113

A Tropical Montane Forest in Borneo
as a Source of Fruit Supply for Frugivorous Birds
Kazuya KIMURA
Institute of Nature and Environmental Technology, Kanazawa University,
Kakuma, Kanazawa, Ishikawa, 920-1192 Japane-mail: kimura@kenroku.kanazawa-u.ac.jp

Abstract
An altitudinal survey of correspondences between fruiting phenology of fleshy-fruited tree species
and seasonal dynamics of frugivorous birds was carried out for 50 weeks across three vegetation types
on Mt. Kinabalu, Borneo: a hill forest (800 m a.s.l.), a lower montane forest (1,700 m a.s.l.) and asubalpine forest (3,100 m a.s.l.). In the hill forest, a large fruiting peak following the general flowering
period was observed during October–November in 1996 and a marked fruitless period was observed
during February–April in 1997. During the fruitless period, the number of resident frugivorous birds
decreased in some families. In the lower montane forest, a bimodal fruiting pattern was observed. Alarge number of frugivorous temperate migrants occurred and removed a lot of the fruit when the
fruiting peak occurred. The number of resident frugivorous birds increased and several lowland bird
species were observed when the number of resident birds decreased in the hill forest. In the subalpine
forest, more continuous and irregular fruiting patterns without outstanding peaks were observed and thenumber of resident frugivorous birds was more stable throughout the year. These suggested (1)temperate migrants visited mainly the lower montane forest to obtain fruit resources and (2) altitudinal
movements of lowland bird species to montane vegetation might occur seasonally, revealing thatseasonal movements and migrations to track fruit resources might be common among frugivorous birds
occurring on Mt. Kinabalu.
Key words: altitudinal migrant, frugivorous bird, fruiting seasonality, lower montane forest,
Mt. Kinabalu, temperate migrant.

1. Introduction
Frugivorous birds move and migrate tracking fruit
resources (Corlett, 1990; Karr, 1976; Leighton &Leighton, 1983; Levey, 1988; Loiselle & Blake, 1991;
van Schaik et al., 1993; Wich & van Schaik, 2000).
In temperate regions, migratory frugivorous birds
which have finished breeding in the north arrive whenfruiting species bear abundant fruit, and consume alarge amount of the fruit (Fuentes, 1992; Herrera,
1984, 1998; Kominami, 1987; Okamoto & Kitajima
1992; Sorensen, 1981; Stapanian, 1982; Thompson &Willson, 1979). In subtropical and tropical regions
where most of the temperate migrants overwinter,
fruiting species produce fruit during theiroverwintering period and provide fruit resources forthem (Noma & Yumoto, 1997). However, tracking
movements of temperate migrants were observed even
where they were the overwintering (Loiselle & Blake,1991).
Also resident frugivorous birds wereobserved moving locally within their habitats(Leighton & Leighton, 1983; Levey, 1988; Loiselle &Blake, 1991; van Schaik et al., 1993), although thedestinations, seasonality and periodicity have not beenclarified for the most part.
In Southeast Asia, a tropical montane area has been
noticed as a destination for migratory frugivorous
birds. Leighton & Leighton (1983) reported that the
number of inhabiting hornbills and pigeons decreased
with decreasing number of fruiting species in alowland forest of Borneo. They suggested montane
regions as one of the destinations of the disappearing
birds. Wells (1990) noted that in the Greater Sunda
regions, frugivorous birds, including temperatemigrants, were often observed in montane regions,and suggested that fruit resource conditions might bemore comfortable in the montane regions. However,no provable study has been reported associating aseasonal change in fruiting conditions with seasonal
dynamics of frugivorous birds in montane regions ofSoutheast Asia.
In this paper, the correspondence between fruiting
phenology and seasonal dynamics of frugivorous birds
are investigated in three forest types located from the

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K. KIMURA

foothills to the mountainside of a Bornean tropicalmountain, in order to clarify the tracking movementsof frugivorous birds on a tropical mountain in Southeast Asia.

2. Study Sites
Mt. Kinabalu is located at 6˚5'N and 160˚33'E innorthern Borneo (Fig. 1). The mountain is 4,095 m
high and several vegetation types appear and disappear altitudinally from the foothills to the summit.
The vegetation types had been classified by several
researchers. This study followed the classification
by Kitayama (1992).
Fieldwork was carried out in Kinabalu Park established in 1964 surrounding the mountain area. Threestudy sites were placed in three vegetation types, thatis, subalpine forest, lower montane forest and hill
forest. The highest site was Paka Cave (PAKA) located at an altitude of 3,100 m in a subalpine forest.
Conspicuous canopy trees were Dacrycarpus
kinabaluensis (Wasscher) de Laubenfels, Ilex, Leptospermum recurvum Hook. f., Lithocarpus havilandii(Stapf) Barnett, Myrica javanica Bl., and Phyllocladus
hypophyllus Hk.f. Small trees and shrubs, Ardisia,
Drymis piperita (Hook.f.) Miers., Ilex, Photinia,
Rapanea, Schefflera, Rhododendron, Rubus andVaccinium are common. The second site was Park
Headquarters (PHQ) located at an altitude of 1,700 m

in a lower montane forest, below the lower limit of thecloud belt. Agathis, Castanopsis, Caulophyllum,
Dacrycarpus, Dacrydium, Magnolia, Palaquim,
Payena, Phyllocladus hypophyllus, Lithocarpus,
Schima wallichii (DC.) Korth., Symplocos, Syzyzium
and Tristaniopsis trees were dominant in the forest
canopy and subcanopy. Numerous small trees andshrubs, Ardisia, Diplycosia, Ficus, Litsea, Medinilla,
Psychotria, Rhododendron, Symplocos and Vaccinium
occurred. The lowest site was Poring (PORING)
located at an altitude of 800 m in a hill forest. The
forest canopy reached 40-50 m in height. Parashorea, Shorea and Dipterocarpus of the Dipterocarpaceae, Koompasia, and Pangium were conspicuous canopy trees. The Canopy Walkway System
was useful for observations, with walkways spaning
158 m in total length at 5-40 m above the ground.
Mt. Kinabalu is located in a humid tropical climate.
The daily mean air temperature is roughly constant all
year round (Kitayama, 1992). There is no dry season,
although severe droughts have occurred once every
several years and have been reported to cause damage
to vegetation (Kitayama, 1996; Kudo & Kitayama,
1999).
One observation period of this study (from July
1996 to June 1997) appeared to be under normal
seasonal trends (Kitayama et al., 1998). Figure 2
shows month-to-month changes in the mean air
temperature and the monthly rainfall derived from theFig. 1 Location of Mt. Kinabalu in the Greater Sunda region.

Seasonality of fruiting and frugivorous birds
30
20

400

10

200

0
30

0
600

(b)

20

400

10

200

0
30

0
600

(c)

20

400

10

200

0

Jul Aug Sep Oct Nov Dec Jan Feb Mar Apr May Jun
96
97

0

Total rainfall (mm)Mean air temperature (℃)

600

(a)

115

most of the marked trees and were identified bymatching them to specimens in the herbaria of
Kinabalu Park and the Forest Research Centre, Sabah
Forestry Department, Sandakan, Malaysia.
To find trends of fruiting phenology in the plantcommunity of each site, I recognized six types offruiting frequency based on frequencies of floweringand fruiting during the study period, referring toNewstrom et al. (1994). These types were ‘continuous (c-) type’, ‘biannual (a2-) type’, ‘annual (a1-)
type’, ‘annual with only fruiting (a1/fr-) type’, ‘noreproduction (nr)’ and ‘others’. The c-type included
plants that bore fruit without a clear intermittence ofreproduction. The a2- and a1-types bore fruits twiceand once a year, respectively. The plants of the a1/frtype were only observed to fruit during the observation period as the result of flowering in the previous period. The ‘others’ included species which
flowered without fruiting. We defined the fruiting
frequency types for particular species based on theindividuals which reproduced most frequently.

MonthFig. 2 Seasonal changes in the monthly mean air temperature(line) and total rainfall (bar) at the three study sites on
Mt. Kinabalu, after Kitayama et al. (1999). From thetop, (a) PAKA, (b) PHQ and (c) PORING.

climate stations which had been set up in an open
place at the median altitude of each vegetation zone
(Laban Rata [3,300 m], PHQ [1,700 m] and PORING[800 m]), after Kitayama et al. (1998). The temperature changed little during the entire observation period
at all sites, although a very slight depression oftemperature was recorded from December to March at
PHQ and PORING. Annual total rainfall ranged
from ca. 2,500 mm to 3,000 mm at all sites. A
synchronous change in rainfall was observed between
Laban Rata and PHQ; prominent peaks occurred in
November and February. The pattern of rainfall at
PORING was different from the others; prominent
peaks occurred in December and February-March.
Although there was no defined dry season, themonthly rainfall did not reach 100 mm in March andJune in Laban Rata and January and June at PORING.

3. Methods
3.1 Fruiting phenology
The fruiting phenology of fleshy-fruited plant
species at the three sites was shown based on recordsof 398 trees/shrubs bearing mature fleshy fruit whichwere observed biweekly from July 1996 until June
1997. We defined ‘fruiting species’ as those inwhich at least one individual was bearing fruit foreach census, and calculated the ratio of the number ofthe fruiting species to the total number of observed
species at each site.
“Fleshy-fruited plants” in this study means ones
which have seeds surrounded by or attached to an
edible part. Voucher specimens were collected from

3.2 Bird census
Biweekly bird censuses were conducted in order toinvestigate seasonal changes in frugivorous birds at all
study sites. The majority of birds recorded in
Borneo were distributed in the region of Mt. Kinabalu(MacKinnon & Phillipps, 1993). A total of 326
species have been documented in Kinabalu Park, andthey have been categorized into three groups based on
their altitudinal zonations: lowland, lower montane
and upper montane (Biun, 1999), corresponding to thethree study sites.
Methods were as follows: at PAKA and PHQ,
route censuses were conducted from 0600 to 0800
along a census route 2 km in length. The route was
the summit trail from Laban Rata (3,300 m) to Carson
Camp (2,700 m) and the road near PHQ (ca. 1,700 m).
In the censuses, the number and species of birds
appearing or singing within a radius of 25 m fromobservation points were recorded. At PORING, I
started at 0600 and observed for 30 min each fromthree fixed points: at an edge of the forest, inside theforest (forest understorey), and on the Canopy Walkway System (forest canopy). Birds which appeared
within a semi-circle with a radius of 25 m from thefixed point were recorded.
The reason for applying a different method at
PORING was that it was too difficult to identify birds
in the forest canopy from the ground because thecanopy trees were too tall and because subcanopy
trees hindered my upward view.
This method
revealed seasonal changes in birds better, covering
more bird species than route censuses would havedone, although this does not allow comparison of thebird density at PORING with the others.
Very few specific descriptions associated with
diets of birds on Mt. Kinabalu are available. Accordingly, we chose major frugivorous species which are

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K. KIMURA

occurrence of the a1/fr-type was overwhelmingly
higher than those at the montane sites (Chi-square test,
χ2=19.8, df=2, p<0.001). Fleshy-fruited plant communities at PAKA included more plants with unclear
fruiting seasons. Those at PHQ included more plants
with clear fruiting seasons, while, those at PORING
included more plants with clear fruiting seasons in asupra-annual cycle.

highly or more frugivorous and minor frugivorous
species which are partially frugivorous (Appendix,
after Kimura et al., 2001), referring to Corlett (1998),
Davison (1992), Leighton & Leighton (1983),
MacKinnon & Phillipps (1993) and Smythies (1999)
and my observations on their feeding behaviour.
Nine families including major frugivores wererecognized: Columbidae (doves and pigeons),
Bucerotidae (hornbills), Megalaimidae (barbets),
Eurylaimidae (broadbills), Aegithinidae (leafbirds),
Pycnonotidae(bulbuls),
Turdidae(thrushes),
Dicaeidae (flowerpeckers), and Corvidae (treepies).
Frugivorous species were categorized into threegroups based on the scale of their seasonal movement(Loiselle & Blake, 1991). The first was ‘resident’
which included resident species of Borneo that occur
in a specific vegetation type all year round. The
second was ‘altitudinal migrant’ which was also
resident species but occurred seasonally across vegetation zones on Mt. Kinabalu. The third was ‘temperate migrant’ which bred in the temperate regions andappeared in the tropical regions during their nonbreeding seasons. Most of the temperate migrants in
the regions come from the north (MacKinnon &Phillipps, 1993). Wells (1990) recorded two temperate migrants, Turdus obscurus Gmelin and Zootherasibirica (Pallas), which eat fruit in the mountains of
the Greater Sunda regions. T. obscurus is a regular
winter visitor to hill and mountain forests of northern
Borneo, but Z. sibirica is a rare visitor to northern
Borneo.

4.2 Fruiting phenology of fleshy-fruited plants
Seasonal patterns in the total number of fruiting
species at the three sites were divided mainly into
three groups by the results of Spearman’s rank correlation test. The first was a montane group at PAKA
and the second was a lowland group at PORING.
The seasonality of the montane group was that fruiting
was less marked and there was no fruitless period,
while that of the lowland group was highly marked
and there was a fruitless period (Fig. 3). The lastgroup was found at PHQ having an intermediate
pattern between these two groups because its seasonalchanges had significant positive correlations with theall other sites. The seasonality of PHQ showed abalanced bimodal pattern with no fruitless period.
Detailed explanations about the seasonality are as
follows (Fig. 3):
PAKA – Several peaks occurred throughout the year,
but there was no outstanding one. Seasonal patterns
of fruiting frequency types except for the a1/fr-type
had significant positive correlations with the pattern of
total fruiting species (Spearman’s rank correlation test,
p<0.05). Although a2- and a1-type species should
exhibit clear fruiting seasons, they did not show anaggregated fruiting trend at the community level but
synchronized with the seasonal pattern of the c-type.
PHQ – A bimodal pattern was observed, with peaks in
October-December 1996 and April 1997.
The
seasonal pattern of the a1-type had a very strong
positive correlation with the pattern of total fruiting
species (Spearman’s rank correlation test, p<0.0001),
although those of c-type, sc-type and a2-type species
also had significant positive correlations.
PORING – An unbalanced bimodal pattern wasobserved; large outstanding peaks during OctoberNovember 1996 and a very small peak in May 1997.
A fruitless period was observed from February to
April 1997. Seasonal patterns of the a1-type and

4. Results
4.1 Fruiting frequency types of fleshy-fruitedplantsDifferent compositions of fruiting frequency typesof fleshy-fruited plant species were clarified among
the three sites (Table 1). Annual fruiting types
represented by the a2-type and a1-type were the mostfrequent at all sites, although there was no significant
difference among sites. The proportion of the annualtypes at PHQ was 49.3%, the highest among the sites.
The occurrence of the c-type was significantly higher
in PAKA (Chi-square test, χ2=14.0, df=2, p<0.01).
At PORING, c-type species were not observed and theTable 1 Number of fleshy-fruited plant species observed at the three study sites on Mt. Kinabalu.
Fruiting frequency types
Study site

N

c

a2

a1

al/fr

nr

othersPAKA

37 (143)

10

8

7

2

5

5

PHQ

73 (166)

7

9

27

5

10

15

POR
46 (89)0
512
17c: continuous, a2: biannual, a1: annual, a1/fr: annual (only fruiting), nr: no reproduction,others: species which flowered without fruiting.
( ): number of observed individuals.

84Seasonality of fruiting and frugivorous birds

Fig. 3

Seasonal changes in proportion of fruiting species tothe total reproducing species at the three study sites,
showing seasonal changes of respective types offruiting frequency; c - continuous, a2 - biannual, a1 annual, and a1/fr - annual (only fruiting).

a1/fr-type had strong positive correlations with thepattern of total fruiting species (Spearman’s rankcorrelation test, p<0.0001), but major fruiting seasonsof both types were different. The major fruiting peakof the a1-type occurred at the end of September andthe peaks of a1/fr-type occurred at that time and in the
middle of November.
4.3 Seasonal dynamics of frugivorous birds
Thirty-nine bird species of nine frugivorous families were recorded in the censuses and six more
species were observed out of censuses at all sites(Table 2). The greater part of frugivorous species of
Bucerotidae, Megalaimidae, Eurylaimidae, Aegithi-

117

nidae, Pycnonotidae and Dicaeidae occurred in
PORING. While, the frugivorous species of Turdidae and Corvidae tended to occur at the montane sites,in particular, one of thrushes, Turdus poliocephalus
Latham, was unique to PAKA. Forty-four species
were residents. Only one species, Turdus obscurus,
which was a temperate migrant and occurred at PHQ
and PAKA.
Columbidae,
Megalaimidae,
Aegithinidae,
Pycnonotidae, and Turdidae species were frequently
observed eating fruit of various fleshy-fruited species:
Ilex (Aquifoliaceae), Schefflera (Araliaceae), Daphniphyllum (Daphniphyllacaceae), Elaeocarpus (Elaeocarpaceae), Vaccinium (Ericaceae), Macaranga(Euphorbiaceae), Lindera and Litsea (Lauraceae),Medinilla (Melastomataceae), Myrica (Myricaceae),
Ficus (Moraceae), Ardisia (Myrsinaceae), Syzyzium(Myrtaceae), Olea (Oleaceae), Dacrycarpus andDacrydium (Podocarpaceae), Photinia and Rubus(Rosaceae), Symplocos (Symplocaceae), Boehmeria(Urticaceae), Drymis (Winteraceae), and so on(unpublished data).
Major frugivorous resident species occurred at allsites but no major frugivorous temperate migrants
were observed at PORING. Seasonal changes in thenumber of residents and temperate migrants are shownin Fig. 4:
PAKA – There was no prominent seasonal change
in the number of major frugivorous resident species.
Four resident species, Macropygia ruficeps, Megalaima pulcherrima, Turdus poliocephalus and Pycnonotus flavescens were common members. Two tofour resident species appeared in every census except
July under windy conditions. Turdus poliocephalus
occurred in every census and Pycnonotus flavescens
often occurred. A temperate migrant species (T.
obscurus) was observed in early December 1996.
The number of major frugivorous resident species
fluctuated irregularly through the year. The number
increased in September-October, December, JanuaryFebruary and April. The highest number was inearly December 1996 when four individuals of T.
obscurus occurred.

Table 2 Observed number of frugivorous bird species of nine families at the three study sites.
FamilyColumbidae
Bucerotidae
Megalaimidae
Eurylaimidae
Aegithinidae
Pycnonotidae
Turdidae
Dicaeidae
CorvidaeTaxonomic groups
Pigeons & Doves
Hornbills
Barbets
Broadbills
Leafbirds & Bluebirds
Bulbuls
Thrushes
Flowerpeckers
Treepies
Total( ): number of species observed out of the census.

PAKA
1
1(1)
1
0
0
1
4(2)
0
1
9(3)

Site
PHQ
3
1
2
1
2(2)
3(1)
3
2(1)
1
18(4)

POR
2
3(2)
6(1)
3(1)
4
10(2)
1
4(1)
1(1)
25(8)

Total
4
3(1)
8(1)
4(1)
4
12(1)
4
5(2)
1
45(6)

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K. KIMURA

Fig. 4 Seasonal changes in the number of frugivorous bird species (left) and individuals (right) observed at the threestudy sites: major frugivorous residents (red), minor frugivorous residents (white) and temperate migrants(slash).

PHQ – The number of major resident frugivorous
species from the end of January to March exceeded
six species (Ducula badia, Macropygia ruficeps,
Megalaima pulcherrima, Alophoixus ochraceus,
Dicaeum monticolum and Dendrocitta cinerascens)which was estimated as the number of regular speciesof the censuses. This increase was caused by aconcentration of occurrences of irregular montane
species and by the rare occurrences of lowland species,that is, Macropygia phasianella, Rhyticeros undulatus
and Pycnonotus atriceps.
The number of individuals of major resident
frugivorous species increased during August-October
and January-March. The former period was due toparticularly large numbers of Columbidae species (D.
badia and M. ruficeps). The latter was caused by anincrease in the number of species.
The occurrence of T. obscurus, a major frugivorous temperate migrant, produced a large peak of
individuals in November 1996. The number of individuals in the peak reached 30, more than the summed
number of individuals of all major frugivorous residents in that census. They were observed from
November 1996 to March 1997 at all sites according
to the census data and non-census data. During thefive months, they overwintered in the Kinabalu region.
PORING – The number of major frugivorous

resident species fluctuated irregularly through the year.
Outstanding decreases in the number were recorded
during November-December and February-Marchwhen only one or two species occurred. The two
periods of decline resulted from fewer observations ofmajor frugivorous taxonomic groups, such as barbets,
leafbirds and bulbuls.
The seasonal pattern of the number of individuals
mirrored the pattern of species. Prominent decreases
were observed during November-December andFebruary-March.
4.4 Seasonal dynamics of each frugivorous bird
familySeasonal changes in the number of individuals ofnine families including major frugivorous species areshown in Fig. 5. Major frugivorous species ofColumbidae, Megalaimidae and Pycnonotidae wereobserved at all sites. Individuals of these families
occurred frequently at PHQ and PORING. However,there were some periods when the number of individuals decreased at PORING but increased at PHQ or
PAKA: during January-March in Columbidae, during
February-March in Megalaimidae and during
November-December and February-March in Pycnonotidae. The increases during the latter period atmontane sites were caused not only by an increase inSeasonality of fruiting and frugivorous birds

individuals of regular species but also an influx ofindividuals of lowland species, such as a dove(Macropygia phasianella) and a bulbul (Pycnonotus
atriceps).
Bucerotidae species were rarely observed at PHQ
and PORING. A few individuals of Rhyticeros
undulatus were observed during January-March in
PHQ or moving up or down along the mountain slope.
Only a single individual of Anthracoceros malayanus
occurred in February 1997 at PORING. Away fromthe study sites, I saw R. undulatus in July 1996 andBuceros vigil in September 1996 and March 1997 in
the foothills of Mt. Kinabalu.
Eurylaimidae, Aegithinidae and Dicaeidae wereobserved occasionally at PHQ and PORING. Two
major frugivorous broadbills, Calyptomena viridis andC. whiteheadi are common residents in lowland andmontane forests, respectively (Smythies, 1999).
However, I had few records because they live mainly
deep in the forests and are difficult to observe. One
Columbidae

119

major frugivorous species of Aegithinidae, Chloropsis
cochinchinensis, was observed eating fruit of Daphniphyllum sp. in April 1997 at PHQ, though no individual of Aegithinidae was recorded during the census.
The major frugivorous species of Turdidae andCorvidae were common at the montane sites. Individuals of Turdidae occurred less frequently and moreseasonally at PHQ than at PAKA. Temperate migrants of T. obscurus amounting to seven times morethan those at PAKA came to PHQ in November 1996.
After November 1996, a few individuals of T.
obscurus were sometimes observed out of censuses
until March 1997. Individuals of the Corvidae also
occurred more commonly at PHQ than at PAKA.
It was probable that the Columbidae, Megalaimidae, Pycnonotidae, Bucerotidae and Aegithinidae
included altitudinal migrants. In the case of the Columbidae, Megalaimidae and Pycnonotidae, the increase in the number of individuals at PHQ corresponded with a decrease in the number of individuals at

Bucerotidae

10

TurdidaeTurdidae
PAKA

5
0
30
20
10
0
10

PHQ

PORING

5

Megalaimidae

Aegithinidae

Observed number of individuals per census

0
J A S O

Eurylaimidae

J

PAKA

0
5

PHQ

Dicaeidae

0
J A S O

0
15
10
5
0

F M A M J

Dicaeidae

55

Pycnonotidae

N D

N D

J

F M A M J

Corvidae
PAKA

CorvidaePHQ

J A S ON D

JF M A M J

Month

Month

Month

Month

Fig. 5 Seasonal changes in the number of individuals of nine families which include major frugivorous species at the three study
sites. Three categories of frugivore are shown; major frugivorous residents (line), minor frugivorous residents (dotted line)
and temperate migrants (red). Arrows indicate periods when the observed number at PHQ increased as the number decreased
at PORING.

120

K. KIMURAPORING during the fruitless period at PORING.
Some individuals of lowland species of the Aegithinidae were also observed at PHQ during the fruitless period. M. phasianella, P. atriceps and C.
cochinchinensis, were likely to be altitudinal migrants.
Species of Bucerotidae inhabiting mainly the lowlands
departed the study sites during the fruitless period.
Among them, R. undulatus moved over a wider range
altitudinally. Megalaima monticola, which usuallyoccurs below 1,600 m, was also likely to be an
altitudinal migrant.

and the accumulated events formed a fruiting peak in
October 1996. In November 1996, mainly temperatemigrants removed the fruit. Accumulated fruiting
events during the migration period formed a fruiting
peak in December 1996, and fruit removal by temperate migrants occurred again. After the second
fruit removal in December 1996, a smaller amount offruit corresponding to a smaller number of start-offruiting events was consumed by a small number ofresidents and temperate migrants staying at PHQ.

5. Discussion
4.5 Relationship between fruiting seasons andmigration periods of temperate migrants
A relationship emerged between the seasonal dynamics of fruiting events and migration periods. We
tried to find the relationship at PHQ by dividing theobservation period into four terms: pre-migration term(the first 9 censuses), migration term (the next 3
censuses), overwintering term (the next 8 censuses)and post-overwintering term (the last 5 censuses).
Table 3 shows the number of start/end of fruiting
events in each term. The number of ‘start-of-fruiting
events’ means the number of trees that bore mature
fruit newly in each census, and the number of ‘end-offruiting events’ means the number of individuals that
had all of their fruit removed or lost in each census.
There was no significant difference in the start offruiting events among the four terms as indicated by achi-squared test, showing that there was no seasonal
trend in the number of start-of-fruiting events throughout the year. However, when the overwintering term
was combined with the migration term, there was asignificantly smaller number in the combined period(χ2=6.80, df=2, p<0.05). As for end-of-fruiting
events, only the migration term had a significant large
number (χ2=11.3, df=3, p<0.01). This suggests thatfruit removal from trees might be concentrated whentemperate migrants arrived at PHQ.
Comparison with the fruiting phenology at PHQ
revealed the following scenario: start-of-fruiting
events accumulated during the pre-migration period,

The difference in fruiting phenologies among thethree sites played an important role in dietary supportof frugivorous birds which were seen in the Mt.
Kinabalu region. In particular, the fruiting phenological groups observed in the lower montane forests
were very important for altitudinal migrants from thelowlands and temperate migrants.
In hill forests, regular fruiting seasons and fruitlessseasons occurred with a large year-to-year fluctuationin the number of fruiting species. This fluctuation
was caused by a mast fruiting (mass flowering) phenomenon, which is common in lowland forests ofSoutheast Asia and is unpredictable because the phenomenon occurs once every several years (Appanah,
1985; Ashton et al., 1989; Kitayama et al., 1998;
Sakai et al., 1999).
These unstable fruiting
conditions make lowland frugivorous birds move orchange their diet. This study showed the movementof lowland birds tracking fruit resources, suggestingthat an altitudinal difference in fruiting seasonality
encouraged the birds to move to montane forests (vanShaick et al., 1993) (Fig. 6). In Costa Rica, theTable 3 The number of starts and ends of fruiting events offleshy-fruited plants at PHQ during the four terms.
Premigration
term

MigraOver- Post-overtion
wintering wintering Total
term
term
term

Duration(number ofcensuses)

9

3

8

5

25

Starts offruiting
events

28

4

16

20

68

Ends offruiting
events

13

13

9

14

49

Fig. 6 A scheme of tracking movements of frugivorous birds
on Mt. Kinabalu. Arrows indicate the direction of
movements of residents (blue), temperate migrants(green) and altitudinal migrants (red) from theirbreeding regions. Dotted arrows indicate their probablemovements.

Seasonality of fruiting and frugivorous birds

opposite direction of movement from montane area tolowlands was reported (Loiselle & Blake, 1991).
These altitudinal migrations corresponding to local
fruit conditions suggest the behaviour of frugivorous
birds tracking fruit resources might be flexible.
Some studies indicated that a tropical montane
region was one of the destinations supplying fruit
resources during periods of fruit scarcity in lowland
forests of the Greater Sunda region (Leighton &Leighton, 1983; van Schaik et al., 1993; Wells, 1990).
The present study supports these studies.
The
montane region of Mt. Kinabalu was probably one ofthe destinations because the increase in the number of
species and individuals at montane sites was not soprominent, suggesting that the scale of altitudinal
movements was not so large. Many studies explained that large lowland birds such as hornbills andpigeons were possible altitudinal migrants because of
their expected long flying range (Leighton & Leighton,1983). However, small birds such as barbets, bulbuls
and leafbirds moved up to montane regions, althoughsurrounding geographical features may have influenced their movements.
Not only altitudinal migrants but also temperatemigrants utilized montane forests for their feedingsites (Fig. 6). The fruiting peak in November 1996
at PHQ was explainable as very convenient for thearriving temperate migrants. The lower montane
forests which have regular fruiting seasons leading toa predictable fruit supply would be a favorable
visiting and overwintering site for regular temperatemigrants. This result supports the previous description by Wells (1990) that frugivorous temperatemigrants often occurred in montane area in the Greater
Sunda region.
T. obscurus must be an important fruit consumer
and seed disperser in lower montane forests of Mt.
Kinabalu, although its quality as a consumer anddisperser should be more thoroughly investigated.
Thrushes are important as migratory birds in fruit-bird
relationships in Asia (Kwok & Corlett, 1999; Noma &Yumoto, 1997; Wells, 1990) as well as on the othercontinents of the Northern Hemisphere (Blake &Loiselle, 1992; Herrera, 1995; Herrera & Jordano,
1981; Loiselle & Blake, 1991; Sorensen, 1981;
Thompson & Willson, 1979; Willson & Whelan,1993).
It was strange that most temperate migrants wereobserved in lower montane forests, even though there
was mature fruits during the migration and overwintering period in hill forests and subalpine forests.
It may be that the seasonal dynamics of temperatemigrants in the two forests may be influenced by thedensity and habits of resident species. In hill forests,
a number of mature fruits were certainly removed byresidents during the fruiting peak, although the fruiting peak had occurred before the migration period oftemperate migrants. Actually, many residents visited
fruiting trees one after another to remove fruits of121

Macaranga hypoleuca (Reichb. f. & Zoll.) Muell. andArdisia corolata Roxb. (unpublished data). In otherwords, the carrying capacity of fruit resources for
frugivores might have been saturated even in a mast
fruiting year. While in subalpine forests, the numberof frugivorous birds might not reach a level matching
the amount of available fruit, because an influx oflowland frugivores and temperate migrants was also
observed. As an alternative to the carrying capacity,
it is probable that T. obscurus competes for fruit resources against closely related species sharing thesame feeding guild (Wells, 1990), such as T. poliocephalus as a resident in the forests.
Tropical montane forests of Mt. Kinabalu holdmore regular and stable conditions in fruit resources
and provide temporal ‘refugia’ for many frugivorous
birds. The role as refugia may be very importantbecause there are more montaneous areas in Southeast
Asia (Whitmore, 1994). It is predictable that, formany lowland frugivorous birds, the tropical montane
forests will be more precious in non-mast-fruiting
years because the shortage of fruit resources in hill
forests will be more severe in non-mast-fruiting years
than in mast fruiting years such as the study period.
In addition, tropical montane forests, especially lower
montane forests, must provide a more precious overwintering area for many frugivorous temperate migrants in fruitless years in the north.

Acknowledgments
I am grateful to Datuk Lamri Ali, the Director, and
Mr. Francis Liew, Assistant Director of Sabah Parks,
for granting me permission for research activities. I
extend my thanks to Prof. Kanehiro Kitayama, Prof.
Kihachiro Kikuzawa, Dr. Takakazu Yumoto and Prof.
Masahiko Osawa for coordination of the cooperative
research project "EcoKinabalu" which gave me
invaluable advice. I thank Dr. Jamili Nais, Ms. Rimi
Repin, Mr. Maklarin Lakim, Mr. Gunik Gunsalam, Mr.
Ludi Apin, and all the Park staff for supporting ourfield work, and the staff of the Forest Research Centre,
Sabah Forestry Department, for helping identify plants.
Finally, I am obligated to Mr. Alim Biun for his
collaborative work in bird studies. This study was
supported by Grants in Aid from the Ministry of
Education, Science, Sports, and Culture of Japan(11691190, 08041148, 09NP1501, and 11213202).

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(Received on 9 January 2003, Accepted on 7 March 2003)