AUTECOLOGY OF THE SUNDA PANGOLIN (MANIS JAVANICA) IN SINGAPORE

LIM T-LON, NORMAN (B.Sc. (Hons.), NUS)

A THESIS SUBMITTED

FOR THE DEGREE OF MASTER OF SCIENCE

DEPARTMENT OF BIOLOGICAL SCIENCES

NATIONAL UNIVERSITY OF SINGAPORE

2007

An adult male Manis javanica (MJ17) raiding an arboreal Oceophylla smaradgina nest. By shutting its nostrils and eyes, the Sunda Pangolin is able to protect its vulnerable parts from the powerful bites of this ant speces. The scales and thick skin further reduce the impacts of the ants’ attack.

ii ACKNOWLEDGEMENTS

My supervisor Professor Peter Ng Kee Lin is a wonderful mentor who

provides the perfect combination of support and freedom that every graduate

student should have. Despite his busy schedule, he always makes time for his

students and provides the appropriate advice needed. His insightful comments and

innovative ideas never fail to impress and inspire me throughout my entire time in

the University. Lastly, I am most grateful to Prof. Ng for seeing promise in me

and accepting me into the family of the Systematics and Ecology Laboratory.

I would also like to thank Benjamin Lee for introducing me to the subject

of pangolins, and subsequently introducing me to Melvin Gumal. They have

guided me along tremendously during the preliminary phase of the project and

provided wonderful comments throughout the entire course.

The Wildlife Conservation Society (WCS) provided funding to undertake

this research. In addition, field biologists from the various WCS offices in

Southeast Asia have helped tremendously throughout the project, especially

Anthony Lynam who has taken time off to conduct a camera-trapping workshop.

The Singapore Zoo provided funding and also assisted in many aspects of the work. I would like to thank Charlene Yeong for the kind patience with all my requests

and the wonderful offer of sending other Singapore Zoo staff (e.g. Faizal Hussin,

Desmond Ling and Joe Ong) to assist in the fieldwork on Pulau Tekong. The vets

(especially Dr. Oh Soon Hock) have never turned down a single request to help

examine and treat wild pangolins before releasing them back into the wild.

The National Parks Board (NParks) and the Ministry of Defence

(MINDEF) granted the permission to conduct the research on both mainland

Singapore and Pulau Tekong respectively. It was most privileged for me to have

iii obtained kind permission from MINDEF to conduct long-term research on the

largely forested island of Pulau Tekong. The staff from both the Public Relations

Branch, MINDEF (especially Jude Ng) and CCO Pulau Tekong (especially Major

Lim and SSG Hasan) have assisted greatly in the logistics. I am also grateful to

the staff of NParks, especially Chew Ping Ting who has provided much assistance

when using the GIS system and Benjamin Lee who is always enthusiastic with

pangolin “rescue operations”.

The research would not have been possible if not for the many people who took the trouble to travel to Pulau Tekong, endured the less-than-comfortable conditions at the base-camp and accompanied me for the many nights of fieldwork. I am most grateful to each and every one of them, and truly enjoyed their company. Of special mention are Chan Kwok Wai, Reuben Clements

Gopalasamy, Jeremy Woon, Alan Yeo and Yeo Suay Hwee, who are ever so keen and responsive to last-minute requests. David Lohman provided much assistance for the identification of ants, while Reuben Clements Gopalasamy provided guidance for the statistical analysis. Friends and colleagues from the Systematics and Ecology Laboratory, and the Raffles Museum of Biodiversity Research gave me much support, advice and encouragement along the way. I am also grateful to the friends and collaborators in the neighbouring countries who provided valuable information on the various aspects discussed in this work.

Last but not least, I would wish to thank my parents, other members of the family and also my fiancée for tolerating my idiosyncrasies (especially that of sneaking into the forest during the night) all this while. This piece of work (and other research projects) would not have been possible without their continued

encouragement and support.

iv TABLE OF CONTENTS

Acknowledgements………………………………………………………………… iii

List of tables, figures and plates…………………………………………………… viii

Summary…………………………………………………………………………… xi

Chapter

1. Introduction

1.1 Pangolin species and taxonomy …………………………………… 1

1.2 Conservation status of Asian pangolins……………………………. 3

1.3 Literature review on Manis javanica………………………………. 4

1.4 Status of Manis javanica in Singapore…………………………….. 9

1.5 Specific objectives…………………………………………………. 12

2. Materials and methods

2.1 Study site…………………………………………………………… 13

2.2 Capture and radio-telemetry……………………………………….. 14

2.3 Camera-trapping and natal den description………………………... 17

2.4 Prey preference…………………………………………………….. 18

2.5 Data analyses

2.5.1 Sexual dimorphism and sex ratio…………………………... 19

2.5.2 Daily activity patterns……………………………………… 20

2.5.3 Home range………………………………………………… 20

2.5.4 Habitat preference………………………………………….. 23

2.5.5 Prey preference…………………………………………….. 25

2.5.6 Miscellaneous (data from mainland Singapore)…………… 26

3. Results

3.1 Body measurements of Sunda Pangolin on Pulau Tekong………… 27

v 3.2 Home-range, activity cycle and other spatial-temporal statistics….. 28

3.3 Habitat preference………………………………………………….. 31

3.4 Natal den usage by pregnant and postpartum Manis javanica MJ6.. 32

3.5 Prey preference…………………………………………………….. 33

3.6 Predation of Manis javanica by Python reticulatus………………... 35

4. Discussion

4.1 Body measurements of Sunda Pangolin on Pulau Tekong………… 37

4.2 Home-range, activity cycle and other spatial-temporal statistics….. 38

4.3 Prey preference…………………………………………………….. 44

4.4 Habitat preference………………………………………………….. 46

4.5 Reproductive biology of MJ6……………………………………… 49

4.6 Predators of Manis javanica……………………………………….. 51

5. Overall conclusions and recommendations

5.1 Challenges for future pangolin research.…………………………... 54

5.2 Priorities for conservation of pangolin species…………………….. 57

5.3 Status of Manis javanica in Singapore…………………………….. 61

5.4 Conclusion…………………………………………………………. 62

References………………………………………………………………………….. 63

Tables, Figures and Plates…………………………………………………………..73

Appendices

I. List of Manis javanica sightings in Singapore for the past two decades……………………………………………. I-1

II. Percentage of the various ant genera collected with cheese bait, sugar bait and the combined values. ………………….. II-1

III. Percentage of foraging time spent on the various ant genera by three adult male Manis javanica..…………………... III-1

vi LIST OF TABLES

1. A summary of information on the eight pangolin species of the Old World.

2. Known uses and supposed benefits of pangolin parts.

3. Body measurements (HB – head-body length; T – tail length, in cm; body mass in kg) and sex of the Manis javanica captured on Pulau Tekong.

4. Speed statistics (m/ hr) of adult male Manis javanica on Pulau Tekong.

5. Home-range estimates (ha) of adult Manis javanica using minimum-convex polygon (MCP), harmonic mean and kernel methods, with the various parameters stated and using non-autocorrelated radio locations.

6. Simplified ranking matrix for Manis javanica based on a) comparing roportional habitat use within minimum convex polygon (MCP) home ranges with proportions of total available habitat types, and b) comparing proportion of radio locations (with 20-m radius buffer) for each animal in each habitat type with the proportions of each habitat types within the animal’s MCP range (see text for more details). “+” implies the habitat type of the r was preferred to the habitat type in the row and “-” implies the reverse; a triple sign represents significant deviation from random at P < 0.05.

7. Jacob’s index for each habitat used by pangolins on Pulau Tekong at second-order and third-order selection.

8. Description, measurements and duration of usage of the three dens used by female Manis javanica MJ6 from September to December 2005.

9. Mean and maximum time (min) spent on feeding by three male Manis javanica.

10. Percentage of time spent feeding on ants and termites by three tagged male Manis javanica.

11. Jacob’s index of the ant subfamily consumed by adult male Manis javanica on Pulau Tekong.

12. Jacob’s index of the ant genera consumed by adult male Manis javanica on Pulau Tekong.

13. Date of the locations of radio-transmitter in Figure 1, distance from previous location and description of location.

14. Reported date of birth and body measurements of neonate Manis spp.

vii LIST OF FIGURES

1. Location of all known records of Manis javanica sightings and roadkills in Singapore, from 1985-2007.

2. Map of Pulau Tekong, relative to mainland Singapore. The shaded grey shaded area is the only reservoir on the island and the cross-shaded patches are the built- up areas. The remainder of the island is covered with the vegetation.

3. Radio-telemetry error polygons under extreme conditions of maximum distance from transmitter (i.e. 200 m) and maximum bearing difference from optimal angle (i.e. 60° and 120°).

4. Diel activity pattern of female Manis javanica MJ6 (mean ± S.E.), based on 30 days of camera-trapping data from 8th September to 12th December 2005.

5. Diel activity pattern of each of the four adult male Manis javanica. No activity was recorded between 0800 hrs to 2000 hrs.

6. Diel activity pattern of adult male Manis javanica (n = 4), with S.E. as error bars. No activity was recorded between 0800 hrs to 2000 hrs.

7. Accumulative 100% minimum-convex polygon home-range estimates of individual adult male Manis javanica with increasing number of radio-tracking days.

8. Autocorrelation plot of Schoener’s index with time interval of Manis javanica MJ9. Reasonably-independent radio locations were obtained at approximately 2- hr interval (green vertical line), where there are three consecutive values of Schoener’s index greater than 1 (see text for more details).

9. Position and shape of 100 % minimum convex polygon home-range of the four adult male Manis javanica (MJ9, MJ12, MJ22 and MJ23) on Pulau Tekong. Location of capture sites of the other pangolins are indicated by crosses.

10. Location of the three natal dens used by female Manis javanica MJ6 (in crosses) and positional points from radio-tracking (in squares).

11. Map of locations of radio-transmitter during the 11 days it was tracked. Dotted lines are streams; solid lines are trails or roads. Refer to Table 13 for date and description of locations.

viii LIST OF PLATES

1. Den A and its entrance (as shown by the arrow).

2. Den B and its entrance (top picture), and fallen tree of Den B (bottom).

3. Den C and its two entrances, as shown by the arrows.

4. Image of MJ6 and its young, taken on 3rd November 2005 by infrared-triggered camera-traps positioned facing the den entrance. Note that the young is slightly longer than the tail length of MJ6 (one month after its first record) and also the severed antenna of the radio-transmitter.

ix SUMMARY

The Sunda pangolin (Manis javanica), like other members of the family

Manidae, is a poorly known species and currently affected by illegal trade for their meat and scales. Wild M. javanica were captured and radio-marked on both mainland Singapore and Pulau Tekong from 2005 to 2006. Pangolins were monitored using radio-telemetry equipment to observe activity cycle, space use, prey preference and habitat preference. Infrared-triggered camera-traps were also deployed for one female pangolin and her young.

Preliminary work on mainland Singapore includes an instance whereby a young radio-marked pangolin was later found to have been consumed by a

Reticulated Python (Python reticulatus). However, it is unclear whether python predation on pangolin is a common event in the wild.

Due to the high drop-off rates of transmitters, of the 21 pangolins captured on Pulau Tekong, only four adult pangolins were successfully monitored. The male pangolins were active for only 165 ± 14 min (mean ± S.E.) every night.

While peak activity period could be observed for the individual pangolins, the peaks occurred at different times of the night and thus the overall activity pattern was relatively uniform. The cumulative 100% minimum-convex polygon (MCP) home-range estimates for three of the adult pangolins stabilised towards the end of the radio-tracking regime. The only exception was due to a shifting of home-range after a territorial encounter with another male pangolin, resulting in a steep climb in the cumulative 100% MCP estimate. The mean 100% MCP home-ranges of the males was 41.3 ha. For the female pangolin, only one young was recorded from this birth event and the period of postpartum maternal care was approximately

x three to four months. A total of three natal dens were used throughout and hollows

of large trees > 50 cm diameter-at-breast-height (DBH) were associated with all

dens. The 100% and 95% MCP home range size was 6.97 ha and 5.63 ha

respectively. The daily active period of the female was 127 ± 13.1 min and peak

activity was between 0300 and 0600 hrs. Eleven genera of ants were observed to

be foraged upon by the male pangolins and foraging took up 11.3 ± 1.8 % of their

daily active periods. Ants and termites made up 67.0% and 33.0% of the foraging

time respectively, but this difference was not statistically significant. Anoplolepis

gracilipes was found to be the only ant species that was significantly preferred;

Philidris, Crematogaster and Myrmicaria were avoided.

The absence of a clear pattern of habitat or prey preference was probably

due to the small sample size. Nevertheless, the available results reflect an

underlying trend – Manis javanica are adaptable animals and can survive in most habitats. However, females during their reproductive phases may require natal dens associated with trees greater than 50 cm DBH for parturition and rearing of the young. This means that female pangolins with young could be restricted to mature forests. With the present habitat degradation in Southeast Asia, the availability of suitable natal dens in mature forests may prove to be an important limitation for their population sustainability.

xi CHAPTER 1. INTRODUCTION

Pangolins (Manis spp.) are largely nocturnal and have adapted to a highly

specialized diet of ants and termites (Lekagul and McNeely, 1988). The

adaptations include a conical-shaped head that does not have teeth, a long sticky

tongue to lick up the ants or termites and powerful long claws on its limb for

digging and breaking apart ant nests or termite mounds (Payne and Francis, 1998).

Their scales, which are composed of keratin, offer excellent protection not only against potential predators, but also from the bites and stings of ant and termite prey (Payne and Francis, 1998).

1.1 Pangolin species and taxonomy

Pangolins are members of the only family (Manidae) in the order Pholidota and

there are only eight extant species in the world. The four Asiatic species are the

Indian Pangolin (M. crassicaudata), Chinese Pangolin (M. pentadactyla), Sunda

Pangolin (M. javanica) and Palawan Pangolin (M. culionensis); the four African

species are the Giant Pangolin (M. gigantea), Tree Pangolin (M. tricuspis),

Ground Pangolin (M. temminckii) and Long-tailed Pangolin (M. tetradactyla).

Heath (1992) provides an identification key to the extant species, except M. culionensis which was only recently proposed to be distinct from M. javanica (see

Gaubert and Antunes, 2005). Table 1 presents a summary of the information on the eight known pangolin species. Note that for M. culionensis, virtually no information is available due to its very recent taxonomic split from M. javanica.

Other than the extant species, there are extensive fossil records of extinct genera in the order Pholidota as well. The oldest fossil pangolin, Eomanis, is

1 approximately 45 million years ago; the more recent genera include Necomanis,

Patriomanis and Cryptomanis (see Gaudin and Wible, 1999; Gaudin et al., 2006).

In addition, a collection of bones (subsequently named Manis paleojavanica), which was morphologically most similar to the extant M. javanica but at least twice the length, was found from sites in South Asia and mainland Southeast Asia from the early to mid 1900s (Dubois, 1907). Bones of a large-bodied Manis taxon radiocarbon-dated to around 40 thousand years ago (i.e. late Pleistocene/

Holocene) was also found in the Niah Cave, together with butchered remains of

M. javanica, suggesting that the two species co-existed and were hunted by humans at a point in time (Piper et al., in press). While the smaller Sunda

Pangolin survives to the present day, the above authors have speculated that hunting pressure on the larger-bodied pangolin species may have led to its extinction.

While it is generally agreed that the extinct forms are more primitive in certain aspects of its morphology than the living species, there is no consensus with regards to the phylogeny amongst the extant species. With a phylogenetic analysis based on 67 cranial characters, Gaudin and Wible (1999) obtained a single most parsimonious tree, with three major clades: 1) the Asian species M. crassicaudata, M. javanica, and M. pentadactyla, 2) the arboreal African species

M. tricuspis and M. tetradactyla, and 3) the terrestrial African pangolins M. temminckii and M. gigantea. However, as there are very limited infraordinal phylogenetic studies on the Pholidota, it is still unclear whether the extant Asian or the African species are the more primitive forms (Gaudin and Wible, 1999;

Gaudin et al., 2006).

2 1.2 Conservation status of Asian pangolins

With the exception of the Palawan pangolin, the other three Asian pangolins (i.e.

M. crassicaudata, M. javanica and M. pentadactyla) are classified as “Lower

Risk: near threatened” (IUCN, 2006) and listed in Appendix II of the Convention on International Trade in Endangered Species of Wild Fauna and Flora (CITES) since 7th January, 1975 (Inskipp and Gillet, 2005). The difference in the

conservation status of M. culionensis from the other Asiatic pangolins is because it was only recently proposed to be distinct from M. javanica (see Gaubert and

Antunes, 2005).

At the national level, all Asian pangolin species are protected by law, except in Laos PDR where the wildlife protection law regarding pangolins is still unclear (IUCN Pangolin Specialist Group, 1996). While being a protected species, pangolins in the region are highly sought after for their meat and scales. In fact, newspapers often report on illegal smuggling of Manis species across countries

(e.g., Abas, 2002; AFP, 2003; Simon, 2004). It is questionable whether the present enforcement of wildlife protection laws are sufficient to curb the rampant illegal

smuggling activities, which are fuelled by the high prices fetched by pangolin parts.

While there is an obvious need for a forum whereby researchers and conservationists can share their ideas to effect directed conservation actions, it is unfortunate that the IUCN Pangolin Specialist Group was dissolved around year

2006 “because of the re-organisation of the IUCN Specialist Groups” (J.T. Chao, in litt.). Furthermore, there was no official white paper generated by the IUCN

Pangolin Specialist Group when it was in commission. The reasons listed above

3 provide the motivation for an in-depth literature review on the Sunda Pangolin (M. javanica), the subject of interest for this project.

1.3 Literature review on Manis javanica

The Sunda pangolin (Manis javanica) is one of the four species of Asiatic pangolins and is found in most parts of the Southeast Asian region. Despite its relatively wide distribution, there is no detailed study on their population levels, ecology and life history.

Most of the existing literature on the ecology of pangolins are of the

Chinese Pangolin M. pentadactyla (e.g., Shi, 1985; Wu et al., 2003), Cape

Pangolin M. temminckii (e.g., Heath and Coulson, 1997; Richer et al., 1997; Swart et al., 1999) and Tree Pangolin M. tricuspis (e.g., Pagés, 1975). While the Sunda

Pangolin resides in their natural habitat of tropical rainforest of Southeast Asia, the other pangolin species inhabit different latitudes (e.g., M. pentadactyla in the temperate regions) and habitats (e.g., M. temminckii in the African savannahs and grasslands), and thus will most probably have differing ecological niches from M. javanica. Nevertheless, albeit limited in numbers, the information and findings on other pangolin species are still invaluable and insightful for the planning of this first ecological study of M. javanica. For instance, Fang and Wang (1980) reported that some of the wild M. pentadactyla only contained Macrotermes barneyi termites in their stomachs, some only contained an unknown species of black ants, while others contained both different types. This observation, together with the findings of the prey preference study of M. temminckii by Swart et al.

(1999), suggests that the Sunda Pangolin is most likely a diet generalist which may consume on a variety of ants and termites species. This will have

4 implications on the technical expertise required for the handling, identifying and

maintaining of potentially large number of ants and termites specimens consumed

by M. javanica in the field.

General information on manids is available in several guidebooks to

mammals (e.g., Harrison, 1969; Nowak and Paradiso, 1983; Lekagul and

McNeely, 1988) and often includes observations which are anecdotal (e.g.,

Ripley, 1964). However, while most of these comments or observations were not

backed with rigorous scientific data, they offer valuable insights into the ecology

of pangolins and can be interesting research questions for any future work on

pangolins. For instance, Davies and Payne (1982) observed that M. javanica is

more often recorded in cultivated areas than forest, while Payne and Francis

(1998) reported that they are more often seen along roads at night. Whether these observations are effects of actual habitat preference or simply a function of biased

“sampling” in the populated cultivated areas will be an important consideration in the formulation of future pangolin conservation policies.

Diet. The fact that these diet-specific myrmecophages could be eating up to

200,000 worker ants in a day (Harrison, 1962) or up to 10% of their body mass

(Fang and Wang, 1980) suggests that they have an important ecological niche in influencing the populations of ants and termites, the dominant constituent of

biomass in any ecosystem (Höfer et al., 2001) and thus having a profound

influence on the nutrient-recycling dynamics. As a result, the conservation of

pangolins, especially that of the Sunda Pangolin which is the most threatened by

the trade (Bräutigam et al., 1994), does not simply involve the continued existence

of the species per se, but also the functional integrity and maintenance of

5 ecosystems through their interactions with the ant and termite communities. On a similar note, Heath (1992a) also suggested that Manis pentadactyla is important to the Chinese because they prey on termites which can cause considerable damage to artificial structures.

In captivity. It is also well-known that pangolins do not survive well in captivity and can suffer 71% mortality in the first year of captivity (Wilson, 1994). This may be surprising to most animal breeders as they are non-aggressive in nature and can feed on a large number of ant or termite species (i.e. generalists).

Nevertheless, this eliminates the option of captive breeding to ease the strong hunting pressure and further supports the importance of in situ conservation of pangolins in their natural habitats. While there were reports of pangolins successfully kept in captive conditions (notably Manis javanica in the Singapore

Zoo and M. pentadactyla in the Taipei Zoo; C. Y.-F. Yeong and J.S.C. Chin, pers. comms. respectively), this seems to be rare exceptions as most organisations that have tried failed to succeed.

Reproductive biology. Pangolins are believed to give birth to one young each time, but twins have been reported at times (Payne and Francis, 1998). However, there are no actual records on the number of births per year, the gestation period and also the duration of the maternal care for M. javanica (Payne and Francis,

1998). It is also not known if there are specific habitat or diet requirements of female Sunda Pangolin during their reproductive phase. On the other hand, the

Taipei Zoo has reported instances of captive births in their enclosure for the

Chinese Pangolin (J.S.C. Chin, unpublished data).

6 Many other important aspects pertaining to their population dynamics are

also unknown. These include basic information about their abundance,

metapopulation dynamics (Hanski and Gilpin, 1997) and population viability

analysis (White, 2000). In fact, at a recent Formosan Pangolin Population and

Habitat Viability Analysis (PHVA) organized by the IUCN Conservation

Breeding Specialist Group, it was acknowledged that many critical parameters necessary for the analysis were not available (D. Reed, pers. comms.).

Habitat destruction. The Sunda Pangolin faces serious threats from habitat destruction and degradation in this “hottest” biodiversity hotspot (Laurance and

Bierregaard, 1997; Myers et al., 2000). For instance, forested areas in both

Indonesia and Malaysia are disappearing at an alarming rate of 1.20% per year, or

1,312,000 ha and 237,000 ha respectively (FAO, 2001). However, the effects of such land use change on the population dynamics of the pangolins are unknown and are most likely to be profound in extent. Therefore, it is crucial for conservation managers to be aware of the preferred habitats of pangolins and better target their conservation efforts in such areas.

Hunting threats. Severe hunting pressures for their meat and scales for purported medicinal properties (see Table 2) only serve to further the decline in numbers. As pangolins are CITES Appendix II species with “zero trade quota” in most of Asian countries, official statistics on the quantity traded is very limited.

The only official statistics of the trade of pangolin scales comes from South

Korea, with 7,067 kg imported from China, 1,850 kg from Indonesia, 1,000 kg from Malaysia and 1,026 kg from Vietnam in 1992 (Bräutigam et al., 1994).

7 Based on the conservative assumption that a single pangolin yields 0.5 kg of scales (TRAFFIC, 2002), this translates to around 14,000 M. pentadactyla and

7,500 M. javanica in one year. Furthermore, there are numerous reports from

TRAFFIC Bulletin on the presence of pangolins in the wildlife trade both within

and outside of the Sunda Pangolin’s range – e.g., Cambodia (Martin and Phipps,

1996), Guangxi and Guangdong (Li et al., 1996), Taiwan (Chang, 1997) and

Yunnan (Li and Wang, 1999).

Within the region, seizures are happening almost daily (Hogg, 2003) and are often reported in local or regional newspapers and magazines. In July 2002,

Thailand officials confiscated a total of 1,737 live pangolins which were believed to be heading for China, Hong Kong or Taiwan (WAR, 2002); and in April 2004,

Malaysian authorities uncovered 1,200 frozen pangolins which are supposedly to be shipped to Vietnam (TRAFFIC, 2004). The high incidence of such opportunistic seizures by the wildlife authorities only goes to show that the true situation is most likely far more serious. Finally, Bräutigam and others (1994) noted that the international trade of pangolins appears to have focused primarily on M. javanica and this exacerbates the need of basic information on their ecology for proper conservation actions.

Given the lack of information on their current status and threats, CITES rejected the recommended transfer of Asian pangolins (including M. javanica) from Appendix II to Appendix I at the Eleventh Meeting of the Conference of the

Parties and concluded that more information was required on pangolin populations

(CITES, 2000). However, even with its Appendix II protection status and “zero quota” trade limits in most Asian countries, large numbers of live pangolin and scales (especially that of M. javanica) have been smuggled across country borders

8 at an alarming rate (Bräutigam et al., 1994). The only conservation action seemed to be the opportunistic seizures and prosecution by the local authorities.

Nevertheless, it is saddening to know that these seizures sometimes end up with the large numbers of live pangolins being sacrificed (e.g., AFP, 2003). The IUCN

Pangolin Specialist Group acknowledged that virtually no information is available on the population levels of any of the Asian pangolins and no population estimates has been located for M. javanica (WCMC et al., 1999). This lack of data severely hampers all conservation efforts and management.

1.4 Status of Manis javanica in Singapore.

The Singapore Red Data Book (Ng and Wee, 1994) listed Manis javanica as

“Vulnerable”, with distribution mainly in the Bukit Timah Nature Reserve

(BTNR) and the Central Catchment Nature Reserves (CCNR). However, there has not been any targeted or organised study on the Sunda Pangolin done in Singapore or Malaysia. The limited information available was from the occasional reports of encounters in the forested areas and their fringes which is often private housing area (e.g., Chestnut Avenue and Adam Drive). Figure 1 presents all known records of sightings and roadkills collected by the author, the National Parks

Board, Singapore (NParks) and the Singapore Zoo over the past two decades

(detailed list of the sightings and roadkills were compiled in Appendix I). While it is evident that the distribution of M. javanica in Singapore is widespread, the intensity of the sightings substantiates the notion of Ng and Wee (1994) that the stronghold of the species seems to be in the forest reserves.

In the Singapore Red Data Book, (Ng and Wee, 1994) also proposed the building of wildlife tunnels under the Bukit Timah Expressway (BKE) to connect

9 the two forest fragments. This recommendation may have stemmed from the observation that the bulk of the sightings were near the fringes of the forest reserves (i.e. suggesting that the pangolin may prefer forest-edge habitats) and the

BKE is a major expressway that divides the BTNR from the CCNR. In addition, with the data collected over the last two decades (see Appendix I), it is clear that there were indeed many instances of roadkills along the expressways and roads running along the edges of the forest reserves (e.g., Old Upper Thomson Road and

Mandai Road). Of note was an instance whereby a 6.7 kg male pangolin was seen at Dairy Farm Crescent on 8 March 2004 and subsequently relocated to CCNR after implanting it with a passive interrogative transmitter (PIT) tag for future identification. On 21 September 2004, the same individual was found at a private housing estate along Ang Mo Kio Avenue 2 and weighed 10.5 kg at that time.

This example is an excellent illustration of the strong dispersing abilities of this species and the potential impacts that habitat fragmentation have on them.

Therefore, it is apparent that the wildlife corridor concept is very applicable and worth pursuing to present a better probability of long-term survival for the species locally.

In addition to the two nature reserves, there were also records of M. javanica in the Western Catchment area (a military training and live-firing area),

Mandai forest (which is adjacent to the Singapore Zoo), Pulau Ubin (an offshore island accessible to the public) and Pulau Tekong (a military island for recruit training purposes). It is currently unclear whether these additional areas constitute a substantial proportion of the population and also whether there is migration of individuals amongst the different patches (especially with the dense network of roads on mainland Singapore).

10 While the Sunda Pangolin is legally protected under the Wild Animals and

Birds Act (Chapter 351) and the Endangered Species (Import/ Export) Act 2006

(Agri-Food and Veterinary Authority of Singapore, http://www.ava.gov.sg), it is

possible that there is some poaching taking place in Singapore. This is because the

pangolin meat is known to be delicious and highly sought after in the region (see

above). In fact, there was an incident on Pulau Ubin whereby some Thailand

construction workers were found to be cooking a Sunda Pangolin, which they

claimed were mortally injured by a dog (R. Teo, in litt.). As a result, in view of the

limited manpower at the various NParks offices, limited enforcement of the

various wildlife laws could be carried out effectively. Nevertheless, in view of the

present state of the Singapore society, it is believed that whatever poaching that

may be present, it is likely to be limited.

Another organisation that is supportive of and active in wildlife

conservation is the Singapore Zoo, and much emphasis is placed on the

conservation of native mammals at this moment in time. Whenever wild pangolins

were handed over to the authorities, the Singapore Zoo vets would assist by

examining and treating the pangolins before they were released or relocated. In

addition, the Singapore Zoo is also attempting to maintain wild pangolins in

captivity with an artificial diet and also to breed them in captive environment,

should they survive on the artificial diet (C.Y.-F. Yeong, pers. comms.).

11 1.5 Specific objectives

Bearing in mind the present situation and lack of knowledge about the Sunda

Pangolin, Manis javanica, the specific objectives of this research project are:

1) To review the available information on pangolins and their

conservation status,

2) To determine the home range and daily activity cycle of the Sunda

Pangolin in the different habitats in Singapore,

3) To investigate the habitat preference and feeding ecology of M.

javanica,

4) To investigate the requirements of the Sunda Pangolin during the

reproductive phase, and

5) To document any other natural behaviour recorded during the

duration of the field study.

12 CHAPTER 2. MATERIALS AND METHODS

2.1 Study site.

The study was conducted on Pulau (=Island) Tekong (1° 24’ N, 104° 02’ E), an

island off the northeastern shore of Singapore (Fig. 2). The climate is

characterized by high relative humidity, temperature (daily mean: 84.3% and 26.8

°C respectively) and rainfall (annual rainfall approximately 2344mm)

(Meteorological Services Singapore; http://www.nea.gov.sg/metsin/). Pulau

Tekong has 2,350 ha of land and was formerly inhabited by villagers until it was

gazetted as a military training area in 1985. Based on the National Parks Board

GIS database, there are three main types of vegetation on Pulau Tekong, namely

the mangrove along the northern shore (38%), herbaceous vegetation on the

reclaimed southern portion (25%) and low secondary forest or adinandra belukar

(about 18%). Patches of Elaeis guineensis and Hevea brasiliensis monoculture

(8%) are also present, in addition to the built-up areas and artificial open spaces

(about 11%) in the southwestern parts. The herbaceous vegetation includes

Imperata cylindrica, Panicum maximum, Pennisetum purpureum, Urochloa mutica and some leguminous trees like Acacia auriculiformis (Chou et al., 2006).

The adinandra belukar forest which occupies most of the central parts of Pulau

Tekong is dominated by Adinandra dumosa and Rhodamnia cinerea (Chou et al.,

2006); some Hevea brasiliensis and tropical fruit trees (e.g., Artocarpus

heterophyllus, Durio zibethinus, Nephelium lappaceum) in abandoned garden

plots are also found within this regenerated forest type (H.T.W. Tan, pers.

comms.).

13 2.2 Capture and radio-telemetry.

From August 2005 to December 2006, pangolins were detected by carefully listening for signs of their activity while walking or cycling with minimal noise along roads and dirt trails during the entire night (2000-0700 h). The sounds of pangolin activity include rustling of leaf litter while the animal moves on the forest floor, and that of an ant nest or termite mound being excavated by an animal. Pangolins were observed to be very sensitive, and they will either promptly flee or freeze in their tracks when they detect human presence in their immediate vicinity (pers. obs.). Pangolins were then caught by hand. Body measurements were then taken and these include head-body length (HB), tail length (T) and body mass (M). Selected tail scales were also clipped along the margins to give the pangolins a long-term identity code (in addition to the radio- transmitter, which may be dislodged over time) and a picture was taken for record-keeping and future comparison. Possible injuries to the animal (especially to the claws) was minimised by performing attachment of the transmitter on natural ground substrate. In addition, the duration of restraining the animal for the attachment was kept to a minimal to reduce the stress induced.

Radio-transmitters AI-2F and RI-2A (216 MHz band; Holohil Systems

Ltd., Ontario, Canada), weighing 21 g and 12 g respectively (i.e., less than 1% of an adult pangolin’s body mass) and an average battery lifespan of six (for RI-2A transmitters) to 12 (for AI-2F) months, were fitted onto the selected scales on the tail with screws and bolts (Richer et al., 1997). The profile of the transmitter was also streamlined using epoxy putty, to reduce the chances of the transmitter being caught on by the dense undergrowth vegetation. After successfully attaching the transmitter, the pangolins were released at the site of capture and they were given

14 at least one week to acclimatise to the transmitter package (White and Garrot,

1990) before radio-tracking commences. This is to minimize the inclusion of

possible unnatural behaviour like abnormal levels of activity or decrease in food

intake (White and Garrot, 1990) during the tracking period. Signals from tagged

subjects were located with a portable telemetry receiver (R-1000;

Communications Specialist Inc., California, USA) and a directional H-antenna

(RA-2A; Telonics Inc., Arizona, USA). Signal maxima was used to determine bearings of the subject.

During radio-tracking, visual confirmation of subjects’ locations was performed as much as possible, for 77% of the location fixes. In cases whereby the terrain did not permit tracking on foot or the pangolin was constantly exhibiting evasive behaviour (i.e. MJ23, see below), triangulation of radio-signals was performed with two azimuth readings taken within 5 min of each other. This

short time interval has the purpose of reducing the error of the triangulated

position by minimising the possible distance the animal moved between the two

readings (White and Garrott, 1990). To further minimise the error polygons, the

positions for triangulation were always less than 200 m away from the subject and

the difference in the signal directions was between 60° to 120° (i.e. optimal angle

of 90° ± 30°). The typical bearing precision of handheld portable radio-telemetry systems is around ± 5° (White and Garrot, 1990). By placing test transmitters at

sites in the study area, the maximum telemetry error was also found to be 5°.

Under the extreme conditions of maximum distance from subject and extremes of

the bearing difference (i.e. 60° and 120°), the maximum distance of triangulated

(i.e. estimated) location from the true location was 40 m (see Fig. 3) and is

15 comparable to or better than the error reported in other habitat preference studies

(e.g., Shepherd and Lank, 2004; Goodman et al., 2005).

All locations, either fixes during active radio-tracking on foot or of

triangulation locations, were recorded using a GPS (GPS 60CS; Garmin

International Inc., Kansas, USA) attached to an active external antenna (Gilsson

Technologies, California, USA); the accuracy of the recorded locations were ≤ 15

m (even when under the forest canopy). The location of the tagged pangolins were

recorded every 15 min, starting from the emergence from their dens, until they

return to the next resting place. In addition, the activity (e.g., foraging, moving)

and vertical strata utilized by the pangolins were also recorded at 1 min interval throughout its active period in the night. All observations were conducted using

the focal animal sampling technique (Lehner, 1996) and with the aid of a 4.8 v

L.E.D. headlamp. Prey items which were fed on were also collected during radio-

tracking sessions (see Prey preference below). Only observations of individuals which were exhibiting normal behaviour (e.g., foraging at a slow and relaxed pace) were used for the data analysis. This translated to at least five additional nights of tracking (after the week for acclimatisation to the transmitter package) before the subjects were habituated to our constant presence and stopped exhibiting evasive behaviour like pausing in the middle of its original activity whenever we make some noise on the forest floor or climbing a nearby tree to evade from us. However, even after a month of habituation, there was still an individual (code MJ23) which was never habituated to our presence and thus prey preference analysis could not be determined for this individual. Nevertheless, triangulation for MJ23’s locational data were possible and adhered to the accuracy stated (see above).

16 For the habitat preference analysis, a minimum of six nights of complete radio-tracking was performed (i.e. the entire active period was captured). This was because with six nights of radio-tracking data, it would require 12 to 20 days since date of capture. It was deemed to be a reasonable compromise between the amount of data collected from each individual and the number of individuals that can be tracked within the sampling period, especially given the high drop-off rate of the transmitter package.

2.3 Camera-trapping and natal den description.

Besides active radio-tracking, infrared-triggered camera-traps were also utilized to monitor the activity of a female Manis javanica (codenamed MJ6) which was rearing a young. When radio-tracking MJ6, it was observed that the individual was particularly wary of extraordinary noise and movement, and often headed straight back to its burrow upon detection of our presence. As a result, radio- tracking during its active period was no longer carried out for MJ6, in fear of MJ6 abandoning the young. Instead, only non-invasive monitoring was conducted by placing infrared-triggered camera-traps at the den entrances and radio-tracking during the day to ascertain possible usage of new dens.

Upon locating a den used by the tagged pangolin, a camera setup was then secured onto a nearby tree trunk with the lens facing the entrance or exit of the den. The infrared-triggered camera-traps were assembled using passive infrared sensor (LE Controller Board; PixController Inc., Pennsylvania) and Olympus C-

120 digital camera. In addition to the 4 ‘AA’-sized batteries in the digital camera, modifications were made to allow for auxiliary power source of 4 ‘C’-sized batteries. The setup was housed in a weatherproof case (Pelican 1020, Pelican

17 Products Inc., California). All cameras were operational 24 hours a day and the interval between successive images was set to 10 sec to reduce the number of shots within a short period of time and yet obtain a precise timing of the exit/ entry.

The term ‘den’ is herein defined as any site or structure used by a pangolin

for extended periods of sleeping or resting. In this instance, the term includes natal

den which is used by the female pangolin for the birth and postpartum rearing of

young until weaning.

2.4 Prey preference.

During radio-tracking, the duration of each feeding bout (i.e. from start of actual

feeding to end of feeding, excluding digging time to excavate the nest) was

recorded to the nearest minute. The prey items that were fed on by the tagged

pangolins were subsequently collected after the pangolin moved away and then

preserved in 75% ethanol for subsequent identification. Special care was taken to include worker caste for ants and soldier caste for termites as identification keys

for these taxa are based on morphology of these specific castes.

In order to assess the relative abundance of the ant and termite fauna

present within the home ranges of each tagged pangolins, five sampling points

were established within the 100% MCP home-range by systematic sampling

(Southwood and Henderson, 2000). Each sampling point is a 10 x 10 m square area and consists of a grid of nine sugar and nine protein baits on the ground, and

another replicate set on the arboreal environment. The sugar baits were in the form

of cotton swabs wetted with 10% honey solution while the protein baits were

grated cheese powder sprinkled on cotton swabs. After setting up, the baits were

18 left for 60 min before collecting and preserving the ants that were attracted onto

the respective cotton swabs. As a result, the ground baits were able to provide a

picture of the subterranean and terrestrial ant fauna while those on trees/ shrubs

were able to do the same for the arboreal species. Only sugar and protein baiting

were employed in this study because these methods provide for a rapid assessment

of the myrmecological fauna and also allow the objective quantification of their

relative abundance in the habitats. While it is acknowledged that a combination of

other methods (e.g., hand-collection and soil-core sampling) will provide a more accurate analysis of the total ant fauna present, their use will unfortunately compound the issue of quantifying the relative abundance (A.K.H. Tham, pers. comms.).

On the other hand, since termites are not attracted to such baits, only hand collecting (by walking around the grid area and breaking open rotten tree trunks or

logs) were performed to assess the number of termite nests and also the species of

termite. It is to be noted that all baits were set up and collected during the

nighttime, as it is also during this same duration that pangolins are active and

forage.

2.5 Data analyses.

2.5.1 Sexual dimorphism and sex ratio.

Intraspecific comparison of sexual dimorphism in the body measurements (i.e.

HB, T and M) of the captured pangolins was investigated using unpaired

Student’s t-test (Zar, 1999). The sex-ratio of the captured pangolins was

19 investigated with Yates’ chi-square test (Zar, 1999), to examine for significant

sex-ratio biasness at the study site.

2.5.2 Daily activity patterns.

For all tagged pangolins that were radio-tracked (i.e. excluding MJ6), the time of

awakening and resting were recorded for all sessions. It is to be noted that for the

latter, care was taken to ensure that the pangolin was resting for the night by

visual confirmation for a lack of movement for at least another 30 min, while not

causing any disturbances in the vicinity at the same time. In addition, the vertical

strata utilised and the behaviour recorded every minute during their active

duration were also analysed.

For individual MJ6, all images taken by the infrared-triggered camera-

traps have the date and time information imprinted by the digital camera. As a

result, the activity periods could then be determined by analyzing the timings of

the events (i.e. from exit till re-entry). Incomplete photo records (i.e. without

either exit or re-entry) which could arise from battery-drainage were excluded

from analysis.

2.5.3 Home range.

Burt (1943: 351) defined home-range as “that area traversed by the individual in

its normal activities of food gathering, mating and caring for young”. The home-

range was calculated by minimum convex polygons (MCP - Mohr, 1947), using

RANGES VII v0.94 software (South et al., 2005). 100%, 95% and 50% MCP

were computed because these estimates provide good comparison for future

20 home-range studies. The comparison of other methods is complicated by different

software packages that use differing algorithms for their computing, and thus

provides different results for the same datasets (Lawson and Rodgers, 1997).

Nevertheless, other home-range estimates were also calculated using

RANGES VII, with all parameters listed for future comparison. These include:

i. fixed kernel estimates (Worton, 1989) using reference bandwidth

(=1),

ii. fixed kernel estimates using least-squares cross-validated (LSCV)

bandwidth,

iii. adaptive (or tail-weighted) kernel estimates (Worton, 1989) using

reference bandwidth (=1),

iv. adaptive (or tail-weighted) kernel estimates using LSCV

bandwidth, and

v. harmonic mean estimates (Dixon and Chapman, 1980).

Unlike for MCP estimates, it is to be noted for kernel and harmonic mean

estimates, highly-autocorrelated radio locations are not desirable as these methods

were originally devised to investigate habitat selection based on the utilisation

distribution within the home-range (Seaman and Powell, 1996). In addition, it is generally viewed that autocorrelated locations will cause an underestimation of

home-range size (Swihart and Slade, 1985). Therefore, temporal autocorrelation

has to be investigated first using the Schoener’s ratio (t2/ r2) (Schoener, 1981) on

RANGES VII software, where t2 is the meaned squared distance between

successive observations, and is defined by:

21 m m 2 1 2 1 2 t = ∑ −1 XX tt )( +− ∑ −1 − YY tt )( m t=1 m t=1 where m is the number of pairs of successive observations. The mean squared distance between each observation and the centre of activity is defined as:

n n 2 1 2 1 2 r = ∑ i XX )( +− ∑ i − YY )( n −1 i=1 n −1 i=1 where n is the number of observations and ( X ,Y ) is the arithmetic mean of the observations (Schoener, 1981). While Swihart and Slade (Swihart and Slade,

1985) suggested that radio locations can be considered spatio-temporally independent if they met a randomness criterion by having three consecutive values of Schoener’s index scoring greater than 2, Kenward (2001) notes that animals often move in ways which fail to meet the independence criterion for days and a more realistic value may be closer to 1 than 2. As such, radio locations were deemed to be reasonably independent at the time when three consecutive values of

Schoener’s index exceed 1. The kernel and harmonic mean estimates for home- range were then calculated accordingly using the independent radio locations.

The radio-locations from the tracking regime were subjected to the autocorrelation test and the Schoener’s index obtained was plotted against increasing time interval. Using the criterion of having three consecutive values of the Schoener’s index greater than 1 (Kenward, 2001), reasonably independent radio-locations were obtained at 2-hr intervals for individual MJ9 (see Fig. 8).

Unfortunately, the criterion of having three consecutive values greater than 1 could not be met for the other three pangolins.

However, based on the maximum speeds of the pangolins (see Table 4), it is possible for the pangolins to travel across its home-range within a night and render daily locations reasonably independent (Kenward, 2001). As such, a

22 maximum of one radio-location was taken from each day (i.e. same dataset for investigating the stability of home-range estimates with time) for the computation of the various home-range estimates. Nevertheless, it is to be noted that there are some authors who feel that eliminating autocorrelation also limit the biological significance of the analyses (e.g., de Solla et al., 1999; Blundell et al., 2001; see

Discussion also).

In addition to the calculation of MCP home ranges, the stability of the home range was also assessed by plotting the cumulative MCP home range with increasing number of radio locations. For this, only one location fix per day was used as the series of 15-min interval fixes from radio-tracking sessions may obscure the true nature of the home-range’s stability. In addition, this also allowed the inclusion of radio locations obtained during the acclimatisation and habituating phase to better evaluate the underlying situation. Basically, a plot which has an asymptote (or near-asymptote) towards the later part signifies a stable and near-complete recording of the animal’s home-range while one which is still increasing steeply may signify an unstable or incomplete home-range.

2.5.4 Habitat preference.

It is to be noted that autocorrelation is not an issue for selection studies if the technique uses the individual radio-tagged animal as the source of replication (e.g. compositional analysis and Jacob’s index in this study; Otis and White, 1999).

Compositional analysis (Aebischer et al., 1993) of habitat use by the tagged pangolins was performed using Compos Analysis version 6.2 (Smith,

2005), a Microsoft Excel add-in software. The method is the log-ratio analysis of the composition of available habitat types (e.g., plantation, urban, secondary forest

23 or mangrove) in the study site (i.e. second-order selection; Johnson 1980) and the composition of the radio-locations within the 100% MCP home range of the respective pangolins (i.e. third-order selection; Johnson, 1980) versus the composition of the utilized habitat types. It is to be noted that the radio-locations used in the analysis of third-order habitat selection have a buffer of 20 m around the locations to account for accuracy of the GPS and triangulation process (if any).

Compositional analysis utilizes the number of radio-tracked animals as the sample size, instead of the number of radio locations; this is desirable because the latter involves inflating the number of degrees of freedom and the pooling data across animals is only justifiable if there is no individual variation in the animals’ behaviour (Aebischer et al., 1993). The software will not accept data with fewer cases (or animals) than the number of habitat categories and this condition is fulfilled in this study. In addition, as recommended by Aebischer et al. (1993), an available habitat type was not utilized by an animal (i.e. 0% in the utilized habitat composition) was assigned a small value of 0.01% to aid in the analysis.

In addition, Jacobs’ (1974) preference index was also computed to obtain an absolute preference value for each habitat, using = − −+ rpprprJ ]2)/[()( , where r is the used proportion and p the available proportion. The index ranges from +1 for maximum preference and -1 for maximum avoidance. Statistical significance was obtained comparing alternative hypotheses, where the null hypothesis corresponds with a Jacobs’ index equal to zero (i.e. habitat was used as available), comparing the obtained value with t-distribution.

Besides the quantitative assessment of habitat selection by compositional analysis, the habitat utilized by MJ6 during its reproductive phase was also examined. This is because the habitat requirements of a female pangolin when

24 caring for its young may be very different from the other tagged pangolins which were not in the reproductive phase. In addition, the requirements (if any) during the reproductive phase often have serious implications in affecting the population and should not be neglected in any wildlife management or conservation policies.

When a den utilized by MJ6 was identified, its various characteristics were recorded. These include a description of the den and its opening(s), the diameter- at-breast-height (DBH) of the tree associated with the den, the diameter of the opening and also the number of days the den was used by the pangolin throughout the period.

2.5.5 Prey preference.

The identification of ant species collected was done to genera level under a stereomicroscope and with reference of important taxonomic keys, mainly

(Bolton, 1994) and (Shattuck, 1999). Identification to species level is deemed to be difficult because the identification keys to species is currently very limited and in a constant state of flux (D. Lohman, pers. comms.). However, while there is limited taxonomic reference for termites of the region (e.g., Tho, 1992), expertise and guidance on termite identification was not available to the author throughout the duration of the project. As such, only ants were analysed for prey preference in this study, with the help of David Lohman (National University of Singapore).

Unfortunately, while compositional analysis (Aebischer et al., 1993) could potentially be performed for prey preference studies, it was not possible in this study because the condition that the number of cases (i.e. animals) exceeding the number of categories (i.e. species of ants) was not fulfilled.

25 Instead, Jacob’s indices (1974) were calculated for the various ant subfamily and also for each ant genus using = − + − rpprprJ ]2)/[()( , where r is the proportion of ants consumed by each pangolin and p the availability of the respective ant genus or subfamily as determined from the baits (see above). The index ranges from +1 for maximum preference and -1 for maximum avoidance.

Statistical significance was obtained comparing alternative hypotheses, where the null hypothesis corresponds with a Jacobs’ index equal to zero (i.e. habitat was used as available), comparing the obtained value with t-distribution.

2.5.6 Miscellaneous (data from mainland Singapore).

While most of the fieldwork was performed on Pulau Tekong, there were also attempts to collect additional data from specimens found on mainland Singapore.

These attempts include preliminary radio-tracking performed on individuals found during the start of the project in mid 2005 (see Capture and radio-telemetry above) and also gut content analysis of roadkills found along the expressways throughout the project duration. For the latter, the entire digestive tract was removed from roadkill specimens and then preserved in 75% alcohol. The contents of the stomachs and intestines were then separately taken out, sorted from the debris and identified. However, as the ants and termites within the digestive tracts were disintegrated to a certain extent, there was difficulty identifying the large amount of specimens within the timeframe of the project.

This aspect of gut content analysis will be taken up further with myrmecologists from Harvard University at a later date.

26

CHAPTER 3. RESULTS

A total of 21 Manis javanica were captured, measured and radio-tagged from Jun

2005 to Nov 2006. However, due to the high drop-off rates within the first few weeks (Table 3), only four adult male pangolins were tracked successfully. MJ9 was tracked for six nights, MJ12 for six nights, MJ22 for seven nights and MJ23 for six nights. A female adult M. javanica MJ6 was tagged and later found to have given birth to a young. Limited radio-tracking was performed on MJ6 in fear of

MJ6 abandoning the young because it was observed that she was very wary and was not habituated to our presence after two weeks.

The high drop-off rate of the transmitters was probably due to the pangolins moving through the naturally-dense vegetation in certain parts of the study site. The transmitter packages were likely to have been caught onto by the vegetation before being dislodged from the tail scales on the pangolins and this was supported by the fact that all the dislodged transmitters were retrieved in areas with dense undergrowth. If the transmitter package suffered physical stress and were dislodged due to the burrowing activities of the pangolins, the packages would have been found within sleeping dens instead, as opposed to at the ground level and amongst dense vegetation.

3.1. Body measurements of Sunda Pangolin on Pulau Tekong.

The apparent sex ratio was 1 : 2, in favour of the males, but this biased sex ratio was not significant (Yates’ χ2 = 1.71, d.f. = 1, P > 0.05). In addition, the sexual dimorphism was also apparent in all three aspects of body measurements (HB: t –

27 value = -3.67, P < 0.005; T: t –value = -4.86, P < 0.005; M: t –value = -4.95, P <

0.005).

3.2 Home-range, activity cycle and other spatial-temporal statistics.

From the radio locations logged every 15-min, the speed statistics of the four adult

Manis javanica (i.e. MJ9, MJ12, MJ22 and MJ23) were calculated and tabulated in Table 4. The pangolins were observed to be moving at their lower speeds when they were foraging intensely within a small patch of area and thus not moving much within the 15-min interval. Conversely, they were observed to be traveling at the upper range of speeds towards the end of their daily active periods when they were heading towards a suitable overnight shelter without stopping much to forage.

Activity cycle

Throughout the entire period of camera-trapping at entrances of MJ6’s natal dens, there were 30 days whereby both entry and exit were successfully recorded by the devices. Based on the timings of the images, the activity pattern throughout the day was compiled (Fig. 4). While peak activity levels were during 0300-0600 hrs, there was some activity during the daytime (i.e. 0800-1800 hrs) and this diurnal activity was only recorded in the month of December. The mean daily active period for MJ6 was 127 ± 13 min (mean ± S.E.; n = 30).

From the 25 nights of radio-tracking for the four adult male pangolins, the mean daily active duration was found to be 165 ± 14 min and the mean distance moved per night was 441 ± 62 m. The overall activity period for the individual pangolins and all four pangolins collectively are as presented in Fig. 5 and Fig. 6

28 respectively. It is to be noted that because of the different peak activity by the respective pangolins (Fig. 5), the overall activity period (Fig. 6) seemed relatively uniform throughout the night when the actual daily activity period only spanned for 165 min on average. In addition, the shelters of the adult male pangolins at the start of each tracking session were always the same as the shelters at the end of the tracking of the previous night. Whenever tracking was done during the daylight hours to ascertain whether there is activity, no activity was detected on all occasions.

Home range estimates

With the exception of MJ12, the plot of cumulative MCP home-range of the other three adult male pangolins with increasing number of radio-tracking days (Fig. 7) exhibited relatively stable home-range estimates towards the end of the radio- tracking regime.

On the other hand, for MJ12, the tail-end of the plot was still increasing with a steep gradient from day 12 to day 15 (Fig. 7). This signified either an incomplete radio-tracking (i.e. a sampling flaw) or that the individual was still expanding its home-range (i.e. a natural behaviour by the subject). During radio- tracking MJ12 on day 12, the author heard very loud shuffling noises amongst the ground leaf litter. When arrived at the sight where the noises originate, MJ12 was observed to be facing another larger untagged pangolin head-on and was subsequently being chased away by the untagged pangolin (which was not caught to ascertain its sex). Since sexual dimorphism is likely to be present for Manis javanica (see section 3.1 above) and MJ12 was already a large male, it is most probable that the untagged pangolin which was larger in size to be a male as well.

29 As such, it is almost certainly that MJ12 encountered another male pangolin and both exhibited aggressive behaviour towards each other. However, MJ12 was unable to overpower its opponent and began to move northwards away from its original home-range for the next few days. As a result, this encounter resulted in a steep climb in the home-range estimate of MJ12 (Fig. 7), which could have remained stable at approximately 40 ha (similar to estimates of MJ9 and MJ23) if not for the extraordinary encounter.

The radio-locations from the tracking regime were subjected to the autocorrelation test and the Schoener’s index obtained was plotted against increasing time interval (Fig. 8). Even though the criterion of having three consecutive values greater than 1 could not be met for three of the pangolins, it is possible for pangolins to travel across its home-range with a single night and thus render daily locations reasonably independent (Kenward, 2001). Therefore, a maximum of one radio-location was taken from each day for the computation of the home-range estimates.

The home-range estimates of the four male pangolins and MJ6 by MCP, harmonic means contours and kernel contours are tabulated in Table 5. It is to be noted that only 100% MCP was performed for MJ6 as the radio-locations of MJ6 were not collected systematically according to the radio-tracking regime and thus, were not appropriate for core area analysis. For MJ6, in addition to the three den locations, the limited radio-tracking yielded nine other fixes whereby MJ6 was seen foraging or resting. Most of the nine fixes obtained were interior to the locations of the three dens, suggesting that the dens were at or near the periphery of MJ6’s home range. The location of the 100% MCP home-ranges and locations of capture sites were plotted in Figure 9.

30 When examining the 100% MCP home-range estimates of the four adult male pangolins with their respectively body measurements HB, T and M, it was

2 found that the home-range correlated significantly with the body mass M (R adj =

98.9%, P < 0.005). The regression equation obtained was: home-range (ha) = -

336.2 + 47.94 [M (kg)].

3.3. Habitat preference.

Compositional analysis of adult male Manis javanica

From the compositional analysis, it showed that the habitat content of the home- ranges was significantly different from availability at both the second-order and third-order selection (-N lnλ = 18.93, P < 0.001, d.f. = 3, n = 4; -N lnλ = 21.05, P <

0.001, d.f. = 3, n = 4 respectively), i.e. habitat use by pangolins was non- random.

However, as evident in the simplified matrix (Table 6), the order of preference differed for both levels of habitat selection. For the second-order selection, the order of preference was: secondary forest > urban > plantation > mangrove. A significant difference in habitat usage was only detected between the top-ranking (i.e. secondary forest) and the bottom-ranking (i.e. mangrove).

The habitat type with the lowest ranking in the second-order analysis (i.e. mangrove) was absent from the MCP ranges of 75% of the individuals. Thus, following the example in Aebischer et al. (1993), mangrove was dropped from the third-order selection analysis. This resulted in the order of preference for the third- order selection being: secondary forest > plantation > urban, with no significant difference in usage detected amongst all habitat types (Table 6).

31 Jacob’s index

At the second-order selection, only the secondary forest habitat was selected for

(i.e. a positive Jacob’s index) but this preference was not significant (Table 7).

Conversely, urban, plantation and mangrove was avoided (i.e. negative Jacob’s index); only mangrove was significantly avoided (P < 0.001). The order of preference is secondary forest > plantation > urban > mangrove.

For the analysis of third-order selection, the mangrove habitat was excluded because it was absent from 75% of the MCP home ranges. Similarly, secondary forest was the only habitat type which was preferred (P = 0.190), albeit being below statistical significance. Plantation and urban habitats were both avoided, with urban being avoided at a level that approached statistical significance (P = 0.051). The order of preference is secondary forest > plantation

> urban (Table 7).

3.4 Natal den usage by pregnant and postpartum pangolin Manis javanica MJ6.

After being captured and tagged on 1st Sep 2005, MJ6 and its young were first captured by the camera-trap on 1st Oct 2005. However, due to the ability of the young to move independently (as captured by the camera-trap on 1st Oct), it is speculated that the birth took place sometime in mid-September. Through occasional radio-tracking during the day to ascertain the location of natal dens, a total of three dens were used by MJ6 (see Fig. 10 for the location of the dens) and the characteristics of the dens are as summarized in Table 8. Plates 1, 2 and 3 show the respective dens and their entrances.

32 From 12th Dec 2005 onwards, MJ6 stopped using the known natal dens and was first observed without its young on 5th Jan 2006. This suggests that maternal care by female MJ6 lasted approximately four months.

3.5. Prey preference.

While it was possible to obtain relatively accurate radio-locations of the tagged pangolins from both radio-tracking and triangulation, the investigation of prey preference requires the visual confirmation and physical collection of ant/ termite specimens for subsequent identification and data analysis. As a result, because of the skittish behaviour exhibited by MJ23, close-range radio-tracking was not possible and thus MJ23 was excluded from prey preference analysis.

From the 15 cheese baits and 15 honey baits placed within the home- ranges of MJ9, MJ12 and MJ22, a total of 18 genera of ants (from four subfamilies) were obtained and the composition of the myrmecofauna within each of the tagged pangolin’s 100% MCP home-range is listed in Appendix II.

From 2136 min of observations in 14 nights, the three tagged pangolins were observed to be foraging for 16.38 ± 2.44 (mean ± S.E.) min per night, or

11.3 ± 1.8% (mean ± S.E.) of their diel activity. The mean duration of each foraging bout was also found to be very short, at about 2 min (Table 9).

In addition, the three adult male Manis javanica seemed to be foraging more on ants than termites (Table 10), but this difference was not statistically significant (T = 2.51, P = 0.087, d.f. = 3). A total of 11 genera of ants (from five subfamilies) were observed to be fed on by the three tagged pangolins. The percentage of time spent feeding on the various ant genera is listed in Appendix

III.

33 As the composition of myrmecofauna within the pangolins’ home-ranges and not the entire study site (i.e. whole of Pulau Tekong) was assessed, only third- order selection could be assessed for prey preference (see Discussion). The

Jacob’s index was calculated for the various ant subfamilies (Table 11) and all 22 ant genera (Table 12), whenever possible. However, there were circumstances whereby an ant genus or subfamily is absent in both the foraging data (i.e. not eaten by the pangolins) and also not collected from the baits (i.e. in very small quantity or absent from site). In such cases, Jacob’s index could not be calculated and would be represented by “Nil” (see Tables 11 and 12).

Furthermore, as a result of the small sample size (n = 3), not all ant subfamilies and genera could be examined for statistically significant preference or avoidance. Third-order prey selection at the subfamily level of organisation, only Dolichoderinae was observed to be significantly avoided while the other subfamilies were not preferred or avoided at a significant level. At the genera level of analysis, Philidris spp. and Myrmicaria spp. was found to be significantly avoided while Polyrachis spp. and Anoplolepis gracilipes was found to be preferred. However, there were a number of genera which scored strongly for the

Jacob’s index (i.e. close to +1 or -1) but could not be tested for statistical significance due to the absence of the genus in both the diet or the baits of one or more pangolins (i.e. having at least one “Nil” and thus has a standard deviation of

“N.A.” in Tables 11 and 12). Of particular note is Oecophylla smaragdina which was both strongly preferred (i.e. Jacob’s index of +1 for two of the pangolins), while genera Technomyrmex, Crematogaster, Monomorium, Rhoptromyrmex and

Diacamma were all strongly avoided (i.e. index of -1 for two of the pangolins).

The former was also supported by personal observations that pangolins often

34 expend much energy by climbing up and down a cluster of trees whenever they could smell the presence of Oecophylla smaragdina arboreal nests, until they finally locate and raid the nests.

Unfortunately, due to the difficulty in identifying disintegrated ants and termites from the gut contents of roadkill specimens from mainland Singapore, the additional source of information for prey preference cannot be analysed within the project’s timeframe.

3.6 Predation of Manis javanica by Python reticulatus.

During preliminary radio-telemetry on mainland Singapore, a juvenile Sunda

Pangolin was captured by a member of the public on 3rd July 2005 (time unknown) and then handed over to the Singapore Zoo. It weighed 2.5 kg (head- body length: 37 cm; tail length: 32 cm) and was certified healthy by a veterinarian at the Singapore Zoo. It was then fitted with a radio-transmitter and released at

Sime forest on 4th July 2005 at 1400 hours.

The individual was then tracked for the next 11 days (see Fig. 11 and

Table 13 for map and description of locations respectively) without any actual sighting of the animal. On 8th July 2005, despite having waited the entire night, the transmitter did not shift position. This remained the same for the next six days.

On 14th July 2005 (1720 hours), the signal was traced to within a fallen tree trunk. On peering into this hollow log from one of the openings, a Reticulated

Python (Python reticulatus) was found coiled up inside. The signal from the transmitter coincided with the position of the python.

The snake was extracted from the tree trunk and captured the next morning. It measured 3.0 m long, weighed about 10 kg in body mass and had no

35 visible bulge along the body length. With the radio-receiver, the transmitter was located at about ¾ down the python’s body. The reptile was then euthanized, dissected and the head was deposited at the Raffles Museum of Biodiversity

Research (catalogue number: ZRC.2.6220). Within the gut, intact pangolin scales and claws were present from the reptile’s midlength to the rectum. These were also deposited in the Raffles Museum of Biodiversity Research (catalogue number: ZRC.4.8135). Upon retrieval, it was also noticed that the metal edges of the radio-transmitter showed signs of corrosion.

36 CHAPTER 4. DISCUSSION

This is the first intensive and long-term study performed on the Sunda Pangolin

(Manis javanica), which included the first use of radio-telemetry equipment for this species in its natural environment.

4.1. Body measurements of Sunda Pangolin on Pulau Tekong.

From the body measurements of the 21 M. javanica captured, it was evident that sexual dimorphism is exhibited in this species. This finding was observed by researchers from non-governmental organisation (NGO) who have personal experience with confiscated M. javanica (P. Chea and V.T. Nguyen, pers. comms.). This difference in body measurements was also reported in both general mammal guidebooks (e.g., Stone, 1990; Dickman and Richer, 2001) and also specifically for the Chinese Pangolin, which is more well-studied than the Sunda species (e.g., Fang and Wang, 1980; Heath, 1992a; Heath, 1992b).

A possible explanation for the larger body size of male pangolins is that male Manis javanica may be territorial in behaviour. This suggestion is supported by two observations: 1) the home-range estimate of the adult males (Table 5) correlated positively and significantly to the body-mass; 2) a personal field observation whereby the author witnessed two large pangolins (one of them being tagged male MJ12) exhibiting aggressive behaviour towards each another (see

Results). Thus, there is strong evidence to suggest that the larger body-mass of adult male pangolins might be advantageous during conflicts with other males for either foraging resources or for mates. In view of the ubiquitous presences of ants and termites at the study site, it is most likely that male M. javanica are competing for mates. This explanation is further supported by the report by Fang and Wang

37 (1980) that male Chinese Pangolin M. pentadactyla also exhibits territorial behaviour in order to secure female mates. Unfortunately, there was no evidence for a size hierarchy in intraspecific competition for mates in this study.

Of interesting note is the apparently skewed sex-ratio of Manis javanica on Pulau Tekong (14 males: 7 females), even though it was not significant. This observed sex-ratio could either be the true underlying ratio of the population (i.e. suggesting that the capture method is unbiased), or a result of differing behaviours in male and female pangolins which render different success with finding and catching them.

However, when analysing the composition in the different age classes, the sex-ratio is 1 male: 3 females for juveniles (i.e. ≤ 3.0 kg body mass) and 13 males:

4 females for adults (i.e. > 3.0 kg). This disparity observed in the two age classes suggests that the true sex-ratio may not be skewed in favour of the males. Instead, the greater proportion of adult males captured ties in with the previous hypothesis that adult male Manis javanica are in competition for female pangolins. This is because most male vertebrates have the additional task of seeking out potential mates, and this has the effect of causing an increase in mobility and thus encounter rate. With these in mind, it is most likely that the skewed sex-ratio observed is the result of the bias in capture success for the different sexes.

4.2 Home-range, activity cycle and other spatial-temporal statistics.

Activity cycle

Based on Figures 5 and 6, it is clear that Manis javanica is a nocturnal species – with most, if not all, of its activity during the nighttime. However, it is noteworthy to mention the diurnal activity of female pangolin MJ6 observed in the last month

38 of camera-trapping data (i.e. December 2005; Fig. 4). This shift in activity towards the daylight hours took place during the final periods of den usage and coincided with an increase in activity recorded from MJ6 together with her young.

Prior to December, complete activity records from the camera-traps (i.e. when both exit and entry were recorded) always showed MJ6 alone, with the exception of relocation with her young to other natal dens. Thus, this suggests that the diurnal activity of MJ6 together with her young could signify the last phase of maternal care before the young is weaned.

But other than this disparity, most of the activity of MJ6 was found to be during the night (Fig. 4) while all of the adult males were active exclusively during the night (Fig. 5). In addition, the mean active duration of MJ6 (127 ± 13 min) was found to be similar to that of the adult males (165 ± 14 min) which were radio-tracked. Thus, it can be said that M. javanica is a nocturnal species with a short daily active period of two to three hours.

Home-range

From the plot of accumulative 100% MCP home-range estimates with increasing radio-tracking days (Fig. 7), it seemed that home-range estimates for the adult male Manis javanica may stabilise as early as about 11 days (e.g., for MJ22 and

MJ23), or may only stabilise after 17 days (for MJ9). On the other hand, it was also observed that the home-range estimate for MJ12 was still increasing steeply at the end of its monitoring period (i.e. day 12 to day 15). As mentioned before, this is due to aggressive behaviour amongst adult males and resulted in MJ12 migrating northwards continually after the aggressive encounter on day 12.

Another piece of evidence which supports the notion that reasonably precise

39 estimate of the pangolins’ home-ranges can be obtained in about 11 to 17 days is the observation that it takes about two weeks or less for some of the adult males to re-visit a previous sleeping shelter, after moving through the remaining parts of their home-range. An example was MJ23 which was sleeping within the canopy of an Elaeis guineensis on 8th Nov 2006 and then back at the same site on 15th

Nov 2006.

On the other hand, Heath and Coulson (1997) reported that at least 85 days were required to achieve 90% of the home-range estimate for Manis temminckii at

180 days. Unfortunately, the transmitter package could not stay attached on M. javanica at Pulau Tekong for long periods of time. This might be attributed to the different habitats that the two species reside in (i.e. savannah grassland versus tropical rainforest) and thus posing different challenges for radio-telemetry work.

As a result of this constraint, the sampling regime for each pangolin was restricted to approximately 15 days. In fact, some of the pangolins (e.g., MJ9 and MJ23) had the transmitter package dangling by only one screw before the end of sampling regime and had to be recaptured to refit the transmitter package to achieve the desired sampling duration. However, while there might be a real difference in the number of radio-tracking days required to obtain a reasonably accurate estimate of the home-range for the two species, this can only be investigated with confidence after the issue of transmitter package falling off prematurely can be resolved.

It was observed that there was a significant positive correlation between the home-range estimates and the body mass of the adult male pangolins. This suggests that body mass may be an important factor in the ability of adult male pangolins to compete for mates and perhaps foraging resources. However, it is to be noted that even though MJ12 has the highest body mass of 8.6 kg, its home-

40 range was still increasing fast from day 12 to day 15 because of its encounter with another adult male. Nevertheless, even before the encounter, MJ12 was also possessing the greatest 100% MCP home-range estimate by day 12, at around 36 ha (Fig. 7). Therefore, it is very likely that this trend would still be valid without the extraordinary encounter of MJ12. As a result, the measurement of body mass may serve as a surrogate measure for extrapolating the home-range size of adult males, if the data could be strengthen with a greater sample size.

In addition to the three den locations, the limited radio-tracking yielded nine other fixes whereby MJ6 was seen foraging or resting and the 100% MCP is much smaller than those of larger adult males, with the exception of MJ22 (Table

5). While limited radio-tracking of MJ6 was performed in view of its cautious behaviour during the reproductive stages, this is unlikely to severely underestimate its home range. This is because 78% of the activity (7 out of 9 fixes) recorded throughout the entire period rest within the boundaries of the three dens and the remaining two fixes were only about 35 m away from the outer boundaries set by the three dens. Furthermore, understanding that pangolins forage around at a slow speed and MJ6 was only active for about two hours each night, it is unlikely that its actual home-range would differ greatly from the estimated values. Therefore, the vast difference between the home range size of

MJ6 and other adult males could be due to a limited number of suitable natal dens and also a result of reduced mobility during the reproductive stages (i.e. returning to the same den for extended periods instead of moving with her young to other dens on a regular basis).

Even though it was recognized that independence of the radio-locations was not achieved for most of the adult males (except MJ9, which achieved

41 reasonably independent fixes after two hours; Fig. 8), this was not a major setback to the various analyses. This is because by definition, the concept of home-range involves autocorrelated movements (i.e. the current position is not influenced by its position during past observations; Swihart and Slade, 1985) and strong autocorrelation often results because animals move in a non-random manner

(Swihart and Slade, 1985; de Solla et al., 1999). As a result, several authors are of the view that such independence is not biologically possible (de Solla et al., 1999;

Powell, 2000; Blundell et al., 2001), and destructive subsampling of radio- locations to achieve independence only reduces the biological relevance of home- range estimates. In fact, the use of Schoener’s index to investigate autocorrelation may serve well as a means to identify important behavioural information

(Blundell et al., 2001), and this appears to be the especially so for this study.

Since the mean daily active duration of the pangolins was very short (at approximately 2 ½ hours), it was not possible to obtain radio-locations at intervals greater than this duration. In addition, M. javanica moves at a relatively slow speed when foraging around, and thus resulting in the high level of autocorrelation observed (i.e. Schoener’s index < 1). Therefore, a maximum of one radio-location from the set of daily locations was employed for the estimation of home-ranges to reduce any potential underestimation caused by the autocorrelated locations.

Additional reasoning for this was that it is theoretically possible for the adult male pangolins to be traversing across its home-range with its maximum speed within a single day of activity and thus rendering daily locations reasonably independent. It is to be reiterated that autocorrelation is not a problem for selection studies if the technique uses the individual radio-tagged animal as the source of replication

42 (e.g., compositional analysis and the use of Jacob’s index in this study) (Otis and

White, 1999).

Looking at the position of the home-ranges of the adult male M. javanica

(Fig. 9), there is some overlap between MJ12 and MJ23 (15% of MJ9 and 41% of

MJ23). While this may seem like adult male pangolins do not actively defend their home-range, it is to be noted that the radio-tracking for the two individuals took place at different times of the year – Nov 2005 to Feb 2006 for MJ12 and Sep

2006 to Nov 2006 for MJ23. The real extent of habitat overlap can only be assessed with confidence if the home-ranges were determined around the same timing and all individuals in the area were studied. As a result of this temporal separation, no conclusions could be made about the habitat overlap between individuals. This inability to investigate habitat overlap also stemmed from the difficulty of keeping the transmitter package attached on the tagged pangolins.

Based on the close proximity of capture sites of the 21 pangolins (Fig. 9), it is most likely that if transmitters were able to remain on all tagged individuals, a substantial amount of habitat overlap would be discerned. In addition, given the highly elusive behaviour of pangolins and the fact that new pangolins were still being captured after more than a year of fieldwork (e.g., MJ23 and MJ24; Table

3), it is probable that there are additional pangolins within the study site that were not captured.

In conclusion, it is found that M. javanica is a nocturnal species which has a short activity period (about two to three hours). It is also relatively slow-moving and travels a limited distance when foraging during the night. It is most likely that physiological experiments of this species will reveal a very low-metabolic rate, especially for a mammal that lives in the tropics.

43 4.3. Prey preference.

In the analysis of third-order prey selection at the subfamily level, there was only one subfamily (Dolichoderinae) that was significantly avoided while none turned up as significantly preferred (Table 11). The noticeable lack of prey preference at the subfamily level is most likely due to an averaging effect across the various genera within a subfamily. This is because there is a great deal of diversity in terms of morphology and habits within the subfamily, especially within the bigger ones like Formicinae (Hölldobler and Wilson, 1990). This is apparent from the data in Table 12 (i.e. Jacob’s index at the generic level), whereby within subfamily Formicinae, Anoplolepis (gracilipes) and Polyrachis were significantly preferred while Camponotus was consistently avoided (i.e. negative values of

Jacob’s index). As a result, potential difference in preference for each individual genus may have been masked when analysing the data at the subfamily level, resulting in the lack of prey preference observed.

For third-order prey selection at the generic level, even though the resolution of the analysis is greater, only four genera were significantly selected by the adult pangolins – Philidris spp. and Myrmicaria spp. were found to be significantly avoided while Polyrachis spp. and Anoplolepis gracilipes were found to be preferred (Table 12). This apparent lack of prey selection amongst the 22 ant genera was mainly due to the inability to test for statistical significance (see below).

At both levels of data analysis, there were certain ant genera or subfamily which were absent in both the foraging data (i.e. not eaten by the pangolins) and also not collected from the baits (i.e. in very little quantity or absent from site). In such cases, the Jacob’s index could not be calculated (thus “Nil” in Tables 11 and

44 12); this further reduced the sample size from the maximum possible of n = 3 and resulted in the inability to perform hypothesis-testing of deviation the Jacob’s index from zero (thus “N.A.” in Tables 11 and 12).

While the pangolins may be very thorough when foraging within their home-ranges, the sampling methods of sugar and cheese baits have its setbacks.

This is because it is known that certain genera of ants (e.g., subterranean ants) are less likely to be collected by such baits and there are more appropriate methods of collecting these genera (e.g., soil-core sampling). Thus, it must be acknowledged that the use of honey and cheese baits were not able to achieve complete sampling of the myrmecofauna at the study site. For instance, Polyrachis spp. (subfamily

Formicinae) are normally found within rotting logs and hand-collection is a more efficient way to find Polyrachis. As a result, even though Polyrachis spp. was observed to be foraged by all pangolins, no specimen of Polyrachis was found to be attracted to the baits. This resulted in Polyrachis being a genus which was significantly preferred. If hand-collection was performed, it is most likely that the genus would be encountered and cause a decrease in the Jacob’s index generated.

Having said that, the sampling protocol of only using cheese and honey baits allowed for the critical task of quantifying the relative abundance of the myrmecofauna collected, which was necessary for the calculation of Jacob’s index. This is because the method was deemed to be efficient in rapid assessments of myrmecofauna (A. Tham, pers. comms.) and the sampling effort can be easily standardised by the number of baits, surface area of the baits and also the duration that it was left out before collecting the ants. On the other hand, if a combination of methods was used (e.g., Quadra-protocol; Iwata et al., 2005), there is the

45 problem of quantifying or weighting the effort by the different methods and the relative abundance of ants could not be obtained.

Second-order prey selection was not performed because the relative abundance of ants was only assessed within the home-ranges of the individual pangolins and not the entire study site. The latter would mean that much more time and effort would have to be invested, and would be beyond the scope of this project. In addition, second-order selection was deemed to be of little relevance as well. This is because for ants (and other invertebrates), the micro-habitat is of much greater importance than the general landscape (Hölldobler and Wilson,

1990). Furthermore, certain rare genera may only be present in a few of the home- ranges while absent from the rest of the study site. An example of this is Dorylus sp. which was only found at a single subterranean nest in the home-range of MJ22 and nowhere else. In such cases, it is not relevant to analyse for prey preference for the other pangolins since it was not present within their home-ranges to begin with. In fact, this will give a false impression of avoidance of such rare genera, as it is assumed that such ants are present, but not consumed at all. On the other hand, analysing at the second-order level would also mean that the relative abundance of such rare genera would be evened out across the entire study site and may potentially accentuate the preference for such genera in home-ranges that they occur in. Therefore, second-order prey selection was omitted to prevent such confusing and potentially erroneous results.

4.4. Habitat preference.

It is to be noted that for both levels of habitat compositional analysis, non-random habitat use by the four adult male pangolins was observed. However, the only

46 significant selection was evident in the second-order selection, whereby the secondary forest (rank = 1) was preferred over the mangrove (rank = 4; Table 6).

This apparent lack of significant differences between preference/ avoidance of habitat types could either be due to small sample size, or it could be the true underlying trend at the study site. For the former, it is acknowledged that if the log-ratio differences all have the same sign, a small sample size of less than

6 will not be able to produce significant results (Siegel, 1956; Aebischer et al.,

1993). Even though the sample size in this study is less than 6, it was observed that all the log-ratio differences were not of the same sign. Therefore, while it is recognised that a bigger sample size would provide a better analysis of habitat selection, this was not possible due to the high drop-off rates of the transmitters.

Furthermore, from field observations during this study and also the limited knowledge on Manis javanica in scientific literature, it is clear that this species feeds on a wide variety of ants and termites every night (i.e. a diet generalist).

Since ants and termites is a group of organism which is ubiquitous in great quantity in all habitats (Hölldobler and Wilson, 1990), it is unlikely that dietary requirements of Manis javanica would require them to be associated with certain habitat types. In addition, adult male pangolins were often observed to be resting within the canopy of tall trees (> 5 m in height; pers. obs.) and thus do not have fidelity with respect to sleeping sites/ dens. Therefore, it is not surprising to uncover a lack of strong preference or avoidance for certain habitat types.

Nevertheless, both compositional analysis and the use of Jacob’s index revealed a preference of secondary forest over the other habitat types (i.e. Elaeis guineensis plantation and urban), albeit being not statistically significant (Tables 6 and 7). This suggests a greater importance of tropical forests (even though it may

47 not be pristine) over E. guineensis plantations, which spans across large tracts of land in neighbouring countries like Peninsular Malaysia. On the other hand, it also poses doubts over claims that M. javanica could be sighted more easily in E. guineensis plantations and may have been poached from such areas for the wildlife trade (e.g., B.L. Lim, pers. comms.). This view may be derived because of the greater amount of human traffic and also the increased visibility within such plantations, a seemingly greater number of pangolin sightings were observed.

Only with the development of a standardised census protocol that can be deployed efficiently in both natural and artificial landscapes can this issue be addressed with scientific data as its grounding.

While there may be little habitat selection exhibited by adult male M. javanica, this may not be the case for females, especially those which are in the reproductive phase of their life cycles (e.g., MJ6). Throughout the entire duration,

MJ6 was noticed to be utilising dens which offered good concealment and also shelter from the elements. This is in contrast to tagged adult male pangolins which often rested within the canopy-level branches of tall trees (pers. obs.). Another differing behaviour of MJ6 from adult male pangolins is the use of the dens for extended period of time before shifting to the next. While repeated use of sleeping sites was also observed for adult tagged males, the sites were only used for a consecutive period of one or two days (pers. obs.). This clearly demonstrates that female pangolin MJ6 had a high level of den fidelity for extended periods during its reproductive stages. Unfortunately, gathering of data on den usage after the reproductive stages was not possible because of the severed antenna.

The strict use of hollows of big trees (> 50 cm DBH) as natal dens by female MJ6 suggests that M. javanica might require reasonably mature forest to

48 locate and utilise suitable den sites during the reproductive stages. This strongly suggests that female pangolins during their reproductive phases may have very different habitat requirements as compared to other solitary pangolins (regardless of sex). In addition, the continued survival of a species is largely dependent on successful reproduction for replacement and population growth. However, with the present rate of habitat degradation in Southeast Asia, the number of suitable natal dens might be reduced with the decrease in mature forests and this will prove to be a limitation for the population sustainability.

4.5 Reproductive biology of MJ6.

By comparing the body measurements of MJ6 to that of similar-sized female pangolins (Table 3), it is most likely that MJ6 was pregnant at the time of capture, thus explaining the big difference in body mass observed with other females of comparable sizes. While there was no direct observation for the birth of the young pangolin, it is speculated that the birth took place sometime within 8-17

September 2005. This is because it is highly probable that pangolins will take refuge in a safer location (e.g., tree hollow; Den A), as opposed to a clump of tall grasses (e.g., on 7th September), when they are giving birth and providing maternal care for their young. As such, the birth might have occurred on one of the nights when MJ6 did not exit the den (i.e. 8th, 9th, 13th or 17th September).

Finally, the fact that the young was able to move independently on 1st October (as recorded by the camera-trap) suggests that the young might have been a few weeks old then. Unfortunately, the gestation period cannot be determined in this study; Payne and Francis (1998) speculated this to be fairly short at 2 to 3 months but they did not provide the basis for this figure.

49 Based on the first image of the young pangolin on 1st October, it was estimated to be around 30 to 35 cm in total length. Although there has not been any published data on the body measurements of Manis javanica neonates, the estimated body length compares well with the data on other pangolin species

(Table 14). On 3rd November, the young pangolin was observed to be slightly longer than the tail length of MJ6 (i.e. 43 cm; see Plate 4). This observation lends support to Prater’s (1965) example whereby a baby pangolin doubled its mass in four months and his view that growth in young pangolins is rapid. In addition, from this study and the limited reported dates of birth of the other pangolin species (Table 14), it seems that pangolins in general may be reproducing all year round.

Unfortunately, due to much-reduced range of the transmitter after 3rd

November, attempts to locate MJ6 for observations on maternal behaviour were mostly unsuccessful. Nevertheless, the observations on 5th January 2006 most likely signify that maternal care by MJ6 would have ended by then. This is supported by the increasing number of events triggered by the young pangolin throughout the period, which clearly demonstrates its increased activity and ability to move around independently by mid December. This can be indirect evidence for the readiness of the young pangolin to be independent. As a result, this suggests that the entire duration of maternal care is approximately 3 to 4 months

(mid-September till mid-December/ early-January) and is in accordance with the speculation of approximately 3 months noted by Payne and Francis (1998). On the other hand, a captive female Chinese Pangolin M. pentadactyla at Taipei Zoo is reported to be exhibiting maternal care as long as 6 months (S.-F. Chen, pers. comms.).

50 With a potentially low rate of fecundity (i.e. one young per birth and a moderate period of maternal care), pangolins are prone to effects of over- harvesting. In fact, of the four Asiatic pangolins, the Sunda pangolin appears to the species most threatened by the trade (Bräutigam et al., 1994). Within its natural range, seizures of illegal shipment in M. javanica with numbers up to

1,200 in one single load happen regularly (Abas, 2002; Simon, 2004). This is made worse by the fact that pangolins do not survive well in captivity (Wilson,

1994), making animal rescue and rehabilitation before release back into the wild an arduous task.

It is to be reiterated that the strict use of hollows of big trees (> 50 cm

DBH) as natal dens by female MJ6 suggests that female M. javanica during the reproductive stages might require reasonably mature forest to locate suitable den sites. (See Habitat preference above.)

4.6 Predators of Manis javanica.

Pythons either lie in wait or actively search for prey (Pope, 1961) and they are not known to scavenge under natural conditions. It is therefore assumed that the pangolin was captured and killed by the snake. This is supported by the observation that the pangolin was in good health and very active when it was released.

It is not known when or where the pangolin was attacked. From the daily location data, there is an apparent lack of movement between the 7th and the 11th of July. In addition, the pangolin was not observed leaving its hiding place throughout the night of 8th July (from 2000 hrs onwards) and early morning of 9th

July (until 0700 hrs). Therefore, it is highly likely that the attack took place before

51 the night of 8th July. In addition, the posterior location of the pangolin scales and transmitter within the gut also support this assumption that the pangolin had been consumed and was in an advanced stage of digestion.

However, it must be emphasised that there has not been any detailed study on the daily activity pattern of the Sunda Pangolin. As such, it might be natural for this animal to stay within the shelter throughout the night and to return to the same shelter for consecutive nights, thus explaining the pattern observed for the period of 7th to 11th of July. While the latter behaviour has been documented for three relocated African Cape Pangolin (Manis temminckii), none stayed in their shelters throughout the entire night (Heath and Coulson, 1997; J. Swart, pers. comms.).

This further supports the suggestion that the pangolin was consumed before the night of 8th July.

It is well-known that pangolins are non-aggressive and often curl up into a ball with the head tucked between the limbs and under the tail when faced with potential threat (see Lekagul and McNeely, 1988). The juvenile might be an easy meal for this medium-sized python, considering the fact that pythons have been recorded to consume larger animals, such as adult Sulawesi pig (Sus celebensis)

(Auliya, 2003) and even the sun bear (Helarctos malayanus) (Fredriksson, 2005).

In addition, given that both pangolins and pythons can be arboreal in habits (pers. obs.) and utilize natural crevices (e.g., tree hollows and underground burrows) extensively (pers. obs. for M. javanica), there is much overlap in the microhabitat utilization and thus a high chance of encountering for the two species. However, it is unclear whether pythons are able to coil around and constrict a curled-up pangolin, especially within a narrow space like a tree hollow. Since pythons in general often wait in ambush at a spot (Slip and Shine, 1998), it is more likely that

52 the attack took place in the open, when the pangolin moved pass the ambushing python.

Based on the stomach contents of 1,070 Reticulated Pythons in Sumatra,

229 contained identifiable remains and six adult pythons held remains of M. javanica (Shine et al., 1998). The observed cases of stomach containing pangolins is less than that of Rice Field Rat Rattus argentiventer (148 cases), Long-tailed

Giant Rat Leopoldamys sabanus (31 cases), Silvered Leaf Monkeys Semopithecus cristatus (11 cases) and domestic chicken Gallus gallus (8 cases) (Shine et al.,

1998). Even though Rahm (1990) listed the python as one of the enemies of pangolins alongside humans and the leopard, no reference was cited to give an indication of the frequency of such occurrences. Perhaps due to limited field studies on the armadillos or anacondas, there has not been any (English language) published accounts of anacondas preying on armadillos, even though it is likely that armadillos may be a prey items for the constrictor (J. Loughry, pers. comms.).

This recorded incident of predation is only possible because the pangolin was fitted with a radio-transmitter. However, due to lack of telemetry studies on

Sunda Pangolins and an equal lack of prey studies of wild reticulated pythons, it is unclear whether python predation on pangolin is a common event.

53 CHAPTER 5. OVERALL CONCLUSION AND RECOMMENDATIONS

5.1 Challenges for future pangolin research.

The present study represents the first intensive and long-term study performed on the Sunda Pangolin (Manis javanica) in Singapore and Malaysia, and likely the region. It also involves the use of radio-telemetry equipment for this species in its natural environment, the first such application regionally.

Radio-telemetry

While efforts were made throughout the entire duration to better streamline the transmitter package (e.g., changing to a slimmer Holohil RI-2A transmitter), the drop-off rates remained unfavourably high (84%) and remained a serious impediment to long-term radio-telemetry studies of M. javanica in their natural environment. One possible solution is to use implant radio-transmitters on pangolins, but this would mean that there is a requirement for a trained veterinarian to be present for the procedure. After the implant, the subjects need to be kept in captivity under observation for a period of time to ensure that there are no secondary infections or rejection of the transmitter (i.e. to ensure the safety of the animals). Furthermore, after the completion of the radio-tracking regime, the individual has to be captured for the removal of the transmitter and again retained in captive conditions to ensure its health after the procedure. Lastly, veterinarians who have performed post-mortems on dead captive pangolins often find stomach ulcers, an indication of stress when kept in captive conditions (L. Clark and J.

Chin, pers. comms.). All these requirements rest on the assumption that pangolins can recover from such operations with little side-effects and be maintained in

54 captivity for extended periods of time with confidence, which has not been proven to be the case as of now.

Another method of transmitter attachment is via a body harness. While this method will have a much greater success of the transmitter package remaining on the subject, it was rejected because of the potential fatal effects on the animals.

This is because the Sunda Pangolin resides in the tropical rainforests and moves through the dense undergrowth. However, the manpower constraint of this project meant that not all tagged pangolins can be monitored each day. As a result, should the harness be caught onto a branch or vine, the subject may not be able to struggle free and may perish if not rescued in time. One way to avoid is to have a weak link in the harness setup, such that the link will break once a sufficiently strong force acts on it. But in such a setup, the chances of the transmitter package dropping off will in fact be higher than via scale attachments. This is because the harness would be have to be over the dorsal surface of the pangolin and will have a higher chance of being caught on by the vegetation when moving through the undergrowth, as compared to the small RI-2A attached at the base of the tail.

It is hoped that improvements and developments in the radio-telemetry technology in the near future may help to alleviate this problem. Even with this limitation, the data collected from this study will still contribute significantly towards the knowledge on the life history and ecology of the M. javanica.

Census

Another major challenge to pangolin research is the current inability to effectively census for pangolins in their wild habitats. This is mainly because the pangolins were observed to be extremely wary of extraordinary sounds and scent in the

55 vicinity. When alerted, pangolins would initially freeze their movement to avoid generating any noise when moving through the undergrowth. In this state, the earthly colour and non-reflective surface of the scales provide excellent camouflage in the natural environment (pers. obs.). Should the pangolin still feel threatened, it will then proceed to climb up a neighbouring tree and hide amongst the canopy, rendering a posteriori detection almost impossible. Thus, it is apparent that it is difficult to trek in the forest environment with little noise generated and find pangolins at the same time.

With the above-mentioned in mind, the complex issue of census can be better appreciated, since it is obvious that the most direct way of performing a census is to detect and count the subjects of interest with confidence. As a result, the highly secretive behaviour of the Sunda Pangolin may prove to be an obstacle for researchers attempting to perform a direct census of them.

Besides the method of direct census, a non-invasive method is the deployment of infrared-triggered camera-traps and using mark-and-recapture analysis to estimate their numbers. However, the latter requires reliable identification of individuals from the images obtained. While this is likely to be possible through the scale patterns on the pangolins, it has not been proven till date. In addition, even though the technology for such devices are improving with time, the total cost of a reasonable setup with sufficient camera-trap units to estimate the population with precision may prove to be an obstacle for most researchers. Having said that, if the issues of reliable identification of individuals and the setup cost could be resolved, there is still the question of how often are pangolins captured on camera-traps. A preliminary estimate of the capture success of pangolins on camera-traps could be inferred from the results of camera-

56 trapping studies. For instance, from 1,632 trap nights in Sarawak, Giman et al.

(2007) obtained 94 images of mammals and only one photograph of M. javanica was taken. Similarly, Mohd. Azlan and Engkamat (2006) only obtained five images of M. javanica, from a total of 218 mammal images. Therefore, it is unlikely that camera-trapping will prove to be a useful method for the census of pangolins in their wild habitat.

Assessment of population numbers can also be performed using indirect signs, e.g., faecal materials, scratch marks and pugmarks. However, in the tropical rainforest setting, it is well-know that such signs are notoriously difficult to locate.

This is made worse by the fact that the faecal materials of the pangolins are not very distinctive and pangolins do not scratch on substrates to mark their home- ranges. Lastly, most field biologists have commented that they have seen pugmarks of pangolins very rarely, if at all (e.g., W. Duckworth, pers. comms.).

Having presented the various challenges in the assessment of their numbers, the census of pangolins in their natural habitats will be an important aspect of our knowledge about this species. However, it is to be noted that even though there exists multitude of census techniques for mammals, most of them are mathematical models and thus require assumptions which may be difficult, or at times impossible, to fulfill in the field (Seber, 1982). Therefore, it is important for workers to be aware of these limitations and plan the methodology with care.

5.2 Priorities for conservation of pangolin species.

In view of the severe hunting pressure on the Asiatic pangolin species – especially the Sunda Pangolin (Bräutigam et al., 1994) – the following research priorities are recommended for the conservation of this species.

57 Wild diet studies

A thorough understanding of the prey preference of M. javanica can aid in the explanation of results of habitat preference studies. This is because it is recognised that the Formicidae are very specialised and specific with regards to the microhabitats that they reside in. Therefore, with the knowledge of the microhabitats and distribution of the preferred ant genera, the prey preference can act as an indirect course to infer the habitat preference of the pangolins.

Having said that, it is to be noted that pangolins have been observed to be foraging on 11 ant genera in this study and are generalists with regards to their diet. Given the ubiquitous presence of ants and termites in both natural and artificial landscape, it may mean that pangolins are very adaptable animals and the use of prey preference to infer about their habitat preference may not be very applicable. This is further supported by the observation that a few ant species that were preferentially preyed upon (e.g., Anoplolepis gracilipes and Oecophylla smaragdina) were “tramp” species that can be easily found in urban areas. Thus more studies on their prey preference are required to explore the underlying relationship with the important issue of habitat preference.

Another increasingly important aspect for pangolin conservation is to develop the protocol to sustain wild pangolins in captive conditions. This is due to the fact that large numbers of pangolins are often confiscated by the various national authorities in Southeast Asia and the rescued pangolins are often in very bad state of health – either dehydrated or wounded (L. Clark, pers. comms.).

However, the current inability to maintain these rescued individuals until suitable for release is a great impediment towards their conservation. Therefore, it is

58 recommended that there will be a greater emphasis for studies on the diet composition of wild M. javanica.

From this study, the few preferred ant species (e.g., A. gracilipes and O. smaragdina) are known to be common in artificial landscapes. In fact, there exist many papers on the biology and ecology of O. smaragdina (e.g., Hölldobler,

1983; Way and Khoo, 1991; Peng et al., 1998; Chapuisat and Keller, 2002). Being a relatively well-studied common species, there is definitely a greater chance of success of maintaining O. smaragdina colonies at a scale large enough to sustain captive pangolins for the above-mentioned purpose.

Habitat requirements

Even though there was no strong preference for a particular habitat type by the adult males based on the results of this study, it is most unlikely that natural habitat destruction and conversion will not have an impact on the population size.

This is because this behaviour might only be exhibited by the solitary adult males.

The strict use of hollows of big trees (> 50 cm DBH) as natal dens by female MJ6 suggests that M. javanica might require reasonably mature forest to locate and utilise suitable den sites during the reproductive stages. However, with the present rate of habitat degradation in Southeast Asia, the number of suitable natal dens might be reduced with the decrease in mature forests and this will prove to be a severe limitation for population sustainability of pangolins.

Census

Many biological studies require estimates of the population size or rate of population change over time and this ecological censusing is important because it

59 can answer many questions (especially those pertaining to conservation biology), e.g., the habitat preference of a species and whether habitat management has been a success. Similarly for the Sunda Pangolin, it is imperative that a standardised census technique can be devised and employed to obtain reasonably precise estimates of their numbers.

(See above for more discussion.)

DNA microsatellite markers characterisation

With the large number of seizures of illegal consignments of pangolins by the neighbouring countries, it is often difficult (if not impossible) to find out the country of origin of the animals and modern molecular techniques may prove to provide a useful application for this issue. Microsatellite markers are useful for assessing population-level genetic diversity and have become an increasingly important genetic tool to assist in conservation decisions in endangered species.

While such markers have been characterised for M. javanica, M. pentadactyla and

M. tricuspis, and also proven to show high variability endemic to populations in

Africa and Asia (Luo et al., 2007), greater resolution is required for the identification of source for confiscated pangolins and possible repatriation to the country of origin. In addition, if sufficient samples from the various countries could be analysed, the data could be pooled together to examine the genetic- makeup differences at the population-level and thus be used to investigate the phylogenetics of Pholidota.

60 5.3 Status of Manis javanica in Singapore.

In view of the large number of records over the past two decades (a total of 54 records), it is certain that M. javanica is widely distributed throughout Singapore, with the stronghold being the forested areas of the Central Catchment Nature

Reserves, Western Catchment Reserves and Pulau Tekong. Nevertheless, there were also a number of sightings at the nature reserve fringes and outside (e.g.,

Bukit Panjang, Old Jurong Road and Woodlands). Even though both the

Singapore Red Data Book (Ng and Wee, 1994) and this current study were not able to provide an estimate for the population size, it is most likely that the current state of the M. javanica is quite healthy and should be sustainable in the near future, if the current natural habitats are preserved.

However, one outstanding concern is the substantial number of roadkills

(15 records) and sightings of pangolins crossing roads (13 records). This has the implication that the pangolins are not very acute of their surroundings and may wander onto roads or expressways at times. Ng and Wee (1994) also proposed the building of wildlife tunnels under the Bukit Timah Expressway (BKE) to connect the Bukit Timah Nature Reserve and the Central Catchment Nature Reserves.

With the considerable sightings along roads, it would seem that wildlife corridors

(especially under the BKE) will be an appropriate measure to implement to help ensure the long-term survival of this species in Singapore. Nevertheless, it is to be noted that few studies have demonstrated the effectiveness of such wildlife corridors (e.g., McDonald and St. Clair, 2004; Ng et al., 2004; Chetkiewicz et al.,

2006) and actual field data supporting the concept is still considered sparse.

(See Introduction for more information.)

61 5.4 Conclusion

From the results of this study, it is clear that M. javanica is a nocturnal myrmecophage that feeds on a variety of ant and termite species. While it mainly forages at the ground-level, it is also very apt in climbing, and will often climb trees to raid ant nests (especially that of Oecophylla smaragdina) and to escape from disturbance.

Even though there was an apparent lack of habitat and prey preference, this observation could be due to the small sample size. Nevertheless, this could also be the true underlying trend – i.e., M. javanica are very adaptable animals and can survive in most habitats (even degraded and semi-natural habitats). However, an exception to this generalisation could be females during their reproductive phases, whereby they require natal dens associated with trees greater than 50 cm

DBH for the rearing of the young. This would mean that female pangolins with young could be restricted to mature forests and the latter will be an important component for the completion of their life cycle (i.e. an important habitat requirement).

62

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72 TABLES

Table 1. A summary of information on the eight pangolin species of the Old World.

Common name Scientific name Body length Mass Habitat Behaviour

African species

Giant Pangolin Manis gigantea HB 75-100 cm, 20-35 kg Forest mosaics and grasslands Terrestrial, nocturnal T 50-70 cm Ground Pangolin M. temminckii HB 34-61 cm, 7-18 kg Woodlands, savannahs and Terrestrial, mainly T 31-50 cm grasslands nocturnal

Long-tailed Pangolin M. tetradactyla HB 30-40 cm, 2.2-3.2 kg Riverine and swamp forests Arboreal, diurnal T 55-80 cm

Tree Pangolin M. tricuspis HB 25-43 cm, 1.6-3.0 kg Lowland rainforests Arboreal/ terrestrial, T 35-62 cm nocturnal

Asian species

Chinese Pangolin M. pentadactyla HB 40-58 cm, 4-9 kg Montane, submontane and mixed Mainly terrestrial, T 30-38 cm deciduous forests nocturnal

Indian Pangolin M. crassicaudata HB 45-75 cm, 8-17 kg Tropical rainforests, subtropical Mainly terrestrial, T 33-45 cm thorn forests and plains nocturnal

Palawan Pangolin M. culionensis ?? ?? ?? Mainly terrestrial, nocturnal

Sunda Pangolin M. javanica HB 40-65 cm, 4.5-14 kg Lowland tropical rainforests and Mainly terrestrial, T 35-57 cm plantations nocturnal

73 Table 2. Known uses and supposed benefits of pangolin parts.

Parts Uses Meat Consumption For subsistence For good health

Scales Purported medicinal To cure toxicosis, inflammation, properties rheumatic pain, and soothing aches and pains As aphrodisiac Skins Stuffed animal As ornament

74 Table 3. Body measurements (HB – head-body length; T – tail length, in cm and M – body mass in kg) and sex of the Manis javanica captured on Pulau Tekong.

Date End of ID Sex captured monitoring Reason HB T M

MJ1 F 25-Jun-05 23-Jul-05 Transmitter dislodged 45 40 5.6 MJ5 M 1-Sep-05 7-Sep-05 Transmitter dislodged 29 25 2.4 MJ6 F 2-Sep-05 21-May-06 With young; transmitter 43 43 6.1 dislodged MJ7 F 2-Sep-05 25-Sep-05 Transmitter dislodged 43 38 4.7 MJ8 M 10-Sep-05 3-Oct-05 Transmitter dislodged 53 55 8.7 MJ9 M 20-Oct-05 4-Jan-06 Tracking completed 59 59 9.0 MJ10 F 29-Oct-05 7-Nov-06 Transmitter dislodged 37 33 2.5 MJ11 F 24-Nov- N.A. Not tagged, scales too 36 34 2.0 05 thin and soft MJ12 M 29-Nov- 28-Feb-06 Tracking completed 62 56 8.6 05 MJ13 M 15-Dec-05 5-Jan-06 Transmitter dislodged 47 54 6.8 MJ14 M 29-Feb-06 8-Apr-06 Transmitter dislodged 50 53 8.5 MJ15 M 29-Feb-06 12-Mar-06 Transmitter dislodged 51 50 8.0 MJ16 M 11-Mar-06 28-Mar-06 Transmitter dislodged 51 52 9.5 MJ17 M 27-May- 12-Jun-06 Transmitter dislodged 47 47 7.0 06 MJ18 F 31-May- 15-Jun-06 Transmitter dislodged 40 41 3.0 06 MJ19 M 8-Jun-06 2-Jul-06 Transmitter dislodged 56 57 8.7 MJ20 M 8-Aug-06 18-Aug-06 Transmitter dislodged 47 57 8.3 MJ21 F 15-Aug- 4-Sep-06 Transmitter dislodged 45 43 4.5 06 MJ22 M 12-Sep-06 27-Sep-06 Tracking completed 47 54 7.2 MJ23 M 30-Sep-06 15-Nov-06 Tracking completed 52 54 7.7 MJ24 M 15-Nov- N.A. Not tagged, scales too 55 55 9.0 06 worn off

75 Table 4. Speed statistics (m/ hr) of adult male Manis javanica on Pulau Tekong.

ID Mean S.E. Maximum Minimum MJ9 197.5 14.3 496.8 33.0 MJ12 283.3 23.3 871.6 14.4 MJ22 115.8 13.0 555.5 8.9 MJ23 119.2 15.1 784.9 4.0

76 Table 5. Home-range estimates (ha) of adult Manis javanica using minimum-convex polygon (MCP), harmonic mean and kernel methods, with the various parameters stated and using non-autocorrelated radio locations (see text for more details).

Home-range estimation method MJ6 MJ9 MJ12 MJ22 MJ23

MCP 100% 7.0 44.5 76.6 8.2 36.0 95%, harmonic mean centre N.A. 37.3 54.9 7.4 34.7 95%, arithmetic mean centre N.A. 37.3 54.9 7.4 34.7 95%, recalculated arithmetic N.A. 37.3 54.9 7.4 34.7 50%, harmonic mean centre N.A. 9.0 7.3 0.9 9.8 50%, arithmetic mean centre N.A. 9.0 7.3 0.9 9.8 50%, recalculated arithmetic N.A. 5.5 7.4 0.5 9.1

Harmonic mean contours 95% N.A. 37.3 70.5 3.7 47.3 50% N.A. 8.9 8.9 1.2 5.2

Fixed kernel contours 95%, fixed bandwidth N.A. 57.9 130.7 11.0 48.6 95%, LSCV N.A. 53.3 137.6 7.1 53.3 50%, fixed bandwidth N.A. 20.9 46.2 5.0 14.8 50%, LSCV N.A. 19.7 49.5 2.3 22.1

Adaptive kernel contours 95%, fixed bandwidth N.A. 68.2 167.3 14.2 61.6 95%, LSCV N.A. 73.9 188.9 18.5 61.6 50%, fixed bandwidth N.A. 21.6 43.9 5.5 14.3 50%, LSCV N.A. 24.0 57.4 6.7 14.3

77

Table 6. Simplified ranking matrix for Manis javanica based on a) comparing proportional habitat use within minimum convex polygon (MCP) home ranges with proportions of total available habitat types, and b) comparing proportion of radio locations (with 20- m radius buffer) for each animal in each habitat type with the proportions of each habitat types within the animal’s MCP range (see text for more details). “+” implies the habitat type of the r was preferred to the habitat type in the row and “-” implies the reverse; a triple sign represents significant deviation from random at P < 0.05.

a) MCP home range vs. total study area (second-order selection) Habitat type Secondary Habitat type Urban Plantation Mangrove Rank forest Secondary forest + + + (+++) 1 Urban - + + 2 Plantation - - + 3 Mangrove - (---) - - 4

b) Buffered radio locations vs. MCP home range (third-order selection)

Habitat type Secondary Habitat type Urban Plantation Rank forest Secondary forest + + 1 Urban - - 3 Plantation - + 2

78 Table 7. Jacob’s index for each habitat used by pangolins on Pulau Tekong at second- order and third-order selection.

Second-order selection Habitat type Mean S.E. n P-value Rank Mangrove -0.977 0.223 4 < 0.001 4 Plantation -0.166 0.497 4 0.761 2 Secondary forest 0.571 0.285 4 0.139 1 Urban -0.232 0.437 4 0.631 3

Third-order selection Habitat type Mean S.E. n P-value Rank Plantation -0.034 0.202 2 0.893 2 Secondary forest 0.243 0.144 4 0.190 1 Urban -0.773 0.181 3 0.051 3

79 Table 8. Description, measurements and duration of usage of the three dens used by female Manis javanica MJ6 from September to December 2005.

Entrance DBH of Total no. Den Description diameter tree (cm) of days (cm)

A Underground burrow which 95 15 16 leads to tree hollow of dead tree

(standing); one entrance

B Dead tree (fallen), tree hollow; 54 19 33 entrance at base of tree C Live tree (standing), tree hollow; 104 i. 24 24 two entrances; entrances are 1.3 ii. 13 m above ground

80

Table 9. Mean and maximum time (min) spent on feeding by three of the Manis javanica.

MJ9 MJ12 MJ22

Mean duration of a feeding bout (± S.E.) 2.15 (0.52) 2.53 (0.36) 2.18 (0.34) Maximum duration 13 9 10 n 24 34 42

81

Table 10. Percentage of time spent feeding on ants and termites by three of the tagged male Manis javanica.

Ants Termites

MJ9 80.6% 19.4% MJ12 67.4% 32.6% MJ22 53.1% 46.9% Mean (± S.E.) 67.0% (8.0) 32.97% (8.0)

82

Table 11. Jacob’s index of the ant subfamily consumed by adult male Manis javanica on Pulau Tekong. Nil = cannot be calculated because not collected and not consumed; N.A. = not applicable; * implies P < 0.05.

Jacob’s index Subfamily P-value MJ9 MJ12 MJ22 Mean S.D. Dolichoderinae -1.000 -1.000 -0.459 -0.820 0.313 0.045 * Dorylinae Nil Nil 1.000 1.000 N.A. N.A. Formicinae 0.884 0.627 0.098 0.536 0.401 0.146 Myrmicinae -1.000 -0.155 -0.954 -0.703 0.475 0.124 Ponerinae 0.336 -1.000 -0.721 -0.462 0.705 0.374

83 Table 12. Jacob’s index of the ant genera consumed by adult male Manis javanica on Pulau Tekong. Nil = cannot be calculated because not collected and not consumed; N.A. = not applicable; * implies P < 0.05.

Jacob’s index Subfamily Genus P-value MJ9 MJ12 MJ22 Mean S.D. Dolichoderinae Dolichoderus -1.000 Nil Nil -1.000 N.A. N.A. Dolichoderinae Philidris -1.000 -1.000 -0.699 -0.900 0.100 0.012 * Dolichoderinae Technomyrmex -1.000 -1.000 Nil -1.000 0.000 N.A. Dolichoderinae Papyrius Nil Nil 1.000 1.000 N.A. N.A. Dorylinae Dorylus Nil Nil 1.000 1.000 N.A. N.A. Formicinae Paratrechina -1.000 0.505 0.081 -0.138 0.776 0.787 Formicinae Anoplolepis (gracilipes) 1.000 0.806 1.000 0.935 0.112 0.005 * Formicinae Camponotus -0.379 -1.000 -0.506 -0.628 0.328 0.080 Formicinae Oecophylla (smaragdina) 1.000 1.000 Nil 1.000 0.000 N.A. Formicinae Polyrachis 1.000 1.000 1.000 1.000 0.000 < 0.005 * Myrmicinae Crematogaster -1.000 Nil -1.000 -1.000 0.000 N.A. Myrmicinae Monomorium -1.000 -1.000 Nil -1.000 0.000 N.A. Myrmicinae Myrmicaria -1.000 -1.000 -1.000 -1.000 0.000 < 0.005 * Myrmicinae Pheidole Nil 0.326 -1.000 -0.337 0.938 N.A. Myrmicinae Pheidologeton -1.000 Nil Nil -1.000 N.A. N.A. Myrmicinae Rhoptromyrmex -1.000 -1.000 Nil -1.000 0.000 N.A. Myrmicinae Tetramorium Nil -1.000 Nil -1.000 N.A. N.A. Myrmicinae Lophomyrmex Nil Nil -1.000 -1.000 N.A. N.A. Myrmicinae Paratopula Nil Nil 1.000 1.000 N.A. N.A. Ponerinae Diacamma Nil -1.000 -1.000 -1.000 0.000 N.A. Ponerinae Odontomachus 0.336 -1.000 -0.566 -0.410 0.681 0.407 Ponerinae Odontoponera Nil -1.000 Nil -1.000 N.A. N.A.

84 Table 13. Date of the locations of radio-transmitter in Figure 11, distance from previous location and description of location.

Distance (m) Location Date from previous Description Comments location Underground; base of 1 4 Jul - Date of release tree 5 and Among dense 2 77 - 6 Jul vegetation Within hollow log Monitored throughout (Shorea sp., DBH 68 the night of 8 Jul but 7-11 3 110 cm); across a small no shift in transmitter Jul stream from previous location; (did not location track on 12 Jul) Within hollow log Visual confirmation 4 14 Jul 252 (Shorea sp., DBH 89 of python cm)

85 Table 14. Reported date of birth and body measurements of neonate Manis spp..

Pangolin species Date of birth Length and mass Reference Manis crassicaudata 6 Jan 0.435 m at 3 days old (Ogilvie and Bridgewater, 1967) ? Jul - (Prater, 1965) 17 Nov 235 g and 0.3 m (Acharjyo and Misra, 1972) ? Nov - (Asdell, 1946) Jan-Mar - (Asdell, 1946; Prater, 1965)

Manis pentadactyla 5 Feb 92 g, 0.2 m (Heath and Vanderlip, 1988) ? Aug - (Ogilvie and Bridgewater, 1967) 14 Nov 93 g, 0.21 m (Heath and Vanderlip, 1988) 25 Dec 200 g at 16 days old (Masui, 1967) Nov-Feb - (Fang and Wang, 1980; Fang, 1981) Manis tricuspis 3 Nov 100 g at birth (Menzies, 1967)

86 FIGURES

Figure 1. Location of all known records of Manis javanica sightings and roadkills in Singapore, from 1985-2007.

87

Figure 2. Map of Pulau Tekong, relative to mainland Singapore. The shaded grey shaded area is the only reservoir on the island and the cross-shaded patches are the built-up areas. The remainder of the island is covered with the vegetation.

88

Figure 3. Radio-telemetry error polygons under extreme conditions of maximum distance from transmitter (i.e. 200 m) and maximum bearing difference from optimal angle (i.e. 60° and 120°).

89

Figure 4. Diel activity pattern of female Manis javanica MJ6 (mean ± S.E.), based on 30 days of camera-trapping data from 8th September to 12th December 2005.

90

Figure 5. Diel activity pattern of each of the four adult male Manis javanica. No activity was recorded between 0800 hrs to 2000 hrs.

91

Figure 6. Diel activity pattern of adult male Manis javanica (n = 4), with S.E. as error bars. No activity was recorded between 0800 hrs to 2000 hrs.

92

Figure 7. Accumulative 100% minimum-convex polygon home-range estimates of individual adult male Manis javanica with increasing number of radio-tracking days.

93 Schoeners index, green = TTI 1, orange = TTI 2 8

6

4

2

0 0.08 0.7 1 2 2 3 Time interval(hrs)

Figure 8. Autocorrelation plot of Schoener’s index with time interval of Manis javanica MJ9. Reasonably-independent radio locations were obtained at approximately 2-hr interval (green vertical line), where there are three consecutive values of Schoener’s index greater than 1 (see text for more details).

94

Figure 9. Position and shape of 100% minimum convex polygon home-range of the four adult male Manis javanica (MJ9, MJ12, MJ22 and MJ23) on Pulau Tekong. Location of capture sites of the other pangolins are indicated by crosses.

95

Figure 10. Location of the three natal dens used by female Manis javanica MJ6 (in crosses) and positional points from radio-tracking (in squares).

96

Figure 11. Map of locations of radio-transmitter during the 11 days it was tracked. Dotted lines are streams; solid lines are trails or roads. Refer to Table 13 for date and description of locations.

97 PLATES

Plate 1. Den A and its entrance (as shown by the arrow).

98

Plate 2. Den B and its entrance (top picture), and fallen tree of Den B (bottom).

99

Plate 3. Den C and its two entrances, as shown by the arrows.

100

Plate 4. Image of MJ6 and its young, taken on 3rd November 2005 by infrared- triggered camera-traps positioned facing the den entrance. Note that the young is slightly longer than the tail length of MJ6 (one month after its first record) and also the severed antenna of the radio-transmitter.

101