PRIMATES,20(4): 475--490, October 1979

475

On the Ecology and Behavior of Cebus albifrons in Eastern Colombia: I. Ecology

THOMAS R. DEFLER Programa Nacional Colombiano de Primatolog[a, INDERENA, and The American Peace Corps ABSTRACT. A-503 contact-hr study of a 35-member group of Cebus albifrons was conducted in eastern Colombia in 1977 and 1978. The group had a female: male socionomic sex ratio of 2.5:1 and used a home range of 110-120 ha which overlapped the home range of another group of C. albifrons about 20-30 ha. The animals spent about 80 ~o of their foraging time eating plant material and about 20 ~ of their foraging time eating animal materials. A birth peak at the end of the dry season extending into the wet season was indicated by data available. Attempted predation was recorded by the mustelid Eira barbara and the black-and-white hawk-eagle Spizastur melanoleucus. Some association was observed with the red howler monkey Alouatta seniculus. The group at times spent more than half the day foraging and traveling on the ground, exhibiting a level of terrestriality not reported for other New World primates. INTRODUCTION The genus Cebus appears to be one of the most adaptive and generalized genera of the New World monkeys, being found widely throughout the neD-tropics in many different forest habitats. Except for C. capucinus (OPPENHEIMER, 1968, 1969, 1973) the genus has not been intensively studied. Other short studies and notes concerning C. capueinus, C. nigrivitattus, and C. apella have been published by BALDWIN and BALDWIN (1977), FREESE (1976, 1977, 1978), HERNANDEZ-CAMACHO and COOPER (1976), HLADIK and HLADIK (1969), HLADIK et al. (1971), IZAWA (1975, 1976, 1978, 1979), IZAWA and MIZUNO (1977), K/3HLHORN(1939, 1940), MOYNIHAN(1976), NOLTE (1958, 1959), OPPENHEIMER and OPPENHEIMER (1973), and STRtIHSAKERand LELANO (1977). Almost nothing has been published for C. albifrons except some short notes about the species by HERNANDEZ-CAMACHO and COOPER (1976), IZAWA (1975), MOYNIHAN (1976), and two laboratory behavioral studies of BERNSTEIN(1965, 1966). During a 5.5-month period from September 17, 1977 until March 3, 1978 a group of Cebus albifrons was intensively studied in an undisturbed forest in eastern Colombia. The site was located in the Territorio Faunistico E1 Tuparro, a 492,000 ha area set aside by the Colombian government to preserve a large tract of the llanos. The Territorio is administered by the Instituto de Recursos Naturales y Renovables ( I N D E R ENA), that part of the Colombian Department of Agriculture which administers natural resources and a national p a r k system. During the study the author was an American Peace Corps Volunteer working as an I N D E R E N A biologist in the Programa Nacional Colombiano de Primatologia (PNCP) (Fig. 1).

STUDY SITE
The study site was an undisturbed semideciduous forest of about 100-110 ha which

476

T . R . DEFLER

I
,,o , :,~

Fig. 1. Locati~ m of the Territorio Faunistico E1 Tuparro in eastern Colombia. The study site was located immediately south of the mouth of the Tomo River. : study site.

surrounded a 100 m high hill consisting of a granitic out-cropping of the Guyana shield. The hill or "cerro" is located directly south of the mouth of the T o m o River in Vichada lntendencia and overlooks the nearby Orinoco River (Figs. 2a & 2b). The majority of the forests in the area are of the gallery type and these are extensively flooded during the rainy season of M a y to October. The particular site was chosen because it remains above the high water mark, allowing entry at all months of the year. The climate of the area is typical of the llanos with a strongly marked wet and dry season. The annual rainfall in 1975 and 1976 as measured by a weather station 2 km north of the cerro was about 2,100 ram. The great majority of rain falls during the wet half of the year. Daytime temperatures vary from 20~176 in the wet season to 30~176 in the dry season. Nighttime temperatures can occasionally drop to 15~ During the dry season extensive savanna fires set by nomadic Indians are common. These fires are strong influences on the forests inasmuch as they kill back seedlings at the forest edge and create sharp borders between forest and savanna. The fires not uncommonly burn far into the forests due to extensive leaf litter caused by leaf fall. This also causes kill-back of seedlings and destruction of large trees with much dead wood and damage of other living trees. Fire damage observed by the author in the study site and in other areas suggests a pyrrhic (fire interrupted) climax for some parts of the savanna forests in the study area.

Fig. 2. View of the study forest on part of the cerro and a view of the llanos toward the southeast from the top of the cerro.

Ecology of Cebus albifrons

d.

477

a.

211ID

-~
t

111-

I
Fig. 3. A 60 m by 5 m transect of cucuritu forest. Note the many granitic boulders and the indicated slope. Cucuritu seedlings (c) and Bactris palms (b) are very commonly scattered throughout the dicots. Adult cucuritu (a) are also typically scattered throughout the dicots (d) represented by Ficus, Dipteryx, Ceiba, etc. The study forest was in most parts well-drained with predominantly granitic rock and course gravel soil with little humus. The cerro forest is located both on flat terrain surrounding the cerro and sloping terrain up to as much as 45 ~ or 50 ~ on the cerro sides. The major portion of the study forest may be divided into two major plant communities. The predominant type is a semideciduous forest with a canopy at between 20-25 m with a few emerging trees up to 30 m. The most common plant is the cucuritu palm (Attalea regia = Maximiliana elegans) found particularly in very gravelly parts of the forest where it is encountered almost as a pure stand, particularly as seedlings and subadult trees (Fig. 3). The other major forest type is found in rockier and drier areas, usually higher on the cerro slopes (although not invariably). This forest type consists of a vegetation with a canopy of about 10 m or less with the emergent palms cucuritu (less common) and Syagrus orinocensis (most common). This type of dry forest (or wood) is found on loose granite boulders with little gravel soil and the typical ground cover are Bromeliaceae of at least two species. By far the most common dicot is the important food shrub majabillo (Oxandra espintana Anonaceae) which grows in thick stands (Fig. 4). Fully one half of the cerro consists of bare, weathered granite with clumps of vegetation consisting of small bushes, Cactaceae, Orchidaceae, and Bromeliacea. In January 1978 a third forest type was added to the home range of the Cebus group under study. This consisted of an area that is flooded during the rainy season but dries out in the dry months so that the maze of water channels could be used as paths to penetrate the forest. The forest was predominantly a mixture of platanota (Phenakospermum guianense) and the important food plant palo pil6n (Goupia glabra Celastraceae) but also seje palm (Jessenia cf. polycarpa), moriche palm (Mauritia flexuosa), and cucuritu. Bactris sp. was scattered throughout. The floor was predominantly covered with lengua de perro (Ischnosiphon Maranthaceae) and the canopy was in general 10-15 m with some emergents to 20 (Fig. 5).

478

T . R . DEFLER

201
g S 1 0 84

a.

Fig. 4. A 60 m by 5 m transect of the dry Syagrus/majavillo wood which is typical of the upper, drier slopes of the cerro. Ground cover is almost exclusively Bromeliaceae (b). Syagrus orinocoensis (a) is the dominant palm while majaviUo (c) is a dominant shrub.

20'

a.

b.

r
m i=

10

Fig. 5. A 60 m by 5 m transect of the seasonally inundated swamp forest with the predominant plants platanota (c) and palo pil6n (a). Other important plants in this community were the seje palm (b) and the moriche palm (d). Dog's tongue (lengua de perro) (e) was scattered through the forest floor. This forest type gives way to the other forest types as the land becomes elevated around large granitic rocks; so that the entire forest utilized by the Cebus group may be described as three types in a spectrum ranging from seasonally inundated swamp Platanota, palo pil6n to well-drained gravelly soil Cucuritu, deciduous forest to rocky, dry Syagrus-Bromeliaceae-Majabillo woods. There is no human colonization in the area and hunting is forbidden so that many other animals are common in and around the site. METHODS During the months of July and August 1977 a trail system of about 5-7 km was developed throughout the forest surrounding the cerro and full-time observations were initiated on September 17, 1977. Observations (attempts at contact) usually began at 7:30 a.m. and continued until

Ecology of Cebus albifrons

479

4:30-5:00 p.m., although some attempts were made to begin contact between 5:005:30 P.m. from the sleeping site and to extend observations until the end of the day at 5:30-6:00 p.m. RESULTS
GROUP NUMBER AND STRUCTURE

The group consisted of 35 individuals with an adult socionomic sex ratio of 2.5 :l female to males. Table 1 shows the age/sex classes of the group. Female adults were defined as the largest females of roughly the same size. An adult female collected from another group in the area weighed 2,228 g. Adult males were males that were a bit larger than adult females in general but also had more heavily muscled heads, especially masseters, broader shoulders, much more prominent canines, and prominent testicles. An adult male collected from a nearby group weighed 2,650 g. A category of subadult males was used which had no counterpart among the females. Subadult males were about the same size as adult females. In two of the three subadult males the testicles were not pendant. In all cases the faces were indistinguishable from adult females and the limbs had the same appearance as adult females. A subadult male collected from a nearby group weighed 2,156 g. Juveniles of both sexes were defined as being smaller than adult females or subadult males but larger than a coherent group representing the smallest animals, which were the infants. USE OF SPACE

Daily Activity Pattern

The group became active very early around sunrise at 5:15-5:30 P.m. When observed this early they stretched, defecated, urinated, and immediately began to travel to another part of their home range, especially if they had been widely foraging the evening before. When foraging on a concentrated food source such as palo pil6n, they began foraging again quite early. Feeding and foraging continued towards midday when a rest period of several hours 0 - 3 ) was often initiated. Such rest periods did not always include all animals but the activity was characterized by many animals resting quietly in trees on their belly or side or by quiet activities such as grooming or low intensity foraging. During such rest periods the observer could easily overlook the group because of the low activity level accompanied by little or no vocalization. Probably the highest intensity activity during these mid-day rest periods was juvenile and infant play. Temperatures of about 35 ~ C and above at mid-day seemed to insure quiet rest periods whereas mid-day temperatures much below 35~ seemed to encourage more mid-day foraging activity.
Table 1. Age/Sex classes of study group

Adult Subadult Juvenile Infant Total

Females 10 0 5 4

Males 4 3 4 3

Unclassified 0 0 1 1

Subtotal 14 3 10 8 35

480

T.R. DEFLER

From early to midafternoon the Cebus began active foraging even if the temperature remained high. By 4:00 or 4:30 the group often headed towards and restricted its activity around the sleeping trees they would be using for the night. Often many were in the sleeping trees grooming or resting 30-45 rain before sundown. Rainfall disrupted the general pattern since heavy rains invariably caused huddling and shelterseeking until the heaviest rainfall was over.

Foraging Strategies
Depending on the concentration and type of food, many types of foraging were evident. The group might feed closely together all day in an area with a concentrated and preferred food source (such as palo pil6n or majabillo). If food items were spread out the group moved in a broad front directly measured up to 250 m wide. Such travels could involve 4-5 km in a day of foraging. The types of food available were effected by the seasonality of food species available. For example, during the first part of the study which corresponded with the end of the rainy season the group spent many hours in the activity termed (by the observer) "'palm leaf stripping." Many of the group would busily search out likely dead palm leaflets of the cucuritu palm which, on drying, role into long tubes. These tubes are the homes of a great variety of invertebrates. A typical search involved a systematic opening of the tubes from the rachis to the apex of the leaf by means of sliding the thumbs along the leaf. Many of the invertebrates appeared to become trapped as they moved into the narrowing tip of the rolled leaflet. A monkey, on finding a well-inhabited palm leaflet, might find several food pieces per leaflet, therefore spending as many as 20-30 rain working a group of leaflets. As the season became drier there was a marked decrease in the palm leaf stripping activity (although it never ceased entirely) and an increase in exploitation of crops of fruits, some of which were extremely abundant at particular times. Thus, in December the group spent much time in dense groves of majabillo. In January they concentrated for several weeks heavily on the sweet palo pil6n which grew in profusion in the seasonally flooded forest. Early on it became evident that the group routinely descended to the ground and crossed bare rock and grassy savanna to reach separate parts of their range. At one habitual crossing over savanna from one part of the forest to another, the animals were found to have worn a trail through the grass which enabled them to pass quickly from forest to forest. The group was seen to use this trail with some frequency (see Fig. 6). With an increase in their confidence near the observer and perhaps with an increased need during the dry season for different types of foraging the animals were seen to spend more and more time on the ground within the forest, where they at first seemed to be merely moving. They were soon seen to be eating fruits of ground Bromelia, to be foraging for insects in the layer of leaves which builds up each dry season and to eat fallen fruits of sarrapia (Dipteryx punctata) and guarai (Couepia ehryso-

calyx).
Towards the end of the study in February, many of the animals were seen at times to spend up to 50 ~ (or more) of the day's observations moving along and foraging on the ground. Often when seen low in a tree or bush an animal would move away from

Ecology of Cebus albifrons

481

Fig. 6. Thirty meter trail worn in savanna grass between two forests by two Cebus groups in overlapping portion of home range. Trail has several rocks and bushes in path which are used as observation posts during crossings. Members of study group passing over 30 m of bare rock to reach a part of study forest. the observer by jumping to the ground to leave. At times he entire group attempted to sneak away from the observer on the ground. Such terrestrial travel seemed very quiet in contrast to the sounds of moving branches often made during tree travel. During January when the animals concentrated on feeding from palo pil6n, they also spent much time examining the wild platanota. The peculiar growth form of this plant allows water to collect in pockets between the axilla of the leaf stems and within this water may be found frogs and aquatic insects. The monkeys spent much time ripping the leaf sheaths away to get at the small water reservoirs and they were seen to eat both insects and a frog. The water was also drunk from the pockets. At the dry season the fruit of the platanota is mostly a hard seed which is extracted from the husk only with great difficulty. The animals worked hard extracting this seed by vigorously pounding the fruit against a hard substrate and biting at it. The monkeys were fond of the mesocarp around the outside of the cucuritu nut and spent much time looking in the clumps of these nuts for perfectly "ready" ones (Fig. 8). When ripe nuts were not available the animals would pick an old nut that had the mesocarp and rind cleaned off by both themselves and other animals. They would spend some time trying to crack the nuts open by either striking the nut on a hard surface (palm rachis or a tree branch) or trying to bite it open. They did not appear to have much success in this endeavor while observed, although the sounds of attempted nut cracking were not uncommon. The observer cracked open several nuts between two rocks and found in some of them a delicious nut of cocomeat, in others a very fat

482

T . R . DEFLER

Fig. 7. Monkey upside down, tearing axil sheaths of wild platanota to extract frogs or aquatic insects. A closeup of a wild platanota that has been torn by monkeys.

Fig. 8. Juvenile monkey picking cucuritu nuts. grub that had been feeding on the cocomeat. It would appear that either cocomeat or grub would be adequate reward for finally cracking open these hard nuts. Two males had been observed another time digging for and eating grubs in what appeared to be an old trogon (Trogonidae: Aves) nest dug into the side of a termite nest plastered around a tree branch. The particular activity appeared to be so rewarding that the original adult male was displaced by the alpha male who continued exploiting the grub cache until it was empty.

Ecology of Cebus albifrons

483

Home Range
The g r o u p used a range o f a b o u t 110-120 ha, m o s t o f which w a s o n the sides a n d at the f o o t o f the cerro. Very often the animals were seen to pass across b a r e r o c k a n d s a v a n n a to get to o t h e r parts o f their range a n d the use o f 3-5 m high vegetation for m o v e m e n t was n o t u n c o m m o n . It g r a d u a l l y became evident t h a t the cerro g r o u p shared 20-30 ha with a n o t h e r Cebus g r o u p whose m a i n range was to the s o u t h o f the cerro a n d three instances were observed at the extreme south limit o f the cerro g r o u p ' s activities when the cerro g r o u p gave w a y to the a p p r o a c h i n g south g r o u p a n d quickly m o v e d t o w a r d s the cerro, a w a y f r o m the south group.

Core Area
M a p s o f the area used by the cerro g r o u p showed several intensive uses o f core

Fig. 9. Map of the home range of study group with overlapping area with second group. R: rock; F : forest; Dotted areas indicate core areas or areas of greatest use. areas which c o r r e s p o n d e d with the highest vegetation 20-30 m, the best foraging a n d the m o s t utilized sleeping areas. O f the f o u r core areas, the largest one was used m o s t intensively o f all a n d was l o c a t e d on the 30~ ~ east-facing slope o f the cerro (Fig. 9).

Sleeping Trees
Certain sites were p r e f e r r e d for sleeping over o t h e r sites a n d the core areas were most often chosen over o t h e r areas. A c o n c e n t r a t e d f o o d source often d e t e r m i n e d in w h a t a r e a the g r o u p w o u l d spend the night. In the favorite core a r e a one g r o u p o f trees including an a d u l t cucuritu p a l m was chosen three times a n d the animals settled at 25-30 m f r o m the ground.

484
Diet

T . R . DEFLER

T h e o v e r w h e l m i n g i m p r e s s i o n while studying f o o d habits o f this species is t h a t they eat all t h a t is eatable. A r o u g h b r e a k d o w n o f the g r o u p ' s feeding w o u l d be a b o u t 80 o f their time feeding on vegetable m a t e r i a l a n d 20 ~ on a n i m a l material. O f the vegetable m a t e r i a l fruits are the m a j o r item; but various nuts, seeds, leaves, a n d flowers m u s t also be listed. A p a r t i a l list o f f o o d items is included in Table 2. A n i m a l materials in the diet included insects ( b o t h adults a n d larvae), o t h e r invertebrates, tree frogs, lizards, a n d h o n e y o f m e l i p o n e bees. The i m p o r t a n c e o f the cucuritu p a l m a n d the role o f the p l a t a n o t a have a l r e a d y been m e n t i o n e d above.
Drinking

The Cebus were observed to d r i n k water f r o m various sources besides f r o m the p l a t a n o t a . Very often the animals t o o k water f r o m tree holes which are filled f r o m rain. All such holes seem to be k n o w n to the m e m b e r s o f the g r o u p as it was n o t unc o m m o n to see an a n i m a l go p u r p o s e f u l l y to a certain tree a n d a certain hole to drink, Table 2. List of food items collected during the study Part Family Species utilized Common name Anacardiaceae Spondiascf. mombin F hogo, jogo, hobo Anonaceae Apocynaceae Araceae Arecaceae
Oxandra espintana Plumeriopsis sp. Anthurium sp. Attalea regia Bactris sp. (?) Bactris sp. Jessenia cf. polycarpa Mauritia flexuosa Syagrus orinocensis

F F I F N F N F N F N N F N F E F F F F F F F F F N F

majabillo merecuri; platanota guanabanare canilla de grulla cucuritu albarico albarico montafiero seje moriche pajuena guama montafiera pifia de danta maya resbalamico catamajaca palo pil6n guaray guaray guaray reventillo cometuru coco de mono

Collection No. D-5 B-491 D-22 E.-488 D-15 B-487 B-483 D-2 B-474 D-30 B-482 D-16 B-470 D-13 D-27 B-468; 469 D-41 D-19 B-506 D-20 D-8 B-478 D-28 B-467 D-11 ; 39 B-481 B-481-A I3-39-A D-32 D-1 D-29 B-466 (continued)

Bignoniaceae Bombaceae Bromeliaceae Burseraceae Celastraceae

Unknown Ceiba sp.

Ananas comosus Bromelia sp. Bursera simarouba Tetragastris mucronata Goupia glabra

Chrysobalanaceae Couepia chrysocalyx

Licania sp. Parinari exelsa

Connaraceae Euphorbiaceae Lecythidaceae

Unknown Unknown
Eschweilera sp.

Ecology of Cebus albifrons Table 2. (continued) Leguminosae Dipteryx punctata

485

D-38 B-482 Inga F guamita D-37 Unknown aceite B-385 Maranthaceae Ischnosiphon sp. ? I lengua de perro B-463 Melastomataceae Bellucia grossularioides F guayabito B-477 Myrtaceae Unknown F curame D-10 Moraceae Brosimun sp. F boche de pajuil D-3 Ficus cf. insipida F D-6 Ficus sp. F laurecito D-7 B-508 Ficus sp. F matapalo D-12; 36 B-486 Ficus sp. F pendarito D-21 ; 25; Ficus sp. F (different) B-472; 475 Musaceae Phenakospermum platanillo D-31 guianense S platanota salvaje B-464 Orchidaceae Maxillaria sp. St 1)--43 B-513 Passifloraceae Passiflora sp. F coroto D-17 Passiflora sp. F coroto D-23 Rubiaceae Randia sp. F palo espinoso; D-14; 42 guayabito B-492 Unknown Unknown F naranjillo D-4 Unknown Unknown F pasa D-24 Unknown Unknown F palo amarillo D-40 Unknown Unknown F tupiritu D-44 F = fruit; I = infloresence; N = nut; St= stem; D = collection of DEFLER; B = collection of BARBOSA; c o m m o n names based on INDERENA informant, RAIMUNDOEVARISTO, a member of the Curripaco Indian tribe and long-time resident of Tuparro. either p u t t i n g the lips to the w a t e r or, in the case o f a smaller hole or low water, p u t ting the h a n d into the w a t e r a n d raising it n e a r the m o u t h where the w a t e r was licked or sucked f r o m the fingers or the hair on the wrist. W a t e r was also c o m m o n l y licked f r o m a n y surface after a rain, w h e t h e r f r o m leaves o r tree branches. I t was n o t u n c o m m o n to see the a n i m a l s d r i n k f r o m flowing w a t e r in a small creek which h a d its source in the cerro. Also, there were m a n y hollows in the r o c k surface which p r o v i d e d watering holes for the animals as t h e y m o v e d across the rock. D u r i n g p a r t o f J a n u a r y a n d m o s t o f F e b r u a r y (except for two brief rains), all w a t e r w i t h i n the h o m e range o f the cerro dried u p except for a small spring which was l o c a t e d t o w a r d s the f o o t o f the eastern slope o f the cerro. D u r i n g this time the animals established a p a t t e r n o f several visits to the small p o o l every d a y to drink, a n d this p r o v i d e d m a n y excellent o p p o r t u n i t i e s for observation. This was p a r t o f the m o s t i m p o r t a n t core a r e a o f the g r o u p a n d the fruits o f the g u a r a i a n d the sarrapia, a p a r t i c u l a r l y i m p o r t a n t p a r t o f the F e b r u a r y diet, were quite c o m m o n in t h a t p a r t o f the forest. The s i t u a t i o n allowed a r a t h e r intensive use o f a small p a r t o f the forest a n d p r o v i d e d unusual o p p o r t u n i t i e s for p h o t o g r a p h y o f the animals as all h a d to descend to the g r o u n d for drinks. Birth Periodicity The following evidence suggests a b i r t h p e a k f r o m the e n d o f the d r y season into the

serapea; serrapia

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T.R. DEFLER

wet season. From the beginning of the observation on September 17 until February 21 there were no births. On the night of February 21 one infant was born. During the end of February three other females were obviously pregnant. Also, when observations were begun in September the smallest infant was seen to be riding across the mother's shoulders. The position was mostly jockey-style (ventral/ dorsal) in October-November and one or two other infants were seen riding in the same style at least into December and at times in January. OPPENHEIMER(1976) suggests that Cebus capucinus babies ride their mothers especially during the first six months and that the across-the-shoulders position is important to that species especially during the first three months when that seems to be the most secure grip. If Cebus albifrons is similar to Cebus capucinus in this behavior, then the youngest infant observed in September 1977 was probably born in June or July. Other infants seen riding jockey-style were probably born one to three months earlier. All animals in the class identified as infants were very similar in size.
]NTERSPECIFICRELATIONS

Predation
No direct predation on this group was observed, although ample indirect evidence suggested various predators were known to this Cebus group. Almost any fast flying bird ellicited danger cries from the group members. Generally the danger calls were brief and stopped, assumedly because the nature of the "threat" was recognized. By far the most frequent danger call elicited from a bird was due to black (Coragyps atratus) and turkey (Cathartes aura) vultures flying over the canopy. Three times an immature balck-and-white hawk eagle (Spizastur melanoleucus) was observed very close to the group and each time a few scattered danger cries were elicited and the group moved away after crying danger (although not intensively). On January 21 an adult ornate hawk-eagle (Spizaetus ornatus) alighted very near foraging members of the group, causing a few intense high-pitched alarm notes. The monkeys then hid very effectively in dense vegetation and during the 2-3 min that the bird quietly perched and 5 min after he flew away. The observer was not able to see or hear the m o n k e y s ' - a very unusual occurrence when the animals were so closeby. The first vocalizations after the bird left were very soft. On five occasions the mustelid Eira barbara was seen close to the Cebus group. Reactions varied from hot pursuit of a young monkey across the forest floor up into a tree by the female Eira (where the monkey easily escaped) to almost completely ignoring a male Eira, which came to a water hole to drink while members of the group calmly observed from 2 m above the water. In the latter instance the alpha male descended to the ground observing the Eira from only 2 m and no danger calls were given whereas in the former case scattered danger calls were given.

Other Primates
Two other primate species shared the forest with the Cebus. These were Aotus trivirgatus andAIouatta seniculus. During initial trail cutting two nesttrees of one group of five Aotus trivirgatus (the night monkey) were located and later a second group was

Ecology of Cebus albifrons

487

found. There were many occasions when the Cebus group passed closely and even used the same tree, but there was no interaction between the two species except that the Aotus peered out of their nest hole at the members of the passing group of Cebus. These Cebus were never observed to take notice of the Aotus. The two species are competitive for certain food trees, however, as both were seen to return to a Ficus tree until most of the fruits were consumed and both ate the fruits of a nearby merecuri (Plumeriensis Apocynaceae). More interactions were noted between the Cebus and members of the four Alouatta seniculus groups resident in the main 100 ha forest. Reactions were variable between the two species and ranged from curious interest to movement away from each other. In a few instances several AIouatta were seen to leave the area when the Cebus arrived. At least some of the instances might have been because the Alouatta sighted the human observer but in other cases this was probably not so. It was also common to see the Alouatta ignore the Cebus and continue feeding in the area. Some instances were seen of several Alouatta passing close to the Cebus but not seeming to react to them. During one observation an association of Cebus and Alouatta was seen for several hours. Watching several Cebus move down the cerro, two Alouatta were seen moving in close association in the same direction, having seen the observer they gave the impression of relying on the other species to cover up their own flight. Thirty minutes later several AIouatta were seen foraging in the middle of the general Cebus activity, somewhat spread out in a few trees. Soon some Cebus moved off further down the cerro towards a particular fruit tree. Three of the Alouatta immediately proceeded in the same direction in front of the Cebus. The adult male Berto then proceeded after the mixed group, passing close to a lone male Alouatta that was hanging by its tail and feeding quietly. Berto was seen to glance at the howler, but both proceeded peacefully with its own activities. Proceeding to the feeding tree at least four AIouatta and several Cebus were observed feeding in the same tree for an hour. Later, as the Cebus began moving across the cerro slope at a right angle to the previous line of travel, two Alouatta were again observed to move proceeded by and closely followed by Cebus. The Alouatta finally passed out of the sight of the observer as he continued to observe the

Cebus.
DISCUSSION These data suggest strong similarities to Cebus capucinus (OPPENHEIMER, 1968), C.

nigrivitattus (OPPENHEIMER OPPENHEIMER,1973), and C. apella (IZAWA, 1978, 1979; DEFLER, pers. obs.) as well as some differences. Cebus albifrons exhibits a diet very
similar in many respects to that known for C. capucinus and C. apella. The three species also show a broad use of the habitat that is highly opportunistic with a strong omnivorous tendency. The home range of C. albifrons is similar to that of C. capucinus (90 ha) and C. apella (ca. lO0 ha; DEFLER,pers. obs.) but the group size is much larger than reported for any of the other Cebus, being more than twice as large as group sizes seen in C. apella (KLEIN & KLEIN, 1976; DEFLER, pers. obs.). HERNANDEZCAMACHO and COOPER 0976) have also commented on the large numbers seen in some groups of C. albifrons.

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The terrestriality of the study group was extreme when compared to any other New World primate species so far studied, although it becomes increasingly clear that some species spend a part of their time on the ground. Cebus albifrons has a deserved reputation as a rnaiz stealer--moving out from the tree cover into the maiz fields that have usually been planted in a patch of cut forest--in effect utilizing part of a home range that has been drastically changed to a monoculture by man. Other data on C. nigrivitattus (OPPENHEIMERt~ OPPENHEIMER,1973) and C. apella (DEFLER,pers. obs.) suggest that these species also regularly descend to the ground for drinking and foraging. This may be a habit much more common than supposed for other New World primates since even the very arboreal Alouatta seniculus has been seen moving across large tracts of savanna from one forest to another (HERNANDEZ-CAMACHO & COOPER, 1976; DEFLER, per. obs.). It is suggested here that opportunistic feeding and a patchy or disrupted forest habitat may be two pressures influencing such terrestrial behavior. The llanos are obviously a good example of a naturally disrupted forest cover; and, in the case of the study group, passage from one part of the home range to another was facilitated by traveling on the ground. The seasonal buildup of leaf litter on the forest floor provided another incentive to descend for foraging in a newly created, though temporary, microniche which provided insect and other arthropod food. Other ground foraging was encouraged by the fruits of ground bromeliads. The lack of water, usually quite abundant in tree holes when there is rain, provided a strong pressure in the case of the study group to go to the ground to drink from a spring; and this probably provides the same pressure for observed groups of C. apella to drink from streams. The study group also traveled quite a lot on the ground. Whether this was coupled strongly with the desire to ground forage or to move quickly and quietly (away from the observer?) must remain open to further study. It is important to realize that in Colombia other demes of this species are found in habitat that seems much more amenable to existence the year round, since they are located in closed canopy forests without the extreme dry season of the llanos. It would seem important to study other populations of this species found in less extreme habitats for comparison as well as to study the closely related species C. apella which is found in the same type of habitat as that of this study. The author is engaged in the latter type of study which will be reported at a future time.

Acknowledgements. The author wishes to acknowledge Dr. EDLrARDOMORA, Jefe de Secci6n de Bot~inica, and Prof. Drs. JESUSIDROBO,ROBERTOJARAMILLO, and GUSTAVOLOZANO,all of the Instituto de Ciencias Naturales de la Universidad Nacional for their collaboration in identifying botanical specimens. For aid in field collection many thanks to Sefiorita NELLY E. SANTACRUZof the Pl'ogTalna Nacional Colombiano de Primatologia and to Sr. C~SAR BARBOSA,botanist of the PNCP for help in field collection and in identification of plant materials. Thanks also to Dr. JORGE HERN.~NDEZ,Jefe de Secci6n de Fauna y Vida Silvestre/ INDERENA, and Dr. CARLOSMEJiA, Director del Programa Nacional Colombiano de Primatologia/INDERENA for a critical reading of the manuscript and for other kind help in realizing this study. The author would not be able to be in Colombia without the help and support of the American Peace Corps.

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