Locomotor behavior ofPan paniscus in Zaire

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AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY 53:69-80 11980)

Locomotor Behavior of Pan paniscus in Zaire RANDALL L. SUSMAN, NOEL L. BADRIAN, AND ALISON J. BADRLAN Department of Anatomical Sciences, Health Sciences Center, State University of New York at Stony Brook, LongIsland, New York 11794 (R.L.S., A.J.B.), and Department of Anthropology, State University of New York at Stony Brook, Long Island, New York 11794 (N.L.B.)

KEY WORDS Pan paniscus, Pygmy chimpanzee

Bonobo, Hominoidea, Locomotor behavior,

ABSTRACT The locomotor behavior of Pan paniscus was studied over a four- week period in Equateur, Republic of Zaire. Bonobos were found to be both arboreal and terrestrial in their daily activities. In the trees adult bonobos are basically quadrupedal, but they also have significant components of armswinging, diving, leaping, and bipedalism in their locomotor repertoire.

Pan paniscus has fascinated primate bi- ologists and especially theorists of human evolution for almost fifty years (e.g., Coolidge, ’33; Schwarz, ’34; Simons, ’72; Tuttle, ’75; Zihlman and Cramer, ’78; Zihlman et al., ’78; Zihlman, ’79; Corruccini and McHenry, ’79). Still, Pan paniscus’, the bonobo or “pygmy chimpanzee,” remains the least well known of the apes. There have been a number of investi- gations ofPanpaniscus since its description by Schwarz (’29) (Fig. 1). These include detailed studies of its morphology (Coolidge, ’33; Miller, ’52; Fenart and Deblock, ’73; Johanson, ’74; Cramer, ’77) and its captive behavior (Yerkes and Learned, ‘25; Jordan and Jordan, ’77; Savage-Rumbaugh et al., ’77). These investiga- tions revealed interesting differences between bonobos and chimpanzees in skull form (Fenart and Deblock, ’73; Cramer, ’771, dentition (Johanson, ’74), limb morphology (Coolidge, ’33; Rode, ’41; Tratz and Heck, ’54; Schultz, ’69; Zihlman and Cramer, ’781, behavior (Yerkes and Learned, ’25), and external appearance (see Coolidge, ’33:&8).

Preliminary reports on free-ranging bonobos have also appeared (Nishida, ’72; Kano, ’791, but information on Panpaniscus in its natural habitat is scant compared to that on the other apes, and all work that has appeared, save that of Kuroda (’79), has failed to yield consistent or conclusive results that might be used as a basis for comparisons of Pan paniscus and Pan troglodytes. Badrian and Badrian (‘77) and MacKinnon (’78) concluded that bonobos are more arboreal than chimpanzees, while brief direct and indirect observations of Horn (‘76) and Nishida (’72) suggest the opposite. To date,

no one has attempted to record systematically and quantify the locomotor behavior of bonobos.

Herein we will describe results of a two- month expedition to observe and record the locomotor behavior of Pan paniscus in the Equator Region of the Republic of Zaire.

METHODS

We spent four weeks in the Lomako Forest of Equateur, Republic of Zaire, in February and March of 1979. Other data were collected in an earlier study done by N.L.B. and A.J.B. in 1974 and 1975. Our work was conducted in primary rain forest bounded by the Lomako and Yekok- ora Rivers (Fig. 2). The study area is roughly 35 sq. km. and is located at 0.50’ N, 21.05’ E (Fig. 3). The period of study spanned the dry season, peak dry seasod, and the immediate dry-wet season transition. We and our local guides made contact with bonobos on 17 of 28 days in the study area. We had 11 hours and 45 minutes of direct visual contact with the subjects. Additional observations were made by our

‘Schwan diagnosed the new taxon as a distinct subspecies, Pun satynrsponrseus. Coolidge (‘333) later conferred species status on the new taxon and first applied the term “pygmy chimpanzee.” Tratz and Heck (‘54) elevated the species to a new genus, Bonobo. The generic separation ofPanpaniscus from Pan troglodytes has not been accepted by other workers, hut the term “honobo” has caught on as a more suitable common name.

*The length and timing of the dry season is variable in the central Zaire basin. Records from Yangambi, east of our study area show an annual dry season from December through February and another brief period of reduced rainfall in June. In our area the brief dry period was slightly later. The effect of the dry seasons is not severe enough in the central hain to inhibit the luxuriant growth of vegetation.

Received August 1, 1979 accepted November 20, 1979.

0092-948318015301-0069$02.30 C 1980 ALAN R. LISS, INC. 69

R.L. SUSMAN, N.L. BADRIAN, AND A.J. BADRIAN

LOCOMOTOR BEHAVIOR OF PAN PANlSCUS 71

Fig. 2. Map of Equateur and location of Lomako Forest.

guides when we were unable to see animals ourselves.

The small streams which bound the study area are not large enough to act as barriers to movements of bonobos. All our observations were made in primary tropical rain forest, though the study area as a whole contained islands of secondary forest and some swamp forest. A forest survey was conducted during 1974-75 in which three blocks of forest 10 m x 120 m and one block 10 m x 90 m were sur- veyed in order to determine tree species com- position and forest types. The primary forest was on firm sandy soil and had a continuous canopy layer a t 30-40m. The canopy was dominated by species of Polyalthia and Scoro- dophloeus. Emergent trees, such as Oxystigma oxyphyllum, Antiaris toxicaria, and many other species reached 45-55 m. The middle story was more open and did not form a continuous layer. The shrub and herbaceous layers were poorly developed; however, in places where large trees had fallen and sunlight could reach the ground there was prolific growth of herbaceous plants such as Palisota ambigua and Haumania lib- rechsiuna. Climbers, stranglers, lianes, and

epiphytes drape the trees of all three layers and provide an important network of connections between adjacent trees in adition to the continuous terminal branch networks. Strangling figs Ficus spp.) are the most significant plants in this group. They were important as food sources (Badrian et al., in prep.) and as a sub- strate for locomotion.

To locate and observe the bonobos, we made daily treks into various parts of the study area. Each of us was accompanied by a guide. Our guides were hunters and superb t racked . They were able to locate animals by sound, sight, and spoor. Upon ctontact we would quietly approach the subjects and seek a strategic position from which to observe the animals unobtrusively. The noise we made while moving through the undergrowth and the sounds of our cameras frequently alerted the bonobos to our presence and this generally evoked excitement and display. At times the animals clamly resumed feeding, grooming, and locomotor activities. The locomotor behavior reported here was no doubt affected by our

"People of the Lomako do not hunt or eat bonobos.

72 R.L. SUSMAN, N.L. BADRIAN, AND A.J. BADRIAN

Fig. 3. Details of inset in Figure 2. They include our base camp, Ndeli, and the study area bounded by Bakumba, Bofua, Yite, Eyengo, and Ndeli Rivers. Broken line indicates our path into the forest and major routes in the study area.

presence, especially on occasions when the subjects noticed us. Because we were not able to approach subjects silently on the ground or to achieve suitable vantage points before bonobos fled, most observations of terrestrial locomotion were made by our guides. We confirmed the accuracy of their reports with evidence such as food remains, footprints, feces, and in some cases impressions left by bonobos sitting or crouching on the ground.

Animals were most frequently encountered while feeding or resting in the trees. We were able to record almost all movements of animals so observed. When we encountered a group of animals, we concentrated on individuals that were moving or, if more than one animal was moving, we focused on a single individual. We recorded locomotion according to the use of hands and feet and gait patterns listed in Table 1, and according to types of substrates upon which they moved (Fig. 4). Trunks are defined

as the stout, primary members of the tree. The trunks of Dialium pachyphyllum, Dioga Zen- keri, Antiaris welwitschii, and Scorodophloeus zenkeri had diameters as large as 30-90 cm. Boughs are defined as secondary elements and are between 15 and 20 cm in diameter. They normally extend horizontally from the trunk in the lower part of the tree and become more oblique toward the crown. Single boughs are capable of supporting a bonobo’s full weight. Branches are tertiary supports that range from 2 to 15 cm in diameter, and the thinner ones are probably capable of supporting bonobos only in networks. The twigs and leaves associated with branches were designated “foliage.” Bonobos frequently use branches and foliage simultane- ously for support.

A bout of locomotion is defined as a movement from one stationary posture to another or as a definable element of a continuous sequence of progression between two points (Fleagle,

LOCOMOTOR BEHAVIOR OF PAN PANISCUS 73

’76a:252). Our mode of recording locomotor sequence by an adult male is illustrated by the following record.

Bipedal-three steps on bough-stop- drumming on bough with hands.

Bipedal-three steps on bough. Armswing-2 m along bough onto slightly

lower branch of adjacent tree.

OBSERVATIONS

Most of our observations of arboreal locomotion were made while the subjects were feeding. Sometimes bouts of feeding were interrupted by us, and the animals displayed and took flight. Bonobos used five types of locomotion in trees. These include: 1) palmigrade and knuckle-walking quadrupedalism; 2) quadrumanous climbing and scrambling; 3) bimanual suspension, including armswinging and dropping; 4) leaping and diving; and 5 ) bipedalism.

Arboreal quadrupedalism This mode of progression recruited all four

limbs in diagonal or, less frequently, lateral gaits. Thirty-four percent of observed bouts involved quadrupedalism on boughs or branches (Table 1). Most frequently, the movement occurred along horizontal or slightly inclined boughs, and less frequently, along branches. The feet were plantigrade on large boughs (> 20 cm). Generally, they were used to grasp smaller horizontal and oblique supports (< 20 cm). Palmigrade grasping hand postures were used on boughs up to 25cm thick. Knuckle-walking occurred on thick horizontal boughs of 30 cm or more. Quadrupedalism was the most frequent form of locomotion. It was employed in all movements to and from the trunk and the central part of the tree.

Quadrumanous climbing and scrambling During climbing and scrambling three or

four cheiridia contact the supports. Transfer- ring behavior that is employed to cross between the branches and foliage of adjacent trees is also included in this category. These three behaviors were observed in 2oo/o of the recorded progressions. Fifty-one percent of quadrumanous bouts took place on vertical supports, 44% were on branches and in foliage, and 5% were on oblique trunks or boughs. Ver- tical climbing involved regular (diagonal) gait patterns on vertical trunks. Scrambling, which utilized no regular gait sequence, was used in all parts of the trees and especially in the leafy networks prior to or after transfers between trees. Excited animals were especially given to

R.L. SUSMAN, N.L. BADRIAN, AND A.J. BADRIAN 74

‘ 1 Fig. 4. Schematic of emergent fruit tree to show the dis-

tribution of trunk, bough, branch, and foliage supports. These emergents reached 50 m in height. Bonobos showed definite locomotor preferences in given parts of the trees (see text for details).

dynamic, unpatterned locomotion that oppor- tunistically employed available supports.

Horn (’76:64) characterized the locomotion of bonobos as “quadrupedal scrambling.” This is an appropriate term for much of the movement we observed.

Bimanual suspension Bonobos employ a significant amount of

bimanual suspension during progression (20% of bouts). Since this movement differs from the brachiation of hylobatid apes, we refrain from using that term. Fifty-five percent of arm- swingingldropping was from branches, while 45% was from larger boughs. Animals of both sexes and all body sizes engaged in armswinging. Animals frequently swung along branches and boughs, especially when movement was downward as well as laterally. Most often, armswinging was along rather than between branches. Frequently, stationary or moving animals would drop or jump to a lower position, catching the bough or branch that they had been atop (or a lower one) with their hands. In one instance we observed a juvenile male miss a handhold after an armswinging sequence onto a lower branch. The animal hung by one hand

for a few seconds, then calmly regained a bimanual hold. In another instance we observed an adult male suspended by one hand from the stump of a broken branch on a thick trunk. The animal remained still, supported by the single grip, for approximately two or three minutes before he continued quadrupedally down the trunk.

Arboreal leaping and diuing Leaping or jumping involves initial hindlimb

propulsion from a bipedal or quadrupedal takeoff. This is preceded by quadrupedal running or by stationary takeoff when the distance crossed is 3 m or less. Eighteen percent of locomotor bouts included leaping or (headfirst) diving. Forty-seven percent of leaping and diving episodes occurred from boughs, 4#0 began on branches and in foliage, and 1Wo were executed from vertical trunks. In all cases leaping was from a higher to a lower support. The longest vertical distance covered in a leap was approximately 10 m; the greatest horizontal distance spanned in a leap was approximately 8 or 10 m. One incident involved an adult male which, after a quiet quadrupedal walk to the end of a branch, hesitated and then leaped feet first across a 6 m gap a t a height of 17 m. We observed headfirst dives in which animals crossed 5-8 m gaps and landed in terminal branches and foliage (Fig. 5) .

Bipedalism Arboreal bipedal walking in bonobos does not

differ from that described for chimpanzees. There appears to be distinctive pelvic rotation accompanying the characteristic bent-knee gait, wherein the body’s center of mass remains well behind, instead of passing over, the knee joint (Jenkins, ’72) (Fig. 6 and 7). Five of the 11 bouts of arboreal bipedalism occurred during displays. Six other bouts were recorded in un- disturbed animals, two of which were feeding and two of which were carrying food. One other incident involved a mother carrying an infant. Seventy-five percent of arboreal bipedal bouts were along horizontal boughs. One brief instance of bipedalism was observed on an inclined trunk and another was noted on a horizontal branch. One sequence covered a distance of 5 m or more. When the diameter of the bough permits, the hallux grasps the support. On very thick boughs the hallux is widely abducted as well, a configuration that probably improves lateral stability and balance. The longest episode of bipedalism was executed by a young adult male carrying bunches ofDialium pachyphyllum fruits in each hand (Fig. 6). He calmly

LOCOMOTOR BEHAVIOR OF PAN PAh'ISCUS 75

Fig. 5. Adult male diving head-first across a 6 m gap in the canopy at a height of approximately 17 m. This leap was preceded by a slow and cautious quadrumanous scramble through the foliage of the higher tree on the right. The animal landed in the foliage and branches on the extreme lower left.

walked 10 paces along a bough 15 cm in diameter from the terminus toward the center of the tree and out of view. Animals frequently stood bipedally on horizontal boughs while reaching with their hands to feed on fruits and leaves.

Terrestrial locomotion On the ground bonobos are knuckle-

walkers4. We observed one incident of bipedal walking on the ground by a large (50+ kg) male. He walked on an animal path holding stalks ofHaurnania librechtsiana in each hand. On spotting the observer he stopped, dropped the stalks, displayed in quadrupedal stance, defecated, then walked off quadrupedally.

To descend to the ground bonobos quadrupedally climb or slide down thick trunks, or they may use climbers and lianes. Animals frequently descended from heights of 25-30 m on boughs, branches, or trunks of large trees then transfered to smaller trees as they neared the ground (the buttresses of large trees may necessitate this). The last 5 or 6 m are normally covered by dropping with a crash into the shrub layer, or by transferring or leaping onto a sap-

ling and riding it to the ground as it bends under the animal's weight.

When threatened or frightened, bonobos descend from the trees and flee on the ground. If danger threatens from the immediate area around a tree, the animals move away to a safe distance before coming to the ground. It is im- possible even for the experienced local hunters to follow frightened bonobos on the ground.

BONOBO-COMMON CHIMPANZEE COMPARISONS

Although there has been a renaissance in comparative primatological studies during the past 15 years (Tuttle, '75), information on primate locomotion under naturalistic conditions is still in the late Middle Ages. The only apes for which there are quantitative locomotor data are the siamang and white-handed gibbon (Fleagle, '76b). Despite field studies on chimpanzees that date back almost 50 years (Nissen, '31), information on the locomotion of wild chimpanzees is scant. There are no quantita-

'Numerous incidences of knuckle-walking were reported to US by our two guides who were carefully instructed In the vanous hand postures assumed by apes such as fist, palm, and knuckle-walking

LOCOMOTOR BEHAVIOR OF PAN PANISCUS

tive data available on chimpanzees that record frequency or context of different locomotor and postural modes. This not only limits the possi- bility of comparisons between Pan paniscus and Pan troglodytes, but also precludes all but the most general attempts to link morphological with behavioral differences in the two species.

The descriptions of chimpanzee locomotion by Reynolds and Reynolds (‘65) are the most explicit. They reported that in forest chimpanzees the time spent on the ground and in the trees is dependent upon food resources and the time of day. Van Lawick-Goodall (’68) also noted that woodland chimpanzees spent 70% to 80% of daylight hours in the trees during the rainy season. Similarly, we found that bonobos spent significantly more time in the trees during periods in which fruit is more abundant. In the brief “dry season”j we did not observe bonobos in the trees a t all during the day (06:OO-14:OO h; 15:OO-17:30 n). The switch from trees to ground is probably dictated by a dimunition of certain food resources (fruit and new leaves).

When in the trees, i t appears that adult bonobos engage in more armswinging locomotion, diving, leaping, and bipedal locomotion than adult chimpanzees, (Kortlandt, ’72; Reynolds and Reynolds, ’65; Van Lawick- Goodall, ’68; Tuttle, ’75). Although Van Lawick-Goodall (’681, Jones and Sabater Pi (‘711, and Reynolds and Reynolds (’65) all observed “brachiation” in chimpanzees, Kort- landt noted that, in the wild, adult chimpanzees seldom brachiate, and when they do it is mainly in intimidation displays rather than in travel (’75:362). MacKinnon (’78) was im- pressed by the agility and “treetop grace and surefootedness of bonobos” compared to the chimpanzees of the Gombe Reserve.

Our observations concur with many of the in- cidents reported by Horn (‘761, but Horn concluded that bonobos are more terrestrial than chimpanzees. We noted that bonobos “ t r ek (i.e., cover distances of 2km or more) on the ground, and that in the dry season they do most of their feeding and traveling on the ground. We think there are good reasons for this: 1) It is faster to travel on the ground over relatively long distances in the forest; the longer distances must be covered when food sources are widely dispersed. 2)Travel on the ground is quieter. 3) For part of the day, and especially in the dry season, bonobos often remain on the ground to escape the sun and heat and to exploit abundant terrestrial food sources. 4) Quadru- pedal travel on the ground is a safer and more

energy efficient means of locomotion; animals traveling in trees must constantly adjust their vertical position to the available supports. With little in the way of predator pressure there is nothing to prevent bonobos from using terrestrial routes. In fact the forest is laced with an extensive network of bonobo and other animal trails. We also found numerous bonobo footprints (but, curiously, no knuckle prints) along stream banks and channel sands.

DISCUSSION

Our observations indicate that bonobos are both arboreal and terrestrial in their daily cycle of activities. The relative frequency of each probably varies according t o food availability. Ripley (‘79:44) noted that “Po- sitional behavior is many things, but most important it is the means by which a species of a particular size locates and harvests enough of those resources appropriate to its trophic role and foraging tactics to sustain life in a particular habitat over a complete seasonal cycle.” Re- quirements imposed by food availability and distribution, sleeping sites, and danger from predators or other animals demand a versatile locomotor repertoire. Bonobos must often cover distances of 2 km or more on the ground in search of fruiting trees, and certain foods are always abundant on the ground (e.g., Haumania librechtsiana and Pallisota ambigua). Preferred fruits are often located high in the trees (up to 50 m) and require great skill in arboreal locomotor behavior. The locomotion of chimpanzees is similarly versatile and linked to the wide ranging needs of a frugivor- ous diet, nesting, arboreal predator avoidance, trekking over long distances, and in some cases discontinuity in the forest habitat. However, like Badrian and Badrian (’77), MacKinnon (’781, Shouteden (’311, and Yerkes and Learned (’251, we infer that bonobos engage in more arboreal leaping, diving, armswinging, and perhaps bipedalism than common chimpanzees do. Adult common chimpanzees seem to engage more in cautious and deliberate climbing and suspensory behaviors. This inference is supported by other indirect evidence, including the restricted rain forest habitat of bonobos, their lighter, more gracile build, their large hallux, and their long narrow scapula.

Dry season is determined from a number ofsources in addition to the climatic conditions of the ’79 study. These included observations of Badrian and Badrian during a n earlier study (‘74’751, published rainfall records from Yangambi (Bultot and Grifiiths, ’721, and information supplied by our guides.

ACKNOWLEDGMENTS

The help and cooperation of many people in Zaire, Belgium, and the United States made this work possible. We thank Professors Tolela Luhata and Oteke Fefe Bochoa of the Institut de Recherche Scientifique, Kinshasa; Dr. Kakiese Onfine of the Institut Zairois pour la Conservation de la Nature; and Citoyen Mbonyikebe Sebahire, Attache de recherches a YInstitut de la Recherche Scientifique. Many people helped us on our journey to the study site. We thank Bruce McCrae, Jeff Buttram, and Christopher Lepp of the Church of the Dis- ciples of Christ, Mbandaka; Chuck Lange, Leann Dorsey, Karen Sullivan, and Mike De Vivo of the Peace Corps, Boende; Mr. Phillipe Van De Werve and Citoyen Dzondo Bolanga of Plantation Bokoli, Culture-Zairoise; and Mr. Paul Clausse of Plantation Bolongo. We also thank the Fathers of Mission Baliko, Boende, for their hospitality.

The L. S. B. Leakey Foundation provided initial funding for this project, and additional funds were granted by the Chicago Zoological Society, Brookfield, Illinois; The University Awards Committee. S.U.N.Y.; a Biomedical Research Support Grant from Basic Health Sciences, S.U.N.Y. Stony Brookand N.I.H.; and a grant from the Explorers Club of New York. Earlier work was supported by Ms. Andrea Guskin, the Boise Fund and the Poulton Fund. We thank all of these people and organizations for their generous support.

Mr. Roger De Champs of the Musee Royal d LAfrique Centrale, Tervuren, kindly iden- tified food plants and the Geology Department of the Musee generously provided maps of Equateur. N. Creel, J. Fleagle, W.L. Jungers, J.T. Stern, and R. Tuttle read and offered help- ful comments on the manuscript. We also thank the reviewers for their thoughtful comments.

LITERATURE CITED

Badrian, A.J., and N.L. Badrian (1977) Pygmy Chimpan- zees. Oryx, 14:46%472.

Badrian, N.L., A.J. Badrian, R.L. Susman (In prep.) The Feeding Ecology of Pun puniscus in Zaire.

Bultot, F., and J.F. Griffiths (1972) The Equatorial Wet Zone. In: World Survey of Climatology, Vol. 10, Climates of Africa. (J.F. Griffths, ed.), pp. 25%311. Elsevier Pub. Co., Amsterdam.

Coolidge, H.J. (1933) Pan puniscus. Pygmy Chimpanzee from South ofthe Congo River. h e r . J. of Phys. Anthrop., 18:2-53.

Corruccini, R.S., and H.M. McHenry (1979) Morphological affinities of Pun puniscus. Science, 204: 1341-1343.

Cramer, D.L. (1977) Craniofacial Morphology of Pun paniscus. Contributions to Primatology, No. 10. (F.S. Szalay, ed.). S. Karger, Basel.

Fenart, R., and R. Deblock (1973) Pun puniscus and Pun troglodytes Craniometrie. Etude Comparative et On- togenique Selon les Methodes Classiques e t Vestibularies. Tome 1. Ann. Mus. Royale Afr. Centrale, Tervuren, Sci. Zool., No. 204.

Fleagle, J.G. (1976a) Locomotion and Posture ofthe Malayan Siamang and Implications for Hominoid Evolution. Folia Primat., 26:245-269.

Fleagle, J.G. i1976b) Locomotor Behavior and Skeletal An- atomy of Sympatric Malaysian Leaf-Monkeys (Presbytis obscuru and Presbytis malalophos). Yearbook of Phys. Anthrop., Vol. 20:44&453.

Horn, A.D. (1976) A Preliminary Report on the Ecology and Behavior of the Bonobo Chimpanzee (Pun puniscus, Schwm 1929) and a Reconsideration of the Evolution of the Chimpanzee. Ph.D. dissertation (Yale University, New Haven, Ct.).

Jenkins , F.A., Jr. (1972) Chimpanzee Bipedalism: Cineradiographic Analysis and Implications for the Evolution of Gait. Science, 178:877-879.

Johanson, D.C. (1974) An Odontological Study of the Chim- panzee with some Implications for Hominoid Evolution. Ph.D. dissertation, University of Chicago.

Jones, C., and J. Sabater Pi (1971) Comparative Ecology of Gorilla gorilla (Savage and Wyman) and Pan troglodytes (Blumbach) in Rio Muni, West Africa. Bibliotheca Primat. No. 13. S. Karger, Basel.

Jordan, C., and H. Jordan (1977) Versuche zur Symbol- Ereignis-Verknupfung bei einer Zwergschimpansen P u n puniscus, Schwarz, 1929). Primates, 181515529.

Kano, T. (1979) A Pilot Study on the Ecology of the Pygmy Chimpanzee, Pan paniscus. In: The Great Apes, ed. by Hamburg and McCown, pp. 361-364. The Benjamin/ Cummings Publ. Co.

Kortlandt, A. (1972) New Perspectives on Ape and Human Evolution. Stichting Voor Psychobiologie. Amsterdam.

Kortlandt, A. (1975) Ecology and Paleoecology of Ape Locomotion. In: Proc. Symp. Fifth Cong. Int’l. Primate Soc., ed. by S. Kondo, M. Kawai, A. Ehara, and S. Kawa- mura, pp. 361-364. Japan Science Press, Tokoyo.

Kuroda, S. (1979) Grouping of the Pygmy Chimpanzees. Primates, 20(2):161-183.

Lawick-Godall, J. Van (1968) The Behavior of Free-Living Chimpanzees in the Gombe Stream Reserve. Animal Behav. Mono., Vol. 1. Bailliere, Tindall, and Cassell, Lon- don.

MacKimon, J. (1978) The Ape Within Us. Holt, Rinehart and Winston, New York.

Miller, R.A. (1952) The musculature ofPun paniscus. Amer. J. Anat., 91:18%238.

Nishida, T. (1972) Preliminary Information of the Pygmy Chimpanzees (Pun paniscus) of the Congo Basin. Pri- mates, 131415-425.

Nissen,H. (1931)AFieldStudyofthe Chimpanzee. Observa- tion of Chimpanzee Behavior and Environment in West- ern French Guniea. Comp. Psych. Mono., 8:l-122.

Reynolds, V.E., and F. Reynolds (1965) Chimpanzees of the Budongo Forest. In: Primate Behavior, Field Studies of Monkeys and Apes. (I. Devore, ed.), pp. 368-424. Holt, Rinehart, Winston.

Ripley, S. (1979) Environmental Grain, Niche Diversifica- tion, and Positional Behavior in Neogene Primates: An Evolutionary Hypothesis. In: Environment, Behavior, and Morphology: Dynamic Interactions in Primates. (M. Mor- beck, H. F’reuschoft, and N. Gomberg, eds.) pp. 37-74. Gustav Fischer, New York.

Rode, P. (1941) Etude d u n Chimpanzee “Pygmee” Adoles- cent (Pun sutyrus puniscus, Schwarz). Mammalia, 5;5&68.

Savage-Rumbaugh, E., B.J. Wilkerson, and R. Bakeman (1977) Spontaneous gestural communication among con- specifics in the pygmy chimpanzee (Pun paniscus). In: Progress in Ape Research, ed. G.H. Bourne, Academic

Press, London, pp. 97-116. Schultz, A.H. (1969) The skeleton of the Chimpanzee. In:

Chimpanzee, Vol. I., (G.H. Bourne, ed.), pp. 5 1 0 3 . S. Karger, Basel.

Schwarz, E. (1929) Das Vorkommen des Schimpansen auf den linken Kongo-Ufer. Revue. Zool. Bot. Afr., 16:424- 426.

Schwarz, E. (1934) On the Local Races of Chimpanzee. Ann. Mag. Nat. Hist., 13.576583.

Shouteden, H. (1931) Le C h i m p a h de la Rive Gauche du Congo. Bull. Cercle Zool. Congolais, 7tll4-119.

Simons, E.L. (1972) Primate Evolution. MacMillan, New York.

Tratz, E., and H. Heck (1954) Der Afrikanische Anthropoide “Bonobo”, eine neue Menscheuaffengattung. Saugetier. Mitteilungen, 2t97-101. Stuttgart.

Tuttle, R.H. (1975) Parallelism, Brachiation and Hominoid Phylogeny. In: Phylogeny of the Primates. (W.P. Luckett and F.S. Szalay, eds.) , pp. 447-480. Plenum Publ. Co., New York.

Yerkes, R.M., and B.W. Learned (1925) Chimpanzee Intelli- gence and its Vocal Expression. Williams and Wilkins, Baltimore.

Zihlman, A.L. (1979) Pygmy Chimpanzee Morphology and the Interpretation of Early Hominids. S. African J. of Sci., Vol. 75:16&168.

Zihlman, A.L., and Cramer, D. (1978) Skeletal Differences Between Pygmy (Pun puniscus) and common chimpanzees (Pan troglodytes). Folia Primat., 29:8&94.

Zihlman, A,, J.E. Cronin, D.L. Cramer, and V.M. Sarich (1978) Pygmy chimpanzee as a possible prototype for the common ancestor of humans, chimpanzees and Gorillas. Nature, 275r744746.

Locomotor behavior ofPan paniscus in Zaire

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