JAYA SEELAN Sathiya Seelan1, Faisal Ali ANWARALI KHAN2, SEPIAH Muid3, M.T. ABDULLAH4 1 Institute for Tropical Biology and Conservation, Locked bag 2073, Universiti Malaysia Sabah, 88999 Kota Kinabalu, Sabah, Malaysia 2 Department of Biological Sciences, Texas Tech University, Lubbock, Texas 79409-3131, USA 3 Department of Plant Science and Environmental Ecology Department of Zoology, Faculty of Resource Science and Technology, 94300 Kota Samarahan, Sarawak, Universiti Malaysia Sarawak, Malaysia 4 ABSTRACT A preliminary survey of chiropterans (bats) with potential zoonotic fungi was conducted as part of the Sowell-UNIMAS Expedition 2006. This survey was conducted at Kubah National Park, Matang, Sarawak from 14th to 16th August 2006. The main aim of this survey was to document variety of fungal isolates from bats external (ears) and internal (saliva and anal) swabs. All of the fungi species were subjected to both macroscopic and microscopic observations to characterize their morphology. Out of 23 species of bats observed, 13 (56.5%) species were found to contain 17 fungi isolates of the genus Aspergillus from five subgenera, five sections and six species. The fungi isolates were Aspergillus restrictus, A. sydowii, A. fumigatus, A. niger, A. clavatus and A. japonicus. The highest numbers of isolates recorded was for A. restrictus with six isolates followed by A. fumigatus and A. sydowii with two isolates respectively. Where as, A. niger, A. clavatus and A. japonicus each recorded with one isolate only. Aspergillus fumigatus was the Keywords: Aspergillus, bats, pathogenic, thermophilic first record isolated from bats the samples (n = 64) from Sarawak. It was reported that this isolate is a pathogenic and thermophilic (able to grow up to 65°C) isolate which was found to be on a lesion near ear opening of Hipposideros cervinus. Further work should be done to discover potential mycoflora in wildlife mammals. INTRODUCTION Wildlife has been an important vector of infectious diseases as they can transmit these diseases to human through direct or indirect contact. Today, zoonoses found in wildlife constitute a major public health problem, affecting all continents. Wild animals seem to be involved in the epidemiology of most zoonoses and serve as major reservoirs for transmission of zoonotic agents to domestic animals and humans (Frederick, 1998; Hilde et al., 2004). The importance of such zoonoses is increasingly being recognized, and the needs for more attention in this area have been widely expressed (Hilde et al., 2004; Chomel et al., 82 CHIROPTERAN RECORDED WITH ASPERGILLUS SPP. FROM KUBAH NATIONAL PARK, SARAWAK 2007). Recent studies showed that wildlife diseases were expanding in geographic range, transferred from one host species to another, increased in impact or severity, undergone a change in pathogenesis, and might also have emerged by recently evolved pathogens (Lederberg et al., 1992; Krause, 1992; Krause, 1994; Daszak et al., 2000). Most of the outbreak of new viruses and emergence of newly evolved pathogens are known mainly from wildlife population (Morse, 1993; Dobson & Foufopoulos, 2001; Antia et al., 2003). region (Raper & Fennell, 1977). Aspergillus fumigatus is the most important group of fungi as a cause of systemic human and animal diseases (Raper & Fennell, 1965; 1977). Since Aspergillus species can be found on many different substrates, they have been extensively studied from animal dung, lungs, ears, intestinal, blood vessels, kidney, bladder, brain and skin for pathogenic strains that leads to fungal infections on wild animals (Ainsworth, 1952). Among wildlife population, several studies have been documented different pathogenic fungi from different hosts (Coon & Locke, 1968; Trevino, 1972; Kaliner & Cooper, 1973; Tham & Purcell, 1974; Ramirez et al., 1976; Peden & Richard, 1985; Speare et al., 1994; Mancianti et al., 1997; Cork et al., 1999; Monteros et al., 1999; Leotta et al., 2002). Fungi are distributed worldwide, with particular species being endemic in particular regions. The species are grouped by natural environment habitat as being primarily associated with humans (anthrophilic), other animals (zoophilic), or soil (geophilic) (Brandt & Warnock, 2003). Zoosporic fungi are one of the key areas around these issues that are currently receiving more attention with regards to the wildlife diseases and yet to be explored as other charismatic pathogens (e.g. virus, bacteria and protozoan). Worldwide distribution of some common wild animal fungal diseases such as Aspergillosis, Chytridiomycosis, Coccidioimycosis, Cephalosporiosis and Otomycosis have the potential to be a major threat to human being as they starts to be transmitted from animal to human (Gitter & Austwick, 1962). Previous cases of fungal infections in wild animals have caused inflammatory lesions in the brains, subcutaneous infections, urinary tract infections, otitis, infraocular infections and genital infections (Halloran, 1955; Conen et al., 1962). For example, chytridiomycosis has caused near extinction of some amphibians (Dendrobates tinctorius) in Australia and other parts of the world (Ells et al., 2003). Bats have been shown to be both important recidence and vectors of pathogens. Some of the pathogens that have been recently reported to be associated with this fauna were rabies (Paez et al., 2003), European lyssavirus (Fooks et al., 2002), Hendra (Halpin et al., 2000) and Menangle (Bowden et al., 2001) in Australia, Nipah and Tioman viruses in Malaysia (Chua et al., 2002a and b), hantaviruses in Korea (Kim et al., 1994) and etc. (Chua et al., 2005). With respect to fungal pathogens, insectivorous bats are known to be the prime contenders as reservoirs of fungi such as Histoplasma capsulatum, Coccidioides immitis, Cryptococcus laurentii and Blastomyces dermatitidis (Yamamoto et al., 1995; GarciaHermoso et al., 1997; Mattsson et al., 1999; Bunnell et al., 2000). Besides from becoming contagious to human, these diseases also have resulted in mass mortalities, population declines, and even extinctions in such wildlife population (Wobeser, 1994). Fungal species in wild animals (from samples of tissues, saliva and anal swab) such as A. fumigatus, A. terreus, A. restrictus, A. versicolour and A. glaucus were the common fungi that have been isolated from temperate Viewing such a condition is important for both human and wildlife, the present study has been initiated in order to screen for pathogenic strains of Aspergillus residing in bats of Borneo Island. This genus is known to be commonly JAYA SEELAN SATHIYA SEELAN et.al. 83 distributed in the environment as well as pathogenic (Raper & Fennell, 1965; Klich, 2001). ectoparasites from some specimens were preserved in 75% ethanol. MATERIALS AND METHODS Bats were sampled in Kubah National Park, Sarawak, Malaysian Borneo (01°36' 42.3"N 110° 26' 39.3"E – elevation 8-35 m) from 14th to 16th August 2006. The study area was mainly covered with mixed dipterocarp forest with a small stream flowing through this park from Mt. Serapi. Anal, ear and saliva swabs were performed using sterile cotton buds and inoculated into screw-capped centrifuge tubes containing 900 μl of PBS buffer to prevent drying. Samples were serially diluted 10-fold up to 10–5. Of the 10–3 to 10–5 dilution, 0.1 ml of aliquots were spread on sabouroud’s agar plates. Three replicates were prepared for each dilution and incubated at 25°C and 37°C for five days. After five days, the mycelia were transferred into selective media for fungal identification. Sampling Method Fungi Identification Ten mist-nets and four harp traps were set in each night. Nets and traps were deployed at night from 6.00 p.m. and were closed at 7.00 a.m. the following day. Nets were checked every 20 minutes during the first 6 hours. Harp traps are much more independent, rarely any bat caught in the pouch can escape and they are not tangled (nor stressed), so these traps were checked at least three times each night, so as to make sure the animals were fine. Bats were also sampled using scoop nets inside roosts (like culverts). The fungi isolates were grown on five different media i.e., Czapek Yeast Extract Agar incubated at 25°C (CYA25), CYA37 incubated at 37°C, CY20S added with 20% sucrose incubated at 25°C, Czapek’s agar (CZ) and Malt Extract Agar (MEA). For each culture, five plates were used as replicates were made. Each plate was inoculated at three points, equidistant from the centre and incubated in the dark for seven days. The strains were identified using current universal identification keys described by Raper & Fennell (1965) and Klich (2002). All the samples were identified to species in the field following the identification keys from Payne et al. (1998); Corbet & Hill, (1992); Kingston et al. (2006); and Khan (1986). A maximum of five individuals per species were taken as voucher specimens. An extra of another three individual were collected for the species, which is identified to have different morphological attributes within the population. Samples were then tagged and field standard measurements were recorded. All specimens were prepared as museum voucher specimens, either as skin and skeletal or as fluid preserved specimen. Tissue samples from liver and muscle were preserved in lysis buffer (Longmire et al., 1997) and ethanol vials, blood samples were collected using Nobuto blood filter strips and Microscopic Observation Study Area Microslide culture technique was used to observe the micromorphological features of the Aspergillus species. A small tuft of mycelium and conidiophores were lifted from a young section of the colony, placed in a drop of alcohol on a microscope slide and gently teased out. A drop of lactophenol blue or acid fuschin was used as a stain. The appearance of foot cell, conidiophores, presence of metulae (sterigmata) and conidia were examined and measurements were recorded. Images were taken using digital camera. 84 CHIROPTERAN RECORDED WITH ASPERGILLUS SPP. FROM KUBAH NATIONAL PARK, SARAWAK RESULTS Thirteen species from a total of 23 species of bats caught were found to host 17 Aspergillus isolates. Isolates were identified to five subgenera, five sections and six species. The isolates were identified as A. restrictus, A. sydowii, A. fumigatus, A. niger, A. clavatus and A. japonicus (Figures 1– 6 ). Aspergillus restrictus was recorded with the highest number of isolates (six isolates), followed by A. fumigatus (two isolates) and A. sydowii (two isolates) and A. niger, A. japonicus and A. clavatus were recorded with lowest number of isolates (one each) (Table 1). Fungal infection was observed near the ear opening of a single insectivorous bat, Hiposideros cervinus. This fungus was incubated at 37°C and was confirmed that this infection was due to the A. fumigatus. Morphological characteristics of all the six species isolated from the bats are described. Table 1: Total number of Aspergillus species isolated from anal, ear and saliva of the bats Family Host Species Name Pteropodidae Cynopterus brachyotis C. brachyotis C. brachyotis C. brachyotis C. brachyotis C. brachyotis C. brachyotis Penthetor lucasi P. lucasi P. lucasi Balionycteris maculata Hipposideridae Hipposideros cervinus H. cervinus H. cervinus H. cervinus H. cervinus** H. cervinus H. cervinus Rhinophidae Rhinolopus sedulous R. trifoliatus Rhinolopus borneensis Vespertilionidae Myotis muricola Glischropus tylopus Fungal Species Source A. restrictus A. restrictus A. restrictus A. restrictus – – A. sydowii A. restrictus A. clavatus A. fumigatus A. sydowii Anal Anal Ears Ears – – A. restrictus – A. fumigatus – – Ears Anal Anal Ears Ears, anal Anal Ears, anal, saliva No. of No. of Isolates Isolates 1 1 1 1 0 0 1 1 1 1 2 0 0 1 0 4 0 0 A. japonicus – – Anal 1 0 0 A. niger – Ears 1 0 **Detected with fungal infection; – is negative JAYA SEELAN SATHIYA SEELAN et.al. Aspergillus japonicus Saito Subgenus: Circumdati Section: Nigri Colony on Czapek’s yeast extract agar (CYA) 60 – 75 mm in diameter (7 days, 25°C), conidial heads on this media was very dark brown to purple brown or purple black; mycelium white to yellowish; no sclerotia was observed; reverse dull brown to purple brown; no exudates present; colonies velutinous to slightly floccose, plane to radially sulcate. On CYA37, the colony diameter was 40 – 50 mm in diameter (7 days, 37°C); reverse brown to black, yellow to brown soluble pigment present; slow growth colony and radially sulcate. On CY20S, colony was rapidly growing and no soluble pigment was observed. On MEA, this isolate can grow about 70 – 80 mm in diameter (7 days, 25°C); conidial heads was brownish black; mycelium yellow in colour. No growth at 5°C and this isolate can grow moderately at 45°C. Conidial heads were radiate; stipes 400 – 600 μm, smooth-walled, uncoloured. Vesicles 15 – 25 μm wide, globose shaped, uniseriate; Phialides (4.5 – 7) × (3 – 4) μm, covering the upper half of the vesicle. Conidia were globose to subglobose, occasionally ellipsoidal, measuring (3 – 4) × (4 – 5) μm, surface echinulate. This isolate produces black spinose conidia (Figure 1, pg. 88). Aspergillus niger Tiegh Subgenus: Circumdati Section: Nigri Colony on Czapek’s yeast extract agar (CYA) 57 – 58 mm in diameter (7 days, 25°C), wrinkled, dense and velutinous, exudates present, white at first and becomes dark brown with forming of conidial heads, reverse dark yellow. Colony on malt extract agar (MEA) 52 – 56 mm in diameter (7 days, 25°C) similar to those on CYA but less dense and conidia in duller colours, reverse dirty yellow. On Czapek’s, morphological characters were similar to those on MEA. No 85 growth at 5°C. Growth at 37°C is exceptionally rapid, colonies on CYA 38 – 40 mm in diameter in three days. This strain can grow at 45°C. Conidial apparatus develops as erect conidiophores. Tips of conidiophores enlarge and form vesicles with many phialides producing conidia in long chains. Conidial heads are compactly columnar, 40 – 48 μm in diameter, black. Conidiophores are unbranched, smooth and dark brown, stipes 200 – 300 μm × 3 – 4 μm in size. Vesicles are round to globose shaped, 20 – 30 μm in diameter. Phialides crowded dark brown, 5 – 7 μm long. Conidia are globose to subglobose, roughened, hyaline and often decidous spinules when young and verruculose when it matures (Figure 2, pg. 88). Aspergillus sydowii (Bain. & Sart.) Thom and Church Subgenus: Nidulantes Section: Versicolores Colony on Czapek’s yeast extract agar (CYA) 20 – 40 mm in diameter (7 days, 25°C), heavily sporulating in dark turquoise to dark green colours, mycelium white, forming white conidial heads, reverse reddish brown to maroon in colour; exudates reddish brown to dark brown when present; soluble pigment was maroon on CYA; colony dense, velutinous to lanose, radially sulcate. Colony on malt extracts agar (MEA) 30 – 40 mm in diameter (7 days, 25°C); conidia on MEA was dark greenish after seven days; mycelium white; colony texture granular and plane. Colony on CY20S was similar to colonies on CYA except exudates usually not formed and texture was more floccose. Colony on CY37 was less dense and the conidial colours less intense. Colony on Czapek’s agar growing 30 – 40 mm with close textured and velvety with crowded conidiophores. No growth at 5°C. Growth at 37°C is moderate. This strain cannot grow at 45°C. Conidial apparatus develops as erect conidiophores. Conidial heads are radiate, 100 86 CHIROPTERAN RECORDED WITH ASPERGILLUS SPP. FROM KUBAH NATIONAL PARK, SARAWAK – 150 μm in diameter, and white in colour. Stipes (200 – 30) μm × (3 – 7) μm smooth, thick-walled colourless, expanding into spathulate vesicles. Vesicles are hyaline, radiate to spathulate shaped, 6 – 15 μm in width; usually sterigmata in two series (biseriate), metulae (4 – 5) × (2 – 3) μm in diameter, phialides (5 – 7) × (2 – 3) μm. Diminutive conidial structures produced by this isolate, looks like penicillate heads. Conidia are spherical, very rough to spinose, 3 – 4 μm in diameter. Hulle cells present in this isolate (Figure 3, pg. 88). Aspergillus restrictus G. Smith Subgenus: Aspergillus Section: Restricti Colony on Czapek’s yeast extract agar (CYA) 4 – 8 mm in diameter (7 days, 25°C), Conidia on CYA25 dull green to grey green; mycelium white or inconspicuous; reverse uncoloured to brown; exudates absent; colonies velutinous, centrally floccose. Colony on malt extract agar (MEA) 3 – 6 mm in diameter (7 days, 25°C); conidia on MEA was dark greenish after seven days; mycelium white; reverse uncoloured to pale tan colour; irregular margin. Conidia on CY20S, dark green, mycelium inconspicuous, reverse uncoloured, colony very slow growth, dense and plane. Colony on Czapek’s agar growing 3 – 5 mm; conidia dark green; mycelium inconspicuous, slow growth and less sporulation. No growth at 5°C. Growth at 37°C is very slow. This strain cannot grow at 45°C. Conidial heads are columnar; conidiophores up to (100 – 200) × (4 – 7) μm, smooth and colourless, stipes (200 – 30) μm × (3 – 7) μm smooth, uncoloured, expanding into pyriform or hemispherical vesicles. Vesicles 8 – 18 μm in wide; uniseriate to biseriate. Phialides (6 – 10) × (2 – 3) μm in diameter. Conidia are variable, often cylindrical when borne, at maturity ellipsoidal or pyriform, rough walled, (4 – 6) × (2 – 3) μm. (Figure 4, pg. 88). Aspergillus fumigatus Fresenius Subgenus: Fumigati Section: Fumigati Colony diameter on CYA attaining about 50 – 75 mm (7 days at 25°C); conidia on this media was dark blue greenish; mycelium white; exudates absent; reverse uncoloured; soluble pigment absent; texture floccose; heavy sporulation. On MEA, colony growth was about 50 – 60 mm (7 days at 25°C); conidial colour was dark bluish green; reverse uncoloured; texture as on CYA25. On CY20S and Cz, the colony colour was similar as in CYA25. Colony on CYA37 was exceptionally rapid, heavy sporulation; conidia colour was greyish green. This isolate cannot grow at 5°C and able to grow until 65°C. Conidial heads was columnar; conidiophores uncoloured, smooth-walled (200 – 350) × (6 – 10) μm, pyriform to spathulate vesicles. Vesicles 15 – 28 μm in diameter; uniseriate; phialides (5 – 7) × (2 – 3) μm, all phialides are parallel to each other and the conidiophore axis. Conidia globose to broadly ellipsoidal, smooth to finely roughned, 2 – 2.5 μm in diameter (Figure 5, pg. 89). Aspergillus clavatus Desm Subgenus: Clavati Section: Clavati Colony on CYA (7 days at 25°C) was 40 – 45 mm; conidia dull green, dark turquoise or green; mycelium white, inconspicuous to floccose; exudates absent; reverse dull yellow to orange brown in colour; colonies dense, radially furrowed. Yellow soluble pigment present. On MEA, colony attaining about 40 – 50 mm in diameter (7 days at 25°C); conidia were dull green to grey green in colour, irregularly distributed; dark yellow soluble pigment present; mycelium white, inconspicuous; colony thin and low except for conidial areas more floccose. On CY20S and CZ colonies were similar as those on CYA 25. Colony on CYA (7 days at 37°C) was JAYA SEELAN SATHIYA SEELAN et.al. very slow, conidia less abundant. This isolate cannot grow at 5°C and colony growth was moderate at 37°C. Conidial heads radiate, splitting into columns when matured; conidiophores rose up to (1000 – 2000) × (15 – 30) μm, smooth-walled, colourless, expanding slowly into clavate a b 87 vesicles. Vesicles 50 – 70 μm wide, smaller vesicles, conidia zone extended from 30 – 175 μm down from the apices of the vesicles; uniseriate, phialides (8 – 11) × (2 – 3) μm. Conidia smooth-walled, ellipsoidal, occasionally pyriform, almost cylindrical, (3 – 5) × (3 – 3.5) μm (Figure 6, pg. 89). c d Figure 1: (a – b) Colonies on CYA at 25°C; 37°C; (c) Biseriate conidial head; (d) Conidia a b c d Figure 2: (a – b) Colony on CYA at 25°C; 37°C; (c) Biseriate conidial head; (d) Conidia a b c d Figure 3: (a – b) Colony on CYA at 25°C; colony on MEA at 37°C; (c) Conidial head; (d) Hulle cells a b c d Figure 4: (a) Colony on CYA at 25°C; (b) Colony on MEA at 25°C; (c) Conidial head; (d) Biseriate conidial head 88 CHIROPTERAN RECORDED WITH ASPERGILLUS SPP. FROM KUBAH NATIONAL PARK, SARAWAK a d b c e f Figure 5: (a – b) Colony on CYA at 25°C; 37°C; (c) Conidial heads columnar; (d – e) Uniseriate conidial head; (f) Conidia shape globose a d b c e Figure 6: (a) Colony on MEA at 25°C; (b) Colony on CYA at 25°C; (c) Conidia shape ellipsoidal; (d – e) Uniseriate conidial head JAYA SEELAN SATHIYA SEELAN et.al. DISCUSSIONS In this preliminary study, six species of Aspergillus were isolated from 13 species of bats. As few studies have been conducted on mycoflora from wild animals, all the Aspergillus species recorded in this study were presumed to be first record for this genus found in bats at least in Sarawak, Borneo. Previous studies done by Kuthubutheen & Webster (1986) have isolated coprophilous fungi from the bats, samba deer and elephants dung in the natural environment. Furthermore, Candida lusitaniae and Debaryomyces hansenii were isolated from bat guano (Takashi et al., 2005). Several pathogenic fungi from different bats species were reported from Brazilian Amazon. In the search of Paracoccidioides from the bats’ viscera, Silva-Vergara et al. (2005) have also documented other types of mycoflora such as Candida krusei, Trichosporum sp., Scytalidium sp., and one unidentified yeastlike fungus from liver, spleen and lungs of frugivorus bats (Carollia perspicillata and Sturnira lilium), Glossophaga soricina (nectarivorous bats) and Desmodus rotundus (hematophagous bat) respectively. In another study by Koilraj et al. (1999) on the distribution of Aspergillus in caves soil from India, documented 13 different species of Aspergillus such as A. niger, A. japonicus, A. flavus, A. versicolour, A. tamarii, A. sydowii, A. chevalieri, A. ochraceous, A. parasiticus, A. fumigatus, A. terreus, A. wentii and Aspergillus sp. Besides that, a study done by Moraes et al. (2001), have proved that arthopod vectors like Culex and Aedes have became as carrier for the Aspergillus species like A. niger, A. flavus, A. nidulans, A. fischerianus and A. heteromorphus. Hence, the transmission of the fungal spores in bats may be due to the mosquitoes bites in their habitat where they live in. Although our sample size is not really large to conclude statistically in which swab location 89 (ear, saliva or anal) contains the highest number of Aspergillus species, but this preliminary data showed that the most diversity of this fungus were observed in anal swabs of frugivorous bats. Thus, this indicates that various types of substrates such as anal, ears, saliva and feaces (guano) results different types of mycoflora in the wild animal population. The high number of fungal isolates documented in frugivorous bats compared to insectivorous bats also does show some correlation on food sources and their roosting site with the number of fungus isolated in this study. Based on the morphological examinations, some colony and microscopic characteristics of the Aspergillus species were found to be different from those stated by Raper & Fennell (1965) and Klich (2002). For example, the colony diameter of A. restrictus on CYA was smaller. It was determined that the colony diameter of A. restrictus ranged between 4.0 – 8.0 mm on CYA and the diameter of the vesicles varied up to 8 – 18μm. The most distinguishing property of A. clavatus, dull green or grey green conidial heads on MEA as stated by Raper & Fennel (1965) was observed in this strain. At the same time, a strong yellow soluble pigment present on this media was another important new characteristic that was observed in this study probably might be a different strain. Moreover, there was a similar morphological characteristics were observed in A. japonicus, A. niger, A. sydowii and A. fumigatus as described by Raper & Fennell (1965), Samson & Pitt (1990), Klich (2002). However, a pathogenic strain of A. fumigatus that was isolated from the Hipposideros cervinus showed thermophilic properties as these isolates able to survive under a wide range of temperature (25 – 65°C). According to Gilman (1959), A. fumigatus strains can grow rapidly up to 35 – 60°C. This study showed that the A. fumigatus isolated from Hipposideros cervinus could grow up to 65°C. 90 CHIROPTERAN RECORDED WITH ASPERGILLUS SPP. FROM KUBAH NATIONAL PARK, SARAWAK In Borneo, the most widespread species of the genus Aspergillus are A. niger Tieghem, A. flavus Link, A. fumigatus Fres, A. ochraceus Wilhelm, A. terreus Thom and A. wentii Wehmer (personal communication). These isolates have been isolated from different types of soil, plants (fresh and senescent leaves), fruits, leaf litters, water samples, food products, indoor and outdoor environments. Thus, Aspergillus could also be isolated from wild animal population because it is thought that these species are more adapted to the prevailing ecological conditions (Sepiah, 1985; Jaya Seelan & Sepiah, 2006). This study provides a comparative analysis on Aspergillus species available in the chiropterans samples from Kubah National Park might be due to climatic agents such as flood and air or wind which can help to introduce fungal spores and mycelium into the cave environment. Besides that, fungal spores might also enter into cave through organic substances such as plant which are carried into the cave by trogloxenes (Cubbon, 1970). Since bats are widely distributed in the cave environment, fungal spores might cause infection for bats when they are exposed or even live as symbionts. Yamamoto et al. (1995) investigated that the bat guano may mediate the exchange of pathogenic fungi just as pigeon excreta mediate the exchange of Cryptococcus neoformans, the causal agent of cryptococcosis. Apart from that, fruits consumed by the frugivore bats are also important factor in understanding the ecology of bats. Sometimes the infected fruit may contain pathogenic microorganisms that present during the fruit decay process (Sepiah, 1985). So, this would be a key factor how the fungi are transmitted to bats since frugivorous bats consume fruits as their main diet. CONCLUSION This study has provided a preliminary list of Aspergillus species found on chiropterans. There were six species of Aspergillus successfully isolated from the 13 species of bats. This study has documented the diversity of Aspergillus species in bats while understanding the macro and microscopic characteristic of this fungus cultured in different media sources. Pathogenic strains of microorganisms could be studied in order to understand their host relationship and also ecological significance in the wild animal population in Malaysia. In general, this preliminary analysis provides novel and basic information on potential sources of mycoflora from the wild animals in Borneo. Malaysian bats may contain several novel fungi species and may be of significant mycological interest. Further study is needed in order to conserve wild animals from emerging infectious diseases. ACKNOWLEDGEMENTS Authors would like to thank Universiti Malaysia Sarawak (UNIMAS) and Texas Tech University (TTU) for giving the opportunity to participate in Sowell-UNIMAS Expedition 2006. The authors are also grateful to Prof. Maren Klich of the United States Agricultural Department (USDA) and Prof. Jens Frisvad Denmark Technical University (DTU) for providing information on the Aspergillus species identification. 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JOURNAL OF TROPICAL BIOLOGY AND CONSERVATION, 4 (1) : 99 – 107, 2008 Short Notes Rapid assessment on the abundance of bird species utilising the Kota Kinabalu Wetland Centre mangroves Andy Russel MOJIOL1, AFFENDY Hassan1, Jocelyn MALUDA2 and Suzen IMMIT3 1 School of International Tropical Forestry, Universiti Malaysia Sabah, 88999 Kota Kinabalu, Sabah 2 Kota Kinabalu Wetland Centre, Off Jalan Bukit Bendera Upper, 88400 Likas, Kota Kinabalu, Sabah 3 Institute for Tropical Biology and Conservation, Universiti Malaysia Sabah, 88999 Kota Kinabalu, Sabah ABSTRACT INTRODUCTION Kota Kinabalu Wetland Centre (KKWC) mangroves have an essential role as a green ecosystem in Kota Kinabalu. The aim of this study was to assess the usefulness of mangrove areas as a site for birdlife by estimating the number of bird species and family, and the population density of bird species. The most frequent bird groups found in KK Wetland Centre were waders (14.70%) followed by herons, storks and bitterns (12.59%), raptors (8.15%) and bulbuls (7.41%). The population density of bird found in KKWC was between 12 – 17 birds/km2. The result shows an estimated population of 3526 individuals from 83 species of birds covering an area of 24 ha. As a conclusion, this area is important as an urban bird habitat in Kota Kinabalu. Conservation of adequate and contiguous suitable mangrove habitat may provide a sanctuary for bird to live and feed between their territories. Ecological improvements of green mangrove ecosystem could be of immediate benefit to the bird population. Swamps, marshes and other wetlands that were once regarded as useless to agricultural and industrial development are now recognized for their great values in recycling chemical and biological materials, and especially for their rich biological diversity. Wetlands filter pollutants, act as reservoirs of nutrients in food chains, produce forage for domestic animals and fuel for humans, provide aesthetics, recreational and cultural benefits to society and are habitats for thousands of unique species of plants and animals (Eric et al., 2000). Keywords: Bird checklist, mangrove environment, birdlife area, conservation and population density The mangrove area is one type of wetlands and in Sabah it consisted of 322,349 hectares which most of them have been constituted as Mangrove Forest Reserve (Sabah Forestry Department, 2003). The ecological importance of mangrove areas can hardly be overestimated as they form the feeding and nursery grounds for many species of birds and other invertebrate species. Mangrove vegetation protects the coastal areas from erosion and acts as a buffer zone against tidal currents, floods and storms. 100 ABUNDANCE OF BIRD SPECIES UTILISING THE KOTA KINABALU WETLAND CENTRE In wetland areas, birds are expected to be an important resource as tourist attraction. Certain species of birds are fully dependent on the mangrove for their habitat and food. Birds play important roles in maintaining wetlands ecosystem which include being pollinators, seed dispersers, pollution regulators providing food for other animal predators, and also contribute in nutrient recycling processes. Birds are closely related to the habitat conditions. Each species rarely occurs in only one type of habitat. They are completely dependent on their habitat, for cover and rich food resources. Habitat type, size of the area, plant community structure and landscape pattern can have a great effect on bird community structure in a given habitat (Wijesekara, 1999). observation was made using a pair of binocular (10 × 50). Each individual bird or groups of birds seen or heard would be identified on the spot using bird checklist book of Borneo (Mackinnon & Phillipps, 1993). This point count method used to record a variety of birds that provides a uniform way of counting birds over time or across locations. Point counts are a standardized method (Ralph et al., 1993) of assessing the diversity and abundance of birds by counting (detected by hearing and by sight) at points (Knapp & Keeley, 2001). In large areas, allocated point counts can be used as representative samples for the area. Point counts are visited over a period of several days or longer to assess how many and what types of birds are found in an area. The aim of this study was to conduct rapid assessment on the density and abundance of bird species utilising the Kota Kinabalu Wetland Centre (KKWC) mangrove area. A total of 32 sampling points were established for bird survey in KKWC. Each point was selected by considering/ marking every 100 metres walk from the provided transect (boardwalk). At each point, the count was last exactly five minutes. Then, waiting around 2 – 4 minutes at each point before counting. MATERIALS AND METHODS Secondary data were obtained from literature, books and scientific reports available from World Wildlife Fund (WWF-Kota Kinabalu) and Sabah Wildlife Department. Secondly are from field survey and observation as a complement and confirmation to the mechanisms. For this study, the chosen location is the mangrove areas in KKWC which is located two kilometres northeast of Kota Kinabalu City centre. This location was chosen due to the large diversity of birds and in addition, it is a suitable location for tourist attraction. KKWC, which covers an area of 24 hectares, is the only remaining patch of once an extensive mangrove forest existed in much of the area in the coastal town of Kota Kinabalu (Fig. 1). Seven days were spent in the field from 14th to 20th November 2005. Point count method had been carried out and species of birds was identified through their vocalization from 6 a.m. to 11 a.m. and 4.30 p.m. to 6.30 p.m. The Every bird species observed was recorded between distances from the 10 – metre intervals out to 100 metres. All individuals of all species detected were counted, and a bird seen first was distinguished from birds heard first. Horizontal distance of the bird relative to the survey point and the distance from above the ground were recorded (Fig. 2). The abundance of bird was analyzed using distance sampling following Buckland et al. (2001). RESULTS AND DISCUSSIONS The total of bird species recorded in KKWC during the survey were 83 species from 31 families and 60 genera (Appendix 1). The group category was based from Clements (1991). The highest abundance of bird group/class observed was heron, storks and bitterns (10.4%), followed by waders (8.9%), pigeons, doves and parrots (5.2%) and kingfishers (3.7%). This group of ANDY RUSSEL MOJIOL et al. 101 Figure 1: Location of Kota Kinabalu Wetland Centre Source: Mapping Department Malaysia, 1998 102 ABUNDANCE OF BIRD SPECIES UTILISING THE KOTA KINABALU WETLAND CENTRE Figure 2: Detailed point count plot for bird survey birds, as exemplified by Purple Heron (Ardea purpurea), Little Egret (Egretta garzetta), Common Greenshank (Tringa nebularia), Sandpiper (Actitis hypoleucos) and Cinnamon Bittern (Ixobrychus cinnamomeus) that fed on small fishes and crustaceans. The pigeon, doves and parrots are usually seen above the mangrove canopy that feed the mangrove flower of Sonneratia alba, Avicennia alba and Lumnitzera racemosa. While the kingfishers such as the Common Kingfisher (Alcedo atthis), Blueeared Kingfisher (Alcedo meninting) and Collared Kingfisher (Halcyon chloris) are usually associated within seasides or river mouths and become predator for small fishs and mudskippers (Periophthalmodon schlosseri). The largest bird family recorded from the study was Ardeidae (13 species) followed by Scolopacidae (9 species), Columbidae (7 species), Alcedinidae (5 species), and Nectariniidae (5 species). The most common bird family found in KKWC is Ardeidae which consists of herons, storks and bitterns which usually easy to be spotted flying in the mangrove mud and coastal areas. Sometimes this bird is known as 'Bangau Air' by the local. Most of the birds observed in KKWC are resident bird with 66% from the total of overall birds surveyed, whereas migratory bird consists of 32% and 2% includes for both resident and migratory bird. Resident bird means, the bird is breeding and stay in the same area or location throughout the year and does not migrate. From ANDY RUSSEL MOJIOL et al. 103 the distance sampling analysis, the estimated population density of birds in KKWC was 14.11 individuals/km2. Its density lies in between a range of 11.53 – 17.25 birds/km2, within 95% confidence interval. The total population of birds was 3526 individuals in an area of about 24 hectares (Table 1). Two assumptions are essential for reliable estimation of density from point transect sampling are; (1) bird directly on the point are always detected at their initial location, prior to any movement in responsive to the observer. (2) Distances are measured accurately or objects are correctly counted in the proper distance interval. In this survey, rare species that were difficult to be spotted belong to woodpeckers, wablers (Tailorbird and Snipe), and sunbird and spiderhunter, while the remotes detected birds are raptors. Sometimes they were spotted flying a distance of 75 m in the sky and only could be identified using binoculars. Generally, the detection function decreases with increasing distance (Buckland et al., 1993). This was correct in this survey when using point count method, where the detection of bird decrease at the distance of 75 m (Fig. 3). Table 1: Population density and abundance of birds in KKWC D (Density) N (Abundance) Estimate %CV df 95% Confidence Interval 14.105 3526.0 10.26 10.26 461 461 11.534 2884.0 17.248 4312.0 1,953 1,7577 1,5824 Detection Probability 1,3671 1,1718 0,9765 0,7812 0,5859 0,3906 0,1953 0 0 10 20 30 40 50 60 70 80 Perpendicular distance in metres Figure 3: Detection probability of all birds recorded perpendicular to distance using point count method in KKWC 104 ABUNDANCE OF BIRD SPECIES UTILISING THE KOTA KINABALU WETLAND CENTRE Sampling error also influence the detection probability, that not all individuals bird species could be detected in the investigated areas, due to numerous variables such as the observer's visual acuity, hearing ability, and experience, the length of time spent at a station, the season of the year, the time of the day, wind, temperature, and other weather conditions, the habitat features and the bird's reproductive status and behaviour. These variables affected the detection function and the occurrence of birds in each survey (a) Natural areas which are currently rich in birdlife and may act as population reservoirs for birds. Adequate protection of these reservoirs may provide a sanctuary for residence and migratory birds. (b) Improvement of vegetated corridors along mangrove areas, swamp areas and green spaces would be of immediate benefit to the bird habitat. These corridors may provide cover, shelter, water, food and space for those birds to move between habitats. CONCLUSIONAND RECOMMENDATIONS ACKNOWLEDGEMENT Kota Kinabalu Wetland Centre mangroves can be considered as one of the most important habitats for birds. Most of the recorded bird species belong to the family of Ardeidae (13 species), Scolopacidae (9 species), Columbidae (7 species), Alcedinidae (5 species) and Nectariniidae (5 species) respectively. This area is also an important habitat for kingfishers which eat small fishes (Mudskipper; Periophthalmodon schlosseri), crustaceans (Mud Lobster; Thalassina anomala) and small aquatic invertebrates, like the Common Kingfisher (Alcedo atthis), Blue-eared Kingfisher (Alcedo meninting) and Collared Kingfisher (Halcyon chloris) they can usually be observed near the mangrove fringe and river mouths. Herons, Bitterns and Storks belong to the Ardeidae family and which usually easy to be spotted flying in the mangrove mud. Most of the birds observed in KKWC are resident birds with 66% of the total overall bird's survey; whereas migratory bird consists of 32%. An estimated population of 3,526 individuals in 24 hectares is considered very high. As recommendations, the presence of birdlife in KKWC environment is a testimony to the quality of the environment. It is an indicator that some balance between the natural and the built environment could be achieved. To enhance the birdlife, it would be necessary to consider a few particular types of bird areas, namely: The authors wish to thank to the management of Kota Kinabalu Wetland Centre, for the support and permission to conduct this study. REFERENCES Buckland, S. T., D. R. Anderson, K. P. Burnham and J. L. Laake. 1993. Distance Sampling: Estimating Abundance of Biological Populations. London: Chapman and Hall. pp 446. Buckland, S. T., D. R. Anderson, K. P. Burnham, J. L. Laake, D. L. Borchers and L. Thomas. 2001. Introduction to Distance Sampling. USA: Oxford University Press. Clements, J. 1991. Birds of the World: A Check List. (4th Ed.).Vista, California: Ibis Publ. Eric, J., Y. Yabi and H. L. Carsten. 2000. A report on the State of the Environment in Sabah, 2000. State Environmental Conservation Department, Sabah. Paper presented at the Environmental Convention, Kuching, Sarawak. 29 – 30 June 2000. Knapp, E. and J. Keeley. 2001. A National Study of the Consequences of Fire and Fire Surrogate Treatments. Sequoia National Park Site Study Plan. Mackinnon, J. and K. Phillipps. 1993. A Field Guide to the Birds of Borneo, Sumatra, Java and Bali: The Greater Sunda Islands. Oxford University Press. ANDY RUSSEL MOJIOL et al. Ralph, C. J., G. R. Geupel, P. Pyle, T. E. Martin and D. F. DeSante. 1993. Handbook of field method for monitoring land birds. General Technical Report PSW-GTR-144. Pacific Southwest Research Station, Forest Service, US Department of Agriculture, Albany, California. Sabah Forestry Department. 2003. Sabah Forestry Department, Annual Report 2003. Sabah Forestry Department. 105 Wijesekara, V. P. 1999. Birds as bio-indicators to assess biotope quality in different land use systems. Case Study in Wet Zone of Sri Lanka. Agricultural University of Norway, Kotagama S. W., University of Colombo. 106 ABUNDANCE OF BIRD SPECIES UTILISING THE KOTA KINABALU WETLAND CENTRE Appendix 1: Taxonomic list of bird species recorded at Kota Kinabalu Wetland Centre Family Species Ardeidae Ardeidae Ardeidae Ardeidae Ardeidae Ardeidae Ardeidae Ardeidae Ardeidae Ardeidae Ardeidae Ardeidae Ardeidae Ciconiidae Charadriidae Charadriidae Scolopacidae Scolopacidae Scolopacidae Scolopacidae Scolopacidae Scolopacidae Scolopacidae Scolopacidae Scolopacidae Recurvirostridae Alcedinidae Alcedinidae Alcedinidae Alcedinidae Alcedinidae Meropidae Pandionidae Accipitridae Accipitridae Accipitridae Rallidae Rallidae Rallidae Columbidae Columbidae Columbidae Columbidae Columbidae Columbidae Columbidae Cuculidae Cuculidae Cuculidae Caprimulgidae Apodidae Apodidae Ardea purpurea Ardea cinerea Nycticorax caledonicus Nycticorax nycticorax Egretta intermedia Egretta eulophotes Egretta sacra Egretta alba Egretta garzetta Butorides striatus Ixobrychus sinensis Ixobrychus cinnamomeus Gorsachius melanolophus Leptoptilos javanicus Pluvialis fulva Charadrius dubius Tringa tetanus Tringa glareola Tringa nebularia Tringa stagnatilis Actitis hypoleucos Xenus cinereus Tringa brevipes Gallinago megala Gallinago sp. Himantopus himantopus Alcedo atthis Alcedo meninting Halcyon chloris Halcyon pileata Pelargopsis capensis Merops viridis Pandion haliaetus Haliaeetus leucogaster Haliastur indus Spilornis cheela Rallus striatus Amaurornis phoenicurus Gallinula chloropus Chalcophaps indica Columba livia Ducula aenea Geopelia striata Streptopelia chinensis Treron olax Treron vernans Cacomantis merulinus Centropus bengalensis Centropus sinensis Caprimulgus macrurus Apus affinis Collocalia esculenta Observed No. 2 1 3 2 6 8 2 4 5 1 1 1 2 1 1 1 12 15 4 4 2 1 1 1 1 2 1 1 1 1 1 1 1 1 1 1 2 1 1 1 1 1 3 3 2 1 1 2 2 1 5 2 Estimated No. Protection Status* 1–5 1–5 1–5 1–5 10 – 20 10 – 20 1–5 5 – 10 5 – 10 1-5 1–5 1–5 1–5 1–5 1–5 1–5 10 – 20 10 – 20 5 – 10 5 – 10 1–5 1–5 1–5 1–5 1–5 1–5 1–5 1–5 1–5 1–5 1–5 1–5 1–5 1–5 1–5 1–5 1–5 1–5 1–5 1–5 1–5 1–5 1–5 1–5 1–5 1–5 1–5 1–5 1–5 1–5 1–5 1–5 P, I P, I P P P, I P, VU, I P, I P, I P, I P, I P P P P, VU I P, I I P, I P, I I I I P, I III I I I I I - ANDY RUSSEL MOJIOL et al. 107 Family Species Observed No. Picidae Hirundinidae Hirundinidae Artamidae Campephagidae Aegithinidae Aegithinidae Irenidae Pycnonotidae Pycnonotidae Pycnonotidae Pycnonotidae Muscicapidae Timaliidae Sylviidae Sylviidae Sylviidae Cisticolidae Corvidae Laniidae Sturnidae Motacillidae Sturnidae Nectariniidae Nectariniidae Nectariniidae Nectariniidae Nectariniidae Estrildidae Estrildidae Passeridae Picoides moluccensis Hirundo rustica Hirundo tahitica Artamus leucorhynchus Lalage nigra Aegithina tiphia Aegithina viridissima Chloropsis sonnerati Pycnonotus goiavier Pycnonotus plumosus Pycnonotus brunneus Pycnonotus zeylanicus Copsychus saularis Trichastoma bicolor Megalurus palustris Orthotomus sericeus Orthotomus ruficeps Prinia flaviventris Rhipidura javanica Lanius cristatus Aplonis panayensis Anthus rufulus Sturnus sinensis Anthreptes malacensis Hypogramma hypogrammicum Nectarinia jugularis Arachnothera longirostra Prionochilus percussus Lonchura fuscans Lonchura malacca Passer montanus 1 6 5 2 1 1 1 1 3 2 2 3 1 1 1 1 1 1 1 1 1 1 1 1 2 3 1 1 2 2 2 Estimated No. Protection Status* 1 5 5 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 – – – – – – – – – – – – – – – – – – – – – – – – – – – – – – – 5 10 10 5 5 5 5 5 5 5 5 5 5 5 5 5 5 5 5 5 5 5 5 5 5 5 5 5 5 5 5 I I I I II I I I - *Notes: (P) – Protected under Schedule 2, Part 1, Section 25(2) protected animals under Wildlife Conservation Enactment 1997, Sabah: (NT) - Near Threatened; (VU) – Vulnerable; Species are classified under IUCN Red Data List, 2006: Appendix I (CITES) - species threatened with extinction. Trade in specimens of these species is permitted only in exceptional circumstances Appendix II (CITES) - species not necessarily threatened with extinction, but in which trade must be controlled in order to avoid utilization incompatible with their survival Appendix III (CITES) - contains species that are protected in at least one country, which asked other CITES Parties for assistance in controlling the trade. (CITES = Convention on International Trade in Endangered Species of Wild Flora and Fauna) JOURNAL OF TROPICAL BIOLOGY AND CONSERVATION, 4 (1) : 109 – 113, 2008 Short Communication A preliminary study on the morphometrics of the Bornean Elephant NURZHAFARINA Othman1,2, MARYATI Mohamed1, Abdul Hamid AHMAD1, Senthivel NATHAN3, Heather Thomas PIERSON2 and Benoit GOOSSENS1,2 1 Institute for Tropical Biology and Conservation (ITBC), Universiti Malaysia Sabah, Locked Bag No. 2073, 88999 Kota Kinabalu, Sabah, Malaysia 2 Cardiff University, PO Box 915, Cathays Park, Cardiff CF10 3TL, Wales UK 3 Sabah Wildlife Department, 5th Floor, B Block, Wisma MUIS, 88100 Kota Kinabalu, Sabah, Malaysia ABSTRACT This is the first morphometric study on the Bornean subspecies of the Asian elephant (Elephas maximus borneensis). The morphological measurements of captive E. m. borneensis in Sabah were taken and compared to those of the captive elephants (E. m. indicus) in Peninsula Malaysia in an attempt to see if there were any morphological differences. No significant differences were found in the selected measurements between Bornean elephants and Peninsula Malaysia elephants (ANCOVA, r > 0.05). Results indicated that there is positive relationship between age and the selected morphometric measurements. INTRODUCTION The Asiatic elephant is a widely distributed species covering much of South Asia in the west to Indochina in the east and a larger part of Southeast Asia including Peninsular Malaysia, Sumatra and Borneo. Some populations are distinguishable through morphological characters such as the colour of Keywords: Bornean measurements elephant, morphometric skin, pigmentation and sometimes by the characteristics veins in the ears (Kurt & Kumarasinghe, 1998). Sometimes, different populations prefer to live in certain habitats. These differences accounted for the recognition of different subspecies. Three are currently recognized i.e Elephas maximus indicus (Indian elephant), E. m. maximus (Sri Lankan elephant) and E. m. sumatrensis (Sumatran elephant) (Sukumar, 1989; Sukumar et al., 1991; Fleischer et al., 2001). The main reason on why the Bornean elephant is categorized under Indian or Sumatran sub-species was because the inadequacy of the original descriptions of the Bornean conspecific in terms of the morphological characters and sample size (Fernando et al, 2003). Although a number of morphometric studies on Asian elephant were done and published (Wemmer & Krishnamurthy, 1992; Daniel, 1998; Othman, 1990; Othman, 2003) there was no morphometric study carried out to differentiate the sub-species. The Bornean elephant, the newly classified sub-species, is believed to be the smallest in size and observed to have larger ears, longer tails, straighter tusks and a more rounded body (Fernando et al., 2003). The subspecies, however, was classified based on genetic analysis by Fernando et al. (2003) 110 despite the known historical accounts of its origin (De Silva, 1968; Ibbotson, 2003; Shim, 2003). A morphological study is desirable to confirm a distinct group of organism (Hawksworth, 1995), which prompted this study. MATERIALS AND METHODS The Captive Populations External morphological measurements of fifteen captive elephants from Peninsular Malaysia were made from April to May 2005 at Malacca Zoo and at Kuala Gandah Elephant Conservation Centre in Pahang. Measurements of six elephants from Sabah were taken at the Lok Kawi Zoological and Botanical Park from July 2005 to January 2006. Measurements were made on selected characters as follows: (a) ear length (EL), (b) ear width (EW), (c) tail length (TL) and (d) chest girth (CG), using a tailor’s tape (Butterfly; 150 cm) and a longer measuring tape (Tricle; 30 m/100 feet) depending on the characters measured (Figure 1). The measurements were repeated three times for each elephant and averaged. Data were analyzed using the Analysis Covariance (ANCOVA) carried out via SPSS version 12.0 (SPSS Inc, Chicago). Elephants are known to grow throughout life and age is an important factor determining their morphological characteristics (Koehl, 1996; Daniel, 1998; Reilly, 2002). Since the sample size was small (Sabah population, n = 6, West Malaysia population, n = 15), we used ANCOVA to control for the age factor in both populations. RESULTS Based on the ANCOVA and controlling for age (Figure 2), there was no significant difference in any of the characters between the two captive populations (p>0.05). However there was a significant relationship between age and each variable (p<0.05), stressing the important influence of age on the morphology of elephants. THE MORPHOMETRICS OF THE BORNEAN ELEPHANT DISCUSSION Morphology is the basic method to classify species but measurements on exceptionally large wild animals are difficult to make. Consequently, most studies were done based on cranial measurements or dental characteristics of museum specimens or fossils (du Toit et al., 1987; Hillis, 1987). Unfortunately, even when using preserved material the most common problem still concerns inadequate data for reliable statistical analysis, a problem especially true for specimens of exceedingly large animals. The physical characteristics of Bornean elephant as being smaller and different in certain characters were not confirmed in this study. The measurements to be tested were not available elsewhere for the Bornean elephant and our data provide the only measurements on those characteristics. Obviously, the confirmation would require many sets of data from many individuals representing all age classes. In some circumstances, such measurements can be done on many animals prior to translocation programs or when the animals are using grassland or opened forests. Othman (2003) analyzed morphometric data from wild elephant gathered over a ten-year translocation program (1993 to 2003) in Peninsular Malaysia. Similarly, Daniel (1998) conducted a five year study on the growth of the Indian elephant and measured them every year on the same dates and replicated each measurement four times. In Borneo, such extensive replication is impossible because of the scattered elephant populations, the typically impregnable forest habitat and the tiny number of individuals in captivity. The importance of morphological analysis is so crucial until Fernando et al. (2003) suggested that a formal reinstatement of the E. m. borneensis taxa await a detailed morphological analysis of Bornean elephants and their comparison with other populations. NURZHAFARINA OTHMAN et al. 111 Figure 1: The external morphological measurement of each variable in cm (EL = ear width, EL = ear length, TL = tail length, CG = chest girth) The drawings are not to scale Measurements definition Ear width : From the starts of the ear to the widest point of the ear Ear length : The upper end of the ear to the lowest point of the ear Tail length : The tail along its entire length and measure at the end of the last vertebra (not including the hair) Chest girth : Measured immediately behind the forelegs by wrapping the tape around the torso 112 THE MORPHOMETRICS OF THE BORNEAN ELEPHANT Figure 2: Interactive scatter plot graphs that showed the linear relationship between each variable and age while the tables below showed the ANCOVA’s results NURZHAFARINA OTHMAN et al. ACKNOWLEDGEMENTS We thank the Sabah Wildlife Department and Malacca Zoo for allowing us to collect data on captive elephants. We are indebted to Jubius Dausip and the team, Ahmad Tajuddin Ali, Dr. Symphorosa Sipangkul, Norsham Mohd Noor and the team and also Nasaruddin Othman for their kind assistance during the data collection. We also thank David Bignell for reviewing an earlier version of this manuscript. REFERENCES Daniel, J. C. 1998. The Asian Elephant: A Natural History. Dehradun: Natraj Publishers. De Silva, S. G. 1968. Elephants of Sabah. Sabah Society Journal. III(4): 169 – 181. Du Toit, F. R., J. T. Foose and M. H. D. Cumming. 1987. The existing basis for subspecies classification of black and white rhinos. Pachyderm No. 9. International Union for Conservation of Nature and Natural Resources. Nairobi. Fernando, P., T. N. C. Vidya, J. Payne, M. Stuewe, G. Davison, R. J. Alfred, P. Andau, E. Bosi, A. Kilbourn and D. J. Melnick. 2003. DNA analysis indicates that Asian elephants are native to Borneo and are therefore a high priority for conservation. Public Library of Science Biology. 1: 1 – 6. Fleisher, C. R., K. Muralidharan, A. E. Perry, E. E. Steven and M. C. Wemmer. 2001. Phylogeography of the Asian Elephant (Elephas maximus) based on mitochondrial DNA. Evolution. 55(9): 1882 – 1892. Hawksworth, D. I. 1995. Biodiversity Measurement and Estimation. London: The Royal Society. Hillis, M. D. 1987. Molecular versus morphological approaches to systematic. Annual Review of Ecology, Evolution and Systematics. 18: 23 – 42. 113 Ibbotson, R. 2003. Domesticated elephants in Borneo. Sabah Society Journal. 20: 1 – 6. Koehl, R. A. M. 1996. When does morphology matter? Annual Review of Ecology, Evolution and Systematics. 27: 501 – 542. Kurt, F. and J. c. Kumarasinghe. 1998. Remarks on body growth and phenotypes in Asian elephant Elephas maximus. Acta Theriologica. 5 (Supply): 135 – 153. Othman, N. 2003. Kajian Penggunaan Ukuran Tapak kaki bagi Menjangkakan Berat, Kelas Umur dan Jantina Gajah Asia (Elephas maximus) di Semenanjung Malaysia. BSc thesis. Universiti Kebangsaan Malaysia. (Unpublished). Kuala Lumpur. Othman, S. 1990. Biometric relationship of elephant measurements. The Journal of Wildlife and Parks. IX: 125 – 131. Reilly, J. 2002. Growth in the Sumatran elephant (Elephas maximus sumatranus) and age estimation based on dung diameter. Journal of Zoology London. 258: 205 – 213. Shim, P. S. 2003. Another look at the Borneo elephant. Sabah Society Journal. 20: 7 – 14. Sukumar, R. 1989. The Asian Elephant: Ecology and Management. Cambridge: Cambridge University Press. Sukumar, R., D. L. Alwis, J. Barnett, L. K. D. Choudhury, P. C. Lee, A. Luxmoore and J. Shoshant. 1991. The Illustrated Encyclopedia of Elephants. New York: Salamander Books Ltd. Wemmer, C. and V. Krishnamurty. 1992. The Asian Elephant: Ecology, Biology, Diseases, Cinservation and Management. Kerala Agri. JOURNAL OF TROPICAL BIOLOGY AND CONSERVATION, 4 (1) : 115 – 120, 2008 Checklist A preliminary survey on the butterfly fauna of Sungai Imbak Forest Reserve, a remote area at the centre of Sabah, Malaysia Mohd. Fairus JALIL¹,2, Hairul Hafiz MAHSOL¹,2, Nordin WAHID² and Abdul Hamid AHMAD¹,2 ¹ Centre for Primate Studies Borneo, Institute for Tropical Biology & Conservation, Universiti Malaysia Sabah, 88999 Kota Kinabalu, Sabah, Malaysia ²Institute for Tropical Biology & Conservation, Universiti Malaysia Sabah, 88999 Kota Kinabalu, Sabah, Malaysia ABSTRACT This paper reports result from a study to document the composition and distribution of butterflies in the Imbak Valley region of the Sungai Imbak Forest Reserve. One hundred and seventy four species (18.6%) of butterflies with six endemic species were recorded from the area. Results also showed that Imbak Valley is valuable for conservation purposes based on its unique butterfly fauna. INTRODUCTION The current rate of species extinction and habitat modification is increasing alarmingly. During the last decades, many of the forested areas are logged, cleared or converted into plantation (Groombridge, 1992; Padoch & Peluso, 1996; John, 1997; Laurance & Bierregaard, 1997). Among the remaining primary forest left are the Sungai Imbak Forest Reserve which consist of several virgin jungle reserve (VJR) located at the centre of Sabah. On the 8th of June 2000, Imbak Valley Scientific Expedition was hosted by the Forestry Department of Sabah, during this one-month Keywords: Butterfly, Imbak, Sabah expedition, flora and fauna were censuses and documented. During this expedition, the butterfly research group of the Institute for Tropical Biology and Conservation, UMS carried out a 14-day surveyed of butterfly fauna within the valley. Objectives of the survey were to document the butterfly fauna of the area and then mapped the data obtained into the WorldMap IV program (Mahadimenakbar, 1999). METHODS Butterfly were surveyed using all available methods that include trapping, netting and transect methods (DeVries, 1987; Upton, 1991). Trapping was carried out using fruit baited traps. Netting was carried out along the ridges, river and other suitable areas. Transect methods were carried out only by experienced staff to ensure reliability of identification. Sweep netting were also carried out at low bushes to chase out crepuscular and resting butterflies. Butterfly were surveyed at the transit camp, logging road leading to base camp, hilltop area near the base camp, forest adjacent to the base camp and along the river. The checklist of butterfly species recorded from Imbak Valley (5° 7’N; 117° 3’E) is presented in a systematic order, arranged by family, 116 BUTTERFLIES OF SUNGAI IMBAK FOREST RESERVE subfamily and genera (Appendix 1). For taxonomy and nomenclature, we follow recent classification and standard reference works by Eliot (1992), Maruyama & Otsuka (1992) and Otsuka (1988). RESULTS AND DISCUSSION A total of 174 species of butterflies from five families, Papilionidae, Pieridae, Nymphalidae, Lycaenida and Hesperiidae were recorded from the survey (Table 1). The majority of the species collected were from the family of Pieridae, Papilionidae and Nymphalidae which contribute about 90%. Lycaenidae and Hesperiidae contribute less that 10% of the total figure even though both are the largest and second largest family in Borneo. Comparison of Different Microhabitats Among all the sites, hilltop area is the most interesting area, which observed many rare and endemic species. The wet seepage area at the hilltop is also an excellent place where many Pierids and Papilionids were found congregating in moderate number. The regenerating forest between transit camp and base camp was not explored thoroughly, it was generally poor in species, though not necessarily in numbers of individuals. Graphium sarpedon, G. doson, Eurema spp. and Catopsilia pomona were characteristic species. DISCUSSION Looking at the hilltop, most of the species found were characteristic of canopy with many species that are usually rare and only occasionally found at the lower level. It was interesting to note that Imbak Valley has four representative of Bornean birdwing namely, Troides brookiana, Troides amphrysus, T. helena and T. andromache. Troides andromache was observed only at the forestcovered hilltop near the base camp with exception of two sighting of females flying above the waterfall. A single female T. helena was captured while nectaring at flowering bushes at the logging road towards the base camp, others were observed nectaring and flying near the hill top. The most common species of Troides notable for this expedition were T. amphrysus and T. brookiana. General Composition Conservation Overall the species collected were characteristic of lowland forest with several representative from the mid to highland forest. Most of the species collected however showed a very low frequency of butterflies. Nevertheless several endemic species and many rare species were collected during the study. Most of the family was well represented except for Lycaenidae and Hesperiidae, each with less than 10% species collected. Even though the number of endemic species in Imbak Valley is low, some of the species observed here were considered rare and endangered. Some species collected were already included in the list of protected fauna of Malaysia (Anon., 1991). With many species found in the area are listed in the list of protected species of Malaysia, Imbak Valley is indeed valuable in conservation of butterfly fauna. Table 1: Percentage of butterfly recorded in Imbak Valley compared to the total number of species recorded in Borneo FAMILY BORNEO IMBAK % Papilionidae Pieridae Nymphalidae Lycaenidae Hesperiidae 44 42 241 394 214 21 26 110 15 2 47.7% 61.9% 45.6% 3.8% 0.9% TOTAL 935 174 18.6% MOHD. FAIRUS JALIL et al. ACKNOWLEDGEMENTS We would like to thank the Forestry Department of Sabah and Forest Research Centre for inviting us to participate in the expedition. We wish to acknowledge the kind assistance of the organizing committee of Imbak Valley Scientific Expedition 2000 who helped with all the logistics and transportation during the study. We also would like to acknowledge the kind assistance of Jacqueline, P.K. for painstakingly spreading all the butterflies from Imbak Valley. This research was partially funded by Universiti Malaysia Sabah through the Institute for Tropical Biology and Conservation. REFERENCES Anon. 1991. Laws of Malaysia: Act A337 – Protection of Wildlife 1972 (Amendment) 1976, PU(A)306/91. Kuala Lumpur: Percetakan Nasional Malaysia Berhad. De Vries, P. J. 1987. The butterflies of Costa Rica and their Natural History. Vol. 1. New Jersey: Princeton University Press. Eliot, J. N. (Ed.). 1992. The Butterflies of Malays Peninsula. (4th Ed.). Malayan Nature Society. Malaysia. Kuala Lumpur. Groombridge, B. (Ed.). 1992. Global biodiversity: Status of the earth’s living resources. London: Chapman & Hall. John, A. G. 1997. Timber production and biodiversity conservation I tropical rainforest. (2nd Ed.). United Kingdom: Cambridge University Press. 117 Laurance, W. F. and R. O. Bierregaard. 1997. Preface – A crisis in the making. In: Laurance W. F. and R. O Bierregaard (Eds.). Tropical forest remnants – ecology, management and conservation of fragmented communities. Chicago: Chicago University Press. Mahadimenakbar, M. D. 1999. Potential use of WorldMap for exploring aspect of spatial pattern in biological data: An introduction use on butterfly diversity assessment in Borneo. In: Hassan, S. T. S., I. Azhar, O. Dzolkhifli and A. S. Sajap. (Eds.). Entomology in Malaysia beyond 2000: Exploration, imploration and digitalization. Maruyama, K. and K. Otsuka. 1991. Butterflies of Borneo. Vol. 2, No. 2. Tokyo: Tobishima Corporation. Otsuka, K. 1988. Butterflies of Borneo. Vol. 1. Tokyo: Tobishima Corporation. Padoch, C. and N. L Peluso. 1996. Borneo people and forests in transition: An introduction. In: Padoc, C. and N. L. Peluso (Eds.). Borneo in transition: people, forests, conservation and development. Oxford University Press. Upton, M. S. 1991. Methods for collecting, preserving and studying insects and allied forms. Australian Entolomological Society. Miscellaneous Publication No. 3. (4th Ed.). Brisbane. Australia. 118 BUTTERFLIES OF SUNGAI IMBAK FOREST RESERVE Appendix 1: Distributional checklist of butterflies from the Imbak Valley region of Sungai Imbak Forest Reserve ‘*’ indicates the species is endemic to Borneo FAMILY PAPILIONIDAE Subfamily Papilioninae Atrophaneura nox (Swainson, [1822]) Graphium agamemnon (Linnaeus, 1758) Graphium antiphates (Cramer, [1775]) Graphium bathycles (Zinken, 1831) Graphium doson (Felder & Felder, 1864) Graphium evemon (Boisduval, 1836) Graphium procles Grose-Smith, 1887* Graphium sarpedon (Linnaeus, 1758) Pachliopta antiphus (Fabricius, 1793) Pachliopta neptunus (Guérin-Méneville, 1840) Papilio demoleus Linnaeus, 1758 Papilio demolion Cramer, [1776] Papilio helenus Linnaeus, 1758 Papilio memnon Linnaeus, 1758 Papilio nephelus Boisduval, [1836] Papilio palinurus Fabricius, 1787 Papilio polytes Linnaeus, 1758 Troides amphrysus (Cramer, [1779]) Troides andromache (Staudinger, 1892)* Troides brookiana (Wallace, [1856]) Troides helena (Linnaeus, 1758) FAMILYPIERIDAE Subfamily Pierinae Appias albina (Boisduval, 1836) Appias cardena (Hewitson, [1861]) Appias indra (Moore, 1857) Appias lyncida (Cramer, [1777]) Appias nero (Fabricius, 1793) Appias pandione (Geyer, 1832) Appias paulina (Cramer, [1777]) Cepora iudith (Fabricius, 1787) Cepora pactolicus Butler, 1865* Delias hyparete (Linnaeus, 1758) Hebomoia glaucippe (Linnaeus, 1758) Leptosia nina (Fabricius, 1793) Pareronia valeria (Cramer, [1776]) Phrissura cynis (Hewitson, 1866) Prioneris cornelia (Vollenhoeven, 1865)* Saletara panda (Godart, 1819) Subfamily Coliadinae Catopsilia pomona (Fabricius, 1775) Catopsilia pyranthe (Linnaeus, 1758) Dercas gobrias (Hewitson, 1864) Eurema ada (Distant & Pryer, 1887) Eurema hecabe (Linnaeus, 1758) Eurema lacteola (Distant, 1886) Eurema nicevillei (Butler, 1898) Eurema sari (Horsfield, [1829]) Eurema simulatrix (Semper, 1891) Gandaca harina (Horsfield, [1829]) FAMILYNYMPHALIDAE Subfamily Danainae Danaus chrysippus (Linnaeus, 1758) Danaus genutia (Cramer, [1779]) Euploea algea (Godart, 1819) Euploea camaralzeman Butler, 1866 Euploea crameri Lucas, 1853 Euploea eyndhovii Felder & Felder, [1865] Euploea leucostictos (Gmelin, [1790]) Euploea modesta Butler, 1866 Euploea mulciber (Cramer, 1777]) Euploea radamanthus (Fabricius, 1793) Euploea sylvester (Fabricius, 1793) Euploea tulliolus (Fabricius, 1793) Idea hypermnestra (Westwood, 1848) Idea stolii (Moore, 1883) Ideopsis gaura (Horsfield, [1829]) Ideopsis vulgaris (Butler, 1874) Parantica agleoides (Felder & Felder, 1860) Parantica aspasia (Fabricius, 1787) Parantica luzonensis (Felder & Felder, 1863) Tirumala septentrionis (Butler, 1874) MOHD. FAIRUS JALIL et al. Subfamily Satyrinae Elymnias dara Distant & Pryer, 1887 Elymnias nesaea (Linnaeus, 1764) Elymnias panthera (Fabricius, 1787) Erites argentina Butler, 1868 Erites elegans Butler, 1868 Lethe europa (Fabricius, 1775) Melanitis leda (Linnaeus, 1758) Melanitis zitenius (Herbst, 1796) Mycalesis amoena Druce, 1873* Mycalesis anapita Moore, [1858] Mycalesis fusca (Felder & Felder, 1860) Mycalesis horsfieldi Fruhstorfer, 1908 Mycalesis janardana Moore, [1858] Mycalesis kina Staudinger, 1892* Mycalesis oroatis Hewitson, [1864] Mycalesis orseis Hewitson, [1864] Neorina lowii (Doubleday, [1849]) Ragadia makuta (Horsfield, [1829]) Xanthotaenia busiris Westwood, [1858] Ypthima baldus (Fabricius, 1775) Ypthima pandocus Moore, [1858] Subfamily Morphinae Amathusia phidippus (Linnaeus, 1763) Amathuxidia amythaon (Doubleday, 1847) Discophora necho Felder & Felder, [1867] Discophora sondaica Boisduval, 1836 Faunis canens Hübner, [1826] Faunis stomphax (Westwood, 1858) Taenaris horsfieldii (Swainson, [1820]) Thaumantis klugius (Zinken, 1831) Thaumantis odona (Godart, [1824]) Thauria aliris (Westwood, [1858]) Zeuxidia amethystus Butler, 1865 Zeuxidia doubledayi Westwood, [1851] Subfamily Nymphalinae Amnosia decora Doubleday, [1849] Athyma kanwa Moore, 1858 Athyma larynma (Doubleday, [1848]) Athyma nefte (Cramer, [1779]) Athyma selenophora (Kollar, [1844]) 119 Bassarona dunya (Doubleday, [1848]) Bassarona teuta (Doubleday, [1848] Cethosia biblis (Drury, [1773]) Cethosia hypsea Doubleday, [1847] Chersonesia rahria (Moore, [1858]) Cirrochroa emalea (Guérin-Méneville, 1843) Cirrochroa malaya Felder & Felder, 1860 Cirrochroa tyche (Felder & Felder, 1861) Cupha erymanthis (Drury, [1773]) Cyrestis cocles (Fabricius, 1787) Cyrestis maenalis Erichson, 1834 Cyrestis nivea (Zinken, 1831) Doleschalia bisaltide Felder & Felder, 1860 Dophla evelina (Stoll, 1790) Euripus nyctelius (Doubleday, 1845) Euthalia monina (Fabricius, 1787) Hypolimnas anomala (Wallace, 1869) Hypolimnas bolina (Linnaeus, 1758) Junonia atlites (Linnaeus, 1763) Junonia hedonia (Linnaeus, 1764) Junonia iphita (Cramer, [1779]) Kallima limborgi Moore, [1879] Kaniska canace (Linnaeus, 1763) Laringa castelnaui (Felder & Felder, 1860) Lasippa tiga (Moore, 1858) Lebadea martha (Fabricius, 1787) Lexias canescens (Butler, [1869]) Lexias dirtea (Fabricius, 1793) Lexias pardalis (Moore, 1878) Moduza procris (Cramer, [1777]) Neptis clinia Moore, 1872 Neptis duryodana Moore, 1858 Neptis hylas (Linnaeus, 1758) Neptis nata Moore, 1857 Paduca fasciata (Felder & Felder, 1860) Pandita sinope Moore, [1858] Parthenos sylvia (Cramer, [1775]) Phalanta alcippe (Stol, 1782) Rhinopalpa polynice (Cramer, [1779]) Tanaecia clathrata (Vollenhoeven, 1862) Tanaecia iapis (Godart, [1824]) Terinos atlita (Fabricius, 1787) Terinos terpander Hewitson, 1862 Vindula dejone (Erichson, 1834) Vindula erota (Fabricius, 1793) 120 BUTTERFLIES OF SUNGAI IMBAK FOREST RESERVE Subfamily Charaxinae Subfamily Miletinae Agatasa calydonia (Hewitson, [1854]) Charaxes bernardus (Fabricius, 1793) Polyura athamas (Drury, [1773]) Polyura delphis (Doubleday, 1843) Polyura hebe (Butler, [1866]) Polyura schreiber (Godart, [1824]) Prothoe franck (Godart, [1824]) Logania malayica Distant, 1884 FAMILYLYCAENIDAE FAMILYHESPERIIDAE Subfamily Riodininae Subfamily Pyrginae Abisara saturata (Moore, 1878) Paralaxita damajanti (Felder & Felder, 1860) Paralaxita orphna (Boisduval, 1836) Paralaxita telesia (Hewitson, [1861]) Celaenorrhinus ficulnea (Hewitson, 1868) Subfamily Lycaeninae Amblypodia narada (Horsfield, [1828]) Arhopala epimuta (Moore, [1858]) Caleta elna (Hewitson, [1876]) Cheritra freja (Fabricius, 1793) Drupadia ravindra (Horsfield, [1828]) Loxura cassiopeia Distant, 1884 Udara placidula (Druce, 1895) Subfamily Curetinae Curetis santana (Moore, [1858]) Curetis sperthis (Felder & Felder, [1865]) Curetis tagalica (Felder & Felder, 1862) Subfamily Hesperiinae Koruthaialos rubecula (Plötz, 1882)

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