Journal of Indonesian Natural History [PDF]

Journal of

Indonesian Natural History

December 2014 Vol.2 No.2

Journal of Indonesian Natural History Editors Dr. Wilson Novarino

Dr. Carl Traeholt

Associate Professor for Biology Department of Biology University of Andalas, Indonesia

Programme Director, Southeast Asia Research and Conservation Division Copenhagen Zoo, Denmark

Email: [email protected]

Email: [email protected]

Editorial board Dr. Ardinis Arbain

Dr. Ramadhanil Pitopang

University of Andalas, Indonesia

Tadulako University, Indonesia

Indra Arinal

Dr. Lilik Budi Prasetyo

National Park Management, Department of Forestry Indonesia

Bogor Institute of Agriculture, Indonesia

Dr. Ahimsa Campos-Arceiz

Dr. Dewi Malia Prawiradilaga

Nottingham University Malaysia Campus, Malaysia

Indonesia Institute of Science, Indonesia

Dr. Mads Frost Bertelsen

Dr. Rizaldi

Research and Conservation Division, Copenhagen Zoo, Denmark

University of Andalas, Indonesia

Dr. Susan Cheyne

Dr. Dewi Imelda Roesma

Oxford University, Wildlife Research Unit, United Kingdom

University of Andalas, Indonesia

Bjorn Dahlen

Dr. Jeffrine Rovie Ryan

Green Harvest Environmental Sdn. Bhd, Malaysia

Wildlife Forensics Lab, Dept. of Wildlife and National Parks, Malaysia

Dr. Niel Furey

Boyd Simpson

Centre for Biodiversity Conservation, Royal University of Phnom Penh, Cambodia

Research and Conservation Division, Copenhagen Zoo, Denmark

Dr. Benoit Goossens

Robert B. Stuebing

Cardiff University, United Kingdom

Herpetology and Conservation Biology, Indonesia

Dr. Djoko Iskandar

Dr. Sunarto

Bandung Institute of Technology, Indonesia

Dr. Matthew Linkie

Fauna & Flora International, Singapore

Dr. Erik Meijaard

People and Nature Consulting International, Indonesia

Dr. John Payne Borneo Rhino Alliance, Malaysia

WWF-Indonesia

Dr. Jatna Supriatna University of Indonesia

Dr. Campbell O. Webb The Arnold Aboretum, Harvard University, USA

Dr. Zainal Z. Zainuddin

Borneo Rhino Alliance, Malaysia

The Journal of Indonesian Natural History is published biannually by the Department of Biology at the Andalas University, Padang, Sumatra Barat, Indonesia, in collaboration with Copenhagen Zoo, Denmark. The Department of Biology at Andalas University is dedicated to educating Indonesian biologists in the study and conservation of Indonesia’s biodiversity and natural history. Copenhagen Zoo, through its Research and Conservation Division, supports in-situ conservation in Southeast Asia by assisting local organizations and individuals who undertake research, capacity building and the implementation of conservation programmes and projects.

The Journal of Indonesian Natural History is published by the Department of Biology, Andalas University, Indonesia in collaboration with Copenhagen Zoo, Denmark. It is available for free from www.jinh.net Cover photo: A flat-headed cat, Priornailurus planiceps, at a recent kill. The species is listed as “Endangered” on the IUCN red-list and currently recorded from Southern Thailand, West Malaysia, Borneo and Sumatra. © Carl Traeholt

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© University of Andalas / Copenhagen Zoo

Editorial

Preparing for El Niño - will Indonesia be ready? Carl Traeholt1 and Wilson Novarino2 Copenhagen Zoo, Southeast Asia Programme, Malaysia University of Andalas, Padang, Sumatra

1 2

Corresponding authors: email: [email protected]

ndonesia endured its worst ever forest fires in 1997, when the El Niño effect, combined with extensive peat-development, caused more than 45.000km2 of forests to dry out and burn (Hansen et al., 2013; Heil and Goldhammer, 2001). Together with extensive forest fires in Peninsular Malaysia and in the Malaysian state of Sarawak, it caused a large part of Southeast Asia to be engulfed in a thick layer of smoke. This resulted in tremendous costs to the society with an estimated 20 million people suffering respiratory illnesses in Indonesia alone (Brauer, 1997; Emmanuel and Lim, 1998; Heil and Goldhammer, 2001; WHO, 1998). The fires resulted in forest degradation and deforestation cost of US$ 1.62-2.7 billion (Tacconi, 2003) and the associated cost of the smoke pollution was estimated at US$ 799 million (Tacconi, 2003). The El Niño effect, a weather phenomenon that arise with shifting temperature in the Pacific Ocean, alternately brings extreme droughts or wet seasons to the region in a cycle of approx. 7-9 years. Following this, 2014 should have been an El Niño year, but while dry it never became extreme. It did, however, send a stark reminder of what is to come, and the weather predictions already warns of an upcoming year with extreme low rainfall. In October 2014, NASA warned that a pattern of sea surface heights and temperatures have formed that resembled the way the Pacific looked in the spring of 1997 (Molina, 2014). That turned out to be the precursor of the most severe El Niño on record. With the early warning system in place, combined with a vastly superior knowledge about the El Niño phenomenon, Indonesia, along with other countries in the region, should take precautionary steps to prevent another disastrous outcome of an El Niño. Compared to 1997, much more is at stake for the nation. The rapid economic development that has blessed the country in this millennium may take a serious hit. Compared to the 1997 landscape, there are hundreds of thousands more hectares of peat swamp that have been cleared and drained for palm oil development (Hansen et al., 2013; Heil and Goldhammer, 2001), and therefore, an extreme

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2014 Journal of Indonesian Natural History Vol 2 No 2

drought has the potential to cause significantly more damage to the Indonesian economy, citizens’ health and the environment than the 1997 event. With this in mind, will Indonesia be ready this time?

References Brauer, M. (1997). Assessment of health implications of haze in Malaysia. Mission Rep RE/97/0441 Rev.1, November, 1997. WHO Regional Office, Manila. Emmanuel, S.C and O.P Lim (1998). Singapore country report on the 1997 smoke-haze. In: Proceedings of Biregional workshop on health impacts of haze-related air pollution, Kuala Lumpur, 1-4 June, World Health Organisation.  eil, A. and J.G. Goldhammer (2001). Smoke-haze H pollution: a review of the 1997 episode in Southeast Asia. Regional Environmental Change 2: 24-37 Hansen, M.C., Potapov, P.V., Moore, R., Hancher, M. et al. (2013). High-Resolution Global Maps of 21stCentury Forest Cover Change. Science 342(6160): 850853. [DOI: 10.1126/science.1244693]. Miettinen, J., Shi, C. and Liew, S.C. (2011). Deforestation rates in insular Southeast Asia between 2000 and 2010. Global Change Biology 17: 2261. Molina, R. (2014). NASA Science News, http://science. nasa.gov/science-news/science-at-nasa/2014/19may_ elnino/ Tacconi, L. (2003). Fires in Indonesia: Causes, costs and policy implications. CIFOR, Bogor, Indonesia. 34pp. World Health Organisation (1998). Report : Bi-regional Workshop on Health Impacts of Haze-related Air Pollution, Kuala Lumpur, Malaysia, 1-4 June 1998, 55 pp.

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News and Notes A new species of amphibian discovered on Sulawi

A team of researchers have discovered a new species of fanged frog. It was named Limnonectes larvaepartus and is unique among anurans in having both internal fertilization and birth of tadpoles. The new species is endemic to Sulawesi Island, Indonesia. This is the fourth valid species of Limnonectes described from Sulawesi despite that the radiation includes at least 15 species and possibly many more. Fewer than a dozen of the 6455 species of frogs in the world are known to have internal fertilization, and of these, all but the new species either deposit fertilized eggs or give birth to froglets. Iskandar DT, Evans BJ, McGuire JA (2014) A Novel Reproductive Mode in Frogs: A New Species of Fanged Frog with Internal Fertilization and Birth of Tadpoles. PLoS ONE 9(12): e115884. doi:10.1371/journal. pone.0115884

A welcome arrest of a wildlife criminal

One of the most serious impact on species population in Indonesia is illegal poaching and trade. In February, 2015, the South Sumatra Military Police, South Sumatra Provincial Natural Resource Conservation Office (BKSDA), and the Wildlife Conservation Society’s Wildlife Crimes Unit (WCU) announced the recent arrest of a major wildlife trafficker illegally trading in tiger parts and other protected wildlife in Indonesia. The suspect had allegedly sold more than 100 stuffed tigers over a ten-year period. The trafficker allegedly utilized an extensive trade network, that included providing illegal wildlife products to buyers in Southern Sumatra, Kalimantan, Sulawesi and Jakarta. The origin of the skins, however, appears to have been from Lampung, Bengkulu, Jambi, and North Sumatra to supply demand in Jakarta and Java --- and possibly China and Vietnam. The arrest followed an extensive and long investigation that began in 2009 with the arrest of a middleman by the Criminal Investigation Division (CID) of the Indonesian National police assisted by WCU. Sumatran tigers (Panthera tigris sumatrae) is listed as “critically endangered” on the IUCN red-list. It is the only remaining tiger-species in Indonesia, following the

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extinction of the Javan tiger (Panthera tigris sundaica) in the 1970s. It is also one of the BKSDA’s priority species listed for increased protection and conservation intervention. It is yet to be seen to what extent a major wildlife criminal will be prosecuted, and if the proposed penalty will be sufficiently serious to act as a deterrent for other wildlife criminals.

Bawean warty pig survey

Indonesia is the most species rich nation when it comes to wild pigs. There are currently eight recognised species, Sus scrofa vittatus, Sus verrucosus, Babirussa babyrousa togeanensis, Babyrousa babyrussa, Babyrousa celebensis, Sus b. barbatus, Sus celebensis and Sus blouchi. Unfortunately, six of these species are either listed as Endangered or Vulnerable on the IUCN red-list. Two of these, the Javan warty hog (Sus verrucosus) and the Bawean wary hog (Sus blouchi) are likely going to be elevated to “Critically endangered” in the near future. The Bawean warty hog (Sus blouchi) is endemic to Bawean island, a small island with a total land area of 200 km2 located 150 km north of East Java. Based on morphological measurements, Bawean warty hogs are considered a separate species from the Javan warty hog (Sus verrucosus) that is endemic to Java. The recent survey is a long overdue welcome initiative to throw more focus on the conservation plight of Indonesia’s suids. Since the Bawean warty hog’s distribution range is extremely limited, small external disturbances such as poaching and/or further reduction in habitat can have enormous and rapid negative impact on the remaining population. Rode-Margono, J. and M. Rademaker (2015). Preliminary results of the first ecological study on Bawean warty pigs Sus blouchi. Suiform soundings 13(2): 16-18.

Rare new species of mammal discovered on Sulawesi

A new rodent was discovered by a team of scientists from Museum Victoria, Louisiana State University and the Dutch Museum Zoologicum Bogoriense in a remote, mountainous forest of Mount Dako, on Sulawesi Island in Indonesia. The creature is a new genus and species of shrew rat and is now known as the hog-nosed shrew rat, Hyorhinomys stuempkei. The new taxon is known

© University of Andalas / Copenhagen Zoo

News and notes

only from the type locality at 1,600m elevation on Mt. Dako, in the district of Tolitoli. It was captured by the team of scientists during a field expedition in 2013. The hog-nosed rat is distinguished from all other Indonesian murines by its large, flat, pink nose with forwardfacing nares. Relative to other Sulawesi murines, the species has extremely large ears (~21% of head and body length), very long urogenital hairs, prominent and medially bowing hamular processes on the pterygoid bones, extremely long and procumbent lower incisors, and unusually long articular surfaces on the mandibular condyles. Morphologically, the new taxon is most similar to a group of endemic Sulawesi rats known commonly as “shrew rats.” DNA sequences analyses put the new shrew rat as sister to the Sulawesi water rat, Waiomys mamasae. Sulawesi is know for its biogeographic complexity and more scientific expeditions will likely disclose even more new charismatic species in the future. Esselstyn, J.A., Achmadi, A.S., Handika, H. and K.C. Rowe (2015). A hog-nosed shrew rat (Rodentia: Muridae) from Sulawesi Island, Indonesia. Journal of Mammalogy 96(5): 895 - 907

The ongoing saga of Homo floresiensis - to be or not to be?

In 2003, hominid fossils were excavated from Liang Bua Cave on Flores, Indonesia. In comparison to modern Homo sapiens, the skeletons were exceptionally small, which prompted the popular name as the “hobbit” of Flores. The authors of the original discovery made extensive comparative research and concluded that there was sufficient evidence to place it as a separate species and named it Homo floresiensis. This came under heavy criticism, with many scientists proclaiming that it was nothing less than a microcephalic “normal” Homo sapiens. Several follow-up paleoneurological and orthopedic studies were carried, however, none were conclusive, and the debate rages on. Critics of the claim for species status continue to believe that these individuals are Homo sapiens possessing pathologies of anatomy and physiology. Several hypotheses in this category have been put forward, including that the individuals were born without a functioning thyroid, resulting in a type of endemic cretinism. The most recent study published in the Proceedings of the National Academy of Sciences focuses on the

The newly discovered hog-nosed shrew rat, Hyorhinomys stuempkei, from Sulawesi. Photograph © Museum Victoria

2014 Journal of Indonesian Natural History Vol 2 No 2

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News and notes

possibility that the hobbit exhibited traits that are consistent with individuals suffering Down syndrome. The study concludes that the human skeletons from Liang Bua Cave are coeval with only Homo sapiens populations worldwide and no other previously known hominins. They report that the brain size of LB1, the principal specimen unearthed from Liang Bua Cave, is in the range predicted for an individual with Down syndrome in a normal small-bodied population from the geographic region that includes Flores. Among additional diagnostic signs of Down syndrome and other skeletal dysplasiae are abnormally short femora combined with disproportionate flat feet. LB1 femora match interlimb proportions for Down syndrome, and predictions based on corrected LB1 femur lengths show a stature normal for other H. sapiens populations in the region. In reality, this means that the Flores hobbit is an “abnormal” modern human that suffered from maladies that stunted its growth and/or reduced its lifespan. In a response to this, Westaway et al. (2015) claims that there remain more than sufficient evidence in the mandibular structures to put the hobbit in its own species category. This interesting and important debate continues unabated, and one can only hope that more work is being put into excavating more specimens that can possibly bring this case to conclusion.

Henneberg, M., Eckhardt, R.B., Chavanaves, S. and K.J. Hsüc (2015). Evolved developmental homeostasis disturbed in LB1 from Flores, Indonesia, denotes Down syndrome and not diagnostic traits of the invalid species Homo floresiensis. PNAS 111(33): 11967–11972, doi: 10.1073/pnas.1407382111 Robert B. Eckhardt, Maciej Henneberg, Alex S. Weller and Kenneth J. Hsü (2014). Rare events in earth history include the LB1 human skeleton from Flores, Indonesia, as a developmental singularity, not a unique taxon. PNAS 111(33): 11961-11966 Westaway, M.C., Durband, A.C., Groves, C.P. and M. Collard (2015). Mandibular evidence supports Homo floresiensis as a distinct species. PNAS 112(7): E604-E605 Sumatran rhino returning to Indonesia The Sumatran rhino, Dicerorhinus sumatrensis, has been listed as “Critically endangered” on the IUCN redlist since 1996, but the population continues to decline. Already declared “extinct” in West Malaysia, and with nothing but a handful left in captivity in Sabah, East Malaysia (Fig. 1), the World’s hope rests on the few wild individuals that still roam remote areas of Sumatra. Despite costly captive breeding efforts in the late 1990s,

Figure 1. One of the few Sumatran rhinos, Dicerorhinus sumatrensis, in captivity in Sabah, East Malaysia.

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© University of Andalas / Copenhagen Zoo

News and notes

only one institution enjoyed modest captive breeding success. The Cincinnati Zoo managed to breed the species merely three times. One of these, Harapan, is the only Sumatran rhino left in the Western Hemisphere, after its elder brother was returned to Sumatra in 2007, and its sister died from disease in 2014. Harapan will be returned to its ancestral origin on Sumatra, Indonesia, where it will paired with a female and given a chance to mate at the Sumatran rhino centre at Way Kambas National Park. The decision to return Harapan to Sumatra was made, because he could no longer contribute to efforts to breed the species if kept alone in the USA. Earlier, it was believed that Indonesia would send another rhino to pair up with Harapan, but recently, Indonesia’s authorities made it clear that they never plan to send another Sumatran rhino out of the country again. At the same time, receiving potential mates from Malaysia, the only other country with captive Sumatran rhinos, was not an option, since all the Malaysian females are infertile. Harapan is expected to undergo a short adaptation period for his travel crate, before he commences on his

long journey back to Sumatra. He is expected to arrive at Way Kambas National Park in the last quarter of 2015. NASA predicts high risk of El Niño effect in 2015 After a record warm and 2014, NASA climate model forecast shows that 2015 will likely be even worse, with an El Niño effect expected to go “off the charts”. Making use of the world’s best-established dynamical climate models, the 2015 El Niño is set to peak in the second and third quarter of 2015, and possibly stretch into the Paris climate summit. Whereas the 20142015 El Niño was slow to develop and increased over months, the 2015 version may set to increase to monster proportions, possibly up to +3oC Pacific temperature anomalies. In practice, this means that Southeast Asia will suffer extreme dry conditions (Fig. 2), with elevated risks of wildfires. One can only hope that landuse managers across the region learned from the smoke disaster that engulfed the entire region in 19971998 that cost regional nations billions in direct, as well as collateral damages.

Figure 2. The red areas are likely to experience below-average rainfall during the end-2015 super El Niño. Green areas are likely to experience above-average precipitation © NOAA NCEP

2014 Journal of Indonesian Natural History Vol 2 No 2

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Morphological variation of the Diadem Leaf-nosed Bat, Hipposideros diadema, Geoffroy, 1813 (Chiroptera: Hipposideridae) in Caves in West Sumatra, Indonesia Ada Chornelia, Djong Hon Tjong and Dewi Imelda Roesma Department of Biologi, Faculty of Mathematics and Natural Science, University of Andalas, West Sumatra, Indonesia Corresponding author: Ada Chorneliaa, email: [email protected] Abstrak Bukit Barisan sebagai barier fisik diprediksi berpengaruh terhadap populasi di Sumatera Barat sebagaimana terjadi pada kelompok hewan terestrial termasuk kelelawar Hipposideros diadema, yang dikenal memiliki kemampuan dispersal yang tinggi. Pengaruh barier ini diharapkan dapat diamati pada perbedaan morfologi. Sejumlah 58 individu dewasa H. diadema dikoleksi dengan menggunakan Harpa trap pada beberapa goa di Sumatera Barat, yang terdiri dari Goa Kalilawa, dan Goa Lereng di bagian barat Bukit Barisan dan Goa Salamaik di bagian timur Bukit Barisan. Pengkoleksian sampel di lapangan dilaksanakan pada bulan Januari-Desember 2013. Pengukuran dilakukan terhadap 26 karakter tubuh dan 15 karakter tengkorak. Uji Mann-Whitney menunjukkan divergensi karakter antar dua populasi yang berbeda. Hasil PCA sesuai dengan fenogram yang disusun dengan UPGMA yang menunjukkan populasi H. diadema di Goa Salamaik (populasi timur) berbeda dengan populasi dari Goa Kalilawa dan Goa Lereng (populasi barat). Disimpulkan bahwa barier Bukit Barisan memungkinkan berpengaruh terhadap divergensi karakter morfologi antara H. diadema di Sumatera Barat. Abstract We assumed that Bukit Barisan as a physical barrier and its acts to population exchanges in West Sumatra, as well as for terrestrial animal group. If it does for bats in case for the Diadem Leaf-nosed Bat, Hipposideros diadema, which have superior dispersal powers to many other terrestrial group, then we might expect to see this some how reflected in morphological divergence. A total of 58 adult of H. diadema were collected directly using harp traps from several Cave in West Sumatra (Kalilawa Cave, Padang; Lereng Cave, Pariaman; (western of Bukit Barisan) and Salamaik Cave, Sawahlunto (eastern of Bukit Barisan)). The samples were collected on January-December 2013. Kruskall Wallis Test, Mann Whitney U Test, Principal Component Analyses (PCA) and Cluster Analysesdemonstrated that these population could be separated clearly from one to another. This analyses based on 26 external and 15 skull measurement. The result showed that population of H. diadema from Salamaik Cave in Sawahlunto differ from H. diadema in Padang and Pariaman. Divergence characters among three population of H. diadema was found using Kruskall Wallis test. Mann-Whiney U test showed divergence characters between two different population. The result of PCA was congruence to phenogram obtained by UPGMA that showed close relationship between population of H. diadema from Kalilawa Cave, Padang to Lereng Cave, Pariaman and different from Salamaik Cave, Sawahlunto. We conclude that Bukit Barisan barriers could be affected to morphological divergence among H.diadema in West Sumatra. Keywords: Bukit Barisan, cave, Hipposideros diadema,morphology, variation.

Introduction West Sumatra has the largest limestone outcrops in Indonesia. Caves are known as karsts, and West Sumatra has 114 limestone caves (UKSDA, 1999; Haznan, Received 9th December, 2013; First revision 28th April, 2014; Second revision accepted 14th May, 2015.

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2003). Limestone biodiversity consists of three types of ecosystem, as troglobin, troglophil and trogloxene (Dunn,1965). A common cave dweller belongs to a group of bats known as trogloxene (Vermeullen &Whitten, 1999) in the order of chiroptera (Findley, 1993; Kitchener, 1996; Nowak, 1994). Based on echolocation calls chiroptera are divided into two sub order, megachiroptera and microchiroptera (Gunnel &

© University of Andalas / Copenhagen Zoo

Morphological variation of leaf-nosed bats

Figure 1. H. diadema collected from Kalilawa Cave, Padang, West Sumatra.

Simmons, 2005; Koopman, 1994; Simmons & Geisler, 1998). Based on molecular evidence and evolution of echolocation in bats, Koopman (1994) proposed that Megachiroptera (family Pteropodidae) is closely related to Microchiroptera (Rhinolipids group includes Rhinolophidae, Megadermatidae, Hipposideridae, Craseonycteridae, Rhinopomatidae) and grouped them as Yinpterochiroptera, whereas Jones and Teeling (2006) grouped Microchiroptera into two infraorders; Yinochiroptera and Yangochiroptera. This group can be found in all habitats with some families preferring caves as roosting sites (Graham, 1994;Vermeullen & Whitten, 1999). H. diadema belongs to the family Hipposideridae (Roundleaf bats), infraorder Yinochiroptera that is sometimes called Diadem roundleaf bats. Description of this species is large body size, FA 76-87 mm and weight 30-47 gram. Fur of upperparts is dark brown with pale bases, white patches on the shoulders and sides; underparts greyish-white. In adult females orange or orange buff often replaces the white. Noseleaf with 3 or 4 lateral leaflets; posterior noseleaf large and rounded (Francis, 2008) (Figure 1). This species has wide distribution from Burma and Vietnam through Thailand, Laos, West Malaysia and Indonesia (including Sumatra, Borneo, and Bali) to New Guinea, Bismarck Archipelago, Solomon Islands and norteasth Australia; Philippines; Nicobar Islands (Simmons, 2005). West Sumatra is separated by Bukit Barisan that stretches from south to north of Sumatra Island. This was formed during Miocene when two unequal parts, the narrow west coast and the wider half of hills and

2014 Journal of Indonesian Natural History Vol 2 No 2

alluvial areas. The different ecological conditions east and west of Bukit Barisan is likely to have influenced the morphology and genetic variation of the species (Colombijn, 2005; Whitten, 1989). Studies about morphological traits and genetical variations associated with ecological conditions suggest that H. diadema distributed across several small and large islands (include in Lesser Sunda Islands) belong to 16 different subspecies (Kitchener et al., 1992). Rahman and Abdullah (2010) found that Penthetor lucasi in three geographical areas of Sarawak (Malaysia) differs in body size and exhibit strong sexual dimorphism in certain characters. Benita (2012) studied morphological variations of Hipposideros larvatus from three caves in west Sumatra and concluded that the barrier created by Bukit Barisan mountain range may have lead to the variation in morphological characters of bats in Sumatra. Currently, there is no other published study that focuses on morphological variation of H. diadema from caves in West Sumatra. Tate (1941) summarized information about the subspecies of H.diadema in the Indo-Australian region and recognized about 16 subspecies. This, however, does not include subspecies grouping of H. diadema populations in west Sumatra. We hypothesized that ecological differences between east and west Bukit Barisan may have induced morphological variation among population of H. diadema. Therefore, the aim of this study is to investigate the morphological variation of population H. diadema from three caves in West Sumatra separated by Bukit Barisan mountain range.

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Chornelia et al.

Figure 1. A diadem leaf-nosed bat, H. diadema, from Kalilawa cave, Padang, West Sumatra.

Methods Bats were captured from three caves in West Sumatra: Kalilawa Cave, Padang (00o56’51.1S, 100o29’50.2E); Lereng Cave, Pariaman (00o92’95.8S, 100o33’89.4E) and Salamaik Cave, Sawahlunto (00o40’11.6S, 100o44’24.1E) (Figure 2). Bats were captured using harp traps (Francis, 1989) setup in entrances of the caves. The traps were deployed in the afternoon and checked in the evening and in the early morning. For each bat were captured, we recorded the age (adult or young) and sex. Presence of growth bands at the finger joints of H. diadema were also recorded (Anthony, 1988). Bat trapping took place during January-February 2013 and the specimens were deposited in the Zoological Museum at the University of Andalas (MZUA). Thirty six characters were measured; twenty one external characters following Rahman and Abdullah (2010), and fifteen skull character following Kitchener and Maryanto (1993). These external characters measurements were as follows, with abbreviations in parentheses; ear length (E), head and body length (HB), tail to ventral length (TV), Forearm length (FA), tibia length (TB), first digit length (PIB), hind foot length (HF), second digit metacarpal (D2MCL), third digit metacarpal (D3MCL), fourth digit metacarpal (D4MCL), fifth digit metacarpal (D5MCL), third digit first (D3P1L) and second phalank length (D3P2L), fourth digit first (D4P1L) and second phalank length (D4P2L), fifth digit first (D5P1L) and second phalank length (D5P2L), antitragus high (TA), eye diameters (DM), posterior nose leaf breadth (LDP) and anterior

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nose leaf width (LDA). The skull characters measured were the great skull length (GSL), cranial length (PIL), least interorbital width (LI), zygomatic width (LTP), width across caninus to another caninus from outer basal face (CCB), palatal bridge length (PBL), width across molar to another molar from outer mass face (MMB), tymphanic bulla length (TBL), tymphanic bulla width (TBB), cochlea width (CW), cranial heigh (CH), rostrum heigh (RH), rostrum length (RL), lower tooth row length (IML) and dentary length (DL) (Figure 3).

Figure 2. Locality of H. diadema specimens used in this study in West Sumatra (insert), Sumatra Island, Indonesia.

© University of Andalas / Copenhagen Zoo

Morphological variation of leaf-nosed bats

B

A

C

D

E

Figure 3. Twentyone external characters (a,b) (modified from Rahman and Abdulllah, 2010) and fifteen skull characters (a;dorsal, b; ventral, c; lateral) (modified from Kitchener and Maryanto, 1993) were used in this study to measure morphological differences.

The data measurements were divided by forearm (external measurements) and great skull length (skull measurements) to standardised body size for all specimens. Morphological variations among the populations were tested using Kruskall-Wallis Test and possible differences between populations were tested using Mann Whitney U Test at a significancy level of 5% using SPSS® software. All data were transformed to log10 values before Principal Component Analyses (PCA) and Cluster analysis shown up by UPGMA (Unweighted Pair Group Method Arithmatic Average) using MVSP 3.1 and NTSyspc Ver 2.0.2i software.

2014 Journal of Indonesian Natural History Vol 2 No 2

Results A total of 58 adult H. diadema consisting of 31 males and 27 females were collected and measured. The number of specimens collected from each cave was: Kalilawa cave (14 male and 4 female), Lereng cave (3 male and 11 female) and Salamaik cave (14 male and 12 female). Morphological characters The morphological characters of male and female specimens from Salamaik Cave population are relative

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Table 1. Measurement of male samples in millimeters, for (a) external character measurements (b) Skull character measurement. For each samples, mean ± standard deviation, df=2, N=sample size, p-value, H=Kruskall-Wallis value. *=significance level p≤0.05, ns=not significant) A) External characters measurements

Kalilawa cave (N=14)

Lereng Cave (N=3)

Salamaik cave (N=14)

Kruskall-Wallis test

E

31.48 ± 2.36

31.5 ± 3.07

28.44 ± 1.56

H = 10.09; p = 0.006*

HB

100.92 ± 6.9

101.75 ± 6.83

102.66 ± 3.17

H = 0.142; p = 0.9313 ns

TV

56.98 ± 3.34

57.87 ± 3.48

52.40 ± 3.22

H = 10.66; p = 0.005*

FA

78.37 ± 2.48

78.35 ± 2.07

75.92 ± 2.39

H = 8.385; p = 0.015*

TB

43.43 ±2.62

41.09-1.68

40.53 ± 2.32

H = 10.8; p = 0.005*

PIB

12.84 ±1.16

11.60 ± 1.15

10.81 ± 0.86

H = 17.37; p = 0.000*

HF

15.39 ± 1.69

14.65 ±1.19

15.80 ± 1.56

H = 0.431; p = 0.806 ns

D2MCL

77.58 ± 3.27

77.64 ± 3.92

71.03 ± 2.68

H = 18.39; p = 0.000*

D3MCL

74.81 ±1.77

73.79 ±1.26

73.92 ± 2.02

H = 1.273; p = 0.529 ns

Characters

D4MCL

72.97 ±3.06

72.35 ±2.46

73.04 ± 2.45

H = 0.264; p = 0.876 ns

D5MCL

66.27 ± 2.10

65.77 ± 2.28

61.53 ± 2.17

H = 16.27; p = 0.000*

D3P1L

33.75 ± 3.01

33.43 ±1.21

27.79 ± 15.85

H = 7.861; p = 0.019*

D4P1L

24.47 ± 2.22

23.59 ±3.03

24.09 ± 2.33

H = 0.188; p = 0.910 ns

D5P1L

26.35 ± 1.93

26.09 ±1.85

26.37 ± 1.17

H = 0.136; p = 0.934 ns

D3P2L

36.33 ± 2.20

34.87 ±1.68

33.45 ± 1.35

H = 11.08; p = 0.003*

D4P2L

21.90 ±7.95

17.21 ±1.71

17.70 ± 1.17

H = 5.768; p = 0.056 ns

D5P2L

20.28 ± 1.96

19.74 ±0.07

18.34 ± 1.26

H = 7.004; p = 0.030*

TA

6.71 ± 1.22

5.27 ±0.31

5.71 ± 0.67

H = 8.149; p = 0.017*

DM

3.12 ± 0.46

2.97 ±0.53

2.40 ±0.34

H = 15.64; p = 0.000*

LDP

14.71 ± 1.41

14.47 ±1.64

16.16 ± 0.54

H = 13.07; p = 0.001*

LDA

14.36 ± 0.86

13.49 ±0.40

14.93 ± 0.60

H = 5.74; p = 0.057ns

GSL

31.57 ± 0.71

31.97 ± 1.49

30.56 ± 0.54

H = 12.77; p = 0.002*

PIL

68.25 ± 6.71

66.03 ± 3.85

69.02 ± 7.75

H = 0.195; p = 0.907 ns

LI

12.66 ± 1.08

12.33 ± 1.97

12.63 ± 1.66

H = 0.160; p = 0.923 ns

LTP

53.43 ± 8.20

54.35 ± 2.10

55.78 ± 1.99

H = 2.452; p = 0.294 ns

CCB

25.56 ± 1.51

24.82 ±1.89

24.71 ± 1.89

H = 1.147; p = 0.564 ns

PBL

30.04 ± 0.88

31.19 ± 2.92

30.23 ± 2.83

H = 1.449; p = 0.485 ns

MMB

39.48 ± 1.84

38.31 ± 3.26

39.98 ± 1.71

H = 1.917; p = 0.384 ns

TBL

13.79 ± 1.58

12.86 ± 0.88

13.62 ± 1.47

H = 1.571; p = 0.456 ns

TBB

45.04 ± 0.94

44.83 ± 2.84

45.68 ± 1.75

H = 0.5819; p = 0.747 ns

CW

10.63 ± 1.49

10.95 ± 0.92

10.17 ± 1.20

H = 0.927; p = 0.629 ns

CH

38.06 ± 2.61

35.69 ± 2.28

36.59 ± 20.41

H = 3.555; p = 0.169 ns

RH

30.62 ± 1.19

30.3 ± 1.44

29.72 ± 1.38

H = 2.059; p = 0.357 ns

RL

14.61 ± 1.88

16.03 ± 1.85

13.28 ± 1.17

H = 9.872; p = 0.007*

IML

45.63 ± 2.63

44.42 ± 2.81

46.45 ± 2.05

H = 2.061; p = 0.357 ns

DL

68.66 ± 2.02

64.74 ± 5.83

69.23 ± 2.21

H = 1.831; p = 0.400 ns

B) Skull measurements

12

© University of Andalas / Copenhagen Zoo

Morphological variation of leaf-nosed bats

Table 2. Measurement of female samples in millimeters for (a) external character measurements (b) Skull character measurement. For each samples, mean ± standard deviation, df=2, N=sample size, p-value, H=Kruskall-Wallis value. *=significance level p≤0.05, ns=not significant) A) External characters measurements

Kalilawa cave (N=14)

Lereng Cave (N=3)

Salamaik cave (N=14)

Kruskall-Wallis test

33.75 ± 2.17

31.99 ±1.83

29.15 ± 1.92

H = 13.87; p = 0.000*

HB

104.45 ± 4.19

105.73 ± 2.91

104.38 ± 4.11

H = 0.8009; p = 0.67 ns

TV

58.44 ± 0.40

57.48 ± 4 49

54.20 ± 3.68

H = 4.325; p = 0.115 ns

Characters E

FA

75.03 ± 0.77

78.39 ± 1.79

78.33 ± 1.91

H = 8.62; p = 0.013*

TB

44.40 ± 0.79

42.22 ± 2.47

39.40 ± 0.93

H = 14.18; p = 0.000*

PIB

12.95 ± 1.76

12.67 ± 1.55

11.63 ± 1.35

H = 3.819; p = 0.148 ns

HF

18.57 ± 0.43

16.76 ± 1.52

15.41 ± 1.23

H = 11.43; p = 0.003*

D2MCL

82.79 ± 2.30

79.1 ± 2.91

82.69 ± 3.40

H = 15.51; p = 0.000*

D3MCL

77.18 ± 1.38

75.16 ± 2.67

73.66 ± 1.43

H = 7.528; p = 0.023*

D4MCL

73.69 ± 0.99

74.01 ± 2.23

71.18 ± 1.68

H = 11.67; p = 0.003*

D5MCL

69.19 ± 2.08

68.72 ± 3.29

60.85 ± 1.39

H = 16.09; p = 0.000*

D3P1L

34.66 ± 0.26

33.29 ± 11.12

31.31 ± 1.95

H = 15.62; p = 0.000*

D4P1L

23.85 ± 1.84

26.56 ± 4.03

24.95 ± 0.88

H = 3.155; p = 0.206 ns

D5P1L

27.02 ± 0.54

25.93 ± 1.96

26.81 ± 1.28

H = 1.194; p = 0.551 ns

D3P2L

38.25 ± 0.18

37.07 ± 5.81

32.25 ± 1.40

H = 15.73; p = 0.000*

D4P2L

17.60 ± 0.75

20.92 ± 9.12

17.20 ± 0.86

H = 4.216; p = 0.122 ns

D5P2L

21.03 ± 0.15

19.79 ± 1.87

18.88 ± 8.73

H = 12.94; p = 0.002*

TA

7.14 ± 0.26

7.16 ± 3.61

5.49 ± 1.17

H = 4.283; p =0.118 ns

DM

3.33 ± 0.05

3.28 ± 1.17

2.50 ± 0.39

H = 10.13; p = 0.006*

LDP

16.60 ± 0.99

14.06 ± 0.67

15.98 ± 0.75

H = 17.33; p = 0.000*

LDA

14.57 ± 0.98

14.50 ± 5.12

14.95 ± 0.54

H = 4.109; p = 0.128 ns

GSL

32.13 ± 0.51

31.99 ± 0.44

31.75 ± 0.58

H = 1.869; p = 0.393 ns

PIL/GSL

64.42 ± 1.21

66.02 ± 7.32

63.83 ± 1.49

H = 4.242; p = 0.119 ns

LI/GSL

12.59 ± 0.60

13.12 ± 2.36

11.15 ± 1.46

H = 5.717; p = 0.057 ns

LTP/GSL

53.72 ± 2.27

55.32 ± 2.15

52.66 ± 1.53

H = 7.225; p = 0.027*

CCB/GSL

24.69 ± 0.35

25.99 ± 1.84

23.19 ± 1.53

H = 14.61; p = 0.000*

PBL/GSL

29.23 ± 0.80

31.03 ± 1.67

27.76 ± 1.26

H = 15.15; p = 0.000*

MMB/GSL

39.29 ± 0.42

38.81 ± 1.99

37.71 ± 1.20

H = 2.165; p = 0.339 ns

TBL/GSL

11.71 ± 0.50

13.47 ± 2.39

9.94 ± 1.00

H = 17.2; p = 0.000*

TBB/GSL

44.32 ± 0.78

45.15 ± 2.68

43.92 ± 1.63

H = 1.022; p = 0.600 ns

CW/GSL

12.14 ± 1.44

11.26 ± 2.88

11.31 ± 7.02

H = 10.52; p = 0.005*

CH/GSL

35.16 ± 1.70

38.21 ± 2.80

34.21 ± 2.19

H = 13.44; p = 0.001*

RH/GSL

30.46 ± 0.53

30.99 ± 2.18

26.73 ± 4.82

H = 14.5; p = 0.000*

RL/GSL

12.80 ± 1.77

29.56 ± 14.81

12.80 ± 1.22

H = 13.75; p = 0.001*

IML/GSL

41.97 ± 4.49

47.58 ± 2.52

40.73 ± 0.70

H = 15.61; p = 0.000*

DL/GSL

66.13 ± 0.60

66.17 ± 4.06

65.70 ± 1.55

H = 0.914; p = 0.6343 ns

B) Skull measurements

2014 Journal of Indonesian Natural History Vol 2 No 2

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Chornelia et al.

small compared to the specimens from Kalilawa cave and Lereng cave. The sample size, mean, standard deviation, maximum and minimum values for all characters measurements, including external and skull characters measurements of H. diadema are presented in Table 1 and 2. Comparison of adult specimens among the tree population showed significant differences among them in 15 morphometric characters among male consist of 13 external characters and 2 skull characters, and 21 morphometric character measurements of female, consist of 13 external characters and 9 skull characters. We recorded significant differences in male externall characters for TV, FA, TB, PIB, D2MCL, D5MCL, D3P1L, D3P2L, D5P2L, TA, DM, LDP, and for skull characters GSL and RL. For females we recorded significant differences for D2MCL, E, FA, TB, HF, D3MCL, D5MCL, D3P1L, D3P2L, D5P2L, DM, LDP, and for skull characters LTP, CCB, TBL, CW, CH, RH, RH, RL, and IML. Significant differences in both characters measurements indicates high divergence of external and skull characters of H. diadema between the three populations (Kalilawa cave, Lereng cave, and Salamaik cave). A Mann Whitney U-test was used to compare remaining characters. The H. diadema populations from Lereng and Salamaik caves differs significantly for both males and females, This was also the case between the Kalilawa and Lereng cave populations, and Kalilawa and Salamaik cave populations. The males from Kalilawa cave and Lereng cave only differed significantly on one character, whereas females differed on two 2 characters. Males and females from Kalilawa and Salamaik caves differed signficantly on two characters. The male populations of Lereng and Salamaik caves differed significantly on three characters and in five characters for females (Table 3). Unweighted Pair Group Method Arithmatic Average and Principall Component Analysis Euclidian distances showed up in a UPGMA analysis as clusters between three population with males and females analysed separately. PCA of 36 characters revealed a clear separation between the three different cave populations (Fig. 4). UPGMA analysis revealed a close relationship between Padang and Pariaman populations (0.25 (male) and 0.14 (female)), and PCA showed that of H. diadema populations from Padang were closely related to the Pariaman populations, and clearly distinct from the Sawahlunto populations.

14

Discussion H. diadema populations from three caves separated from each other by Bukit Barisan in West Sumatra revealed variations and morphological character divergences. Our data suggest that the individuals from Kalilawa cave are more closely related to individuals from the Lereng cave, whereas it differed from Salamaik cave. From 21 external and 15 skull characters used in this analysis the H. diadema population from Salamaik cave are significantly smaller than conspecifics from Kalilawa and Lereng caves. Ecological circumstances related with breeding, foraging, crowding and resources avaibility may differ between the three populations due to their separation by the Bukit Barisan range. Kalilawa and Lereng caves are located on the western side of Bukit Barisan and at a lower altitude than the Salamaik cave on the eastern side. The ecological different conditions, combined with a lower inter-population migration, may have required different behavioural adaptation and resulting morphological variations. Euclidian distance among H. diadema populations from the three study sites showed that geographic distance is reflected in the relationship distance. Kalilawa cave is closer geographically and in relationship distance to Lereng cave than to Salamaik cave. Rahman and Abdullah (2010) reported morphological variations between geographical separated populations of Penthetor lucasi in Sarawak and suggested that ecological conditions as the likely main cause of the differentiation. Kitchener and Suyanto (1996) suggest that the Pleistocene- modern time island arrangement have caused relatively recent morphological changes. Kitchener, Konishi and Suyanto (1996) assumed that longitude was the most important variable when predicting overall skull and body size. In contrast Whitten (1987) argued that Bukit Barisan was formed already during Miocene, and therefore separated populations of H. diadema in West Sumatra at a much earlier stage. Kitchener et al., (1992) noted that H. diadema in Lesser Sunda Island was divided into three phenetic grouping based on external and skull measurements: H.d. diadema, H.d. reginae and H.d. masoni in one group; H.d. griseus and H.d. oceanitis in a second group, and H.d.nobilis in a separate cluster. The study indicated that the eastern form of H. d. diadema is smaller than the western form, suggesting different ecological conditions had required different adaptational strategies and eventually morphological unique forms.

© University of Andalas / Copenhagen Zoo

Morphological variation of leaf-nosed bats

Whereas morphological variation could give rise to speciation, we were unable to determine from morphological characters alone that individuals of H. diadema from the three different study sites belong to different subspecies. Further studies on the genetic variation of H. diadema in West Sumatra is needed to confirm if there are indeed three different subspecies.

Acknowledgement We gratefully acknowledge the support of all teachers at Biology Department, Faculty of Mathematic and Natural Science, Andalas University especially to Genetics and Cytology Laboratory, Biologi Department and Museum Zoology Universitas Andalas, to Dr. Syaifullah, Dr. Rizaldi, Dr. Wilson Novarino and all assistants. Thank you to our colleagues who assisted us in the field, KCALH Rafflesia FMIPA UNAND, particularly Fajri, Beny Ramdani, Rezi Rahmi Amolia, Vivi Martinsyah, Riki Novtian Burlis, Reki Kardiman, Heru Handika, Kedhy Lavandino and all members. Thanks a lot to all friends who supported this research; Jiji, Rahma, Widia, Nova, Putri, Fitri, Anita, Wita, Ami, Icha and Nurul.

References Anthony, E.L.P. (1988). Age Determination in Bats. In Ecological and Behavioral methods for the study of Bats (T.H. Kuntz, ed). Smithsonian Institution Press, Washington D.C Benita, N.D. (2012).Variasi Morfometri Kelelawar Hipposideros larvatus (Horsfield, 1823) pada Beberapa Goa di Sumatera Barat. Skripsi Sarjana Biologi FMIPA. Padang; Universitas Andalas. Bookstein, F.L. (1982). Foundation of Morphometrics. Annual Review of Ecology and Systematic 13: 451-470. Colombijn, F. (2005). A Moving History of Midle Sumatra 1600-1870. Modern Asian Studies 39: 1-38. Dunn, F.L. (1965) Goa Anak Takun Ecological Observation. Malay Nature Journal 19: 75-78. Findley, J.S. (1993). Bats: A Community Perspective. Australia: Press Syndicate of The University of Cambridge.

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Francis, C.M. (1989). A comparison of Mist Nets and Two Design of Harp Trap for capturing Bats. Journal of Mammalogy 70: 865-870. Graham, G.L. (1994). Bats of The World. Wisconsin: Western Publishing Company. Inc. Gunnel, G.F. and Simmons, N.B. (2005) Fossil evidence and the originof bats. Journal of Mammal Evolution 12: 209–246. Haznan, D. (2003). Jenis-jenis Chiroptera Pada Beberapa Goa di Sumatera Barat. Skripsi Sarjana Biologi FMIPA. Padang; Universitas Andalas. Jones, G. and E.C. Teeling. (2006). The Evolution of Echolocation in Bats. Trends in Ecological and Evolution 21: 149-156. Kitchener, D.J., How, R.A., Cooper, N.K and A Suyanto. (1992). Hipposideros diadema (Hipposideridae: Chiroptera) in The Lesser Sunda Islands Indonesia: Taxonomy and Geography Morphological Variation. Record of the Western Australian Museum 16: 1-60. Kitchener, D.J. and I. Maryanto.(1993). Taxonomic Reappraisal of The Hipposideros larvatus Species Complex (Chiroptera: Hipposideridae) in The Greatwer and Lesser Sunda Islands, Indonesia. Record of the Western Australian Museum 16: 169-173. Kitchener, D.J., Packer, W.C. and I. Maryanto. (1994). Morphological variation in the Maluku population of Syconycteris australis (Peters, 1867) (Chiroptera: Pteropodidae). Record of the Western Australian Museum 16: 485-498. Kitchener D.J., Konishi, Y. and A. Suyanto. (1996). Morphological variation among eastern Indonesian Island population of Hipposideros bicolor (Chiroptera: Hipposideridae), with Description of Three New Species. Record of the Western Australian Museum 18: 179-192. Koopman, K.F. (1994) Chiroptera: Systematics. Part 60. Handbook of Zoology Vol. 8, Walter de Gruyter. Munshi, J.S.D. and H.M. Dutta (1996). Fish Morphologiy: Horizon of New Research. New York; Science Publisher

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Nowak, R.M.(1994). Walkers Bat’s of The World. Baltimore and London; The Johns Hopkins University Press. Payne, J. (2000). Panduan Lapangan Mamalia di Kalimantan, Sabah, Serawak dan Brunei Darussalam. Jakarta; The Sabah Society-Wildlife Conservation Society-WWF Malaysia. Rahman, M.R., Abdullah, M.T. (2010). Morphological Variation in The Dusky Fruit Bat, Penthetor lucasi, in Sarawak Malaysia. Tropical Natural History 10(2): 141-158. Simmons, N.B. and J.H. Geisler (1998). Phylogenetic relationships of Icaronycteris, Archaeonycteris, Hassianycteris, and Palaeochiropteryxto extant bat lineages, with comments on the evolution of echolocationand foraging strategies in Microchiroptera. Bull. Am. Mus. Nat. Hist. 235: 1–182.

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Simmons, N.B. (2005). Order Chiroptera. In: Mammal species of the World: a taxonomic and geographic reference, Third Edition (D. E. Wilson and D. M Reeder, eds.). Smithsonian Institution Press. Tate, G.H.H. (1941). A review of the genus Hipposideros with special reference to Indo-Australian species. Results of the Archoold Expedition No. 35. Bull. Am. Mus. Nat. Hist.78: 353-393. Vermeullen, J. and T. Whitten. (1999). Biodiversity and Cultural Property in the Management of Limestone Resources. Washington DC: The World Bank. Whitten, E.H.T. (1989). Mathematical Geoscience. Kluwer Academic Press. Whitten, A.J., Anwar, J. and N. Nisyam. (1987). The Ecology of Sumatra. Yokyakarta: Gadjah Mada University Press

© University of Andalas / Copenhagen Zoo

Birds as provider of ecosystem services at Bukit Barisan Selatan National Park, Indonesia Nurul L. Winarni1 and Indartono Sosro Wijoyo2 Research Center for Climate Change – University of Indonesia. Gd. PAU lt. 8.5. Kampus UI Depok. Indonesia. Deparment of Biology, Faculty of Mathematics and Science – University of Indonesia. Gd. E FMIPA UI. Kampus UI Depok.

1 2

Corresponding author: Nurul L. Winarni, email: [email protected] Abstrak Burung-burung frugivora dan nektarivora dikenal sebagai penyedia jasa ekosistem dalam bentuk polinasi dan penyebaran biji. Struktur dan komposisi burung di tepi hutan kawasan Taman Nasional Bukit Barisan Selatan dievaluasi. Transek disiapkan pada tiga lokasi berbeda di areal Pemerihan yang melalui tepi hutan dan kebun pertanian. Survei burung dilakukan dengan metode titik hitung, yang dilaksanakan pada bulan Juli-September 2012 di daerah Sumberejo-Pemerihan. Survei vegetasi juga dilakukan pada setiap titik. Hasil penelitian memerlihatkan batas yang jelas pada struktur habitat antara tepi hutan dan kebun pertanian meskipun terdapat perambahan di tepi hutan. Keanekaragaman burung serupa antara kedua tipe habitat. Terdapat tiga jenis burung cucak-cucakan (Pycnonotidae) umum yang mengkarakterisasi komposisi burung sepanjang tepi hutan. Kehadiran burung cucak-cucakan sebagai penyebar biji mengindikasikan terakselerasinya regenerasi alami dalam kawasan tersebut. Abstract Frugivores and nectarivores birds are known to provide ecosystem services in the form of pollination and seed dispersal. In the forest edge of Bukit Barisan Selatan National Park the structure and species composition of birds was evaluated. Transects were set up at three different locations in the Pemerihan area, traversing both forest edge and agricultural gardens. Birds were surveyed using point counts, which were carried out during July-September 2012 in the Sumberejo-Pemerihan area of the national park. Vegetation surveys were also undertaken at each point. The results suggest a clear demarcation of habitat structure between forest edges and agricultural gardens, although encroachment was present in the forest edge. Bird diversity was similar between the two habitat types. Three common bulbul species characterized the bird composition along the forest edge. The presence of bulbuls as seed dispersers may indicate that natural regeneration is accelerated within the area. Keywords: birds, bulbuls, ecosystem service, forest edge, vegetation structure

Introduction Ecosystem services are the processes and the conditions of natural ecosystems that support human activity and sustain human life (Chapin III et al., 2000). In line with this, forests provide ecosystem service such as controlling local and global climate, soil erosion, maintenance of other ecosystem processes (seed dispersal, pollination), as well as carbon storage

Received 2nd February, 2014; Second revision accepted 27th April, 2015

2014 Journal of Indonesian Natural History Vol 2 No 2

(Böhning-Gaese, 2012; Locatelli et al., 2008; Wenny et al., 2011). Important ecological processes such as pollination and seed dispersal are carried out by birds, insects and mammals, for example, bats, large mammals and primates (Bodmer, 1991; CamposArceiz et al., 2011, 2008; Culot et al., 2010; de Marco and Coelho, 2004; Giombini et al., 2009; Kremen, 2005; Wotton and Kelly, 2011). Pollination and seed dispersal services contribute to human well-being by improving production of agricultural, fibre, timber and non timber forest products commdities (Hougner et al. 2006; Kremen et al. 2007; Traveset et al., 2012; Whelan et al., 2008). The ongoing deforestation influences

17

Birds as provider of ecosystem services

pollination and seed dispersal processes negatively and has serious impact on forest regeneration. Successful natural reforestation of native plant species in degraded areas from seeds dispersed by animals depends on distance from the nearest source forest, seed rain, plant species composition in the source forest and the rate of seed predation (Cole et al., 2010; Guevara et al., 2004; Harvey, 2000; Shono et al., 2006; Teegalapalli et al., 2009; Wotton and Kelly, 2011). Ricketts (2004) suggested that the distance between forest fragments will increase the activity of coffee pollinating agents. For this to take place, however, pollination agents and agents of seed dispersers must be present. Birds are known as important pollinators and seed dispersers and play an important role in facilitating the recolonization of natural vegetation in degraded areas (Borges, 2007; Caves et al, 2013; Clout and Hay, 1989; Duncan and Chapman, 1999; Padilla et al, 2012; Sekercioglu, 2006), as long as perching sites, the complexity of vegetation structure and suitable food sources are available (Duncan, 2006 ; Holl, 1999; Sekercioglu et al. 2002; Wunderle, 1997). Bukit Barisan Selatan National Park (BBSNP) in Southern Sumatra contains important populations of endangered wildlife species, including Sumatran rhinoceros, Dicerorhinus sumatrensis, Sumatran tiger, Panthera tigris sumatrae, elephant, Elephas maximus sumatrensis and over 300 bird species. Surrounded by human settlements, BBSNP is also important to the livelihood of the surrounding community, being the source of many types of non-timber forest products. Unfortunately, the human activities have lead to continuous deforestation at a rate of 1.69% per year between 1972-2002 (Gaveau et al., 2007). In the last three decades, forest cover has been reduced by 50% (3,470 km2) in West Lampung and South Bengkulu, the districts in which the park lies, and by 17% (520 km2) in the park (Gaveau et al., 2007). Although forest regrowth occur, illegal agricultural encroachment continues at an unabated rate, resulting in a net forest loss. The development of lowland coffee (Coffea robusta) plantations within park boundaries constitutes one of the major challenges, as deforestation rates appear to be linked to Global robusta prices (O’Brien and Kinnaird, 2003). Rice, coconut, damar, and pepper are other popular crops produced at the expense of BBSNP’s forest habitat (Gaveau et al., 2007). Due to its elongated shape BBSNP has over 700 km of boundaries and is particularly vulnerable to fragmentation by

18

encroachment from human settlements surrounding it. Roads bisect the park in two areas, one in the north and one in the south. As humans settle along these roads, villages are formed and residents begin to plant and expand their gardens and fields, which have create in gaps that exceed 3 km at certain places. The lowland dipterocarp forest of BBSNP is a key habitat for animal pollinators and seed dispersers. Several hornbill species are wide-ranging species and are described as effective seed dispersers (Holbrook and Smith, 2000; Holbrook et al, 2002; Kinnaird and O'Brien, 2007; Kitamura, 2011; Lenz et al., 2010; Whitney et al., 1998). Biodiversity is an integral part of ecosystem services, and by preserving the integrity of forest edge of the park, pollination and seed dispersal agents are maintained. Deforestation may decrease the diversity of pollinating and seed dispersing agents and with a significant negative effect to agricultural crop production (de Marco and Coelho, 2004). There remain limited information about pollinators and seed dispersers associated with forest edge, and to what degree they support the integrity of the forest edge, as well as agricultural production adjacent to the park boundary. This study aims at evaluating the community composition of bird species as provider of ecosystem services along the edge of Bukit Barisan Selatan National Park.

Methods Study Area This study took place in Bukit Barisan Selatan National Park (BBSNP), Sumatra, from July-September, 2012. This park is the third largest protected area (3,568 km2) in Sumatra and located in the southwestern part of Sumatra, spanning the two provinces of Lampung and Bengkulu (O’Brien and Kinnaird, 1996). BBSNP contains the largest tracts of lowland rain forest remaining in Sumatra, with an incredible high species diversity that includes the critically endangered Sumatran tiger (Panthera tigris sumatrae) and Sumatran rhino (Dicerorhinus sumatrensis) along with an abundance of primates and more than 200 species of birds. BBSNP is the primary watershed for southwest Sumatra (O’Brien and Kinnaird, 1996). The fieldwork was carried out along the Pemerihan River at the boundary of Bukit Barisan Selatan National Park (Lat -5.61527045, Lon 104.39306726), with

© University of Andalas / Copenhagen Zoo

Winarni and Wijoyo

Figure 1. Study area in Pemerihan area of the Bukit Barisan Selatan National Park (BBSNP) with position of transects along forest within the park and agricultural gardens

serious encroachment (Suyadi and Gaveau, 2007). The three study sites were at Sumberejo, Pemerihan Atas and Pemerihan Bawah, with study plots setup in the ecotone between forest edge and agricultural fields. Bird Survey Bird surveys were conducted using point counts (Bibby et al., 2000). We selected three sites (Pemerihan bawah, Pemerihan atas, and Sumberejo) and setup monitoring plots (transects) along the forest edge of Bukit Barisan Selatan National Park around the Pemerihan area. Two transects of 2km at each site were set up at both side of the edge at positions parallel to each other (Fig.1). Points were set up on the bird survey transects at 200m interval. Bird point counts were carried out for 10 minutes at each point. Surveys were carried out for during July-September 2012. Vegetation survey Concurrently with the bird surveys, we set up 72 PointCentered Quartered (PCQ) plots with 20m radius

2014 Journal of Indonesian Natural History Vol 2 No 2

following Shukla and Chandel (1996). PCQs were divided into four quadrants and habitat variables were identified and quantified within these. At each PCQ we identified the four nearest trees to the centre and recorded the species, diameter at breast height (DBH), distance from the central point, canopy openness and the under-storey vegetation density. At the four nearest trees, we conducted phenology observation during three months of survey (July-September 2013) by estimating the proportion of flowering and fruiting in the canopy. This was estimated using four categories (1 = 0 – 25%; 2 = 26 – 50%; 3 = 51 – 75%; 4 = 76 – 100%) following Kinnaird et al. (1999). Vegetation analysis Principal Component Analysis (PCA) was used to determine the main characteristics of vegetation structures and habitat types. Vegetation structures used for the analysis were canopy openness, under-story density, mean girth of large trees, number of cultivated trees, and flower and fruit phenology during July – September 2012. The

19

Birds as provider of ecosystem services Table 1. Habitat structure at the border of BBSNP

Location

Forest PA

Forest PB

Forest SR

Agri PA

Agri PB

Agri SR

Tree girth (m) (average)

16.31

15.16

16.75

17.73

16.99

15.63

Distance of trees (m)

2.46

2.76

3.00

2.38

2.68

1.97

Canopy openness

0.09

0.36

0.06

0.34

0.44

0.59

Understorey

0.59

0.66

0.61

0.12

0.10

0.12

Count of % Flower 1

0.00

2

1

9

21

16

Count of % Fruit 1

1

13

0.00

9

22

19

Count of % Flower 2

4

5

7

17

28

5

Count of % Fruit 2

10

14

4

12

26

12

Count of % Flower 3

7

10

10

14

24

10

Count of % Fruit 3

3

7

8

17

26

14

Total plant species

29

26

32

9

10

7

Coffea robusta

0

0.00%

0

10.83%

4.17%

18.33%

Erythrina - pepper

0

0.83%

0

10.83%

5.00%

12.50%

Cacao

0

2.50%

0

10.00%

23.33%

1.67%

PA = Pemerihan Atas, PB = Pemerihan Bawah, SR = Sumberejo Table 2. Principal component of vegetation structure in the two habitats with factor loadings > 0.40 PC1

PC2

PC3

Eigen Value

4.09

3.00

1.63

% of Variance

31.45

23.08

12.52

Cumulative %

31.45

54.53

67.05

Average of % Fruit (Sep)

0.82

Average of % Flower (Sep)

0.79

Average of % Fruit (Aug)

0.74

Cacao (count)

0.74

Average of % Fruit (Jul)

0.72

Average of % Flower (Aug)

0.68

Average of % Flower (Jul)

0.59

0.45 0.49

Cultivated plants (count)

0.86

Erythrina - pepper (count)

0.81

Average of understory plants (%)

-0.77

Coffea Arabica (count)

0.63

Average of DBH (cm) Average of Canopy openness (count)

0.52 -0.77

0.40

0.55

first and second Principal Component (PC) scores were plotted graphically. We used Discriminant Function Analysis (DFA) to determine the rate of vegetation structure misclassification between habitat types to

20

identify the degree of overlap between the forest and agricultural gardens. Bird Analysis The bird communities from the different habitat types were compared using Shannon-Wiener and Simpson Indices (Magurran, 2004). We used t-test to test for any differences in abundance of the three bird guilds at two habitat types. Bird assemblages within the two habitat types were categorised by guild abundance (1 = frugivores, 2 = partial frugivores/insectivores, 3 = nectarivores) at the inner forest, the middle and edge of the forest, the edge of agriculture/forest, the middle of agricultural fields, the outer of agriculture fields, strata (1 = terrestrial and under-storey, 2 = mid-canopy, 3 = canopy) and morphological cue (1 = indistinct, 2 = intermediate, 3 = distinct). The data were then clustered using hierarchical clustering and tested by DFA. Results from these analyses were tested using binary logistic regression to evaluate, if the presence-absence of a particular species was correlated to habitat structures such as DBH of four nearest trees, average distance of four nearest trees, canopy openness, under-storey, and presence of cultivated trees in the study plots. The occurrence of bird species was calculated using Indicator Value (IV) following Dufrene and Legendre (1997).

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Winarni and Wijoyo

Figure 2. Percentage of dominant cultivated plants in the forest edge and agriculture gardens

Figure 3. Distribution of vegetation plots along PC1 and PC2 of the Principal Component Analysis

Results Habitat structure on forest edge We recorded 69 species of tree species in the forest transects and 13 tree species in agricultural garden

2014 Journal of Indonesian Natural History Vol 2 No 2

transects. All trees in the agricultural plots were cultivated trees (Appendix 1). Three cultivated plants, coffee, Coffea robusta (83.3%), Erythrina lithosperma (70.8%), and cacao, Theobroma cacao (87.5%) were the most common tree species in the agricultural gardens

21

Birds as provider of ecosystem services

(Fig. 2; Tab. 1). Cultivated plants such as E. lithosperma (31.2%) and cacao (6.25%) were also recorded in the forest area. The Erythrina trees were used to support pepper plants (Piper aduncum). Although cultivated trees were recorded in the forest plots, the PCA analysis suggested that there was clear demarcation between forest and agriculture fields. Flowering and fruiting were mostly recorded in the agriculture fields (Table 1). Principal Component Analysis (PCA) showed that each component explains only a small percentage of the original variation and that the four together explain less than 69% of the variation and that the three together explain 67% of the variation (Table 2; Figure 3). The first component was characterized by higher flowering and fruiting and higher percentage of cacao. The second component represented the open areas dominated by cultivated trees (Coffee and Erythrina trees). The distinct separation between forest and agriculture fields was also supported by the Discriminant Function Analysis that suggested 98.6% of point count sites were correctly assigned to their habitat types. The classification success ranged between 97.2 – 100%. Bird structure and composition We recorded 47 bird species (frugivores, partial frugivores-insectivores, nectarivores) (Appendix 2) of which most were considered to be generalist. Rhinoceros hornbill (Buceros rhinoceros) and helmeted hornbill (Buceros vigil) were recorded in the forest edge, but not observed in agriculture gardens. Bird diversity in the forest sites and agriculture gardens were similar (Fig. 4; Shannon diversity index t = - 0.643, df = 4, P > 0.05; Simpson diversity index t = -0.194, df = 4, P > 0.05). The number of partial frugivores-insectivores was higher than frugivores and nectarivores. Black-capped bulbuls (Pycnonotus melanicterus) were recorded mostly in the forest, while the agricultural gardens was dominated by Sooty-headed bulbuls (Pycnonotus aurigaster) and Yellow-vented bulbuls (Pycnonotus goiavier). The cluster analysis put the bird assemblage into two separate groups (Fig. 5). The first group contained the most species recorded in the survey without specific characteristics. The second group was mostly Pycnonotidae, which was abundant around the edge and agriculture, such as P. aurigaster, P. goiavier and P. melanicterus (Fig. 5). The results from testing the three species using binary logistic regressions showed that both P. goiavier (66.7% correctly classified, P = 0.011)

22

Figure 4. Diversity indices (Shannon-Wiener’s and Simpson’s) of birds within forest edge of BBSNP

and P. aurigaster (70.8% correctly classified, P = 0.041) were correlated to the average distance to the nearest trees, while P. melanicterus was not significantly correlated to habitat structures (P = 0.117). Similar results were evident from the Indicator Value. Sooty-headed bulbuls were present at 75% of all plots indicating the high IV, while in the forest the IV for all species was less than 50% in all plots. Black-capped

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bulbuls were more common in forest plots. A complete list of birds including the Indicator Value (IV) is presented in Appendix 2.

Discussion Bird structure on forest edge Birds often have very specific habitat preferences (Cody, 1985) and changes to the tree density, and floristic composition will affect the composition of the bird community and the predominance of different bird guilds (Barlow et al, 2006; Duncan, 2006 ; Holl, 1999; Raman et al., 1998; Sekercioglu et al. 2002; Traveset et al., 2012). The forest edge, however, was not attractive to nectarivores bird species, but to “partial frugivores” species that also consume insects (Corlett and Hau, 2000). Plants within the agriculture sites seemed to offer a higher volume of nectar producing flowers than the forest (Table 1), although this did not affect the number of nectarivores species present in our study sites. Several species of bulbuls (Pycnonotidae sp.) are known for their tolerance for human-disturbed areas and secondary forest (Corlett and Hau, 2000). As facultative frugivore consumers, bulbuls are important seed dispersers and colonists (Corlett, 1988) as they eat the small fruits of pioneer trees (Thornton, 1997). Their high abundance in the forest edge may be an indicator that regeneration of the forest edge is slowly taking place. Thornton (1997) described that two bulbul species, the Sooty-headed bulbul (P. aurigaster) and the Yellow-vented bulbul (P. goiavier) were the first to colonise Krakatau island within the first 25 years after eruption, they may be able to carry seeds long-distance. In our study, the tree bulbul species, including the Black-capped bulbul (P. melanicterus), were the most common species along the edge of the national park. The high abundance of Black-capped bulbuls at the forest edge suggests that the species could play an important role in restoration of secondary forest (Wunderle, 1997). Forest edge may be able to attract seed dispersing birds depended on agricultural gardens, where food availability remains high (Parrotta et al., 1997). Corlett and Hau (2000) added that proximity of fruiting trees is important to attract seed dispersers, although this study suggested that many species made use of resources available in agricultural gardens. The presence at high abundance in the forest edge may be an indicator of regeneration function of forest edge. This is supported by the highest IV. Structural

2014 Journal of Indonesian Natural History Vol 2 No 2

complexity which depicted by the closed canopy, dense under-story, no or less agricultural plants were important forest characteristics that attract bird species (Wunderle, 1997). The forest may also attract frugivory (Janzen, 1988), although this should be further studied as this is related to the presence of wind-dispersed versus animal-dispersed trees. Implication to forest edge of national park Seed dispersing birds constitute one of the important factors that can help accelerate the natural regeneration of a forest (Caves et al, 2013; Clout and Hay, 1989; Duncan and Chapman, 1999; Hardwick et al., 2004; Padilla et al, 2012; Sekercioglu, 2006). Sooty-headed and Yellow-vented bulbuls are known to prefer habitat with close spacing of trees with an abundance of perching sites (Gorchov et al., 1993; Medellin and Gaona, 1999). The presence of known seed dispersing bird species suggests that the habitat at our forest study site is attractive to these species, and that regeneration may take place in the area. The area around Pemerihan at the boundary of Bukit Barisan Selatan National Park has been subject to illegal logging since 1998 (Suyadi and Gaveau, 2007). The presence of cultivated plants within the forest at the edge suggests that, while deforestation is a threat to the Pemerihan area, according to Hardwick et al. (2004) the presence of seed-dispersing birds is accelerating the natural regeneration process within the area. The lowland habitats of BBSNP have been subjected to deforestation at a higher rate than hilly areas (Kinnaird et al., 2003), and the clear demarcation between the forest and agricultural plots can be considered positive. Cultivated trees were mostly confined to agricultural gardens, although some pepper trees have invaded the forest at the boundary. Canopy openness and under-story density were reciprocal between forest and agricultural gardens. Forests around the edge of BBSNP have more structural complexity with dense under-story, offering more ecological appeal to seed dispersers. In addition, this separation seemed to support habitat segregation among the three bulbuls, in which the Black-capped bulbuls were more confined to forest edge, while the other two species were more abundant in agricultural gardens. The Black-capped bulbul is probably the first species to colonize degraded forest (Corlett and Hau, 2000). Therefore the fate of the remaining forest may be depended on the presence of seed dispersal agents.

23

Birds as provider of ecosystem services

Acknowledgement This work was carried out under the project of the Research Centre for Climate Change – University of Indonesia funded by Rufford Small Grants for Nature. We would like to thank the head of Bukit Barisan Selatan National Park for the collaboration and permission to work in the park. We would also like to thank the Wildlife Conservation Society – Indonesia Program (WCS-IP), particularly Dr. Noviar Andayani and Meyner Nusalawo for their support and collaboration during our study. The fieldwork would have been impossible without the help of many people, Sephy Noerfahmi, Jaka Ramadhan, Prescillia Rindang Putri, Rahman, Janjiyanto, Marji, Maya D. Prasetyaningrum and the people of Pemerihan village.

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Teegalapalli, K., Hiremath, A.J. and D. Jathanna (2009). Patterns of seed rain and seedling regeneration in abandoned agricultural clearings in a seasonally dry tropical forest in India. Journal of Tropical Ecology 26: 25 doi:10.1017/S0266467409990344 Thornton, I.W.B. (1997). Krakatau: The destruction and reassembly of an island ecosystem. Harvard University Press, Boston. Traveset, A., González-Varo, J.P. and A. Valido (2012). Long-term demographic consequences of a seed dispersal disruption. Proceedings of the Royal Society B 279: 3298–3303. doi:10.1098/rspb.2012.0535. Wenny, D.G, Devault, T.L., Johnson, M.D., Kelly, D., Sekercioglu, C.H., Tomback, D.F. and C.J. Wheelan (2011). The need to quantify ecosystem services provided by birds. The Auk 128: 1–14. doi: 10.1525/ auk.2011.10248 Whelan, C.J., Wenny, D.G. and R.J. Marquis (2008). Ecosystem services provided by birds. Ann. NY. Acad. Sci. 1134: 25–60, doi:10.1196/annals.1439.003. Whitney, K.D., Fogiel, M.K., Lamperti, A.M., Holbrook, K.M., Stauffer, D.J., Hardesty, B.D., Parker, V.T. and T.B. Smith (1998). Seed dispersal by ceratogymna hornbills in the Dja Reserve, Cameroon. Journal of Tropical Ecology 14(3): 351-371. Wotton, D.M. and D. Kelly (2011). Frugivore loss limits recruitment of large-seeded trees. Proceedings of the Royal Society B 278: 3345–3354. doi: 10.1098/ rspb.2011.0185 Wunderle Jr, J.M. (1997). The role of animal seed dispersal in accelerating native forest regeneration on degraded tropical lands. Forest Ecology and Management 99:223-235.

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Short communications

Sacred uses of Indo-Malay native fruits in Balinese Adat Ida Bagus Ketut Arinasa1 and Wawan Sujarwo1,2 Bali Botanic Garden, Indonesian Institute of Sciences (LIPI), Candikuning, Baturiti, Tabanan, Bali, Indonesia Department of Science, University Roma Tre, Viale G. Marconi 446 Rome Italy

1 2

Corresponding author: Wawan Sujarwo, email: [email protected]; [email protected]

Introduction Every Balinese traditional ceremony make use of different plant species for various tributes. The five basic traditional ceremonies practiced among the Hindu community in Bali are known as Panca yadnya. Panca means five and Yadnya means a pure praise or tribute to God. The five ceremonies are know as: Dewa yadnya - the worship of divinities. Pitra yadnya - offerings to ancestors. Resi yadnya - a tribute to spiritual leaders. Manusa yadnya - feeding and praise of human beings. Bhuta yadnya - feeding and praise of all living creatures. The Manusa yadnya traditions consist of a range of ceremonies - engagement, marriage, birth and cremation. Manusa yadnya ceremonies also include Megedonggedongan for the unborn baby; Tutug kambuhan for 42 days old babies; Telu bulanan for 105 days old babies; Otonan for 210 days old babies; Menek bajang for the youth; Mesangih or Metatah for tooth filling. In daily practice, the ceremonies cannot be separated, because they form a continuous process with each step engulfing a meaningful value; a manusa yadnya ceremony is always followed by the dewa yadnya, pitra yadnya, resi yadnya and bhuta yadnya ceremonies. Plants and other natural components are very important ingredients of all the ceremonies. Animals, toyam (holy water), dipan and dupa (holy fire), and mantram are also used for the ceremonies, as noted in the sacred Hindu text (Bagawadgita IX, 1928). Panji (1979) described that whole plants or part thereof e.g. leaves (sarwa pattram ), flowers (sarwa puspam), Received 15th August, 2014; Revision accepted 2nd April, 2015.

2014 Journal of Indonesian Natural History Vol 2 No 2

stems and fruits (sarwa phalam) are used in Balinese ceremonies. Wedding ceremonies (manusa yadnya) use all the components above. The traditional Balinese ceremonies, as described in Lontar Agastia Purana (1928), make use of plant derivatives from the Indo-Malay region, as well as other locations. This paper will discuss the use of fruits from, primarily, the Indo-Malay region in Balinese engagement and wedding ceremonies.

Methods Information about the Balinese ceremonies was collected through interviews with the religious leaders, tukang banten and through observation of actual Balinese wedding ceremonies. The tukang banten is responsible for building the facilities and preparing the tools for the ceremony, while religious leaders are Hindu spiritual leaders. The ceremony described in this paper took place at Penarukan Village, Buleleng District, Bali.

Results and discussion Engagement ceremony The engagement ceremony is known as memadik, meminang and merangkat and is the first to be undertaken prior to the wedding ceremony. The memadik ceremony is performed in five consecutive steps, although it may vary depending on the place (desa), time (kala) and condition (patra) of the area as well as the community where the ceremony is going to be held. Sudarta (1979) describes the procedures in a Balinese engagement ceremony include:

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Sacred use of native fruits

1. Pengrawat/ngokasang A family member of the groom visits the bride’s family to validate if the bride has had any previous relationship with other man. No ceremony is undertaken at this time. 2. Penangsek/penegasan Selected family members of the groom and his followers visit the bride’s family to propose, but no ceremony is held at this time. 3. Memadik A ceremony is held with more of the groom’s relatives, and a traditional leader (brahmana) visits the bride’s house with gifts usually of fruits and snacks (canang pengerawos, rarapan and canang wakul). Before starting the engagement deliberations a family member of the groom hands over the gifts to the bride’s family seeking God’s blessings to ensure that the engagement negotiations are successful. Banten, canang, and pengerawos contain fruits of the pinang palm (Areca cathecu) and betel (Piper betle). The groom’s family also gives rarapan (fruits, vegetable and various kinds of cake) as symbols of the families. The fruits are not necessarily special types of fruits but whichever is in season, for example, bael (Aegle marmelos), menteng (Baccaurea racemosa), mangosteen (Garcinia mangostana), langsat (Lansium domesticum), mango (Mangifera indica), banana (Musa paradisiaca), rambutan (Nephelium laplaceum), Crab apple (Pyrus malus), Chinese pear (Pyrus pyrifolia), jackfruit (Artocarphus heterophyllus), breadfruit (Artocarpus altilis), salak (Salacca edulis) and grapes (Vitis vinifera). Vegetables such as common beans (Phaseolus vulgaris) and winter squash (Cucurbita moschata) are also commonly used. Other kinds of rarapan are various kinds of cake typically made from flour of rice (Oryza sativa), glutinous rice (Oryza sativa var. glutinosa), maize (Zea mays) and sorghum (Sorghum bicolor). 4. Mejantos A few days before the transfer day, the groom’s entourage brings basan tamba - cosmetics made from floral plant materials - a ring, fabric and clothes for the woman (pesalin), canang ajengan and canang wangi (flower and food offerings for the spirits). The most important deliberation of the mejantos is the transfer day. Banten, canang, pengerawos and rarapan are also held together with the memadik session. The basan tamba is made from parts of mature fruits of the Indian rose chestnut (Mesua ferrea) mixed with a powder made of seeds, bark and flowers of the plant to create a cosmetic that is given to the bride.

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5. Hari pengambilan/nganten The bride is transferred to the groom’s house. This ceremony is held with canang wangi, canang pemendak, dakshina ceremony while the bride doning a yellow veil (kerudung kuning). The Banten dakshina is performed as a praise for the Gods with the purpose of announcing the transfer day. Many species of fruits are used for the banten dakshina such as coconut (Cocos nucifera), candlenut (Aleurites moluccana), butter bean (Phaseolus lunatus), lablab (Dolichos lablab), Goa bean (Psophocarphus tetragonolobus), rice (Oryza sativa) and glutenous rice (Oryza sativa var. glutinosa). Approximately 21 different fruits species are used for the five consecutive parts of the engagement ceremony (see Table 1). Wedding ceremony The Medengen-dengen or mekalah-kalahan ceremony is one of the most important of the Balinese wedding ceremony (Agastia, 1995). A ceremony is undertaken in a yard near to the most sacret Hyang Gni, or in a temple with the purpose of eliminating potential objections to the wedding. Family members of the groom and the bride, along with community members, religious leaders and government officials appear as witnesses. Leaves, flowers, stems and fruits from a variety of plant species are used for this ceremony and often joined together as banten. The different kinds of banten in the wedding ceremony include: offerings and tributes (suci, sesayut nganten, tebasan, prasista, pengambean, pulagembal, pejati), soul purifying (biakaon), fruit decoration (pajegan, raka-rakaan), offering tools (caru patemon, kuangen, tegen-tegenan), vegetables potpourri (janganan), food offerings (ajuman), rice boiling tool (tipat kelanan) and traditional baskets for carrying offerings (sok pedagangan). Balinese banten suci is a praise for the God and very important. The ritual it is very complex, because it consists of many kinds and parts of plant materials e.g. fruits, leaves, flower, tuber and even animal derivatives. In addition, the various offerings and trinkets are traditionally placed in containers made of palm leaves and known as tamas. Each offering is placed in a special type of tamas specifically made for it. Fruits involved in banten suci are: 1) Plants and derivatives such as butter bean (Phaseolus lunatus), eggplant (Solanum ngelongena), Goa bean (Psophocarphus tetragonolobus), Hyacinth bean

© University of Andalas / Copenhagen Zoo

Arinasa and Sujarwo

(Dolichos lablab), bitter gourd (Momordica charantia) and papaya (Carica papaya) are put in tamas lampadan. 2) Bananas (Musa paradisiaca) are placed in tamas tetamper.

wedding ceremony come from outside the Indo-Malay region, three species are of unknown origin and 48 species are native to the Indo-Malay region. Many of these (36) are grown for cultural conservation purposes in Bali Botanical Garden.

3) Tamarind (seed of Tamarindus indica) is placed in tamas sajen.

References

4) Cucumber (Cucumis sativus), salak (Salacca edulis), jackfruit (Artocarpus heterophylus), Indian mango (Mangifera indica) and banana (Musa paradisiaca) are placed in tamas sancak.

Agastia, I.B.G. (1995). Panca Yadnya, Dewa Yadnya, Bhuta Yadnya, Resi Yadnya, Pitra Yadnya, Manusa Yadnya. Dinas Kebudayaan Pemerintah Provinsi Bali, Denpasar.

5) Noni (Morinda citrifolia) and sugar palm (Borassus flabellifer) are placed in tamas madu kalpa.

Bagawadgita IX. (1928). Sacred Balinese Texts Written on Palm Leaves. Gedong Kirtya library, Singaraja, Bali, Indonesia.

In addition, many kinds rice, for example, (Oryza sativa), glutenous rice (Oryza sativa var. glutinosa) and black rice (Oryza sativa var. nigra) form the ingredients of cakes in banten suci. Among 103 plant species used in a Balinese wedding ceremony, some have a special purpose such as noni (Morinda citrifolia), Indian rose chestnut (Mesua ferrea), tamarind (Tamarindus indicus), banana (Musa paradisiaca), and sugar palm (Borassus flabellifer). Some fruits are used in both the engagement and wedding ceremonies, either processed further into different kinds of snacks or mixed with other fruits. Lontar Widisastra (1928) describes that the shells of coconuts (Cocos nucifera) are carved into a Lingga Yoni symbolising the groom and bride in the ceremony. Twenty two species of fruits used in the Balinese

2014 Journal of Indonesian Natural History Vol 2 No 2

Lontar Agastina Purana. (1928). Sacred Balinese Texts Written on Palm Leaves. Gedong Kirtya library, Singaraja, Bali, Indonesia. Lontar Widisastra. (1928). Sacred Balinese Texts Written on Palm Leaves. Gedong Kirtya library, Singaraja, Bali, Indonesia. Panji, I.G.B.N. (1979). Jajahitan Bali Serta Fungsinya [Balinese Customs and Practices]. Proyek Sasana Budaya Bali, Denpasar. Sudarta. (1979). Panca Yadnya: Proyek Peningkatan Sarana dan Prasarana Kehidupan Beragama [Infrastructure Improvement of Religious Life]. Dinas Kebudayaan Pemerintah Provinsi Bali, Denpasar.

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Sacred use of native fruits

Table 1. A list of plants used in the five parts of a traditional Balinese engagement ceremony (E) and wedding ceremony (W). 36 species are currently grown at the Bali Botanical Garden.

No Latin Name

Local Name

Family

Uses

Origin

1

Aegle marmelos (L.) Corrêa

Bila

Rutaceae

W

Indonesia

2

Aleurites moluccanus (L.) Willd.

Tingkih

Euphorbiaceae

E, W

Indonesia

3

Ananas comosus (L.) Merr.

Manas

Bromeliaceae

W

Latin America

4

Annona muricata L.

Srikaya

Annonaceae

W

Tropical America

5

Annona squamosa L.

Silik

Annonoceae

W

Tropical America

6

Antidesma bunius (L.) Spreng.

Buni

Phyllanthaceae

W

South East Asia

7

Areca catechu L.

Buah

Arecaceae

E, W

Indonesia

8

Arenga pinnata (Wurmb) Merr.

Jaka

Arecaceae

W

Indonesia

9

Artocarpus altilis (Parkinson ex F.A.Zorn) Fosberg

Timbul, Sukun

Moraceae

W

South East Asia

10

Artocarpus heterophyllus Lam.

Nangka

Moraceae

W

Malaysia

11

Averrhoa carambola L.

Blimbing besi

Oxalidaceae

12

Baccaurea racemosa (Reinw. ex Blume)

Kepundung

Phyllanthaceae

13

Borassus flabellifer L.

Ental

14

Capsicum annuum L.

15

Carica papaya L.

16

Citrullus lanatus (Thunb.) Matsum. & Nakai

W

South East Asia

E, W

Indonesia

Arecaceae

W

India, Indonesia

Tabia, Cabai

Solanaceae

W

Tropical America

Gedang

Caricaceae

W

America

Semangka

Cucurbitaceae

W

South Africa

17

Citrus aurantiifolia (Christm.) Swingle

Juwuk lengis

Rutaceae

W

Asia

18

Citrus × aurantium L.

Juwuk peres

Rutaceae

W

China

19

Citrus amblycarpa (Hassk.) Ochse

Limo

Rutaceae

W

Indonesia

20

Citrus limon (L.) Osbeck

Juwuk purut

Rutaceae

W

Asia

21

Citrus maxima (Burm.) Merr.

Juwuk bali

Rutaceae

W

South East Asia

22

Citrus nobilis Lour.

Sumaga

Rutaceae

W

Asia

23

Citrus sinensis (L.) Osbeck

Juwuk manis

Rutaceae

W

Asia

24

Cocos nucifera L.

Nyuh, Kelapa

Arecaceae

E, W

South East Asia

25

Coffea arabica L.

Kopi bali

Rubiaceae

W

Ethiopia

26

Coriandrum sativum L.

Ketumbah

Apiaceae

W

Central Asia

27

Cucumis melo L.

Melon

Cucurbitaceae

W

Middle East

28

Cucumis sativus L.

Ketimun

Cucurbitaceae

W

Unknown

29

Cucurbita moschata Duchesne

Waluh

Cucurbitaceae

W

Unknown

30

Durio zibethinus L.

Duren

Malvaceae

E,W

Indonesia

31

Dimocarpus longan Lour.

Longan

Sapindaceae

W

Thailand, China

32

Garcinia dulcis (Roxb.) Kurz

Mundeh

Clusiaceae

W

Indonesia

33

Garcinia parvifolia (Miq.) Miq.

Badung

Clusiaceae

W

Indonesia

34

Garcinia × mangostana L.

Manggis

Clusiaceae

E, W

Indonesia, Malaysia

35

Gossypium herbaceum L.

Kapas

Malvaceae

W

Indonesia

36

Lablab purpureus (L.) Sweet

Komak

Fabaceae

E, W

Unknown

37

Lansium parasiticum (Osbeck) K.C.Sahni & Bennet

Ceroring, Langsat

Meliaceae

E, W

South East Asia

38

Litchi chinensis Sonn.

Leci

Sapindaceae

W

China

39

Malus domestica Borkh.

Apel

Rosaceae

E, W

Indonesia

40

Mangifera caesia Jack

Wani

Anacardiaceae

E, W

Indonesia

30

© University of Andalas / Copenhagen Zoo

Arinasa and Sujarwo 41

Mangifera indica L.

Poh, Mangga

Anacardiaceae

E, W

South East Asia

42

Mangifera odorata Griff.

Poh pakel

Anacardiaceae

W

Indonesia

43

Manilkara zapota (L.) P.Royen

Sabo

Sapotaceae

W

Central America

44

Mesua ferrea L.

Nagasari

Calophyllaceae

E,W

South East Asia

45

Momordica charantia L.

Paya

Cucurbitaceae

W

Indonesia

46

Musa × paradisiaca L.

Biu, Pisang

Musaceae

E, W

South East Asia

47

Nephelium lappaceum L.

Buluan, Rambutan

Sapindaceae

E, W

South East Asia

48

Oryza sativa L.

Padi

Poaceae

E, W

Indonesia

49

Oryza sativa var. glutinosa

Ketan

Poaceae

E, W

Indonesia

50

Pangium edule Reinw.

Pangi

Achariaceae

W

Indonesia

51

Parartocarpus venenosa Becc.

Utu

Moraceae

W

Indonesia

52

Passiflora ligularis Juss.

Anggur bogor

Passifloraceae

W

South America

53

Phaseolus lunatus L.

Kacang barak

Leguminosae

E

America

54

Phaseolus vulgaris L.

Kacang lilit

Leguminosae

E,W

America

55

Piper betle L.

Base

Piperaceae

E, W

Indonesia

56

Piper nigrum L.

Mica

Piperaceae

W

India

57

Piper retrofractum Vahl

Tabia bun

Piperaceae

W

Indonesia

58

Psidium guajava L.

Sotong

Myrtaceae

W

Tropical America

59

Punica granatum L.

Delima

Lythraceae

W

Persia

60

Pyrus pyrifolia (Burm.f.) Nakai

Pir

Rosaceae

E, W

China

61

Salacca zalacca (Gaertn.) Voss

Salak

Arecaceae

E, W

Indonesia

62

Schleichera oleosa (Lour.) Merr.

Kesambi

Sapindaceae

W

Indonesia

63

Solanum melongena L.

Tuwung kanji

Solanaceae

W

Indonesia

64

Sorghum bicolor (L.) Moench

Jagung gembal

Poaceae

W

Indonesia

65

Spondias pinnata (L. f.) Kurz

Kedondong

Anacardiaceae

W

Indonesia

66

Syzygium aqueum (Burm.f.) Alston

Nyambu

Myrtaceae

W

Indonesia

67

Syzygium cumini (L.) Skeels

Juwet

Myrtaceae

W

Indonesia

68

Syzygium polycephalum (Miq.) Merr. & L.M.Perry

Kaliasem

Myrtaceae

W

Indonesia

69

Syzygium racemosum (Blume) DC.

Nyambu bol

Myrtaceae

W

Indonesia

70

Syzygium samarangense (Blume) Merr. & L.M.Perry

Nyambu semarang

Myrtaceae

W

South East Asia

71

Tamarindus indica L.

Asem, Celagi

Fabaceae

W

India

72

Vigna radiata (L.) R.Wilczek

Kacang ijo

Leguminosae

W

Indonesia

73

Vitis vinifera L.

Anggur

Vitaceae

E, W

West Asia

74

Zea mays L.

Jagung

Poaceae

W

Central America

2014 Journal of Indonesian Natural History Vol 2 No 2

31

Growth and survival rates of tree seedlings in a rehabilitation area of Central Kalimantan, Indonesia Ummi Farikhah1 and Carl Traeholt2 United Plantations Bhd / PT Surya Sawit Sejati, Central Kalimantan, Indonesia Copenhagen Zoo, Research and Conservation Division, Roskildevej 38, Copenhagen, Denmark

1 2

Corresponding author: Ummi Farikhah, email: [email protected]

Introduction Agricultural development has been one of the corner stones in developing human societies (Elasha, 2010; Larsen, 1995; Lipton et al., 2002; Marlowe, 2005; Ranis, 2004). Indeed, as of 2011 more than 1.3 billion people were active in agricultural production on the Earth (FAO, 2012), and agriculture continue to play a major part of most countries’ gross national product (FAO, 2012). In 2010 approximately 4.9 billion hectares of the Earth was allocated for some form of agriculture (FAO, 2012). Of this, palm oil plantations take up less than 0.5%, but due to the extraordinary high yields palm oil production is a key revenue earner for many countries, particularly, Malaysia and Indonesia, the World’s two largest palm oil producers. At a Global scale, palm oil occupies a very small land area compared to other food crops (e.g. wheat, maize, rice and soy) that occupies 10-15 times more land area per crop (FAO, 2010). Despite the relatively small land area used for palm oil production and the importance in contributing to nations’ economic development, the extensive landuse change has also come with significant environmental costs (Dermawan, 2001; Fuller et al., 2004; Greenpeace, 2008a, b, c; Greenpeace 2007; Koh, 2007; Malcolm et al., 2006; UNEP, 2007) with large tracts of intact tropical forested regions cleared for oil palm development (Koh et al., 2011; Carlson et al., 2013; Carlson et al., 2012). With the formation of the Round Table of Sustainable Palm Oil (RSPO) in 2004, the sector has seen a progressive shift towards environmentally sound development practices that increasingly integrates Received 15th August, 2014; Revision accepted 2nd November, 2014.

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environmental concerns into standard operational practices. In some cases RSPO-certified companies are required to rehabilitate degraded land and restore riparian zones to its original conditions. This also applies, when companies take over already degraded land or areas where previous owners were in violation of respective national environmental laws or the RSPO rules. The RSPO Principles and Criteria (RSPO, 2007) stipulate that member companies are responsible for rehabilitating land areas that were cleared in contravention of the RSPO P&C by its previous owner after 2000. Tropical forest rehabilitation can be a complicated and tedious process (Kettle, 2010), because different species require different sprouting, growth and survival conditions that are usually determined by micro-habitat (Dalling and Hubbel, 2002; Herault et al., 2010; Kettle, 2010; Rey et al., 2004), seed size (Baraloto and Forget, 2007; Khan, 2004; Rees and Venable, 2007; Ruger et al., 2011; Turnbull et al., 2012), competition (Baraloto et al., 2005; Gonzalez et al., 2010; Muscarella et al., 2013; Paz et al., 2005), predator pressure (Eichorn et al., 2010; Eichorn et al., 2007; Koricheva, 2002; Lamarre et al., 2012; Shuldt et al., 2012) and local light conditions (Baraloto and Forget, 2007; Bloor and Grubb, 2003; Kettle, 2010; Ruger , 2011). In addition, the significant time required to restore clear felled areas to tropical rainforests habitat means that very little practical knowledge is available to support and guide an effective rehabilitation and restoration programme of tropical forests in Southeast Asia. In areas, where oil palms have already been planted, restoration often begins with clearing and uprooting existing vegetation with subsequent planting of tree seedlings. Various tree species require different light and microhabitat conditions for optimal growth rate in the

© University of Andalas / Copenhagen Zoo

Farikhah and Traeholt

early and later growth stages (Baraloto et al., 2005; Bloor and Grubb, 2003; Kettle, 2010; Ruger et al., 2011). Some seedlings adapt well to elevated light exposure, though it may impair the growth rate, whereas overexposure to the sunlight inhibits growth rates for others (Krause et al., 2012; Krause et al., 2006). Many tropical rainforest tree species require shady conditions in the early stages of growth to reduce the negative effects of temperature and evaporation (Muscarella et al., 2013; Bloor and Grubb, 2003). Therefore, complete removal of existing palms may not necessarily provide suitable growth and survival conditions for some native tree seedlings and, consequently, clear felling of palms may not necessarily be advisable when restoring tropical forests habitat. This study aimed at testing the effect of three different rehabilitation approaches for the restoration of a tropical flooded forest in Central Kalimantan, Indonesia. Methods Study area The study area is located in Central Kalimantan, Indonesia (2°29’33.14”S; 111°47’32.86”E) and consists of 36ha of degraded freshwater swamp forest. The area was cleared and planted with oil palm in 2005, but because it contravened with the RSPO P&C, the new owner – an RSPO-member - set it aside for rehabilitation purposes. Since there had been no tree species inventory undertaken in the area prior to clear felling, the species composition was assumed to be similar to adjacent forests in Central Kalimantan. Acep Komara (2008) and Irwanto (2006) were used as additional guidance. Preparation of seedlings We collected and propagated seeds from 17 different tree species. In the rehabilitation process we focused on five species only, namely; Rengas (Gluta renghas), Ubar (Calophyllum castaneum), Idat (Cratoxylum arborescens), Belangiran (Shorea balangeran) and Penaga (Mesua sp). All five species were propagated in polybags and watered once per day for five months, before being out planted into the study area. Site preparation The study site was left without external treatment (weeding, fertilizer) for more than 12 months to prevent residual chemicals and/or fertilizer from influencing growth and survival rates of the tree seedlings.

2014 Journal of Indonesian Natural History Vol 2 No 2

Harvesting of the remaining oil palms continued at regular intervals. The study site was divided into three different categories; Category A: All planted oil palms remained and tree seedlings were planted between the palm rows in grids of 10m by 10m. Harvesting continued but no additional treatment (weeding, fertilizer) was carried out. Category B: 50% of the oil palms were uprooted and removed. Tree seedlings were planted in the empty palm rows in grids of 20m by 10m. Harvesting continued but no additional treatment (weeding, fertilizer) was carried out. Category C: All palms were uprooted and removed. Tree seedlings were planted in grids of 10m by 10m. A total of 1358 seedlings from five different species were planted in Plots A, B and C in the period 12th of January to 22nd of February, 2011. The growth rate (height) was measured in centimetres (cm) from substrate to highest leaf point; the trunk growth rate was measured in millimetres as the diametre at 20cm above substrate. Results Growth rates (Fig. 1) The growth rates measured in height (cm) and trunk diameter (mm) varied significantly between species and Pstudy lot. Compared across all three study plots, Rengas’ vertical growth rate (height, cm) was reversely correlated with its trunk growth rate (diameter, mm) (Pearson, r = -0.83). The growth rate patterns of Idat showed no correlation between height and trunk growth rates (Pearson, r = 0.03) and for Penaga there was a positive correlation between height and trunk growth rates (Pearson, r = 0.90). There were also no correlation between height and trunk growth rate across study plots of Ubar and Belangiran (Pearson, r = 0.03 and 0.027, respectively). Survival rates (Fig. 2) There was no significant difference in survival rate between the study plots when all species were combined (p>0.05, t-test). In each individual category, Rengas sp survived significantly better than Idat in Plot A and C (p