Communication Mechanisms

and Social Integration in

the Black Spider Monkey,

Ateles fusciceps robustus,

and Related Species

JOHN F. EISENBERG

m

WUi.

SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY • NUMBER 213
SERIAL PUBLICATIONS OF THE SMITHSONIA N INSTITUTION

The emphasis upon publications as a means of diffusing knowledge was expressed

by the first Secretary of the Smithsonian Institution. In his formal plan for the Institution, Joseph Henry articulated a program that included the following statement:

"It is proposed to publish a series of reports, giving an account of the new discoveries

in science, and of the changes made from year to year in all branches of knowledge."

This keynote of basic research has been adhered to over the years in the issuance

of thousands of titles in serial publications under the Smithsonian imprint, commencing with Smithsonian Contributions to Knowledge in 1848 and continuing with

the following active series:

Smithsonian Annals of Flight

Smithsonian Contributions to Anthropology

Smithsonian Contributions to Astrophysics

Smithsonian Contributions to Botany

Smithsonian Contributions to the Earth Sciences

Smithsonian Contributions to Paleobiology

Smithsonian Contributions to Zoology

Smithsonian Studies in History and Technology

In these series, the Institution publishes original articles and monographs dealing

with the research and collections of its several museums and offices and of professional

colleagues at other institutions of learning. These papers report newly acquired facts,

synoptic interpretations of data, or original theory in specialized fields. These publications are distributed by mailing lists to libraries, laboratories, and other interested

institutions and specialists throughout the world. Individual copies may be obtained

from the Smithsonian Institution Press as long as stocks are available.

S. DILLON RIPLEY

Secretary

Smithsonian Institution
SMITHSONIA N CONTRIBUTION S T O ZOOLOG Y • NUMBE R 21S

Communication Mechanisms

and Social Integration in

the Black Spider Monkey,

Ateles fusciceps robustnsy

and Related Species

John F. Eisenberg

SMITHSONIAN INSTITUTION PRESS

City of Washington

1976
ABSTRACT

Eisenberg, John F. Communication Mechanisms and Social Integration in the

Black Spider Monkey, Ateles fusciceps robustus, and Related Species. Smithsonian Contributions to Zoology, number 213, 108 pages, 63 figures, 40 tables,

1976.—The study describes the mechanisms of communication employed by the

individuals of a captive colony of Ateles fusciceps robustus studied by the author

for some ten years. The signal system is compared and contrasted with that of a

free-ranging group of A. geoffroyi panamensis. The signal systems are discussed

within the functional contexts in which they occur. Sexual, grooming, and grappling behaviors are given special quantitative treatment. Auditory signals are

considered from the standpoint of syntactic description. A rigorous analysis of

the vocalizations is presented together with* a contextual description leading to

a functional classification. The motivational basis for vocalizations is then

explored. The development of vocalizations in the young Ateles is described

together with the effects of auditory isolation on vocal development. The vocal

repertoire of Ateles is compared with that of Lagothrix, the woolly monkey, and

Alouatta, the howler monkey. Preliminary ethograms for Alouatta and Lagothrix

are presented in the appendices. It is concluded that the vocal repertoire of

Ateles can develop without imitative learning and that the signal system of

Ateles shares homologous elements with that of Alouatta and Lagothrix. The

degree of similarity is highest between Ateles and the woolly monkey.

OFFICIAL PUBLICATION DATE is handstamped in a limited number of initial copies and is recorded

in the Institution's annual report, Smithsonian Year. SI PRESS NUMBER 6067. SERIES COVER DESICN:

The coral Monlaslrca cavernosa (Linnaeus).

Library of Congress Cataloging in Publication Data

Eisenberg, John Frederick

Communication mechanisms and social integration in the black spider monkey, Ateles fusciceps

robustus, and related species.

(Smithsonian contributions to zoology ; no. 213)

Supt. of Docs.: SI 157:213

1. Black spider monkey—Behavior. 2. Central American spider monkey—Behavior. 3. Monkeys—Behavior. 4. Animal sounds. 5. Social behavior in animals. I. Title: Communication

mechanisms and social integration in the black spider monkey .. . II. Series: Smithsonian

Institution. Smithsonian contributions to zoology ; no 213

QL1.S54 no. 213 [QL737.P925] 59l'.08s [59y.82] 75-619208
Contents

Page

Acknowledgments v i

Introduction I

Captive Research 1

Field Research 2

Natural History of Ateles 3

Some Motor Patterns and Their Functional Contexts 4

Maintenance Behavior 4

Patterns of Interaction 4

Reproductive Biology 4

Sexual Behavior of Ateles 6

Agonistic Behavior 9

Allogrooming 10

Grappling 12

Embracing and Hugging 13

Genital Display and Genital Sniffing (Male-Male) 14

Some Complex Interactions 14

Looking into Mouths 14

Rough Grooming and Normal Allogrooming 14

Riding 14

Tail Wrapping 14

Role Summary 15

Signal Systems in Ateles 17

Problem of Communication Analysis 17

Olfactory Communication 18

Visual Communication 20

Male Agonistic Display 20

Facial Expressions 20

Vocalizations of Ateles fusciceps and A. geoffroyi 23

Syntactic Analysis • 23

Syllabic Key to Some Calls of Ateles fusciceps 24

Syllables of Calls That Are Uniform in Structure 24

Compound Calls 26

Syllabic Transformations and the Genesis of Calls 27

Call Types Named and Denned : 27

Compound Calls and Their Genesis 35

Contextual Analysis of Adult and Juvenile Sounds 36

Considerations of Caste Differences 37

Contexts of Sound Production 38

Frequency of Calling and the Contexts for Free-ranging Ateles 43

Some Calling Frequencies for Captive Ateles fusciceps 44

Mood of the Sender 46

Dynamics 46

Alternation, Insertion, and Ambivalence 48

Function and Influences on the Receiver 49

Structure and Functions of Calls 49

Ontogeny of Behavior in Spider Monkeys 52

Condition at Birth and during First Weeks of Life 53

Later Stages of Development 55

Development of Expressive Movements and Vocalizations 57

Comparisons of Ceboid Communication Systems 59

Introduction 59

Nonauditory Signal Systems 60

iii
i v SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

Postures, Expressions, and Movements 60

Marking Behaviors 60

Penile Displays 60

Grooming 61

Embracing 61

Patterns of Sexual Behavior 61

Comparisons of Vocalizations 62

The Signal Systems and Social Structure of Ateles 65

Dimorphism 65

Parental Investment 66

Foraging Strategy 68

The Male Group and Its Genesis 68

Social Pathologies 69

Signals in Context 69

Appendix I: Physical Measurements and Description of Measurement Techniques for the

Sounds of Ateles fusciceps and Related Species 72

Appendix II: Reproductive Data, Medical Histories, Hand-rearing, and Genealogies 81

Reproductive Data 81

Ateles geoffroyi 81

Ateles fusciceps 81

Medical Histories 84

Nutrition , 84

Lead Poisoning 85

Hand-rearing Procedures for Ateles fusciceps robustus 85

Appendix III: Infant Vocalizations, Their Physical Measurements and Variation 87

Appendix IV: Behavior Patterns for Captive Lagothrix and Alouatta 90

Behavior Patterns in Lagothrix lagotricha 90

Methods and Subjects 90

Patterns of Social Behavior 90

Expressive Movements 90

Vocalizations 91

Contact and Contact-promoting Patterns 91

Agonistic Patterns 95

Sexual Patterns 95

Social Structure in a Captive Group 96

Autogrooming Analysis 96

Display Analysis 96

Marking Analysis 97

Allogrooming Analysis 97

Grappling Analysis 97

Embracing Analysis 97

Different Roles and Relationships within the Captive Group 97

The Maternal-Young Relationship 97

The Paternal-Young Relationship 98

Role of Adult Male 98

Behavior Patterns in Alouatta palliata 98

Methods and Subjects 98

Patterns of Social Behavior 98

Expressive Movements 98

Vocalizations 99

Patterns of Interaction 101

Contact and Contact-promoting Patterns 101

Agonistic and Avoidance Patterns 102

Sexual Patterns 102

Interaction Analysis 102

Nonsexual Interaction Forms 102

Anal-Genital Investigation Analysis 102

Tongue-flick Analysis 102
NUMBER 213

Page

Grappling Analysis 103

Individual Behaviors 103

Displays 103

Olfaction-related Behaviors 103

Summary 104

Literature Cited 105
Acknowledgments

The data described here could not have been established without close cooperation from a variety of people. I am especially indebted to Mr. M. Rowe, senior

keeper, National Zoological Park; Dr. C. W. Gray, veterinarian; Dr. Nan

Muckenhirn; Ms. C. Niemeyer; Mr. M. Roberts, associate curator; and Ms. Lisa

McLanahan, the latter participated ably in the data gathering during the summers of 1972 and 1973 and prepared Appendix IV. Ms. Ann Underhill assisted

with the analysis of vocalizations in young Ateles during 1967. Janet DavisArmstrong was instrumental in hand-rearing two specimens used in the developmental study. Additional data were forthcoming from hand-raised specimens in

the care of Ms. W. Holden, Karl Eisenberg, and Ms. S. Wilson. Data concerning

the history of the Barro Colorado Island spider monkeys were forthcoming

from Mr. R. Dare, Dr. G. G. Montgomery, Dr. M. Moynihan, Dr. M. Hladik,

Dr. N. Smythe, and Ms. Carrie Thorington. Clarification concerning some of

the problems attendant on the motivational analysis came about through an

exchange of ideas with Drs. L. Klein, J. Oppenheimer, E. Gould, D. G. Kleiman,

and E. Morton. The manuscript was prepared by Ms. W. Holden; Ms. B. Howser

prepared Figures 22, 23,'and 29. Ms. C. Dorsey prepared Figure 7. Ms. D. Pyle

assisted in the data reduction. Dr. R. W. Thorington graciously critiqued my

final draft.

During 1970 support for the field work came from Smithsonian Research

Foundation Grant No. 435090. Subsequent work on Barro Colorado Island was

financed in part by the National Zoological Park. The earlier parts of the study

were financed in part from NSF Grant GB 3545.

Finally I should say that the researches on the vocalizations of the Cercopithecidae by Peter Marler and his associates have been of great value in stimulating

my thoughts and approaches (Marler, 1970, 1972, 1973). My all too infrequent

discussions with Steve Green produced an independent convergence in several

approaches to syntactic analysis (Green, 1975). To all of my colleagues and to

Elise, Devra, and Karl, I offer my thanks and gratitude.

VI
Communication Mechanisms

and Social Integration in

the Black Spider Monkey,

Ateles fusciceps robustus,

and Related Species

John F. Eisenberg

Introduction

This report concerns the behavior patterns of

two species of spider monkeys, Ateles fusciceps and

Ateles geoffroyi. The major portion of the material

consists of observations on a captive group of A.

fusciceps robustus maintained for some 14 years at

the National Zoological Park. The history of this

group through 1972 has been reviewed (Eisenberg,

1973). Except for some notes made by C. O. Handley in 1964, field data are lacking for this species.

In order to expand our knowledge of communication in free-ranging Ateles, I conducted observations on an introduced group of A. geoffroyi panamensis on Barro Colorado Island, Canal Zone. The

early history of this group has been described by

Eisenberg and Kuehn (1966) and R. Dare (1974).

The vocalizations, gestures, and maintenance

behavior patterns of these two species are quite

similar and, for this reason, I have chosen to use

the Ateles geoffroyi field data as a means of inferring the functional role in the field for some of the

forms of communication shown by the captive A.

fusciceps group. Appendix I contains a comparison

of the physical characteristics of selected vocalizaJohn F. Eisenberg, National Zoological Park, Smithsonian

Institution, Washington, D.C. 20009.

tions for A. geoffroyi, A. fusciceps, A. belzebuth,

and A. paniscus. Great similarities are indicated.

That the first three species are closely related was

already evident in the taxonomic review by Kellogg and Goldman (1944). Recently Hershkowitz

(1972:353) has suggested that only one specific

name for Ateles is valid, i.e., Ateles paniscus. I do

not wish to take sides in any taxonomic controversy; however, in my opinion the four species

show great behavioral homogeneity, although

minor differences can be discerned. Thus, it seems

fair to utilize the field data from the A. geoffroyi

study to clarify the function of the homologous

vocalizations displayed by A. fusciceps in captivity.

Captive Research

Four Ateles fusciceps robustus were received on

17 May 1961 at the National Zoological Park. This

served as the founder stock for our colony, which

has been maintained until the present time. The

reproductive history of the group was reviewed in

the publication by Eisenberg (1973). To date

(September, 1974), 13 live births have occurred

and of these 4 young were taken for hand rearing

and the study of their behavioral development.

1
SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

The results of these developmental studies are reviewed on pages 52-58 ("Ontogeny of Behavior").

The Ateles fusciceps group was studied intensively in the autumn of 1964 and 1965 and during

the summers of 1966 and 1967. During the winter

of 1967, observations were continued, but detailed

behavioral studies were not initiated again until

the spring and summer of 1972 and 1973. The

composition of the study groups is summarized in

Appendix II.

Most of the quantitative data referred to in this

paper were taken during the summers of 1972 and

1973, and in the fall and winter of 1974-1975. During 1972-1973, the captive group of Ateles fusciceps

consisted of an adult male, 3 adult females, and a

juvenile male born in August of 1970. In 1974 the

main study group included an adult male, 2 adult

females, one juvenile female and 2 infant males.

During the summers, the animals were housed in

an outdoor enclosure measuring 5X3X 3 meters.

The enclosure was equipped with benches and a

series of vertical poles. The bars of the cage permitted overhead brachiation. Food consisted of

bread, carrots, sweet potatoes, kale, apples, oranges,

bananas, and a prepared supplement (Zupreem

Marmoset Diet). Water was obtainable at all times.

Data concerning the behavior patterns of these

captive spider monkeys were recorded by direct

observation and written notes in a semi-coded form

on prepared checksheets. Alternatively, the behavior was described by speaking into a tape recorder

and later transcribed onto prepared data sheets

with the appropriate time intervals inserted.

During 1964 and 1965, adult and juvenile vocalizations were recorded and analyzed. In 1966 and

1967 hand rearing, behavioral ontogeny, and the

development of vocalizations in isolation were described and analyzed. Over 300 hours of observations and recordings were logged in these years.

Observation periods involving transcribed recordings were conducted by a balanced series of 30-

minute sessions in 1973 and 15-minute sessions in

1972. Over 50 hours of quantified observations

were made during these two summers. Total hours

of observation with hand notes or recordings exceeded 100 hours. Observation periods were balanced during various parts of the day to avoid

bias induced by such activities as cage cleaning and

feeding. In the interval 1974-1975, observations

were again divided into 30-minute sessions for a

total of 40 hours of data.

Vocalizations, for the most part, were recorded

on Uher 4000 Report-L tape recorders at 3y4 or

7y2 inches per second. Since most of the energy in

Ateles vocalizations lies below 5000 Hz, the Uher

microphone-tape recorder combination served as

an adequate recording system. Some recordings during the last year of the study were made with a

Nagra IV SJ. Vocalizations were analyzed utilizing

a Kay Electric Company Missilyzer No. 675. Most

of the analyses were carried out with 5000 Hz as

the maximum setting. Within this range, the frequency band width is 20 Hz for narrow band analyses or 200 Hz for wide band analyses. When using

the wide band setting, the frequencey of the

sound so reproduced was estimated at the midpoint or darkest portion of the sonographic display.

Many of the sounds produced by Ateles do not

exhibit a single frequency but, upon sonographic

analysis, display side bands. These may be true

harmonics or may be artifacts inherent in the

functioning of the Kay Missilyzer (Watkins, 1967).

In order to check on the actual energy distributions in the recordings of some Ateles sounds that

showed little discrete harmonic structure, the

sounds were passed through a Tektronix Type 323

oscilloscope. The overall energy distribution in

complex sounds could thus be assessed with respect

to the dominant frequency. Clearly, some of the

Ateles calls are truly harmonic in structure, others

are definitely not—regardless of the sonographic

portrayal. Thus, when referring to sonographs, the

term side bands will be used uniformly, but in

those cases where the sounds are purely harmonic

it will be so indicated in the text (see also Appendix I).

Field Research

Ateles geoffroyi panamensis on Barro Colorado

Island were studied by Eisenberg in 1964, 1965,

1966, 1970, and 1974. Altogether some 14 weeks

were spent in observing these monkeys. A total of

some 105 hours were spent recording behavior.

Appendix II contains a synopsis of the history of

this group. I am indebted to Dr. N. Smythe, Dr. M.

Hladik, Dr. R. Dare, Dr. G. G. Montgomery, and

Dr. A. Richard (1970) for filling in the gaps concerning the history of this group during the long
NUMBER 213 3

intervals when I was not present on the island. The

main thrust of the observations on the group of

A. geoffroyi concerned (1) the identification of the

contexts in which vocalizations were produced,

and (2) an attempt to understand the develop

ment of social relationships among group members

as the colony grew through births to the founding

females from 5 to 15 individuals.

Natural History of Ateles

The genus Ateles ranges in tropical evergreen or

semi-evergreen forests from southern Mexico to

southeastern Brazil (Kellogg and Goldman, 1944).

Field observations on A. geoffroyi in Mexico are

described by Wagner (1956) and Eisenberg and

Kuehn (1966). Ateles geoffroyi in Panama was

studied by Carpenter (1935). Additional data for

an introduced but free-ranging, breeding population of A. geoffroyi on Barro Colorado Island,

Panama, have been collected by Eisenberg and

Kuehn (1966), Richard (1970), Hladik and Hladik (1969), and Dare (1974). Klein (1972) has

completed an extensive field study of A. belzebuth

in Columbia, and Durham (1971, 1975) has reported preliminary results on A. paniscus in Peru.

It is generally agreed that Ateles is primarily

frugivorous and feeds selectively at moderate to

extreme heights in mature forests (Carpenter,

1935; Hladik and Hladik, 1969). Diurnally active,

the bands tend to feed intensely in the early morning only to renew feeding in the afternoon. Carpenter (1935) noted that the troops of A. geoffroyi

panamensis frequently broke up into subgroups

during their feeding cycle. Indeed, such subgroups

did not necessarily reconstitute themselves into the

same social unit in sleeping trees at the end of the

day's activity. Especially noticeable was a tendency

for adult, unisexual subgroup formation and allmale groups were commonly censused. Eisenberg

and Kuehn (1966:35-38) noted the tendency for

independence in male activity in both a field and

a captive population. Klein (1972) made similar

observations on A. belzebuth and concluded that

the all-male subgroups were composed of males

who offered mutual support to one another during

both intratroop conflicts and intertroop encounters.

Based on further observations of the A. geoffroyi

group in Panama, Eisenberg, Muckenhirn, and

Rudran (1972) suggested that such all-male subgroups may be composed of related individuals and

age-graded in the sense that mutual tolerance

among such males has an orderly developmental

succession based on continually renewed contact

over many years.

Wagner (1956) had noted that under some circumstances an Ateles troop could exhibit a unimale structure; that is, only one adult male associated with a female subgroup and their progeny.

Eisenberg and Kuehn (1966:56-57), on the basis

of a brief censusing operation in Chiapas, suggested

that such unimale troops could be shown in areas

of reduced carrying capacity. Freese (1975) noted

similar troop structures during censusing in Costa

Rica. Klein (1972) suggested that such unimale

troops recorded in the literature may well have

been the result of incomplete censusing, especially

since adult males are very independent of the

females in their movements. In Klein's study, the

troops of A. belzebuth each had two or more adult

males periodically in association with the females.

Recently Durham (1975) has offered evidence for

both unimale and multimale troops in A. paniscus

from Peru. The unimale condition is typically

shown in the smaller troops at high elevation

habitats, which presumably have a reduced carrying capacity.

Thus, there is some disagreement concerning the

typical form of the social organization shown by

Ateles. In part, the multimale versus unimale controversy is artificial (Eisenberg, Muckenhirn,

and Rudran, 1972), but only long term studies in

the future will clarify the genesis of the so-called

multimale troop. Further comparisons will be

necessary before the relation between troop size

and carrying capacity can be firmly established.

In spite of the uncertainties, there is agreement

on the following points: (1) The home range of

an Ateles troop is much larger than a comparably

sized troop of howler monkeys (Alouatta) in a

comparable habitat. (2) Compared to Alouatta

and Cebus, the Ateles troop is less cohesive and

subject to fractionation. (3) Males tend to be independent in their movements with respect of the

rest of the troop. (4) Females with dependent

infants and juveniles form the most cohesive subunit in a troop. (5) Adult males may be intolerant
SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

of other males belonging to a distinct but neighboring troop. (6) A subgroup of age-graded males

may act as a cooperative unit during offensive

and defensive behaviors. (For a definition of agegraded, see Eisenberg, Muckenhirn, and Rudran,

1972.)

Some Motor Patterns and Their Functional Contexts

Maintenance Behavior

The maintenance behavior patterns of Ateles

fusciceps in captivity do not appreciably differ

from those described for Ateles geoffroyi by Eisenberg and Kuehn (1966). Several points are worthy

of comment, however, since in the intervening

eight years we have had to modify earlier conclusions.

Locomotion is controversial, since Ateles has

been considered a brachiator by Erikson (1963),

on the one hand, and essentially quadrupedal by

Napier and Napier (1967) at the other extreme.

Recently Tuttle (1975) has described the long

arms of Ateles as adaptation for feeding by hanging

vertically and performing vertical lifts and drops

during terminal branch feeding, as originally described for Hylobates (Grand, 1972). While it is

true that Ateles feeds in a manner reminiscent of

Hylobates, it is also true that Ateles locomotes by

brachiation. The form of brachiation by Ateles

differs from that of Hylobates in that Ateles uses

its tail as an "assist" with each or one arm in a

given two-arm cycle of brachiation (see Grand,

1975, for a complete discussion).

Leaping by Ateles geoffroyi is awesome and

often involves considerable vertical descent, especially when it is part of the male display sequence

(see "Male Agonistic Display," p. 20). Adult females carrying young (see "Infant-2," p. 55) will

attempt leaps across gaps of 2 meters. At the moment of leaping the arms are generally extended

to maximize the reach (Figure 1).

Activity is not strictly confined to daylight. As

noted earlier (Eisenberg and Kuehn, 1966:55),

some social interaction can and does take place

after dark, and Handley (in litt.) comments that

Ateles fusciceps has been noted to move a considerable distance as a troop on a moonlit night.

Concerning feeding patterns, Hladik and Hladik (1969) report that Ateles geoffroyi can consume up to 20 percent of its diet in the form of

young leaves. This is somewhat higher than the

values obtained by Carpenter (1935), but still

considerably less than the 40 percent value computed for Alouatta by the Hladiks. While it is still

reasonable to consider Ateles geoffroyi primarily

a frugivore, no doubt further studies of its foraging

behavior are warranted.

It is worth mentioning that, as in A. geoffroyi,

self-grooming (autogrooming) in A. fusciceps occupies a very small percentage of their time (Eisenberg

and Kuehn, 1966:33). In 72 separate 30-minute

observation periods, autogrooming accounted for.

only 0.64 percent of the total observation time

(Table 1). These data are quite comparable with

the earlier data obtained for A. geoffroyi.

TABLE 1.—Autogrooming frequencies and durations

for individual Ateles fusciceps, 1973

V

B

M

s

T

Subjects 2 /

0

13

0

6

8

0

393

0

234

201

Of

/o

0

47.4

0

28.3

24.3

2f = total frequency of grooming shown; Sd = total

duration (sec) of grooming shown; % = percentage of

summed durations of all autogrooming for all observation

periods.

Total percent of observation time spent in autogrooming

was 0.64%. The average duration of an autogrooming bout

was 30.6 seconds.

Patterns of Interaction

REPRODUCTIVE BIOLOGY

During the course of our preliminary studies

(Eisenberg and Kuehn, 1966), we had difficulty

determining the receptivity of females and had no

knowledge of the unique posture assumed during

copulation. Indeed, we witnessed copulation once

but did not interpret the behavior correctly (Eisenberg and Kuehn, 1966:19-20). The situation was

clarified for us through subsequent observations

from 1970 to 1972. Klein (1971) had correctly in-
NUMBER 213

FIGURE 1.—A leap by an A teles geoffroyi female while carrying her infant dorsally. Note the

extension of the forearms. (Photo by N. Smythe.)

terpreted the significance of the copulatory posture

and he further called attention to the role that

urine may play in coordinating the activities of

adult males and females (Klein, 1971).

Although spider monkeys have been studied off

and on for the last 50 years, the details of their

reproduction have remained obscure. Goodman

and Wislocki (1935) described cyclical uterine

bleeding, which occurred every 26 to 27 days in

adult females. Blood could be obtained through a

vaginal lavage procedure for roughly 3 to 4 days.

From time to time, we have noted what appeared

to be dark secretions present on the sulcus of the

pendulous clitoris but in no case were we ever able

to determine on a regular basis by visual inspection when a female spider monkey was undergoing

menstruation. The experience has been similar for

other workers. The opening of the vagina itself

and the clitoral structure may appear moist and

somewhat tumescent around the time of estrus;

however, precise criteria remain to be developed

for a visual determination of estrus in the female

spider monkey.

Behaviorally, female spider monkeys show an

increased tendency to manipulate, inspect, and lick

the clitoris prior to maximum sexual receptivity.

In addition, females approaching estrus tend to

groom other group members with a greater frequency and will approach the adult male and

present their genitalia or posteriors for his inspection. The male becomes more active in his own

grooming activity when a female in the group is

approaching estrus (Table 2).

In an established group, there are very few

preliminaries which can be noted that indicate that

a couple intends to copulate. We observed that the

pair may move away from the main group to a

point of seclusion and that juvenile animals may

sometimes interfere with the copulation by the

parents, especially the offspring of the copulating

female (see "Sexual Behavior," p. 8).

The male may often sit or recline slightly with
SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

or without an erection and be approached by the

female who will sit in his lap, whereupon he will

assume the copulatory position by clamping his

hind legs firmly over hers. On the other hand, this

locking of the male's legs over the female's, as

described by Klein (1971), may occur outside the

mating context (see "Role Summary," p. 15).

The copulations we have observed with Ateles

fusciceps differ little from those described by Klein

(1971) for A. behebuth. Some thrusting movements are made by the male throughout the course

of intromission, which may last in excess of 35

minutes. The male may mate with a given female

over a 48-hour period; we have noted two such

copulation sequences (see "Patterns," p. 9).

Gestation has been calculated at 226 and 232

days. This does not differ from the figure (ly2

months) quoted for Lagothrix by Williams (1967).

In the captive group of Ateles fusciceps, the interval between births is a function of the duration

of lactation. If the young were taken at birth or

were stillborn, the interval ranged from 8 months to

11 months 28 days (N = 5). If lactation occurred,

the interbirth interval was in part a function of

the duration of lactation. Intervals ranged from 15

months 13 days to 29 months 28 days (N = 8)

(Eisenberg, 1973).

Our observations on the Ateles fusciceps colony

suggest that youngsters may actively suckle from

their mothers until at least 16 months of age,

although they have begaun to eat solid food some

8 months earlier. It would appear that the period

of dependency on the part of the newborn is prolonged when compared with that of the macaque

and baboon. Furthermore, the data suggest that

mothers should produce a youngster every 22 to 36

months. Data concerning the long period of infant

dependency are confirmed by field observations on

Ateles geoffroyi panamensis on Barro Colorado

Island. From 1966 to 1974, 14 births were recorded

from 4 adult reproducing females (Appendix II).

Klein (1971) also remarks upon the prolonged

period of infant and juvenile dependency in his

field study of Ateles behebuth in Colombia.

Klein (1971) suggests that Ateles geoffroyi in

the captive colony at San Francisco and Ateles belzebuth in Colombia exhibit no birth season. I am

inclined to agree that Ateles can mate throughout

most of the year, but the 19 births occurring at the

National Zoological Park during the last 11 years

show a tendency toward two peaks, since 11 of the

19 full term births occurred in April, May, or

June, and 5 births occurred during November,

December-January. If the gestation is 7i/2 months,

then we have the suggestion of an optimal breeding

period for this captive group of A. fusciceps during

the months of July, August, and September, and

March and April. Perhaps mating in Washington,

D. C, is in part regulated by a shift in the amount

of light, since optimal breeding periods seem to

occur around the periods following the spring and

autumnal equinoxes. It is impossible at the present

time to determine whether birth peaks are a result

of male spermatogenic activity or female cycling.

It is noteworthy, however, that estrus synchrony is

suggested in our captive group of Ateles fusciceps,

since 4 out of 19 births were within 5 days of each

other and 8 births were less than or equal to 28

days apart (Appendix II).

SEXUAL BEHAVIOR OF Ateles

In an earlier publication (Eisenberg and Kuehn,

1966), an attempt was made to discuss some aspects

of the sexual behavior of Ateles behebuth, even

though complete sexual behavior had not been

observed. Eisenberg and Kuehn reproduced a protocol from 17 March 1964, which was based on an

encounter between an adult male and an adult

female. That particular set of observations was

made during the course of an encounter series

where adults were kept separated and allowed to

come together in a large exercise cage. Because of

the method of holding the animals in separate

cages unless they were being studied in the

encounter situation, certain aspects of contactpromoting behavior were exaggerated. Furthermore, grappling bouts occurred in an encounter

situation at an exaggerated frequency than when

compared with the field data (see "Grappling,"

p. 12). In such an encounter situation, grappling

should resolve itself in the re-establishment of a

dominance relationship between the pair but, as

I have noted previously, grappling can terminate

either with mixed elements of sexual behavior or

terminate in aggressive arousal. This is especially

true if the grappling bout involves individuals that

have an imperfectly established dominance relationship. I agree with Klein (1971), however, that

the sounds often associated with grappling, "ook-
NUMBER 213

ook," and the appeasement sounds or slightly

frightened sounds of "squeaking" need not necessarily be associated with sexual receptivity or

sexual motivation.

An encounter previously reported (Eisenberg

and Kuehn, 1966:19) involved the assumption of

the copulatory posture on two occasions. The first

bout of interaction following upon grappling

involved the male sitting on the swing with which

the cage was provided. This swing had a baseboard

approximately 8 inches wide and 3 feet long,

which provided a rather secure resting place. As

the male sat upright looking at the female, she

approached him brachiating and hung above him;

then she sat in his lap for about I14 minutes.

During this time there was some movement on the

part of the male and she turned to embrace him

face to face while remaining seated in his lap.

Prior to sitting in his lap, she made low squeak

vocalizations and he intermittently uttered low

ook-ook sounds with a long interval between each

emission. The vocalizations probably do not have

anything to do with sexual receptivity but reflected

a general ambivalence on the part of both animals.

Upon rising from the male's lap, it was noted that

the female's vaginal opening was somewhat dilated

and moist, but no trace of an erection could be

seen for the male. In retrospect now, we realize

that the couple had assumed the copulatory posture, although our old notes do not permit us to

say whether or not intromission took place.

After an interval of approximately 15 minutes,

the animals began to interact heavily again. At

this time it was noted that the male had an erection. He approached the female facing her while

hanging up; the female was braced upright in a

corner of the cage. He made a pelvic movement

and then moved away. This we termed a "thrusting

movement." He then sat and the female approached

following him and sat in his lap. This again was the

second assumption of the copulatory posture. She

moved away after about 2 minutes followed by the

male. They then hung up by the arms facing one

another and showed alternate bouts of moving

away by the male with following by the female;

eventually the male remained hanging and manipulated his genitalia with his hind foot. The female

was hanging opposite him, facing him, and once

again he made a thrusting movement toward her.

She moved away and he remained hanging where

he was.

Upon approaching him again, the female manipulated his genitals whereupon the male moved

away followed by the female. Upon facing one

another again, the male exhibited another thrusting movement and then moved to the swing and

sat. The female followed, hanging over him, whereupon the male manipulated her clitoris; then he

assumed a suspended position hanging behind her

and, reaching out with his hind legs, he grasped

at one of her hind legs and made a thrusting movement. This we termed "mounting," but we now

realize that this was an attempt on the part of the

male to lock his hind legs over her thighs and pull

her into a copulatory position. "Mounting" in the

fashion of macaques is not part of the normal

mating sequence in Ateles (see "Patterns," p. 61).

Hence, Eisenberg and Kuehn (1966:19) stated

that intromission was not actually seen; rather it

should have been stated that intromission was

uncertain and that the "copulatory position" was

assumed.

I agree with Klein (1971) that the attainment of

an erection by the male prior to copulation and

hanging up while making pelvic thrusts at the

female is not necessarily a standard part of the precopulatory repertoire. The fifth element of sexual

behavior that Eisenberg and Kuehn (1966) mentioned, sitting in the lap, is definitely part of the

sexual pattern since this is in fact an element of the

copulatory position. What was termed "mounting" now turns out to be a movement preparatory to intromission shown in a slightly novel context (see also "Complex Interactions," p. 14).

A certain amount of variation is shown in the

mating behavior of spider monkeys. Here follow

three abbreviated protocols of copulation for

Ateles fusciceps in our captive colony.

Copulation 1, 1330 hours, 6 July 1972 (observer, L. MeLanahan): Female approaches male who is sitting alone. She

places an arm around his neck and he leans forward to sniff

at her pectoral region. He then bends down and sniffs at her

genital area. As he does so, the female assumes a quadrupedal

stance with her genital area facing the male. The male continues to sniff and lick at her clitoris, being somewhat impeded by interruptions from subadult female B and the

juvenile male who is the offspring of the interacting pair.

Approximately 2y2 minutes later, the female again approached the male and presented her anogenital area to him.

The male immediately began to sniff and rub her pectoral
8

area with his hands and manipulated her clitoris and hind

legs. The female was now directly in front of the male and,

turning to face him, would stroke his head and arms only to

turn around again and allow him to continue manipulating

her clitoris and rub her pectoral region.

Thus, aside from turning around, for most of the initial

interaction, the female was standing quadrupedally with her

back to the male who was standing over her.

Then the male grasped the female with his forearms

around her chest and, while sitting, pulled her down on him

into the copulatory position. While pulling her down, he

made an upward thrust. As he did so, the female stretched

her body forward as the male hooked his hind legs over her

thighs. The thrusting movements by the male subsided and

he made a growling noise toward the juvenile male who attempted to insert himself between his father and mother. The

next time the juvenile attempted this interruption, the male

pushed him and he went to the other side of the cage squeaking and twittering.

The subadult female B would approach the copulating

pair and occasionally allogroom the male. To this, the male

did not particularly object. Throughout the copulation, the

adult female would turn to stroke the male's head and neck.

At 4 or 5 minute intervals, the male would resume active

thrusting. The subadult female groomed the male less

throughout and, at one time, grasped the copulating female

and embraced her. Eventually the subadult female withdrew

and curled up sitting to one side. Duration of copulation was

slightly less than 25 minutes. At the end of the period of

intromission, the male made three or four violent thrusts in

which he raised his posterior from the ground.

This copulation occurred in a group context.

Some interference occurred when the juvenile male

and subadult female attempted to become involved.

The subadult female was in estrus at the same time

and the male copulated with her on the following

day.

Copulation 2, 7 July 1972, 0950 (in this instance intromission was already in progress at the time the observer took

notes) (observer, L. McLanahan): The male's legs were

hooked over the female's thighs in the typical copulatory

position. During this copulation the male was mating with

the so-called subadult female B. The female with whom he

had copulated previously was now sitting next to the male

occasionally embracing his torso with her arms. He would

respond to this by putting one arm on the old female's

shoulder and extending his head toward her. [The significance of these interactions will be discussed under "Embracing and Hugging," p. 13]. The amount of interference was

considerable from both the adult female and the juvenile.

Once again, at the termination of the intromission, the male

thrusted 5 or 6 times and then appeared to withdraw his

penis from the vagina of the female.

Couplation 3 (observer, J. F. Eisenberg): The male left the

main group of animals at about 1335 and moved to a seSMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

eluded spot in the cage, namely the doorway giving access

from the outer cage to the inside cage. The female approached him extending her hand, touched him on the head,

entered the doorway, and turning and standing above him

presented her genitals to his face, and then sat in his lap.

The male immediately assumed the copulatory posture and

they remained intromitted for 3 minutes 40 seconds. Thrusting movements were difficult to discern. During the time of

intromission, the female turned around and looked at the

male several times and touched him on the shoulder. Intromission terminated when the female began to rise and then

turned and began grooming the male's neck and face. The

female continued to groom the male on the chest and sniffed

his genitalia. Since patrons began to initiate feeding, the

female came to the front of the cage and the male followed

after momentary inspection of his genitalia.

Eisenberg and Kuehn (1966:19) listed six aspects of primary sexual behavior. These included:

(1) initial contact including embrace, followed by

(2) genital manipulation, erection and pelvic

thrusts by the male, sitting in the lap by the female,

and (3) mounting by the male. Since it was incorrectly assumed that mounting by the male was

in a conventional macaque pattern, sitting in the

lap was not assumed to be a copulatory posture.

Extension of the male's legs to grasp the female's

hindlegs and lock his legs firmly over her thighs

was interpreted as an attempted mount.

Following "contact" by the animals, I would

now list as the primary elements of sexual behavior: (1) presentation of the genitals on the part of

the female, followed by (2) sitting in the lap.

Erection for some time prior to intromission on

the part of the male, thrusting at the female as she

approaches with an erect penis, and genital manipulation are not invariant components leading up

to the copulatory position. In this, I concur with

Klein (1971).

It is noteworthy that in all the copulations I

have observed, the female plays an active role in

approaching the male, touching, and eventually

sitting in his lap. The male also may be active in

initiating the copulatory position by extending

toward her with his hindlegs and attempting to

lock them around her torso (p. 7). We agree that

copulation can take place in a group situation, but

it would appear that the pair attempts to seek out

seclusion since some interference from juveniles

and subadults can occur in a confined captive situation. In the field, pairing off separately may occur

more often than is suspected.

I no longer feel that grappling (play fighting) is
NUMBER 213

tied to primary sexual behavior, rather it is recognized that grappling is an interactional system

whereby animals reinforce dominance status in

ambivalent situations and is a play syndrome in

juveniles. Induction of abnormal amounts of grappling as a result of Eisenberg and Kuehn's (1966)

original encounter techniques, as suggested by

Klein (1971), would appear to be the case. Excessive grappling between the male and the females

of the Ateles geoffroyi panamensis group on Barro

Colorado Island in the summers of 1964 and 1965

was undoubtedly associated with an imperfect

dominance situation existing between the male and

at least one of the four females. Nevertheless,

during the latter period of field observations in

Panama (Eisenberg and Kuehn, 1966:48), copulation did indeed take place, since the first infant

was born in early January of 1966. Klein (1971)

himself described a grappling bout that occurred

in two free-ranging Ateles belzebuth prior to

mating, but the grappling bout occurred some 7

hours prior to the first observed copulation.

Klein (1971) has implied that Eisenberg and

Kuehn (1966) considered ook-ook, squeaking, and

grappling as primary elements of sexual behavior.

At no time in that paper were the ook-ook and

squeak vocalizations referred to as being motivated

primarily by sexual tendencies; rather, it was noted

(Eisenberg and Kuehn, 1966:19) that, although

the squeak may be given during the initial phases

of primary sexual behavior, it would appear that

the sound is given during a contact-seeking situation after the animal has been repulsed. In other

words, the squeaking animal produces the sound

as an appeasement signal and it is given with some

overtones of fear. The ook-ook vocalization,

although associated with grappling, is produced

with many subvariants and may grade into aggressive growling or be produced in a low intensity

variant, which may accompany certain aspects of

sexual behavior. At no time was it inferred that

ook-ook and squeak vocalizations were entirely

sexually motivated or occurred entirely in a sexual

context. In the same vein, it was not asserted that

grappling was entirely motivated by sexual behavior, but rather only noted that it may sometimes

have sexual "overtones" and occur prior to the

expression of sexual behavior.

In the 1966 description of grappling, Eisenberg

and Kuehn indicated that it involved elements of

embracing, pushing, pulling toward, mock biting,

and slapping. Further, it was indicated that it may

grade into agonistic behaviors, including a chase,

and that sometimes it may occur prior to a sexual

interaction. I do concur with Klein (1971) completely, however, that the encounter situation that

was employed distorts the frequency of many of

the behavior patterns in adult Ateles, and I certainly agree that sexual behavior may take place

during the day and need not be confined to the

evening.

Eisenberg and Kuehn (1966:18) erroneously

assumed that copulation may often occur in the

evening, since at this time much grappling occurred in the Ateles geoffroyi group on Barro Colorado Island. I now feel that this grappling was

induced by the unstable dominance situation, the

age of the animals, and the fact that interaction

intensified in the early evening when the animals

assembled at the sleeping trees. Copulations that

were observed in captive A. fusciceps had occurred

at 0830, 0950, 1330, 1335, and 1400.

AGONISTIC BEHAVIOR

Agonistic behavior in the captive colony of

Ateles fusciceps was extremely rare. The adult

male very often could cause two fighting animals

to separate merely by approaching them rapidly;

often progressing quadrupedally while showing

pilo erection. Upon coming close to the fighting

animals, the adult male would often show a partially opened mouth with the corners retracted thus

exposing his teeth. This was not invariant, however, since a rapid approach by the male often

sufficed to separate the combatants. Behavior on

the part of the adult male directed toward an

observer or keeper often assumed a threatening

aspect. Frequently he would brachiate rapidly

around the cage, flinging himself suddenly at the

bars while staring directly at the object of his

hostility. If the observer stared back at the male,

he would frequently turn away, or, if the male

attempted to maintain his gaze, he would retract

the corners of his mouth while raising his lips

slightly thus exposing his teeth. Very often shaking

the bars could accompany this display (see "Male

Agonistic Display," p. 20).

When they occur, aggressive interactions in the

group are generally very swift. A rapid approach
10

SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

TABLE 2.—Allogrooming bouts recorded for Ateles fusciceps through estrus, 1972

Subjects 27Jun 28Jun 29 Jun 30 Jun 1 Jul 2 Jul 5 Jul 6 Jul 7 Jul* 8 Jul 9 Jul 10 Jul 11 Jul 12 Jul

M -» B

B -»V

B -»M

V -»M

V ->B

Total 11

• Dates of copulation for females B and V. Data based on two 30-minute samples per day (see text).

may resolve itself into a chase with the approached

animal fleeing. Sudden aggression may be displayed

when an animal slaps another. Rarely does biting

occur, but when it does, it is often swift with the

bitten animal fleeing immediately, screaming, and

remaining as far away from the attacking animal

as possible. The attacked animal often shows extreme avoidance for some time after and may withdraw sitting crouched with his head buried between his knees. An animal so attacked may begin

to utter twitter calls and screeches until it is approached by another group member, embraced,

and held. Such behaviors of withdrawal and protest

sounds were frequently shown by the juvenile

male J upon being punished by his mother. Frequently it was the adult male that approached and

embraced.

Recently the agonistic patterns of Ateles have

been reviewed in depth by Klein (1974). Klein

draws on both captive studies of A. geoffroyi and

his field study of A. belzebuth. Klein emphasizes

that in strong aggression there is relatively little

active submission and generally an attack ends

with one animal fleeing. Yet, if I define agonistic

behavior broadly to include the numerous intragroup "spats" observed between mothers and

young and between siblings, then the distress calls

and solicitation of contact by an attached animal

certainly qualify as an alternative to active submission. Sitting alone while hunching and lowering the head is to my mind a form of active submission, although this occurs after an intragroup

altercation. Interspecific aggression and intertroop

agonistic displays are carefully summarized by

Klein.

ALLOCROOMING

Grooming relationships among 16 members of

an Ateles geoffroyi colony were analyzed by.Eisenberg and Kuehn in the 1966 publication. Grooming interactions among the colony members were

summarized for the entire observation period and

discrete relationships were not analyzed for restricted periods of time. In the small colony of

Ateles fusciceps, it was possible during 1972, 1973,

and 1974 to analyze grooming relationships in

much greater detail, with special reference to the

exact relationship of the members of the group to

one another. This has allowed me to extend our

discussion beyond that of the conclusions drawn

in 1966. In the 1966 study, Eisenberg and Kuehn

concluded that the adult male received very little

grooming, but dispensed grooming to a great many

lower ranking individuals. The most grooming

activity appeared to be shown by sexually mature

females with dependent young. Indeed, these

TABLE 3.—Allogrooming frequencies and durations

in Ateles fusciceps, 1973

Initiator

M

M

M

V

V

V

B

B

B

J

J

S

Recipient

V

J

B

B

M

J

V

J

M

V

B

B

2/

1

7

2

2

3

14

33

3

4

1

1

1

4

135.5

222

79

70

527

4319

159

63

7

11

66

%

0.1

2.4

3.9

1.4

1.2

9.3

76.3

2.8

1.1

0.1

0.2

1.2

2f = total frequency of grooming shown; 2d = total

duration of grooming shown (sec); % = percentage of total

duration of all allogrooming for all observation periods.

Total percent of observation time spent in allogrooming

was 4.4%. The average duration of an allogrooming bout

was 78.6 seconds.
NUMBER 213 11

FIGURE 2.—Allogrooming between two adult female Ateles geoffroyi. Female spider monkeys can

form persistent grooming relationships that may involve mother-daughter dyads in captivity.

(Photo by C. M. Hladik.)

"mothers" tended to give more grooming than they

actually received (Figure 2).

In the small Ateles fusciceps group, once again

the male appeared to receive little grooming and

donated quite a bit of grooming to animals subordinate to him, including females S and B and

young male J (Figure 3). Interestingly enough, the

grooming relationships of J to other members of

the colony changed significantly from 1972 to 1973

as he became more mature. In 1972 he received

little attention from the male, but received a dramatic increase in attention in 1973 (Table 3).

One pecularity of the Ateles fusciceps data concerns the tendency of female B to groom her

mother, V. This tendency for B to show grooming

toward her mother was consistent in both 1972 and

1973. The subordinate female S showed very poorly

developed grooming relationships to all members

of the colony, although she groomed male J in

1972. Female S had been hand raised and reintroduced to the group as a juvenile (Appendix II).

Female V showed a pronounced grooming tendency with respect to her offspring J in 1972 and,

although this trend persisted in 1973, its duration

decreased (Table 4). One aspect of allogrooming,

which was not evident when all data were summarized in the Ateles geoffroyi group, concerned

the shift in grooming through a female's estrous

cycle. An estrous female tends to groom more during her period of receptivity than at other times.

The male's tendency to groom a given female shifts

one week prior to her period of receptivity, showing an increase (Table 2). Finally, the amount of

grooming shown by the Ateles fusciceps colony

amounted to less than 5 percent of total observation time, which is comparable to that of the Ateles

geoffroyi colony described by Eisenberg and Kuehn

(1966).
12 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

TABLE 4.—Allogrooming shifts as the

juvenile male matures

Initiator

M

M

M

V

V

V

V

B

B

B

B

S

s

s

s

J

J

J

J

Totals

Recipient

V

B

J

B

M

S

J

V

J

M

S

J

V

M

B

V

S

M

B

/

2

16

-

3

7

1

22

42

5

6

-

5

3

2

2

3

1

3

4

127

1972

%

1.6

12.6»

0**

2.3

5.5

0.7

173

33.0

3.9

4.7

0

3.9

2.3

1.6

1.6

2.3

0.7

2.3

3.1

1973

f

1

2

7

2

3

-

14

33

3

4

-

_

-

-

1

1

1

-

-

72

%

1.3

2.7

9.7

2.7

4.1

0

19.4

45.8

4.1

5.6

0

0

0

0

1.3

1.3

1.3

0

0

• Includes estrus grooming shifts.

• • Italic figures are discussed in text.

1972 1973

FIGURE 3.—Sociogram indicating allogrooming shifts as young

male J matures (1972-1973). Animals are ranked (top to

bottom) in order of decreasing age. (d=donor; r=recipient,

see Table 3 for numerical values; M=adult male; V=adult

female; B=daughter of V; J=son of V; S=subordinate adult

female—note the tendency for S to be excluded from grooming dyads.)

GRAPPLING

This behavior pattern (Eisenberg and Kuehn,

1966; see also "Sexual Behavior," p. 6) is most

frequently shown by juvenile and subadult animals, although adults may participate with them

in the exhibition of this behavior (Figure 4).

An invitation to grapple often involves approaching a partner and either standing near or

hanging above him. The initiator then extends a

hand, often shaking its head slightly, while uttering

the low ook-ook vocalization. The interaction then

takes the form of a wrestling match including mock

biting and occasional genital manipulation.

During intensive observation of the A teles fusciceps group in 1972 and 1973, the juvenile male

initiated almost all of the grappling. Most of it was

directed toward subordinate females or to the

adult male and, altogether, it accounted for 4.5

percent of the total observation time (36 hours)

(Table 5).

Grappling in the maturing juvenile appears to

serve as a form of mock fighting. No doubt the relative strengths of the interactants can be tested without any serious harm coming to either of the

participants. In previous studies (Eisenberg and

Kuehn, 1966), grappling could be induced in

, i

j 1

\ •

FIGURE 4.—Grappling bout between a male and a female

Ateles. Kicking, pushing, and grasping are employed in a

complex pattern of "mock fighting."
NUMBER 213 13

Initiator

J

J

J

J

M

M

BV

TABLE 5

Recipient

V

B

S

M

J

S

J

MUTUAL:

S&B&J

S & B

J&S

J&B

J&M

JfeV

.—Grappling

2 /

16

19

26

9

1

1

1

2

1

3

2

2

1

574

1827

1097

1108

12

1.5

20

17

66

397

501

74

222

%

9.7

31

18.6

18.7

0.2

0

0.3

0.3

1.2

15

8.5

1.2

3.8

2f = total frequency of grappling shown; Zd = total

duration of grappling shown (sec); % = percentage of total

duration of all grappling for all observation periods.

Grappling involved 4.57% of total observation; the average

duration for a grappling bout was 6.96 seconds. J (juvenile

male) initiated almost all grappling and the greatest percentage of it involved female B.

adults that were kept apart and allowed to encounter in a neutral arena. While such activities

are not shown with such frequency and intensity

in normal adult encounters in the wild, it no doubt

serves the same purpose; namely, achieving contact

and testing the relative strengths of the participants. The exact motivation of grappling is difficult to evaluate. At times it seems to have aggressive overtones, while at other times it seems to have

some sexual significance. It should not, however,

be thought of as a necessary prelude to sexual behavior (see "Sexual Behavior," p. 6).

EMBRACING AND HUGGING

Embracing, leading to hugging or clasping one

another, is a form of contact behavior shown frequently in the captive group (Table 6). A juvenile

initiating an embrace with its mother accounts for

an extremely high percentage of all embracing

activities. Juvenile males frequently embrace adult

males as part of their development of a social bond

with the adult male (see "Male Group," p. 68).

The form of the embrace very often depends

upon previous actions. An animal that is insecure

or frightened may approach an older dominant

while exhibiting pursed lips and perhaps trilling.

An embrace will follow, whereupon the initiator

buries its face in the neck or breast region of the

adult. This brings the nose of the initiator in contact with the region of the pectoral gland or the

axilla. Brief embracing following genital sniffing or

accompanied by sniffing the pectoral regions is

analyzed in Table 7. An exchange of olfactory information is strongly implied (see "Olfactory Communication," p. 18).

When an adult male initiates an embrace with

a juvenile male, he may often continue on in the

TABLE 6.—Embracing leading to hugging in

Ateles fusciceps

Initiator

M

J

J

J

J

V

V

s

s

s

s

Recipient

J

B

M

S

V

M

B

B

M

V

J

2 /

1

8

10

10

13

1

1

1

1

2

1

Sd

20

1656

1276

634

3059

353

17

65

550

659

8

%

05

19.9

15.4

7.6

37

4.3

02

0.7

6.6

7.9

0.1

2f = total frequency of embracing shown; 2d = total

duration of embracing and hugging shown; % = percentage

of total duration of all embracing for all observation periods.

Embracing accounts for 6.4% of total observation time; the

average duration of a hugging bout is 169.3 seconds. J to V

(J's mother) embracing accounts for the highest percentage

of all embracing. No quantitative rises or decreases were

noted throughout the study period. J to M (J's father) embracing accounts for the third highest percentage.

TABLE 7.—Sniff-embrace frequency analysis

Subject

V

B . ...

S

T

M

V

B

S

T

M

Mutual sniff

Individual sniff

I

PECTORAL

10 5

4 9

6 7

17 8

23 11

GENITALIA

0

0

0

9

9

R

SNIFF-EMBRACE

3

5

3

8

21

SNIFF-EMBRACE

Total

15

13

13

25

34

0

0(0(0 0
14

SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

direction of his progression and step over the young

animal. At the point of stepping over, a genital

display may occur.

GENITAL DISPLAY AND GENITAL SNIFFING

(MALE-MALE)

Aside from attentions paid to the external genitalia between a male and female during sexual

behavior (see "Sexual Behavior," p. 6), a form

of genital display seems to occur between an adult

male and a juvenile or subadult male. The adult

male will approach the juvenile, who may be sitting on a perch. As he approaches quadrupedally,

the adult may emit the slow, gutteral whinny

while cocking his head to one side. He may then

pause and either touch the younger male or embrace him, and then step over him. While stepping

over he may pause again and raise one of his hindlegs so that adult male's genitalia are presented

directly to the face of the younger male, whereupon the young male sniffs. The adult then proceeds in the original direction. A variation on the

preceding consists of a mutual quadrupedal

approach, often times with both animals pursing

their lips and emitting low, gutteral whinnies. This

may be followed by a mutual embrace and sniffing

of the pectoral region, then the adult male may

step over the younger male and again permit an

opportunity for the genital sniff.

Genital sniffing can also occur in a slightly different context. For example, the adult male may

hang up from an overhead support, clinging with

both hindlegs and arms to form a hammock in

front of the juvenile male. The juvenile male then

may groom the adult, followed by sniffing the adult

male's genitals. Very often after sniffing, a grappling bout can occur.

SOME COMPLEX INTERACTIONS

Looking into Mouths

A juvenile may, during a feeding bout, approach

a subordinate adult and by retracting its lips attempt to see into its mouth and extract food. This

same behavior may be shown by an adult female

to one of her full-grown offspring. Looking into a

partner's mouth has also been observed in a nonfeeding context, but its exact significance cannot

be ascertained.

Rough Grooming and Normal Allogrooming

It has been frequently observed that an adult

may approach a subordinate or juvenile individual

and force it down with its hands, while grooming

its fur in an agitated fashion. This category is

now recognized as "rough grooming" and should

be separated from normal allogrooming, which is

of a more deliberate nature and often solicited by

the recipient. Such rough grooming, when tabulated with otherwise relaxed grooming, may give

rise to a correlation of grooming frequency with

dominance status (Eisenberg and Kuehn, 1966:

38-41). It is now thought desirable in future allogrooming analyses to distinguish carefully between

these two categories for, when this separation is

done, it is apparent that the grooming relationships do not always reflect a strictly hierarchical

pattern (see "Agonistic Behavior," p. 9).

Riding

As is well known from previous descriptions,

the infant A teles rides on the ventrum of the

mother for approximately the first 4 to 5 months

of life, thereupon transferring to her dorsum and

continuing to be carried with decreasing frequency

until almost li/£ years of age (Carpenter, 1935;

Eisenberg and Kuehn, 1966). What was not noted

before, however, is the tendency for adult males to

permit juvenile males to ride on their backs during

the transition phase from mother transport to independent locomotion. Although this is not a frequently exhibited behavior pattern in captivity,

our adult male A. fusciceps frequently allowed

juvenile males, less than 2 years of age, to ride on

his back for brief periods. These "rides" were often

accompanied by grappling interaction and an increased attention on the part of the male toward

his juvenile sons.

Tail Wrapping

As mentioned earlier (Eisenberg and Kuehn,

1966:4), an agitated Ateles, while pacing in the

cage, may wrap its tail around its own body. The
NUMBER 213 15

same type of behavior has been noted with the A.

geoffroyi group in the field. Occasionally two Ateles

may wrap their tails around each other's body

while locomoting together either quadrupedally

or bipedally. This frequently occurs when the two

animals have embraced and are seeking to approach a stimulus situation which has frightened

one or both of them (Klein and Klein, 1971). It

would appear that this is a mutually reinforcing

behavior pattern.

ROLE SUMMARY

fc In this section, I wish to briefly comment on the

relationships in the captive Ateles fusciceps group

and contrast them with the relationships as we now

understand them in the free-ranging group of

Ateles geoffroyi on Barro Colorado Island.

The adult male A. fusciceps is rather independent of the females in his movements. A considerable

portion of his time is spent in active locomotion

around the cage. When new visitors approach, it

is the adult male who takes notice of the fact and

increases his brachiation rate. He may display aggressively to noisy patrons in the zoo and has his

own special aggressive relationships with certain

members of the keeper staff. It is he that participates in leaping displays, bar shaking, and marking

behavior with his pectoral gland (see "Olfactory

Communication," p. 18, and "Male Agonistic Display," p. 20).

In the caged situation, it is the adult male who

exclusively initiates long calls. The adult male

shows increasing attention to juvenile males as

they become independent of their mothers. He

actively encourages interaction with them and

shows protective responses toward them. During

ambivalent interactions, the adult male may solicit

participation of a juvenile male by approaching,

embracing with a low, gutteral whinny, and mutual pectoral sniffing. Then continuing to keep an

arm around the young male, the adult male can

lead him to the front of the cage to participate in

threatening calls or can lead him to a corner of the

cage whereupon the adult male will initiate a series

of long calls. Thus, the adult male actively solicits

participation in the performance of the long call

acts or in the performance of mutual trilling to a

potentially hostile stimulus source (see also "Male

Group," p. 68).

Because of a special relationship between the

adult male and myself, I was able to induce a variety of behavioral responses, most of which were

quite predictable. When I attempted to interact

with adult female V, the male would always approach me and generally his first act would be to

hang up behind female V and grasp her about the

waist with his hindlegs in a movement reminiscent

of hindleg grasping and locking during copulation.

The gesture with the hindlegs would be shown

only for less than 5 seconds, whereupon he would

generally brachiate away after touching the female.

His rate of brachiation around the cage would

vastly increase when I would approach without

food.

Such behavior patterns by the captive male

Ateles fusciceps were reminiscent of those shown

by the free-ranging Ateles geoffroyi in Panama. It

is the adult male who directs attention toward

maturing juvenile and subadult male offspring.

Through his efforts and the young male's efforts

to remain near him, a subgroup of males is formed

which ranges quite independently of the core

group of females and their dependent offspring.

Table 8 gives some indication of these subgrouping

tendencies during 1970 and 1974.

It is the adult and subadult males, with supporting participation from juveniles, who respond to

an intruder coming in upon them while resting in

the trees. Rapid brachiation with descents of over

15 feet to land with a crash, branch shaking, and

brachiation with branch breaking over the head

TABLE 8.—Subgrouping* tendencies for

Ateles geoffroyi

Subgroups

Adult $ (alone)

••Adult $ + 2 or more $

Adult 9 (alone)

> 2 Adult 9

Adult 9 + J or I

2 Adult 9 + J or I

^ 2 Adult 9 + J or I

Total

Number of sightings

1970 1974

3

3 7

2 1

1

5 1

2 1

3

13 16

• Subgroup is less than half of total troop and found moving or resting at a distance > 100 m from other individuals.

• • All male subgroup.

The male subgroup was seen resting near or moving with

the females three times in 1970 and eight times in 1972.
16

SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

FIGURE 5.—Typical subgrouping of two female Ateles geoffroyi and their dependent offspring.

Note the enlarged mammae of the female on the left. (Photo by C. M. Hladik.)

of an observer are often initiated by the male

group (Carpenter, 1935). In the confines of captivity, the male A. fusciceps cannot display the full

range of behavior shown in the field; nevertheless,

his interest in juvenile males and their mutual

participation in activities reflect the same sorts of

processes manifested in the free-ranging group of

Ateles geoffroyi.
NUMBER 213 17

Adult females, on the other hand, form their

own subgroup. Affiliations among females are apparently based on long-term processes. Mothers

and daughters often show a special affiliation with

attendent grooming relationships. Females with

offspring of a similar age class often form play

groups, which permit the young to interact (Figure

5). As reported by Eisenberg and Kuehn (1966:45)

adult females with young appear to be group promoters. Females with nearly mature young, however, may become much less bound to mothers

with young of an equivalent age. In brief, then,

females tend to segregate into subgroups based

upon their particular phase in the infant rearing

cycle. It is safe to say that any female can act

independently of others and does so. Thus, even

temporary subgrouping of mothers with young

of an equivalent age can break up with females

moving independently, accompanied only by their

infant or dependent juvenile.

Signal Systems in Ateles

Problem of Communication Analysis

Marler in his theoretical article of 1961 adopts

Morris' (1946) model for the study of semiotics.

The three aspects of semiotic analysis include semantics, syntactics, and pragmatics. Syntactics involves the study of signs or signals and included

in such a study are efforts to give a physical description of the signal itself and to compare such descriptions with other signals in order to formulate

a classification of signal types. Such an effort eventually leads to the formulation of a "vocabulary"

for the channel of communication under investigation. The study of syntactics can be extended in

an ontogenetic or phylogenetic sense by comparison and by outlining criteria for discrimination

between homologous and analogous signals.

Pragmatics involves the determination of the

function of the signal. In other words, you attempt

to infer the significance to the communicant by

noting the nature of the response to the signal.

There are four categories noted by Marler for the

function of sounds: (1) Identifiers are signals that

give spatio-temporal information. (2) Designators

are signals that dispose the communicant to do

something because the performance of that act

will lead to a goal. (3) Appraisers are signals

which communicate a preferential status concerning the sender. (4) Prescriptors are category signals

that predispose an animal to choose to do (a)

rather than (b), (c), (d), etc., because the performance of (a) leads to a goal more desirable than

any of the alternatives. In a sense, then, prescriptors

are tied to designators. Marler concluded that the

semantic aspect of communication was more or

less closed to the biologist.

A divergence in approach arose because Hockett

(1960) listed "semanticity" as one of the attributes

of a true communication system. Semanticity for

Hockett evidently involves the relationship between the signal and a designata or referrent in

the environment. This theme of semantic analysis

has in turn been expanded and developed as an

approach by Smith (1965, 1968). It would appear

to me, however, that this excursion into the semantic aspects of animal communication is fraught

with certain difficulties. The "meaning of meaning"

in terms of Ogden and Richards (1949) involves a

triadic relationship between the symbol, the referrent, and the thought in the mind of the communicant. In other words, the signal from a sender,

upon being perceived by the receiver (given a defined external environment), involves both the

perception of the signal and an association with

the designata through memories. The cognitive act

then leads to a selection of a response, which may

involve the production of other signals or physical

responses. But thought and selection of a response,

when taken from a subjective standpoint of the

receiver of information, leads us too far into unverifiable realms. We may be disposed to return

to pragmatics (which, of course, implies semantics)

as a more rigorous approach to the analysis of

animal communication.

Semantics is the study of the relationship between the signal and the meaning, and meaning

itself involves two aspects: connotation and denotation. Denotation refers to the object for which the

signal (symbol) stands. Connotation involves the

relationship between the referrent for the symbol

and what memories and recollections the receiver

conjures up. Meaning, in the semantic sense, is
18

SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

applicable to both the sender and receiver and, as

such, involves the establishment of connections

between the features of the signal and the corresponding mental processes in the act of signaling

itself. In the broadest sense, the analysis of human

language involves a consideration of the "meaning

of meaning" and can do so only because we as

humans have the capacity to introspect and relate

our introspections to one another. This possibility

is denied us when we stand as external observers

describing the communication processes of animals

via some metalinguistic system. As Cherry (1961:

222) points out, semantics and syntactics are indeed contained within the realm of the field of

pragmatics, but pragmatics relies in the end on the

description of the ongoing process rather than on

inferences of what is internal to the animal itself.

Language for a human is used not only to

express thought, but also shapes our categories of

thinking (Whorf, 1959), and human language is

not completely tied to emotional state, but in fact

is a learned system albeit that the learning involves

the shaping of an innate substrate (Chomsky, 1957;

Count, 1973).

Thus, if I am an observer watching a troop of

spider monkeys feeding and a man is approaching

on the ground, I may note that the adult male near

the terminal end of a branch indicates he has

perceived the man by his attentive posture. The

adult male may then show some pilo-erection,

tensing of the muscles, rising to a more upright

position, fixation of the man, and may commence

uttering a barking vocalization. While continuing

to vocalize, he may then shake the branches, bound

down to a lower branch and shake again, continuing to utter the cry. Since I have observed similar

behavior under conditions where attack or flight

could be shown with equal probability, I can infer,

on the basis of pilo-erection and branch shaking,

that the male is highly aroused and that his mood

implies a tendency to attack, as well as a tendency

to flee. Meanwhile, the result of his vocalization

causes a feeding subadult male to turn, assume

similar postures, and utter barking cries while tending to move backward toward the trunk of the tree

and away from the direction of the man. Furthermore, going back in time to the beginning of signal production by the adult male, I had noted that

an adult female gathered a young to herself and

moved away without making a sound.

By describing the whole contexts, I can ascribe

a function to the call. The function may be phrased

as a prescriptive category disposing the subadult

male to perform action (a) and the adult female

to perform action (b). I can also associate the sending of the signal with a specific mood of the adult

male and with a certain set of physical circumstances. I do not think that I am justified in ascribing to the barking sound a denotative characteristic; that is, I do not think it necessarily means

"man close," rather, if it means anything, it may

mean that the male is highly aroused, and in a

state of ambivalence between attack and flight. If

this be denotative, it has the prescriptive function

of inducing a response on the part of the receivers

appropriate to their age and sex class.

It is possible to speak of the presumptive information content of the signal. Once again, without

making a full excursion into semantics, if I confine

the presumptive information content to be that

information allowing the receiver to choose among

several possible actions, I have still not entered the

domain of the unknown mental processes of the

sender and receiver.

Such excursions into semantics may have great

heuristic value for workers following the theoretical structure developed by W. J. Smith, but for

the purposes of this study I will confine myself in

the main to contextual analyses inferring two types

of information: (1) the mood of the sender and

(2) its effect upon the receiver. From this may be

derived a presumptive function and an inferred

information content in the prescriptive sense. In

no way, however, will there be any implication concerning the mental processes, other than the fact

that some learning may be involved in the selection shown by the receiver with respect to the host

of responses it may make upon perceiving the signal itself.

Olfactory Communication

Aspects of olfactory communication in Ateles

belzebuth have been considered by Klein (1972)

and Klein and Klein (1971). The Kleins (1971)

point out that urine very probably conveys information concerning the estrous state of the female.

Sniffing urine is predominantly a male activity. The

Kleins further point out that the pendulous clitoris

of the female with its median groove could serve
NUMBER 213 19

as a urine-retaining organ, thus allowing the scent

of urine to be spread wherever the female sits.

Similar behaviors have been noted with A. fusciceps. The male tends to sniff the urine spots of

females, especially throughout the course of an

estrous cycle (Table 9). Furthermore the clitoris of

the female may frequently be touched by the male

and the hands subsequently sniffed. The data from

observing captive A. fusciceps have tended to confirm the Kleins' hypotheses.

Eisenberg and Kuehn (1966:18) mentioned the

pectoral gland of A teles and considered that during

the embrace, secretions from the pectoral gland

could be sniffed by the contacting animal. Very

often during the embrace, the sniff is directed at

the junction of the neck and chest or perhaps toward the axillary region. Thus, direct sniffing of

the pectoral gland appears to be unnecessary. This

may well be a result of the fact that the animals

have a tendency to rub their pectoral area with

their hands thus serving to spread the scent over

the hairs of the venter and chest. Epple and Lorenz (1967) have reviewed the structure and placement of sternal glands in the Plattyrhine monkeys.

They have called attention to the fact that adult

male spider monkeys frequently rub the gland

during aggressive arousal.

My observations on Ateles fusciceps suggest that

several processes may be at work in the spreading

TABLE 9.—Urine sniffing and marking behaviors in

captive Ateles fusciceps

Subject

M

B

M

J

M

M

V

2/ Sd Activity

6

2

1

1

3

8

1

239

6

8

11

10

19

2.5

83.6

6.4

3.4

6.2

0.5

Sniffing urine

Sniffing urine

Sniffing marked

Sniffing marked

Food sniff and

Ventral rub

Anal rub

artifacts

artifacts

chest rub

2f = total frequency of urine sniffing and related behaviors

shown; 2d = total duration of urine sniffing and related

behaviors shown; % = percentage of total duration of all

urine sniffing and related behaviors for all observation

periods.

Sniffing involved 053% of total observation time. M's

(adult male) urine-sniffing accounts for the highest percentage

of all olfaction-related activities. A quantitative rise in urinesniffing is noted in connection with estrus and copulation

since a 232-second bout of M's urine sniffing occurred after

his first copulation with female B.

of scent by adult males and females, although

marking frequency seems to be higher among adult

males. During aggressive arousal, the male A. fusciceps may salivate greatly while brachiating around

the cage. Saliva may be wiped from the chin and

then the forepaw rubbed on the chest. In addition,

without noticeable aggressive arousal, the male A.

fusciceps would often rub strong smelling substances in his pectoral area.

Example: The male Ateles fusciceps, M, was noted to rub

some food objects upon his chest after taking them from my

hand and before biting into them to commence feeding. This

movement was rather interesting, but somewhat puzzling

with respect to interpertation. Initially I thought that because I had given him the food and since he regarded me as

a rival, he may have found it necessary to mark the food with

his chest gland thus making it familiar to him. However, it

appeared that not all foodstuffs were marked in this way. He

seemed particularly prone to rub his chest with slices of

orange, thus it may be that the aromatic scent of orange

helps lower the threshold for marking and the fact that I had

given it to him had further raised his level of uncertainty to

the point where marking has a reassurance function. He did

not exhibit this rubbing behavior when he was handed string

beans or apples.

The adult male Ateles fusciceps would also

mark by rubbing his pectoral gland either on

branches in the cage or on the vertical upright

bars. This was done on four successive days immediately after my approach to the cage after I had

been absent for some time. This same adult male

would also mark during periods of aggressive

arousal. Often a marking bout would be followed

by a leap to the front of the cage and shaking the

bars. Two forms of marking behavior were shown:

(1) where the male would stand upright and wipe

his chest up and down on a vertical support in the

cage, or (2) alternatively, he would mark quadrupedally. Quadrupedal marking often occurred

while the animal was in motion. As he depressed

the forequarters, he would slide his chest for perhaps some 5 centimeters and then lift up his chest

by increasing the foreleg extension phase as he continued walking. Preferred rubbing spots were

shown on plane surfaces of the bench at the rear

of the indoor cage. During successive marking

bouts, the same spot would be marked. On two

occasions, one of the females, upon approaching

the spot, would sniff and mark in a corresponding

fashion.

Not only is the pectoral region and the vicinity
20

SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

of the sternum a target for sniffing during an

embrace, but spider monkeys frequently sniff the

genital and anal areas of each other during other

forms of encounter behavior. The juvenile male

frequently contacted the adult male when he was

reclining by sniffing in the inguinal region or sniff

ing at the adult male's genitalia (see "Genital

Display," p. 14). Finally, it should be mentioned

that both males and females occasionally depress

the anogenital region to a branch and slide forward, thus performing an anogenital rub. While

some of these movements seem to be related to a

comfort movement or relieving some irritation, at

other times it would appear to be an incipient

marking movement. Both males and females have

been noted to rub their anogenital regions after

copulation.

Clearly, then, chemical traces involving the use

of urine or glandular secretions from such an area

as the sternal gland are involved in the coordination and integration of spider monkey behavior

patterns. Experiments have not been performed to

elucidate clearly the functional aspects of marking

behavior, but the association of sternal gland

rubbing and aggressive display on the part of the

male strongly implies that impregnating his immediate surroundings with his own scent may serve to

communicate his individual and sexual identity to

newcomers or intruders in his living space.

Visual Communication

Obviously the movement patterns of an individual monkey can, in and of themselves, impart information of intent to a potential receiver. Approaches, movements away from, reaching out to

touch, reaching out to slap, are all aspects of a

communicatory situation. In this section, I hope

to discuss certain outstanding features of visual

communication removed from the context in

which they normally appear.

MALE AGONISTIC DISPLAY

Adult males characteristically perform a movement sequence towards intruders which may be

termed a threat display. In captivity it may be

shown toward handlers; in the field situation, it

has been observed by adult males responding to

human observers on foot. Aspects of the male display may also be shown toward potential predators,

such as the tayra (Eira bar bard). The male may

run along a limb or bench in a cage with a crossed

extension quadrupedal gait. During the quadrupedal gait, the back may be arched slightly in a

manner reminiscent of the "arch display" by Aotus,

but it is in no way ritualized and may in fact be a

mechanical adjunct of forward, quadrupedal locomotion on a tree limb. The tail is held up and

curled at the tip approximating a question-mark

in form. Typically the male shows pilo-erection.

He may stoop during his quadrupedal run, flex his

forelimbs, and touch his sternal gland or chest region to the substrate. At the termination of a quadrupedal run, the male will exhibit rapid brachiation while looking toward the offending object,

still showing pilo-erection, and, at some point

while hanging by his tail, swing toward the offending object and grasping nearby branches (or in

captivity, cage bars) shake the branches. At the

time of shaking and while orientating toward the

intruder, the adult male often shows an open

mouth with full tooth exposure.

FACIAL EXPRESSIONS

Facial expressions may be given in the absence

of vocalizations or associated with certain vocalization types. Vocalizations are described on page

23 ("Vocalizations"), but will be referred to in

this section where appropriate. The lips of the

spider monkey are rather mobile, thus the teeth

and, in particular, the canines may be displayed

conspicuously. Tooth exposure does not always

accompany the opening of the mouth; indeed, the

animal can yawn with little tooth exposure.

Van Hooff (1967) has outlined a scheme of

facial expressions for higher primates. Most of his

work was based upon an analysis of facial expressions in Macaca and Pan, but it would appear that

his overall scheme is applicable to a wide variety

of primates. Recently Chevalier-Skolnikoff (1973)

has reviewed primate facial expressions building

upon the analyses of Van Hooff. Van Hooff distinguished 8 major facial expressions involving

variations in ear position, eye closure, and retraction or extension of the lips. Partial squinting,

ears forward, and lips contracted but not exposing

the teeth was termed the "tense mouth," and was

associated by Van Hooff (1967) with attack tend-
NUMBE

R 213

encies. Varying degrees of staring with open

mouth, with or without bared teeth, appeared to

involve a balance between attack and flight

tendencies. Often these expressions were accom-

panied by vocalizations. A silent expression with

squinted eyes and retraction of mouth corners with

tooth exposure, termed the "silent bared teeth,"

was associated with a weak flight tendency and

seemed to have an appeasement function. Exten-

sion of the lips in the "pout face" appeared to

accompany a desire to approach an object or ex-

press, in the case of a young animal, a wish to be

with the mother. An open mouth with relaxed

lips accompanied a so-called "play face" expres-

sion and was often involved in ludic behavior.

In Eisenberg and Kuehn (1966), the facial ex-

pressions of Ateles were broken down into cate-

gories: open mouth with no canine exposure, open

mouth with canine exposure, the grimace which

was similar to the preceding but the corners of the

mouth more retracted, and pursed lips similar to

the pout face or protruded lip face defined by Van

Hooff. Eisenberg and Kuehn (1966:25) remarked

that expressions of Ateles corresponded roughly

to the series proposed by Van Hooff and suggested

an evolutionary parallelism in the development

of facial expression in the Cebidae, when com-

pared to the Old World macaques.

The 1966 work was based primarily on Ateles

geoffroyi. Current analysis of Ateles fusciceps and

further consideration of expressions and their use

in A. geoffroyi leads me to make the following

additional comments. The term "grimace" as ap-

plied to an expression showing extreme retraction

of the lips and full tooth exposure is best not

treated as a separate expressive type, but rather it

should be considered as part of the class of ex-

pressions involving tooth exposure. Partially open

mouths with the corners of the mouth retracted

and exposure of the teeth are seen to occur in

"tense" contexts such as: (1) when a juvenile is

frightened by a sudden movement, or (2) when

an animal has been teased by another member by

having its tail or hair pulled, or (3) when another

FIGURE 6.—Contrasting facial expressions by Ateles behebuth:

a, pursed lips with half closed eyes during approach to a

dominant social partner; b, open mouth with no tooth expo-

sure; c, open mouth with slight lip retraction and moderate

tooth exposure. (Drawings by C. Dorsey from the author's

photographs.)

21

a
22

SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

individual approaches too closely towards an animal having a desired food item. There may be no

accompanying vocalization with this expression.

Staring at a partner with a partially opened

mouth and little tooth exposure often involves

the production of a twitter or trill-awk call. An

animal may produce this call and expression when

a social partner moves away and the communicator

wishes contact; as, for example, when a mother

withdraws from a suckling juvenile. A similar face

and the trill-awk phase of vocalization may be

produced by a juvenile after being slapped, but,

during high intensity expressions of trilling, the

facial expression may involve an open mouth and

some tooth exposure. The same expression and

vocalization may be produced when an individual

is frightened by a sudden movement.

On the other hand, protruding the lips and the

production of a slow, growling whinny sound may

be involved with approach and embrace. The

same facial expression can be employed while the

animal is trilling when an approach-retreat game

is being played involving role reversal between a

male and a female. Protruded lips may also be

shown during initial approaches at the onset of a

grappling bout, again seeming to indicate contact

receptivity. It should be pointed out, however,

that during a grappling bout or mock fighting the

animals may show open mouth with retracted

corners thus exposing the teeth. Tooth exposure

in this context appears to imply "mock agonistic

behavior."

Exhibiting a chin-up often accompanies a greeting call of the tee-tee or whinny. Production of

whinnies and tee-tees is often done with a virtually

closed mouth and the vocalization seems to be

produced through the nose. However, during slow

whinnies which often accompany an approach and

embrace, pursed lips may be shown (Figure 6).

It seems fair to say that facial expressions of the

spider monkey parallel those of the macaque, but

I have been unable to subdivide the expressive

forms as finely as that accomplished by Van Hooff.

It is true that an open mouth with no canine

exposure or an open mouth with some canine exposure appears to accompany frightening situaFIGURE 7.—Facial expressions by Ateles: a, relaxed face prior

to sleep, A. geoffroyi; b, direct stare (nonhostile), A. paniscus;

c, expression during whinny, A. behebuth. (Drawings by C.

Dorsey from the author's photographs.)

a '
NUMBER 21S 23

tions. Extreme tooth exposure may be involved in

a threat context. Lifting the chin appears to accompany the production of greeting sounds, but the

lips are generally kept closed. Protruding the lips

does appear to correlate with a contact receptivity,

although the vocalization accompanying lip protrusion may vary and include the ook-ook and

grappling receptivy all the way to slow, growling

whinnies and embraces. Protruded lips may be

shown even while the animal squeaks, if the animal is both withdrawing from a dominant, yet

exhibiting aspects of contact receptivity.

Aside from the play contexts which will be

elaborated on later, it is fair to say that canine

exposure accompanies situations that suggest propensity to attack with perhaps a balanced tendency

to withdraw. Pursed lips seem to be associated

with friendly sounds and contact receptivity. The

chin-up, which often accompanies the production

of tee-tees, whinnies, and slow whinnies, may be

involved in the production of the sound itself, but

I am inclined to think that it has in part a ritualized function that decreases tension in the

recipient.

Direct eye contact can be a threatening expression depending on the receiver. In my relationship with the adult male A. fusciceps, staring at

him directly could cause him to avoid and then

immediately respond with an aggressive display

(see "Male Agonistic Display," p. 20). On the

other hand, direct eye contact with the females

generally caused them to lift their chins and produce one of the whinny variants. (For diagramatic

clarification, see Figures 6 and 7.)

Vocalizations of Ateles fusciceps

and A. geoffroyi

SYNTACTIC ANALYSIS

Utilizing the Missilyzer (Kay Electric Co., Model

675), selected tapes were analyzed to prepare sonograms of representative vocalizations (see "Captive

Research," pp. 1-2). Tracings on the sonograph

paper were analyzed with respect to frequencies

emphasized, duration, and interval. Vocalizations

showing numerous side bands indicative of pulse

modulation were also analyzed on a Tectronix

Oscilliscope (Type 323) for a more refined frequency analysis.

The following definitions are employed throughout the text (adapted from Struhsaker, 1967): A

syllable is an uninterrupted tracing by the sonograph. A phrase is a group of syllables separated

from another group by an interval longer than

any intersyllabic interval. A call is a phrase or

group of phrases which is distinctive in form. Calls

are generally referred to by a descriptive or onomatopoetic name. A bout is a group of calls which

forms a temporally distinct unit.

Syllabic transformation is common in the production of sounds by spider monkeys. Some simple

forms of intergrading were discussed by Eisenberg and Kuehn (1966), but in general this topic

was unexplored. While it is true that certain calls

can be defined with respect to context and structure, the existence of intergrading syllables makes

it now possible to describe the vocalization system

of Ateles as a graded system. As will become apparent the syllabic transformations involved in the

genesis of calls include the following mechanisms:

(1) prolonging the duration of the syllable while

shortening the interval between syllables in a

phrase or shortening the interval greatly, which

may result in (2) fusion of syllables to form a

longer syllable of the same structure, and (3)

frequencies may be modulated between individual

syllables to achieve a different tonal quality.

Before proceeding to a discussion of the calls,

the syllabic structure will be considered in some

detail. For convenience, syllables, as displayed on

the sonograph, can be broken into four "morphological" classes (Figure 8): (1) Clucks: short sound

<0.05 seconds in duration with little harmonic

structure. (2) Clear, harmonic calls: syllables

which emphasize a single frequency band with true

harmonics present. The syllable may be brief,

<0.05 seconds, or quite long, >2.0 seconds, and

may show either little or a great deal of frequency

modulation. (3) Syllables with a vibratto form:

On the sonograph numerous side bands are evident. The energy is not displayed in a single narrow frequency range. Some or all of these syllables

may result from rapid pulsing of extremely short

emissions (Watkins, 1967). (4) Syllables that show

little structuring and approximate noise.

Utilizing syllable structure as displayed on a

sonograph (Missilyzer), the following key can be

designed which specifies the call types formed from

the syllable variants. Two keys are offered. The

first key considers calls composed of relatively

uniform syllable types; the second key considers

calls composed of two or more syllable types.
24

SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

FIGURE 8.—The four basic syllable types: a, syllables with a vibratto form, side bands are evident;

b, clear, harmonic syllables; c, syllables that show little structuring, side bands, and approximate

white noise; d, short syllables, "clicks or clucks," showing little structure and side bands.

(Ordinate in Khz, abscissa in seconds.)

Syllabic Key to Some Calls of Ateles fusciceps

Syllables of Calls That Are Uniform in Structure

I. Low Intensity Calls.

A. Unvoiced: Syllable consists of rather uniform energy distribution; results from an exhalation termed a hiss (Eisenberg and Kuehn, 1966).

B. Voiced.

1. Syllables are brief pulses (<0.03 sec) of sound almost click-like. An infant sound and

a precursor to several adult sounds (see "Ontogeny," p. 52), clucks or chuckles.

2. Syllables are short in duration (5:0.07 and <0.2 sec) and grunt-like, termed "ook-ook"
NUMBER 213 25

(Eisenberg and Kuehn, 1966), each syllable when analyzed on a missilyzer shows

numerous side bands, i.e., the energy may be pulse modulated. The lower frequencies

are emphasized with most energy lying below 1.5 Khz. The syllables are repetitive

and rhythmic. The call may vary in its intensity.

II. Variable Intensity Calls.

A. High pitched calls (much energy >2 kc) with a relatively strong emphasis on a narrow

frequency range with true harmonics.

1. Calls composed of syllables which are short (<0.5 sec) in duration, but show little

frequency modulation from one syllable to the next,

a. Each syllable shows considerable frequency modulation (over a range of ~0.5 Khz).

(1) Calls which are composed of extremely short syllables (<0.07 sec) separated by

short intervals (<0.19 sec); trills and twitters.

(a) Syllables chervon in form with long intervals (0.08-0.19 sec): trill.

(b) Syllables with complex modulation but in other respects comparable to the

above: trill.

(c) Syllables with complex modulation but with very short durations (<0.05 sec)

and brief intervals (<0.08 sec): twitter.

(2) Calls which are composed of short syllables (>0.07-<0.20 sec) separated by

short intervals (<0.3 sec). Syllables are complex generally beginning with a

frequency modulated pulse which ascends over a range of 1 Khz: yip-yip or

pulsed trill. At low intensity with intersyllabic modulation, it may grade to a

slow whinny (II.A.2.a(l)), or it may show fusion of syllables to a pulsed chitter

b. Each syllable shows some frequency modulation. High frequencies are emphasized

(~3 Khz).

(1) Duration of syllable exceeds 0.4 seconds; may be uttered in bursts with short

intervals: squeak (Eisenberg and Kuehn, 1966), can grade to chitter.

(2) Duration of syllable between 0.16 and 0.38 seconds, intervals between syllables

are short; energy as high as 5.4 Khz may be emphasized: pulsed trill or pulsed

chitter. (Eisenberg and Kuehn, 1966). This call may grade by fusion of syllables

to a longer call, e.g., pulsed chitter.

2. Calls composed of short syllables but some are lengthened in duration (>0.5 but

<1.0 sec).

a. Inter- or intra-syllabic modulation over a range of around 1 Khz.

(1) Syllables may range from 0.03-0.92 seconds in duration. A given syllable may

differ in pitch from the preceding syllable by as much as 1 Khz. Intervals

between syllables are variable from <0.04 to 0.3 seconds. Fusion of syllables

converts to a true whinny. In its present form, the call is referred to as a

yip-yip or slow whinny variant (Eisenberg and Kuehn, 1966).

(2) Syllables typically long from around 0.5 to 0.8 second.

(a) Highly modulated syllable with frequencies rising and falling three to four

times over a range of 0.8 Khz during a period <0.9 seconds. Pitch may

range from 3.0 to 5.0 Khz: tee-tee (Eisenberg and Kuehn, 1966).

b. Syllables relatively unmodulated from one to the other, duration of syllable ~0.7

seconds. Several harmonics may be present: chitter.

3. Calls containing long syllables which exceed 0.8 seconds in duration.

a. High pitched syllables which show frequency modulation over a wide range. The

duration may be 2.0 to 2.3 seconds with energy emphasized at 1.4 to 4.8 Khz:

whinny (Eisenberg and Kuehn, 1966).

b. Syllables of intermediate pitch (~1.5 Khz) with some modulation.

(1) Descending call with energy concentrated from 1.8 to 1.5 Khz: eeeaw (P.B.2).

(2) Ascending (1.8 to 2.2 Khz), often ends in a screech; about 1.0 seconds in duration and repetitive: grunt-trill (Eisenberg and Kuehn, 1966) ah eee.

c. Syllables of intermediate pitch with little modulation (see III. Loud Calls).

B. Calls which may emphasize low frequencies (<1.5 Khz) or high frequencies (>1.5 Khz)

but have an imperfect harmonic structure. Each syllable is composed of many brief

pulses which upon sonographic analysis display numerous side bands.

1. Low frequencies (<1.0 Khz) emphasized.

a. Each syllable within a phrase is brief (<0.5 sec).
26

SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

(1) Syllables within a phrase exhibit relatively uniform frequencies.

(a) Syllables >0.15 but <0.5 seconds in duration; the intervals range from 0.17

to 0.60 seconds. A repetitive sound with energy emphasized between 0.6 and

1.4 Khz: bark or yap (Eisenberg and Kuehn, 1966; see also III. Loud Calls).

(b) Syllables average between 0.6 and 0.14 seconds in duration. They are rhythmic and repetitive. Intervals range from 0.06 to 0.22 seconds: ook-ook; ak-ak

(Eisenberg and Kuehn, 1966); panting (Klein, 1972).

(2) Syllables within a phrase show frequency shifts from one syllable to another.

Each syllable may be <0.05 seconds with an equal interval. The phrase or

call may be 1.8 seconds in duration with energy emphasized at 0.5 and 0.2 Khz:

gutteral whinny or sobs (see slow whinny, p. 39).

b. Syllables may be long (>0.6 sec) and intermittent in their utterance. Energy is

typically concentrated below 1.0 Khz.

(1) Syllable 0.6 to 0.9 seconds: growl (Eisenberg and Kuehn, 1966:13).

(2) Syllable >1.2 seconds: caw (Eisenberg and Kuehn, 1966:15). (See also III. Loud

Calls.)

2. Higher frequencies emphasized.

a. Each syllable is very brief (0.03 to 0.12 sec); frequency emphasized can vary

within a call from 2.0 to 3.0 Khz. Intervals between elements can be from 0.04

to 0.13 seconds. Phrase duration may exceed 2.0 seconds: slow gutteral whinny

(Eisenberg and Kuehn, 1966); sobs (Klein, 1972).

b. Syllables longer in duration: >0.20 second: screams (juvenile) or >1.0 second:

scream (adult).

C. Calls with little harmonic structure or poorly denned side bands.

1. Frequencies <0.7 Khz emphasized.

a. Short (<0.3-sec): cough (Eisenberg and Kuehn, 1966:14).

b. Very short (<0.09 sec): terminal notes (see I'. Intermediate Intensity Calls).

c. Long (>0.5 sec): growl and roar (Eisenberg and Kuehn, 1966).

III. Loud Intensity, Repetitive Calls.

A. Short syllables.

1. Short, repetitive syllables, low frequency (see II.B.l.a(l)(a)).

2. Short, repetitive syllables emphasizing high frequencies (see II.A.l.b(2)).

B. Intermediate length syllables (^1.0 <1.5 sec).

1. Complex modulation, single frequency emphasized. Includes the grunt-trill or eeeaw

(two subtypes described in II.A.3.b(l) and (2)).

2. Little modulation, not repeated, no single frequency emphasized: caw (II.B.l.b(2)).

C. Long calls (>1.5 sec) often complex with terminal syllables (Il.C.l.b).

1. Rather uniform energy distribution confined to a single frequency band at about 0.7

Khz but harmonics are present. Terminal notes may be present (see also II'. Loud

Intensity Calls): wail (Klein, 1972).

2. Pulsed phrasing with subsequent side band production when sonographed. Maximum

energy at -0.6 to 0.9 Khz: caw (Eisenberg and Kuehn, 1966:15); whoop (Klein, 1972)

roar (Oppenheimer, 1968) (see also II'. Variable Intensity Calls).

Compound Calls

F. Intermediate Intensity Calls.

A. High pitched elements in call (much energy >2 Khz); calls containing long syllables

which exceed 0.7 seconds in duration. Ascending (1.8 to 2.2 Khz), often ends in a screech;

about 1.0 second in duration and repetitive: grunt-trill (Eisenberg and Kuehn, 1966).

B. Calls that begin with a relatively narrow frequency range but end with a noisy sound:

compound call.

1. Descending pitch from 3.0 to 0.16 Khz. Duration 0.10 to 0.20 seconds: awk (juvenile

sound).

2. Ascending from 1.6 to 2.0 Khz. Duration 0.20 to 0.8 seconds: uh eeek (juvenile sound).

IF. Loud Intensity, Repetitive Calls.

Rather uniform energy distribution confined to a single frequency band at about 0.7 Khz

but harmonics are present. Short, terminal notes may be present: wail, caw or roar (III C 1

and III.C.2).
NUMBER 213 27

Syllabic Transformations and the Genesis of Calls

Given the key based on syllabic structure, the

manner in which syllables can be transformed will

be best understood by a systematic description of

each major call type. The call types intergrade

according to the chart in Figure 22. In spite of the

intergrades, certain call forms are distinctive with

respect to form and general context. Their existence leads the investigator in a first order analysis

to describe what appears to be a "paniculate" or

discrete system. The existence of intergrades does

not negate the older more typological approach

(see "Influences," p. 49).

Since the naming of calls in a dynamic system

is only a convenience for written communication,

Table 10 offers a portrayal of phonetic equivalents

for the more mundane names applied by the

author in earlier publications (Eisenberg and

>.35

.30

.20

.10

.05

Kuehn, 1966). Appendix 1 includes a summary of

the physical measurements for all call types.

Call Types Named and Defined

LOUD, SHORT CALLS WITH A REPETITIVE PATTERN

AND AN EMPHASIS ON LOWER FREQUENCIES.—This

call form is often termed "barking" (Eisenberg and

Kuehn, 1966:13) or yapping (Key II.B.l.a(l) (a)).

The syllables vary with respect to the frequencies

emphasized. The syllable may sonograph showing

a harmonic structure with energy at ~ 800 and

1400 Hz. When higher frequencies are emphasized, it may have a pealing quality with a longer

duration. It would appear that intervals between

syllables and syllable length itself can vary as a

function of mood shifts on the part of the sender.

Figure 9 illustrates this principle with five forms

.05 .10 .20 .30 .40 <50

FIGURE 9.—Temporal patterning of barks. Intervals separating consecutive syllables are plotted

on the ordinate in seconds. The abscissa indicates the average syllable duration in seconds. Each

sample point includes the average of at least five entries. The points represent numerical values;

however, the sonographic display properties of a bark syllable are drawn for several points as

visual reference only (Appendix I).
28 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

CCCCBCC C

£>>>>>> >

3 3 3 .3 ,3^ ,3^ S 3

OOOOOOO O

3333333 3

CCCCCCC

iliumC

OOOOOOO O

ZZZZX^Z Z

n M n n n n

V $3 tj a, 4) V 4>

J3 ,C J3 3 J3 .C .C «

OH a, DH .Q &• O< Q. cd

3

«

3

u

O

"3

•o

3

3

u

O

"3

(9

3

T3

3

O

"3

rt

3

3

O

"3

a

=3 be

S .5

5

z z

I

"2 -

a 1 =

H 1ST

J 1 ^

1 1

Is

11

c c

o o

z y.

3 S

1c

2 jg £

iu _C »9 '« — ,«. iS »3 *v •«

« t £

IU Ml

•a *a

•3 "3

<3

f

w rt ••* ^ flj C

in __

(9 S

5 ?? w i

n

8 I S

6-1

I S £ S

•S *

- 2 ^ c .S 2 i 3 ==

o S S ^ 3 -5 5 ^ ^

 u

PH sl £ <;

8.

5 "8 I •& fi |

! *

a;

C3 pD

pa xj

5 : ed pa

B B > g S

> >
NUMBER 213 29

?!1

3 3

"O 'O

3 3

113 3

u tJ

3 3

« E

S2

2 2= 2

pq p5 ^

u

^ ^ o U < S

<U CJ CL>

111

K (U «J

Ptf Btf P(!

« 3 3

W H «"
30 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

>35

.30

.20

.10

\

.10 .20 .30 .40 .50

FIGURE 10.—Trill, twitter, squeak, and chitter temporal relationships. (Syllabic transformation is

indicated by the broken line; scales as in Figure 9; syllable types are assigned a roman numeral

corresponding to the call form as designated in Table 10.)

1.0

4 *

3"

2>

1 •

i

N

.3

a

if

•

A

6 .9

1

JvkuoiiiM

1.2

I

1.5 1.8 2.1 24

11.—Sonographs of trill variants: a, trill to chirp series; b, fusion of trill to chitter.

(Ordinate in Khz, abscissa in seconds.)
NUMBER 213 31

of the bark portrayed. Syllable duration ranges

from 0.15 to 0.46 seconds with intervals from 0.16

to 0.59 seconds. The longer, pealing barks with

emphasis on higher frequencies are characteristic

of an animal in distress ("Contexts," p. 38). Bouts

of barking may persist for over 30 minutes.

This analysis of the bark illustrates well the

importance of temporal patterning as an indicator

of arousal level. The question can be raised as to

whether we are justified in treating this as one

type of call. I believe we can, for the following

reasons: (1) the syllable is relatively uniform in

structure for all forms, and (2) the context appears

to be functionally similar ("Influences," p. 49).

The call can be heard at a considerable distance

and is easily localized by a. human observer. It

would appear to function as a "mobbing" call as

will be described later.

INTENSE, HIGH FREQUENCY SOUNDS AND THEIR

DERIVATIVES.—Two call forms are involved, one

in which the syllables are incompletely fused, giving a pulsed quality; the second type demonstrating syllabic fusion and a smooth emission of sound.

Pulsed phrases: Trills and twitters (Key II.A.

l.a(l)). These high pitched calls include syllables

which are brief (<0.05 sec) in a twitter or 0.20

6 .9 1.2 1.5 2.1

FIGURE 12.—Sonographs of trill to chitter transforms: fused trill or harsh "metallic" chitteT.

(Ordinate in Khz, abscissa in seconds.)

4 -

3 -

2>

1 >H -

.3 .6

| i

I

.9

|

1.2

X 1

1.5

mm 1 1

1.8 2.1

•

FIGURE 13.—Sonographs of the whinny. Note extreme frequency modulation. See Appendix I.

(Ordinate in Khz, abscissa in seconds.)
32 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

seconds in the trill. The form of the syllable is

variable but high frequencies 3 to 5 Khz are

emphasized. Syllabic elements may be separated

by intervals as short as 0.05 seconds and ultimately

the syllables may fuse to form the pulsed chitter

(Key II.A.l.a(2)) (Figure 10). The figure illustrates a fundamental rule for syllabic transformation, namely fusion of elements by shortening the

interval between syllables. Figure 11 illustrates

the trill variants.

Continuous emissions: The squeak is a high

pitched call with little modulation and of moderately high pitch; it may grade into the chitter form

(Key II.A.l.b(l) and (2)). Chitters of long duration (>0.7 sec) may transform to an ee awk form

by ending with a noisy syllable (Key I'.B). These

sounds seem to be related functionally and form

a graded series. Some call forms, such as the squeak,

are relatively distinct to the human ear, but the

other call forms more or less intergrade. This complex of intergrading sounds illustrates the "rule

of fusion" in syllabic transformation (Figure 12).

HIGH FREQUENCY CALLS EXHIBITING EXTENSIVE

FREQUENCY MODULATION.—The tee-tee call is brief

and nonrepetitive, generally <0.9 seconds in duration. It appears to function as a greeting. Frequencies are modulated over a range of 800 Hz.

The whinny is similar in structure but longer (may

exceed 2 seconds). The whinny has variable intervals separating the phrases and its elicitation depends on variable external input (see "Mood,"

p. 46, and Key II.A.3.a). The whinny is related to

the slow whinny or chirp series and appears to be

formed from syllabic fusion (Figure 13).

CALLS WITH VARIABLE FREQUENCIES EMPHASIZED.—

These calls are rhythmic and their frequency is

modulated from one syllable to the next. These

calls are formed from brief syllables (<0.1 sec),

but the syllabic structure is variable (Figure 14).

Highly modulated syllables may grade to the

true whinny. The syllables emphasizing lower frequencies can grade to a long call form (Figure 15).

The uniting feature for this class of syllables

appears to be the rhythmic shift of pitch from one

syllable to the next; however, classifying low, gutteral whinnies (Key II.B.l.a(2)) with the chirp

series (Key II.A.2.a (1)) may in effect be artificial

since two moods may be confounded (see "Mood,"

p. 46). Nevertheless, there is a functional continuity for this class of vocalizations (see "Influences,"

p. 49).

REPETITIVE, RHYTHMIC, LOW FREQUENCY SOUNDS

(Key II.B.l.a(l) (b)).—These calls are composed

of brief (<0.1 sec) syllables having a relatively

unmodulated energy distribution. Intensity shifts

and shifts in the frequencies emphasized correlate

FIGURE 14.—Sonographs of two whinny variants: a, slow whinny note, modulation from one

syllable to the next; b, gutteral whinny, modulation from one syllable to the next but low

fundamental. (Ordinate in Khz, abscissa in seconds.)
NUMBER 213

>.35

.30

.25

20

.1 5

.10

.05

(V

K-.

mi

- ZU \

/

\

\

.05 .10 .15 .20 .25 0 1.0 2.0 3.0

FIGURE 15.—Temporal patterning and transformation within the whinny series. (Scales as in

Figure 9; roman numerals refer to call form as described in Table 10; broken lines indicate

known syllabic transformations.)

with different levels of excitation. The calls sound

like ook-ook or ak-ak. Context and function appear

to be well defined (see "Grappling," p. 12;

Figure 16).

HARSH, ATONAL SOUNDS (Key II.B.l.b (1)).—

May be low in intensity (low growl) or extremely

loud (roar). Characteristically frequencies <1.0

Khz are emphasized. These calls are not to be confused with the long, loud calls (Figures 16, 17).

INTERMEDIATE LENGTH LOUD CALLS (Key III.B.).—

These calls are difficult to classify. Some types

appear to be transitions to the long loud calls,

others appear to be high intensity variants of other

call forms. This category may be somewhat artificial. In Eisenberg and Kuehn's earlier work (1966:

12), the grunt-trill was described for A. belzebuth,

which now appears to be two call types: (1) either

a preface note or a low intensity precursor to long,

loud calls showing little pulse modulation (see

below), or (2) an ascending trill often ending in

noise. In the 1966 paper, the former variant was

termed the grunt-trill plus the caw; it is not to be

confused with the caw (see p. 34).

The grunt-trill is typically from 0.7 to 1.3 seconds in duration. It may be relatively pure in

tone and ascend in frequency from 2 to 3 Khz. It

may be described as: ah ee ee ee aah or ee ee

ooch, and be quite repetitive; except for the modulation, the call resembles the chitter. On the

other hand, these calls may descend from ~2.0

to 1.6 Khz during 0.7 seconds and sound like a5h

uuh or Ih aaah 5aah. This latter variant has

not been described before (Figures 11, 18 and Appendix I).

LONG, LOUD CALLS (Key III.C.l and Key IF).—

Call types in this category are often uttered in a
34

SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

FIGURE 16.—Ook-ook to growl series showing syllabic transformation. (Ordinate in Khz, abscissa

in seconds.)

compound phrase. The syllables contained in a

phrase are long in duration, often exceeding 2.7

seconds in duration, but within a phrase terminal

syllables may be as short as 0.03 seconds. These

terminal syllables follow upon a longer syllable by

an interval of some 0.1 to 0.3 seconds and are

separated from each other by short intervals of

around 0.04 seconds. In the field the terminal notes

may be missed by an observer at ranges of several

hundred meters, but the long syllables carry up

to 0.5 km. Referred to for A. geoffroyi as the "caw"

(Eisenberg and Kuehn, 1966:15) and as a "roar"

by Oppenheimer (1968). In the A. belzebuth

population studied by Klein (1972), these call

variations were referred to as "whoops."

Ateles fusciceps: Two syllable types are noted:

The short terminal notes have a duration from

0.02 to 0.04 seconds. The long syllables range from

1.5 to 2.7 seconds. Energy distributions average from

0.87 to 3.3 Khz (a range of 2.4 Khz). The average

frequency is about 2.0 Khz, but the average energy

emphasized lies at 1.16 Khz (N = 19). Some three

to four harmonics are involved (Figure 19).

At least two main subtypes can be distinguished:

(1) the clear form, and (2) the vibratto or harsh

form; both types can occur in the same series of

phrases. The clear form shows little frequency

modulation whereas the vibratto form is pulsed

in its delivery with slight modulations over some

50 Hz within each pulse (Appendix I).

Syllables in a phrase are separated by intervals

^0. 3 seconds. The terminal syllables when present are separated from each other by intervals of

less than 0.3 seconds. Phrases average some five

syllables of which three are generally the short

terminal form (Appendix I). Bouts of calling may

last up to 30 minutes. Ten minutes thirty-five

seconds of continuous recording showed that the

calling male emitted phrases during 53 percent of

the total time. He produced 36 phrases with an

average duration of 9.4 seconds. The average number of syllables per phrase exceeding 1.5 seconds

in duration equaled to 3.9 (N=15), range = 2 to 6

(Appendix I).

In the captive situation, this call is given by the

adult male. Juvenile males may also be included

in a chorusing behavior. Females approximate the

call when in captivity, confined alone and visually

separated from the group.

Ateles geoffroyi: In the field, A. g. panamensis

males may show long, loud calls as a chorus. In

addition long, loud calls may be uttered by either

males or females when alone. Several variants

have been distinguished. Oppenheimer (1975) has

described a series of roars uttered in phrases of

three calls, which are given by an adult male and

apparently promote assembly by the females. This

is the "caw" described by Eisenberg and Kuehn

(1966). Calls by females are discussed on page 39.

Male chorusing may occur after assembly through

the use of intermediate length loud calls or chitters (see "Signals," p. 69).
NUMBER 213 35

>.35

..30

.25

.20

.15

.10

.05

VIII

inn*

SI YIL

sm v

.05

j A

.10 .15 .20 .25 1.0 2.0 3.0

FIGURE 17.—Temporal patterning and transformation within the ook-ook to growl series. (Scales

as in Figure 9; roman numerals refer to call form as described in Table 10.)

Compound Calls and Their Genesis

Thus far the main thrust of the discussion has

been concerned with calls that appear to be derived from a single syllable type, which is transformed by alterations in the rate of utterance

(fusion) or a rhythmic shift of pitch (the whinny

series). A number of calls, however, involve two

or more syllable types. For example, the eeeaw

(trill-awk) when repeated, seems to involve a

possible alternation between a "clear" syllable and

a "noisy" syllable. This may indicate a simple shift

between two motivational states (see "Mood,"

p. 46) or it may imply a more simplistic explanation. For example, if we consider rising excitation

as accompanied by increasing energy output during

excitation, then during the delivery of a trill the

glottis may become more open allowing a greater

volume of air to escape, but causing a definite

shift in pitch to a lower frequency.

In the case of the long calls, the inclusion of

terminal syllables which appear to differ in syl-
36

SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

T r

.3 .6

FIGURE 18.—Intermediate length long calls; ascending trill descending to a noisy syllable e aaahaah. (Ordinate in Khz, abscissa in seconds.)

labic structure from the preceding longer syllables

may not imply a motivational shift. If the terminal

notes convey information concerning the precise

location of the sender, then we must assume selection has favored this call form as an entity. The

terminal syllables are thus best considered as part

of a call that has resulted from long term evolutionary processes, which may have "fixed" the

neuromuscular complex responsible for its genesis.

CONTEXTUAL ANALYSIS OF ADULT

AND JUVENILE SOUNDS

In analyzing the function of a signal, one must

designate a presumptive sender and receiver (the

roles are interchangeable) for each dyad that is

examined. In his essay concerning the biology of

expression and impression, Leyhausen (1967)

notes that the innate propensity to express patterns

of presumptive communicatory value, such as vocalizations, gestures, facial expressions, and postures, may in fact take place in situations where a

definite response upon the part of a presumptive

receiver is not evoked. Expressive movements and

sounds to a large extent are shaped by the social

situation in which they are performed. As will be

seen (see "Ontogeny," p. 52), expressive movements can develop in young Ateles fusciceps without imitative learning and in the absence of a

"normal" social environment. To quote Leyhausen

(Lorenz and Leyhausen, 1973:304), "An animal

with a fair amount of learning ability and a fixed

set of innate mechanisms for expression and impression, with the help of which it stimulates specific behavior in a conspecific and reacts itself to

the other's expressive behavior, naturally cannot

with time help noticing that this is so." In my

work with hand-raised Ateles, I was not prepared

to take data in a fashion which would allow precise

discrimination of what effects the artificial rearing situation had with respect to the frequency of

certain forms of expressive behavior. Nevertheless,

the conclusion is inescapable, that most of the

expressive movements and vocalizations of Ateles

do not require imitative learning for their initial

performance. It is also evident that the utilization

of vocalizations and expressive movements on the

part of Ateles can be specific to certain situations

and presumably have an influence on the activities of some of the presumptive receivers. If the

signal in question is to carry information from the

sender to the receiver, we must infer the information content from a contextual analysis. In short,

what happens during the signal exchange, and

what happens after?

Obviously one primary function of a signal is

to pass on information concerning the mood of

the sender. A motivational analysis is thus a necessary step, which can yield a motivational classification. It should also be possible to relate syllabic

transformation to motivational shifts.

It seems intuitively obvious that as an animal
NUMBER 213 37

15*

1.2'

. 9 '

.6'

. 3-

5"

4"

3"

1 PJ

a 1

h

A A

2 3

A A

.6 .9

A A

4 5

1.2 1.5

6

AAkg

1.8

7

i

2.1

A

8

24

FIGURE 19.—Long call variants for Ateles fusciceps: a, undulating long call, possible derivative

from gutteral whinny; b, harsh long call series showing variation in syllable length (wide band

analysis 200 Hz increments). (Ordinate in Khz, abscissa in seconds.)

becomes more aroused, a signal may vary in intensity by increasing the amplitude and/or syllabic

frequency as for example during barking (see

"Mood of Sender," p. 46). Can we then distinguish between intensity changes within a single

mood and shifts in mood as evidenced by a change

in syllable form? This question will be dealt with

under "Alternation" (p. 48).

Considerations of Caste Differences

As will be shown (see "Ontogeny," p. 52), the

vocalizations of Ateles are developed in their basic

form without imitative learning. Basic syllable formation and temporal patterning develop with a

minimum of environmental influence. Nevertheless, there may be subtle learning involved in the

full maturation of long call temporal patterning.

In general, the two adult sexes have equivalent

vocal repertoires, but females do not produce loud,

long calls in the presence of an adult male. Juvenile males are actively sought out by adult males

and allowed to participate in long call bouts. What

effect this has on their adult repertoire has not

been adequately assessed.
38 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

Contexts of Sound Production

BARKING.—Ateles fusciceps display this behavior

rarely in captivity. They have barked at a stray dog

wandering in the park and often bark after initial

confinement in a shift cage. During the latter context, the barks are often of the "pealing" form.

Ateles geoffroyi in the field bark at human observers if the troop is unhabituated. Where spider

monkeys are hunted, barking and mobbing will

not be shown to humans (Wagner, 1956; K. Green,

pers. comm.). The A. g. panamensis group has

been noted to bark at the tayra, Eira barbara (see

Eisenberg and Kuehn, 1966:53).

While barking the animal may show varying

degrees of pilo-erection and when a group begins

barking, urination and defecation may be noticeable during the initial barking response. When

group members bark at a tayra, they may remain

in the vicinity for 20 to 30 minutes peering at the

intruding animal. Under these circumstances, one

may speak of a "mobbing behavior." Tendencies

to approach and withdraw are noticeable.

From a contextual analysis, it appears that barks

are delivered in response to a novel stimulus from

which the animals can escape or when the animal

is confined but unharmed and within hearing

range of its group. The pilo-erection, urination,

and defecation suggest high autonomic arousal

with simultaneous tendencies to defend itself and

avoid the stimulus object (s). The intensity of the

response is somewhat graded.

TRILLS AND TWITTERS AND THEIR DERIVATIVES

FOR Ateles fusciceps.—These high pitched intergrading calls are involved in situations where the

animal is excited (as evinced by some piloerection), socially attracted to the stimulus object,

and at the same time ambivalent or actually fearful,

since it avoids a close approach. It is given by a

subordinate avoiding a dominant and appears also

in play situations where a dominant reverses roles

with a subordinate.

Slow twitter: Given by juvenile male as he slips

during climbing.

Twitter to trill: Performed by adult female to a

patron who has a noise-maker; performed by adult

female V to daughter B as V chases B away from

the vicinity of adult male.

Twitter with half open mouth, no tooth exposure: Given by female V to me when food is withheld from her; juvenile male to adult male as

adult male persistently follows him.

Twitter to eek-eek (squeak): Given with partially open mouth, incisors showing, lips lifted, by

M and J. Open mouth, no tooth exposure: J after

V slaps him.

Metallic trill (chitter): Given with chin up, lips

parted to lips pursed, by adult male to me as I

leave the Monkey House. An awk syllable may be

incorporated on the end of the metallic chitter to

make it approximate an eee awk.

Squeaks: Contexts are similar to the preceding

but a more definite avoidance is shown by the

sender. This call may also be given if the animal

slips and falls, thus lending support to the idea

that this is a "fear" sound.

Squeak, which is low in volume and almost

"crooning": Appears to be less than 1.0 second,

not recorded. Given by adult female to infant

when the infant is off the mother playing just

prior to a shift in locus by the mother. The mother

will reach out to the infant while uttering the call,

thereby focusing the infant's attention on the

mother. Cannot be heard at a distance exceeding

3 meters in captivity.

Trill-awk (ee-awk): Expressed by juveniles

when isolated or when companion moves away. A

similar sound is given by adults at the departure

of a familiar attendant. Will be shown by adults

when isolated from a *group and confined (captivity).

Example of trill and trill-awk production by Ateles fusciceps (J = juvenile male, M = adult male): J sniffs M's

genitalia; they break apart, then M starts to follow as J moves

away, mutual emission of trilling awk calls continues. Lips

are pursed during the call. M catches J, they embrace. J

moves away with trill calls. As M catches J, he gives a low

growling whinny (sobs). M trills following J. J trilling. They

embrace. M low whinny (sobs); J moves away. They come

together, M and J embrace as they do so, M gives a low

whinny, they break apart, M to the bars and gives a low

bark (cough) to the patrons. J hangs trilling and twittering,

trill-awk to patron. Then they come together and renew

following on the part of M, moving away on the part of J.

TRILLS, TWITTERS, SQUEAKS AND THEIR DERIVATIVES FOR Ateles geoffroyi.—As with A. fusciceps,

the contents exhibit high degrees of excitement

and ambivalence.

Example of scream: Juvenile female roughly 7 to 8 months

of age screams and flees at approach of adult female (who

has no baby), while retreating to her mother. If male ap-
NUMBER 213 39

proaches, juvenile female will squeak to trill and move away,

but does not flee.

Example of low squeak: As an animal attempts to effect

crossing on a sapling that bends under its weight in the

direction of the next tree. Second animal in tree reaches out

to the animal on the bending sapling; they join hands and

the animal on the sapling effects the crossing, whereupon

they embrace and sniff their pectoral regions (similar to

mother-infant call).

Example of rapid twittering-squeak series: Given by an

infant when it slipped and fell; later female approached and

carried the infant on her back.

Example of twitter series: Given by adult female as she

notices me in blind and drops down to lower branches to

observe more closely.

CHITTER.—A high intensity derivative of the trill

series. Appears to derive from a thwarting context

where the sender is somewhat intimidated but

threatening. It may be followed by branch shaking

and violent brachiation (for further examples, see

"Signals," p. 69).

TEE-TEE; WHINNY AND SLOW WHINNY.—This frequency modulated class of vocalizations can actually be broken into three categories: (1) A high

intensity, rapid, nonrepetitive form, termed the

"tee-tee-tee," is used as a greeting call to persons

that the monkeys have associated with feeding.

Example: Tee-tee-tee given with chin up and

pursed lips or nonpursed lips, but mouth closed;

appears to be a greeting to persons associated

with feeding. (2) A shrill quick call, often repeated

several times, is given by several members of the

group when all foraging for an abundant and

desirable food item on the floor of the cage. The

variant is termed the "whinny" and is often given

with chin up and lips closed. (3) As feeding progresses, the animals may from time to time give a

slow, harsh whinny, which is the third variant. If

another animal approaches closely while feeding,

the slow harsh whinny form may grade into an

awk sound.

Ateles fusciceps: When soliciting food, they may

give a whinny to a bystander in the slow, low

intensity form. When this is done, the lips may be

pursed but almost closed. This is termed the "yipyip whinny" or "slow whinny." The chin is held

up in most cases, but occasionally no lift of the

chin is shown. It is given as a greeting to an attendant or observer or to a cage mate. A lower

pitched variant, the growling whinny, can almost

grade to an ook-ook. It is often given with pursed

lips, but may also be given with closed mouth.

Chin up is a common association. It is demonstrated when feeding is well under way or may

be given as a greeting, or during embrace (see

"Slow Gutteral whinny or sobs," p. 39).

Ateles geoffroyi panamensis: Although the

whinny is associated with feeding, it appears to

involve contact maintenance and can involve

group movements.

Example 1: While sitting as skies darken and wind increases, animals whinny to each other. Whinny calls at rate

of 3 in 4 minutes. After the rain begins, it seems to promote

whinnying back and forth among assembled females. Three

whinnies are then recorded in 4 minutes. By now all females

have assembled and huddled in the same tree throughout

the rain.

Example 2: Female gives whinny as male approaches. Male

replies with whinny. They join and move together into the

lower part of the canopy.

Example 3: Whinny call given twice in one minute following upon thunder. Calls from one of three females who are

sitting near each other in the same tree. Whinny again after

a 2-minute pause, fourth animal joins other three. Whinny.

At onset of rain, again the animals whinny to one another.

Ten whinny calls in period of 12 minutes.

SLOW GUTTERAL WHINNY OR SOBS FOR Ateles

fusciceps.—This is prominent during embracing

as well as during feeding.

Example 1: Animal J performing the trill grading to eek

sound at roughly 1 per second. Animal delivers the call with

an open mouth and no tooth exposure. M approaches juvenile who is sitting alone vocalizing (call this the distress call),

male embraces juvenile, as he does so gives a low, gutteral

whinny.

The slow, gutteral sobbing can grade to a long

call intermediate form (see "Mood," p. 46).

Example 2: M and J embrace. As they do so, M gives a

low, gutteral whinny, they break apart; M to bars and gives

a single, low bark (cough) to patrons. J hangs trilling and

twittering. Then M gives a rolling ooo-ooo-aah-aah call or

whoop; J approaches and again they initiate following and

moving away; trill-awk by M; awk-awk-trill by J. The interaction breaks off. J hanging, extends his hand to M; M reaches

out; J jumps at M; they embrace, M gives a slow whinny;

they break apart, trilling by J as he moves away; he hangs

and reaches out; M reaches toward J.

OOK-OOK OR AK-AK SERIES.—Soft ook-ooks are

correlated with play fighting or grappling; this

activity may precede sexual play in newly encoun-
40 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

tering individuals (see "Grappling," p. 12). As

play becomes more aggressive, the sound grades

to the ak-ak form. At high intensity, the call can

grade into growls (see below).

GROWL-ROAR COMPLEX FOR Ateles geoffroyi.—

The growl may terminate aggressive play and lead

into the roar often with a chase by the dominant

animal.

Example 1, growl: Two animals in a tree grappling, ookook sounds grading to growls, finally ending in a roar. They

break apart, a slight chase; one being chased utters low

squeals. Grappling between females or between male and females often accompanied by low ook-ook sound which may

grade to growl.

Example 2, roar: Accompanying a three-way grappling bout

which breaks up. Male approaches group of females. As he

does so, he gives a loud roar.

Example 3: Long roar from male at approach of Cebus.

Another aggressive roar produced by the male Ateles while

chasing a Cebus monkey.

COUGH.—This appears to be a warning sound,

the function of which is poorly understood (Eisenberg and Kuehn, 1966:14). Structurally the cough

resembles a single syllable of a bark. It is produced

in what appears to be conflict situations but it is

of rare occurrence and little data are available to

elucidate its function.

INTERMEDIATE LENGTH LONG CALLS.—The grunttrill or rolling grunt-trill, as defined in Eisenberg

and Kuehn (1966), is much too broad in its original definition and included at least two distinct

vocalization types: (1) the ascending intermediate

call, gnd (2) the grunt-trill-caw combination

which is in reality one possible form of the long

call series. The ascending call or eeah appears to

be given by an animal either at the departure of

a companion or by an isolated animal. The descending form ooah or aah may be a precursor to

a fully developed long call.

LONG, LOUD CALLS.—Several forms of the long

call can be distinguished. They share in common

the fact that they are relatively harmonic in tonal

structure, generally exceed 2 seconds in duration,

are quite loud, and often repeated. In Ateles

fusciceps a long call phrase typically has a terminal

series of grunts termed the "coda." The following

variants are classified on the basis of physical form.

Although the call shows a relatively constant frequency, it may have two subforms: (1) clear,

monotonic where the energy bands are relatively

"pure" in a sonograph, and (2) harsh, monotonic

which shows less tonal purity and superimposition

of more noise. This latter variant of the long call

was referred to in 1966 (Eisenberg and Kuehn,

1966:15) as the caw. Generally only an adult male

or satellite subadult males call when they are with

females. Females do call in the absence of the

male.

Ateles fusciceps (captive contexts): The male

A. fusciceps generally gives long calls while highly

aroused. He may brachiate between bouts. He

called frequently when the juvenile male and one

female were isolated from his group, but also

called on the day they were returned (see "Calling

Frequencies," p. 43).

Example 1: When the male was held alone in a cage, a

long call undulating aa-aaa-awk given as a single call was

given during high excitement.

Example 2: A series of long calls were given at the onset

of rain. It was a prolonged series lasting some 30 minutes

and given in phrases of 4 or 5 syllables. The total duration

of a phrase often exceeded 6 seconds and was given without

reference to any specific stimulation.

Ateles geoffroyi (field contexts): For further

details of contexts for A. geoffroyi long calls, see

"Signals," p. 69.

Example 1, male calling: Male calls with a prolonged aawkaawk-aawk, generally given as a triad, may be given singly,

often while brachiating (Oppenheimer, 1975).

Example 2, female calling: One adult female in B canyon

alone uttering a call: aawk, eeaawk, eeawk, awk, etc., repetitive and harsh sounding (similar to the caw, as well as the

ending of a roar given during a grappling bout that turns

aggressive). Called for about 7 minutes, then crossed to A

canyon; no reply.

Example 3, female calling: Rain appears to be imminent;

sky darkens, wind rises. One female is somewhat isolated

from the group and begins to call: ooo-ooo-ooo in rhythm of

the whinny, ooo-ooo-ooo ooo-ooo-ooo, it has a low plaintive

quality, then the ooo's are terminated with an awk rising at

the end very similar to the intermediate length ascending call

(grunt-trill), then pure aawk calls are given alternating with

eeaawk calls as on a previously noted occasion. (I propose that

the ooo portion has a rhythmic quality like the whinny that

can grade into a grunt-trill type call that may have a terminal

awk and then grade into pure aawks that have a roar quality.) This roaring whoop continues for some time.

Example 4: The eeeoook call, long, moderately high

pitched, caw-like quality, repeated; sound produced by adult

female sitting alone. Others assemble from rest spots and

they move off together.
NUMBE

R 213

41

urren f occ o^2XOVj S<o

•OHall QJ11.- w0

IIIc- ar //a •oA VI. ion Situat;

iaApproach <

IiIiiiiiI XXXX111111111111 friend .. familiar

iiiiiiii Xiiiiiiiiiiiii*Pi

'I

1111111111XXXXXXXX11111111Ling While feed

ing or While feed

iIiiiiiiiii XX1XX11111111tner

ctbO

to a par

Approachir

1

XXXX111•11111

XX i XX i 1111111 111111111imal

"crying"

juvenile

Isolated ani

r avoid Approach o

iI yiiiiiiiiiiiiiiii

iIiBiiiiiiiiiiiiiiiiiiitening

superior

While thre;

iIiiiiiiIiiiiIiii XXXX1111fight Play, mock

iiiiii,iIiiiiiii XX1XXXI11

*5-Aggressive

Prior to

iiiiiiiiiiiiiiiii Xiiiigoiou111111111111111111111XXXedator .. Ground pr<

iIiiiiiiiiiiiii,iiii XXXXXuli Novel stimIIIIIIIiIIIIiIIIIiI XXii:tted) .. . Caught (ne

iIiiiiiiIiiiiIii XXiiiii tack Prior to atiiiiiiiiiiiiiii XX111111o rival .. Approach t

eat During thi

IiI XXX111riiiiiiiiiiiiii displayIiIIIIiiIIIIiI

><IiiiiII|"E

1XX1111111111111111111

J

Fleeing

ioDeparture

iiIiIi XXiIiiiiiiiiiiiii a rival .. .iiIiis•11111111111,1 a friend

Avoiding

IIIIiIi XIIiiIiiii,iiii dominant

iiiiiii XX111111111,1111Play avoid

I
42

SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

•S|CD.tele < ;o tanc

<*> e circut

"XS•Ho,?c.a53 o1. SIIh

3

Sitting tent hrea si ££35 °

enintersnales BeforeHer moving'pa- as a

'raid

cross

•K ° | | *l e o O

Prior

to or

during 1

Initial

\c

alone Eira loth « 5 bus VO lee 8"Cn group 1oc1g£a move t* _c

•*•go3ment s 'I11 type u

1111111I111•11I1. ch-whinny .. Scree _X

iiiIiiiiiii * • 0 0111

entIXX

IIII1I

-

I,

f—4 ( M

041111Whinny ... . or VI

rt

I -* X

1111111111111111•aSque; Xiiii^iiiIiiIiiIIii M

'IV(•

• ••

NM

11111111,1111110 0111cs

IIi . IIIiIiiIIIIIi•scall-hai BOC©B

i

•H1111111111_11sX>—

111111—11|1111111aah aah Aah XI1111111111111111h (caw) Oooa Xi

iiiiii1iiiiiii oo111•aOok-<

i—i

iiiiii!1111111111b

oBarki

iiii,iiiiiiiiiiii X11

to111111111111111

fc

Coug

rhitfi >

11M11,111111111111Eeaw .. XoXiI,iiiiiiiiiiiiii call-pulsed Long
NUMBER 213 43

Klein (1972), in his study of A. belzebuth,

implicates whoops in intertroop encounters and

wails (long call—clear form) as a means of facilitating subgroup mergers.

The foregoing outline of contexts for the various

calls can be summarized in tabular form (Tables

11, 12). For comparative purposes, I have utilized

in Table 11 contexts similar to those employed by

Winter, Ploog, and Latta (1966) for Saimiri.

Although I agree with the preceding authors that

a given call type tends to occur in several contexts,

I feel that certain syllabic forms and certain types

of temporal patterning can be associated with

moods or intentions on the part of the sender.

Within any mood the calls show variations in

intensity and rhythm, which suggest that a range

of arousal patterns can be discerned; that is to

say, a series of "excitation indicators" is discernable within a mood. Transitional call forms then

connect or serve as "bridges" between two motivational tendencies (see "Mood," p. 46).

Frequency of Calling and the

Contexts for Free-ranging Ateles

As indicated previously, the vocalizations for

Ateles geoffroyi were very similar to those produced by Ateles fusciceps. In order to elucidate the

functional significance of the vocalizations for the

captive A. fusciceps, reference is made to homologous vocalizations and their cotexts for A.

geoffroyi.

For the purposes of this analysis, I have selected

13 hours of continuous recording of interactions

broken down into 52 15-minute blocks. Each 15-

minute observation period was balanced with

respect to time of day, so that samples were drawn

throughout the entire activity period of the animals. Ten hours of data were taken during 1964

with an average of 3 animals visible at any one

time. Three hours of data were taken in 1974 with

an average of 7 animals visible at any given time.

Thus, 51 "animal-hours" of data were taken for

183,600 "animal-seconds." During these sample

periods, an attempt was made to record every bout

of vocalizations heard. Since the average observeranimal distance exceeded 20 meters, low amplitude

vocalizations were undoubtedly missed, thus this

sample is biased toward louder vocalizations.

Nevertheless, the data are instructive.

The data can be reported in two ways, either

with respect to the frequency of vocalization types

uttered or the summed durations. Durations were

calculated by multiplying average frequency of

vocalization times average duration as determined

by recording and sonographic techniques. Two

classes of vocalizations required an additional calculation; these were barking and the chorusing

long calls, since both of these types involved the

participation of several animals. In each case, calculations of duration were based on the number

of animals participating in the chorusing behavior.

Whinnies were the most frequently heard vocalizations as indicated in Figure 20; the least frequently heard vocalizations in terms of bouts were

barking and the long call. Agonistic calls were of

infrequent occurrence. The tee-tee and ook-ook

calls were of moderately frequent occurrence.

When we consider, however, the duration of the

calls emitted in terms of animal units, then we see

that one bout of barking occupied more time than

all of the other vocalizations taken together. Similarly, the participation of several animals in long

calls results in a great deal of energy expended

when these calls are given; however, they are

given infrequently. Thus, group calls such as barking or the long calls of males, although of infrequent occurrence, involve considerable expenditure of time when they are given. On the other

hand, whinny calls and tee-tee, although very brief,

are given frequently, but do not account for a very

great percentage of time involved in emission of

calls.

To summarize then, out of the 51 animal-hours

of observation, only 568 seconds of vocalization

were noted, or only three-tenths of 1 percent of

the time did the animals indulge in vocalizations

that were audible to the observer over the range

so noted. This analysis supports the notion that

calls promoting contact in the forest while feeding

(whinny calls) are frequent but do not carry far.

Sounds which carry far (barking and long, loud

calls) are infrequent but of great significance. The

former (barks) are utilized as part of the antipredator mobbing response. The long-loud calls

are distinctive and are related to intertroop encounters and troop assembly (Klein, 1972). They

may be considered as partial analogs of gibbon

calls or the long calls of Alouatta (see "Comparisons," p. 62).
44

SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

u. d=<

w tt o ch g a Lc. b

FIGURE 20.—Frequency and duration of vocalization forms for free-ranging Ateles geoffroyi

(solid line=frequency (f) of vocalization bouts, left ordinate; dotted line=total duration (d) in

seconds of each vocalization type as recorded during the entire sample interval, right ordinate;

w=whinny; tt=tee-tee; o=ook-ook; ch=cough; g=growl; a = long call intermediate length;

r=roar; s=scream; l.c.=long call; b=bark).

Some Calling Frequencies for Captive

Ateles fusciceps

The type of analysis presented in the previous

section for free-ranging Ateles geoffroyi is difficult

to perform in a captive situation, since there is

uncontrolled external disturbance; however, Table

11 presents an indication of the relative frequencies

of various vocalization forms shown throughout a

series of set observation periods. Perhaps of greater

interest will be a consideration of the form and

context of vocalizations shown when the captive

group of Ateles had to be separated during June

of 1973. At this time the group consisted of the

founding father "M," a female of his age class

"V," her son "J" and daughter "B" and an adult

female hand-reared in 1966 and reintroduced to

the group in 1967, "S." During testing for tuberculosis, subadult female B and J were isolated

from the main group, which was on exhibit in an

outside cage. B and J were placed in an inside

cage in auditory contact with the family group,

but visually isolated from them. Upon separation

on 13 June, J proceeded to give a repetitive series

of eee-awk calls interspersed with trills fusing to

chitters. During a sample period of 330 seconds

recording, calls were given by J during 18 percent
NUMBER 213 45

TABLE 13.—Call analysis of separation and reuniting series of Ateles fusciceps

Calls after separation of B and J

from Group VI/13/73; recorded

sample 330 sec

Call forms for J

Eee-awk (or eeet-aaht)

Trill—chitter (or twi twi twi

eee-e)

Calls on VI/14/73 during long call

series by Father "M"—recorded

sample 229 sec

Call forms for M

Long call type II aaaah f vibratto (see appendix I) Number

of phrases: 4; duration of phrases

1.5-5.5 sec; range of interphrase

intervals 2.5-3.5 sec

Call forms for B

Intermediate length long calls

(frequency of calls 21, summed

duration 13 sec) ukauaaakk h f ...

Call form for J

Trill-chitter

Calls on VI/16/73 during reuniting;

recorded sample 270 sec

Call forms for M

Slow whinny, gutteral (sobs) aah

aah ih ah during embrace

Call forms for J

Metallic chitter kkk eeeeet

ah ach aa ee.e k

Energy

(Khz)

D

(sec)

/

(sec)

Average %

Rate of time

(calls/sec) calling

0.1-1.8,2.7-3.8

0.29

0.23

0.75 18

0.2-1.0,1.2-1.8

0.1-1.8,2.7-3.8

1.3-2.5

0.7,1.6,3.0

1.2-3.6

0.90 Var.

0.20 Var. 0.19

0.19

0.06

0.17

0.07

0.02 1

0.05 J

0.41

0.77

5.6

50

58

of the time. B was relatively silent. On the following day, the father, M, initiated a long call series.

The exact amount of calling by the male was

imperfectly quantified, because the calls of subadult female B and juvenile male J were studied

intensively. B tended to respond to the calls of her

father with an intermediate length long call having

a frequency similar to the calls of the male, but a

far shorter temporal patterning. J responded by

an excited series of trills grading to chitters, but

his percentage of time calling during the male's

long call bouts dropped to 5.6 percent. On 16

June 1973, B and J were reunited with the family

and their vocal behavior recorded for 270 seconds.

The adult and subadult females, after greeting

one another with whinnies, settled down immediately; however, the interaction between the adult

male and his son was intense. Essentially, it consisted of repeated approaches on the part of the

adult male, while uttering the slow gutteral

whinny (sobs) and embracing the young male

while the young male alternated between withdrawal and approach to the male, giving intermediate length calls including a metallic pulsed

chitter alternating with an aah aah ee. During

the entire recording session, the adult male was

calling 50 percent of the time and the juvenile 58

percent. These data are summarized in Table 13.

The interpretation of this would be as follows:

Separation induced an extreme anxiety situation

in the juvenile male, who responded by repeatedly

calling in the eee-awk or trill-chitter variant. On
46

SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

FIGURE 21.—Transformation of sobs (gutteral whinny) into a long call by adult male Ateles

fusciceps: a, sobs (slow gutteral whinny), wide band; b, undulating long call derived from a,

narrow band analysis. (Ordinate in Khz, abscissa in seconds).

the following day, the adult male responded to the

absence of part of the group by emitting a long

call series, which was responded to on the part of

the subadult female with intermediate length long

calls. At a lower level of arousal, the juvenile male

exhibited the anxiety separation call. During reuniting the most intense interaction took place

between the adult male and the juvenile male.

The adult male showing embracing and "sobbing;"

the juvenile male alternating between extreme

withdrawal and anxiety and approach touched

with anxiety. This leads us then to the question

of motivation.

MOOD OF THE SENDER

Dynamics

Referring to Table 11, it can be seen that the

true whinny and slow whinny variants are often

tied to feeding and made with reference to group

members. The slow, gutteral whinny (sobs) is made
NUMBER 213

47

OS JO IS 20 10 to 30

DUMTION IN SEC

F^s1^V:r^!; n d syl!

abic simiiarity'a romposite dia^m

 ^^ ^

figures 9, 10, 15, and 17. The discrete call forms (roman numerals, Table 10} are shown with

transitional syllables. Calls beHeved to be indicate of the same general moL^ ^S^ S

face^ncl^ * ^ ^ **** """"

 indiCatC pathw ^ °f

 ^bi T transformation. T^e thret

a long cl u

 A' eXPrCSS1On g l

: C' ex Pressio n durin 8

during friendly approach to a group member. The

tee-tee-tee is made to an approaching group member. It would appear that such highly modulated

sounds reflect a nonhostile mood and function

m greeting and location. Slow whinnies can grade

to long calls, which may be employed in distance

communication of location and facilitate subgroup

encounters in the dense forest (Figure 21).

The twitter, trill, squeaks, and chitter involve

varying degrees of withdrawal or anxiety. They are

associated with the approach of a dominant, loss

of physical support, separation from a partner

withdrawal of a familiar attendant, and, in the

highest form, may accompany an ambivalent

threat display. Glottal tension produces high frequencies, but little rhythmic modulation as in the

preceding class of sounds. At low intensity, the

slow whinny series ties the two moods. During

extreme fright a noisy scream can be produced.

Low frequency, loud, unmodulated sounds appear to be involved in an aggressive, approachprone mood. Ook-ook is a low intensity ritualized

signal, which is rhythmic and tied to play fighting

but, through intergrades, growls or roars agonistic

in character can be produced.

Barks form a graded series, which appear to be
48

SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

TABLE 14.—Some common syllabic transitions*

Call types II Ilia Illb IIIc IV Via VIb Vic VId VII VIII XII

I

II

Ilia

Illb .

IIIc

IV ..

V ....

Via

VIb

Vic

VId

VII

VIII

XII

31

36

21

2

3

2

30

42

31 7

22

2

1

18

78

3

16 42

• Roman numerals refer to call numbers as used in Table 10; sample is drawn from tabulated summaries in Appendix I.

•• Defining interval too long to be described as sequential.

related to the growl series, but may be a highly

ritualized call form indicative of extreme ambivalence coupled with moderately high arousal. Barks

can rarely grade to roars or screams.

The long calls and intermediate long calls are

motivationally puzzling. They may represent high

intensity variants within one of the previously

defined moods. For example, the ascending ee-awk

or grunt-trill may be motivationally related to the

trill series. The loud long calls, however, may be

phylogenetically derived from roars or slow gutteral whinnies (vibratto form and clear form,

respectively), but presently they are ritualized and

seem to have taken on a distance communication

function that could help unite subgroups and repel

neighboring troops (see "Comparisons," p. 62).

The 10 calls as defined on pages 38-42 ("Contexts") are arranged in Figure 22 to portray mood

similarities, transitionals, and excitation changes.

The conceptual scheme parallels that developed

for caviomorph rodents (Eisenberg, 1974), marsupials (Eisenberg, Collins, and Wemmer, 1975),

and insectivores (Gould, 1971).

The existence of syllabic transforms is readily

evident from an inspection of the sonographs in

Figures 15, 17, and 21. The slow gutteral whinny

can serve as preface notes and be converted by

lengthening and maintaining the frequency constant into a long call. The ak-ak variant during

play can be converted to a growl by decreasing

the interval separating the syllables. Growls can

convert to loud roars by increasing amplitude and

prolonging the duration of each individual utterance. Slow chirping whinnies can convert to the

true whinny by fusion of the syllables to form a

continual utterance. These syllabic transformations,

which do not include drastic changes in the form

of the syllable, would appear to indicate excitation extremes within the same mood.

On the other hand, call forms consisting of several syllable types may in fact reflect alternations

in mood. There is no reason to assume that an

animal's prevailing mood is subject to no shift at

all. It is a truism to say that, given the utterance

of a certain syllable type, there is a high probability that the same syllable will follow it. Table

14 illustrates that syllable type Ilia is most often

followed by itself, as is the case with syllable type

IIIc and syllable type V. On the other hand, Ilia

can convert to syllable form IIIc or even to V

through fusion. Syllable type VIII, through fusion,

can convert to syllable type VII. Syllable type VId

can convert to II. These do not involve a necessary

alternation in basic mood.

Alternation, Insertion, and Ambivalence

We have now come to the problem of considering an actual shift in mood during the course of a

session of intense expression. The simplest case

may be taken from the following example: A

group of A teles geofjroyi is barking at an Eira. The

barking response of three of the members of A teles

causes a fourth to approach the tree in which the
NUMBER 213 49

action is taking place. As the fourth animal approaches, one of the barking animals looks up,

sights it, and immediately gives a tee-tee-tee call,

only to return to barking. This is clearly a case of

mood shift (insertion) and a return to a previous

motivational state.

A second example might be taken from the

Ateles fusciceps interaction between the adult male

and the juvenile male in the summer of 1972.

Many of their interactions took on a play-like

quality, which made it difficult to ascribe a specific

mood to the participants. For example, the young

male may show extreme avoidance behavior toward the adult, uttering trill-awks and trills to

chitters. The adult male would approach and look

away, would approach and extend his hand. The

young male would eventually allow himself to be

touched and embraced, and the adult male would

utter slow gutteral whinnies (sobs). Whereupon

the adult male would move rapidly away from the

juvenile male, trilling, giving extended trills, ascending in tone, whereupon the young male

would begin to follow him. This type of mood

alternation has a play-like quality in that the adult

male would begin to exhibit mock "anxiety" behavior toward the juvenile, apparently reinforcing

the juvenile to take upon the role of a pursuer.

Perhaps the best examples of mood shift and

ambivalence during interaction come from my

own experience in handling the adult male Ateles

fusciceps. I could induce him to grapple with me

through the bars of his cage by shaking my head

laterally and uttering soft ook-ook sounds. He

would extend a hand and attempt to grasp mine,

whereupon we would begin a grappling bout.

Nevertheless, he would often alternate between

two tendencies. If I stared directly at him, he

might open his mouth exposing all of his teeth,

squeak, and try to withdraw his hand. At other

times, if I pretended to be weak and allowed him

to draw my arm into the cage, he might change

from the ook-ook to rapid ak-ak and growl and

actually slap at my hand. Clearly I was participating with him in a shift from anxiety on the one

hand to agonistic behavior on the other. In fact, I

could modulate the situation by controlling my

own tendencies to look directly at him while exerting great pressure on his arm or look away and

exhibit weakness in my grip. The same sorts of

interaction could be seen time and again at a

lower intensity level during the "mock fighting"

or grappling session between the adult male and

juvenile male or the juvenile male and subadult

females. These three examples suffice to clarify the

reality of alternation in mood, insertion of an

expressive form within the context of a prevalent

mood, and out-and-out ambivalence resulting from

a conflicting set of motivational tendencies. The

reality of such mood-shifts greatly complicates the

interpretation of the function of various expressive movements and ultimately an understanding

of prevailing mood and the form of expression

associated with it must rely upon the actual responses of the receiver within the social context to

clarify the function of the expression system for

the social context in question.

FUNCTION AND INFLUENCES ON THE RECEIVER

It should be obvious from the preceding section

that auditory signals can impart considerable information to a presumptive receiver. Roars reinforced with a rush promote withdrawal. Trills by

a juvenile stimulate approach and embrace by a

dominant. Whinnies during a rain storm promote

clumping; barks stimulate mobbing; ook-ook plus

a head-shake facilitate grappling (Table 15).

It should also be evident that most close contact

vocalizations involve facial expressions, gestures,

touching, and odors. Obviously a functional analysis of vocalizations requires that the entire "gestalt"

for the receiver be taken into consideration. Table

16 attempts to integrate the sound form with other

signals and specify the functional aspects.

STRUCTURE AND FUNCTIONS OF CALLS

The classical work of Richard Andrew (1963)

demonstrates the possibility of describing the

origins of signal systems in higher mammals, such

as primates, from a consideration of sound production in morphologically conservative species, such

as tree shrews, lorisoids, and lemurs. The key contribution in Andrew's papers concerns the recognition of a graded series of signal types accompanying mood change or alternation of mood in a

sender. Further, Andrew links a graded series of

sound types to rather simple stimulus input

changes, which induce the motivational shift in
50

SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

TABLE 15.—Overt responses to vocalizations*

Call type

Actions by receiver

Vocalizations by receiver Assume Turn to

Move Change Approach attentive Look and Head- _

away position and join posture at "assist" shake Tee-tee Whinny Ook-ook Eee-awk

A teles geoffroyi

(field)

Tee-tee

Whinny

Ook-ook

Low squeak

Growl

Caw (ooo ah-ah) ..

A teles fusciceps

(captive)

Tee-tee

Whinny

Ook-ook

Low squeak

(mother)

Squeak or screech

(infant)

Twitter

Chitter

Growl

Ascending trill

(juvenile)

Long call

1 1

1

1 1

•Low numbers result because only responses which were clearly subsequent to a vocalization without accompanying movements are included; ambiguous cases are not enumerated. All notes used and only frequencies tabulated; data in Table 13

not included.

the presumptive sender. The simplest stimulus

input is the "stimulus contrast situation," where,

regardless of the many qualitative aspects that

might be considered in the stimulus source, attention of the investigator is focused on the shift in

the intensity of the stimulus input, which can be

reflected in the shift of intensity of mood in the

animal by a corresponding shift in the intensity of

signal output. Andrew goes beyond a simple motivational classification. He departs from the classical approach where animal behavior patterns are

related to three fundamental moods: sexual,

aggressive, and fearful. In attempting to describe

the origin of signal systems in mammals, Andrew

(1964) expands the motivational analysis to cover

a wide range of categories including contactseeking, greeting, avoidance, appeasement, feeding. (For a revaluation of this earlier theoretical

position, see Andrew, in Hinde, 1972:179-204).

To my way of thinking the impact of Andrew's

papers includes two fundamental postulates: (1)

Primate vocalizations have resulted from natural

selection to promote effective indicators of mood

shift or changes in arousal within a mood, and (2)

the diversity of syllable types has resulted from

selection on a finite number of basic syllable forms.

An underlying similarity in the structure of

sound types produced by neotropical primates has

been pointed out by Moynihan (1967). It would

appear that the repertoires of different primate

species can be expanded or contracted within any

given functional or motivational class of syllables.

The vocal repertoires of the woolly monkey,

howler monkey, and spider monkey are closely

compared on page 63 (see also Appendix IV).

However, for this section we must only recognize

that it is possible to arrange the vocalizations of

several species of neotropical primates within the

same classification scheme that I have developed

for the spider monkey.
NUMBER 213 51

TABLE 16.—Some calls and associated movements for Ateles

Call type

Frequently

associated expression

Head position

or movements

Other

signal elements Function

Long call (harsh)

Long call (clear) ..

Bark

Chitter

Tee-tee

Whinny

Ook-ook-ak-ak

Gutteral whinny

or sobs

Growl

Various, open mouth

with little tooth

exposure

No tooth exposure;

open mouth

Little or no tooth exposure; mouth open

May be extensive tooth

exposure by lip retraction; mouth often

partially open

No special head movement; tendency to

locomote

Little locomotor

movements

No special movements,

or head position

No special head position

Mouth may be closed Head often lifted

vertically

Mouth may be closed Head often lifted

vertically

Mouth may be open

with pursed lips; no

tooth exposure or

may show pronounced

lip retraction

Lips may be pursed

Head is often shaken

horizontally

Head is lifted vertically

Mouth may be open; lip Gaze is fixated

retraction may not be

pronounced; direct

stare is noticeable

Sounds of shrubbery or

branch movements

No special movements

May involve branchshaking and/or jumps

May involve branchshaking and/or leaps

No special movements

unless signaler is

preparing to depart

No special movements

unless signaler is

preparing to depart

Accompanies grappling

or mock fighting

Often accompanies slow

approach to receiver

No special signal elements, but sender is

often approaching

Position indicator and identifier; mood is confident to

assertive

Position indicator and potential identifier may promote

assembly

Position indicator, promotes

assembly; can serve as a

warning signal

Not specifically a position indicator; focuses attention

of potential receiver on

disturbances in the environment; can serve as a

warning to conspecifics

Position indicator; nonhostile

greeting

Position indicator; nonhostile

greeting; accompanies feeding, may serve to indicate

availability of food

Indicator of arousal level;

may function as an invitation to play

Signifies nonhostile approach,

may accompany an embrace

Signal indicates a hostile approach

If we turn to the woolly monkey, Lagothrix, as

described by Williams (1968), then in a contextual

sense and in a morphological sense, the "eeolk"

series of Lagothrix is directly comparable to the

whinny series of Ateles. Tuff-tuff, oo, and hu-hu

are comparable to the ook-ook, ak-ak growl series.

Nyonk, argh, yook-yook are comparable to the

Ateles bark series. Squeaks and screams are comparable to the twitter, chitter, scream series of

A teles.

A small species, such as Saimiri sciureus, has a

rapid temporal patterning in the delivery of its

syllables. In addition, the pitch of most syllables

is higher than that shown by Ateles or Lagothrix.

Yet if we slow the vocalization down by half speed

during playback on a tape recorder, many calls

sound very much like the calls of Ateles. With

this compensation in mind, then in the Winter,

Ploog, and Latta (1966) classification for Saimiri,

the peep, twitter, trill, and chirp are comparable

to the Ateles whinny series; the play peep, err-arr,

are comparable to the ook-ook, ak-ak series; the

yap series is functionally equivalent to the bark.

Cackle, arr, and keeker are comparable to the

growl-roar series of Ateles.

The comparison of Ateles, Saimiri, and Lagothrix suggests that similar physiological mechanisms underlie the expression of these calls and that

the calls reflect a common evolutionary history,

but the form of a call not only reflects its evolutionary history, but also the selective influences

that have shaped the call in the species microenvironment. Marler (1957) has pointed out that

the warning cries of many Passeriform birds have a
52

SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

remarkable structural similarity. Without attempting to investigate the question of similarity in

structure as a function of relatedness or homology,

Marler approaches the structure of sounds from a

functional standpoint. Obviously the warning cries

of Passeriform birds are functional analogs, indeed the sound form allows an individual to give a

warning cry to conspecifics, but minimizes its vulnerability to predation since the sound can be

localized only with great difficulty. Similarly, sounds

that are repetitive, low frequency pulses having a

clear onset and ending permit a maximum possibility for localization on the part of a receiver;

such sounds are employed in mobbing vocalizations by birds. By a similar application of logic, one

can also conclude that barks and short grunts may

be used to indicate the position of a sender and

thus, in mobbing responses in primates, the bark

is a functional analog across species (Marler, 1973).

Morton (1970) presents some evidence from the

analysis of bird song suggesting that the environment in which the vocalization is produced and

the function for which it is intended put constraints on the form of vocalization which the animal may exhibit. Following on early suggestions

by Moynihan (1964:51-52), Morton points out

that the transmission of sound differs significantly

when forest conditions are compared with those

of the savanna. Obviously within the physical limitations of the animal, the lower the frequency

sound produced in the forest the better its propagation will be, since the foliage and trunks act as

absorbers of high frequency sound energy. Morton's research suggests that birds which call in the

lower parts of the forest call with a narrow range

of frequencies with an average of 2.2 Khz. This

can be contrasted with grassland singing birds,

which sing with an average frequency of 4.5 Khz

and a much wider frequency range. It would seem,

then, that loud, long calls of primates in the forest,

.which function to either communicate with conspecifics over a great distance to promote contact

or are used to repel close approach by neighboring

troops, tend to emphasize lower frequencies. In

the case of the loud, long calls of A teles, the frequencies emphasized conform to the model

proposed by Morton. Further consideration of

these factors are taken up on pp. 62-64 ("Comparisons").

Ontogeny of Behavior in Spider Monkeys

Since 1966, four (1 male and 3 females) A.

fusciceps infants were hand-reared. Three of these

specimens were studied in some detail with special

attention given to growth and motor development.

Of these, two (one male and one female) were

selected for special recording of vocalizations at

selected intervals during their maturation. Details

concerning hand rearing are included in Appendix

II. Of the four specimens hand-raised, one was

removed from the mother after an interval of less

than 8 hours, two specimens were removed at

intervals less than 48 hours following birth, while

the fourth animal was removed after some 7 days

with the mother. Two subjects were raised alone

and the other two raised together.

During hand-rearing the young animals were

unable to hear or see adult animals. They were

not deprived of sensory input, however, and interacted with the individuals rearing them. Thus, any

inferences concerning the development of vocalizations and expressive movements do not refer to

animals in any way deprived of sensory input;

however, we feel that three of the individuals

studied certainly had a minimal exposure to the

vocalizations of adults and the associated expressive

movements. It seems reasonable to assume that

TABLE 17.—Ages when removed from mother

Subject*

1 9

2 S

3 9

4 9

Date born Date removed Age at removal

26 Apr 1966

6 Aug 1966

25 Nov 1969

25 Feb 1973

28 Apr 1966

8 Aug 1966

25 Nov 1969

13 Mar 1973

<48 hours

<48 hours

8 hours

16 days

• Animals 1 and 2 raised together from 8 August 1966; Animals 3 and 4 raised alone.
NUMBER 213 53

imitative learning is ruled out as a possible source

of information to these hand-reared individuals.

Table 17 summarizes the foregoing information.

As a control, the maturation of behavior was

studied by observing two (one male and one female) young who were mother-raised in the captive group. These data, where appropriate, will be

compared with observations on hand-reared

animals. In addition, data obtained from observing

mother-reared young of A teles geoffroyi on Barro

Colorado Island will be introduced.

Condition at Birth and during

First Weeks of Life

At birth, the young of A. fusciceps weigh slightly

less than 500 grams, incisors are present and the

first premolars in both the upper and lower jaw

are visible through the gums. The grasping reflex

is well developed and the tail shows some prehensile ability. The face and ears are pink and this

flesh coloring is retained until over 14 months of

age. The face gradually becomes pigmented, but

the skin around the eyes can still be pink at 19

months of age. They are covered with black hair,

especially prominent on the dorsum. The ventrum

is only sparsely haired. The ventrum of the torso

shows pink skin with little evidence of pigment

as does the underside of the tail. The mid-dorsum

of the back likewise shows little pigment in the

skin, however, the lateral aspects of the dorsum,

as well as the dorsal parts of the hind and fore

limbs, are pigmented with black. The dorsum of

the tail is sparsely haired and the skin is visible.

The clitoris in the infant female may be 40 mm

in length. The testes are undescended in the young

male. The neonate can produce soft cluck-like

chuckles when lightly tickled and a loud squawk

in response to sudden stimulus contrast.

At two weeks of age, the young animal will try

to avoid noxious stimuli by turning its head away.

It will push objects away from its vicinity using its

hand; its tail will readily support its entire weight.

Vocalizations include a well-defined chuckle, cluckawk, and squawk. The chuckle seems to be produced when the animal is attempting to obtain

something (e.g., food) that is being withheld from

it. The squawk vocalization is produced when the

T600

1600

1500

1400

1300

1200

1100

1000

900

800

700

600

500

500

400

300

200

100

8

FIGURE 23.—Growth of infant Ateles fusciceps during the first

eight months of life. (Ordinate, left, weight in grams, solid

line; ordinate, right, tail length in millimeters, dashed line;

lower growth curve represents growth of A. paniscus as

reported by Gensch, 1965.)

Subject

1

2

Sex

$

9

TABLE

Age*

(day)

18

17

18.—Physical data of

f i i2 Pmr

erupted subcutaneous

erupted subcutaneous

infant

Arm

span

(mm)

369

481

Ateles fusciceps

Tail

(mm)

258

245

Skull

diameter

(mm)

220

190

Torso

(mm)

150

160

Weight

(gm)

720

534"

• When first measured.

••Dehydrated.

Note: Clitoris may be 40 mm at birth.

i = incisor; Pm = premolar.
54 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

animal is disturbed or when it is removed from

the handler. The premolars have still not emerged

from the gums.

In mother-reared animals, the young at this age

clings almost exclusively to the mother's ventrum.

The mother will support the infant with one hand

while climbing, although the infant is able to cling

to the mother without any support. Measurements

of young between 2 and 3 weeks of age are presented in Table 18, and a growth curve during the

first 8 months of development is presented in

Figure 23.

Between 8 and 9 weeks of age, the animals will

begin to show a chin-up with pursed lips toward

the handler. The whinny vocalization (or precursor of the whinny) is uttered at this time. Interest

in the environment around the infant increases.

It begins to pick up objects and sniff them. At

roughly 10 weeks of age, the animals can hang

independently by their tails while manipulating

objects and they begin to show increasing self care;

scratching with the hindleg begins to be demonstrated at 9 weeks of age. At 3 months of age, the

animals are hanging by their tails, playing with

one another, demonstrating the head-shake to one

another, and the vocal repertoire has expanded

greatly. High-pitched trills may be given during

thwarting situations.

The common vocal repertoire developed at 3

months of age and accompanying expressive movements may be summarized as follows: When held

by an attendant and tickled or stroked, the animal

may emit short grunts or brief grunts in a .series

(chuckles) with the lips either tightly closed or

slightly open (see Figure 24). If the animal is

handed to an unfamiliar person or approached

by a stranger, it may show a slightly open mouth

and emit a squawk or a high-pitched chirp, which

grades to a squeak. These vocalizations may be

repetitive. If the young animal has something

forcibly removed from it, such as food or a blanket,

then with an open mouth it may give a loud ee

aw, which shows a slight shift in pitch, and we

believe this to be a precursor to the chitter in the

adult. Continued deprivation of a desired object

can lead to a shriek or a series of grunts which

fuse to rise to a shrieking cry (Figure 25).

During the fourth and fifth months, interactive

play increases. A rhythmic grunting or precursor

of the adult ook-ook with head-shakes may be

demonstrated. In mother-reared animals, the youngster now may move several feet away from the

mother, climbing alone. There is an increased

tendency to climb on the mother's back. Most of

the adult vocalizations can be recognized at 5 to 7

months of age.

FIGURE 24.—Some infant calls for Ateles fusciceps: a, chuckle series or ook-ook precursor, 14 days

of age; b, ee ah call, 14 days of age. (Ordinate in Khz, abscissa in seconds.)
FIGURE 25.—Some ee-aw variants (squawks) by infant Ateles fusciceps.

(Ordinate in Khz, abscissa in seconds.)

Later Stages of Development

Figure 26 indicates a growth curve for Ateles

fusciceps. This is based on the growth of two females through the seventh year of age and one

male up to 4i/2 years of age. As can be seen the

growth of males and females remain quite similar

until 3i/2 years of age, when the male shows an

increased rate of growth relative to the female.

Ateles fusciceps is a dimorphic species, the male

averaging 1i/2 kg greater in weight than the female

and being somewhat longer. Head and body measurements of one male exceeded the largest adult

Kg

12

II

10

9

8

7

6

5

4

3

2

7 Yrs

female by 40 mm (Kellogg and Goldman, 1944).

Ateles fusciceps development may be broken

down into the following age classes: Infant-1, 1 to

4 months of age. Almost all nutrition derived from

the mother, tendency to hang to the mother's ventrum, little tendency to leave mother or break

contact.

Infant-2, approximately 5 to 12 months of age.

At the end of this period, the youngster weighs

approximately 2 kg. During this time interactive

play with like-aged animals and increasing inde100

80

60

40

20

1

FIGURE 26.—Growth records over a seven year period for one

male and two female Ateles fusciceps.

FIGURE 27.—Changing amount of time the infant Ateles fusciceps spends clinging to the mother. Data averaged only for

daylight hours; infants and juveniles sleep with the mother

until over one year of age. (Ordinate is percent of time

infant is off the mother—infant is almost always near the

mother; abscissa is age in months.)
56

SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

FIGURE 28.—The mother-infant unit in Ateles geoffroyi. (Photo by C. M. Hladik.)

pendent movement from the mother manifest

themselves. Most of the expressive movements and

vocalizations are employed at this time in social

interactions. Youngster still returns to female for

nursing, tends to ride on the back of the female

(see Figures 27, 28).

Juvenile-1, 12 to 24 months of age. Growth is

very rapid and the young animal may reach onehalf of the adult weight. It is much more independent in its movements from the female. During

this period weaning takes place, perhaps as early

as 14 months, but intermittent suckling may continue until 18 months of age. Youngster tends to

sleep with the mother.
NUMBER 213 57

Juvenile-2, approximately 24 to 36 months of

age. Growth begins to slow down. Females and

males still growing at approximately the same rate.

At the end of the 3-year period, the animal may

be three-fourths the weight of the adult. Behavioral differences between males and females are

evident during this life phase. Males begin to show

increasing affiliation with the adult male and

other subadult males. The young male may participate in "male activities." It will join the adult

male in his movements and may participate in the

long calls. Females, on the other hand, within the

Juvenile-2 age class remain bound into the core

mother group, although they may tend to move

independently.

Subadult female, 3 to 4 years of age. Females

still show some juvenile characteristics including

participation in grappling bouts with each other

and with males. First estrous cycles may perhaps

be shown at the middle of this phase. Earliest

conception in captivity by A. fusciceps was at 4i/£

years of age.

Subadult male, 4 to 5 years of age. Males begin

to show an increased rate of growth relative to

females. Earliest age of successful insemination

for a subadult male was at 4 years, 9 months. The

subadult male is as large as an adult female at the

end of the fifth year, and may be almost indistinguishable from the adult male, but apparently

continues to grow well into the fifth year of age.

Although I do not have a growth curve for A.

geoffroyi panamensis on Barro Colorado Island,

its chronology of devleopment is very similar to

that for Ateles fusciceps and the major difference

concerns the condition of the young at birth.

Young A. geoffroyi are born entirely black and the

reddish pattern on the dorsum does not begin to

manifest itself until about 5 months of age. This

feature then defines a transition to the Infant-2

class. Infant-2 animals from about 6 to 12 months

of age show the adult color pattern. The young

now ride on the back of the mother and only go to

her venter to nurse. At approximately 12 months

of age, the youngster may move as much as 17

meters away from the mother. Youngsters from 6

to 12 months of age show a great deal of interactive play with one another and feeding on solids

increases.

During the Juvenile-1 age class, young males

are singled out for special attention on the part of

subadult and adult males; thus, the transition to

Juvenile-2 is facilitated by the increasing attention

on the part of males toward juvenile males.

Subadult females, from about 3 to 4i/£ years of

age, still show some juvenile behaviors; they

grapple and their first estrous cycles may be shown

at the end of this phase. Females of A. geoffroyi

appear to conceive in Panama at about 4 to 4i/£

years of age. An adult female generally has her

first infant during the early part of her fifth year.

Subadult A. geoffroyi males are almost fully

grown at 5 years of age. At this time they show

participation in all the male activities; they are

part of a male subgroup. They may subtly challenge the Alpha male for a dominance position

and may be increasingly involved in dominance

contests with some of the subadult or adult females.

The adult male at 5 years of age generally exhibits

features of male behavior including initiation of

long call choruses and some leadership role with

respect to extended group movements. At this age,

he may display frequently, including chest rubbing.

The secretory activity of the pectoral glands is

markedly increased during the last year and a half.

Although capable of fertilizing females, he may

not be sociologically dominant unless he achieves

ascendency over the current male leader.

Development of Expressive Movements

and Vocalizations

Expressive movements, such as chin-up, pursed

lips, relaxed open mouth, open mouth with tooth

exposure, and retracted mouth corners, all appear

to develop without imitative practice and to be

displayed in appropriate contexts. Although the

vocalizations of infants and juveniles differ from

those of adults with respect to intensity and distribution of frequencies, they show great similarities

in their morphology. In their temporal patterning,

the sounds suggest homologs with adult calls. Such

vocalizations appear to develop without imitative

practice, and once again be displayed in appropriate contexts.

Vocalizations for infants, between 5 and 6

months of age, show the following relationships

to the vocalizations of adults: (1) Series of repetitive grunts with varying emphasis on frequencies

that are basically derived from a click form are

homologous with adult ook-ook and specific to a
58 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

ook ook,

growl

.OS .10 JS .20 25 1.0 2.0 50

trill^squeek,

chitter

JO 20 >.5O

whinney series

.10 jS .10 .15- l.o Z.0 Jo

FICURE 29.—Temporal patterning of young A teles vocalizations. Three vocalization forms are

portrayed for isolate reared AteUs at 8-11 months of age. The values for the young animals are

contrasted with a sample from group-raised adults and juveniles.

• isolate-raised # group-raised

grappling context. (2) Chirp-like calls composed

of different syllable types may be a sliding chirp

or a whistle, but invariably they are given as a

series and in situations where the animal is insecure and is perhaps seeking contact; they are

related to twitter-trill series of adults. (3) Squawk,

with two variants, is a high pitched or low pitched

call, noisy and loud, sounding like an aak or awk,

given in frustrating situations. It may be higher

pitched when the animal is somewhat frightened
NUMBER 213 59

and thwarted. The syllables are similar to those

produced by adults when emitting the intermediate

length calls. (4) Separation call of young, eee-awk,

which is produced when seeking contact after

forcible separation from partner or handler. It is

an ascending long loud call. Frequencies are concentrated around 1 Khz and it exceeds 0.5 seconds

in duration. Perhaps it is related to ee-awk of the

adult. (5) Chirrup call, repetitive; homologous

to the whinny series of adults.

The calls of the young appear to differentiate

out of fundamental elements demonstrated by

the infants within their first 2 weeks of life. Frequency and amplitude modulation appear to

develop without imitative practice. Homologous

calls for isolation-reared infants and group-reared

infants are compared in Appendix III with respect

to various physical parameters. These infant and

juvenile calls are then again compared with adult

homologs in Figure 29. It would appear that with

a minimum of environmental feed-back, young

spider monkeys can develop a vocal repertoire

similar to that of group-raised counterparts. Unfortunately, analyses of the long loud calls produced by adults have not been made on isolatereared animals, since all hand-reared animals were

eventually returned to mother-reared animals or

to their original mother after 12 to 14 months of

separation. It is entirely possible that some modulation and context specificity is learned from older

adults, especially by young males when they participate in chorusing behavior with adult males (see

"Contexts," p. 69).

Winter, et al., (1973) studied the development

of vocalizations in Saimiri under conditions of

extreme acoustic isolation including the deafening

of one subject. The vocal repertoires of the experimental animals were virtually identical to the

normal subjects. His evidence is supportive of our

findings. Newman and Symes (1974) found that

Macaca mulatta infants raised in acoustic isolation

showed some structural modification in their clear

calls, but most other calls appeared structurally

normal. The conclusion then that many primate

species develop species typical calls without imitative learning seems unavoidable.

Comparisons of Ceboid Communication Systems

Introduction

The Callithricidae and Cebidae comprise the

two living families of neotropical primates which

underwent an adaptive radiation in the neotropics

in isolation from similar radiations of continental

Old World primate stock giving rise to the families

Cercopithecidae, Pongidae, and Hylobatidae. The

existence of the Ceboidea allows for fruitful comparisons with their Old World counterparts in

order to elucidate questions concerning convergent

and parallel evolution. Andrew (1963, 1964)

pioneered in the analysis of primate vocalizations

and expressions. He proposed an evolutionary sequence for vocalizations and defined fundamental

syllable types.

Moynihan (1967) and Oppenheimer (1975)

have called attention to the fundamental unity of

the New World primates with respect to certain

communication mechanisms. In this section, I

would like to expand on Moynihan's earlier ideas

by comparing some displays and, in particular,

closely comparing vocalization forms. The author

regrets that he was unable to include the excellent

analysis of Miopithecus vocalization by J.-P. Gautier

(1974) in this discussion. The publication arrived

after submission of this study to the press.

In any comparison, the question of homology

immediately arises. The determination of homologies has been given a rigorous theoretical treatment by Wickler (1961). The special difficulties

encountered in establishing homologies among

vocalizations of closely related species are reviewed

for marsupials (Eisenberg, Collins, and Wemmer,

1975) and caviomorph rodents (Eisenberg, 1974).

There are several examples of sound types produced by closely related forms which are nonhomologous. For example, click sounds produced by

tooth-chattering may sound almost identical to

clicks produced by short expirations. Yet clearly,

because different physiological mechanisms underlie

their production, these sounds must be considered

nonhomologous, but, if functionally similar then

they are functional analogs (Eisenberg, Collins,
60 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

and Wemmer, 1975). On the other hand, it is

probably safe to assume that two sound forms are

homologs when they are nearly identical structurally or, if they differ, intermediate forms can be

found linking the two sounds. Overall pitch of

the sound may not be an indicator of homology,

but rather similarities in discrete syllable structure

and temporal patterning may reflect homologous

neuromuscular mechanisms employed in the production of the sound type. For this section, the

question of behavioral homologs is of less interest

than the description of functional analogs and,

thus, the question of homology will not be stressed.

Rather, we will discuss behavior patterns that

seem to have identical functions, highlighting those

behavior patterns that appear to be homologs.

In order to expand the discussion in this section,

comparisons will be made relying heavily on previous studies. The display repertoires for Callicebus,

Aotus, and Saguinus oedipus geoffroyi were described in the series of publications by Moynihan

(1964, 1966, 1970). Alouatta has been described by

Carpenter (1934) and Altmann (1959). Cebus

capucinus was treated by Oppenheimer (1968)

and C. nigrivittatus by Oppenheimer in 1974.

Saimiri sciureus has been rigorously studied by

Winter, Ploog, and Latta (1966), Winter (1972),

Ploog, Hopf, and Winter (1967), and others (e.g.,

Rosenblum and Cooper, editors, 1968). Epple

(1967, 1968, 1975) has summarized the displays of

the Callithricidae. In the remainder of the discussion, I will draw upon the series of observations

presented by the preceding authors and include

previously unpublished data from observations on

ceboids at the National Zoological Park. These

data include observations on Alouatta palliata,

Lagothrix lagotricha, and Saguinus oedipus geoffroyi (Muckenhirn, 1966, 1967). These first two

species were studied intensively in captivity by

Ms. L. McLanahan (see Appendix IV).

Nonauditory Signal Systems

POSTURES, EXPRESSIONS, AND MOVEMENTS

The arch back posture assumed in a quadrupedal stance has been carefully described for Aotus

trivirgatus (Moynihan, 1964) and for Cebuella

pygmaea (Christen, 1964). As Moynihan mentions,

this posture is also shown in a similar form by

Callicebus torquatus and several of the marmoset

species, including Callithrix geoffroyi (Muckenhirn, 1967, Moynihan, 1970). Moynihan (1967)

also notes the occurrence of the quadrupedal arch

posture in Alouatta palliata. Our observations at

the National Zoological Park confirm the scheme

as outlined by Moynihan. A modified form of the

arch may be shown while the animals are bipedal.

These arch postures are not shown in a ritualized

form by either Lagothrix or A teles (Appendix IV).

Tongue protrusion, during male-female interaction, is commonly displayed by Saguinus, Callithrix, Leontopithecus, Aotus, and Alouatta, but

ritualized tongue protrusion is not demonstrable

in Lagothrix and A teles. Lagothrix has a unique

expression during sexual behavior, which involves

lip retraction, rapid jaw movements, and some

tongue movements. This so-called lip smacking is

reminiscent of a similar expression shown by the

genus Macaca (Appendix IV).

Table 19 summarizes the foregoing, as well as

aspects of display and movement patterns shown

by the better studied species of ceboids. It is evident

that Alouatta shares some aspects of display with

Aotus, Saguinus, Callicebus, and Callithrix. Lagothrix and A teles, on the other hand, appear to be

somewhat distinct by the absence of tongue protrusion and the arch posture.

MARKING BEHAVIORS

Most of the ceboids possess specialized glands

in association with the genitalia, as well as a chest

gland. The morphology of the so-called sternal

gland has been reviewed by Epple and Lorenz

(1967). Although the movement patterns involved

in scent deposition vary within the Ceboidea, the

deposition of secretions from the chest gland on

various objects in the environment is common to

all members. Ateles and Lagothrix appear to have

reduced gland fields in association with the genitalia and do not exhibit anogenital rubbing movements in as ritualized a fashion as those movements

shown by Aotus, Saguinus, and Callithrix (Oppenheimer, 1975).

PENILE DISPLAYS

The penile display of Saimiri sciureus has been

described by Ploog and MacLean (1963). Although
NUMBER 213 61

TABLE 19.—Expressive movements or postures for the Ceboidea

Species

Quadrupedal

arch

Bipedal

arch

Chin up

& stare

Chest rub

(object)

Chest rub

(self)

Jaw movement ir

lip smack

Tongue

protrusion

Callithrix geoffroyi ..

Saguinus oedipus

Alouatta palliata

Lagothrix lagotricha

Ateles fusciceps

m

m

m = modified and no longer comparable with other species; + = behavioral pattern demonstrated; - = behavioral pattern

not noted.

no comparable ritualization has been described for

other species of ceboids, certainly the presence of

an erection excites great interest on the part of

females and juveniles in Ateles. Although genital

display in Ateles is not comparable in its degree

of ritualization to that shown in Saimiri, the behavior is noteworthy (see "Genital Display," p. 14,

for a more complete discussion).

GROOMING

Patterns of grooming, as we understand them

for the Ceboidea, are summarized by Oppenheimer

(1975). Compared with cercopithecid primates,

the proportion of allogrooming displayed by

ceboids appears to be somewhat lower. Grooming

in Lagothrix and Ateles appears to be strongly

associated with estrus in the female and also in

mother-infant dyads.

EMBRACING

Embracing as a mechanism of bond reinforcement is frequently shown in all the ceboids, but

the degree of embracing and mutual sternal gland

sniffing seems to reach a high frequency in Lagothrix and Ateles. Special vocalizations accompanying embracing, such as sobbing, or the slow whinny,

are characteristic for Lagothrix and Ateles.

PATTERNS OF SEXUAL BEHAVIOR

Data concerning mating behavior in ceboid primates is sparse, but what data we have would

indicate some interesting divergences. The temporal patterning of copulation has been only

sporadically studied. Carpenter (1934, 1965) found

that the howler monkey, Alouatta palliata, is characterized by short copulations with continuous

thrusting during intromission. A copulation bout

averages some 22 seconds in duration. Similarly,

the squirrel monkey, Saimiri sciureus, exhibits a

series of mounts with intromission and thrusting.

Multiple ejaculations can occur, and the duration

of intromission is comparable to that of Alouatta

(Clewe, 1969; Latta, Hopf, and Ploog, 1967).

Copulation in Saguinus oediups and Leontopithecus rosalis again appears to involve multiple

mounts with intromission and a brief mount duration (Epple, 1975; Kleiman, pers. coram.). Mounting, intromission, and duration of copulation in

Lagothrix involves postures similar to those of

Ateles. The male hooks his hindlegs over the thighs

of the female while she reclines forward or upright on a branch or bench. Intromission can exceed 4 minutes (Appendix IV). Ateles is characterized by a long intromission with thrusting, but

no multiple intromissions. It is as if Ateles achieves

the same amount of female stimulation by a single

long intromission as is accomplished by the other

species with a multiple intromission system. Details

on the temporal patterning of copulation in Ateles

have been published by Klein (1971) and Eisenberg (1973).

The peculiar copulation posture of Ateles and

Lagothrix with the male sitting down may be an

adaptation to prolonged intromissions in an

arboreal situation. More conventional mounting

with the female standing quadrupedally as in

Saguinus or Cebus may be possible arboreally if

the male's mount is brief. The long mount of

Ateles and Lagothrix may in some manner correlate with an anatomical peculiarity of the Atelinae,

namely the absence of an os penis (Hill, 1962:

163). In this respect the Atelinae resemble the
62 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

perissodactylans, which have no baculum and exhibit prolonged foreplay and mount durations

when they are contrasted with the Artiodactyla.

Comparisons of Vocalizations

Although the smaller ceboid primates tend to

have a great many high pitched vocalizations and,

further, their rhythm of delivery often is somewhat

faster than that of the larger ceboids, the overall

temporal patterning appears to show remarkable

similarities (Oppenheimer, 1975). This similarity

can be enhanced by playing back tape recordings

of the smaller species at one-half or one-fourth

the normal recording speed. It is as if the whole

temporal patterning of Saguinus or Saimiri is from

four to five times faster than the patterning shown

by Ateles, Alouatta, and Lagothrix. This evidence

is strongly indicative of underlying, homologous

neuromuscular mechanisms. Table 20 compares

those species of ceboid primates for which we have

data with respect to the form of vocalizations occurring in selected functional contexts. As can be

seen from an inspection of the table, play-fighting

tends to be accompanied by rhythmic vocalizations

exhibiting a blurred harmonic structure. Antipredator calls leading to mobbing generally

involve the production of rhythmic calls; the sylFICURE SO.—Classic E-olk! call by Lagothrix lagotricha. Note modulation similar to tee-tee of

Ateles. (Ordinate in Khz, abscissa in seconds.)

FIGURE SI.—Some vocalizations of Alouatta palliata (narrow band analysis). Undulating roar or

long call by male Alouatta palliata. Fundamental energy is 0.4 Khz (apparent fundamental is

background noise). Note the slight modulation at around 1.65 seconds. (Ordinate in Khz,

abscissa in seconds.)
NUMBER 213 63

bo g —.

111

3 .3 O

t#> O

3

 1I

2 v e ""

g

rt C41

^ 3

8.

a,

O

^j o

£ .S'a

o "S C bp

bou ^ g

^

o

snot uck

Si

O

c

1

1rt

rt. rt. ^

beblir Gob

rt

,2 «. i—i cu

P! «

W W w5 Z

e 4 o<i 5r> •<«<

ti £~ *rt

U S h

i ti^ S it *

"B I "g

bo „ 8 -S

 rt

•S . g * S S G

•g fe u .s j3 ^j «

-e, u iJ « ^3 H

o >< o i O
64 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

lables are uttered in long sequences with a clear

onset and termination of each individual syllable.

These mobbing calls tend to be loud. Sounds produced in situations involving submission or slight

withdrawal tend to be high pitched twitters. A

graded series is shown under conditions of extreme

fright; such sounds fuse to produce noisy screams

with emphasis on higher frequencies. Feeding calls

tend to be clear in their harmonic structure and

show a great deal of frequency modulation (Figure

30). Agonistic sounds tend to be unharmonic and

loud.

Long calls involved in contact over a great distance tend to be loud with long duration syllables;

such calls involved in maintaining contact among

troop members tend to be clearer in syllable

structure. Those long calls involved in intertroop

encounters and displays tend to show a more

blurred harmonic structure (Figure 31).

Clearly some of these similarities may indicate

homologous neuromuscular mechanisms in the

production of the sound itself. However, it is

important to point out that structural similarities

in calls may equally well be the result of environmental pressures setting limits on variability in

the call form whenever the specific function of the

call necessitates clarity in transmission. The long

loud calls of primates used to communicate location and identity over reasonable distances in the

forest are a case in point (Oppenheimer, 1975).

Propagation of sound in the forest is severely interfered with by the presence of trees, which serve as

sound absorbers. A low frequency sound, all things

being equal, has the best propagation over distance, but in the forest the physical structure of

the forest itself may force primate species to a

more restricted frequency band than would be the

case in more open environments. Such an hypothesis was explored by Morton (1975) in an

analysis of the calls of Panamanian passeriform

birds. By comparing the frequencies employed in

the songs of various bird species, Morton concluded

that forest birds were under more environmental

restriction in that they produced songs having a

narrower range of frequency distribution than did

their grassland and forest-edge counterparts.

Figure 32 portrays the frequencies emphasized

in the syllables produced by seven primate species.

The graph has been prepared in such a way that

the size of the species is taken into consideration.

The question may well be raised, if a smaller primate species such as Saguinns might not be incapable of producing low frequency sounds. An inspection of the figure will indicate that Saguinus

geoffroyi does in fact produce higher pitched

sounds than does the larger A teles fusciceps. Nevertheless, the range of frequencies emphasized is very

broad for Saguinus; so it is evident that this species

is quite capable of producing low frequency sounds.

The correlation that emerges from an inspection

of the graph is that the larger primate species have

a more restricted range of sound production or,

in general, tend to produce syllables that emphasize lower frequencies than do the smaller ceboid

species. The long distance calls for all of the forest

dwelling primate species, with the exception of

Saguinus and Cebuella, appear to fall within the

range of 0.4 to 1.5 Khz. Lagothrix is somewhat

exceptional in that its complex long call repertoire

tends to emphasize frequencies up to 2.5 Khz as

well as at 1.5 (Appendix IV).

Although Saguinus geoffroyi shows the greatest

range of frequencies emitted in its syllables, its

long calls consistently show emphasis of energies

at 3.5 Khz. In Morton's study of avian song, he

found that forest-edge birds and grassland birds

sang with average frequencies at 4 to 4.3 Khz. If

Saguinus geoffroyi is a forest-edge or second

growth adapted form, as suggested by Moynihan

(1970:2-3), then perhaps its higher pitched, long

calls show a relaxation of selective pressure when

compared with mature forest dwellers, such as

Callicebus, Aotus, Cebus, Lagothrix, Ateles, and

Alouatta. On the other hand, the use of higher

frequencies for long loud calls in Saguinus may

be related to its small size, in that, it is more difficult to produce the requisite amplitude in a low

frequency loud call. The series of long loud calls

discussed here for the Cebidae may not reflect true

homologs in all cases, but, if they do, they surely

also reflect a similarity in environmental selection,

producing call types having frequencies consistent

with long distance communication.

In spite of the similarity in the frequencies

utilized for long ranging calls, the temporal patterning of such calls renders them completely

distinct and species specificity is retained by making use of such temporal parameters. Callicebus

calls tend to resemble the gobbling of turkeys. The

hooting call of Aotus is distinct from the ara call
NUMBER 213 65

1 U U

 200 300 360 360 400 _ 500 600

S Ca Ao Ce L At Al

FIGURE 32.—Correlation of body size and frequencies employed in ceboid vocalizations (analyzed

to 15 Khz only). (Shaded portion = infant and juvenile calls; <-= frequencies emphasized in

long, loud calls; ordinate in Khz, abscissa in average mm of head-body length; small scale at the

top of each species' axis=number of calls utilizing a given frequency; S = Saguinus oedipus

geoffroyi (Muckenhirn, 1967; Moynihan, 1970), CA = Callicebus (Moynihan, 1966), Ao=Aotus

(Moynihan, 1964), Ce = Cebus (Oppenheimer, 1968), L=Lagothrix (see Appendix IV), At=Ateles

(see Appendix I), Al=Alouatta (see Appendix IV); avian singing ranges (from Morton, 1970):

Fe = forest edge, G= grassland, Fh = high in forest, Fl = low in forest.)

of Cebus. Lagothrix has an exceedingly complex

long call employing a wide range of syllable types,

but having a patterning similar to barking mixed

with long syllables. A teles employs long syllables

with terminals and Alouatta resembles Ateles in

its temporal patterning, but the sound quality is

entirely different and the amplitude is much

greater in the howler monkey.

The Signal Systems and Social Structure of Ateles

Dimorphism

In a recent review it has been suggested that the

female of Ateles is larger than the male (Crook,

1972). Unfortunately, the data published in the

sources consulted by Crook represent samples in

which the absolute age of the specimens was imperfectly known. As indicated on page 52 ("Ontogeny"), the weight of subadult males of A.

fusciceps begins to surpass that of females toward

the end of their third year of life. The reason

that some of the published summaries of data seem

to indicate that females are larger may be attrib-
66

SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

uted to two causes: (1) Total lengths are often

given rather than head and body lengths. The tail

of Ateles is quite variable in its length relative to

the head and body and, as a result, a long-tailed

female may give the misleading impression that

she is larger than is actually the case. (2) Most

preserved specimens in museums are the result of

rather unselective shooting on the part of museum

collectors. Since subadult and juvenile males form

a subgroup and the number of fully adult males

relative to subadults and juveniles may be rather

small, one can anticipate that a "male" sample

would be somewhat biased toward the younger

age classes.

Table 21 contains some measurements of adult

Ateles (probably in excess of 7 years of age) with

respect to linear measurements. It can be clearly

seen that, although the species is not greatly dimorphic, the male tends to be heavier and its torso

is somewhat longer than that of the female. What

is noteworthy, however, is that the degree of dimorphism is not nearly as great as that shown by many

species of the Old World genera, Macaca, Cercocebus, and Papio. The demorphism shown by

the latter genera no doubt arises from complex

processes of sexual selection. The morphological

differences derive from a combination of (1)

TABLE 21.—Maximum external measurements

(mm) for Ateles*

Species

A. paniscus paniscus

A. paniscus chamek

A. belzebuth behebuth ....

A. belzebuth marginatus

A. belzebuth hybridus

A. fusciceps robust us

A. geoffroyi gucatanensus

A. geoffroyi panamensis

Sex TL HB*

1450

1413

1270

1380

1450

1330

1250

1245

1248

1330

1220

1260

1141

1176

1280

1225

570 880

660(?) 753

450 820

880

810

500

640

635

500

475

498

474

590

510

397

420

594

440

695

750

770

750

856

630

750

744

756

786

785

• All records from Kellogg and Goldman, 1944, except for

$ Ateles belzebuth belzebuth from Museo Ciencas Naturales,

Caracas, Venezuela.

•• HB derived by subtracting T from TL.

competition among males for consortships when

females are in estrus, and (2) actual selection on

the part of females for males possessing certain

characteristics, among which may be a larger size.

On the other hand, differences in size alone may

also be related to nonsexual selection where the

roles of the two sexes are differentiated so that

they come under different types of environmental

pressures. These factors will be dealt with in

subsequent sections.

Parental Investment

Trivers (1972), in a provocative essay, points

out that some dimorphism between the sexes may

be in fact related to different reproductive strategies. In brief, if a male wishes to increase his individual fitness and at the same time has little involvement in parental care, then his reproductive

strategy would involve an attempt to mate with

as many females as possible; such a polygynous

system would of necessity put the male in a competitive position with respect to other males in

the troop. Such male-male competition could

account for sexual selection leading to a size dimorphism when the two sexes are compared. The

female in such a system increases her own fitness

by concentrating her care on an infant born to

her while at the same time attempting to mate

with males having a high potential fitness; thus,

influencing to some extent by their own selection

the same and other characteristics of the observed

dimorphism (see also Crook, 1972).

On the other hand, males of species that show a

great deal of parental investment—approximating

that of the female—may be disposed to concentrate

their reproductive efforts with only one female,

thus insuring their own fitness by increasing the

survivorship of the offspring of a given mate. In

most mammals, the degree of initial parental investment by the male is low. This results from the

fact that the early nutrition of the young by means

of mammary gland secretions generally precludes

the participation of the male (Figure 33). Exceptions have occurred, however, in some Carnivora

(Kleiman and Eisenberg, 1973), and in the primates of the famile Callithricidae (Eisenberg,

1966; Epple, 1975). There is some evidence to

indicate that male participation in the early phases

of parental care is high in some cebid primates,
NUMBER 213 67

FIGURE 33.—Even temporary contact between an adult male Ateles and its juvenile offspring can

be a powerful socializing influence as affiliation develops in the years ahead.

including the genera Aotus, Callicebus, and some

species of Pithecia (Moynihan, 1967; Mason,

1971). All of the foregoing genera are not conspicuously dimorphic in size, although some species

of Pithecia show a pronounced color dimorphism.

Considering that the degree of parental investment is in some way reflected in the degree of size

dimorphism is a useful concept, Nevertheless,

when species are compared the correlations are

not consistent, no doubt a result of the additional

selective pressures which were outlined (p. 66;

see also Kleiman, 1976). It is worth noting,

however, that parental investment by males may

be influential at different stages of the development of the young animal than is the case with

the female. Whereas the female's parental investment may be initially very high, in some species

male parental investment may be significant as

the young become more mature (Eisenberg, 1966:

18, 65). In addition, it is important to concentrate

on the fact that the degree of parental investment

by an adult may not be equally directed toward

juvenile animals; in short, males may in fact direct

more parental investment toward their juvenile

male offspring than toward their daughters (Dittus,

1974, 1975). The affiliations manifested by adult

males toward juvenile males are profoundly developed in both Ateles geoffroyi and in Ateles fusciceps. These behavior patterns no doubt contribute

to the early survivorship of young males born

into a troop. Indeed, these attentions on the part

of adult males probably contribute in no small

manner to the formation of the unisexual subgroupings which are characteristic of Ateles.

These groups ultimately may lead to a differential

use of the home range on the part of the two sexes.
68 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

Foraging Strategy

Females with dependent infants and juveniles

have been shown to form subgroupings (see "Natural History," p. 3). No doubt the mobility of

such encumbered females is reduced somewhat

and this lack of mobility may account in part for

the formation of subgroups based upon reproductive castes. The net result, however, is that the

foraging strategies of the different subgroupings

may tend to spread a troop out over its home range

in a more uniform fashion especially during

periods of food scarcity (Klein, 1972). The utilization of a long call complex can promote assembly

of troop members over a considerable distance,

especially during times when intertroop encounters are taking place. The long calls thus could

serve the purpose of assembly, as well as proclamation of the occupancy of an area. In the latter

case, the long loud calls may have a function similar to those homologous calls shown by the howler

monkey, Alouatta, and Callicebus (see "Comparisons," p. 62).

As suggested by Klein (1972) in his field study

of Ateles belzebuth, the foraging strategies of a

spider monkey troop are reminiscent of those described by Goodall (1968) for the chimpanzee,

Pan satyrus. Much more attention should be given

in subsequent field studies to the differences in

foraging strategies displayed by the subgroups that

are formed out of an Ateles troop.

The Male Croup and Its Genesis

Figure 34 demonstrates the formation of male

subgroupings in the Ateles geoffroyi troop studied

on Barro Colorado Island. The male subgrouping

which derives out of this troop through internal

recruitment is one example of what has previously

been called an age-graded male system (Eisenberg,

Muckenhirn, and Rudran, 1972). It gives the

Ateles troop the appearance of a multimale troop

although in reality the males comprising the subgroup may be related by descent and not of equivalent age. The tendency for males of 5 years of age

and above to move somewhat independently with

a satellite younger male may lead to the dispersion

of males to neighboring troops. Since the long term

studies on Barro Colorado Island involve only a

single troop, we are unable to say how much

interchange between neighboring troops might

take place as young males mature. Certainly some

must take place in a more natural situation.

Such an age-graded system does not in any way

alter the fact that mating may be the prerogative

of one or two males, thus some tendency toward

the maintenance of a polygynous mating system is

not incompatible with the presence of several

males attached to a core female group. The tendency of older males to actively seek out and affiliate with younger males reinforces the formation

of this all-male group. The adaptive advantage of

all-male subgroups foraging independently of the

•**, '

Y

( f }(/ 2>

(% ?W

*•

T

FIGURE 34.—Genesis of male subgroup in Ateles geoffroyi on Barro Colorado Island. Founder

male serves as a focus for the formation of a unisexual subgroup, which then becomes somewhat

detached from the infant rearing group composed of the mothers and their progeny.

t adult male $ j 2 ma le J juvenile

4, subadult male $ female I infant
NUMBER 213 69

females remains to be demonstrated, but the data

suggest that a more efficient utilization of dispersed

resources in a home range could be achieved

thereby. The necessity for young males to disperse

and join a male subgroup is probably not only

adaptive but essential for the normal maturation

processes of young males. Evidence from captive

studies would suggest that, if young males cannot

form an affiliation with older males, independent

of the influence of females, they may be severely

persecuted.

Social Pathologies

Eisenberg and Kuehn (1966) observed that the

young males maturing in the captive colony at

Vancouver appeared to suffer a significantly

higher mortality than was the case with young

females. At first we assumed that this could possibly be due to the fact that young males were

stressed considerably during their maturation

phases through continual conflict with subadult

females. Although this may be the case in certain

captive groups, it is also possible that young males

are more susceptible to calcium deficiency; this

suggestion was raised by Du Boulay and Crawford

(1968:230). Nutritional deficiencies induced by

low levels of vitamin D3 may have been responsible for the low survivorship of young males in

the colony at Vancouver; however, it is undeniable

that in close confinement young males may be subjected to abnormal amounts of social stress

(Appendix II).

Since sexual maturation in the spider monkey

precedes sociological maturation (see "Sexual Behavior," p. 6), I suggest that the maintenance of

a successful dominance relationship over females

may be a necessary prerequisite before a male can

mate. It would appear that grappling or mock

fighting is a means of establishing and maintaining

dominance relationships among troop members.

It would appear then that under close confinement, some zoo colonies may show abnormal stressing of young males on the part of an increase

intensity of grappling which can turn into an outand-out aggressive encounter. As the young males

attempt to dominate females, unnecessary stressing

of young males can occur. I still cling to the conviction that the formation of an all-male subgroup

and its capacity to spatially separate from the core,

mother-rearing group is an important attribute for

social health in groups of spider monkeys.

In crowded zoo colonies, direct conflict among

males of an equivalent age grade can also occur,

especially at the time that females are in estrus.

Recently Ms. Eve Mitchell reported to me an

increased mortality among young male spider monkeys in the zoo colony at Birmingham, Alabama.

According to her data, the male mortality is so

pronounced that out of a colony of 44 monkeys,

there are only 5 males 2 years of age or older (2

adults, 1 juvenile-2, 2 juvenile-1).

At Birmingham some of the aggressive behavior

toward maturing males derives from the two adult

males, but this may in part be an artifact of the

close confinement of adult males in the presence

of reproductive females. Once again, the inference

is clear that the ability of a subgroup of young

males to form spatially separate groups from the

females is essential. Of course, a great deal depends

on the structure of the cage and the history of

the group itself. No such excessive male mortality

has been observed in the colony of Ateles geoffroyi

in San Francisco (Klein and Klein, 1971). Thus,

social pathologies in captivity are far from being

understood completely. The genesis of social pathology no doubt is a function of the individual

history of the colony founders, the structure of the

cage, and the total area in which the group can

develop (see also Klein and Klein, 1971).

Signals in Context

It seems necessary to conclude this monograph

with some attempt to place the signaling system of

the Ateles troop into an environmental context.

I have attempted to avoid imputing a semantic

content to the signals expressed by interacting

Ateles. Indeed, I personally lean toward the view

that the signals tend to reflect the immediate

emotional state of the presumptive sender and, if

they evoke responses from a presumptive receiver,

they probably do so by inducing an empathetic

mood rather than imparting discrete or quantifiable information (Langer, 1973:141-214).

Consider the Ateles geoffroyi troop on Barro

Colorado Island. Upon awakening at dawn in the

sleeping trees, the individual members will begin

arousal, yawning, self-scratching; infants will begin to play with one another. Some individual
70 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

movements to get up and disperse commence. A

5-year old male may begin brachiating suddenly

and emitting a long loud call type 2, perhaps with

three phrases. There is no noticeable effect on other

troop members. A 3-year old male may be following closely behind the 5-year old. Gradually, the

younger males through following begin to move

toward a feeding tree. A female with a 2-year old

young may follow. A young male upon finding

fruit in the tree will utter a twee-twee-twee call.

This will be answered by a following animal; as

each member of the male subgroup arrives at the

tree or a neighboring tree, the call may be repeated.

In the meantime, a female with a dependent

infant may reach down and grab her infant, which

immediately settles upon her back, and initiate

brachiation either toward the feeding spot where

the twee-twee calls have come from or toward

another spot, which may be nearer. This female

will then be followed by a second female who has

assembled her infant in a similar manner. Upon

reaching the feeding tree, the infants may descend

from the females and perhaps take food from the

mother. The mother upon reaching the tree will

have uttered the twee-twee call. This may be followed by a slower whinny as feeding proceeds,

taken up perhaps by a third individual, a subadult female who has followed the mothers at some

distance.

At the conclusion of a 15-minute feeding bout,

one female may begin to move off, pausing to look

back at her infant who will, upon perceiving her

movement, attempt to follow her. The mother

jumps to a branch, the infant utters a low squeaking call, the mother turns, extends her arms to the

infant, the infant grasps the mother's arm and is

pulled to her. The mother then proceeds with the

infant riding and she may or may not be followed

by the other two females.

The foregoing descriptions give some idea of the

kinds of vocalizations performed during the normal

maintenance activities of the animals. Certainly

the twee-twee call serves to maintain contact. Its

association with feeding would indicate that the

call functionally serves to signal food, but the

intent of the caller may only be guessed at. Squeaks

of an infant unwilling to jump concentrate the

mother's attention toward it and elicit an extension of herself to permit the infant to traverse a

gap. The long loud call of a seemingly boisterous young male could function as a territorial

announcement call, although the intent of the

signaler again remains unknown. Certainly it seems

to accompany an exuberant display of initial activity in the morning.

The complex of calling during an unexpected

encounter with a sloth will conclude this monograph. Here follows a description from field notes

where agonistic, fearful, and chorusing behavior

are combined. It was an unusual incident reminiscent of the kind of serious situation that might

happen during an intertroop encounter (Klein,

1972), but instead resulted from the presence of a

two-toed sloth (Choloepus) in a favorite resting

tree, a place where the sloth was "unexpected."

Notes on A teles geoffroyi taken 26 February

1974, 1250-1330, at the laboratory clearing on

Barro Colorado Island. A most extraordinary series

of events occurred with the Ateles troop. The situation was as follows:

A two-toed sloth was present in a tree near the edge of the

clearing; this is the most recent afternoon resting area for

the Ateles male subgroup. The adult male, Chumbo, was

about 50 meters away in an entirely different tree. The male

Class-5, Rico, encountered the sloth and began to scream and

display. The display included brachiating and leaps, piloerection, roar; roar followed by a grimace, then approach

and move away from the sloth. He then went into a shriek

or pulsed chitter while shaking the branches, continued to

chitter, ee-ee-ee-ee-ee-ee, continues to brachiate, roar to croon,

then this croon approximates the old "grunt-trill," eoooch,

ee-ee-oooch, awk, ee-awk, ee-awk, in short, a mixed display

with aggression and fear alternating. He redirects display to

the human observers. He recruits by this display two other

males, a Class-4 and a Class-3; these three proceed to attack

the sloth who fights back with clawing and open mouth. The

Ateles slap at the sloth and alternate calls of ee-ee-ee, ee-ahah, ah-ah, this latter sound approximates aggressive transition

growl heard in a grappling bout.

After arriving with the Class-5 male, the other males embrace, sniff pectoral, sniff arm-pit, and then "attacked" the

sloth. They will break to re-embrace one another. This is a

reassurance behavior. Ee-ee-awk, ee-ee-awk while approaching, slap, and pull away from the sloth. Then the 3, 4, and

5 males brachiate to Chumbo (the founder, adult male), each

embraces and touches him, and Chumbo initiates a long call,

the Class-4 and -5 males join in to form a chorus; it is the

pulsed long call oo-oo-rah oo-oo-oo-rah oo-oo-oo-rah chorus

for around 2 minutes. Chorus consists of the voices of

Chumbo, the Class-5 male, the Class-4 male; then the males

4 and 3 return to the sloth tree; they are more relaxed. A

second Class-3 male approaches, embraces, pectoral sniffs, and
NUMBER 213 71

the other Class-3 male chases the second away. Meanwhile

male 5 returns to watch the sloth, the male 4 teases it occasionally. This persists for some 16 minutes.

This interaction clearly shows the chitter (eeeeee), roar, eee awk, and long loud calls in a context of high arousal, aggression, withdrawal,

mutual reassurance, and finally a long call chorus

reminiscent of a "triumph ceremony."

The description of these behaviors allows for a

functional interpretation as outlined on page 38

("Contexts). There may be alternative possibilities for functional interpretations but such hypotheses must await further study. The most fruitful pursuit would seem to lie with the analytical

techniques as developed for Macaca fuscata by S.

Green (1975).
Appendix I

Physical Measurements and Description of Measurement Techniques for the

Sounds of Ateles fusciceps and Related Species

The vocalizations of Ateles form a graded system.

Although it is possible to define and classify certain calls as discrete entities, any physical description must indicate the range of variation and

display transitional forms. Seventeen calls and

transitional forms are illustrated by photographs.

The defining criteria for the measurements are

portrayed on each figure (see Marler (1973 )for a

similar system of measurement). The measurements are then included for each call form in a

series of tables. Sample sizes are variable since

only recordings of the best quality were utilized in

the tabulations. Standard deviations were calculated when the sample sizes were sufficiently large.

The syllable types are referred to in the figure

legends according to the syllabic key outlined on

pages 24-26. The call types are similarly referred to

by numbers corresponding to the list in Table 10.

FIGURE 1-1.—Bark, Call Number I [[Key II.B.la(l)(a)]. Letter code refers to tabulation in Table

I-A. Throughout the remainder of the figures, the letter codes define the measurements as

recorded in the tables corresponding to each call type. (Ordinate in Khz, abscissa in seconds.)

Call form

A. fusciceps

Slow

A. behebuth

Rapid

All barks

TABLE I-A.—Bark,

n

11

20

72

D(sec)

Av. SJ).

05

0.2S

0.15 ±0.06

Call

n

10

19

69

Number I

/(sec)

Av. SJ).

0.25

0.17

0.24 ±0.14

Frequencies

Ft

0.8

0.9

0.8

F,

1.2-1.8

1.1

(Khz)

F,

22-2.8

72
NUMBER 213 73

FIGURE 1-2.—(left) Trill, Call Number IIIc [Key IIA.la(l)(c)] and (right) Call Number HlaIllb [Key II.A.l.a(l) (a) or (b)]. (Ordinate in Khz, abscissa in seconds.)

4>

3

'

1 •

.3 .6 .9 1.2

«-»

D

1.5

t it *

1.8

V *~

2.1 24

FIGURE 1-3—Twitter, Call Number IV fKey IIA.la(l)(c)]

(Ordinate in Khz, abscissa in seconds.)

TABLE

Call form

HIa

IHb

IIIc

IIIc Ilia

IV

n

37

2

32

50

46

I-B.—Trills and

Z>(sec)

Av.

0.047

0.03

0.022

0.027

0.034

SD.

-•-0.053

+0.009

±0.013

±0.04

twitters

n

V?

«W)

48

42

of Ateles

/(sec)

Av.

0.198

0.091

0.086

0.069

SJ).

+0.28

+0.10

±0.08

±0.059

fusciceps,

FB

_

4.2

3.8

3.4

Call

Ft

_

3.6

3.1

1.8

Numbers HIa, \

Average

F,

0.4-0.6

32-4

frequenciei

F,

1.1-1.9

-

b, c, and

(Khz)

F,

2.8-4.8

-

IV

F,

_

-

-

_

_

059-0.98

1.03
74

SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

4 "

3>

I

1 •

D

t^^ A

flmm%

.9

•

1.2

!

1.5 1.8

- 5 .

TABLE I-C —

Ateles

species

fusciceps

belzebuth

•Fused

n

3

10

trill, squeak

D(sec)

Av.

0.53

0.40

or chitter, Call

/(sec)

n Av.

2 0.23

Variable

Numbers

Av.

X to V

frequencies (Khz)

F

2.9-3.1

3.6-4.1

TABLE I-D.—Pulsed trill or chitter of Ateles fusciceps,

Call Numbers Mb to V

Series call

Chitter Series 1

Chitter Series 2 ..

Pulsed trill Series 3

n

3

3

13

D(sec)

Av. SJ).

0.64 ±052

0.75

0.163 ±0.13

n

2

1

11

/(sec)

Av. SJ).

0.3-0.05 -

0.09

0.110 ±0.074

Av. frequencies

Fm,

2.7

2.8

3.3

Fmt

4.5

4.3

(Khz)

Fr

0.8
NUMBER 213 75

1.2 1.5 1.8 2.1 24

FIGURE 1-6.—Slow whinny (chirp series or yip whinny), Call Number Vic [Key II.A.l.a(2),

grades to II.A.2.a(l) or II.AJ2.a(l)]. (Ordinate in Khz, abscissa in seconds.)

TABLE

Ateles

species

A. fusciceps

IE.—Slow

D(sec)

n Av.

16 0.03

whinny (chirp

Dp (sec)

2.1-2.3

or

n

18

yip form),

/(sec)

Av.

0.10

Call Number Vic

Frequencies (Khz)

FE H L

0.2-0.7 3 2.1

FIGURE 1-7.—True whinny, Call Number XHa [Key

(Ordinate in Khz, abscissa in seconds.)

TABLE LF.—True whinny, Call Number XHa

A.

A.

A.

Ateles

species

fusciceps

belzebuth

eeoffrovi

L

n

2

7

2

)(sec)

Av.

0.96

0.98

0.95

/(sec)

n Av.

: :

B

7

6.9

7-8

LLF

0.9-1.8

1.8-3

1.0-2

Frequencies (Khz)

LHF

1.4-2.9

2.4-4.2

3-3.1

ULF

1.9-3.4

3.5-3.8

23-3.8

UHF

4.4-4.8

4-5.2

52
76 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

B

1.5 1.8 2.1

FIGURE 1-8.—a, Tee-tee (twi-twi-twi), Call Number XHb [Key II.A2.a (2)]; b, slow whinny, Call

Number Via or VIb [Key II.A.2.a(l)] (Ordinate in Khz, abscissa in seconds.)

A.

A.

Ateles

species

fusciceps

geoffroyi

TABLE

n

1

1

I-G.—Tee-tee

D (sec)

Av.

0.69

0.65

/(sec)

n

1

1

(twi-twi-twi),

Av. B

7

5

Call Number XHb

LLF

2.2

1.2

Frequencies (Khz)

LHF ULF

3.8 3.3

3.2 2.4

UHF

5.4

5

FICURE 1-9.—Slow, gutteral whinny, Call Number VId [Key II.B.2.a].

(Ordinate in Khz, abscissa in seconds.)
NUMBER 213 77

TABLE I-H.—Slow whinny, Call Numbers Via or VIb

Ateles

species

A. fusciceps

n

65

D(sec)

Av.

0.05

S.D.

±0.08

Dp (sec)

<2.4

n

60

I (sec)

Av.

0.07

S.D.

±0.05

Av. frequencies (Khz)

UHF LHF ULF LLF

4.1 3.8 2.2 2.4

TABLE I-I.—Slow, gutteral whinny, Call Number VId

Ateles

species

A. fusciceps

n

11

19

6

47

D (sec)

Av.

0.02

0.196

0.092

0.087

S.D.

±0.06

±0.05

±0.15

n

11

17

6

44

/(sec)

Av.

0.06

0.07

0.13

0.07

S.D.

±0.05

±0.08

±0.07

UHF

3.8

2.6

Frequencies (Khz)

ULF

3

1.8

MHF

2.2

2.5

1.2

MLF F,

1.8 0.8-1.2

1.3

FIGURE 1-10.—Sobs (slow, gutteral whinny variant), Call Number VId [[Key II.B.l.a(2)]. narrow

band analysis. (Ordinate in Khz, abscissa in seconds.)

TABLE I-J.—Sobs

Ateles

species

A. fusciceps

(slow, gutteral

D(sec)

n Av. S.D.

19 0.19 ±0.06

whinny

n

17

variant), Call

/(sec)

Av. SD.

0.07 ±0.05

Number VId

Av. frequencies (Khz)

F, Fm Fh

05 1.3 25
till

If

• JL-.JJL.Jfcr^fcS. .

1.5 1.8 2.1 24

Call form

A. fusciceps

Ak-ak

Ook-ook

Ak-ak

A. bekebuth

Ook-ook

Ak-ak

TABLE

n

20

10

9

7

4

I-K.—Ook-ook

D(sec)

Av. SJD.

0.075

0.09

0.08 ±0.008

0.14

0.07

or ak-ak, Call Number VIII

• n

17

6

8

6

5

/(sec)

Av. SI

0.14

0.1

Frequencies (Khz)

1. Ff

0.4

05-0.8

0.162 ±0.007 05

0.112 - 0.6-15

0.16 0.6-0.8

Ft F,

0.8 1.4

2-3

2.2

2-2.4

2

1.2 1.5

TABLE I-L.—Grow I of Ateles fusciceps, Call Number VII

Call form

Growl

Ak-ak to growl

intergiades

n

13

49

D(sec)

Av. SJ>.

0.67 ±0.31

0.152 ±0^05

n

3

46

/(sec)

0.14

0.071 ±0.056

Ft

02,

0.4-0.6

0.5

Frequencies (Khz)

Ft

05,

1.2

1.6

Ft

1.2-1.4.

2-25

2.5

F,

2.6
NUMBER 213 79

FIGURE 143.—Intermediate length compound calls: ascending trill (grunt-trill of adult and

eee-awk of juvenile), Call Number IX [[Key I'A]. (Ordinate in Khz, abscissa in seconds.)

TABLE I-M.—Intermediate length compound calls of Ateles fusciceps,

Call Number XI [Key II.A.S.b (1) or I'.A]

Call form

Ascending trill

Eee-ah:

Eee

Aah

n

4

4

Z>(sec)

Av. S.D.

0.7

026

0.38

/(sec) -

n Av. S.D.

0.6

\<0.01

F,

0.8

Av. frequencies (Khz)

Ft Fm F, F,

2.5 - -

2.8

2.1 - 1 2

F,

;

3

FIGURE 1-14.—Intermediate length compound calls: variant of trill awk: aah aak aa-eeeee ah

II A.3.b (1)]. (Ordinate in Khz, abscissa in seconds.)

Ateles

species

A. fusciceps

TABLE I-N.—Intermediate

D(sec)

n Av. SD. Dp

9 0.16 ±054 1.2

length

n Av.

8 0.05

compound

/(sec)

SJ>.

±0.10

calls

Av. frequencies (Khz)

Ff Fm, Fm,

0.8 1.4 3.4
80

SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

1.5-

1.2'

. 9 '

J6-T

. 3"

id

F?

1

Ik 1

2

phrase

it* iJiiM

3 4 5

m

A

•

6

t

7 8

FIGURE 1-15.—Long call phrasing of Ateles fusciceps short syllables, long syllables and terminal

notes "t" are shown (see Tables I-O, I-P). (Ordinate in Khz, abscissa in seconds.)

TABLE I-O.—Long calls by Ateles fusciceps (narrow frequency modulation; emphasis onE ^ 1 Khz)

Series*

a

b

c ..

d

e

f

Long, loud

syllable

1

1

1

1

1

Intermediate

length syllable

^1.5 < 2

1

3

3

Long terminal

note

> 0J2 < 1

2

2

3

8

2

2

2

Terminal

note

~0.l

_

_

3

2

Comments

Wail form

Vibratto (harsh) form, caw

Wail, v-syllables almost merge

to vibratto form

Undulating wail

Harsh call, caw

Harsh call, caw

• Consecutive series of long calls on a single recording for A. fusciceps.

•• Times defined in seconds.

Range 2.4 Khz; average frequency emphasized 1.15 Khz or 0.7 Khz; average frequency 2.04 Khz.

Frequencies

emphasized

(Khz)

0.58, 0.74, 1.6

TABLE I-P.—Long call

No. of

syllables/

phrase

1-6

bout for Ateles

D

(sec)

1.02

fusciceps M

l

(sec)

0.11

Average

duration of

phrase (sec)

9.4

Total time of recording = 635 seconds; % of time calling = 53%.
Appendix II

Reproductive Data, Medical Histories, Hand-rearing, and Genealogies

Reproductive Data

ATELES GEOFFROYI

Ateles geoffroyi panamensis was reintroduced

on Barro Colorado Island (BCI) during the years

1959 to 1961. It is impossible now to ascertain

the fate of all introduced animals, but by 1964 five

subadult and adult individuals (1 $ , 4 $) were

established at the laboratory clearing. A juvenile-2

female was introduced in 1966 and successful

reproduction by at least three of the females

commenced in 1965 with three live births in 1966

(Eisenberg and Kuehn, 1966). From 1966-1970

the exact patterns of reproduction are imprecise,

mainly because the individual identity of the

founding four females was not maintained in the

recording system, but birth dates were recorded

and Eisenberg made a new census in 1970. Dare

(1974) has documented the group composition during 1971 and 1972. In 1973 Ms. Carrie Thorington

prepared a photographic record of all individuals

named by Dare, and Eisenberg recensused the group

in 1974.

In Table II-A, I present a possible genealogy,

which is based on known birth dates and presumed

identities of the mothers. This table differs from

Dare's interpretation, but I present the table as a

basis for my calculations concerning interbirth

interval and population growth. In Table II-B, I

have compared interbirth intervals from my probable genealogical tree with Dare's intervals from

his own interpretation of the data. Since there is

little difference in the range and the mean, I assume that for all practical purposes the population

analyses derived from my life table are essentially

correct.

For comparison the interbirth intervals for those

zoo births where the mother raised her baby are

included. The captive interbirth intervals are

shorter (2 years 9 months versus 2 years 4 months)

and this is to be expected, considering the more

predictable nutrition plane in captivity.

In my publication of 1973, I stated that the

Ateles geoffroyi births appeared to have an interval of 22 to 36 months. With data through February of 1974 and given the errors inherent in the

reconstruction of genealogies, the range according

to Dare would be 17 to 45 months and for myself

22 to 45 months. The range for captive A. fusciceps is 22.8 to 31.5 months (including only cases

where the mother reared her young to social weaning). With a gestation of 714 months and milk

dependency for 10 months in captive A. fusciceps,

then 17.5 months may be taken as the theoretical

minimum in captivity. In the wild it is surely

longer and I now feel that 28 to 30 months is a

reasonable mode.

Table II-C presents reproduction data for the

BCI Ateles, which allows a calculation of rx. This

value, based on a cohort of females, reflects the low

reproductive rate of wild Ateles. It is almost onehalf the value obtained by Dittus (1974) for Macaca sinica. The lesson is clear. Given the inherent

errors in the interpretation of the BCI records

between 1967 and 1970, both Dare and I agree

that Ateles geoffroyi have a rather long interbirth

interval. These conclusions are supported by the

data from the captive A. fusciceps. The conclusion

for management is quite clear. Ateles populations

are slow to recover from any form of hunting or

cropping. In terms of conservation then the genus

Ateles is very sensitive to hunting and probably

will be the first species to decline under severe

hunting pressures.

ATELES FUSCICEPS

The reproductive history for our captive group

of A. fusciceps robustus through 1972 has been

published (Eisenberg, 1973). Table II-D includes

81
TABLE II-A.—Breeding records for Ateles geoffroyi (BCI)

founding females through 1974*

Consecutive

birth dates

Survivorship status

of young

Mother-young

association prior

to next birth

(days)

Interbirth

interval

(days)

5 Jan 1966.

3 Sep 1969

24 Jun 1972

10 Apr 1966.

4 Oct 1969..

31 Jul 1972

21 May 1966.

30 Jan 1970.

5 Dec 1972

2 Feb 1966

? Mar 1967 .

12 Dec 1969

17 Oct 1971

? Oct-Nov 1968.

FEMALE 1

Survived to weaning

Survived to weaning

Survived to weaning

1340

1024

FEMALE 2

Survived to weaning

Survived

Survived

Survived

Survived

Survived

Did not

Survived

Did not

Survived

Survived

to weaning

to weaning

FEMALE

19 months

to weaning

to weaning

FEMALE

survive

to weaning

survive

to weaning

FEMALE

to weaning

3

4

5

1272

1030

570

675

7

1005

14

_

1340

1024

1272

1030

1313

675

390

1005

673

* R. Dare discusses the difficulties in maintaining a consistent genealogy; this table should be

taken as an approximation (see Dare, in litt.). Introductions on BCI extend from 1959 to 1961

and by 1964 1 male and 4 females were established in the vicinity of the laboratory clearing

(see Dare, 1974; Eisenberg and Kuehn, 1966).

TABLE II-B.—Interbirth intervals for young

that survived until social weaning

TABLE II-C.—Life table data for female

Ateles geoffroyi (BCI)

Ateles fusciceps (NZP) Ateles geoffroyi (BCI)* Year

2 years 6.5 months

1 year 10.8 months

2 years 15 months

x = 2 years 42 months

3 years 9 months

3 years 8 months

3 years 6 months

2 years 10 months

2 years 10 months

2 years 9 months

1 year 10 months

x = 3 years

• Data concerning interbirth intervals taken by R. Dare

(1974) equals 2 years 9 months for an average.

1964

1965

1966

1967 ....'.

1968

1969

1970

1971

1972

1973

1974

Total

Ix mx

4-5

5-6

6-7

7-8

8-9

9-10

10-11

11-12

12-13

13-14

14-15

0

0

1

0.25

055

0.75

0.25

0.25

0.75

0

0.50

Ixmx xlxmx

4

1

1

3

1

1

3

0

2

16

28

8

9

30

11

12

39

0

30

167

16

Ro = — = 4

4

167

T = = 10.4 years of production

16

log. Ro log. 4 1.39

•rt = = = = 0.133 young per female per

T 10.4 10.4 year of a female's life

•rx = approximate value since cohort has not ended its life

span
NUMBER 213 83

the previous data and new data through 1974. A

rash of premature deliveries in 1973 retarded reporduction in this colony. An unidentified virus infection was suspected. Reproduction returned to

normal in 1974 concommitant with changes in

the diet and treatment of the females.

Since young were removed for hand-rearing at

various times in the history of the colony, we can

say a few important things concerning lactation

anestrus. When captive females raised their own

young, the interbirth intervals ranged from 22.8 to

31.5 months. If the female gave birth to a preTABLE II-D.—Reproduction records of Ateles fusciceps robustus females

through December 1974

Consecutive

birth dates

3 Jan 1962

13 Apr 1963

2 Nov 1964

5 Aug 1966

29 May 1967

29 Nov 1969

4 Aug 1970

20 Jun 1972

17 Sep 1973

11 May 1974

18 Apr 1962

17 Apr 1963

27 May 1964

26 Apr 1966

20 Apr 1967

25 Nov 1969

8 Jun 1970

27 Jun 1964

13 Dec 1965

25 Feb 1973

28 Oct 1973

23 Jul 1974

19 Nov 1973

Date young removed

from mother

FEMALE V

22 Mar 1962

 a

9 May 1964 •

3 Sep 1965

5 Aug 1966 • (Max)

Left in colony (Beatrice)

4 Dec 1969

Left in colony (Junior)

20 Jun 1972

 b

17 Sep 1973b

Left in colony (David)

FEMALE H

18 Apr 1962"

5 Sep 1963

11 Apr 1965

26 Apr 1966 • (S or April) •

29 Jan 1969

25 Nov 1969 • (Binky)

8 Jun 1970"

FEMALE R

4 Jul 1964

4 Jan 1966

FEMALE B (Beatrice)

11 Mar 1973* (Princess)4

28 Oct 1973"

Left in colony (Eddie)

FEMALE S

19 Nov 1973*

Mother-young

association

prior to

next birth

(days)

_

78

391

305

0

915

6

685

0

0

-

0

141

319

0

649

0

-

7

-

7

0

-

Interbirth

interval

(days)

-

465

568

641

297

915

249

685

443

237

-

364

405

699

359

949

196

-

544

-

245

269

-

m

 Taken for hand-rearing.

"Stillborn, premature.

c

 Returned to group July 1967.

4

 Reintroduced to group October 1973.

Arrived 17 May 1961: Male M (Macho) ^ 4 years; female V ^ 4 years; female H (Happy)

^ 3.5 years; female R ~ 2 years. Female R died 19 October 1966; female H sold in 1971 with

Max. S and J formed as a pair separate from M, V, and B in September 1974. Females V, Happy,

and R listed simply as A, B, and C, respectively, in Eisenberg, 1973.
84 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

TABLE

Study year

and

grouping

1964

1965

Group 1 ....

Group 2.. .

1966

1967

Group 1....

Group 2.. .

Group 3....

1968

Group 1....

Group 2 .

1970

1971

1972

1973

1974

Group 1 ....

Group 2.. .

II-E.—Compositions of study groups

Adult

$

M

M

M

M

M

M

M

M

M

M

9

V.H.R

V,R

H

V.R.H

V.R.H

V,H

V,H

V

v

v,s

V,B

s

Subadult

$ 9

s

s

B

J

Juvenile II

$ 9

Max S

s

B

T B j "

T

J

P

Juvenile I

$

1

Max

Q

T

J

9

1

for Ateles fusciceps

Infants

$ 9

1 1

2

6

-> 4

2 1

All young removed J

S

B

B

for hand-rearing

Q B

T

J

D,E

4

2 r J

5

\

2 J

6

5

5

5

61

2 /

2 2

5

7

i

Q

0

mature foetus and subsequently gave birth to a

full term infant, the range of interbirth intervals

was 7.9-14.7 months. Given a gestation of 7.7

months, it then seems conclusive that the female

giving birth to a full term infant will pass into a

lactation anestrus for a period of 15.3 to 24 months.

On the other hand, if she does not sustain lactation, she can come into estrus within 8-10 days

of losing her infant. Variability in interbirth interval for females losing their young at birth may

result from a complex of possible factors, but some

seasonality in conceptions is suggested from our

records (Eisenberg, 1973).

The composition of study groups has varied from

year to year. Table II-E includes a synopsis of

study group compositions.

Medical Histories

NUTRITION

As noted in an earlier study (Eisenberg and

Kuehn, 1966), the breeding colony of Ateles geoffroyi at the Vancouver Zoological Park was characterized by a certain amount of bone deformation

developing in young animals born to the group.

Two out of seven subadult animals exhibited deformities suggestive of ricketts. Although this particular colony had access to an outdoor enclosure

on almost every day of the year, the extreme overcast to which this area is subjected may have

reduced the efficiency of vitamin D3 synthesis by

the animals when they were exposed to sunlight.

Dietary deficiencies with respect to Ca and P levels

may have accentuated the situation.

The colony of Ateles fusciceps in Washington,

D. C, was allowed access to an outdoor enclosure

for approximately 6 to 7 months of each year;

during the remaining months the animals were

held indoors. From 1962 through 1965, 7 young

were born to the founding females. One young was

stillborn and the other 6 were raised by their

mothers for varying periods of time. No mother

succeeded in rearing her young beyond the age of

12 months and all of the young surviving to an

age of greater than 4 months began to exhibit signs

of nutritional bone disease (for a review of the

problems, see du Boulay and Crawford, 1968).

Encouraged by the Hamptons' research on marmosets (Hampton, Hampton, and Landwehr,

1966) Dr. C. W. Gray and myself instituted the

following prophylactic procedures. Ultraviolet
NUMBER 213 85

lamps were installed over the indoor cages and

the animals were subjected to UV radiation for 15

minutes during 2 periods of each day, one in the

morning and the other in the afternoon. In addition, vitamin D3 supplement was added to the

food. This procedure was adopted not only for the

spider monkeys, but also the woolly monkeys

housed under the same conditions. In order to

study the efficiency of this procedure, we agreed to

take the first two young born to the colony for

hand-rearing, using vitamin D3 supplements in

the feeding formula. These young were taken in

April and August of 1966 and were successfully

reared with the D3 supplements, and no bone

deformities resulted. In accordance with our plan,

the next two young born were allowed to remain

with the mothers. These were born in April and

May of 1967. Both young were successfully reared

to weaning.

Since our 1966 and 1967 efforts, diets have been

improved and changed so that now the colony is

fed on Zu-Preem Marmoset Diet, which contains

adequate amounts of D3 supplements. Ultraviolet

radiation has been discontinued. Ten births have

occurred from 1966 to 1973; 4 were stillborn and

the factors underlying these stillbirths have yet to

be determined. Three of the young were handreared and three were mother-raised.

We have concluded that successful rearing of

spider monkeys demands either that the animals

have continual access to outdoor cages and be

exposed to sufficient sunlight so that requisite

amounts of vitamin D3 can be synthesized by the

animals or the animals must be fed a diet which

includes vitamin D3 as a supplement. In addition, we recognize that the protein content of the

diet must be reasonably high and that sufficient

calcium and phosphorus be present in the food so

that the D3 can effectively promote recovery and

deposition of these minerals from the dietary intake. Adequate amounts of vitamin D3 must be

provided in dietary supplements in the absence of

direct sunlight, particularly for neotropical primates, which is confirmed in the review by du

Boulay and Crawford (1968).

LEAD POISONING

Although lead-free paint has been used in the

primate house for more than twenty years, certain

deaths in our primate collection were diagnosed

as chronic lead toxicity by Drs. R. Sauer and B.

Zook. The specimens were able to ingest leadbearing material from old layers of paint which

had been covered by new applications. In contrast

to macaques and mangabeys, Ateles was not

significantly affected by lead poisoning because of

its low tendency to allogroom, manipulate artifacts,

gnaw bars, and/or pick at the walls. (For details,

see Zook, Eisenberg, and McLanahan, 1973.) The

old primate house was completely renovated in

1972-1973 .

Hand-rearing Procedures for

Ateles fusciceps robustus

Initially for Max and April (= S), a basic milk

formula, Bermol, was employed with the following

supplements: Vitamin D3 drops, one per day

added to milk mixture at a specified feeding, and

a calcium additive to the milk mixture in the proportion of one teaspoon of calcium for each two

ounces of milk (Calcium DCP 340). The Bremol

mixture was prepared in the ratio of 4 tablespoons

of Bremol for each 8 ounces of water. At 85 days

of age, the young animals were introduced to

solid food. A commercial baby cereal, Pablum,

thinned with the milk mixture, was offered in

small quantities from a plastic spoon. Small slices

of fresh pear were also offered, as were grapes and

banana. At 110 days of age, Vitamin D3 supplement in the milk was discontinued and the young

animals were exposed to ultraviolet radiation for

10 minutes twice a day for about a month's time;

after that, ultraviolet radiation was given for 20

minutes once a day. The lamp was maintained at

approximately 2 meters distance from the floor of

the cage. Bottle feeding was discontinued gradually

and complete weaning was achieved by approximately 10 months of age.

A second spider monkey hand-rearing technique

involved the preparation of Esbilac, 3 parts Esbilac

to one part water. The newborn animal did not

accept this mixture, and the formula was changed

to one part Carnation evaporated milk to 2 parts

water. This formula with vitamin additives appeared to work very well and steady weight gains

were made as indicated in Figure 23.

In some cases the hand-reared specimens were
86 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

initially held in an incubator at approximately

80°F for maintaining their body temperature during the first months of life. However, in two cases

the young animals were wrapped and kept with

the handler even at the handlers' bedtime, thus

insuring adequate warmth.

Yet a third hand-rearing technique included the

following procedures. The animal was initially

placed on a diet of Carnation milk mixed with

water, one part milk to two parts water. Until

about 10 days, between 2 and 2]/2 ounces of liquid

were consumed in each 24-hour period. The

amount consumed increased to 3i/£ ounces by 16

days of age. Baby formula custard (Gerbers) was

introduced into the diet at 20 days of age in the

amount of 6 teaspoons per day. Milk intake was

held at approximately $y2 ounces per day. At 27

days of age, milk intake was increased to 414

ounces; the custard intake was maintained at the

same level. By 35 days of age, milk intake had

increased to 4% ounces per day, given in three

separate feedings, and custard intake had increased

to 10 cc. Milk intake was increased to approximately 5 ounces thereafter and held constant, while

the custard intake was raised to approximately 15

cc per day. Pieces of biscuit and banana were

introduced at 45 days of age into the diet and

gradually increased over the next three months.

Weaning procedures were scheduled as in the

first case.
Appendix III

Infant Vocalizations, Their Physical Measurements and Variation

As in Appendix I, the sonograras of vocalizations

are prepared as figures indicating the manner in

which the measurements of duration, frequency

and intervals were performed. The tables corresponding to the figures include the actual tabulations of the measurements. Refer to pages 90-91

("Expressive Movements" and "Vocalizations") for

a full discussion.

FIGURE III-l.—Chuckle series, ook-ook precursor, Ateles fusciceps, 14 days of age (letters define

the measurements as portrayed in the tables of Appendix III; ordinate in Khz, abscissa in

seconds).

TABLE III-A.—Chuckle series, ook-ook precursor, Ateles fusciceps, 14 days of age

Series

I

n

13

D(sec)

Av.

0.027

SD.

-

n

14

/(sec)

Av.

0.176

SJ>.

-

Av. frequencies (Khz)

Fr, Fr,

0.75 1-1.6

87
FIGURE III-2.—Screech (left) and ee-ah (right) call by 14 day old Ateles fusciceps.

(Ordinate in Khz, abscissa in seconds.)

TABLE

Call type

Screech

(14 days)

Ee-ah

(14 days)

Screech

(5 months) ....

n

1

1

4

8

III-B.—Screech

D (sec)

Av. S.D.

0.3

-

0.3

0.25

0.56 ±0.19

and

n

-

-

2

6

ee-ah by young Ateles

/(sec)

Av.

Variable

Variable

0.49

0.25

fusciceps

Av. frequencies (Khz)

SJ). Ff

-

1.5

-

±0.09

F,

2.5

2.8

2.6

1.2

F,

2

2

1.2

2.1

FT

2.2-3.6

-

-

1.2-3.8

24

FIGURE III-3.—£-ak (awk) call by Ateles fusciceps, 14 days old.

(Ordinate in Khz, abscissa in seconds.)

TABLE

Series

I

III-C—E-ak (awk)

D (sec)

n Av.

2 0.165

call

S.D.

-

by Ateles fusciceps,

/(sec)

n Av. S.D.

- Variable -

14 days old

Av. frequencies (Khz)

F, F,

3 1.6
NUMBER 213 89

5*

4 >

3

2>

1

5*

4*

1 »

0

F

2

i

1

1

.3 .6 .9 1.2 1.5 1.8

FIGURE IIM.—Eeeaah call by 5 month old Ateles jusciceps.

(Ordinate in Khz, abscissa in seconds.)

D

2.1

fctM

FIGURE III-5.—Ee ah to ah ee alternations, a separation call by 5 month old Ateles jusciceps.

(Ordinate in Khz, abscissa in seconds.)

Species

A. jusciceps

TABLE

n

2

2

111-D. —Eeeaah

D(sec)

Av. SJ).

0.58

0.63

call

n

1

1

at 5 months of

/(sec)

Av. SJ).

0.63

0.31

age

Av.

Ft

0.9

1.3

frequencies (Khz)

F,

2.3

2.4

F,

3.4

3.4
Appendix IV

Behavior Patterns for Captive Lagothrix and Alouatta

Within the body of the text, frequent comparisons of the repertoire of A teles were made with

the behavior patterns of the larger cebids, Lagothrix and Alouatta. Although these genera have

been studied by a variety of workers, Lagothrix

has not been the subject of an intensive field study

and Alouatta has not been studied in detail under

captive conditions. Williams (1965, 1968) has described the behavior of captive Lagothrix in

detail, and Schifter (1968) has documented marking behavior, as well as the development of the

young in the Zurich Zoo. Alouatta palliata was

studied intensively on Barro Colorado Island by

Carpenter (1934) and later by Altmann (1959),

Collias and Southwick (1952), and Chivers (1969).

In all these studies aspects of free-ranging behavior

are described and interpreted. In spite of the preceding work, the sonographic analysis of vocalizations has not been performed.

Since the study of Ateles fusciceps in captivity

necessitated the development of standardized

data recording procedures, it was deemed desirable

to extend the same procedures to captive groups

of Alouatta and Lagothrix. The resulting data

could then be used for base line comparisons of

Lagothrix and Alouatta with Ateles. Thus this

appendix presents the results of an observation

series performed by L. McLanahan with our captive cebids, together with a preliminary analysis

of vocalization patterns carried out by J .F. Eisenberg. These data should be considered in conjunction with the monographic material of Carpenter

(1934) for Alouatta and Williams (1968) for

Lagothrix.

Behavior Patterns in Lagothrix lagotricha

METHODS AND SUBJECTS

A group of three Lagothrix lagotricha was observed during June and July 1973. One adult male

^ 9 years old, one adult female ^ 8 years old, and

their 10-month-old offspring comprised the group.

For the month of June, the group was housed

indoors in a small 3X2X 3 meter cage of wire

mesh to prevent the infant's having contact with

lead-painted bars and artifacts (Zook, Eisenberg,

and McLanahan, 1973). On 3 July the group was

moved outdoors to a lead-free cage measuring 4 X

4 X 5 meters. Numerous branches and artifacts

were provided for climbing and brachiation. The

animals were fed and watered daily between the

hours of 9:30 and 11:00 a.m.

The group was observed for 30 minutes twice

daily. Observation periods were balanced so that

significant activity samples from each of the daylight hours between 7:30 a.m. and 6:30 p.m. might

be recorded within the two-month period. The

total observation time was 30 hours.

Quantitative data was taken on all interaction

and individual behaviors, such as displays and

self-care. A frequency measure was taken for

vocalizations. All observations were recorded manually and summarized weekly. For prolonged

periods of interaction, such as copulation, a detailed description was made in addition to the

recording of duration and frequency measures of

the accompanying behaviors.

PATTERNS OF SOCIAL BEHAVIOR

Expressive Movements

HEAD-SHAKE.—While looking at partner, the animal moves its head from side to side rapidly. The

head-shake can accompany grappling, vigorous

playing in infants, and agonistic encounters.

GROOM SOLICITATION.—The body is turned to

expose the pectoral area and one or both arms

are extended to touch the partner.

GRIMACE.—A facial expression in which the lips

are partially opened to expose the lower teeth

90
NUMBER 213 91

row and canines. It is seen most frequently in

adult males during displays, long call sessions, and

vigilant behavior. Adult animals tend to grimace

during defecation.

BRANCH-SHAKING.—An arousal-related movement.

CAGE-SHAKING.—Performed by grasping a part of

the cage with the hands and feet and alternately

pushing against and pulling away from it rapidly.

LEAPING.—A series of springing movements. The

movement is usually correlated with a high degree

of arousal in the performer. It can be done in

either a quadrupedal or bipedal posture.

ANAL DRAG.—A movement in which the animal,

while sitting erect, drags its anus across a flat surface by pulling itself forward with the arms. The

movement is usually 2 to 3 seconds in duration.

ANAL RUB.—A movement similar to the anal

drag except that the animal remains in one place

and moves its anus in a circular pattern over a

flat surface for approximately 2 seconds.

CHEST RUB.—The animal drags its chest over a

flat surface for anywhere from 1 to 175 seconds.

BACK ROLL.—The animal, lying on its back does

a series of side to side rolls for approximately 5

seconds. Each bout is comprised of 5 to 7 rolls.

LIP SMACKING, TOOTH CHATTERING, AND RELATED

MOVEMENTS.—While looking at the partner, the

lips are retracted to expose the upper and lower

teeth rows striking against each other repeatedly.

This gesture is often accompanied by head-shaking

when the animal is begging for food. It is interpreted as an appeasement and contact-promoting

gesture when the mouth is pressed against one

arm. Head-shaking may also accompany the latter

variant.

HEAD ROLL.—The head is moved rapidly in a

counterclockwise circle. The movement may occur

in 3 or 4 bursts. It may accompany food-begging

and also agonistic encounters. In the case of the

latter, the grimace may also occur. The head roll

has only been observed in the adult male.

Vocalizations

The following definitions apply to sounds produced by adults unless otherwise noted (terminology adapted from Williams, 1967) Tables IV-A,

IV-C).

E-OLK.—A sound of approximately 0.05 seconds

duration. The call is given prior to feeding and

can be an accompaniment to contact-promoting

gestures. The vocalization is uttered most often by

the adult female. The lips are slightly pursed in

production of the sound (Figures IV-1, IV-2).

SLOW EOLK.—A sound of 1 to 2 seconds duration. It is correlated with feeding and may be

uttered during mastication. Only the adult female

has been heard to produce this sound (Figure

IV-1).

UH-UH (tuff-tuff).—A broken series uttered by

an animal that is grappling or is involved in a

vigorous play bout. Adult and infant versions of

this sound are similar. The head-shake frequently

accompanies this vocalization (Figure IV-2).

LONG CALL BOUTS.—A high intensity call uttered

by adult animals in a state of arousal. The vocalization has only been heard in the early morning

and evening hours. The female and male long calls

have the same pitch range and frequency modulation, but the male's call is louder.

LONG CALL SESSION.—Composed of long calls,

this session may last for up to 20 minutes and involves one animal, most frequently the adult male.

Exposure of the lower canines, excessive salivation, and displaying are components of this activity and indicate a high level of autonomic arousal

in the animal (Figures IV-3, IV-4).

Contact and Contact-promoting Patterns

EXTEND.—The act of extending an arm, leg,

or the tail to touch another animal.

TOUCH.—Contacting another animal by touching lightly with any part of the body.

EMBRACE.—A gesture which may be either mutual or unidirectional. It involves placing the arms

and/or tail around a second animal's body.

ANAL-GENITAL INVESTIGATION.—A pattern whereby the mouth and/or nose are brought near the

anal-genital area of another animal.

GROOMING.—This act may be preceded by soliciting. The groomer parts the fur of another individual with its fingers and then either licks or nips

the dried skin or fur.

GRAPPLING.—A pattern accompanied by the uhuh vocalization. Grappling is comprised of several

components including wrestling, pushing, mock

biting, slapping, and chasing. Grappling can be a

prelude to an agonistic encounter.

MUZZLE SNIFFING.—A pattern that may be
92

SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

5"

4-

-

2"

i .

1

5"

4>

3*

2*

1 •

a

b

.3

.3

s

.6

.6

s

.9

.9

r

z

1.2

1.2

n

D

A A A A

1.5 1.8 2.1 24

1.5 1.8 2.1 24

FIGURE IV-1.—Frequency modulated calls of Lagothrix (E-olk series—nomenclature from Williams, 1967): a, slightly modulated form; b, modulated form with sidebands. (See also Figure 30.)

(Ordinate in Khz, abscissa in seconds.)

Syllable

type

Modulated form

with sidebands

Slightly modulated form ..

Classic form

n

2

5

8

5

TABLE

D(sec)

Av.

0.75

0.21

0.13

054

IV-A.—E-olk syllables

SJ).

±0.08

±0.14

/(sec)

n Av. SJ).

Variable

Variable

6 0.10 ±0.07

Variable

F»

2.1

3.2

3.4

Frequencies (Khz)

Ft F.,

1.3

2.4

1.2

0.9

Fr

0.8-3.8
1.2 1.5 1.8 2.1

FIGURE IV-2.—Uh-uh or chuckles for Lagothrix. (Ordinate in Khz, abscissa in seconds.)

TABLE IV-B.—Uh-uh or chuckles

Species

A. fusciceps

D(sec) / (sec) Frequencies (Khz)

n Av. n Av. Fn F, Fr

11 0.08 10 0.05 2.6 1.5 0.1-S.4

FIGURE IV-3.—Syllable forms employed in long call session by adult male Lagothrix lagotricha:

a, roar to bark; b, trills with side bands. (Ordinate in Khz, abscissa in seconds.)
TABLE IV-C.—Long call analyses for Lagothrix male

Roar

Bark

Clear

With

Series

Series

Series

Call type

noise:

1

2

3

n

32

15

D

n

5

4

4

5

ROAR-LIKE SYLLABLES (FIGURE IV-3a)

AND BARK-LIKE SYLLABLES (FIGURE IV-36)

D (sec) / (sec) Frequencies (Khz)

Av. SJ). n

0.33 - 27

0.13 - 12

TRILL-LIKE SYLLABLES

(sec)

Av.

0.84

0.93

0.79

0.63

n

3

2

4

3

Av. SJ).

0.13

022

(CLEAR) WITH NOISE

/(sec)

Av.

0.29

023

0.19

0.30

Fr F(Av.)

0.2-3 1.46

0.2-3 159

(FICURE IV-4a)

Frequencies (Khz)

2.7

3

3.2

3.4

F, F^V.;

2.4 2.27

0.5 1.68

0.6 1.74

0.2 1.24

94
NUMBER 213 95

either mutual or unidirectional and in which one

animal sniffs or licks the muzzle of another. This

pattern is frequently correlated with feeding and

occurs between the infant and adult female.

Agonistic Patterns

BOUNCING.—A pattern in which one animal

raises an arm to hit another, but instead places the

arm on the partner's shoulder and leaps up and

down two or three times. Frequently seen between

the adult male and female.

BOXING.—A series of light blows directed at the

head area. This pattern is correlated with food

stealing.

Sexual Patterns

Primary sexual behavior in the genus Lagothrix

is seldom observed in either the field or captive

situations. The following three protocols offer a

partial description of the sexual behavior of Lagothrix lagotricha.

Protocol 1, 28 June 1973, 1430-1440 hours (observer, L.

McLanahan): Adult male and adult female. Observer approached and stood immediately outside the cage. Male

moved toward observer and began to tooth-chatter. Three

minutes later, female approached and extended her arm to

observer. Male immediately moved behind female, hooked

his legs over her legs and wrapped his arms very tightly

around her abdomen. Approximately 5 seconds later, male

exhibited a series of 7-10 pelvic thrusts. When female

abruptly disengaged him from her; the male was observed

to have an erection.

Protocal 2, 2 October 1974, 0905 hours (observer, J. F.

Eisenberg): Subadult female around 3 years of age has been

allowed to encounter with adult male and his son about 2

years of age. Before the animals are allowed together, an exchange of ee-olk-ee calls are given by the male, generally

replied to by the female with an ah-olk or ee-och and finally

a slow ee-olk. New female enters; the juvenile male is active,

hanging upside down, shaking the bars, and pays a great

deal of attention to the juvenile female. The adult male

shows broadside quadrupedal standing and little movement.

The adult male and juvenile male approach one another,

hug. The juvenile male approaches the juvenile female twice.

Then the female approaches the juvenile male who is hanging by his tail and sniffs his face. Juvenile male head-shakes.

Then they begin to interact, mutually hanging upside down,

head-shaking and tagging at each other, giving an uh-uh-uh

grading to eek-eek-eek calls interchanged. This is homologous

to grappling in A teles. Occasionally, a low and inflected

version of the ee-olk will be given. Expressions on the face

include half open mouth with teeth exposed. This expression

may grade into a complete "grimace" with the mouth corners

retracted on the part of the juvenile male. Suddenly the

juvenile female screams, showing open mouth and teeth exposure. The juvenile male runs to the adult male and hugs

him.

The two juveniles then ee-olk back and forth. Occasionally

the adult male utters a loud and pronounced ee-olk! At the

terminal part of the ee-olk there is a vibratto. Then the

grappling interaction between the juvenile male and the

juvenile female commences again. When grappling during

this phase, the lips are often slack when they look at one

another. The mouth may be open but only the lower teeth

may be showing. Preparatory to grappling the animals may

stand bipedally slightly hunched over, the back now assumes

an arch; this may be homologous to the bipedal arch of

Alouatta, but it is relatively unritualized. In this posture the

tail often grips the branch of a tree.

During grappling, whichever member of the pair is showing defensive behavior lowers its head and appears to offer

the crown of thick black hair, which is then nipped by the

other. In this case, the juvenile male is doing most of the

nipping. The juvenile female seems to solicit this biting behavior by lowering her body quadrupedally, resting on her

arm, with her head facing the opponent, and her lips slack

at the corners, with the lower lip drooping slightly. During

the grappling that ensues, one partner may look away and,

at the time that it looks away, the lips are drawn back and

the teeth are displayed. Grappling breaks off.

The female has learned to turn on the drinking fountain

and both animals drink while she holds the stream on. Then

the female looks at the male and begins tooth-chattering. The

juvenile male now has an erection and the juvenile female

continues this chattering and lip smacking and extends a

hand and touches the young male's genitalia. He moves behind the female and makes several pelvic thrusts at the base

of her tail. She continues to remain quadrupedal, turns and

looks at the juvenile male while tooth-chattering (lip smacking). He thrusts at the base of her tail. Both are now hanging

up. They are not properly positioned but it is definitely play

with strong sexual overtones.

The young male now sits to one side of the female. She

sniffs at his erection. He manipulates his genitalia. She continues to tooth chatter. He begins rubbing on her thigh with

his erection. She hangs up. He begins to show slow jaw

champing movements and some tongue movements. She begins to play with his tail. This sexual interaction (it is now

0940) is persisting.

During chattering movements, there may be some lip retraction, thus showing the teeth. The young male Lagothrix

mounts the female and begins thrusting rhythmically, orientation is nearly correct, but the penis is hitting high at the

base of the tail. The juvenile male's legs are not hooked over

the female's thighs; however, this is not necessarily a normal

orientation. The adult male has been sitting alone and feeding. The amount of tooth exposure during chattering is not

as extensive as that shown during a full lip retraction and

grimace, but the teeth are definitely visible.
96

SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

Protocol 3, 20 November 1974, 1235 hours, (observer, L.

McLanahan), observations on Lagothrix: Adult male, subadult female, and juvenile male have been housed together

since 2 October. This sequence involves sexual behavior on

the part of the adult male toward the subadult female.

Female to the male, approaching 4 times, sniffs his genital

area, and twice presents her genital area to him. Juvenile

male approaches adult male and adult female attempting to

grapple. Female tooth chatters (lip smacks) whenever in

visual and/or physical contact with the adult male. The juvenile and adult male lip smack during their grappling bouts.

The female's lip smacking appears to correlate with her

sexual receptivity. 3:28# Female to adult male, contacts him,

they embrace and huddle. 3:31 Male mounts female. Male is

vigilant and lip smacks intensely as he looks at juvenile male

who is around 4 feet away. The juvenile male approaches

the couple and attempts to grapple with the adult male. All

are now lip smacking. Male thrusts briefly and shallowly, but

is interrupted by the activities of the juvenile male. 4:43 Two

deep thrusts by male. 4:51 Two deep thrusts from a momentary bipedal stance. 4:58 Female leaves. Male was not observed to leg lock during this thrusting bout and intromission

probably was not sustained. 5:00 Female follows male and

sniffs his genitals approximately every 3 seconds. Female

approaches male and presents her genital area to him 3

times. 5:27 to 5:46 Male mounts female, juvenile male disrupts the mount. 5:50 to 6:34 Female approaches male 3

times, attempts to mount him twice and once pectoral sniffs.

Then female approaches male, male mounts female, juvenile

disrupts mount, all huddle and lip smack. Male leaves. Female approaches male and anogenital sniffs him twice. Male

sniffs female's genitalia once. Female follows male with frequent anogenital sniffing. Female presents her genitalia to

male. 6:47 Female approaches male, female mounts, holds

male and thrusts for about 8 seconds. Male mounts, holds

female, female leaves. Male approaches female. Male mounts

and holds female, female leaves. 7:06 to 7:23 Male approaches

female, holds her in a mount for 17 seconds. Juvenile attempts grappling with male and female. 7:23 Male mounts

female, distinguished from previous mounts in that he now

locks his legs over her thighs. Juvenile approaches and attempts to grapple with male. 7:23 to 9:30 Male thrusts briefly

and shallowly while attempting to grapple with juvenile

simultaneously, all are lip smacking. Juvenile calms down

* Minutes and seconds elapsed.

and rests against male for the remainder of the mount. 9:30

Male thrusts deeply 3-4 times, female's lip smacking becomes

louder and more rapid. 9:42 Two deep thrusts. 9:53 Male

leaves. Copulation judged to have been complete, total intromission time around 150 seconds. 10:03 to 10:43 Female approaches male 6 times, 4 times anogenitally sniffs, and

presents her genitalia once. 11:17 The animals are now being

fed and all sexual activity subsides.

SOCIAL STRUCTURE IN A CAPTIVE GROU P

The following analyses of quantitative data

taken on contactual, grouping, and individual

behavior are drawn for purposes of clarifying existing roles and relationships within the observed

group so that the processes of group social organization might be better understood.

Autogrooming Analysis

Only the adult female was observed to autogroom and this comprised 5.72 percent of the total

time spent in all grooming for all observation

periods. The frequency of autogrooming was approximately 25 percent that of the frequency of

allogrooming.

Display Analysis

All observed displays were performed by the

adult male and in three contexts: (1) during vocalization sessions, (2) in response to loud noises

or public disturbance, and (3) just prior to feeding. Three separate displays were noted: cageshaking, which occurred in response to noise and

disturbance; leaping, which occurred prior to feeding; and head-rolling, which frequently occurred

between long calls during vocalization sessions.

Displaying accounted for only 0.28 percent of the

total observation time (see Table IV-D).

Subject

Male

TABLE IV-DCage-shake

Tf Pd D

102 0.787 1.7

-Display

Tf

2

analysis

Leaping

Pd

0.03

D

4

Tf

15

Head-roll

Pd

0.188

D

4

Tf = total number of times display occurred for all observation periods; Pd = proportion of

the total duration of all displays for all observation periods; D = mean duration of seconds of

display.
NUMBER 213 97

Marking Analysis

Marking behaviors were exhibited by both the

adult male and the adult female and consisted of

the anal drag or rub, and the chest rub. The chest

rub occurred most often and was observed only in

the male. The context in which marking behaviors

occurred was not determined. These activities

accounted for 0.24 percent of the total observation

time (see Table IV-E).

TABLE IV-E.—Marking analysis

Subject

Male

Female

Tf

5

0

Chest rub

Pd

0.709

0

D

37.5

0

Anal

Tf

9

31

drag or

Pd

0.132

0.203

rub

D

2

2.6

Tf = total number of times display occurred for all observation periods; Pd = proportion of the total duration of

all displays for all observation periods; D = mean duration

of seconds of display.

threat, and agonistic behavior patterns are learned

and exercised.

Grappling might also be considered to be instrumental in expanding the mother-infant and fatherinfant bonding into familial and three-way bonding. Evidence for this is the fact that grappling was

the only contactual behavior, besides wrestling,

in which all three animals were seen to participate

simultaneously (see Table IV-F).

Initiator

Infant

Infant

Infant

TABLE IV-F.—Grappling

Recipient

Male

Female

Male/Female

Tf

14

3

2

analysis

Pd

0.729

0.167

0.103

D

162.2

130

128.3

Tf = total number of times display occurred for all observation periods; Pd = proportion of the total duration of

all displays for all observation periods; D = mean duration

of seconds of display.

Allogrooming Analysis

Allogrooming comprised 94.34 percent of all

grooming observed and roughly 1.35 percent of all

summed activity durations. Allogrooming was

always observed to be initiated by the female and

directed at the infant. It should be noted that the

female allogroomed the infant only after he had

initiated either an embrace or embrace/suckle.

The average duration of an allogrooming bout

was 52 seconds. These results indicate a cohesive

bond between the mother and infant in spite of

the fact that the infant was almost in the weaning

stage. An analysis of grappling data provides additional information on parent-infant bonding.

Grappling Analysis

Grappling comprised 2.16 percent of the total

observation time and was most frequently observed

between the infant and the adult male. All observed grappling bouts were initiated by the infant.

That grappling bouts were directed at the adult

male roughly 4 times more than at the adult female

indicates two possibilities as to its function: (1) a

means by which male-male bonding is developed,

and (2) a means by which male avoidance-flight,

Embracing Analysis

Embracing comprised 8.02 percent of all observed activity, which is the largest percentage for

any contactual behavior observed. That it was

most frequently observed between the female and

infant further supports the existence of a cohesive

mother-infant bond. The activity was always observed to be initiated by the infant. Embracing

usually occurred in one of two contexts: during

rest or during adult male cage-shaking displays

by which the infant was terrified.

DIFFERENT ROLES AND RELATIONSHIP

WITHIN THE CAPTIVE GROUP

The Maternal-Young Relationship

Mother and infant show a close bond. At this

age (10-12 months), the infant frequently clings

to the mother during rest, suckling, or when

frightened. During suckling or embracing, the infant is usually groomed by the mother. The female

dispenses more grooming to the infant than to

either herself or the adult male. Contact between

the mother and infant occurs more frequently and

for longer periods of time than it does between

either the male and female or the male and infant.
98 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

The Paternal-Young Relationship

The most frequent form of father-infant contact

is grappling, and it is hypothesized that this grappling may be a means by which specifically fatherinfant and more generally male-male bonding is

developed and also by which male avoidanceflight, threat, and agonistic movements are learned

and exercised.

Role of Adult Male

As the grouping data indicates, the adult male

is usually by himself at an average distance of 2.5

to 3 yards from either the female or infant. With

the exception of occasional grappling and embracing bouts, the male devotes his energy to vigilant

behavior. Lengthy morning and evening vocalization sessions and displays, which are correlated

with a high degree of arousal, are often the outgrowths of this vigilant behavior.

Behavior Patterns in Alouatta pailiata

METHODS AND SUBJECTS

A pair of Alouatta pailiata was studied for two

months for a total of 36 hours observation time.

The animals, one adult male ^ 5 years old and

one adult female ^ 5 years old, had been handraised from birth with two other animals and were

later introduced to their captive setting.

Housing consisted of a 5 X 1 X 2 yard indoor

enclosure equipped with branches, an overhead

exercise pole, and two resting benches. The cage

was divided into two areas, which were used respectively for feeding and activity. The animals

were fed a daily ration of grapes, apples, oranges,

bananas, cottage cheese, kale, bread, and strained

meat. Water was provided through a push-lever

dispenser.

Thirty-minute observation periods were conducted twice daily, during morning and late afternoon hours. Data were recorded manually and

vocalizations were taped for sonograph analysis.

PATTERNS OF SOCIAL BEHAVIOR

Expressive Movements

TONGUE-FUCK.—(1) While the animal visually

fixates on its partner, the tongue is extended

through pursed lips and rapidly flicked up and

down for an average duration of 2.7 seconds. Dependent on context, the tongue-flick can be interpreted as a contact-promoting, greeting, or an

appeasement gesture; (2) during auto-investigation, the flicking tongue may be brought into contact with that part of the body under examination;

and (3) during contact, one animal may tongueflick the genitalia, muzzle, or tail of another.

ARCH.—In fixating an animate object, the animal, most frequently the male, drops its head so

that the chin is at ground level and arches its back.

The movement is usually accompanied by toothgrinding and eye-squinting and is interpreted to

be an aggressive display.

EYE-SQUINT.—Associated only with male aggressive displays, this expression involves half-closure

of the eyelids and scalp retraction.

TOOTH-GRIND.—This movement involves full exposure of the upper and lower teeth rows, which

are grating against each other in a sideways motion.

Tooth-grinding occurs in agonistic encounters and

male displays.

BACK-ROLL.—The animal, lying on its back, does

a series of side-to-side rolls for an average duration

of 10.2 seconds. This movement may be an artifact

of captivity.

LEAP AND REAR.—Always associated with the

arch, the movement involves the animal's leaping

straight up and, upon landing, sliding backwards

on the hind limbs. It is an extremely aggressive

gesture.

CHIN RUB.—A male behavior pattern comprised

of moving the chin back and forth along a surface

for the mean duration of 5.5 seconds. It is correlated with a high level of arousal in the animal.

CHIN AND CHEST RUB.—A male behavior in

which the chest and chin are alternately rubbed

against a flat surface in a circular-horizontal

motion. The animal sits erect during this activity.

The mean duration is 17.5 seconds.

ANOGENITAL RUB.—A female behavior in which

the anus and vulva are rubbed on a flat surface in

a sideways motion. Mean duration is 2.5 seconds.

ANOGENITAL DRAG.—A female behavior in which

the anus and vulva are dragged across a flat surface

for an average of 3 seconds. There is no specific

context in which the latter two behaviors are

performed.

URINE SNIFFING.—A male behavior in which
NUMBER 213 99

urine on the ground is sniffed or licked. An animal

may dip its fingers in a urine puddle and lick them

clean.

Vocalizations

BARK.—A short sound usually uttered by the

male and in stimulation-related situations or prior

to feeding. The sound is approximately 0.27 seconds in duration and may be repetitive ("chah")

(Figure IV-5, Table IV-G).

WHINE.—A drawn-out and high pitched vocalization only heard in the female. Approximately

1.0-1.5 seconds in duration, it is correlated with

contact situations. The vocalization is uttered with

no less than a 2-second interval between sounds.

GROWL.—A sound of approximately 0.5 seconds

duration, which may be repeated, and is correlated with aggressive arousal in the male.

SHRIEK HISS.—A shrill sound of 1.5 seconds

duration, which is uttered by the female in aggressive encounters with the male. The lips are retracted to expose the upper and lower teeth rows.

The mouth is usually closed, but may be slightly

opened.

LONG CALL (Roar).—A drawn out, "legato"

vocalization of anywhere from 2-5 seconds duration, which is uttered by both the male and female.

It contains elements of the bark and growl and is

correlated with an abundance of external stimuli,

i.e., crowd noise and vocalizations of other animals.

The female's long call is more high-pitched than

the male's (Table IV-H, Figure IV-6).

E-UH-UH.—A series of sharp, low-intensity sounds

averaging approximately 0.3 seconds with a small

interval between. This vocalization is uttered by

the female during grappling (Figure IV-7).

O-EH O-EH.—Brief repetitive syllables with

great frequency modulation. Often given by the

male when alert and in low stages of autonomic

arousal. It can serve as a group warning sound

(Figure IV-8).

SOFT CHIRP.—Brief high pitched notes given by

animals in ambivalent contexts, not necessarily

repetitive (Figure IV-9).

5"

FIGURE IV-5.—Barking by Alouatta palliata male (narrow band analysis).

(Ordinate in Khz, abscissa in seconds.)

TABLE IV-G.—Bark series preceding roar

by adult male Alouatta palliata

A.

Species

palliata ..

D(sec)

n Av.

10 0.27

/(sec)

n Av.

6 0.07

D/> (sec)

n Av.

3 3.6

Frequencies (Khz)

Fr Ft

0.42 0.84
100 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

FIGURE IV-6.—Roar by Alouatta palliata male. Note modulation and terminal notes (see Table

IV-H). (Ordinate in Khz, abscissa in seconds.)

TABLE IV-H.—Undulating roar or long call by male Alouatta palliata

(fundamental energy is ~0.4 Khz)

Grouping

Single $

Chorus

Terminals

D+ I,

n Av. n Av.

2 1.25 2 0.1

Phrases

Z)(sec)

n Av. n

2 4.8

4 3.7 4

/(sec)

Av.

9.8

Frequencies (Khz)

Fr Ft

0.42-0.3 0.84-0.7

or

0.42-0.48

0.42-0.3 0.84-0.7

or

0.42-0.48

1.5 1.8 2.1 24

FIGURE IV-7.—£-uh call by Alouatta (chuck). (Ordinate in Khz, abscissa in. seconds.)
NUMBER 213 101

1.5

FIGURE IV-8.—O eh 6 eh series by male Alouatta. (Ordinate in Khz, abscissa in seconds.)

FIGURE IV-9.—Soft chirp series by Alouatta approximates a trill.

(Ordinate in Khz, abscissa in seconds.)

Patterns of Interaction

Contact and Contact-promoting Patterns

APPROACH.—One animal moves toward another,

meanwhile visually fixating on it. No particular

facial expression or vocalization may accompany

an approach.

TOUCH.—Intentionally contacting another animal

with hands, tail, or feet.

TONGUE-FLICK.—Contacting the genitalia, muzzle

or limb of another animal by means of a rapid

tongue extension.

ANAL-GENITAL INVESTIGATION.—One animal investigates the anus and/or genitalia of another

with mouth, nose, or hands.

MUZZLE TOUCHING.—Unidirectional or mutual

mouth-to-mouth contact.

GRAPPLING.—A play behavior composed of

"mock" agonistic and avoidance patterns and accompanied by the "uh-uh" vocalization in the

female and the low "growls" in the male. Muzzling,

genitalia nipping, poking, pushing, and tugging

are components of grappling behavior.

HEAD-WRESTLING.—Two animals butt and push
102 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

each other with their heads.

RUMP-NUDGING.—A male to female wrestle,

which is usually subsequent to a female anogenital

presentation.

MUZZLE-POKE.—A female-initiated pattern, which

involves the poking of a finger into either the

mouth or nose of the male. This poke may lead

to either grappling or sexual behavior.

LIMB-GRABBING.—A prelude to grappling.

Agonistic and Avoidance Patterns

BITE.—A rapid slash to any part of the body

applied by the canines or incisors.

DUCK.—Behavior involving backing off from an

encounter and cowering.

THREAT.—A female behavior involving extending the head towards the opponent and hiss

shrieking.

Sexual Patterns

ANOGENITAL PRESENTATION.—An animal approaches its partner, turns, and directs its anal and

genital areas at the partner for an average duration of 15 seconds.

SCROTAL TONGUE-FLICK.—During presentation,

the female flicks her tongue against the male's

genitalia. In performing this behavior, the female

forms a half-circle around the male. The scrotal

tongue-flick accompanies the majority of female

presentations to the male.

VULVAL TONGUE-FLICK.—The male approaches

the female from behind and flicks his tongue

against her vulva.

INTERACTION ANALYSIS

Nonsexual Interaction Forms

Nonsexual interaction refers to behaviors that

are initiated by one animal and directed towards

another, which usually grade into grappling or

sexual behavior and are far less complex patterns

of interaction in themselves. They are analyzed

under a separate heading. Rump-nudging and

head-wrestling are usually sex-related and muzzling, muzzle-handling, and limb-grabbing are

grapple-related (Table IV-I).

TABLE IV-I.—Nonsexual

Activity

Head-wrestle

Rump-nudge ..

Muzzle

Muzzle-handling

Limb-grabbing

Subjects*

i'-l

interaction

2 /

4

2

4

8

3

2d

177

28

7

81

24

analysis

Pd

0.558

0.088

0.023

0.253

0.076

D

44.2

14

1.8

10.1

8

• First sign initiates, second is recipient; 2f = total number of times activity occurred; 2d = total number of seconds

for each activity class; Pd = proportion of all allo-activity

time spent in a given activity; D = mean duration of activity

in seconds.

Anal-Genital Investigation Analysis

Anal-genital investigation accounted for 0.5 percent of total observation time and this was the

largest percentage of any observed contactual behavior (Table IV-J). Further evidence for such

an imbalanced participation in sexual behavior is

exhibited in an analysis of the anogenital presentation (Table IV-K).

Anogenital presentations were most frequently

observed subsequent to such allo-activities as muzzling, muzzle-handling, and limb-grabbing. As the

compound behaviors analysis indicates (Table

IV-L), the scrotal tongue-flick was often an accompaniment to these presentations.

"Compound Behaviors" (Table IV-L) refers to

two or more separate activities, which are participated in sequentially during one interaction

bout. They accounted for 0.21 percent of total

observation time and were interpreted to be ambivalence related.

TABLE IV-J.—Anal-genital

Subjects*

£-$

$

Q — it

$

2 /

10

1

17

68

investigation

2d

62

3

147

442

Pd

0.095

0.046

0525

0.675

analysis

D

62

0.5

8.7

63

• First sign initiator, second sign is the recipient.

2f = total number of times activity occurred; 2d = total

number of seconds for each activity class; Pd = proportion of

all allo-activity time spent in a given activity; D = mean

duration of activity in seconds.

Note that the female spends roughly 600% more time in

auto-investigation than the male and about 200% more time

in allo investigation.
NUMBER 213 103

9-8

TABLE

Subjects

IV-K.—Anogenital

» 2 /

29

presentation

2d D

403 2.7

• First sign initiator, second sign is the recipient.

2f = total number of times activity occurred; 2d = total

number of seconds for each activity class; D = mean duration

of activity in seconds.

TABLE IV-L.—Compound behaviors analysis

Grappling Analysis

Second to anal-genital investigation, grappling

accounted for the largest percentage of total observation time and was the only contactual behavior in which male and female participation was

almost equal. It should be noted (Table IV-N)

that sequential measures are very low in comparison with those of other contactual behaviors.

Subjects*

9-4

9-ct

9-ct

2 /

3

2

5

2d

71

87

117

Pd

0.258

0.316

0.425

D

23.6

43.5

23.4

Activities

Presentation /scrotal

tongue-flick

Presentation/grapple

Allogroom/grapple

3-9

9-8

TABLE

Subjects*

IV-N.—Grappling

2 / 2d

8 222

9 212

analysis

Pd

0.513

0.487

D

27.7

235

* First sign initiator, second is the recipient.

2f = total number of times activity occurred; 2d = total

number of seconds for each activity class; Pd = proportion of

all allo-activity time spent in a given activity; D = mean

duration of activity in seconds.

* First sign initiator, second is the recipient.

2f = total number of times activity occurred; 2d = total

number of seconds for each activity class; Pd = proportion

of all allo-activity time spent in a given activity; D = mean

duration of activity in seconds.

Tongue-flick Analysis

For each of the three separate contexts in which

it occurs, tongue-flicking is hypothesized to have a

different function. It can be an appeasement or

greeting gesture when it accompanies partnerfixation; it can have a cleaning and testing function when it is used against parts of the animal's

own body; and it can be a method of ascertaining

receptivity and promoting contact when it is used

against parts of the partner's body. Table IV-M

presents an analysis for all instances in which

tongue-flicking can occur.

TABLE IV-M.—Tongue-flick analysis

Subjects*

9-$

9-S

ct-9

$-9

9

$

2 / 2d Pd Circumstance

19

36

2

1

3

7

156 0.389

165 0.412

27 0.067

2 0.005

36 0.089

15 0.037

82

4.6

13.5

1

3

2.1

Scrotal

Fixation

Vulvar

Fixation

Vulvar

Scrotal

• First sign initiator, second is the recipient.

2f = total number of times activity occurred; 2d = total

number of seconds for each activity class; Pd = proportion

of all allo-activity time spent in a given activity; D — mean

duration of activity in seconds.

Note that female to male scrotal and fixational tongue-flicks

account for the largest percentages of total tongue-flick time.

INDIVIDUAL BEHAVIORS

Displays

Because these animals had been hand-raised,

they were extremely responsive to keepers and

sometimes to visitors, positive and negative reactions to a familiar face were registered in the

form of frequent and vigorous displays, occasionally accompanied by specific vocalizations.

The inverted quadrupedal display was observed

only in the male and occurred most frequently in

the early morning and afternoon hours when he

was involved in vigilant behavior. The display is

labeled "inverted" because the animal would climb

rapidly along an overhead pole in an upside-down

posture.

Olfaction-related Behaviors

Olfaction-related behaviors were recorded on

the basis of their possible connection with female

receptivity. It was hypothesized that as the female

became more solicitous and initiated more contact

a quantitative rise in female anogenital marking

and male urine-sniffing would occur. Table IV-O

presents data on anogenital marking, urine-sniffing,

and contact behaviors recorded during the same

time spans.
104 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

Although significant conclusions cannot be

drawn between contact- and olfaction-related behaviors on the basis of quantitative changes, differences in the intensity with which the animals

participate in the separate behaviors can be determined. Table IV-O illustrates that the female

initiates 89.3 percent of all contact, yet 37.2 percent of all olfaction-related behavior. Two hypotheses can be drawn: (1) Since male olfactionrelated behavior does not increase with solicitation

behavior in the female, but rather remains relatively stable, it may have a territorial and not an

investigative function, and (2) when the female is

receptive, it may be that instead of the male initiating contact with her, she initiates contact with

him on an even greater scale.

TABLE IV-O.—Marking and contact behavior analysis

4 Jun 11 Jun 20 Jun 28 Jun 10 Jul 18 Jul

Tf 33 <9)

Tf 7 (<$)

AGI210 ($)

AA 188 (9)

CC 98 ($)

SU 7 <<$)

AGI 134 (9)

CB 117 (9)

AA 157 (9)

Tf 123 (9)

AGI 161 (9)

CB 30 (9)

Tf 20 (9)

CB 103 (9)

AGI 23 (9)

AGI 104 (9)

Tf 275 (9)

AA 40 (9)

CC 52 ($) CC 174 ($) SU

AD

CC

8 (4) CC

2.5 (9) SU

26 ($) AD

118 (4)

0.5 ($)

2 (9)

AGI 56 ($)

AGI 29 (9)

CB 76.5 (9)

AA 52(9 )

CC

AD

22 («$)

125 (9)

Tf = tongue-flick; AGI = anal-genital investigation and presentation; AA = allo-activities;

CC = chin and chest mark; SU = sniffing urine; AD = anal drag; CB = compound behaviors;

(9)

 = female is initiator; ($) — male is initiator.

Description: Con tactual behaviors include grappling, compound behaviors, allo-activities, analgenital investigation, anogenital presentation, and tongue-flicking. All figures represent directional

measurements.

SUMMARY

A captive pair of Alouatta palliata was observed

twice daily for two months. Expressive movements,

postures, and vocalizations were described and

interpreted. Patterns of interaction were analyzed

quantitatively with the following conclusions being

drawn concerning social roles and structure:

(1) The male expends a large amount of time and

energy in vigilant behavior and associated displays.

(2) Male-female interaction is most often initiated by the female. (3) Grooming is of reduced

importance in social behavior. (4) Sexual activity

is initiated by the female and most often in the

form of the combination genital presentation and

tongue-flick to scrotum. (5) Marking and other

olfaction-related activities are performed regularly

by the male and are not correlated with the female's estrous cycle. (6) Male domination in the

form of ritualized mounting and supplanting is

not present in Alouatta.
Literature Cited

Altmann, S. A.

1959. Field Observations on a Howling Monkey Society.

Journal of Mammalogy, 40:317-330.

Andrew, R. J.

1963. The Origin and Evolution of the Calls and Facial

Expressions of the Primates. Behaviour, 20(1-2): 1-

110.

1964. Vocalization in Chicks, and the Concept of "Stimulus Contrast." Animal Behavior, 12:64-76.

Carpenter, C. R.

1934. A Field Study of the Behavior and Social Relations

of Howling Monkeys. Comparative Psychology Monographs, 19 (2): 1-168.

1935. Behavior of Red Spider Monkeys in Panama. Journal of Mammalogy, 16(3):171-180.

1965. The Howlers of Barro Colorado Island. Pages

250-291 in volume 1 of I. DeVore, editor, Primate

Behavior. New York: Holt, Rinehart and Winston.

Cherry, C.

1961. On Human Communication. 333 pages. Boston:

Massachusetts Institute of Technology Press.

Chevalier-Skolnikoff, S.

1973. Facial Expression of Emotion in Nonhuman Primates. Pages 11-90 in P. Ekman, editor, Darwin and

Facial Expression. New York: Academic Press.

Chivers, D. J.

1969. On the Daily Behaviour and Spacing of Howling

Monkey Groups. Folia Primatologica, 10:48-102.

Chomsky, N.

1957. Syntactic Structures. 116 pages. 'S-Gravenhage:

Mouton & Co.

Christen, A.

1974. Fortpflanzungsbiologie und Verhalten bei Cebuella

pygmaea und Tamarin tamarin. Fortschritte der

Verhaltensforschung, 14:1-79.

Clewe, T. H.

1969. Observations on Reproduction of Squirrel Monkeys

in Captivity. Journal of Reproduction and Fertility,

supplement, 6:151-156.

Collias, N., and C. Southwick

1952. A Field Study of Population Density and Social

Organization in Howling Monkeys. Proceedings of

the American Philosophical Society, 96:143-156.

Count, E.

1973. Being and Becoming Human. 259 pages. New York:

Van Nostrand Reinhold Company.

Crook, J. H.

1972. Sexual Selection, Dimorphism, and Social Organization in the Primates. Chapter 9 in B. Campbell,

editor, Sexual Selection and the Descent of Man.

Chicago: Aldine Publishing Company.

Dare, R.

1974. The Social Behavior and Ecology of Spider Monkeys

A teles geoffroyi on Barro Colorado Island. PhD

dissertation, Department of Anthropology, University of Oregon.

Dittus, W. J. P.

1974. The Ecology and Behavior of the Toque Monkey,

Macaca sinica. PhD dissertation, University of Maryland.

1975. Population Dynamics of the Toque Monkey, Macaca

sinica. In E. Tuttle, editor, Primates: Socio-ecology

and Psychology. The Hague: Mouton. £ln press.]

du Boulay, G. H., and M. A. Crawford

1968. Nutritional Bone Disease in Captive Primates. Pages

223-236 in M. A. Crawford, editor, Comparative

Nutrition of Wild Animals. 429 pages. London:

Academic Press.

Durham, N. M.

1971. Effect of Altitude Difference on Group Organization

of Wild Black Spider Monkeys (Ateles paniscus).

Proceedings of the 3rd International Congress of

Primatology, 3:32-40.

1975. Some Ecological, Distributional, and Group Behavioral Features of Atelinae in Southern Peru, with

Comments on Interspecific Relations. 18 pages. In

IXth International Congress of Anthropological and

Ethnological Sciences. [Preprint.]

Eisenberg, J. F.

1966. The Social Organization of Mammals. Handbuch

der Zoologie, VIII(10/7), 39:1-92.

1973. Reproduction in Two Species of Spider Monkeys,

Ateles fusciceps and A. geoffroyi. Journal of Mammalogy, 54:955-957.

1974. The Function and Motivational Basis of Hystricomorph Vocalizations. Pages 211-247 in Rowlands

and Weir, editors, The Biology of Hystricomorph

Rodents. London: Academic Press.

Eisenberg, J. F., L. R. Collins, and C. E. Wemmer

1975. Communication in the Tasmanian Devil (Sarcophilus

harissii) and a Survey of Auditory Communication

in the Marsupialia. Zeitschrift fur Tierpsychologie,

37:379-399.

Eisenberg, J. F., and R. E. Kuehn

1966. The Behavior of Ateles geoffroyi and Related Species.

Smithsonian Miscellaneous Collections, 151 (8): 1-63.

Eisenberg, J. F., N. A. Muckenhirn, and R. Rudran

1972. The Relationship between Ecology and Social Structure in Primates. Science, 176:863-874.

Epple, G.

1967. Vergleichende Untersuchungen iiber Sexual- und

Sozialverhalten der Krallenaffen (Hapalidae). Folia

Primatologica, 7:37-65.

105
106 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

1968. Comparative Studies on Vocalization in Marmoset

Monkeys (Hapalidae). Folia Primatologica, 8:1-40.

1975. The Behavior of Marmoset Monkeys (Callithricidae). Pages 195-235 in volume 4 in L. A. Rosenblum, editor, Primate Behavior: Developments in

Field and Laboratory Research. New York: Academic Press.

Epple, G., and R. Lorenz

1967. Vorkommen, Morphologie und Funktion der Sternaldruse bei den Platyrrhini. Folia Primatologica,

7:98-126.

Erikson, G. E.

1963. Brachiation in New World Monkeys and in Anthropoid Apes. Pages 135-163 in Napier and Barnicot,

editors, The Primates. 285 pages. London: Academic

Press.

Freese, C.

1975. Censusing Alouatta palliata, Ateles geoffroyi and

Cebus capucinus in the Costa Rican Dry Forest. In

Thorington and Heltne, editors, Distribution and

Abundance of Neotropical Primates. Washington,

D.C.: National Academy of Science. (In press.)

Gautier, J.-P.

1974. Field and Laboratory Studies of the Vocalizations

of Talapoin Monkeys (Miopithecus talapoin). Behaviour, 51:209-273.

Gensch, W.

1965. Birth and Rearing of a Black-faced Spider Monkey,

Ateles paniscus chamek Humboldt, at Dresden Zoo.

International Zoo Yearbook, 5:110.

Goodall, J. van Lawick

1968. The Behaviour of Free-living Chimpanzees in the

Gombe Stream Reserve. Animal Behaviour Monographs, 1 (3):1-311.

Goodman, L., and G. B. Wislocki

1935. The Cyclical Uterine Bleeding in a New World

Monkey (Ateles geoffroyi). Anatomical Record,

61:379-387.

Gould, E.

1971. Studies of Maternal-Infant Communication and

Development of Vocalizations in the Bats Myotis

and Eptesicus. Communications in Behavioral Biology, 5:263-313.

Grand, T.

1972. A Mechanical Interpretation of Terminal Branch

Feeding. Journal of Mammalogy, 5S(l):198-201.

1975. Motion Economy within the Forest Canopy: Horizontal and Vertical Displacement in Two Old and

Two New World Genera. In volume 4 of S. L.

Washburn and E. R. McCown, editors, Perspectives

on Human Evolution. [In press.]

Green, S.

1975. Variation of Vocal Pattern with Social Situation in

the Japanese Monkey (Macaco fuscata): A Field

Study. Pages 1-102 in volume 4 in L. A. Rosenblum,

editor, Primate Behavior. 420 pages. New York:

Academic Press.

Hampton, J. K., Jr., S. E. Hampton, and B. T. Landwehr

1966. Observations on a Successful Breeding Colony of

the Marmoset, Oedipomidas oedipus. Folia Primatologica, 4:265-287.

Hershkowitz, P.

1972. The Recent Mammals of the Neotropical Region:

A Zoogeographic and Ecological Review. Pages 311-

432 in Keast, Erk, and Glass, editors, Evolution,

Mammals and Southern Continents. 543 pages.

Albany: State University of New York Press.

Hill, W. C. O.

1962. Primates: Comparative Anatomy and Taxonomy,

V: Cebidae. Part B. Edinburgh: University Press.

Hinde, R. A., editor

1972. Non-verbal Communication. 443 pages. Cambridge,

England: Cambridge University Press.

HIadik, A., and C. M. Hladik

1969 Rapports trophiques entre vegetation et primates

dans la foret de Barro Colorado (Panama). La Terre

et la Vie, 1-169:25-117.

Hockett, C. F.

1960. Logical Considerations in the Study of Animal

Communication. Pages 392-403 in W. E. Lanyon

and W. N. Tavolga, editors, Animal Sounds and

Communication. 443 pages. Washington, D.C.:

American Institute of Biological Sciences.

Kellogg, R., and E. A. Goldman

1944. Review of the Spider Monkeys. Proceedings of the

U.S. National Museum, 96 (3186): 1-45.

Kleiman, D. G.

1975. A Review of Social, Sexual and Parental Behavior

in Monogamous Mammals. Quarterly Review of

Biology (submitted).

Kleiman, D. G., and J. F. Eisenberg

1973. Comparisons of Canid and Felid Social Systems from

an Evolutionary Perspective. Animal Behaviour,

21:637-659.

Klein, L. L.

1971. Observations on Copulation and Seasonal Reproduction of Two Species of Spider Monkeys, Ateles

belzebuth and A. geoffroyi. Folia Primatologica,

15:233-248.

1972. The Ecology and Social Organization of the Spider

Monkey, Ateles belzebuth. PhD dissertation, University of California, Berkeley.

1974. Agonistic Behavior in Neotropical Primates. Pages

77-122 in R. L. Holloway, editor, Primate Aggression, Territorially and Xenophobia. 513 pages.

New York: Academic Press.

Klein, L., and D. Klein

1971. Aspects of Social Behaviour in a Colony of Spider

Monkeys at San Francisco Zoo. International Zoo

Yearbook, 11:175-181.

Langer, S. K.

1973. Mind: An Essay on Human Feeling. Volume 2, 400

pages. Baltimore: Johns Hopkins Press.

Latta, J., S. Hopf, and D. Ploog

1967. Observation on Mating Behaviour and Sexual Play

in the Squirrel Monkey (Saimiri sciureus). Primates,

8:229-246.
NUMBER 213 107

Leyhausen, P.

1967. Biologie von Ausdruck und Eindruck. Psychologische

Forschung, 31:113-176.

Lorenz, K., and P. Leyhausen

1973. Motivation of Human and Animal Behavior: An

Ethological View. Translated by B. A. Tonkin.

New York: Von Nostrand Reinhold.

Marler, P.

1957. Specific Distinctiveness in the Communication Signals of Birds. Behaviour, 2:13-39.

1961. The Logical Analysis of Animal Communication.

Journal of Theoretical Biology, 1:295-317.

1970. Vocalizations of East African Monkeys, I: Red Colobus. Folia Primatologica, 13:81-91.

1972. Vocalizations of East African Monkeys, II: Black and

White Colobus. Behaviour, 42:175-197.

1973. A Comparison of Vocalizations of Red-tailed Monkeys and Blue Monkeys, Cercopithecus ascanius and

C. mitts, in Uganda. Zeitschrift fur Tierpsychologie,

33:223-247.

Mason, W. A.

1971. Field and Laboratory Studies of Social Organization

in Saimiri and Callicebus. Pages 107-137 in volume

2 of L. A. Rosenblum, editor, Primate Behavior,

New York: Academic Press.

Morris, C. W.

,1946. Signs, Language and Behavior. New York: Prentice

Hall.

Morton, E. S.

1970. Ecological Sources of Selection on Avian Sounds.

PhD. dissertation, Yale University, New Haven,

Connecticut.

1975. Ecological Sources of Selection on Avian Sounds.

American Naturalist, 109:17-34.

Moynihan, M.

1964. Some Behavior Patterns of Platyrrhine Monkeys,

I: The Night Monkey (Aotus trivirgatus). Smithsonian Miscellaneous Collections, 146(5):l-84.

1966. Communication in the Titi Monkey, Callicebus.

Journal of Zoological Society of London, 150:77-127.

1967. Comparative Aspects of Communication in New

World Primates. Pages 236-266 in D. Morris, editor,

Primate Ethology. 374 pages. Chicago: Aldine Publishing Company.

1970. Some Behavior Patterns of Platyrrhine Monkeys,

II: Saguinus geoffroyi and Some Other Tamarins.

Smithsonian Contributions to Zoology, 28:1-77.

Muckenhirn, N. A.

1966. Vocalizations of the Marmosets, Saguinus oedipus

oedipus and Saguinus oedipus geoffroyi. American

Zoologist, 6:550.

1967. The Behavior and Vocal Repertoire of Saguinus

oedipus (Hershkovitz, 1966) (Callithricidae, Primates). M.S. thesis, University of Maryland.

Napier, J. R., and P. H. Napier

1967. A Handbook of Living Primates. 456 pages. London:

Academic Press.

Newman, J. D., and D. Symes

1974. Vocal Pathology in Socially Deprived Monkeys.

Developmental Psychobiology, 7 (4):351-358.

Ogden, C. K., and I. A. Richards

1949. The Meaning of Meaning. London: Routledge &

Kegan Paul, Ltd.

Oppenheimer, J. R.

1968. Behavior and Ecology of the White-faced Monkey,

Cebus capucinus, on Barro Colorado Island, C.Z.

PhD dissertation, University of Illinois, Urbana.

1974. Social and Communicatory Behavior in the Cebus

Monkey. Pages 251-271 in C. R. Carpenter, editor,

Behavioral Regulators of Behavior in Primates.

Lewisburg, Pennsylvania: Bucknell University Press.

1975. Communication in New World monkeys. In T.

Sebeok, editor, How Animals Communicate. Bloomington: University of Indiana Press. [In press.]

Ploog, D., S. Hopf, and P. Winter

1967. Ontogenese des Verhaltens von Totenkopf-Affen

{Saimiri sciureus). Psychologische Forschung, 31:

1-41.

Ploog, D., and P. D. MacLean

1963. Display of Penile Erection in Squirrel Monkey

(Saimiri sciureus). Animal Behavior, 11:32-39.

Richard, A.

1970. A Comparative Study of the Activity Patterns and

Behavior of Alouatta villosa and Ateles geoffroyi.

Folia Primatologica, 12 (4):241-263.

Rosenblum, L. A., and R. W. Cooper, editors.

1968. The Squirrel Monkey. 451 pages. New York: Academic Press.

Schifter, H.

1968. Zucht und Markierungsverhalten von Wollaffen im

Zoologischen Garten Zurich. Der Zoologische Garten,

36(1-3): 107-132.

Smith, W. J.

1965. Message, Meaning, and Context in Ethology.

American Naturalist, 99:405-409.

1968. Message-meaning Analyses. Pages 44-60 in T. A.

Sebeok, editor, Animal Communication. 686 pages.

Bloomington: Indiana University Press.

Struhsaker, T. T.

1967. Auditory Communication Among Vervet Monkeys

(Cercophithecus aethiops). Pages 281-324 in S. A.

Altmann, editor, Social Communication among Primates. 392 pages. Chicago: University of Chicago

Press.

Trivers, R. L.

1972. Parental Investment and Sexual Selection. Chapter

7 in B. Campbell, editor, Sexual Selection and the

Descent of Man. Chicago: Aldine Publishing Company.

Tuttle, R.

1975. Musculoskeletal Evidence Bearing on Anthropoid

Phylogeny: Lessons on Parallelism. In Szalay and

Luckett, editors, Phylogeny of the Primates: An

Interdisciplinary Approach. New York: Plenum

Press. [In press.]

Van Hooff, J. A. R. A. M.

1967. The Facial Displays of the Catarrhine Monkeys and

Apes. Pages 7-68 in D. Morris, editor, Primate Etho-
108 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

logy. 374 pages. Chicago: Aldine Publishing Company.

Wagner, H. O.

1956. Freilandbeobachtungen an Klammeraffen. Zeitschrift

fur Tierpsychologie, 13:302-313.

Watkins, W. A.

1967. The Harmonic Interval: Fact or Artifact in Spectral

Analysis of Pulse Trains. Pages 15-43 in volume 2

of W. N. Tavolga, editor, Marine Bio-Acoustics.

Elmsford, New York: Pergamon Press.

Whorf, B. L.

1959. Language, Thought and Reality. 278 pages. New

York: John Wiley and Sons, Inc.

Wickler, W.

1961. Okologie and Stammesgeschichte von Verhaltensweisen. Forschritte der Zoologie, 13:303-365.

Williams, L.

1965. Samba and the Monkey Mind. 144 pages. London

and Becdes: William Clowers and Sons, Limited.

1967. Breeding Humboldt's Woolly Monkey at Murrayton

Woolly Monkey Sanctuary. International Zoo Yearbook, 7:86-89.

1968. Man and Monkey. 203 pages. Philadelphia and New

York: J. B. Lippincott Company.

Winter, P.

1972. Observations on the Vocal Behaviour of Freeranging Squirrel Monkeys (Saimiri sciureus). Zeitschrift fiir Tierpsychologie, 31:1-7.

Winter, P., P. Handley, D. Ploog, and D. Schott

1973. Ontogeny of Squirrel Monkey Calls under Normal

Conditions and under Acoustic Isolation. Behaviour,

47:230-239.

Winter, P., D. Ploog, and J. Latta

1966. Vocal Repertoire of the Squirrel Monkey (Saimiri

sciureus), Its Analysis and Significance. Experimental Brain Research, 1:359-384.

Zook, B. C, J. F. Eisenberg, and E. McLanahan

1973. Some Factors Affecting the Occurrence of Lead

Poisoning in Captive Primates. Journal of Medical

Primatology, 2:206-217.

U.«. GOVERNMENT PRINTING OFFICE: l»76 586-384/*4


Publication in Smithsonian Contributions to Zoology

Manuscripts for serial publications are accepted by the Smithsonian Institution Press, subject to substantive review, only through departments of the various Smithsonian museums. NonSmithsonian authors should address inquiries to the appropriate department. If submission is

invited, the following format requirements of the Press will govern the preparation of copy.

Copy must be typewritten, double-spaced, on one side of standard white bond paper, with

W'i" top and left margins, submitted in ribbon copy with a carbon or duplicate, and accompanied by the original artwork. Duplicate copies of all material, including illustrations, should be

retained by the author. There may be several paragraphs to a page, but each page should begin

with a new paragraph. Number consecutively all pages, including title page, abstract, text, literature cited, legends, and tables. The minimum length is 30 pages, including typescript and illustrations.

The title should be complete and clear for easy indexing by abstracting services. Taxonomic

titles will carry a final line indicating the higher categories to which the taxon is referable:

"(Hymenoptera: Sphecidae)." Include an abstract as an introductory part of the text. Identify

the author on the first page of text with an unnumbered footnote that includes his professional

mailing address. A table of contents is optional. An index, if required, may be supplied by the

author when he returns page proof.

Two headings are used: (1) text heads (boldface in print) for major sections and chapters and (2) paragraph sideheads (caps and small caps in print) for subdivisions. Further

headings may be worked out with the editor.

In taxonomic keys, number only the first item of each couplet; if there is only one couplet,

omit the number. For easy reference, number also the taxa and their corresponding headings

throughout the text; do not incorporate page references in the key.

In synonymy, use the short form (taxon, author, date:page) with a full reference at the

end of the paper under "Literature Cited." Begin each taxon at the left margin with subsequent lines indented about three spaces. Within an entry, use a period-dash (.—) to separate

each reference. Enclose with square brackets any annotation in, or at the end of, the entry.

For references within the text, use the author-date system: "(Jones, 1910)" and "Jones

(1910)." If the reference is expanded, abbreviate the data: "Jones (1910:122, pi. 20: fig. 1)."

Simple tabulations in the text (e.g., columns of data) may carry headings or not, but they

should not contain rules. Formal tables must be submitted as pages separate from the text, and

each table, no matter how large, should be pasted up as a single sheet of copy.

Use the metric system instead of, or in addition to, the English system.

Illustrations (line drawings, maps, photographs, shaded drawings) can be intermixed

throughout the printed text. They will be termed Figures and should be numbered consecutively; however, if a group of figures is treated as a single figure, the components should be

indicated by lowercase italic letters on the illustration, in the legend, and in text references:

"Figure 9b." If illustrations (usually tone photographs) are printed separately from the text as

full pages on a different stock of paper, they will be termed Plates, and individual components

should be lettered (Plate 96) but may be numbered (Plate 9: figure 2). Never combine the

numbering system of text illustrations with that of plate illustrations. Submit all legends on

pages separate from the text and not attached to the artwork. An instruction booklet for the

preparation of illustrations is available from the Press on request.

In the bibliography (usually called "Literature Cited"), spell out book, journal, and

article titles, using initial caps with all words except minor terms such as "and, of, the." For

capitalization of titles in foreign languages, follow the national practice of each language.

Underscore (for italics) book and journal titles. Use the colon-parentheses system for volume,

number, and page citations: "10(2) :5-9." Spell out such words as "figures," "plates," "pages."

For free copies of his own paper, a Smithsonian author should indicate his requirements

on "Form 36" (submitted to the Press with the manuscript). A non-Smithsonian author will

receive 50 free copies; order forms for quantities above this amount with instructions for payment will be supplied when page proof is forwarded.
i