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Effects of El Niño and large-scale forest fires on the ecology and conservation of Malayan sunbears (Helarctos malayanus) in East Kalimantan, Indonesian Borneo
Fredriksson, G.M.
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Citation for published version (APA):Fredriksson, G. M. (2012). Effects of El Niño and large-scale forest fires on the ecology and conservation ofMalayan sun bears (Helarctos malayanus) in East Kalimantan, Indonesian Borneo.
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Download date: 01 Jan 2020
Effects of El Niño and large-scale forest fi reson the ecology and conservation
of Malayan sun bears(Helarctos malayanus)
in East Kalimantan,Indonesian Borneo
Gabriella Fredriksson
Effects o
f El N
iño
and
forest fi res o
n th
e ecology an
d co
nservatio
n o
f sun
bears, In
do
nesian
Bo
rneo
G. F
redriksso
n
Effects of El Niño and large-scale forest fires
on the ecology and conservation of
Malayan sun bears (Helarctos malayanus)
in East Kalimantan, Indonesian Borneo
Effects of El Niño and large-scale forest fires
on the ecology and conservation of
Malayan sun bears (Helarctos malayanus)
in East Kalimantan, Indonesian Borneo
ACADEMISCH PROEFSCHRIFT
ter verkrijging van de graad van doctor
aan de Universiteit van Amsterdam
op gezag van de Rector Magnificus
prof. dr. D.C. van den Boom
ten overstaan van een door het college voor promoties
ingestelde commissie,
in het openbaar te verdedigen in de Agnietenkapel
op donderdag 15 november 2012 om 12:00 uur
door
Gabriella Margit Fredriksson
Geboren te Amsterdam, Nederland
Promotiecommissie
Promotor: Prof. Dr. S.B.J. Menken
Co-Promotores: Dr. D.L. Garshelis
Prof. Dr. J.E. Swenson
Overige leden: Prof. Dr. P. van Tienderen
Dr. H.D. Rijksen
Prof. Dr. A.M. Cleef
Prof. Dr. J.H.D. Wolf
Prof. Dr. H. de Iongh
Faculteit der Natuurwetenschappen, Wiskunde en Informatica
© G.M. Fredriksson
Illustrations cover and chapters: Timbul Cahyono
Layout: Corien Smit
Printing: Haveka BV
Front cover illustration: In the foreground a sun bear is holding a wild durian fruit (Durio dulcis), which only fruits during the mast episodes. On the left is a strangling fig (Ficus spp.) a species that fruits at irregular inter-vals, one of the most important fruit species in the sun bear diet during the prolonged inter-mast period. To the right is a tree with clawmarks left behind after a bear climbed the tree. In the center a sun bear is feeding on a termite mound. Fires, set by humans, are looming in the background.
Back cover illustration: On the right a sun bear is climbing a tree to investigate a stingless bee’s nest: only the characteristic nest entrance tube can be seen at the top of the tree. Small pitcher plants at the base of the tree hold rainwater, occasionally used by sun bears to quench their thirst. In the lower left corner a large reticulated python can be seen, one of the few natural predators of sun bears. Behind the snake, coconut trees planted near the forest edge by farmers have been covered with metal sheeting to protect them from sun bears climbing up and eating the growth shoot. In the back farmers have set fires to clear land.
This publication (cover and interior) is printed on recycled paper, Revive®.With ink from renewable resources and alcohol free fountain solution.Recycled, EU Flower, FSC, ISO 14001.
More info: http://www.haveka.nl/greening
This thesis is dedicated to sun bears, in particular my bear friends
Ganja, Ucil, Schizo and si Kecil
may enough forest be conserved for this wonderful species
to persist till eternity!
And to Ingmar…
may he become inspired to safe forests and wildlife in the future!
Contents
Chapter 1: General introduction 1
Chapter 2: Frugivory in sun bears (Helarctos malayanus) is linked to
El Niño-related fluctuations in fruiting phenology,
East Kalimantan, Indonesia 17
with S. A. Wich and Trisno
Biological Journal of the Linnean Society (2006), 89(3): 489-508
Chapter 3: Movement and activity patterns of female sun bears in
East Kalimantan, Indonesian Borneo: implications for conservation 53
with D. L. Garshelis
Chapter 4: Impacts of El Niño-related drought and forest fires on
sun bear fruit resources in lowland dipterocarp forest of
East Borneo 81
with L. S. Danielsen and J. Swenson
Biodiversity and Conservation (2006), 15(4): 1271-1301
Chapter 5: Human-sun bear conflicts in East Kalimantan,
Indonesian Borneo 103
Ursus (2005), 16: 130-137
Contentsviii
Chapter 6: Predation on sun bears by reticulated python in
East Kalimantan, Indonesian Borneo 119
The Raffles Bulletin of Zoology (2005), 53(1): 165-168
Chapter 7: Exploring the use of sign surveys for monitoring relative
abundance of sun bears: a case study in burned and unburned
forests in East Kalimantan, Indonesian Borneo 131
with D.L. Garshelis, W.J. Sastramidjaja, S.B.J. Menken
Chapter 8: Synthesis and conclusions 163
Acknowledgements 179
Summary 185
Samenvatting 189
Ringkasan 195
Curriculum Vitae and List of Publications 201
Chapter 1
General introduction
General introduction 3
General introduction
Among the world’s tropical regions, Southeast Asia is of particular conservation con-
cern because it has the highest rate of habitat loss (Sodhi et al. 2004, 2010, Miettinen et al.
2011). Most of Southeast Asia is considered a biodiversity hotspot because it is home to an
exceptionally high number of endemic species that are threatened by the loss of >70% of
original habitats (Myers et al. 2000). Southeast Asia is also highlighted as an area where past and
present human-driven land-use changes are expected to cause extinctions across a wide range
of taxa (Brook et al. 2003, Cardillo et al. 2006, Lee and Jetz 2008). Furthermore, environmental
apathy, corruption, poor natural resource governance, poverty, and limited conservation fund-
ing constitute difficult obstacles for conservationists in Southeast Asia (Sodhi et al. 2004, 2010,
Sodhi and Brook 2006, Posa et al. 2008).
Indonesia, the country with the largest expanse of remaining contiguous forest
in Southeast Asia, has put its forests and wildlife under serious pressure in recent decades
through a combination of unsustainable logging practices (Curran et al. 2004, Fuller et al. 2004,
Meijaard et al. 2005), high rates of deforestation for plantation development (Hansen et al.
2009, Miettinen et al. 2011), and a succession of devastating forest fire events (Lennertz and
Pfanzer 1984, Malingreau 1985, Siegert et al. 2001).
Kalimantan, the Indonesian part of Borneo that covers 73% of the island, has experi-
enced two extreme forest fire events in modern times, the first in 1982-83 and the second in
1997-98. Both these fire events coincided with severe and prolonged droughts associated with
severe El Niño-Southern Oscillation (ENSO) phenomena (Siegert et al. 2001). The fire event in
1982-83 affected an estimated 3.5 million ha (Mha) of forest in Kalimantan alone (Guhardja et
al. 2000), whereas the disastrous fire event of 1997-98 affected circa 5 Mha of land in the prov-
ince of East Kalimantan (Indonesian Borneo) alone, including 2.6 Mha of forest (Hoffmann et al.
1999, Siegert et al. 2001). Between 1997 and 2006, a total of 16.2 Mha of Borneo’s landmass1
(21% of total land surface area) have been affected by fires (Langner and Siegert 2009) (Fig. 1).
These fires also entered several national parks and other protected areas (Curran et al.
2004, Langner and Siegert 2009), affecting their biodiversity value (Kinnaird and O’Brien 1998).
At present the island is troubled by frequent smaller fire events, now occurring even during
‘normal’ dry seasons. This increased fire frequency is caused by a combination of droughts, for-
est degradation leading to increased susceptibility to fires, and the growing use of fire as a cheap
tool for land clearing by plantation companies and farmers (Hoffman et al. 1999).This increase
1 For size comparison, the total land surface area of the Netherlands is 3.35 Mha.
Chapter 14
of fires has primarily been connected with land speculation and development projects (Siegert
et al. 2001, Page et al. 2002, Goldammer 2007). These recurring fire events are not only degrad-
ing vast areas of rainforest, including their biodiversity, but are also causing massive carbon
dioxide emissions, which contribute to global warming (Page et al. 2002, Achard et al. 2004).
Figure 1: Map of Borneo depicting fire affected areas (1997-2006) adapted from Langner and Siegert (2009).
Although forest fires have been recorded historically in western Indonesia (Goldam-
mer and Seibert 1989), their incidence was rare, with intervals of hundreds to thousands of
years (Cochrane et al. 1999). As a result, these tropical forests are maladapted to fire events
(Slik et al. 2010), with fires having a devastating effect on tree survival (Leighton and Wirawan
1989, Woods 1989, Slik et al. 2002, van Nieuwstadt 2002). The combined effects of extreme
drought and fire lead to more than 70% mortality of trees (>10 cm DBH) in once-burned areas
two years after the fires in 1997-98 (van Nieuwstadt 2002).
Animal populations are also affected by these forest fires, either directly through fire
General introduction 5
injury or indirectly through changes in food availability or habitat structure (Whelan 1995).
Mammals provide vital ecological services in tropical rainforests and are key in the structuring
of biological communities through their roles in, amongst others, seed dispersal and predation,
pollination, folivory, and frugivory, and as top predators (Terborgh 1988, 1992). Apart from a
handful of papers on mortality in the immediate aftermath of fires (e.g. Kinnaird and O’Brien
1998, Peres 1999), and a small number of qualitative reports following the 1982–1983 ENSO
event (Berenstain 1986, Leighton and Wirawan 1986, Azuma 1988, Doi 1988), information on
the effects of fires on large vertebrates remains scarce and anecdotal (Oka 1999, O’Brien et
al. 2003). Barlow and Peres (2006) examined the effects of both single and recurrent wildfires
on fruit production and large vertebrate abundance in a central Amazonian terra firme forest,
showing that many large frugivores and other vertebrate species declined in response to single
fires, and most species dependent on primary forest were extirpated from twice-burnt forest
(Barlow and Peres 2006). The only study on large vertebrate responses to forest fires from In-
donesia by O’Brien et al. (2003) reported on the negative effects of forest fires on demography
and persistence of siamang (Symphalangus syndactylus) groups in Sumatra. Their study indicated
that it was doubtful whether groups of this large primate would be able to persist in burned-
over areas for more than two generations.
Besides their sensitivity to fires, forests in Southeast Asia are characterized by irregular,
supra-annual, mast fruiting [i.e. synchronous variable production of large fruit crops (‘masts’)
amid years of smaller crops] events (Appanah 1985, Ashton et al. 1988). These events are pos-
sibly triggered by environmental factors occurring during ENSO events (Ashton et al. 1988),
although the influence of ENSO events on mast fruiting varies throughout Southeast Asia
(Wich and van Schaik 2000): mast fruiting events and ENSO phenomena are most strongly
correlated on the eastern side of the Malesian landmasses, specifically eastern Borneo (Ashton
et al. 1988). The canopy and emergent trees of these forests are dominated by trees of the
Dipterocarpaceae, distinguished by a unique reproductive pattern (Medway 1972, Appanah
1985, Curran et al. 1999), causing them to flower and fruit at intervals of 2-10 years with
little or no reproductive activity in between (Medway 1972, Ashton et al. 1988, Curran and
Leigthon 2000). A large proportion of individual trees covering varied taxonomic groups (Ap-
panah 1985, Sakai et al. 1999) and flowering syndromes (Momose et al. 1998), flower and fruit
synchronously with these dipterocarps. During these mast fruiting events, an overabundance
of fruit is produced for a short period of time but these are often followed by periods of low
fruit production. These large fluctuations in fruit availability (both temporal and spatial) can
affect primary consumers in a variety of ways and in order to compensate for low fruit avail-
Chapter 16
ability, mammals have developed a variety of behavioural adaptations, ranging from local dietary
shifts to long-distance migrations (e.g. Leighton and Leighton 1983, Curran and Leighton 2000).
During these prolonged intermast periods a number of ‘keystone’ species, especially figs (Ficus
spp.) still produce fruit (van Schaik et al. 1993). Janzen (1974) hypothesized that prolonged food
scarcity in these dipterocarp forests can limit populations of frugivores and granivores during
non-mast years, and on rare occasions food scarcity during these intermast periods may lead
to starvation (Curran and Leighton 2000, Wong et al. 2005).
Malayan sun bears (Helarctos malayanus), the smallest of the extant bear species, are
currently the largest member of the order Carnivora on Borneo. Bornean sun bears are
considered a separate subspecies (H. m. eurispylus), considerably smaller than their Sumatran
and mainland counterparts, H. m. malayanus (Pocock 1941, Meijaard 2004). Sun bears occur
throughout Southeast Asia, with the westernmost part of their distribution starting in eastern
India, throughout Burma, possibly southern China (Yunnan), Laos, Cambodia, Vietnam, Thailand,
Malaysia, Indonesia (Sumatra, Kalimantan), and Brunei (IUCN/BSG 2006) (Fig. 2). The species
now occurs patchily through much of its former range, and has been extirpated from many
areas, especially in mainland Southeast Asia. Sun bear fossils from the Pleistocene have been
found much further north into China and on the island of Java (Erdbrink 1953), but sun bears
did not occur there in more recent historical times (Meijaard 2004).
When this study commenced in 1997, no field research had yet been undertaken on
sun bears anywhere in their distribution area. Sun bears were listed as Data Deficient in the
IUCN Red List and only rather crude distribution maps were available (Servheen 1999). Reli-
able estimates of sun bear population numbers were lacking (and still are). In the available
literature at the time, sun bears were described as nocturnal frugivores, augmenting their
diet with a variety of insects, small mammals, and honey (Lekagul and McNeely 1977, Kunkun
1985, Payne et al. 1985). Sun bears rely on tropical forest habitat, with two ecologically distinct
categories of tropical forest occurring within their range (Fredriksson et al. 2008). These two
types of forests are distinguished by differences in climate, phenology, and floristic composition.
Tropical evergreen rainforest is the sun bear’s main habitat in Borneo, Sumatra, and peninsular
Malaysia. This aseasonal habitat receives high annual rainfall that is relatively evenly distributed
throughout the year. Tropical evergreen rainforest, includes a wide diversity of forest types
used by sun bears, including lowland dipterocarp, peat swamp, freshwater swamp, limestone/
karst hills, hill dipterocarp, and lower montane forest. In contrast, sun bears in mainland South-
east Asia inhabit seasonal ecosystems with a long dry season (3–7 months), during which
rainfall is <100 mm per month. Seasonal forest types are usually interspersed in a mosaic that
General introduction 7
Figure 2: Sun bear distribution range (IUCN/BSG, Japan Bear Distribution Mapping Workshop, 2006).
Chapter 18
includes semi-evergreen, mixed deciduous, dry dipterocarp (<1,000 m elevation), and montane
evergreen forest (>1,000 m). The range of sun bears overlaps that of Asiatic black bears (Ursus
thibetanus) in this seasonal forest mosaic. Sun bears occur from near sea level to over 2,100
m elevation, but appear to be most common in lower-elevation forests (Steinmetz et al. 2011).
This study commenced a few months before the onset of the catastrophic forest fires
of 1997-98, in a small lowland reserve (10,000 ha), the Sungai Wain Protection Forest (SWPF)
in East Kalimantan. At that time, this forest was still connected to a number of other forest
areas to the west and north beyond the boundaries of the reserve, and although encroached
by illegal settlers on the eastern border, the SWPF still covered some 8,000 ha of primary
coastal lowland forest. A great opportunity for close behavioural observations of these other-
wise extremely cryptic bears presented itself in January 1998, when we received the first of
three young confiscated sun bears, with a request from the Conservation Department (Balai
Konservasi Sumber Daya Alam) to rehabilitate and release them in the reserve. In March 1998
forest fires entered the reserve, towards the end of the long ENSO drought, initially from a
neighbouring state-owned logging concession, but subsequently also from surrounding agricul-
tural lands. Despite two months of extensive fire extinction efforts, approximately 50% of the
reserve was affected by forest fires (Fredriksson 2002) leaving an unburned central core of
some 4,000 ha of primary forest. Subsequent to these fires, a number of studies commenced
in the SWPF to investigate the effects of fires on plant communities (van Nieuwstadt 2002, Slik
et al. 2002, Slik and Eichhorn 2003, Slik 2004), butterflies (Cleary 2003), and birds (Slik and van
Balen 2006).
This study on sun bears spanned five continuous years in the field. Between August
1997 and July 2002 fieldwork was primarily carried out in SWPF. Subsequently sun bear sign
surveys were carried out in different forest types throughout Kalimantan, covering the main
forest types found on the island. Additional sign surveys of sun bears in burned and unburned
forest were carried out in 2005 and 2010 in SWPF.
Due to the lack of reference material, a broad approach was taken to gain insight into
the ecology of this species, ranging from phenology plots to monitor production of flowers and
fruit over several years, behavioural observations of sun bears, collection of fecal samples to
look at dietary composition and seasonal changes herein, seed germination trials to investigate
seed dispersal efficiency, trapping of wild sun bear for radio-tagging to gain insight into ranging
and activity patterns, sampling of insects in burned and unburned forest, interviews with forest-
edge communities to gain insight into sun bear activity in agricultural areas, as well as using sign
transects to monitor sun bear usage of burned and unburned areas over time.
General introduction 9
Outline of this thesis
Chapter 1 General introduction
Chapter 2 describes frugivory in sun bears and how this is linked to periodic mast
fruiting events in Kalimantan, monitored through monthly phenology censuses. We describe
the importance and occurrence of various tree families in the diet of the sun bears over
a period of 55 months. This chapter highlights the importance of the need for long-term
monitoring in these aseasonal forests where supra-annual, rather than annual, changes in
phenology affect sun bear ecology. Although sun bears were feeding primarily on fruits dur-
ing the start of this study coinciding with a mast fruiting event, invertebrates dominated the
diet during the subsequent prolonged intermast period, which lasted up to four years at this
study site.
Chapter 3 describes the movement and activity patterns of sun bears in unburned
forest through telemetry studies. Sun bears within the reserve were found to be primarily di-
urnal, as opposed to sun bears living at the forest edge, which displayed more nocturnal activity.
Female sun bears ranged over relatively small areas (approx. 5 km2) over a period of 12 months.
The ranges of several female bears that we monitored were strictly confined within the small
reserve. Sun bears seem to shun areas with human traffic, with bears avoiding the main trail
leading to the research station. Sun bears also appeared to avoid entering the burned forest
areas for several years after the fire event. This avoidance of areas with human disturbance
in combination with relatively small ranges implies that even small reserves like SWPF are
relevant for sun bear conservation, although the long-term survival of sun bear populations in
such smaller protected areas will depend on the matrix of forest habitat and connectivity to
other forest areas outside these reserves.
Subsequent to the large fire event in 1997-98, the impacts of forest fires on sun bear
fruit resources and invertebrates were studied in more detail. In Chapter 4 we describe the
effects of drought and forest fires on density and diversity of fruit trees important in the diet
of sun bears. The forests of Borneo are maladapted to withstand the impacts of prolonged
drought and fires, and sun bear fruit trees experienced 80% mortality in areas affected by the
fires. Drought also affected sun bear fruit trees in unburned forest areas, with elevated mortal-
ity rates. Species diversity of sun bear fruit taxa also declined by 44% in burned forest areas
impacting future species composition in these once-burned areas.
In Chapter 5 we look at the interface between humans and sun bears at the for-
est edge. Elevated levels of human-sun bear conflict were reported after the forest fires in
Chapter 110
1997-98. We discuss methods on how to reduce some of these conflicts and how human-bear
conflict will affect conservation of this species.
Chapter 6 describes the predation of an adult female sun bear, which we had radio-
collared, by a python (Python reticulatus) during the prolonged intermast period. I discuss the
physical condition of sun bears caught for telemetry studies at this study site compared to that
of other sun bears caught for research purposes simultaneously in Sabah (Malaysian Borneo). I
discuss how the reduced physical condition of the sun bear predated upon by the python might
be linked to a combination of lack of fruit resources and increased competition in unburned
forest by bears displaced after the fires.
In Chapter 7 we present data from sign transects where we explore the usage of sun
bear sign (i.e. claw marks, broken termite nests, ripped logs) as an index of relative abundance
to monitor the usage of burned and unburned forest areas by sun bears over more than a dec-
ade. Sun bear sign densities/hectare were close to zero in burned forest areas for several years
after the fire event, although sign densities increased slowly by the 7th years after the fires and
were close to 65% of sign densities encountered in adjacent primary forest, 12 years after the
fire event. These once-burned forest areas still have important regeneration and conservation
potential as long as source populations are found nearby.
Chapter 8 Synthesis and concluding remarks
ReferencesAchard, F., H. D. Eva, P. Mayaux, H.-J. r. Stibig, and A. Belward. (2004). Improved estimates of net carbon emis-
sions from land cover change in the tropics for the 1990s. Global Biogeochem. Cycles 18:GB2008.
Appanah, S. (1985). General flowering in the climax rain forests of South-east Asia. Journal of Tropical Ecol-
ogy 1:225-240.
Ashton, P.S., Givnish, T.J., and Appanah, S. (1988). Staggered Flowering in the Dipterocarpaceae - New In-
sights into Floral Induction and the Evolution of Mast Fruiting in the Aseasonal Tropics. American
Naturalist 132, 44-66.
Azuma, S. (1988). Distribution and abundance of primates after the forest fire in the lowland forest of East
Kalimantan 1983-1986. Pages 94-116 in H. Tagawa and N. Wirawan, editors. A research on the
process of earlier recovering of tropical rain forest.
Barlow, J. and C. Peres. (2006). Effects of Single and Recurrent Wildfires on Fruit Production and Large Ver-
tebrate Abundance in a Central Amazonian Forest. Biodiversity and Conservation 15:985-1012.
General introduction 11
Berenstain, L. (1986). Responses of Long-tailed macaques to drought and fire in eastern Borneo: A prelimi-
nary report. Biotropica 18:257-262.
Brook, B. W., N. S. Sodhi, and P. K. L. Ng. (2003). Catastrophic extinctions follow deforestation in Singapore.
Nature 424:420-423.
Cardillo, M., A. Purvis, W. Sechrest, J. L. Gittleman, J. Bielby, and G. M. Mace. (2004). Human population density
and extinction risk in the world’s carnivores. PLoS Biology 2:0909-0914.
Cochrane, M. A., A. Alencar, M. D. Schulze, C. M. Souza, D. C. Nepstad, P. Lefebvre, and E. A. Davidson. (1999).
Positive feedbacks in the fire dynamic of closed canopy tropical forests. Science 284:1834-1836.
Curran, L. M., I. Caniago, G. D. Paoli, D. Astianti, M. Kusenti, C. E. Nirarita, and H. Haeruman. (1999). Impact
of El Nino and logging on canopy tree recruitment in Borneo. Science 286:2184-2188.
Curran, L. M. and M. Leighton. (2000). Vertebrate responses to spatiotemporal variation in seed production
of mast-fruiting dipterocarpaceae. Ecological Monographs 70:101-128.
Curran, L.M., Trigg, S.N., McDonald, A.K., Astianti, D., Hardiono, Y.M., Siregar, P., Caniago, I., and Kasischke,
E. (2004). Lowland forest loss in protected areas of Indonesian Borneo. Science 303, 1000-1003.
Doi, T. (1988). Present status of the large mammals in the Kutai National Park, after a large scale fire in
East Kalimantan, Indonesia. Pages 82-93 in H. Tagawa and N. Wirawan, editors. A research on the
process of earlier recovery of tropical rain forest.
Erdbrink, D. P. (1953). A review of fossil and recent bears of the old world. With remarks on their phylogeny
based upon their dentition. PhD. University of Utrecht, Drukkerij Jan De Lange, Deventer.
Fredriksson, G.M. (2002). Extinguishing the 1998 forest fires and subsequent coal fires in the Sungai Wain
Protection Forest, East Kalimantan, Indonesia. In: Communities in flames: proceedings of an inter-
national conference on community involvement in fire management (Bangkok, Thailand, FAO and
FireFight SE Asia).
Fredriksson, G., Steinmetz, R., Wong, S. and Garshelis, D.L. (IUCN SSC Bear Specialist Group) (2008).
Helarctos malayanus. In: IUCN 2012. IUCN Red List of Threatened Species. Version 2012.1. <www.
iucnredlist.org>. Downloaded on 20 July 2012
Fuller, D.O., Jessup, T.C., and Salim, A. (2004). Loss of forest cover in Kalimantan, Indonesia, since the 1997-
1998 El Niño. Conservation Biology 18, 249-254.
Goldammer, J. G. and B. Seibert. (1989). Natural rain forest fires in Eastern Borneo during the Pleistocene
and Holocene. Naturwissenschaften 76:518-520.
Goldammer, J. G. (2007). History of equatorial vegetation fires and fire research in Southeast Asia before
the 1997–98 episode: A reconstruction of creeping environmental changes. Mitigation and Adapta-
tion Strategies for Global Change 12:13-32.
Chapter 112
Guhardja, E., M. Fatawi, M. Sutisna, T. Mori, and S. Ohta, editors. (2000). Rainforest Ecosystems of East Kali-
mantan. El Nino, Drought, Fire and Human Impacts. Springer-Verlag, Tokyo.
Hansen, M.C., Stehman, S.V., Potapov, P.V., Arunarwati, B., Stolle, F., and Pittman, K. (2009). Quantifying
changes in the rates of forest clearing in Indonesia from 1990 to 2005 using remotely sensed data
sets. Environmental Research Letters 4, 034001.
Hoffmann, A.A., Hinrichs, A., and Siegert, F. (1999). Fire damage in East Kalimantan in 1997/98 related to
land use and vegetation classes: Satellite radar inventory results and proposal for further actions.
IFFM-SFMP Report No.1a (Samarinda, East Kalimantan, MOFEC, GTZ and KfW).
Janzen, D. H. (1974). Tropical blackwater rivers, animals, and mast fruiting by the dipterocarpaceae. Bio-
tropica 6:69-103.
Kinnaird, M.F., and O’Brien, T.G. (1998). Ecological effects of wildfire on lowland rainforest in Sumatra.
Conservation Biology 12, 954-956.
Kunkun, J. G. (1985).Short information on Malayan sun bear in Indonesia.Pages 67-69 in First Asiatic Bear
Conference, Utsunomiya & Nikko, Tochigi Prefecture.
Langner, A. and F. Siegert. (2009). Spatiotemporal fire occurrence in Borneo over a period of 10 years.
Global Change Biology 15:48-62.
Lee, T. M. and W. Jetz. (2008). Future battlegrounds for conservation under global change. Proceedings of
the Royal Society B: Biological Sciences 275:1261-1270.
Leighton, M. and D. R. Leighton. (1983). Vertebrate responses to fruiting seasonality within a Bornean rain
forest. Pages 181-196 in S. L. Sutton, T. C. Whitemore, and A. C. Chadwick, editors. Tropical Rain
Forest Ecology and Management. Blackwell Scientific Publications, Cambridge UK.
Leighton, M. and N. Wirawan. (1986). Catastrophic drought and fire in Borneo Tropical Rain Forest Associ-
ated with the 1982-1983 El Nino southern oscillation event. Pages 75-101 in G. T. Prance, editor.
Tropical rain forest and world atmosphere. Westview Press, Boulder, Colorado, USA.
Lekagul, M. D. B. and B. A. J. A. McNeely. (1977). Mammals of Thailand. Kurusapha Ladprao Press, Thailand.
Lennertz, R. and K. F. Panzer. (1984). Preliminary assessment of the drought and forest fire damage in
Kalimantan Timur. DFS German Forest Inventory Service for Gesellschaft fur Technische Zusam-
menarbeit (GTZ), Germany.
Malingreau, J. P., G. Stephens, and L. Fellows. (1985). Remote sensing of forest fires: Kalimantan and North
Borneo in 1982-83. Ambio 14:314-321.
Medway, L. (1972). Phenology of a tropical rain forest in Malaya. Biological Journal of the Linnean Society
4:117-146.
Meijaard, E. (2004). Craniometric differences among Malayan sun bears (Ursus malayanus); evolutionary and
taxonomic implications. Raffles Bulletin of Zoology 52, 665-672.
General introduction 13
Meijaard, E., Sheil, D., Rosenbaum, B., Iskandar, D., Augeri, D., Setyawati, T., Duckworth, W., Lammertink, M.J.,
Rachmatika, I., Nasi, R., et al. (2005). Life after logging: reconciling wildlife conservation and produc-
tion forestry in Indonesian Borneo (Bogor, Indonesia, CIFOR, WCS and UNESCO).
Miettinen, J., Shi, C., and Liew, S.C. (2011). Deforestation rates in insular Southeast Asia between 2000 and
2010. Global Change Biology 17, 2261-2270.
Myers, N., R. A. Mittermeier, C. G. Mittermeier, G. A. B. da Fonseca, and J. Kent. (2000). Biodiversity hotspots
for conservation priorities. Nature 403:853-858.
Nieuwstadt, M.G.L. v. (2002). Trial by fire-Postfire development of a dipterocarp forest (PhD thesis Univer-
sity of Utrecht, Netherlands), pp. 1-143.
O’Brien, T. G., M. F. Kinnaird, A. Nurcahyo, M. Prasetyaningrum, and M. Iqbal. (2003). Fire, demography and
the persistence of siamang (Symphalangus syndactylus: Hylobatidae) in a Sumatran rainforest.
Animal Conservation 6:115-121.
Page, S. E., F. Siegert, J. O. Rieley, H. D. V. Boehm, A. Jaya, and S. Limin. (2002). The amount of carbon released
from peat and forest fires in Indonesia during 1997. Nature 420:61-65.
Payne, J., C. M. Francis, and K. Phillipps. (1985). A field guide to the mammals of Borneo. World Wildlife Fund
Malaysia, Kuala Lumpur, Malaysia.
Peres, C. A. (1999). Ground fires as agents of mortality in a Central Amazonian forest. Journal of Tropical
Ecology 15:535-541.
Pocock, R. I. (1941). The Fauna of British India, including Ceylon and Burma. Mammalia Vol. II. Carnivora
(suborders Aeluroidae (part) and Arctoidae).Taylor & Francis, Ltd., London, United Kingdom.
Posa, M. R. C., A. C. Diesmos, N. S. Sodhi, and T. M. Brooks. (2008). Hope for Threatened Tropical Biodiver-
sity: Lessons from the Philippines. BioScience 58:231-240.
Sakai, S., K. Momose, T. Yumoto, T. Nagamitsu, H. Nagamasu, A. A. Hamid, and T. Nakashizuka. (1999). Plant
reproductive phenology over four years including an episode of general flowering in a lowland
dipterocarp forest, Sarawak, Malaysia. American Journal of Botany 86:1414-1436.
Schaik, C. P. v., J. W. Terborgh, and S. J. Wright. (1993). The phenology of tropical forests: adaptive significance
and consequences for primary consumers. Annual Review of Ecology and Systematics 24:353-377.
Servheen, C. (1999). Status of Bears of the World. Presentation at the 3rd International Symposium on the
Trade of Bears and Bear Parts, Seoul, Korea.
Siegert, F., G. Ruecker, A. Hinrichs, and A. A. Hoffmann. (2001). Increased damage from fires in logged forests
during droughts caused by El Niño. Nature 414:437-440.
Slik, J. W. F. (2004). El Niño droughts and their effects on tree species composition and diversity in tropical
rain forests. Oecologia 141:114-120.
Chapter 114
Slik, J.W.F., Verburg, R.W., and Kessler, P.J.A. (2002). Effects of fire and selective logging on the tree species
composition of lowland dipterocarp forest in East Kalimantan, Indonesia. Biodiversity & Conser-
vation 11, 85-98.
Slik, J. W. F. and K. A. O. Eichhorn. (2003). Fire survival of lowland tropical rain forest trees in relation to stem
diameter and topographic position. Oecologia 137:446-455.
Slik, J. and S. Van Balen. (2006). Bird Community Changes in Response to Single and Repeated Fires in
a Lowland Tropical Rainforest of Eastern Borneo. Biodiversity and Conservation 15:4425-4451.
Slik, J., F. Breman, C. Bernard, M. van Beek, C. Cannon, K. Eichhorn, and K. Sidiyasa. (2010). Fire as a selective
force in a Bornean tropical everwet forest. Oecologia 164:841-849.
Sodhi, N. S., L. P. Koh, B. W. Brook, and P. K. L. Ng. (2004). Southeast Asian biodiversity: an impending disaster.
Trends in Ecology & Evolution 19:654-660.
Sodhi, N. and B. Brook. (2006). Southeast Asian biodiversity crisis. Cambridge University Press, Cambridge,
UK.
Sodhi, N., Posa, M., Lee, T., Bickford, D., Koh, L., and Brook, B. (2010). The state and conservation of South-
east Asian biodiversity. Biodiversity and Conservation 19, 317-328.
Steinmetz, R., D. L. Garshelis, W. Chutipong, and N. Seuaturien. (2011). The Shared Preference Niche of
Sympatric Asiatic Black Bears and Sun Bears in a Tropical Forest Mosaic. PLoS One 6:e14509.
Terborgh, J. (1988). The big things that run the world - a sequel to E.O.Wilson. Conservation Biology
2:402-403.
Terborgh, J. (1992). Maintenance of diversity in tropical forests. Biotropica 24(2b):283-292.
Whelan, R. J. (1995). The ecology of fire. Cambridge University Press, Cambridge.
Wich, S. A. and C. P. van Schaik. (2000). The impact of El Niño on mast fruiting in Sumatra and elsewhere in
Malesia. Journal of Tropical Ecology 16:563-577.
Wong, S.T., Servheen, C., Ambu, L., and Norhayati, A. (2005). Impacts of fruit production cycles on Malayan
sun bears and bearded pigs in lowland tropical forest of Sabah, Malaysian Borneo. Journal of Tropi-
cal Ecology 21, 627–639.
Woods, P. (1989). Effects of Logging, Drought, and Fire on Structure and Composition of Tropical Forests
in Sabah, Malaysia. Biotropica 21:290-298.
Chapter 2
Frugivory in sun bears (Helarctos malayanus)
is linked to El Niño-related fluctuations in
fruiting phenology, East Kalimantan, Indonesia
With S.A. Wich and Trisno
Biological Journal of the Linnean Society (2006), 89(3): 489-508
Chapter 218
Abstract
We investigated sun bear (Helarctos malayanus) frugivory and fruiting phenology in a
lowland dipterocarp forest in East Kalimantan, Indonesia. Two mast fruiting events, both coin-
ciding with El Niño/Southern Oscillation events, occurred four years apart, resulting in large
fluctuations in fruit availability. Sun bear fruit availability decreased from 13 trees ha-1 fruiting
month-1 during the mast fruiting to 1.6 during the inter-mast period. Almost 100% of sun bear
diet consisted of fruit during mast fruiting period, whereas during inter-mast periods sun bear
diet was predominantly insectivorous.
The majority of sun bear fruit trees displayed ‘mast-fruiting’ and ‘supra-annual’ fruiting
patterns, indicating sporadic productivity. Sun bears fed on 115 fruit species covering 54 gen-
era and 30 families, with Ficus (Moraceae) being the main fallback fruit. The families Moraceae,
Burseraceae and Myrtaceae contributed more than 50% to the sun bear fruit diet. Sun bear
fruit feeding observations were unevenly distributed over forest types with more observa-
tions in high-dry forest type despite fewer fruiting events, possibly a side-effect of high insect
abundance which causes bears to use these areas more intensively. We discuss the possible
evolutionary pathways of sun bears in relation to the Sundaic environment.
Phenological influences on sun bear frugivory 19
Introduction
Irregular community flowering and fruiting have been recorded throughout Southeast
Asian forests (Wood, 1956; Medway, 1972; Appanah, 1985; Ashton et al., 1988; Sakai, 2002). The
canopy and emergent trees of these forests are dominated by trees of the Dipterocarpaceae,
distinguished by a unique reproductive pattern (Medway, 1972; Appanah, 1985; Curran et al.,
1999), causing them to flower and fruit at intervals of 2-10 years with little or no reproductive
activity in between (Medway, 1972; Ashton et al., 1988; Curran and Leigthon, 2000). A large
proportion of individual trees covering varied taxonomic groups (Appanah, 1985; Sakai et al.,
1999) and flowering syndromes (Momose et al., 1998), flower and fruit synchronously with
these dipterocarps. The size of the area taking part in such a general flowering/mast fruiting
event and intensity can vary substantially, from a river valley to the whole of Peninsular Malaysia
(Ashton et al., 1988; Yasuda et al., 1999).
It is unclear which mechanism triggers these synchronized flowering events, although a
drop in night-time temperature (≥2ºC for 3 or more consecutive days) some 2 months before
the onset of flowering, has received substantial support (Ashton et al., 1988; Yasuda et al., 1999,
but see Corlett and Frankie, 1998). In Borneo, temperature drops associated with the El Niño/
Southern Oscillation (ENSO) phenomenon have preceded mast events (Ashton et al., 1988),
although Yasuda et al. (1999) reported a night-time temperature drop preceding a mast fruiting
event during a La Niña episode in Peninsular Malaysia. The influence of ENSO on mast fruit-
ing varies throughout Southeast Asia (Wich and van Schaik, 2000), but is reportedly strongest
on the eastern sides of the Malesian land masses, especially in East Kalimantan (Ashton et al.,
1988).
Mast fruiting events provide an overabundance of fruit for a short period of time and
are often followed by periods of low fruit production, probably due to exhaustion of energy
reserves (van Schaik 1986; Sork et al., 1993). The temporal and spatial patchiness and high vari-
ability in fruit production in Southeast Asia cause these forests to have a much lower overall
productivity than tropical forests in Africa and South America (Appanah, 1985). Janzen (1974)
hypothesized that prolonged fruit scarcity in these dipterocarp forests limits populations of
granivores and frugivores during non-mast years. These primary consumers have adapted in a
variety of ways to the lack of fruit. Many mammals show a dietary switch and resort to feeding
on items of lower nutritional value (Leighton and Leighton, 1983; Peres, 1994; Knott, 1998),
materials with increased handling time (e.g., palm-nuts, Strushaker and Leyland, 1977), plants
that contain chemical deterrents (Foster, 1977), or diffusely scattered resources that increase
Chapter 220
foraging time (Terborgh, 1983). The synchronized timing of reproduction in relation to peri-
ods of fruit abundance (Fogden, 1972; van Schaik and van Noordwijk, 1985; Goldizen et al.,
1988), changes in range use (e.g. Joshi et al., 1995), and migration (Caldecott, 1988; Curran and
Leighton, 2000) have also been recorded for certain mammal species.
Only rarely has food scarcity between mast events been so severe that it leads to doc-
umented famine and starvation. Curran and Leighton (2000) observed emaciated and starving
bearded pigs at their study site in West Kalimantan during inter-mast periods and Knott (1998)
found that orangutans suffered negative energy budgets during the lean fruit period after a
mast at the same study site.
A variety of plant species that produce edible parts during periods of low fruit availabil-
ity have been labelled fallback resources (e.g. Conklin-Brittain et al., 1998). Fallback resources
are critical for metabolic maintenance when preferred foods are unavailable (Leighton and
Leighton, 1983; Terborgh, 1986) and their abundance potentially sets the carrying capacity for
primary consumers (van Schaik et al., 1993). The magnitude and duration of the period of fruit
scarcity, the availability of fallback foods, and the physiological and behavioural flexibilities of
animal species all play an important role in determining how successfully animals adapt to lean
periods. Figs have been reported to be the main fallback food item during fruit lows for many
frugivorous species in East Kalimantan (Leighton, 1993), as well in Neotropical sites (Terborgh,
1986).
The sun bear (Helarctos malayanus), one of the largest mammals of the Bornean rainfor-
est, has mainly been described as a frugivore, augmenting its diet with a variety of insects, small
mammals and honey (Lekagul and McNeely, 1977; Kunkun, 1985; Wong et al., 2002). They are
effective dispersers of the seeds of several plant species (McConkey and Galetti, 1999; G.M.
Fredriksson, unpubl. data). We chose the sun bear as a model large frugivore faced with annual
and supra-annual variations in fruit availability in East Kalimantan, where effects of ENSO on
mast fruiting events are strong (Ashton et al., 1988; Wich and van Schaik, 2000). This study was
carried out at the eastern-most limit of the sun bear distribution range, which covers most of
tropical mainland Southeast Asia, from the Eastern tip of India, through Myanmar, Laos, Thailand,
Cambodia, Vietnam, and Malaysia to the islands of Sumatra and Borneo (Servheen, 1999).
The aims of this study were: i) to study the extent of frugivory in sun bear diet; ii) to
investigate the temporal variations in fruit availability in East Kalimantan; iii) to investigate fruit-
ing patterns of fruit species important in the diet of the sun bear and distribution of these over
topographical types; and iv) to determine which fruit taxa are important as fallback resources
for sun bears during inter-mast periods.
Phenological influences on sun bear frugivory 21
Materials and methods
Study site and climate data
The study was carried out in a lowland dipterocarp forest, the Sungai Wain Protection
Forest, East Kalimantan, Indonesian Borneo (1º 05’ S and 116º 49’ E) (Fig. 1). The reserve cov-
ers a watercatchment area of circa 10,000 ha. Approximately 50% of the reserve was affected
by forest fires in March-April 1998 (Fredriksson, 2002), during one of the most severe ENSO
related droughts ever recorded (McPhaden, 1999), leaving an unburned central core of some
4000 ha of primary forest. Data for this study were collected in the unburned primary forest.
The topography of the reserve consists of gentle to sometimes steep hills, and is intersected
by many small rivers. Elevations range from 30 to 150 metres a.s.l. The most common families
(diameter at breast height, dbh, >10 cm), are Euphorbiaceae, Dipterocarpaceae, Sapotaceae,
and Myrtaceae. The relative dominance of Dipterocarpaceae increases substantially in larg-
er size classes. Together, the 25 most common species form 40% of total stem density (van
Nieuwstadt, 2002). Palmae (also called Family Arecaceae) are common in the subcanopy and
understory, and Zingiberaceae, Marantaceae, Araceae, and Pandanaceae are widespread in the
understory.
Daily rainfall, minimum-maximum temperature and humidity data were collected be-
tween January 1998 and October 2002, at ground level in the primary forest. Rainfall patterns
were calculated on a yearly basis, using Mohr’s Index (Whitmore, 1985). At the start of the
study rainfall was below average due to the ENSO event that was in progress (van Nieu-
wstadt 2002). Although rainfall patterns in the region are not consistent on an annual basis, a
distinction could be made between a ‘wet’ season (Nov-April) and a ‘dry’ season (May-Oct)
(t-test, t=4.96, df=6, p=0.002). Out of 58 months that rainfall data were collected 12 months
had rainfall below 100 mm, classified as dry months (Walsh and Newbery, 1999). Nine of
these occurred between May-September, the remaining 3 dry months were during the 1998
ENSO (Jan-March 1998). Rainfall type falls within the category of ‘slightly seasonal’ according
to Mohr’s index, with average annual rainfall 2968 ± 510 mm y-1. Temperature remained stable
throughout the study period with average maximum of 29.7 ± 0.7ºC and minimum 23.2 ±
0.4ºC, with an annual average of 26.5 ± 0.2 ºC, equal to the average temperature of 26.5ºC
reported for the region historically (Berlage, 1949).
Chapter 222
Figure 1. Map of the Sungai Wain study site in East Kalimantan, showing the unburnt forest core where
data were collected.
Classification of topographical types
Five topographical types were discerned: swamp, alluvial, slope, high-flat, and ridge
(Fredriksson and Nijman, 2004). Swamp type was assigned to areas that showed signs of regu-
lar inundation (pneumatophore roots) or were permanently inundated, and had a high density
of rattans, small trees and saplings, and a large numbers of climbers. This classification of swamp
forest refers to swampy patches within the drier forest matrix and has no relation to large
areas of peat or fresh-water swamp forest as found in e.g. south-central Borneo. Alluvial type
was allocated to flat, non-inundated areas close to rivers characterized by large trees. High-flat
type was assigned to flat areas at higher elevated sites away from rivers, usually with large trees.
Slope type was assigned when an area had a relatively steep inclination (>12°). Ridge type was
allocated to narrow hill tops with steep sides, or crests of longer hill chains. The relative avail-
Phenological influences on sun bear frugivory 23
ability of these forest types was determined by means of transects (total length 18.5 km) laid
out in an east-west and north-south direction where every 25 m the topographical type was
recorded. Slope topographical type covered 45.3 ± 9.1 % of the study area, followed by high-flat
(24.8 ± 9.3 %), alluvial (17.3 ± 4.0 %), ridge (6.7 ± 2.7 %) and swamp (5.9 ± 4.6 %).
Fruiting phenology data collection
Two phenology data sets were collected during this study, using the same methodol-
ogy. Phenology studies commenced in January 1998 and continued until July 2002. Data were
collected in all but two of 55 months (March ’98 and February ’02).
i) Phenology plots Ten 0.1-ha phenology plots (100 x 10 m), were established with
two plots located in each of the five topographical types. All trees ≥10 cm dbh were measured,
labelled, and identified by botanists from the Wanariset Herbarium. The total number of live
trees in the 1-ha of plots at the start of the study was 549 individuals covering some 186 spe-
cies. Every month around the same date (third week), all trees in these plots were observed
with 10 x 40 Leica binoculars. The relative abundance of flowers, young and mature fruits, and
young and old leaves, in relation to size of the crown, was estimated, though for analysis here
only presence/absence of fruit is considered.
ii) Specific sun bear fruit trees The second data set contained 104 trees of 11 spe-
cies (≥10 cm dbh) known or thought to be important in the diet of the sun bear. The spe-
cies of trees in this sample were based on primary fruits found in sun bear scats and trees
frequently covered with sun bear claw marks (signs of bears climbing the trees), as well as
information from local people. Individual trees of these species were encountered by chance
in the forest, measured, labelled, and reobserved on a monthly basis. The following taxa were
included: Monocarpia kalimantanensis (n=10) (Annonaceae), Durio dulcis (n=10), D. oxleyanus
(n=10), and D. zibethinus (n=2) (Bombacaceae), Dacryodes rugosa (n=11), D. rostrata (n=10), and
Santiria spp. (n=10) (Burseraceae), Ficus spp. (n=11), and Artocarpus integer (n=10) (Moraceae),
Ochanostachys amentaceae (n=10) (Olacaceae), and Tetramerista glabra (n=10) (Tetramerista-
ceae). Three of the 11 taxa were added later during the study period, when it was found that
bears fed substantially on them (Monocarpia June 1999; Ficus spp. June 1999; Santiria spp. June
2000).
Frugivory in sun bears
The study on the extent of frugivory in sun bears was based on faecal samples and
direct feeding observations. Faeces were systematically collected between October 1997 and
Chapter 224
July 2002 from both wild and reintroduced bears, with sun bear scats being clearly identifi-
able due to their scent, texture and size. Collection occurred along transects and trails that
intersected the home ranges of three wild radiocollared female sun bears, monitored between
1999 and 2001, and at specific sites where these bears were located by triangulation. Randomly
located scats from unmarked wild bears were collected as well throughout the forest when-
ever encountered. Scats from three captive-reared bears that were radiocollared and gradually
reintroduced into the forest were also collected. Scats from these bears were included only
after they had been acclimated to living in the forest for at least 6 months.
All faecal samples were weighed and washed through a 0.2 mm mesh-sized sieve and
dried in the sun. Identification of seeds, and seedlings after germination trials, were done
by the Wanariset Herbarium. Scat contents were sorted into a five main categories i) fruit
(whole or broken seed counts), ii) flowers, iii) insects, iv) pith (meristem), v) debris (termite
nest remains; wood; resin). A visual estimate was made of the relative volume of each cat-
egory. To calculate the frequency of occurrence of fruit in scats for each month, the running
mean was calculated for three consecutive months. This was done as fruit scats collected in a
given month could be up to several weeks old when collected, representing fruits eaten that
month or the month before. Secondly, faecal data collected late in the month, might be more
comparative with the fruit situation for the following month, as phenology data was collected
towards the end of each month. Faecal samples were collected in all but five out of 57 months
of scat collection.
Direct feeding observations were obtained on a regular basis from reintroduced bears
as well as ad libitum from wild sun bears. Reintroduced bears were habituated for visual ob-
servations and twice a week observations of each bear were carried out. Data collection from
observations was continuous, and time of initiation and termination of each activity recorded.
Bears were observed on average 7.0 ± 1.5 hours during observation days (n=711), approxi-
mately 50% of their active hours in a day (G.M. Fredriksson, unpubl. data). During foraging
observations we recorded the total time handling a food source (e.g. foraging in or around
a fruiting tree, or handling a termite nest), as well as actual time spent feeding on that food
source (how much time spent actually swallowing food), and which part of a food item was
eaten (e.g. pulp, seeds, exocarp). With larger food items (e.g. large fruits), the exact number
of items consumed was recorded. Samples were collected of all food items for subsequent
identification. Data from the initial 6-8 months of observations were not used for data analyses
here, because during this time released bears still received supplementary foods. The period
of direct observations used for analysis spanned 31 months from October 1998–April 2001.
Phenological influences on sun bear frugivory 25
Classification of fruiting types and spatial distribution
of sun bear fruit species
The flowering and fruiting patterns of all trees combined, and separate species/genera,
were classified according to timing and frequency of flowering and fruiting events. The ‘mast
fruiting’ period was defined as the period where fruit production was 1.96 standard deviations
above the mean, following the definition for mast fruiting proposed by Wich and van Schaik
(2000). When all fruiting events of a species occurred during this mast fruiting period, the spe-
cies was categorized as a ‘mast-species’. When fruiting frequency was >1 /yr the species would
be categorized as ‘sub-annual’, when it fruited once a year it was classified as ‘annual’, and when
fruiting occurred less than once a year, but not during mast fruiting periods, it was classified as
‘supra-annual’ (following Sakai et al., 1999). When a species included individuals of more than
one fruiting type, we assigned the fruiting type of the majority of individuals as the fruiting type
for this species.
We use the term ‘fruiting event’ to describe a tree with fruit during one monthly
observation period or several consecutive observation periods. The term ‘sun bear food tree’
refers to trees from species that were found to occur in the diet of the sun bear. The distribu-
tion of sun bear fruit species among topographical types was determined by classifying all trees
(≥ 10 cm dbh) from the ten 0.1 ha phenology plots into sun bear food and non-food species,
and calculating the percentage of sun bear food trees for each topographical type.
Data analysis
Two analyses were performed to evaluate the temporal pattern of fruiting events. First
an index of aggregation, Morisita’s Index, Id, (Morisita, 1962), independent of sample size, was
calculated based on temporal distribution of fruiting events for 17 three-month periods (sensu
Sakai et al., 1999) from January 1998 to July 2002. Id is near 1 in distributions that are essen-
tially Poisson, >1 in clumped distributions, and <1 in cases of regular or seasonal reproduction
(Morisita, 1962; Krebs, 1999). Second, a χ2 test for goodness of fit was performed to examine
whether the observed distribution of fruiting events significantly deviated from random distri-
bution. This test was performed assuming that fruiting events occurred at random throughout
the 17 three-month periods (when sample size of fruiting events was ≥70) or 8 six-month
periods (when sample size of fruiting events was between 35-69) as the expected number of
fruiting events in a unit period (3 or 6 mo) must be five or more (Sokal and Rohlf, 1981). These
two analyses were conducted on separate genera important in the diet of the sun bear, as well
as for all trees monitored for their monthly phenology combined.
Chapter 226
To test for differences in number of trees fruiting between periods, the study period
was divided into four periods of 12 months starting May ’98, after the first mast-fruiting event.
Kruskal-Wallis one-way analyses of variance and Chi-squared tests were applied to test for dif-
ferences between periods, and habitat types with significance levels set at p=0.05. When multi-
ple comparisons between treatments were conducted (Siegel and Castellan, 1988), Bonferroni
techniques were applied to limit overall experiment-wise error (Sokal and Rohlf, 1981). All
values reported are mean ± 1 standard deviation (SD) and statistical analyses were performed
with Sigma Stat 1.0.
Results
Temporal variation in fruiting phenology
Mean percentage of all trees fruiting in the ten 0.1-ha plots over the 53 months (Jan ’98-
July ’02) was 2.4 ± 3.4 %; masting was thus defined as >9.1% of trees fruiting (2.4 + [1.96*3.4])
Two distinct mast-fruiting peaks lasting 2 months each were discerned, with the first in pro-
gress at the start of data collection in January-February 1998, and a second peak almost four
years later, during November-December 2001 (Fig. 2). Both masting events took place during
ENSO episodes (NOAA-CIRES, 2003).
During the first masting event, 15.7 % of trees (86 of 549) fruited, and during the sec-
ond 10.3 % of trees (49 of 474) carried fruit. During the inter-mast period, fruit production av-
eraged 1.6 ± 0.6 % of trees fruiting ha-1 month-1. Fruit production differed significantly between
years (years 1-4 in Fig. 2A), following the 1998 masting event (Kruskal-Wallis, H=18.1 df=3,
p<0.001). Fruit production was significantly lower in the first two years (April 1998-March
2000) than in the fourth year (April 2001-March 2002) (Dunn-Šidák, Q>3.6, p<0.05 for both
years).
In the ten 0.1-ha plots, 26.2% of trees (144 of 549) were species encountered in the
diet of sun bears, although only 37% (53 of 144) of these trees were reproductively active
during the study, representing 9.7% of all trees (≥10 cm dbh) found in 1 ha. From these 53
reproductively active sun bear fruit trees, 128 fruiting events were recorded over 53 months
of monitoring, with 52 events (40.6%) during the two masting events (4 months). During mast
fruiting months, 13.0 ± 2.2 sun bear fruit trees ha-1 month-1 fruited, whereas during the inter-
mast interval only 1.6 ± 1.8 sun bear fruit trees ha-1 month-1 produced fruit. In the first two
years after the 1998 masting event fruiting by sun bear tree species was very low with only
Phenological influences on sun bear frugivory 27
Figure 2. A. Temporal changes in fruiting phenology of trees (≥10 cm dbh, n=549) from ten 0.1-ha plots,
showing two mast fruiting events. B. Fruiting phenology of selected sun bear fruit trees (n=104, data set II),
mast and non-mast species combined. Horizontal line indicates the threshold above which masting is defined
to occur.
0.6 ± 0.8 sun bear fruit trees ha-1 month-1 producing fruit. In the third year fruiting increased to
2.5 ± 2.1 sun bear fruit trees ha-1 month-1 producing fruit.
Fruiting by selected sun bear fruit trees (second phenology data set) also differed sig-
nificantly over years (Kruskal-Wallis, H=14.8, df=3, p=0.002), with three years after the 1998
masting event having lower fruit production than the fourth year (Dunn-Šidák, Q>2.8, p<0.05
Chapter 228
for all years) (years 1-4 in Fig. 2B). Fruit production was almost absent in the first year following
the 1998 mast fruiting event. Mean percentage of sun bear trees fruiting, over the 53 months
was 8.9 ± 10.2 %; hence, mast-fruiting for these was defined as when >29 % of trees under
observation were fruiting. Two distinct mast-fruiting peaks for these selected sun bear trees
coincided with the two mast fruiting events among all trees (Fig. 2).
Three times during the study period did temperature drop below the ‘critical’ value of
21ºC, proposed as the low night-time temperature threshold triggering the onset of general
flowering (Ashton et al., 1988). Each of these minima lasted only one night and lowest tempera-
ture recorded was 20.7 ºC (July ’02). These minor drops in temperature did not correlate to
a subsequent onset of general-flowering. The temperature drop in July 2002 occurred when a
smaller general flowering event was already well under way.
Fruiting patterns and types
In total, 639 fruiting events were recorded from all trees (n=549) in the ten 0.1 ha plots
(Table 1). More than half of these fruiting events (330 of 639; 51.6%) were concentrated dur-
ing the mast-fruiting periods. Fruiting events were significantly clustered over 3-month periods
(Table 1) (Id=2.52, χ2=946.9, df=16, p<0.001). A high proportion of trees (61.4%) were never
observed to fruit during the study period (Table 1). The most common fruiting type in the plots
was mast-fruiting (16.4% of trees), followed by supra-annual fruiting pattern (14.4% of trees).
Only 2 % of trees displayed an annual fruiting pattern and 5.8% of individuals a sub-annual pattern.
Among 104 sun bear trees that we monitored, 378 fruiting events were recorded.
These were also found to be clustered over 3-month periods (Id=1.77, χ2=363.6, df=16,
p<0.001). Several species/genera displayed highly clumped fruiting patterns (Durio spp., Artocar-
pus integer, Dacryodes spp., Ochanostachys amentaceae) (Table 1). Intermediate fruiting patterns
were observed for Tetramerista glabra and Santiria spp. The former species had significantly
lower number of trees fruiting though in the first 18 months after the 1998 masting and ENSO
event than in the subsequent 18 months (Mann-Whitney U Rank Sum test: Mean rank 1=14.3,
Mean rank 2=22.7, n=36, Z=-2.614, p=0.017).
The lowest index of aggregation (most random fruiting) was found in Ficus spp. Mono-
carpia kalimantanensis had the second lowest index of aggregation, but fruiting was not ran-
domly distributed (Id=1.07, χ2=19.72, df=11, p<0.05) (Table 1). Mean dbh of selected sun bear
fruit trees was larger (44.7 ± 21.1 cm) than the mean dbh of all monitored trees in the 0.1-ha
plots (21.1 ± 14.3 cm) (Mann-Whitney U Rank Sum test: Mean rank1=501, Mean rank 2=285,
n=617, Z=9.4, p<0.001). Still, 31.7% of these selected sun bear fruit trees were never observed
Phenological influences on sun bear frugivory 29
Tabl
e 1.
Mor
isita
inde
x an
d fr
uitin
g pa
tter
ns fo
r th
e 1
ha p
heno
logy
plo
ts (≥1
0 cm
DBH
) an
d fo
r m
ain
sun
bear
frui
t ge
nera
/spe
cies
.
Frui
ting
patt
ern
N
(mon
ths)
N
(tre
es)
N (
frui
ting
even
ts)
Mor
isita
in
dex
(I d)χ2
Non
-fru
iting
Mas
t-Fr
uitin
gSu
pra-
annu
alA
nnua
lSu
b-an
nual
1) P
heno
logy
plo
ts (
1 ha
) al
l tre
es c
ombi
ned:
5354
963
92.
52**
*61
.4a
16.4
14.4
25.
8
Bear
food
spe
cies
5314
412
82.
35**
*63
.113
.218
.80.
74.
2
Non
-bea
r fo
od s
peci
es53
405
511
2.55
***
60.8
17.5
12.8
2.5
6.4
2) S
elec
ted
frui
t tr
ees
(sec
ond
data
set
):52
102
378
1.77
***
31.7
34.6
10.6
2.9
20.2
Arto
carp
us in
tege
r52
1044
5.69
***
10b
Dac
ryod
es r
ostr
ata
and
D. r
ugos
a52
2144
6.72
***
119
1
Dur
io d
ulci
s an
d D
. oxl
eyan
us52
2232
4.69
-10
12
Ficu
s sp
p.38
1129
0.99
-2
32
4
Mon
ocar
pia
kalim
anta
nens
is37
1011
81.
07*
11
8
Och
anos
tach
ys a
men
tace
ae53
109
5.19
-4
51
Sant
iria
spp.
2510
82.
32-
54
1
Tetr
amer
ista
glab
ra52
1094
2.06
***
11
8
‘-’ =
too
sm
all s
ampl
e si
ze; *
indi
cate
s p
=0.
05; *
** in
dica
tes
p<0.
001;
a=
% o
f tre
es; b
=no
of t
rees
Chapter 230
fruiting. Based on the majority of observations, taxa were divided into those only found fruiting
during masting events (mast species: Durio spp., A. integer, Dacryodes spp., and O. amentaceae)
and those that also fruit during inter-mast periods (non-mast species: Ficus spp., Santiria spp.,
T. glabra, and M. kalimantanensis) (Table 1).
Faecal analyses
A total of 1209 sun bear scats were collected (77 between Oct 1997-April 1998, 280
in the first year after the 1998 mast (May 1998-April 1999), 305 in second year, 391 in the
third year, 137 in the fourth year, and 19 in May-June 2002). Fruit remains were encountered
in 58.5% of faecal samples (706 of 1209), and in 46 of 52 months (88.5%) that scats were col-
lected. Insect remains (primarily termites) were encountered in 75.4% of scats (911 out of
1209). Among all 706 fruit scats, most (74.2%) contained remains of one fruit species, 20.8%
contained two species, 4.2% contained three, and 0.7% contained four species of fruit. Of 706
scats collected with fruit remains, 40.4% (238) contained 100% fruit.
Remains of 83 distinct fruit species belonging to 39 genera in 23 different families were
identified in sun bear scats. The most common genera encountered in scats were Ficus spp.
(23.2% of scats), Dacryodes spp. (12.5% of scats; D. rugosa and D. rostrata combined), Syzigium
spp. (12.3% of scats) and Santiria spp. (11.2% of scats) (Appendix I). Bears primarily fed on
fruits from trees (60% of identified species) with remaining fruit species being primarily from
monocots (Appendix II). Only 4 species of liana were positively identified to be consumed by
sun bears and liana fruit resources made up <1 % of fruit scats.
Moraceae was the most species rich family occurring in the diet of sun bears, with 14
species, followed by Palmae which featured with 10 species (Appendix II). The family Euphor-
biaceae, which dominated in the phenology plots (21.4% of stems ≥ 10 cm dbh), featured with
only 4 species in the diet, three of which were Baccaurea spp. (Appendix II). The 11 selected sun
bear fruit tree taxa monitored for their phenology were encountered in 66.1% of fruit scats,
indicating their importance in the fruit diet of sun bears.
Frequency of occurrence of fruit in scats differed between years (Fig. 3) (Kruskal-Wallis
H=23.0, df=3, P<0.001). The first year after the 1998 mast had significantly lower occurrence
of fruit than the three subsequent years (Dunn-Šidák, Q>3.1, p<0.05 for all years). Sun bears
appeared to be almost entirely frugivorous during the two mast-fruiting events (fruits found
in 73 of 74 scats and 83 of 85 scats, respectively). Sun bears primarily fed on mast fruit spe-
cies during the short period when they were available (Fig 4), ignoring the ‘non-mast’ species,
although these also had higher fruiting activity during the masting events, possibly indicating a
Phenological influences on sun bear frugivory 31
Figure 3. Frequency of occurrence of fruit in scats (n=706 out of 1209) based on running mean of 3 con-
secutive months.
Figure 4. Faecal samples containing fruit remains divided into mast and non-mast species (706 of 1206
scats collected). Bars indicate scats containing mast fruit species, lines indicate scats containing non-mast fruit
species. Most scats collected in the first year contained insect matter.
Chapter 232
preference for the mast species. By contrast, fruits were nearly absent in the diet of sun bears
for a period of 12 months following the 1998 masting event (Fig. 4). All sun bear scats collected
during this first post ENSO/mast period primarily contained insect remains.
Temporal variation in use of fruit resources
Based on faecal samples collected between Oct 1997-July 2002, the family Moraceae
dominated the fruit diet of sun bears (26% of fruit scats), followed by Burseraceae (19%),
Myrtaceae (9%), Annonaceae (8%), Palmae (8%), Tetrameristaceae (6%), and Bombacaceae (3%).
The importance of various fruit families, genera, and species varied substantially over seasons
and years (Fig. 5 and Fig. 6). In the first year, incorporating the first mast-fruiting event, the
main plant genera in the diet were Artocarpus (Moraceae), Dacryodes (Burseraceae), and Durio
(Bombacaceae). Sun bears consumed copious amounts of these, mostly large seeded (up to 45
mm), fruits. For example, a single scat could contain >400 Dacryodes rugosa seeds (seed length
15 mm; max scat weight 400 gr).
In the second year, with the lowest overall fruit availability, Ficus (Moraceae) was the
dominant genus. Figs were the most frequently occurring fruit genus encountered in scats
throughout the study period (164 of 706 fruit scats), and also occurred in 58.7% of months that
scats were collected. Still, occurrence of scats containing fig remains were clumped temporally
(Id=1.96, χ2=170.7, df=14, p<0.001). After the 1997-98 ENSO figs hardly featured in faecal sam-
ples for a period of 12 months. No correlation was found between number of fruiting fig trees
and number of scats encountered each month with fig remains (Spearman Rank Correlation:
R2=0.22, p=0.193, n=37).
A number of taxa from the Palmae family also featured in the diet during these periods
with extreme fruit lows (viz., Oncosperma horridum, Borassodendron borneensis, Polydocarpus sp.,
the rattans Calamus spp., Daemonorops spp., Korthalsia spp.). Fruits of O. horridum, clusters of
small hard drupes, were encountered in 49 scats.
Certain species in the family Annonaceae were also found to be important for sun
bears during the inter-mast period. Two unidentified species of Polyalthia with large (up to 55
mm) fatty fruits were frequently encountered in scats (51 of 706) in the third year of the study,
whereas Polyalthia sumatrana, which reaches high densities in the forest, was not encountered
in scats at all. Fruits of Monocarpia kalimantanensis, though available throughout most of the
study period, were only consumed during the fruit low period.
In the third year Ficus spp., Santiria spp. and Tetramerista glabra dominated the fruit diet.
In the fourth year Syzigium spp. dominated the fruit diet and to a lesser extent figs. The ginger
Phenological influences on sun bear frugivory 33
Hornstedtia cf. reticulata (Zingiberaceae) also appeared in scats. In the fifth year Dacryodes spp.
and Durio spp. were again consumed copiously during the masting event, followed by Santiria
spp. (post masting event) (Fig. 5).
Figure 5. Annual fluctuations in contribution of main plant genera to the sun bear diet. The category ‘rattan’
covers several genera.
Figure 6. Annual changes in contribution of plant families to the sun bear diet.
Chapter 234
Direct feeding observations
From direct observations (n=4977 hours) sun bears were found to feed on fruits for
10.3 ± 4.3% of their feeding time (n=3 bears), although the observation period did not include
the mast fruiting events. Remaining feeding time was primarily spent on insect matter (termites,
ants, beetle larvae, cockroaches, stingless bees), as well as small quantities of flowers and veg-
etative matter. Although relatively little time was spent feeding on fruits, sun bears were still ob-
served to feed on fruits on 43.3 ± 6.0% of days that observation were carried out (n=711 days).
We directly observed 568 fruit feeding events during which bears fed on at least 58 dif-
ferent fruit species of 30 genera and 20 families (Appendix II). Plants of 62 fruit-feeding events
remained unidentified. Sun bears mainly fed on fruits that had dropped to the forest floor,
and trees were only climbed in 25.4% of fruit-feeding events (144 of 568). Average diameter
of trees climbed by sun bears for fruit feeding was 33.6 cm dbh (range 5-150 cm). The three
main genera observed to be fed upon during direct observations almost make up 50% of fruit
feeding time (Appendix I).
Several fruit species which rank high in occurrence from scats, especially mast fruiting
species, were not observed to be fed upon during direct observations (Appendix I), as the
observation period did not cover the masting events. The genus Litsea (Lauraceae) ranks fourth
in frequency during direct observations but was rarely found in scats. This is probably due to
the fact that seeds from these fruits are soft and were probably destroyed during feeding, with
few remains of Litsea spp. identified in scats. Fruits of the palm Borassodendron borneensis were
relatively frequently observed to be fed upon by the bears (ranking ninth), although this pri-
marily constituted of chewing on the fibres which surround the extremely hard endocarp. In
scats one would occasionally encounter fibres, which in most cases remained unidentified. The
total number of different fruit species fed upon by sun bears, from both scats and observations
combined was at least 115, belonging to 54 genera in 30 families (Appendix II).
Fruit resources in relation to topographical types
Fruit feeding observations were found unevenly distributed over topographical types
when looking at their relative availability (χ2=476.6, df=4, p<0.001). More fruit-feeding was ob-
served in swamp (χ2=429.5, df=1, p<0.001) compared to the other topographical types com-
bined, and significantly less fruit feeding observations in slope habitat (χ2=106.1, df=1, p<0.001)
than expected. Actual fruiting events by sun bear fruit trees, derived from the ten 0.1 ha phe-
nology plots, were also found unequally distributed among topographical types (χ2=35.1, df=4,
p<0.001), with more fruiting events in swamp (χ2=13.1, df=1, p<0.001) and ridge topographical
Phenological influences on sun bear frugivory 35
type (χ2=11.6, df=1, p<0.001) compared to all other topographical types combined, and less
fruiting events in high-flat topographical type (χ2=10.4, df=1, p<0.01) than expected (Table 2).
The distribution of fruit feeding observations in relation to actual fruiting events (fruit pro-
duction) in the different topographical types was also unequally distributed (χ2=417.9, df=4,
p<0.001). Despite a high number of fruiting events, ridge topographical type was significantly
less used (χ2=206.9, df=1, p<0.001) compared to all other topographical types combined. More
fruit feeding observations where observed in high-flat (χ2=170.4, df=1, p<0.001) and slope
habitat (χ2=115.3, df=1, p<0.001) than expected from the number of actual fruiting events
(Table 2).
Discussion
Fruiting phenology in Sungai Wain was highly aseasonal and fluctuated largely between
years. The majority of reproductive fruit trees used by sun bears displayed a supra-annual or
mast fruiting pattern, indicating that fruit production by species occurring in the diet of the sun
bear is irregular and consists of a short boom and prolonged bust situation. Two mast fruit-
ing events that occurred during the 53 month of observations were spaced four years apart,
Table 2. Chi-square test results of the distribution of sun bear fruit feeding observations and fruiting events
of sun bear fruit trees in relation to availability of topographical types.
Topograph-ical types
Availability topogr. types
aSun bear fruit trees
bFruiting events sun bear fruit
trees
cFruit feeding observations
% ± SD no of fruit trees
no of fruiting events
χ2 no of obs χ2 FFO vs ATT
χ2 FFO vs FE
Swamp 5.9 ± 4.6 40 42 ** > 150 * > * <
Alluvial 17.3 ± 4.0 39 21 125 * >
High-flat 24.8 ± 9.3 14 11 * < 136 ** >
Slope 45.3 ± 9.1 28 13 135 * < ** >
Ridge 6.7 ± 2.7 23 41 ** > 22 ** <
Total 144 128 568
aNumber of sun bear fruit trees in ten 0.1 ha phenology plots (0.2 ha/topographical type); bNumber of fruiting events from sun bear trees in phenology plots between Jan 1998-July 2002; cNumber of fruit feeding observations during 711 days of observations; FFO= Fruit Feeding Observations; ATT= Availability of topographical types; FE = Fruiting Events; * p<0.01; ** p<0.001; > indicates more than expected; < indicates less than expected
Chapter 236
falling well in the ~2-10 year interval that has been reported for other sites in Southeast Asia
(Medway, 1972; Appanah, 1985; Ashton et al., 1988, Curran and Leighton, 2000; Wich and van
Schaik, 2000; Sakai, 2002; Marshall, 2004). During the two masting events 15.7% and 10.3% of
trees respectively produced fruits. This coincides with the figure reported by Sakai et al. (1999)
for ‘general flowering’ when >10% of individuals under observation were flowering in Sarawak
(Malaysian Borneo).
A combination of exhausted energy reserves from mast fruiting species, and possibly
disrupted fruiting patterns of inter-mast fruit resources resulted in a prolonged period of fruit
scarcity. Fruit production slowly built up over 4 years to the second masting event. Both mast-
ing events took place during ENSO episodes (NOAA-CIRES, 2003). The strong influence of
ENSO events in East Kalimantan can also be witnessed from prolonged droughts and associ-
ated forest fires that repeatedly affect the region (Leighton and Wirawan, 1986; Hoffman et al.,
1999; Siegert et al., 2001). No temperature drop, proposed as a potential trigger for general
flowering (Ashton et al., 1988; Yasuda et al., 1999), was observed in the ~2 months preceding
general flowering in 2001, indicating that possibly other factors play a role in the onset of mass-
flowering (see Corlett and LaFrankie, 1998).
Over the ~5 years study period sun bears were found to feed on a large variety of
fruits (115 species). Although 60% of scats collected contained fruit remains sun bears were
found to spend only 10% of their feeding time on fruits during direct observations. The remain-
der of feeding time was spent on invertebrates. This discrepancy could be due to two factors.
Firstly, decay rates of scats containing primarily insect remains are much quicker than those
containing fruit remains. Insect scats disappear within 24 hours due to dung beetle activity,
whereas fruit scats remain visible up to 3 weeks (G.M. Fredriksson unpubl. data). This indicates
that studying the diet of sun bears based on faecal analysis alone could strongly bias the results
towards frugivory. On the other hand, most fruits are large compared to insects and during a
short fruit foraging session large quantities of fruits can be consumed, the remains of which
can be expelled in several scats.
During mast fruiting events sun bears were found to be almost purely frugivorous.
Mast fruiting species fed upon by sun bears produce succulent fleshy fruits, and are probably
important in the ecology of sun bears for building up energy reserves or restoring lost energy
reserves for the prolonged inter-mast periods when few fruit resources are available. The main
sun bear mast fruit genera (Durio spp., Dacryodes spp., and Artocarpus spp.) have high energy,
protein, fat and potassium values (Voon and Kueh, 1999). The ability to store large amounts
of energy as fat to survive periods of food shortages is well developed in bear species living
Phenological influences on sun bear frugivory 37
in temperate regions, where bears hibernate during winter. Orangutans, which occur sympa-
trically with sun bears throughout much of the lowland forests in Sumatra and Borneo have
substantial dietary overlap with sun bears (Galdikas, 1988; Leighton, 1993; Knott, 1998; G. M.
Fredriksson, unpubl. data), at least on Borneo. Orangtans in West Kalimantan were found to
gorge themselves during a masting event on non-dipterocarp fruits and consumed 2-3 times
the amount of calories needed for daily energy requirements, putting on fat reserves (Knott,
1998). Subsequently, during the inter-mast period orangutans were living off these stored re-
serves and loosing weight (Knott, 1998). Sun bears in East Borneo appear seriously affected
by prolonged fruit scarcity with potentially elevated mortality due to predation (Fredriksson,
2005) or starvation (G.M. Fredriksson, unpubl. data; Wong et al., in press). Most of the mast
species consumed by sun bears and orangutans are higher in caloric content than non-mast
fruits (Leighton, 1993; Knott, 1998; Voon and Kueh, 1999; G.M. Fredriksson, unpubl. data). This
might explain why intermast species were not consumed by bears during the mast period, even
though many of these also produced larger crops during general masts.
Densities of large strangling figs in Sungai Wain are low, but small hemi-epiphytic figs,
producing minor fruit crops, are relatively abundant (G.M. Fredriksson unpubl. data). Despite
the scarcity of large stranglers, figs were the most commonly consumed fruit genus by sun
bears during the prolonged intermast period, witnessed both from scats and direct observa-
tions. Although figs are low in overall energy value compared to many of the mast fruit spe-
cies, they contain high protein and calcium values (O’Brien et al., 1998; Voon and Kueh, 1999).
Figs also displayed the most random fruiting pattern and were the most frequently available
fruit genus. Probably due to the combination of these factors, figs appear one of the main fall-
back fruit resources for sun bears, as for a variety of other wildlife in the Southeast Asia (e.g.
Leighton and Leighton, 1983; Sugardjito et al., 1987; van Schaik, 1996; Kinnaird et al., 1999). Figs
are also encountered in the diet of several other bear species inhabiting (sub) tropical regions
(e.g. Sloth bear Melursus ursinus, Joshi et al., 1997; Asiatic Black bear Ursus thibetanus, Hwang et
al., 2003; Spectacled bear Tremarctos ornatus, Peyton, 1980).
In the first year after the strong ENSO, few scats with fig remains were encountered
even though fruiting by all other intermast species was negligible. An increase in fig consump-
tion was only observed after May 1999 (13 months after the ENSO event). Monitoring of fig
phenology commenced in June 1999, after which fig fruits appeared available on a continuous
basis. Harrison (2001) reported that flower and fruit production of dioecious figs decreased or
even ceased after the 1997-98 ENSO drought in Sarawak (Malaysian Borneo). Under normal
conditions figs produce fruits all year round in order to maintain species-specific pollinator
Chapter 238
relationships with fig wasps which have a short live span (Harrison, 2001; Shanahan et al., 2001).
Fig wasps became locally extinct after the ENSO event and for some fig species took more
than two years to recover (Harrison, 2001). Although monoecious figs in Sarawak did not suf-
fer extinction of pollinators, Harrison (2001) found that pollination rates were lower after the
ENSO drought for some of these (e.g. F. benjamina). It is therefore possible that sun bears hard-
ly consumed figs in the first year after the ENSO event, as simply fewer fig fruits were available.
Fruit production of Tetramerista glabra, another important intermast fruit resource, also
appeared disrupted after the 1998 ENSO event. This species normally produces fruit year round
(Soerianegara and Lemmens, 1993), but after the 1998 mast T. glabra only became available again
in early 2000. Although T. glabra featured in only 8% of fruit scats, most large trees of this spe-
cies in Sungai Wain are covered with multiple-age claw marks, indicating frequent and repeated
usage by sun bears. T. glabra has been identified as an important fruit species during lean periods
for orangutans (Singleton and van Schaik, 2001) and bearded pigs (Curran and Leighton, 2000).
During the initial period post-ENSO, when fruits like Ficus and T. glabra were virtually
absent, various fruits from the Palmae family featured in the bear diet. Although few palms were
included in the monthly phenology, our general observations suggested that many species in
the palm family displayed a continuous fruiting pattern. Many fruits in the Palmae family are rich
in oils and carbohydrates and have been found to be important food for primates in Southeast
Asia during food lean periods (Lucas and Corlett, 1991). Fruits of the ginger Hornstedtia cf.
reticulata started appearing in the diet after 2001. Densities of this ginger species increased
substantially in later stages of the study (G.M. Fredriksson, pers. obs.), probably due to increased
light conditions at the forest floor level, following elevated mortality of large trees after the
1998 ENSO drought (van Nieuwstadt, 2002).
Acorns (Lithocarpus spp. and Quercus spp. Fam. Fagaceae), popular in the diet of several
other bear species (Asiatic black bear: Huygens and Hayashi, 2001; Hwang et al., 2003; American
black bear Ursus americanus, Inman and Pelton 2002) were rarely encountered in the diet of
sun bears at this lowland site, despite a relatively high density of these genera. On the other
hand, half of scats collected in the mountainous interior of Borneo during other surveys, con-
tained acorns remains (G.M. Fredriksson, unpubl. data), in accord with Davies and Payne’s (1982:
91) statement that sun bears ‘feed on large quantities of the hard seeds of the Fagaceae family’.
It is possible that sun bears living at higher elevations feed more on oaks because densities
of species with succulent fruits decrease rapidly at higher altitudes (Djojosudharmo and van
Schaik, 1992), whereas Fagaceae increase in density (Pendry and Proctor, 1996).
Interestingly, sun bears were found feeding more on fruits in high-flat forest type, com-
Phenological influences on sun bear frugivory 39
pared to other topographical types, despite lower fruit production. This could be due to the fact
that sun bears used this forest type more intensively because insect food resources reach higher
densities in this drier forest type (G.M. Fredriksson unpubl. data). Sun bears focus on the more
stable invertebrate food resource during the intermast period, opportunistically feeding on
fruits encountered whilst foraging for insects, making the overall foraging strategy more efficient.
Conversely, sun bears spent less time feeding on fruit resources in ridge topographical types
despite the fact that fruit productivity was higher than expected. Ridge tops are disproportion-
ally used by humans for travel through the forest. In Sumatra, Griffiths and van Schaik (1993)
found that sun bears switched to a more nocturnal activity pattern in areas of high human usage,
and although at this study site sun bears remained diurnal (G.M. Fredriksson unpubl. data), it is
possible they spatially avoided this topographical type due to higher levels of human passage.
Overall at this lowland study site, three plant families (Moraceae [26%], Burseraceae
[19%], and Myrtaceae [9%]) made up more than 50% of the sun bear fruit diet throughout the
study period. The density and distribution of these genera could be a contributing factor to
regional differences in sun bear densities, and conservation of fruit trees from these genera
should be incorporated in forest management practices as they contribute disproportionately
to the diet of sun bears.
In order to obtain a comprehensive picture concerning which fruit resources are im-
portant in the diet of sun bears it is essential to carry out long term observations, taking into
account the multi-year phenological cycles observed in Sundaic forests. The proportional rep-
resentation of various food items depended heavily on the overall phenological status of the
forest during the sampling period. During the initial stages of this study it appeared that sun
bears were pure frugivores, though if the study would have commenced several months later,
sun bears would have appeared primarily insectivorous.
From our analysis a picture emerges of the general feeding ecology of sun bears. They
are adaptable and easily switch to more nutritious resources whenever these become avail-
able, while they appear able to effectively store fat and thus survive during periods of low food
availability. Sun bears share these traits with other large frugivores and omnivores in island
Southeast Asia, such as the orangutan (Leighton and Leighton 1983; Knott, 1998) and bearded
pig (Caldecott, 1988). We speculate that these species have evolved these traits in response to
the specific ecological challenges posed by an environment dominated by supra-annual periods
of low food availability interspersed by brief periods of glut. To test this it is interesting to
compare the evolution of sun bears with its nearest relatives in mainland Southeast Asia, where
such intra-annual cycles are less dominant.
Chapter 240
The taxomic classifcations and phylogenetic relationships within the Ursidae remain
subject to controversies. The main problem being that the family Ursidae represents a typical
example of rapid evolutionary radiation and recent speciation events, dating back to mid-
Miocene about 6-8 Mya (Kurtén, 1968; Goldman et al., 1989; Talbot and Shields, 1996; Waits et
al., 1999; Yu et al., 2004). Previous phylogenetic studies placed the sun bear as a sister taxon to
the youngest diverging clade, containing brown bears and polar bears (e.g. Talbot and Shields,
1996; Waits et al., 1999). A more recent analysis, based on nuclear DNA (Yu et al., 2004) and
morphology (Sacco and van Valkenburgh, 2004) provides strong support for the sun and sloth
bear being sister taxa. This seems more reasonable from the morphological standpoint, the
sloth bear and sun bear being Asian subtropical or tropical species, markedly distinguished
from other bears, including the sympatric Asiatic black bear, by their morphological and be-
havioral specialization which are likely due to recent adaptive change (Hall, 1981; Nowak and
Paradiso, 1983; Goldman et al., 1989).
The sun bear, which is the only bear species living in island Southeast Asia, probably di-
verged between 4 and 2.5 mya from the other species of Southeast Asia (see Talbot and Shields,
1996; Waits et al., 1999). It remains unclear what caused the rapid split between these species,
although Meijaard (2003; 2004b) hypothesized a vicariance model in which the ancestral sun
bear became isolated in what is now Sundaland. By that time, the rising Himalayas had resulted
in increasing dry Asian climates and stronger monsoonal patterns, causing a change in the veg-
etation of this region (Morley, 2000). It is possible that by the time sun bears evolved in Sunda-
land they did so in an environment more and more affected by supra-annual fruiting patterns.
Did these environmental conditions shape the present-day ecology of Bornean sun bears?
The closest relative of the sun bear, the sloth bear (Yu et al., 2004), currently ranges
from Nepal south through India and Sri Lanka and is the ursid species most specifically adapted
to feeding on insects (Laurie and Seidensticker, 1977; Joshi et al., 1997). Laurie and Seidensticker
(1977) speculated that the sloth bear was able to enter the myrmecophagous niche as com-
petitors that feed on insects are allopatric in sloth bear habitat.
For the sun bear it might not have been an option to evolve into the insectivorous niche
due to a number of sympatrically occurring myrmecophages (pangolins: Manis spp.), nor to
evolve into a more carnivorous niche due to the presence of several more efficient feline com-
petitors, and a relatively low prey biomass in Southeast Asia (Meijaard, 2004a). Hence, the sun
bear appears to have evolved more in the direction of primates; being agile in trees and able to
access a variety of fruit resources when available, but also feeding substantially on insects, which
are the most stable food resource in tropical forests (see Kikkawa and Dwyer, 1992). The sun
Phenological influences on sun bear frugivory 41
bear has evolved a combination of morphological adaptations to exploit these two main food
resources in the tropical rainforest. Some of these useful for tree climbing like small body size
(weight between 27-65 kg [Lekagul and McNeely, 1977]), extremely long claws, naked soles, flat-
tened chest, and strongly inward curving feet (Pocock, 1941), but also several physical features
which are indicative of insect feeding such as the longest tongue among the ursids, mobile lips, a
nearly naked snout, huge canines (practical for opening hardwood in search for insects), and ex-
ceptionally large paws comparative to body size useful for digging up termites and ants, as well
as breaking into logs. They are thus well adapted to use a wide variety of resources in different
feeding strata. Additionally, the Bornean sun bear is significantly smaller than the Sumatran or
Malaysian/mainland sun bear (Meijaard, 2004b), possibly another adaptation linked to evolution
in the most nutrient poor part of Sundaland (see MacKinnon et al., 1996). All of these factors
combined make evolution of sun bears in the typical Sundaic environment a likely scenario.
AcknowledgementsWe thank the Indonesian Institute of Sciences (LIPI) for granting GMF permission to
carry out research on sun bears in East Kalimantan. GMF would like to express gratitude to
the Forest Research Institute in Samarinda for their assistance. The Tropenbos Foundation, the
Borneo Orangutan Foundation, and the Conservation Endowment Fund of the American Zoo
and Aquarium Association provided financial assistance. Dave Garshelis is thanked for logistical,
financial and technical assistance. The Wanariset Herbarium, especially Ambrianshyah and Arifin
are thanked for identification of plant samples. Field assistants Lukas, Damy and Adi are thanked
for various assistance in the forest throughout the years, as well as many people from the Sungai
Wain village. SBJ. Menken, D. Garshelis, V. Nijman and E. Meijaard are thanked for useful comments
of previous drafts. MJ Lammertink and G. Usher are thanked for the map. SAW was funded by
the Dutch Foundation for the Advancement of Science (NWO) while working on this paper.
Literature citedAppanah S. 1985. General flowering in the climax rain forests of South-east Asia. Journal of Tropical Ecology
1: 225-240.
Ashton PS, Givnish TJ, Appanah S. 1988. Staggered flowering in the Dipterocarpaceae - New insights into
floral induction and the evolution of mast fruiting in the aseasonal tropics. American Naturalist
132: 44-66.
Chapter 242
Berlage HP. 1949. Regenval in Indonesie. Koninklijk Magnetisch en Meteorologisch Observatorium te Ba-
tavia. Verhandelingen no. 37.
Caldecott J. 1988. Hunting and wildlife management in Sarawak. IUCN Tropical forest programme.
Conklin-Brittain, NL, Wrangham, RW, Hunt, KD. 1998. Dietary response of chimpanzees and Cercopith-
ecines to seasonal variation in fruit abundance: II. Macronutrients. International Journal of Primatol-
ogy 19: 949-970.
Corlett RT, LaFrankie JV. 1998. Potential impacts of climate change on tropical Asian forests through an
influence on phenology. Climatic Change 39: 439-453.
Curran LM, Caniago I, Paoli GD, Astianti D, Kusneti M, Leighton M, Nirarita CE, Haeruman H. 1999. Impact
of El Niño and logging on canopy tree recruitment in Borneo. Science 286: 2184-2188.
Curran LM, Leighton M. 2000. Vertebrate responses to spatiotemporal variation in seed production of
mast-fruiting dipterocarpaceae. Ecological Monographs 70: 101-128.
Davies G, Payne J. 1982. A faunal survey of Sabah. Kuala Lumpur, Malaysia: IUCN/WWF. 1-297.
Djojosudharmo S, van Schaik CP. 1992. Why are orang utans so rare in the highlands? Tropical Biodiversity
1: 11-22.
Fogden MPL. 1972. The seasonality and population dynamics of equatorial forest birds in Sarawak. Ibis 114:
307-341.
Foster MS. 1977. Ecological and nutritional effects of food scarcity on a tropical frugivorous bird and its
fruit source. Ecology 58: 75-85.
Fredriksson GM. 2002. Extinguishing the 1998 forest fires and subsequent coal fires in the Sungai Wain
Protection Forest, East Kalimantan, Indonesia. In Moore P, Ganz D, Tan LC, Enters T and Durst PB,
eds. Communities in flames: proceedings of an international conference on community involve-
ment in fire management. Bangkok, Thailand: FAO and FireFight SE Asia, 74-81.
Fredriksson GM. 2005. Predation on sun bears by reticulated python in East Kalimantan, Indonesian Bor-
neo. The Raffles Bulletin of Zoology 53:165-168.
Fredriksson GM, Nijman V. 2004. Habitat-use and conservation of two elusive ground birds (Carpococcyx
radiatus and Polyplectron schleiermacheri) in Sungai Wain protection forest, East Kalimantan, Indo-
nesian Borneo. Oryx 38: 297-303.
Galdikas BMF. 1988. Orangutan diet, range, and activity at Tanjung Puting, Central Borneo. International
Journal of Primatology 9: 1-35.
Goldizen AW, Terborgh J, Cornejo F, Porras DT, Evans R. 1988. Seasonal food shortage, weight-loss, and the
timing of births in saddle-back tamarins (Saguinus fuscicollis). Journal of Animal Ecology 57: 893-901.
Goldman D, Giri PR, O’Brien S. 1989. Molecular genetic-distance estimates among the ursidae as indicated
by one- and two-dimensional protein electrophoresis. Evolution 43: 282-295.
Phenological influences on sun bear frugivory 43
Griffiths M, van Schaik CP. 1993. The impact of human traffic on the abundance and activity periods of
Sumatran rain forest wildlife. Conservation Biology 7: 623-626.
Hall ER. 1981. The Mammals of North America. Wiley, New York.
Harrison RD. 2001. Drought and the consequences of El Niño in Borneo: a case study of figs. Population
Ecology 43: 63-75.
Hoffmann AA, Hinrichs A, Siegert F. 1999. Fire damage in East Kalimantan in 1997/98 related to land use
and vegetation classes: satellite radar inventory results and proposals for further actions: IFFM-
SFMP. 1-44.
Huygens OC, Hayashi H. 2001. Use of stone pine seeds and oak acorns by Asiatic black bears in central
Japan. Ursus 12: 47-50.
Hwang M-H, Garshelis DL, Wang Y. 2002. Diets of Asiatic black bears in Taiwan, with methodological and
geographical comparisons. Ursus 13: 111-125.
Inman RM, Pelton MR. 2002. Energetic production by soft and hard mast foods of American black bears in
the Smoky Mountains. Ursus 13: 57-68.
Janzen DH. 1974. Tropical blackwater rivers, animals, and mast fruiting by the dipterocarpaceae. Biotropica
6: 69-103.
Joshi AR, Garshelis DL, Smith JLD. 1995. Home ranges of sloth bears in Nepal: Implications for conserva-
tion. Journal of Wildlife Management 59: 204-214.
Joshi AR, Garshelis DL, Smith JLD. 1997. Seasonal and habitat-related diets of sloth bears in Nepal. Journal
of Mammalogy 78: 584-597.
Kikkawa J, Dwyer PD. 1992. Use of scattered resources in rain forest of humid tropical lowlands. Biotropica
24: 293-308.
Kinnaird MF, O’Brien TG, Suryadi S. 1999. The Importance of figs to Sulawesi’s imperiled wildlife. Tropical
Biodiversity 6: 5-18.
Knott CD. 1998. Changes in orangutan caloric intake, energy balance, and ketones in response to fluctuat-
ing fruit availability. International Journal of Primatology 19: 1061-1079.
Krebs CJ. 1999. Ecological Methodology. 2nd eds. Benjamin/Cummings.
Kunkun JG. 1985. Short information on Malayan sun bear in Indonesia. Asiatic Bear Conference, 67-69.
Kurtén B. 1968. The Pleistocene Mammals of Europe, Aldine, Chicago, MA.
Laurie A, Seidensticker J. 1977. Behavioural ecology of the sloth bear (Melursus ursinus). Journal of Zoology,
Lond 182: 187-204.
Leighton M. 1993. Modeling dietary selectivity by Bornean orangutans-Evidence for integration of multiple
criteria in fruit selection. International Journal of Primatology 14: 257-313.
Chapter 244
Leighton M, Leighton DR. 1983. Vertebrate responses to fruiting seasonality within a Bornean rain forest.
In: Sutton SL, Whitmore TC and Chadwick AC, eds. Tropical Rain Forest Ecology and Management.
Cambridge UK: Blackwell Scientific Publications. 181-196.
Leighton M, Wirawan N. 1986. Catastrophic drought and fire in Borneo tropical rain forest associated with
the 1982-1983 El Niño southern oscillation event. In: Prance GT, ed. Tropical rain forest and world
atmosphere. Boulder, Colorado, USA: Westview Press. 75-101.
Lekagul MDB, McNeely BA. 1977. Mammals of Thailand. Kurusapha Ladprao Press, Thailand.
Lucas PW, Corlett RT. 1991. Relationship between the diet of Macaca fascicularis and forest phenology. Folia
Primatologica 57: 201-215.
MacKinnon K, Hatta G, Halim H, Mangalik A. 1996. The ecology of Kalimantan. Periplus Editions Ltd., Hong
Kong.
Marshall AJ. 2004. Population ecology of gibbons and leaf monkeys across a gradient of Bornean forest
types Harvard University, USA.
McConkey K, Galetti M. 1999. Seed dispersal by the sun bear (Helarctos malayanus) in Central Borneo.
Journal of Tropical Ecology 15: 237-241.
McPhaden MJ. 1999. El Niño-The child prodigy of 1997-98. Nature 398: 559-562.
Medway L. 1972. Phenology of a tropical rain forest in Malaya. Biological Journal of the Linnean Society 4:
117-146.
Meijaard E. 2003. Mammals of south-east Asian islands and their Late Pleistocene environments. Journal of
Biogeography 30: 1245-1257.
Meijaard E. 2004a. The biogeographic history of the Javan leopard Panthera pardus based on a craniometric
analysis. Journal of Mammalogy 85: 302-310.
Meijaard E. 2004b. Craniometric differences among Malayan sun bears (Ursus malayanus); evolutionary and
taxonomic implications. Raffles Bulletin of Zoology 52: 665-672.
Momose K, Yumoto T, Nagamitsu T, Kato M, Nagamasu H, Sakai S, Harrison RD, Itioka T, Hamid AA, Inoue
T. 1998. Pollination biology in a lowland dipterocarp forest in Sarawak, Malaysia. I. Characteristics
of the plant-pollinator community in a lowland dipterocarp forest. American Journal of Botany 85:
1477-1501.
Morisita M. 1962. Id-Index, a measure of dispersion of individuals. Researches in Population Ecology 4: 1-7.
Morley RJ. 2000. Origin and evolution of tropical rain forests. John Wiley & Sons, Ltd, Chichester, United
Kingdom.
NOAA-CIRES. 2003. Climate Diagnostics Centre. http://www.cdc.noaa.gov/people/klaus.wolter/MEI/.
Nowak RM, Paradiso JL. 1983. Walker’s Mammals of the World. Johns Hopkins University Press, Baltimore, MD.
Phenological influences on sun bear frugivory 45
O’Brien TG, Kinnaird MF, Dierenfeld ES, Conklin-Brittain NL, Wrangham RW, Silver SC. 1998. What’s so
special about figs? Nature 392: 668.
Pendry CA, Proctor J. 1997. Altitudinal zonation of rain forest on Bukit Belalong, Brunei: soils, forest struc-
ture and floristics. Journal of Tropical Ecology 13: 221-241.
Peres CA. 1994. Primate responses to phenological changes in an Amazonian terra-firme forest. Biotropica
26: 98-112.
Peyton B. 1980. Ecology, distribution, and food habits of spectacled bears, Tremarctos Ornatus, in Peru. Journal
of Mammalogy 61: 639-652.
Pocock RI. 1941. The fauna of British India, including Ceylon and Burma. Mammalia-Vol II. Carnivora (suborders
Aeluroidea (part) and Arctoidea). Taylor and Francis ltd, London, UK.
Sacco T, van Valkenburgh B. 2004. Ecomorphological indicators of feeding behaviour in the bears (Carnivora:
Ursidae). Journal of Zoology, Lond 263: 41-54.
Sakai S. 2002. General flowering in lowland mixed dipterocarp forests of South-east Asia. Biological Journal
of the Linnean Society 75: 233-247.
Sakai S, Momose K, Yumoto T, Nagamitsu T, Nagamasu H, Hamid AA, Nakashizuka T. 1999. Plant reproduc-
tive phenology over four years including an episode of general flowering in a lowland dipterocarp
forest, Sarawak, Malaysia. American Journal of Botany 86: 1414-1436.
Servheen C. 1999. Sun bear conservation action plan. In: Servheen C, Herrero S and Peyton B, eds. Bears.
Status Survey and Conservation Action Plan. Gland, Switserland: IUCN. 219-223.
Shanahan M, Compton SG, So S, Corlett R. 2001. Fig-eating by vertebrate frugivores: a global review. Biologi-
cal Reviews 76: 529-572.
Siegel S, Castellan NJJ. 1988. Nonparametric statistics for the behavioural sciences. McGraw-Hill, New York.
Siegert F, Ruecker G, Hinrichs A, Hoffmann AA. 2001. Increased damage from fires in logged forests during
droughts caused by El Niño. Nature 414: 437-440.
SigmaStat 1.0, 1992-1994, Jandel Corporation.
Singleton I, van Schaik CP. 2001. Orangutan home range size and its determinants in a Sumatran swamp
forest. International Journal of Primatology 22: 877-911.
Soerianegara I, Lemmens RH. 1993. Plant resources of South-East Asia. Timber trees: major commercial
timbers. Pudoc, Wageningen, Netherlands. 454-457.
Sokal RR, Rohlf J. 1981. Biometry. W.H. Freeman, New York, USA.
Sork VL. 1993. Evolutionary ecology of mast-seeding in temperate and tropical oaks (Quercus spp.). Vegeta-
tio 107/108: 133-147.
Strushaker TT, Leyland L. 1977. Palm-nut smashing by Cebus a. apella in Colombia. Biotropica 9: 124-126.
Chapter 246
Sugardjito J, te Boekhorst IJA, van Hooff JARAM. 1987. Ecological constraints on the grouping of wild
orangutans (Pongo pygmaeus) in Gunung Leuser National Park. International Journal of Primatology
8: 17-41.
Talbot S, Shields G. 1996. A phylogeny of the bears (Ursidae) inferred from complete sequences of three
mitochondrial genes. Molecular Phylogenetics and Evolution 5: 567-575.
Terborgh J. 1983. Five new world primates: A study in comparative ecology. Princeton University Press, Prince-
ton, USA.
Terborgh J. 1986. Keystone plant resources in the tropical forest. In: Soulé ME, ed. Conservation Biology: the
science of scarcity and diversity. Sunderland, Mass. USA: Sinauer Associates. 330-344.
van Nieuwstadt MGL. 2002. Trial by fire-Postfire development of a dipterocarp forest. Unpublished PhD
Thesis, University of Utrecht. 1-143.
van Schaik CP. 1986. Phenological changes in a Sumatran rain forest. Journal of Tropical Ecology 2: 327-347.
van Schaik CP. 1996. Phenology: Forest seasonality in an everwet environment. In: van Schaik CP and Supri-
atna J, eds. Mt Leuser, a Sumatran Sanctuary. 120-131.
van Schaik CP, Terborgh JW, Wright SJ. 1993. The phenology of tropical forests - Adaptive significance and
consequences for primary consumers. Annual Review of Ecology and Systematics 24: 353-377.
van Schaik CP, van Noordwijk MA. 1985. Interannual variability in fruit abundance and reproductive season-
ality in Sumatran Long-tailed macaques (Macaca fascicularis). Journal of Zoology, Lond 206: 533-549.
Voon BH, Kueh HS. 1999. The nutritional value of indigenous fruits and vegetables in Sarawak. Asia Pacific
Journal of Clinical Nutrition 8: 24-31.
Waits LP, Sullivan J, O’Brien SJ, Ward RH. 1999. Rapid radiation events in the family Ursidae indicated by
likelihood phylogenetic estimation from multiple fragments of mtDNA. Molecular Phylogenetics and
Evolution 13: 82-92.
Walsh RPD, Newbery DM. 1999. The ecoclimatology of Danum, Sabah, in the context of the world’s rain-
forest regions, with particular reference to dry periods and their impact. Philosophical Transactions
of the Royal Society of London Series B-Biological Sciences 354: 1869-1883.
Whitmore TC. 1985. Tropical rainforests of the Far East. Clarendon Press, Oxford.
Wich SA, van Schaik CP. 2000. The impact of El Niño on mast fruiting in Sumatra and elsewhere in Malesia.
Journal of Tropical Ecology 16: 563-577.
Wong ST, Servheen C, Ambu L. 2002. Food habits of malayan sun bears in lowland tropical forest of Borneo.
Ursus 13: 127-136.
Wong ST, Servheen C, Ambu L. Norhayati A. in press. Impacts of fruit production cycles on Malayan sun
bears and bearded pigs in lowland tropical forest of Sabah, Malaysian Borneo. Journal of Tropical
Ecology.
Phenological influences on sun bear frugivory 47
Wood GHS. 1956. The dipterocarp flowering season in North Borneo, 1955. Malaysian Forester 19: 193-201.
Yasuda M, Matsumoto J, Osada N, Ichikawa S, Kachi N, Tani M, Okuda T, Furukawa A, Nik AR, Manokaran N.
1999. The mechanism of general flowering in Dipterocarpaceae in the Malay Peninsula. Journal of
Tropical Ecology 15: 437-449.
Yu L, Li QW, Ryder OA, Zhang YP. 2004. Phylogeny of the bears (Ursidae) based on nuclear and mitochon-
drial genes. Molecular Phylogenetics and Evolution 32: 480-494.
Chapter 248
Appendix 1:
Main sun bear fruit taxa from faecal analyses (N = 1209, October 1997 to June 2002) and direct
observations (N = 4977 h, October 1998 to April 2001).
Faecal analyses Family % Feeding observations
Family %
Ficus spp. Moraceae 23.2 Ficus spp. Moraceae 17.6
Syzigium spp. Myrtaceae 11.8 Syzigium spp. Myrtaceae 17.3
Santiria spp. Burseraceae 11.2 Santiria spp. Burseraceae 14.2
Dacryodes rugosa* Burseraceae 10.3 Litsea sp. Lauraceae 6.4
Tetramerista glabra Tetrameristaceae 8.1 Rattan spp. Palmae 6.4
Polyalthia spp. Annonaceae 7.4 Monocarpia kalimantanensis
Annonaceae 5.8
Oncosperma horridum Palmae 6.9 Oncosperma horridum Palmae 5.5
Artocarpus integer* Moraceae 5.8 Tetramerista glabra Tetrameristaceae 4.0
Cryptocarya sp. Lauraceae 2.3 Borassodendron borneensis
Palmae 2.8
Hornstedtia cf reticulata Zingiberaceae 2.3 Polydocarpus sp. Palmae 2.6
Monocarpia kalimantanensis
Annonaceae 2.3 Diospyros spp. Ebenaceae 1.2
Dacryodes rostrata* Burseraceae 2.1 Cryptocarya sp. Lauraceae 1.0
Artocarpus anisophyllus* Moraceae 2.0 Garcinia spp. Guttiferae 0.9
Durio dulcis* Bombacaceae 1.8 Polyalthia spp. Annonaceae 0.8
Durio oxleyanus* Bombacaceae 1.8 Knema sp. Myristicaeae 0.8
Rattan spp. Palmae 1.7 Mangifera spp. Anacardiaceae 0.8
Baccaurea spp. Euphorbiaceae 1.6 Baccaurea spp. Euphorbiaceae 0.8
Artocarpus nitidus Moraceae 1.4 Lithocarpus gracilis Fagaceae 0.7
Garcinia spp. Guttiferae 1.4 Aglaia sp. Meliaceae 0.6
Mangifera spp. Anacardiaceae 1.3 Barringtonia sp. Euphorbiaceae 0.4
* Mast-fruiting species; percentages indicate % of faecal samples containing a particular taxon, or percentage of fruit feeding time spent on a taxon; ‘Rattan’ incorporates several genera.
Phenological influences on sun bear frugivory 49
Appendix 2:
Overall list of plant species occurring in the diet of the sun bear (faecal analyses and observa-
tions) in Sungai Wain between October 1997 to July 2002.
Species Family Scat/Observation*
Part eaten Growth form
Aglaia sp. Meliaceae S fr tree
Alangium ridley Alangiaceae S fr tree
Annonaceae sp. 1 Annonaceae S/O fr liana
Annonaceae sp. 2 Annonaceae S/O fr liana
Artocarpus anisophyllus Moraceae S/O fr tree
Artocarpus dadah Moraceae S/O fr tree
Artocarpus integer Moraceae S/O fr tree
Artocarpus nitidus Moraceae S/O fr tree
Artocarpus sp. 1 Moraceae O fr tree
Artocarpus sp. 2 Moraceae O fr tree
Baccaurea bracteata Euphorbiaceae S/O fr tree
Baccaurea macrocapra Euphorbiaceae S/O fr small tree
Baccaurea sp. 1 Euphorbiaceae S fr small tree
Barringtonia sp. 1 Lecythidacae O flo small tree
Borassodendron borneensis Palmae S/O fr, flo big palm
Calamus sp. 1 Palmae S/O fr rattan palm
Calamus sp. 2 Palmae S/O fr rattan palm
Crypteronia sp. Crypteroniaceae S/O fr tree
Cryptocarya sp. Lauraceae S/O fr tree
Dacryodes rostrata Burseraceae S/O fr tree
Dacryodes rugosa Burseraceae S/O fr tree
Daemonorops sp. 1 Palmae S/O fr rattan palm
Dehaasia sp. Lauraceae S/O fr tree
Dialium indum Caesalpiniaceae S/O fr tree
Diospyros sp. 1 Ebenaceae S/O fr tree
Diospyros sp. 2 Ebenaceae S/O fr tree
Diospyros sp. 3 Ebenaceae S/O fr tree
Durio dulcis Bombacaceae S fr tree
Durio graveolens Bombacaceae S fr tree
Durio lanceolata Bombacaceae S/O fr tree
Durio oxleyanus Bombacaceae S/O fr tree
Dysoxylum sp. Meliaceae S fr tree
Eugenia polyanthe Myrtaceae S/O fr small tree
Ficus benjamina Moraceae S/O fr strangler
Ficus lowii Moraceae O fr small tree
Ficus sp. 1 Moraceae O fr strangler
Ficus sp. 2 Moraceae S/O fr strangler
Ficus sp. 3 Moraceae O fr strangler
Chapter 250
Species Family Scat/Observation*
Part eaten Growth form
Ficus sp. 4 Moraceae O fr strangler
Ficus sp. 5 Moraceae O fr strangler
Ficus sp. 6 Moraceae O fr tree
Garcinia mangostana Guttiferae S/O fr tree
Garcinia parvifolia Guttiferae S/O fr tree
Garcinia sp. 1 Guttiferae S/O fr tree
Glochidion sp. Euphorbiaceae S fr tree
Hornstedtia cf reticulata Zingiberaceae S fr undergrowth
Horsfieldia sp. Myristicaceae S/O fr tree
Ilex sp. Aquifoliaceae S fr tree
Knema laterica Myristicaceae S/O fr tree
Knema sp. 1 Myristicaceae S/O fr tree
Korthalsia sp. 1 Palmae S/O fr rattan palm
Korthalsia sp. 2 Palmae S/O fr rattan palm
Lansium domesticum Meliaceae S fr tree
Licuala spinosa Palmae O fr, lb, flo undergrowth palm
Lithocarpus gracilis Fagaceae S/O fr tree
Lithocarpus sp. 1 Fagaceae S/O fr tree
Litsea angulata Lauraceae S/O fr tree
Litsea sp. 1 Lauraceae S/O fr tree
Litsea sp. 2 Lauraceae S/O fr tree
Madhuca kingiana Sapotaceae S/O flo tree
Magnoliaceae sp. 1 Magnoliaceae O fr tree
Magnoliaceae sp. 2 Magnoliaceae O fr tree
Mangifera caesia Anacardiaceae O fr tree
Mangifera foetida Anacardiaceae O fr tree
Mangifera sp. 1 Anacardiaceae O fr tree
Mangifera torquenda Anacardiaceae O fr tree
Marantaceae sp. 1 Marantaceae O lb, flo undergrowth
Microcos sp. Tiliaceae S/O fr tree
Monocarpia kalimantanensis Annonaceae S/O fr tree
Nephelium sp. Sapindaceae S/O fr tree
Oncosperma horridum Palmae S/O fr, flo palm
Palaquium sp. Sapotaceae S/O fr tree
Pandanus sp. 1 Pandanaceae O lb, fr undergrowth
Pinanga sp. Palmae O lb, flo small palm
Polyalthia sp. 1 Annonaceae S/O fr tree
Polyalthia sp. 2 Annonaceae S/O fr tree
Polydocarpus sp. Palmae S/O fr palm
Pternandra sp. Melastomataceae S/O fr small tree
Quercus argentata Fagaceae S/O fr tree
Quercus sp. 1 Fagaceae S/O fr tree
Appendix 2 Continued
Phenological influences on sun bear frugivory 51
Species Family Scat/Observation*
Part eaten Growth form
Santiria oblongifolia Burseraceae S/O fr tree
Santiria tomentosa Burseraceae S/O fr tree
Sida sp. Malvaceae S fr shrub
Syzigium tawahense Myrtaceae O fr tree
Syzigium sp. 1 Myrtaceae S/O fr tree
Syzigium sp. 2 Myrtaceae S/O fr tree
Syzigium sp. 3 Myrtaceae S/O fr tree
Tetramerista glabra Tetrameristaceae S/O fr tree
Uvariastrum sp. Annonaceae S/O fr liana
Walsura sp. 1 Meliaceae S/O fr tree
Willughbeia angustifolia Apocynaceae S/O fr liana
Xerospermum norhonianum Sapindaceae S/O fr tree
Xerospermum sp. 1 Sapindaceae S/O fr tree
Unidentified (22 diff species) S/O fr
Total species = 115; Total genera = 54; Total families= 30*S=encountered in scats; O=direct feeding observation; S/O= both encountered in the diet from scats and observations; fr=fruit; flo=flower; lb=leafbase/pith
Appendix 2 Continued
Chapter 3
Movements and activity patterns of female
sun bears in East Kalimantan, Indonesian
Borneo: implications for conservation
With David L. Garshelis
Chapter 354
AbstractSun bears (Helarctos malayanus) in Indonesia are primarily threatened by destruction
of their forest habitat, with poaching for body parts a secondary threat. Protected areas are
increasingly becoming important for the conservation of this species, as non-protected forest
areas are rapidly being converted to other landuses, but relevant data on spatial and habitat
requirements of sun bears are limited. Radio-telemetry was used to study the movements and
activity patterns of Bornean sun bears (H. m. euryspilus) in a small lowland rain forest reserve
in East Kalimantan, Indonesian Borneo. Three wild and two rehabilitated-released female bears
were fitted with motion-sensitive VHF radio-collars; three of these bears were tracked contin-
uously for 1-3 years during 1999-2003. A total of 5,470 locations were recorded. Home range
sizes (12-month period) were 4-5 km2 (95% MCP and 95% fixed kernel). Home range overlap
was considerable. Small home ranges may have been related to a diet composed predominantly
of insects. No mast fruiting event occurred during the period of study. Activity monitoring
(169 days, 4,049 hours, 24,294 readings) revealed that sun bears were predominantly diurnal
and crepuscular throughout the year with activity commencing about 0.5 h before sunrise and
lasting until 2.5 h after sunset, and low levels (20-30%) of activity at night. Bears were active
61.6% of the day (14.8 ± 2.3 hours), on average, with higher levels of activity associated with
insect feeding than fruit feeding.
A combination of relatively small home range size, bounded entirely within the reserve,
and avoidance of areas with human disturbance (trails, burned forest) suggest that small re-
serves are still valuable for the conservation of sun bears. Long-term persistence will depend
on prevention of poaching and maintaining connectivity to other forested areas.
Movements and activity patterns of female sun bears 55
IntroductionHabitat reduction, combined with unsustainable levels of hunting, has put many bear
populations at risk (Garshelis, 2009). Ursids (bears) generally have large home ranges (Garshe-
lis 2004), often with distinct movements to seasonal ranges in response to temporal variations
in the distribution and availability of food (Garshelis and Pelton 1981, Blanchard and Knight
1991, Joshi et al. 1995, Ferguson et al. 1999, Liu et al. 2002, Hwang et al. 2010, Castellanos
2011). Radio-telemetry has provided important insights into the lives of bears, and has been
instrumental for obtaining data on movement patterns and habitat use (Garshelis 2004) that
has been of use for management and conservation planning. Although this technology has been
used for several decades to study bears in northern regions (see Garshelis 2004) only a handful
of radio-telemetry studies have been carried out on bears in the tropics (Nomura et al. 2004,
Wong et al. 2004, Paisley and Garshelis 2006, Hwang et al. 2010, Castellanos 2011).
The sun bear (Helarctos malayanus), ranging throughout much of Southeast Asia (Fig. 1),
has been listed as ‘Vulnerable’ based on significant habitat loss over the last 30 years (Fredriks-
son et al. 2008). Southeast Asia experiences some of the highest levels of forest conversion
in the world including deforestation, forest degradation and fragmentation (FAO 2010, Sodhi
et al. 2010, Broich et al. 2011, Miettinen et al. 2011), and clearing for rapid expansion of the
plantation sector (Koh 2007, Butler and Laurance 2008, Fitzherbert et al. 2008). Levels of threat
to this bear species vary across the region with poaching for body parts being the greatest
threat on mainland Southeast Asia (Dang 2006, Nea and Nong 2006, Vinitpornsawan et al.
2006), whereas habitat loss and fragmentation are currently considered the greatest threat in
Indonesia and Malaysia (Tumbelaka and Fredriksson 2006, Wong 2006).
Sun bears are a forest-dependent species, found in a variety of forest types (Fredriks-
son et al. 2006a, Steinmetz et al. 2011) up to 2500 m above sea level (a.s.l.) and have been found
to persist in logged-over (Wong et al. 2004, Meijaard et al. 2005, Linkie et al. 2007), and other
disturbed forest areas (Fredriksson et al. 2006b). They have even been found to make foraging
excursions into oil palm plantations (Nomura et al. 2004). Sun bears on the island of Borneo
have been recognized as a subspecies, H. m. euryspilus, substantially (~30%) smaller than their
mainland and Sumatran counterpart H. m. malayanus (Horsfield 1825, Meijaard 2004).
Some 45% of the extant distribution range of sun bears lies in Indonesia (IUCN Bear
Specialist Group, Japan Mapping Workshop 2006), making it the single most important country
for the conservation of this species. Some 24 million ha of forest are under some form of
protected status on Sumatra and Kalimantan (Indonesian Borneo) (FWI/GFW 2002), although
the area of forest under protection has not increased in the last decade (FAO 2011). Protected
Chapter 356
Figure 1. Sun bear distribution range in Southeast Asia and location of the Sungai Wain Protection Forest,
East Kalimantan, Indonesian Borneo.
areas are seen as one of the most effective tools for conservation in the tropics (Kramer et al.
1997, Bruner et al. 2001, Terborgh et al. 2002), despite the fact that the effectiveness of many
of these protected areas is limited due to lack of, or weak, in-situ management implementa-
tion (e.g. FWI/GFW 2002, Kinnaird et al. 2003, Curran et al. 2004, Gaveau et al. 2009, Linkie
et al. 2010, Harrison 2011). The conservation value of large expanses of unprotected logged-
over areas in Borneo has also been highlighted (Meijaard et al. 2005, Meijaard and Sheil 2008),
although many of these areas are under further threat by corporate conversion (Butler and
Laurance 2008). The size of protected areas, or available safe habitat, is important for many
species, especially those with large ranges (Powell et al. 1996, Beringer et al. 1998, Woodroffe
and Ginsberg 1998, Woodroffe 2001, Wielgus 2002).
Movements and activity patterns of female sun bears 57
Lowland dipterocarp forest, richest in terms of biodiversity and previously covering
large expanses of Borneo, is now becoming increasingly rare, fragmented, and affected by vari-
ous forms of human disturbance (Curran et al. 2004). In order assess the spatial, ecological, and
habitat requirements of sun bears in this threatened forest type in Kalimantan, we studied their
ranging and activity patterns in relation to fruiting patterns and human disturbance in a small
lowland forest reserve in East Kalimantan, Indonesian Borneo.
Methods
Study site
This study was carried out in a lowland dipterocarp forest, the Sungai Wain Protection
Forest (SWPF), near Balikpapan, East Kalimantan, Indonesian Borneo (1º 05’ S and 116º 49’ E),
at the easternmost edge of the sun bears’ distribution range (Fig. 1). The reserve covers a
watercatchment area of circa 10,000 ha. Approximately 50% of the reserve was burned by
forest fires in March-April 1998 (Fredriksson 2002), during one of the most severe El Niño-
Southern Oscillation (ENSO) related droughts ever recorded (McPhaden 1999), leaving an
unburned central core of 4,000 ha of primary forest as well as unburned forest along rivers.
The geomorphology of the reserve is of eroded sedimentary formations with a relatively low
elevational range (30 - 150m), intersected by many small rivers. No roads traverse the reserve
and access is only by foot. One main trail leads northwards from the nearest village and forest
edge following a ridge separating 2 main sub-watersheds in the reserve. Less than 2 km before
this ends, the track splits with the west branch descending to a research station located in the
middle of the reserve. This trail was used as the main access route to the research station, for
ferrying logistical supplies to the research station twice a week by porters, as well as for varied
research purposes. There was little other foot traffic on this trail.
Fruiting phenology, and rainfall
The most common tree families above 10 cm dbh (diameter at breast height) were
Euphorbiaceae, Dipterocarpaceae, Sapotaceae and Myrtaceae. The relative dominance of Dip-
terocarpaceae increased substantially in the larger size classes. Together, the 25 most common
species formed 40% of the total stem density (van Nieuwstadt 2002). Two phenology data sets
were collected during this study, using the same methodology. Phenology studies commenced
in January 1998 and continued until July 2002. Ten 0.1-ha phenology plots (100 x 10 m) were
Chapter 358
established where all trees ≥10 cm dbh were measured, labeled, and identified by botanists
from the Wanariset Herbarium. The total number of live trees in the 1-ha plots at the start of
the study was 549 individuals of 186 species. Every month around the same date (3rd week),
all trees in these plots were observed with 10 x 40 binoculars. The relative abundance of
flowers, young and mature fruits, and young and old leaves, in relation to size of the crown,
was estimated, though for analysis here we only considered presence or absence of fruit. The
second data set contained only trees known, or thought to be, important in the diet of the sun
bear; we chose 104 trees of 11 species (≥10 cm dbh) at scattered sites throughout the forest
(Fredriksson et al. 2006a). Trees in this forest undergo synchronized supra-annual flowering and
fruiting (masting), providing a burst of food for sun bears (Fredriksson et al. 2006a), but no such
events occurred during this portion of our study.
Daily rainfall, minimum-maximum temperature and humidity data were collected be-
tween January 1998 and October 2002, at ground level in the primary forest. Although rainfall
patterns in the region are not consistent on an annual basis, a distinction could be made be-
tween a ‘wet’ season (Nov-April) and a ‘dry’ season (May-Oct) (t=4.96, df=6, p=0.002). Rainfall
type falls within the category of ‘slightly seasonal’ according to Mohr’s index, with average
annual rainfall 2968 ± 510 mm y-1. Temperature was stable throughout the study period with
average maximum of 29.7 ± 0.7ºC and minimum 23.2 ± 0.4ºC. The study area lies almost on
the equator so there is little variation in the timing of sunrise (~06:00 h) and sunset (~18:00 h)
year-round.
Bear captures and radio-tracking
We captured sun bears in locally-constructed barrel traps spaced 1-2 km apart. We
also set Aldrich spring-activated foot snares in cubby sets (Johnson and Pelton 1980). Traps
were checked daily by foot along an 8-hour trapline. Traps were baited with a variety of food
items, including honey, fruits, mixtures of cow blood and fish juices, with chicken intestines
finally proving the most productive lure. We trapped from October 1998 until July 2000.
We immobilized captured bears with a mixture of Zolatil (tiletamineHCl/zolazepam-
HCl; Virbac, France) at 5 mg/kg, and Domitor (medetomidine hydrochloride, Orion Pharma,
Espoo, Finland) at 0.027 mg/kg via a blowpipe. Bears were weighed, ear tagged, measured, and
fitted with conventional VHF (very high frequency; 164-166 MHz) radio-collars (Advanced
Telemetry Systems, Isanti, MN, USA). Each collar contained an activity sensor that altered the
base signal of approximately 65 pulses per minute (ppm) when stationary with additional pulses
(170 ppm, range 138-210 ppm) when tilted or moved. We attached radio-collars with a leather
Movements and activity patterns of female sun bears 59
breakaway link that was designed to drop off the bear’s neck after about 1–2 years (Garshelis
and McLaughlin 1998). We administered Antisedan (atipamezole hydrochloride, Orion Pharma,
Espoo, Finland) at the capture site to reverse the anesthesia, after completion of handling.
We also radio-collared two female sun bears that had been orphaned in the wild as
cubs and were undergoing a rehabilitation and release programme (Fredriksson 2001); they
were incorporated into this study when they started becoming independent at 1.5-2 years
of age, and able to live in the forest. These bears were habituated for behavioural observa-
tions by the primary investigator and one assistant, which aided in verifying activity associated
with pulses emitted by the radio-collars, telemetry accuracy, movement patterns, and provided
unique insight into various other aspects of sun bear ecology. The rehabilitated bears received
supplemental food (primarily fruits) in the beginning of the study, which we gradually reduced
and fully discontinued by the time these bears were 2-2.5 years of age.
We located collared bears by ground-based triangulation with a hand held 2-element
directional antenna (Rubber ducky, Telonics Inc., Mesa, AZ, USA). Radio-locations were taken
along an extensive foot-trail system (~60 km), including the main ridge trail that was used for
quick movement between telemetry readings and more efficient movement between distant
locations in the forest. We attempted to obtain locations of all collared bears three times a
day: morning (06:00-10:00 h), midday (10:00-14:00) and late afternoon (14:00-18:00). Bearings
were plotted on a 1:35,000 topographic map. We assigned a precision rating to each location
based on the size of the error polygon, and discounted those where the location could not be
fixed within 150 m.
Home range and movements
Home range sizes were calculated using 3 methods: 100% and 95% minimum convex
polygons (MCP) as well as a fixed kernel probability density estimator with a band width us-
ing least squares cross validation to calculate the smoothing parameter, and using the 95%
isopleth to determine area (Powell 2000). The 95% MCP were generated by discarding the 5%
of points furthest from the mean location of all points used for generation of the 100% MCP
(Worton 1987). MCP ranges are indicative of the total area needed to sustain the bears, includ-
ing some heavily-used patches separated by gaps with little use, whereas probabilistic home
range models (kernel) estimate the area actually used most of the time; the former is more
useful for conservation (our purpose), whereas the latter may be more biologically relevant. In
addition, MCP is less sensitive than other methods to variations in sampling intensity and lack
of independence among successive radiolocations (Garshelis 1983). We calculated home range
Chapter 360
sizes for monthly and annual (12-month) periods. For monthly range calculations we only used
months with more than 15 days of location data. In order to test whether fruiting patterns
and rainfall had an effect on ranging patterns we used monthly phenology data (percentage of
monitored trees in fruit) and monthly ranging data calculated by 100% MCP and kernel (95%),
using a stepwise linear regression.
To test whether human traffic along the ridge-trail affected sun bear movement pat-
terns, we generated a 70% minimum convex polygon using all combined locations, and com-
pared all bear locations within that polygon to the same number of random points within the
polygon. Specifically, we compared the distribution of bear locations to random points with
respect to the main trail, using a raster grid with a 20-m cell size.
To test the accuracy of our triangulated movement data, we measured real distances
traveled by one of our rehabilitated bears by closely following it for several hours on differ-
ent days using a Walktax Distance Measurer (Forestry Suppliers Inc, Jackson, MS, USA). This
created a step-by-step track of its travel route. We then estimated the total average distance
that this bear traveled in a day by expanding the sampled distance during active hours to the
average number of hours of total activity per day (see below). These distance measurements
were compared with distances obtained from 4 subsequent 24-hour tracking sessions where
locations of this same bear were obtained by triangulation. We used ArcGis 10/ArcView spatial
analyst tool (ESRI Inc, Redlands, CA, USA) to plot and measure movements. MCP and kernels
were generated using Geospatial Modeling Environment (Spatial Ecology LLC).
Activity patterns
We quantified diel activity by listening to radio signals at 10-minute intervals for 24-
hour periods, once a week for each bear during Feb 1999 - Oct 2002. We categorized signals as
either active or inactive. To test whether monthly activity patterns (percentage time active for
all bears pooled) were affected by monthly changes in fruiting phenology or rainfall we carried
out a linear regression, using reduced major axis regression.
Results
Study subjects
We captured 3 female sun bears in barrel traps during 1,538 barrel-trapnights (513
barrel-trapnights/bear capture) over a period of 22 months. One of the rehabilitated sun bears
Movements and activity patterns of female sun bears 61
was also inadvertently captured in an Aldrich foot snare after 1,048 snare-trapnights. All foot
snares were removed after this event and not redeployed, as the bear developed severe ne-
crosis on the wrist after having been caught for less than 3 hours. Based on sign, we discerned
that bears visited trapsites but were not captured on 66 occasions.
Two of the captured sun bears were caught on consecutive days (5-6 July, 1999), after
almost one year of trapping. Both were emaciated, weighing 23-25 kg, ~35% less than two fe-
male sun bears caught at a similar time in Sabah (Malaysian Borneo) (35 and 39 kg; Nomura et
al. 2004). One (Nenek) appeared to be at least 20 years old based on the extreme wear of her
canine teeth and molars, and scattered white hairs covering her feet and flanks. The other (Bibi)
also had worn canines but appeared to be somewhat younger (Table 1). These two females
were each later found to have a cub, which we estimated to be 1-2 months and 3-4 months
old, for Bibi and Nenek, respectively. Bibi was only monitored for 1 month, after which she was
swallowed by a large reticulated python (Python reticulatus) (Fredriksson 2005a). Nenek was
monitored for 2 months, after which she was found dead, partially scavenged by bearded pigs
(Sus barbatus). Neither of the cubs was seen again but both were too small to have survived
independently.
The third bear (Liar) was captured in March 2000. This female appeared in a better
physical condition, both in terms of body mass (30 kg) and tooth condition. We estimated her
age at 10-15 years. At the time of capture she did not appear to be lactating and no subsequent
observations were made of this bear in the company of cub(s). This bear was monitored for
almost 1 year (Table 1), at which time the leather breakaway link degraded and the collar
dropped off.
Table 1. Identity, condition, period of monitoring and total number of locations (coordinates) obtained for
5 radio-collared female sun bears.
Bear SexWeight (in kg)
Physical Condition Estimated Age Monitoring period
Months monitored
Total number locations
Nenek F 25 Very poor Very old-20 yr+ 5 July 1999-9 Sep 1999 2 162
Bibi F 23 Very poor Adult- 15-20 yr 6 July 1999-31 July 1999 1 66
Liar F 30 Fair Adult-10-15 yr 13 March 2000-20 Feb 2001 11 877
Ganja F 34 Fair (sub) adult (2-6 yr) 1 Nov 1998-24 April 2003 54 (35 A)* 2,579
Ucil F 36 Fair (sub) adult (2-6 yr) 8 Jan 1999-8 June 2002 42 (27 A)* 1,786
5,470
* Data collected over the last 35 months (out of 54) and 27 (out of 42) months, respectively, were used for calculating
activity patterns.
Chapter 362
Table 2. Annual (12-month period) home range sizes (in km2) calculated by 100% and 95% Minimum
Convex Polygon (MCP), and 95% fixed Kernel.
Table 3. Monthly range sizes (in km2) calculated for months with >15 days data, between July 1999-
October 2002.
Home ranges (in hectares) for 3 female sun bears with simultaneous monitoring over 12-month periods
Bear Tracking period # mo 100% MCP n locations 95% MCP n locations 95% Kernel
Liar March 2000-Feb 2001 12 762 877 449 833 485
Ganja March 2000-Feb 2001 12 812 610 438 579 539
Ucil March 2000-Feb 2001 12 708 602 452 572 502
average 760 445 521
SD 74 10 26
Bear Tracking period # mo 100% MCP n locations 95% MCP n locations 95% Kernel
Ucil May 2000-April 2001 12 864 628 466 597 537
Ucil May 2001-April 2002 12 688 851 493 808 518
Ganja May 2000-April 2001 12 825 648 478 616 570
Ganja May 2001-April 2002 12 655 907 441 862 499
Ganja May 2002-April 2003 12 584 477 451 453 542
average 723 466 533
SD 118 21 27
Bear 100% MCP 95% MCP 95% Kernel Days # mo Locations
Nenek 1.6 (0.6) 1.2 (0.3) 2.2 (0.8) 56 2 151
Bibi 3.0 2.3 4.1 25 1 66
Liar 2.7 (1.0) 2.1 (0.9) 4.1 (1.5) 321 12 877
Ganja 2.9 (0.9) 2.2 (0.7) 4.5 (1.3) 876 38 2,281
Ucil 2.9 (0.9) 2.3 (0.8) 4.4 (1.4) 580 25 1,548
Average 2.8 2.2 4.3
SD 0.9 0.8 1.4
range (1.1-5.5) (0.9-4.4) (1.7-8.7)
Movements and activity patterns of female sun bears 63
During the period that these bears were radio-tracked another 6-8 sun bears, judged
to be different independent individuals, were encountered in the study area, including at least 4
other females with different-aged cubs (one with twins). The two rehabilitated females (Ganja
and Ucil) were monitored over a period of 4.5 and 3.5 years respectively.
Ranging patterns
We obtained 5,470 locations for the three wild and two rehabilitated bears during July
1999-June 2002 (Table 1). We were highly successful in obtaining radio-locations of the collared
bears because of access to a trail system: location data were missing for only 9 days of 437 days
(2.1%) of continuous attempted daily monitoring of the three wild sun bears.
Yearly ranges were calculated for the 12-month period Mar 2000-Feb 2001, during
which we collected simultaneous data for 3 female sun bears monitored over the longest
period of time (Table 2). Their 12-month 100% MCP home range sizes were 7-8 km2. Home
ranges were only 4-5 km2 when calculated with the outer 5% of locations excluded (95% MCP)
or using the 95% kernel method, indicating that a sizeable portion of the range was used infre-
quently. Home range sizes remained consistent through time (especially 95% MCP and kernel)
for the 2 rehabilitated sun bears, which were tracked in multiple years (Table 2). Ranges of
these two bears, Bibi and Nenek, overlapped each other by 54 and 43%, respectively, for the
short period of time (1 month) they were radio-tracked simultaneously.
Each of the five bears had monthly home range sizes (95% MCP) of 2 km2 (average 2.2
± 0.8[SD] km2; monthly variation 0.85-4.4 km2; Table 3). Monthly range sizes were slightly larger
when more trees were fruiting (linear regression with 100% MCP: R2=0.079, p=0.015; with
95% kernel: slope=55, R2=0.073, p=0.020), with range size increasing with increasing number
of trees in fruit. Rainfall had a minor effect on monthly ranging patterns (linear regression with
100% MCP: p=0.302; with 95% kernel: p=0.041).
Distribution of locations
Fewer bear locations (317 of 3818 = 8.3%) in the 70% MCP formed by pooling all bears
were within 100 m of the main trail than would have been expected from a random distribu-
tion (910 locations, 23.8%, χ2 =507, df=1, p=0.001).
Very few bear locations (n=58, 1%) were obtained in the forest area that was affected
by forest fires in 1998. Some of the locations that were mapped in the burned parts of the
forest could have been in unburned river corridors or in burned forest areas close to rivers,
as location error and coarseness of the GIS river layer precluded differentiation on this scale.
Chapter 364
Figure 2. Annual home ranges of three radio-collared female sun bears in the SWPF, East Kalimantan,
Indonesian Borneo, during March 2000-Feb 2001. Ranges were calculated using 100% and 95% MCP, and
95% fixed kernel. Within the 95% fixed kernel border, progressively darker gradients represent 80%, 60%,
40%, 20%, an 10% contours. Ganja and Ucil were rehabilitated and released, whereas Liar was wild-caught.
From the shape of the 95% kernel (Fig. 2) generated for bear Liar it appears that she avoided
entering the burned forest bordering the southwestern part of her range.
All of the radio-collared bears remained within the boundaries of the reserve during
the time they were monitored. However, based on interview data and surveys along forest
edge areas (Fredriksson 2005b), a number of untagged bears ventured near the forest edge.
Daily movement
We obtained measurements of actual distance traveled by one bear (Ganja) on 16
days (during Nov 2000-Mar 2001) that she was visually observed. On these days we observed
the bear for an average of 6.5 hours (range 5-8 hours) during which she traveled an average
of 2,025 ± 444 m (SD) (range 1,053-2,671 m). Based on an average of 14.8 hours activity per
day, which excluded all periods of non-activity (see below), this extrapolated to 4,604 ± 888 m
(SD) travelled daily. In fact, this is an under-estimate as during each day of direct observations,
the bear would usually be “inactive” for some of the time, thus the “active” period in which
she travelled the average 2,025 m would be obtained in less than 6.5 hour. During this active
time the bear fed at a rapid rate, zigzagging between primarily invertebrate food resources.
Distances measured using telemetry locations obtained 3x per day (n=604 days with locations
in morning, midday, and afternoon and another location the next day) yielded a much lower
estimate of 24-hour movements (1,481 ± 606 m (SD)).
Movements and activity patterns of female sun bears 65
Table 4. 24-hour activity monitoring session and percentage of time that sun bears were found active.
Figure 3. 24-hour activity pattern of 5 radio-collared female sun bears monitored between 1999-2003.
Standard error (SE) bars are shown.
Activity patterns
We obtained 24-hour activity data during 169 days of monitoring (producing >24,000
readings, Table 4) over a period of 3 years (Feb 1999-Jan 2002). We were unable to categorize
activity on only 42 attempts (0.2%).
Bear ID 24-h sessions # hours # readings % time active (± SD)
Nenek 7 168 1,008 62.0 ± 11.0
Bibi 4 96 576 69.8 ± 5.6
Liar 42 1,004 6,022 57.7 ± 7.1
Ganja 89 2,135 12,807 64.2 ± 9.0
Ucil 27 647 3,881 58.0 ± 9.9
Total 169 days 4,050 24,294 61.6 ± 9.4
Chapter 366
Overall, female sun bears were active 14.8 ± 2.3 h (SD) per day (61.6 ± 9.4% SD, all
24-hour sessions combined, n=169). Average activity per day among four of the five bears was
consistent (58–64%), with no indication that the rehabilitated bears were different than the
wild bears. One wild bear (Bibi) had a higher level of activity (69%) for the 1-month that she
was monitored, but this could have represented normal short-term variation.
Sun bears were distinctly more active during daylight hours (85.5 ± 4.8 % SD) than at
night (37.9 ± 20.0% (SD), n=169, t=19.6, df=142, p=0.001). They tended to become active about
0.5 h before sunrise and ceased activity about 2.5 h after sunset (Fig. 3). Peaks of activity gen-
erally occurred during 07:00-09:00 and 16:00-18:00 h (Fig. 3), with diminished activity during
10:00-14:00 h. The human-habituated individuals that we visually observed frequently slept for
brief periods during the hottest time of day on a fallen log or on the forest floor. When these
bears were cubs (< 1 year), they spent large parts of the day resting alone in trees.
Activity levels were higher during the first 12-month period of data collection (Feb
1999-Jan 2000) than during the subsequent 2 years (average % activity = 69, 58, 57 for years
1-3, respectively; year 1 vs 2, t=6.7, df=21, p<0.001, 2-tailed; year 1 vs 3, t=5.1, df=21, p<0.001).
This period of higher activity coincided with the period of lowest fruit availability, when bears
were primarily foraging for invertebrates. Monthly activity decreased slightly with increased
fruiting phenology, although not significantly so (R2=0.067, p=0.139). Rainfall did not seem to
affect monthly activity levels (R2=0.063, p=0.151), although rain did seem to affect daily activi-
ties. Anecdotally we observed that bears occasionally sought refuge in a tree nest for several
hours during persistent rainfall, whereas light rainfall after a hot dry day would trigger intense
play activity among the rehabilitated bears.
Discussion
Home ranges
Our study presents the first year-round ranging and activity data of female sun bears
in their range. Wong et al. (2004) presented similar data for male sun bears in northeastern
Borneo. In this aseasonal lowland forest at the easternmost edge of their distribution range,
where fruit resource availability is highly influenced by supra-annual community mast fruiting
events, and where there is minimal seasonal variation in day length, ranges of female sun bears
were relatively small, and entirely encompassed within the reserve boundaries. Home range
sizes of bears are related to body size (McNab 1963, Gittleman and Harvey 1982, Gomp-
Movements and activity patterns of female sun bears 67
per and Gittleman 1991), metabolic needs (McNab 1983) and distribution and abundance of
food (McLoughlin et al. 1999, 2000, Gompper and Gittleman 1991), resulting in large inter-
and intraspecific variation. Insectivorous carnivores usually have relatively small home ranges
(Gittleman and Harvey 1982) seemingly because protein-rich insect prey, especially ants and
termites, are abundant and omnipresent over relatively small areas (e.g. Wood and Sands 1978,
Redford 1987). As such, the sloth bear (Melursus ursinus), the most insectivorous (mymecopha-
gus — ant and termite eating) ursid, appears to have the smallest home ranges of any species
of bear. During our study, sun bears had a comparable diet to sloth bears, spending up to 90%
of their foraging time consuming insects. Ants and termites are among the few food resources
consistently common in lowland rainforests (Collins 1989, Kikkawa and Dwyer 1992) and sun
bears rely heavily on this resource during prolonged inter-mast intervals that occur on Borneo
(Wong et al. 2005, Fredriksson et al. 2006a). The female sun bears in our study had somewhat
larger home ranges than female sloth bears during periods (5-12 months) when sloth bears
relied predominantly on insects (Nepal x = 4.7 km2 [100% MCP], Sri Lanka = 2.5 km2 [fixed
kernel]; Joshi et al. 1995, Ratnayeke et al. 2007). However, sloth bears significantly expanded
their ranges during seasons, or in places, where fruits were common in their diet (Joshi et al.
1995, K. Yoganand, unpubl. report).
Sun bears on Borneo become much more frugivorous during rare mast fruiting events
(Wong et al. 2002, 2005, Fredriksson et al. 2006a). Mast fruiting events occur 2-10 years apart
(Medway 1972, Ashton et al. 1988, Curran and Leigthon 2000). No mast fruiting event occurred
within the period that we were radio-tracking, so we cannot assess ranging patterns during
times when these bear are predominantly frugivorous. Nevertheless, we did observe a slight
increase in their area of use when more trees were in fruit, suggesting that it is energetically
profitable for sun bears to range farther to find fruit. Fruit trees favored by sun bears are
widely scattered and found at low densities throughout this forest (Fredriksson et al. 2006a).
Yearly home range sizes (daily locations for 12-month period) for female sun bears
in this study ( x = 5.1 km2, 95% fixed kernel) were smaller than those reported for male sun
bears in Malaysian Borneo ( x = 14.8km2, 95% adaptive kernel) during a period when they also
fed largely on insects (Wong et al. 2004). This was true even though three of four male bears in
Wong et al.’s (2004) study were tracked for <1 year and were periodically out of range of the
tracking equipment. Nomura et al. (2004) also recorded smaller ranges for female than male
sun bears, although home range size calculated during their study was affected by a limited
number of locations and bears being frequently out of telemetry range. Ursids, in general,
display large variation in home range sizes between individuals, sexes, species, and even among
Chapter 368
populations within the same species (Garshelis 2004, 2009). Larger range size for male bears
(2-5x) is a common trait seen in all bear species where range size has been studied. Typically,
the ranges of adult males overlap those of several females (Koehler and Pierce 2003, Dahle and
Swenson 2003, Garshelis 2004, 2009, Castellanos 2011).
No data are available yet on the effects of cub rearing on ranging patterns in sun bears.
Although two emaciated female sun bears with small cubs were caught during this study, both
died shortly after radio-tracking began, so our data on them are very limited. Moreover, the
fact that we caught these two bears on consecutive days, after a year of unsuccessful trapping,
suggested that they were in dire condition and finally succumbed to our bait. At the time when
these bears were caught there had been a lack of fruits for almost 1.5 years (Fredriksson et
al. 2006a). Hence, their movements may not have been indicative of healthy females with cubs.
Sun bears during this study displayed high levels of range overlap, which might have
been exacerbated by potentially elevated densities due to an influx of bears from the uninhab-
itable burned areas. During the fires we heard frequent vocalizations (seemingly indicative of
aggression), which were virtually never heard in subsequent years. Sun bear use of burned-over
areas remained low for close to a decade post fires, based on repeated sign transects there
(Fredriksson et al. in prep).
Both this study and the study by Wong et al. (2004) monitored only a small number of
individuals in a limited geographical area. We expected home range sizes for sun bears to be
relatively small due the small size of this subspecies and their predominantly insect dominated
diet. It is possible that ranges of sun bears in western parts of their range (Sumatra and main-
land Southeast Asia) are somewhat larger, due to more available fruit (Wich et al. 2011) and
hence a higher proportion of fruit in their diet (Steinmetz et al. 2012).
Sun bears have long been considered the most arboreal species of bear (Ewer 1973),
so this three-dimensional use of the forest might suggest that they would have correspondingly
small home ranges. However, most of the foraging that we observed (75%) was on the forest
floor, where bears found both insects and fallen fruits. This might be different during a mast-
fruiting event, or in places where sun bears are more frugivorous.
Activity patterns
Sun bears at our study site had a clear diurnal activity pattern similar to that reported
for sun bears in Sabah, approximately 700 km north of our study site (Wong et al. 2004). Daily
activity rhythms and time budgets in bears have been related to seasonal changes in sunrise and
sunset, weather conditions, food type and abundance, human disturbance, presence of other
Movements and activity patterns of female sun bears 69
bears (of the same or another species) and the bear’s sex, age and family associations (e.g.,
Amstrup and Beecham 1976, Garshelis and Pelton 1980, Ayers et al. 1986, Roth and Huber
1986, Clevenger et al. 1990, Reid et al. 1991, Lariviere et al. 1994, MacHutchon et al. 1998,
Holm et al. 1999, MacHutchon 2001, Wagner et al. 2001, Paisley and Garshelis 2006, Hwang and
Garshelis 2007). Our study area had minimal seasonal variation in day length and the sun bears
showed only short-term changes in activity patterns related to rainfall.
Contrary to the strictly diurnal pattern of activity among our radio-collared bears, sun
bears that raided farmers’ crops adjacent to our study site were reported to be nocturnal
(Fredriksson 2005b). This is consistent with other reports indicating a switch to nocturnal be-
havior when sun bears were near humans. Griffiths and van Schaik (1993) reported nocturnal
activity among sun bears in a forest area with human activity in Aceh, Northern Sumatra, and
Nomura et al. (2004) reported that sun bears forayed into oil palm plantations in Sabah only at
night. Likewise, Wong et al. (2004) found that that camera trap photos of bears showed a more
crepuscular-nocturnal pattern than the telemetry data, and suggested that this was because
camera traps were set in places with more human odors. Other bear species are also known
to become more nocturnal in areas with high human activity (Beckmann and Berger 2003,
Kaczensky et al. 2006, Schwartz et al. 2010).
Activity levels were higher during the first year of monitoring, coinciding with the lat-
ter part of a prolonged period (1.5 years) when virtually no fruit was available in the forest
(Fredriksson 2006a). Sun bears at this time were feeding predominantly on invertebrate food
resources. To obtain sufficient quantities of this widely available, though frequently difficult to
obtain food source (i.e. termites living in hard mounds, large logs) sun bears were active for
longer periods of time. During this time they would travel relatively long distances (> 4.5 km
over a 24-hour period) but in a small area, zigzagging between predominantly invertebrate
food resources and feeding at rapid rates, a foraging behavior described for other insectivores
(Gittleman and Harvey 1982).
Distribution of locations
Consistent with their temporal response to humans, sun bears also showed spatial
avoidance of human activity. Collared sun bears in this study tended to avoid a ridge trail used
by humans during day-time. Accordingly, we conjecture that the low capture rates during this
study might also have been related to an aversion to human smells and objects, as sun bears
in the interior of the Sungai Wain Protection Forest have little experience with humans. Sun
bears that were apparently more desensitized to human influences (close to logging operations
Chapter 370
or near oil palm plantations) were caught more easily in similar traps (Nomura et. al. 2004).
Sun bears during this study also rarely ventured into forest areas that had previously
been burned. Avoidance of these areas was probably caused by a variety of factors, starting
with the inaccessible nature of burned forest areas for several years post-fire event due to
a thick impenetrable understory of ferns. Secondly, food availability was significantly reduced,
with close to 80% mortality in sun bear fruit trees (Fredriksson et al. 2006b), as well as a signifi-
cant decrease in invertebrate food resources important in the diet of sun bears (Fredriksson
et al. in prep). Reduced canopy cover due to high tree mortality post-fires, lack of cover and
resultant changes in the micro-climate (i.e., higher temperature) in burned forest areas might
also have affected sun bear use of these areas.
Conservation implications
Insular Southeast Asia still suffers the one of the highest deforestation rates in the
tropics (Butler and Laurance 2008, Sodhi et al. 2010), with lowland and peat swamp areas disap-
pearing fastest (e.g. Miettinen et al. 2011). Small patches of lowland forest, considered the rich-
est in terms of biodiversity, are now becoming the last remaining examples of this habitat, one
example of which is the SWPF. This small reserve is currently one of the last protected areas
with (partially) unburned coastal lowland rainforest in East Kalimantan, a forest type previously
covering several million ha. Can these small reserves continue to play a role for the conserva-
tion of sun bears? Several of the results from our study indicate that they can.
The sun bears monitored in SWPF were found to have relatively small home ranges,
with significant home range overlap. Sun bears here did not display seasonal movements, nor
did ranges of female sun bears monitored in the center of the reserve go near the forest edge.
In addition, a considerable number of (breeding) sun bears were observed in the area.
Sun bears in SWPF also tended to avoid humans, both spatially as well as temporally, a
useful trait as humans pose the prime threat to this species.
Sun bear populations can thus seemingly persist, even in such small reserves; the same
result was found for mainly insectivorous sloth bears, which also have small ranges (Ratnayeke
et al. 2007). However, persistence of large wildlife in these small reserves strongly depends
on poaching pressure (Harrison 2011). Bears may be killed for their parts, or as a result of
conflicts with humans. Bears living near forest edges are attracted to crops, especially when
natural food supplies are low, making border areas potential demographic sinks (Woodroffe
and Ginsberg 1998). Sun bears are also a frequent by-catch in snares placed for primarily for
ungulates at forest edges in Kalimantan (G. Fredriksson pers. obs.). Poaching of bears for their
Movements and activity patterns of female sun bears 71
body parts has been on the rise in Southeast Asia (Mills et al. 1995, Dang 2006, Shepherd and
Nijman 2007, Shepherd and Shepherd 2010, Foley et al. 2011) and in several parts of mainland
Southeast Asia sun bears have been hunted close to extinction, even from large protected
areas (Scotson 2011).
The long-term future of sun bears living in such small reserves will also depend on the
habitat matrix surrounding these areas, and their connectivity to other forest areas. The fact that
sun bears are a forest dependent species, combined with their tendency to avoid human distur-
bance, might hamper their movement though human-dominated areas between forest patches.
AcknowledgementsWe thank the Indonesian Institute of Sciences (LIPI) for granting GMF permission to
carry out research on sun bears in East Kalimantan. GMF would like to express gratitude to
the Forest Research Institute in Samarinda for their assistance. The Tropenbos Foundation, the
Borneo Orangutan Foundation, and the Conservation Endowment Fund of the American Zoo
and Aquarium Association provided financial assistance. Field assistants Trisno, Lukas, Damy and
Adi are thanked for various help in the forest throughout the years, as well as many people
from the Sungai Wain village who helped with ferrying logistical supplies and traps. Various
students from the Mulawarman University in Samarinda are thanked for their collaboration in
the forest during various student projects, especially Wiwin Effendi, Joned, Eko and Ali Mustofa.
Ente Rood and Matthew Nowak are thanked for assistance with statistics. Graham Usher is
thanked for all help with GIS analysis and maps for this paper.
ReferencesAmstrup, S.C., and Beecham, J. (1976). Activity patterns of radio-collared black bears in Idaho. Journal of
Wildlife Management 40, 340-348.
Ashton, P.S., Givnish, T.J., and Appanah, S. (1988). Staggered flowering in the Dipterocarpaceae - New in-
sights into floral induction and the evolution of mast Fruiting in the aseasonal tropics. Am Nat
132, 44-66.
Ayres, L.A., Chow, L.S., and Graber, D.M. (1986). Black Bear Activity Patterns and Human Induced Modifica-
tions in Sequoia National Park. Bears: Their Biology and Management 6, 151-154.
Beckmann, J. P. and J. Berger. (2003). Rapid ecological and behavioural changes in carnivores: the responses
of black bears (Ursus americanus) to altered food. Journal of Zoology 261:207-212.
Chapter 372
Beringer, J., S.G. Seibert, A.J. Brody, M.R. Pelton, and Gilder, L.D.V. (1988). The influence of a small sanctuary
on survival rates of black bears in North Carolina. Journal of Wildlife Management 62, 727–734.
Blanchard, B.M., and Knight, R.M. (1991). Movements of Yellowstone Grizzly bears. Biological Conservation
58, 41-67.
Broich, M., Hansen, M., Stolle, F., Potapov, P., Margono, B.A., and Adusei, B. (2011). Remotely sensed forest
cover loss shows high spatial and temporal variation across Sumatera and Kalimantan, Indonesia
2000-2008. Environmental Research Letters 6, 014010.
Bruner, A.G., Gullison, R.E., Rice, R.E., and da Fonseca, G.A.B. (2001). Effectiveness of parks in protecting
tropical biodiversity. Science 291, 125-128.
Butler, R.A., and Laurance, W.F. (2008). New strategies for conserving tropical forests. Trends in Ecology &
Evolution 23, 469-472.
Castellanos, A. (2011). Andean bear home ranges in the Intag region, Ecuador. Ursus 22, 65-73.
Clevenger, A.P., Purroy, F.J., and Pelton, M.R. (1990). Movement and Activity Patterns of a European Brown
Bear in the Cantabrian Mountains, Spain. Bears: Their Biology and Management 8, 205-211.
Collins, N.M. (1989). Termites. In Tropical Rain Forest Ecosystems Biogeographical and Ecological Studies,
H. Lieth, and M.J.A. Werger, eds. (Amsterdam, Elsevier), pp. 455-471.
Curran, L.M., and Leighton, M. (2000). Vertebrate responses to spatiotemporal variation in seed production
of mast-fruiting dipterocarpaceae. EcolMonogr 70, 101-128.
Curran, L.M., Trigg, S.N., McDonald, A.K., Astianti, D., Hardiono, Y.M., Siregar, P., Caniago, I., and Kasischke,
E. (2004). Lowland forest loss in protected areas of Indonesian Borneo. Science 303, 1000-1003.
Dahle, B., and Swenson, J.E. (2003). Seasonal range sizes in relation to reproductive strategies in brown
bears Ursus arctos. Journal of Animal Ecology 72, 660-667.
Dang, N.X. (2006). The status and conservation of bears in Vietnam. In Understanding Asian bears to secure
their future (Ibaraki, Japan, Japan Bear Network), pp.61-65.
Ewer, R.F.(1973). The carnivores. Cornell University Press, Ithaca, NY, USA.
FAO (2010). Global Forest Resources Assessment: Indonesia. (Rome, Food and Agricultural Organization
of the United Nations, Forestry Department). FRA2010/095.
FAO (2011).State of the World’s Forests 2011. (Rome, Food and Agricultural Organization of the United
Nations).
Ferguson, S. H., M. K. Taylor, E. W. Born, A. Rosing-Asvid, and F. Messier (1999). Determinants of Home Range
Size for Polar Bears (Ursus maritimus). Ecology Letters 2:311-318.
Fitzherbert, E.B., Struebig, M.J., Morel, A., Danielsen, F., Brühl, C.A., Donald, P.F., and Phalan, B. (2008). How
will oil palm expansion affect biodiversity? Trends in Ecology & Evolution 23, 538-545.
Movements and activity patterns of female sun bears 73
Foley, K.E., Stengel, C.J., and Shepherd, C.R. (2011). Pills, Powders, Vials and Flakes: the bear bile trade in Asia
(Petaling Jaya, Selangor, Malaysia, TRAFFIC Southeast Asia).
FWI/GFW (2002). The State of the Forest: Indonesia (Bogor, Indonesia, and Washington D.C., Forest Watch
Indonesia, Global Forest Watch), pp. 104.
Fredriksson, G.M. (2001). Conservation threats facing sun bears, Helarctos malayanus, and experiences with
sun bear reintroductions in East Kalimantan, Indonesia. In: The evaluation of bear rehabilitation
projects from a conservationist viewpoint (Ouwehands Zoo, Rhenen, Netherlands).
Fredriksson, G.M. (2002). Extinguishing the 1998 forest fires and subsequent coal fires in the Sungai Wain
Protection Forest, East Kalimantan, Indonesia. In: Communities in flames: proceedings of an inter-
national conference on community involvement in fire management (Bangkok, Thailand, FAO and
FireFight SE Asia).
Fredriksson, G.M. (2005a). Predation on sun bears by reticulated python in East Kalimantan, Indonesian
Borneo. The Raffles Bulletin of Zoology 53, 197-200.
Fredriksson, G.M. (2005b). Human sun bear conflicts in East Kalimantan, Indonesian Borneo.Ursus 16,
130-137.
Fredriksson, G.M., Wich, S.A., and Trisno (2006a). Frugivory in sun bears (Helarctos malayanus) is linked to
El Niño-related fluctuations in fruiting phenology, East Kalimantan, Indonesia. Biological Journal of
the Linnean Society 89, 489-508.
Fredriksson, G.M., Danielsen, L.S., and Swenson, J.E. (2006b). Impacts of El Niño related drought and forest
fires on sun bear fruit resources in lowland dipterocarp forest of East Borneo. Biodiversity and
Conservation 15, 1271-1301.
Fredriksson, G., Steinmetz, R., Wong, S. &Garshelis, D.L. (IUCN SSC Bear Specialist Group) 2008.Helarc-
tosmalayanus. In: IUCN 2012. IUCN Red List of Threatened Species. Version 2012.1. <www.iucn-
redlist.org>. Downloaded on 20 July 2012.
Garshelis, D.L., and Pelton, M.R. (1980). Activity of black bears in the Great Smoky Mountains National
Park.Journal of Mammalogy 61, 8-19.
Garshelis, D.L., and Pelton, M.R. (1981). Movements of black bears in the Great Smoky Mountains National
Park. Journal of Wildlife Management 45, 912-925.
Garshelis, D. L. (1983). The role of sampling intensity in the selection of a home range model. Pages 321-334.
Int. Conf. Wildl. Biotelem.
Garshelis, D.L., and McLaughlin, C.R. (1998). Review and evaluation of breakaway devices for bear radiocol-
lars. Ursus 10, 459-465.
Garshelis, D.L. (2004). Variation in Ursid life histories – is there an outlier? In Giant Pandas: biology and
conservation: 53–73. Lindburg, D. & Baragona,K.(Ed.). Berkeley: University of California Press.
Chapter 374
Garshelis, D.L. (2009). Family Ursidae (Bears). Pages 448–497 in D.E. Wilson and R.A. Mittermeier, editors.
Handbook of the mammals of the world. Volume 1. Carnivores. Lynx Edicions, New York, USA.
Gaveau, D.L.A., Epting, J., Lyne, O., Linkie, M., Kumara, I., Kanninen, M., and Leader-Williams, N. (2009). Evalu-
ating whether protected areas reduce tropical deforestation in Sumatra. Journal of Biogeography
36, 2165-2175.
Gittleman, J.L., and Harvey, P.H. (1982). Carnivore home-range size, metabolic needs and ecology. Behavio-
ral Ecology and Sociobiology 10, 57-63.
Gompper, M.E., and Gittleman, J.L. (1991). Home range scaling: intraspecific and comparative trends. Oe-
cologia 87, 343-348.
Griffiths, M., and Van Schaik, C.P. (1993).The impact of human traffic on the abundance and activity periods
of Sumatran rain forest wildlife. Conservation Biology 7, 623-626.
Harrison, R.D. (2011). Emptying the Forest: Hunting and the Extirpation of Wildlife from Tropical Nature
Reserves. BioScience 61, 919-924.
Holm, G.W., Lindzey, F.G., and Moody, D.S. (1999).Interactions of sympatric black and grizzly bears in north-
west Wyoming. Ursus 11, 99-108.
Horsfield, T. (1825). Description of the Helarctos euryspilus; exhibiting in the bear from the island of Borneo,
the type of a subgenus of Ursus. Zoological Journal 2, 221-234.
Hwang, M.-H., and Garshelis, D.L. (2007). Activity patterns of Asiatic black bears (Ursus thibetanus) in the
Central Mountains of Taiwan. Journal of Zoology 271, 203-209.
Hwang, M.-H., Garshelis, D.L., Wu, Y.-H., and Wang, Y. (2010). Home ranges of Asiatic black bears in the Cen-
tral Mountains of Taiwan: Gauging whether a reserve is big enough. Ursus 21, 81-96.
Johnson, K.G., and Pelton, M.R. (1980). Prebaiting and snaring techniques for black bears.WildlSoc Bull 8,
46-54.
Joshi, A.R., Garshelis, D.L., and Smith, J.L.D. (1995). Home ranges of sloth bears in Nepal: Implications for
conservation. Journal of Wildlife Management 59, 204-214.
Kaczensky, P., D. Huber, F. Knauer, H. Roth, A. Wagner, and J. Kusak (2006). Activity patterns of brown bears
(Ursus arctos) in Slovenia and Croatia. Journal of Zoology 269:474-485.
Kikkawa, J., and Dwyer, P.D. (1992). Use of scattered resources in rain forest of humid tropical lowlands.
Biotropica 24, 293-308.
Kinnaird, M.F., Sanderson, E.W., O’Brien, T.G., Wibisono, H.T., and Woolmer, G. (2003). Deforestation trends
in a tropical landscape and implications for endangered large mammals. Conservation Biology 17,
245-257.
Koehler, G.M., and Pierce, D.J. (2003). Black bear home-range sizes in Washington: climatic, vegetative, and
social influences. Journal of Mammalogy 84, 81-91.
Movements and activity patterns of female sun bears 75
Koh, L.P. (2007). Potential Habitat and Biodiversity Losses from Intensified Biodiesel Feedstock Production.
Conservation Biology 21, 1373-1375.
Kramer, R.A., van Schaik, C.P., and Johnson, J., eds. (1997). Last Stand: Protected areas and the defense of
tropical biodiversity (New York, Oxford University Press).
Lariviere, S., Huot, J., and Samson, C. (1994).Daily activity patterns of female black bears in a northern
mixed-forest environment. Journal of Mammalogy 75, 613-620.
Linkie, M., Dinata, Y., Nugroho, A., and Haidir, I.A. (2007). Estimating occupancy of a data deficient mamma-
lian species living in tropical rainforests: Sun bears in the Kerinci Seblat region, Sumatra. Biological
Conservation 137, 20-27.
Linkie, M., Rood, E., and Smith, R. (2010).Modelling the effectiveness of enforcement strategies for avoiding
tropical deforestation in Kerinci Seblat National Park, Sumatra. Biodiversity and Conservation 19,
973-984.
Liu, X., A. K. Skidmore, T. Wang, Y. Yong, and H. H. T. Prins (2002). Giant Panda Movements in Foping Nature
Reserve, China. The Journal of Wildlife Management 66:1179-1188.
MacHutchon, A.G. (2001). Grizzly bear activity budget and pattern in the Firth River Valley, Yukon. Ursus
12, 189-198.
MacHutchon, A.G., Himmer, S., Davis, H., and Gallagher, M. (1998). Temporal and spatial activity patterns
among coastal bear populations. Ursus 10, 539-546.
McLoughlin, P.D., Case, R.L., Gau, R.J., Ferguson, S.H., and Messier, F. (1999). Annual and seasonal movement
patterns of barren-ground grizzly bears in the central Northwest Territories. Ursus 11, 79-86.
McLoughlin, P.D., Ferguson, S.H., and Messier, F. (2000). Intraspecific Variation in Home Range Overlap
with Habitat Quality: A Comparison among Brown Bear Populations. Evolutionary Ecology 14,
39-60.
McNab, B. K. 1963. Bioenergetics and the determination of home range size. American Naturalist
97:133-140.
McNab, B. K. 1983.Ecological and behavioral consequences of adaptation to various food resources. Pages
664-697 in J. F. Eisenberg and D. G. Kleiman, editors. Advances in the study of mammalian behavior.
American Society of Mammalogists Special Publication 7.
McPhaden, M.J. (1999). El Niño -The child prodigy of 1997-98.Nature 398, 559-562.
Medway, L. (1972). Phenology of a tropical rain forest in Malaya.Biological Journal of the Linnean Society
4, 117-146.
Meijaard, E. (2004).Craniometric differences among Malayan sun bears (Ursus malayanus); evolutionary and
taxonomic implications.Raffles Bulletin of Zoology 52, 665-672.
Chapter 376
Meijaard, E., Sheil, D., Rosenbaum, B., Iskandar, D., Augeri, D., Setyawati, T., Duckworth, W., Lammertink, M.J.,
Rachmatika, I., Nasi, R., et al. (2005). Life after logging: reconciling wildlife conservation and produc-
tion forestry in Indonesian Borneo (Bogor, Indonesia, CIFOR, WCS and UNESCO).
Meijaard, E. and D. Sheil. 2008. The persistence and conservation of Borneo’s mammals in lowland rain
forests managed for timber: observations, overviews and opportunities. Ecological Research
23:21-34.
Miettinen, J., Shi, C., and Liew, S.C. (2011). Deforestation rates in insular Southeast Asia between 2000 and
2010. Global Change Biology 17, 2261-2270.
Mills, J.A., Chan, S., and Ishihara, A.P. (1995).The bear facts. The East Asian market for bear gall bladder
(Cambridge, TRAFFIC International), pp. 41.
Nea, C., and Nong, D. (2006). The conservation of bears in Cambodia. In Understanding Asian bears to
secure their future (Ibaraki, Japan, Japan Bear Network), pp. 57-60.
Nomura, F., Higashi, S., Ambu, L., and Mohamed, M. (2004).Notes on oil palm plantation use and seasonal
spatial relationships of sun bears in Sabah, Malaysia. Ursus 15, 227–231.
Paisley, S., and Garshelis, D.L. (2006).Activity patterns and time budgets of Andean bears (Tremarctos orna-
tus) in the Apolobamba Range of Bolivia. Journal of Zoology 268, 25–34.
Powell, R.A., Zimmerman, J.W., Seaman, D.E., and Gilliam, J.F. (1996). Demographic analyses of a hunted
black bear population with access to a refuge. Conservation Biology 10, 224-234.
Powell, R. A. ()2000. Animal home ranges and territories and home range estimators. in L. Boitani and T.
K. Fuller, editors. Research techniques in animal ecology. Columbia University Press, New York.
Ratnayeke, S., van Manen, F.T., and Padmalal, U.K.G.K. (2007). Home Ranges and Habitat Use of Sloth Bears
Melursusursinusinornatus in Wasgomuwa National Park, Sri Lanka. Wildlife Biology 13, 272-284.
Redford, K. H. (1987). Ants and termites as food.Patterns of Mammalian Myrmecophagy. Pages 349-397 in
H. H. Genoways, editor. Current Mammalogy. Plenum press, Nebraska.
Reid, D., Jiang, M., Teng, Q., Qin, Z., and Hu, J. (1991). Ecology of the asiatic black bear (Ursus thibetanus) in
Sichuan, China. Mammalia 55, 221-237.
Roth, H.U., and Huber, D. (1986). Diel Activity of Brown Bears in Plitvice Lakes National Park, Yugoslavia.
Bears: Their Biology and Management 6, 177-181.
Schwartz, C. C., S. L. Cain, S. Podruzny, S. Cherry, and L. Frattaroli (2010). Contrasting Activity Patterns of
Sympatric and Allopatric Black and Grizzly Bears. Journal of Wildlife Management 74:1628-1638.
Scotson, L. (2011). The distribution and status of Asiatic black bears Ursus thibetanus and sun bears Helarc-
tos malayanus in Xe Pian National Protected Area, Lao PDR (Free the Bears Fund, WCS, WWF).
Movements and activity patterns of female sun bears 77
Shepherd, C., and Nijman, V. (2008). The trade in bear parts from Myanmar: an illustration of the ineffective-
ness of enforcement of international wildlife trade regulations. Biodiversity and Conservation 17,
35-42.
Shepherd, C.R., and Shepherd, L.A. (2010). The Poaching and Trade of Malayan Sun Bears in Peninsular Ma-
laysia: New legislation to provide stronger deterrents. TRAFFIC Bulletin 23, 49-52.
Sodhi, N., Posa, M., Lee, T., Bickford, D., Koh, L., and Brook, B. (2010).The state and conservation of South-
east Asian biodiversity. Biodiversity and Conservation 19, 317-328.
Steinmetz, R., Garshelis, D.L., Chutipong, W., and Seuaturien, N. (2011).The shared preference niche of
sympatric Asiatic Black Bears and Sun Bears in a tropical forest mosaic. PLoS One 6, e14509.
Steinmetz, R., Garshelis, D.L., Chutipong, W., and Seuaturien, N. (2012).Foraging ecology and coexistence
of Asiatic black bears and sun bears in a seasonal tropical forest in Southeast Asia. Journal of
Mammalogy
Terborgh, J., Schaik, C.P.v., L.Davenport, and Rao, M., eds. (2002). Making parks work (Island Press,USA).
Tumbelaka, L., and Fredriksson, G.M. (2006). The status of sun bears in Indonesia. In Understanding Asian
bears to secure their future (Ibaraki, Japan, Japan Bear Network), pp. 73-78.
van Nieuwstadt, M.G.L. (2002). Trial by fire-Postfire development of a dipterocarp forest (PhD thesis Uni-
versity of Utrecht, Netherlands), pp. 1-143.
Vinitpornsawan, S., Steinmetz, R., and Kanchanasakha, B. (2006).The status of bears in Thailand.In Under-
standing Asian bears to secure their future (Ibaraki, Japan, Japan Bear Network), pp. 50-56.
Wagner, R.O., Hightower, D.A., and Pace, R.M., III (2001). Measuring levels and patterns of activity in black
bears. Ursus 12, 181-188.
Wich, S. A., E. R. Vogel, M. D. Larsen, G. M. Fredriksson, M. Leighton, C. P. Yeager, F. Q. Brearley, C. P. van Schaik,
and A. J. Marshall. 2011. Forest Fruit Production Is Higher on Sumatra Than on Borneo. PLoS ONE
6:Published online 2011 June 2028.doi: 2010.1371/ journal.pone.0021278.
Wielgus, R.B. (2002). Minimum viable population and reserve sizes for naturally regulated grizzly bears in
British Columbia. Biological Conservation 106, 381–388.
Wong, S.T., Servheen, C., and Ambu, L. (2002). Food habits of malayan sun bears in lowland tropical forest
of Borneo. Ursus 13, 127-136.
Wong, S.T., Servheen, C., and Ambu, L. (2004). Home range, movement and activity patterns, and bedding
sites of Malayan sun bears, Helarctos malayanus in the rainforest of Borneo. Biological Conserva-
tion 119, 168-181.
Wong, S.T., Servheen, C., Ambu, L., and Norhayati, A. (2005). Impacts of fruit production cycles on Malayan
sun bears and bearded pigs in lowland tropical forest of Sabah, Malaysian Borneo. Journal of Tropi-
cal Ecology 21, 627–639.
Chapter 378
Wong, S.T. (2006). The status and conservation of bears in Malaysia. In Understanding Asian bears to secure
their future (Ibaraki, Japan, Japan Bear Network), pp.66-72.
Wood, T. G. and W. A. Sands (1978). The role of termites in ecosystems. Pages 245-292 in M. V. Brian, editor.
Production ecology of ants and termites. Cambridge University Press, Cambridge, UK.
Woodroffe, R., and Ginsberg, J.R. (1998). Edge effects and the extinction of populations inside protected
areas. Science 280, 2126-2128.
Woodroffe, R. (2001). Strategies for carnivore conservation: Lessons from contemporary extinctions. In
Carnivore conservation, J.L. Gittleman, S.M. Funk, D.W. Macdonald, and R.K. Wayne, eds. (Cam-
bridge, UK, Cambridge University Press), pp. 61–92.
Worton, B. J. 1987. A review of models of home range for animal movement. Ecological Modeling 38:277-298.
Chapter 4
Impacts of El Niño related drought and forest
fires on sun bear fruit resources in lowland
dipterocarp forest of East Borneo
With L.S. Danielsen and J.E. Swenson
Biodiversity and Conservation (2006), 15(4): 1271-1301
Chapter 482
Abstract
Droughts and forest fires, induced by the El Niño/Southern Oscillation (ENSO) event,
have increased considerably over the last decades affecting millions of hectares of rainforest.
We investigated the effects of the 1997-98 forest fires and drought, associated with an excep-
tionally severe ENSO event, on fruit species important in the diet of Malayan sun bears (Helarc-
tos malayanus) in lowland dipterocarp forest, East Kalimantan, Indonesian Borneo. Densities
of sun bear fruit trees (≥10 cm DBH) were reduced by ~80%, from 167 ± 41 (SD) fruit trees
ha-1 in unburned forest to 37 ± 18 fruit trees ha-1 in burned forest. Densities of hemi-epiphytic
figs, one of the main fallback resources for sun bears during periods of food scarcity, declined
by 95% in burned forest. Species diversity of sun bear food trees decreased by 44% in burned
forest. Drought also affected sun bear fruit trees in unburned primary forest, with elevated
mortality rates for the duration of 2 years, returning to levels reported as normal in region
in the third year after the ENSO event. Mortality in unburned forest near the burn-edge was
higher (25 ± 5% of trees ≥10 cm DBH dead) than in the forest interior (14 ± 5% of trees),
indicating possible edge effects. Combined effects of fire and drought in burned primary forest
resulted in an overall tree mortality of 78 ± 11% (≥10 cm DBH) 33 months after the fire event.
Disturbance due to fires has resulted in a serious decline of fruit resources for sun bears and,
due to the scale of fire damage, in a serious decline of prime sun bear habitat. Recovery of sun
bear populations in these burned-over forests will depend on regeneration of the forest, its
future species composition, and efforts to prevent subsequent fire events.
Effects of fires on sun bear fruit resources 83
Introduction
Severe droughts, associated with increased occurrences of El Niño/Southern Oscil-
lation (ENSO) events, have become more frequent over the past decades (e.g. Timmermann
et al. 1999). These droughts have created conditions conducive for uncontrolled fires, which
have damaged extensive areas of forest throughout the tropics, with fires in Southeast Asia
being particularly severe on the islands of Borneo and Sumatra (Goldammer and Mutch 2000;
Tacconi 2003). In recent years, forest fires have caused more deforestation than intentional
clearing in some tropical regions (e.g. Cochrane et al. 1999). On Borneo between 3-5 million
ha of primary forest were affected by fires in 1982-83 during a severe ENSO related drought
(Lennertz and Panzer 1984; Malingreau et al. 1985). Smaller fire events occurred in 1990, 1992
and 1994, all coinciding with ENSO episodes (Salafsky 1998). During the severe 1997-98 ENSO
event primary forest areas burned easily (Siegert et al. 2001) as prior drought stress led to
the shedding of leaves by evergreen species and accumulation of dry litter on the forest floor
(GMF pers. obs.). In 1997-98 in the Indonesian province of East Kalimantan alone, 5.2 million
ha of land were affected by the fires, 2.6 million ha of which were forest, including several
protected lowland reserves (Hoffman et al. 1999; Siegert et al. 2001; Fuller et al. 2004). Areas
previously affected by fires have also become susceptible to more intense fires due to higher
fuel loads and rapid desiccation, now even during ‘normal’ dry seasons (Cochrane and Schulze
1999; Cochrane et al. 1999; Laurance 2003).
Several studies have investigated the effects of the 1997-98 drought and fires on tree
mortality and forest structure (e.g. Nakagawa et al. 2000; Williamson et al. 2000; van Nieu-
wstadt 2002; Slik et al. 2002; Potts 2003; Slik and Eichhorn 2003; Slik 2004). Their findings
showed that drought significantly increased mortality rates in unburned forest (Nakagawa et al.
2000; van Nieuwstadt 2002; Potts 2003; Slik 2004; van Nieuwstadt and Sheil 2005), that overall
tree mortality was extremely high in burned areas (van Nieuwstadt and Sheil 2005), that fire
resulted in a strong reduction of climax tree density (Slik and Eichhorn 2003), and that spe-
cies composition changed after fire damage due to disproportionate mortality of certain tree
species groups and tree size classes (Slik et al. 2002; Slik 2004). Shifts in species composition
in natural forest occur slowly under ‘normal’ conditions (Swaine et al. 1987), but catastrophic
disturbances like repeated fires can reduce structural and biological complexity in forests
(Schindele et al. 1989). Fire-return intervals of less than 90 years can eliminate rainforest tree
species, whereas intervals of less than 20 years may eradicate tree growth entirely resulting in
savanna-like landscapes (Cochrane et al. 1999).
Chapter 484
Few studies however have investigated the effects of drought and forest fires on wild-
life or their food resources in Indonesia (Doi 1988; Anggraini et al. 2000; O’Brien et al. 2003).
Forest-dependent species tend to become less abundant or even locally extinct and other,
less-forest-dependent species invade the area or increase in abundance (Doi 1988; Anggraini
et al. 2000; see also Barlow et al. 2002; Peres et al. 2003). Some of the larger, long-lived species
persist, reluctant or unable to relocate themselves (Suzuki 1992; Anggraini et al. 2000), although
effects on their life-history remain largely unknown (but see O’Brien et al. 2003). Furthermore,
the proximate causes of why individual species perish or flourish – e.g. decreased or increased
food-availability, reduced nest-sites – remain unstudied.
We studied the effects of fires on a variety of food resources important in the diet
of one of the largest extant mammals on Borneo, the Malayan sun bear. Sun bears are partly
frugivores (McConkey and Galetti 1999; Wong et al. 2002; Fredriksson et al. in press), although
during periodic mast-fruiting events fruit makes up almost 100% of the diet (Fredriksson et al.
in press). These mast-fruiting events provide the opportunity for sun bears to gorge themselves
on large amounts of succulent fruits, probably enabling them to build up, or recover, fat and
energy reserves for the prolonged period of fruit lows preceding and following these supra-
annual mast fruiting events (Fredriksson et al. in press). Sun bears are considered important
actors in forest dynamics, in part due to their seed dispersal abilities (McConkey and Galetti
1999), especially of large-seeded fruits (Fredriksson unpubl. data). Preliminary data suggests
that sun bears make little use of burned forest areas for several years after a fire event (Doi
1988; Fredriksson unpubl. data).
The aims of this study were i) to investigate the effect of forest fires on the density of
sun bear fruit resources; ii) to quantify the effect of forest fires on species diversity of sun bear
fruit resources; and iii) to study the effect of drought on mortality of sun bear food trees in
unburned forest and based on the above iv) discuss the effects of these changes on sun bear
populations in fire affected areas.
Methods
Study area
The study was carried out in the lowland dipterocarp forest of the Sungai Wain Protec-
tion Forest (SWPF), a reserve near Balikpapan, East Kalimantan, Indonesian Borneo (1º 16’ S
and 116º 54’ E) (Fig. 1). The reserve covers a watercatchment area of ca 100 km2. Average
Effects of fires on sun bear fruit resources 85
Figure 1. Map showing the location of Sungai Wain forest on the island of Borneo. The enlargement shows
the Sungai Wain forest, indicating the unburned area (dark grey), and burned areas (light grey). The location
of pairs of burned and unburned edge plots is shown. The circular inset shows an example of the lay out of
one pair burned-unburned edge plots over the fire edge.
annual rainfall was 2740 ± 530 mm (1998-2003). The topography of the reserve consists of
gentle to sometimes steep hills, and is intersected by many small rivers. The area varies in
altitude from 30 to 150 metres a.s.l. Trees with stems greater than 10 cm DBH (diameter at
breast height) are dominated by the families Euphorbiaceae, Dipterocarpaceae, Sapotaceae, and
Myrtaceae. The relative dominance of Dipterocarpaceae increases substantially in the larger
size classes. Due to an altitudinal gradient, with rivers running in a north-south direction, the
southern part of the reserve is moister. Dipterocarpaceae, dominant in the northern part of
the reserve (above 10 cm DBH) decrease in abundance towards the moister south where Sa-
potaceae and Euphorbiaceae become more dominant. The 25 most common tree species form
40% of the total stem density (van Nieuwstadt 2002). Several palm genera (Borassodendron,
Oncosperma, Polydocarpus, Licuala) are common in the subcanopy and understory (especially
rattans), and ginger species (Costaceae and Zingiberaceae) as well as Marantaceae, Araceae,
and Pandanaceae are common in the understory. This paper only deals with trees >10 cm DBH.
All growth forms of figs (Ficus spp.) were included. Only hemi-epiphytic figs with a diameter of
≥3 cm were included as potential food resources, as these were observed to bear fruits and to
be fed upon by sun bears (Fredriksson pers. obs).
Chapter 486
History of forest fires at the study site
Most of the reserve was unaffected by fires at the start of the study in 1997, except
for a small area near the eastern border that had burned in 1982-83. The prolonged drought of
the 1982-83 ENSO, and several subsequent shorter ENSO droughts, probably caused elevated
levels of mortality among large trees, resulting in an irregular canopy cover. Consequently the
primary forest became increasingly vulnerable to desiccation during droughts and more sus-
ceptible to fires. Drought in the region started in May 1997 and continued intermittently till
late April 1998, with 6 out of 12 months having no rainfall at all, or well below 100 mm. Fires
entered the SWPF in March 1998, initially from a neighbouring state-owned logging concession,
but subsequently also from surrounding agricultural fields. Fires moved slowly through the leaf
litter and remained mainly in the undergrowth. Occasionally the fire reached into the crowns
of older trees with hollow trunks, or dead standing trees with resin residues. In burned areas,
all leaf litter and surface soil humus was reduced to ash, and mortality of seedlings and sap-
lings was close to 100% (Fredriksson pers. obs.). Fire breaks were created over a period of 2
months but nevertheless approximately 50% of the reserve was affected by the fires (Fredriks-
son 2002), leaving an unburned central core of some 4,000 ha of primary forest.
Permanent sampling plots
In the SWPF, 18 permanent sample plots (PSP), of 20 x 200 m (0.4 ha) each, were estab-
lished in once-burned forest and adjacent unburned forest after the fire event in 1998 (Fig. 1)
by the Wanariset Research Station (Tropenbos-Kalimantan Project). The set-up of the PSPs was
designed around man-made firebreaks of ~1.5 m wide (see van Nieuwstadt 2002). Because
the fire-breaks did not correspond to any topographical feature in the places where the PSPs
were positioned, this allowed for a random sampling scheme with paired plots of unburned and
burned forest at a short distance from each other. The PSPs were laid out in nine pairs, each
pair of PSPs adjacent to each other over the firebreak between burned and unburned forest,
forming one contiguous transect of 20 x 400 m, half in burned and half in unburned forest. The
unburned PSPs lie adjacent to the burn edge and these plots are labelled ‘unburned edge plots’.
The PSPs were nested in three groups and spread over a total area of circa 20 km2 (Fig. 1).
The distance between two pairs of PSPs was more than 500 m. We counted and meas-
ured all trees (≥10 cm DBH) in the PSPs 33 months after the fires, and calculated the percent-
age of live trees in both burned and unburned edge PSPs. Liana’s were not sampled, as they only
make up a small proportion (<1%) of fruits encountered in the diet of sun bears at the study
site (Fredriksson et al. in press).
Effects of fires on sun bear fruit resources 87
Mortality rates
Annual mortality rates were calculated from ten 0.1-ha phenology plots (total 1 ha, all
trees ≥10 cm DBH, n=549 trees at the start of the study) which were monitored on a monthly
basis between January 1998–July 2004. These phenology plots were positioned in unburned
forest at least 1 km from the burn edge, and are subsequently called ‘unburned interior’ plots.
Annual mortality rates for the interior plots are calculated based on exact 12 month periods
(Jan-Dec).
Mortality rate was determined as: m={1-(Nt /N
0)1/t}* 100
where ‘m’ is mortality per year, N0 is the initial number of live individuals and N
t is the number
of live individuals at re-census interval t (e.g. Sheil and May 1996). Percentage of live trees was
calculated for the interior plots for the same time interval as for the burned and unburned
edge plots.
Densities of tree species important in the diet of the
sun bear
A list of 115 fruit species eaten by sun bears in the study area was available from Fre-
driksson et al. (in press). All trees (≥ 10 cm DBH) that provided these fruits were subsequently
labelled ‘sun bear fruit trees’. Densities of sun bear fruit trees and all Ficus spp. were subse-
quently calculated for the three subsets of plots.
Two common species-rich genera which occur in the diet of the sun bear (Syzigium spp.
[Fam. Myrtaceae]; Diospyros spp. [Fam. Ebenaceae]) posed a problem for density calculations as
identification to species level is difficult. Only certain species from these genera were fed upon
by the bears, whereas others were consistently ignored. In order to avoid overestimation of
the density of these genera, we first calculated the percentage of trees from these genera in the
1 ha interior plots that belonged to species actually fed upon by sun bears, based on leaf and
fruit samples collected during direct feeding observations of sun bears. For both genera this
was found to be approximately 50% of the individual trees in the 1 ha interior plots. Therefore,
the density of these taxa as potential sun bear food resources was reduced by 50% for further
analyses in all plots. Two other taxa, Madhuca kingiana [Fam Sapotaceae] and Pternandra spec.
[Fam Melastomataceae], were infrequently encountered in the diet of the bears, but are com-
mon in the forest. In order to avoid overestimating the densities of sun bear fruit trees, we
reduced the density of these species also by 50% in the analyses.
Chapter 488
Statistical analysis
Differences between burnt and unburned forest plots were compared with paired t-
tests. A one-way ANOVA, with a Bonferroni multiple comparison test, was used to check for
differences in mortality rates between sampling regimes and years. Standard deviation is always
given when the average is presented (average ± SD). An α-level <0.05 was chosen to indicate
statistical significance.
Results
Density of fruit resources
Density of live fruit trees important in the sun bear diet, 33 months after the fire was 167
± 41 trees ha-1 in unburned edge plots and 37 ± 18 trees ha-1 in burned plots, indicating a drought
and fire-related reduction of nearly 78% (paired t-test: t=8.7, df=8, p<0.001) (Table 1). Densities
of sun bear fruit trees in the unburned interior plots was 144 trees ha-1 (total area sampled 1 ha)
at the start of the study in 1998 and declined to 133 trees ha-1 33 months after the drought.
Densities of all important sun bear fruit genera were lower in burned forest compared
to unburned edge plots, although this was only significant for 8 out of 19 genera (Table 1).
Several genera, generally occurring at low-medium densities, were not represented by any live
trees in burned plots (e.g. Monocarpia [Fam. Annonaceae], Quercus [Fam. Fagaceae], Litsea, Cryp-
tocarya [Fam. Lauraceae]). The difference in densities for these genera was not significant due
to the large variation in number of trees encountered in the 9 unburned edge plots (Table 1).
Two of the main sun bear fruit genera, Artocarpus and Dacryodes, which contribute the
bulk of fruit eaten by bears during masting events, declined significantly in densities, respectively
from 11.9 ± 6.6 trees ha-1 to 1.9 ± 2.4 trees ha-1 and 11.4 ± 7.8 trees ha-1 to 2.5 ± 2.5 trees ha-1
(Table 1). The palm Oncosperma horridum, whose fruits are favoured by sun bears, declined from
8.1 ± 4.2 trees ha-1 in unburned edge plots to zero in burned areas (Table 1).
The most important plant genus for sun bears which provides fruits during intermast
periods, Ficus spp., declined significantly in burned forest. Most epiphytic, hemi-epiphytic and
climber figs were encountered in the unburned edge plots, with only 4 of 74 figs (all sizes com-
bined) observed in burned plots (paired t-test: t=6.5, df=8, p<0.001). Densities of figs important
in the sun bear diet declined significantly from 5.6 ± 1.6 figs ha-1 in unburned edge plots and
0.3 ± 0.3 figs ha-1 in the burned plots (paired t-test: t=3.7, df=8, p=0.006), corresponding to a
reduction of ~95% following fire.
Effects of fires on sun bear fruit resources 89
Table 1. Densities (stems ≥10 cm DBH, average ± SD ha-1) calculated from 18 vegetation plots (total
7.2 ha) of the main fruit-bearing genera important in the sun bear diet in unburned edge forest (UBF-edge)
and burned forest (BF) 33 months after the 1997-98 fire event. Genera only include species that have been
found to occur in the bear diet. Densities of Ficus mainly comprise of hemi-epiphytic stranglers ≥ 3 cm diam.
P indicates significance level for paired t-test (df=8).
No significant differences were found in densities for the variably common genera
Madhuca and Diospyros. Madhuca kingiana is a dominant tree species in the permanent sample
plots in the south of the reserve, which is the moister part of the forest due to topography.
One unburned edge plot in the southern part of the forest (0.4 ha) contained 22 trees (≥10 cm
DBH) of this species compared to several unburned edge plots in the western or northern
part of the forest which contained zero trees of this species.
Density
Genera Family UBF-Edge SD Burned SD P
Madhuca Sapotaceae 16.5 21.3 2.9 4.4 ns
Artocarpus Moraceae 11.9 6.6 1.9 2.4 0.003
Dacryodes Burseraceae 11.4 7.7 2.5 2.5 0.017
Syzigium Myrtaceae 11.4 7 3.1 3.4 0.011
Baccaurea Euphorbiaceae 8.1 3.7 0.6 1.1 0.001
Oncosperma Palmae 8.1 10.5 0 - ns
Diospyros Ebeneceae 7.8 6.4 3.3 2.8 ns
Santiria Burseraceae 6.1 4.9 0.6 1.1 0.013
Ficus * Moraceae 5.6 3.9 0.3 0.8 0.006
Litsea Lauraceae 5.6 5.3 0 - 0.013
Lithocarpus Fagaceae 4.7 3.2 0.8 1.8 0.005
Garcinia Guttiferae 3.6 3.3 0.8 1.8 ns
Polyalthia Annonaceae 3.3 2.5 1.1 1.8 ns
Durio Bombacaceae 2.5 3.8 0.6 1.1 ns
Quercus Fagaceae 1.4 2.8 0 - ns
Cryptocarya Lauraceae 1.1 1.8 0 - ns
Mangifera Anacardiaceae 0.6 1.7 0.3 0.8 ns
Monocarpia Annonaceae 0.6 1.1 0 - ns
Tetramerista Tetrameristaceae 0 - 0.6 1.1 ns
All sun bear fruit species combined 166.9 40.7 36.8 17.8 <0.001
Chapter 490
Species diversity of fruit trees in burned and unburned forest
Species diversity of sun bear fruit resources declined significantly following fire (paired
t-test: t=11.9, df=8, p<0.001). At least 66 species which feature in the diet of sun bear occurred
in unburned edge plots, whereas only 37 of these were observed in burned plots, representing
a decrease of ~44% in richness of sun bear fruit species in burned forest areas (Appendix 1).
The family Lauraceae, representing the sun bear fruit genera Cryptocarya and Litsea, as well as
the family Caesalpiniaceae with the sun bear fruit genus Dialium were not encountered with
any live trees in burned sampling plots, whereas in the unburned edge plots the genus Litsea
(all species combined) occurred in 8 out of 9 plots and were represented with 20 trees. The
genus Dialium was found in 6 out of 9 unburned edge plots. A total of 46 sun bear food tree
species were encountered in the unburned interior plots (total area sampled 1 ha versus 3.6
ha sampled of burned and unburned edge plots each).
Tree mortality
Overall tree mortality (both sun bear fruit trees and tree species not fed upon by
bears) in burned forest was extremely high, with 77.5 ± 10.8% trees dead 33 months after the
fire event (range 58.2-90.0%, n=9 plots). In unburned edge plots mortality was also high with
24.9 ± 5.4 % of trees dead (range 17.7-35.6%, n=9 plots). Cumulative percentage of dead trees
in the unburned interior plots 33 months after the drought was 14.1 ± 5.2 %, some 40% lower
than encountered in the unburned edge plots.
Table 2. Annual mortality rates (%) of trees (≥10 cm DBH) in unburned interior plots calculated from ten
0.1 ha phenology plots. Mortality rates are presented separately for sun bear food trees and non-food trees,
as well as for all trees combined.
Non-bear trees Bear trees All trees combined
(n=405) (n=144) (n=549)
1998 4.69 3.47 4.37
1999 7.25 4.32 6.48
2000 2.79 0.00 2.04
2001 2.01 0.00 1.46
2002 2.35 2.26 2.32
2003 2.40 3.08 2.59
Average 3.58 2.19 3.21
Effects of fires on sun bear fruit resources 91
Mortality rates between years differed significantly (one-way ANOVA F=6.6 df=5,
p<0.001) although only mortality in 1999 was significantly different (higher) than all other
years (Bonferroni, t>3.8, p<0.006 for all comparisons). Mortality remained elevated for two
years in the interior plots and approached ‘normal’ rates reported for the region in the third
year after the drought (Table 2). Mortality rates did not differ significantly between sun bear
fruit species and species that do not occur in the diet of bears in the interior plots (t-test,
t=2.3, df=5, p=0.067), although the p-value suggested a tendency. No significant difference was
found in mortality of sun bear food trees and non-food trees between burned and edge plots
33 months after the fire (paired t-test, t>0.04, df=8, p>0.3).
DiscussionThe 1997-98 fires reduced the density of sun bear fruit tree species by nearly 80%,
three years after the fire. Fruit resources are important in the diet of sun bears, partly to
regain energy after periods of fruit scarcity and partly to build up fat reserves to cope with
prolonged intermast periods (Fredriksson et al. in press). When few fruit resources are avail-
able sun bears subsist primarily on insects although densities of these were also highly reduced
in burned forest areas (Fredriksson unpubl. data). The reduction in fruit trees measured during
this study is almost double the 44% decline reported by Leigthon and Wirawan (1986) for
fruit species important in the diet of frugivorous primates like Bornean gibbons (Hylobates
muelleri) and orangutans (Pongo pygmaeus) after the 1982-83 fires in Kutai National Park, East
Kalimantan. Possibly the figures presented Leigthon and Wirawan (1986) are underestimates
of the true extent of damage as their sampling was carried out shortly after the fire event. We
documented delayed mortality due to the fires and drought, which continued for at least two
years after the ENSO event. Mortality rates approached ‘normal’ rates reported for the region
in the third year after the drought (average 1.7 % for 9 study sites in the region see Phillips et
al. 1994; Wich et al. 1999; Potts 2003).
Fire reduced the important sun bear fruit genus Ficus spp. by 95% three years after the
fires. This serious decline might well have negative consequences in terms re-establishment or
persistence of frugivore populations, as figs have been found to be one of the main fruit re-
sources during periods of food lows for a variety of wildlife (e.g. Leighton and Leighton 1983).
Besides the large reduction of fig densities in burned areas, Harrison (2000) reported on local
extinctions of fig wasps after the ENSO drought, which affected fig fruit production, even in
forest areas unaffected by fires. Putz and Susilo (1994) however reported that ten years after
Chapter 492
the 1982-83 forest fires regeneration of hemi-epiphytic figs by establishment of new terrestrial
connections was close to 60%.
The reduction of almost 44% in species richness of sun bear fruit taxa in once-burned
forest could lead to permanent changes in the composition of sun bear fruit resources in these
areas, especially as certain sun bear fruit tree genera disappeared altogether from the burned
plots. Fires affect dominant tree species more than rare species (Slik et al. 2002; Potts 2003),
but the disappearance of rare species is more worrying as they might become locally extinct
(Cochrane and Schulze 1999). Regeneration of the forest will largely depend on the crop of
trees that sprouts after the fires. The proportion of seedlings that grew up five years after the
1982-83 fires in Sabah showed a close resemblance to the distribution of families in primary
forest, although few Dipterocarp saplings were encountered (Woods 1989). Slik et al. (2002)
found that lowland dipterocarp forest, 15 years after being affected by fire, did not show an
increase in species richness, although stem density increased, but these primarily belonged to
a few pioneer tree species (Macaranga). The recruitment of Macaranga, both in the under- and
over-storey, indicated that recovery of species composition in burnt forests takes longer than
in selectively logged forest, where after 15 years pioneer species were being replaced by pri-
mary forest species (Slik et al. 2002). Whitmore (1985) reported that a lowland dipterocarp
forest, extensively damaged by storm and fire in 1880, was still unusually poor in diversity of
upper-canopy species when surveyed some 70 years later. Close to 18 % of the burned forest
in our study area has remained as unburned forest patches in swampy areas or near streams
(Fredriksson and Nijman 2004), which might facilitate a more uniform regeneration due to
seed dispersal of forest-interior species into the burned areas. But overall, it will take decades,
if not centuries, for many slow-growing climax species to begin fruiting and provide food for
wildlife (Whitmore 1985).
Fruiting phenologies of remaining fruit trees in burned areas might also deviate from
fruiting patterns in unburned forest due to changes in environmental conditions and exposure
to higher levels of drought. Kinnaird and O’Brien (1998) reported that occurrence of flower-
ing and fruiting by trees in burned areas was lower than in adjacent unburned areas just after
the 1998 fires. The storage of water reserves in trees, which depends on availability of subsoil
water, has been found to influence flowering, although water storing capabilities differed greatly
between species (Borchert 1994). The possible influences of changed environmental conditions
in burned forest on phenological patterns calls for further studies.
Drought by itself had significant effects on sun bear food trees in unburned forest,
with elevated mortality rates up to two years after the drought. Effects of the drought on
Effects of fires on sun bear fruit resources 93
trees have been found to be differential, relative to abundance and habitat factors (Potts 2003),
with trees in moister areas less affected (Potts 2003; Slik and Eichhorn 2003; Fredriksson and
Nijman 2004). The combined effects of fire and drought were far more severe than the effects
of drought alone. Heavily burned forest areas have become dominated by pioneer species
(Woods 1989; Nykvist 1996; Toma 1999; Slik et al. 2002), have lower species diversity (Matius
et al. 2000; Slik et al. 2002; this study), and decreased soil fertility due to a loss of inorganic
nutrients (Nykvist et al. 1994; Malmer 1996). Several studies investigated the regeneration po-
tential of burned forest areas after the 1982-83 fires. Above-ground biomass in a lowland forest
in Sabah eight years after the fire was still only a quarter of adjacent unburned forest (Sim and
Nykvist 1991, Nykvist 1996).
The significant decrease in both density as well as species diversity of sun bear fruit
resources due to fire could partially explain the reduced usage of burned forest by sun bears
(Fredriksson unpubl. data). Few fresh signs of sun bears were encountered in burned areas
up to five years after the fire event, and radio-collared bears rarely entered burned forest. Al-
though the extent of the home ranges of our radio-collared bears before the fire was unknown
(as they were caught in unburned forest following the fire event), sun bears ranged throughout
the reserve prior to fires (Fredriksson 2005, Fredriksson unpubl. data,). Environmental condi-
tions like an increase in temperature due to lack of canopy cover, exposure to rain, and also the
inaccessible nature of burned areas due to a thicket of ferns which blocked the understory for
approximately four years after the fires, hampering movement for large ground-dwelling mam-
mals, probably discouraged usage by bears. Additionally, densities of various invertebrate food
resources, especially termites, declined significantly after the fires (Fredriksson et al. unpubl.
data). Doi (1988) reported that sun bears did not recover quickly after the 1982-1983 fires in
the largest lowland conservation area in East Kalimantan, the 200,000 ha Kutai National Park,
with few bear signs found even in the core of the park three years after the fires. Leighton and
Wirawan (1986) reported a decrease in vertebrate densities after the 1982-83 fires, although
large-bodied primates reportedly seemed to be the least affected, possibly due to their gener-
alized omnivorous diets and behavioural flexibility to switch food types (van Schaik et al. 1993).
On the other hand O’Brien et al. (2003) found a significant decrease in siamang (Symphalangus
syndactylus) group sizes, as well as infant and juvenile survival, after forest fires in Sumatra to a
point where it seems unlikely that groups will survive for more than two generations in burned
areas.
Tree mortality figures differed substantially between edge and interior plots in un-
burned forest. Almost 40% more dead standing trees were encountered in the unburned edge
Chapter 494
plots compared to interior plots. Although no study as yet has specifically investigated edge
effects in Borneo, Laurance et al. (2000, 2001) reported that mortality along forest edges in
Amazonia is higher than in the forest interior, with increased tree mortality levels penetrating
up to 300 metres from the forest edge. The extremely high mortality recorded in burned areas
might also be a cumulative effect of several severe ENSO events over the last decades, each of
which probably has caused elevated mortality, resulting in a more open canopy and higher wa-
ter stress during subsequent droughts. The fact that annual mortality rates in unburned forest
were elevated for two years post-ENSO, could indicate that, with an increased rate of ENSO
events, such prolonged elevated mortality rates will also be occurring on a more frequent basis.
If forests in these drought prone areas experience mortality rates of 6-7 % every 15 years for
extended periods of time, recruitment might not balance mortality and significant changes in
forest structure could occur even without any direct human influence.
ConclusionsLarge changes in vegetation structure and environmental conditions in burned forests,
coupled with a significant decrease in fruit resources important in the diet of sun bears, have
caused a significant reduction of suitable habitat for this bear species in fire-affected areas. The
slow regeneration of these burned areas will probably influence re-colonization by bears, even
if they have been able to maintain large enough population numbers within the burned forest
matrix and adjacent unburned forest areas. Little is known about the ability of sun bears to
exploit new pioneer fruit resources which have sprouted since the fires. The most dominant
pioneer genus (Macaranga) has dehiscent fruits with small arillate seeds primarily attractive
to birds (Davies and Ashton 1999; Slik et al. 2000), and has not (yet) been encountered in the
sun bear diet.
The damage due to fires in primary forest has far surpassed that encountered in
logged-over areas (Woods 1989; Slik et al. 2002). Unburned logged-over areas might have high-
er potential for biodiversity conservation than primary forest that has burned once, although
long-term monitoring of floral regeneration patterns and wildlife diversity and abundance in
burned areas needs to be carried out in order to determine the future value of such forest for
conservation. The massive spatial scale of these fire disturbances and the relatively short times-
pan during which they have affected vast areas (usually 2-3 months of fires) is a new and worry-
ing phenomenon. With the increase in the frequency and severity of ENSO (Timmermann et al.
1999), the future of these burned over forests looks grim as regeneration will only take place
Effects of fires on sun bear fruit resources 95
if no further fires affect these areas, whereas repeated fire damage is common (Cochrane et al.
1999, Siegert et al. 2001). These factors, aggravated by low fire prevention activities and a lack
of law enforcement in the region, call for highly increased conservation efforts in these drought
prone rainforest areas if productive sun bear habitat is to be retained.
AcknowledgementsWe thank the Indonesian Institute of Sciences (LIPI) for granting GMF permission to
carry out research on sun bears in East Kalimantan. GMF would like to express gratitude to
the Forest Research Institute in Samarinda for their assistance. The Tropenbos Foundation and
the Conservation Endowment Fund of the American Zoo and Aquarium Association provided
financial assistance. We especially thank Dave Garshelis for logistical, financial and technical as-
sistance. We thank the Wanariset Herbarium, especially Ambrianshyah and Arifin for identifica-
tion of plant samples. The Tropenbos Foundation is thanked for usage of the permanent sample
plots. Field assistants Trisno, Lukas Nyagang, and Damy da Costa are thanked for various as-
sistance in the field throughout the years, as well as many people from the Sungai Wain village.
LSD received financial and technical assistance from the Norwegian University of Life Sciences.
We thank SBJ. Menken, D. Garshelis, and V. Nijman for useful comments of previous drafts and
G. Usher and M. van Nieuwstadt for the map.
ReferencesAnggraini, K., Kinnaird, M. and O’Brien, T. 2000. The effects of fruit availability and habitat disturbance on an
assemblage of Sumatran hornbills. Bird Conservation International 10: 189-202.
Barlow, J., Haugaasen, T. and Peres, C.A. 2002. Effects of ground fires on understorey bird assemblages in
Amazonian forests. Biological Conservation 105: 157-169.
Borchert, R. 1994. Soil and stem water storage determine phenology and distribution of tropical dry forest
trees. Journal of Ecology 75: 1437-1449.
Cochrane, M.A., Alencar, A., Schulze, M.D., Souza, C.M.J., Nepstad, D.C., Lefebvre, P. and Davidson, E.A. 1999.
Positive feedbacks in the fire dynamic of closed canopy tropical forests. Science 284: 1832-1835.
Cochrane, M.A. and Schulze, M.D. 1999. Fire as a recurrent event in tropical forests of the Eastern Amazon:
effects on forest structure, biomass, and species composition. Biotropica 31: 2-16.
Davies, S.J. and Ashton, P.S. 1999. Phenology and fecundity in 11 sympatric pioneer species of Macaranga
(Euphorbiaceae) in Borneo. American Journal of Botany 86: 1786-1795.
Chapter 496
Doi, T. 1988. Present status of the large mammals in the Kutai National Park, after a large scale fire in East
Kalimantan, Indonesia. In: Tagawa, H. and Wirawan, N. (eds.), A research on the process of earlier
recovery of tropical rain forest, pp. 82-93.
Fredriksson, G.M. 2002. Extinguishing the 1998 forest fires and subsequent coal fires in the Sungai Wain
Protection Forest, East Kalimantan, Indonesia. In: Moore, P., Ganz, D., Tan, L.C., Enters, T. and Durst,
P.B. (eds.), Communities in flames: proceedings of an international conference on community
involvement in fire management. FAO and FireFight SE Asia, pp. 74-81.
Fredriksson G.M. 2005. Human-sun bear conflicts in East Kalimantan, Indonesian Borneo. Ursus 16:130-137.
Fredriksson, G.M. and Nijman, V. 2004. Habitat-use and conservation of two elusive ground birds (Carpo-
coccyx radiatus and Polyplectron schleiermacheri) in Sungai Wain protection forest, East Kalimantan,
Indonesian Borneo. Oryx 38: 297-303.
Fredriksson, G.M., Wich, S.A. and Trisno. in press. Frugivory in sun bears (Helarctos malayanus) is linked to
El Niño-related fluctuations in fruiting phenology, East Kalimantan, Indonesia. Biological Journal of
the Linnean Society.
Fuller D.O., Jessup T.C., and Salim A. 2004. Loss of forest cover in Kalimantan, Indonesia, since the 1997-
1998 El Nino. Conservation Biology 18(1):249-254.
Goldammer, J.G. and Mutch, R.W. 2001. Global forest fire assessment 1990-2000. FAO, pp. 1-495.
Harrison, R.D. 2000. Repercussions of El Niño: drought causes extinction and the breakdown of mutualism
in Borneo. Proceedings of the Royal Society of London Series B-Biological Sciences 267: 911-915.
Hoffmann, A.A., Hinrichs, A. and Siegert, F. 1999. Fire damage in East Kalimantan in 1997/98 related to land
use and vegetation classes: satellite radar inventory results and proposals for further actions.
IFFM-SFMP, pp. 1-44.
Kinnaird, M.F. and O’Brien, T. 1998. Ecological effects of wildfire on lowland rainforest in Sumatra. Conser-
vation Biology 12: 954-956.
Laurance, W.F. 2003. Slow burn: the insidious effects of surface fires on tropical forests. Trends in Ecology
& Evolution 18: 209-212.
Laurance, W.F., Delamonica, P., Laurance, S.G., Vasconcelos, H.L. and Lovejoy, T.E. 2000. Rainforest fragmenta-
tion kills big trees. Nature 404: 836-836.
Laurance, W.F., Williamson, B.G., Delamoˆ Nica, P., Oliveira, A., Lovejoy, T.E., Gascon, C. and Pohl, L. 2001.
Effects of a strong drought on Amazonian forest fragments and edges. Journal of Tropical Ecology
17: 771–785.
Leighton, M. and Leighton, D.R. 1983. Vertebrate responses to fruiting seasonality within a Bornean rain
forest. In: Sutton, S.L., Whitemore, T.C. and Chadwick, A.C. (eds.), Tropical Rain Forest Ecology and
Management. Blackwell Scientific Publications, pp. 181-196.
Effects of fires on sun bear fruit resources 97
Leighton, M. and Wirawan, N. 1986. Catastrophic drought and fire in Borneo Tropical Rain Forest Associ-
ated with the 1982-1983 El Niño southern oscillation event. In: Prance, G.T. (ed.) Tropical rain
forest and world atmosphere. Westview Press, pp. 75-101.
Lennertz, R. and Panzer, K.F. 1984. Preliminary assessment of the drought and forest fire damage in Kalim-
antan Timur. DFS German Forest Inventory Service for Gesellschaft fur Technische Zusammenar-
beit (GTZ), pp. 1-45.
Malingreau, J. P., Stephens, G. and Fellows, L. 1985. Remote sensing of forest fires: Kalimantan and North
Borneo in 1982-83. Ambio 14: 314-321.
Malmer, A. 1996. Hydrological effects and nutrient losses of forest plantation establishment on tropical
rainforest land in Sabah, Malaysia. Journal of Hydrology 174: 129-148.
Matius, P., Toma, T. and Sutisna, M. 2000. Tree species composition of a burned lowland dipterocarp forest in
Bukit Suharto, East Kalimantan. In: Guhardja, E., Fatawi, M., Sutisna, M., Mori, T. and Ohta, S. (eds.),
Rainforest Ecosystems of East Kalimantan. El Niño, Drought, Fire and Human Impacts. Springer-
Verlag, pp. 99-106.
McConkey, K. and Galetti, M. 1999. Seed dispersal by the sun bear (Helarctos malayanus) in Central Borneo.
Journal of Tropical Ecology 15: 237-241.
Nakagawa, M., Tanaka, K., Nakashizuka, T., Ohkubo, T., Kato, T., Maeda, T., Sato, K., Miguchi, H., Nagamasu, H.,
Ogino, K., Teo, S., Hamid, A.H. and Seng, L. H. 2000. Impact of severe drought associated with the
1997-1998 El Niño in a tropical forest in Sarawak. Journal of Tropical Ecology 16: 355-367.
Nykvist, N. 1996. Regrowth of secondary vegetation after the ‘Borneo fire’ of 1982-1983. Journal of Tropi-
cal Ecology 12: 307-312.
Nykvist, N., Grip, H., Sim, B.L., Malmer, A. and Wong, F.K. 1994. Nutrient losses in forest plantations in Sabah,
Malaysia. Ambio 23: 210-215.
O’Brien, T.G., Kinnaird, M.F., Nurcahyo, A., Prasetyaningrum, M. and Iqbal, M. 2003. Fire, demography and the
persistance of siamang (Symphalangus syndactylus: Hylobatidae) in a Sumatran rainforest. Animal
Conservation 6: 115-121.
Peres, C.A., Barlow, J. and Haugaasen, T. 2003. Vertebrate responses to surface wildfires in a central Ama-
zonian forest. Oryx 37: 97-109.
Phillips, O.L., Hall, P., Gentry, A.H., Sawyer, S.A. and Vasquez, R. 1994. Dynamics and species richness of tropi-
cal rain forests. Proceedings National Academy of Sciences USA 91: 2805-2809.
Potts, M.D. 2003. Drought in a Bornean everwet rain forest. Journal of Ecology 91: 467–474
Putz, F.E. and Susilo, A. 1994. Figs and fire. Biotropica 26: 468-469.
Salafsky, N. 1998. Drouht in the rainforest, part II. An update based on the 1994 ENSO event. Climatic
Change 39: 601-603.
Chapter 498
Schaik, C.P. v., Terborgh, J.W. and Wright, S.J. 1993. The phenology of tropical forests: adaptive significance
and consequences for primary consumers. Annual Review of Ecology and Systematics 24: 353-377.
Schindele, W., Thoma, W. and Panzer, K.F. 1989. The forest fire 1982/1983 in East Kalimantan. Part 1: The fire,
the effects, the damage and technical solutions. German Forest Inventory Service Ltd.
Sheil D., and May R.M. 1996. Mortality and recruitment rate evaluations in heterogenous tropical forests.
Journal of Ecology 84:91-100.
Siegert, F., Ruecker, G., Hinrichs, A. and Hoffmann, A.A. 2001. Increased damage from fires in logged forests
during droughts caused by El Niño. Nature 414: 437-440.
Sim, B.L. and Nykvist, N. 1991. Impact of forest harvesting and replanting. Journal of Tropical Science 3:
251-284.
Slik, F., Verburg, R.W. and Keßler, P. 2002. Effects of fire and selective logging on the tree species composi-
tion of lowland dipterocarp forest in East Kalimantan, Indonesia. Biodiversity and Conservation
11: 85-98.
Slik, J.W.E., Priyono and Welzen. P.C. 2000. Key to the Macaranga Thou. and Mallotus Lour. species (Euphor-
biaceae) of East Kalimantan, Indonesia. Gardens’ Bulletin Singapore 52: 11-87.
Slik, J.W.F. 2004. El Niño droughts and their effects on tree species composition and diversity in tropical
rain forests. Oecologia 141: 114-120.
Slik, J. W.F. and Eichhorn, K.A. O. 2003. Fire survival of lowland tropical rain forest trees in relation to stem
diameter and topographic position. Oecologia 137: 446-455.
Suzuki, A. 1992. The population of orangutans and other non-human primates and the forest conditions
after the 1982-1983’s fires and droughts in Kutai National Park, East Kalimantan. In: Ismail, G.,
Mohamed, M. and Omar, S. (eds.), Forest Biology and Conservation in Borneo. Yayasan Sabah, pp.
190-205.
Swaine, M.D., Lieberman, D. and Putz, F.E. 1987. The dynamics of tree populations in tropical forest: a review.
Journal of Tropical Ecology 3: 359-366.
Tacconi, L. 2003. Fires in Indonesia: Causes, costs and policy implications. CIFOR, pp. 1-34.
Timmermann, A., Oberhuber, J., Bacher, A., Esch, M., Latif, M. and Roeckner, E. 1999. Increased El Niño fre-
quency in a climate model forced by future greenhouse warming. Nature 398: 694-696.
Toma, T., Matius, P., Hastaniah, Kiyono, Y., Watanabe, R. and Okimori, Y. 2000. Tree species composition of a
burned lowland dipterocarp forest in Bukit Suharto, East Kalimantan. In: Guhardja, E., Fatawi, M.,
Sutisna, M., Mori, T. and Ohta, S. (eds.), Rainforest Ecosystems of East Kalimantan. El Niño, Drought,
Fire and Human Impacts. Springer-Verlag, pp. 107-119.
van Nieuwstadt, M.G.L. 2002. Trial by fire-Postfire development of a dipterocarp forest. Ph.D. thesis. Uni-
versity of Utrecht.
Effects of fires on sun bear fruit resources 99
van Nieuwstadt, M.G.L. and Sheil, D. 2005. Drought, fire and tree survival in a Borneo rain forest, East
Kalimantan, Indonesia. Journal of Ecology 93: 191–201.
Whitmore, T. C. 1985. Tropical rainforests of the Far East. Clarendon Press.
Wich, S.A., Steenbeek, R., Sterck, E.H.M., Palombit, R.A. and Usman, S. 1999. Tree mortality and recruitment
in an Indonesian rain forest. Tropical Biodiversity 6: 189-195.
Williamson, G.B., Laurance, W.F., Oliviera, A.A., Delamonica, P., Gascon, C., Lovejoy, T.E. and Pohl, L. 2000.
Amazonian tree mortality during the 1997 El Niño drought. Conservation Biology 14: 1538-1542.
Wong, S.T., Servheen, C. and Ambu, L. 2002. Food habits of malayan sun bears in lowland tropical forest of
Borneo. Ursus 13: 127-136.
Woods, P. 1989. Effects of Logging, Drought, and Fire on Structure and Composition of Tropical Forests in
Sabah, Malaysia. Biotropica 21: 290-298.
Chapter 4100
Appendix 1:
List of sun bear fruit genera/species of trees (≥10 cm DBH) encountered in unburned-edge
(UBF) and burned (BF) vegetation plots (total 7.2 ha), 33 months after the 1997-98 fire. A ‘√’
indicates that the genus/species was encountered in the plots, a ‘0’ indicates it was absent.
Number of plots indicates in how many of the 0.4 ha plots (9 plots in burned and 9 plots in
unburned edge forest) the genus/species was encountered.
Genus Species Family UBF-edge No of plots BF No of plots
Aglaia spec. Meliaceae √ 7 0 0
Alangium ridleyi Alangiaceae √ 3 √ 1
Artocarpus anisophyllus Moraceae √ 9 √ 3
Artocarpus dadah Moraceae √ 1 0 0
Artocarpus integer Moraceae √ 3 √ 1
Artocarpus lanceifolius Moraceae √ 2 0 0
Artocarpus nitidus Moraceae √ 3 0 0
Artocarpus spp. Moraceae √ 4 √ 2
Baccaurea bracteata Euphorbiaceae √ 3 0 0
Baccaurea macrocarpa Euphorbiaceae √ 6 0 0
Baccaurea spec. Euphorbiaceae √ 8 √ 2
Baccaurea stipulata Euphorbiaceae √ 1 0 0
Borassodendron borneensis Palmae √ 7 √ 8
Canarium spp. Burseraceae √ 4 0 0
Crypteronia spec. Crypteroniaceae √ 7 √ 1
Cryptocarya spec. Lauraceae √ 3 0 0
Dacryodes costata Burseraceae √ 3 √ 1
Dacryodes rostrata Burseraceae √ 7 √ 1
Dacryodes rugosa Burseraceae √ 2 √ 1
Dacryodes spec. Burseraceae √ 5 √ 4
Dialium indum Ceasalpiniaceae √ 4 0 0
Dialium platysepalum Ceasalpiniaceae √ 1 0 0
Dialium spec. Ceasalpiniaceae √ 4 0 0
Diospyros borneensis Ebenaceae √ 6 √ 4
Diospyros cf buxifolia Ebenaceae 0 0 √ 1
Diospyros spec. Ebenaceae √ 7 √ 4
Durio dulcis Bombacaceae √ 1 √ 1
Durio graveolens Bombacaceae √ 1 0 0
Durio kutejensis Bombacaceae √ 1 0 0
Durio oxleyanus Bombacaceae √ 3 √ 1
Dysoxylum spec. Meliaceae √ 2 √ 1
Eugenia spec. Myrtaceae √ 2 0 0
Eugenia tawahense Myrtaceae √ 5 √ 3
Effects of fires on sun bear fruit resources 101
Appendix 1: Continued
Genus Species Family UBF-edge No of plots BF No of plots
Ficus spp Moraceae √ 8 √ 1
Garcinia parvifolia Guttiferae √ 4 0 0
Garcinia spp Guttiferae √ 4 √ 2
Glochidion spec. Euphorbiaceae √ 2 0 0
Ilex cymosa Aquifolicaeae √ 1 √ 1
Irvingia malayana Simaroubaceae √ 1 √ 4
Lansium domesticum Meliaceae √ 1 √ 1
Lansium spec. Meliaceae √ 1 0 0
Lithocarpus gracilis Fagaceae √ 1 0 0
Lithocarpus spp. Fagaceae √ 8 √ 2
Litsea firma Lauraceae √ 4 0 0
Litsea spp. Lauraceae √ 7 0 0
Madhuca kingiana Sapotaceae √ 6 √ 4
Magnolia lasia Magnoliaceae √ 2 0 0
Mangifera macrocarpa Anacardiaceae √ 1 0 0
Mangifera spp. Anacardiaceae √ 1 √ 1
Monocarpia kalimantanensis Annonaceae √ 2 0 0
Nephelium spec. Sapindaeae √ 5 √ 1
Ochanostachys amentaceae Olacaeae √ 9 √ 2
Oncosperma horridum Palmae √ 6 0 0
Palaquium spp. Sapotaceae √ 9 √ 3
Polyalthia lateriflora Annonaceae 0 0 √ 1
Polyalthia laterifolia Annonaceae √ 2 0 0
Polyalthia rumphii Annonaceae √ 3 √ 1
Polyalthia spec. Annonaceae √ 5 √ 2
Polydocarpus spec. Palmae √ 3 √ 2
Prunus volgens Rosaceae √ 6 0 0
Pternandra spec. Melastomataceae √ 8 √ 2
Quercus spp. Fagaceae √ 2 0 0
Sandoricum spp. Meliaceae √ 3 0 0
Santiria cf apiculata Burseraceae √ 1 0 0
Santiria spp. Burseraceae √ 6 √ 2
Santiria tomentosa Burseraceae √ 5 0 0
Syzygium spp. Myrtaceae √ 9 √ 7
Tetramerista glabra Tetrameristaceae 0 0 √ 2
Xerospermum spec. Sapindaeae √ 1 0 0
Unburned edge plots: 66 speciesBurned plots: 37 species
Chapter 5
Human-sun bear conflicts in East Kalimantan,
Indonesian Borneo
Ursus (2005), 16: 130-137
Chapter 5104
AbstractInterviews with farmers in 5 communities situated along the edge of the Sungai Wain
Protection Forest, East Kalimantan, Indonesian Borneo, indicated that crop damage caused by
sun bears (Helarctos malayanus) was higher than normal following the 1997–98 El Niño South-
ern Oscillation Event. Widespread drought and forest fires reduced habitat and fruit availability
for sun bears on the islands of Borneo and Sumatra. The main source of antagonism toward
bears resulted from the damage they caused to stands of old coconut trees (Cocos nucifera),
thereby frequently killing the trees. This prompted farmers to seek removal of the bears. Bear
damage to annual crops generally spurred a less hostile reaction. Experiments with metal
sheeting affixed to the trunks of coconut trees to deter climbing by bears were successful, at
least in the short term (≥3 years). Inexpensive and easily applicable crop-protection devices
such as this could help protect sun bears in the future, as increased human-bear conflicts are
anticipated due to rapid human population growth, unabated forest destruction and fragmenta-
tion, and increased susceptibility of remaining forests to future fires.
Human-sun bear conflicts 105
Most species of bears are opportunistic omnivores that may become considered pests
when attracted to human-related foods. North American bears (grizzly bears Ursus arctos and
American black bears U. americanus) are known to use apiaries, crops, orchard fruits, garbage,
and livestock (Ambrose and Sanders 1978, Knight and Judd 1983, Garshelis et al. 1999). They
also may afflict considerable damage to timber stands (Stewart et al. 1999). In Japan, Asiatic
black bears (U. thibetanus) raid crops, orchards, and fish farms (Huygens and Hayashi 1999).
Sloth bears (Melursus ursinus) have been reported to do considerable damage to sugarcane and
groundnut plantations (Iswariah 1984). Andean bears (Tremarctos ornatus) in South America
have been reported to predate on livestock (Goldstein 2002). Until a few decades ago bounties
were commonly used as a means of reducing or eliminating bears to protect crops or livestock
(Azuma and Torii 1980, Swenson et al. 1994, Mattson and Merrill 2002).
In Southeast Asia, sun bears probably commenced crop-raiding when attractive foods
were first planted close to forest habitat. Early reports from colonialists in Indonesia described
ways of deterring or killing marauding bears in fruit plantations (O-Viri 1925), even when adja-
cent forest habitat was still extensive. In recent years, the combined effects of timber harvest-
ing and forest fires have significantly reduced forest coverage in Kalimantan (Curran et al. 2004,
Fuller et al. 2004). Increased human encroachment on Indonesian forests have led to increased
human-wildlife conflicts (Meijaard 1999, Rijksen and Meijaard 1999), although little information
is available on conflicts specifically with sun bears.
On the islands of Borneo and Sumatra, sun bear habitat has recently been severely re-
duced or damaged by forest fires linked to the 1997–98 El Niño Southern Oscillation (ENSO)
event. Approximately 5.2 million ha of land, of which 2.6 million ha was forest, were burned
over a period of 4 months in the province of East Kalimantan alone (Siegert et al. 2001). Sun
bear fruit resources (mainly tree-borne fruits) declined significantly in burned forests, with tree
mortality (≥10 cm dbh) reaching >90% in certain areas (van Nieuwstadt 2002, G. Fredriksson,
unpublished data). Insects, an alternative bear food (Wong et al. 2002), were also reduced
significantly (G. Fredriksson, unpublished data). Suitable sun bear habitat in these fire-affected
areas has become progressively fragmented, increasing the chances of edge-related conflict
with humans (Woodroffe and Ginsberg 1998).
After the large-scale forest fires in 1997–98 a widespread fruiting failure prevailed for
more than one year. Although some fruits (e.g. Ficus spp.) are generally available year-round,
abundant fruiting in forests in this region occurs at intervals of about 2-10 years (Medway 1972,
Ashton et al. 1988, Curran and Leigthon 2000). The combination of rapid loss of habitat as well
as inter-annual shortages of food may increasingly compel sun bears to seek nearby human food
Chapter 5106
sources, especially crops planted along the forest edge.
The objectives of this study were: (1) to determine the types and extent of crop dam-
age caused by sun bears; (2) to assess the reactions of farmers to different types of bear-related
crop damage; and (3) to find ways of alleviating the most disturbing types of sun bear damage.
Study Area
The study was carried out in 5 farmer communities along the southern and eastern
periphery of the Sungai Wain Protection Forest (SWPF), near Balikpapan, East Kalimantan,
Indonesian Borneo (1º 16’ S and 116º 54’ E) (Fig. 1). The reserve covers a lowland dipterocarp
forest watercatchment area of approximately 10,000 ha.
Forest fires entered the SWPF in early March 1998, initially from a neighboring state-
owned logging concession, but subsequently also from surrounding agricultural fields, affecting
some 60% of the reserve. After the fires in 1998, connections to forest areas north and west
of the reserve were significantly reduced. To the south and east the reserve is bordered by ag-
ricultural plots, unproductive grassland and shrublands. At the time this study commenced, the
SWPF consisted of approximately 40 km2 primary forest, 40 km2 regenerating burned forest,
and 20 km2 affected by human encroachment (Fredriksson 2002).
Methods
Interviews
Semi-structured household interviews were conducted in 5 farmer communities
around the SWPF (Fig. 1) to compile information on sun bear damage to crops and orchards.
Interviews were initiated just after the 1998 fires, and continued in 1999 and 2000. Each year,
my assistants and I interviewed 99 farmers representing 40% of the 246 families in these com-
munities. The number of farmers interviewed in each community was relative to the number
of inhabitants/farmers in that community. We attempted to carry out the same number of
interviews annually in each community, though the identity of interviewees differed slightly
over the years. We focused on farmers who frequently visited or worked in their gardens, as
opposed to landowners who would only visit their orchards on an irregular basis. In one com-
munity all families relied on farming for their income, whereas in the remaining 4 communities
approximately 80% of families did. We posed questions regarding ethnic origin of farmers,
farming history, farming practices, types and amount of crops grown, and location of the farm
Human-sun bear conflicts 107
Figure 1. Location of the 5 farmer communities surveyed adjacent to the Sungai Wain Protection Forest,
East Kalimantan, Indonesia.
in relation to the forest edge. Crop damage would be recorded through interviews as detailed
as possible, with information on species and quantity of crops fed upon, number of trees dam-
aged and type of damage, frequency of bear visits, bear crop raiding behavior, damage to crops
by other wildlife species, and methods used to reduce wildlife-related crop damage. Whenever
possible we directly observed crop damage in the gardens.
Damage mitigation trials
We attempted to reduce sun bear consumption of farmer’s fruits through conditioned
taste aversion with thiabendazole (TBZ). TBZ-induced conditioned taste aversion has been
used to reduce consumption of human-related foods and livestock by American black bears
Chapter 5108
(Ternent and Garshelis 1999) and several species of canids (e.g. Gustavson et al. 1983). TBZ
powder (Sigma Chemical, Saint Louis, Mo) was mixed into samples of ripe fruit (14-23 mg
TBZ/g food) that were targeted by sun bears in gardens or orchards. TBZ was mixed thor-
oughly in the soft, ripe pulp of breadfruit (Artocaprus heterophyllus), pineapple (Ananas sp.), and
papaya (Carica papaya). Diluted TBZ, as opposed to TBZ powder, was injected into snakefruit
(Salacca spp.) because it has a hard mesocarp. Treated fruits were placed where farmers indi-
cated that sun bears had entered their gardens recently.
We attempted to inhibit sun bears from climbing and damaging coconut palms by
nailing smooth metal sheeting around their trunks, between the heights of 0.5-1 m from the
base extending 2-3 m up the trunk. Two types of metal sheeting were used: new zinc sheets
as well as recycled metal sheets produced from old food containers. The price of the lat-
ter was 50% cheaper/m2 than zinc plates. In one garden all remaining undamaged coconut
trees (n=15) were protected with metal sheeting. In five gardens, which had been repeatedly
targeted by sun bears, 2-4 coconut trees were protected with metal sheeting interspersed
among unprotected palm trees. As one of the aims was to test a cheap method how to
discourage sun bears from damaging trees, farmers were involved in placement of the metal
sheeting. During subsequent interviews protected trees were monitored for success rate
of the metal sheeting in deterring bears from climbing to them, as well as condition of the
sheeting. Unprotected coconut trees growing in the vicinity of protected trees (n=75) were
monitored simultaneously.
Results
Farmer profiles and practices
Most farmers near the SWPF were immigrants originating from other islands (e.g.
Sulawesi, Java), with only 18% originating from Borneo (Dayak or Pasir tribes). The average size
of gardens, owned or leased, was 2.6 = 0.4 (SD) ha. Farmers had lived in the area on average
for 20 = 7 (SD) years. Mixed orchards (43%), snakefruit plantations (24%), bananas (8%, Musa
spp.), vegetables (7 %, e.g. cassava [Manihot esculenta], beans [Fabaceae], spinach [Basellaceae]),
rice (Poaceae, 7%) and coconut trees (Palmae, 6%), constituted the main crop coverage by area.
Snakefruit is a continuously fruiting low-growing palm species, and several tree species in the
mixed orchards also produced fruits throughout the year, even though their wild congeners in
the forest were more seasonal.
Human-sun bear conflicts 109
Crop damage
The main wildlife species reported to raid gardens throughout the study period were
bearded pigs (Sus barbatus, 98% of gardens), followed by sun bears (43%), barking deer (Mun-
tiacus spp., 42%), civets (20%, [Viverridae]), squirrels (12%, [Sciuridae]), and a variety of other
species including macaques and pythons (raiding chicken coops). Nearly one-quarter (22%)
of farmers reported that sun bears raided their gardens before the 1997–98 forest fires and
fruiting failure. This increased to over half (56%) in 1998 and 1999, the first two post-fire years,
and declined to 39% in the year 2000.
Sun bears most often damaged coconut trees (36%), followed by snakefruit (32%), and
a variety of fruits in mixed orchards (breadfruit [Moraceae] 12%; durian [Bombacaceae] 8%;
rambutan [Sapindaceae] 8%; mango [Anacardiaceae] 4%). Damage to coconut trees was par-
ticularly disliked by farmers because sun bears fed primarily on the growthshoot (palmite), fre-
quently killing over 20 years old fruit-bearing trees (Fig. 2). Only on rare occasions did sun bears
feed on the coconut fruits. Farmers developed less antagonism toward bears that fed on ripe
Figure 2. Coconut palm tree damaged (and probably killed) by a sun bear in a garden adjacent to the
Sungai Wain Protection Forest, East Kalimantan, Indonesia 1998 (photo courtesy D. & J. Garshelis).
Chapter 5110
fruits from orchards or snakefruit, because trees or snakefruit palms were rarely damaged and
usually only a small proportion of the overall crop was consumed by bears. The only account
of attempted livestock depredation involved a sun bear trying to break into a chicken coop.
Farmers generally considered financial losses related to sun bear damage to be low and
few farmers expressed the feeling that financial compensation would be justified. Moreover, no
active wildlife authority existed in the district to whom farmers could forward any complaints
or damage claims. In a few cases, where entire coconut stands had been killed by bears or when
a large proportion of a small stand of snakefruit had been consumed by a bear, farmers asked
our survey team for compensation or removal of the bear.
Mitigation practices and trials
Most farmers (57%) used dogs to guard their gardens, followed by small wooden fences
(32%), and regular nocturnal check-ups of their gardens (6%). None of these were efficient in
keeping sun bears out as bears still entered these gardens. Poisoned fruit baits were put out
by a small number of farmers. Although these poisoned baits were primarily targeted against
bearded pigs, a variety of wildlife could be killed by this. Some farmers surrounded their garden
with wire neck snares, mainly for pigs and barking deer, but a few also put out locally made
foot snares designed to capture bears. Two farmers indicated that they had looked into hiring a
hunter who could spear a bear climbing down from a coconut tree. Only 2 farmers admitted to
killing bears before this study period, but this type of information was difficult to obtain during
interviews, as such killing is illegal and farmers may have feared prosecution.
Sun bears did not consume any of the 15 TBZ-treated fruit samples that we placed
in gardens in an attempt to create conditioned taste aversions toward garden fruits. None of
the ~30 coconut trees that we protected with metal sheeting were subsequently climbed by
bears. Several unprotected trees (n=27) growing in proximity to these protected trees were
still climbed and damaged by bears. An additional small number of coconut trees were covered
with metal sheeting by farmers themselves and none of these were subsequently climbed by
bears, at least during the study period.
Sun bear crop-raiding behavior
All farmers that reported sun bear visits to their gardens stated that sun bears entered
their gardens during the night. Frequently sun bears built nests in small orchard trees, usually
close to the main trunk, 2–5 m from the ground. These nests were created by bears breaking
surrounding branches toward them and constructing a ‘V’ shaped structure (in contrast to the
Human-sun bear conflicts 111
flat platforms usually out on limbs constructed by orangutans [Pongo pygmaeus], which also live
in the surrounding forest). These nests appeared to function as resting platforms rather than
feeding platforms, which were occasionally encountered in fruiting trees within the forest. Such
nests in orchards possibly provide some security, being off the ground, and by offering a wider
olfactory range to detect approaching humans or dogs. Bears probably left these nests before
daybreak as no farmer reported seeing bears in the morning.
Discussion
Main causes for human-carnivore conflicts concern the perceived risk of predation on
humans and livestock (Sillero-Zubiri and Laurenson 2001, Treves and Karanth 2003). In places
where bears are feared and hated, it is generally for either or both of these reasons (polar bear
Ursus maritimus: Gjertz and Persen 1987; brown bear and American black bear: Herrero 1985;
sloth bear: Rajpurohit and Krausman 2000; Asiatic black bear: Chauhan 2003; Andean bear:
Goldstein 2002). No reliable reports of sun bears killing humans or livestock were found in the
literature or discovered during this study from local informants. Hence, there has been little
negative publicity regarding this species. During this study, however, some local farmers found
them to be troublesome pests, especially in the 2 years after the fires and subsequent fruiting
failure in the neighboring forest.
Although bearded pigs were the main agricultural pest in the gardens around the SWPF,
farmers were less antagonistic toward this species than toward sun bears. This was because
bearded pigs primarily targeted annual crops (corn, cassava, pineapples), whereas bears fre-
quently killed productive coconut trees by feeding on the palmite. If bears had just eaten the
coconuts, the effect would have been much less detrimental, and even could have been benefi-
cial to fruit production (Siex and Strushaker 1999).
Few recent reports have been written about sun bear crop raiding. Fetherstonhaugh
(1940: p. 21) reported that “the Malayan sun bear is an inoffensive jungle dweller and unlike
some species, conflicts very little with human activities when it comes in contact with cultiva-
tion, the glaring exception being coconuts to which the bears are a positive menace … but
there is nothing to fear from their presence near other forms of cultivation”. O-Viri (1925) on
the other hand gives a lengthy description of how sun bears were devastating pests in coconut
plantations where they fed on the palmite, as well as causing damage to papaya plantations, sug-
arcane, pineapple and fruit orchards. Several Dutch colonial sources mention damage in planta-
Chapter 5112
tions due to sun bear depredations, especially to coconut stands (van Balen 1917, Feuilletau-de
Bruyn 1933, Nederlandsch-Indische Vereeniging 1939). In other parts of Borneo and Sumatra,
sun bears have been reported to enter sugarcane fields (L. Nyagang, local resident, personal
communication), and more recently to feed on fruits in oil palm plantations (Nomura 2003;
T. Maddox, Zoological Society of London, personal communication).
Sun bears were frequently killed by colonial plantation owners at the turn of the
century by various means, the most effective being the shooting of bears when they would
climb down a fruit tree. Poisons, primarily phosphor, were already used to kill nuisance pigs in
those days, and although meant to target sun bears as well, these were rarely effective (O-Viri
1925). TBZ trials attempted during this study were unsuccessful, possibly either because of the
availability of a wide array of untreated fruits in gardens or due to human or chemical scent
residues on treated fruits which repelled the bears.
Reducing availability of crops near forested areas is likely to be the most effective
means of mitigating human-wildlife conflicts. Naughton-Treves et al. (1998) recommended that,
in general, crops attractive to wildlife should be planted >500 m from the forest edge, and
that non-palatable plant barriers should be planted between the forest and human agricultural
fields. This recommendation would not be feasible around Sungai Wain, where 250+ farmers
would need to be translocated and their fields replaced with unpalatable vegetation. High hu-
man population densities, and the complicating factors linked to landownership and compensa-
tion issues obstruct these mitigation options in the Indonesian context.
Electric fencing has been found to be an effective deterrent against damage to agri-
cultural crops and apiaries in North America and Japan (Jonker et al. 1998, Garshelis et al.
1999, Huygens and Hayashi 1999). We did not experiment with electric fences, as this type of
mitigation was not deemed applicable for small-scale private farmers in Indonesia. Farmers in
Borneo or Sumatra would not have funds or easy access to procure the necessary materials.
This method though, should be tested in the future as it could be effective for mitigating sun
bear-human conflicts near certain protected areas or commercial plantations.
Compensation for financial losses due to bear depredation has been used on private
lands in North America and Europe (Cozza et al. 1996, Wagner et al. 1997). Although popular
with the public, compensation does not address the source of the problem (Witmer and Whit-
taker 2000). In some cases translocation or removal of the nuisance bears has been applied
(e.g. Azuma and Torii 1980, Garshelis 1989). Neither of these mitigation procedures would
currently apply to the Indonesian context as forest conservation and wildlife management have
not reached that level of attention or public support.
Human-sun bear conflicts 113
Figure 3. Balikpapan district logo, East Kalimantan, Indonesia, featuring the sun bear as its new mascot.
Increased human-wildlife conflicts in Indonesia are likely linked to the rapid reduction
of forest habitats. We noticed a sharp increase in conflicts with bears shortly after much of
the forest burned, coincident with a fruiting failure. Despite the increased problems that this
caused, no government officials were available to assist local farmers with their wildlife con-
flicts. This led local farmers to feel that they had no choice but to attempt killing the nuisance
animals themselves, even though this was prohibited by law. Often farmers requested help
from our research team, and we worked with them to develop non-lethal means of protecting
their crops.
Metal sheeting placed around the trunks of large coconut trees functioned well to
deter sun bears from climbing up to the growth shoot. These metal sheets can be obtained
locally, at a low cost, and are easily installed. The sheeting will likely need to be replaced every
3–4 years, as it deteriorates quickly due to high humidity, but this appears to be manageable to
Chapter 5114
these farmers. This method is likely to become more widespread as its effectiveness becomes
known, and this process could be hastened through conservation education programs.
During this study conservation education programs were initiated targeting schools,
local communities and local government agencies and focusing on forest functions and the role
of wildlife slowly brought about a local change in attitude towards forest conservation and sun
bears. In 2001 the sun bear was chosen to become the mascot of the district where this study
was carried out (Fig. 3). This seemed to instill a sense of pride and ownership of the species.
In addition, a multi-stakeholder management body was established for management of the
reserve, fully funded by the local government, where the issue of human-wildlife conflicts has
finally received a place on the management agenda. It still remains to be seen, though, whether
this slow attitude change towards bears and forest conservation will translate into behavioral
changes and tolerance of low-level agricultural losses related to crop raiding, associated with
living and farming at a forest edge.
AcknowledgementsI would like to express my gratitude to the Indonesian Institute of Sciences (LIPI)
for permitting me to do field research on sun bears, as well as to the Forest Research Insti-
tute (BPK-Samarinda) for their research invitation and support. I would like to thank my field
assistants Lukas Nyagang, Trisno, Rachman, Agusdin, Babam and Iman from Sungai Wain, and
students Whiwien, Eko, Joned and Ali from the Mulawarman University, Samarinda, for their
assistance with the surveys. Financial support for field work was received from the Tropenbos
Foundation. D. Garshelis provided ongoing logistical and technical support for the study, pro-
vided useful comments on an earlier draft of the manuscript, as well as the TBZ for the taste-
aversion trials. S.B.J. Menken, V. Nijman and M. Lammertink, O. Huygens and E. Meijaard are also
thanked for useful comments on earlier drafts of this paper.
Literature citedAmbrose, J.T., and O.T. Sanders. 1978. Magnitude of black bear depredation on apiaries in North Carolina.
Proceedings of the Eastern Black Bear Workshop 4:167–177.
Ashton, P.S., T.J. Givnish, and S. Appanah. 1988. Staggered Flowering in the Dipterocarpaceae - New Insights
into Floral Induction and the Evolution of Mast Fruiting in the Aseasonal Tropics. American Natu-
ralist 132:44–66.
Human-sun bear conflicts 115
Azuma, S., and H. Torii. 1980. Impact of human activities on survival of the Japanese black bear. Int. Conf.
Bear Res. and Manage. 4:171–179.
Chauhan, N.P.S. 2003. Human casualities and livestock depredation by black and brown bears in the Indian
Himalaya, 1989–98. Ursus 14:84–87.
Cozza, K., R. Fico, M.L. Battistini, and E. Rogers. 1996. The damage-conservation interface illustrated by
predation on domestic livestock in central Italy. Biological Conservation 78:329–336.
Curran, L.M., and M. Leighton. 2000. Vertebrate responses to spatiotemporal variation in seed production
of mast-fruiting dipterocarpaceae. Ecological Monographs 70:101–128.
Curran, L.M., S.N. Trigg, A.K. McDonald, D. Astianti, Y.M. Hardiono, P. Siregar, I. Caniago, and E. Kasischke.
2004. Lowland forest loss in protected areas of Indonesian Borneo. Science 303:1000–1003.
Fetherstonhaugh, A.H. 1940. Some notes on malayan bears. The Malayan Nature Journal 1:15–22.
Feuilletau-de Bruyn, W. K. H. 1933. Bijdrage tot de kennis van de afdeeling Hoeloe Soengei (Z. en O.- afdee-
ling Borneo). Koloniale Studiën 17: 53-93 and 183-211(in Dutch).
Fredriksson, G.M. 2002. Extinguishing the 1998 forest fires and subsequent coal fires in the Sungai Wain
Protection Forest, East Kalimantan, Indonesia. Pages 74–81 in P. Moore, D. Ganz, L.C. Tan, T. Enters,
and P.B. Durst, eds. Communities in flames: proceedings of an international conference on com-
munity involvement in fire management. FAO and FireFight SE Asia, Bangkok, Thailand.
Fuller, D.O., T.C. Jessup, and A. Salim. 2004. Loss of forest cover in Kalimantan, Indonesia, since the 1997–
1998 El Nino. Conservation Biology 18:249–254.
Garshelis, D.L. 1989. Nuisance bear activity and management in Minnesota. Bear-people conflicts: Pro-
ceedings of a symposium on management strategies Northwest territories Dept. of Renew.
Res.:169–180.
Garshelis, D.L., R.S. Sikes, D.E. Andersen, and E.C. Birney. 1999. Landowners’ perceptions of crop damage
and management practices related to black bears in east-central Minnesota. Ursus 11:219–224.
Gjertz, I., and E. Persen. 1987. Confrontations between humans and polar bears in Svalbard (Norway). Polar
Research 5:253–256.
Goldstein, I. 2002. Andean bear-cattle interactions and tree nest use in Bolivia and Venezuela. Ursus
13:369–372.
Gustavson, C.R., J.C. Gustavson, and G.A. Holzer. 1983. Thiabendazole-based taste aversion in dingoes
(Canis familiaris dingo) and New Guinea wild dogs (Canis familiaris hallstromi). Applied Animal Ethol-
ogy 10:385–388.
Herrero, S. 1985. Bear attacks: Their causes and avoidance. Nick Lyons Books, New York, USA.
Huygens, O.C., and H. Hayashi. 1999. Using electric fences to reduce Asiatic black bear depredation in
Nagano prefecture, central Japan. Wildlife Society Bulletin 27:959–964.
Chapter 5116
Iswariah, V. 1984. Status survey report and recommendations for conservation of the sloth bear in Ramna-
garam Taluk, Karnataka. World Wildlife Fund-India, Bangalore.
Jonker, S.A., J.A. Parkhurst, R. Field, and T.K. Fuller. 1998. Black bear depredation on agricultural commodities
in Massachusetts. Wildlife Society Bulletin 26:318–324.
Knight, R.R., and S.L. Judd. 1983. Grizzly bears that kill livestock. Int. Conf. Bear Res. and Manage. 5:186–190.
Mattson, D.J., and T. Merrill. 2002. Extirpation of Grizzly bears in the contiguous United States, 1850–2000.
Conservation Biology 16:1123–1136.
Medway, L. 1972. Phenology of a tropical rain forest in Malaya. Biological Journal of the Linnean Society
4:117–146.
Meijaard, E. 1999. Human-imposed threats to sun bears in Borneo. Ursus 11:185–192.
Naughton-Treves, L., A. Treves, C. Chapman, and R. Wrangham. 1998. Temporal patterns of crop-raiding
by primates: linking food availability in croplands and adjacent forest. Journal of Applied Ecology
35:596–606.
Nederlandsch-Indische Vereeniging tot Natuurbescherming. 1939. Natuur in Zuid- en Oost- Borneo. Fauna,
flora en natuurbescherming in de Zuider- en Ooster-Afdeeling van Borneo. 3 Jaren Indisch natuur
leven. Opstellen over landschappen, dieren en planten. Elfde verslag (1936-1938), Batavia, Indone-
sia. Pages 334-411 (in Dutch).
Nomura F. 2003. Seasonal trends of habitat usage in two ursine species, a destructive beast Ursus arctos
yesoensis and an agricutural pest Helarctos malayanus. PhD thesis. University of Hokkaido: 1-46.
O-Viri. 1925. Tusschen de beren. de Tropische Natuur XIV:81–88.
Rajpurohit, K.S., and P.R. Krausman. 2000. Human-sloth bear conflicts in Madhya Pradesh, India. Wildlife
Society Bulletin 28:393–399.
Rijksen, H.D., and E. Meijaard. 1999. Our vanishing relative. The status of orangutans at the close of the
centrury. Tropenbos, Kluwer Academic Publishers, Dordrecht, Boston, London.
Siegert, F., G. Ruecker, A. Hinrichs, and A.A. Hoffmann. 2001. Increased damage from fires in logged forests
during droughts caused by El Niño. Nature 414:437–440.
Siex, K.S., and T.T. Struhsaker. 1999. Colobus monkeys and coconuts: a study of perceived human-wildlife
conflicts. Journal of Applied Ecology 36:1009–1020.
Sillero-Zubiri, C., and K. Laurenson. 2001. Interactions between carnivores and local communities: conflict
or co-existence? Pages 282–312 in J. L. Gittleman, S. M. Funk, D. W. MacDonald, and R. K. Wayne,
eds. Carnivore conservation. University of Cambridge Press, Cambridge, UK.
Stewart, W.B., G.W. Witmer, and G.M. Koehler. 1999. Black bear damage to forest stands in Western Wash-
ington. Western Journal of Applied Forestry 14:128–131.
Human-sun bear conflicts 117
Swenson, J.E., F. Sandegren, A. Bjarvall, A. Soderberg, P. Wabakken, and R. Franzen. 1994. Size, trend, distribu-
tion and conservation of the brown bear Ursus arctos population in Sweden. Biological Conserva-
tion 70:9–17.
Ternent, M.A., and D.L. Garshelis. 1999. Taste-aversion conditioning to reduce nuisance activity by black
bears in a Minnesota military reservation. Wildlife Society Bulletin 27:720–728.
Treves, A., and K.U. Karanth. 2003. Human-carnivore conflict and perspectives on carnivore management
worldwide. Conservation Biology 17:1491–1499.
van Balen, J. H. 1914. De dierenwereld van Insulinde in woord en beeld. I. De Zoogdieren. W.J. Thieme & Cie,
Zutphen, the Netherlands (in Dutch).
van Nieuwstadt, M.G.L. 2002. Trial by fire-Postfire development of a dipterocarp forest. PhD thesis. Uni-
versity of Utrecht, Utrecht.
Wagner, K.K., R.H. Schmidt, and M.R. Conover. 1997. Compensation programs for wildlife damage in North
America. Wildlife Society Bulletin 25:312–319.
Witmer, G.W., and D.G. Whittaker. 2001. Dealing with nuisance and depredating black bears. Pages 73–82
in D. Immell, editor. 7th Western Black Bear Workshop.
Wong, S.T., C. Servheen, and L. Ambu. 2002. Food habits of Malayan sun bears in lowland tropical forests
of Borneo. Ursus 13:127-136.
Woodroffe, R., and J.R. Ginsberg. 1998. Edge effects and the extinction of populations inside protected
areas. Science 280:2126–2128.
Chapter 6
Predation on sun bears by reticulated python
in East Kalimantan, Indonesian Borneo
The Raffles Bulletin of Zoology (2005), 53(1): 165-168
Chapter 6120
Abstract
The Malayan sun bear is the largest member of the order Carnivora on the island of
Borneo. Few records exist of predation on this species beside humans, whereas accurate re-
cordings of natural predation events can teach us about the ecology of the prey species. Here
I report on an attempted and a successful predation of Malayan sun bears by a reticulated
python, both in a lowland dipterocarp forest in East Kalimantan. The successful predation was
accomplished by a ~7 m reticulated python. The python preyed and swallowed an adult female
sun bear, possibly weakened at the time due to a fruiting failure and nursing of a cub. Both
predation events occurred at night, with the python probably surprising the bears during their
sleep.
Sun bear predation by reticulated python 121
Introduction
Throughout the world bears are at the top of the food chain with few natural preda-
tors, apart from man and congeners, which are capable of killing and eating an adult individual
(e.g. Garshelis, 2004). The Malayan sun bear is the smallest bear species, with the Bornean
subspecies (Helarctos malayanus euryspilus) weighing between 20-40 kg for females and 30-60
kg for males in the wild (Fredriksson unpubl. data; F. Nomura pers. comm.; Wong et al., 2004).
The distribution range of the sun bear covers most of tropical mainland Southeast Asia’s for-
ests as well as the islands of Sumatra and Borneo (Servheen, 1999). Sun bears are primarily
diurnal (Wong et al., 2004; Fredriksson, in prep.), though reportedly more nocturnal in forests
with much human traffic (Griffiths and van Schaik, 1993). Usually sun bears are encountered
solitary and the most common social grouping is a female with cub(s), though infrequently 3
bears have been sighted together (Fredriksson, unpubl. data.). Sun bears are mainly terrestrial
though expert tree climbers, with a diet that primarily comprises of insects and fruits (Wong
et al., 2002; Fredriksson, in prep.).
The main predator of sun bears throughout its range is by far man (Meijaard, 1999;
Fredriksson, in review). Tigers and other large felines are also potential predators (e.g. Kawani-
shi and Sunquist, 2004). Here I report on a predation of a wild female sun bear, radio-collared
at the time for an ecological study, by a reticulated python, and another unsuccessful predation
attempt, in East Kalimantan, Indonesian Borneo.
The reticulated python (Python reticulatus, Pythonidae), is thought to be the world’s
largest or second largest snake (Shine et al., 1999), or at least the world’s longest snake (Mur-
phy and Henderson, 1997). They inhabit tropical rainforests of Southeast Asia from Myanmar
(Burma) to most of the islands of the Philippines and Indonesia (Auliya and Abel, 2000a; Auliya,
2003a). The longest recorded length of a python comes from the island of Sulawesi, Indonesia,
where a reticulated python measuring 10.05 m was caught (Raven, 1946; Murphy and Hender-
son, 1997). Females can attain much larger body sizes than males when mature (Shine et al.,
1998), but sexual dimorphism varies between areas (Shine et al., 1999). Large (>6 m) pythons
are rarely encountered and during Shine et al’s (1999) study of reptile slaughterhouses few
were recorded. Very large specimens may be relatively scarce as well in other natural python
populations (Bhupathy, 1990). Huge pythons can attain a body mass of up to 150 kg (Pope, 1975).
The reticulated python has a broad head and a huge gape enabling it to swallow large
prey. Long curved teeth ensure that once the snake has caught its prey, it rarely loses grip.
The snake is a powerful constrictor and when adult it can overpower and kill animals as large
Chapter 6122
as pigs, deer, and dogs (Auliya, 2003a, 2003b). Prey are killed by asphyxiation, looping its body
around the victim, squeezing until it stops breathing. The reticulated python is a nocturnal
hunter that heavily relies on ambush tactics to catch prey. The thick and heavy body is usually
firmly anchored when the python strikes. Due to their good camouflage prey may come close
without detecting them. Pythons have sensory organs (infrared-sensitive labial pits) in order to
locate prey accurately, even in total darkness. Pythons allegedly often wait in ambush at a spot
where wildlife frequently passes by (Slip and Shine, 1988), although it might be possible that
prey are traced during inactivity (Auliya, 2003a). Despite their massive size, a reticulated python
is surprisingly hard to spot due to its excellent camouflage and partly because it is less active
during the day and remains extremely silent. Prey size increases with larger body size (Shine et
al., 1998, 1999; Auliya, 2003a), with small pythons mainly feeding on rats but shifting to larger
mammals at 3-4 m body length, depending on prey availability (Shine et al., 1998; Auliya, 2003a).
Prey recorded for pythons in Indonesia range from small mammals like rats (Muridae) and
shrews (Soricidae), to larger animals like civets (Viverridae), pangolins (Manidae), porcupines
(Hystricidae), binturong (Arctictis binturong), primates, wild pigs (Suidae), as well as domesticated
prey like chickens, dogs, cats in agricultural/urban areas (Shine et al., 1998; Auliya and Abel,
2000b). It is one of the few snakes in the world known to eat humans occasionally. Kopstein
(1927) reports on a 14-year old boy eaten by a 5.17 m reticulated python, and Schmidt (1998
in Auliya, 2003a) reports of a 32 year-old man eaten by a 7 m python.
Study Site
The reported case of sun bear predation took place in the Sungai Wain Protection For-
est, near Balikpapan, East Kalimantan, Indonesian Borneo (1º 05’ S and 116º 49’ E). The reserve
covers a watercatchment area of circa 10,000 ha. The topography of the reserve consists of
gentle to sometimes steep hills, and is intersected by many small rivers. The area varies in alti-
tude from 30 to 150 metres a.s.l. The most common tree families above 10 cm dbh (diameter
at breast height) are Euphorbiaceae, Dipterocarpaceae, Sapotaceae and Myrtaceae. Poaching is
rare and primarily restricted to the borders of the reserve (Fredriksson and de Kam, 1999).
The reserve contains relatively large populations of potential prey species for pythons. Bearded
pigs (Sus barbatus), barking deer (Muntiacus spp.), and mouse deer (Tragulus spp.) are common
(pers. obs.), as well a primarily ground-dwelling pig-tailed macaques (Macaca nemestrina). Civets,
pangolins (Manis javanica) and other ground dwelling mammals like porcupines are also present.
Sun bear predation by reticulated python 123
Predation attempt
On June 21, 1999, a probable python attack occurred on a 3-year-old, 31-kg female sun
bear. This bear had been confiscated as a cub and subsequently taken to the forest where I had
raised her for several months before releasing her in the study area with a radiocollar, 1.5 years
prior to the predation event. The bear’s activity was being monitored continuously that day,
and it had been sleeping for several hours when, at 01:30, 4 loud barks were heard, suggesting
that it was involved in an agonistic encounter. Afterwards, the bear was heard growling for 30
min up in a tree.
The next morning the bear was observed in a tree nest, with blood drops covering
nearby undergrowth. At 18:00 it climbed down and could be examined more closely (having
been raised in captivity, the bear could be touched). The left side of the bear’s face was swollen
with a row of small superficial scabs found on the skin. On both back feet 2 claws each were
torn out, causing the blood that was encountered on the undergrowth below the nest. Other-
wise no obvious physical wounds could be found, nor were any signs of other animals (e.g. fe-
line, pig) encountered at the place of attack. From the nature of the wounds and by eliminating
all potential predators a python appeared the most likely attacker. The subsequent successful
predation event occurred only 100 m from the site of this predation attempt.
Predation event
A wild adult female sun bear weighing 23 kg, with a small cub (1–2 months old), was
trapped on July 6, 1999. This bear was in a poor physical condition (probably >10 kg under-
weight), due to a prolonged fruit shortage at the time compounded with nutritional stress from
nursing a small cub. The bear’s canines were worn down to stumps and her age was estimated
to be >10 years. She was fitted with an activity and mortality-sensing radiocollar (ATS, Isanti,
Minnesota, U.S.A.).
The bear was monitored on a daily basis, with locations obtained by triangulation, in
the morning, midday and afternoon. A 24-hour activity monitoring was conducted once a week
by listening and recording the pulse rate of the bear’s radio transmitter every 10 minutes.
On the afternoon of July 30, the bear was located and found to be active. The next
morning she was located 550m from the previous location, but her radio signal indicated that
she had not moved for ≥4 hours, which was indicative of either mortality or a dropped radio
Chapter 6124
Figure 1. Reticulated python (~7 m) lying in a small stream after having swallowed an adult female sun
bear ; the bulge on the left hand side in the python contains the sun bear.
collar. I tracked the collar to a swamp, and ultimately found that the signal was being emitted
from the stomach of a large python, which was curled under a thicket. After being poked with a
stick, it fled into a nearby stream, producing, as it twisted, the sound of breaking bones (Fig 1).
The bulge of the bear was ~2 m from the python’s head. No traces of a struggle were found
near the site where the python was encountered nor any signs of the sun bear’s cub.
The python remained resting in the stream until August 3, when it moved into a large
hollow log (Shorea laevis), 120 m from the site where it was initially encountered. The log had
an outer diameter of 153 cm and was hollow for approximately 8 m. The python was back
about 5 m from the entrance. A few metres from the log entrance a large skin shedding of a
python was found.
The radiocollar remained functioning and hence the python’s movements could be
monitored on a regular basis. The signal of the collar remained fully inactive for 26 days, while
the python remained inside the log. On August 30 the python left the tree hollow and entered
the swamp again. As the radiocollar contains batteries in a metal casing it was decided to moni-
tor closely whether the python would regurgitate remains of the bear, including the radiocollar.
Sun bear predation by reticulated python 125
Figure 2. Reticulated python being pulled out of an underground stream 1.5 month after it swallowed a
radio-collared adult female Malay sun bear (photo courtesy M. van Nieuwstadt).
On September 8, I decided to catch the python and hold it in captivity to facilitate collection
of regurgitated remains. Ten villagers were recruited and the python was caught manually and
put in a steel-barred cage. That same night the python escaped by dislodging the bars of the
cage through squeezing. The next day the python was caught again (Fig. 2), now encountered in
a small underground stream. This time it was placed inside a barrel trap, designed for catching
the sun bears.
After holding the python for a month, it only passed remains of bones. Thus, on Oc-
tober 29 I retrieved the collar surgically. The snake was sedated with zolazepam–tiletamine
(Telazol® 3.75 mg/kg for an estimated weight of 80 kg). Full sedation took several hours due
to initial low dosage of drugs (recommended dosage 20mg/kg, Kreeger et al., 2002). Once fully
anaesthetized the python was palpated to find the radiocollar and an incision was made in the
skin and large intestine and the radiocollar removed.
The python measured 6.95 m and weighed 59 kg, after having not eaten for nearly 3
months. Sex was not determined. The snake was held in captivity and monitored for another 3
weeks, twice being fed a chicken, and then released on November 20.
Chapter 6126
Discussion
This is the first detailed record of predation of bears by a python, and could only have
been recorded due to the fact that the bear was radiocollared. By its very nature, predation is a
once in a life time experience, hence difficult to observe. Although anecdotal, accurate record-
ings of predation events can teach us about the ecology of the prey species. The only other
published case of a radio-collared mammal being eaten by a python was reported by Martin
(1995), involving an amethystine python (Morelia amethystina) that preyed on a Bennett’s tree-
kangaroo (Dendrogalus bennettianus) in North Queensland, Australia.
Few published records exist of bear predation by other animals. Kurt and Jayasurya
(1968) report of a sloth bear (Melursus ursinus) eaten by a leopard (Panthera pardus). Sloth
bears, due to their less arboreal and more aggressive nature, might be less inclined than sun
bears to climb a tree when threatened by a leopard; however, leopards are also expert tree
climbers (Laurie and Seidensticker, 1977). A number of records exist of bears being predated
upon by conspecifics (Ursus arctos, S. Brunberg. pers.comm.), or congenerics (Garshelis, 2004).
In terms of animal predation on sun bears, few published records exist. Kawanishi and Sunquist
(2004) report on 3 tiger (Panthera tigris) scats containing sun bear remains from peninsular
Malaysia. Other predators on mainland Southeast Asia and Sumatra could potentially be the
common leopard, and the clouded leopard (Neofelis nebulosa), which occur sympatrically with
sun bears. The moon bear (Ursus thibethanus), also occurring sympatrically throughout parts of
the sun bears range, being substantially larger than the sun bear, could potentially pose a risk
to sun bears.
A sun bear, with its long claws and powerful jaws with large canines, would be a formi-
dable prey for a python. In the cases reported here, it appeared that the sun bears were prob-
ably caught by surprise while they were sleeping. It is possible that a python had come across
the sleeping bear, which usually spend the night resting on a log or on the forest floor. Although
it has been described that pythons attack from ambush, it is possible that the python followed
a scent trail (M. Auliya, pers. comm.), came across the bear, bit it in the face (indicated by the
scars from the predation attempt) while trying to constrict it. Moreover, in the successful pre-
dation event, the python was >3 times the mass of the bear. Animals much larger than bears,
such as >60-kg wild pigs have been swallowed by pythons (Shine et al., 1998; Auliya, 2003b).
Although little is known about what body size a python would need to attain in or-
der to successfully overpower a sun bear, it seems likely that it will need to be a fairly large
specimen. The python that predated on the sun bear during this study was large (~7 m), and
Sun bear predation by reticulated python 127
densities of such large pythons are probably low, even more so as large pythons are becoming
extremely rare due to unsustainable harvesting (Shine et al., 1999). Of >1000 python stomach
contents examined in Sumatra, none contained remains of a sun bear (Shine et al. 1998), al-
though predation of a sun bear by a python in the interior of Borneo was reported by a local
Dayak (Domalian 1991 in Auliya and Abel, 2000b).
It remains unclear whether the incidents reported here were truly rare events. During
the course of my study, only 6 sun bears were radiocollared, 3 wild caught and 3 partially reared
in captivity. One of the captive-reared bears was killed by a person, and one of the wild-caught
bears apparently starved after a prolonged fruiting failure, subsequent to the 1997-1998 ENSO
event. The fruiting failure possibly contributed to the death of the bear that was captured by
the python, due to her weakened physical condition. Perhaps these predation events are not
uncommon during such periods of food scarcity, which on Borneo occur at irregular intervals.
AcknowledgementsI thank the Indonesian Institute of Sciences (LIPI) for granting me permission to carry
out research on sun bears. Gratitude is expressed as well to my field assistants: Adi, Nono,
Moudy, Bahronni, Lukas and Damy and the villagers from Sungai Wain who assisted with catch-
ing the python. Financial assistance from the Tropenbos Foundation is gratefully acknowledged.
The Conservation Endowment Fund of the American Zoo and Aquarium Association pro-
vided financial assistance for purchasing the radiocollars. M. Auliya, V. Nijman, S. Menken and
D. Garshelis made comments on an earlier draft. An anonymous reviewer is also thanked for
valuable comments. M. van Nieuwstadt is thanked for the picture of the python capture.
Literature citedAuliya, M., and F. Abel, 2000a. Zur Taxonomie, geographischen Verbreitung und Nahrungsökologie des Netz-
pythons (Python reticulatus) - Teil 1 (geographische Verbreitung). Herpetofauna 22(127): 5-18.
Auliya, M., and F. Abel, 2000b. Zur Taxonomie, geographischen Verbreitung und Nahrungsökologie des Netz-
pythons (Python reticulatus) - Teil 2 (Nahrungsökologie). Herpetofauna 22(128): 19-28.
Auliya, M., 2003a. Taxonomy, Life History and Conservation of Giant Reptiles in West Kalimantan (Indonesian
Borneo). Ph.D thesis, Universität Bonn, 513 pp.
Auliya, M., 2003b. A reticulated python (Python reticulatus) preys on an adult Sulawesi pig (Sus celebensis).
Asian Wild Pig News 3(1): 11-12.
Chapter 6128
Bhupathy, S., 1990. Blotch structure in individual identification of the Indian python (Python molurus molu-
rus Linn.) and its possible usage in population estimation. Journal Bombay Natural History Society
87:399-404.
Fredriksson G. M., and M. de Kam, 1999. Strategic plan for the conservation of the Sungai Wain Protection For-
est, East Kalimantan, Indonesia. The International Ministry of Forestry and Estate Crops-Tropenbos
Kalimantan Project. Pp. 1-46.
Fredriksson, G. M., In press. Human-sun bear conflicts in East Kalimantan, Indonesian Borneo. Ursus.
Garshelis, D.L., 2004. Variation in ursid life histories - is there an outlier ? In: Lindburg D. and K. Baragona.
(eds). Giant pandas. Biology and conservation. University California Press, Berkeley. Pp. 53-73.
Griffiths, M., and C. P. van Schaik, 1993. Camera trapping: a new tool for the study of elusive rain forest
mammals. Tropical Biodiversity 1:131-135.
Kawanishi, K., and M. E. Sunquist, 2004. Conservation status of tigers in a primary rainforest of Peninsular
Malaysia. Biological Conservation 120:329–344.
Kopstein, F., 1927. Over het verslinden van Menschen door Python reticulatus. Tropische Natuur 16:65-67.
Kreeger, T. J., J. M. Arnemo, and J. P. Raath, 2002. Handbook of wildlife chemical immobilization. Wildlife Pharma-
ceuticals, Inc., Fort Collins, Colorado. Pp.1-402.
Kurt, F., and A. Jayasuriya, 1968. Notes on a dead bear. Loris: 182-183.
Laurie, A., and J. Seidensticker, 1977. Behavioural ecology of the sloth bear (Melursus ursinus). J. Zool., Lond
182:187-204.
Martin, R. W., 1995. Field observation of predation on bennetts treekangaroo (Dendrolagus bennettianus) by
an amethystine python (Morelia amethistina). Herpetological Review 26:74-76.
Meijaard, E., 1999. Human-imposed threats to sun bears in Borneo. Ursus 11:185-192.
Murphy, J.C. and R.W. Henderson, 1997. Tales of Giant snakes – A historical natural history of Anacondas and
Pythons. Krieger Publ. Comp., Malabar, Florida. Pp. 1-221.
Pope, C. H., 1975. The giant snakes. Albert A. Knopf, New York. Pp.1-221.
Raven, H. C., 1946. Adventures in python country. Natural History 55: 38-41.
Servheen, C., 1999. Sun bear conservation action plan. In: Servheen, C., S. Herrero and B. Peyton (eds.),
Bears. Status survey and conservation action plan. International Union for Conservation of Nature
and Natural Resources, Gland, Switzerland and Cambridge, United Kingdom. Pp. 219-224.
Shine, R., P. Ambariyanto, S. Harlow, and Mumpuni, 1999. Reticulated pythons in Sumatra: biology, harvesting
and sustainability. Biological Conservation 87:349-357.
Shine, R., P. S. Harlow, J. S. Keogh, and Boeadi, 1998. The influence of sex and body size on food habits of a
giant tropical snake, Python reticulatus. Functional Ecology 12:248-258.
Sun bear predation by reticulated python 129
Slip D.J., and R. Shine, 1988. Feeding habits of the diamond python, Morelia s. spilota: ambush predation by a
boid snake. Journal of Herpetology 22: 323-330.
Wong, S. T., C. Servheen, and L. Ambu, 2002. Food habits of Malayan sun bears in lowland tropical forests
of Borneo. Ursus 13:127-136.
Wong, S. T., C. Servheen, and L. Ambu, 2004. Home range, movement and activity patterns, and bedding
sites of Malayan sun bears, Helarctos malayanus in the rainforest of Borneo. Biological Conservation.
119: 169-181.
Chapter 7
Exploring the use of sign surveys for
monitoring relative abundance of sun bears:
a case study in burned and unburned forests
in East Kalimantan, Indonesian Borneo
With D.L. Garshelis, W.J. Sastramidjaja and S.B.J. Menken
Chapter 7132
Abstract
Sun bears, Helarctos malayanus, the largest carnivore on the island of Borneo, are threat-
ened by habitat loss. Besides direct cutting and forest conversion, forest fires and drought,
related to recurring El Niño Southern Oscillation (ENSO) events, have degraded vast areas of
sun bear habitat on Borneo. In this study we explore the use of sign (e.g., claw-marked trees,
raided termite nests) surveys as a way to monitor changes in relative abundance of sun bears
following an ENSO-related forest fire in 1998. We compared sign densities to an adjacent low-
land dipterocarp forest that was not burned. We searched for sign in 92 1-ha strip transects
(45 in unburned forest and 47 in burned forest) in 2000, 2001, 2002, 2005 and 2010. Densities
of sun bear sign were close to zero in burned forest areas for several years after the fire, but
by 2010 had increased to 28.0 ± 12.9 (SD) sign/ha, indicating re-colonization by sun bears. Sign
densities in adjacent unburned forest remained stable over the years, averaging 41.6 ± 11.6
(SD) sign/ha. Densities of sun bear sign were still 35% lower in burned forest, which showed a
paucity of certain types of sun bear foods, especially fruiting trees and above-ground termite
colonies. Nevertheless, it is evident that these once-burned forest areas can still play an impor-
tant role in the conservation of sun bears, as long as source populations for re-colonization
are present in adjacent undisturbed forest. We discuss the potential and challenges to further
develop sign transects as a tool for monitoring population trends of this species.
Exploring the use of sign surveys for monitoring relative abundance of sun bears 133
Introduction
Monitoring population abundance and trends is essential for the management and con-
servation of many wildlife species, including large carnivores (Kendall et al. 1992, Mowat and
Strobeck 2000). These parameters are used to assess population status, evaluate the effects of
management measures or decisions (Wilson and Delahay 2001), decide quotas for harvested
populations (Kindberg et al. 2011), or to obtain parameters for conservation principles, includ-
ing IUCN criteria for Red-listing evaluations (Kühl et al. 2008, Vié et al. 2009).
For animals that are cryptic, occur at low densities but over extensive areas, and have
large home ranges, it might be more practical to monitor indices of population size or trends
in key areas, rather than obtain actual estimates of abundance. Bears represent one such taxon
in which population estimation is expensive, impractical in some remote areas, and frequently
lacks the precision necessary to monitor population trends (Garshelis and Hristienko 2006).
Bears habitually leave signs of characteristic appearance that indicate their presence. These
range from distinct claw marks on trees, various feeding sign, scats, footprints, and even feeding
or sleeping platforms in trees.
Relative abundance can be judged from the frequency of signs per standardized unit of
sampling effort (Wilson and Delahay 2001), which is assumed to be related to densities of the
species depositing that sign (Kühl et al. 2008). However, various other factors may affect sign
density as well, including: sign production rates and seasonal movement of animals (e.g. Kutilek
et al. 1983, Stanley and Bart 1991), persistence of sign (Bider 1968), and variation in detection
of sign (Kühl et al. 2008).
Sun bears, Helarctos malayanus, have not been surveyed systematically in Southeast Asian
forests, but are thought to be in widespread decline (Fredriksson et al. 2008). It appears that sun
bears have recently been extirpated in Bangladesh (Islam et al. 2010) and possibly China (Wang
Dajun unpubl. report) and are declining in several protected areas throughout their range (Mei-
jaard 1999, Steinmetz et al. 2006, Harrison 2011). The sun bear is a forest-dependent species and
is threatened by high rates of habitat loss (Miettinen et al. 2011), fragmentation and degradation
of remaining habitat, as well as poaching for body parts throughout much of its range (Foley
et al. 2011). Indonesia, covering some 45% of the sun bear distribution range (IUCN/SSC Bear
Specialist Group 2006), has the highest rates of deforestation in the region (Hansen et al. 2009).
Sun bears have been protected by Indonesian law since 1973, but most of their habitat is not.
Fires associated with El Niño/Southern Oscillation (ENSO) are recurring events in
Indonesia. Within the past two decades, major fires have occurred during five ENSO events
Chapter 7134
(Meijaard and Dennis 1997, Barber and Schweithelm 2000). In Indonesia, the scale of ENSO-
related forest fires has been extensive with more than 3.6 million ha of forest and scrub
burned in 1982–83. The 1997–98 fires damaged at least 2.6 million ha of concession and con-
servation forests in the Indonesian province of East Kalimantan alone (Hoffman et al. 1999,
Siegert et al. 2001, Tacconi 2003, Fuller et al. 2004). These fires caused loss of primary forest,
large-scale habitat change and resource availability as well as loss of biodiversity (Singer et al.
1989, Kinnaird and O’Brien 1998, Barber and Schweithelm 2000). However, changes to wildlife
communities, including patterns of recovery or extinction of specific species, resulting from
fires remain poorly understood (Whelan 1995, Kinnaird and O’Brien 1998, O’Brien et al. 2003,
Barlow and Peres 2006). The objective of this study was to explore the potential of using sign
surveys as a monitoring tool to assess trends in the relative abundance of sun bears in a burned
lowland dipterocarp forest versus an adjacent unburned area in East Kalimantan, over a period
of 11 years.
Methods
Study area
The study was carried out in lowland dipterocarp forest of the Sungai Wain Protection
Forest (SWPF), a reserve near Balikpapan, East Kalimantan, Indonesian Borneo (1°16’ S and
116° 54’ E) at the eastern edge of the sun bear distribution range (Fig. 1). The reserve covers a
watercatchment area of ca 100 km2. The topography of the reserve consists of gentle to some-
times steep hills, and is intersected by many small rivers. The area varies in altitude from 30 to
150 m above sea level. Trees with stems greater than 10 cm DBH (diameter at breast height)
are dominated by the families Euphorbiaceae, Dipterocarpaceae, Sapotaceae, and Myrtaceae.
The relative dominance of Dipterocarpaceae increased substantially in the larger size classes.
Due to an altitudinal gradient, with rivers running in a north-south direction, the southern
part of the reserve has more moist, swampy areas. Dipterocarpaceae (> 10 cm DBH), which
are dominant in the northern part of the reserve decrease in abundance towards the moister
south where Sapotaceae and Euphorbiaceae become more dominant. The 25 most common
tree species form 40% of the total stem density (van Nieuwstadt 2002).
Rainfall patterns in the region are not consistent on an annual basis, however a distinc-
tion could be made between a ‘wet’ season (Nov-April) and a ‘dry’ season (May-Oct) (t=4.96,
df=6, p=0.002). Rainfall type falls within the category of ‘slightly seasonal’ according to Mohr’s
Exploring the use of sign surveys for monitoring relative abundance of sun bears 135
Figure 1. Sun bear distribution range in Southeast Asia and location of the Sungai Wain Protection Forest,
East Kalimantan, Indonesian Borneo.
index (Whitmore 1984), with average annual rainfall 2968 ± 510 mm y-1. Mean annual maxi-
mum and minimum temperature was 29.7 ± 0.7ºC and 23.2 ± 0.4ºC, respectively, measured in
unburned forest on a daily basis during January 1998 – October 2002. Temperature in burned
forest was not measured as regularly, but maximum temperatures (in the shade) of up to
34.6ºC were measured.
The prolonged drought of the 1982-83 El Niño/Southern Oscillation (ENSO) had
probably caused elevated levels of mortality among large trees, resulting in an irregular canopy
cover. Consequently the primary forest became increasingly vulnerable to desiccation dur-
ing droughts and subsequently more susceptible to fires. Most of the reserve was unaffected
Chapter 7136
by fires in 1997, when this study on sun bears commenced, except for a small area near the
eastern border that had been burned in 1982-83. Fires entered the SWPF in March 1998,
initially from a neighbouring state-owned logging concession, but subsequently also from sur-
rounding agricultural fields. Fires moved slowly through the leaf litter and remained mainly in
the undergrowth. In burned areas, all leaf litter and surface soil humus was reduced to ash, and
mortality of seedlings and saplings was close to 100% (GM Fredriksson pers. obs.). Fire-breaks
were created over a period of 2 months but nevertheless approximately 50% of the reserve
was affected by the fires (Fredriksson 2002), leaving an unburned central core of some 4,000
ha of primary forest (Fig. 1) with unburned gallery forest along rivers in the burned-over forest
areas covering between 7-18% of burned areas (van Nieuwstadt 2002, Fredriksson and Nijman
2004).
Burned forest areas suffered elevated tree mortality up to several years after the fires
with close to 80% mortality of sun bear fruit trees (>10 cm DBH) (Fredriksson et al. 2006b).
Densities of various invertebrates (especially termites), which are food resources for sun
bears, declined significantly after the fires in the burned areas (Fredriksson et al. unpublished
data). In addition, burned forest areas became virtually inaccessible for almost 4 years after the
fire event due to a thick groundcover of ferns (Dicranopteris linearis and Nephrolepis biserrata),
which obstructed the understory, impeding movement for large ground-dwelling mammals.
Sign transects
Bear signs were recorded along 10 x 1000m (1 ha) strip-transects. Transects were laid
out along straight lines (primarily running across watersheds in a east-west direction, Fig. 2)
and were surveyed by a team of three people, with one person moving slowly along the midline
whilst recording data and distances with a Walktax Distance Measurer (Forestry Suppliers Inc.,
USA), and two people zigzagging on either side of the midline in search of sign throughout the
5-m strip of forest on either side of the midline. Transects were spread widely (at least 250 m
apart) throughout the unburned and burned areas in the reserve (Fig. 2). Sign surveys were
carried out over a period of >10 years starting in 2000, with follow-up surveys in 2001, 2002,
2005 and 2010.
Sign surveys between 2000-2002 were carried out by GMF with 2 field assistants.
Surveys in 2005 were carried out by two trained field assistants and a biology volunteer over
a period of 3 months. In 2010, transects were again carried out by two trained field assistants
and WJS over a period of approximately 5 months. A training session of 2 days was provided
by GMF both in 2005 and 2010 in the forest, with several trial transects carried out with each
Exploring the use of sign surveys for monitoring relative abundance of sun bears 137
Figure 2. Layout of transects in 2010 in the SWPF.
survey team in order to synchronize identification and categorization of sun bear sign and ag-
ing, and to reduce inter-observer differences.
All sun bear sign (Table 1) encountered within the strip-transect was investigated in
detail and recorded after consensus was achieved among the researchers. We recorded type of
sign, estimated age of sign, and forest category in which sign was encountered (i.e. ridge, swamp,
slope). All tree stems >5 cm DBH were investigated for claw marks, and the forest floor was
searched for dug up or broken termite nests, soil excavations, or logs ripped by sun bears. On av-
erage 4.5 hours were used to record sign along one 1-km strip-transect. Within strip-transects,
Chapter 7138
Table 1. Main categories of sun bear sign encountered in SWPF.
Sign category: Deposited during what activity:
Broken stumps/rotten logs/toppled trees foraging for termites, ants/brood, beetles/beetle grubs, cockroaches
Broken aboveground termite nests foraging for termite larvae/eggs/reproductives
Dug up & destroyed underground termite nests foraging for termite larvae/eggs/reproductives
Soil digs foraging for termite larvae/eggs/reproductives
Claw mark, and associated sign climbing trees, primarily for obtaining fruit
- Broken into stingless bee nests foraging for honey
- Bite marks on trees marking behaviour (?)
- Tree nests resting/feeding platforms
Scat pile defecation
Foot print walking
live aboveground termite nests and figs (Ficus spp., both trees and hemi-epiphytes) were also
recorded during surveys in 2005 and 2010, as termites and figs make up a large proportion of
the sun bear diet (Wong et al. 2002, Fredriksson et al. 2006a). A small sample was inspected of
each termite mound for signs of activity as well as species identification for those nest types
that could contain different genera. Termite nests >5 m up tree trunks or in the canopy were
not included. Figs were identified as such by means of checking latex with a small incision in the
stem, as well as confirming the genus through its specific leaf venation.
Sign deposition by sun bears and recording of bear sign
along strip-transects
Identification of sun bear sign was greatly assisted by behavioural observations of three
orphaned sun bears that were rehabilitated between 1998-2002 and closely observed after
their release in the forest. Continuous focal observations (Altman 1974) were made at least
twice a week of each bear, during which we recorded each activity (i.e. breaking into termite
mound, climbing tree, breaking into rotten log), duration of each activity, whether or not items
were consumed (samples collected for species identification), and if so, how many (for larger
items like fruits or beetle grubs) and/or for how long (licking up termites or ant brood).
We also occasionally made observations of other wild bears (including three that were
radio-collared) while they foraged and produced sign. Sun bears in the study area, and during
the study period, were found to predominantly feed on insect matter (88% of feeding time)
Exploring the use of sign surveys for monitoring relative abundance of sun bears 139
supplemented by a large variety of fruit species (Fredriksson et al. 2006a). We classified sign
into categories related to the type of activity of the bear and type of food sought (Table 1).
Decaying logs
Sun bears searched for a variety of wood-boring and -living insects (beetle grubs, cock-
roaches, ants, termites) in dead wood. These ranged from small decaying broken branches (5 cm
diameter) to massive rotten tree stumps or toppled trees (>200 cm) in varying degrees of de-
cay. Along transects all decaying tree trunks with signs of sun bear damage were investigated in
detail, but only recorded as sun bear sign when secondary proof was present at the site (e.g. hair,
partial claw mark or dental impressions) or when all three researchers were in agreement that
the sign could only have been produced by a sun bear. We were cautious in classifying ripped
logs as sun bear sign because bearded pigs (Sus barbatus) also trampled logs in search of insects.
Termite nests
Sun bears feed extensively on a variety of termite species. We categorized five main
shapes of aboveground termite nests (Fig. 3a-e) plus one subterranean termite nest (Proham-
itermes mirabilis; Fig. 3f) that sun bears were observed to consume. Sun bears located under-
ground nests by smell, and dug up, and ripped apart the chambers to varying degrees. Nests of
this species were occasionally clumped in distribution, with a number of nests connected un-
derground within an area of several square meters. We observed one sun bear that excavated
more than 40 nests of this species within 6 hours.
Along transects, we recorded broken termite nests as sun bear sign when there was
significant damage to nests, or when subterranean nests of P. mirabilis were excavated. Bear
damage included large sections missing from termite nests glued on tree trunks between but-
tresses (Hospitalitermes spp.), toppled and damaged termite nest pillars or drupes (Fig. 3b-c,
Dicuspiditermes spp. or Termes spp.), or large sections missing from nests of Microcerotermes
dubius usually constructed some 1-2 m off the ground onto tree trunks (Fig. 3d). We recorded
the type of termite (assessed by opening a section of the remaining nest and identifying the
species-specific soldiers), and estimated the time since it was broken into by a sun bear.
Sympatrically occurring mammal species at the study site that are reported to feed
on termites include pangolins (Manis javanica), orangutans (Pongo pygmaeus) and bearded pigs.
Although we never directly observed any of these species feeding on termite nests, care was
taken to look for characteristic signs of sun bear foraging whenever a broken or excavated
termite nest was encountered.
Chapter 7140
Figure 3a-e. Main termite mound shapes in SWPF. Constructed by species of the genera Dicuspiditermes
and Termes (3a-c); Microcerotermes (2d); Bulbitermes (2e).
Figure 3f. Detail of an opened underground termite mound of the species Prohamitermes mirabilis and the
typical posture of a sun bear breaking into a nest of this species.
Soil digs
Sun bears also dug up soil in search of certain underground termites species that do
not produce solid nest structures (primarily Macrotermes spp. and Odontotermes spp.). Species
within the latter genus produce small (<10 cm), extremely brittle nests, but with extensive
underground tunnels systems (Darlington 1997). Sun bears excavated nests in search of their
winged reproductive forms (alates). Holes dug in the soil in search of these termites could be
relatively deep (up to 30 cm) and frequently clustered, with several locations dug up in a small
area. Along transects, soil digs were identified as produced by sun bears when associated sun
bear sign was encountered (e.g. claw marks on large roots, or thick roots ripped apart during
digging) or when excavation was of characteristic size and with backward piled excavated soil
(similar to a dog digging in soil). Other mammals that produced soil excavations in this area
Exploring the use of sign surveys for monitoring relative abundance of sun bears 141
include bearded pigs who till the soil shallowly with their noses, or potentially pangolins and
porcupines (Hystrix brachyura) although their digging behavior was never directly observed.
Claw marks and other tree-related sign
Sun bears climbed trees to feed on fruits or stingless bees nests, and occasionally to
rest. Sun bear claw marks were easily distinguished from claw marks of other large tree-climb-
ing species (e.g., monitor lizard Varanus salvator, clouded leopard Neofelis diardi), which leave
finer, wavy marks. Along transects, all trees with sun bear claw marks were measured (diameter,
height), identified to species whenever possible, and highest point of claw marks recorded. Each
trunk with claw marks was investigated in detail to see whether multiple-age claw marks could
be found, indicating separate climbing events.
Ripped open tree trunks, or less frequent extensive diggings at the base of trees under
the root system, to predate nests of stingless bees in search of honey and larvae, were one
of the most characteristic sun bear signs. This sign was frequently associated with claw marks
when recent. Large holes in trees, with sun bear bite marks, could remain identifiable as sun
bear sign for many years, even when claw marks disappeared.
Sun bears also left bite marks on trees, frequently with a section of the trunk debarked.
These were usually associated with claw marks (the bear holding onto the tree with its front
paws whilst biting) or associated dental indentations left in the bark.
Figure 3g. A sun bear ripping into a tree trunk to access a stingless bees nest and the aftermath of such a
foraging session.
Chapter 7142
Tree nests or feeding platforms were another characteristic sign of sun bears. These
were constructed close to tree trunks, distinctive ‘V’ shaped, and usually associated with claw
marks, quite easily differentiated from orangutan nests.
Other sign
Sun bear scats were easily identified as such due to their size, neutral smell and con-
tents. Footprints, though easily identified (as no other bear species occurs on Borneo), were
rarely encountered due to the thick layer of leaf litter.
Ageing of sign and decay rates
We assigned an age category to each sign encountered along transects: extremely fresh
(<1 week); fresh (<1 month); relatively fresh (2-6 months); recent (6-12 months); intermediate
(1-2 years); old (≥ 2 years). These categories were developed by examining decay rates of sign
deposited during observations of habituated rehabilitated sun bears that were released in the
forest. For subsequent analysis of sign we grouped all sign <1 year as ‘fresh’, sign aged at 1-2
years as ‘intermediate’, and sign >2 years as ‘old’.
After watching a sun bear break into a termite nest, we monitored approximately 25
nests of each main nest type (Fig. 3a-e) and 45 excavated P. mirabilis nests (Fig. 3f) regularly
for patterns of change. Decay rates of termite nests were affected by the level of destruction
caused by sun bears, with nests that were heavily destroyed becoming difficult to identify as
sun bear sign within 12 months. Likewise, decay of soil digs was affected primarily by the size
and depth of excavation and weather conditions. Most soil digs were not identifiable as bear
excavations after 12 months.
Claw marks and chewed tree trunks (from predated stingless bees nest) persisted
from several months up to several years. Ageing of claw marks was monitored after observa-
tion of climbing events by human-habituated sun bears; trees were marked and checked on
regular intervals. Ageing was similar to that described for decay trials carried out by Steinmetz
and Garshelis (2010). Trees with multiple-age claw marks were treated as separate sign deposi-
tion events.
Sun bear scats were primarily aged as very fresh or fresh, though most scats containing
insect remains disintegrated in <36 hours. Sun bear scats containing seeds could be recognized
as such for 6-43 days. Seedling clumps growing from fruit scats could be recognized up to 3
years after deposition. Footprints were recognizable for hours to 1 week, depending primarily
on weather conditions or physical disturbance.
Exploring the use of sign surveys for monitoring relative abundance of sun bears 143
Table 2. Decay rates of main categories of sun bear sign encountered in SWPF.
Sign category Subtype of sign Decay range
Logs rotten logs 1 mo-1 yr
firm dead wood 3 mo-2 yrs
Termite nests dug up-but not broken 3 yrs
partially destroyed 2 yrs
entirely destroyed 1 yr
Soil digs small 1 mo-1 yr
large 3 mo-1 yr
Claw marks - 6 mo-8+ yrs
Stingless bee nests under tree bases 6 mo- 2 yrs
cavity chewed in stem 3 yrs-13+ yrs
Bite marks small 6 mo-8+ yrs
large 2 yrs
Scats termites 12-36 hours
figs 6-17 days
various hard seeds 6-43 days
Seedling clump from scat - 3 yrs
Foot prints 1 hour-1 week
Clusters of similarly aged sign
Sun bear soil excavations, as well as excavations of P. mirabilis nests, estimated to be
of the same age and clustered within 25 m of each other along a transects, were treated as a
single feeding event based on our observations of foraging bears.
Ad-hoc searches of fresh sign after foraging activity by
radio-collared sun bears
We searched for fresh foraging sign of radio-collared wild sun bears on several occa-
sions, when a bear was found (through telemetry readings) to have been active in a confined
area for an extended period of time.
Statistical analysis
Differences in sign density between burned and unburned forest were first compared
using a two-way analysis of variance (ANOVA), with burned/unburned and years (n= 5) as
Chapter 7144
independent variables. When significant differences were found, a series of one-way ANOVA’s
in conjunction with Bonferroni post-hoc tests were used to evaluate sign types and year ef-
fects within the two sampled forest types (i.e., burned and unburned forest). Differences in the
ages of sign between years in burned and unburned forest were evaluated using log likelihood
ratio tests (i.e., G tests), and P values were estimated via Monte Carlo randomization (using
SPSS’s default 10,000 permutations). In the case of a significant G test, implying that there was
a significant amount of variation between variables, the adjusted standardized cell residuals
were evaluated in order to identify which cells were most responsible for the observed vari-
ation. Following Agresti (2002), adjusted standardized cell residuals ≥ |2.0| were considered
significant. Between year differences of fig and aboveground termite nest densities (2005 and
2010) were compared with paired sampled t-tests. Analyses were carried out with SPSS and R.
Results
We surveyed 92 strip transects, 45in unburned forest and 47 in burned areas, during 5
years over a period of a more than 10 years. Differences in sign densities were found between
unburned and burned forest (two-way ANOVA, F=157.9, df=1,90, p<0.001) (Fig. 4), with a sig-
nificant interaction effect in sign frequencies between years and treatment (burned/unburned)
(F=5.1, df = 4, 91, P=0.001).
Sign density in unburned forest remained stable across years, averaging 41.6 ± 11.6
(SD) sign/ha (Table 3, Fig. 4) (one-way ANOVA, F=0.28, df=4,40, p=0.891). We found some sun
bear sign (range 9-71 sign/ha) in all transects in unburned forest. Lowest sign density encoun-
tered was on one transect that crossed an open swamp area, rarely used by sun bears. We cata-
logued 1,871 sign events in 45 ha of unburned forest, the most common of which was broken
termite nests (63.7%, n= 1,192), of which 24.3% were above ground and the remainder exca-
vated underground nests (n=738). Claw marks (22.9%, n=429), and broken logs (7.9%, n=148)
were next most common. Soil digs, broken logs and footprints all showed significant changes
over the years (one-way ANOVA, soil: F=3.07, df=4,40, p=0.027; broken logs: F=3.12, df=4,40,
p=0.025; prints: F=5.43, df=4,40, p=0.001) although only differences in soil digs between the
years 2005-2010 remained significant (p=0.032) after post hoc Bonferroni tests.
Sign densities in burned forest increased significantly over the years (one-way ANOVA,
F=21.51, df=4,42, p<0.001), with 2005 and 2010 each having higher sign densities than all
previous years (Bonferroni post hoc test, 2005: p<0.05 for all tests, 2010: p<0.01 for all tests).
Exploring the use of sign surveys for monitoring relative abundance of sun bears 145
Figure 4. Average number of sun bear sign encountered along strip transects in burned and unburned
forest 2000-2010.
Sign densities in burned forest areas were extremely low in 2000-2002 ranging from 0-4 sign/ha
(Table 3). Sign density increased by 2005 (16.1 ± 6.3 (SD) sign/ha) but was still 60% lower than
in adjacent unburned forest (40.8 ± 10.9 (SD) sign/ha) (t=7.10 df=24, p<0.001). By 2010 sign
densities in burned forest areas had increased to 28.0 ± 12.9 (SD) sign/ha, though still 35%
less than in adjacent unburned forest (44.1 ± 16.1 (SD) sign/ha) (t=3.04, df=28, p<0.005).
Underground termite nest sign was significantly higher in 2010 compared to all previous years
(Bonferroni post hoc tests, p<0.001). No between-year differences were found in aboveground
termite nest sign. By 2010, the most common sign categories encountered in burned forest (16
transects, n=439 sign) were broken termite nests (51.0%, n=224) consisting mostly of dug-up
underground nests (40.5%, n=178), followed by claw marks (40.1%, n=176). Broken logs only
made up 3.6% of sign (n=16).
The three main categories of sign (broken termite nests, claw marks, broken/ripped
logs) made up 90-97% of sign encountered in burned and unburned forest. In unburned forest,
the percentage of sign related to termite diggings (62-71%), claw marks (23-25%) and dead
wood (4-13%) remained stable over time (Fig. 5). In burned forest, by contrast, types of sign
varied across years. The proportion of dead wood sign decreased over the years, whereas
Chapter 7146Ta
ble
3. S
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200
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2000
2001
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1 km
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Exploring the use of sign surveys for monitoring relative abundance of sun bears 147Ta
ble
3. C
ontin
ued.
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Chapter 7148
Figure 5. Ratio of main sign categories in unburned and burned forest areas.
proportion of termite sign increased steadily. Termite sign (above- and underground nests
combined) made up 35.9% of sign in burned forest in 2005 whereas in unburned forest this
was 65.5% of total sign (Fig. 5). By 2010 termite sign in burned forest areas rose to 50.2% of
total sign. Most of this rise was related to excavation of underground termites; density of that
sign increased from 4.2 ± 3.0 nests/ha in 2005 to 11.1 ± 5.6 (SD) nests/ha in 2010 (compared
to ~17 nests/ha in unburned forest; Table 4).
Claw marks dominated the sign in burned areas in 2005, making up 47.4% of encoun-
tered sign compared to 21.3% in unburned forest, with equivalent densities between the two
areas (Table 3). Trees with claw marks that belonged to taxa known to occur in the diet of
sun bears (Fredriksson et al. 2006a) made up 77% of identified climbed trees in 2005 (both
in burned and unburned forest), and 68-82% of trees in 2010 in burned and unburned forest,
respectively.
The proportions of different types of sun bear sign encountered along transects in un-
burned forest (all years combined) differed substantially from either the types of sign deposited
during observations of bear foraging activity or the fresh sign encountered during searches of
known bear foraging locations (Table 4). Direct observations of three rehabilitated sun bears
between 1998-2002 (n=4,964 hours) provided a record of some 26,131 visually-confirmed sign.
More than half of this sign was ripped decaying logs, which was similar to what we found when
searching areas where wild-caught radio-collared bears had previously fed for an extended
Exploring the use of sign surveys for monitoring relative abundance of sun bears 149
Table 4. Percentage of sign allocated to different categories from 1) direct observations; 2) searches of sign
left by radio-collared bears after prolonged activity in a restricted area; 3) sign encountered along transects
in unburned forest.
Observations (n=26,131 sign)
Sign searches of known bear location
(n=147 sign)
Transects (45 km) in unburned forest (n=1,871 sign)
Ripped logs 54.4 (n=14,224) 55.8 (n=82) 7.9 (n=148)
Broken termite nests 21.1 (n=5,515) 21.2 (n=31) 63.7 (n=1,192)
Claw marks 10.3 (n=2,701) 8.8 (n=13) 22.9 (n=429)
Soil digs 7.5 (n=1,964) 8.8 (n=13) 3.9 (n=73)
Bite marks 3.1 (n=808) 0 0
Foot prints n/a 4.8 (n=7) 0
Scats 2.2 (n=584) 0.7 (n=1) 0.3 (n=6)
Stingless bee nests 0.2 (n=52) 0 1.2 (n=23)
Tree nests 0 0 0
Others 1.1 (n=283) 0 0
period (Table 4). In contrast, ripped logs represented only 8% of sign along transects in un-
burned forest. Whereas broken termite nests comprised >60% of the sign along transects, they
represented only 21% of the sign observed associated with foraging by radio-collared bears
Densities of active termite nests and figs along
transects
Densities of active aboveground termite nests (all nest shapes combined) counted
along strip transects were significantly lower in burned areas, both in 2005 and 2010 (2005,
t=9.73, df=24, p<0.001; 2010, t=4.58, df=28, p<0.001) with densities reaching only 33% of those
encountered in unburned forest those years. Densities of hemi-epiphytic figs did not differ
significantly between burned and unburned areas, both in 2005 (t=-0.78, df=24, p=0.44) and
2010 (t=-0.32, df=28, p=0.75).
Changes in density of sign in different age categories
over years
The ratio of age categories, to which each sign was allocated, changed considerably
in both burned (G statistic = 52.96, df=4, P<0.001) and unburned (G statistic = 90.45, df=4,
P<0.001) areas over the sampling period. Density of sign allocated to the fresh (<1 year) cat-
egory decreased in unburned forest during 2000-2010, from 27.6±11.4 (SD) sign/ha in 2000
Chapter 7150
Figure 6. Densities of sign/hectare of different age categories in burned and unburned forest for all
survey years.
Exploring the use of sign surveys for monitoring relative abundance of sun bears 151
to16.9±8.5 (SD) in 2010 (Fig. 6). In burned forest the density of both fresh and old sign in-
creased over the years, the latter from 2.6 ± 2.3 (SD) sign/ha in 2005 to 9.9 ±6.9 (SD) in
2010, whilst density of fresh sign only increased slightly from 10.2±5.1 (SD) sign/ha in 2005 to
11.1 ± 6.5 (SD) in 2010.
Discussion
Interpretation of sun bear sign surveys in the context
of the SWPF
Our comparison of sun bear sign densities between adjacent unburned and burned
areas, through replicated sampling over time, showed that sun bears are slowly re-colonizing
these once-burned areas, although they did not yet recover to pre-fire levels after more than
a decade of forest regeneration. Sign densities increased from close to zero 2 years after the
fire event, to 65% of that encountered in adjacent unburned forest habitat 12 years after the
fire event. Sign densities in unburned forest remained relatively stable (44.1 ± 16.1 (SD) sign/
ha) over the decade of monitoring.
The increase in sun bear sign observed in burned areas must be related to a slow
recovery of food resources, as habitat use by bears has been found to be highly influenced
by food availability (Steinmetz et al. 2011). The main increase of sign in burned areas was that
of excavated underground termite nests (P. mirabilis) and claw marks on fruit-producing trees.
Fruit resources play an important part of the sun bear diet, but availability varies drastically
over time and is heavily influenced by aseasonal and rare mast fruiting events (Fredriksson
et al. 2006a). In burned forest, close to 80% of sun bear fruit trees died, 3 years after the fire
(Fredriksson et al. 2006b); however densities of claw marks in burned forest areas in 2010
were similar to those recorded in unburned forest (Table 4). This would indicate that sun bears
were climbing remaining trees in these burned areas at a higher rate than in unburned forest.
Close to 70% of trees with claw marks in burned areas in 2010 were taxa important in the diet
of sun bears, and it might be that trees were more frequently climbed even if they had small
fruit crops. Figs are one of the main fruit resources for sun bears during the prolonged inter-
mast periods (Wong et al. 2002, Fredriksson et al. 2006a), and densities of hemi-epiphytic figs
counted along transects, both in 2005 and 2010, were similar in burned and unburned forest.
Putz and Susilo (1994) also reported quick recovery of root connections of hemi-epiphytic figs,
10 years after the extensive fire event of 1982-83 in East Kalimantan.
Chapter 7152
Density of foraging sign of aboveground termite nests in burned forest was still very
low 12 years after the fire event. Densities of active epigeal nests were still 60% lower than in
adjacent unburned forest, indicating that recovery of aboveground termite species after fire
disturbance is a slow process. Jones et al. (2003) reported the collapse of termite assemblages
along a disturbance gradient in Sumatra related to changes in forest canopies, which normally
buffer the forest interior from extreme variations in microclimate. Temperature, relative humid-
ity, wind speed and solar radiation at ground level are all highly sensitive to changes in canopy
depth and structure (Chen et al. 1999).In burned forest areas the buffering capacity of the
canopy was much reduced as almost 80% of trees(>10 cm DBH) died after the fire event (Fre-
driksson et al. 2006b). Gathorne-Hardy et al. (2002) hypothesized that termite recovery after
heavy disturbance might take 60 years, if source populations of forest termites are found nearby.
The reduction in density of fresh sign in unburned forest in 2010 (Fig. 6) could be in-
terpreted in a number of ways. Sign transects only commenced after the fire event and hence
any increase in sign densities from an influx of bears displaced from the burned area would not
have been discernable. Bears fed mainly on insect resources in the remaining unburned area
after the forest fires because fruits, even Ficus spp., were virtually absent. This fruiting low was
possibly caused by disrupted phenologies after the prolonged El Niño drought (Harrison 2000,
2001), combined with exhausted energy reserves after the mast fruiting event (van Schaik
1986, Sork et al. 1993). Termites and ants, on the other hand, have been found consistently com-
mon on the forest floor in tropical forests (Kikkawa and Dwyer 1992), with highest termite
densities found in lowland forests (Collins 1989). The diffuse but abundant distribution of this
food resource, as opposed to highly sought-after, but low density fruit resources, might have
enabled some bears from burned areas to squeeze into or between the homeranges of resi-
dent bears in unburned forest. The subsequent decrease in density of fresh sign might indicate
that some bears moved back into regenerating burned areas, as substantiated by increasing
sign densities there.
Unexpectedly, data collected in 2010 in unburned forest showed an increase in inter-
mediate and old sign, whereas in earlier years fresh and intermediate sign showed a decline.
If fresh sign declined, old sign also should have declined, but with a time lag. The 5-year gap
between 2005 and 2010 should have been a sufficient time lag to witness a decline in old sign
(since most was <5 years old). That this was not the case might indicate that age estimation
of sign during surveys in 2010 was inconsistent with previous surveys (i.e., some sign allocated
to an older age category than it was). That is, inter-observer variability could have affected the
results, despite our training course.
Exploring the use of sign surveys for monitoring relative abundance of sun bears 153
Our results also suggest that temporal changes in regeneration of the forest and re-
colonization by sun bears in SWPF are still in flux; this emphasizes the importance of long-term
studies. Had this study only been carried out within the first 4 years post-fires, the conclusion
would have been that there was virtually no use of the burned areas by sun bears. While true
at the time, this would not have documented the potential value of these areas for re-coloni-
zation. Few studies so far have looked at the recovery of large mammals after forest fires in
Indonesia (O’Brien et al. 2003) despite the immense scale of the impacted area: the fire event
of 1997–1998 affected 5.2 million ha of land in the province of East Kalimantan alone, 2.6 mil-
lion ha of which were forest including several protected lowland reserves (Hoffman et al. 1999,
Siegert et al. 2001, Fuller et al. 2004).
Post-fire regeneration potential and conservation
implications
The re-colonization of sun bears into these once-burned forest areas implies that
these forest areas can still be important for sun bear conservation, if there is undisturbed for-
est nearby that supports a source population. Sun bears are known to persist in logged-over
areas (Wong et al. 2004, Linkie et al. 2007), but fire causes much more severe damage to forest
integrity than selective logging (Slik et al. 2002). Most sun bear fruit resources are tree-borne
(versus shrubs or understory plants) and regeneration of this food resource after a fire prob-
ably takes several decades, if not longer.
Primary rainforest in Indonesia can rapidly be converted to savanna grasslands if af-
fected by repeated fires (Goldammer 1999).Fire-return intervals of less than 90 years can
eliminate rainforest species, whereas intervals of less than 20 years may eradicate trees entirely
(Cochrane et al. 1999). Many of these fire-disturbed areas have seen further fire damage dur-
ing smaller drought events in subsequent years (2002, 2004), or have been converted to other
uses altogether. Dennis and Colfer (2006) calculated that 70% of forest initially damaged by fire
and drought during the 1982–83 El Niño event was classified as non-forest by 2000, following
a degradation pathway starting with commercial logging, followed by government sponsored
transmigration schemes, then by government-licensed timber and oil palm plantations and, fi-
nally, the devastating fires of 1998. A similar, though faster, trajectory of conversion of degraded
forests to plantations was evident for many fire-affected forest areas after 1997-1998 (Fuller
et al. 2004, Miettinen et al. 2011).
Thus remaining sun bear habitat has become increasingly fragmented, impairing post-
fire immigration of bears from other habitat blocks. Recovery of populations in forest areas
Chapter 7154
disturbed by severe ecological catastrophes, such as the combined effects of fires, fragmenta-
tion and fruiting failure discussed in this paper, will now in many cases have to rely on recruit-
ment from within remaining patches of less-disturbed habitat. Unfortunately, with the current
minimal capacity to prevent or control forest fires in Indonesia, it seems unlikely in the near
future that fire threat to forest areas will be reduced.
Further development of sign surveys as a monitoring
tool
Sun bears are currently listed as ‘Vulnerable’ by the IUCN (Fredriksson et al. 2008)
primarily based on high rates of habitat loss over the last 30 years and increasing hunting
pressures throughout mainland Southeast Asia (Foley et al. 2011). There is a pressing need to
develop monitoring tools for this species, especially as poaching rates are on the rise and sun
bears have already gone quietly extinct in several countries. Our current use of sign transects,
as described here, to monitor changes in sun bear use of burned forest areas, with adjacent
unburned forest as our control site, has proven to be a useful method. The implementation
of these transects was relatively cheap and time efficient, although inter-observer variability in
ageing sign might have been a problem.
However, several challenges still remain in further developing this method as a tool to
monitor trends in relative abundance of sun bears in key conservation areas. Steinmetz and
Garshelis (2008) stressed that caution is required in inferring differences in population size
over time or space from sign abundance as sign production can vary not only with changes in
the number of bears but also their foraging behaviour.
A number of issues related to the classification and interpretation of sign data need
further attention. Different decay rates of different types of sign can cause potential problems.
Certain sign categories can remain identifiable as sun bear sign for more than a decade (e.g., big
holes ripped in tree trunks to predate stingless bees) whereas other types of sign disappear or
become difficult to identify within months (e.g., broken logs or soil digs). This large variation in
decay rates of different sign categories implies that it will be more prudent to focus trend data
analysis on fresh sign only, where variance in decay is less pronounced. During our observa-
tions of rehabilitated sun bears we documented sign creation rates for different sign categories;
these results were consistent with what we observed in areas where a wild sun bear had been
foraging shortly before, but differed considerably from the ratio of sign categories encountered
along transects (Table 4). The disparity, we believe, is primarily related to variation of decay
rates of different sign types: sign types that decayed quickly were still evident a short time after
Exploring the use of sign surveys for monitoring relative abundance of sun bears 155
a sun bear foraging bout, but had decomposed before our transect sampling. Thus, long-lasting
sign (e.g., clawmarks and broken termite nests) were over-represented on transects. Other
sign, like ripped-open logs, had decayed to the extent that they could no longer be positively
identified as sun bear sign.
One other important issue that will need further scrutiny is the definition of a single
sign ‘event’. This is currently open to varied interpretation. Based on our feeding observations
of bears in this study area, we considered similarly-aged dug-up underground termite nests, as
well as soil digs, encountered within 25 m of each other as a single sign event, as bears would
frequently create such sign during one feeding bout. In some cases this could mean that 10 dug
up termite nests, all of similar age, would be recorded as 1 sign. We did not however group
similarly-aged sign of different types, nor did we group two nearby trees with claw marks of
similar age. To some extent, such decisions about grouping sign may affect results.
Seasonality in the deposition of certain sign types related to seasonal differences in
food availability might also be an issue. Sun bears foraged for termites year-round but certain
mounds were more severely destroyed, and probably more sought after, when alates were
ready to emerge. In the tropics, mass emergence of alates (swarming) is triggered by seasonal
phenomena, initially thought to be rainfall (Nutting 1969), though species can swarm over
prolonged periods of time (Neoh and Lee 2009a) with triggers for swarming linked to atmos-
pheric pressure and temperature (Neoh and Lee 2009b). Sun bears in Borneo were found
to feed heavily on fruits during the short and irregular mast fruiting season that occurs once
every 2-10 years (Medway 1972, Ashton et al. 1988, Curran and Leighton 2000). During our
study a significant mast fruiting event occurred toward the end of 1997-early 1998 and lasted
for 2 months, 2 years prior to the start of sign transect work; no large fruiting event occurred
during subsequent years but larger quantity of fruiting trees might lead to higher rates of claw
marked trees.
A final topic that would be most useful to further investigate is the feasibility of con-
verting sign densities into estimates of bear abundance. During our observations of rehabili-
tated sun bears we documented sign creation rates and, on some occasions, measured real dis-
tances traveled by one bear (Fredriksson et al. in prep). These data, in combination with decay
rates of different sign and sign detection along transects in the same forest area, might produce
a workable relationship between sign densities and bear abundance. As sun bear behaviour is
influenced by the distribution and abundance of different food resources, their sign deposition
rates and the proportion of different sign types will differ amongst different ecosystems, mak-
ing the conversion of sign densities to bear abundance a site-specific issue.
Chapter 7156
AcknowledgementsWe thank the Indonesian Institute of Sciences (LIPI) for granting GMF permission to
carry out research on sun bears in East Kalimantan. GMF would like to express gratitude to
the Forest Research Institute in Samarinda for their assistance and the Wanariset Herbarium.
Homathevi Rahman is thanked for identifying termite samples during a visit to Sungai Wain.
Timbull is thanked for all illustrations. We would like to thank Claire Palmer for supervising
the transect work in 2005. The Tropenbos Foundation, the Borneo Orangutan Foundation, and
the Conservation Endowment Fund of the American Zoo and Aquarium Association provided
financial assistance. Field assistants Trisno, Lukas, and Damy are thanked for assistance in the
forest throughout the years, as well as many people from the Sungai Wain village who helped
with ferrying logistical supplies. WJS would like to thank Ristek for granting permission to
carry our research in 2010, as well as field assistants Ulir, Fitri, Misran and Anto. E. Rood and M.
Nowak are thanked for assistance with statistics. Graham Usher is thanked for all help, as well
as GIS analysis and maps for this paper.
ReferencesAgresti, A. (2002). Categorical data analysis. Wiley & Sons, New Jersey.
Altmann, J. (1974). Observational study of behavior: sampling methods. Behaviour 49:227-265.
Ashton, P.S., Givnish, T.J., and Appanah, S. (1988). Staggered Flowering in the Dipterocarpaceae - New In-
sights into Floral Induction and the Evolution of Mast Fruiting in the Aseasonal Tropics. American
Naturalist 132, 44-66.
Barber, C.V., and Schweithelm, J. (2000). Trial by fire. Forest fires and forestry policy in Indonesia’s era of
crisis and reform (Washington D.C, USA, World Resources Institute (WRI), Forest Frontiers Ini-
tiative. In collaboration with WWF-Indonesia and Telapak Indonesia Foundation).
Barlow, J., and Peres, C. (2006). Effects of single and recurrent wildfires on fruit production and large ver-
tebrate abundance in a Central Amazonian forest. Biodiversity and Conservation 15, 985-1012.
Bider, J.R. (1968). Animal activity in uncontrolled terrestrial communities as determined by a sand transect
technique. Ecological Monographs 38, 269-308.
Chen, J., Saunders, S.C., Crow, T.R., Naiman, R.J., Brosofske, K.D., Mroz, G.D., Brookshire, B.L., and Franklin,
J.F. (1999). Microclimate in forest ecosystem and landscape ecology. Bioscience 49, 288–297.
Cochrane, M. A., A. Alencar, M. D. Schulze, C. M. J. Souza, D. C. Nepstad, P. Lefebvre, and E. A. Davidson. (1999).
Positive feedbacks in the fire dynamic of closed canopy tropical forests. Science 284:1832-1835.
Exploring the use of sign surveys for monitoring relative abundance of sun bears 157
Collins, N.M. (1989). Termites. In Tropical Rain Forest Ecosystems Biogeographical and Ecological Studies,
H. Lieth, and M.J.A. Werger, eds. (Amsterdam, Elsevier), pp. 455-471.
Curran, L.M., and Leighton, M. (2000). Vertebrate responses to spatiotemporal variation in seed production
of mast-fruiting dipterocarpaceae. Ecological Monographs 70, 101-128.
Darlington, J.P.E.C. (1997). Comparison of nest structure and caste parameters of sympatric species of
Odontotermes (Termitidae, Macrotermitinae) in Kenya. Insectes Sociaux 44, 393-408.
Dennis, R.A., and Colfer, C.P. (2006). Impacts of land use and fire on the loss and degradation of lowland
forest in 1983–2000 in East Kutai District, East Kalimantan, Indonesia. Singapore Journal of Tropical
Geography 27, 30-48.
Foley, K.E., Stengel, C.J., and Shepherd, C.R. (2011). Pills, Powders, Vials and Flakes: the bear bile trade in Asia
(Petaling Jaya, Selangor, Malaysia, TRAFFIC Southeast Asia).
Fredriksson, G.M. (2002). Extinguishing the 1998 forest fires and subsequent coal fires in the Sungai Wain
Protection Forest, East Kalimantan, Indonesia. In: Moore, P., Ganz, D., Tan, L.C., Enters, T. and Durst,
P.B. (eds.), Communities in flames: Proceedings of an international conference on community
involvement in fire management. FAO and FireFight SE Asia, pp. 74-81.
Fredriksson, G.M., and Nijman, V. (2004). Habitat-use and conservation of two elusive ground birds (Carpo-
coccyx radiatus and Polyplectron schleiermacheri) in Sungai Wain protection forest, East Kalimantan,
Indonesian Borneo. Oryx 38, 297-303.
Fredriksson, G.M., Wich, S.A., and Trisno (2006a). Frugivory in sun bears (Helarctos malayanus) is linked to
El Niño-related fluctuations in fruiting phenology, East Kalimantan, Indonesia. Biological Journal of
the Linnean Society 89, 489-508.
Fredriksson, G.M., Danielsen, L.S., and Swenson, J.E. (2006b). Impacts of El Niño related drought and forest
fires on sun bear fruit resources in lowland dipterocarp forest of East Borneo. Biodiversity and
Conservation 15, 1271-1301.
Fredriksson, G., Steinmetz, R., Wong, S. & Garshelis, D.L. (2008). Helarctos malayanus. In: IUCN 2011. IUCN
Red List of Threatened Species. Version 2011.2. <www.iucnredlist.org>. Downloaded on 27 April
2012.
Fuller, D.O., Jessup, T.C., and Salim, A. (2004). Loss of forest cover in Kalimantan, Indonesia, since the 1997-
1998 El Niño. Conservation Biology 18, 249-254.
Garshelis, D.L., and Hristienko, H. (2006). State and Provincial Estimates of American Black Bear Numbers
versus Assessments of Population Trend. Ursus 17, 1-7.
Gathorne-Hardy, F.J., Jones, D.T., and Syaukani (2002). A regional perspective on the effects of human distur-
bance on the termites of Sundaland. Biodiversity and Conservation 11, 1991-2006.
Chapter 7158
Goldammer, J. G. (1999). Forest on fire. Science 284:1782-1783.
Hansen, M.C., Stehman, S.V., Potapov, P.V., Arunarwati, B., Stolle, F., and Pittman, K. (2009). Quantifying
changes in the rates of forest clearing in Indonesia from 1990 to 2005 using remotely sensed data
sets. Environmental Research Letters 4, 034001.
Harrison, R. D. (2000). Repercussions of El Niño: drought causes extinction and the breakdown of mu-
tualism in Borneo. Proceedings of the Royal Society of London Series B-Biological Sciences
267:911-915.
Harrison, R. D. (2001). Drought and the consequences of El Niño in Borneo: a case study of figs. Population
Ecology 43:63-75.
Harrison, R.D. (2011). Emptying the Forest: Hunting and the Extirpation of Wildlife from Tropical Nature
Reserves. BioScience 61, 919-924.
Hoffmann, A.A., Hinrichs, A., and Siegert, F. (1999). Fire damage in East Kalimantan in 1997/98 related to
land use and vegetation classes: Satellite radar inventory results and proposal for further actions.
IFFM-SFMP Report No.1a (Samarinda, East Kalimantan, MOFEC, GTZ and KfW).
Islam, M.A., Muzaffar, S.B., Aziz, M.A., Kabir, M.M., Uddin, M., Chakma, S., Chowdhury, S.U., Rashid, M.A.,
Chowdhury, G.W., Mohsanin, S., et al. (2010). Baseline survey of Bears in Bangladesh, 2008-2010
(Wildlife Trust of Bangladesh).
IUCN/SSC Bear Specialist Group (2006), Workshop on Rangewide Mapping of Asian Bears, 17th Inter-
national Conference on Bear Research and Management, International Bear Association (IBA),
Karuizawa, Japan.
Jones, D.T., Susilo, F.X., Bignell, D.E., Hardiwinoto, S., Gillison, A.N., and Eggleton, P. (2003). Termite assem-
blage collapse along a land-use intensification gradient in lowland central Sumatra, Indonesia. Jour-
nal of Applied Ecology 40, 380-391.
Kendall, K.C., Metzgar, L.H., Patterson, D.A., and Steele, B.M. (1992). Power of sign surveys to monitor
population trends. Ecological Applications 2, 422-430.
Kikkawa, J., and Dwyer, P.D. (1992). Use of scattered resources in rain forest of humid tropical lowlands.
Biotropica 24, 293-308.
Kindberg, J., Swenson, J.E., Ericsson, G.r., Bellemain, E., Miquel, C., and Taberlet, P. (2011). Estimating popu-
lation size and trends of the Swedish brown bear Ursus arctos population. Wildlife Biology 17,
114-123.
Kinnaird, M.F., and O’Brien, T.G. (1998). Ecological effects of wildfire on lowland rainforest in Sumatra.
Conservation Biology 12, 954-956.
Kühl, H., F. Maisels, M. Ancrenaz, and E. A. Williamson. (2008). Best Practice Guidelines for Surveys and
Monitoring of Great Ape Populations. IUCN, Gland, Switzerland.
Exploring the use of sign surveys for monitoring relative abundance of sun bears 159
Kutilek, M.J., Hopkins, R.A., Clinite, E.W., and Smith, T.E. (1983). Monitoring population trends of large
carnivores using track transects. In Renewable resource inventories for monitoring changes’ and
trends, J. F. Bell, and T. Atterbury, eds. (Corvallis, Oregon State University), pp. 104-106.
Linkie, M., Dinata, Y., Nugroho, A., and Haidir, I.A. (2007). Estimating occupancy of a data deficient mamma-
lian species living in tropical rainforests: Sun bears in the Kerinci Seblat region, Sumatra. Biological
Conservation 137, 20-27.
Medway, L. (1972). Phenology of a tropical rain forest in Malaya. Biological Journal of the Linnean Society
4, 117-146.
Meijaard, E., and Dennis, R.A. (1997). Forest fires in Indonesia; Bibliography and background information
(Zeist, WWF Netherlands), pp. 38.
Meijaard, E. (1999). Human-imposed threats to sun bears in Borneo. Ursus 11, 185-192.
Miettinen, J., Shi, C., and Liew, S.C. (2011). Deforestation rates in insular Southeast Asia between 2000 and
2010. Global Change Biology 17, 2261-2270.
Mowat, G., and Strobeck, C. (2000). Estimating population size of grizzly bears using hair capture, DNA
profiling, and mark-recapture analysis. Journal of Wildlife Management 64, 183-193.
Neoh, K.-B., and Lee, C.-Y. (2009). Flight Activity of Two Sympatric Termite Species, Macrotermes gilvus and
Macrotermes carbonarius (Termitidae: Macrotermitinae). Environmental Entomology 38, 1697-1706.
Neoh, K.-B., and Lee, C.-Y. (2009). Flight activity and flight phenology of the Asian subterranean termite,
Coptotermes gestroi (Isoptera: Rhinotermitidae). Sociobiology 54, 521-530.
Nutting, W.L. (1969). Flight and colony foundation. In Biology of Termites, K. Krishna, and F.M. Weesner, eds.
(New York, Academic Press), pp. 233-282.
O’Brien, T.G., Kinnaird, M.F., Nurcahyo, A., Prasetyaningrum, M., and Iqbal, M. (2003). Fire, demography and
the persistence of siamang (Symphalangus syndactylus: Hylobatidae) in a Sumatran rainforest. Ani-
mal Conservation 6, 115-121.
Putz, F.E., and Susilo, A. (1994). Figs and fire. Biotropica 26, 468-469.
Siegert, F., Ruecker, G., Hinrichs, A., and Hoffmann, A.A. (2001). Increased damage from fires in logged for-
ests during droughts caused by El Niño. Nature 414, 437-440.
Singer, F. J., W. Schreier, J. Oppenheim, and E. O. Garton. (1989). Drought, Fires, and Large Mammals. BioSci-
ence 39:716-722.
Slik, J.W.F., Verburg, R.W., and Kessler, P.J.A. (2002). Effects of fire and selective logging on the tree species
composition of lowland dipterocarp forest in East Kalimantan, Indonesia. Biodiversity & Conser-
vation 11, 85-98.
Sork, V. L. (1993). Evolutionary ecology of mast-seeding in temperate and tropical oaks (Quercus spp.).
Vegetatio 107/108:133-147.
Chapter 7160
Stanley, T.R.J., and Bart, J. (1991). Effects of roadside habitat and fox density on a snow track survey for foxes
in Ohio. Ohio Journal of Science 91, 186-190.
Steinmetz, R., Chutipong, W., and Seuaturien, N. (2006). Collaborating to Conserve Large Mammals in
Southeast Asia. Conservation Biology 20, 1391-1401.
Steinmetz, R., and Garshelis, D.L. (2008). Distinguishing Asiatic Black Bears and Sun Bears by Claw Marks
on Climbed Trees. Journal of Wildlife Management 72, 814-821.
Steinmetz, R., and Garshelis, D.L. (2010). Estimating ages of bear claw marks in Southeast Asian tropical
forests as an aid to population monitoring. Ursus 21, 143-153.
Steinmetz, R., Garshelis, D.L., Chutipong, W., and Seuaturien, N. (2011). The Shared Preference Niche of
Sympatric Asiatic Black Bears and Sun Bears in a Tropical Forest Mosaic. PLoS One 6, e14509.
Tacconi, L. (2003). Fires in Indonesia: Causes, costs and policy implications (Bogor, CIFOR), pp. 1-34.
van Nieuwstadt, M.G.L. (2002). Trial by fire- Postfire development of a dipterocarp forest. Ph.D. thesis.
University of Utrecht, Netherlands.
van Schaik, C. P. (1986). Phenological changes in a Sumatran rain forest. Journal of Tropical Ecology 2:327-347.
Vié, J-C., Hilton-Taylor, C. and Stuart, S.N. (2009). Wildlife in a changing world - An analysis of the 2008
IUCN red list of threatened species. IUCN, Gland, Switzerland, 180 pp.
Whelan, R.J. (1995). The ecology of fire (Cambridge, Cambridge University Press).
Whitmore, T.C. (1984). Tropical rain forests of the Far East, 2nd edn. (Oxford, Clarendon Press).
Wilson, G. J. and Delahay, R. J. (2001). A review of methods to estimate the abundance of terrestrial carni-
vores using field signs and observation. Wildl. Res. 28: 151–164.
Wong, S.T., Servheen, C., and Ambu, L. (2002). Food habits of Malayan sun bears in lowland tropical forest
of Borneo. Ursus 13, 127-136.
Wong, S.T., Servheen, C., and Ambu, L. (2004). Home range, movement and activity patterns, and bedding
sites of Malayan sun bears, Helarctos malayanus in the rainforest of Borneo. Biological Conserva-
tion 119, 168-181.
Chapter 8
Synthesis and Conclusions
Synthesis and conclusions 165
Synthesis and Conclusions
The Malayan sun bear, Helarctos malayanus, is the smallest of the eight extant bear spe-
cies, and is distributed throughout Southeast Asia including the large islands of Sumatra and
Borneo. Research on sun bears in the wild, including those in Kalimantan (Indonesian Borneo),
was non-existent before the work that is presented in this thesis commenced in 1997, in a
small lowland reserve in East Kalimantan. Apart from a few anecdotal records, virtually nothing
was known about basic aspects of sun bear ecology and they were listed as Data Deficient by
the IUCN Red list at the time. The results of this study have filled some of the bigger gaps in
our knowledge on various aspects of sun bear behaviour, ecology, and conservation.
Setting the stage: El Niño-Southern Oscillation and
forest fires
The start of this research in the Sungai Wain Protection Forest (SWPF) coincided with
a strong El Niño-Southern Oscillation (ENSO) episode. Global climatic cycles, such as ENSO,
affect diverse ecological processes including community dynamics and landscape disturbances
in tropical regions (Webster and Palmer 1997). The onset of ENSO events in Asia is marked by
a reduction in rainfall, resulting in drought conditions (Walsh 1996, Walsh and Newbery 1999).
Furthermore, climatic conditions associated with ENSO provide an irregular supra-annual,
regional trigger which initiates asynchronous, widespread flowering in Bornean Dipterocar-
paceae (Curran et al. 1999). Interestingly, a variety of other taxonomic groups flower and fruit
synchronously with these dipterocarps (Appanah 1985, Sakai et al. 1999, Cannon et al. 2007).
One of these rare community mast fruiting events [supra-annual production of large seed
crops interspersed by irregular periods of low seed production] triggered by the 1997-98
ENSO took place at our study site towards the end of 1997 (Chapter 2).
This same ENSO event also provided the enabling conditions, through prolonged
drought, for the catastrophic forest fires of 1997-98. This fire event affected circa 5 million
hectares (Mha) of land in the province of East Kalimantan (Indonesian Borneo) alone, including
2.6Mha of forest (Hoffmann et al. 1999, Siegert et al. 2001). In March 1998, fires burned half
of the forest in the reserve where this research project had started. Between 1997-2006, a
total of 16.2 Mha of Borneo’s landmass (21% of total land surface area) was affected by fires
(Langner and Siegert 2009). Habitat degradation due to large-scale forest fires, combined with
a prolonged fruiting low after the ENSO event, put large strains on the sun bear population
in the area.
Chapter 8166
Sun bear responses to large-scale fluctuations in food
availability
Sun bears, like most bear species, are omnivores. During rare mast-fruiting events in
East Kalimantan, sun bears opportunistically switched their diet to become frugivores (Chap-
ter 2). During these short periods, when calorie-rich fruits are available, sun bears gorged
themselves on large quantities of large-seeded fruits, for which they are effective seed dispers-
ers (McConkey and Galetti 1999, Chapter 2). In SWPF this brief glut only lasted two months,
followed by almost four years with very little fruit available (Chapter 2). This fruiting low was
probably caused by exhausted energy reserves after the mast fruiting event (van Schaik 1986,
Sork et al. 1993), but might have been aggravated by disrupted phenologies after the prolonged
El Niño drought (Harrison 2000, 2001).
The extent of frugivory in sun bears will vary considerably throughout their distribu-
tion range as patterns of fruit production differ substantially among tropical forests (van Schaik
et al. 1993, Wich and van Schaik 2000, Clark et al. 2001, Cannon et al. 2007). Bornean forests,
despite their food-rich appearance, display a significantly lower productivity than Sumatran
forests (Wich et al. 2011). Fruit productivity is generally thought to set carrying capacity for
rainforest vertebrates, which in turn may affect plant life history, seed dispersal, and vertebrate
population dynamics (Janzen 1974, Curran and Leighton 2000, Wich et al. 2004).
During the prolonged inter-mast period, sun bears shifted their diet to insects, primar-
ily termites and ants, complemented by a large variety of other saproxylic insects like beetle
grubs, cockroaches, and adult beetles. Although food resources in lowland tropical forests in
general are considered to be widely scattered and scarce, termites and ants are found to be
relatively abundant (Collins 1980, Kikkawa and Dwyer 1992). However, a large amount of en-
ergy is expended in obtaining these small quantities of food.
A small number of plant taxa were still producing fruit during the inter-mast period,
some of which were highly sought after by sun bears (Chapter 2). Sun bear ranging patterns
during these inter-mast periods were influenced by the number of trees in fruit, with bears
ranging over larger areas in search for these widely dispersed but highly sought after fruit
resources (Chapter 3).
Female bears captured in the unburned forest core, 16 months after the fire event and
well into the inter-mast period, showed signs of serious undernourishment and weighed 30-
40% less than female bears caught simultaneously 700 km to the north in the Tabin Reserve, Sa-
bah, Malaysian Borneo. Bears at Tabin were found to be foraging on oil palm fruits in plantations
adjacent to the reserve (Nomura et al. 2004) during this period of fruit scarcity. At my study
Synthesis and conclusions 167
site, few external food resources were available for bears, except for bears living near the for-
est edge, some of which were augmenting their diet with fruits grown in orchards neighbouring
the forest edge (Chapter 5). The emaciated appearance of the female sun bears caught in SWPF,
without access to additional food supplies, suggests that prolonged survival solely on insect
resources was insufficient and that energy requirements were not met. Increased competition
due to immigration of displaced bears from the fires might have been an additional strain fac-
tor. The predation of one of the bears by a large python might have been related to the poor
nutritional condition of the bear, which might have rendered the bear less effective in fighting
off an attack or having a lowered vigilance (Chapter 6).
Simultaneous to the period of fruit scarcity in SWPF, a prolonged fruiting low was also
reported from the Danum Valley Conservation Area in Sabah, Malaysian Borneo: emaciated
bears and bearded pigs (Sus barbatus) were encountered at the same time in primary forest
there (Wong et al. 2005). In Danum, bears also had no access to human-related food resources
like oil palm fruits, unlike bears living near the forest edges in Tabin Reserve (Nomura et al.
2004). Curran and Leighton (2000) reported on emaciated and dead pigs after a prolonged
fruiting low during the same inter-mast period in West Kalimantan, further indicating that
this famine was possibly an island-wide occurrence. They speculated that the length of the
inter-mast cycle was long enough to suppress populations of bearded pigs, with piglets only
seen during mast fruiting events. Survival during periods of fruit scarcity is viewed as the criti-
cal determinant of frugivore vertebrate densities in Southeast Asian forests (van Schaik et al.
1993). Famine following fruiting failures has also been reported from other parts of the world.
Following a year of extremely low fruit production, mass mortality of Japanese macaques was
reported by Hanya et al. (2004), when 56% of individual primates of several well-studied groups
died. They hypothesized that the shortage of high-quality foods caused poor nutritional condi-
tions for the primates, making them highly vulnerable to diseases, with death as the ultimate
result. Wright et al. (1999) reported that on Barro Colorado Island, Panama, over a period of
49-years, four episodes of famine occurred every time an El Niño event was followed by a mild
dry season with very low fruit production.
Reproductive behavior of Bornean sun bears has been found to be aseasonal and poly-
estrous (Schwarzenberger et al. 2004, Frederick et al. 2012). These breeding habits of sun bears
might be an adaptation to the unpredictable availability of fruit, both in space and time, allowing
female sun bears to come back into estrous soon after having lost a cub. In SWPF female sun
bears were observed throughout the period of extreme fruit low as well as during mast fruiting
events with small cubs. Two undernourished female sun bears caught during the peak of fruit
Chapter 8168
scarcity in SWPF for telemetry studies, both had small cubs. However, both female bears died
subsequently leaving the fate of the cubs unknown. This indicates that these bears were still
able to find sufficient food resources to give birth, but it seems that the extreme food scarcity
following the ENSO event and fires, and possibly competition for food, meant that there was
insufficient food to sustain both lactation and maintenance of themselves. For American black
bears, which are seasonal breeders, a clear link between mast fruiting failure and a subsequent
decline in reproduction has been shown in several regions (Jonkel and Cowen 1970, Elowe and
Dodge 1989, Costello et al. 2003).
Impacts of fire on sun bear populations
The fires in 1998 burned 40% of SWPF in six weeks, depriving the sun bears living there
of their habitat. Forest fires had a destructive effect on the main sun bear food resources (tree-
borne fruits and social insects), with a decrease of > 80% in the density of sun bear fruit trees
(Chapter 4), as well as a significant reduction of densities of above- and underground termite
nests. Besides a decrease in food resources, reduced canopy cover due to high post-fire tree
mortality caused large changes in the micro-climate of the burned forest areas. Temperatures
during daytime were several degrees higher than in unburned forest, and a smothering thicket
of ferns dominated the understory in once burned areas (Slik and Eichhorn 2003), creating a
physical barrier for large ground-dwelling mammals.
While it is possible that some bears could have become trapped and burned, there are
a number of possibilities as to what happened to bears displaced from burned forest areas.
During the period of active fires, a high rate of sun bear roaring calls were heard near the fire
front indicating an increase in antagonistic encounters between bears, suggesting that bears
were displaced by fires and moved into home ranges of bears living in unburned forest. It is
possible that some bears subsequently were able to fit into the remaining unburned forest,
thus increasing densities of bears in the central core of the reserve. Sign transects, developed in
order to monitor relative abundance of sun bears (Chapter 7), only commenced after the fire
event and hence any increase in sign densities that would have occurred could not be detected.
The diffuse but abundant distribution of termites and ants, the main inter-mast food resource,
as opposed to highly sought after but low density fruit resources, might have allowed bears
from burned areas to fit into the homeranges of resident bears in unburned forest.
Crop-raiding activity increased in gardens adjacent to the forest edge after the forest
fires (Chapter 5), suggesting that bears were being displaced either from the core remaining
forest or from burned areas. In response to the crop-raiding certain farmers laid out poisoned
Synthesis and conclusions 169
baits and snares, and it is possible that bears were killed due to this increased encounter rate
with humans. Another possibility is that certain bears survived in unburned forest islands with-
in the burned forest matrix. Between 7-18% of the burned forest remained unscathed by the
fires as unburned patches, primarily near rivers or swamps (van Nieuwstadt 2002, Fredriksson
and Nijman2004). The use of such unburned patches and avoidance of burned areas has also
been reported for black bears in Arizona after fires (Cunningham et al. 2003).
Ranging and Activity
Annual ranging patterns for female sun bears measured during this study were 4-5 km2
(Chapter 3), with ranging patterns of collared bears entirely encompassed within the reserve
boundaries. Home range sizes of bears are related to body size (McNab 1963, Gittleman and
Harvey 1982, Gompper and Gittleman 1991), metabolic needs (McNab 1983) and distribution
and abundance of food (McLoughlin et al. 1999, 2000, Gompper and Gittleman 1991), resulting
in large inter- and intraspecific variation. Insectivorous carnivores usually have relatively small
home ranges (Gittleman and Harvey 1982) seemingly because protein-rich insect prey, espe-
cially ants and termites, are abundant and omnipresent over relatively small areas (e.g. Wood
and Sands 1978, Redford 1987). As such, the sloth bear (Melursus ursinus), the most insectivo-
rous ursid, appears to have the smallest home ranges of any species of bear (Ratnayake et al.
2007). During our study, sun bears had a comparable diet to sloth bears, spending up to 90% of
their foraging time consuming insects. It is possible that ranging patterns were slightly enlarged
during the inter-mast period due to the bears searching over a wider area for the few available,
scattered fruit trees, as opposed to smaller ranging patterns which would have been expected
on a predominantly insect diet (Gittleman and Harvey 1982).
Sun bears were found to display diurnal activity patterns within the SWPF (Chapter 3),
although more nocturnal behavior was reported for bears living near the forest edges (Chap-
ter 5). Consistent with their temporal response to humans, sun bears living in the core of the
reserve also showed spatial avoidance of human activity. Bears living near forest edges are at-
tracted to crops, especially when natural food supplies are low, making border areas potential
demographic sinks (Woodroffe and Ginsberg 1998).
Re-colonization of burned forest areas
Our comparison of sun bear sign densities between adjacent unburned and burned
areas showed that sun bears are slowly re-colonizing these once-burned areas, although they
did not yet recover to pre-fire levels after more than a decade of forest regeneration. Sign
Chapter 8170
densities increased from close to zero 2 years after the fire event, to 65% of that encountered
in adjacent unburned forest habitat 12 years after the fire event. Sign densities in unburned
forest remained relatively stable (44.1 ± 16.1 (SD) sign/ha) over the decade of monitoring
(Chapter 7).
In burned forest areas, claw marks and dug up underground termite nests dominated
sign density, but density of foraging sign of aboveground termite nests was still very low 12
years after the fire event. Densities of active epigeal nests were still 60% lower than in adjacent
unburned forest, indicating that recovery of aboveground termite species after fire disturbance
is a slow process. Jones et al. (2003) reported the collapse of termite assemblages along a dis-
turbance gradient in Sumatra related to changes in forest canopies, which normally buffer the
forest interior from extreme variations in microclimate. Temperature, relative humidity, wind
speed and solar radiation at ground level are all highly sensitive to changes in canopy depth and
structure (Chen et al. 1999). In burned forest areas the buffering capacity of the canopy was
much reduced as almost 80% of trees (>10 cm DBH) died after the fire event (van Nieuwstadt
2002, Chapter 4). Gathorne-Hardy et al. (2002) hypothesized that termite recovery after heavy
disturbance might take 60 years, if source populations of forest termites are found nearby.
Temporal changes in regeneration of the forest and re-colonization by sun bears in
SWPF are still in flux, which emphasizes the importance of long-term studies. Had this study
been carried out only within the first 4 years post-fires, the conclusion would have been that
there was virtually no use of the burned areas by sun bears. While true at the time, this would
not have documented the potential value of these areas for re-colonization.
Conservation implications
Few studies so far have looked at the recovery of large mammals after forest fires
in Indonesia (O’Brien et al. 2003) despite the immense scale of the impacted area. The re-
colonization of sun bears into these once-burned forest areas implies that these can still be im-
portant for sun bear conservation, if there is undisturbed forest nearby that supports a source
population. Sun bears are known to persist in logged-over areas (Wong et al. 2004, Linkie et al.
2007), but fire causes much more severe damage to forest integrity than selective logging (Slik
et al. 2002). Most sun bear fruit resources are tree-borne (versus shrubs or understory plants)
and regeneration of this food resource after a fire probably takes several decades, if not longer.
Primary rainforest in Indonesia can rapidly be converted to savanna grasslands if af-
fected by repeated fires (Goldammer 1999). Fire-return intervals of less than 90 years can
eliminate rainforest species, whereas intervals of less than 20 years may eradicate trees entirely
Synthesis and conclusions 171
(Cochrane et al. 1999). Many of these fire-disturbed areas have seen further fire damage dur-
ing smaller drought events in subsequent years (2002, 2004), or have been converted to other
uses altogether. Dennis and Colfer (2006) calculated that 70% of forest initially damaged by fire
and drought during the 1982–83 El Niño event was classified as non-forest by 2000, follow-
ing a degradation pathway driven by successive government policies starting with commercial
logging, followed by government sponsored transmigration schemes, then by timber and oil
palm plantations and, finally, the devastating fires of 1998. A similar, though faster, trajectory of
conversion of degraded forests to plantations or wasteland was evident for many fire-affected
forest areas after 1997-1998 (Fuller et al. 2004, Miettinen et al. 2011).
Thus remaining sun bear habitat has become increasingly fragmented, impairing post-
fire immigration of bears from other habitat blocks. Recovery of populations in forest areas
disturbed by severe ecological catastrophes, such as the combined effects of fires, fragmenta-
tion and fruiting failure discussed in this thesis, will now in many cases have to rely on recruit-
ment from within remaining patches of less-disturbed habitat. Unfortunately, with the current
minimal capacity to prevent or control forest fires in Indonesia, it seems unlikely in the near
future that fire threat to forest areas will be reduced.
Importance of monitoring population trends in the
face of increasing conservation threats
Sun bears are now listed as Vulnerable on the IUCN Red List (Fredriksson et al. 2008).
Poaching for bears and their body parts is reaching alarming rates in mainland Southeast Asia
(Foley et al. 2011). Although current poaching rates are lower in Sumatra and Borneo, where
the main threat to sun bear populations comes from habitat loss, it is probable that the con-
tinuing economic growth in the primary markets for bear products, namely China, will lead to
increased poaching in Indonesia, particularly as mainland populations become increasingly de-
pleted. In this scenario, the track record of the conservation institutions in Indonesia respon-
sible for species protection and control of wildlife trade does not provide much reassurance
that they would be able to mitigate this threat.
Monitoring of sun bear population trends in key conservation areas will become the
next imperative. Results from our research show that changes in sun bear relative abundance
can be monitored using relatively simple and inexpensive sign surveys. At the moment, six me-
dium sized to large (1,000-10,000 km2) protected areas have been designated in Kalimantan,
still consisting of good quality habitat. Kalimantan still holds the largest contiguous expanse
of forest in the Indo-Malayan realm, primarily in the mountainous interior of the island. These
Chapter 8172
remote, inaccessible, large protected areas provide the most secure future prospect for sun
bears and other wildlife. Indonesia, with its remaining forests on Sumatra and Kalimantan,
currently covers some 45% of the sun bears distribution range, making it the most important
country for the conservation of this bear species.
ReferencesAppanah, S. (1985). General flowering in the climax rain forests of South-east Asia. Journal of Tropical Ecol-
ogy 1:225-240.
Cannon, C. H., L. M. Curran, A. J. Marshall, and M. Leighton. (2007). Long-term reproductive behaviour of
woody plants across seven Bornean forest types in the Gunung Palung National Park (Indonesia):
suprannual synchrony, temporal productivity and fruiting diversity. Pages 956-969. Wiley-Blackwell.
Chen, J., Saunders, S.C., Crow, T.R., Naiman, R.J., Brosofske, K.D., Mroz, G.D., Brookshire, B.L., and Franklin,
J.F. (1999). Microclimate in forest ecosystem and landscape ecology. Bioscience 49, 288–297.
Clark D.A., Brown S., Kicklighter D., Thommlinon J.R., and N. J. (2001). Net primary production in tropi-
cal forests: an evaluation and synthesis of existing field data. Ecological Applications 11:371–384.
Cochrane, M. A., A. Alencar, M. D. Schulze, C. M. J. Souza, D. C. Nepstad, P. Lefebvre, and E. A. Davidson. (1999).
Positive feedbacks in the fire dynamic of closed canopy tropical forests. Science 284:1832-1835.
Collins, N. M. (1980). The effect of logging on termite (Isoptera) diversity and decomposition processes in
lowland dipterocarp forest. Tropical Ecology and Development:113-121.
Costello, C., D. E. Jones, R. M. Inman, K. H. Inman, B. Thompson, and H. B. Quigley. (2003). Relationship
of variable mast production to American black bear reproductive parameters in New Mexico.
Ursus14:1-16.
Cunningham, S. C., W. B. Ballard, L. M. Monroe, M. J. Rabe, and K. D. Bristow. (2003). Black bear habitat use in
burned and unburned areas, central Arizona. Wildlife Society Bulletin 31:786-792.
Curran, L.M., and Leighton, M. (2000). Vertebrate responses to spatiotemporal variation in seed production
of mast-fruiting dipterocarpaceae. Ecological Monographs 70, 101-128.
Curran, L. M., I. Caniago, G. D. Paoli, D. Astianti, M. Kusenti, C. E. Nirarita, and H. Haeruman. (1999). Impact
of El Nino and logging on canopy tree recruitment in Borneo. Science 286:2184-2188.
Dennis, R.A., and Colfer, C.P. (2006). Impacts of land use and fire on the loss and degradation of lowland
forest in 1983–2000 in East Kutai District, East Kalimantan, Indonesia. Singapore Journal of Tropical
Geography 27, 30-48.
Elowe, K. D. and W. E. Dodge. (1989). Factors affecting black bear reproductive success and cub survival.
Journal of Wildlife Management 53:962-968.
Synthesis and conclusions 173
Foley, K.E., Stengel, C.J., and Shepherd, C.R. (2011). Pills, Powders, Vials and Flakes: the bear bile trade in Asia
(Petaling Jaya, Selangor, Malaysia, TRAFFIC Southeast Asia).
Frederick, C., R. Kyes, K. Hunt, D. Collins, and S. K. Wasser. (2012). Reproductive timing and aseasonality in
the sun bear (Helarctos malayanus). Journal of Mammalogy 93.
Fredriksson, G.M., and Nijman, V. (2004). Habitat-use and conservation of two elusive ground birds (Carpo-
coccyx radiatus and Polyplectron schleiermacheri) in Sungai Wain protection forest, East Kalimantan,
Indonesian Borneo. Oryx 38, 297-303.
Fuller, D.O., Jessup, T.C., and Salim, A. (2004). Loss of forest cover in Kalimantan, Indonesia, since the 1997-
1998 El Niño. Conservation Biology 18, 249-254.
Gathorne-Hardy, F.J., Jones, D.T., and Syaukani (2002). A regional perspective on the effects of human distur-
bance on the termites of Sundaland. Biodiversity and Conservation 11, 1991-2006.
Gittleman, J.L., and Harvey, P.H. (1982). Carnivore home-range size, metabolic needs and ecology. Behavio-
ral Ecology and Sociobiology 10, 57-63.
Goldammer, J. G. (1999). Forest on fire.Science 284:1782-1783.
Gompper, M.E., and Gittleman, J.L. (1991). Home range scaling: intraspecific and comparative trends. Oe-
cologia 87, 343-348.
Hanya, G., M. Matsubara, H. Sugihara, S. Hayakawa, S. Goto, T. Tanaka, J. Soltis, and N. Noma. (2004). Mass
mortality of Japanese macaques in a western coastal forest of Yakushima. Ecological Research
19:179-188.
Harrison, R. D. (2000). Repercussions of El Niño: drought causes extinction and the breakdown of mu-
tualism in Borneo. Proceedings of the Royal Society of London Series B-Biological Sciences
267:911-915.
Harrison, R. D. (2001). Drought and the consequences of El Niño in Borneo: a case study of figs. Population
Ecology 43:63-75.
Hoffmann, A.A., Hinrichs, A., and Siegert, F. (1999). Fire damage in East Kalimantan in 1997/98 related to
land use and vegetation classes: Satellite radar inventory results and proposal for further actions.
IFFM-SFMP Report No.1a (Samarinda, East Kalimantan, MOFEC, GTZ and KfW).
Janzen, D. H. (1974). Tropical blackwater rivers, animals, and mast fruiting by the dipterocarpaceae. Bio-
tropica 6:69-103.
Jones, D.T., Susilo, F.X., Bignell, D.E., Hardiwinoto, S., Gillison, A.N., and Eggleton, P. (2003). Termite assem-
blage collapse along a land-use intensification gradient in lowland central Sumatra, Indonesia. Jour-
nal of Applied Ecology 40, 380-391.
Jonkel, C. J. and I. Mc.Cowan. (1970). The Black Bear in the Spruce-Fir forest. Wildlife Monographs 27:1-57.
Chapter 8174
Kikkawa, J., and Dwyer, P.D. (1992). Use of scattered resources in rain forest of humid tropical lowlands.
Biotropica 24, 293-308.
Langner, A. and F. Siegert. (2009). Spatiotemporal fire occurrence in Borneo over a period of 10 years.
Global Change Biology 15:48-62.
Linkie, M., Dinata, Y., Nugroho, A., and Haidir, I.A. (2007). Estimating occupancy of a data deficient mamma-
lian species living in tropical rainforests: Sun bears in the Kerinci Seblat region, Sumatra. Biological
Conservation 137, 20-27.
McConkey, K. and M. Galetti. (1999). Seed dispersal by the sun bear (Helarctosmalayanus) in Central Borneo.
Journal of Tropical Ecology 15:237-241.
McLoughlin, P.D., Case, R.L., Gau, R.J., Ferguson, S.H., and Messier, F. (1999). Annual and seasonal movement
patterns of barren-ground grizzly bears in the central Northwest Territories. Ursus 11, 79-86.
McLoughlin, P.D., Ferguson, S.H., and Messier, F. (2000). Intraspecific Variation in Home Range Overlap with
Habitat Quality: A Comparison among Brown Bear Populations. Evolutionary Ecology 14, 39-60.
McNab, B. K. (1963). Bioenergetics and the determination of home range size. American Naturalist
97:133-140.
McNab, B. K. (1983). Ecological and behavioral consequences of adaptation to various food resources.
Pages 664-697 in J. F. Eisenberg and D. G. Kleiman, editors. Advances in the study of mammalian
behavior. American Society of Mammalogists Special Publication 7.
Miettinen, J., Shi, C., and Liew, S.C. (2011). Deforestation rates in insular Southeast Asia between 2000 and
2010. Global Change Biology 17, 2261-2270.
Nomura, F., Higashi, S., Ambu, L., and Mohamed, M. (2004). Notes on oil palm plantation use and seasonal
spatial relationships of sun bears in Sabah, Malaysia. Ursus 15, 227–231.
O’Brien, T.G., Kinnaird, M.F., Nurcahyo, A., Prasetyaningrum, M., and Iqbal, M. (2003). Fire, demography and
the persistence of siamang (Symphalangus syndactylus: Hylobatidae) in a Sumatran rainforest. Ani-
mal Conservation 6, 115-121.
Ratnayeke, S., van Manen, F.T., and Padmalal, U.K.G.K. (2007). Home Ranges and Habitat Use of Sloth Bears
Melursus ursinus inornatus in Wasgomuwa National Park, Sri Lanka. Wildlife Biology 13, 272-284.
Redford, K. H. (1987). Ants and termites as food. Patterns of Mammalian Myrmecophagy.Pages 349-397 in
H. H. Genoways, editor. Current Mammalogy. Plenum press, Nebraska.
Sakai, S., K. Momose, T. Yumoto, T. Nagamitsu, H. Nagamasu, A. A. Hamid, and T. Nakashizuka. (1999). Plant
reproductive phenology over four years including an episode of general flowering in a lowland
dipterocarp forest, Sarawak, Malaysia. American Journal of Botany 86:1414-1436.
Schaik, C. P. v., (1986). Phenological changes in a Sumatran rain forest. Journal of Tropical Ecology 2:327-347.
Synthesis and conclusions 175
Schaik, C. P. v., J. W. Terborgh, and S. J. Wright .(1993). The phenology of tropical forests: adaptive significance
and consequences for primary consumers. Annual Review of Ecology and Systematics 24:353-377.
Schwarzenberger, F., G. M. Fredriksson, K. Schaller, and L. Kolter. (2004). Fecal steroid analysis for monitoring
reproduction in the sun bear (Helarctos malayanus). Theriogenology 62:1677-1692.
Siegert, F., Ruecker, G., Hinrichs, A., and Hoffmann, A.A. (2001). Increased damage from fires in logged for-
ests during droughts caused by El Niño. Nature 414, 437-440.
Slik, J.W.F., Verburg, R.W., and Kessler, P.J.A. (2002). Effects of fire and selective logging on the tree species
composition of lowland dipterocarp forest in East Kalimantan, Indonesia. Biodiversity & Conser-
vation 11, 85-98.
Slik, J. W. F. and K. A. O. Eichhorn. (2003). Fire survival of lowland tropical rain forest trees in relation to stem
diameter and topographic position. Oecologia137:446-455.
Sork, V. L. (1993). Evolutionary ecology of mast-seeding in temperate and tropical oaks (Quercus spp.).
Vegetatio107/108:133-147.
van Nieuwstadt, M.G.L. (2002). Trial by fire- Postfire development of a dipterocarp forest. Ph.D. thesis.
University of Utrecht, Netherlands.
Walsh, R. P. D. (1996). Drought frequency changes in Sabah and adjacent parts of northern Borneo since
the late nineteenth century and possible implications for tropical rain forest dynamics. Journal of
Tropical Ecology 12:385-407.
Walsh, R. P. D. and D. M. Newbery. (1999). The ecoclimatology of Danum, Sabah, in the context of the
world’s rainforest regions, with particular reference to dry periods and their impact. Philosophical
Transactions of the Royal Society of London Series B-Biological Sciences 354:1869-1883.
Webster, P. J. and T. N. Palmer. (1997). The past and the future of El Niño. Nature 390:544-564.
Wich, S. A. and C. P. van Schaik. (2000). The impact of El Niño on mast fruiting in Sumatra and elsewhere in
Malesia. Journal of Tropical Ecology 16:563-577.
Wich, S., R. Buij, and C. van Schaik. (2004). Determinants of orangutan density in the dryland forests of the
Leuser Ecosystem. Primates 45:177-182.
Wich, S. A., E. R. Vogel, M. D. Larsen, G. M. Fredriksson, M. Leighton, C. P. Yeager, F. Q. Brearley, C. P. van Schaik,
and A. J. Marshall. (2011). Forest Fruit Production Is Higher on Sumatra than on Borneo. PLoS
ONE 6: Published online 2011 June 2028.doi: 2010.1371/ journal.pone.0021278.
Wong, S.T., Servheen, C., and Ambu, L. (2004). Home range, movement and activity patterns, and bedding
sites of Malayan sun bears, Helarctos malayanus in the rainforest of Borneo. Biological Conserva-
tion 119, 168-181.
Chapter 8176
Wong, S.T., Servheen, C., Ambu, L., and Norhayati, A. (2005). Impacts of fruit production cycles on Malayan
sun bears and bearded pigs in lowland tropical forest of Sabah, Malaysian Borneo. Journal of Tropi-
cal Ecology 21, 627–639.
Wood, T. G. and W. A. Sands (1978). The role of termites in ecosystems. Pages 245-292 in M. V. Brian, editor.
Production ecology of ants and termites. Cambridge University Press, Cambridge, UK.
Woodroffe, R., and Ginsberg, J.R. (1998). Edge effects and the extinction of populations inside protected
areas. Science 280, 2126-2128.
Wright, S. J., C. Carrasco, O. Calderon, and S. Paton. (1999). The El Niño Southern Oscillation: variable fruit
production, and famine in a tropical forest. Ecology 80:1632-1647.
Acknowledgements
There are many people I would like to thank for helping, supporting and stimulating me
throughout my research on sun bears and the conservation purpose this developed into. First
of all are my parents, Einar and Zosia, who encouraged me during my initial biology endeavors
and continued their enthusiastic support throughout the following 15 years, most of which I
spent in Indonesia. Your ongoing interest and encouragement means a lot!
Once my interest in tropical wildlife ecology had become rooted, Dr. Herman Rijksen
is most to be thanked (or cursed...) for the route my life has taken. Herman initially encouraged
me in 1994 to do my masters’ fieldwork on orangutans in Kalimantan, during which I had my
first observation of two sun bears in the wild raiding a stingless bee’s nest high up in a giant
Dipterocarp tree. Subsequently Herman supported and advised me through many different
Indonesian conservation challenges, starting in Sungai Wain but later in North Sumatra and
Aceh, and I am grateful for all his pep talks and advise.
This fist sun bear encounter spurred my interest in this species, especially as I could
not find any information on field studies carried out on this bear species anywhere in the wild.
Once my interest in sun bear’s had been triggered, Dr. Dave Garshelis has been instrumental in
many ways and I am grateful for his generous guidance and advice. Dave encouraged me, when
I first contacted him in 1996 about sun bear research, to learn more about bears in general
before embarking on a sun bear field study. Dave put me in touch with Prof. Jon Swenson, who
then invited me to visit the Scandinavian Brown Bear project in Dalarna, Sweden, to learn the
basics about various other aspects of bear fieldwork and telemetry. In Sweden I was welcomed
by Sven Brunberg, who enthusiastically allowed me to join a variety of bear research activities,
from aerial telemetry, moose follows, to sneeking up on a brown bears in the beautiful boreal
forest. The months I spent with the Scandinavian Bear Project were invaluable training and
preparation for studying sun bears in Indonesia.
I would like to thank the Indonesian Institute of Sciences (LIPI) for granting me permis-
sion to study sun bears in Kalimantan, especially Ibu Ina Syarief and Ibu Krisbiwati for help with
arranging the necessary permits and letters. I would like to thank Dr. Willie Smits for putting
Sungai Wain on the map by releasing orangutans there and facilitating my initial research there,
as well as building the nice research camps that became my home for many years. I would like
to thank the Tropenbos Foundation, especially Tinus de Kam, for collaboration and support
Acknowledgements180
with the initial Sungai Wain management plan we wrote in 1998, and for establishment of the
permanent sample plots. I would like to thank the Wanariset Herbarium, especially Dr. Kade
Sidiyasa, Ambriansyah, Arifin and Insyah for help with plant identification. Balai Penelitian Kehu-
tanan (BPK), Bapak Boen Purnama and Bapak Selamat Gadaz, are gracefully thanked for their
collaboration. I would also like to express my gratitude to the former Mayor of Balikpapan,
Bapak Imdaad Hamid, and Bapak Saleh Basrie for their enthusiasm to establish a new manage-
ment system for the Sungai Wain forest.
I would gratefully like to acknowledge financial support for the research from the
Tropenbos Foundation, the Gibbon Foundation, the American Zoo and Aquarium Associa-
tion, the Balikpapan Orangutan Society, the World Society for Protection of Animals (Victor
Watkins), the University of Amsterdam, the van Tienhoven Foundation, Virbac, the Artis Zoo
(Peter Klaver), the International Bear Association, the Bevins Foundation, the Stichting Doctor
Catharina van Tusschenbroek Fonds, and the Great Bear Foundation.
During many years in the field several research assistants, especially Trisno, Lukas and
Dami, provided invaluable help and I thank them for their dedication, hard fieldwork and com-
panionship. I would like to thank the fire teams and subsequent coal fire extinguishing teams
who helped between 1998-2001 to save the Sungai Wain forest, as well as Willie Smits and Al
Whitehouse for financial and logistical support for the fire extinguishing efforts. I would es-
pecially like to thank Agusdin, Babam, Iman, Juahir and Parmin for all their help with the forest
protection work, especially during the initial years. I would also like to thank a large number of
villagers from Sungai Wain for helping as porters and bringing in logistical supplies to the forest,
especially Almarhum Pak Yasin.
In Balikpapan a number of people provided invaluable help and friendship, particularly
Judy O’Dwyer, Sam and Yanti are thanked warmly for all their help with delivering fruit and food
supplies for our bears during the fires and a comfortable place to sleep in Balikpapan where
I could regain energy. I would also like to thank Jane Vincent who took care of sun bear cub
Schizo for several months before we could take him to the forest, as well as for providing a
welcome place for me to stay in Balikpapan. The Unocal School and Peter Karsono are thanked
for looking after sun bear Ganja for some months until she got fed up being pestered by the
gang of gibbons.
Once my sun bear fieldwork had started to take shape, I want to thank Prof. Steph
Menken for his offer to do a PhD at the University of Amsterdam. I would especially like to
thank him for his patient reminders over the years to finish it, as I became caught up with more
and more conservation work in Kalimantan and Sumatra.
Acknowledgements 181
I would also like to thank various researchers for their collaboration over the many
years working on sun bear ecology. Dr. Homathevi Rahman is thanked for the mammoth
task of identifying more than 3000 termite samples whilst sitting in the forest. Dr. Decha
Wiwatwittaya from Kasetsart University, Bangkok, Thailand is thanked for identification of ant
samples. I would like to thank Live Solbrekken, Anders Endrestøl, and Karen Marie Matthiesen
from the University in Ås, Norway, for their hard fieldwork in Sungai Wain in 2001. I want to
thank Claire Palmer and Wiwit Sastramidjaja for their interest in sun bear research and for
their help with coordinating and carrying out the sun sign transect work in 2005 and 2010,
not always under easy conditions. I would like to thank Lydia Kolter and Rebecca Riese for
collaboration on sun bear nutrition, as well as Franz Schwartzenberger for collaboration on
sun bear reproductive patterns. I would like to thank Ente Rood and Matthew Nowak for
assistance and advise on various statistical matters and Dandy Irawan and Jurgen van Gessel
with translations of the summaries to Indonesian and Dutch, and Corien Smit for the lay-out
of this thesis.
I would also like to thank students from Universitas Mulawarman (UNMUL) in Sama-
rinda in particular Wiwien Effendi, Joned, Eko and Ali Mustofa as well as their supervisors Dr.
Chandradewana Boer and Dr. Agung Sardjono. I want to thank Nunuk Kasyanto for his ongoing
friendship, visits to the forest, and the NGO LORIES for helping with various programmes in
the forest and conservation awareness campaigns for the Sungai Wain forest in the early days.
I am very grateful for all the support, advise and help Dave Garshelis provided over all
the years, ranging from training on trapping bears to telemetry equipment and various visits to
the forest, as well the Garshelis family for providing as a welcome home in Minnesota during a
period of writing up, and to Judy, Daren and Brian for visiting the forest. Many thanks as well to
Ruth and Laura Pierce for their warm hospitality in Grand Rapids and letting me stay at your
home, and all the wonderful staff at the DNR especially Karen Noyce and Sharon, Nancy and
July for showing me around Minnesota!
I would like to thank Mark van Nieuwstadt for being such a nice ‘housemate’ in Camp
Djamaludin where we lived together for quite some time, as well as for many stimulating dis-
cussions. I would also like to thank fellow researchers Martjan Lammertink, Vincent Nijman,
Ferry Slik, Karl Eichhorn and Danny Cleary who spent some of their research time in Sun-
gai Wain for interesting discussions and collaboration. Fellow Asian bear researchers Siew Te
Wong, Rob Steinmetz, Mei-Hsiu Hwang, and Dave Augeri are also thanked for their nice visits
to Sungai Wain, useful discussion and collaboration over the years, and sharing experiences and
difficulties studying Asian bears.
Acknowledgements182
I very much enjoyed the various visits of my friends and family over the years I lived
in the forest in Sungai Wain, especially Vincent Nijman, Erik Meijaard and Graham Usher
with whom I had many good talks and walks through the forest. The visits by Sven Brunberg,
Darin Collins, Cheryl Fredericks, Anja Hoffman, Georg Buchholz, Frank Momberg, Resit Sözer,
Danielle Kreb, Teguh, Rani, Daniel and Chris, Timbul, Nunuk, Cabok, Gigih, Serge Wich and Tine
Geurts were much appreciated. My close friends Arlette and Jan Jaap, Bas Huijbregts and Jurgen
van Gessel are thanked for their fun forest visit and subsequent holidays. The visit by the Fami-
lie de Vos (Bunkie, Lucy, Claire and Fiona) to the forest in the early days is also fondly remem-
bered. I would like to thank my parents Einar and Zosia for their visits, as well as my brother
Hjalmar (and Martijn) who made me laugh so many times during his visits and hikes through
the forest. Also many thanks to my friends in Amsterdam, with whom I have shared many of
my bear stories and forest tribulations over the years and with whom I could revive socially,
especially Eva and Frank, Arlette and Jan Jaap, Mark and Marchien, Jurgen, and Claire and family.
Although no longer with us, I would also like to express my warm feelings and gratitude
to my grandparents in Sweden and Poland, where I spent some time writing up intermittently
during annual visits when back from the forest, especially my grandmothers Margit Fredriksson
and Gabriela Biernacka.
Bvll is thanked warmly for all his wonderful illustrations that have helped so much with
the conservation awareness campaigns for the Sungai Wain forest and all our subsequent sun
bear education work, as well as the wonderful cover and illustrations in this thesis!
I would especially like to thank my wonderful companion and partner Graham Usher.
Your many visits to the forest in the early years, and your ongoing support, encouragement,
patience, enthusiasm throughout all aspects of my work with the bears, conservation of the
forest, and subsequent years working on the education center, as well as many other conserva-
tion challenges are immensely appreciated! Without you I would probably not have achieved
half! I would also like to thank you very much for all technical and GIS help you have provided,
all the maps in this thesis, and for reading and commenting on many parts of this thesis.
And last but certainly not least, immense gratefulness towards the wonderful sun bears
that allowed me to get insight into their ecology and behavior, especially Ganja, Ucil, Schizo and
si Kecil. Life in the forest never had a dull moment when they were around. The many years
we had together in the forest include some of my happiest moments. I wish I could have done
more for them and all other sun bears!
Summary
The Malayan sun bear, Helarctos malayanus, smallest of the eight extant bear species,
is distributed throughout Southeast Asia including the large islands of Sumatra and Borneo.
Research on sun bears in the wild, including those in Kalimantan (Indonesian Borneo), was
non-existent before the work that is presented in this thesis commenced in 1997, in a small
lowland reserve in East Kalimantan. Apart from a few anecdotal records, virtually nothing was
known about basic aspects of sun bear ecology and they were listed as ‘Data Deficient’ by the
IUCN Red list at the time. In order to fill in some of the bigger gaps of knowledge on this spe-
cies, data were collected on various aspects of sun bear behaviour, ecology, and conservation
during 5 years of intensive research from mid 1997 until mid 2002, with further surveys carried
out in 2005 and 2010.
During the early stages of this study, large-scale forest fires, related to severe drought
in the region triggered by recurring El Niño Southern Oscillation (ENSO) events, affected
millions of hectares of forest in Kalimantan, including the reserve where this study had com-
menced. Between 1997 and 2006, a total of 16.2 Mha of Borneo’s landmass (21% of the total
land surface area) have been affected by fires, a considerable percentage of this being forested
areas. Prompted by the scale of this environmental disaster, part of my research focused on
investigating the effects of these fires on the ecology and conservation of sun bears.
ENSO events, besides causing drought conditions in the region, have also been linked
to mast fruiting in Southeast Asia, especially the eastern parts of Borneo. The canopy and
emergent trees of these forests are dominated by trees of the Dipterocarpaceae, which display
a unique reproductive pattern. Flowering and fruiting occurs at intervals of 2-10 years with
little or no reproductive activity in between, and a large proportion of other trees covering
varied taxonomic groups and flowering syndromes, flower and fruit synchronously with these
dipterocarps. These masting events provide a brief period of high fruit availability, aimed at sati-
ating seed predators, but also providing a glut of nutritious fruits. Through monthly phenology
surveys of more than 600 trees, we documented that sun bear fruit availability decreased from
13 trees ha-1 fruiting month-1 during the mast fruiting to only 1.6 trees ha-1 during the prolonged
inter-mast period.
Sun bears were found to become almost completely frugivorous during these short
periods (approx. 2 months) of high fruit availability. During this study, sun bears were found
Summary186
to feed on at least 115 fruit species, with the families Moraceae, Burseraceae and Myrtaceae
contributing more than 50% to the sun bear fruit diet, whereas Ficus spp. (Moraceae) were
the main fallback fruit during the prolonged intermast. Most sun bear fruit species only fruited
during the rare masting events or displayed supra-annual fruiting patterns, indicating sporadic
availability of favored fruits. During the prolonged intermast period, subsequent to the fire
event, sun bears switched to an insectivorous diet, dominated by termites, ants, beetles and
beetle grubs, and cockroaches.
Two female bears captured for telemetry studies in the unburned forest core, 16
months after the fire event and well into the inter-mast period, showed signs of serious un-
dernourishment. Both females had small cubs at the time, probably exacerbating their already
weakened condition. The emaciated appearance of the female sun bears suggests that pro-
longed survival solely on insect resources was insufficient and that energy requirements were
not met. The predation of one of the bears by a large python might have been related to the
poor nutritional condition of the bear, possibly rendering the bear less effective in fighting off
an attack or having a lowered vigilance.
To gain insight into the movement and activity patterns of sun bears, three wild and
two rehabilitated-released female bears were fitted with motion-sensitive VHF radio-collars.
Three of these bears were tracked continuously for 1-3 years during 1999-2003. Home range
sizes (12-month period) were 4-5 km2 (95% MCP and 95% fixed kernel) with considerable
home range overlap. These relatively small home ranges may have been related to a diet com-
posed predominantly of insects, as no mast fruiting event occurred during the period of te-
lemetry study. Activity monitoring revealed that sun bears were predominantly diurnal and
crepuscular throughout the year with activity commencing about 0.5 h before sunrise and
lasting until 2.5h after sunset, and low levels (20-30%) of activity at night. Bears were active
61.6% of the day (14.8 ± 2.3 hours), on average, with higher levels of activity associated with
insect feeding than fruit feeding.
Forest fires and drought caused extreme mortality of sun bear fruit trees, with close to
an 80% reduction in densities of fruit trees in burned areas from 167 ± 41 (SD) fruit trees ha-1
in unburned forest to 37 ± 18 fruit trees ha-1 in burned forest. In addition a 44% reduction in
species diversity of sun bear fruit trees was measured some 3 years after the fire event. Densi-
ties of hemi-epiphytic figs, an important fruit species during the prolonged intermast period,
declined by 95% in burned forest.
Sun bear use of burned forest areas was monitored through repeated sign surveys (i.e.
claw marks, broken termite mounds, diggings) over a period of 10 years, with transects carried
Summary 187
out in adjacent primary and burned forest areas. Densities of sun bear sign were close to zero
in burned forest areas for several years after the fire, but by 2010 had increased to 28.0 ± 12.9
(SD) sign/ha, indicating re-colonization by sun bears. Sign densities in adjacent unburned forest
remained stable over the years, averaging 41.6 ± 11.6 (SD) sign/ha. Densities of sun bear sign
were still 35% lower in burned forest 12 years after the fire event, linked to a paucity of certain
types of sun bear foods, especially fruiting trees and above-ground termite colonies. Steady
recolonization of sun bears into these once-burned areas indicates the recovery potential of
these areas as sun bear habitat, as long as source population of sun bears are present in adja-
cent unburned forest.
Subsequent to the drought and fire event, we carried out repeated interviews with
farmers in 5 communities situated along the edge of the Sungai Wain Protection Forest to
investigate sun bear crop raiding. Results from these interviews indicated that crop damage
caused by sun bears subsequent to the forest fires was higher than in years prior to the ENSO
and fire event. The main source of antagonism toward bears resulted from the damage they
caused to stands of old coconut trees (Cocos nucifera), frequently killing the trees. This prompt-
ed farmers to seek removal of the bears. Bear damage to annual crops generally spurred a less
hostile reaction. Experiments with metal sheeting affixed to the trunks of coconut trees to
deter climbing by bears were successful, at least in the short term (≥3 years). Inexpensive and
easily applicable crop-protection devices such as this could help protect sun bears in the future,
as increased human-bear conflicts are anticipated due to rapid human population growth, una-
bated forest destruction and fragmentation, and increased susceptibility of remaining forests
to future fires.
Habitat degradation due to large-scale forest fires, combined with a prolonged fruit-
ing low after the ENSO event, put large strains on the sun bear population in the area. As sun
bear habitat is continuing to be destroyed at an alarming rate in Borneo, even small reserves
are becoming more important for the conservation of this species. Behavioural characteristics
such as a relatively small home range size, bounded entirely within the small reserve where this
research was carried out, and avoidance of areas with human disturbance (trails, burned forest)
suggest that small reserves can still be valuable for the conservation of sun bears. Long-term
persistence of sun bears in these areas will depend on prevention of poaching, forest degrada-
tion from fires, and maintaining connectivity to other forested areas.
Samenvatting
De Maleise zonbeer, Helarctos malayanus, is de kleinste van de huidige acht beersoor-
ten. De zonbeer komt voor door heel Zuidoost-Azië, ook op de grote eilanden van Sumatra en
Borneo. Het onderzoek dat ik in dit proefschrift presenteer ging in 1997 van start in een klein
laaglandreservaat in Oost-Kalimantan. Voor die tijd was er nog geen veldonderzoek gedaan
naar zonberen in het wild; ook niet naar die in Kalimantan, het Indonesisch deel van Borneo.
Behalve de informatie uit een paar anekdotische verslagen was er nagenoeg niets bekend van
de fundamentele aspecten van de ecologie van de zonbeer. De soort stond toen nog in de
categorie ‘Data Deficient’ (‘onvoldoende gegevens’) op de Rode Lijst van de IUCN. Om een
voornaam deel van de ontbrekende kennis over de zonbeer aan te vullen, hebben we in het
kader van deze studie gedurende vijf jaar (van halverwege 1997 tot halverwege 2002) intensief
data verzameld rond verschillende aspecten van het gedrag, de ecologie en het behoud van de
zonbeer. Verder onderzoek is uitgevoerd in 2005 en in 2010.
Ten tijde van de eerste fase van deze studie had de regio te maken met grootschalige
bosbranden, veroorzaakt door ernstige droogte die gerelateerd was aan herhaaldelijke El Niño
Southern Oscillation (ENSO)-verschijnselen. De branden tastten in Kalimantan miljoenen hec-
tare bos aan, inclusief het reservaat waar het onderzoek plaatsvond. Tussen 1997 en 2006 is in
totaal 16,2 miljoen hectare van Borneo’s landmassa getroffen door brand; dat is 21 procent van
de totale landoppervlakte van het eiland. Een groot gedeelte hiervan bestond uit bosgebieden.
Vanwege de grote schaal van deze milieuramp heb ik een deel van mijn studie gewijd aan het
onderzoeken van de effecten van de branden op de ecologie en het behoud van zonberen.
De ENSO-verschijnselen veroorzaken niet alleen droogte, maar spelen ook een rol
bij het voorkomen van mast fruiting (fenomeen waarbij grote hoeveelheiden bomen gelijktijdig
fruit produceren) in Zuidoost-Azië, in het bijzonder in de oostelijke delen van Borneo. Het
bladerdak en de emergente bomen in de bossen hier worden gedomineerd door bomen uit de
familie van de Dipterocarpaceae die een uniek regeneratief patroon laten zien. De bloei en het
dragen van vruchten doen zich voor met intervallen van 2 tot 10 jaar; in de tussenperioden
vertonen deze bomen geen of bijna geen voortplantingsactiviteit. De bloei en het dragen van
fruit door een groot deel van de andere bomen – afkomstig uit verschillende taxonomische
groepen met gevarieerde bloeiverschijnselen – verloopt hier synchroon met deze Dipterocar-
paceae. Mast fruiting voorziet daardoor in een korte periode waarin fruit in zeer grote mate
Samenvatting190
beschikbaar is; de functie hiervan is zaadpredatoren te verzadigen en voorziet ook in een
overvloed aan voedzame vruchten. Door maandelijks fenologisch onderzoek aan meer dan
600 bomen hebben we kunnen vastleggen dat de beschikbaarheid van fruit voor de zonberen
afnam van 13 fruitende bomen per hectare/maand tijdens de mast fruiting-periode tot slechts
1,6 bomen die fruit produceerden per hectare/maand tijdens de langdurige inter-mast-periode.
Het bleek dat zonberen bijna compleet frugivoor worden tijdens deze korte perioden
van ongeveer 2 maanden waarin het fruit zo rijkelijk aanwezig is. In deze studie stelden we vast
dat zonberen zich voeden met minstens 115 verschillende soorten fruit. De families Moraceae,
Burseraceae en Myrtaceae dragen voor meer dan 50 procent bij aan het dieet van de zonberen;
de beren vielen in de langdurige inter-mast-periode vooral terug op het fruit van het genus Ficus
spp. (Moraceae). De meeste boomsoorten waarvan de zonberen het fruit eten droegen alléén
fruit tijdens de zeldzame mast fruiting-periodes óf vertoonden fruitpatronen die zich uitstrek-
ken over meer jaren; dat duidt op sporadische beschikbaarheid van het favoriete fruit van de
zonberen. Tijdens de langdurige inter-mast-periode, volgend op de bosbranden, schakelden de
zonberen over op een dieet van insecten, vooral termieten, mieren, kevers en keverlarven, en
kakkerlakken.
Twee vrouwelijke beren die we vingen voor een telemetriestudie in het niet-verbrande
hart van het bos vertoonden tekenen van ernstige ondervoeding, 16 maanden na de branden
en diep in de inter-mast-periode. Beide vrouwtjes hadden op dat moment jonge welpen, waar-
door ze waarschijnlijk verder verzwakt waren. De uitgemergelde verschijning van de beren
suggereert dat een dieet van niets anders dan insecten gedurende een langere periode niet
afdoende is en niet in de energiebehoefte van de beren voorziet. De predatie van een van deze
vrouwtjesberen door een grote python zou gerelateerd kunnen zijn aan haar slechte conditie;
mogelijk kon zij de aanval minder effectief weerstaan of was ze minder waakzaam.
Om inzicht te krijgen de bewegings- en activiteitenpatronen van zonberen, zijn drie
wilde en twee vrijgelaten gerehabiliteerde vrouwelijke beren uitgerust met VHF-radiokragen
met bewegingssensors. Drie van deze beren zijn continu gevolgd gedurende 1 tot 3 jaar in de
periode van 1999 tot 2003. Hun home range omvatte (in een periode van 12 maanden) 4 tot
5 km2 (95 procent Minimum Convex Polygon en 95 procent fixed kernel) met een aanzienlijke
onderlinge overlap van de home ranges. De relatief kleine omvang van de home ranges kan
gerelateerd zijn aan een dieet dat voornamelijk bestond uit insecten, omdat zich in de periode
van de telemetriestudie geen mast fruiting voordeed. Het monitoren van de activiteit toonde
aan dat zonberen het hele jaar door hoofdzakelijk dag- en schemerdieren zijn. Ze worden
ongeveer een half uur voor zonsopgang actief en blijven dat tot 2,5 uur na zonsondergang. Het
Samenvatting 191
activiteitsniveau ’s nachts is laag (20 tot 30 procent). De beren waren gemiddeld 61,6 procent
van de dag actief (14,8 ± 2,3 uur); hogere activiteitsniveaus hingen sterker samen met het eten
van insecten dan met het eten van fruit.
De bosbranden en de droogte veroorzaakten extreme sterfte van fruitbomen die ges-
chikt zijn voor zonberen, met een reductie van bijna 80 procent in dichtheid van fruitbomen in
verbrande gebieden: van 167 ± 41 (SD) fruitbomen per hectare in onaangetast bos tot 37 ± 18
fruitbomen per hectare in verbrand bos. Bovendien stelden we een reductie van 44 procent in
de diversiteit van fruitbomen voor zonberen vast ongeveer 3 jaar na de brand. De dichtheden
van hemi-epifytische vijgen – een belangrijke fruitsoort tijdens de inter-mast-periode – namen
af met 95 procent in verbrande delen van het bos.
De manier waarop de zonberen het verbrande bos benutten is gedurende 10 jaar lang
gemonitord door regelmatig onderzoek naar sporen (zoals gebroken termietenheuvels, klau-
wsporen en graafsporen). Transecten zijn uitgevoerd in aan elkaar grenzende stukken van ver-
brand en ongeschonden bos. In een aantal jaren na de branden waren de dichtheden van zon-
beersporen bijna nul in de aangetaste delen van het bos. Maar in 2010 waren die dichtheden
weer toegenomen tot 28,0 ± 12,9 (SD) sporen per hectare; de toename wijst op rekolonisatie
van deze delen van het bos door de zonberen. De dichtheid van sporen in de aangrenzende
ongeschonden delen van het bos bleef in de loop der jaren stabiel, gemiddeld 41,6 ± 11,6 (SD)
sporen per hectare. De dichtheden van zonbeersporen waren 12 jaar na de bosbranden nog
steeds 35 procent lager in de verbrande delen van het bos; dit had te maken met schaarste van
sommige soorten voedsel voor zonberen, vooral fruitbomen en bovengrondse termietenkolo-
nies. De gestage rekolonisatie van deze verbrande delen van het bos door de beren laat zien
dat deze gebieden zich kunnen herstellen tot geschikte habitat voor de zonbeer; voorwaarde
is wel dat er een bronpopulatie van zonberen aanwezig is in aangrenzende ongeschonden delen
van het bos.
Aansluitend op de periode van droogte en de bosbranden hebben wij boeren her-
haaldelijk geïnterviewd in vijf gemeenschappen die langs de randen van het Sungai Wain Protec-
tion Forest gesitueerd zijn. Het doel was te onderzoeken in welke mate de zonberen gewassen
plunderen. De uitkomsten van de interviews gaven aan dat schade aan de gewassen groter
was in de periode volgend op de bosbranden dan in de jaren vóór de ENSO-verschijnselen en
de branden. Vijandigheid van de boeren ten opzichte van de beren was vooral het gevolg van
de schade die ze toebrachten aan stammen van oude kokospalmen (Cocos nucifera); als gevolg
daarvan gingen de bomen vaak dood. Daarom wilden de boeren de beren weg hebben. De
schade die beren toebrachten aan de jaarlijkse gewassen leidde in het algemeen tot een minder
Samenvatting192
vijandige reactie. Een experiment met het vastmaken van metalen platen aan de stammen van
de kokospalmen om beren het klimmen onmogelijk te maken was succesvol, in elk geval op de
korte termijn (≥ 3 jaar). Goedkope en gemakkelijk toe te passen gewasbeschermingsmiddelen
als deze zouden in de toekomst kunnen helpen zonberen te beschermen; een toename in de
conflicten tussen mensen en beren wordt verwacht door de groei van het aantal mensen, de
niet-aflatende vernietiging en fragmentatie van het bos, en de toegenomen vatbaarheid voor
brand van de stukken bos die overblijven.
De achteruitgang van de habitat door de grootschalige bosbranden in combinatie met
een langere periode met weinig fruit na de ENSO-verschijnselen, zette de zonberenpopulatie
in het gebied zwaar onder druk. Omdat de habitat van de zonberen op Borneo nog steeds in
een schrikbarend hoog tempo wordt vernietigd, worden ook kleine reservaten steeds belang-
rijker voor het behoud van deze soort. Ook gedragskenmerken van de beren wijzen erop dat
kleine reservaten van waarde kunnen zijn voor het behoud van de zonberen: onder andere de
relatief kleine home ranges – volledig begrensd binnen het kleine reservaat waar dit onderzoek
is uitgevoerd – en het vermijden van gebieden met verstoring door mensen, zoals paden en
verbrande delen van het bos. Het overleven van zonberen in deze gebieden op de lange termijn
zal afhangen van de preventie van stropen en de instandhouding van verbindingen met andere
bosgebieden.
Ringkasan
Beruang Madu (Helarctos malayanus), jenis terkecil dari 8 jenis beruang yang ada di
dunia, tersebar di seluruh negara di daratan Asia Tenggara serta di Pulau Sumatera dan
Kalimantan (Borneo). Penelitian terhadap beruang madu di alam bebas, termasuk Kalimantan,
tidak pernah ada sebelum penelitian yang ditampilkan dalam tesis ini yang dimulai pada tahun
1997 di suatu hamparan kecil hutan dataran rendah di Kalimantan Timur. Terlepas dari beberapa
catatan singkat, aspek dasar ekologi beruang madu hampir tidak diketahui pada saat itu dan
beruang madu didaftar sebagai ‘Data Deficient’ (Kekurangan Data) dalam Daftar Merah IUCN
(IUCN Red List). Untuk mengurangi kesenjangan pengetahuan atas jenis ini, saya kumpulkan
data mengenai berbagai aspek beruang madu mulai dari perilaku, ekologi dan konservasi selama
5 tahun penelitian intensif (mendalam) dari pertengahan 1997 sampai dengan pertengahan
2002, dengan penelitian lebih lanjut yang dilakukan pada tahun 2005 dan 2010.
Pada awal penelitian ini, kebakaran hutan besar yang dikarenakan kemarau
berkepanjangan di daerah tersebut terkait dengan terjadinya El Niño Southern Oscillation
(ENSO), telah mempengaruhi jutaan hektar hutan di Kalimantan, termasuk hutan lindung di
mana penelitian ini berlangsung. Antara tahun 1997-2006, sekitar 16.2 juta hektar dari luas
wilayah Borneo (21% dari luas total daratannya) telah terpengaruhi kebakaran, dan persentase
yang besar dari luasan terebut merupakan hutan. Merujuk kepada skala bencana alam ini,
sebagian dari penelitian saya fokuskan pada dampak dari kebakaran tersebut terhadap ekologi
dan konservasi beruang madu.
Peristiwa ENSO, selain menyebabkan kondisi kekeringan di daerah tersebut, juga
berkaitan dengan proses musim buah besar (panen raya, mast fruiting) di Asia Tenggara, khususnya
di bagian timur Pulau Kalimantan. Kanopi dan pohon-pohon besar di dalam hutan-hutan ini
didominasi oleh pohon dari marga Dipterocarpaceae, yang menampilkan pola reproduksi yang
unik. Proses pembungaan dan pembuahan berlangsung dengan senjangan waktu 2-10 tahun
dengan sedikit ataupun tidak adanya aktivitas reproduksi selama senjangan waktu tersebut, dan
sebagian besar dari pohon dari marga lainnya di hutan, terdiri dari berbagai kelompok taksonomi
dan sindrom pembungaan yang berbeda-beda, berbunga dan berbuah bersamaan dengan pohon
dipterokarpa. Kejadian panen raya buah menyediakan buah dalam jumlah banyak dalam periode
yang singkat, yang bertujuan untuk memuaskan para pemakan biji, namun juga menyediakan
buah bernutrisi berlebihan. Dari penelitian fenologi selama beberapa tahun terhadap lebih dari
Ringkasan196
600 pohon, kami mencatat bahwa ketersediaan buah makanan beruang madu menurun dari 13
pohon ha-1 bulan-1 selama panen raya buah menjadi hanya 1.6 pohon ha-1 bulan-1 selama periode
panjang antar musim panen raya buah.
Ditemukan bahwa beruang madu hampir tidak menkomsumsi makanan selain buah
selama masa-masa periode singkat (kira-kira 2 bulan) tersedianya buah. Selama penelitian ini,
beruang madu diketahui mengkonsumsi setidaknya 115 spesies buah, dengan lebih dari 50%
buah yang dimakan berasal dari marga Moraceae, Burseraceae dan Myrtaceae, sedangkan Ficus
spp. (Moraceae) merupakan kelompok buah utama yang dikonsumsi beruang madu selama
period antar musim buah besar. Kebanyakan jenis buah yang dimakan oleh beruang madu hanya
berbuah selama masa panen raya buah atau menampilkan pola berbuah yang ‘supra-annual’
(tidak setiap tahun). Hal ini menunkukkan ketersediaan buah makanan beruang yang sangat
sporadis. Selama masa antar musim panen raya buah, yang mengikuti peristiwa kebakaran
hutan, beruang madu berubah menjadi pemakan serangga, yang didominasi oleh rayap, semut,
kumbang, anak kumbang (larva) dan kecoa.
Dua beruang madu betina yang ditangkap untuk penelitian radio-telemetry (radio
pemantauan jarak) di wilayah inti hutan yang tidak terbakar, 16 bulan setelah peristiwa kebakaran
dan musim panen raya buah, menunjukkan tanda kekurangan nutrisi yang serius. Kedua betina
tersebut mempunyai anak yang kecil, yang kemungkinan membuat kondisi fisik mereka lebih
tertekan. Kondisi malnutrisi pada beruang madu betina menunjukkan bahwa bergantung pada
memakan hanya serangga selama jangka waktu yang panjang tidak cukup, dan sumber makanan
ini tidak mencukupi kebutuhan energi mereka. Pemangsaan salah satu beruang madu betina
oleh ular sawah besar mungkin berkaitan dengan kondisi malnutrisi yang dialaminya, yang
menyebabkan dia kurang mampu membela diri atau kurang wasapada.
Agar dapat memahami gerak gerik dan pola aktifitas beruang madu, 3 ekor beruang
madu betina liar dan dua ekor yang dilepasliarkan, dipasangkan kalung radio VHF yang peka gerak
(motion-sensitive VHF radio-collars). Tiga dari beruang ini terpantau secara berkelanjutan selama
1-3 tahun selama 1999-2003. Wilayah jelajah (periode 12 bulan) adalah 4-5km2 (95% Poligon
konvex minimal atau MCP dan 95% fixed kernel) dengan tumpang tindah antara wilayah jelajah
masing-masing individu yang cukup besar. Wilayah jelajah yang cukup kecil ini kemungkinan
berhubungan dengan pola makan yang didominasi oleh serangga, dan tidak adanya periode
panen raya buah di hutan selama penelitian telemetry. Aktifitas monitoring menunjukkan bahwa
beruang madu mempunyai pola aktifitas diurnal (aktif pada siang hari) dan crepuscular (aktif pada
saat fajar dan senja) sepanjang tahun dengan aktifitas dimulai pada 0.5 jam sebelum matahari
terbit dan berlangsung sampai 2.5 jam setelah matahari terbenam, dengan aktifitas rendah di
Ringkasan 197
malam hari (20-30%). Beruang aktif selama 61.6% dalam kurun waktu 24 jam (14.8 ± 2.3 jam),
dengan aktifitas lebih tinggi ketika memakan serangga dibanding ketika memakan buah.
Kebakaran hutan dan kemarau panjang menyebabkan mortalitas ekstrim pada pohon-
pohon buah yang dimakan beruang madu sehingga berkurang hampir 80% di daerah yang
terbakar, dari 167 ± 41 (SD) pohon jenis yang dimakan oleh beruang ha-1di hutan yang tidak
terbakar menjadi 37 ± 18 pohon buah ha-1 di hutan yang terbakar. Selain itu, juga diukur
pengurangan 44% pada keragaman jenis pohon buah 3 tahun setelah peristiwa kebakaran.
Kepadatan pohon ara setengah epifit (hemi-epiphytic figs), jenis buah yang penting selama musim
paceklik, menurun sebanyak 95% di area yang terbakar.
Pemanfaatan hutan yang terbakar oleh beruang madu dipantau melalui penelitian
tanda/bekas (misalnya tanda cakaran kuku, bongkaran sarang rayap, penggalian) berkala selama
periode 10 tahun, dengan peninjauan transek dilakukan di hutan primer dan hutan terbakar
yang berdekatan. Tanda beruang madu hampir tidak ada di wilayah terbakar selama beberapa
tahun setelah kebakaran, tapi pada tahun 2010 telah meningkat menjadi 28.0 ± 12.9 (SD)
tanda ha-1. Hal ini mengindikasikan re-kolonisasi oleh beruang madu. Kepadatan tanda/bekas
di hutan primer terlihat stabil dengan rata-rata 41.6 ± 11.6 (SD) tanda ha-1 sepanjang periode
monitoring. Kepadatan tanda beruang madu masih lebih rendah 35% di wilayah yang terbakar 12
tahun setelah peristiwa kebakaran, terkait dengan degradasi/ pengurangan dari beberapa jenis
makanan beruang madu, khususnya pohon buah dan sarang rayap di atas tanah. Re-koloniasasi
beruang madu pada area yang dulunya terbakar mengindikasikan potensi pemulihan area ini
sebagai habitat beruang madu, selama masih ada sumber populasi beruang madu di hutan yang
tidak terbakar yang dekat.
Setelah kemarau panjang dan peristiwa kebakaran, kami melakukan wawancara berkala
dengan petani di 5 pemukiman yang terletak di sepanjang pinggir Hutan Lindung Sungai Wain
untuk mengetahui gangguan beruang madu terhadap tanaman. Hasil dari wawancara tersebut
mengindikasikan bahwa pengrusakan tanaman oleh beruang madu meningkat setelah terjadi
kebakaran hutan dan ENSO. Kerusakan pada pohon kelapa tua yang seringkali mematikan
pohon tersebut menjadi sumber konflik paling tinggi dan membuat para petani berkeinginan
memusnahkan beruang. Pada umumnya, pengrusakan oleh beruang terhadap tanaman tahunan
tidak menimbulkan reaksi berat dari para petani. Percobaan dengan menempelkan lapisan senk
pada batang pohon kelapa berhasil menghalangi beruang memanjat pohon kelapa, setidaknya
pada periode singkat (sekitar 3 tahun). Pengamanan tanaman petani dengan pola yang mudah
dipraktekkan dan terjangkau seperti ini dapat membantu melindungi beruang ke depan, karena
konflik antara manusia dan beruang kemungkinan akan meningkat seiring dengan pertumbuhan
Ringkasan198
populasi manusia yang pesat, kerusakan dan fragmentasi hutan yang berlangsung terus-menerus
serta meningkatnya ancaman persistiwa kebakaran pada hamparan hutan yang tersisa.
Degradasi habitat yang disebabkan kebakaran hutan berskala besar, dikombinasikan
dengan ketersediaan buah yang tidak memadai setelah peristiwa ENSO, membuat populasi
beruang madu tertekan di wilayah ini. Dengan rusaknya habitat beruang madu dengan laju yang
menkhawatirkan di Pulau Kalimantan, hamparan hutan yang kecil pun menjadi sangat penting
untuk melindungi jenis beruang ini. Karakteristik perilaku seperti wilayah jelajah yang relatif
kecil, yang dibatasi dalam hutan lindung seperti ditemukan dalam penelitian ini, dan sifat beruang
untuk menghindari wilayah dimana terdapat gangguan manusia, menunjukkan bahwa hutan kecil
pun masih sangat penting bagi perlindungan beruang madu. Keberadaan jangka panjang beruang
madu di wilayah seperti ini akan bergantung pada pencegahan perburuan, kebakaran hutan, dan
pemeliharaan hubungan langsung dengan daerah hutan lainnya.
Curriculum Vitae
Gabriella Fredriksson was born on the 27th of June 1971 in Amsterdam, Netherlands.
After finishing high school, she studied biology at the University of Amsterdam and carried out
her MSc fieldwork in 1994 on reintroduced orangutans in East Kalimantan, Indonesia. In 1996
she did a short period of fieldwork in Gabon on mandrills, after which she returned in 1997
to East Kalimantan to start research on sun bears. During her work on sun bears she became
involved in forest protection activities, starting with fighting fires and illegal loggers, followed
by setting up an innovative collaborative management system for the Sungai Wain Protection
Forest, which became formalized in local legislation in 2002. In the same year, the sun bear was
proposed as the official mascot of Balikpapan. Starting in 2004 she initiated the development of
an environmental education facility in East Kalimantan, focusing on sun bears and conservation,
and though still further developing the facility currently receives over 50,000 local visitors per
year. Gabriella was honoured for her conservation work by being knighted in the ‘Order of the
Golden Ark’ in 2004 bestowed upon her by HRH Prince Bernhard. In 2006 Gabriella started
working in North Sumatra to establish protection for an area of primary forest that is home
to the southernmost population of Sumatran orangutans. Between 2008-2009 she became
involved with a forest redesign team established by the Governor of Aceh. Currently her time
is divided between conservation work in East Kalimantan and North Sumatra. Since 2004 she
has co-chaired the Sun Bear Expert Team of the IUCN/SSC Bear Specialist Group.
List of publications
Fredriksson, G. M. (1995). Reintroduction of orangutans: A new approach. Study on the behaviour and ecol-
ogy of reintroduced orangutans in the Sungai Wain Nature Reserve, East Kalimantan, Indonesia.
University of Amsterdam, Amsterdam, Netherlands.
Fredriksson, G. M. (1996). Conservation status of the mandrill (Mandrillus sphinx) in Central Africa. Ecologie
en Ontwikkeling 4.
Fredriksson, G. M. and M. de Kam. (1999). Strategic plan for the conservation of the Sungai Wain Protec-
tion Forest, East Kalimantan, Indonesia. The International Ministry of Forestry and Estate Crops-
Tropenbos Kalimantan Project.
Fredriksson, G. M. (2001). Conservation threats facing sun bears, Helarctos malayanus, and experiences with
sun bear reintroductions in East Kalimantan, Indonesia. In: The evaluation of bear rehabilitation
projects from a conservationist viewpoint, Ouwehands Zoo, Rhenen, Netherlands.
Fredriksson, G. M. (2002). Extinguishing the 1998 forest fires and subsequent coal fires in the Sungai Wain
Protection Forest, East Kalimantan, Indonesia. Pages 74-81 In Communities in flames: proceedings
of an international conference on community involvement in fire management. FAO and FireFight
SE Asia, Bangkok, Thailand.
Wich, S. A., G. Fredriksson, and E. H. M. Sterck. (2002). Measuring fruit patch size availability for three sym-
patric Indonesian primates. Primates 43:19-27.
Fredriksson, G. and V. Nijman. (2004). Habitat use and conservation status of two elusive ground brids
(Carpococcyx radiatus and Polyplectron scheiermacheri) in the Sungai Wain Protection Forest, East
Kalimantan, Indonesian Borneo. Oryx 38:297-303.
Schwarzenberger, F., G. M. Fredriksson, K. Schaller, and L. Kolter. (2004). Fecal steroid analysis for monitoring
reproduction in the sun bear (Helarctos malayanus). Theriogenology 62:1677-1692.
Fredriksson, G. M. (2005). Human sun bear conflicts in East Kalimantan, Indonesian Borneo. Ursus
16:130-137.
Fredriksson, G. M. (2005). Predation on sun bears by reticulated python in East Kalimantan, Indonesian
Borneo. The Raffles Bulletin of Zoology 53:197-200.
Fredriksson, G. M., S. A. Wich, and Trisno. (2006). Frugivory in sun bears (Helarctos malayanus) is linked to
El Niño-related fluctuations in fruiting phenology, East Kalimantan, Indonesia. Biological Journal of
the Linnean Society 89:489-508.
Curriculum vitae and list of publications204
Fredriksson, G. M., L. S. Danielsen, and J. E. Swenson. (2006). Impacts of El Niño related drought and forest
fires on sun bear fruit resources in lowland dipterocarp forest of East Borneo. Biodiversity and
Conservation 15:1271-1301.
Tumbelaka, L. and G. M. Fredriksson. (2006). The status of sun bears in Indonesia. Pages 73-78 In: Under-
standing Asian bears to secure their future. Japan Bear Network, Ibaraki, Japan.
Fredriksson, G., Steinmetz, R., Wong, S. & Garshelis, D.L. (IUCN SSC Bear Specialist Group) (2008). Helarc-
tos malayanus. In: IUCN 2012. IUCN Red List of Threatened Species. Version 2012.1. <www.iucn-
redlist.org>. Downloaded on 01 September 2012.
Marshall, A. J., M. Ancrenaz, F. Q. Brearley, G. Fredriksson, N. Ghaffar, M. Heydon, S. Husson, M. Leighton, K. R.
McConkey, H. Morrogh-Bernard, J. Proctor, C. P. van Schaik, C. P. Yeager, and S. A. Wich. (2009). The
effects of forest phenology and floristics on populations of Bornean and Sumatran orangutans: are
Sumatran forests more productive than Bornean forests? Pages 97–117 in S. A. Wich, S. S. Utami-
Atmoko, T. Mitra Setia, and C. P. van Schaik, editors. Orangutans: Geographic variation in behavioral
ecology and conservation. Oxford University Press, Oxford.
Slik, J. W. F., S.-I. Aiba, M. Bastian, F. Q. Brearley, C. H. Cannon, K. A. O. Eichhorn, G. Fredriksson, K. Kartawi-
nata, Y. Laumonier, A. Mansor, A. Marjokorpi, E. Meijaard, R. J. Morley, H. Nagamasu, R. Nilus, E. Nurt-
jahya, J. Payne, A. Permana, A. D. Poulsen, N. Raes, S. Riswan, C. P. van Schaik, D. Sheil, K. Sidiyasa, E.
Suzuki, J. L. C. H. van Valkenburg, C. O. Webb, S. Wich, T. Yoneda, R. Zakaria, and N. Zweifel. (2011).
Soils on exposed Sunda Shelf shaped biogeographic patterns in the equatorial forests of Southeast
Asia. Proceedings of the National Academy of Sciences 108:12343-12347.
Wich, S. A., E. R. Vogel, M. D. Larsen, G. M. Fredriksson, M. Leighton, C. P. Yeager, F. Q. Brearley, C. P. van Schaik,
and A. J. Marshall. (2011). Forest Fruit Production Is Higher on Sumatra Than on Borneo. PLoS
ONE 6:Published online 2011 June 2028. doi: 2010.1371/journal.pone.0021278.
Wich, S. A., G. M. Fredriksson, G. Usher, H. H. Peters, D. Priatna, F. Basalamah, W. Susanto, and H. Kühl. (2012).
Hunting of Sumatran orang-utans and its importance in determining distribution and density.
Biological Conservation 146:163-169.
Effects of El Niño and large-scale forest fi reson the ecology and conservation
of Malayan sun bears(Helarctos malayanus)
in East Kalimantan,Indonesian Borneo
Gabriella Fredriksson
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