Journal of Indonesian Natural History

July 2014 Vol.2 No.1 Journal of Indonesian Natural History Editors Dr. Wilson Novarino Dr. Carl Traeholt Associate Professor for Biology Programme Director, Department of Biology Research and Conservation Division University of Andalas, 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 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 Institute of Technology, Indonesia WWF-Indonesia Dr. Matthew Linkie Dr. Jatna Supriatna Fauna & Flora International, Singapore University of Indonesia Dr. Erik Meijaard Dr. Campbell O. Webb People and Nature Consulting International, Indonesia The Arnold Aboretum, Harvard University, USA Dr. John Payne Dr. Zainal Z. Zainuddin Borneo Rhino Alliance, Malaysia Borneo Rhino Alliance, Malaysia

The Journal of Indonesian Natural History is published biannually by the Department of Biology at the University of Andalas, Padang, Barat, Indonesia, in collaboration with Copenhagen Zoo, Denmark. The Department of Biology at University of Andalas 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, University of Andalas, Indonesia in collaboration with Copenhagen Zoo, Denmark. It is available for free from www.jinh.net Cover photo: The beautiful Javan black-winged starling, Acridotheres melanopterus, known locally as Jalak Putih is almost extinct in the wild. It is listed as Critically Endangered on the IUCN red-list © Anaïs Tritto

2 © University of Andalas / Copenhagen Zoo Editorial Indonesia 20-years after ratifying the Convention on Biological Diversity - a status check

Carl Traeholt1 and Wilson Novarino2

1Copenhagen Zoo, Southeast Asia Programme, Malaysia 2University of Andalas, Padang, Sumatra

Corresponding authors: email: [email protected]

When the “Convention on Biological Diversity” also be supported by enforcement agencies and penal (CBD) was launched in 1992, it was an important codes formulated for law-breakers. It needs to be adopted milestone for the World’s conservation community and at provincial and district level too, and mainstreamed for the Global community as a whole. It was the first into local governance. Finally, it requires local citizens comprehensive far-reaching international agreement to embrace the idea and voluntarily make a concerted that attracted support from most nations across the attempt to manage their lives accordingly. Whereas Globe. For the first time in history, a majority of the policy formulation, legal framework development and World’s nations acknowledged the value of biological enforcement may seem daunting tasks, the biggest diversity and the impending crisis if nothing was challenges often remain with the local citizens and done to prevent the onslaught on the World’s natural transforming the current economic structure into a resources. Since then, the human population passed system that incorporates environmental and social 7.15 billion in July, 2013 (Worldometer, 2014), the total values into overall budget evaluations. The value of, for excretion of CO2 has grown more than predicted and example, “clean air” or the cost of “polluted water” is reached 34.5 billion tons in 2012 (Boden et al., 2011; inherently difficult parameters to incorporate into the Oliver et al., 2013; Peters et al., 2012. Raupach et al., current economic system. 2007), the dependency on fossil fuel is at its highest In a Global perspective, biodiversity conservation is ever, the Earth’s seas are getting increasingly polluted an enormous task that most nations are not yet willing to and overfished (FAO, 2011; Olden et al., 2007; Pham commit to --- at least not at a scale that makes real positive et al., 2014) and the destruction of tropical rainforests differences. The cost of managing, for example, the takes place at an unprecendent rate at all continents World’s terrestrial biodiversity sustainably is estimated with tropical rainforests (Hansen et al., 2013; Hansen et at approximately US$ 80 billion annually, and only 12% al., 2010; Margono et al., 2014, 2012). In light of this, is currently being committed to this task (McCarthy et it is tempting to claim that the Rio Convention merely al., 2012; CBD, 2012). Despite the Global community’s sputters on, and many have questioned its relevance in pledged support and commitment to CBD’s 2020 Aichi the 21st Century. targets there is a huge financial shortfall if all types Whilst the adoption of the Rio Convention is a straight of habitats (e.g terrestrial, freshwater, marine) should forwards process, the operationalization of it requires be sustainably managed. Some of the World’s largest far more commitment at national and international economies continue to pursue wealth creation through levels. The task for each nation and the international extraction based economic development despite the community is monumental. For the ideas behind the launch of many international policy intitiatives (e.g. Rio Convention to have real effect on the ground it REDD, Climate Change, UNEP Fi). requires that relevant national policies are formulated, Indonesia ratified the CBD on the 23rd of August, 1994, mainstreamed and implemented. This process requires exactly 20 years ago. So where does Indonesia rank in most sectors of society and governance to collaborate a conservation conext? Has there been any meaningful constructively. A policy needs a supporting legislative commitment to the CBD and conservation progress? framework, and a responsible agency must be Indonesia has 566 national parks, nature reserves appointment with the mandate to implement the policy and wildlife sanctuaries covering 360,693 km2, which cross-sectorally. The implementation of the policy must consist of 490 terrestrial protected areas (225,401

2014 Journal of Indonesian Natural History Vol 2 No 1 3 km2) and 76 marine protected areas (135,291 km2). The in the process of updating the IBSAP (2003) to 2020. The terrestrial protected areas include 43 National Parks, intention is for the updated IBSAP to be mainstreamed 239 Nature Reserves, 70 Game Reserves, 13 Hunting into sectoral policies, plans and programmes through its Parks, 22 Grand Forest Parks, and 103 Nature Tourism integration in the Medium-term National Development Parks. Yet, after Brazil, Indonesia has the second highest Plan (2014-2019). The updated IBSAP will also include rate of primary forest loss in the World (Hansen et al., elements for monitoring and evaluating implementation 2013; Stibig et al., 2014; Wilcove et al., 2014). Even at the national and local levels. issue that has with the Indonesian forest moratorium in place since received criticism is that the IBSAP remains a voluntary 2011 new licenses covering approximately 5.5 million concept that provinces and districts can chose to accept hectares have been issued by the Ministry of Forestry or reject. for various development purposes. Critics claim that 4.5 Considering Indonesia’s diverse cultural heritage, million hectares of it have been excised from areas that economic challenges and vast territory, it is not surprising were originally classified for conservation and that data that conservation progress has been slow. Policy unavailability undermines confidence in the moratorium, implementation lacks behind, too many management highlighting transparency issues (Sloan, 2014). plans collect dust on shelves in offices and the majority The implementation and mainstreaming of the CBD of Indonesia’s national parks and protected areas are concepts does not always progress optimally in Indonesia. considered “paper parks”. Yet, important policies are However, serious actions are being taken to meet the being institutionalised to guide sustainable development 2020 Aichi Biodiversity Targets. In situ conservation is processes, and an increasing amount of resources is carried out through the establishment of conservation being allocated for environmental and biodiversity areas, such as biosphere reserves, wildlife sanctuaries, management. “Green” technology and innovation is national parks, ecotourism parks, forest parks and encouraged and supported, and economic initiatives hunting parks. Coverage of these areas increased from are set in motion that aim to transform Indonesia’s 7.628 million ha in 1981 to 27.968 million ha in 2007 economic framework from classic “extraction based” (MoE, 2009). Community-based forestry projects, into a “resource-based” system. Indonesia has also seen covering 2 million ha, have also been established, and a surge in international education being offered for despite vast tracts of land being developed into palm oil its citizens. One of the most visionary developments estates, a significant portion of these are also being set is the establishment of the Indonesia Learning Center aside as “high conservation value” areas. Furthermore, (ILC) by American conglomerate General Electric in ex-situ conservation activities have increased the number collaboration with three Indonesian state enterprises: of species of flora and fauna being successfully bred in Pertamina (state oil & natural gas mining company), captivity from 171 species in 2006 to 416 species in 2008 PLN (government-owned electricity company), and (MoE, 2009). Garuda Indonesia (the national airline of Indonesia). Breeding species in captivity is in itself a poor The ILC intends to provide leadership-training courses measurement for conservation success, however. Instead, both for internal employees and external customers the Ecosystem Approach is being used to develop a according to World famous Crotonville’s curriculum programme for the conservation and management of and learning experience. Senior faculty members at marine and fish resources. Management plans have also Crotonville, New York, are brought to Indonesia to been approved for more than 100 conservation areas, deliver leadership training to the nation’s current and while others are still being developed. Several regencies future talents. Since good leadership is essential to good have been designated as conservation areas realising that governance, Crotonville’s entering into Indonesian these play a vital role in regional development. education and corporate governance promises very Many conservation initiatives are based in the 2003 positive development prospsects for the nation. “Indonesian Biodiversity Strategy and Action Plan One of the major challenges for the incoming (IBSAP)” that was developed with a focus on achieving President will be to continue to support the processes five goals: 1) to encourage changes in attitude and of economic change and transformation. His cabinet behavior of Indonesian individuals and society, as and advisers must be able to set aside conventional well as in existing institutions and legal instruments, economic approaches that continue to propose economic 2) to apply scientific and technological inputs, and deficiencies are best fixed with the same problems local wisdom, 3) to implement balanced conservation that created them. At the current Global economic and sustainable use of biodiversity, 4) to strengthen slowdown, Governments across the World institute institutions and law enforcement, and 5) to resolve various conventional economic mechanisms (e.g. lower conflicts over natural resources. Currently, Indonesia is interest rates; public bail-outs) to encourage public and

4 © University of Andalas / Copenhagen Zoo coporate spending. In reality, it is like pretending there Ministry of Environment (2009). The 4th National Report for CBD. is consumer demand for various goods even if there Biodiversity Conservation Unit, Ministry of Environment. , is none. At the onset of the 21st century the incoming Indonesia. Government must be steadfast and refrain from the Margono, B.A., Potapov, P.V., Turubanova, S., Stolle, F. and temptation to follow conventional economics and not M.C. Hansen. (2014). Primary forest cover loss in Indonesia over attempt to combat budget deficiency by creating more 2000–2012. Nature Climate Change 4: 730–735. doi:10.1038/ depth. nclimate2277. With a population of 230 million citizens, urban Margono, B. A., Turubanova, S., Zhuravleva, I., Potapov, P., planning plays a significant role in biodiversity Tyukavina, A., Baccini, A., Goetz, S. and M.C. Hansen (2012). conservation too. It is tempting to solve urban housing Mapping and monitoring deforestation and forest degradation in deficiency by setting up standardised concrete buildings, Sumatra (Indonesia) using Landsat time series data sets from 1990 because these can be erected rapidly and rationally. to 2010. Environ. Res. Lett. 7: 034010. This approach, however, remains rooted in an utopian Olden, J. D., Hogan, Z. S. and Zanden, M. J. V. (2007). Small fish, belief that “livability” can be calculated according to big fish, red fish, blue fish: size-biased extinction risk of the world’s mathematical and economic models. At a planning level, freshwater and marine fishes. Global Ecology and Biogeography, it is easy to subscribe to mapping urban development 16: 694–701. doi: 10.1111/j.1466-8238.2007.00337.x. according to functionality, vis-a-vis separate housing estates, working areas and recreational areas from each Oliver, J.G.J., Janssens-Maenhout, G., Muntean, M. and J.A.H.W. Peters (2013). Trends in global CO2 emissions, 2013-Report, The other. Whilst it may have economic merrits, it creates a Hague: PBL Netherlands Environmental Assessment Agency; Ispra: one-dimensional environment that rarely meets modern Joint Research Centre. urban citizens’ demands for livelihood diversity and experience. Peters, G., Marland, C., Le Quere, T., Boden, J., Canadell, G. and There remain substantial biodiversity challenges M.R. Raupach (2012). Rapid growth in CO2 emissions after the for Indonesia in the immediate and long-term future. 2008-2009 global financial crisis.Nature Climate Change 2: 2–4. However, the nation has made a commendable beginning Pham C.K., Ramirez-Llodra E., Alt C.H.S., Amaro T., Bergmann and, despite many challenges, Indonesia lives up to its M., et al. (2014). Marine Litter Distribution and Density in European CBD-responsibilities to a much larger degree than most Seas, from the Shelves to Deep Basins. PLoS ONE 9(4): e95839. of its peers. doi:10.1371/journal.pone.0095839. Raupach, M.R., Marland, G., Ciais, P., Le Quere, C., Canadell, J., Klepper, G. and C. Field (2007). Global and regional drivers of References accelerating CO2 emissions. Proceedings of the National Academy of Sciences 104(24): 10288–10293. BAPPENAS (2003). Indonesian Biodiversity Strategy and Action Plan. The National Development Planning Agency (BAPPENAS). Sloan, S. (2014). Indonesia’s moratorium on new forest licenses: An 140pp. update. Land Use Policy 38: 37–40.

Boden, T.A., Marland, G. and R.J. Andres (2011). Global, Regional, Stibig, H. J., Achard, F., Carboni, S., Rasi, R. and J. Miettinen and National Fossil-Fuel CO2 Emissions. Carbon Dioxide ((2014). Change in tropical forest cover of Southeast Asia from Information Analysis Center, Oak Ridge National Laboratory, U.S. 1990 to 2010. Biogeosciences 11: 247–258. Department of Energy, Oak Ridge, Tenn., U.S.A. doi 10.3334/ CDIAC/00001_V2011. UNEP/CBD/COP (2012). Resourcing the Aichi Biodiversity Targets: A first assement of the resources required for implementing FAO (2011). Review of the state of world marine fishery resources. the Strategic Plan for Biodiversity 2011-2020. UNEP/CBD/COP. 83 FAO Fisheries and Aquaculture Technical Paper 569. Rome, Italy. pp. 354pp. Wilcove, D.S., Giam, X., Edwards, D.P., Fisher, B. and Koh, L. Hansen, M.C., Potapov, P.V., Moore, R., Hancher, M. et al. (2013). P. (2014). Navjot’s nightmare revisited: Logging, agriculture, and High-Resolution Global Maps of 21st-Century Forest Cover Change. biodiversity in Southeast Asia. Trends Ecol. Evol. 28: 531–540. Science 342(6160): 850-853. [DOI:10.1126/science.1244693].

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2014 Journal of Indonesian Natural History Vol 2 No 1 5 News and Notes

Fatwa against illegal wildlife trafficking in Indonesia

In March 2014, the Indonesian Council of Ulama --- Indonesia's top Muslim clerical body --- issued a fatwa (Fatwa No. 04, 2014) on Conservation of Threatened Wildlife to maintain Ecosystem balance. In a religious context, it effectively requires Indonesia’s 200 million Muslims to take an active role in protecting and conserving endangered species, including tigers, Figure 1. A female Sumatran rhino a day after capture, rhinos, elephants, and orangutans. At the same time, it March 2014, from Danum Valley, Sabah. The rhino named declares illegal hunting or illegal trading of endangered “Iman” was in poor reproductive health © John Payne species to be haram (forbidden). The fatwa is believed to be the first of its kind in the World and is a welcome rhino experts and agreed that the only way to ensure that example of a religious body engaging proactively and every Sumatran rhino in Sabah plays a role in saving the responsibly in an area usally covered by existing civil species is to bring all of them into a managed, fenced laws. facility, with the necessary local and global expertise The fatwa is not “implementable” per se, but is issued and collaboration to breed them. to give an explanation, as well as guidance, to all Once Iman is settled into Tabin, the Sabah Wildlife Muslims in Indonesia on the sharia law perspective on Department and Borneo Rhino Alliance (BORA) will issues related to conservation. It will supplement review all the potential options on how she can best existing Indonesian law and it is hoped that this contribute to her species. But it is expected that Iman will proactive initiative by the Indonesian Council of Ulama be given a reasonable time to mate with the male, Tam, will have positive impact on the current exscallating at the BRS. Ealier Tam had been slotted to be loaned illegal wildlife trade in the country. to Cincinnati Zoo as part of a breeding collaboration, where there is already a fertile female. If Iman proves to be fertile and the pair compatible, it might not be Female Sumatran rhino rescued in Sabah, necessary for Tam to fly to Cincinnati to mate. Malaysia

On the 21st of March, 2014, a critically endangered female Sumatran rhino (Dicerorhinus sumatrensis) was Drastic measures needed to save successfully rescued from a very remote area in Danum Sumatran rhinos from extinction Valley and translocated to join male (Tam) and a female (Puntung) rhinos at the Borneo Rhino Sanctuary (BRS) The successful capture of a female Sumatran rhino Facilities in Tabin Wildlife Reserve. Due to the remote in Danum Valley, Sabah, in March 2014 renewed capture area, she had to be flown in a Sikorsky S-64 hope of establishing a local breeding population in Helicopter that was made available by Erickson Air- Sabah. After capture Iman, as the rhino was named, Crane Inc. She was named “Iman” (Fig. 1), after a exhibited various indications similar to pregnancy but small river near where she was caught, and her rescue a detailed ultrasound examination under anesthesia was a result of a year of intense efforts to make every by specialists from the Leibniz Institute for Zoo and last rhino in Malaysia count towards efforts to prevent Wildlife Research Berlin (IZW) with local counterparts the extinction of one of the world’s most critically revealed that what had been suspected to be a fetus was endangered species. The Sabah State Cabinet had in fact a collection of tumors in the uterus. A thorough previously heeded advice from local and international examination revealed that some of the tumors were as

6 © University of Andalas / Copenhagen Zoo big as footballs. This indicates that Iman has not been Also highlighted was the need to develop standard sexually active for 5-10 years, most likely because there surveying methods, technical guidelines on the are too few males left, if any at all, in the wild. protection of the victimized in conflicts and the The discovery of the poor reproductive condition of establishment of the Javan Leopard Forum. Iman is simmilar to that of Puntung, a female captured There is still no accurate population estimate for Javan in 2011, and a young poached female from 2001. It leopard, although it is expected to number in the range is a big blow to the Global Sumatran Rhino Breeding of 400-500 indviduals. The main reason for the general program and it reiterates the critical need for assisted decline of the species is believed to be associated reproduction techniques such as in vitro fertilisation. with habitat loss, due to expanding production forests It is evident that Sabah’s rhino population is far too and agricultural land. A Javan Leopard Forum was small to recover without human intervention. While declared by 10 representatives of various stakeholders Sumatran populations appear to reproduce naturally from state-run forestry enterprise PT Perhutani, Foksi, in the wild the threat of poaching continues to push Carnivore Awareness, the Indonesia Institute of Sciences (LIPI), the Bogor Agricultural Institute, the Sumatra’s remaining small wild populations into a Conservation Breeding Specialist Group Indonesia and similar irreversible extinction vortex as is undeniably the Zoological Society of London. The Javan leopard happening to the rhinos in Sabah. conservation strategy and action plan is expected to be BORA executive director, Dr. Junaidi Payne, stated that approved by the Forestry Ministry in the near future, “everyone concerned with preventing the extinction of this and it will provide a much needed guidance to ensuring magnificent species really ought to work collaboratively the long-term survival of Java’s top predator. to share knowledge, ideas, experience, gametes and rhinos. That includes Indonesia and Malaysia, and the various specialists, notably IZW”. Global forest watch tracks where trees fall More plans made to save Javan leopard It is well knowned that forests across the world are vanishing at an astonishing rate, and with it biodivesity. Recently the Indonesian Forestry Ministry held a two day Sometimes it is hard to visualise just how serious the “National Conference on Javan Leopard” workshop at problem is. The World Resources Institute (WRI) the Indonesia Safari Park in Cisarua, Bogor, , recently released a new online mapping tool that aims to develop a Javan leopard conservation strategy and to put all the eyes of the world on forests everywhere in action plan aimed at saving the species from extinction. the World, with near-real time monitoring. The system Dozens of participants from insitutions including combines satellite pictures, computer algorithms and the Indonesian Wild Animals Conservation Forum crowd-sourced data to provide an up-to-date look at the (FOKSI), the Indonsian Zoo and Aquarium Association health of forests across the World. The system named (PKBSI), Indonesia Safari Park, the Harimau Kita “Global Foresty Watch” is developed in collaboration Forum, Java Carnivore Awareness, the Indonesian with dozens of partners and will allow users with Institute of Sciences (LIPI), Bogor Agricultural Institute a computer and internet access to zoom into a forest and research institutions provided the ministry with four anywhere in the world and see where trees are being key recommendations: a) conservation of Javan leopard lost as well as how fast it is being lost. The system has in its natural habitat, b) the need to include conservation a resolution of 30 meters and will be able to detect if institutions (e.g. zoos and wildlife refuges), c) public a stand of trees is felled by logging or fire, or wasted awareness tasks, and d) financing conservation and away by disease. A very important fact is that WRI research activities. An important addition to the stategic provides the Global Forest Watch as an “open source” approach was the inclusion of ex-situ conservation platform that any person can use for free. Hopefully, actions. The participants agreed that it is critical to the system will contribute to ending the procrastinated manage the genetic quality of all captive Javan leopard denial and secrecy of forest clearings across the Globe individuals, and that a studbook keeper should be and begin a more factual and progressive debate about appointed to oversee this. how to manage, protect and replace forested areas.

2014 Journal of Indonesian Natural History Vol 2 No 1 7 Nepal celebrates ‘zero poaching year’ work there, where there will also be a campus that has a mosque, a sports center and a 2,000-seat auditorium for for rhino, tiger and elephant the performing arts. The design appears like a funnel, the top of the tower opens at the top, capturing wind and Nepal recently celebrated a monumental conservation sucking it inside to run a series of vertical wind turbines achievement: 365 days without a single incident of that provide 25 percent of the building’s electricity. rhino, tiger or elephant poaching record in any of the The façade will be calibrated for Jakarta’s proximity to country’s protected areas. The achievement has to the equator to mitigate solar heat gain throughout the be seen in contrast to the huge increases in elephant day as well as year. The sides of the building will be and rhino poaching worldwide, and is testament to made as sun-shading “leaves” that allow daylight to the collective commitment of Nepal’s Department of enter while shielding the building from glare and heat National Parks and Wildlife Conservation (DNPWC) from the sun, and airconditioners will be replaced with and its national and international collaboraters. The radiant cooling systems. The power will be supplied by last reported incident of rhino poaching in the country thousands of solar panels and geothermal facilities. occured on February 16, 2013. In recent years, the In the past decade, Indonesia has developed a long Nepalese Government have focused increasingly on its range of policies aimed at guiding the Nation into a conservation plight, aomng others by establishing the path of sustainable development. The Pertamina Energy Wildlife Crime Control Coordination Committee at the Tower will reflect Indonesia’s sustained commitment national level and the Wildlife Crime Control Bureau at to sustainable development, and possible propell the the district level and increased law-enforcement. In 2013 nation into a small group of elite nations taking a big alone, law enforcement officials arrested more than 700 step towards a resource based economy. wildlife criminals in the country. This has resulted in a significant decrease in poaching and illegal wildlife trade, and a rise in the rhino population.The success is a ew initiative to protect biodiversity good example of combined efforts in protected area and N EU species management IUCN’s country representative and fight wildlife crime pledged continued support to the DNPWC in the future. Despite this recent success, the large number of arrests On the International Day for Biological Diversity in 2013 indicate that Nepal is still a major transit point today, the Commission is launching a major new for trade and the smuggling of body parts of endangered initiative to halt biodiversity loss and eradicate poverty animals. Between February 2013 and February 2014 in developing countries. The EU Biodiversity for Life authorities seized 1,200 grams of tiger bone, two rhino (B4Life) initiative is designed to assist needy countries horns, a rhino toe, six leopard hides, and 11 red panda protect their national ecosystems, combat wildlife crime hides. and develop green economies. B4Life will operate with A 2011 rhino census revealed that 534 Greater One- an estimated budget of up to €800 million for the period horned rhinos still persist in Nepal; 503 of these occur 2014-2020 and will focus on Least Developed Countries in Chitwan National Park, 24 in Bardiya National Park and countries containing “biodiversity hotspots”, the and seven in Shuklaphanta Wildlife Reserve. places where ecosystems and their services are the richest but also the most threatened. The past two decades have manifested that biodiversity and development are closely linked and mutually The world’s first net-zero energy reinforcing --- that is, healthy ecosystems sustain rises in Indonesia development while development impacts on habitats. Therefore, the B4Life focus on ecosystem conservation The Pertamina Energy Tower will soon become the and restoration as an opportunity to generate growth, world’s first net-zero energy skyscraper. It will be create jobs and reduce poverty through developing new built in of Indonesia’s capital, Jakarta, and strategic frameworks for green economy. B4Life will expected to be complited by 2019. It will consists of operate in three priority areas: 99 stories and serve as the headquarters of Pertamina, the national energy company. Up to 20,000 people will • Promoting good governance of natural resources.

8 © University of Andalas / Copenhagen Zoo • Securing healthy ecosystems for food security. The Asia-Pacific Chapter meeting reconstituted the • Developing nature-based solutions towards a green chapter board and decided that the 2015 AP-meeting economy. will take place in Cambodia. The team will be preparing for this event. In addition to the three priority areas, B4Life will include a special ‘Wildlife Crisis Window’ (WCW), dedicated to combating the increase in the illegal trade Forests Asia Summit, Jakarta of endangered species, particularly in Africa. As well as threatening species, wildlife poaching and trafficking One of the most important and largest events in the harm local and national security. There are mounting region took place in Jakarta from 5-6th of May, 2014. evidence that rebel militias and possibly terrorist groups The Forests Asia Summit: Sustainable Landscapes for are involved in elephant and rhino poaching as a means Green Growth in Southeast Asia was organised by the of financing their actions. The WCW aims at tackling Center for International Forestry Research (CIFOR) poaching and trafficking at all levels --- at a local level and co-hosted by the Indonesian Ministry of Forestry. by securing the management of priority protected areas; The event was the largest in Asia in recent years and at a national level by reinforcing the rule of law by attracted more than 1,000 leading stakeholders from tackling corruption and improving investigation; at a Southeast Asia and across the world. It saw ministers regional level by promoting anti-criminal networks from across Southeast Asia join CEOs, civil society leaders, development experts and the world’s top and the creation of cross-border protected areas, and by scientists, to share knowledge on how the region can improving species monitoring; and internationally by accelerate the shift toward a green economy by better supporting organisations specialised in the fight against managing its forests and landscapes. Thousands more wildlife crime, illegal trade and smuggling. participated online or through nationwide broadcasts, and there were special learning events with leading global experts on the Green Economy, the Southeast Association for Tropical Biology and Asian haze crisis, climate change negotiations and the Sustainable Development Goals. onservation meeting airns C , C As a testament to the importance of the occasion H.E. President of Indonesia Susilo Bambang Yudhoyono The Association for Tropical Biology and Conservation delivered the opening address, with ministers and high st (ATBC) held its 51 annual meeting in Cairns, Australia. ranking Government officials and corporate players The event also included the Asia-Pacific Chapter (AP) from most of SE Asia also making presentations. meeting and was co-hosted by James Cook University. One notable absentee from this important event was The 2014 annual meeting became the largest Malaysia. congregation of tropical biologists ever in Australia, The aim of the Forests Asia Summit was to lay the with 589 registered scientists and conservationists foundations for continued dialogue, transitions toward from 55 nations participating. The event theme was sustainable investments, and further research to support The Future of Tropical Biology and Conservation and evidence-based policymaking, all directed toward almost 200 oral presentations were delivered in five achieving equitable green growth and more sustainable concurrent sessions along with almost 100 posters. management of landscapes across Southeast Asia. In lieu of the recent plans for port development Following the event, an outcome statement was compiled from reporting from the sessions at the Forests and associated dredging in the Abbott Point area near Asia Summit to provide an overview of messages Bowen, Queensland, the meeting produced the ATBC throughout the conference. In summary, the reporting 2014 Cairns Declaration in Support of Stronger concludes that: Protection of the Great Barrier Reef. The declaration focus particularly on the feasibility of the offset • To achieve equitable and sustainable green growth requirement for reducing net sediment input into the in Southeast Asia, all stakeholder groups must strive Great Barrier Reef Marine Park, and the cumulative to overcome communication barriers, engage in effect of this development to the marine ecosystem. The continued, participatory dialogue, and act together ATBC Cainrs Declaration can be downloaded at: http:// within a landscape and multilevel governance tropicalbiology.org/atbc-2014-cairns-declaration/. framework.

2014 Journal of Indonesian Natural History Vol 2 No 1 9 • Government, the corporate sector and the finance Tigers in peril sector must work together to create enabling conditions to unlock private capital and support The annual Global Tiger Day took place worldwide investments in sustainable landscapes and on 29 July 2014. Unfortunately, there is still very little smallholders. cause to celebrate with tiger populations continueing to decline across its ranges. Poaching and habitat • The scientific community, with support from destruction remain the primary causes of decline, along the public and private sectors, must engage in with an increasing loss of prey base. These are some of integrated and targeted research aimed at increasing ther concerns that were highlighted in a comprehensive understanding of the dynamics that shape landscapes report co-authored by TRAFFIC into the progress made and communicate findings to government and by the countries implementing measures to protect business in a way that supports evidence-based Asia’s four big cat species. The report states that in changes in policy and practice toward a sustainable the period from 2000-2014 a minimum of 1590 tigers future and action on the ground. sustainable have been seized - an average of two animals per week landscapes and smallholders. - with most recorded from India (536) (Fig.1). Despite formulating policies, high level meetings, pledges and • The scientific community, with support from plans the number of tigers represented in seizures has the public and private sectors, must engage in increased from less than 100 in 2000 to 150 per year integrated and targeted research aimed at increasing in 2014. While this can also be a result of improved understanding of the dynamics that shape landscapes law enforcement, it is a trend that concerns many and communicate findings to government and conservation biologists across the region. business in a way that supports evidence-based Indonesia reportedly lost 103 tigers in the 2000-2014 changes in policy and practice toward a sustainable period. While this figure is small in comparison to future and action on the ground. India’s loss of tigers, the report warns that Indonesia must improve its law enforcement if tigers are to The detailed Outcome statement with associated survive in Sumatra. In the period 2010-2012 Indonesia explanation can be found at: http://www.cifor.org/ contributed with 20% of all tiger parts seizures despite forestsasia/about/outcome-statement/. only having less than 10% of the global tiger population.

Figure 1. Number of killed and traded tigers in range countries suggest that the illegal trade florishes as much as ever. From TRAFFIC (2014).

10 © University of Andalas / Copenhagen Zoo Debate Forum thieves in Java show that Indonesian wildlife crime knows no boundaries

Anais Tritto1 and Resit Sozer1

1Cikananga Conservation Breeding Centre, West Java, Indonesia

Corresponding authors: Anais Tritto, email: [email protected]

A large theft of endangered captive bred from listed as “critically endangered” on the IUCN Red-list. the Cikananga Wildlife Centre in West Java has seriously Cikananga does not breed them for markets though, but ruffled the feathers of the Indonesian conservation release them back into the Javan countryside at secret community. Burglars succeeded in stealing a total of 156 rare birds from the centre, likely to feed Indonesia’s burgeoning bird trade. Enough is enough, say bird conservationists. Indonesia’s national emblem is a large mythical bird or bird-like creature, Garuda. The Garuda is a reference to both Indonesia’s Hindu and Buddhist past, as well as to the cultural importance of birds in the country. The speed at which Indonesians are consuming and trading local wild bird species, however, suggests that the only birds left will soon live in cages, or are exotics like the ubiquitous tree sparrow introduced from Europe. Forest areas that used to resonate with bird calls are now silent. The Yellow-vented Bulbul, Pycnonotus goiavier, previously very common in Bogor and Jakarta, is now rare, because its pretty song makes it a popular cage bird. Once one of the most common birds in Indonesia’s rice fields, the beautiful Java Sparrow, Lonchura oryzivora, was hunted extensively for keeping in cages too, but also shot and poisoned because it fed on rice. This species roamed in flocks of thousands but has almost disappeared from the wild. Bird collectors and traders are finding ever more devious (and often illegal) ways to obtain birds that are increasingly hard to find in the wild. A recent victim of this conniving approach was the Cikananga Figure 1. The Javan Black-winged starling, Acridotheres Wildlife Centre, near Sukabumi, West Java. After five melanopterus, is listed as “Critically endangered” on the IUCN-redlist. For the past five years Cikananga Wildlife years of painstaking captive breeding efforts the centre Centre, West Java, successfully bred more than 500 succeeded in breeding over 500 individuals of the Black- individuals of the species to help save it from extinction. winged Starling, Acridotheres melanopterus, known Many pairs have been reintroduced back to its natural locally as Jalak Putih (Fig.1). Due to its popularity habitat on Java. Recently, several hundreds were stolen by as a cage bird thousands were captured and sold, and professional thieves, aledgely to supply Indonesia’s rampant today it has become close to extinct in the wild and illegal bird trade. © Roland Wirth

2014 Journal of Indonesian Natural History Vol 2 No 1 11 locations for local villagers to enjoy their splendid Indonesian authorities in preventing such thefts from songs again and benefit from the starlings as biological occurring and prosecute the culprits. A reward of pest controllers of insects in rice fields. In the past few 15,000,000 Rupiahs has been offered by one of the months 10 attempts of theft have been recorded of donors to anyone who can give information that leads which three were successful. The audacious thieves to the recovery of at least some of the stolen birds trespassed into Cikananga, avoided a range of security and identification of the thieves. Unfortunately, the measures and stole 156 birds. The total loss at Cikananga Cikananga theft is one of many indications of a growing amounted to: one Bali Starling (near extinction in the biodiversity conservation challenge in Indonesia. To wild; listed as Critically Endangered on the IUCN red- date, the Indonesian conservation authorities continue list), two Black-winged Starlings of the Bali subspecies, to struggle with mainstreaming conservation related three Sumatran Laughing-Thrushes, 149 Black-winged policies and enforcing relevant laws. The occasional Starlings from Java (listed as Critically Endangered on raids on bird markets constitute merely inadequate the IUCN red-list) and one Javan green . This authoritative signals that usually do not have any also is a big blow to the centre’s staff who, supported by deterring effect illegal bird poaching and other illegal meagre salaries, have worked for years to breed these wildlife trade in the country. birds in an attempt to save them from extinction and to Does anyone care? Many Indonesians will probably the benefit of all Indonesians. never see an undisturbed forest in their life – after all, These were not some local dudes out on a cash run. such forests are now rare on Java where most people Locks were picked with chemicals, they brought wire live. Would it bother anyone if the last of Indonesia’s cutters, knew exactly where to go, and had clearly hornbills were caught for their beaks to be used in studied security operations. Rumours suggested that Chinese medicine? Or that no more eagles would soar all birds were sold at Jakarta’s bird markets the same overhead? Perhaps not now, but one day in the future morning, a tell-tale sign that the birds had been pre- many will likely bemoan the loss of a whole range of ordered. Although the thieves hit several times, and incredible species that makes this country one of the with the increased security measures, including extra most biodiversity rich in the World. By then, it is a little security guards patrolling the aviaries, they always too late. managed to escape. What is needed are major efforts by both governmental Theft was also reported at the release site for Black- and non-government organizations to crack down hard winged starlings. On the the 22nd of July, three chicks on illegal bird trade and poaching, and provide the public were stolen from a “secure” nest box after removing the with good and informative education and awareness padlock. Whereas the pair rearing the chicks was not about wild birds. Without such efforts, there is a real caught the theft is a big setback for the Cikanganga’s risk that many of Indonesia’s wild birds will disappear reintroduction programme. Of an initial 40 released over the next decade. If that happens, Indonesia’s birds individuals only seven birds remain in the area at present, will become mythical creatures just like Garuda and and therefore each hatching is of critical value to the people might ponder about the days when wild birds effort of reestablishing a wild population of the species. still roamed the countryside and bless gardens, fields A few days before this theft, one juvenile approx three and forests with intricate songs and calls. months old was stolen but local people forced the thief to release it. Consequently, the security at the release site will be improved with the employment of two local security guards. The efforts in Cikananga to save endangered Indonesian birds from extinction through captive breeding and re-introduction has been funded by generous donations from many philanthropic people in Germany, Switzerland, England, the Czech Republic, Poland and the USA. Naturally, these people are frustrated about the greed of bird thieves, traders and buyers in Indonesia, and the limited success of the

12 © University of Andalas / Copenhagen Zoo The Rufford Foundation: Grant Recipient Conference

The Rufford Foundation held its “Grant Recipient opportunities for collaboration through their own Conference” in Sabang, Sumatra in January 2014. The local networks. After two days of information sharing, conference was organised jointly by Fauna & Flora discussions and deliberations the participants arrived at International and the Rufford Foundation with the main the following recommendations: objectives to, • A future Rufford conference should include grantees • Provide a forum for grant recipients to discuss ideas, from eastern Indonesia and also those focussing on problems, issues and create invaluable networking marine issues. opportunities; and, • Indonesia holds the second highest number of • Increase communication and information between RSG project awards but not a single RSG recipient Rufford and its grant recipients. has advanced to the Continuation stage. This was because they had progressed in their career and felt The participants consisted of 16 Nature award winners that they were no longer suitable. from Indonesia ranging from first-time grantees to • Rufford should include a sub-section or set of Booster recipients. The first day was allocated for guidelines as part of the RSG proposal format to project presentations, which were designed to highlight enable project information and dissemination to a the logical progression in project implementation and wider audience (e.g. IUCN, national parks). evolution of project design from the first Rufford Small • Rufford should create an alumni network with Grant (RSG) to a second RSG to Booster. The second regional meetings and opportunities for wider day involved a field trip to an FFI marine project site, peer learning. Also, an electronic Rufford mail-list including visiting a mangrove forest rehabilitation site would enable a global alumni network to connect. with the local customary marine leader. • Conduct a gap analysis to identify locations The RSG is a relatively small contributor to (e.g. eastern Indonesia) and issues (e.g. marine conservation projects. Nevertheless, RSG have resulted biodiversity conservation) that are under- in significant and tangible conservation impacts. represented in RSG. Rufford has also enabled early career conservationists • Consider setting up a small grants scheme, whereby to get that all important first start and mobilized sooner a pool of student projects (e.g. £1000 each) could be than they would have done otherwise. Grant recipients funded under a single RSG capacity building grant include what is now widely acknowledged conservation of £6000 that is award to the supervisor. This could officers in Indonesia, many which were participating in increase the number of projects and opportunities the conference, including the co-editor of the Journal for early career conservations who will benefit from of Indonesian Natural History, Wilson Novarino. The the experience of initially managing a smaller grant. grantees were engaged in subjects varying from local policy and legislation support, to protecting Malay tapirs The Editors and Sumatran tigers, and using gibbons as a flagship species to support income generating activities for local coffee farmers on Java. It also allowed grantees to pursue and test creative and innovative initiatives and disseminate results widely. Finally, one of the most important results of RSG support is that it has enabled grantees to train up a future generation of conservationists, and often focus on critically important species or ecosystems that would otherwise have received little attention. The conference also aimed at forging new collaborations in Indonesia. It set out to identify and establish areas for collaboration between grantees and increase further

2014 Journal of Indonesian Natural History Vol 2 No 1 13 Genetic diversity of Macaca fascicularis (Cercopithecidae) from , Malaysia as inferred from mitochondrial control region segment J.J. Rovie-Ryan1, M. T. Abdullah2,3, F. T. Sitam1, S. G. Tan4, Z. Z. Zainuddin5, M. M. Basir1,6, Z. Z. Abidin1,6, C. Keliang1, A. Denel1, E. Joeneh1 and F. M. Ali1

1Outbreak Response Team, Wildlife Genetic Resource Bank Laboratory, Ex-Situ Conservation Division, Department of Wildlife and National Parks Peninsular Malaysia, Kuala Lumpur, Malaysia. 2Kenyir Ecosystem Research Centre, Universiti Malaysia Terengganu, 21030 Kuala Terengganu, Terengganu, Malaysia.. 3Department of Zoology, Faculty of Resource Science and Technology, Universiti Malaysia Sarawak, Malaysia. 4Dept. of Cell and Molecular Biology, Faculty of Biotechnology and Biomolecular Sciences, Universiti Putra Malaysia, Malaysia. 5Borneo Rhino Alliance, Sabah, Malaysia. 6Deputy Director General I and II Office, DWNP, KM 10 Cheras Road, 56100 Kuala Lumpur.

Corresponding author: J.J. Rovie-Ryan, email: [email protected]

Abstrak Keanekaragaman genetic kera ekor panjang (Macaca fascicularis) dari Penang, termasuk Pulau Jerejak dan daratan utama Negeri Penang Malaysia telah dianalisis dengan menggunakan 1.042 bp control region (CR) segment DNA mitochondria (mtDNA). Dua puluh haplotipe menunjukkan adanya satu haplotipe tunggal yang sama antara daratan utama dan pulau, hal ini menandakan bahwa ini merupakan genetic yang diterima dari daratan. Dibandingkan dengan penelitian sebelumnya yang dilakukan berdasarkan CR, semua haplotipe dari Penang merupakan gambaran baru dan tidak ada yang sama dengan populasi M. fascicularis lainnya di wilayah ini. Adanya satu deletion mutasi unik pada contoh dari penang (Kelompok I dan II) bisa menjadi indicator yang baik untuk upaya konservasi keunikan genetic dan mungkin bisa dikelola sebagai satu unit pengelolaan. Sebuah ringkasan pohon filogenetik (NJ, MP, ML dan Bayesian) mendukung pengelompokan monofiletik dari M. fascicularis seperti digambarkan pada penelitian penelitian sebelumnya. Pemisahan topologi dari haplotype Penang kedalam tiga kelompok utama secara umum berhubungan dengan distribusi geografis mereka. Penelitian ini juga mencatat bahawa haplotipe Penang memiliki garis keturunan dari wilayah continental yang telah terpisah dari garis keturunan insular sekitar 1.04 juta tahun yang lalu. Penelitian ini juga menunjukkan bahwa CR dari mtDNA sangat baik digunakan untuk mengkuantifikasi keanekaragaman genetic intraspesifik pada M. fascicularis.

Abtract The genetic diversity of the long-tailed macaques (Macaca fascicularis) from Penang, Malaysia, including Jerejak Island and the mainland area of the state of Penang, Seberang were examined using 1,042 bp control region (CR) segment of the mitochondrial DNA (mtDNA). Twenty haplotypes were described with a single haplotype sharing between the mainland and the island which suggests that it is a remnant of the genetic makeup from the mainland. Compared to previous studies based on the CR, all the Penang haplotypes are newly described with none shared with the other regional populations of M. fascicularis. A single deletion mutation unique to the Penang samples (Groups I and II) could be a good indicator for the conservation of the genetic uniqueness and possibly should be managed as a management unit (MU). A summarised phylogenetic tree (NJ, MP, ML and Bayesian) supports the monophyletic clustering of the M. fascicularis as described in previous studies. The topology separates the Penang haplotypes into three major groups, which generally corresponds to their geographical distribution. We also noted that the Penang haplotypes are of the continental lineage which separated from the insular lineage at around 1.04 mya. Finally, we showed that the CR of the mtDNA is powerful and suitable for the quantification of intraspecific diversity in M. fascicularis.

Keywords: Macaca fascicularis, , phylogenetics, hypervariable segments I and II

Introduction southeast Asia (Thailand, Cambodia, Vietnam, Laos, Myanmar, Peninsular Malaysia and Singapore) and the The long-tailed macaque, Macaca fascicularis, also Greater and (Indonesia, Brunei, known as the cynomolgus macaques, are widely and the Malaysian Borneo) and the (Eudey, distributed in nature and occupies vast areas of mainland 2008; Fooden, 1995). They can be found almost everywhere especially at low elevations preferring Received 26th February 2014; Revision accepted 2nd May, 2014 the mangrove and swampy forests, river banks, and

14 © University of Andalas / Copenhagen Zoo Genetic diversity of M. fascicularis seashores (Eudey, 2008). In Peninsular Malaysia they (1) to examine the genetic diversity of the Penang M. are very common and populate areas in sympatry with fascicularis and (2) to investigate the efficiency of the the human settlements [Department of Wildlife and mtDNA control region in assessing the genetic diversity National Parks (DWNP), 2006]. In Penang particularly, of M. fascicularis in Malaysia. M. fascicularis is distributed throughout the islands (Penang Island and smaller adjacent islands including Jerejak Island) and the mainland portion of Seberang Methods Perai (DWNP, 2006; Karimullah & Shahrul, 2011). Historically, Peninsular Malaysia was part of Sample Collection the Sundaland which was heavily influenced by Sampling was conducted by the Outbreak Response events during the Quaternary Period (Pliocene and Team (ORT) of the DWNP on conflict long-tailed Pleistocene) (Voris, 2000). During the Pleistocene, macaques as part of a Wildlife Disease Surveillance periods of intermittent glacial caused the fluctuation Programme (WDSP) launched by DWNP in 2011 to of sea levels and at its maximum fell by 120 m below monitor the emergence of zoonotic diseases in wildlife present-day levels and landmasses (Malay Peninsula, species. Figure 1 shows the sampling sites (A-L) while Borneo, Sumatra, Java, Bali, Palawan, the Mentawai Table 1 provides the details of each of the samples used Islands, and the smaller intervening islands), which are in this study. All samples were kept at the Wildlife currently separated were joined and formed Sundaland Genetic Resource Bank (WGRB) Laboratory, DWNP. (Bird et al., 2005; Harrison et al., 2006; Sathimurthy & Voris, 2006; Voris, 2000). Consequently, Penang DNA Extraction, PCR Amplification and Sequencing Island which is currently situated about four km off the Total genomic DNA was extracted from 46 samples coast of and separated by the narrow Penang Straits at a maximum depth of 20 m (Asadpour either from blood (preserved in lysis buffer) or from liver et al., 2011) would experience repeated connection to samples (see Table 1) using the QIAamp DNeasy Blood the mainland during Pleistocene, thus limiting faunal and Tissue Kit (QIAGEN Ag., Germany) protocol for interchanges. blood and tissue samples as provided by the manufacturer. In Malaysia, very few genetic studies had been A pair of oligonucleotides; WGRB/MFCR/F15978 (5’– conducted on M. fascicularis. Most studies were ACCACCAACACCCAAAGCTGGC–3’) and WGRB/ conducted to investigate their conflict with humans MFCR/R580 (5’-TCAGTGTCTTGCTTTGGGTGGGT-3’), (DWNP, 2006), association with zoonotic diseases were designed using the program Primer3 (Rozen & Skaletsky, (Cox-Singh & Singh, 2008; Thayaparan et al., 2013, 2000) as a plug-in in the Geneious v5.6 (Drummond et 2014), distribution (DWNP, 2006; DWNP, unpublished al., 2012) to cover the complete length of the CR segment. data; Karimullah & Shahrul, 2011), and behaviour Amplifications were carried out in an Arktik Thermal (Ling, 2006; Ping, 2003; Shuan, 2006). In other Cycler (Thermo Scientific, USA), using a 15 µl reaction regional populations of M. fascicularis (Indochinese, volume consisting of 0.5 µl of DNA template (~15–20 Indonesian, Philippines, Singapore, and Mauritius) ng), 0.2 µl (0.13 µM) of each primer and 14.5 µl of however, numerous genetic studies have been conducted GoTaq® Colorless Master Mix (Promega, USA). using mitochondrial DNA (mtDNA) markers (Blancher Amplification was done using the following PCR et al., 2008; Harihara et al., 1988; Kawamoto et al., profile: a preliminary denaturation at 98oC for 2 min 2008; Lawler et al., 1995; Perwitasari-Farajallah et al., followed by 30 cycles of 95oC for 30 sec, 69oC for 30 1999; Perwitasari-Farajallah et al., 2001; Schillaci et sec and 72oC for 40 sec. This was followed by a final al., 2011; Shiina et al., 2010; Smith et al., 2007; Tosi & extension period of 72oC for 3 min before the samples Coke, 2007; Tosi et al., 2002). In this study, we employ were cooled to 4oC. Cycle sequencing on both primers the mtDNA control region (CR) as part of a major were done on an ABI PRISM®377 DNA Sequencer by research initiative by the DWNP to comprehensively a sequencing service provider (1st Base Laboratories examine the population genetics, phylogeography, and Sdn. Bhd., Malaysia). the diseases associated with M. fascicularis in Malaysia (both from Peninsular Malaysia and from Sarawak Sequence Analysis and Sabah states on Borneo Island). In summary, this Multiple alignments of the sequences were done and pilot study is designed to achieve these objectives; ambiguous flanking regions were identified and removed

2014 Journal of Indonesian Natural History Vol 2 No 1 15 Rovie-Ryan et al.

Table 1. Detailed information on each M. fascicularis samples collected from the Penang State.

Haplotype Haplotype GenBank Acc. No Sample Label Location/GPS of capture Map Sample type** Sex Designation Frequency No. 1 WDSP/11/0037 Sg. Kecil, Seberang Perai, Penang F L BLB 20 0.130 JX113316 2 WDSP/11/0038 Sg. Kecil, Seberang Perai, Penang F L BLB 20 0.130 JX113317 3 WDSP/11/0039 Kuala Juru, Seberang Perai, Penang M J BLB 9 0.022 JX113318 4 WDSP/11/0040 Kuala Juru, Seberang Perai, Penang M J BLB 5 0.022 JX113319 5 WDSP/11/0041 Permatang Kriang, Seberang Perai, Penang M I BLB 4 0.043 JX113320 6 WDSP/11/0042 Permatang Kriang, Seberang Perai, Penang M I BLB 19 0.022 JX113321 7 WDSP/11/0043 Ladang Byram, Seberang Perai, Penang F K BLB 20 0.130 JX113322 8 WDSP/11/0044 Ladang Byram, Seberang Perai, Penang F K BLB 20 0.130 JX113323 9 WDSP/11/0045 Ladang Byram, Seberang Perai, Penang F K BLB 20 0.130 JX113324 10 WDSP/11/0046 Ladang Byram, Seberang Perai, Penang F K BLB 20 0.130 JX113325 11 WDSP/11/0047 Jerejak Rainforest Resort, Jerejak Island M H BLB 12 0.065 JX113326 12 WDSP/11/0048 Jerejak Rainforest Resort, Jerejak Island M H BLB 12 0.065 JX113327 13 WDSP/11/0049 Jerejak Rainforest Resort, Jerejak Island M H BLB 11 0.022 JX113328 14 WDSP/11/0050 Jerejak Rainforest Resort, Jerejak Island M H BLB 10 0.087 JX113329 15 WDSP/11/0051 Jerejak Rainforest Resort, Jerejak Island M H BLB 10 0.087 JX113330 16 WDSP/11/0052 Jerejak Rainforest Resort, Jerejak Island M H BLB 12 0.065 JX113331 17 WDSP/11/0053 Jerejak Rainforest Resort, Jerejak Island M H BLB 10 0.087 JX113332 18 WDSP/11/0054 Jerejak Rainforest Resort, Jerejak Island M H BLB 10 0.087 JX113333 19 WDSP/11/0055 Jerejak Rainforest Resort, Jerejak Island M H BLB 15 0.022 JX113334 20 WDSP/11/0056 Jerejak Rainforest Resort, Jerejak Island F H BLB 13 0.022 JX113335 21 WDSP/11/0057 Jerejak Rainforest Resort, Jerejak Island M H BLB 16 0.022 JX113336 22 WDSP/11/0058 Sg. Baru, , Penang Island M G BLB 17 0.043 JX113337 23 WDSP/11/0059 Sg. Baru, Teluk Kumbar, Penang Island F G BLB 17 0.043 JX113338 24 WDSP/11/0060 Surau MK 2, Tg. Bungah, Penang Island M B BLB 6 0.022 JX113339 25 WDSP/11/0061 Batu Feringghi, Penang Island M A BLB 14 0.022 JX113340 26 WDSP/11/0062 , , Penang Island M E BLB 18 0.022 JX113341 27 WDSP/11/0063 Surau MK 2, Tg. Bungah, Penang Island M B BLB 7 0.109 JX113342 28 WDSP/11/0064 Surau MK 2, Tg. Bungah, Penang Island M B BLB 7 0.109 JX113343 29 WDSP/11/0065 Surau MK 2, Tg. Bungah, Penang Island M B BLB 7 0.109 JX113344 30 WDSP/11/0066 Surau MK 2, Tg. Bungah, Penang Island F B BLB 7 0.109 JX113345 31 WDSP/11/0067 Surau MK 2, Tg. Bungah, Penang Island F B BLB 8 0.022 JX113346 32 WDSP/11/0068 Bkt. Gambir, , Penang Island M F BLB 1 0.217 JX113347 33 WDSP/11/0069 Bkt. Gambir, Gelugor, Penang Island M F BLB 1 0.217 JX113348 34 WDSP/11/0070 Bkt. Gambir, Gelugor, Penang Island M F BLB 1 0.217 JX113349 35 WDSP/11/0071 Permatang Pasir, Balik Pulau, Penang Island M E BLB 3 0.043 JX113350 36 WDSP/11/0072 Bkt. Gambir, Gelugor, Penang Island F F BLB 2 0.022 JX113351 37 WDSP/11/0073 Bkt. Gambir, Gelugor, Penang Island M F BLB 3 0.043 JX113352 38 WDSP/11/0074 Jln. Perak, Penang Island M D BLB 7 0.109 JX113353 39 ZMW486 , Penang Island F C L 1 0.217 JX113354 40 ZMW487 Tanjung Tokong, Penang Island M C L 1 0.217 JX113355 41 ZMW488 Tanjung Tokong, Penang Island F C L 1 0.217 JX113356 42 ZMW489 Tanjung Tokong, Penang Island F C L 1 0.217 JX113357 43 ZMW490 Tanjung Tokong, Penang Island M C L 4 0.043 JX113358 44 ZMW491 Tanjung Tokong, Penang Island M C L 1 0.217 JX113359 45 ZMW492 Tanjung Tokong, Penang Island F C L 1 0.217 JX113360 46 ZMW493 Tanjung Tokong, Penang Island M C L 1 0.217 JX113361

16 © University of Andalas / Copenhagen Zoo Genetic diversity of M. fascicularis

Figure 1. The map showing the sampling locations and haplotype designation of M. fascicularis in the Penang Island, Jerejak Island, and Seberang Perai (mainland). Each letter (A-L) represents a sampling location while the numbers (1-20) represents the assigned haplotype number (for details see Table 1). Dotted arrows indicate haplotypes sharing between the locations.

2014 Journal of Indonesian Natural History Vol 2 No 1 17 Rovie-Ryan et al. from the analysis by using the program Geneious v5.6. at around 5.5 million years ago (mya) between the Sequence characterisations (variable sites, conserved African and the Asian Macaca lineage. Therefore, for sites and parsimony-informative sites) were done the complete CR dataset, members from both lineages using Mega v5 (Tamura et al., 2011). Standard genetic were included in the analysis; the Asian lineage diversity indices including the number of haplotypes was represented by M. mulatta (AY612638) and M. (H), haplotype diversity (h), and nucleotide diversity thibetana (EU294187), while the African lineage was (π) (Nei, 1987) were calculated in DnaSP v5 (Librado represented by M. sylvanus (AJ309865). All trees were et al., 2009). rooted with the outgroup species of the tribe Papionini, The mtDNA CR contains two segments; hypervariable Papio hamdryas (Y18001). To assess the robustness of segment I (HVI) and II (HVII). Apparently, there has the trees, bootstrapping (Felsenstein, 1985) with 10,000 been no comprehensive study utilizing the complete CR replicates were conducted on all the NJ, MP, and ML in M. fascicularis. However, several authors worked on trees. either one of the segments. Thus we split our dataset To compare our dataset with the other regional to compare our sequences with the available sequences populations of M. fascicularis, we constructed the ML of the HVI (Chu et al., 2007; Smith et al., 2007), and tree, as described above. However, due to computational the HVII (Blancher et al., 2008; Kawamoto et al., 2008; limitations, we ran the analysis with 100 bootstrapping Shiina et al., 2010). replicates. The trees were rooted with sequences of To analyse the genetic structuring between the M. cyclopis (HVI-DQ143986, HVII- AB261600), mainland and the island as well as among the other M. fuscata (HVI-AJ419862, HVII- AB261557), and regional populations, an estimate of population M. mulatta from China (HVI-DQ373357, HVII- subdivision (FST) (Hudson et al., 1992) was calculated AB261958) and India (HVI-DQ373369, HVII- using DnaSP v5. Apart from that, the genetic distances AB245416). By using the estimate of 1.6 million years between populations were also calculated by using ago (mya) for the divergence time between M. mulatta the Kimura two-parameter model (Kimura, 1980) as and M. fascicularis (Purvis, 1995; Hayasaka, 1996; performed using Mega v5. Blancher et al., 2008), we re-calibrated the branch length of the ML tree in an attempt to date the divergence time of a major bifurcation event in the course of their Phylogenetic Trees and Estimation of Divergence evolution. Time To infer the phylogenetic relationships, haplotypes data were used to generate the trees. Trees were Results constructed by using the neighbour-joining (NJ), maximum parsimony (MP), and maximum likelihood Genetic Diversity (ML) methods as implemented in Mega v5 and also the An alignment of 1,042 bp in length was produced from Bayesian method by using MrBayes (Huelsenbeck & the 46 individual samples including the other Macaca Ronquist, 2001) as a plug-in in the Geneious program. species and outgroup sequences (N= 51) obtained from A median-joining network was also constructed using the GenBank. The sequences were later registered with the Network program (Bandelt et al., 1999). NJ was the GenBank and were given accession numbers from performed by using the Kimura 2-parameter distance JX113316-JX113361 (see Table 1). model (Kimura, 1980) with pairwise deletion option The nucleotide diversity (π) for the complete CR while the MP analysis was done by using the Close- dataset was 0.012. Although the pooled island samples Neighbour-Interchange (CNI) option. The best-fit (Penang and Jerejak Island) consisted of 36 individuals, substitution model for ML was calculated in Mega v5 the π of 0.009 was observed to be lower than the and the tree was constructed based on the HKY+G mainland π of 0.013 which was represented by only model using the Nearest-Neighbour-Interchange (NNI) 10 individuals. In total 20 haplotypes were detected option. The Bayesian analysis was performed by using using the complete dataset with a haplotype diversity the default settings with the HKY85 model (Hasegawa (h) of 0.921. Considering the indels, the mainland et al., 1985). Four heated Markov chains were initiated had 5 haplotypes (h= 0.667) while the island had 16 from random trees and sub-sampled at every 200 cycles. (h= 0.895). A single haplotype sharing between the Delson (1996) proposed an early separation occurring mainland and the island was observed (Hap4; Fig. 1).

18 © University of Andalas / Copenhagen Zoo Genetic diversity of M. fascicularis

Seg. No Population N CS VS PIS π H h Length 1 Jerejak Island 11 536 514 23 22 0.01445 4 0.764 2 Penang Island 25 536 504 33 21 0.0135 9 0.793 Table 2. Comparison among the different 3 Seberang Perai1 10 536 501 36 21 0.02276 5 0.667 regional populations of M. fascicularis using 4 Malaysia* 149 536-9 378 163 147 0.064 104 0.99 the HVI segment. Number of haplotypes (H) 5 Indonesia 70 537-9 390 152 131 0.075 55 0.99 and haplotype diversity (h) were calculated 6 Philippines 83 537-40 430 110 64 0.023 34 0.81 by considering sites with alignment gaps. 7 Vietnam 89 538-40 441 99 85 0.039 48 0.97 8 Mauritius 68 537 523 14 10 0.001 8 0.27 Total 505 546 345 198 173 0.074 246 0.98 Seg. Length= Sequence Length, CS= Conserved sites, VS= Variable sites, PIS= Parsimony informative sites, π= Nucleotide diversity (Nei, 1987), H= No. of haplotypes, h= Haplotype diversity (Nei, 1987). 1Mainland

No Population 1 2 3 4 5 6 7 8 1 Jerejak Island 2.0 3.4 6.1 7.5 9.6 5.3 13.5 2 Penang Island 0.3 3.0 5.9 7.3 9.7 4.9 13.7 Table 3. Estimates of population subdivision (FST) (below 3 Seberang Perai 0.4 0.4 6.2 7.4 9.7 6.0 12.9 the diagonal) and pairwise distances (%, above the diagonal) 4 Malaysia* 0.4 0.4 0.4 7.7 8.8 7.6 12.2 among the geographical populations of M. fascicularis 5 Indonesia 0.4 0.4 0.4 0.0 8.5 8.6 11.2 analysed. 6 Philippines 0.8 0.8 0.8 0.5 0.4 9.8 8.9 7 Vietnam 0.6 0.6 0.6 0.3 0.3 0.7 12.4 8 Mauritius 0.9 0.9 0.9 0.7 0.6 0.9 0.8

Table 2 compared the genetic diversity indices of the III which consisted of a mixture of haplotypes from the Penang populations to the other regional populations mainland and the island samples. In Group I, subgroup based on the HVI segment while Table 3 compared the I-1 consisted of haplotypes from the north-eastern part estimates of population subdivision (FST) as well as of the island (sites C, E, and F), subgroup I-2 consisted the genetic distances. Separately, our finding revealed of haplotypes from the mainland (site J) which was that the HVI segment contained more variations when adjacent to the island, while subgroup I-3 contained compared to the HVII segment (see Appendix 1 for of a mixture of haplotypes from the rest of the island comparison between the HVI and HVII segments). (sites A, B, D, and G). Furthermore, the single deletion mutation observed as mentioned earlier delineated Phylogeography Groups I and II from Group III. The phylogenetic trees constructed using the NJ, MP Both the HVI and HVII segment produced similar (CI= 0.76, RI= 0.70), ML (–lnL= 3738.65), and Bayesian topologies (data not shown). A broader comparison of methods produced similar topologies and thus we the Penang haplotypes with that of the other regional summarised them using the ML tree as shown in Fig. 2A populations revealed that they were clustered within while Fig. 2B represents the median-joining haplotype the continental lineage (Fig. 3). Additionally, in network. Overall, the tree showed the monophyletic Figure 3, by calibrating node A which represents the grouping of M. fascicularis. The tree topology and the bifurcation between M. mulatta and M. fascicularis, haplotype network generally separated the 46 samples an estimated date of 1.04 mya at node B was obtained, into three major groups: (1) Group I which consisted which represents the last common ancestor between the of three subgroups, (2) Group II which was formed continental and insular lineage. entirely by the Jerejak Island samples, and (3) Group

2014 Journal of Indonesian Natural History Vol 2 No 1 19 Rovie-Ryan et al.

Figure 2. A. Phylogenetic relationships of the M. fascicularis haplotypes from Penang as represented by the ML tree. Values above the branches represent bootstrap confidence levels (10,000 replications) for NJ, MP and ML respectively. Values below the branches represent the Bayesian posterior probability. B. Median-joining haplotype network of the Penang M. fascicularis that formed the 20 haplotypes. Mutational steps are indicated in dotted circles (if not indicated, mutational step is equal to one; link lengths are proportional to mutational steps). The median vectors that represent hypothetical intermediates or missing (unsampled) haplotypes are shown in squares. The areas of the circles are proportional to the haplotype frequency.

Discussion Thus, only a handful of the complete CR sequences were available in Genbank for comparison. Smith et Several studies on M. fascicularis have showed al. (2007) used the HVI on the Malaysian, Indonesian, differences in variations between the HVI and HVII Mauritius, Philippines, and Vietnamese M. fascicularis of the CR (Smith et al., 2007; Blancher et al., 2008; while Shiina et al. (2010) worked on three Indochinese Kawamoto et al., 2008; Shiina et al., 2010). Similarly, subpopulations including the populations from our findings also revealed that the HVI harboured more Indonesia and the Philippines. Our finding revealed that variations compared to the HVII. Thus, we recommend all the haplotypes detected from Penang represent newly that future studies on the CR should concentrate on the described haplotypes with none shared with the other HVI. M. fascicularis regional populations. Additionally, none Previous studies investigating the genetic variations of the haplotypes matched the samples (149 samples of and diversity of M. fascicularis either examined the unknown localities from Malaysia) used by Smith et al. HVI (Smith et al., 2007) or HVII (Blancher et al., (2007). Therefore, we would assume that the samples 2008; Kawamoto et al., 2008; Shiina et al., 2010). used by Smith et al. (2007) did not originate from

20 © University of Andalas / Copenhagen Zoo Genetic diversity of M. fascicularis the Penang population. However, the small number of samples used in this study could prevent us from detecting any possible haplotypes sharing. The π within the island for all three datasets (complete CR, HVI, and HVII) showed lower genetic diversity when compared to the mainland. This condition is very similar with the other island populations of Philippines and Mauritius, which could suggest a bottleneck or a small founder size following colonisation from the mainland (Blancher et al., 2008; Kawamoto et al., 2008). Nevertheless, the small sample number could also provide bias to the diversity observed. The distribution pattern of the haplotypes in this study strongly correspond to their geographical distributions (Fig. 1). Macaca in particular displays an extreme level of sex-biased dispersal (Melnick & Hoelzer, 1992) where only males disperse from one population to another while the females remain sedentary in nature. This will lead to geographically structured mitochondrial haplotypes which shows structuring of populations according to historical cladogenic events (Melnick et al., 1993; Tosi & Coke, 2007). In this study, we observed moderate structuring between the Penang mainland and the two island populations (FST of 0.43 and 0.37 respectively for Jerejak and Penang Island) as well as to the other neighbouring populations (FST of 0.37 for both the other Malaysian and Indonesian populations). The genetic distances between the mainland to the island populations are however low as compared to the other populations (Table 3). The narrow Penang Strait would act as a contemporary barrier to the gene flow between the mainland and the island apart from the sedentary nature of the females. The historical connectivity and the close proximity would explain the low genetic distances between the mainland and the island populations. On the other hand, the single haplotype sharing (Hap4) observed between the mainland and island could be explained as a remnant of the ancestral genetic makeup from the earlier colonisation from the mainland. The emergence of past land bridge connections permitted gene flow between the mainland and island populations. This is supported by our recent work on Figure 3. ML tree the HVI segment (-lnL= 8267.40) the Y-chromosomal gene flow of the males using the constructed using the HKY+G model (Hasegawa et al. 1985) same samples set (Rovie-Ryan et al., 2013) where with 100 bootstrapping. Note that the Penang haplotypes similar haplotypes sharing were observed. However (Group I, II, and III) are clustered within the continental in the past, translocations of M. fascicularis by the lineage. Following the ISO 3166-1 alpha-2 codes for the authorities from the island to the adjacent mainland as a names of countries, MY codes for Malaysia, ID for Indonesia, response to the increasing human-macaque conflict due VN for Vietnam, PH for Philippines, MU for Mauritius, CN for to the urbanisation (S. Elagupillay, pers. comm.) could China, and IN for India. No major discrepancy was observed also explain the haplotype sharing. between the HVI and HVII trees (tree not shown).

2014 Journal of Indonesian Natural History Vol 2 No 1 21 Rovie-Ryan et al.

The single indel observed at np 217 distinguished the provided evidence on the historical connectivity three major groupings of the Penang M. fascicularis. between the mainland and island. The unique The insertion mutation represents the haplotypes haplotypes observed in the Penang samples (especially within Group III while the deletion mutation represents the island population) would be a good indicator to the haplotypes for Groups I and II as also seen in the conserve the genetic uniqueness of M. fascicularis in phylogenetic tree and the haplotype network (Fig. 2). Penang. These findings could be used in management Based on the basal positioning in the phylogeny tree, and conservation strategies especially in the population we suggest that the haplotypes of Group III represents control, and would also be beneficial to other studies for the ancestral form of M. fascicularis in Penang. On a example on the co-evolution of primates with vectors wider scale, all the sequences from the other regional of diseases associated with primates (like evolution of populations of M. fascicularis using the HVI dataset simian malaria parasite) and biogeographical history of also displayed the insertion mutation. Therefore, the Penang Island. Finally, we also discovered that the the deletion mutation observed in Group I and II is CR of the mtDNA is a powerful region to be used in unique only to the Penang M. fascicularis. Due to this addressing the genetic structuring of M. fascicularis. uniqueness, we propose that the Penang M. fascicularis We acknowledge that the small sample numbers could particularly from the island should be managed as a be a source of bias in our findings. Therefore, for a management unit (MU). MUs are a second category more robust and geographically wide analysis, more of population subsets that are demographically distinct samples should be collected from Penang and from a and are much smaller than the evolutionary significant wider range of localities covering the entire Peninsular units (ESUs) (Moritz, 1994). In Peninsular Malaysia, Malaysia, Sabah and Sarawak. Also, to infer current several strategies of population management has been gene flow, further studies utilizing the Y-chromosome used by the DWNP to control the human-Macaca and microsatellite markers are currently being done. conflicts including on-going population inventories, public awareness programmes, translocation, culling (DWNP, 2006), and recently experimenting on chemical castration (Karuppannan et al., 2013). The findings Acknowledgements from this study would therefore provide policy makers with information on which priority areas or populations We would like to thank the Department of Wildlife and to preserve. National Parks (DWNP), Malaysia, for providing the facilities, equipments, and personnels to conduct this The monophyletic clustering of the M. fascicularis pilot study. Also thanks to the State Director of DWNP as shown in the phylogenetic trees (Fig. 2 and 3) were Penang, Mr. Jamalun Nasir Ibrahim and his staff for in agreement with previous molecular studies using their assistance. This project was funded by the DWNP, mtDNA data (Blancher et al., 2008; Hayasaka et al., and partly by the Proboscis Genome Research grant 1996; Tosi et al., 2002). Comparisons with the other awarded to M. T. Abdullah and colleagues. The sampling regional populations revealed that the Penang samples work for ZMW coded samples was supported in part were clustered within the continental lineage (Fig. 3). by the USAID Emerging Pandemic Threat Program The dichotomy between the continental and the insular – PREDICT Project and by the Skoll Foundation and lineage were first discovered by Harihara et al. (1988) Google Incorporated through Global Viral. We would and later confirmed by Tosi et al. (2002, 2003), Tosi also like to thank the following individuals for their and Coke (2007), and Blancher et al. (2008). Based dedication and help during sampling: Tang Teong Kim, on our calibration, we propose that by the middle Osman Bakar and Rozeta Hj. Zahran. The samplings Pleistocene, around 1.04 mya (Fig. 3), the separation of conducted complied with the rules, regulations and the continental and the insular lineage of M. fascicularis ethical standards in the treatment of the animals as laid occurred. This estimate is close to that proposed by Tosi down by all the relevant wildlife authorities in Malaysia et al. (2003) and Blancher et al. (2008) at ~1.2 mya. as well as the guidelines by the Institutional Animal Care The findings of this study revealed that genetic and Use Committee (IACUC), University of California, diversity and divergence of M. fascicularis were lower Davis, USA as adopted by the PREDICT Project. We in the island as compared to the mainland which could also acknowledge the comments by two anonymous suggest a bottleneck or small founder size following reviewers who helped to improve the earlier version of colonisation from the mainland. The shared haplotype this manuscript.

22 © University of Andalas / Copenhagen Zoo Genetic diversity of M. fascicularis

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Appendix 1. Comparison between the HVI and HVII of the mtDNA CR from different regional populations of M. fascicularis. Number of haplotypes (H) and haplotype diversity (h) were calculated by considering sites with alignment gaps.

HVIa (546 bp) HVIIb (466 bp) Seg. Seg. No Population N CS VS PIS π H h N CS VS PIS π H h Length Length 1 Penang1 46 536-7 490 47 40 0.021 17 0.91 46 461 451 10 6 0.003 9 0.64 2 Malaysia 149 536-9 378 163 147 0.064 104 0.99 3 Indonesia 70 537-9 390 152 131 0.075 55 0.99 65 438-61 384 82 64 0.033 56 0.99 4 Philippines 83 537-40 430 110 64 0.023 34 0.81 14 438-58 451 13 8 0.010 7 0.87 5 Vietnam 89 538-40 441 99 85 0.039 48 0.97 23 461-2 408 55 35 0.027 22 1.00 6 Cambodia 48 441-62 392 71 35 0.021 42 0.99 7 Mauritius 68 537 523 14 10 0.001 8 0.27 6 439-59 461 1 1 0.001 4 0.87 Total 511 546 346 200 176 0.072 261 0.98 202 466 332 134 93 0.05 140 0.98

Seg. Length= Sequence Length, CS= Conserved sites, VS= Variable sites, PIS= Parsimony informative sites, π= Nucleotide diversity (Nei, 1987), H= No. of haplotypes, h= Haplotype diversity (Nei, 1987). aSmith et al. (2007) bShiina et al. (2010), Kawamoto et al. (2008), and Blancher et al. (2008)

2014 Journal of Indonesian Natural History Vol 2 No 1 25 Asiatic Soft-shell Turtle Amyda cartilaginea in Indonesia: A Review of its Natural History and Harvest

Mirza D. Kusrini1, Ani Mardiastuti1, Mumpuni2, Awal Riyanto2, Sri M. Ginting3, and Badiah3

1Department of Forest Resources Conservation and Ecotourism, Faculty of Forestry, Bogor Agricultural University, Indonesia 2Museum Zoologicum Bogoriense, Research Center for Biology, Indonesian Institute of Science, Indonesia 3Ministry of Forestry, Republic of Indonesia

Corresponding author: Mirza D. Kusrini, Email: [email protected]

Abstrak Makalah ini mengulas tentang biologi dan pemanenan labi-labi Amyda cartilaginea di Indonesia. A. cartilaginea tersebar secara luas di Indonesia, terutama pada lahan basah di pulau-pulau besar. Dari berbagai survey diketahui bahwa A. cartilaginea ditemukan pada berbagai habitat perairan tawar, sebagian bahkan dapat ditemukan di sekitar permukiman. Individu betina dapat bertelur beberapa kali dalam setahun, namun masa biak tidak dapat ditentukan dengan pasti. Labi-labi betina diperkirakan mulai mampu bereproduksi sekitar usia 3 tahun. Meski pun labi-labi tidak pernah ditemukan dalam jumlah banyak pada suatu wilayah karena warnanya yang tersamar, jumlah populasinya secara umum melimpah. Mengingat bahwa spesies ini telah terdaftar dalam CITES Appendiks II, maka pemanenan labi-labi A. cartilaginea untuk tujuan ekspor telah diatur oleh pemerintah Indonesia. Pemanenan labi-labi dilakukan sepanjang tahun, tanpa memperhatikan jenis kelamin. Penelitian lebih mendalam tentang ekologi labi-labi dan dampak pemanenannya masih diperlukan. Pemanenan labi-labi dianggap mengkhawatirkan bagi kelestarian spesies ini. Untuk pengelolaan spesies, pemantauan tahunan terhadap pemanenan dengan menggunakan metoda standard perlu dilakukan, khususnya pada lokasi dengan jumlah pemanenan yang tinggi.

Abstract This paper provides a review of the natural history and harvest levels of the Asiatic soft-shell turtleAmyda cartilaginea in Indonesia. A. cartilaginea is distributed widely in Indonesia, mostly in wetlands of the major islands. Surveys have found that A. cartilaginea reside in various freshwater habitats, even some near the vicinity of human settlements. There is no apparent breeding season, and females might lay more than one clutch during the year. It is estimated that females become reproductive around 3 years of age. Although A. cartilaginea is never seen in large numbers in one area, mostly due to its cryptic nature, it is generally considered abundant. Harvest of A. cartilaginea for export is regulated by the Government of Indonesia, as part of its inclusion in Appendix II of CITES. In practice, harvest is conducted all year, with no apparent preference for sex, but more research is needed regarding the species ecology and impact of harvest. The harvest of A. cartilaginea in Indonesia is a major concern for the conservation of the species. Annual monitoring of harvest levels using standardized methods should be carried out especially in locations subjected to high harvesting pressure, to assist management of the species.

Keywords: Amyda cartilaginea, harvest, trade, population

Introduction rivers, swamps, and oxbow lakes adjacent to large rivers (Lim & Das, 1999). In Indonesia, the species is found The Asiatic soft-shell turtle, Amyda cartilaginea, almost in all big islands, such as Borneo, Sumatra, Java, is distributed in Southeast Asia from Myanmar to Bali and except for Papua (Auliya, 2000; Indonesia. It is one of the largest fresh-water turtle Iskandar, 2000; Koch et al., 2008). species in Indonesia with a carapace length reaching up A. cartilaginea is exploited for consumption in to 80 cm (Iskandar, 2000). The turtles occupy a wide Indonesia (Asian Turtle Trade Working Group, 2000; range of habitats, such as muddy rivers, ponds and Iskandar, 2000) and due to years of extensive harvesting irrigation canals, slow moving lowland streams and the population has declined in all range countries except Brunei Darussalam, Cambodia and India (CITES, 2004). The species is now listed as “Vulnerable” on Received 4th February 2014; Revision accepted 29th April, 2014 the IUCN Red-list, mostly due to habitat loss and

26 © University of Andalas / Copenhagen Zoo Natural history and harvest of A. cartilaginea over-exploitation (Asian Turtle Trade Working Group, longest carapace length reported, based on survey data, 2000). As the only country with a quota for export, is 80 cm in East (Kusrini et al., 2009) and Indonesia is under scrutiny for its extensive legal 70 cm in Riau (Mumpuni and Riyanto, 2010). In East hunting of A. cartilaginea. According to data by the Kalimantan, turtles harvested for trade typically weigh WCMC database, the harvest quota for individuals of 13.5 kg (n = 612) but have been recorded up to 65 kg this species was 25,200 heads in 2013. At the inclusion (Kusrini et al., 2009). There is no literature available on of this species in CITES as Appendix II, exports of growth rates. live turtles in Indonesia exceeded quota levels (2005 to There are no records on A. cartilaginea longevity, age at 2007), whereas after 2008 the export never exceeded first reproduction or maximum breeding age. However, the legal quota (Tab.1). Despite the large off-take of Mumpuni and Riyanto (2010) reported that the CL of a this species, information pertaining to harvesting effort, 2 year old mature female measure approximately 30 cm. demography, ecology or conservation of the species in Using data from East Kalimantan (Kusrini et al., 2009), Indonesia is lacking. From 2009 to 2012, a series of a 30 cm CL corresponds to a 3 kg body mass for A. research activities on A. cartilaginea were conducted cartilaginea. Results from dissections of female turtles in various locations in Indonesia, consisting of harvest collected in Jambi Province (Sumatra) showed that the monitoring in Kalimantan and Sumatra, and breeding smallest size of sexually mature females measured 28.5 biology in experimental breeding farms. This paper cm CL, 24 cm Carapace Width (CW) and 2.2 kg body aims to compile available knowledge about a) ecology mass (Mumpuni & Riyanto, 2010). Ginting (2012) and life history, b) population dynamics, and c) review reported that the smallest sexually matured female the existing information about harvest and trade of A. turtle dissected with egg follicles measured 32.4 cm cartilaginea in Indonesia. CL and 3.19 kg body mass. Therefore, it is reasonable to assume that a 2 year old female is already able to reproduce. Ecology and life history Reports on the number of eggs per clutch varied. Iskandar (2000) indicates 40 as the maximum clutch The Asian soft-shell turtle, Amyda cartilaginea, is a big size, whereas Liat and Das (1999) stated that the clutch sized freshwater turtle. The maximum carapace length sizes range from 5 – 30 eggs. Hunters in East Kalimantan (CL) of A. cartilaginea has been reported to reach 100 reported that the number of eggs per clutch was 20-50 cm, although the CL of most A. cartilaginea found (Kusrini et al., 2009). From nine nests occurring at in the wild measure up to 60 cm (Iskandar, 2000). The Belawa Villages (West Java), the number of eggs found was 3 – 17 per nest (Kusrini et al., 2007). Susanti (2013) reported that the number of eggs from 10 nests at an experimental farm was 11 – 19 eggs per clutch. Based Table 1. Exports and quotas of Amyda cartilaginea from 2005 – 2013 (Source: WCMC, CITES Trade Database*, Directorate on dissection of 6 specimens, Mumpuni and Riyanto General of Forest Protection and Nature Conservation). (2010) found the number of follicles ranged from 16 – 29 with at least two different sizes, which suggest that Export Actual Year Purpose the species might be able to release eggs at least twice Quota Exports* during breeding season. 2005 27000 34066 Consumption New eggs are usually pure white in color, translucent 2006 27000 32665 Consumption (somewhat transparent) and the outer skin of the egg is 2007 27000 26710 Consumption soft. Eggs that have been long in the nest are a white 2008 25200 25197 Consumption or creamy white bone colour (not shiny), smooth, and 2009 25200 25200 Consumption hard-shelled, but fragile (Kusrini et al., 2007). The size of A. cartilaginea eggs is shown in Table 2. 2010 25200 25104 Consumption Incubation time differs for each clutch, which reflects 2011 23400 Consumption 24764 environmental variables such as nest temperature and 1800 Pet humidity, as is the case for other turtle species. Iskandar 2012 25200 No data Consumption (2000) reported that eggs of A. cartilaginea hatch 2013 25200 No data Consumption after 135-140 days, whereas Susanti (2013) reported

2014 Journal of Indonesian Natural History Vol 2 No 1 27 Mirza et al.

Mean Range Diameter Weight Diameter Weight Source (mm) (g) (mm) (g) Pritchard (1979) - - 30.5 – 35.5 - Table 2. Diameter and weight of Amyda cartilaginea Liatt & Das (1999) - - 21.0 – 40.0 - eggs. Kusdinar et al. (1999) 32.3 17.2 31.1 – 33.2 14.5 – 18.8 Iskandar (2000) - - 21.0 – 33.0 - Kusrini et al (2007) 30.0 17.6 27.0 – 32.0 13.9 – 21.4 Susanti (2013) 31.8 19.5 28.4 – 34.6 12.0 – 24.0

Approximate age Age group # of dead individuals (year) Un-reproductive adults > 80 7 Table 3. Amyda cartilagenea mortality in Belawa Reproductive adults 3-20 80 Village Cirebon during the infection episode in 2010 (Source: Sunyoto 2013). Juveniles 0-1 125 Total 212

Table 4. Habitat characteristics of Amyda cartilagenea at different locations in Indonesia.

Vegetation Habitat Adjacent Water body Location Depth (m) around water Source type landscape width bodies Bulungan, Berau, and Hard wood and Malinau Regencies at Rural and ex logging Kusrini et al River 5-20m 3-8 bushes, mostly the northern part of East concession area 2009 unshaded Kalimantan Province Sambas and Ketapang Not River Not available Not available Not available Lily 2010 Regency, West Kalimantan available 25m (river) River, swamp Ogan Komering Ilir 1200ha Grass and bushes, and flood 2-7 Oktaviani 2007 Regency, South Sumatra (fresh-water Mostly unshaded plain swamp) Rokan Hulu and Siak 2-5m (river) River and Grass and bushes, Mumpuni & Regency of Riau Province, Palm oil plantation 5-7ha 1.5-2 peat swamp mostly unshaded Riyanto 2010 Sumatra (peat swamp) 0.5 – 2m Paddy, grass, Irrigation Rice fields, human Mumpuni et West Sumatra (water 0.3-1.2 garden , channel, river habituation al. 2011 irrigation) mostly unshaded Belawa Village, Cirebon Few garden Man-made Kusrini et al. Regency of West Java Human habituation 0.01-0.2ha 1.5-3 plants, mostly fish pond 2007 Province unshaded

28 © University of Andalas / Copenhagen Zoo Natural history and harvest of A. cartilaginea that from three clutches of eggs induced by artificial habitats consist of a variety of freshwater habitats: incubation, juveniles emerged after 95 - 102 days of ponds, lakes (including oxbow lakes adjacent to incubation. Newly hatched juveniles live primarily on large rivers), streams and rivers (upland streams and their egg yolk for 3-5 days after hatching. The size of muddy, slow-flowing lowland streams, and rivers), newly hatched juveniles range from 4.0 – 5.1 cm CL peat swamps, canals, and possibly estuaries (Auliya, with a body weight of 9.0 – 17.0 g (Susanti, 2013). 2007; Iskandar, 2000). Surveys in the last few years in In Riau, Mumpuni and Riyanto (2010) reported that Kalimantan, Sumatra and Java shows that key habitat the diet of A. cartilaginea consisted of oil palm seeds, is not necessarily situated in natural areas with dense cassava, scrap, fish, unidentified leaf and seeds and vegetation surrounding the water bodies (Ginting, avifauna. Furthermore, Mumpuni et al. (2011) indicated 2012; Kusrini et al., 2009; Lilly, 2010; Mumpuni & that the soft-shelled turtle at Bandar Gadang (West Riyanto, 2010; Mumpuni et al., 2011; Oktaviani, 2008). Sumatra Province) in rice fields consumed primarily Instead, A. cartilaginea is well adapted to water bodies snails of the species Pomacea canaliculata, similar to near human habitation or man-made habitats such as the finding of Ginting (2012) in Jambi, suggesting that fish ponds and water channels adjacent to paddy fields A. cartilaginea is an important predator of this pest. (Tab. 4). This might explain its wide distribution. In Belawa (West Java) the turtles are sometimes given Nesting usually take place near water bodies. In East food by villagers consisting of water spinach, dried fish, Kalimantan, hunters reported that A. cartilaginea lays and other food scraps (Kusrini et al., 2007). All of this eggs underground in muddy substrate or among tree is relevant to the conclusions of previous researchers buttresses covered with leaves and rotten wood (Kusrini that A. cartilaginea is an opportunistic omnivore (Amri et al., 2009). Surveys by Mumpuni et al. (2011) in & Khairuman, 2002; Iskandar, 2002; Jensen & Das, West Sumatra found a nest containing 6 eggs near an 2006; Pritchard, 1979). irrigation channel for rice fields, beneath a kapok tree Information on the diseases of A. cartilaginea is scarce. (Ceiba pentandra). In Belawa, Cirebon (West Java), In 2010, Indonesian media reported that hundreds of nests were found on sloping ground at the edge of the A. cartilaginea died in Belawa, West Java (Haryadi pond, covered by grass, with the distance to the water of & Pamungkas, 2010). An unpublished report by the about 1.9-4.5 m (Kusrini et al., 2007). fisheries quarantine laboratories in Cirebon revealed that these turtles were infected by Saprolegnia sp. fungus, along with Edwardsiella tarda and Aeromonas Population estimates veronii bacteria (Badan Karantina Ikan Pengendalian Mutu dan Keamanan Hasil Perikanan, undated). Previous reports categorized the population of A. Sunyoto (2010) reported that more than 200 turtles died cartilaginea in Indonesia as “common” or “locally from the infection in a very short time (Tab. 3). abundant” (Samedi & Iskandar 2000). In contrast, a A report by Indonesia CITES MA (2008) cited report by Setyobudiandi and Zairion (1997) mentioned information by traders in Kalimantan and Sumatra difficulties in finding the species in West Java, which that many A. cartilaginea were infested by leeches. resulted in A. cartilaginea in Java being considered Information by Sudiana et al. (2000) in Java showed “not suitable for commercial harvest”. However, to that 90% of the samples of wild A. cartilaginea were date there exists no reliable population estimate with infested by the ectoparasite worm, Pseudocalceostoma the current estimates subjected to various biases. For sp. both on the carapace and plastron. example, in Belawa Cirebon, the local people often There has been little information on micro-habitat reported that the present harvesting numbers of A. use and movement of the A. cartilaginea. Kusrini et al. cartilaginea were lower compared to past harvesting (2009) reported that hunters in East Kalimantan find numbers. While it may provide a relative indication A. cartilaginea in underground cavities of riverbanks, of population size, it may also merely reflect changes where they rest, mate, and congregate. Furthermore, in harvesting efforts. In 1995, Kusdinar et al. (1999) hunters reported that 7 to 12 A. cartilaginea can use the found 88 individual turtles in Cikuya River in Belawa same mud cavity at the same time. (consisting of 6 hatchlings, 12 juveniles and 70 mature A. cartilaginea is primarily aquatic but, as with individuals). This is approximately half of what was most turtles, females lay eggs in terrestrial nests found in a 2007 survey (Kusrini et al., 2007) where 161 near water bodies. Almost all reports stated that key individuals were recorded. Low sightings and capture

2014 Journal of Indonesian Natural History Vol 2 No 1 29 Mirza et al. rates do not necessarily mean low population size but the hunters remove it and transports them to a collector can be a result of sampling bias as experienced in many alive. The use of baited hooks was also reported by other herpetological surveys (Plummer et al., 2008; Walter (2000) in Sentarum Lake, West Kalimantan. Wilson et al., 2008), especially for cryptic species. In West Sumatra, harvesting is carried out by pole Since A. cartilaginea tends to stay covered in mud for fishing and a blunt stick (Mumpuni et al., 2011). The prolonged periods of time (Sunyoto, 2012) they are first method is usually applied by fishermen mainly to particularly subject to estimation bias. catch fish, with turtles not the main target and being a Efforts to estimate populations were carried out in by-catch. The second method is used by professional East Kalimantan (Kusrini et al., 2009) and Sumatra turtle hunters. A team consisting of 3 to 5 people will (Mumpuni et al., 2010, 2011). Using a series of baited walk along small creeks or tunnels to search turtle using hooks for two weeks, 36 individual A. cartilaginea were a blunt stick to probe the bottom. Whenever the tip of captured collectively in East Kalimantan (Kusrini et the stick strikes a turtle, the hunters will surround and al., 2009). A rough estimate revealed a relative density catch it. The method is usually applied during dry season of 0.66 A. cartilaginea per kilometer of river in East between February and June. In Air Hitam Dalam River Kalimantan. A higher value was provided by Mumpuni in Sumatra, professional turtle hunters used fishing rods et al. (2011) in their survey in West Sumatra, where the to capture A. cartilaginea as well as rattan funnel traps relative density of A. cartilaginea in water irrigation using duck-meat as bait. The fishing rod was checked channels reached 16 individuals/km. In Lubuk Dalam every day in the afternoon. In Riau and Jambi, nylon peat swamp in Riau, in the vicinity of an oil palm funnel traps known as lukah measuring 100 cm x 80 cm plantation, the relative density of A. cartilaginea was x 100 cm and metal funnel traps (pengilar), measruing 21 individuals/ha (Mumpuni et al., 2010). These results 80 cm long and 40 cm in diameter were also used, as indicate that the density of the soft-shelled turtles varied well as electric fishing methods (Mumpuni & Riyanto, according to location. However, there might be bias in 2010). calculating density due to (1) observer variation, (2) In general, hunters do not differentiate between males unequal capture effort and difficulties, (3) inclusion and females of A. cartilaginea in Indonesia, which is of escaped captured turtles, and (4) movement and illustrated by the equal proportion of females and males migration of turtle. Surveys showed that the soft-shelled captured (Kusrini et al., 2009; Lilly, 2010; Ginting, turtle tend to be solitary, able to be submerged in water 2012). Instead, the sex ratio of the harvested specimens for long periods of time, thus visually difficult to detect of A. cartilaginea seemed to illustrate the success of and most probably has a wide home range. Irrespective capture effort. We assumed that these conditions were of natural densities or habitat types, tens of thousands primarily caused by the nature of harvesting, which of turtles are captured and traded every year (Tab. 1). occurs all year round, excluding the possibility of catching only one specific sex (e.g. if only hunting in the nesting season). In addition, there are no specific Harvest and trade consumer preference for neither males nor females. This is of critical conservation importance, because Harvesting techniques varied according to location. preference for particularly breeding females can have In East Kalimantan Kusrini et al. (2009) reported that several negative consequences. A high proportion of hunters harvest turtles using baited hooks, except in female Pig-nosed turtle (Carettochelys insculpta) is Sebuku, where respondents used long sticks to locate harvested in Papua New Guinea, which are typically turtles. To fish for turtles, a series of 10 – 70 baited captured during the nesting seaon (Eisemberg, 2010), hooks are placed at certain distances along a riverbank. and similarly for the Mekong snail-eating turtle Bait consists of meat from a variety of species such (Malayemys subtrijuga) in Cambodia, because of as chicken, fish, wild boar (Sus scrofa), monitor comsumer demand for females with eggs as special lizard (Varanus salvator), reticulated python (Python dishes (Platt et al., 2008). reticulatus), and even primates e.g. Harvest size-limits are imposed by Indonesia’s CITES (Nasalis larvatus). Fishing lines with hooks are usually Management Authority, and are based on weight. By placed during high water and checked at least three these rules hunters are allowed to harvest specimens times, each with an hour interval, before the hunter weighing less than 5.5 kg (mostly for pets) or more moves to another hunting site(s). If a turtle takes the bait, than 13.5 kg (for meat/consumption), leaving most of

30 © University of Andalas / Copenhagen Zoo Natural history and harvest of A. cartilaginea the reproductive individuals (Indonesia CITES MA, Konsumsi Indonesia; Association of Turtle and Soft- 2008). Unfortunately, in practice all measurements shelled Turtle Traders). Quota levels for turtle harvest of the harvested turtles reveal that more than half fell set by Indonesia CITES MA were disseminated to within the prohibited range of 5.5-13.5 kg. Based on the members of the Association. Export quotas for A. surveys carried out in Kalimantan (Kusrini et al., 2009; cartilaginea is based on heads, and not by weight. Since Lily, 2010), and Sumatra (Ginting, 2012; Mumpuni et the price of A. cartilaginea for consumption depends al., 2011; Oktaviani, 2007), the population structure, on weight, traders prefer to sell bigger sized turtles, based on the body weight, showed a heavy bias towards rather than smaller sized. All exporters get turtles small individuals, with the smaller turtles captured at a from their collectors, and although exporters might much higher rate than larger reproductive individuals. decide to refuse turtles when quota limits are passed The fact that harvests mostly captured small size (Indonesia CITES MA, 2008), in reality traders claim turtles probably corresponds with the size structure that rejecting harvesters is not possible due to social of actual populations in the wild. Assuming that the concerns (Maraden Purba, pers. comm). Small turtles demography of A. cartilaginea in Belawa represented are sometimes kept in holding ponds until they grow to the wild population elsewhere, results of Kusrini et sufficient sizes (Ginting, 2012; Indonesia CITES MA, al. (2009) surveys showed that the population of A. 2008; Oktaviani, 2007) or they are sold for domestic cartilaginea scattered in ponds in Belawa consisted and international markets beyond the quota limits. At mostly of small individuals. Of the 161 turtles found, the moment, there is no information on the estimated 3.7% were hatchling, 50.9% were juvenile, 33.6% were number of turtles used for domestic consumption. sub-adult and only 11.8% were adult. The export quota for A. cartilaginea remained stable In 2009, 18 exporters established the association at 27,000 heads between 2005 and 2007. In 2008, APEKLI (Asosiasi Pengusaha Kura-kura dan Labi-labi the export quota for A. cartilaginea was adjusted

Figure 1. The distribution of 2010 harvest of Amyda cartilagenea from Indonesia (Data Source: Directorate General of Forest Protection and Nature Conservation).

2014 Journal of Indonesian Natural History Vol 2 No 1 31 Mirza et al. downwards to 25,200. The quota covers two purposes, breeding trials are already underway in several namely for consumption and for pets, in which more locations. In Siak Regency, Riau (Sumatra), the pulp than 80% are for consumption (Tab. 4). Based on 2005- and paper company of Sinar Mas Group has prepared 2012 CITES trade data, A. cartilaginea from Indonesia a facility to breed A. cartilaginea, and started with a is exported to 22 countries from Asia, Europe, North holding of 48 parent stock (Mumpuni et al., 2010). America and Middle East, with the majority going to Unfortunately, there have been no further reports on Singapore (49%), Hong Kong (36%) and China (9%). the development or success of this facility over the Except for the Netherlands, that still imports of small past several years. The association of turtle traders has numbers of A. cartilaginea in 2010 and 2011, export begun to encourage members to carry out breeding of Indonesian A. cartilaginea to Europe stopped after a trials in Tangerang (Banten Province), and nine parent European Union Wildlife Trade Regulation suspended stock (6 females and 3 males) kept in a pond by PT A. cartilaginea from Indonesia in 2008. Ekanindya Karsa since 2008 successfully breed at the Based on data published annually by Indonesia CITES end of 2011 (Susanti, 2013). The company, whose MA, the source of A. cartilaginea came from two main main commodity is captive breeding of crocodiles, islands of Indonesia: Kalimantan and Sumatra. Using has expanded with ponds designed to house the new the 2010 harvest data, two provinces have the highest juvenile A. cartilaginea. production of A. cartilaginea namely East Kalimantan and North Sumatra Province (Fig. 1). The high number of reproductively active A. Conservation recommendations cartilaginea captured each year has raised concerns about maintaining a stable population in the wild. It is clear from the limited available data that there is The available data on the relative density of the A. a need for more information to assess the impact of cartilaginea from previous surveys might be useful to harvesting on the populations of A. cartilaginea in gain insight into the number of harvestable specimens site specific regions. Further research on reproduction, within a province. The risk of this, however, is that ecology and population dynamics should be undertaken such data may provide an inaccurate estimation of A. at localities across the range of A. cartilaginea for cartilaginea population in a province and, therefore, comparative purposes. Long term research should be a false foundation for quota setting. Whereas key initiated in areas where the A. cartilaginea is abundant, habitat of A. cartilaginea consists mainly of fresh water in harvested and non-harvested areas. Standard wetlands, possibly shallow freshwater wetlands located methods to monitor A. cartilaginea population should below 500 m above sea levels (Oktaviani, 2007) there is be developed, including methods to mark individual no available data on size of freshwater wetlands in each for the purpose of mark-recapture studies. Modeling of province in Indonesia. It is estimated that there are more than 20 million ha of freshwater habitat in Indonesia, habitat suitability of A. cartilaginea should be carried excluding rivers (Komite Nasional Pengelolaan Lahan out. Basah Indonesia, 2004). Considering the availability of Trade monitoring should be done monthly and be a wide range of key habitats for A. cartilaginea, it is reported annually by the respective Regional Forestry estimated that the potential number of harvestable turtles Office in each province (BKSDA). To assess population is in fact higher than the existing quota. Estimations structure and seasonal fluctuation, exporters should of harvest levels in East Kalimantan indicate that the provide a record of size/weight collected by harvesters. capture rate was still far below the production of A. Trade monitoring should also include monitoring of A. cartilaginea in the survey area. However, without cartilaginea for domestic consumption. accurate data on national or international trade, or turtle populations, a precautionary approach should be used in harvesting regimes. References The export harvest for two companies in Balikpapan in 2008 was 3,979 heads which included 13% mortality Amri K and Khairuman (2002). Mengenal lebih dekat (ID CITES MA, 2008). Currently, there are no A. Labi-labi: Komoditas Perikanan Multimanfaat. PT. cartilaginea breeding farms in Indonesia, however, Agro Media Pustaka, Jakarta.

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Asian Turtle Trade Working Group (2000). Amyda Iskandar, D.T. (2000). Turtles and crocodiles of cartilaginea. In: IUCN 2012. IUCN Red List of Indonesia and Papua New Guinea with notes on other Threatened Species. Version 2012.2. . Downloaded on 29 March 2013. Jensen, K.A. and I. Das (2008). Dietary observations Auliya, M (2007). An identification guide to the tortoise on the Asian softshell turtle (Amyda cartilaginea) from and freshwater turtles of Brunei Darussalam, Indonesia, Sarawak, Malaysian Borneo. Chelonian Conservation Malaysia, Papua New Guinea, Philippines, Singapore and Biology 7(1): 136–141. and Timor Leste. TRAFFIC Southeast Asia. Petaling Jaya, Malaysia. Koch, A., Ives, I., Arida, E. and D.T. Iskandar (2008). On the occurrence of the Asiatic softshell turtle, Amyda Badan Karantina Ikan Pengendalian Mutu dan cartilaginea (Boddaert, 1770), on Sulawesi, Indonesia. Keamanan Hasil Perikanan (Undated). Kura Kura Hamadryad 33: 121 – 127. Belawa, Fauna Khas Cirebon Yang Terancam Punah: Laboratorium Stasiun Karantina Ikan Kelas II Cirebon Komite Nasional Pengelolaan Ekosistem Lahan Basah Mendektesi adanya Bakteri Edwardsiella tarda HPIK golongan II. Download at http://www.bkipm.kkp.go.id/ (2004) Strategi Nasional dan Rencana Aksi Pengelolaan new_puskari/detil_kegiatan.php?id=139 on 8 January Lahan Basah Indonesia. Kementerian Lingkungan 2012. Hidup. Jakarta.

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Mumpuni and A. Riyanto (2010). Harvest, population Setyobudiandi, I. and Zairion (1997). Studi habitat and natural history of Soft-shelled turtle (Amyda dan distribusi penyu air tawar Amyda cartilaginea di cartilaginea) in South Sumatera, Jambi and Riau Kabupaten Bogor. Lembaga Penelitian dan Pengabdian provinces, Indonesia: A report submitted to APEKLI. kepada Masyarakat. Institut Pertanian Bogor. [Abstract Cibinong. only].

Mumpuni, Mulyadi, Suharto, S., Adrinaldi and Sudiana, R., Taruni, P.S., Farajallah, A. (2000). M.S. Nur (2011). Asiatic soft-shell turtle (Amyda Cacing parasit pada labi-labi (Dogania subplana dan cartilaginea) population survey for sustainable harvest Amyda cartilaginea) di Bogor. Paper presented at in West Sumatera, Indonesia: A report submitted to Seminar Nasional Aplikasi Biologi dalam Peningkatan CITES Secretariat. CITES Scientific and Management Kesejahteraan Manusia dan Kualitas Lingkungan. Authority of The Republic of Indonesia. Jakarta. Fakultas Biologi, Universitas Gadjah Mada, 22 September 2000. . [Abstract only]. Oktaviani, D. (2007). Kajian habitat, biologi, dan perdagangan labi-labi (famili: Trionychidae) di Sunyoto (2012). Konservasi labi-labi Amyda cartilaginea Sumatera Selatan dan implikasinya terhadap konservasi (Boddaert, 1770) di Desa Belawa, Kecamatan Lemah labi-labi di masa datang. [MS Thesis]. Program Studi Abang, Kabupaten Cirebon, Provinsi Jawa Barat. [MS Biologi, Fakultas Matematika dan Ilmu Pengetahuan Thesis]. Sekolah Pasca Sarjana. Institut Pertanian Alam, Universitas Indonesia. Jakarta. Bogor.

Platt, S.G., Sovannara, H., Kheng, L., Holloway, R., Susanti, F.N. (2013). Pemeliharaan labi-labi (Amyda Stuart, B.L., T.R. Rainwater (2008). Biodiversity, cartilaginea Boddaert, 1770) dan uji coba preferensi exploitation, and conservation of turtles in the Tonle pakan anakan di penangkaran PT. Ekanindya Karsa, Sap Biosphere Reserve, Cambodia, with notes on Kabupaten Serang. [Skripsi] Fakultas Kehutanan. reproductive ecology of Malayemys subtrijuga. Institut Pertanian Bogor. Chelonian Conservation and Biology 7(2):195–204. Walter, O. (2000). A study of hunting and trade of Plummer, M.V., Krementz, D.G., Powell, L.A. and N.E. freshwater turtles and tortoises at Danau Sentarum. Mills (2008). Effects of habitat disturbance on survival Borneo Research Bulletin. Retrieved on 13 Apr, 2009 rates of softshell turtles (Apalone spinifera) in an urban from http://findarticles.com/p/articles/mi_hb036/ stream. Journal of Herpetology 42: 555–563. is_2000_Annual/ai_n28816646/ Pritchard, P.C.H. (1979). Encyclopedia of turtle. T. F. Willson, J.D., Winne, C.T. and M.B. Keck (2008). H. Publication, Neptune N. J. Samedi , Iskandar DT Empirical tests of biased body size distributions in (2000). Freshwater turtle and tortoise conservation aquatic snake captures. Copeia 2008: 401–408. utilization in Indonesia. Chelonian Research Monographs 2:106-111.

34 © University of Andalas / Copenhagen Zoo Short communications Aromatic Plants in Bali Botanic Garden Indonesia

Wawan Sujarwo1,2 and Ida Bagus Ketut Arinasa1

1Bali Botanic Garden - Indonesian Institute of Sciences (LIPI), Candikuning, Baturiti, Tabanan, Bali, Indonesia. 2Department of Science, University Roma Tre, Viale G. Marconi 446, Rome, Italy.

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

Introduction for preserving their habitat and monitoring the effect of rehabilitative efforts. Further, aromatic plants have Aromatic plants have a pleasant, characteristic fragrant considerable potential both in national and international smell. The fragrance of these plants is carried in market. Indonesia could increase its contribution to meet the essential oil fraction. Many aromatic plants are the growing demand by supplying high quality aromatic condiment (Okigbo et al., 2009). Chandarana et al. and its products. It contribute significantly to the (2005) defined spices as any dried, fragrant, aromatic or nation’s foreign earnings and strengthen the economy of pungent vegetables or plant substances in whole, broken the country. There remain tremendous possibilities for or in ground forms that contributes relish or piquancy increasing the production and trade of aromatic plant, of foods and beverages. Moreover, aromatherapy is a both for internal consumption and export, but it calls form of alternative medicine in which healing effects for an integrated and continuous effort in conservation, are ascribed to the aromatic compounds in essential oils sustainable utilization, cultivation, maintenance and and other plant extracts (Prabuseenivasan et al., 2006). production of aromatic plant resources. Currently, Aromatic plants are also used for preservation of food Indonesia has not yet initiated any in-situ and ex-situ and for adding pleasant and exotic flavours, fragrance, conservation efforts of aromatic plants. color and even texture. Bali Botanic Garden (BBG) has become one of the Indonesia - due to its wide range of geographical, conservation centers in Indonesia. The BBG is situated ecological and biological diversities - possesses many in the mountain tourist resort, . It is situated species that are directly or indirectly used as sources on the east slope of Bukit Tapak Hill, at an elevation of 1,250-1,400 m above sea-level, adjacent to the of herbal, allopathic or homeopathic medicines and Batukahu Nature Reserve (15,390 ha). The total area aromatic. However, many of these plant species of the BBG measures 157.5 ha (Sumantera, 1993). are facing threats of extinction due to over and By December 2013 BBG boasted 2693 species in its improper exploitation, habitat loss, fragmentation and collection, consisting of 405 families, 1326 genera and degradation of land, urbanization pressure and our including 336 species of medicinal plant and 216 species ignorance about them. On the other hand, the increasing of ceremonial flora (Bali Botanic Garden, 2014). global demand for aromatic and products warrants The collection and recording of a comprehensive accelerated cultivation, marketing and conservation of aromatic plants list is important for the categorizing and aromatic plants. Hence, the scientific study of aromatic, understanding of the aromatic qualities of these plants derivation of essential oil through bioprospecting and that are freely available to interested users. This study systematic conservation of the concerned aromatic provides an overview and discussion of aromatic plants plants are of great importance. collected by BBG. The major drawback in this area is scarcity of comprehensive and authoritative information on aromatic plants, which hinders an assessment of their status of availability, implementation activities necessary Methods

Received 28th March 2014; Revision accepted 12th August, Literature on Java and Bali Flora published since 2014 1963 was consulted for information about aromatic

2014 Journal of Indonesian Natural History Vol 2 No 1 35 Sujarwo and Arinasa plants. This included several books (e.g., Backer and Lontar Usada almost 500 different species are described Van Den Brink 1963, 1965, 1968; Ochse and Van Den for its aromatic and medicinal properties (Adiputra, Brink, 1977; Van Steenis, 1997; Tengah et al., 1995; 2013; Sutomo, 2007). Lugrayasa et al., 2009). Information about species and Leaves are the most cited parts of plants used for the properties attributed to each plant, the plant part, life aromatic properties and condiments. Of the 66 plants form, habitat and propagation technique was compiled identified in this study, leaves of 31 species, flowers (Tab. 1). The information also included plants used as of 16 species, stems, rhizomes, seeds, and roots of 4 condiments, but excluding beverages such as liqueurs species, gum or barks of 2 species, and rind of 1 species and herbal teas. Scientific nomenclature was updated were used for aromatic properties and condiment (Fig. using databases (The Plant list, 2013). In order to extract 2). A total of 66 species was distributed into different information about the bioactive compounds for each groups with trees (53%) being the most common, plant, we conducted a search in recent international followed by herbs (24%), shrubs (17%), and woody scientific literature, using scientific names to identify climber (6%) (Fig. 3). and review specific families (e.g., Chauhan, 1999).

Results and Discussion

Plants of Cupressaceae and Rutaceae are important botanical resources of aromatic properties. This study classified 66 taxa of ethno flora, 56 with aromatic properties and 8 with condiment properties. The 66 species belonged to 50 genera in 31 families. The five most frequently used families are illustrated in Figure 1. All 66 species (100%) identified in this study are also documented in the “Lontar Usada Bali”, ancient Balinese scripts that are written on palm leaves and describes forms of healing, medicinal ingredients and methods in traditional Balinese medicine (Sutomo, Figure 2. The frequency of use of different aromatic plants 2007; Tengah et al., 1995). In the traditional Balinese divided into parts of the plant.

Figure 1. The frequency of use of different aromatic plants Figure 3. The distribution of aromatic plant taxa arranged by divided into families. life forms.

36 © University of Andalas / Copenhagen Zoo Aromatic plants in Bali Botanic Garden

Table 1 presents a comprehensive summary of plants Lamiaceae with aromatic and condiment uses described in at least This group of plants is used in aromatherapy, because five books (Backer and Van Den Brink, 1963, 1965, they possess chemical components in their leaves that 1968; Ochse and Van Den Brink, 1977; Van Steenis, provide aromatherapy properties (Chauhan, 1999). The 1997; Tengah et al., 1995; Lugrayasa et al., 2009). A therapeutic properties of these plants are used to cure few species, which are not native to tropical southeast headaches, provide relief in case of nasal congestion Asia but commercialised locally are also included in and suppress any muscular pain. this table. All of these species are recorded in Balinese traditional medicine literature as plants with medicinal properties. Conclusion Usages and dosages differs if they are used for medicinal purposes under the guidance of Balinese traditional This study constitutes one of few ethno-botanical medicine theory. reviews of aromatic plants used on Bali. Results can be used to check the authenticity and origin of aromatic General properties of relevant plant families plants on Bali. It listed 66 aromatic plant species The use of traditional Balinese medical treatment can belonging to 50 genera in 31 families that were used be traced back for centuries, and there is little doubt in traditional Balinese medicine and aromatherapy. that guidance described in “Lontar Usada Bali” result Since many are believed to have beneficial effects on in positive effects. This does not mean, however, that health these plants may be offer good potential for each guidance and treatment method has been tested commercialization. Therefore, more resources should in a systematic scientific manner and the following be allocated to search for new aromatic products from descriptions of the properties and use of various plants plants, especially in plants indigenous to the tropical reflects only traditional use and beliefs of many Balinese countries. citizens.

Cupressaceae Acknowledgement Species belonging to this family have perfect expectorant qualities that is believed to produce a very The authors wish to thank all the colleagues who effective treatment for a number of respiratory ailments contributed to this study with their knowledge and such as coughs and bronchitis. Inhaling the aromatic friendship. We also thank anonymous reviewers for vapour of these plants is supposed to speed up the constructive comments to improve the manuscript. healing process of ulcers and other wounds. They are also known to minimize the appearance of any form of cellulite, combat insomnia, stress and nervous tension References (Chauhan, 1999). Adiputra, I.G.K (2013). Tinjauan taksonomi dan Rutaceae metabolit sekunder coumarins pada tanaman usada These plants are used primarily for pain relief and for Bali. Widaya biologi 4(2): 10-21. the improvement of blood circulation. They contain properties believed to cure acne and contain essential Backer, T.C.A. & Van Den Brink, R.C. (1963). Flora oils that reduce chances of cholesterol related ailments of Java Vol I. Wolters Noordhoff N.V, Groningen, The (Chauhan, 1999). Netherlands.

Lauraceae and Myrtaceae Backer, T.C.A. & Van Den Brink, R.C. (1965). Flora of Plants such as Cinnamomum burmanni, Cinnamomum Java Vol II. Wolters Noordhoff N.V, Groningen, The camphora, Cinnamomum verum and Massoi aromatica Netherlands. are used as tonic, stimulant, bactericide, antiviral and antifungal. They are known to alleviate complications Backer, T.C.A. & Van Den Brink, R.C. (1968). Flora of in the respiratory tract and the respiratory system at Java Vol III. Wolters Noordhoff N.V, Groningen, The large (Chauhan, 1999). Netherlands.

2014 Journal of Indonesian Natural History Vol 2 No 1 37 Sujarwo and Arinasa

Bali Botanic Garden (2013). Updated Collection Sumantera, W. (1993). Bali’s Botanic Garden, Number: February 2014. Bali Botanic Garden. Indonesia, BGC News.

Chandarana, H., Baluja, S. and S.V. Chand (2005). Sutomo (2007). Exploitation and inventory of the Comparison of Antibacterial Activities of Selected Usada Bali medicinal plants in some areas of Buleleng Species of Zingiberaceae Family and Some Synthetic district, Bali. In: Seminar Konservasi Tumbuhan Usada Compounds. Turc J.Biol 29:83-97. Bali dan Peranannya dalam Mendukung Ekowisata (eds M. Siregar, H.M. Siregar, I. B. K. Arinasa and Chauhan, N.S. (1999). Medicinal and Aromatic Plants W. S. Lestari), 2007; pp. 92-7. UPT Balai Konservasi of Himachal Pradesh. Indus Publishing Company, New Tumbuhan Kebun Raya “Eka Karya” Bali Lembaga Delhi. Ilmu Pengetahuan Indonesia, Kebun Raya Bali. Lugrayasa, I.N., Warnata, I.W. and I.B.K. Arinasa Tengah, I.G.P., Arka, I.W., Sritamin, N.M., Gotama, (2009). An Alphabetical List of Plant Species Cultivated I.B.K. and H. Sihombing (1995). Studi Tentang: in Eka Karya Bali Botanic Garden Catalogue. LIPI Inventarisasi, Determinasi dan Cara Penggunaan Press, Jakarta. Tanaman Obat Pada “Lontar Usada” di Bali. Puslitbang Ochse, J.J. & Van Den Brink, R.C. (1977). Vegetables of Farmasi Balitbang Kesehatan Departemen Kesehatan the Dutch East Indies. A.Asher & Co. B.V, Amsterdam, RI, Jakarta. The Netherlands. The Plantlist (2013). The Plantlist Database. Http:// Okigbo, R.N., Anuagasi, C.L. and J.E. Amadi (2009). www.theplantlist.org [accessed 1 February 2014]. Advances in Selected Medicinal and Aromatic Plants Indigenous to Africa. Journal of Medicinal Plants Van Steenis, C.G.G.J. (2007). Flora Pegunungan Jawa. Research 3: 86-95. Pusat Penelitian Biologi LIPI, Cibinong, Jawa Barat.

Prabuseenivasan, S., Jayakumar, M. and S. Ignacimuthu (2006). In Vitro Antibacterial Activity of Some Plant Essential Oils. BMC Complement Altern Med 6:39.

Table 1. Aromatic and condiment Plants currently found in Bali Botanic Garden along with descriptions of its basic use. Scientific name, botanical family Local names Part(s) used Use Life form Habitat Propagation Abelmoschus moschatus Medik. (Malvaceae) Gandapura Seed Aromatic Shrub Full sun Seed

Acorus calamus L. (Acoraceae) Jangu Rhizome Condiment Herb Semi shade Rhizome

Acronychia trifoliata Zoll. (Rutaceae) Empag Leaf Aromatic Tree Full sun Seed

Agathis dammara (Lamb.) L. C. Rich (Araucariaceae) Agatis Gum Aromatic Tree Full sun Seed

Alyxia reinwardtii Bl. (Apocynaceae) Pulesari Stem Aromatic Woody climber Semi shade Seed

Amomum cardamomum L. (Zingiberaceae) Kapulago Rhizome Aromatic Herb Semi shade Rhizome

Aquilaria malacensis Lam. (Thymelaeaceae) Garu Gum Aromatic Tree Semi shade Seed

Artemisia vulgaris L. (Asteraceae) Daun sudamala Root Aromatic Herb Full sun Stolon

Bixa orellana L. (Bixaceae) Kesumba Leaf, root, seed Aromatic Shrub Full sun Seed

Boenninghausenia albiflora (Hook) Rchb. ex Meissn. (Rutaceae) Inggu gunung Leaf Aromatic Herb Semi shade Seed

Brunfelsia uniflora (Pohl.) D. Don. (Solanaceae) Kembang pagi sore Flower Aromatic Shrub Full sun Seed

Camellia sinensis (L.) O. K. (Theaceae) Teh Flower Aromatic Shrub Full sun Seed

Cananga odorata (Lmk) Hook. F. & Thoms. (Annonaceae) Cananga Flower Aromatic Tree Full sun Seed

Cestrum nocturnum L. (Solanaceae) Sedap malam Flower Aromatic Shrub Full sun Seed

38 © University of Andalas / Copenhagen Zoo Aromatic plants in Bali Botanic Garden

Chamaecyparis lawsoniana (A. Murr.) Parl. (Cupressaceae) Keires Leaf Aromatic Tree Full sun Seed

Chamaecyparis obtusa (Sieb. & Zucc.) Endl. (Cupressaceae) Cemara kipas Leaf Aromatic Tree Full sun Seed

Chamaecyparis thyoides (Britton.) Stem & Poggenb (Cupressaceae) Cemara kipas Leaf Aromatic Tree Full sun Seed

Cinnamomum burmanni Nees ex Bl. (Lauraceae) Kayu manis Bark Condiment Tree Full sun Seed

Cinnamomum camphora (L.) Presl. (Lauraceae) Kamper Bark Aromatic Tree Full sun Seed

Cinnamomum sintoc Bl. (Lauraceae) Sintok Leaf Aromatic Tree Full sun Seed

Cinnamomum verum J.S. Presl. (Lauraceae) Sintok lue Leaf Aromatic Tree Full sun Seed

Citrus aurantifolia (Christm. & Panz.) Swingle (Rutaceae) Jeruk nipis Fruit Condiment Shrub Full sun Seed

Citrus grandis (L.) Osbeck (Rutaceae) Jeruk Bali Rind Aromatic Tree Full sun Seed

Citrus hystrix DC. (Rutaceae) Jeruk purut Fruit Condiment Shrub Full sun Seed

Cleome gynandra L. (Capparaceae) Boangit Leaf, flower Aromatic Herb Full sun Seed

Coleus atropurpureus Bth. (Lamiaceae) Miana Leaf Aromatic Herb Full sun Cutting

Cosmos caudatus H.B.K. (Asteraceae) Kenikir Leaf Aromatic Herb Full sun Seed

Cupressus benthamii Endl. (Cupressaceae) Cemara lilin Leaf Aromatic Tree Full sun Seed

Cupressus chasmeriana Royle ex Carriere (Cupressaceae) Cemara kipas Leaf Aromatic Tree Full sun Seed

Cymbopogon citratus (DC.) Stapf. (Poaceae) See Leaf Condiment Herb Full sun Stolon

Cymbopogon winterianus Jowitt (Poaceae) See wangi Leaf Aromatic Herb Full sun Stolon

Dysoxylum caulostachyum Miq. (Meliaceae) Majagau Stem Aromatic Tree Full sun Seed

Eucalyptus alba Reinw. ex. Bl. (Myrtaceae) Ampupu Leaf Aromatic Tree Full sun Seed

Eucalyptus deglupta Bl. (Myrtaceae) Leda Leaf Aromatic Tree Full sun Seed

Eucalyptus urophylla S.T. Blake (Myrtaceae) Huek Leaf Aromatic Tree Full sun Seed

Foeniculum vulgare Mill. (Apiaceae) Adas Leaf Aromatic Herb Full sun Seed

Gardenia jasminoides Ellis (Rubiaceae) Jempiring Flower Aromatic Shrub Full sun Cutting

Jasminum sambac (L.) W.Ait. (Oleaceae) Menuh Flower Aromatic Woody climber Semi shade Cutting

Juniperus procera Hochst. ex Endl. (Cupressaceae) Cemara natal Leaf Aromatic Tree Full sun Seed

Leptospermum amboinense Bl. (Myrtaceae) Mica bolong Leaf Aromatic Tree Full sun Seed

Libocedrus formosana Florin (Cupressaceae) Kipres pormosa Leaf Aromatic Tree Full sun Seed

Lophopetalum javanicum (Zoll.) Turcz. () Tahlan Stem Aromatic Tree Full sun Seed

Massoi aromatica Becc. (Lauraceae) Mesui Stem Aromatic Tree Full sun Seed

Melaleuca leucadendra (L.) L. (Myrtaceae) Kayu putih Leaf Aromatic Tree Full sun Seed

Mentha arvensis L. (Lamiaceae) Poo Leaf Aromatic Herb Full sun Stolon

Mesua ferrea L. (Clusiaceae) Nagasari Seed Aromatic Tree Full sun Seed

Michelia champaca L. (Magnoliaceae) Cempaka Flower Aromatic Tree Full sun Seed

Michelia montana Bl. (Magnoliaceae) Kayu base Flower Aromatic Tree Full sun Seed

Mimosops elengi L. (Sapotaceae) Tanjung Flower Aromatic Tree Full sun Seed

Moringa pterygosperma Gaertn. (Moringaceae) Kelor Root, leaf Aromatic Tree Full sun Seed

Murraya paniculata (L.) Jack. (Rutaceae) Kemuning Flower Aromatic Tree Full sun Seed

Ocimum basilicum L. (Lamiaceae) Kencarum Flower Aromatic Herb Full sun Seed

Orthosiphon aristatus (Bl.) Miq. (Lamiaceae) Kumis kucing Flower Aromatic Herb Full sun Seed

Pandanus amaryllifolius Roxb. (Pandanaceae) Pandan arum Leaf Aromatic Shrub Semi shade Stolon

Pandanus inermis Reinw. (Pandanaceae) Pudak Flower Aromatic Shrub Semi shade Stolon

Piper cubeba L.f. (Piperaceae) Kemukus Leaf Aromatic Woody climber Semi shade Cutting

Piper nigrum L. (Piperaceae) Merica Seed Condiment Woody climber Semi shade Seed

Pittosporum ferrugineum W. Ait. (Pittoporaceae) Belalang puak Root Aromatic Tree Full sun Seed

Pogostemon cablin Bth. (Lamiaceae) Dondelem Leaf Aromatic Herb Full sun Cutting

Protium javanicum Burm. f. (Burseraceae) Tenggulun Leaf Condiment Tree Full sun Seed

Schima wallichii (DC.) Korth (Theaceae) Puspa Flower Aromatic Tree Full sun Seed

Talauma candollii Bl. (Magnoliaceae) Cempaka gondok Flower Aromatic Shrub Semi shade Seed

Thuja occidentalis L. (Cupressaceae) Cemara kipas Leaf Aromatic Tree Full sun Seed

Thuja orientalis L. (Cupressaceae) Cemara kipas Leaf Aromatic Tree Full sun Seed

Zingiber casummunar Roxb. (Zingiberaceae) Bangle Rhizome Aromatic Herb Semi shade Rhizome

Zingiber officinale Roxb. (Zingiberaceae) Jahe Rhizome Condiment Herb Semi shade Rhizome

2014 Journal of Indonesian Natural History Vol 2 No 1 39 Not just mangroves: range expansion required for the mangrove whistler (Pachycephala grisola) on Borneo

Marc L. Dragiewicz1, David A. Ehlers Smith1,2 and Mark E. Harrison1,2,3

1Orangutan Tropical Peatland Project (OuTrop), Jl. 91, Palangka Raya, Central Kalimantan, Indonesia 2Centre for International Cooperation in the Management of Tropical Peatlands (CIMTROP), University of Palangka Raya, Indonesia 3Department of Geography, University of Leicester. Leicester LE1 7RH, United Kingdom.

Corresponding author: David A. Ehlers Smith, Email: [email protected]

Introduction one month during the wet season (February 2010) in the Mentaya-Katingan peat-swamp forest (2o25’ S, The mangrove whistler Pachycephala grisola (referred 113o07’ E); one month during the wet season (January to as P. cinera by some authors) is considered a common 2010) in the Mungku Baru ironwood Eusideroxylon inhabitant of coastal forest < 200 m above sea level zwageri / heath forest (1o30’ S, 113o44’19 E); one week throughout its range in South and South-East Asia (Del during the dry season (July 2010) in the Bawan heath / Hoyo et al. 2007; MacKinnon & Phillipps 1993; Myers peat-swamp forest (1o36’ S, 113o59’ E); and two weeks 2009). Its range spans from India to the island of New in the dry season (August 2011) in Kalampangan peat- Guinea, though it does inhabit forest in land-locked swamp forest, Block C of the ex-Mega Rice Project Laos (ibid). On Borneo, both Birdlife International area (2o20’ S, 114o02’ E; Figure 1). These sites are all (2013) and recent field guides illustrate its distribution part of larger contiguous lowland (≤ 55 masl) forest as a ring circling the coastal regions of the island, blocks, located approximately 100, 60 and 175 km, implying that mangrove forest is the species’ preferred respectively, from the nearest coastline. All peat-swamp habitat (Myers 2009; Phillipps & Phillipps 2009). forest areas studied had been heavily logged, while the Myers (2009) and Birdlife International (2013) also list Mungku Baru heath forest site remains unlogged. The sub-tropical/tropical moist lowland forest (including Kalampangan forest is highly degraded, as a result of heath and peat-swamp forest), sub-tropical/tropical severe drainage during the ex-Mega Rice Project, and moist montane forest as “suitable” habitats, and rural much of the original heath forest in Bawan has been gardens and plantations as “marginal” habitats used by logged. this species, however, suggesting that these distribution We surveyed the avifauna using a combination of maps may be in need of updating. Indeed, it is curious forest walks, formal line transects and point counts that the Birdlife International map only illustrates the between 05:00 and 11:30 (Lambert 1992; Bibby et al. species distribution as coastal, given these habitat 2000). suitability descriptions on its website.

Results Methods Mangrove whistlers were seen at all five sites surveyed We studied avifauna in Central Kalimantan, Indonesian (see Figure 1). It is one of the most abundant birds in Borneo over eight months spanning two dry seasons Sabangau and is one of the few birds that can be heard (July-Aug 2005, 2007) in the Natural Laboratory of throughout the day at all study locations. We recorded Peat-Swamp Forest, Sabangau (2o19’ S, 113o54’ E); the species occasionally foraging in mixed-species flocks with several babblers (Timaliidae spp.), hook- billed bulbuls (Setornis criniger), grey-chested jungle th rd Received 12 March, 2014; Revision accepted 23 April, 2014 flycatchers (Rhinomyias umbratilis) and white-tailed

40 © University of Andalas / Copenhagen Zoo Dragiewicz et al.

Figure 1. Location of study sites and sightings of mangrove whistlers in Central Kalimantan, Indonesia. Grey shading indicates range illustrated in current ornithological guidebooks for the region (Myers 2009; Phillipps & Phillipps 2009) and by Birdlife International (2013). shamas (Copsychus malaaricus). It has also been seen belt described in the Birdlife International (2013) feeding at swarms of Leptogenys sp. army ants, where it factsheet and contemporary field guides (Myers joins mixed flocks of understoryTimaliidae babblers, the 2010; Phillipps & Phillipps 2009), including areas of grey-chested jungle-flycatcher and hook-billed bulbul, Bornean peat-swamp and ironwood / heath forest up to sallying for flying insects flushed by the ants. While 175 km from the nearest coastline. This indicates that this behavior is well documented in Latin America and current distribution maps for this species on Borneo Africa, it has not previously been described in Asian require revision and, combined with observations of birds. this species’ occurrence in areas of Laos > 200 km In the Mentaya-Katingan peat swamps, mangrove inland (Round 1988), suggests that the species may whistlers were seen on the River Tarantang, a tributary not be as restricted to coastal distribution as previously of the River Mentaya, and on the River Perigi, a tributary indicated (although some inland surveys have failed of the River Katingan. Over a five-day period at Mungku to detect the species in other parts of Kalimantan, e.g. Baru, at least one individual was encountered daily near Woxyold & Noske 2011). It is possible that the ongoing camp in alluvial forest alongside the River Rakumpit anthropogenic destruction of natural habitats on Borneo and, two others were seen in the heath forest. The (Curran et al., 2004; Miettinen et al., 2011) is forcing species was regularly encountered (> 3 individuals per avian species to expand outside of their natural range; survey day) in Kalampangan and Bawan and forests. however, the frequency with which the species was recorded at the study sites indicating that these habitats outside of this coastal range are in fact suitable for Discussion supporting populations. Additionally, the majority of sites surveyed here are themselves degraded, suggesting These observations confirm the presence of the that the birds’ presence may not be due to avoidance of mangrove whistler outside of the coastal mangrove habitat disturbance.

2014 Journal of Indonesian Natural History Vol 2 No 1 41 Range expansion of mangrove whistler

These records are pertinent for conservation planning, Birdlife International. (2013). Mangrove whistler as accurate distribution maps are a vital component Pachycephala grisola. http://www.birdlife.org/datazone/ of assessing a species threat status and developing speciesfactsheet.php?id=5639&m=0. Accessed 2nd appropriate species management. The absence of November 2013. previous inland records in Borneo may be as a result of the scarcity in ornithological surveys conducted Del Hoyo, J. Elliott, A.D. and D. Christie (2007). in Kalimantan outside of Barito or , Handbook of the Birds of the World. Volume 12: especially in peat-swamp forest. This observation Picathartes to Tits and Chickadees. Lynx Edicions, highlights the need for more extensive ornithological Barcelona, Spain. work at sites in Kalimantan. Lambert, F.R. (1992). The consequences of selective logging for Bornean lowland forest birds. Philosophical Acknowledgements Transactions of the Royal Society of London B 355: 443-57. We thank the Centre for International Cooperation in Sustainable Management of Tropical Peatlands MacKinnon, J. and K. Phillipps (1993). A Field Guide (CIMTROP) and the Indonesian Ministry of Science to the Birds of Borneo, Sumatra, Java, and Bali: The and Technology (RISTEK) for research permissions. Greater Sunda Islands. Oxford University Press, Nicholas Boyd contributed the record for Kalampangan. Oxford, UK. Funding for research in Sabangau was provided by the US Fish and Wildlife Service Great Apes Conservation Myers, S. (2009). Birds of Borneo: Brunei, Sabah, Fund, Wallace Foundation and Arcus Foundation. This Sarawak, and Kalimantan. Princetown University work was conducted as part of the OuTrop-CIMTROP Press, Princetown, USA. multidisciplinary research project in Sabangau, Kalampangan and Bawan; with Starling Resources Phillipps, Q., Phillipps, K. (2009). Phillipps' Field and PT. Rimba Makmur Utama in the Mentaya- Guide to the Birds of Borneo: Sabah, Sarawak, Brunei Katingan peat swamps; and with International Animal and Kalimantan. John Beaufoy Books, Oxford, UK. Rescue-Indonesia in Mungku Baru. We thank Hendri and all other research assistants for help and support Round, P.D. (1988). Resident Forest Birds in Thailand: in the field, and Simon Husson for comments on that Their Status and Conservation. International Council helped improve the manuscript, and much support for Bird Preservation, Cambridge, UK. and encouragement over the years. Finally thanks to Fransiskus Agus Harsanto for Indonesian translations. Woxvold, I., Noske, R. A. (2011) The avifauna of kerangas, mixed dipterocarp and riparian forests in Central-East Kalimantan, Indonesia, and its References conservation significance.Forktail 27: 44-59. Bibby, C.J., Burgess, N.D., Hill, D.A. and S.H. Mustoe (2000). Bird Census Techniques: Second Edition. Academic Press, London, UK.

42 © University of Andalas / Copenhagen Zoo First breeding record evidence of Hooded Pitta Pitta Sordida in mainland Sumatra, Indonesia

Muhammad Iqbal, Ahmad Ridwan and Fadly Takari

1Daemeter Consulting. Jalan Tangkuban Perahu No.6, Taman Kencana, West Java 16151, Indonesia 2KPB-SOS, Jalan Tanjung api-api km 9 Komplek P and K Blok E 1, Palembang 30152, Indonesia.

Corresponding Author: Muhammad Iqbal, email: [email protected]

Introduction mainland (Holmes, 1996; Marle and Voous, 1988; Balen et al., 2011; Balen et al., 2013). “Breeding” is defined Hooded Pitta, Pitta sordida, range from the North Indian as a record of nest-building, nests, eggs, fledging or subcontinent, Nicobar Island, Southwest China, Greater young being fed (Davison, 1988). To our knowledge, Sundas, Philippines, Sulawesi and New Guinea region this paper describes the first evidence that Hooded Pitta (Robson, 2011). It is reported to occupy a wide range breed in mainland Sumatra. of habitat, from all types of forest to overgrown rubber and coffee plantations (Erritzoe, 2003). Therefore, it is listed as “Least Concern” in on the IUCN red-list Methods (IUCN, 2012) despite experiencing population decline in Thai-Malay Peninsula. In Greater Sundas, P. s. Study area cucullata overwinters in the Malay Peninsula, Sumatra The study site is located in Kuro village, Pampangan (including , Islands in Malaca Straits and Bangka) subdistrict, Ogan Komering Ilir district (3°12′S, and Java; and P. s. mulleri is resident on Borneo and 104°59′E), South Sumatra Province, Indonesia. The Java (MacKinnon and Phillipps, 1993). The movement area consists of secondary forest bordering with rubber pattern of P. s. mulleri on Borneo is poorly understood plantations from <50 m asl. The individual described and is further obscured by the possible winter visitor in this paper was kept in a cage by local people during P. s. cucullata from northern Southeast Asia (Smythies, a birdwatching event on 10th June, 2004, in Kuro 1981; Mann, 2008). village. The bird was observed and photographed for In Sumatra, Hooded Pitta is recorded throughout the identification and documentation. mainland, but very little is known about its ecology and phylogenic history (Marle and Voous, 1988). The intermediate subspecies P. s. bangkana is found in Results and discussion Bangka and Belitung Island, southeast of Sumatra (Dickinson and Decker, 2000; Mees, 1986). Hooded During a birdwatching trip on 10th of June, 2004, we Pitta is believed to be resident (P. s. mulleri on mainland; encountered some local people with a bird kept in a P. s. bangkana endemic on Bangka and Belitung) and cage. It turned out that the specimen was not a common winter visitor (P. s. cucullata) from mainland Southeast cage bird usually kept by local people in the region Asia (Marle and Voous, 1988). (e.g. Magpie Robin Copshychus saularis or Bulbuls The endemic subspecies (P. s. bangkana) was recorded Pycnonotus spp). The specimen was a young fledgling to breed in Belitung island west of Sumatra, because with a yellow base bill. Local people reported that eggs were collected in March, April and May (Chasen, they had collected it two weeks earlier from a nest in 1937; Marle and Voous, 1988). No breeding evidence Lebak Johor, approximately 5 km from Kuro Village, was recorded for Hooded Pitta on the Sumatran Ogan Komering Ilir district, South Sumatra Province. The habitat consists of secondary forest bordering with rubber plantation, Hevea braziliensis, near lebak Received 28th March, 2014; Revision accepted 30th August, 2014 (floodplain).

2014 Journal of Indonesian Natural History Vol 2 No 1 43 Breeding record of hooded pita

The bird was identified as a juvenile Hooded Pitta (P. Chasen, F.N. (1937). The birds of Billiton Island. s. mulleri) by its yellow base bill, short-tail, green with Treubia 16: 205-238. black head, upperparts duller, throat mostly white, rest of underparts dull brownish with pinkish-red vent, black Davison, G.W.H. (1988). Breeding seasonality. In The bill, and wing coverts green with white wing patches. birds of Sumatra: an annotated check-list (No. 10) The specimen differed from a juvenile Mangrove Pitta, (eds. J.G. van Marle & K.H. Voous), pp 35-36. British Pitta megarhyncha, by having a black head without buff, Ornithologists’ Union, Tring, UK crown-sides and wing coverts with wing patches. These Dickinson, E.C. and R.W.R.J. Dekker (2000). Systematic characters fit the descriptions of a juvenile Hooded notes on Asian birds. 4. A preliminary review of the pitta in various references (Grimmet et al., 2011; Pittidae. Zoologische Verhandelingen 331:89-99. MacKinnon and Phillipps, 1993; Robson, 2011; Wells, 2007). Combined with information obtained from local Erritzoe, J. (2003). Family Pittidae (Pittas). In Handbook people, this provides evidence that Hooded Pitta breeds of the Birds of the World, Vol. 8. (eds. J. del Hoyo, A. in mainland Sumatra. The rapid deforestation, however, Elliott & D.A. Christie), pp 106-160. Lynx Editions, may result in declining an already sparse population, Barcelona, Spain. even if has already been recorded in degraded forest and secondary woodland, including bamboo jungle and Grimmett, R., Inskipp, C. and T. Inskipp. (2011). Birds old, over grown tree or rubber plantation (Wells, 2007). of India, Pakistan, Nepal, Bangladesh, Bhutan, Sri Langka and the Maldives. Princeton University Press, UK. Acknowledgements Holmes, D.A. (1996). Sumatra bird report. Kukila 8: 9-56. We would like to thank Dr. Richard Noske and Dr. Bas van Balen for identification and earlier discussion MacKinnon, J. and K. Phillipps. (1993). A field guide on Hooded Pitta in Sumatra. Thanks to Dr. Wilson to the birds of Borneo, Sumatra, Java and Bali. Oxford, Novarino and Dr. Carl Traeholt for their constructive U.K.: Oxford University Press. discussion and advise. van Marle, J.G. and K.H. Voous. (1988). The birds of Sumatra: an annotated check-list. Tring, U.K.: British References Ornithologists’ Union (Check-list 10).

Balen, S. van., R. Noske. and A.A. Supriatna. (2011). Mees, G.F. (1986). A list of the birds recorded from Bangka Island, Indonesia. Zoologische Verhandelingen Around the archipelago. Kukila 15: 126-143. 232: 1-176.

Balen, S. van., Trainor, C. and R. Noske. (2013). Around Robson, C. (2011). Birds of South-east Asia. New the archipelago. Kukila 15: 126-143. Holland Publishers, London.

BirdLife International (2012). Pitta sordida. The IUCN Wells, D.R. (2007). The birds of the Thai-Malay Red List of Threatened Species. Version 2014.2. . Downloaded on 17 July, 2014. London.

44 © University of Andalas / Copenhagen Zoo Kalimantan’s tropical peat-swamp forests are important for Storm’s stork (Ciconia stormi) conservation

Susan M. Cheyne1,2,3, Simon J. Husson2,3, Marc Dragiewicz2, Lindy J. Thompson2, Adul2,3, Karen A. Jef- fers2,3, Suwido H. Limin3 and David A. Ehlers Smith2,3

1Wildlife Conservation Research Unit (WildCRU), Department of Zoology, Oxford University, Abingdon Road, OX13 5QL, UK 2Orangutan Tropical Peatland Project (OuTrop), Jl. Semeru 91, Palangka Raya, Central Kalimantan, Indonesia 3Centre for International Cooperation in the Management of Tropical Peatlands (CIMTROP), University of Palangka Raya, Indonesia

Corresponding Author: David A. Ehlers Smith, Email: [email protected]

Introduction and is one of the largest areas of lowland rainforest remaining in Borneo. It is important both as a major store The Storm’s stork (Ciconia stormi) is listed on the of terrestrial organic soil carbon and for biodiversity IUCN Red List 2012 as endangered, because it has a conservation (Cheyne, 2008; Ehlers Smith & Ehlers small, rapidly declining population owing to destruction Smith, 2013; Morrogh-Bernard, et al., 2003; Page et al., of lowland forest habitat throughout its range (BirdLife 1999; Page et al., 2002). The forest has been intensely International, 2001; IUCN, 2012). Its reported range selectively-logged, first by commercial operations from extends from southern Thailand, where it is almost the 1970s to 1997 and illegally until 2003 (Morrogh- certainly extinct (Round, 1988; Round & Brockelman, Bernard et al., 2003). Approximately 15% of the 1998), through most of Sundaland (Peninsular Malaysia original forested area has been burnt by fire since 1997, and the islands of Sumatra and Borneo.) It is known a consequence of peat drainage and extended periods from six river systems in Peninsular Malaysia (Hancock of drought (Page et al., 2002). Disturbance levels vary et al., 1992; Luthin, 1987) and is reportedly widespread throughout, from pristine to heavily-degraded. Much of (albeit rare and found at extremely low density) in the forest was designated as Sebangau National Park Sumatra and Borneo, with apparent concentrations by the Indonesian Government in 2004, and subsequent in Sabah and Brunei, northern Borneo, and in south- conservation management has largely stopped illegal eastern Sumatra (BirdLife-International, 2001). It favors logging and reduced the severity of fire events. forested lowland habitat, occurring in both dry and Fifty thousand hectares in the northern Sabangau Forest swamp forests, as long as there is access to permanent was established for research purposes and is managed by sources of freshwater (BirdLife-International, 2001; the Centre for International Cooperation in Management Collar et al., 1994; Danielsen et al., 1997). The global of Tropical Peatland (CIMTROP). Since 1993, this population is estimated to be 400-500 individuals with is the site of a long-term program of field research on estimates of up to 250 individuals in Indonesia and 150 peat-swamp forest ecology, biodiversity, restoration and individuals in Malaysia (BirdLife-International, 2013). sustainability. The principal research site is the Natural Laboratory for Peat-swamp Forest Studies (NLPSF) field station (2º 19’ S; 113º 54’ E). Methods

Study site and study species Data collection The Sabangau Forest is a 568,000 ha area of tropical peat-swamp forest located between the Sabangau and Animal sightings have been recorded here since 1993, Katingan Rivers in Central Kalimantan, Indonesia, either opportunistically or by transect survey and point count; and since 2008 by automatic camera traps. Cuddeback Expert cameras (http://www.cuddeback. Received 12th March, 2014; Revision accepted 23rd April, 2014. com/) were set up within the 15 km2 core study area

2014 Journal of Indonesian Natural History Vol 2 No 1 45 Storm’s stork in peatland

Figure 1. Study location and boundary of the Natural Laboratory for Peat-Swamp Forest Studies (NLPSF) within Sabangau Forest, Central Kalimantan. by the Orangutan Tropical Peatland Project (OuTrop) Results with the primary objective of surveying cats. Twenty- two cameras have been permanently sited in pairs at 11 Storm’s stork was first recorded here in peat-swamp locations since May 2008 and checked once every 14 forest near to the NLPSF in July 1993 (Page et al., days. The date and time of all photos is automatically 1997); subsequent sightings were made in sedge swamp recorded and the location of each camera was recorded along the Rasau River (2º 29’ S; 114º 00’ E) in July by GPS. 1999; in forest near to Paduran River (2º 44’ S; 114º 48’ E) in July 2002 and in forest near to the NLPSF in February 2005 (Tab. 1; Fig. 1). Each sighting consisted of a lone individual. During a 4 year period, Storm’s storks were photographed 32 times at 5 different locations (Tab. 2; Fig. 2). 4 of these locations, where 78.1% (N = 25) of the photographs were taken, have a permanent water source nearby in the form of a logging canal (Fig. 3).

Discussion

The camera-trap photographs presented here provide Figure 2. Location of camera traps throughout the Natural evidence of a population of Storm’s stork in Sabangau Laboratory for Peat-swamp Studies (NLPSF) within Sabangau Forest in Central Kalimantan, Indonesia and highlight tropical peat-swamp forest (TPSF). the contemporary importance of peat-swamp forests for

46 © University of Andalas / Copenhagen Zoo Cheyne et al.

Table 1. Dates and locations of Storm’s stork sightings in Sabangau tropical peat-swamp forest. Area A = close to permanent water; Area B = open areas accessible to flying storks.

Date Time Location # birds Area A Area B Jul-93 - 1 - Jul-99 - 2 - Jul-02 - 3 - Feb-05 - 1 - 14-Jul-08 14:34 9 1 Y Y 07-Aug-08 11:17 5 1 Y Y 28-Sep-08 08:26 10 1 Y Y 06-Oct-08 06:40 10 1 Y Y 07-Oct-08 05:48 9 1 Y Y 13-Dec-08 12:11 10 1 Y Y 06-May-09 07:00 10 1 Y Y 06-May-09 15:30 10 1 Y Y 07-May-09 13:52 10 1 Y Y 12-May-09 05:43 10 1 Y Y 16-May-09 11:47 9 1 Y Y 16-May-09 11:50 10 1 Y Y 18-May-09 05:22 10 1 Y Y 01-Jul-09 12:04 10 1 Y Y 08-Aug-09 16:28 10 1 Y Y 10-Aug-09 06:44 10 1 Y Y 21-Nov-09 11:34 5 1 Y Y 09-Dec-09 12:33 5 1 Y Y 09-Dec-09 12:35 5 2 Y Y 27-Sep-10 07:05 N5 1 N N 25-Dec-10 12:19 N7 1 N N 25-Dec-10 09:09 N8 1 N N 28-Dec-10 15:37 N7 1 N N 16-Jan-11 08:04 N8 1 N N 17-Feb-11 14:18 N5 1 N N 13-Jul-12 15:28 N12 1 N N

Table 2. Total trap nights and trap night frequency of Storm’s storks recorded in Sabangau tropical peat-swamp forest between August 2008 and August 2012

Total trap Total Storm’s Trap night Total independent Total independent Frequency of Storm’s nights stork trap nights frequency animal photos Storm’s stork photos stork photos 35,129 22 0.06 2,955 32 1.08

2014 Journal of Indonesian Natural History Vol 2 No 1 47 Storm’s stork in peatland species conservation in Sundaland. Borneo’s forested notion has since been dispelled (Cheyne et al., 2007; lands, both dryland and swamp and mangrove forests, Morrogh-Bernard et al., 2003; Ehlers Smith & Ehlers are being lost at an unprecedented rate (Curran et al., Smith, 2013; Neuzil 1997; Page et al., 1999; Page et 2004; Langner et al., 2007; Miettinen et al., 2011) al., 2002). It is likely, therefore, to play a similar role and the threat to its’ fauna and flora is severe (e.g. for many species of birds, particularly wetland species Rautner et al., 2005; Wich et al., 2012; Ehlers Smith such as the Storm’s stork. Contemporary and historical 2014). The destruction of much of Sundaland’s primary locality data describe peat-swamp forests as important dryland (including dipterocarp and kerangas) forests habitat for the Storm’s stork across Southeast Asia, has led to peat-swamp forest being recognised as a including Sumatra, Peninsular Malaysia, and Borneo vital refuge for many lowland specialists in Sundaland (Birdlife International, 2012). While it is without including primates (Cheyne et al., 2007; Ehlers Smith question that anthropogenic disturbances have resulted & Ehlers Smith, 2013; Morrogh-Bernard et al., 2003); in a decline in the Storm’s stork across its’ range, it bats (Struebig et al., 2007); arthropods (Houlihan et may be that peat-swamp forests have been providing a al., 2012) and felids (Cheyne & MacDonald, 2011). crucial refuge for the species during the accelerated loss Peatland covers a vast area (ca. 6 million ha) of the of riverine and lakeland habitats within dryland forests. lowlands of Kalimantan (Rieley et al., 1996) and most Indeed, the frequency with which this endangered of this remains forested. Prior to 1990 this habitat was species has been photographed here is particularly little studied and believed to be low in biodiversity and encouraging, especially as this area was previously unimportant for conservation (Neuzil 1997), but this heavily logged; the assertion that Storm’s stork may

Figure 3. Camera trap records of Storm’s storks in Sabangau tropical peat-swamp forest at the same location.

48 © University of Andalas / Copenhagen Zoo Cheyne et al. persist in selectively-logged forest is supported here References (Lambert, 1992). In addition to Sabangau, Storm’s stork has been reported from several other peat-swamp forests BirdLife-International. (2001). Threatened birds of in Kalimantan (C. Traeholt, pers. comm.), including Asia: the BirdLife International Red Data Book. Tanjung Puting National Park, Central Kalimantan; BirdLife International, Cambridge, UK. Gunung Palung National Park, West Kalimantan; and the catchments of the Kapuas, Kahayan, Rungan BirdLife-International. (2012). Ciconia stormi. IUCN and Seruyan Rivers in Central Kalimantan (BirdLife- 2012: IUCN Red List of Threatened Species. International 2001; BirdLife-International 2008). Danielsen et al., (1997) estimated a species density of Cheyne, S.M., Thompson, C.J.H., Phillips, A.C., Hill, ca. one stork per 30-60 square kilometres in primary R.M.C. and S.H. Limin (2007). Density and population swamp forest in in Sumatra. A estimate of gibbons (Hylobates albibarbis) in the Sebangau Catchment, Central Kalimantan, Indonesia. crude application of that density to the 5,680 km2 of the Primates 49:50-56. Sabangau National Park suggests a possible population of 95-190 individuals here, and perhaps a further 100- Cheyne, S.M. and D.W. Macdonald (2011). Wild felid 200 individuals in the adjacent and ecologically-similar diversity and activity patterns in Sabangau peat-swamp peat-swamp forests in the catchments the Katingan, forest, Indonesian Borneo. Oryx 45:119–124. Kahayan, Rungan and Kapuas Rivers. Further surveys to determine the distribution, Collar, N., Crosby, M.J. and A.J. Stattersfield (1994). population and habitat requirements of Storm’s storks Birds to Watch 2. Birdlife International : Cambridge, are urged by the IUCN Red List 2012 authors (IUCN, UK. 2012), although locating nests, necessary for accurate surveys, is particularly difficult (Danielson et al., Curran, L.M., Trigg, S.N., McDonald, A.K., et al. 1997). Additional data from rivers and lakes in dryland (2004). Lowland forest loss in protected areas of habitats may offer insights into the species; movements Borneo. Science 303:1000–1003. in response to habitat loss. Regardless, the peat-swamp forests of southern Kalimantan are likely to form a Danielsen, F., Kadarisman, R., Skov, H., Suwarman, major refuge for this species, and further peatland U. and W.J.M. Verheugh (1997). The Storm’s stork protection, rehabilitation and restoration measures are Circonia stormi in Indonesia: breeding biology, urgently required. population and conservation. Ibis 139:67-75. Ehlers Smith, D.A. and Y.C. Ehlers Smith (2013). Population density of Presbytis rubicunda in Sabangau cknowledgements A tropical peat-swamp forest, Central Kalimantan. American Journal of Primatology 75:837-847. We thank the Indonesian State Ministry of Research and Technology (RISTEK), the Directorate General of Ehlers Smith, D.A. (2014). The effects of land-use Forest Protection and Nature Conservation (PHKA) and policies on the conservation of Borneo’s endemic Center for the International Cooperation in Sustainable Presbytis monkeys. Biodiversity and Conservation Use of Tropical Peatlands (CIMTROP) for research 23:891-908. permissions. This work was supported by grants from the Panthera Foundation. The camera trapping research Hancock, J.A., Kushlan, J.A. and M.P. Kahl (1992). is part of a collaborative project between Panthera, Storks, Ibises and Spoonbills of the World. Academic WildCRU and the Orangutan Tropical Peatland Project Press: London and San Diego. (OuTrop). We gratefully acknowledge the contribution of all the researchers who assisted with the project: Houlihan, P.R., Harrison, M.E. and S.M. Cheyne Ambut, Andri Thomas, Iwan, Ramadhan, Santiano, (2012). Habitat preference and community composition Twentinolosa, Yudhi Kuswanto and all the OuTrop of tropical butterflies in a Bornean peat-swamp forest: volunteers. Finally thanks to Fransiskus Agus Harsanto Impacts of forest disturbance on butterfly diversity. doi: for Indonesian translations. 10.1016/j.aspen.2012.10.003

2014 Journal of Indonesian Natural History Vol 2 No 1 49 Storm’s stork in peatland

IUCN. 2012. Red List of Threatened Species. IUCN. Page, S.E., Siegert, F., Boehm, H.D.V., Jaya, A. and S. Limin (2002). The amount of carbon released from Lambert, F.R. (1992). The consequence of selective peat and forest fires in Indonesia during 1997. Nature logging for Bornean lowland forest birds. Philosophcial 420:61-5. Transactions of the Royal Society of London 335:443- 457. Rautner, M., Hardiono, M. and R.J. Alfred (2005). Borneo: treasure island at risk. Status of forest, wildlife, Langner, A., Miettinen, J. and F. Siegert (2007). Land and related threats on the island of Borneo. Frankfurt: cover change 2002–2005 in Borneo and the role of fire WWF Germany. derived from MODIS imagery. Global Change Biology 13:2329–2340. Round, P.D. (1988). Threatened Forest Birds of Thailand. International Council for Bird Protection: Luthin, C. (1987). Status and conservation priority for Cambridge, UK. the world’s stork species. Colonial Waterbirds 10:181- 202. Round, P.D. and W.Y. Brockelman (1998). Bird Miettinen, J., Shi, C. and S. Liew (2011). Frontiers in the communities of disturbed lowland forest habitats in ecology and environment: two decades of destruction southern Thailand. Natural History Bulletin of the Siam in Southeast Asia’s peat-swamp forests. Frontiers in Society 46:171-196. Ecology and Environment 10:124–128. Struebig, M.J., Harrison, M.E., Cheyne, S.M., and Morrogh-Bernard, H., Husson, S., Page, S.E. and J.O. S.H. Limin (2007). Intensive hunting of large flying- Rieley (2003). Population status of the Bornean orang- foxes (Pteropus vampyrus natunae) in the Sebangau utan (Pongo pygmaeus) in the Sebangau peat swamp Catchment, Central Kalimantan, Indonesian Borneo. forest, Central Kalimantan, Indonesia. Biological Oryx 41:1-4. Conservation 110:141-52. Wich, S.A., Gaveau, D., Abram, N., Ancrenaz, M., Neuzil S.G. (1997). Biodiversity and Sustainability of Baccini, A., et al. (2012). Understanding the impacts Tropical Peatlands. Samara: Cardigan, UK. of land-use policies on a threatened species: Is there a future for the Bornean orang-utan? PLoS ONE Page, S.E., Rieley, J.O., Shotyk, Ø.W. and D. Weiss doi:10.1371/journal.pone.0049142 (1999). Interdependence of peat and vegetation in a tropical peat swamp forest. Philosophical Transactions of the Royal Society of London B 354:1885-1807.

50 © University of Andalas / Copenhagen Zoo Society for Conservation Biology

Melaka Declaration in Support of Conservation and Stronger Protection of Malaysia's Biodiversity

22nd August, 2014

Malaysia's biodiversity is among the richest on earth, a natural capital asset which is critical to the wellbeing and sustained development of the nation. Malaysia has the potential to lead the world by setting an example of enlightened development. Recognising that biodiversity is our life, our heritage and our future, we, as one of the largest gatherings of conservation biologists ever in Malaysia, representing 400 scientists, experts, researchers, policy makers and students from 45 nations, recommend that the Government of Malaysia: • Take immediate actions to strengthen leadership in biodiversity conservation at both federal and state levels. Safeguarding the nation's natural capital, which biodiversity and ecosystem services underpin, will be essential for Malaysia to meet its development aspirations in a sustainable, inclusive and equitable manner in line with the government's transformation agenda and the commitment to keep 50% of land under natural forest cover. • Take immediate steps to implement the Global Biodiversity Strategy 2011-2020 and meet the Aichi Biodiversity Targets, to which Parties to the Convention on Biological Diversity - including Malaysia - have committed themselves. • Make available the necessary financial and human resources to implement the Central Forest Spine master plan, backed by strong political commitments at both federal and state levels, while creating the needed legal frameworks, innovative financing schemes and public engagement to make it a reality. • Commit to the effective implementation of national laws and policies, including obligations under Multilateral Environment Agreements that Malaysia is Party to. Such actions require the development of rigorous, effective and transparent monitoring, reporting, evaluation and adaptive management systems. • Mobilise and enhance cross-sectoral mechanisms to curb illegal encroachment in Protected Areas, including toaching, and strive towards achieving zero net degradation of Protected Areas and prevent further decline of endangered species as a first step in promoting their recovery. • Invest in fundamental sciences such as , pure biological research, biodiversity inventory and monitoring. This will allow for the conservation of biodiversity and also its sustainable utilisation, based on a robust science-policy interface with the socio-economic wellbeing of the nation at its heart.

It is our obligation to humanity and future generations, and we must act now. By the adoption of this Melaka Declaration, participants of SCB Asia 2014 and the SCB pledge to assist the Government of Malaysia in delivering sustainable development, as well as call upon the international community to join and support this call to conserve one of the world's most important biodiversity hotspots.

2014 Journal of Indonesian Natural History Vol 2 No 1 51 Review and editing Guidelines for Authors All contributors in English are strongly advised to ensure that their spelling and grammar is checked by a native English speaker before The Journal of Indonesian Natural History will publish original work the manuscript is submitted to the Journal. The Editorial Team by: reserves the right to reject manuscripts that are poorly written. • Indonesian or foreign scientists on any aspect of Indonesian Submission in Bahasa Indonesia is also accepted and the Journal natural history, including fauna, flora, habitats, management secretariat will undertake a preliminary review of all manuscripts policy and use of natural resources • Indonesian or foreign scientists on any aspect of regional for suitability of content and format. Manuscripts that are rejected natural history, including fauna, flora and habitats at this stage will not be sent for peer review and translation.

Preference is given to material that has the potential to; Manuscripts that pass through the preliminary review will be sent for translation and peer review by a minimum of two reviewers. • Improve conservation intervention and management in Authors are welcome to suggest appropriate reviewers. Indonesia • Enhances understanding of conservation needs in Indonesia Proofs will be sent to authors as a portable document format (PDF) • Enhances the understanding of Indonesia's natural history file attached to an e-mail note. PDF-readers can be downloaded free of charge from http://www.adobe.com and http://www. The Journal language will be in English with abstracts in Bahasa nitropdf.com for viewing PDF files. Corrected proofs should be Indonesia as well as English. Authors of full papers are encouraged returned to the Editor within 3 days of receipt. Minor corrections to provide a Bahasa Indonesia/English translation of their abstract. can be communicated by e-mail. Submissions in Bahasa Indonesia will be accepted and translated into English only if accepted for publication. The Editorial Team also welcomes contributions to the other sections of the journal: Papers and Short Communications Full Research Papers (2,000-7,000 words) and Short Communications News (200-2,000 words) are invited on topics relevant to the Journal’s Concise reports (<300 words) on news of general interest to the focus, including: study and conservation of Indonesia's natural history. News reports may include, • The conservation status, ecology or behaviour of wild species • Announcements of new initiatives; for example, the launch of • Status or ecology of habitats new projects, conferences or funding opportunities. • Prehistoric and extinct species and new findings • Announcements of important new reports or other • Checklists of species, nationally or for a specific area publications related to Indonesian natural history. • Discoveries of new species records or range extensions. • Summaries of important news from an authoritative published • Biodiversity value associated with land use change, plantation source; for example, new Indonesian species described development and forestry in other journals, a new research technique, or a recent • Biodiversity in High Conservation Value areas development in conservation. • Reviews of conservation policy and legislation • Summaries and analysis of new policies, decrees and laws • Conservation management plans for species, habitats or areas relevant to the conservation of Indonesian natural history. • The nature and results of conservation initiatives, including case studies Letters to the Editor • Sustainable use of wild species Informative contributions (<650 words) in response to material • Community use and management of natural resources published in the Journal. • Abstracts of unpublished student theses (Short Communications only) Preparation of manuscripts The Journal will not accept descriptions of new species, subspecies Full papers follow the style and format of papers published in the or other taxa. journal Conservation Biology. Authors should consult examples in Conservation Biology for guidance on general style. How to Submit a Manuscript Manuscripts should be submitted by e-mail to the Editor at: Contributions should be in Bahasa Indonesia and/or UK English, double-spaced and in ‘doc, ‘rtf’ or ‘wpd’ format, preferably as one [email protected] file attached to one covering e-mail.

In the covering e-mail, the Lead Author must confirm that: The cover page should contain; The title and full mailing address, e-mail address and address of the • The submitted manuscript has not been published elsewhere, Lead Author and all additional authors. • All of the authors have read the submitted manuscript and agreed to its submission, Contributing Papers should contain the following sections and be • All research was conducted with the necessary approval and arranged in the following order: Abstract, Introduction, Methods, permits from the appropriate authorities Results, Discussion, Acknowledgments, Literature Cited. Tables,

52 © University of Andalas / Copenhagen Zoo Figures and Plates (including legends), if included, should follow Pastorini, J., Leimgruber, P., Fernando, P. and L. Santamaria (2008). the Literature Cited. Behavior rather than diet mediates seasonal differences in seed dispersal by Asian elephants. Ecology 89: 2684–2691. All pages should be numbered consecutively. Do not number section headings or subheadings. MacArthur, R.H. & Wilson, E.O. (1967). The Theory of Island Biogeography. Princeton University Press, Princeton, USA. Title: This should be a succinct description of the work, in no more than 20 words. Sutherland, W.J. (ed.) (1998). Conservation Science and Action. Blackwell Science, Oxford, UK. Abstract: Abstracts should only be submitted for Full Papers. This should describe, in 100-300 words, the aims, methods, major Beck, B.B., Rapaport, L.G. & Stanley Price, M.R. (1994). findings and conclusions. It should be informative and intelligible Reintroduction of captive-born animals. In Creative Conservation: without reference to the text, and should not contain any references Interactive Management of Wild and Captive Animals (eds P.J.S. or undefined abbreviations. Authors are encouraged to submit an Olney, G.M. Mace & A.T.C. Feistner), pp. 265-286. Chapman & Hall, English translation of Indonesian text and an Indonesian translation of an English text. London, UK.

Keywords: From five to eight pertinent words, in alphabetical order. Traeholt, C., Bonthoeun, R., Rawson, B., Samuth, M., Virak, C. and Sok Vuthin (2005). Status review of pileated gibbon, Hylobates Literature cited in text: Enclose citations in text in parentheses pileatus and yellow-cheeked crested gibbon, Nomascus gabriellae, e.g. “Asian tapirs are no elephants when it comes to seed dispersal in Cambodia. Fauna & Flora International, Phnom Penh, Cambodia. (Campos-Arceiz et al., 2011).” Sun H. (2000). Status of the tiger and its conservation in Cambodia. Use an ampersand (&) between author surnames when the citation MSc thesis, University of Minnesota, Minneapolis, USA. is parenthetical: (Traeholt & Idris, 2011). IUCN (2010). 2010 IUCN Red List of Threatened Species. Http:// When a citation is not parenthetical, use "and": “Our results agree www.redlist.org [accessed 1 February 2011]. with the predictions of Wolf and Rhymer (2001).” Biography: This should describe the main research interests of all For citations with more than two authors, use et al.: (Campos- authors (<150 words total), apart from what is obvious from the Arceiz et al., 2011). Do not italicize et al. subject of the manuscript and the authors’ affiliations.

List parenthetical citations in alphabetical order and chronologically Tables, figures and plates: These should be self-explanatory, each from oldest to most recent and separate entries with a semicolon: on a separate page and with an appropriate caption. Figures can (Campos-Arceiz et al., 2011; Geissman, 2009, 2010). be submitted in colour as well as in black and white. The Editorial

Team may decide to convert coloured figures into black and white Separate the years with commas when citing multiple papers by the same author: (Corlett, 2007, 2010; Geissman, 1984, 1995, 1999, should it be necessary due to printing cost and without diluting the 2000). message. Plates (black and white only) will only be included in an article if they form part of evidence that is integral to the subject “In press” means the cited paper has been accepted unconditionally studied (e.g., a photograph of a rare species), if they are of good for publication. Provide the year of publication in the text (Bird, quality, and if they do not need to be printed in colour. 2010) and in Literature Cited section provide the volume number, and substitute “in press” for page numbers (Bird, I.M. 2010. Nesting Appendices: Lengthy tables, and questionnaires are discouraged. success in arid lands. Conservation Biology 24: in press.). In special circumstances these may be made available for viewing online. Papers in review must be cited as unpublished and should not appear in the Literature Cited section. Species names: The first time a species is mentioned, its scientific name should follow in parenthesis and in italics: e.g., Asian Use an initial for the first (given) name and spell out the last name elephant (Elephas maximus). English names should be in lower case (surname) for other sources of unpublished data or information: (R. throughout except where they incorporate a proper name (e.g., Fowler, unpublished data; M.E. Soulé, personal communication). Asian elephant, Cookson's wildebeest, long-billed vulture).

Software: capitalize the first letter only if the name of the program Abbreviations: Full expansion should be given at first mention in is a word (e.g., Vortex, ArcGIS). If the name of the program is not a the text. word, use all capital letters (e.g., SAS). Units of measurement: Use metric units only for measurements of The following are examples of Literature Cited house style: Campos-Arceiz, A. and R.T. Corlett (2011). Big animals in a shrinking area, mass, height, etc. world—studying the ecological role of Asian megafauna as agents of seed dispersal. Innovation 10: 50–53.

Campos-Arciez, A., Larringa, A.R., Weerasinghe, U.R., Takatsuki, S.,

2014 Journal of Indonesian Natural History Vol 2 No 1 53 Contents

3 Editorial Indonesia 20-years after ratifying the Convention for Bioloical Diversity - a status check Carl Traeholt and Wilson Novarino 6 News and Notes 11 Debate Forum Bird thieves in Java show that Indonesian wildlife crime knows no boundaries Anais Tritto and Resit Sozer

Contributing papers 14 Genetic diversity of Macaca fascicularis (Cercopithecidae) from Penang, Malaysia as inferred from mitochondrial control region segment J.J. Rovie-Ryan, M. T. Abdullah, F. T. Sitam, S. G. Tan, Z. Z. Zainuddin, M. M. Basir, Z. Z. Abidin, C. Keliang, A. Denel, E. Joeneh and F. M. Ali 26 Asiatic Soft-shell Turtle (Amyda cartilaginea) in Indonesia: A Review of its Natural History and Harvest Mirza D. Kusrini, Ani Mardiastuti, Mumpuni, Awal Riyanto, Sri M. Ginting, and Badiah

Short communications 35 Aromatic Plants in Bali Botanic Garden Indonesia Wawan Sujarwo and Ida Bagus Ketut Arinasa 40 Not just mangroves: range expansion required for the mangrove whistler (Pachycephala grisola) on Borneo Marc L. Dragiewicz, David A. Ehlers Smith and Mark E. Harrison 43 First evidence breeding record of Hooded Pitta (Pitta Sordida) in mainland Sumatra, Indonesia Muhammad Iqbal, Ahmad Ridwan and Fadly Takari 45 Kalimantan’s tropical peat-swamp forests are important for Storm’s stork (Ciconia stormi) conservation Susan M. Cheyne, Simon J. Husson, Marc Dragiewicz, Lindy J. Thompson, Adul, Karen A. Jeffers, Suwido H. Limin and David A. Ehlers Smith 51 The Melaka Declartion 2014 52 Guidelines for authors

ISSN: 2338 865x