Maliau bird project

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Bird assemblage on a fruiting fig (Ficus caulocarpa) in Maliau Basin, Malaysia: analysis of species composition and foraging behaviour

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We analysed the species composition and abundance of birds in different layers on a fruiting hemi-epiphytic fig (Ficus caulocarpa) in Maliau Basin, Sabah, Malaysia. Observations were conducted for 32 hours over five days. Fourty-five species of birds were recorded. Overall the assemblage of large birds, such as hornbills, was poor, which may be due to the small size of the fruit. In contrast, the diversity of smaller bird species was relatively high. Most of the species preferred lower outer and mid-outer regions of the canopy. Inter and intra-specific aggressions were observed among the species foraging on the tree in competition for space and food. This study outlines the significance of Ficus caulocarpa to the smaller frugivorous bird species, especially the birds belonging to the family Pycnonotidae (Bulbuls). Sixty-nine percent of bird visits to the tree were Bulbuls belonging to 13 species.


Fruiting plants that provide critical resources for frugivores during periods of scarcity are known as keystone plant resources (Lambert and Marshall 1991, Leighton and Leighton 1983, Terborgh 1986a, Shanahan et al. 2001). Frugivores are an important group of vertebrates in the tropics and their diversity correlates with the abundance and diversity of fruits (Orians 1969, Karr 1976). Malaysian forests are extremely rich in Ficus species, with about 16% of known world species (Ng 1978). In Borneo there are over 160 Ficus species (Harrison 2005), which are probably the most important group of keystone plant resources (Leighton and Leighton 1983, Lambert and Marshall, 1991, Shanahan et al. 2001). They play an important role in sustaining the frugivore community over periods when food is in short supply (Terborgh 1986b, Kinnaird et al. 1999, Korine et al. 2000, Shanahan et al. 2001). Surveys of bird diets in both the New World (Snow and Snow 1971, Cruz 1974, Lack 1976, Morton 1973, Snow 1981, Wheelwright et al., 1984) and Old World (Terborgh and Diamond, 1970, Corlett 1998, Savini et al. 2009) shows that around 990 bird species feed on Ficus species (Shanahan et al. 2001).

The present study was designed specifically to examine spatial variations and abundance of birds visiting a fruiting Ficus caulocarpa individual over a 5-day period in Maliau Basin, Sabah, Malaysia. Here we discuss patterns of variability and their possible causes and consequences.

Study Area and Methods

This study was conducted in Maliau Basin Study Centre, Sabah, East Borneo from 14 – 17 July 2009 at a fruiting hemiepiphytic Ficus caulocarpa individual that was supported by a Koompassia excelsa tree. The fig had a crown volume of 1777 m3 and a fruit size of 5.4mm wide and 5.9 mm long. Maliau Basin is a pristine hill dipterocarp forest lying 40 50' North of the Equator, it has typical aseasonal climate with constant high temperature, humidity, and annual rainfall of approximately 3800 mm.

We observed the fruiting Ficus caulocarpa from a tree house about 20 m above the ground and 10m from the nearest edge of the fig canopy. We used two pairs of binoculars (10x50 and 8x42) and a camera with a 500mm zoom lens for documentation. We arrived at the station before 6 am and recorded all the vertebrates that visited the tree over five mornings from 06:00 – 11:30 and two afternoons from 13:00 -15:00. We divided the tree spatially: upper, medium, lower layers and inner and outer regions. We used chi-square tests to examine the pattern of spatial distribution of three groups of birds; frugivorous, insectivorous, and omnivorous. The birds less than 25 cm were categorized as small birds and the birds greater than or equal to 25 cm were categorized as larger birds. Smythies (1999) and MacKinnon and Phillipps (1993) were used to identify the birds and obtain details on their body size and biology.


Figure 1. Family composition of bird species recorded in the study. Number of species in the brackets
Table 1. Species composition and number of visits recorded. Up.out: upper and outer layer, outer and inner layer, Med.out: medium and outer layer, medium and inner layer, Low.out: lower and outer layer, lower and inner layer, En: endangered according to IUCN Red Book.
Table 2. Number of visits of three bird groups in different spatial layers.

During 32 hours of observation, 45 bird species were recorded to frequent the tree with a total of 491 visits during. Regarding species composition, three raptors, 19 frugivores, 11 insectivores, and 12 ominivores belonging to 17 families either foraged on the tree for fruits, insects or used the fig tree as a vantage to look for food(Fig.1). We found that species belonging to the family Pycnonotidae were the key species, contributing 13 species and 337 visits that is 69% of the total bird visits on the tree. Interestingly, 17 bird species that is 38% of the birds visiting this Fig tree are listed under the IUCN Red Book (see Table 1).

During 32 hours of observation, 45 bird species were recorded to frequent the tree with a total of 491 visits (Appendix 1). Regarding species composition, three raptors, 19 frugivores, 11 insectivores and 12 ominivores belonging to 17 families either foraged on the tree for fruits and insects or used the fig tree as a vantage to look for food. Eight species of large frugivores and raptors were observed perching on the tree without foraging, mostly in the early hours of the day. We found that species of the family Pycnonotidae were the most abundant species, contributing 13 species and 337 visits that are 69% of the total bird visits to the tree (Fig. 1). Small birds dominated in the tree with 32 species and 452 visits compared to larger bird species, which had only 14 species and 39 visits. However, larger bird species like Hornbills (Bucerotidae), Pigeons and Doves (Columbidae) were sighted around the tree in good numbers but the birds seldom visited the tree, and no recordings were made of these birds feeding on the figs. Interestingly, 17 bird species that is 38% of the birds that visited this fig tree are listed under the IUCN Red Book (Appendix 1).

Among the two vertical layers of the tree, the outer region (380 visits) attracted more number of birds than the inner region (111 visits). Among the three horizontal layers, the lower layer (237 visits) and the middle layers (218 visits) attracted the roughly same number of birds but visits to the upper layer were very few, less than 8%. Moreover, most of the birds that visited the upper part of the tree did not feed on figs. They mostly comprised bark gleaners, raptors and other birds that perched for preening and sunning. We tested the spatial pattern of foraging among feeding guilds and found there was a significant difference in the canopy use among the guilds (X2 = 68.6481; d.f. = 10; p = 8.082e-11).

We also noticed that birds visited the tree more frequently during the early morning and became less active in the afternoon. During the periods from 06:00 – 08:30, 08:30 – 11:00, and 13:00 – 15:00, the mean number of visits was 76, 36 and 19 respectively and the number of bird species visited was 37, 25 and 10 respectively.

Interspecific aggression was observed between Greater Green Leafbird Chloropsis sonnerati and Pycnontidae species, Lesser Green Leafbird Chloropsis cyanopogon and Dicaeidae species resulting in fast aerial chases. The Chloropsis species in all the observations chased away the smaller birds in the region before feeding on the figs. We also observed a pair of Jerdon’s Baza Aviceda jerdoni bornensis chasing Bulbuls (Pycnonotidae) into the bole region.

Intraspecific aggression was observed among Pycnontidae species, especially in Spectacled Bulbul Pycnonotus erythropthalmos and in Hairy-backed Bulbul Tricholestes criniger. The birds were very commonly sighted in fast aerial chases. Often two or three birds were observed chasing a bird of the same species. The birds were also sighted performing mid-air fights by interlocking their legs together and free-falling into the thickets below. When this occurred only one of the two Bulbuls returned to feed on figs.


A large number of birds comprising a high diversity species were recorded at the Ficus caulocarpa individual during its fruiting period. This can be attributed to the large crop size, synchrony of fruit ripening, and accessibility to fruits (Lambert and Marshall 1991). The thick foliage also offered some protection from predators and thus possibly attracting more mid-layer and canopy bird species. About 74% of bird species feeding on fruits were frugivore and omnivore species.

We also notice dominance in species composition by small sized birds with small gape size, such as Pycnonotidae, Irenidae and Dicaeidae with gape sizes 15-36 mm, 23-43 mm & 7-10 mm respectively (Lambert 1989). This most likely reflects the small size of the fruit. For larger birds it may not be an efficient investment of energy to feed on such small figs. Our observation supported previous studies in Peninsular Malaysia and Borneo in which large and small birds prefer large and small fig fruits accordingly (Lambert 1989, Shanahan and Compton 2001).

Some hemi-epiphytic figs with large fruit are known to depend on large vertebrates like Hornbills to disperse their seeds (Harrison et al. 2003, Harrison 2005, Harrison and Shanahan 2005), which in turn provide a high quality dispersal service as they fly large distances and perch in the crowns of large trees (Corlett 1998). However, such species also lose a large proportion of their crops to seed predators, such as Green Pigeons (Shanahan et al 2001). Thus, figs with smaller fruit may escape seed predators to a greater extent but are more dependent on smaller birds which are likely to disperse the seeds shorter distances and often to unfavourable sites in the understorey.


We thank all the staff and students of Biodiversity of Borneo (BoB) course and all the Maliau Basin park rangers for their constructive suggestions and support during the study. Special thanks to Rhett Harrison, Aasheesh Pittie, Campbell O. Webb and Kinari Webb for their help and guidance during the study and commenting on the draft manuscript. We acknowledge Serena Zhao for helping with references.


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