Animal Biodiversity and Conservation 43.1 (2020)

97

Terrestrial mammal community richness
and temporal overlap between
tigers and other carnivores
in Bukit Barisan Selatan National Park,
SumatraM. L. Allen, M. C. Sibarani, L. Utoyo, M. Krofel

Allen, M. L., Sibarani, M. C., Utoyo, L., Krofel, M., 2020. Terrestrial mammal community richness and temporal
overlap between tigers and other carnivores in Bukit Barisan Selatan National Park, Sumatra. Animal Biodiversity and Conservation, 43.1: 97–107, DOI: https://doi.org/10.32800/abc.2020.43.0097
Abstract
Terrestrial mammal community richness and temporal overlap between tigers and other carnivores in Bukit
Barisan Selatan National Park, Sumatra. Rapid and widespread biodiversity losses around the world make it
important to survey and monitor endangered species, especially in biodiversity hotspots. Bukit Barisan Selatan
National Park (BBSNP) is one of the largest conserved areas on the island of Sumatra, and is important for theconservation of many threatened species. Sumatran tigers (Panthera tigris sumatrae) are critically endangered
and serve as an umbrella species for conservation, but may also affect the activity and distribution of othercarnivores. We deployed camera traps for 8 years in an area of Bukit Barisan Selatan National Park (BBSNP)
with little human activity to document the local terrestrial mammal community and investigate tiger spatial andtemporal overlap with other carnivore species. We detected 39 mammal species including Sumatran tiger andseveral other threatened mammals. Annual species richness averaged 21.5 (range 19–24) mammals, and remained stable over time. The mammal order significantly affected annual detection of species and the numberof cameras where a species was detected, while species conservation status did not. Tigers exhibited a diurnal
activity pattern, and had the highest temporal overlap with marbled cats (Pardofelis marmorata), dholes (Cuon
alpinus), and Malayan sun bears (Helarctos malayanus), but little overlap with other carnivores. These findings
suggest that some smaller carnivores might be adjusting temporal activity to avoid tigers or mesocarnivores.
The stable trends in richness of terrestrial mammal species show that BBSNP remains an important hotspot
for the conservation of biodiversity.
Key words: Activity patterns, Carnivores, Conservation, Interspecific interactions, Panthera tigris sumatrae
Resumen
Riqueza de la comunidad de mamíferos terrestres y solapamiento temporal entre el tigre y otros carnívoros en
el Parque Nacional Bukit Barisan Selatan, Sumatra. Debido a la pérdida rápida y generalizada de biodiversidad
en todo el mundo, es importante estudiar las especies en peligro de extinción, en especial en zonas de granbiodiversidad, y de hacer un seguimiento de dichas especies. El Parque Nacional Bukit Barisan Selatan (BBSNP
en sus siglas en inglés) es una de las mayores zonas de conservación de la isla de Sumatra y es importante parala conservación de muchas especies amenazadas. El tigre de Sumatra (Panthera tigris sumatrae) se encuentra
en peligro crítico de extinción y sirve de especie paraguas para la conservación, pero también puede afectar a laactividad y la distribución de otros carnívoros. Utilizamos cámaras de trampeo durante 8 años en una zona delParque Nacional BBSNP con escasa actividad humana, a fin de documentar la comunidad local de mamíferos
terrestres y estudiar el solapamiento espacial y temporal del tigre con otras especies de carnívoros. Detectamos
39 especies de mamíferos como el tigre de Sumatra y otros varios mamíferos amenazados. La riqueza anual deespecies se situó de media en 21,5 mamíferos (intervalo 19–24) y se mantuvo estable a lo largo del tiempo. A
diferencia de la situación de conservación de la especie, el orden de los mamíferos tuvo un efecto significativoen la detección anual de especies y el número de cámaras en las que se detectó una especie. El tigre mostró
una pauta de actividad diurna y el mayor solapamiento temporal con el gato jaspeado (Pardofelis marmorata), el
cuón (Cuon alpinus) y el oso malayo (Helarctos malayanus), pero poco solapamiento con otros carnívoros. Estos
resultados sugieren que algunos carnívoros de menor talla podrían estar ajustando la actividad temporal para
ISSN: 1578–665 X
eISSN: 2014–928 X© 2020 Museu de Ciències Naturals de Barcelona
Papers are published under aCreative Commons Attribution 4.0 International License

98

Allen et al.

evitar a los tigres o a mesocarnívoros. La tendencia estable de la riqueza de especies de mamíferos terrestrespone de manifiesto que el BBSNP sigue siendo una zona importante para la conservación de la biodiversidad.
Palabras clave: Pautas de actividad, Carnívoros, Conservación, Interacciones interespecíficas, Panthera tigris
sumatrae
Received: 31 VII 19; Conditional acceptance: 20 IX 19; Final acceptance: 18 XI 19
Maximilian L. Allen, Illinois Natural History Survey, University of Illinois, 1816 S. Oak Street, Champaign, IL 61820,
U.S.A.– Marsya C. Sibarani, Laji Utoyo, Wildlife Conservation Society–Indonesia Program, Jalan Tampomas
Ujung No. 35, Bogor, West Java 16151, Indonesia.– Miha Krofel, Department of Forestry, Biotechnical Faculty,
University of Ljubljana, Večna pot 83, SI–1000 Ljubljana, Slovenia.
Corresponding author: Maximilian L. Allen. E–mail: maxallen@illinois.edu

Animal Biodiversity and Conservation 43.1 (2020)

Introduction
The effects of humans are widespread and in thepast centuries have led to historically high rates ofextinction around the world (Pimm et al., 1995; Chapin
et al., 1998). In order to guide effective conservation
efforts to address biodiversity loss it is important tosurvey and monitor endangered species and thebiodiversity in crucial areas for conservation, suchas large protected areas in biodiversity hotspots(Johnson et al., 2009; Gopal et al., 2010). The effectsof humans are often strongest on carnivores (Ripple
et al., 2014), which occupy high trophic levels andstructure ecosystems and community composition
through predation and other interspecific interactions(Estes and Palmisano, 1974; McLaren and Peterson,1994). Carnivores also act as umbrella species as theyrequire large areas for viable populations and throughtheir preservation protect the habitat of many otherco–occurring species (Sibarani et al., 2019). Camera
trapping is one of the many emerging technologies
that is increasingly being used to monitor wildlife(O'Brien, 2008; Karanth and Nichols, 2010), and canbe a critical non–invasive tool in documenting cryptic
and endangered wildlife (Linkie et al., 2007; Tobler
et al., 2008). Surveys of carnivores are important,particularly when they are threatened or endangered,and surveys via camera trap also allow for surveying
a diversity of other species.
The Indonesian island of Sumatra is located in oneof the global hotspots of biodiversity and represents a
conservation priority (Myers et al., 2000). Bukit Barisan
Selatan National Park (BBSNP) is one of the largest
conserved areas on the island of Sumatra, making
it important for the conservation of several criticallyendangered species (e.g., Sumatran rhinoceros, Dicerorhinus sumatrensis, and Sunda Pangolin, Manis
javanica) and subspecies (e.g., Sumatran tigers,
Panthera tigris sumatrae; and Sumatran elephant,
Elephas maximus sumatranus) (O’Brien and Kinnaird,
1996; Pusparini et al., 2018; Allen et al., 2019). Tigers
are an endangered apex carnivore throughout theirrange (Goodrich et al., 2015), but four subspecies
are likely now extinct in the wild (Seidensticker etal., 1973; Goodrich et al., 2015). The Sumatran tiger
subspecies is one of the most critically endangeredcarnivores in the world (Linkie et al., 2008b), andSumatran tigers serve as an umbrella species forscientific studies and conservation in many areasof their range. As a national park, BBSNP acts as apreserve and stronghold for biodiversity, but there isno buffer between the park and adjacent agriculture,
resulting in frequent illegal encroachment into the park
(O’Brien and Kinnaird, 1996; Pusparini et al., 2018).
Repeated surveys are needed to understand the biodiversity of the park, as well as trends in threatened
and endangered populations over time.
The ecology of most carnivore species occurringon Sumatra, including their activity patterns, is poorly
studied (Hunter, 2015), but it is important to understand in order to develop effective means for theirconservation. The interactions between carnivores
are important as the conservation of one species

99

can have detrimental effects on other species, andmanagement plans need to account for interspecificinteractions to mitigate these side–effects (Krofel and
Jerina, 2016). Camera trapping is frequently used
to monitor wildlife, providing a wealth of informationon the spatial and temporal activity of species in thelocal community (Swanson et al., 2015; Rich et al.,2016; Allen et al., 2019). Temporal patterns are important aspects of niche partitioning among sympatriccarnivores (Romero–Munoz et al., 2010; Karanth etal. 2017; Herrera et al., 2018), with subordinate carnivores often adjusting their temporal activity to avoid
overlap with dominant carnivores (Foster et al., 2013;
Lynam et al., 2013; Wang et al., 2015), but not always(Balme et al., 2017; Allen et al., 2018). Determining
temporal patterns and overlap among species is a
way to inform our understanding of cryptic species
and their interactions (e.g., Van Schaik and Griffiths,
1996; Linkie and Ridout, 2011; O'Brien et al., 2003).
We deployed camera traps in BBSNP in Sumatra
over eight years to document trends in the local
terrestrial mammalian community, as well as temporal overlap between tigers and other carnivores
to inform conservation efforts. Our objectives were:(1) Determine the trends in annual mammal species
richness, and relative abundance of species in the
study area. We hypothesized that trends in richness
would be stable due to the relatively short time periodof the surveys. We also hypothesized that camera
traps would detect higher relative abundances for
Artiodactyla than Carnivora which occur at lower
densities and primate species due to their arboreal
nature. (2) Define factors affecting annual detection
for species. We hypothesized that mammals species
from lower trophic levels and of lower conservation
concern would be detected in more years due to theirgreater abundance. (3) Compare mammal detections
from our camera trapping with previous surveys using
track surveys and interviews with local experts fromBBNSP by O'Brien and Kinnaird (1996). (4) Determine
factors affecting species occupancy. We hypothesizedthat camera traps would detect higher occupancies
for Artiodactyla than Carnivora which occur at lower
densities and primate species due to their arboreal
nature. We also hypothesized that the conservation
status of species would be related to occupancy, withendangered species being detected at fewer cameras
then species of less concern. (5) Analyze the temporal
overlap of tigers with four other felids and six othercarnivores, hypothesizing that subordinate competitor
carnivores would have low temporal overlap with the
apex predator, the Sumatran tiger (e.g., Lynam et al.,2013; Wang et al., 2015).
Material and methods
Study area
Our study site is located in BBSNP in the South Barisan Range ecosystem on the Indonesian island of
Sumatra (fig. 1). BBSNP is the third largest protectedarea (3,560 km²) on Sumatra (O'Brien and Kinnaird,

Allen et al.

1001996), spanning two provinces: Lampung and Bengkulu. Topography ranges from coastal plains and lowland
rainforest at sea level in the southern peninsula ofthe park to mountains up to 1,964 m in the middle tonorthern parts of the park (Pusparini et al., 2018). The
park contains montane forest, lowland tropical forest,
coastal forest and mangrove forest. Rainfall is mostabundant in the monsoon season from November toMay, with approximately 3,000–4,000 mm of rainfall(O'Brien et al., 2003); and annual temperatures are
between 22 ºC to 35 ºC (O'Brien et al., 2003). BBSNP
contains a high diversity of wildlife, with tigers and76 other species listed in CITES with Endangered toCritical IUCN status.
Field methods
We set camera traps to monitor biodiversity as partof the Tropical Ecology and Assessment Monitoring(TEAM) network for Bukit Barisan (teamnetwork.org).
We set two arrays of 30 camera traps placed at adensity of 1 camera trap per 2 km2 (fig. 1) covering a
total of 128.43 km2. We attempted to set each camera
trap annually from 2010–2017, and we deployed thecamera arrays sequentially rather than simultaneously
within the same dry season from April to July (Array
1 from April to May and Array 2 from June to July)to complete at least 30 days of sampling for eachpoint. We placed camera traps in strategic locations
on game trails. We set all camera traps in lowland
forests, with an elevation range of 16 to 320 m.
Statistical analyses
We defined a detection event as any series of photos
triggered by a human or wildlife species. To avoid
pseudo–replication, we considered consecutive photo
captures of the same species within 30' to be thesame event (Rovero and Zimmermann, 2016; Allenet al., 2018). We calculated the number of independent events for each species and relative abundance(RAB) as:RAB = events / trap nights x 1,000
and then report the mean annual RAB (0 RAB) for
each species. We calculated annual species richness
by totaling the number of unique mammal species
detected each year. We also calculated the naïve
annual occupancy and mean naïve annual occupancy
for each species (Nichols et al., 2007; O'Connell andBailey, 2011).
We used generalized linear mixed models (GLMMs) to determine if the RAB of species was affectedby either their order or conservation status, using theannual RAB of a species as our dependent variable,
their order or conservation status as the independent
variable, and species as a random effect. We also
used GLMs to determine if the number of years a
species was detected was affected by either their order or conservation status, using the number of years
a species was detected as our dependent variable,
their order or conservation status as the independent

variable, and species as a random effect. We also
compared species richness between our surveys andthe previous survey by O'Brien and Kinnaird (1996),
using a t–test to compare our annual values to theprevious value. We then used GLMMS to determine
if the occupancy of species varied annually by either
their order or conservation status. We used the annual
occupancy of a species as our dependent variable,
their order or conservation status as the independent
variable, and the species as a random effect.
We used kernel density estimation to determine
activity patterns and quantify overlap among species(Ridout and Linkie, 2009). We considered interactions with other carnivores for which we obtained> 3 detections. Other felids included Asiatic goldencat (Catopuma temminckii), leopard cat (Prionailurus
bengalensis), marbled cat (Pardofelis marmorata),
and Sunda clouded leopard (Neofelis diardi). Other
carnivores included banded linsang (Prionodon
linsang), banded palm civet (Hemigalus derbyanus),
binturong (Arctictis binturong), dhole (Cuon alpinus),
masked palm civet (Paguma larvata), and sun bear
(Helarctos malayanus). We changed the time of each
event to radians for each species, and then used
the overlap package (Meredith and Ridout, 2017) inprogram R version 3.3.1 (R Core Team, 2016) to fit
the data to a circular kernel density and estimated theactivity level at each time period from the distributionof the kernel density. We then used the overlapEst
function to test for the degree of overlap in activity
patterns between tigers and the other species using
their Δ1 scores (where a higher score indicates more
overlap). We calculated 95 % confidence intervals bybootstrapping 10,000 estimates of activity for eachspecies, and then using the bootEst and bootCI
functions to estimate overlap between each species
pair based on the boot0 score.
Results
Sixty camera traps functioned from 2010 to 2017 fora total of 11,896 trap nights, registering 53,120 photos, representing 3,245 independent detection eventsof 49 species. We detected one critically endangered species, Sunda pangolin (0 RAB = 1.31),
and two critically endangered subspecies, Sumatran tiger (0 RAB = 2.41) and Sumatran elephant(0 RAB = 1.42), as well as with seven endangered
species and seven vulnerable species (table 1). We
found that the mammal order had a significant effecton the relative abundance of species, with Artiodactyla
species having higher RAB (0 = 28.81) than Carnivora
species (0 = 0.78, F = –3.55, p = 0.0004), but notother orders (p > 0.12). The conservation status of
species, however, did not have a significant effect on
the relative abundance of species (p > 0.51).
Our observed annual species richness averaged
21.5 (range 19–24) mammals, with a relatively stable
trend that did not vary significantly across time (df = 7,
F = 0.91, p = 0.37). We documented eight species inall eight years, three species in seven years; but ninespecies were detected in only one year. We foundAnimal Biodiversity and Conservation 43.1 (2020)

101

BBSNP

ra

at
um

S

Camera trap
locations
Array 10
Array 2510 km

Fig. 1. Study site within Bukit Barisan National Park on the island of Sumatra (BBSNP), and camera traparrays. We did not display the coordinate reference grids because of conservation concerns and someof the recorded species are hunted for illegal wildlife trading.
Fig. 1. Zona del estudio dentro del Parque Nacional Bukit Barisan en la isla de Sumatra (BBSNP) y disposición de las cámaras de trampeo. No se muestran las cuadrículas de coordenadas de referencia por
motivos de conservación y porque algunas de las especies son objeto de caza para el comercio ilegal.

that the mammal order had a significant effect on thenumber of years detected, with Artiodactyla species
found in more years (0 = 6.50) than Carnivora species (0 = 3.33, F = –2.81, p = 0.005), but not otherorders (p > 0.08) including Eulipotyphla (0 = 6.00),
Perissodactyla (0 = 8.00), Pholidota (0 = 7.00), Primates (0 = 4.00), Proboscidea (0 = 6.00), Rodentia(0 = 4.75), or Scandentia (0 = 4.00). The conservation
status of species, however, did not have a significant
effect on how many years a species was detected(p > 0.53).
The number of species we observed in any given
year did not vary significantly from the previous surveys by O'Brien and Kinnaird (1996) (df = 7, p = 0.77).
We detected 39 mammal species, 26 (excluding
humans and domestic dogs) of which had not been
documented in previous surveys by O'Brien and
Kinnaird (1996); but we did not detect eight mammal
species which had previously been detected (table 1).
We found that the species' order had a significant
effect on their occupancy, with Artiodactyla species
having significantly higher mean annual occupancy(0 = 0.28) than Carnivora (0 = 0.02, T = –3.62,
p = 0.0003), but not other orders (p > 0.08). The
conservation status of species, however, did not havea significant effect on how many cameras they were
documented at annually (p > 0.59).
Tigers exhibited a diurnal activity pattern (fig. 2,3). We documented four other felid species, all withlower relative abundance than tigers. Marbled cats

had a peak of activity in the morning and were active
during the day, leading to the highest overlap withtigers (fig. 2). Asian golden cats were crepuscularwith their highest activity at dawn, leading to someoverlap with tigers, while leopard cats and Sunda
clouded leopards were primarily nocturnal and had
little overlap with tigers (fig. 2).
We documented six other carnivore species, withbanded palm civets and sun bears having higher RAB
than tigers. Dholes were diurnal and had the highest
temporal overlap with tigers, while Malayan sun bears
were cathemeral and had less overlap with tigers.
Banded linsangs, banded palm civets, binturongs,
and masked palm civets were primarily nocturnal andexhibited little overlap with tigers (fig. 2).
Discussion
BBSNP and other protected areas in Sumatra containmany threatened and endangered species whose
populations are imperiled primarily by encroachment
and habitat destruction. Effective conservation for
species or ecological communities is dependent oninternational teamwork among government agencies,
local communities, and scientific organizations. Using
camera trap surveys, we were able to monitor numerous mammal species, including critically endangered
Sunda pangolins, Sumatran tigers and Sumatranelephants, along with over a dozen other threatenedAllen et al.

102

Table 1. Mammal species, IUCN status (IUCN: EN, endangered; NT, near threatened; VU, vulnerable;;LC, least concern; CE, critically endangered; NE, not evaluated), number of years documented (N),mean annual relative abundance (0 RAB), mean annual percent area occupied (0 PAO), and whether the
species was documented in previous surveys O’Brien and Kinnaird (1996), last column: * subspecies
critically endangered
Tabla 1. Especie de mamífero, situación de la UICN, número de años documentado (N), abundancia media
anual relativa (0 RAB), superficie media ocupada anual (0 PAO) y si la especie se había documentado
en estudios anteriores O'Brien y Kinnaird (1996), en la última columna: * subespecies en peligro crítico.
(Para las abreviaturas de la situación de la IUCN, véase arriba).

Common nameScientific name

IUCN

N

0 RAB

0 PAO

Tiger

Panthera tigris

EN*

6

2.41

0.05

Yes

Asian golden cat

Catopuma temminckii

NT

6

0.88

0.03

No

Marbled cat

Pardofelis marmorata

NT

4

0.6

0.02

No

Sunda clouded leopard

Neofelis diardi

VU

3

0.39

0.01

Yes

Leopard cat

Prionailurus bengalensis

LC

7

1.07

0.03

No

Oriental small–clawed otter

Aonyx cinerea

VU

1

0.10

< 0.01No

Binturong

Arctictis binturong

VU

2

0.34

0.01

No

Small–toothed palm civet

Arctogalidia trivirgata

LC

1

0.07

< 0.01No

Domestic dog

Canis familiaris

NE

2

0.15

< 0.01No

Dhole

Cuon alpinus

EN

2

0.33

0.01

No

Otter civet

Cynogale bennettii

EN

1

0.07

< 0.01

No

Malayan sun bear

Helarctos malayanus

VU

7

2.61

0.07

Yes

Banded palm civet

Hemigalus derbyanus

NT

6

2.68

0.07

No

Short–tailed mongoose

Herpestes brachyurus

NT

1

0.11

0.00

No

Eurasian otter

Lutra lutra

NT

1

0.08

< 0.01No

Hairy–nosed otter

Lutra sumatmna

EN

0

0.00

0.00

Yes

Yellow–throated marten

Martes flavigula

LC

1

0.07

0.00

No

Asian palm civet

Paradoxurus hermaphroditus

LC

1

0.11

< 0.01No

Masked palm civet

Paguma larvata

LC

6

0.83

0.03

No

Banded linsang

Prionodon linsang

LC

4

0.43

0.01

No

Domestic water buffalo

Bubalus bubalis

NE

0

0.00

0.00

Yes

Plantain squirrel

Callosciurus notatus

LC

0

0.00

0.00

Yes

Sumatran serow

Capricornis sumatraensis

VU

3

0.32

0.01

No

Sumatran rhinoceros

Dicerorhinus sumatrensis

CE

0

0.00

0.00

Yes

MoonratEchinosorex gymnura

LC

6

2.34

0.05

No

Sumatran elephant

Elephas maximus

EN*

6

1.42

0.03

Yes

Human

Homo sapiens

NE

5

1.24

0.03

No

Dark–handed gibbon

Hylobates agilis

EN

0

0.00

0.00

Yes

Common porcupine

Hystrix brachyura

LC

8

30.34

0.33

No

Three–striped ground squirrel

Lariscus insignis

LC

8

9.95

0.10

No

Long–tailed macaque

Macaca fascicularis

LC

3

0.24

0.01

Yes

Pigtail Macaque

Macaca nemestrina

VU

8

43.76

0.63

No

Sunda pangolin

Manis javanica

CE

7

1.31

0.04

No

Red muntjac

Muntiacus muntjak

LC

8

71.99

0.71

Yes

Animal Biodiversity and Conservation 43.1 (2020)

103

Table 1. (Cont.)

Common nameScientific name

IUCN

N

0 RAB

0 PAO

Sumatran surili

Presbytis melalophos

EN

4

0.48

0.02

Yes

Flying fox

Pteropus vampyrus

NT

0

0.00

0.00

Yes

Black giant squirrel

Ratufa bicolor

NT

0

0.00

0.00

Yes

Sambar deer

Rusa unicolor

VU

8

9.69

0.18

Yes

Horse–tailed squirrel

Sundasciurus hippurus

NT

1

0.07

< 0.01No

Wild boar

Sus scrofa

LC

8

29.4

0.39

Yes

SiamangSymphalangus syndactylus

EN

1

0.14

< 0.01

Yes

Malayan tapir

Tapirus indicus

EN

8

8.07

0.15

Yes

Silvery lutung

Trachypithecus cristatus

NT

0

0.00

0.00

Yes

Lesser mouse deer

Tragulus kanchil

LC

4

21.99

0.23

No

Greater mouse deer

Tragulus napu

LC

8

12.55

0.17

No

Long–tailed porcupine

Trichys fasciculata

LC

2

0.63

0.01

No

Large treeshrew

Tupaia tana

LC

4

1.37

0.03

No

or endangered mammals. Tigers are threatened anddeclining worldwide (Seidensticker, 2010; Walston etal., 2010), and protected areas, including BBSNP, areimportant for their populations (Kawanshi and Sunquist, 2004, Wibisono et al., 2009) our surveys showed
the importance of BBSNP to the critically endangered
tiger population in Sumatra. High species richness ofterrestrial mammal species, which remained similar
across the eight years of our survey, also confirms
the conservation value of BBSNP and other protectedareas for other threatened and endangered mammal
species (Linkie et al., 2008a).
Camera trapping is an informative way to gather
ecological data, especially for cryptic or rare species,
but is best used in conjunction with other surveys.
The project documented 26 mammal species withcamera trap surveys that had not been detected by
O'Brien and Kinnaird (1996) in a previous survey
using transects and interviews with local citizens,but our survey missed eight that had been previously
documented. The additional species we identified wereprimarily terrestrial species, while the ones not documented were primarily arboreal species. Both survey
methods detected a similar number of species in any
given annual survey, though not the same species.
Each method has costs and benefits that should
be considered in future studies. Camera trapping iseffective for documenting terrestrial cryptic mammal
species, and can be used 24 hours a day over weeks
or months, while transect surveys are more effective
for documenting birds and amphibians. There is thepossibility of misidentification of photographs or signs
with either method, although misidentification shouldbe less frequent for photographs. Using both methods
in conjunction is a good approach to document the

mammal community, especially in such a criticallyimportant area for conservation.
Tigers exhibited diurnal activity patterns and had
moderate temporal overlap with marbled cats, dholes,
and sun bears, but most other carnivores had little
temporal overlap with tigers. Sun bears are known
for their arboreal habits and insectivorous–frugivorous
diet, and therefore have less overlap in dietary andspatial use with tigers, but are also generally diurnal
throughout their range (Fitzgerald and Krausman,2002). Common leopards (Panthera pardus) wereextirpated from Sumatra, and now dholes and Sunda
clouded leopards are the other carnivores nearest to
tigers in size, and may be their closest competitors.
Sympatric carnivores that are smaller than their competitors use adaptive strategies, including temporal
avoidance, to exploit the same resources and avoid
intra–guild predation (Lesmeister et al., 2015; Wanget al., 2015). Contrary to our hypothesis, dholes werealso diurnal and exhibited greater temporal overlap
with tigers than we expected. This may be due to lackof fear of tigers on the part of dholes (e.g., Burton,
2019). Among felids, Sunda clouded leopards andleopard cats were nocturnal, while Asian goldencats and marbled cats were crepuscular, which is
generally in accordance with previous studies (Van
Schaik and Griffiths, 2009; Grassman et al., 2005).
Temporal patterns and overlap can be complex inecosystems with many carnivores, as competitive
suppression of mesocarnivores by apex carnivores
can release subordinate small carnivores from competitive pressure (e.g., Levi and Wilmers, 2012; Wanget al., 2015; Allen et al., 2017), but species are most
likely to avoid the species that they perceive as thegreatest threat. For example, marbled cats had a highAllen et al.

104

A					
Δ1 = 0.41 (0.23–0.60)

B

Tiger
As. golden cat

0.20

Δ1 = 0.29 (0.11–0.48)

0.10

Tiger
Leopard cat

0.10
0.0

0.0
00:00 06:00 12:00 18:00 24:00

00:00 06:00 12:00 18:00 24:00

Δ1 = 0.20 (0.41–0.93)
C					

D

Δ1 = 0.29 (0.09–0.54)

Tiger
Marbled cat

0.10

0.10

0.0

0.0
00:00 06:00 12:00 18:00 24:00

00:00 06:00 12:00 18:00 24:00

E					
Δ1 = 0.21 (0.05–0.41)

Δ1 = 0.25 (0.11–0.41)

F

Tiger
Banded linsang

0.10

Tiger
S. clouded leopard

Tiger
Banded palm civet

0.10

0.0

0.0

00:00 06:00 12:00 18:00 24:00
G					
Δ1 = 0.18 (0.03–0.35)
0.20

00:00 06:00 12:00 18:00 24:00

H

Tiger
Binturong

Δ1 = 0.60 (0.42–0.77)
Tiger
Dhole

0.20

0.10

0.10

0.0
00:00 06:00 12:00 18:00 24:00

0.0
00:00 06:00 12:00 18:00 24:00

Δ1 = 0.26 (0.09–0.46)
I					
0.10

Tiger
Masked palm civet

Δ1 = 0.60 (0.42–0.77)

J
0.12

Tiger
Sun bear

0.06
0.0

0.0
00:00 06:00 12:00 18:00 24:00
00:00 06:00 12:00 18:00 24:00
Time of day

Fig. 2. Temporal activity and overlap (kernel density), of tigers and other carnivores: A, Asian golden
cat; B, leopard cat; C, marbled cat; D, Sunda clouded leopard; E, banded linsang; F, banded palm civet;
G, binturong; H, dhole; I, masked palm civet; J, sun bear. Tiger activity is represented as a solid line andthe other carnivore activity as a dotted line, and temporal overlap as the shaded area.
Fig. 2. Actividad temporal y solapamiento (densidad de kernel) del tigre y otros carnívoros: A, gato dorado
asiático; B, gato de Bengala; C, gato jaspeado; D, pantera nebulosa de Borneo; E, linsang rayado; F,
civeta de las palmeras rayada; G, binturong; H, cuón; I, civeta de las palmeras enmascarada; J, oso
malayo. La actividad del tigre se representa con una línea continua y la de los otros carnívoros con una
línea discontinua; el solapamiento temporal es la superficie sombreada.

Animal Biodiversity and Conservation 43.1 (2020)degree of overlap with tigers, and this may be due totemporally avoiding Sunda clouded leopards. Sunda
clouded leopards are also arboreal, which increase
the probability of encounters with marbled cats andmay thus be perceived as a more direct threat. The
temporal patterns and overlap among the carnivore
community suggest that tigers may be structuring thecarnivore guild, but smaller carnivores may also use
different resources (prey and habitat) as a means oflimiting competition and overlap with tigers (Karanth
et al., 2017).
Camera trapping surveys using TEAM protocols
appear effective for monitoring the richness andrelative abundance of the terrestrial mammal community, but may best be used in conjunction with othersurvey methods. Our surveys focused on terrestrial
mammals, but camera trapping can also be effective
for arboreal species with appropriate adjustments(Gregory et al., 2014). The TEAM protocol is set for
short bursts (one month) of camera trapping, and tobe effective for monitoring threatened and endangered
terrestrial species. Surprisingly, the conservation status of species did not predict the number of years they
were detected, relative abundance or occupancy. Thismay be due to the inherent differences in abundance
among species of different trophic levels, or because
species can be locally abundant but of conservation
concern globally. Our surveys also highlight the importance of BBSNP and other parks for biodiversity
and many endangered species, and there is muchpotential to use BBSNP for future species–specificsurveys, including for critically endangered Sunda
pangolins, Sumatran tigers or Sumatran elephants.
The development of new analyses, such as kernel
density overlap (Ridout and Linkie, 2009), help us
understand the ecological interactions of species, anddevelopment of new techniques in the future should
be used for further understanding cryptic species.
Acknowledgements
All data in this publication are available through theTropical Ecology Assessment and Monitoring (TEAM)
Network, a collaboration between Conservation International, the Missouri Botanical Garden, the Smithsonian Institution, and the Wildlife Conservation Society.
The work was partially funded by these institutions,
the Gordon and Betty Moore Foundation, and theIllinois Natural History Survey. Monitoring activities
were managed by the Wildlife Conservation Society incollaboration with the Bukit Barisan Selatan National
Park and the Ministry of Environment and Forestry,
Republic of Indonesia. We thank all the field staff andforest rangers involved in the camera trap deployment,
and W. Marthy and F. R. Affandi for field coordination.
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