THE RAFFLES BULLETIN OF ZOOLOGY 2009 THE RAFFLES BULLETIN OF ZOOLOGY 2009 57(1): 189–198 Date of Publication: 28 Feb.2009 © National University of Singapore AN ASSESSMENT OF FOOD OVERLAP BETWEEN GIBBONS AND HORNBILLS Chuti-on Kanwatanakid-Savini and Pilai Poonswad Department of Biology, Faculty of Science, Mahidol University, Rama 6 Rd. Phayathai, Bangkok 10400 ,Thailand Thailand Hornbill Project, Department of Microbiology, Faculty of Science, Mahidol University, Rama 6Rd., Phayathai, Bangkok 10400, Thailand Emails:[email protected] (CKS); [email protected] (PP) Tommaso Savini Conservation Ecology Program, School of Bioresources & Technology, King Mongkut’s University of Technology Thonburi, 83 Moo. 8 Thakham, Bangkhuntien, Bangkok 10150, Thailand Email: [email protected] (Corresponding author) ABSTRACT. – Hornbills and gibbons are considered to be potential competitors for food. They show considerable overlap in their frugivorous diet, foraging site (outer part of tree crowns), and reproductive period. However, the extent and nature of such overlaps have never been measured. Here we characterize the dietary overlap of the Great Hornbill, Wreathed Hornbill, Oriental Pied Hornbill, White-throated Brown Hornbill and White-handed Gibbon based on a long-term data on their feeding ecology at Khao Yai National Park, Thailand. Results from a Correspondence Analysis showed a slight overlap between the diets of the hornbills and gibbon, which may be attributed primarily on the dietary consumptions of Ficus spp. and, to a lesser extent, Polyalthia viridis. Due to the large crown size of Ficus and the overall low nutritional quality of its fruits, we hypothesized that a dietary overlap between the hornbills and gibbon for Ficus is energetically inconsequential for either groups. In contrast, P. viridis has comparatively small crowns, is present in the site in low densities, and produces fruits high in protein. Therefore, the overlap in diet between hornbills and gibbon for P. viridis may create the basis for competition, which in any event will be limited to pseudo-interference. KEY WORDS. – Food overlap; Resources exploitation; Khao Yai National Park; Thailand. INTRODUCTION coexisting species, face increase in energy requirement due to reproduction. In mammals, the physiology of reproduction, The coexistence of two different animal species using regular cycling, gestation, and nursing, place females under overlapping niches, defi ned by the full range of ecological substantial energetic pressure, (Lee & Bowman, 1995), and conditions and resources under which they can survive, is thus access to resources plays an important limitation in linked to their capacity for sharing such niches and their regulating overall reproductive success. Similarly, in birds, resources, in a way that allows both of them to survive and reproductive success has been related directly to the level of reproduce optimally (Edgerly et al., 1998; Park et al., 1998; dietary protein available during the nesting period (Beckerton Cross & Benke, 2002; Elmberg et al., 2003). & Middleton, 1982; Wikelski et al., 2000). Those general effects have been so far documented for food overlaps Overlap in the use of niches and their resources may cause between closely related coexisting species (Luiselli et al., competition that result in separation of the two species into 1999; Neale & Sacks, 2001; Mitchell & Bank, 2005), and specifi c parts of their original niche (Terborgh & Diamond, not closely related coexisting species (Morin, 1999; Brown 1970). However, competition will not arise when two et al., 1997). coexisting species that share resources are limited to different resources (Tilman, 1977) or to one unlimited resource Two separate long-term ecological research projects have (Camillo & Garofalo, 1989; Geoffrey, 1998; Krasnov et been conducted for more than two decades at Khao Yai al., 2005). National Park, Thailand, on the White-handed Gibbon (Hylobates lar) (Brockelman et al., 1998) and four sympatric Feeding overlap may acquire ulterior importance if species of hornbill, Buceros bicornis (Great Hornbill), Aceros accentuated during parts of the year when one, or more of the undulatus (Wreathed Hornbill), Anthracoceros albirostris 189 1155__KKaann__PPgg 118899--119988..iinndddd 118899 22//1199//0099 1122::0055::3322 PPMM Kanwatanakid-Savini et al.: Food overlap in gibbons and hornbills (Oriental Pied Hornbill) and Anorrhinus austeni (White- from the moment when the female in the nest began to take throated Brown Hornbill) (Poonswad et al., 1998a). Both food from the male until all food items had been passed to animal groups have been observed to feed on the outer part of the female. We identifi ed and characterized every plant and the forest canopy and share the same niche (Carpenter, 1967; animal food item that was consumed. Kemp, 1995), where they select primarily ripe, sugar-rich, juicy fruits (Leighton, 1998; Poonswad et al., 1998a) with We defi ned gibbon diet using direct observations of fi ve bright colors (Suryadi et al., 1994; Kanwatanakid, 2000). well-habituated gibbon groups. For a period of two and a half Moreover, a recent investigation of gibbon reproduction has years (May 2001 to Sep.2003), two trained fi eld assistants also highlighted signifi cant overlap with hornbills during observed each group for a minimum of 5 days per month. that period of the year when they have a strong dependence Data on feeding activities were collected by continuous on resources (Poonswad, 1993; Savini et al., 2008). The observations during the time between leaving and re-entering objective of this study was to characterize the dietary overlap a night-tree (cf. Martin & Bateson, 1993), alternating every between the White-handed Gibbon and the four sympatric hour between males and females. Food sources were known hornbill species, as suggested by Kemp (1995), specifi cally by the observers or where identifi ed later from collected plant during the fi rst half of the year when both animal groups face samples (for details see Savini et al., 2008). strong feeding pressure due to their reproductive energetic demands (Poonswad, 1993; Savini et al., 2008). Resource abundance – The spatial distribution of plant resources was measured in order to quantify their abundance in the area by using 13 north–south transects (total length MATERIALS AND METHODS 19.4 km, range 620–2,100 m) located within the gibbon study area of 39.8 ha (0.398 km2). Along each transect, trees larger Study site and species – The study was conducted between than 10 cm diameter at breast height (DBH) were marked, May 2001 and Dec.2005 at Khao Yai National Park, Thailand measured, and identifi ed to species, so that a total of 19,524 (2,168 km2; 14°26'N 101°22'E), in slightly hilly terrain at individual trees were included in our analyses. We calculated about 600–890 m above sea level. The study area (Fig. 1) the amount of resources as the percentage of the total tree covered approximately 60 km2 and was inhabited by a large sample, based on both stem number and basal area. population of four sympatric hornbill species that have been studied in detail for the past twenty years (Poonswad, Statistical analysis – Correspondence Analysis (CA) using 1993; 1995; 1998a). The area was also inhabited by a large Minitab 15 (Minitab Inc.) was employed to compare feeding population of White-handed Gibbon, which has been studied assemblages between White-handed Gibbons and the four since the late 1970s (see Raemaekers & Raemaekers, 1985; hornbill species, following Ter Braak (1986) whereby Reichard, 2003; Bartlett, 2003; Brockelman et al., 1998). data points are projected on a two-dimensional space that Khao Yai supports mainly a seasonally wet, evergreen forest maximizes the correspondence between categories on the (Kitamura et al., 2005), which experiences a distinct dry rows and columns (Poulsen et al., 2002). CA also helps to season (November–April) and wet season (May–October). The mean annual rainfall from 1993–2002 was 2,360 mm (Kitamura et al., 2005). Average daily temperature varied annually between 18.7 to 28.3°C and mean humidity ranged from 64.6% to 77.1% during the dry and wet season. Although fi gs (Ficus spp.) produce syconia through out the year (Poonswad et al., 1998b), the diversity and abundance of non-fi g fruiting species are relatively high only in the rainy season and beginning of the dry season (Bartlett, 2003; Savini et al., 2008). Diet composition – During the breeding season, the female hornbill imprisons herself in the nest site, a cavity in a tree trunk, and is fed by the male during the entire period of her egg incubation and chick development. The male moves constantly between the nest and the selected feeding sources (Kemp & Poonswad, 1993). We studied characteristics of food items consumed by hornbills in the fi eld by using direct observations of feeding behaviour at nests by continuous observation of the visiting male (Altman, 1974). At least six nests of each hornbill species were monitored each breeding season, for a total of 24 nests over a period of two breeding seasons (2004 and 2005). The fi rst author, with the help of research assistants, made feeding observations at each nest during four days per month for 10 hours per day (between 0500–1700 hrs). We scored each feeding visit by the male Fig. 1. Hornbill and gibbon study site. 190 1155__KKaann__PPgg 118899--119988..iinndddd 119900 22//1199//0099 1122::0055::3344 PPMM THE RAFFLES BULLETIN OF ZOOLOGY 2009 fi nd the best simultaneous representation of the diet records observation where some plant species were not fruiting each (Gorchov et al., 1995), with frugivorous species as column year. More in detail were the two components that accounted and fruit species as rows. Species showing similar diets for 35% of the variance (variance for Component 1 was will appear positioned close to each other. To determine 21% and Component 2 was 14%) when all plant species which food items generated overlaps, we removed targeted were considered (Fig. 4a). After excluding Ficus sp. and P. plant species and re-ran the CA analysis. We included in viridis from the analysis (Fig. 4b), we observed that both the CA all plant species and animals consumed per hour by components accounted for 33% of the variance (variance for gibbon and hornbills based on direct observation. We used Component 1 was 19% and Component 2 was 14%). When the Shannon-Wiener diversity index to defi ne the diversity only P. viridis was removed from the analysis (Fig. 4c), both of each species’ diet. components accounted for 35% of the variance (variance for Component 1 was 21% and Component 2 was 14%). After removing only the genus Ficus from the analysis, our result RESULTS was similar to removing both Ficus sp. and P. viridis from the analysis, where the grouping along the two components Diet composition – The general composition of the diet accounted for 33% of the variance (variance for Component during the breeding and/or nesting season in the fi rst half 1 was 19% and Component 2 was 14%; Fig. 4d). of the year (January to June), for both hornbill and gibbon species had a higher component of fi g and animal matter Resource abundance - Sample percentages of individual in the diet of hornbills, while the gibbon diet had a higher species of diet trees that overlapped did not vary much proportion of non-fi g fruits (Fig. 2; see Table 1 for species between the fi ve species (Table 2). However, the proportion details). Diet diversity, measured using the Shannon-Wiener of trees included in the non-overlapping portion of the diet diversity index, was: Gibbon (GB) = 2.1, Great Hornbill showed a distinct difference between the gibbon and the (GH) = 1.2, Wreathed Hornbill (WH) = 1.6, Oriental Pied four hornbill species, with the gibbons having a much higher Hornbill (PH) = 1.7 and White-throated Brown Hornbill (BH) proportion of their diet non-overlapping. This suggests that = 1.8; where higher numbers show a higher diet diversity. gibbons feed on a much larger set of resources that they do The mean estimate for hornbill Shannon-Wiener diversity not share with hornbills. index was 1.575 with a 95% confi dence interval of ±0.515 with the Gibbon value falling just above the interval. A comparison of the density and basal area between Ficus spp. and P. viridis, the two species composing most of the Food overlap – Fig. 3a shows the results for CA calculated diet overlap, indicated there was a larger amount of fi gs by including all plant species (n = 58) consumed by gibbons available, mainly as a low number of individuals but of a and hornbills. The two components account for 84% of large size. Conversely, P. viridis was present in the area the variance (variance for Component 1 was 66% and as a large number of individual trees but of much smaller Component 2 was 18%), separating BH and PH from WH size (Table 1). and GH, among hornbills, and from GB, which are isolated from the hornbills. After excluding from the analysis Ficus sp. and P. viridis (Fig. 3b), we observed a clear separation DISCUSSION between GB and the four hornbill species, which appeared grouped, with the two components accounting for 88% From a general dietary perspective, hornbills were less of the variance (variance for Component 1 was 69% and frugivorous, fed on a smaller number of plant species, Component 2 was 19%). To isolate the cause of this overlap, and fed more on insects, small mammals and birds than we analyzed the importance of the genus Ficus and of P. gibbons. Based on the correspondence analyses, overall we viridis separately. When removing only P. viridis from the detected only a moderate degree of overlap between gibbons analysis, we saw no obvious change from what was observed and the two larger species of hornbill (Great hornbill and in Fig. 3a, with the separation of the fi ve species along the Wreathed hornbill), while the two smaller hornbill species two component accounting for 85% of the variance (variance (Oriental pied hornbill and White-throated Brown hornbill) for Component 1 was 67% and Component 2 was 18%; Fig. appear more clearly separated. Even this moderate degree 3c). After removing only the genus Ficus from the analysis, of overlap fell away once trees of the genus Ficus and, in we obtained a result similar to as when Ficus sp. and P. a lower proportion, of the species P. viridis, were removed viridis was excluded, where the grouping along the two from the calculation. As a consequence of the relatively low components accounted for 87% of the variance (variance nutritional quality (O’Brien et al., 1998) and the abundant for Component 1 was 68% and Component 2 was 19%; distribution of the genus Ficus, we assumed a low importance Fig. 3d). These results suggest that the main component in for any such overlap to both animal groups. the overlap was represented by species of the genus Ficus, with a smaller proportion represented by P. viridis. Overall, both hornbills and gibbons persist in habitats of similar forest structure. Hornbills, as well as other large A similar pattern was observed when CA considered all the birds are able to observe the forest during fl ight and so detect individual nests observed for hornbill and each group observed fruits in the upper strata of the canopy (Kemp, 1995). This for gibbons (Fig. 4). Note that the two clusters observed in differs from most primate species, which are more likely all hornbill species are the consequence of two years nest to detect fruits in the middle strata of the canopy while 191 1155__KKaann__PPgg 118899--119988..iinndddd 119911 22//1199//0099 1122::0055::3366 PPMM Kanwatanakid-Savini et al.: Food overlap in gibbons and hornbills traveling through the forest (Poulsen et al., 2002). However, (Poonswad, 1993; Savini et al., 2008). For the gibbon, this gibbons show the peculiar capacity to forage mainly on the period coincides with the pre-conception period when females outer part of tree canopy, a consequence of their specialized must acquire a certain amount of body reserves in order to morphology and physiology (Carpenter, 1967). start cycling regularly and therefore conceive successfully (Savini et al., 2008). For the hornbills, as for other bird We observed an overlap in the reproductive season between species, the nesting period is considered the period of the hornbills and gibbons at the study site during the fi rst half year where high costs are faced by both the reproductive of the year, when dependence on resources was higher male and female (Poonswad et al., 2004). Fig. 2. Diet composition variation, during breeding season, between hornbill species [Great Hornbill (GH), Wreathed Hornbill (WH), Oriental Pied Hornbill (PH), and White-throated Brown Hornbill (BH)] and White-handed Gibbons (GB). 192 1155__KKaann__PPgg 118899--119988..iinndddd 119922 22//1199//0099 1122::0055::3366 PPMM THE RAFFLES BULLETIN OF ZOOLOGY 2009 Table 1. Species list in the diet of the four hornbill species hornbill species [Great Hornbill (GH), Wreathed Hornbill (WH), Oriental Pied Hornbill (PH), and White-throated Brown Hornbill (BH)] and White-handed Gibbons (GB). Plant Density Chemical Composition Percentage in the Diet Basal area / hectare Protein Fat Calory Ca+ GH WH BH PH GB g% g% kal/g g% Animal - - - - - 3.57 4.42 16.97 8.18 0.30 Acacia megaladena - - - - - - - - - 2.99 Adinadra integerrima 20.9 - - - - - - - - 0.37 Aglaia elaeagnoidea 37.8 7.72 - 4259.77 0.46 - - - - 0.30 Aglaia lawii 120.9 10.32 48.47 6493.3 0.59 0.64 0.48 0.67 0.76 - Aglaia spectabilis - 3.67 6.39 2200.77 0.31 0.93 2.46 0.26 0.20 - Alphonsea boniana 36.3 - - - - - - - - 0.18 Anthocephalus chinensis - - - - - - - - - 0.08 Antiaris toxicaria 7.2 12.18 11.84 4670.6 0.4 0.03 - - - - Aphanamixis polystachya 66.8 8.01 - 6489.79 0.44 - 0.97 0.04 - - Aquilaria crassna 218 - - - - - - - - 7.26 Arthocarpus lakoocha - 5.27 9.83 4113.76 0.4 0.10 - - - - Baccaurea ramiflora 125.1 - - - - - - - - 1.33 Balakata baccata 586.2 4.04 1.63 3877.47 - - - - - 3.51 Beilschmiedia balansae - 4.65 6.93 2675.51 0.45 0.09 0.43 0.58 0.11 0.10 Beilschmiedia glabra 69.9 8.34 32.84 5969.97 0.17 0.00 0.07 0.29 0.02 - Beilschmiedia maingayi 70.02 9.92 - 4842.06 0.68 0.31 0.83 1.97 0.80 0.14 Beilschmiedia sp. - - - - - 0.06 0.01 0.04 0.03 - Bhesa robusta 12.2 12.75 - 6195.61 0.78 2.40 2.28 7.06 2.06 - Canthium glabrum - - - - - 0.71 - 0.32 0.73 - Carallia brachiata 68.8 - - - - - - - 0.62 - Cinnamomum subavenium 395.3 5.71 31.92 6390.68 0.3 19.12 12.84 37.06 15.57 2.89 Cleistocalyx opercolatus 768.9 5.83 - - - - - - - 4.41 Combretum acuminatum - - - - - 0.29 - - 4.57 - Cryptocarya impressa - 12.73 26.69 6512.13 0.52 0.16 2.81 1.50 1.20 - Desmos chinensis climber 5.38 1.87 4465.84 0.63 0.90 0.05 0.43 0.11 4.58 Dipterocarpus gracilis 873.7 - - - - - - - - 0.07 Duabanga grandiflora - - - - - - - - - 2.51 Dysoxylum cyrtobotryum 143.3 7.4 16.33 4653.66 0.52 0.38 0.10 5.08 3.18 - Dysoxylum densiflorum - 11.84 - 6355.67 0.63 1.11 2.09 3.27 1.57 - Elaeagnus latifolia climber 4.81 0.12 1500.27 0.29 0.17 0.35 0.04 0.07 2.44 Ericybe elliptilimba climber - - - - - - - - 4.90 Ficus sp. 108.2 4.84 5.07 3093.59 1.57 57.56 44.15 9.84 38.12 33.59 Gironniera nervosa 348.8 - - - - - - - - 1.71 Gnetum montanum climber 13.2 2.33 4655.83 0.45 - - - 0.46 1.35 Horsfieldia glabra 6.6 3.56 41.61 6939.2 0.32 1.27 1.36 3.15 3.33 - Knema elegans 132.5 5.93 18.2 4955.44 0.68 0.00 0.59 0.12 0.23 0.74 Livistona speciosa - 4.16 30.61 5472.85 0.26 1.99 3.40 - - - Mangifera sp 21.3 - - - - - - - - 0.07 Nauclea orientalis 205.5 - - - - - - - - 0.01 Nephelium melliferum 250.4 5.8 11.61 3996.05 0.34 - - - - 8.02 PPeenniinnssuullaarr _sspp. - - - - - - - - - 0.79 Platea latifolia 63.3 3.24 - 2062.74 0.66 - - 0.11 0.28 0.04 Polyalthia jucunda - 11.59 6.36 4723.72 0.57 1.27 3.13 1.17 0.95 - Polyalthia viridis 56.1 9.9 12.78 4939.84 0.6 5.03 14.73 2.08 5.10 5.36 Prunus arborea 12.4 - - - - - 0.08 - - - Prunus javanicus 22.5 - - - - 0.25 1.06 0.58 0.66 1.35 Ratan sp. ground vegetation - - - - - - - - 1.25 Sabia limoniacea - - - - - - - - - 0.73 Salacia chinensis climber - - - - - - - - 0.31 Sarcosperma arboreum 206.9 - - - - - 0.05 1.28 - - Symplocos cochinchinensis 764.5 - - - - - - - - 3.22 Sterculia balanghas - - - - - - 0.05 - - - Sterculia sp. - - - - - 0.14 1.11 0.11 0.20 - Syzygium sp. - 2.03 - 4453.14 0.05 0.71 - 5.58 10.86 0.01 Ternstroemia wallichiana 8.7 - - - - 0.80 0.13 0.39 - - Walsura robusta 79.1 4.6 4.74 3654.17 0.42 - - - - 2.15 Ziziphus attopoensis - - - - - - - - 0.04 0.94 193 1155__KKaann__PPgg 118899--119988..iinndddd 119933 22//1199//0099 1122::0055::3366 PPMM Kanwatanakid-Savini et al.: Food overlap in gibbons and hornbills For several reasons, this small overlap in resources might suggested that the structure of fruits might infl uence their affect hornbills more than gibbons. The gibbon’s diet selection by gibbons, which prefer ripe fruits with juicy appears to be more diverse than that of hornbills. Overall, pulp in bright colors (red, orange and yellow) and with Asian primates are known among all primate species for one large generally well-protected seed. White-handed their high diversity in diet (Kappeler & Heymann, 1996). gibbons are also generalized frugivores, consuming various However, the higher diversity of primate diet versus hornbill morphological types of fruits because of the advantage of diet has also been observed in lowland rainforest of south- hands for manipulation and long digestive tracts that allow central Cameroon (Poulsen et al., 2002). In more detail, consumption of fruit species with hard covers and fl esh the diversity of the gibbon’s diet is a consequence of both attached to seeds (e.g. Choerospondias axillaris, Sandoricum lower selectivity by gibbons, in terms of fruit morphology, koetjape and Garcinia xanthochymus) (Kanwatanakid, 2000). and their travel mode, which allows them to move through Conversely, hornbills do not consume these fruit species the canopy by brachiating at relatively low energetic cost because their feeding adaptations are restricted by their bill (Usherwood & Bertram, 2003). From the point of view of morphology, which signifi cantly reduces their capability to fruit morphology, Kanwatanakid & Brockelman (2005) manipulate and extract food. Hornbills tend to select the Fig. 3. Correspondence Analysis per animal species: a, with all plant species included (n = 58); b, with the genus Ficus and P. viridis excluded; c, with only P. viridis excluded; d, with only the genus Ficus excluded. Hornbill species [Great Hornbill (GH), Wreathed Hornbill (WH), Oriental Pied Hornbill (PH), and White-throated Brown Hornbill (BH)] and White-handed Gibbons (GB). 194 1155__KKaann__PPgg 118899--119988..iinndddd 119944 22//1199//0099 1122::0055::3377 PPMM THE RAFFLES BULLETIN OF ZOOLOGY 2009 Table 2. Amount of individual trees belonging to overlapping and non-overlapping diet species (data expressed in % over total tree population measured in the 40 hectare botanical plot). Hornbill species [Great Hornbill (GH), Wreathed Hornbill (WH), Oriental Pied Hornbill (PH), and White-throated Brown Hornbill (BH)] and White-handed Gibbons (GB). GB GH WH OPPPHHH BH Overlapping sp. 5.2 5.2 4.4 5.2 1.8 non-overlapping sp. 22.5 4.0 4.1 4.4 5.0 Fig. 4. Correspondence Analysis per hornbill nest and gibbon group: a, with all plant species included (n = 58); b, with the genus Ficus and P. viridis excluded; c, with only P. viridis excluded; d, with only the genus Ficus excluded. Hornbill species [Great Hornbill ◆, Wreathed Hornbill ■, Oriental Pied Hornbill ▲, and White-throated Brown Hornbill ■] and White-handed Gibbons ▲. 195 1155__KKaann__PPgg 118899--119988..iinndddd 119955 22//1199//0099 1122::0055::3399 PPMM Kanwatanakid-Savini et al.: Food overlap in gibbons and hornbills ripest fruits that show split (dehiscent) husks when ripening more resources (Milinski & Parker, 1991), also referred to and high nutritional value (Poonswad et al., 1998a). During as pseudo-interference (Free et al., 1977). We do not exclude digestion, seeds do not pass through the digestive track and the presence of aggressive behaviour, but we expect the allow complete detachment of the nutritious fl esh from the limit of such events to be sporadic. From our study, we can seed. In birds in general, regurgitated seeds spend less time classify gibbons as “depleting competitors”, the species that in the digestive track than seeds defecated by other animals is more effi cient in reaching and depleting a food resource, (Johnson et al., 1985), to limit body weight and reduce fl ight and hornbills as “unsuccessful competitors” that may suffer costs. An alternative explanation for the low diet diversity from the exploitation effects (Milinski & Parker, 1991). in hornbills may be due to their larger home ranges (from 5.9 km2 for BH to 30.8 km2 for WH, Poonswad & Tsuji, 1994), compared to gibbon [on average 25 hectares (0.25 ACKNOWLEDGMENTS km2), Savini et al., 2008], which allows hornbills to select only high quality resources that can be found more easily We are grateful to Alan and Meg Kemp for facilitating the by covering a larger area. participation of CK-S and TS at the 4th International Hornbill Conference held on 6–10 November 2005 in South Africa, Due to the high cost of fl ying (Gill, 1989), the selection of where an early stage of this work was presented. G. A. Gale, foraging sites for birds is affected by the distance from the A. Kemp, A. Koenig, R. Corlett, L. P. Koh and S. Kitamura nesting site and quality of the resources (Drent & Daan, have provided useful comments in the various stages of the 1980). Hornbills will fl y preferentially to larger resources development of this manuscript. S. F. Yap and G. A. Gale that will provide them with suffi cient nutritional rewards. provided guidance in the statistical analysis. We would like On the other hand, the low cost of brachiation for gibbons to thank P. Chuylua, P. Desgnam, M. Kinglai, U. Martmoon, (Usherwood & Bertram, 2003) allows them greater mobility, C. Mungpoonklang, T. Ong-in, K. Plongmai, W. Soonpracon, resulting in multiple visits to a larger variety of sources due S. Sornchaipoon, U. Sunarat, A. Sungwal, P. Suwanlikid, to the relatively low cost of traveling. M. Tofani who assisted us during data collection in the fi eld (both for the gibbon and hornbill sections). We thank the Hornbill diet showed a relatively higher proportion of animal Department of National Park, Wildlife and Plant Conservation food items, which were absent in the gibbon’s diet, with the (CK-S and TS) and the National Research Council of complete absence of vertebrates reported in the Khao Yai Thailand (TS) for granting permission to conduct research population and insect consumption recorded at less than at Khao Yai National Park, and the park superintendent P. 1% over the study period (T. Savini, unpublished data). Vohandee, and his staff, for their assistance in the park. We may assume that the vertebrate component of hornbill’s This research was supported fi nancially by the Thailand diets may reduce the direct impact of resource overlap with Research Fund (the Royal Golden Jubilee PhD Program), gibbons for protein-rich fruit (e.g. P. viridis), and on which Mahidol University (Research Assistantships), and Thailand gibbons may be more successful foragers. The evolution of Hornbill Project (CK-S), and by the Max-Planck Institute the hornbill’s diet to include a higher quantity of vertebrates for Evolutionary Anthropology (Graduate Fellowship), and as a source of protein may also have arisen as a result of the Christian Vogel Fond (TS). competition with other frugivorous animals that feed on protein-rich plant parts. Our interpretation was supported partly by observations of Great Hornbill diets in southern LITERATURE CITED of Thailand (Budo Sungai Padi National Park), where the Great Hornbill consumed less than 5% of animal matter Altman, J., 1974. Observational study of behaviour: sampling during the late nesting period (Chaisuriyanun, 2005). This methods. Behaviour, 49: 227–267. amount is lower, although not signifi cantly lower, than the Bartlett, T. Q., 2003. Intragroup and intergroup social interactions 8% observed for the same species during the same nesting in white-handed gibbons. 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