PRIMATES,35(1): 1-14, January 1994 1 Seasonal Change in the Composition of the Diet of Eastern Lowland Gorillas JUICH! YAMAGIWA, Kyoto University NDUNDA MWANZA, Centre de Recherches en Sciences Naturelles TAKAKAZU YUMOTO, Kobe University and TAMAKI MARUHASHI, Musashi University ABSTRACT. Details are presented of the composition of the diet of eastern lowland gorillas, derived mainly from a study of their fresh trails and fecal analysis, during the course of an entire year in the tropical lowland forests of the Itebero region, Zaire. Gorillas ate 194 plant foods from 121 species and 45 families. They consumed 48 species of fruits; and 89~ of fecal samples contained fruit seeds, but fruits were a relatively small part (25070) of the total number of food items. The composition of their diet changed seasonally. When consumption of fruit decreased in the long rainy and the long dry seasons, the gorillas ate, in addition to Zingiberaceae and Marantaceae, many kinds of leaf and bark, which may be an important buffer against the shortage of fruits. Gorillas also fed regularly on ants (Ponerinae), and the frequency of consumption showed small seasonal variations. From a comparison of diet composition, eastern lowland gorillas appeared to be intermediate between the other two subspecies. The choice of food showed differences in preference of fruits and insects between subspecies and may reflect high similarities within subspecies in lowland and montane forests. Key Words: Diet; Seasonal change; Frugivory; Insectivory; Gorilla gorilla graueri. INTRODUCTION Primate species that live in a variety of habitats show variations in the composition of their diet. Data from a single population may be atypical of the species as a whole and may obscure generalizations that are necessary for inter-species comparisons. Variety in respect to diet differs widely between populations as a direct result of differences in the availability of particular foods (CLUTTON-BROCK,1977). By contrast, a high similarity in the choice of particular foods is always found between local populations within species, and a comparison of diets a m o n g local populations helps us to reconstruct details of the previous differentiation and dispersal of the species (UEHARA, 1977). Gorillas live in a wide range of habitats in Equatorial Africa and have been classified into three subspecies, namely, western lowland gorillas (Gorilla gorilla gorilla), eastern lowland gorillas (G. g. grauerl), and mountain gorillas (G. g. beringet). The former two subspecies inhabit both lowland and montane forests, and the latter inhabits higher montane forests. From a comparison of their morphological traits, it appears that G. g. graueri is intermediate between the other two subspecies (GRovEs, 1967; CORBET, 1967; GOODALL & GROVES, 1977). From the sizes of males, GROVES (1970) noted that G. g. gorilla was the smallest and G. g. graueri was the largest of the three subspecies, and HARCOURT et al. (1981) suggested that this order of male size matches the median group size in the range of distribution of each species. 2 J. YAMAGIWAet al. Most of the information available about the ecology of gorillas comes from mountain gorillas that live in the small, isolated habitat of the Virunga Volcanoes. Mountain gorillas are regarded as relatively specialized, terrestrial folivores (SCHALLER,1963; FOSSEY, 1974; FOSSEY & HARCOURT, 1977; Vedder, 1984; WATTS, 1984). With the exception of bamboo shoots, the availability of particular plant foods does not appear to change throughout the year. The gorillas eat insects deliberately but such insectivory is infrequent and is not necessary for meeting their nutritional needs (HARCOURT8r HARCOURT, 1984; WATTS, 1989). Recent studies of western lowland gorillas indicate that these gorillas eat a great variety of fruits (SABATERPI, 1977; TUTIN & FERNANDEZ,1985; WILL1AMSONet al., 1990; ROGERS et al., 1990; NISHIHARA, 1992). Gorillas range in both secondary regenerating forests and mature primary forests (JONES& SABATERPI, 1971; TUT1N & FERNANDEZ,1984), and they tend to feed regularly on insects, such as termites and ants (TUTIN & FERNANDEZ,1983, 1992; CARROLL, 1986; NISHIHARA& KURODA, 1991). Western lowland gorillas may exploit a broad frugivorous niche, as do chimpanzees in West Africa. Unlike the other two subspecies, eastern lowland gorillas have been rather poorly characterized. Gorillas inhabiting montane forests of the Kahuzi region have recently been classified as G. g. graueri (CASIMIR, 1975; GROVES & STOTT, 1979). Gorillas in this region are regarded as folivores, although they eat large amounts of fruits seasonally (CASIMIR, 1975; GOODALL, 1977). The variety of types of vegetation in the Kahuzi region and the seasonal variation in the distribution of particular foods, such as fruits and bamboo shoots, may be the cause of their longer travel distances and the larger size of their home ranges, as compared to those of mountain gorillas (CASIMIR& BUTENANDT, 1973; CASIMIR, 1975; GOODALL, 1977; YAMAGIWA,1983). Eastern lowland gorillas inhabiting lowland forests also range in various types of vegetation (MWANZAet al., 1992). They have a more conspicuously frugivorous diet than gorillas in montane forests and they also tend to feed regularly on insects, as do western lowland gorillas (YAMAGIWAet al., 1991, 1992). Such frugivory and insectivory may possibly enlarge the breadth of their diet and act to extend their daily travel distances. However, the limited available information about their diet prevents us from making far-reaching comparisons of the ecology of the three subspecies. This report presents, for the first time, the composition of the diet of eastern lowland gorillas in lowland forests. Seasonal changes in the composition of their diet are described, and their choice of food is compared within and among subspecies. STUDY AREA AND METHODS The survey was conducted in the Itebero region, Zaire (Fig. 1). The study area is located at an altitude of 600 to 1300 m, and it has been protected since 1980 as an extension of Kahuzi-Biega National Park. It is covered with tropical forests, which include primary forest, secondary forest, ancient secondary forest, abandoned cultivated fields and swamps. High stands of trees, such as Gilbertiodendron dewevrei, Staudtia gabonensis, Michelsonia microphylla, and Cynometra alexandri, are frequently found together with scarce ground vegetation in the primary forest. Musanga cecropioides and herbaceous plants, such as Zingiberaceae or Marantaceae, are found in gaps in the forest, beside ravines and along rivers. Secondary forests are characterized by Musanga cecropioides and Macaranga spinosa with densely distributed herbaceous plants. Several, small, cultivated fields, surrounded by secondary forest, were abandoned by the local people prior to 1985. Palm trees (Elaeis guineensis) are frequently found in these areas. Ancient secondary forests were Diet of Eastern Lowland Gorilla 3 = ZAIRE N 1 0 1 ]00 ~ , E~rd KAHUZI-BIEGAEpGA}"'''",{, Tang""" 200kin ~Laken .... Fig. 1. Map showing the Kahuzi-Biega National Park in eastern Zaire. The black area and the dotted area show the original part of the Park (montane forests) and the extension of the Park (tropical forests), respectively. The black circle show the study area of the Itebero region. produced as a result of deforestation by a mineral company in the colonial era and subsequent successional reforestation. Ficus sur, Uapaca guineensis, and Celtis brieyi are c o m m o n l y found in this forest. Halopegia azurea is one of the dominant herbaceous plants, and Uapaca corbisieri is occasionally found in swamps. By reference to the annual rainfall records of the Meteorological Station near Mt. Kahuzi, a year in the study area can be divided into four seasons: the long rainy season, M a r c h - J u n e ; the long dry season, J u n e - S e p t e m b e r ; the short rainy season, S e p t e m b e r - D e c e m b e r ; and the short dry season, D e c e m b e r - March. Data were collected intermittently from 1987 to 1991 (Table 1). The periods during which we collected fresh samples of gorillas' feces cover 11 months. March was not sampled, and only one month, October, was sampled twice. We found at least ten groups of gorillas and nine solitary males in 1987 within the study area, which covered an area of 340 km 2. The density of the population was estimated to be 0.27 - 0.32 gorillas/km 2. Gorillas in this area did not tolerate the presence of humans because of the previous high incidence of hunting. Low visibility in the tropical forest also prevented us from observing gorillas. Therefore, data cited here are mostly derived from fresh fecal samples (up to 1 day old) and fresh feeding signs (up to 2 days old) collected on the gorillas' fresh trails. Since the size of dung Table 1. Study period and trail evidences. No. of days on which trail evidence was collected Period Feeding signs* Fecal samples** A p r - May 1991 23 28 J u l - A u g 1987 20 31 J u n - Jul 1991 Short rainy S e p t - Oct 1987 34 38 O c t - Nov 1989 Short rainy Dec 1989-Feb 1990 41 37 *Number of days on which fresh trails (up to 2 days old) were followed for more than 100 m; **number of days on which flesh fecal samples (up to 1 day old) were collected. Season Long rainy Long dry 4 J. YAMAGIWAet al. balls is correlated with the gorilla's age (SCHALLER,1963), we measured the diameter of flesh feces left by gorillas on their trails and inside or beside beds at each bed site. In order to avoid overlapping of samples, we collected one fecal sample from each night bed and a few fecal samples on the trails per day. We allocated the feces by reference to size to five age-sex classes (infant: less than 3 cm in diameter; immature: 3 - 5 cm; subadult and adult: 5 - 7 cm; silverback male: more than 7 cm). Feces collected in the field were washed in 1-mm mesh sieves, dried in sun-lightand stored in plastic bags. The contents o f each sample were divided into seeds, fruit skins, fiber, leaves, fragments of insects, and other matter. Large seeds were counted. Small seeds, fiber, and leaves were rated as being abundant, common, or rare. Samples of seeds and insects were preserved in 10% ethanol. Plant specimens were identified at the National Botanical Garden in Belgium. To define the forest's structure, we made a belt transect of 10 m in width and 8,000 m in length, and every tree above 10 cm in diameter at breast height (DBH) was recorded. We also made a short transect (2 m in width and 50 m in length) and counted the number of other plants of each type. RESULTS COMPOSITION OF THE D I E T Appendix 1 lists all the plant species consumed by gorillas at least twice during the study periods in the Itebero region. Gorillas were found to eat 194 foods from at least 121 plant species that represent 45 families (Table 2). The list of food items come from 50 tree species, 12 shrubs, 23 vines, 20 herbs, 4 palms, 8 epiphytes, 2 ferns, and 2 grass species. More than one third (38%) of the total tree species (132 species) above 10 cm in D B H were used for food by gorillas. A m o n g them, 11 species are listed among the 20 species that were presented at the highest densities in the belt transect. Staudtia gabonensis, Polyalthia suaveolens, Gilbertiodendron dewevrei, Diospyros hoyleana, and Pycnanthus angolensis were among the ten species present at highest densities. Plant parts eaten by gorillas were divided into fruit/seed (48 species), leaf (79 species), pith/stem/twig (39 species), bark (17 species), root (10 species), and rotten trunk (1 species, Table 2). Most kinds of fruit (71%) and bark (71%) eaten by gorillas were from trees. About half (46%) the kinds of pith were from herbs. Seeds of Gilbertiodendron dewevrei and the rotten trunk of Maranthes glabra were also eaten. Fragments o f petioles, epithelium from roots, galls, tendrils, and fungus were detected in the feces. Table 2. Number of species per plant form per plant part eaten by gorillas in the Itebero region, Zaire. Total* Plant form Fruit/seed Leaf Pith/stem/twig Bark Tree Shrub Vine Herb Other 34 2 2 7 3 28 12 21 5 13 6 3 4 18 8 12 1 3 0 1 Root 5 0 1 4 0 Other 1 0 0 0 0 Sp. 50 12 23 20 16 86 18 31 34 25 Total 48 79 39 17 10 1 121 194 *Total shows number of species per plant form (Sp.) and number of species x parts (Parts). Parts Diet of Eastern Lowland Gorilla 5 Table 3. Number of plant species of which a given number of different parts was eaten by gorillas. No. of parts eaten Life form 1 2 3 4 Total Tree Shrub Vine Herb Other 27 7 15 12 7 14 4 8 4 9 5 1 0 2 0 4 0 0 2 0 50 12 23 20 16 Total 68 39 8 6 121 From most (88~ of the plant species eaten, gorillas ate two or fewer different parts (Table 3). Most of the plant species of which gorillas ate more than three parts were trees and herbs. They ate four different parts of some tree species, namely, Ficus sur, Pentadesma lebrunii, Symphonia globulifera, and Uapaca guineensis, and o f some herbs, namely, Aframomum laurentii and Megaphryniurn macrostachyum. Most feces (89.0~ of a total o f 327 fecal samples) included seeds of fruits; 33.6070 included rare and 25.4070 included abundant fruit seeds, and all the feces included fibers or fragments of leaves. These seeds were swallowed whole by gorillas. The seeds of Gilbertiodendron dewevrei and Klainedoxa gabonensis were found as fragments in feces and seemed to have been crushed by the gorillas' teeth. Most parts of shrubs, vines, herbs, and other plant species were eaten on the ground. Large number o f feeding signs, in the case of Aframomum laurentii and Halopegia azurea, for example, were found on the gorillas' trails in valleys and swamps. Leaves and bark of Landolphia owariensis, Urera hyposelodendron, Celtis brieyi, Ficus spp., Myrianthus arboreus, and Uapaca spp., were sometimes eaten in trees. Fruits of trees were eaten both on the ground and in trees, and leaves, barks, stems or roots were eaten from immature trees on the ground. Leaves of Pycnanthus angolensis were the most frequently eaten food item in primary and ancient secondary forests. Fallen ripe fruits, such as those of Anonidium mannii and Klainedoxa gabonensis, were eaten on the ground, and fruits of Dialium polyanthum, Ficus sur, Gambeya lacouritiana, and Uapaca guineensis were eaten in trees. Immature gorillas were occasionally observed to climb up to more than 20 m above the ground to eat fruits of Dialium polyanthum and Canarium schweinfurthii. About half (42070) of the 375 night beds were found in trees. In primary forest, 25~ of the beds were found 10 - 30 m above the ground in trees. Gorillas in this area must be excellent climbers. About 38070 of total fecal samples included fragments of insects: 31070 included ants, 4070 included termites, and 3070 included other insects. Most of the fragments found in feces were chitinous, such as heads, mandibles or legs, that had not been digested during their passage through the gorillas' intestines. The amount of insect remains in each fecal sample was always very small. The ants collected at the feeding sites were identified as Ponerinae, which form relatively small colonies of 10 to 1,000 adults ( H O L L D O B L E R & W I L S O N , 1990). Most of the termites consumed by gorillas were Cubitermes sp. These termites build gray, earthen mounds against living tree trunks. No evidence was found to suggest that the gorillas used tools to acquire insects. The mounds seemed to be destroyed manually by the gorillas, as reported for western lowland gorillas in G a b o n (TtJTIN & FERNANDEZ, 1983). The other insects found in feces were larvae, bees, and caterpillars and were probably ingested inadvertently with vegetable matter. Field signs showed that gorillas collected ants by scratching or digging in the soil. All the ant-feeding sites were found in primary or ancient secondary forests on ridges or slopes. 6 J. YAMAGIWAet al. SEASONAL VARIATIONS The composition of the gorilla's diet changed seasonally. Less than half (40%) of the plant species used for food were eaten by gorillas in three or more seasons. Herbaceous plants tended to be used during the whole year, while trees and vines were used in a single season (Fig. 2). About half kinds (44%) of pith were eaten during the whole year. By contrast, many kinds of fruits (44%), leaf (48%), and bark (53%) were eaten in single season. Plant species from which different parts were used for food, were eaten in more different seasons. Among 14 plant species from which more than three different parts were used for food, all species were eaten in three seasons and ten were eaten in four seasons. Figure 3 shows the seasonal changes in the number of food-plant species in terms of each part eaten by gorillas in the Itebero region. In the long rainy season, gorillas ate the most kinds of food item, in which leaves constituted the major parts. The number of fruit species gradually increased from the long rainy season to the short rainy season, while the numbers of leaf, pith, and bark species decreased. The prominent decrease in kinds of fruiting tree in May (the long rainy season) and June (the long dry season) may possibly be responsible for such a change. A difference in composition of diet is distinguishable between the minor-fruiting seasons (the long rainy and the dry seasons) and the major-fruiting seasons (the short rainy and the dry seasons). Most of the leaves (64%) and bark (93%) eaten in the former season, but not eaten in the latter, were from trees and vines. These non-fruit foods may possibly compensate for the scarcity of fruits in the minor-fruiting seasons. Quantitative analysis of fecal samples also revealed the infrequent fruit-eating in the minor-fruiting seasons (Table 4a). In the long rainy and the long dry seasons, 13% and No. o f species 40 ~ L / 30 Plant form Part 20 / eaten t F V 10 0 4 3 2 1 No. of seasons Fig. 2. Number of plant species eaten by eastern lowland gorillas during the whole four seasons to single season. Plant form: T: tree; S: shrub; V: vine; H: herb; O: other form. Part eaten: F: fruit; L" leaf; P: pith; B: bark; O: other part. Diet of Eastern Lowland Gorilla 7 NO. of species 50 4O F k P 30 2O ~~ 0 Long rainy Long dry (]17) Short (93) rainy Short dry Season (84) (No. of food (84) items) Fig. 3. Number of food-plant species in terms of each part eaten by gorillas during each season in the Itebero region. F: Fruit; L: leaf; P: pith/stem/twig; B: bark; O: other parts. 33~ respectively, o f fecal s a m p l e s d i d n o t include any seeds, a n d feces t h a t i n c l u d e d abundant seeds were very few in number. By contrast, n o feces w i t h o u t seeds were f o u n d , a n d over 40~ o f fecal s a m p l e s i n c l u d e d abundant seeds in the s h o r t rainy a n d the s h o r t d r y seasons. A l t h o u g h s o m e feces i n c l u d e d abundant seeds in the long rainy season, the percentage o f abundant seeds in this season (13o70) was significantly lower t h a n those in the s h o r t rainy (41o70) a n d the s h o r t d r y (45o70) seasons (X2=16.5 a n d 18.0, df=l, p < 0 . 0 1 ) . T h e s e o b s e r v a t i o n s suggest t h a t n o t o n l y the n u m b e r o f fruit species b u t also the a m o u n t o f fruit c o n s u m e d by gorillas decreased in the m i n o r - f r u i t i n g seasons. T h e frequency o f insect-eating d i d n o t a p p e a r to c h a n g e s e a s o n a l l y (Table 4b). F r o m the fecal analyses, it seemed likely t h a t gorillas o f each age a n d sex class, except for infants, Table 4. Number of fecal samples that included seeds (a) and fragments of insects (b) as a percentage of the total samples collected in each season (N). (a) Season Minor-fruiting Long rainy Long dry Major-fruiting Short rainy Short dry Relative amount of seeds (~ + ++ +++ 76 80 13 33 44 51 25 16 13 0 87 67 102 69 0 0 22 14 37 41 41 45 100 100 N Total (b) Season Long rainy Long dry Short rainy Short dry N 76 80 102 69 Percentage Ants 20 29 41 30 of fecal samples (070) Termites Other insects 0 0 5 9 4 1 9 3 Any insect 20 41 45 42 8 J. YAMAGIWAet al. ate ants on at least one occasion during the study period. Silverback males, adults, subadults, and solitary males (usually young silverback males) fed on ants in all four seasons. Although these adult and subadult gorillas tended to consume ants more often in the short rainy season than in the long rainy season (X2=9.20, df=l, p<0.01), no differences were found between any other pairs of seasons (X2-- 1.72, 2.22, 3.02, 0.05, and 2.04, df= 1, p > 0.05). Fecal samples including fragments of termites or other insects were very few in number. However, such fragments were found in feces of all age-sex classes, with the exception of infants, and they were found in feces collected in the long dry, the short rainy, and the short dry seasons. DISCUSSION Eastern lowland gorillas inhabiting the tropical lowland forests of the/tebero region eat a more varied diet than previously anticipated. During a short visit to the Utu region (which is very close to the Itebero region), SCHALLER(1963) recorded that only 20 foods from 17 plant species were eaten by gorillas, including 4 species of fruits, and he reported that the diet of gorillas in this region depended as heavily on foliage as does that o f mountain gorillas. By contrast, our study identified 194 foods from at least 121 plant species. This number exceeds the number of plant-food species for gorillas identified in the montane forests o f Virunga (49 species: FOSSEY, 1983; 41 species: WATTS, 1984) and Kahuzi (56 species: CASIMIR, 1975), and is equivalent values obtained to those in the tropical lowland forests of Equatorial Guinea (92 species: SABATER PI, 1977) and Gabon (134 species: WILLIAMSON et al., 1990). From a comparison of the composition of their diet, eastern lowland gorillas appear to be intermediate between mountain gorillas and western lowland gorillas. A mere three species of fruits were listed in the diet and were eaten only infrequently by mountain gorillas in the Central Virunga (WATTS, 1984). Leaves and stems of herbaceous plants were their major food items. By contrast, western lowland gorillas exhibit frugivorous characteristics in various habitats in lowland forests (SABATERPI, 1977; TUTIN & FERNANDEZ, 1985; CARROLL,1986; N1SHIHARA,1992). Remains of fruits were recorded in 98% of feces, and fruits constituted more than half (55~ of the recorded food items eaten by western lowland gorillas in Gabon (WILLIAMSON et al., 1990). In this study we also found fruit seeds in 89% of feces, but fruits form a relatively small part (25%) of total number of food items eaten by eastern lowland gorillas in the Itebero region. These gorillas eat many kinds o f leaf and the fibrous parts o f various plants. The Itebero region is located about 100 km from the Kahuzi region (Fig. 1), The former lowland forests are connected by a corridor to the latter montane forests. More than 90% o f plant foods do not overlap between the two regions and are not available in both of the two regions. Nevertheless, this study suggests that the diet of eastern lowland gorillas in the lowland forests may bear some resemblance to that in the montane forests. Gorillas in the Itebero region eat many kinds of leaf and bark o f vines, as observed in the case of gorillas in the Kahuzi region (CASIMIR, 1975; GOODALL, 1977). Although the Kahuzi gorillas eat few kinds o f fruit, they eat a large amount o f fruit from two types of tree (Syzygium guinense and Myrianthus holstiO. The Itebero gorillas also eat fruits of Syzygiurn rowland# and Myrianthus arboreus. Ficus spp., and Symphonia globulifera provide many parts (fruits, leaves, and bark) as food for gorillas in both regions. Leaves and pith of Urera hypselodendron (vine) and the pith of Cyathea rnanniana (tree fern) are staple and important foods for the Kahuzi gorillas, and they are also eaten by the Itebero gorillas. Diet of Eastern Lowland Gorilla 9 GOODALL and GROVES (1977) reported that the Kahuzi gorillas climbed trees frequently and skillfully when they ate fruits, as deduced in the case of the Itebero gorillas in this study. The composition of the diet of gorillas may primarily reflect the diversity of food in their habitats. However, the choice of food may reflect high similarities within subspecies in lowland and montane forests. Eastern lowland gorillas in the Itebero region eat a great variety of fruits, as reported in the case of western lowland gorillas. Western lowland gorillas tend to avoid unripe or fatty fruits in Gabon (ROGERS et al., 1990). We found that eastern lowland gorillas generally ate ripe fruits in trees and on the ground. They also totally ignored several fruits with a high lipid content, such as Pycnanthus angolensis and Staudtia gabonensis, of which they frequently ate the leaves and bark. However, eastern lowland gorillas also ate fatty fruits, such as Canarium schweinfurthii, Dacryodes edulis, and Elaeis guineensis. These fruits are a major part of the diet of sympatric populations of chimpanzees in both Gabon and Zaire, where the two kinds of ape tend to use same kinds of plant for food (TUTIN & FERNANDEZ, 1985; ROGERS et al., 1990; YAMAGIWAet al., 1992). These differences should be analyzed in relation to the sympatry of gorillas and chimpanzees in future studies. Eastern lowland gorillas in the Itebero region consumed more than 19 species of fruits in each season. However, the frequency of fruit-eating by gorillas changed seasonally. Gorillas may change their choice of food between the minor-fruiting and the major-fruiting seasons. They tended to eat many kinds of leaf and bark in response to a decrease in fruiting trees in the minor-fruiting seasons. An increase of foliage and a decrease in fruits in the diet was also observed in the case of chimpanzees during the dry season in Gombe National Park, Tanzania (WRANGHAM, 1977). Bark consumption by both western lowland gorillas in Gabon and chimpanzees in Tanzania tends to increase when few fruits are available (NISHIDA, 1976; ROGERS et al., 1990). When fruits were scarce, the eastern lowland gorillas also increased their intake of fibrous foods from herbaceous vegetation, such as Zingiberaceae and Marantaceae, as reported for western lowland gorillas in Gabon (ROGERS et al., 1988). These herbaceous plants are staple foods of gorillas in tropical lowland forests (SABATERPI, 1977; TUTIN & FERNANDEZ, 1985; NISHIHARA, 1992; YAMAGIWAet al., 1992). Terrestrial herbaceous plants and other forms of foliage could serve as an important buffer against seasonal shortages o f fruits for both gorillas and chimpanzees across their habitats in tropical lowland forests (HLADIK, 1973; ROGERS& WILLIAMSON, 1987). Gorillas in lowland forests tend to feed regularly on insects. Fecal samples of gorillas have included insects at similar frequencies across various habitats of tropical forests: 30% in Gabon (TuTIN & FERNANDEZ, 1992); 43% in the Central African Republic (CARROLL, 1986); 24% in Congo (NISHIHARA, 1992); and 38% in Zaire (this study). These observations contrast with the rather inadvertent ingestion of insects by mountain gorillas (HARCOURT & HARCOURT, 1984) and the infrequent feeding on driver ants by young mountain gorillas (WATTS, 1989) in the Virunga region. Neither eastern nor western lowland gorillas seem to use tools for the acquisition of insects. They collect ants by scratching or digging in the soil (YAMAGIWAet al., 1991; NISHIHARA & KURODA, 1991), and they capture termites by breaking up mounds by hand (TuTIN & FERNANDEZ, 1983, 1992, this study). This study revealed no age differences and only small seasonal variations in the frequency of insect-eating by eastern lowland gorillas, as reported for western lowland gorillas (TUTIN & FERNANDEZ, 1992). Eastern lowland gorillas that inhabit the montane forests of Kahuzi occasionally feed on ants (Crematogaster spp.), but the frequency of ant fragments in feces is very low (unpubl. data). 10 J. YAMAGIWAet al. T h e t y p e o f insect eaten by gorillas a n d the frequency o f c o n s u m p t i o n show local differences within t r o p i c a l l o w l a n d forests. A n t s constitute the m a j o r i t y o f insects eaten by eastern l o w l a n d gorillas, while b o t h ants a n d termites are frequently eaten by western l o w l a n d gorillas (TUTIN & FERNANDEZ, 1983, 1992; CARROLL, 1986). NO fecal s a m p l e s o f eastern l o w l a n d gorillas included weaver ants ( O e c o p h y l l a l o n g i n o d a ) , which a c c o u n t e d for 88~ o f insect r e m a i n s in feces o f western l o w l a n d gorillas in G a b o n (TuTIN & FERNANDEZ, 1992). E a s t e r n l o w l a n d gorillas eat six species o f ants t h a t b e l o n g to the Ponerinae, which possess a p a i n f u l sting. By contrast, stinging ants are n o t eaten by western l o w l a n d gorillas in G a b o n . Such local differences in insect-eating have also been r e p o r t e d for c h i m p a n z e e s (NISHIDA, 1973; MCGREW, 1983; UEHARA, 1986). A l t h o u g h m o r e d a t a are n e e d e d o n the e c o l o g y o f these insects in E q u a t o r i a l A f r i c a , t h e frequencies o f insect-eating by gorillas m a y reflect differences in the d i s t r i b u t i o n o f insects between the l o w l a n d a n d m o n t a n e forests, a n d / o r m a y reflect t r a d i t i o n a l differences between h a b i t a t s or communities. Acknowledgements. This study was financed by the Monbusho (Ministry of Education, Science, and Culture, Japan) International Scientific Research Program (Nos. 630430810, 01041089) in cooperation with C.R.S.N. (Centre de Recherches en Sciences Naturelles) in Zaire. We would like to thank I.Z.C.N. (Institut Zairois pour Conservation de la Nature) for granting permission to carry out research in their National Park; Dr. N. ZANA, Dr. B. BALUKU, Dr. M. M. MANKOIO, Mr. M. O. MANKOTO, Dr. BERND STEINHAUER-BURKART,Mr. M. MASHAGmO,Mr. M. E. LINZOMm, Mr. K. K. B. KIMVUN1, and Mr. M. M. A. WATHAUTfor their administrative help and hospitality; and Mr. K. NIgUMBOand Mr. N. BOS1LANAfor their technical help. We are also greatly indebted to all guides, guards, and field assistants at the Kahuzi-Biega National Park for their technical help and hospitality throughout the fieldwork. Appendix 1. Species of plants and their parts eaten by gorillas in the Itebero region, Parts eaten Scientific name Family LR LD SR Trees F Afrosersalisia cerasifera Sapotaceae F A lbizia gummifera Mimosaceae B B, R F Anonidiurn mannff Annonaceae L Anthonota gilletii Caesalpiniaceae L Antiaris toxicaria Moraceae L, B F Antrocaryon nannanii Anacardiaceae F Canarium schweinfurthii Burseraceae F F L Carpolobia glabrescens Polygalaceae F, L F Celtis brieyi Ulmaceae F, L, B L, B L Chlorophora excelsa Moraceae L F Dacryodes edulis Burseraceae F Dialium polyanthum Caesalpiniaceae Diospyros spp* Ebenaceae L Fagara inaequalis Rutaceae E L Ficus densistipulata Moraceae L F, L Ficus natalensis Moraceae EL EL,~B Ficus sur Moraceae F, L F, L F Ficus sp. 1 Moraceae F Ficus sp. 2 Moraceae F Gambeya lacouritiana Sapotaceae Garcinia epunctata Guttiferae Garcinia ovalifolia Guttiferae R F Gilbertiodendron dewevrei Leguminosae F Grewia mildbraedii Anacardiaceae F F Zaire. SD F R F L F,L F F F EL EL EL F F EL F F (continued) 11 Diet o f Eastern Lowland Gorilla A p p e n d i x 1. (continued) Scientific name Grossera multinervis Khaya ivorensis Klainedoxa g a b o n e n s i s Lebrunia bishaie Macaranga spinosa Maranthes g l a b r a Musanga cecropioides Myrianthus arboreus Pentadesma lebrunii Phylanthus sp. Piptadeniastrum africanum Polyalthia suaveolens Pycnanthus a n g o l e n s i s Ricinodendron africanum Staudtia gabonensis Symphonia globulifera Syzygium rowlandii Treculia africana Trichilia welwitschii Trilepisium madagascariensis Titrraeanthus africana Uapaca guineensis Uapaca paludosa Uapaca corbisieri Uvariopsis congolana Zanthoxylum lemairei Family Euphorbiaceae Meliaceae Irvingiaceae Guttiferae Euphorbiaceae Chrysobalanaceae Moraceae Moraceae Guttiferae Euphorbiaceae Mimosaceae Annonaceae Myristicaceae Euphorbiaceae Myristicaceae Guttiferae Myrtaceae Moraceae Meliaceae Moraceae Meliaceae Euphorbiaceae Euphorbiaceae Euphorbiaceae Annonaceae Rutaceae Parts eaten LR LD F F SR SD F L P F, L B L, B L, B F L, B F L R F, L F, L F, B L, B, R L F, L L P T F, L, P F, L L, B L L, B L, B L T F, L F F, L L, B F, L F F, F, R F, P, L L P, B B F L R F, P F, B F F L F, P F F, L, P L, P L L, P F,L,P F L Shrubs Alchornea floribunda Alchornea c o r d i f o l i a Heckeldora staudtii Massularia acuminata Mimulopsis arborescens Pseuderanthemum ludovicimussi Psychotria kimuenzae Rinorea oblongifolia Rothmannia fischeri Thomandersia hensii Euphorbiaceae Euphorbiaceae Meliaceae Rubiaceae Acanthaceae Acanthaceae Rubiaceae Violaceae Rubiaceae Acanthaceae Unidentified sp. 1 Unidentified sp. 2 P F,L,P L F, L L L, P L L L L L L L,B L L,B P L L L L Vines Ancylobotrys pyriformis Baissea axillaris Baissea mortehanii Baissea multiflora Cissus dinklagei Cuervea m a c r o p h y l l a Efulensia montana Eremospatha haulbevilleana Hugonia platysepala lodes africana Landolphia o w a r i e n s i s Maesobotrya floribunda Salacia kivuensis Salacia adolf-friedericff Salacia c h l o r a n t h a Strychnos congolana Strychnos memecyloides Tetratoria poggei Apocynaceae Apocynaceae Apocynaceae Apocynaceae Vitaceae Hippocrateaceae Passifloraceae Palmae Linaceae Icaninaceae Apocynaceae Euphorbiaceae Hippocrateaceae Hippocrateaceae Hippocrateaceae Loganiaceae Loganiaceae Dilleniaceae L L L L, P L L P L, P L L, B L L L L, B L L L P L, P L F L L, B L L L L L (continued) 12 J. YAMAGIWAet al. Appendix 1. (continued) Scientific name Tylophora s y l v a t i c a Urera hypselodendron Unidentified sp. 3 Unidentified sp. 4 Unidentified sp. 5 Family Asclepiadaceae Urticaceae Acanthaceae Curcubitaceae Parts eaten LR L, B L L L L LD SR SD L, P L L, R P L Herbs Aframomum l a u r e n t i i Aframomum sanguineum Aframomum sp. Ataenidia conferta Brillantaisia cicatricosa Costus afer Culcasia angolensis Dicellandra b a r t e r i Halopegia azurea Haumania liebrechtsiana Marantochloa holostachya Marantochloa l e u c a n t h a Megaphrynium macrostachyum Palisota ambigua Palisota hirsuta Palisota schweinfurthii Renealmia c o n g o l a n a Sarcophrynium leiogonium Thaumatococcus daniellii . ..~n!d~nt.!f. ! ~ . s ~ : . 6 . . . . . . . . . . . . . . . . . . . . . Zingiberaceae Zingiberaceae Zingiberaceae Marantaceae Acanthaceae Zingiberaceae Araceae Melastomataceae Marantaceae Marantaceae Marantaceae Marantaceae Marantaceae Commelinaceae Commelinaceae Commelinaceae Zingiberaceae Marantaceae Marantaceae E P F P L P F, P F F P P P L P F, P P P L, P P P P P P P P P F, P P P L, P P P P F P F, P ~a~.ant.ac~.a~ ........... P ................ (. ............... F, L, P, R F P F, P F F P L, P, R P P P P F P P L, P P P P P F, R P P E L, P, R P P P P P P ................ (. .............. Others (palm, epiphyte, fern, grass, etc.) Afroraphidophora africana Araceae L, P L L L Anubis heterophyllum Araceae L L Barteria sp. Passifloraceae L, P Calamus deerratus Palmae P P P Cyathea manniana Cyatheaceae L, P P P P Elaeis guineensis Palmae P P F, P P Elaphoglossum sp. 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THOMPSON(eds.), Univ. of Tokyo Press, Tokyo, pp. 267-281. - - -- Received: May 20, 1993; Accepted: August 30, 1993 Authors' Names and Addresses: JuIcHl YAMAGIWA,Primate Research Institute, Kyoto University, Kanrin, Inuyama, Aichi 484, Japan; NDUNDAMWANZA,Centre de Recherches en Sciences Naturelles, Lwiro, D. S. Bukavu, Zaire; TAKAKAZUYUMOTO,Faculty of Science, Kobe University, Nada-ku, Kobe, Hyogo 657, Japan; TAMAKI MARUHASHI,Department of Human and Cultural Sciences, Musashi University, Toyotamakami, Nerima-ku, Tokyo 176, Japan.