Mammal Study 28: 161–165 (2003)
© the Mammalogical Society of Japan
Short communication
Arboreal fruit visitors in a tropical forest in Sri Lanka
Palitha Jayasekara1,*, Seiki Takatsuki2, Udayani R. Weerasinghe3 and Siril Wijesundara4
1
Faculty of Agriculture, Gifu University, Yanagido 1-1 Gifu 501-1193, Japan
The University Museum, the University of Tokyo, Hongo 7-3-1, Bunkyo-ku, Tokyo 113-0033, Japan
3
Royal Botanic Gardens, Peradeniya, Sri Lanka
2
Tropical forests exhibit extremely high biodiversity, and
provide complex habitats for wildlife (Harrison 1962).
More than 60% of woody plants in the tropical forest
bear fruits, which are important foods for birds and
mammals (Fleming 1979). Recent studies on frugivory
have revealed that birds and primates are the main fruit
consumers (Terborgh 1990; Wrangham et al. 1994; Dew
and Wright 1998). However, past studies have been conducted during the daytime, thus it is possible that many
nocturnal animals have been overlooked, leaving information on frugivores incomplete and biased to diurnal
animals (with the exception of bats, which have been
relatively well studied (Thomas 1984; Banack 1998; Eby
1998). This bias is the result of methodological limitations.
Using traditional observational methods, it has been
difficult to study animals, particularly in tropical forests,
technological developments, however, such as automatic
cameras, are helping to overcome these limitations (e.g.
Miura et al. 1997; Yasuda 1998). Miura et al.’s (1997)
and Yasuda’s (1998) studies pioneered such techniques
in Asian tropical forests, but focussed on ground dwelling species. This research, also using automatic cameras, therefore aimed to expand studies of frugivores into
the arboreal layers of a tropical forest in Sri Lanka. This
study also aimed to describe differences of fruit types,
which might affect fruit users, and so contribute to a
better understanding of frugivory in the tropical forest.
Methods
Fieldwork was carried out in the Sinharaja tropical
rain forest in Sri Lanka during two periods: from June
2000 to January 2001, and from July to December 2001.
The 88 km2 Sinharaja forest consists of natural and mod-
ified forests. The topography, vegetation, and climate of
the area have been described in detail by De Zoysa and
Raheem (1990) and Gunatilleke and Gunatilleke (1996).
In brief, however, the forest is dominated by trees
belonging to the family Dipterocarpaceae (Gunatilleke
and Gunatilleke 1996). Rainfall ranges from 3,000 mm
to 6,000 mm per year and temperature ranges from 19°C
to 31°C.
Since biodiversity is high in tropical forest, it was
expected that various species of animals might be
observed visiting various types of fruits. We focused on
mammalian frugivores, and so selected 10 large fleshy
fruit species belonging to nine families representative of
different strata of the forest (Table 1). The trees selected
varied in height from approximately 20 m to 40 m, and
in fruit color, pulp type, and size (18.4–137.0 mm3) and
weight (3.9–328.5 g). Fruit type was defined following
Bell (1991) and the color of the external surface was
used to categorize the color of the fruit. However, for
dehiscent fruits the color of the external surface of the
edible part was used.
To identify fruit consumers, wooden platforms were
set on branches in the study tree, and fully ripened fruits
harvested from the same tree were placed in a clump on
the platform. Only one fruit species was used per fruit
clump. The number of fruits placed on the platform
varied according to the fruit size (Table 2).
Automatic camera systems (Marif Co., Japan) were
used for recording visitors. These consisted of an automatic camera with a built-in far-infrared sensors and
auto-quartz timepieces to record the time of animal
visits. Cameras were placed 15–20 m up on the trunks
or branches of selected trees. Cameras were automatically triggered by the far-infrared rays radiated by animals visiting fruit. If an animal remained at the fruit,
*To whom correspondence should be addressed. Present address: c/o The University Museum, the University of Tokyo, Hongo 7-3-1, Bunkyo-ku,
Tokyo 113-0033, Japan. E-mail: [email protected]
162
Mammal Study
Table 1.
Fruit species used in the study and their fruit characteristics.
Species
Family
Fruit type
Colour
Protection
Pulp type
Artocarpus nobilis
Coscinium fenestratum
Cullenia ceylanica
Cullenia rosayroana
Diospyros racemosa
Dysoxylum ficiforme
Garcinia hermonii
Myristica dactyloides
Podadenia thwaitesii
Semecarpus walkeri
Moraceae
Menispermaceae
Bombacaceae
Bombacaceae
Ebenaceae
Meliaceae
Clusiaceae
Myristicacea
Euphorbiaceae
Anacardiaceae
compound
drupe
schizocarp
schizocarp
drupe
drupe
drupe
schizocarp
drupe
achine
brown
brown
white
white
green
brown
green
orange
green
red
thick husk
thick husk
no
no
no
thin husk
no
no
thick husk
no
juicy fibrous
juicy soft
aril
aril
juicy fibrous
juicy soft
less juicy fibrous
aril
juicy soft
less juicy fibrous
Table 2.
Number of fruits and duration of the experiment.
Fruit species
Number of bait fruits
Experiment duration
(days)
5
16
35
7
3
40
40
34
30
20
50
12
15
22
12
21
15
26
14
12
Artocarpus nobilis
Coscinium fenestratum
Cullenia ceylanica
Cullenia rosayroana
Diospyros racemosa
Dysoxylum ficiforme
Garcinia hermonii
Myristica dactyloides
Podadenia thwaitesii
Semecarpus walkeri
28 (2003)
the camera was triggered every five seconds.
The cameras were set in the morning and checked at
an interval of two to three days to minimize human disturbance. The numbers of fruits eaten were recorded,
and fruits damaged by insects or pathogens, or consumed
by animals, were replaced with new ones. Data were
collected continuously over two to three weeks per fruit
species (Table 2) and at least two rolls of film (24 shots
per roll) were used per fruit species in each selected tree.
One photograph was considered to represent one visit.
Because the duration of the experiment differed among
the fruit species (Table 2), frequency of visits was
expressed per day to avoid this bias. The animals
recorded were identified according to Kotagama and
Karunarathna (1983) and Kotagama and Fernando
(1994).
Results and discussion
Visitor composition
A total of twelve different taxa were identified, and in
addition several unidentified species of murid rodents
Fresh weight (g) Seed size (mm3)
287.7
5.2
69.5
328.5
11.2
10.5
115.2
28.7
21.5
3.0
13.6
17.1
20.8
28.0
15.2
16.7
27.2
24.3
17.6
10.1
(rats and mice), were recorded making 479 visits to fruit
during the study period (Table 3). Nine taxa were identified to the species level and one was identified to the
genus level. It was difficult, or impossible, to identify
murids, bats, and loris even to the generic level. Since
bats visited fruit baits, it is likely that they were fruit
bats, but there remains the possibility that other bats also
visited opportunistically. It is also known that two loris
species belonging to the genera Loris and Nycticebus
occur in the area, but we were unable to identify them
from photographs. Among the animals recorded, eight
were mammals (four species of Rodentia, two Primates,
one Carnivora, one Chiroptera) and four were birds
(Table 3). Miura et al. (1997) have previously recorded
all of these animal groups on the ground in Pasoh forest
in peninsula Malaysia, which suggests that these animals
move between arboreal layers and the ground. They
reported 35 animal species. Only the loris (species
unidentified) was newly recorded during this study as a
nocturnal arboreal frugivore.
Timing of visits
Our study was able to reveal not only diurnal animals
but also nocturnal animals visiting fruit (Table 3).
Among the animals recorded, seven species visited fruits
during daytime, and the others (4 species and murids)
at night. The major diurnal visitors were: the western
purple–faced leaf monkey Trachypithecus vetulus, the
western giant squirrel Ratufa macroura melanochra, the
Sri Lanka mynah Gracula ptilogenys, and the Sri Lanka
grey hornbill Ocyceros gingalensis (Table 3). The
major nocturnal visitors were: the small flying squirrel
Petynomys fuscocapillus layardi and a bat (Table 3).
Five fruit species, Artocarpus nobilis, Coscinium fenestratum, Cullenia rosayroana, Diospyros racemosa, and
Semecarpus walkeri were visited during both day and
Jayasekara et al., Frugivores in a Sri Lankan forest
163
Table 3. List of frugivore species taken by automatic cameras. * bold letters show nocturnal visits, and plain letters show diurnal visits.
Group
Rodentia
Primates
Chiroptera
Carnivora
Mammal total
Birds
Common name
Abbreviations
Murids
Jungle squirrel
Western giant squirrel
Small flying squirrel
Purple face leaf monkey
Loris
Bats
Golden palm civet
Murid
J. squirrel
G. squirrel
F. squirrel
L. monkey
Loris
Bat
G. civet
Sri Lanka mynah
Sri Lanka grey hornbill
Ashy headed laughing thrush
Sri Lanka orange billed babbler
Mynah
Hornbill
Thrush
Babbler
Scientific name
Number of visits
28
21
65
88
90
19
41
9
361
60
40
9
9
118
479
Funambulus sublineatus obscurus
Ratufa macroura melanochra
Petynomys fuscocapillus layardi
Trachypithecus vetulus
Loris sp. or Nycticebus sp.
Paradoxurus zeylonensis
Gracula ptilogenys
Ocyceros gingalensis
Garrulax cinereifrons
Turdoides rufescens
Bird total
Grand total
Table 4.
Fruit species
Frequency of visit (/day) to each fruit by each frugivores. See Table 3 for animal name abbreviations.
Murid J. squirrel F. squirrel G. squirrel L. monkey G. civet Loris
Artocarpus nobilis
—
Coscinium fenestratum
Cullenia ceylanica
Cullenia rosayroana
—
—
3
Diospyros racemosa
—
0.9
—
Dysoxylum ficiforme
—
—
—
—
Garcinia hermonii
0.9
—
—
—
—
—
—
—
—
Myristica dactyloides
—
—
—
—
—
—
—
—
2.3
Podadenia thwaitesii
—
—
—
—
1.1
—
—
—
—
Semecarpus walkeri
—
1
1.3
—
—
—
—
—
Number of species visited
2
2
3
2
4
1
2
2
2.4
2
5.3
4.5
5.6
1
1.5
2.9
Number of visits
1.5
—
—
1.5
—
—
3
—
—
—
—
—
—
—
—
2
—
—
1
—
—
—
—
1.4
—
—
—
—
2
—
1
—
0.5
—
—
—
0.4
0.4
5
—
1.1
—
—
1.5
—
—
—
—
3
2.4
—
—
—
—
—
—
—
1
—
—
—
1
1.5
—
—
2
—
—
—
1
—
—
—
—
2
1
1
1
1
2.3
1.5
0.4
0.4
night. The fruits of Dysoxylum ficiforme, Myristica
dactyloides, and Podadenia thwaitesii were visited only
during daytime, while those of Cullenia ceylanica and
Garcinia hermonii were visited only at night.
Dominant animal species
Mammals accounted for 361 of the 479 visits to fruit
(Table 3), and most of these (243 of 361) were made by
leaf monkeys, flying squirrels, and giant squirrels. Birds
made fewer visits than mammals, presumably because
the fruits we used were large, and only two species (the
mynah and the hornbill) accounted for most of the visits
(100 of 118).
It is noteworthy that the golden palm civet Paradoxu-
—
1
1
Bat Mynah Hornbill Babbler Thrush Total
—
—
—
—
—
3
rus zeylonensis, a member of the Carnivora, also visited
the fruits, indicating that they are omnivorous (see also
Boonsong and McNeely 1988; Miura et al. 1997). Two
species of insectivorous birds, the ashy headed laughing
thrush Garrulax cinereifrons and the Sri Lanka orangebilled babbler Turdoides rufescens also visited the fruits,
suggesting that they consume fruits opportunistically.
Fruit preferences
The leaf monkey visited four fruit species, but made
most visits to Dysoxylum ficiforme (Table 4). The fruit
of D. ficiforme is brown, and contains juicy, soft pulp,
and has fruit protection (Table 1). Fruits with such
characters are known as typical monkey-preferred fruits
164
(Gautier-Hion et al. 1985). The flying squirrel visited
three fruit species (Cullenia rosayroana, Cullenia
ceylanica, and Semecarpus walkeri), but visited C.
rosayroana most frequently (Table 4).
Murids visited two fruit species, Coscinium fenestratum and Garcinia hermonii, both of which contained
relatively small amounts of pulp. The giant squirrel, the
dusky-striped jungle squirrel Funambulus sublineatus
obscurus and a loris species visited fruits with very different characters. For example, the giant squirrel visited
both Artocarpus nobilis and Coscinium fenestratum
(Table 4). A. nobilis produces large compound fruit with
large amounts of juicy fibrous pulp, while C. fenestratum
produces small drupes with very little juicy, soft pulp
(Table 1). Thus the giant squirrel chooses widely
varying fruit types. The jungle squirrel visited both
Diospyros racemosa and Semecarpus walkeri, and it
seems that both the jungle squirrel and the loris species
take widely varying fruit types.
Among the birds, both the mynah and the hornbill
visited specifically Myristica dactyloides. The aril of
which is bright orange. Such colorful fruits are known as
typical bird preferred fruits (Knight and Siegfried 1983).
Cullenia rosayroana was visited by five different
frugivores (Table 4). It produces dehiscent fruits that
seem easier to handle and eat for animals that have
neither special morphology nor skills. This type of fruit
may be used by various frugivores, thus it is a generalist
in terms of attracting frugivores.
By contrast, Dysoxylum ficiforme, Podadenia thwaitesii, and Garcinia hermonii were visited by a limited
numbers of animals. Dysoxylum ficiforme and P. thwaitesii were visited only by the leaf monkey, and Garcinia
hermonii was visited only by murids (Table 4). They are
specialists in attracting frugivores. It is likely that protection of D. ficiforme, for example, limits visitors other
than leaf monkeys, which have strong fingernails, and
these fruit characters attract particular animals that have
special morphology or skills to consume them (Turner
2001). However, the functional aspects of these fruit
characters are mostly unknown.
Conclusions
The present study has confirmed that a considerable
number of species of frugivores may be active in the
arboreal layers in tropical forests at night as well as
during daytime. Clearly, conclusions concerning the
arboreal frugivore community of a tropical forest are
Mammal Study
28 (2003)
likely to be biased and misleading without due consideration of nocturnal animals.
Acknowledgments: We are grateful to the Forest Department of Sri Lanka, for granting permission to work in
the Sinharaja forest. The Forest Department Office of
the Sinharaja forest reserve supported us in numerous
ways. Professors I. A. U. N. Gunatilleke and C. V. S.
Gunatilleke at Peradeniya University gave many valuable suggestions and advice. Without Mr. Rupasinghe’s
tree climbing to set cameras in the canopy layer, this
study would have been impossible. Dr. M. Yasuda
advised us on automatic camera mechanics. Professor
T. Kikuchi of Yokohama National University, and Professor H. Koizumi of Gifu University encouraged us
throughout this study. We also thank Dr. Monika
Shaffer-Fehre, Dr. Mark Carine, and Dr. Mark A. Brazil
for helpful comments on the manuscript. This study was
partly supported by the Nagao Foundation (Japan) and
the Centre for International Development at Harvard
University, USA.
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