M. MOYMH, Some Behavior

Patterns o

Platyrrhine Monkeys

FII. Saguinus geoffroyi

and Some Other Tamarins

SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY • 1970 NUMBER 28
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SMITHSONIAN CONTRIBUTIONS TO

ZOOLOGY

NUMBER 28

M. Moynihan Some Behavior

Patterns of

Platyrrhine Monkeys

II. Saguinus geoffroyi and

Some Other Tamarins

SMITHSONIAN INSTITUTION PRESS

CITY OF WASHINGTON

I97O
ABSTRACT

Moynihan, M. Some Behavior Patterns of Platyrrhine Monkeys. II. Saguinus

geoffroyi and Some Other Tamarins. Smithsonian Contributions to Zoology, 28:1-77.

1970.

The Rufous-naped Tamarin, Saguinus geoffroyi, is a rather small species of

Panama and northern Colombia. It is diurnal, slightly gregarious, omnivorous (with a

preference for insects), quadrupedal, and most characteristic of dense scrub and low

forest in areas of medium humidity. It interacts with some other species in peculiar

ways which may involve social mimicry. It has a few tactile and olfactory signals, a

moderate number of vocalizations, and many kinds of visual signals, mostly displays.

The communication systems of other members of the genus seem to be similar. They all

include points of resemblance to both the Night Monkey, Aotus, and the marmosets,

Callithrix and Cebuella. Some of the resemblances are difficult to interpret. The

phylogenetic relationships among the three types, and between them and Callicebus,

remain thoroughly obscure. There must have been considerable parallel or convergent

evolution of either behavioral or morphological characters during the history of the

group.

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Contents

Page

Introduction 1

Saguinus geqffroyi 1

Habitus 3

Social organization and territories 5

Relations with other species 7

Signal and other social behavior patterns of adults 11

"Pure" attack, escape, and fighting 12

Copulatory behavior 13

Allogrooming 15

Olfactory communication and related activities 16

Acoustic communication 21

Long Whistles 21

Twitters 25

Trills 29

Loud Sharp Notes 30

Soft Sharp Notes 31

Sneezing Sharp Notes 32

Long Rasps 33

Broken Rasps 35

Persistent infantile patterns 35

General comment 35

Visual communication 36

Some body and head movements 36

Apparently irrelevant acts 42

Tail patterns 45

Pilo-erection and "smoothing" patterns 52

Facial expressions 56

Significance of colors 58

General comment adult signal repertory 59

Behavior of infants and young juveniles 60

Appearance 60

Relations with parents 61

Infantile vocalizations 62

Other patterns 66

Signals of other species of Saguinus 66

Further comparisons 70

Previous descriptions of S. geqffroyi vocalizations 70

Signals of marmosets 71

Final comments 74

Summary 75

Acknowledgments 76

Literature cited 76

Illustrations

Page

1. A typical leaping posture of an adult Rufous-naped Tamarin 2

2. Rubbing postures of adult Rufous-naped Tamarins 16

3. A two-note Long Whistle series by an adult Rufous-naped Tamarin 22

4. The latter part of the second note and the whole of the third note of a three-note Long

Whistle series by an adult Rufous-naped Tamarin 22
SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

5. A Sharp Note followed by four Twitter Notes (Short Whines) by an adult Rufous-naped Page

Tamarin 26

6. A Twitter by an adult Rufous-naped Tamarin 26

7. A Twitter by an adult Rufous-naped Tamarin 27

8. A Trill by an adult Rufous-naped Tamarin 29

9. A Trill by an adult Rufous-naped Tamarin 29

10. Another Trill by an adult Rufous-naped Tamarin 30

11. The lower parts of two typical Loud Sharp Notes by an adult Rufous-naped Tamarin . . 31

12. The lower parts of two typical Sneezing Sharp Notes by an adult Rufous-naped Tamarin . 32

13. Two "Long" Rasps by an adult Rufous-naped Tamarin 33

14. A typical Broken Rasp by an adult Rufous-naped Tamarin 34

15. Miscellaneous visual signals of adult Rufous-naped Tamarins 37

16. Special postures and movements of adult Rufous-naped Tamarins 44

17. Special postures of the tail indicating alarm 47

18. Extreme but "loose" Upward Tail-coiling of adult Rufous-naped Tamarins 51

19. Copulation postures of Rufous-naped Tamarins 53

20. General Ruffle by an adult male Rufous-naped Tamarin in a stand-up posture ... . 54

21. A young juvenile Rufous-naped Tamarin uttering Infantile Squeaks 61

22. Vocalizations of a young Rufous-naped Tamarin 64

23. Vocalizations of a young Rufous-naped Tamarin 64

24. Vocalizations of a young Rufous-naped Tamarin 65

25. Vocalizations of a young Rufous-naped Tamarin 65
M. Moynihan Some Behavior

Patterns of

Platyrrhine Monkeys

II. Saguinus geoffroyi and

Some Other Tamarins

INTRODUCTION

The group of New World primates (or Platyrrhini)

which is most frequently recognized as a distinct assemblage includes the genera Callimico, Leontideus,

Saguinus, Callithrix, and Cebuella. (The genera accepted here, and their scientific names, follow Hershkovitz, 1958.)

Sometimes all the members of this group are called

"marmosets." It is more convenient, however, to restrict this name to species of Callithrix and Cebuella

and to refer to all the others as "tamarins."

Saguinus is the largest and most varied genus of

tamarins. It also is the most widely distributed, ranging

through a large part of warm tropical South America

and a small part of Central America.

The only Central American form should be called

geoffroyi, according to Hershkovitz (1949). It may be

provisionally recognized as a distinct species. (Hershkovitz, 1966, relegates it to the status of a subspecies of

S. oedipus. He does not, however, cite his evidence in

favor of this arrangement. The two forms certainly are

closely related, but they differ in some characters which

may be of considerable biological significance. See also

below.)

Saguinus geoffroyi does not have any generally

recognized English vernacular name which is both

M. Moynihan, Director, Smithsonian Tropical Research Institute, P.O. Box 2072, Balboa, Canal Zone.

suitable and exclusive; i.e., which has not also been

applied to other species. I would suggest, therefore,

that it be called "the Rufous-naped Tamarin." This

emphasizes the most conspicuous of its distinctive

morphological features.

The social behavior of the Rufous-naped Tamarin

is the principal subject of the following account. A few

other forms of Saguinus will be discussed very briefly,

and some behavior patterns of the genus will be compared with those of other New World primates, especially other types of tamarins, marmosets, the Night

Monkey (Aotus trivirgatus), and titi monkeys (Callicebus moloch and C. torquatus). All references to the last

two genera are based upon Moynihan (1964 and

1966). All references to other Platyrrhini are based

upon personal observation (summarized in Moynihan,

1967) unless specifically stated otherwise.

SAGUINUS GEOFFROYI

This is a rather small monkey (medium sized for a

tamarin). Individuals of both sexes have the same

color pattern, which is quite complex (see the accompanying illustrations). The face is largely bare (more

so in adults than in young) and dark gray in color,

but there are stripes of white hair on the cheeks and

the sides of the nose or snout. There also is a triangular

patch or "blaze" of white on the forehead and front

of the crown, and the sides of the bare face are framed

by another pair of whitish stripes (passing behind the
SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

FIGURE 1.—A typical leaping posture of an adult Rufous-naped Tamarin, with Tail-ruffling.

naked black ears). The rear part of the head and the

nape are chestnut or rufous red. The upper part of the

body is largely brindled black and grayish-yellow (the

precise arrangement of black and yellow differs considerably in different individuals). The underparts

and most of the arms and legs are white, sometimes

tinged with yellowish-orange on the breast and belly

(see also page 21). The proximal part of the tail is

deep rufous, and the distal part is black (with a white

tip in all or most infants and young juveniles).

As a whole, this pattern is conspicuous in some circumstances and "disruptive" in others.

The species ranges from the Choco region of northern Colombia to at least central Panama.

In Panama, it seems to be most characteristic of

regions of moderate humidity. The Pacific side of the

isthmus is generally less humid than the Atlantic side.

Rufous-naped Tamarins are abundant in some parts

of the Pacific coastal region, and also occur in some

central areas approximately equidistant from both

coasts. To my knowledge, however, they are completely

absent from the whole of the Atlantic coast of the

isthmus, except for one small, highly modified or

"unnatural" area (see below).

They also are most common in forest and scrub

which are dense but not very tall. They do not seem

to flourish in either high rain forest or mature humid

seasonal ("monsoon") forest with little understory

vegetation.
NUMBER 2 8

This may be illustrated by the history of the species

on Barro Colorado Island. The island is located in

Gatun Lake, in the center of the Canal Zone in central

Panama, and has a rather humid climate. Nevertheless, tamarins were abundant there in the 1920s and

early 1930s (Chapman, 1929, and Enders, 1935),

when much of the island was covered with obviously

young second-growth forest. Since then, the forest

has been allowed to grow up, and large parts of it

seem to be approaching maturity, becoming typical

monsoon forest (Bennett, 1963). During the same

period, with the gradual change in the vegetation,

the tamarins have become increasingly rare.

The one area on the Atlantic coast where tamarins

are definitely known to occur is the Atlantic side of

the Canal Zone and adjacent parts of the Republic

of Panama, where all or most of the original forest

has been destroyed by human activities and replaced

by second growth. In all probability, the tamarins have

invaded this area only recently.

It is conceivable that some aspects of the ecology

of the species are different in Colombia. Much of the

Choco region is very humid indeed. Unfortunately,

however, it is not known if the tamarins occur throughout the region as a whole or only in particular, restricted, and possibly drier, areas within it.

During the course of the present study, I observed

a substantial number (at least 125) wild Rufous-naped

Tamarins living in more or less natural conditions.1

Most of my observations were made in three different areas of the isthmus of Panama: (1) Ancon Hill,

an "enclave" between the towns of Balboa and Ancon,

on the Pacific coast, east of the canal; (2) near several

roads (currently called K-6 and K-9), and in the

adjacent Rodman Naval Station, on the Pacific coast,

west of the canal; and (3) in the Canal Zone Forest

Reserve, in the center of the isthmus approximately

10 miles north of Balboa. Most of Ancon Hill is

covered by dense vegetation which could be described

either as tall 6crub or low forest. Some of this may be

mature. It may be prevented from growing higher by

edaphic factors (the rocky soil and steep slopes of the

hill). The area on the west side of the canal includes

1

 Obviously, no conditions in Panama or adjacent regions

at the present time are really completely natural. Man's influence has been exerted everywhere, in some form or another,

for thousands of years. But the term "natural conditions" is

useful, and will be used in this paper, as a general label

for environments and situations in which man and his artifacts are not overwhelmingly evident at all times.

a variety of different types of young second-growth

forest and scrub. Most of the Reserve is composed of

somewhat older second-growth forest.

Briefer observations of a few wild individuals were

made on Barro Colorado Island, on the Atlantic side

of the Canal Zone, and in the lower hill forest of Cerro

Campana approximately 30 miles west of the Canal

Zone.

I also studied some 35 individuals kept in captivity.

These animals were housed in a variety of cages and

pens of different sizes and shapes on Barro Colorado

Island. (The pens were outside in the forest. They were

made of wire netting, and roofed with the same material. The animals in the pens were given food, but

left exposed to the external climate. They did very

well in these circumstances, and some of them bred.

This would suggest that the recent decrease of the

wild tamarin population on the island may have been

due to increasing scarcity of suitable food in the maturing forest.)

Both wild and captive individuals were observed

intermittently, at very irregular intervals, between

August 1958 and August 1967.

Habitus

Rufous-naped Tamarins are essentially arboreal insofar as they almost always prefer to remain in trees or

large bushes. They do come down to the ground

occasionally, but apparently only in special circumstances ; e.g., in order to get certain special foods, such

as the fruits of Cardulovica palmata (C. M. Hladik,

personal communication) or when they cannot pass

from one bush or tree to another by any other means.

In forest, they move through a wide range of heights

above ground. In areas such as the Forest Reserve, they

are most frequently seen between 10 and 40 feet above

ground. They may go much higher in certain other

environments. They usually move and feed near the

edges of forest and scrub; and they seem to like the

vicinity of the upper edges, the top of the forest, at

least as well as areas near the lateral borders. Thus, the

relatively few individuals inhabiting very tall forests,

such as the remnant on Barro Colorado, frequently

range as high as 60-75 feet above ground.

It should be stressed that this preference for the

vicinity of edge is not quite the same thing as a

preference for edge itself. Rufous-naped Tamarins ob-
SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

viously try to remain several inches, or even feet,

inside the outermost or uppermost limits of the edge.

This habit may be protective, an adaptation to reduce

vulnerability to aerial predators. (I have never seen

tamarins actually preyed upon. And the only reliable

record of apparent predation is an observation by N. G.

Smith, personal communication, who saw a Tayra,

Eira barbara, carrying a dead tamarin in its mouth.

M. H. Robinson, personal communication, has observed extreme alarm reactions to snakes by captive

tamarins. But it is obvious that these monkeys are at

least as frightened of most birds of prey. In my experience, they keep a weather eye out for possible aerial

predators much more consistently than for any other

kind of danger. And their reactions to the actual appearance of a hawk usually are quite unmistakable. See

page 10.)

Under natural conditions, they move along a great

variety of tree trunks and branches of very diverse

sizes. They also show a strong preference for dense

"tangles" of vines or lianas. They usually avoid palms

and other large monocotyledons such as Heliconia and

related genera (except when they are searching for a

few special foods and/or the leaves of a monocotyledon

provide the only convenient "bridge" between other

trees or bushes which are particularly favored).

They are almost completely quadrupedal. They only

stand up on their legs (hind limbs) very occasionally,

during certain disputes (see page 39) or to get a

better view of some distant animal or object. They

usually run on the ground and on branches in much

the same way as squirrels. But they tend to leap

from branch to branch somewhat more frequently than

do the squirrels which occur in the same habitats, and

their leaps seem to be somewhat longer on the average

(see also Figure 1). Their tails are not really or fully

prehensile. In locomotion, they are used only as balancing "counterweights" or signaling organs (see page

45 et seq.). When an individual sits or stands, however, it may "drape" its tail over an adjacent branch;

and this may enhance the stability of its position or

posture.

The diet of the species is being studied by C. M.

Hladik at the present time. All I can say, here, is that

it seems to be broad and varied. Captive individuals

show a definite preference for insects, which they hunt,

catch, and eat very efficiently. Some of their searching

and catching methods are described by M. H. Robinson (in press). They also catch and devour small

lizards of the genera Anolis and Mabuya (Robinson,

personal communication), and will eat freshly killed

bats and small birds. Wild individuals obviously search

for and try to catch insects, but apparently they are

frequently unsuccessful. During my own observations,

most of the foods seen to be taken were vegetable, including a wide assortment of fruits and buds. Insects

probably are less abundant, or less immediately available, than fruits and buds in many of the environments

inhabited by the species, at least at certain times of the

day or periods of the year. Nevertheless, it is quite

possible, even probable, that an appreciable amount

of animal food is absolutely essential to the tamarins.

If so, this may help to explain some aspects of their

choice of habitats, periods of activity, and social behavior (see pages 7 and 8).

They seem to be completely diurnal. Captive individuals always spend the night in boxes or holes in

tree trunks, whenever these are available. It seems

very probable that wild individuals also sleep in holes

in trees at night. I have never seen them actually enter

or leave such holes; but many individuals were seen to

move toward tall trees which were known to have suitable holes in the late afternoon or evening, and then

reappear in the same places in the morning.

Their activity rhythm during the day is highly distinctive. Unlike the other diurnal monkeys with which

I am familiar, and most other diurnal mammals and

birds in the same habitats, these tamarins do not become active at, or very shortly after, dawn. In the wild,

they are never seen moving around until at least a

quarter of an hour after it has become fully light. In

most cases, they apparently do not get up until approximately three quarters of an hour, or more, after full

light. (This habit may be advantageous for several

reasons—see also below. But it is so remarkable that

one wonders if the animals do not become torpid or

semi torpid at night.) After arising, they remain quite

active throughout most of the rest of the day. They

may rest briefly in the middle of the morning. But,

(again) unlike most other diurnal tropical mammals

and birds, they usually show little or no tendency to

slow down or take a "siesta" at noon or during the first

part of the afternoon, when the heat is greatest. It is

only approximately an hour or half hour before sunset

that they gradually stop feeding and drift off in the

general direction of their sleeping trees.
NUMBER 2 8

Social Organization and Territories

My observations of the social organization of Rufousnaped Tamarins in the wild were restricted in several

ways. No attempt was made to follow individuals or

groups continuously for long periods of time, simply because much of the vegetation in most of the areas inhabited by the species is too dense to permit quiet movement by a human observer. Instead, I repeatedly returned to particular places, more or less open paths and

clearings (cleared long before this study began), and

observed the animals whenever they appeared and as

long as they remained in view. In some areas, where

there was a fairly extensive network of paths and clearings, it was possible to obtain a rather detailed impression of many of the social activities of the animals

throughout the day.

None of the individuals observed in the wild was

collected, as it was considered undesirable to alarm

other animals in the neighborhood. Nor were any

wild individuals marked artificially. Thus, it often was

impossible to identify adults personally, especially when

all the members of a group were not visible simultaneously, or even to be sure of the sexes of particular

animals. (There is little or no sexual dimorphism in

size; and the sex organs are not distinguishable at a

distance.) But infants and juveniles usually could be

identified by their relative sizes, and some adults could

be recognized by certain distinctive morphological

characters (e.g., variant color patterns) and/or some

consistent peculiarity behavior.

Rufous-naped Tamarins tend to be more gregarious

than Night Monkeys, insofar as they may form "bands"

which include more than a single adult pair with their

young of the year. Some of these bands also are larger

than the family groups which seem to be the typical

"basic" social units of most Callicebus moloch observed

in the wild (Mason, 1966).

Nevertheless, there is considerable variation in the

actual size of geoffroyi groups. At one extreme, it is

not uncommon to see apparently single individuals.

At the other extreme, I have seen groups which included six or more individuals.

This may be illustrated by the figures in Table 1.

They show the sizes of 28 social units (groups and apparently single individuals) observed under particularly

favorable conditions in all the environments in which

the species was studied.

TABLE 1.—Social Units of Saguinus geoffroyi

in the Wild

Number of

Individuals per Unit

1

2

3

4

5

6

9

Number of

Units Seen

5

6

5

5

2

4

1

The total number of units counted was 28. The total number

of individuals counted was 95. The average number of individuals per unit was 3.39.

All the single individuals seen were apparently adult. All the

groups of two also were composed of adults, presumably mates

in all or most cases. Some groups of three included one individual which was obviously young. And all the larger groups

ncluded one or more young.

Most Rufous-naped Tamarin social units seem to

be quite stable. Groups of the same size, sometimes including identifiable individuals, can be seen in the same

areas day after day for months on end. Naturally,

some individuals disappear from time to time, and

appreciable numbers of young are born each breeding

season. But most of these changes are "accommodated"

with minimal disturbance of the pre-existing social

structure. I saw only one case of a "permanent"

merger between two groups which had appeared to

be distinct earlier, and no cases of permanent splitting

of a large group.

Infants usually are carried by a parent, and young

juveniles either are carried by or remain close to a

parent (see also page 61). Adults and older juvenile

members of a band sometimes stray 500 feet or more

from (well out of sight of) the nearest other member

of the band—or get left far behind when the rest of

the group moves on—but this is not particularly common. Usually the adults and older juveniles are only

3-30 yards apart. And even the individuals which

become most widely separated usually rejoin their

companions, or are rejoined, within minutes rather

than hours.

In view of the occasional variations which do occur,

it may be useful to explain how the figures in Table

I were derived. All the social units recorded in this

table were observed for at least one-half hour. Most

were observed repeatedly for at least several hours on

different days. In a few cases, what was largely the
SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

same unit was recorded twice. This occurred when

there was a definite change in the composition of a

group, an apparently permanent subtraction or addition of one or more individuals. In these cases, the

unit was counted and recorded once before the change

and once afterward. But none of these counts was

made during the time of year when most of the young

are born, when fluctuations in numbers are most frequent (see page 13).

It should also be noted that these counts probably

do not convey a perfectly accurate picture of the "normal" population structure of the species under completely "normal" conditions. Possibly, I overlooked one

or more individuals in some counts of the larger groups.

More important, Rufous-naped Tamarins are hunted

intensively in many areas, such as some of those west

of the canal, and this certainly must affect the average

size of groups.

Thus, it seems likely that the population of geoffroyi

in central Panama has been affected in two different

and partly contradictory ways by human settlement

and activities. The cutting of mature forest, followed

by shifting agricultural activities and the subsequent

spread of second growth, probably has increased the

area of habitats suitable for tamarins. But hunting

probably has reduced the density of tamarin populations in all or most of the most favorable localities.

Chapman (op. cit.) states that geoffroyi individuals

occur in groups as large as 12 or more. Various inhabitants of the Canal Zone have reported seeing

equally large groups in recent years. I think, however,

that many or all of these recent records must be gross

over-estimates.

Apart from some parent-young relations, there

usually are very few overt, conspicuous, indications of

special personal connections among the members of

a large band in the wild. Certainly, none of the groups

observed was found to have a definite "leader," consistently controlling or initiating group movements. But

the appearance of general social homogeneity probably

is misleading. More precise and detailed studies probably would reveal that some individuals are dominant

over others and/or usually are more friendly to some

fellow members of the group than to others. There certainly were some dominant-subordinate relationships

among the tamarins kept in captivity. Even more important, the captive individuals tended to form definite

pair bonds. When several males and females were kept

together, each individual tended to select an individual

of the opposite sex as its "mate." Mates tended to associate more closely with one another than with the other

individuals in the same cage, to perform all or most of

their copulatory behavior together, and to fight with

one another less frequently than with other individuals

(see also below). Some of the pair bonds between captives were not only strong but long sustained, enduring

for at least four years (as long as my observations continued in any given case). Of course, it seems overwhelmingly probable that the groups of only two adults

(alone or with young) observed in the wild also were

pairs of mates. Perhaps the members of larger groups

in the wild are equally likely to form semipermanent

sexual attachments among themselves. If so, their pair

bonds may not be conspicuous, to a human observer,

simply because mates do not stick particularly close

together during the daily search for food. (I might

add that I never saw copulations in the wild; i.e., I did

not see the reactions which should reveal the existence

of pair bonds most clearly.)

Each band of tamarins (and probably each individual living by itself alone) has its own "home range."

These ranges may also be considered territories. They

are defended, although usually in a rather peculiar way

(see page 23). As would be expected, in view of the

usual structure of social units, they tend to be quite

stable for long periods of time. They also are quite large

on the average. They are very diverse in shape, presumably in correlation with variations in topography

and vegetation; but many of them extend for more

than a quarter of a mile along their longest dimension.

These ranges are comparable in size to those of families or bands of other species of Platyrrhini in central

Panama, such as the Night Monkey, the capuchin,

Cebus capucinus (J. R. Oppenheimer, personal communication) , and the howler, Alouatta palliata—or A.

villosa—(Carpenter, 1934). They are very much larger

than the ranges of Callicebus moloch families in Colombia (Mason, op. cit.).

Rufous-naped Tamarins always or almost always

move through a large part of their ranges every day.

They may even cover the whole of their ranges several

times during the course of a single day. In this extreme

mobility and speed of progression, they resemble both

Cebus capucinus and (probably) Aotus, but differ

greatly from Alouatta. Bands of howlers usually move

through only a small part of their ranges each day

(Carpenter, op. cit.). Callicebus moloch groups also

cover all or most of their ranges each day; but their
NUMBER 2 8

ranges are so small that their travels usually are comparatively slow, and their degree of mobility is much

more like that of Alouatta than like that of S. geoffroyi

or C. capucinus.

These differences probably are correlated with,

causally related to, differences in feeding ecology.

Alouatta seems to be as nearly completely vegetarian

as any primate known, and Callicebus moloch is hardly

less so (Mason, op. cit.). These species apparently can

find sufficient vegetable food, at least on any given day,

in comparatively small areas. But the other species may

have to move over large areas repeatedly and rapidly

in order to obtain the insects and other animal foods

that probably are essential to them.

There is very little overlapping of ranges among

Rufous-naped Tamarins. Only very rarely will individuals trespass a few feet or yards into the normal ranges

of others. And most trespassing seems to occur when

the owners of the areas intruded upon are far way, at

the opposite ends of their territories, at the time. In

this respect also, the tamarins resemble the Cebus capucinus, Callicebus moloch, and (probably) Aotus; and

differ from Alouatta. (Overlaps of ranges are relatively

frequent among bands of howlers in Panama. This presumably is an inevitable consequence of the combination of large ranges with slow movements of individuals through the ranges.)

Tamarins whose ranges border on areas not occupied

by other individuals of the same species (probably, in

most cases, areas which are usually unfavorable at most

times of the year) may make long "excursions" in exceptional circumstances. Thus, for instance, there

usually are no tamarins in the gardens of the town of

Balboa. But these gardens sometimes are invaded by

tamarins who come to feed on mangoes when the fruit

is ripe. The invaders obviously have descended from

Ancon Hill. They probably are able to enter the gardens because there is no resident population of their

own species to bar their way.

Such exceptional behavior indicates that Rufousnaped Tamarins are "opportunistic." Some individuals

of the species probably are constantly "probing" new

areas to determine if they are both available and suitable for occupancy.

Relations with Other Species

Many other species of vertebrates feed on the same

fruits and buds as S. geoffroyi and search for and

catch insects in the same places. Some of the same species, and many others, also compete with geoffroyi for

other features of the environments; e.g., branches to

move along, holes to sleep or nest in, shelters from

heavy rain, and lookout posts.2 As would be expected,

therefore, the social, ecological, geographical, and

temporal relations and interactions among the tamarins

and some of the other species are complex and /or

highly specialized.

The other primates which occur in Panama are

are Alouatta palliata (or villosa), Ateles "geoffroyi"

panamensis, Ateles "fusciceps" robustus, Cebus capucinus, Saimiri "oerstedi," and Aotus trivirgatus.3

Alouatta, Ateles, and Cebus are (or were at one

time) widespread in Panama. They also are diurnal.

But they are all much larger than S. geoffroyi, and

largely or completely inhabitants of tall forest. C. capucinus, the smallest and least vegetarian of these large

forms, is the only one which might compete with the

tamarins to any appreciable extent. But I have never

seen any overt behavioral interactions between the two

species, or even observed them in the same area at

the same time. And 5. geoffroyi is so rare in the areas

where capucinus is common that one cannot be sure

that the usual lack of contact between them is not

purely accidental.

2

 The terms "compete" and "competition" are used in a

very broad or probabilistic sense in this paper. Two animals

will be said to compete with one another when one occupies or uses a resource which otherwise would be available

to the other. It is assumed that the second animal would be

in a position to utilize the resource if it were not already preempted by the first. This assumption seems very highly

probable in all the examples cited, but I have no conclusive evidence to prove it in any given case. It also is assumed,

and seems to be equally probable, that the resource being

used or occupied is actually or potentially in short supply

and/or that some examples of the resource are more "favorable" or "advantageous" than others. (This latter statement

may be clarified by an example. There obviously are many

lookout posts in any given patch of forest, but some are much

better placed; e.g., give better views of possible sources of

food and/or danger, than are others. An individual occupying a better placed post presumably has a significant advantage over an individual occupying a less well placed post.)

3

 As noted in Moynihan (1967), all the forms of Ateles s.s.

may be conspecific. Certainly, A. "geoffroyi" panamensis and

A. "fusciceps" robustus hybridize in Panama (or did hybridize until a very few years ago, before their populations were

greatly reduced by hunting). It also is possible that Saimiri

"oerstedi" is only a well-marked subspecies of S. sciureus.
8 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

(C. M. Hladik [personal communication] saw individuals of the two species close together once. The

tamarins were uttering Loud Sharp Notes—see

below—and performing other alarm reactions. These

behavior patterns appeared to be directed toward the

capucinus.)

Possible relations between Rufous-naped Tamarins

and Squirrel Monkeys of the genus Saimiri are even

more problematical. It is not definitely known that

they ever come into actual contact with one another.

Squirrel Monkeys have been observed and collected

in many areas of the province of Chiriqui, the westernmost of the Pacific coastal provinces of Panama, approximately 250-300 miles west of the Canal Zone

(see, for instance, Goldman, 1920). They certainly

are still abundant in some parts of the province (personal observation). To my knowledge, there are no

published records of the species east of Chiriqui in the

isthmian region. As noted above, Rufous-naped

Tamarins certainly occur in the eastern half of the

Pacific side of Panama, from the Colombian border to

Cerro Campana, approximately 30 miles west of the

Canal Zone. They are abundant in many areas at least

as far west as the Zone. On Cerro Campana, they have

been seen only around 1000-1500 feet elevation. These

facts are well established. They do not, in themselves,

indicate sympatry between the two species. But there

are other data which tend to confuse the issue. There

is one recent and reliable sight record of a small band

of Squirrel Monkeys at 3000 feet elevation on Cerro

Campana (F. A. McKittrick and N. G. Smith, personal

communication). There is a nineteenth-century record

of a Rufous-naped Tamarin from Chiriqui (Alston,

1879). This was questioned by Goldman (op. cit),

who noted that there had been no further records of

the species from this province up to his own time. But

Carpenter (1935) says that the species occurs in the

Coto region of Chiriqui, although "very scarce" there.

He does not, however, expressly state that he saw any

individuals himself. Two brief visits by members of

the staff of the Smithsonian Tropical Research Institute to the Burrica Peninsula, the countryside around

Puerto Armuelles, and coastal areas south of David,

all in Chiriqui, in February and July of 1967, failed to

reveal any tamarins. Many other visits by some of the

same and other scientists to Pacific side areas between

Cerro Campana and Chiriqui have not produced any

records of either species.

Thus, even if the two species are not completely

allopatric, they are nowhere both abundant in the

same area. It seems very likely, in fact, that they

definitely tend to exclude one another. They are at

least potentially strong competitors. Squirrel Monkeys

are comparatively small, only slightly larger than S.

geoffroyi, and apparently completely diurnal. In Panama, they also are primarily animals of second growth

and forest edge. They certainly feed on vegetable matter, and search for insects, in much the same way as

tamarins. The only obvious ecological difference between the two species in Panama is that all or most of

the areas inhabited by Squirrel Monkeys are usually

more humid than most of the areas inhabited by

tamarins. It probably would not be too much of an

oversimplification to say that Squirrel Monkeys fill

the "Rufous-naped Tamarin niche" in wet forest edge

and second growth in Panama, while Rufous-naped

Tamarins fill the "Squirrel Monkey niche" in most

slightly drier areas of superficially similar vegetation.

Either species would be expected to extend its range if

the other became extinct.

Aotus certainly is broadly sympatric with S. geoffroyi.

It occurs throughout most of Panama, in both tall

forest and at least some of the second-growth areas

inhabited by tamarins. Like Saimiri, it is only slightly

larger than S. geoffroyi. It eats some of the same types

of fruits and buds, and possibly some of the same species

of insects. It even sleeps in holes in trees. It is, however,

completely "separated" from the tamarins in being

completely nocturnal (and crepuscular) under natural

conditions.

Probably equally or more important to the tamarins

are many species of birds, especially flycatchers of the

family Tyrannidae. These are all diurnal. Many of

them are sympatric with tamarins in Panama, and

have overlapping feeding habits. They also eat the

same berries and fruits, and catch insects in many of

the same places (although usually not with the same

techniques).

Some of the sounds uttered by some of the flycatchers, e.g., Myiozetetes spp., Tyrannulus elatus,

Legatus leucophaius, Elaenia flavogaster, and Megarynchus pitangua, are similar to certain tamarin

sounds, i.e., Trills and Long Whistles (see below), in

form and pitch or tone, and possibly even motivation

and function in some cases. (All names of birds cited

throughout this paper follow Eisenmann, 1955.) As

noted in Moynihan (1968a), it is possible, even

probable, that some of these resemblances among fly-
NUMBER 2 8

catchers and tamarins are examples of "social mimicry." The tamarins may recognize areas that are

favorable; i.e., in which food is abundant, simply

because they hear many flycatcher sounds, similar to

their own, coming from them.

It probably is significant, therefore, that the flycatchers also are partly separated from the tamarins by

differences in timing.

Like most other diurnal birds (see above), the flycatchers are most active during the first hour or so

after dawn, and tend to slow down during the middle

of the day—in contrast to the tamarins which get up

later in the morning, but remain active almost continuously afterwards. Both flycatchers and tamarins

probably feed most frequently during their periods

of greatest general activity. Thus, the tamarins probably do not compete with the flycatchers for food

during most of the period when the birds are feeding

most intensively, but they do feed frequently at the

time when the birds are resting.

This distinction may be exaggerated by another

factor. Data collected by C. M. Hladik (personal communication) suggest that tamarins may eat relatively

more fruit in the morning (presumably they are most

hungry then, and take everything that comes to hand)

and relatively more insects in the afternoon (when they

may be more discriminating). If the flycatchers take

as many insects, per unit time period, in the morning

as in the afternoon—as seems quite possible—this

might tend to reduce interspecific competition for the

most nourishing (protein) foods even further.

The flycatchers also vocalize most frequently early

in the morning before the tamarins get up. This may

facilitate intraspecific communication. Simply because

some of the sounds of tamarins and flycatchers are so

similar, they might tend to get their signals confused

if they were all vocalizing with maximum frequency

simultaneously. But this possible difficulty also is

avoided or reduced by the different activity rhythms of

the different species.

(These contrasts should not be interpreted as evidence against the existence of mimicry. Although

flycatchers vocalize less frequently during the middle

of the day than at dawn, they continue to be noisy

enough at all times to permit the tamarins to notice

them and to assess the suitability of different areas by

the comparative frequency of flycatcher sounds coming

from them.)

The fact that S. geoffroyi is more or less effectively

separated from most of the principal competitors with

which it is broadly (or frequently) sympatric, i.e., both

Aotus and the flycatchers, in essentially the same way,

i.e., by differential timing, would seem to indicate

that this type of segregation is highly advantageous in

the Panamanian environment.

It may, in fact, have one widespread general advantage in almost all areas, in relations among almost

all species, plus a variety of other advantages in more

limited sets of circumstances, in relations between particular individual species or small groups of species.

The general advantage probably is that it provides

separation without fighting, and the consequent risk

of physical injury, or the waste of time which might be

entailed by the repeated performance of "repellent"

interspecific displays (the only other "easy" ways of

maintaining segregation among sympatric competing

forms). This, in itself, must always be useful to some

extent.

It may be the only advantage involved in the separation of Night Monkeys from Rufous-naped Tamarins. The segregation of these two species probably is

maintained by adaptations which are "mutual," although not necessarily exactly equivalent. From the

point of view of Rufous-naped Tamarins, it probably

is advantageous to avoid encounters with Night Monkeys simply because such encounters might turn hostile and Night Monkeys are just large enough to be

potentially dangerous opponents. Aotus, on the other

hand, may have evolved (or retained) its nocturnal

habits as an adaptation to reduce or control competition with a great many other species in addition to

5". geoffroyi. Its geographic range is very much larger

than that of geoffroyi, extending over more of Central

America and most of tropical South America. Its

nocturnal habits must limit the amount or severity

of competition with many other species of Platyrrhini,

including other tamarins, Saimiri, Callicebus spp.,

Pithecia spp., and Cebus spp., some of which are larger

and/or have more highly specialized and possibly more

efficient methods of locomotion and feeding.

A comparable factor may be involved in the relations between S. geoffroyi and the flycatchers. Rufousnaped Tamarins probably could not repel organisms as

extremely mobile as birds without expending a great

deal of energy over considerable periods of time.

Even more important, however, they cannot "afford" to repel flycatchers too effectively if they are to

rely upon the birds as indicators of favorable areas.
10

The peculiar activity rhythm of Rufous-naped

Tamarins—so different from that of most other comparable species in the same environment—suggests

that the special relationship between the tamarins and

the flycatchers is essentially "one-sided." The tamarins

seem to have adjusted their activities to those of the

birds; but there is no evidence that the birds have adjusted their activities to those of the tamarins.

Of course, this sort of relationship must have disadvantages as well as advantages. If the tamarins are

"dependent" upon the flycatchers as suggested here,

they are using what might be called "indirect" clues to

locate necessary resources. There is reason to believe

(Moynihan, 1968b) that species which use indirect

clues comparatively frequently will tend to be more

opportunistic (see also page 7), and consequently

better able to colonize "new," previously unfamiliar,

areas and habitats than otherwise similar species which

place greater reliance upon direct clues. This may help

to explain why Saguinus is the only genus of tamarin

or marmoset which has been able to invade Central

America. But when the use of indirect clues is combined with segregation by differential timing, the situation may become very complicated indeed. Probably,

the advantages of such segregation outweigh the disadvantages only in regions in which food is relatively

abundant. The balance may well be different in regions

in which food is scarcer, where it may be relatively

more advantageous to spend more time looking for

things to eat, irrespective of the dangers or difficulties

of awkward interspecific encounters. If so, then the

potential drawbacks of the differential timing method

may help to explain why Saguinus is less widely

distributed than some other genera of Platyrrhini such

as Cebus and Alouatta.

Squirrels, as well as Squirrel Monkeys, may also

compete with tamarins. There are several species of

squirrels in Panama; but the only one I have observed

at any length is Sciurus granatensis. Individuals of this

species are abundant in some of the same areas as

tamarins, move along many of the same "pathways"

through trees and bushes, and sometimes eat the same

fruits. It would appear, however, that there is some

sort of avoidance reaction between the two species.

This seems to be a matter of spacing rather than timing.

The squirrels seem to be active throughout the day.

But individuals of the two species are seen close together much less frequently than would be expected

by chance alone in view of their abundance and habitat

SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

preference. It has already been suggested (Moynihan,

1968a) that the similar coloration of the tail in the

two species (largely rufous in granatensis, partly rufous

in geoffroyi) may facilitate this avoidance. (In both

species, the tail is conspicuous during locomotion. If

nothing else, it must serve to emphasize the direction

in which an individual is moving).

Only once did I see the two species within 50 feet

of one another. This occurred when a group of

tamarins approached a single squirrel. Apart from the

approach itself, the tamarins appeared to ignore the

squirrel, but the latter gave a long burst of loud vocalizations. These did not seem to be "friendly." They

probably were expressions of a strong escape tendency

(alone or in combination with other types of

motivation).

This would suggest that all or most of the usual

avoidance between the two species is due to evasive

action by the squirrels. Possibly the relationship between

the two species is as one-sided as that between tamarins

and flycatchers—with the tamarins playing the opposite

"role." There probably has not been strong selection

pressure upon the tamarins to develop special timing

mechanisms to regularize or minimize their contacts

with squirrels because they would usually win, and win

rapidly and decisively, any overtly hostile encounters

between the two species. The squirrels are somewhat

smaller and much less gregarious than the tamarins—

and certainly no more agile. Thus it probably is the

squirrels who have had to adapt to the tamarins rather

than vice versa. (Why the squirrels have not adapted

by developing a special timing mechanism of their own

is another problem. And this can be solved only by

further study of the squirrels. Possibly they cannot

afford the periods of inactivity which such a mechanism might inevitably entail.)

As mentioned above, Rufous-naped Tamarins seem

to be very much afraid of most birds of prey. They

usually perform violent escape movements, with appropriate vocalizations (see pages 29 and 30), whenever a

hawk flies by. In this respect, they differ very greatly

from Callicebus moloch.

The probable importance and value of such reactions is revealed by the fact that the tamarins usually

do not wait to make sure that an approaching bird of

prey, or any other species of somewhat similar appearance, is really dangerous. Thus, for instance, they will

burst into high intensity escape behavior when a Turkey Vulture (Cathartes aura) flies by, even though the
NUMBER 2 8

vulture is paying no attention to them and probably

could do them little damage even if it wanted to.

To my knowledge, the only bird of prey which does

not provoke such reactions is the Double-toothed Kite

(Harpagus bidentatus). Single individuals and pairs of

this rather small species frequently associate with bands

of Cebus capucinus (probably feeding on reptiles disturbed by the monkeys, N. G. Smith, personal communication) . They are much less regular attendants upon

tamarins, but they will occasionally follow bands of the

latter in areas in which Cebus is absent. The tamarins

apparently always ignore the kites completely, even

when they fly or land only a few feet away.

(Epple [1968] conducted some experiments with a

few captive S. geoffroyi [which she calls Oedipomidas

spixi\. She tested their reactions to "flying" objects. The

objects presented included a stuffed buzzard—presumably Buteo buteo—a stuffed cuckoo, cardboard models

of a buzzard and a falcon, a cardboard circle, a triangle, and a wooden staff. "When the objects suddenly

appeared moving rapidly above the animals' heads,

they reacted with warning calls." [Note: By "warning

calls," Epple may mean something like the patterns

which are termed "Loud Sharp Notes" in this paper.

See also page 30.] "When the objects moved slowly, so

that the animals could easily recognize them, only the

buzzard elicited warning calls."

(Epple's discussion of the theoretical implications of

marmoset and tamarin alarm behavior is not overwhelmingly clear in all respects. But she does say that

"The warning and escape responses given to flying

objects . . . may well be inborn." If so, and since

Double-toothed Kites are quite Buteo-\ike in shape

and coloration, it seems likely that the apparent indifference of the tamarins to the kites is acquired, the

result of learning [presumably maintained by tradition].

(This indifference is all the more remarkable if wild

tarmarins ever feed on lizards in the same way as some

captives [see page 4]. In this case, they would have

come to tolerate a direct [and synchronized] competitor. But they probably have had little choice. They do

not have the physical equipment to drive away even

a small hawk. And they can hardly avoid a direct

follower, especially something as swift and active as

a bird, if the latter is going to search them out or wait

for them to appear at any time of the day.)

It may be added that motion is not always necessary

to provoke alarm among tamarins. I have seen wild

individuals become greatly disturbed, obviously fright11

ened, upon catching sight of perched and immobile

birds of prey such as Buteo magnirostris.

Signal and Other Social Behavior Patterns of Adults

The term "social" should be used in a very broad

sense, to include all reactions, even hostile (agonistic)

and sexual, among any two or more individuals. The

terms "hostile" and "agonistic" may be applied to all

behavior patterns produced by a tendency to attack

and/or a tendency to escape. The term "sexual" may

be applied to all patterns which are largely or completely restricted to encounters or other reactions between individuals of opposite sex. The term "signal"

may be applied to any pattern which often and effectively conveys information from one individual to

another, even if it has other functions as well. Any

signal which seems to have become "ritualized," i.e.,

specialized in form or frequency or any other way,

expressly as an adaptation to permit or facilitate communication among individuals may be considered a

"display." All vocalizations are almost certainly displays in this sense. So are many distinctive postures and

movements, and all patterns which produce or distribute pheromones.

The following account will be concerned with both

the intraspecific social relations of Rufous-naped

Tamarins and the various signal patterns, especially

displays, which they may use in intraspecific and/or

interspecific communication.

For practical reasons, it will be convenient to distinguish between "adult" and "infantile" patterns.

Some of the patterns classified as adult here also

are performed by older infants and juvenile individuals as soon as they become partially independent; i.e.,

as soon as they are no longer carried by their parents

all or almost all the time. Juveniles may not show very

much in the way of high intensity sexual (at least

copulatory) behavior, but they certainly can, and

sometimes do, perform many of the same hostile patterns as completely mature individuals. They probably

also show the whole of the adult range of friendly

or gregarious responses.

At the same time, they continue to perform some

typically infantile patterns; e.g., some vocalizations,

with appreciable frequency (see pages 62 and 63).

This is true of both wild and captive individuals, but

not always to the same extent. Individuals which are

hand-raised by humans in captivity tend to retain the
12

habit of uttering essentially infantile calls relatively frequently until much later stages of juvenile development than individuals which are raised by their own

parents. This may be partly due to the fact that handraised young tend to adopt their human keepers as

parent substitutes. The humans are never completely

satisfactory in this role (again see page 63) ; but they

always remain overwhelmingly larger than the young

tamarins, and highly "impressive" or intimidating,

while continuing to provide food and some other comforts and pleasures.

Thus the behavior of juveniles, as a whole, is strongly

"bivalent," combining adult and infantile patterns,

rather than intermediate.

Completely mature and "normal" adult individuals

do not perform infantile patterns in most circumstances, but they may "revert" to an earlier phase in a

few situations of apparently extreme "stress."

The behavior of adult individuals, including their

reversions, will be described immediately below. The

behavior of infants will be described on page 60 et seq.

"PURE" ATTACK, ESCAPE, AND FIGHTING

Overt and active attack, with or without subsequent

fighting, can be induced very easily among Rufousnaped Tamarins in captivity. It is not rare among

groups of three or four individuals kept in fairly small

cages (8x8x8 feet), even when the individuals have

been kept together for a long time and are thoroughly

familiar with one another. It is a common, almost inevitable, reaction when any individual is introduced

into any cage, even a very large one, already occupied

by other individuals who are not acquainted with the

introduced animal and who have been in the cage long

enough to have adopted it as their own home range or

territory.

Attack itself takes the form of a more or less rapid approach to an opponent. If the opponent retreats, the

aggressor may follow. This may develop into a rapid

chase. If the opponent does not retreat, or does not

retreat fast enough, the aggressor may leap upon it.

Attack movements may be quite silent and unritualized in all respects. In this case, they may be considered "pure" attack, and probably are produced

when attack motivation is relatively very much stronger

than any counteracting tendency. But other attack

movements, essentially similar in form, may be accompanied by or combined with Long Rasps, Broken Rasps,

SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

and/or various Pilo-erection patterns4 (see below).

As these latter patterns also occur in some other circumstances, it seems likely that they also express some

other types of motivation. Thus, the attacks with which

they are combined probably are more ambivalent than

the silent unritualized attacks.

When an attacking individual leaps onto another,

the two animals usually begin to wrestle. This is accompanied by biting, and sometimes kicking. It may be so

violent that both individuals roll off the branch on

which the fight began and fall down to the ground.

In all cases observed, one individual managed to disengage itself after a few seconds or minutes, and then

ran away. Such breaking away may or may not be followed by (further) chasing.

Some fighting is completely unritualized and silent,

but most is accompanied by Long Rasps, Broken Rasps,

and Pilo-erection.

Once, I saw a chase among captive animals which

ended with the two individuals standing up on their

legs, facing one another, and striking one another with

their hands. But this case was thoroughly unusual.

The fact that Rufous-naped Tamarins use their

teeth as offensive weapons much more frequently than

their hands is a marked difference from Night Monkeys. It may be correlated with differences in the

dentition of the two species. Tamarins have much

sharper teeth, and relatively longer canines, than Night

Monkeys.

Fights among captive tamarins were never allowed

to continue for more than five minutes. Even during

such short periods of time, however, the fighting individuals usually become quite exhausted, and occasionally severe wounds may be inflicted.

Overt attacks are relatively very rare among Rufousnaped Tamarins in the wild, much rarer than among

Callicebus moloch individuals. The only observed attack performances by tamarins under natural conditions were brief rushes or chases, with or without

Rasping vocalizations. Apart from one very exceptional

incident, all these attacks involved individuals belonging to the same social unit. I never saw actual physical

combat, serious wrestling and biting, in the wild.

This rarity is interesting in view of the obvious aggressiveness of tamarins in captivity. It seems to be

due to several causes. The proximate causes are spacing

factors. Individuals of the same group usually have

* Throughout this paper, the initial letters of all certainly

or probably ritualized patterns are capitalized.
NUMBER 2 8 13

plenty of room to retreat from one another in the

wild. And individuals of different groups usually do

not approach one another closely enough to permit

fighting (see also page 7). The ultimate cause probably is that fighting is particularly dangerous among

tamarins. It probably is more likely to produce exhaustion or injuries, or produce such results more

rapidly, among tamarins than among titi monkeys or

some other species of New World primates.

Thus the aggressive behavior of Rufous-naped

Tamarins may seem to be "paradoxical." But it conforms to a widespread general rule, typical of many

other species with particularly effective offensive weapons. Tamarins will use their weapons when "forced"

to fight, but they usually manage to avoid fighting

under natural conditions. In both respects, they resemble many other mammals and birds cited by Lorenz,

(1952).

The escape behavior of adult and sub-adult S. geoffroyi is more or less rapid retreat. This may be silent

or accompanied by such vocalizations as Trills or Loud

Sharp Notes (see below). As in the case of attack, it

seems likely that the silent patterns are less ambivalent

than the vocal ones. (Younger juveniles may respond

to alarm by leaping upon an adult's back, in a typically

infantile manner.)

One distinctive form of escape or partial escape

behavior is a common reaction to "potential predators,"

such as man, gradually approaching from a distance

(on the ground). When the members of a band of

tamarins first become aware of the alarming stimulus,

all the individuals usually begin to vocalize (see also

page 28). They are very conspicuous at this time. As

the source of the alarm comes closer, however, one

individual after another will fall silent. Each individual

also begins to run away as soon as it shuts up. Finally,

in many cases, only a single individual is left vocalizing.

Then it too falls silent and runs away. This behavior

is obviously adaptive. The initial outburst of calling,

and then the change from conspicuous vocalization

to silence, may be confusing. And the last remaining

individual certainly helps to "cover" the retreat of its

companions. It concentrates the attention of the potential predator upon itself while the other individuals

disappear unobserved. Similar behavior is characteristic of other more or less highly gregarious Platyrrhini

which have large ranges or territories, e.g., Cebus

capucinus, but not such species as Callicebus moloch.

(Of course, the whole performance also is comparable

to the "distraction displays," or even "mobbing," of

many birds.)

Saguinus geoffroyi individuals alarmed by a bird

flying overhead may roll under a branch (M. H. Robinson, personal communication), but they seldom or

never dodge and hide behind a branch when a potential predator is approaching on the ground. In this

latter respect also, they resemble the larger Platyrrhini,

but differ from the smaller Cebuella pygmaea and

may arboreal squirrels.

COPULATORY BEHAVIOR

As noted by Wislocki (1930 and 1939) and Enders

(op. cit.), Rufous-naped Tamarins seem to have a

definite breeding season in central Panama. The evidence for this is good, but rather heterogeneous. Wislocki found young embryos in the uteri of many females

collected in January and early February. Most

young probably are born in April and early May. In

the course of the present study, I was never able to do

much field work in these or the immediately adjacent

months; and I never observed actual births. But large

numbers of infants appear, quite suddenly, for sale as

pets, in the markets of Panama City every May (personal observation).

As might be expected, there is some variation in the

timing of breeding. Some of this may reflect individual

differences in responsiveness to the same or similar

stimuli. Another part may be due to the instability of

the climate in central Panama. The onset and termination of the "wet" and "dry" seasons may differ, by a

factor of several weeks, in successive years. The amount

of rainfall during both seasons also is quite variable.

There are records of very early breeding. One infant

conceived in captivity on Barro Colorado Island was

born on 19 February. N. G. Smith (personal communication) saw one pair of very young infants in the

wild on 29 March.

There also are records of late breeding. Three sets

of infants conceived in captivity on Barro Colorado

were born in late May and early June. Wislocki found

advanced embryos in the uteri of some females collected in June. One female caught in the wild in an

advanced stage of pregnancy gave birth to two normal

young in late June. I observed one very young infant

in the wild in July.

It seems probable, nevertheless, that the number of

births usually decreases very rapidly after the usual

356-597 O - 70 - 2
14

late April-eariy May peak. Fewer infants appear for

sale in Panama in June than in May. Even fewer appear in July, and none appears later in the year. By

August and September, when I was able to resume

intensive field work during most years, only older

young are present.

It has already been mentioned that I never saw

copulations in the wild. Wislocki's data suggest, however, that they are most apt to occur, or most likely

to be effective, in January. This is supported by evidence from the captive individuals on Barro Colorado

Island. Individuals accustomed to captivity and kept

in large cages with individuals of the opposite sex

performed many apparently successful ("complete")

copulations. They did so more frequently in January

than in any other month of the year. (The same individuals, and even more characteristically other individuals kept in less optimal conditions, also were

observed to copulate, or attempt to copulate, occasionally during every month of the year between September and July. But such behavior may have been more

or less highly "aberrant.")

All this would suggest that the onset of normal or

effective breeding behavior is "triggered" by the beginning of the dry season, which usually or often occurs

during the last week of December or the first week of

January in central Panama. (And this, in turn, may be

an adaptation to ensure, or enhance the probability,

that the birth of the young will coincide with the beginning of the rainy season, which more often than not

occurs around the end of April.)

There may be two reasons why copulations were not

observed in the wild during the course of the present

study. In the first place, all wild individuals are more or

less shy, and observation of captive individuals suggests

that almost all forms of sexual behavior are inhibited

by even slight alarm. Secondly, copulations probably

are actually infrequent under natural conditions. Captive adults who have been kept apart from mature

individuals of the opposite sex for a long time may perform a remarkably large number of copulations remarkably rapidly when finally given access to a suitable

and receptive partner (I have seen a male copulate 15

times within an hour in such circumstances!). But this

is very different from apparently more normal behavior. The captive animals which seemed to have

formed the closest and most stable pair bonds, including

the individuals which bred successfully, did not attempt

to copulate more than once or twice during a 24-hour

period, even at the height of the sexual season. Some

SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

apparently well adjusted pairs may have copulated

even less frequently.

In this respect, Rufous-naped Tamarins differ from

Callicebus moloch, but probably resemble Aotus.

The actual copulatory movements of captive tamarins are rather simple.

Apparently successful copulations are usually, but

not always, preceded by some display(s), at least extreme Upward Tail-coiling by the female (see page

48). In any case, the male eventually mounts the

female from the rear; and sits behind and partly on

top of her, clasping her tightly around the "waist" (just

above or in front of her thighs) with his arms, and

continuing to grasp the perch with his feet. He usually seems to insert his penis and begin pelvic thrusts

almost immediately. These movements are irregular

and not very conspicuous. Their number is variable but

usually ranges from 3 to 20. Sometimes the male presses

his face down into the fur of the female's back throughout all or most of the copulation. He may then also

wrinkle his nose, partly close his eyes, and perform

Tongue-protrusion movements (see Figure 15a) and

occasional Head-flicks. The whole group of patterns

can be considered a type of "Sexual Sniffing" (see also

page 57). During some particularly prolonged and

vigorous copulations, the male may eventually take his

feet off the perch and begin to climb up the female's

back! He always lets his tail hang more or less straight

downward throughout the whole performance. The

female usually sits quietly, in a rather hunched posture.

More often than not, she lowers her head, bringing

it forward and down, just as the male mounts, and

then keeps it in this position. If she raised her tail in

Upward Tail-coiling beforehand, she usually lowers

and partly uncoils it as the copulation progresses. Typical copulation postures are illustrated in Figure 19.

The whole performance usually is rapid and brief.

The male dismounts immediately after the last pelvic

thrust. There is no elaborate post-copulatory display.

Frequently, however, the male puts his hand down to

scratch or massage his genitals, and/or bends his head

down in an apparent attempt to lick the genital region,

within a few seconds after the end of copulation.

Incomplete and obviously unsuccessful copulation

attempts may take various forms. Sometimes a male

simply mounts and dismounts without making any

pelvic thrusts. An unwilling female may walk away

when a male attempts to mount. Or she may simply sit

and turn her head, to look at him over her shoulder.

This seems to be a very effective way to discourage him.
NUMBER 2 8 15

It usually stops him dead in his tracks, or even induces

him to retreat, at least temporarily.

The great majority of the copulations observed were

heterosexual. But I also have seen homosexual mountings, with pelvic thrusts, among males, in the absence

of a female, and among females, in the presence of

an adult but sexually inactive male.

ALLOGROOMING (THE GROOMING OF ON E INDIVIDUAL

BY ANOTHER)

This seems to be the only display of the species which

is mediated primarily by the sense of touch (but see also

page 18).

All or almost all other Platyrrhini have homologous

patterns. But different species use them in rather different ways. Among adult Aotus, Allogrooming occurs

very frequently in close association with copulations,

but is rare or absent in other social circumstances.

Among adult Callicebus moloch, by contrast, it is comparatively rare in association with copulations, but

very common in many other nonhostile situations. In

an earlier paper (Moynihan, 1967), it was suggested

that the Allogrooming of adult Rufous-naped Tamarins may be almost as purely sexual as that of Aotus,

although not necessarily copulatory. This statement

still seems to be true, on the whole or as an average,

as a description of the most "typical" patterns of the

species; but it needs to be qualified even further. The

Allogrooming behavior of S. geoffroyi is really quite

complex.

It is comparatively very rare, much rarer than the

corresponding behavior of Callicebus moloch or Cebus

capucinus. I have never seen it in the wild, probably

because it is inhibited by the slightest degree of alarm

(just like the copulatory reactions).

It was, however, performed by many of the individuals kept in captivity, and in a variety of social situations.

It sometimes is performed by individuals who do not

seem to have formed their bonds with one another.

This type of Allogrooming certainly occurs throughout

the year; i.e., both during and outside of the season of

most frequent copulations. It usually is mutual, but

never simultaneously so. First one individual grooms

another; then they exchange roles. The former

"groomer" becomes the "groomee" and vice versa.

Roles may be reversed repeatedly. Very occasionally,

one individual grooms another individual of the same

sex. More often, a female grooms a male, or a male

grooms a female. I have seen at least one female groom

two different males in rapid succession. As a general

rule, during this type of Allogrooming, subordinate individuals tend to groom dominant individuals more

frequently than the reverse and/or continue Allogrooming for longer periods of time. In this respect,

these reactions resemble the only type of Allogrooming

of Callicebus moloch.

Among Rufous-naped Tamarins, however, such performances are relatively less common than Allogrooming between mates. And the Allogrooming between

mates is performed more frequently during the breeding, copulatory, season than at any other time of the

year. But even this Allogrooming may be somewhat

heterogeneous. It only occurs very rarely just before

actual copulation. The great majority of performances

of Allogrooming between mates, although characteristic of the breeding season, may be said to occur

"apart" from copulation insofar as they are not performed immediately before or immediately after an

overt copulation attempt.

To my eyes, the Allogrooming between mates apart

from copulation is identical in form with that of nonmates. It also seems to be equally reversible.

Nevertheless, the two types of performance may be

produced by different causal factors, different kinds

of motivation. The rarer type between non-mates, may

be an expression of some "general gregarious" tendency. The more common type, between mates, may be

an expression of some sexual drive—but this can hardly

be copulatory. Possibly it is an expression of some sort

of "pairing tendency."

The very rare Allogrooming immediately before

copulation is slightly more distinctive. In these circumstances, it is always the male who grooms the female.

Possibly these performances are purely copulatory in

the same way as the corresponding behavior of Aotus.

(They may also be partial "substitutes" for copulation,

being performed when the initiation of overt copulatory movements is delayed for one reason or another.)

The possible functions of Allogrooming, and its

probable course of evolution within the Platyrrhini,

have already been discussed elsewhere (Moynihan,

1967).

Twice, the Allogrooming of Rufous-naped Tamarins

before copulation was seen to be accompanied, or interrupted, by wrestling. This was quite vigorous, but did

not appear to be serious fighting. The wrestling animals

apparently did not attempt to bite or strike one

another.
16

All the actual Allogrooming movements of S. geoffroyi, in all situations, are quite similar to those of both

Aotus and Callicebus moloch in form. All three species

use both hands and teeth during Allogrooming. (In

this respect, their Allogrooming differs from their selfgrooming. The latter usually consists of little or nothing

else but scratching with the hands or feet.)

All types of Allogrooming by S. geoffroyi seem to be

very strongly and positively correlated with sunshine.

They seldom or never begin unless the sun is shining

quite brightly, and the individuals involved usually

are fully exposed to the sunlight at the time. In some

cases, however, grooming begun in sunshine may continue after clouds have come up.

All types of Allogrooming also have similar orientation. The groomer always pays most attention to certain

special areas of the fur of the groomee, i.e., the rufous

area of the back of the head and nape, and the

brindled parts of the back and limbs. The white areas of

the forehead and underparts usually are ignored.

An individual being groomed often raises the rufous

hairs of the head and nape to a more or less extreme

degree. Occasionally, these hairs are raised by one

individual sitting next to another in what seems to be

an attempt to "solicit" grooming. Apart from this

(which may be considered a special display, the Rufous

Ruffle, see also page 55), the methods used to invite

grooming are very simple. An individual wanting to

be groomed just approaches a companion, and sits or

lies down, usually facing away in such a manner as to

"present" its back to the companion.

OLFACTORY COMMUNICATION AND RELATED

ACTIVITIES

Like both Aotus and Callicebus, Saguinus seems to have

an acute sense of smell, and appears to rely upon this

sense for much of its information about the outside

world.

The usual initial reaction of any Rufous-naped

Tamarin to a stranger, of its own or another species,

or an unfamiliar object, is to sniff at it. When two

previously unacquainted geoffroyi individuals encounter one another for the first time, they may sniff

one another nose to nose, or one may sniff at the

genito-anal region of the other, or (most frequently)

the two individuals may place themselves in a mutual

"nose to tail" position and sniff one another's genitoanal regions simultaneously. (This may provide visual

as well as olfactory information. Not only is the base

SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

of the tail rufous, but so are the hairs immediately

surrounding the genito-anal region.)

Such simple behavior probably should not be considered ritualized per se. In a few particularly "exciting" social situations, however, otherwise typical

sniffing movements may be combined with additional

patterns which are unmistakably ritualized. These will

be described separately on page 57.

Some more elaborate olfactory displays may be

called "Rubbing." Various kinds of Rubbing patterns

are performed by many species of New World primates.

S. geoffroyi seems to have two main types. These have

been mentioned in earlier publications (see, for

instance, Moynihan, 1967; Epple, 1967; and Epple

and Lorenz, 1967), but deserve to be described and

analyzed in somewhat more detail.

The first type is done in a sitting position. An individual simply sits, presses its genito-anal region down

against the substrate, and then rubs it back and forth,

and/or from side to side, usually repeatedly. This pattern was called "Anal-Rubbing" in Moynihan (1967),

but the term "Sit-rubbing" may be more convenient

and appropriate. The Sit-rubbing of S. geoffroyi is

basically similar to the only type of Rubbing observed

to be done by Aotus in physical form although not in

all other respects (see below).

The second type of Rubbing by Rufous-naped

Tamarins may be called "Pull-rubbing." In this pattern, an individual lies down on its stomach, presses its

genital region against the substrate, and then pulls

itself forward with its hands. In order to get adequate

leverage for pulling, the animal may have to raise its

shoulders and chest off the substrate. Even then, however, the abdominal and genital regions almost always

remain firmly pressed downward throughout the whole

of the performance. Pull-rubbing does not intergrade

morphologically with Sit-rubbing.

According to Epple (1967), similar-appearing Pullrubbing is performed by several species of Callithrix

(which she calls Hapale), one species of Leontideus

(which she calls Leontocebus), and Saguinus oedipus

(which she calls Oedipomidas oedipus).

The Rubbing patterns of S. geoffroyi are illustrated

in Figure 2: Sit-rubbing in la, and Pull-rubbing in 26.

Most Rubbing of both types by Rufous-naped

Tamarins is done against branches. This was the

orientation of all Rubbing observed in the wild (see

also below). In captivity, however, individuals may

rub against many other objects and surfaces, including

the ground and the wire netting of their cages. Once,
NUMBER 2 8 17

FIGURE 2.—Rubbing postures of adult Rufous-naped Tamarins, with Crown-smoothing: a {top),

Sit-rubbing, with tail curved as in lashing; b (bottom), Pull-rubbing.
18

I saw an individual perform Sit-rubbing on the back

of another individual. Presumably as an "artifact" of

the conditions of captivity.

On branches, Rufous-naped Tamarins prefer to rub

against small protuberances, such as knots, stumps of

twigs, or projecting pieces of bark.

Both types of Rubbing are performed by both males

and females.

Both patterns may serve to spread some odoriferous

secretion(s) on the substrate. Wislocki (1936) has

described glands in the genito-anal region which might

produce such substances. It probably is significant, in

this connection, that an individual may put its hand

down to its groin, immediately after either typical Sitrubbing or Pull-rubbing, to perform what appear to be

scratching, massaging, and/or squeezing movements.

These movements may accelerate the flow, or facilitate the spread, of secretions (see also below).

Epple and Lorenz (op. cit.) have described a variety of apparently secretory glands in the sternal regions of many different Platyrrhini, including one in S.

geoffroyi. They (and Epple, 1967) suggest that the

pattern called Pull-rubbing here also spreads secretions from the sternal gland. This may well be true in

many, perhaps most, cases. But the sternal gland seems

to be less well developed in geoffroyi than in many

other species. And the "point of emphasis," the region

pressed most strongly against the substrate, is far back

of the sternum in all typical Pull-rubbing performances

by Rufous-naped Tamarins. It also seems unlikely that

much of the sternal gland substance(s) can be spread

during the performances in which the shoulders and

chest are lifted up.

Rubbing is performed very frequently by S. geoffroyi

individuals in captivity (probably more frequently than

the corresponding patterns of Aotus or Callicebus

moloch in comparable situations).

Most Rubbing occurs during disputes and other apparently hostile encounters. Both forms of Rubbing

are common during the hostilities which usually break

out when a "stranger" is introduced into a cage already

occupied by one or more other individuals who have

come to regard it as their "home." In these circumstances, the Rubbing is almost always performed by

the "owner(s)," and almost never by the intruder.

Both forms of Rubbing also occur, but less commonly,

during disputes among individuals who are familiar

with one another but on generally bad terms. In these

circumstances, the Rubbing is more likely to be perSMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

formed by apparently dominant individuals than by

apparently subordinate ones. Very occasionally, either

one or both types of Rubbing may be performed by a

very bold individual as a reaction to the approach of a

human being.

Rubbing usually is accompanied by Crown-smoothing (see page 53), a hostile display, and follows or is

followed by unritualized hostile movements. These may

be either escape and/or attack, but most frequently

the latter. Rubbing itself is usually silent; but it also

may follow or be followed by vocalizations such as

Loud Sharp Notes, Trills, and Twitters. All these

vocalizations are partly or wholly hostile.

These facts indicate that Rubbing is produced by

hostile motivation. Probably, it is produced by simultaneous activation of both attack and escape tendencies. Probably, the attack tendency is strongly

preponderant during all or most Rubbing performances. But the escape component cannot be negligible.

Crown-smoothing seems to express an appreciable

amount of escape, and the escape tendency is stronger

than the attack tendency in the vocalizations uttered

immediately before and/or after Rubbing.

Probably, the actual strength of the attack and

escape tendencies is quite different in different Rubbing performances. Rubbing occurs frequently during

both brief, apparently low-intensity disputes, and prolonged, vigorous, and apparently high-intensity disputes. Sit-rubbing is the characteristic form during

brief and not very energetic hostile encounters. Pullrubbing is the characteristic form during the most

prolonged and serious hostilities. Most disputes following the introduction of a stranger into a cage begin

very actively and excitedly, and then gradually die

down. When both forms of Rubbing occur during such

a dispute, most of the Pull-rubbing is performed during the early stages and most of the Sit-rubbing later.

These facts would suggest that Pull-rubbing is produced when both the attack and escape tendencies are

stronger, on the average, than when Sit-rubbing is

produced. But Sit-rubbing may also be performed by

particularly aggressive individuals during some disputes which are of unmistakably high intensity. In such

circumstances, it is performed very rapidly in brief

pauses between attacks. Possibly, these aggressive individuals do this Sit-rubbing instead of Pull-rubbing

simply because it takes less time (the preliminary "getting into position" is simpler), but it also is possible

that all or most Sit-rubbing is slightly more aggressive,

on the average, than Pull-rubbing. Sit-rubbing may
NUMBER 28

be performed when the relative strength of the attack

tendency, compared with the escape tendency, is

slightly greater than when Pull-rubbing is performed,

irrespective of the actual strength of the two tendencies

at any given instant.

Some Pull-rubbing by tamarin males certainly is

accompanied by erection of the penis. Some by females

probably is accompanied by erection of the clitoris.

M. H. Robinson (personal communication) also has

seen one case of erection during Sit-rubbing by a male.

Such patterns may be considered forms of masturbation. But they do not seem to be correlated with activation of sexual drives in the same way as the Rubbing

of Aotus. Neither type of Rubbing by S. geoffroyi is

largely or completely confined to encounters between

individuals of different sex.

The general form of the Rubbing patterns of

Rufous-naped Tamarins, and the circumstances in

which they occur in the conditions of captivity, would

suggest that they should function as ways of "marking" territories, of proclaiming or advertising territorial

ownership. But there are other indications that the

situation is not so simple. The performance of Rubbing

by one captive individual seldom induces a clear-cut

immediate response by its cage mates. Individuals certainly do not usually sniff at, or avoid, sites where other

individuals have Rubbed. (Once, I saw a male do

Pull-rubbing at the exact same place where a female

had performed a similar pattern a few seconds earlier,

but the male's behavior may not have been a direct

reaction to that of the female.) More important,

Rubbing is performed only very rarely by wild individuals under natural conditions. I saw a few cases

of Sit-rubbing in the wild, but no Pull-rubbing; and

most of this Sit-rubbing seemed to be a reaction to

me rather than to other tamarins.

The rarity of Rubbing in the wild must be correlated with the fact that groups of Rufous-naped Tamarins, under natural conditions at the present time,

usually are able to repel one another and prevent "trespassing" by the use of vocal patterns, alone or in combination with visual information (see page 23).

As many other mammals of other orders "mark"

their territories with olfactory information in order

to advertise ownership, it seems very probable that the

Rubbing of platyrrhine monkeys was originally evolved

to subserve the same function (and/or is a direct descendant of a primitive mammalian pattern adapted to

this function). At the present time, however, the Rubbing of S. geoffroyi would seem to be in process of

19

becoming obsolescent as a method of conveying information, at least by olfactory means. As a social signal,

it seems to be nothing more than a "second-line reserve" method of territorial defense, only used in more

or less strongly abnormal circumstances.

It seems possible, in fact, that even some of the Rubbing of captive individuals is less a signal or means of

social communication than an "outlet" for thwarted

motivation or a way of "relieving" frustration. The

clearest examples of this phenomenon were provided

by some animals being tested by M. H. Robinson on

Barro Colorado. Dr. Robinson was interested in the

tamarins' ability to recognize cryptic insects, and he

conducted a series of experiments in which single individuals were released into cages in which various

cryptic insects were hidden among twigs and leaves.

Some of the tamarins took a very long time to discover the insects, and a few were completely unsuccessful during the time periods allotted for the experiments.

Some of them performed Sit-rubbing and/or Pull-rubbing when first released into the experimental cages.

These reactions may have been attempts to "claim" territories. But some of the individuals also performed

progressively more and more Rubbing the longer they

remained unsuccessful in finding the insects. And, at

least in some cases, they stopped Rubbing when they

finally did discover and eat the insects.

If this suggestion is correct, and the Rubbing of

Rufous-naped Tamarins is in process of changing from

a signal pattern to a method of relieving frustration, it

is remarkable that the Rubbing movements are so complex, and conspicuous, in form. They certainly are at

least as elaborate as the corresponding movements of

other Platyrrhini. Possibly, relatively complex patterns

are more suitable as outlets for thwarted motivation

than are less complex patterns.

Some other platyrrhines, e.g., Callicebus moloch, occasionally perform movements which are more or less

similar to the Sit-rubbing movements of tamarins immediately after defecation and/or urination in obviously non-hostile and non-sexual situations. In these circumstances, the movements appear to be purely cleaning patterns, and may not have special signal functions.

Saguinus geoffroyi itself may retain a trace of such

cleaning behavior. At least, I have seen several captive

tamarins perform what looked like typical Sit-rubbing

movements, on two or three different occasions, immediately after defecation or urination, when they were

not involved in overt disputes. But all the individuals
20

who performed such patterns had cage mates at the

time; and it is impossible to be certain that their Rubbing was not motivated by some otherwise concealed

feeling of hostility. It may also, of course, have been

due to "postural facilitation."

In any case, it seems quite probable that the original

signal version of Sit-rubbing was a derivative of a nonsignal cleaning pattern.

If so, the Sit-rubbing and "pre-Sit-rubbing" movements of S. geoffroyi have subserved three very different functions in the course of evolution; i.e., cleaning,

signaling, and channeling frustration. And they have

done so with remarkably few changes in physical form.

This is of some interest from a theoretical point of

view. In Moynihan (1967), it was suggested that the

tactile (Allogrooming) and acoustic signal repertories

of New World primates, unlike their visual signals,

tend to be very adaptable (changeable) in function

while remaining conservative in form. It would now

appear that at least some of the olfactory signals are

more similar to Allogrooming and vocalizations than

to visual displays in this respect.

Pull-rubbing may have evolved as a simple exaggeration of the forward movements sometimes included in

Sit-rubbing.

Incidentally, it should be noted that the typical Pullrubbing of Rufous-naped Tamarins is almost perfectly

intermediate, in form, between Sit-rubbing and the

"Chest-rubbing" of Callicebus moloch. The latter may,

in the course of evolution, have been derived from,

or passed through a stage comparable to, Pull-rubbing.

Epple and Lorenz (op. cit.) show a photograph of

a geoffroyi male performing a pattern which looks remarkably like the typical Chest-rubbing of Callicebus,

i.e., the breast is pressed against a branch while the

hindquarters are raised. In my experience, this sort of

behavior is very rare among geoffroyi individuals.

When it does occur, it appears to be abnormal, perhaps hurried, Pull-rubbing rather than a different,

qualitatively distinct, signal.

The original connection between cleaning and specialized signal or outlet Rubbing may also be revealed

by another type of performance by Rufous-naped

Tamarins. Like many other Platyrrhini, these animals

clean their faces, especially after eating messy food, by

rubbing their "muzzles" along a branch. Usually, they

turn the head from side to side as they do so, thus

cleaning each side of the face in turn. Rather surprisingly, individuals occasionally perform identical or

very similar movements during Pull-rubbing, even

SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

when their faces are not dirty at the time. This is most

likely to occur during obviously high-intensity disputes. The face rubbing in such circumstances appears

to be due to some peculiar (see below) sort of "overflow" of rubbing motivation. One gets the impression

that the individuals which behave in this way are

"driven" by such a strong tendency that they will rub

anything and everything available. In any case, the

occurrence of such face rubbing during apparently

ritualized Pull-rubbing suggests that the internal casual

factors producing the two activities are (still) linked

together in some way.

(Face rubbing in these circumstances certainly is

not a simple reaction to a change in the external

stimuli confronting the performing animal. It is not a

simple response to the fact that the face is brought

close to the substrate during Pull-rubbing. Individuals

do not usually perform face rubbing when they lie down

in other circumstances. Nor is it a conventional "overflow activity" as the term is usually used by ethologists

[see Bastock, et al., 1953]. In some ways, it resembles

more the type of behavior frequently called "displacement activity." But the latter term is vague and possibly

misleading [see comments in Moynihan, 1955a]. The

application of the term to face rubbing during Pullrubbing would be particularly misleading if the two

activities are linked as suggested above.)

Although probably not always functioning as olfactory signals themselves, the more specialized Rubbing patterns may still (or also) play a variety of roles,

or subserve several functions, in visual communication, at least occasionally.

Both Sit-rubbing and Pull-rubbing are more or less

conspicuous to the eye, even when performed by themselves alone and in the simplest possible manner.

Some Sit-rubbing also is combined with visually conspicuous Tail-lashing. In this pattern, the tail is

switched violently from side to side (see Figure 2a).

This usually or always occurs when the Sit-rubbing

movements themselves are lateral; but the tail movements definitely are not simple "mechanical" consequences of the body movements. I have seen

Rufous-naped Tamarins perform vigorous side to side

Sit-rubbing without conspicuous Tail-lashing. In some

other species, e.g., Callicebus moloch, Tail-lashing occurs apart from Rubbing, by itself alone and/or in

combination with other signal patterns. But the Taillashing of S. geoffroyi seems to be absolutely confined

to some Sit-rubbing performances. In this respect, it

resembles the Tail-lashing of Aotus.
NUMBER 2 8 21

The white underparts of many captive Rufous-naped

Tamarins often are suffused with a tinge of yellowishbrown or brownish-orange. Sometimes this is quite

bright, almost rufous. It appears to be a stain. It is

quite variable, varying in the same individual at different times, and differing in different individuals. I think

that this stain may be produced by the secretion (s)

spread during Rubbing, especially Pull-rubbing. Individuals which perform a great deal of Pull-rubbing

usually have more extensive and brighter stains of yellow-orange-brown than individuals which perform

comparatively little Rubbing.

ACOUSTIC COMMUNICATION

Rufous-naped Tamarins have a moderate number of

acoustic signals. All are largely or completely vocal.

(There seems to be nothing comparable to the

"Gnashing of teeth" of titi monkeys.) These vocalizations can be roughly divided into nine main types,

some of which intergrade with one another through

more or less continuous series of intermediates. Two

major patterns may be considered "essentially infantile"; the others are "essentially adult."

Some brief citations in the published literature (e.g.,

Enders, op. cit.) might suggest that S. geoffroyi is a

rather noisy species, but this seems to be only partly

true of the population as a whole. The species is noisy

only in certain circumstances. Wild adults may, sometimes, vocalize very conspicuously when they can see

or hear a human observer or other potential predator,

and when reacting to (or attempting to influence)

other tamarins belonging to other social groups. But

they tend to be very quiet indeed when they are not

concerned with individuals of other social units and

are not aware of being observed. On the whole, wild

adult geoffroyi are very much less noisy than wild Callicebus moloch, or even Aotus. This probably is another

adaptation to avoid attracting the attention of enemies in most circumstances (but see also pages 13 and

27).

The order in which particular vocalizations are

listed below is not perfectly logical. It also differs from

the order in which homologous and analogous patterns

of Aotus and Callicebus were discussed in previous

publications. It is used simply for practical convenience

in description. The most important parts of the following descriptions will be illustrations of sound spectrograms. These will be supplemented by brief verbal

summaries and comments which are essentially accessory. In general, verbal descriptions will refer to

patterns as they sound in human ears. This may be

deceptive in some cases. Rufous-naped Tamarins, like

many other Platyrrhini, sometimes utter vocalizations

which sound like single notes to human ears but which

can be shown, by spectrographic analysis, to be "compound" ; i.e., composed of several discrete units uttered

in very rapid succession. Simply as a matter of convenience, however, I will refer to any group of sounds

which seem continuous to my ears as "a note." If a

note in this sense is really compound, the various units

included will be called "components of a note."

• Long Whistles.—These are the most prolonged

notes in the repertory of the species, with the possible

exception of certain Long Rasps. They are relatively

loud and "plaintive" in tone.

They are rather stereotyped in some ways. They can

be uttered singly or in series of two, three, or four

notes. But series of two or three notes are very much

more common than either single notes or series of four.

Series of two are slightly more common than series of

three. Series may be repeated at frequent intervals, but

never so rapidly that they "run together" and lose

their individual identity. In all or most series, the first

note is appreciably shorter than the succeeding ones.

Thus, the sequence and arrangement of the notes would

appear to have become almost as ritualized as the notes

themselves.

A typical two-note series is shown in Figure 3. The

last part of a typical three-note series is shown in

Figure 4.

It will be seen that these patterns are really very

complex, much more complex than they sound to

human ears. Each note is composed of a very large

number of separate "pulses" of sound. The "fundamentals" are rather low frequency (cycles per second)

and very soft. It is the higher harmonics which provide

the loudness. Apparently, the different harmonics

of a single sound may vary in loudness independently

of one another.

Figures 3 and 4 also reveal another peculiar feature

of the Long Whistle. They seem to indicate that some

of the notes are really composed of two partly independent series of pulses of sounds, partly overlapping

one another. (This is particularly obvious at the beginning of the second note in Figure 3 and throughout

most of the last note of Figure 4.) This may indicate

that sounds are transmitted through two channels. The

mouth always is wide open during Long Whistles.

Possibly sounds also are emitted through the nostrils.
22

8,000-

SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

i' ,11 «

;.q*«

, rf "

1.0 2.5

FIGURE 3.—A two-note Long Whistle series by an adult Rufous-naped Tamarin. All the

Spectrograms illustrated in this paper were produced by a Kay Electric Company "Sonagraph"

6061 A. They were derived from recordings by a Nagra III NP, used with a Sennheiser

MKH—104 microphone. This figure, and Figures 7 and 14, are based upon spectrograms made

with a wide-band pass filter of 300 cps. All the other spectrograms illustrated were made with

a wide-band pass filter of 600 cps.

16,000 -«

t r tft 4

i i

0.5 1.0

Time (sec.)

FIGURE 4.—The latter part of the second note and the whole of the third note of a three-note

Long Whistle series by an adult Rufous-naped Tamarin. Some of the general "fuzziness" may

be background noise or some other artifact, but certainly not all of it.

As might be expected, in view of their loudness,

Long Whistles seem to be purely long-distance signals.

They are uttered in a very peculiar and complex set

of social and environmental circumstances.

They are uttered most frequently by individuals

who have become separated from their usual companions; i.e., the other members of the same social unit

(pair, family, or band). In the wild, a separated individual usually begins Long Whistles when, and as soon

as, it realizes that its companions are no longer in

sight. Captive individuals can be induced to utter

Long Whistles even when their usual companions are

in full view, if they are prevented from rejoining the

companions by some physical barrier such as a wirenetting screen. Long Whistles also are the first or only

response of any normal adult individual kept in both

physical and visual isolation in captivity when it hears

a tape-recording of any sound of the species.

These facts would suggest that Long Whistles can

function as "lost calls" or "location calls." They must

reveal the location of a calling individual, and often

indicate that it is alone.
NUMBER 2 8 23

The responses to Long Whistles by an isolated individual in the wild, under natural conditions, are rather

varied. Usually, when the notes are being uttered by

an individual who is a member of an established social

group, the other members of the group go on about

their business, perhaps uttering a few Long Whistles of

their own in "reply" to the separated animal, but otherwise apparently unconcerned. In such cases, in the

wild, the isolated individual sooner or later starts to

search for, or runs to catch up with, its companions. It

continues Long Whistles during these movements. But

it stops them as soon as it finds and rejoins its companions. Occasionally, the isolated individual is particularly slow in beginning to search or follow. In these

circumstances, the companions may eventually begin

to search for it, and usually rejoin it after more or

less of a delay. Again, the Long Whistles usually stop

as soon as the group is reassembled. Such reactions

would suggest that Long Whistles by one member of a

group are more or less strongly attractive to some or

all of the other members of the same group.

It is possible that Long Whistles also play a role

in "pair formation" in certain circumstances.

Actually, as might be inferred from many preceding

comments, I saw very little behavior which could be

characteristic of an initial or other "early" stage of

pairing in the wild. It is my impression that Rufousnaped Tamarins probably usually form pair bonds

with a sibling or some other member of their own

family group, and that such pair formation is a gradual

process, accompanied by a minimum of conspicuous

display. But I did see one individual (sex unknown)

in the wild who was apparently unmated and quite

solitary, and who uttered many Long Whistles for

hours on end over a period of several days, while it

roamed back and forth over its extensive home range

or territory. A few days later, this individual was found

to have acquired a companion, presumably a mate.

Possibly, the mate had been attracted by the Long

Whistles. In any case, once the pair was formed the

Long Whistles were uttered much less frequently.

Long Whistles probably also subserve other functions in other circumstances. Certainly, they apparently

are not always attractive. Sometimes, in fact, they may

be just the opposite. They apparently can be used to

maintain the integrity of territories.

The usual (and only acceptable) definition of territory is "any defended area." In many New World

primates, defense of territory is obvious as such. It may

take the form of actual attacks upon, or fights with,

neighbors and intruders. Or it may be effected by displays whose nature is unmistakably hostile. This does

not, however, usually seem to be true of S. geoffroyi.

As noted above, I never saw contact fighting, i.e.,

wrestling with biting and kicking, among tamarins in

the wild. I saw only one encounter between individuals

of different scoial groups in the wild which involved

other hostile movements, some brief aggressive chasing

back and forth. Even more remarkably, I never saw

individuals of different social groups in the wild direct

toward one another such unmistakably hostile vocalizations (which are characteristic of disputes in captivity) as Long Rasps, Broken Rasps, and Loud Sharp

Notes. (All disputes in the wild which were accompanied by such notes, and the few other cases of

obviously aggressive chasing, were among individuals of

the same social group.)

I have, however, occasionally seen two or three different bands (or smaller social units) of tamarins remain for considerable periods of time (10 to 30 minutes) in trees only 10-100 yards apart, while some or

all of the members of the different groups uttered

numerous series of Long Whistles in steady and rapid

succession. The notes obviously were directed toward

individuals of the other group(s). The vocalizing animals usually looked straight toward the other group (s).

And they continued to utter Long Whistles throughout

the whole of the period of "confrontation," even

when all the other members of their own group were

gathered close around. Eventually, one or all of the

groups retreated. And then the Long Whistles stopped.

This would suggest two things. One, Long Whistles

can be released by factors other than physical isolation.

And secondly, the Long Whistles of one individual can

be definitely repellent to individuals of other groups in

at least some circumstances.

The most interesting feature of such reactions is not

that the repulsion of other groups, in effect the defense

of territory, can be accomplished without overt fighting, but that the signals employed or involved, the

Long Whistles, do not seem to be primarily hostile in

motivation.

That the immediate causation of Long Whistles is

essentially non-hostile is indicated by much of the evidence cited or referred to above. Long Whistles by

isolated individuals really are very much more common

than similar notes by individuals of different groups

confronting one another. More important, it was possible to arrange a very great number of overtly hostile

encounters of many different types among the indi-
24 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

viduals kept in captivity; and the overwhelming

majority of these encounters were not accompanied by,

or associated with, Long Whistles.

Of course, there were some problematic and probably ambiguous reactions. Thus, for instance, the one

observed case of aggressive chasing among individuals

of different groups in the wild was associated with Long

Whistles—and no other vocalizations. In captivity,

Long Whistles were observed to be uttered during one

violent hostile encounter which developed after a

stranger was introduced into a cage already occupied

by a group of four. These Long Whistles were uttered

while vigorous chasing and actual contact fighting were

in progress, and were associated with many other unmistakably hostile vocalizations; but all or most of them

were uttered by individuals who were not actually

fighting with the stranger at the precise moment

of utterance.

Both these individuals and the ones involved in less

active "confrontations" between groups in the wild

may have had very "mixed" feelings toward their

"opponents."

(I have also heard captive Rufous-naped Tamarins

utter Long Whistles in apparent response to the approach of wild spider monkeys, Ateles, and anteaters,

Tamandua; but captive primates often are not very

discriminating in their reactions between their own

and other species.)

On general methodological grounds, it would seem

to be desirable to "explain" all performances of any

given type of display, or any other behavior pattern

for that matter, as direct consequences of the same

ciusal factor(s) in all the circumstances in which the

display or other pattern may occur. This is not always

possible (viz., the Allogrooming described above). But

it may be feasible in the case of the Long Whistles of

Rufous-naped Tamarins. They may all be the results

of thwarting some gregarious and/or pairing motivation, produced when the motivation is prevented from

being expressed overtly, by joining, either by the interposition of some physical barrier (or ignorance of

the location of other individuals) and/or the counteracting effects of some other simultaneously activated

but "incompatible" type of motivation (such as feeding, escape, attack, or what have you).

The length of the series of notes in a typical Long

Whistle performance obviously is correlated with the

strength of the gregarious or pairing motivation and/or

the strength of the thwarting. When many Long

Whistles are uttered, the average number of notes

per series is higher than when fewer Long Whistles

are uttered in the same length of time. (This is true

only of typical Long Whistles. The general rule does

not apply to performances which may be intermediate

between typical Long Whistles and typical Twitters.

See also below.)

The bivalent signal effects of geoffroyi Long

Whistles, i.e., the attraction of members of the same

group and the repulsion of members of other groups,

are the same as those of the Songs of many species

of birds. The Long Whistles probably are, in fact,

strictly analogous to many bird Songs. Their relationships to patterns of other species of Platyrrhini are less

obvious or, at least, more complex.

Some of the social circumstances in which Long

Whistles are uttered are reminiscent of the "Hoots"

of Aotus. The Hoots also are uttered by isolated individuals, apparently as a result of thwarting gregarious

and /or pairing motivation. (Hoots have not been observed to be used to maintain the integrity of territories;

but observations of Night Monkeys in the wild are

so difficult that reactions of this type could be easily

overlooked.) Hoots also resemble Long Whistles in

being usually uttered in a series of two or three notes,

each one of which is actually compound. These facts

would suggest, very strongly, that the Long Whistles of

S. geoffroyi are strictly homologous with the Hoots of

Aotus.

The principal difference between Hoots and Long

Whistles is pitch or frequency (cycles per second). The

audible components of Hoots are much lower in pitch

than the loud components of Long Whistles. But the

importance of this difference should not be overestimated. As noted in Moynihan (1967), there seems to

have been strong selection pressure in favor of raising

the pitch, or maintaining the original high pitch, of all

the vocal patterns of tamarins and marmosets. Simply

because these animals are small, they probably are

particularly vulnerable to predation. High-pitched

sounds do not carry as far as low-pitched sounds. (The

energy of a sound is lost in heating the air through

which it passes, and sounds of higher pitch are used

up more rapidly than sounds of lower pitch. Also,

the relatively short waves of high pitched sounds will

be more "scattered" by obstructions such as leaves and

branches than the longer waves of low-pitched sounds.)

Thus, high-pitched sounds are relatively less likely to

attract the attention of potential predators, and this

quality may be particularly valuable to tamarins and

marmosets. In the case of Aotus, by contrast, there may
NUMBER 28 25

have been strong selection pressure in favor of low

pitch, simply because the species is nocturnal, and has

to rely upon vocalizations more nearly exclusively than

all or most other New World primates. This may put a

"premium" upon sounds which carry a long distance.

(Possibly, the nocturnal habits of this species also make

it less vulnerable to predation, at least predators approaching from a distance.) In any case, it is obvious

that homologous vocal patterns have undergone major

changes in pitch during the evolution of one or more

groups of New World primates.

To human ears, individual Long Whistle notes also

sound rather similar to both the Whistles and Screams

of Callicebus moloch. This apparent resemblance is

confirmed by analysis of sound spectrograms. Individual Long Whistles of Rufous-naped Tamarins are

not very different from some Screams of C. moloch in

basic structure. (They are less similar to moloch

Whistles in structure, but there is other evidence that

the latter patterns are closely related to Screams.)

Nevertheless, it probably is significant that the Screams

and Whistles of C. moloch are not usually arranged in

short series like the Long Whistles of S. geoffroyi (or

the Hoots of Aotus). They also occur in rather different sets of circumstances. The Screams of C. moloch

(like the Long Rasps of Rufous-naped Tamarins) certainly are completely hostile. The Whistles of moloch

probably are at least partly hostile. It is equally suggestive (in a different way) that individual Long

Whistles of S. geoffroyi also sound rather like some

Whistle patterns of other tamarins; i.e., S. fuscicollis,

Callimico goeldii, and Leontideus rosalia. These also

are partly or completely hostile and not usually arranged in specialized short series. Possibly all these patterns (including the Long Rasps of geoffroyi) are

related phylogenetically. If so, the Long Whistles of

geoffroyi probably are descended from a pattern originally produced by hostile motivation. (It seems likely

that displays have changed from hostile to non-hostile,

in the course of evolution, more frequently than the

reverse, for obvious reasons. See also Moynihan, 1962.)

If this assumption also is correct, then the Long Whistle

patterns may represent an intermediate stage in evolution. They are almost exactly halfway between the

Whistle and Scream patterns of many other Platyrrhini, on the one hand, and the Hoots of Aotus on the

other hand. Possibly, the Hoots of Aotus passed through

a similar stage in the course of evolution, probably

before the species became completely nocturnal. (Some

of these patterns, and other related sounds, are also

discussed on page 68.)

Although the Long Whistle performances of Rufousnaped Tamarins seem to be analogous to the Songs of

many birds, they certainly are not homologous with

the whole of the complex of vocal patterns of Callicebus moloch which has been called "Song." At best,

they are homologous only with the Whistle phases of

the (relatively few) Song performances of the latter

species which include such phases.

(As an illustration of the difficulties which may be

encountered in attempting to decipher the phylogenetic relationships and functional equivalence of the

display patterns of different Platyrrhini, it may be mentioned that the most spectacular components of the

majority of "complete" Songs by C. moloch are "Resonating Notes," and that these notes probably are

strictly homologous with the "Resonant Grunts" of

Aotus which probably do not function as Song.)

• Twitters.—These patterns are among the most

characteristic of the vocalizations of adult Rufousnaped Tamarins. A typical Twitter performance consists of a series of moderately soft, rather high pitched,

moderately short notes. The intervals between notes

of a single series are quite variable, but usually not

more (and often much less) than twice the length of a

single note. The general effect, to the human ear, is

usually quite rapid (almost "bubbling"). The number

of notes per series also is variable. Probably the great

majority include four to ten notes. Single notes essentially similar to the notes of series occasionally are

uttered by themselves alone. It may be convenient to

refer to both the single notes by themselves alone and

the individual notes of series as "Short Whines." They

all have something of the same plaintive quality as

Long Whistles. Several Twitters are shown in Figures

5, 6, and 7. It will be seen that some of the notes in

these series are almost flat, but that the majority rise

in pitch. In some cases, the rise is steep. Also in some

cases, the rise is preceded by a relatively brief descending phase. Very occasionally, a single note may

first rise, then fall, and then rise again (see the second

Short Whine in Figure 5).

(It may be necessary to add one more comment on

terminology here. Series of Short Whines have been

called Twitters in this paper because they belong to

the class of sounds usually described as "twittering"

in ordinary, every day, English speech. This usage

must be distinguished from that of Andrew [1963],

who uses the term in a restricted and rather special
26

16,000

SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

,II/II mil11

0.5

Tim* (sec.)

1.0

FIGURE 5.—A Sharp Note followed by four Twitter Notes (Short Whines) by an Adult Rufousnaped Tamarin. The Sharp Note may be intermediate between the typical Loud and Soft forms.

All series of notes illustrated throughout this paper are "natural." Each series was uttered by a

single individual. The intervals between successive sounds are those shown on the spectrograms.

16,000-^

I'!

<«<**• i * i • ••

T

0.5

Time (sec.)

FIGURE 6.—A Twitter by an adult Rufous-naped Tamarin. The individual notes show a slight

tendency to "run together." This may be an indication of relationship to (or intergradation with)

Long Whistles.

T

1.0

sense. He defines "a Twitter" as a "high short call

which ascends or decends steeply [or does both in a

chevron]." Some of the Short Whines of Rufous-naped

Tamarins conform to this definition, but others do not.

And there are other patterns in the repertory of the

species which conform much more consistently to Andrew's defiinition, but which are quite distinct from

the Short Whines and do not sound at all twittering in

the ordinary sense of the word. Andrews also states

that "Twitters" are the "main type of vocalization" in

all genera of tamarins and marmosets. Unfortunately,

"Twitters" in his sense include so many different types

of vocalizations, some of them only distantly related,

that the statement is essentially meaningless. Some

other features of Andrew's account will be discussed

on page 70).
NUMBER 2 8

8,000-4

27

1.0

Time (tec.)

FIGURE 7.—A Twitter by an adult Rufous-naped Tamarin. The resemblance to Long Whistles is

even stronger than in the preceding example.

2.0

The Twitters (as the term is used here) of Rufousnaped Tamarins are uttered in a wide range of social

situations and probably are very highly ambivalent.

They are uttered very frequently as reactions to potential predators; i.e., by wild individuals to the appearance of human beings and by both wild and captive

individuals to other large mammals and hawks. They

also are uttered by captive tamarins during some disputes among themselves. In both sets of circumstances,

they often are closely associated with unmistakably

hostile Loud Sharp Notes and/or Trills. Occasionally,

they are combined with equally hostile visual signals

such as Swaying, Crown-smoothing, and related or

associated patterns (see below). All this would indicate

that the Twitters themselves are at least partly hostile.

Probably, the hostile motivation involved is purely or

predominantly the escape tendency. Twitters occur

relatively frequently immediately before, during, or

after overt retreat, but relatively very seldom immediately before attack. On the other hand, there are very

strong indications that many or all Twitters are also

partly non-hostile. They are uttered by very tame,

hand-reared, captive individuals as reactions to the

approach of human beings from whom they expect to

get food. In such circumstances, they appear to be a

form of "greeting" (or even "food-begging"). The

great majority of Allogrooming performances and copulation attempts are silent, but a few are accompanied

by sounds, and Twitters and single Short Whines are

among the least uncommon of such sounds. Twitters

also are uttered when captive individuals who are well

acquainted with one another (and well adjusted to

one another) move around their cages, in more or less

close proximity, without any signs of overtly hostile

movements. It will be remembered that Twitters resemble the apparently non-hostile Long Whistles in

tone (see above). More important, they actually intergrade with Long Whistles with some appreciable frequency. (This intergradation may take either one of

two forms. In some cases, a single note of a Twitter is

unusually prolonged. In other cases, all the notes of a

whole Twitter series tend to "run together" to form

a long semicontinuous pattern which is quite reminiscent of some Long Whistles when analyzed on a spectrogram. Figures 6 and 7 illustrate this phenomenon

to varying degrees.)

Thus, all the evidence, taken together, would suggest that all or most Twitters are produced when the

escape tendency and some friendly and/or sexual

tendency are activated simultaneously.

From some points of view, it may be convenient

to consider the Long Whistles, Twitters, and Short

Whines as different "parts" of a single "complex" of

patterns. This complex may be given the name of

"Plaintive Notes."

Probably, all or most Twitter performances are low

to moderate intensity; i.e., produced when all the

activated tendencies are only moderately strong (at

best). They are uttered relatively most frequently by

animals which do not seem to be very excited. Thus,
28 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

for instance, a wild individual reacting to a potential

predator which is nearby but stationary (and not making any threatening gestures) usually begins by uttering many Loud Sharp Notes and/or Trills as well as

Twitters. Then, if the individual does not run away,

and as it becomes accustomed to the presence of the

disturbing stimulus, it gradually stops uttering the Loud

Sharp Notes and Trills, while continuing the Twitters.

As habituation proceeds even further, the Twitters also

decline in frequency, until finally the animal relapses

into silence. Similarly, of course, it is the Long Whistles

and not the Twitters which are usually uttered by individuals which have become widely separated from

mates or other social companions.

Short Whines uttered singly, by themselves alone,

probably are produced by much the same type of

motivation, combinations of the same tendencies, as

the Twitters of several notes. But they probably are

even lower intensity, produced when all the tendencies

involved are actually weaker. They occur in much the

same range of social circumstances as Twitters, but they

are relatively much less common in the more "tense"

or exciting situations, and relatively much more common in the less exciting ones. Thus, for instance, they

are relatively rare during initial reactions to potential

predators, but relatively very common when well adjusted cage mates are moving around together.

The Short Whines and full Twitters which are most

plaintive in tone, or otherwise most similar to Long

Whistles, probably are produced when the non-hostile

motivation is relatively stronger (compared with the

hostile motivation) than when less plaintive or less prolonged patterns are produced.

Although Twitters and Short Whines must be signals, they do not seem to be invariably precise and

consistent "commands." When Twitters are uttered

by one individual as a reaction to a potential predator,

they may function as alarm or warning signals. They

may induce immediate retreat by other members of

the same social group or "trigger" the performance of

"distraction" or "mobbing" patterns. In the latter

case, the other members of the group usually gather

around the first individual and utter more Twitters

or, more frequently, Trills and/or Loud Sharp Notes,

before drifting away, one by one, as described on page

13. In other circumstances, the Twitters do not seem

to induce any overt movements, not escape nor approach nor anything else. Possibly, such Twitters may

serve as another type of "contact pattern" or "location

call," roughly comparable to Long Whistles in helping

to maintain the cohesion of a social group, but presumably effective only over shorter distances. In any

case, as the Twitters seem to reflect or express the motivation (and perhaps other aspects) of a calling animal

quite precisely, they must be capable of conveying this

information to all or many other individuals within

earshot. The information may be stored away "for

future reference" even when it is not reacted to

immediately.

As a partial summary, it may be said that most

Twitters and Short Whines seem to be more "priming"

than "releasing."

Some of their relationships to patterns of other species are fairly clear. Their plaintive quality, some of the

circumstances in which they occur, and their mixed

hostile and non-hostile motivation, are all more or less

strongly reminiscent of the Moans of Callicebus spp.

and both the Moans and Low Trills (which may be

nothing more than rapid series of abbreviated Moans)

of Aotus. Possibly they are largely homologous with

all these patterns. But they differ conspicuously from

both the Callicebus and Aotus patterns in some (other)

aspects of form, especially in being much higher

pitched. Thus, the physical differences between Twitters and Short Whines and the most nearly equivalent

Callicebus and Aotus patterns is exactly parallel to that

between Long Whistles and the Hoots of Aotus.

These suggested homologies are supported by other

evidence; i.e., some aspects of timing. Thus, for instance, when Twitters and Loud Sharp Notes are

uttered together, apart from other patterns, the usual

sequence is one Loud Sharp Note followed by one

Twitter series (see Figure 5). There is reason to believe

that the Loud Sharp Notes (and the not very dissimilar Sneezing Sharp Notes) of S. geoffroyi are phylogenetically related to the Sneeze-grunts of Aotus and the

"hostile sneezes" of Callicebus moloch (see page 42).

Thus, it is interesting, and probably it is significant,

that C. moloch individuals tend to utter Sneeze-Moan

series, and that Night Monkeys utter both Sneezegrunt-Moan and Sneeze-grunt-Low Trill series relatively frequently.

It would appear that the arrangement of some

acoustic signals has been even more conservative than

their form during evolution.

Of course, even if the Twitter and Short-Whine patterns of Rufous-naped Tamarins are largely homologous with the Moans and Low Trills of Callicebus and

Aotus, this does not necessarily mean that they may not
NUMBER 2 8

16,000-

29

" \

0.4 0.8 1.2

Tim* (sac.)

FIGURE 8.—A Trill by an adult Rufous-naped Tamarin. The third, fourth, and fifth notes of the

scries may be quite similar to individual Soft Sharp Notes.

16,000-

I \

Tim* (sac)

0.8

FIGURE 9.—A Trill by an adult Rufous-naped Tamarin. Some of the "fuzz" may be an

artifact. But the notes of this series certainly are not absolutely identical with those

illustrated in the preceding figure.

also be related to some other patterns of the same species; e.g., some of the high-pitched Squeaks of Aotus

which are uttered in sexual situations. Although it is

possible to trace homologies among the patterns of different Platyrrhini, the correspondence is not always

perfectly one to one. See also below.

• Trills.—These patterns, and the next three cited

below, may be considered parts of another "complex."

This may be given the inclusive general name of "Sharp

Notes." It seems to be roughly comparable to the

Plaintive Note complex in scope.

The Trills are the most Twitter-like of the Sharp

Note patterns. They are rapid series of short notes.

Usually, there are seven to twelve notes per series, but

the individual notes do not sound at all plaintive to human ears. They also differ from Short Whines in sequence of changes of pitch. A single Trill note usually

begins with a rise, or a nearly horizontal phase, and

then falls. The emphasis always is on the terminal

downbeat rather than the preceding upbeat. The

transition between the phases of a single note is more

or less abrupt. All typical Trills also are appreciably

louder than typical Twitters. Several Trills are illustrated in Figures 8, 9, and 10.

Brief experiments with a "bat detector" indicate that

some, if not all, Trill notes include loud ultrasonic

356-597 O - 70 -3
30 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

16,000-

0.8

Tim* (set.)

FIGURE 10.—Another Trill by an adult Rufous-naped Tamarin. The last two notes of

the series would appear to represent intergradation with Rasping patterns.

components, up to at least 24 kilocycles. (Probably

such components are absent in Plaintive Notes.)

In a very few cases, the first "regular," rising, phase

of a Trill note is preceded by a very rapid and short

"introductory" phase which is steeply descending. This

is illustrated by several of the notes in Figure 10. These

introductory phases may not have any functional significance. They certainly cannot be detected by the

human ear. They may also be too brief to be heard by

other animals.

Most Trills are obviously reactions to disturbing

stimuli; i.e., potential predators. Some of the circumstances in which they occur have been mentioned

above. Shy individuals in the wild frequently utter

Trills when they see a human being. Both wild and

captive individuals utter Trills when other large mammals pass by and birds of prey fly overhead. Trills

may be accompanied by Swaying and (very occasionally) Head-flicks, and are uttered rather frequently immediately before, during, and/or immediately after retreat movements. All this would indicate that they are

hostile. Unlike the Twitters, they probably are purely

hostile. They are relatively much less common during

intra-specific encounters. They may be quite absent

during encounters or reactions among individuals

which are familiar with one another. They are apparently never uttered as "greetings" or "food-begging"

by captive individuals.

It has already been indicated that Trills probably

are of higher intensity than Twitters on the average.

They are never uttered by individuals which seem to

be as little excited or disturbed as some individuals

uttering Twitters. Some Twitters certainly are produced when hostile motivation is weaker than in any

Trills. Possibly, some Trills are produced when hostile

motivation is (actually) stronger than in any Twitters.

The frequent association of Trills with overt retreat would suggest that they usually or always are

produced when the escape tendency is stronger than the

attack tendency. But the actual strength of attack motivation probably is not negligible. The retreats closely

associated with Trills usually are not very rapid or

prolonged. More important, Trills sometimes are

closely associated with Rasping sounds, which certainly

include some aggressive tendencies (see pages 33 and

35). They may even intergrade with Rasping sounds.

One type of intermediate between the two classes of

vocalizations is shown in Figure 10.

The function(s) of Trills probably are not very

different from those of the Twitters which are uttered

in interspecific hostile situations. They seem to be

primarily warning or alarm notes (see also below).

• Loud Sharp Notes.—These notes may be uttered

singly or in irregular, variable, and obviously unritualized series. Single Loud Sharp Notes are very similar

to single Trill notes in basic form, but much louder

and with higher ultrasonic components (more harmonics). In some cases, at least, they include loud

components up to 45 kilocycles. The lower parts of

two more or less typical Loud Sharp Notes are shown

in Figure 11.

Such notes certainly are another type of alarm call.

They are uttered as reactions to potential predators.

Particularly as an initial reaction and/or when a preda-
NUMBER 2 8 31

16,000 -

Tim* (sac.)

0.8

FIGURE 11.—The lower parts of two typical Loud Sharp Notes by an adult Rufous-naped

Tamarin.

tor is very close (see above). They also occur during

particularly violent intraspecific disputes. They usually

are closely associated with escape movements, usually

vigorous and rapid escape ("blind panic" during intraspecific fights). They may be combined with Swaying,

Crown-smoothing, Head-flicks, and/or Tail-ruffling.

They are extremely "contagious." The sound of Loud

Sharp Notes by one individual usually induces the utterance of similar notes by all other members of the

same species in the immediate neighborhood. Once

started, they may continue to utter such notes for ten

minutes or more (a very long time for tamarins, which

tend to be extremely "changeable" or rapidly variable

in behavior). Loud Sharp Notes certainly are more

contagious than either Twitters or Trills. They also

stimulate escape movements by other individuals (relatively) more frequently than do either of the latter

patterns.

Obviously, the Loud Sharp Notes are high intensity,

produced by strong hostile motivation. And they probably are purely hostile. They are never closely associated with even partly friendly reactions among individuals of the same species. In these respects (also),

they resemble Trills. But the relative strength of the

escape tendency must be greater in Loud Sharp Notes

than in Trills. Not only are Loud Sharp Notes frequently associated with particularly vigorous overt

escape movements, but they seldom or never intergrade

or alternate with Rasps. Possibly the actual strength

of hostile motivation (as a whole) also is greater in

some or all Loud Sharp Notes. Some individuals uttering such notes seem to be more excited than any individuals uttering Trills.

The Loud Sharp Notes of Rufous-naped Tamarins

probably are largely or completely homologous with

the equally loud and almost equally abrupt alarm notes

of many other Platyrrhini, e.g., Cebus spp. As noted

above, they also seem to be related to several patterns

of Aotus and Callicebus moloch. Some or all of the

latter may not (usually) function as warning signals

now; but they may have been derived from, or contributed to the development of, such patterns in the

past. This subject is discussed in more detail on page

42 et seq.

Another point of comparative interest is considerably more problematic. Rufous-naped Tamarins seem

to have more different types of vocal alarm signals than

any other New World monkey whose behavior has

been studied. This may be correlated with their apparent vulnerablity to predation. But the exact nature

of the relationship remains obscure. All I can suggest

is that combinations of different types of signals may

provide more precise information about the positions

and probable intentions of potential predators, and/or

may be more effective in attracting and retaining

attention (of the predators and/or other tamarins),

than even a multitude of variations on a single type of

signal.

• Soft Sharp Notes.—Individual Soft Sharp Notes

are essentially identical with both Loud Sharp Notes

and individual Trill notes in basic form. They can

be distinguished only by other features. They are comparatively very soft, much softer than typical Trill
32 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

notes, to say nothing of typical Loud Sharp Notes.

(This is true at leafit in the range of frequencies, cycles

per second, audible to human ears. Some, although certainly not all, Soft Sharp Notes include ultrasonic components up to 44 kilocycles. But these also may be

softer than the equivalent parts of Loud Sharp Notes.)

Some Soft Sharp Notes sound approximately as loud,

in human ears, as many Twitters and single Short

Whines; others may be even softer. They always are

uttered singly or in short irregular series. These series

are rather similar to series of Loud Sharp Notes, but

probably are shorter, including fewer notes, on the

average, and relatively rarer (by comparison with

single notes).

Several of the individual notes shown in the illustration of a Trill in Figure 8 probably are (loudness excepted) very similar to the most common type of Soft

Sharp Note.

Soft Sharp Notes certainly intergrade with Loud

Sharp Notes (see Figure 5). They probably do so

rather frequently. They may also intergrade with Short

Whines, but I was never able to record an unmistakably intermediate pattern.

The significance of Soft Sharp Notes is difficult to

determine, for practical reasons. Notes of this type

certainly are uttered by individuals in the wild, but

they are so soft that a human observer may fail to hear

them. Thus, it is impossible to say anything very definite about their frequency, or the circumstances in

which they usually occur, under natural conditions.

16,000

Captive individuals sometimes utter many Soft Sharp

Notes while they move around their cages, as long as

they are not engaged in more elaborate forms of social

behavior, such as disputing or Allogrooming. This is

reminiscent of the single Short Whines (see above).

But Soft Sharp Notes differ from the Short Whines in

being apparently non-friendly. Captive individuals

sharing the same cage, and more or less well adjusted

to one another, utter Short Whines both when they are

close together and when they are far apart. But they

usually utter Soft Sharp Notes only when apart.

Soft Sharp Notes must be very low intensity patterns. Possibly, they are produced by much the same

type of motivation as Trill notes and/or Loud Sharp

Notes, when both attack and escape tendencies are

much weaker. One might expect that an individual

of a vulnerable species would be slightly "nervous"

whenever it moved around by itself, even in a familiar

environment. Also, I have heard Soft Sharp Notes

uttered in apparent response to usual loud noises outside the cages. Possibly, therefore, the Soft Sharp Notes

are the lowest intensity alarm call of the species. They

may also, at least occasionally, function as another

type of contact note. (If so, their evolutionary history

may have been somewhat comparable to those of the

"Gulps" and Sneeze-grunts of Aotus. See below.)

• Sneezing Sharp Notes.—Both typical Loud and

typical Soft Sharp Notes are quite "thin" and "clean."

Both might be transcribed as "Tsit." But Rufous-naped

Tamarins also emit notes which sound like "hoarse"

¥

0.5

Tim* (t«c.)

FIGURE 12.—The lower parts of two typical Sneezing Sharp Notes by an adult Rufous-naped

Tamarin.

1.0
NUMBER 2 8 33

versions of Soft Sharp Notes. A single note of this type

might be transcribed as "Tchuck." The actual sound is

almost as reminiscent of the "ordinary" unritualized

sneezes (which tamarins also perform in certain circumstances, see below) as of the other vocalizations.

Two typical "Tchuck" notes are shown in Figure 12.

It will be seen that both consist of two parts: first,

a single clear sound, beginning horizontal and then

descending abruptly, followed immediately by a thin

column of "white noise." This second part is very

similar to the Sneezes of Callicebus moloch in form

(unfortunately, I do not have a recording of the

ordinary sneezes of S. geoffroyi). Thus, it seems very

probable that the "Tchuck" notes really are ritualized

combinations of sneezes and Soft Sharp Notes.

Such Sneezing Sharp Notes certainly intergrade

with typical Soft Sharp Notes. They also are uttered

by captive individuals in much the same circumstances.

(I did not identify them in the wild, but there is no

reason to supose that they do not also occur under natural conditions.) Possibly, all or most captive individuals were a little more obviously "nervous" when

they uttered Sneezing Sharp Notes than when they

uttered ordinary Soft Sharp Notes. In any case, it seems

likely that both Sneezing and Soft Sharp Notes subserve much the same range (s) of functions.

• Long Rasps.—This pattern and the next are

parts of another complex which may be given the name

of "Rasping." Morphologically, the components of this

complex are the most distinctive of the vocalizations of

the species. All the other notes and calls (with the

partial exception of the Sneezing Sharp Notes) usually

are clear in tone, to human ears. But the Rasping patterns are definitely and unmistakably harsh.

Long Rasps themselves are loud harsh screeches.

Their actual length is variable, but the great majority

are more or less prolonged. Figure 13 shows one of the

shortest types, plus one of moderate (possibly average) length. It will be seen that each note is composed

of a very large number of separate pulses of sound, and

that the longer note is gradually ascending throughout

most of its length.

Long Rasps intergrade with both Broken Rasps and

(usually only in young individuals) Infantile Rasps.

They are uttered in a more restricted range of social

situations than most other vocal patterns of the species.

They are most common during extremely violent intra-

.specific disputes, when two individuals are actually

wrestling with one another. In such circumstances, they

may be uttered by the individual which begins the fight

and/or by the individual which is attacked. They also

occur occasionally during vigorous hostile chases. In

which case, they usually are uttered by the pursued

rather than the pursuer. Very rarely, they are uttered

during less vigorous disputes over food, quite apart

from chasing or contact fighting. One individual

simply stands and screeches in the face of another.

Finally, they are uttered by individuals caught and held

16,000 -^

,

I '

k» ' •

0.5

Tim* (sec.)

FIGURE 13.—Two "Long" Rasps by an adult Rufous-napcd Tamarin. The first note is rather

shorter than usual.

1.0
34 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

by human beings. Such individuals make violent attempts to escape, but they may also attempt to bite or

hit their captors.

These facts indicate that Long Rasps are purely

hostile, and high intensity on the average. Probably,

the escape tendency is stronger than the attack tendency during all or most Long Rasp performances, but

the attack tendency may be relatively stronger than

in any of the Plaintive or Sharp Note patterns described above.

The signal effects of Long Rasps are difficult to

identify, simply because they cannot be separated from

those of the accompanying or associated movements

and (other) visual signals. Possibly all or most Long

Rasps are slightly intimidating; i.e., function as threat

in the usual sense of the term.

The length of the Long Rasps, their motivation,

and the circumstances in which they occur, would suggest that they are strictly homologous with the Screams

of Callicebus moloch and Aotus.

They probably are less similar in form to the Screams

of C. moloch than are the Long Whistles (see page

25). But the differences in form may be less significant

(or less useful), in determining homologies, than the

other similarities between the two patterns. Particularly as it is not difficult to see how the differences

could be immediately adaptive.

The distinctive characteristics of the Long Rasps, in

this context, are both their harshness and the fact that

their loudest components are somewhat lower in pitch

than many or most of the loudest components of the

apparently homologous moloch pattern. This last feature really is quite remarkable. The Long Rasp is perhaps the only vocal pattern of the species which seems

to be closely related to a moloch vocalization without

being equally high, or higher, in pitch to human ears.

This apparent "discrepancy" may be correlated with

the relative rarity of Long Rasps, and their virtual

restriction to extreme emergencies. Selection pressure

in favor of high pitch, to avoid attracting the attention

of predators, may have been less severe in the case

of the Long Rasps than for most other vocal patterns

of the species. One might even suppose that attracting

the attention of other non-predatory and non-aggressive individuals, both other Rufous-naped Tamarins

and individuals of other species, might be positively advantageous in the circumstances in which Long Rasps

are most likely to be uttered. An individual being

chased, or engaged in a violent fight, might be relieved

by the appearance of some other animal (s) which

might distract its enemy or opponent. And, of course,

the mere contrast with most of the other vocalizations

of the species which is provided by the harshness of

the Long Rasps may enhance their "attention getting"

8,000

0.5 1.0

-f

1.5

Time (sec.)

FIGURE 14.—A typical Broken Rasp by an adult Rufous-naped Tamarin.
NUMBER 2 8 35

power, and thus increase the probability of attracting

distractors.

• Broken Rasps.—These are rapid series of short

harsh notes. Each series sounds like a single Long Rasp

which has been "broken up." Figure 14 shows a typical

series of this type.

Broken Rasps occur in much the same range of situations as typical Long Rasps, but they are even rarer

on the whole. During fights, they are most likely to

be uttered at the exact "moment of impact," just as

one individual leaps upon another.

The rhythm of Broken Rasp series is quite like that

of the most rapid Trills. Broken Rasps also alternate

and intergrade (see Figure 10) with Trills more frequently than do any other Rasping patterns.

These facts would suggest that they are produced

by much the same type of motivation as Long Rasps,

but are slightly higher intensity, on the average, and/or

include a slightly stronger escape component.

They also may function as threat.

• Persistent Infantile Patterns.—As noted above,

tamarins raised in captivity tend to retain essentially

infantile vocal patterns much longer than individuals

which have grown up under natural conditions. More

precisely, they tend to utter essentially infantile notes

more frequently at later ages than do wild individuals.

Sooner or later, however, even the most "backward"

individuals usually stop uttering such notes as part of

their "normal" repertory. This does not necessarily

mean that they cease completely. I have heard captive

adults, who have been behaving in an entirely adult

manner for some considerable time, suddenly utter

brief bursts of Infantile Squeaks and/or Infantile

Rasps, when obviously badly frightened (see page 12)

or in certain complex and extremely ambivalent social

circumstances, such as particularly vigorous Allogrooming performances. Possibly, these "recrudescent"

patterns function as some sort of "appeasement" and/

or "deceptive" signals (see both page 38, and Moynihan, 1955b). If so, they may (also) be related to the

Squeaks uttered by adult Night Monkeys in certain

sexual situations.

• General Comment.—Before proceeding to other

subjects, it may be useful to add some further comments on comparative aspects of the organization,

articulation, and functioning of the vocal repertory of

adult Rufous-naped Tamarins as a whole.

The only other Platyrrhini whose signal patterns

have been analyzed in detail, in both captivity and in

the wild, are Aotus trivirgatus and Callicebus moloch.

Many of the vocalizations of these two species certainly

are homologous. They tend, however, to be used in

very different ways. Intermediates among major types

of vocalizations are common in C. moloch, but relatively rare in adult Aotus. Many vocal patterns of

adult Night Monkeys are rather precise commands or

releasers (i.e., they can be described quite legitimately

in such terms as threat and appeasement). The same

patterns tend to induce the same responses in all other

individuals of the same species in a wide variety of

circumstances. The comparable and/or homologous

patterns of C. moloch, by contrast, are very much less

precise as commands or releasers. Each pattern tends to

produce different effects in different circumstances;

i.e., a listener of the same species seldom reacts to a

vocalization per se, but rather to the sounds interpreted

in the light of other stimuli perceived earlier or at the

same time.

With respect to these features, the acoustic signal

system of adult S. geoffroyi, as a whole, may be considered almost exactly "half way" between extremes.

Adult Rufous-naped Tamarins utter intermediates between major vocal patterns more frequently than adult

Aotus but less frequently than C. moloch. Some of the

vocalizations of adult S. geoffroyi are rather precise releasers and tend to produce the same effects in most

circumstances, like the patterns of adult Aotus; while

others are less precise or "imperative" as releasers,

produce less consistent reactions, and apparently need

to be combined with information from other sources,

like the patterns of C. moloch.

Another way in which the adult repertory of S. geoffroyi seems to be intermediate between those of the

other two species is the form or timing of associations

between different patterns. Of course, Rufous-naped

Tamarins frequently utter many different types of

notes in more or less rapid succession. It has already

been mentioned (see page 28) that Loud Sharp Notes

usually precede Twitters when the two patterns are

uttered together. When Trills are uttered also, the

usual sequence is Loud Sharp Notes-Trill-Twitter.

When Long Whistles are uttered in association with

hostile notes, the usual sequence is Long WhistlesTrill-Twitter. These sequences are so much more

common than any other combinations of the same patterns as to suggest that they are ritualized per se. S.

geoffroyi has more ritualized "linkages" of this type

than Aotus, but fewer than C. moloch. Moreover, none

of the ritualized series of geoffroyi is as complex, including as many notes of different types of patterns, as
36 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

the most complex ritualized series of C. moloch, the

so-called Songs.

Possibly, the Songs of C. moloch passed through a

stage, in the course of evolution, roughly comparable

to the series of S. geoffroyi in complexity. But the

ritualization of sequences would appear to have proceeded independently in the two species. The patterns

usually involved are either non-homologous, or occur in

different places in the sequences, in the two species.

It will be noted that the ritualized series of vocalizations of adult S. geoffroyi begin with high-intensity

patterns and end with the relatively low-intensity

Twitter. Also, there is an alternation of more and less

"aggressive" patterns. The Trill, which contains an

appreciable attack component, is interjected between

the high-intensity non-aggressive Long Whistle or Loud

Sharp Notes and the low-intensity non-aggressive Twitter. This sort of "alternating decrease" probably is a

very effective way of expressing highly ambivalent

motivation. It seems to be characteristic of many groups

of vertebrates; e.g., the Laridae (Moynihan, 1962). It

is not, however, the usual arrangement in C. moloch

Songs.

VISUAL COMMUNICATION

Adult Rufous-naped Tamarins have a larger number

of visual displays than either Aotus or C. moloch.

The groups of patterns described below includes

both unmistakable visual displays and a few other

unritualized patterns which are comparable in some

respects and/or homologous with displays of other

species. They all appear to have been evolved,

originally or primarily, to convey or control the transmission of visual information. Other patterns which

probably originated or developed as adaptations to convey olfactory information, but which may also function as visual signals at the present time, have been

described elsewhere (see page 20).

• Some Body and Head Movements.—Obviously

alarmed or frightened Rufous-naped Tamarins may

"freeze"; i.e., suddenly stop and stand or sit without

moving for an appreciable length of time. Silent freezes

may occur as a reaction to potential predators. Freezing

also is performed by captive geoffroyi when introduced

into a cage already occupied by other individuals of the

same species. In these circumstances, the frightened individual usually freezes in a crouch posture, and often

performs Crown-smoothing. This may be silent or accompanied by "recrudescent" Infantile Squeaks. A

typical crouch-freeze, with Infantile Squeaks, is illustrated in Figure \bb.

During both intraspecific and most interspecific encounters, an individual usually freezes just where it is

when it first sees the alarming stimulus. Probably only

during some responses to birds of prey (see page 13), is

a tamarin very likely to take shelter, dodge below a

branch, before freezing.

The freeze and crouch patterns of Rufous-naped

Tamarins are not particularly stereotyped or exaggerated in form. They probably are not displays in the

sense of the term used here (see page 11). But they

certainly are involved in visual communication. And

probably in quite opposite ways in different circumstances.

They must frequently be "anti-signals." They appear

to be primarily adapted to prevent the release of reactions. Even though an individual performing these patterns may not be really concealed, it may well be less

noticeable (and therefore less objectionable or appetizing) to a potential predator or opponent than it would

be if it were doing something else.

On the other hand, the two patterns are quite distinctive, rather unlike anything else in the repertory

of the species. Thus, when and if they should be observed, they may reveal a great deal about the state of

the individual performing them.

Freeze and crouch patterns seem to be relatively

very rare, or even absent, in Callicebus moloch, but

they are not uncommon in Aotus. (The crouch was not

distinguished as such in the account of Aotus in Moynihan, 1964, but it certainly is sometimes combined with

both the simple freeze and Head-down patterns of

the species.)

Another reaction of Rufous-naped Tamarins to potential predators is Swaying. (It is my impression that

Swaying probably is much commoner than freezing,

but I do not know how many freezing individuals may

have been overlooked.) During Swaying, the body is

moved repeatedly from side to side. The movements

sometimes are very extreme, but the head always remains facing forward, while the performing individual

fixates the disturbing stimulus. An individual may sit

with both hands and feet firmly clasping its perch

throughout the whole of a Swaying performance, or

it may stand up on its legs (see also below), or it may

lift its hands during the actual sideways movements

and clasp the perch again between movements. In apparently high-intensity performances, the movements

from side to side are moderately rapid, with little or
NUMBER 2 8 37

FIGURE 15.—Miscellaneous visual signals of adult Rufous-naped Tamarins: a (top), Tongueprotrusion, with some Nose-wrinkling and Eye-closing; b (center), crouch posture with Crownsmoothing (the mouth is opened as during the utterance of "recrudescent" Infantile Squeaks) ;

c (bottom), head-down posture with Crown-smoothing.
38

nothing in the way of intervening pauses. In apparently

low-intensity performances, by contrast, there may be

relatively long pauses (the performing individual

usually remaining tilted to one side throughout a

pause).

Swaying may be silent or accompanied by Loud

Sharp Notes, Trills, and/or Twitters. It frequently is

combined with Tail-ruffling, and may also be associated

with Crown-smoothing and/or Head-flicks.

It obviously is. at least in part, an expression of an

activated escape tendency. Probably, the escape tendency is quite strong during all or most Swaying. Swaying is most common during initial reactions to the appearance of a potential predator, and disappears

rapidly when habituation sets in.

Interestingly enough, it apparently never occurs during intra-specific encounters.

As noted in Moynihan (1967), Swaying is one of

the most widely distributed of platyrrhine patterns.

It seems to be common, exaggerated, and/or stereotyped enough in all species to be considered ritualized

in all. But it may be more or less "highly" developed.

The Swaying of S. geoffroyi is generally quite similar

to that of Aotus in both form and frequency. It is

somewhat less common and less exaggerated on the

average than that of Callicebus moloch. The Swaying

display probably subserves the same function(s) in all

species. It must alert predators to the fact that they

have been seen, and thus probably discourages them

from giving chase. It may also act as a (supplementary) warning signal to other individuals of the same

species.

S- geoffroyi shares another simple pattern with Aotus,

Callicebus, and many other Platyrrhini. This is the

head-down posture. As performed by Rufous-naped

Tamarins, it is not very conspicuous, at least at a distance. The neck is bent and the head is lowered a little.

This may be done while an individual sits still or walks

slowly. In both cases, the performance usually is silent,

but may be accompanied by Crown-smoothing (see

Figure 15c).

The actual head movement is so slight that one

hesitates to call the pattern a display. But there is

evidence that it may be of social significance. In its

typical form, at least, the posture is maintained for a

considerable number of seconds, or even several minutes. And it is performed only during certain types of

social encounters (see below). The comparative data

also are interesting in this connection. The head-down

SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

pattern of Night Monkeys is just as slight as that of

Rufous-naped Tamarins, although performed somewhat more frequently; but the most extreme versions

of the same pattern in Callicebus moloch are much

more exaggerated, and almost certainly ritualized.

Thus, it may be convenient to discuss some aspects

of the head-down of Rufous-naped Tamarins as if it

were a display, irrespective of its precise status at the

present time.

It probably is another alarm pattern, of some sort.

It is seldom performed except before or during retreat,

but it does not usually occur in the same situations as

Swaying and it is much rarer on the whole. More important, it is almost or completely confined to intraspecific reactions. It occurs during a variety of obviously ambivalent encounters between cage mates,

when the animals perform some overtly hostile movements, but still seem reluctant to fight. It may also

be performed before or during Allogrooming, especially grooming among individuals which are not (yet)

perfectly adjusted to one another.

This would suggest that it is produced by some combination of non-hostile motivation and the escape tendency (with or without some minimal attack component) . Possibly it is lower intensity on the average, and/

or contains relatively more escape, than such vocal

patterns as Twitters and single Short Whines.

An individual assuming a head-down posture usually "faces" toward the other individual which released

or induced the performance. Thus, the latter individual sees the posture from in front. It gets a particularly good view of the rufous nape patch (which is

usually more or less hidden from the front in other

postures). It also gets a good view of the white crown

patch; but the white or whitish of the chest and upper

arms is partly obscured by the lowered head. Thus, the

general effect of the pattern is to present more rufous

and less white than usual.

The quietness and inconspicuousness of the headdown of geoffroyi, and the circumstances in which it

occurs, indicate that it cannot be an antipredator device or warning pattern comparable to Swaying or

Loud Sharp Notes. Possibly, it usually functions as

appeasement; i.e., directly reduces the strength of attack tendencies in the companions toward which it is

directed, without simultaneously increasing their escape (or other) tendencies. (The existence of appeasing effects is always very difficult to confirm. But, at

least it can be said that individuals which assume
NUMBER 2 8 39

head-down postures are not usually attacked immediately afterwards.)

One wild Rufous-naped Tamarin was observed to

perform some peculiar patterns which may have been

related to typical head-down postures. This individual

reacted to my approach by uttering Trills and Twitters

while performing Swaying with Tail-ruffling. All this

was perfectly conventional. But, at the same time, the

individual also "bowed" its head very rapidly and repeatedly. These downward movements (quite different

from the lateral Head-flicks) looked like brief "intention movements" of assuming the head-down.

Possibly, a head-down component also was involved

in the remarkable "slow scratching" performance of

one captive individual described on page 43.

A spectacular Lie-back pattern was observed only

during a few unusually prolonged and violent disputes

between captive animals, when two individuals (see

below) fought over particularly choice bits of food

(grasshoppers) and one chased the other back and

forth for minutes on end. Several times, the pursued

individual became exhausted, or trapped in a corner of

the cage. Each time, it stopped trying to escape. It

then, either immediately or after a few seconds of violent wrestling, rolled or leaned over onto its back. It

lay there motionless and silent, making no attempt to

protect its exposed underparts. Rather astonishingly,

this stopped attack by the opponent immediately, or

prevented attack from developing. It appeared to inhibit all attempts to bite or hit by the opponent, even

when the latter was standing right over the reclining

individual. This pause endured for some seconds or

minutes. Then, the reclining individual (having caught

its breath or observed a possible route for further

escape) turned over and started to run again. Sometimes this induced further chasing and fighting, with

or without more Lie-back performances.

I think that Lie-back postures were assumed by only

one of the individuals kept in captivity. (Certainly,

they were not assumed by more than two.) But the

pattern produced such remarkable and stereotyped

effects that it can hardly have been a really individual

peculiarity. Probably, it is a ritualized and "normal"

part of the usual repertory of the species, but very high

intensity and confined to extreme emergencies. Possibly the reason that I did not observe it more frequently

is because such emergencies are very rare under natural

conditions, and most fights among captive individuals

were interrupted (by us) before they reached a sufficiently extreme stage.

To my knowledge, nothing similar to the Lie-back

of S. geoffroyi has been observed in any other Platyrrhini.

The performance might inhibit attack either because

it is threat or because it is appeasement. The few examples seen did not provide any direct evidence which

would permit a choice between these alternatives. But

it should be noted that the effectiveness of the pattern

may be correlated with the fact that it reveals and emphasizes larger expanses of white or whitish coloration

than any other display of the species.

The implications of this fact will be considered below (page 59), in connection with a general discussion of the functional significance of different colors.

Another somewhat problematic pattern is a standup posture. It has already been mentioned that Rufousnaped Tamarins occasionally stand up on their (hind)

legs in order to get a better view of some distant animal or object, and also during certain hostile encounters. In both cases, the standing up seems to be

quite unritualized per se; nothing more than a preliminary intention movement, a "preparation" for leaping,

and/or an initial phase of leaping suddenly arrested

by the effect of some counteracting stimulus ( I have

seen an aggressive individual stand up when its opponent assumed a Lie-back posture).

There are indications, however, that the simplicity of

some stand-up performances may be the result of a

rather complex evolutionary history. The best evidence

was provided by a particularly aggressive and fearless

adult male kept in captivity, in a very large outdoors

cage. For a period of several weeks, this male showed

a definite tendency to attack any human being who

entered his cage. He would rush forward, usually silently but sometimes uttering vocalizations which included attack components, and then stop short, only

a few inches or feet away from the human. He usually

stopped in a stand-up posture, or assumed such a posture immediately after stopping, and then remained

in the posture for some seconds. He also usually raised

his whole pelage, in a General Ruffle (see page 52),

during both the rush and the subsequent standing. His

appearance at this stage is shown in Figure 20. After

the rush and stand-up, he often performed a great deal

of very rapid Sit-rubbing, just like some very aggressive individuals during intraspecific disputes. He probably was trying to "demonstrate" that the cage "belonged" to him.

There was nothing about his stand-up postures, in

themselves, to suggest that they were basically differ-
40

ent from any other stand-ups; i.e., to suggest that they

were anything more than locomotory intention movements. The accompanying General Ruffles, although

undoubtly significant in some respects (see below),

probably were "accessory." (General Ruffles can be

combined with different postures and movements in

other circumstances, and the other stand-ups observed

were not combined with General Ruffles.)

The real interest of this behavior is comparative.

Many other Platyrrhini have a conspicuous, obviously

ritualized, Arch posture. This is characterized by extreme raising and arching of the back (in much the

same way as in the well-known hostile display of

domestic cats). Both Aotus and Callicebus moloch

have two principal variants of the Arch. In one, both

hands and feet remain firmly grasping the perch. In

the other, the hands are lifted, and the performing

animal stands up on its feet alone. The stand-up postures of the male tamarin cited above were not accompanied by raising or extreme curving of the back;

but they were quite similar to the standing Arch

postures of Aotus and Callicebus moloch in all other

aspects of form, such as the relative positions of head,

arms, and legs. The Arch of C. moloch also is combined

with a General Ruffle (Aotus does not seem to have any

special Pilo-erection patterns in any circumstances).

And there seem to be other resemblances in causation.

The Arch patterns of Aotus and Callicebus occur in

social situations which are comparable to those in

which the male tamarin stood up; i.e., they are performed by more or less aggressive individuals during

disputes of moderate or (more frequently) high

intensity.

These facts would suggest that there is some phylogenetic relationship between stand-up and Arch

patterns.

It seems likely, in fact, that the Arch postures were

originally derived (by a process of stereotyping and

exaggeration) from a locomotory intention movement

more or less similar to a stand-up. (There probably

was nothing else available, occurring at the right times

and in appropriate circumstances, to be "seized upon"

for ritualization when the development of an Arch

display first became advantageous.)

But this does not necessarily mean that the stand-up

pattern of S. geoffroyi, at least as shown by the aggressive male, is truly "primitive." The distribution of

ritiualized Arch postures among Platyrrhini is really

very wide indeed. They are performed by species which

are both different in ecology and only distantly related

SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

to one another. Among the larger platyrrhines, for

instance, they are characteristic of both Pithecia

monacha and Alouatta "palliata" as well as Aotus

and Callicebus. According to Epple (1967), they also

are performed by many other species of tamarins and

marmosets, including Callimico goeldii, Leontideus

rosalia, Callithrix jacchus, C. "leucocephala," and C.

argentata (Epple refers the last species to the probably

invalid genus Mico). This suggest that a ritualized

Arch display is an ancient feature of the Platyrrhini,

or a large part thereof, and that it must have been

present in the repertory of the ancestors of S. geoffroyi.

If so, then some of the stand-up postures of Rufousnaped Tamarins at the present time probably are

secondarily simplified or dedifferentiated remnants of

the more elaborate Arch. Such a process of simplification may be called "de-ritualization."

If these suggestions are correct, then the most remarkable feature of the history of the Arch display

in the S. geoffroyi lineage is that it seems to have come

full circle. The display seems to have decayed back

into a form which cannot be very different from that

of the original pattern from which it arose.

There are several reasons why all displays would

be expected to decay eventually (see discussion in

Moynihan, in press). But the de-ritualization of the

Arch during the evolution of geoffroyi may have been

facilitated or accelerated by a special factor. A conventional Arch of the usual platyrrhine type would not

reveal or emphasize the characteristic color pattern of

the species in a particularly advantageous way. Again,

see page 59.

(The account of the Arch and stand-up patterns in

Epple [1967] is unfortunately confusing. In one final

comparative summary paragraph, she states both that

all species of tamarins and marmosets perform Arches

and that such patterns were never observed in S. geoffroyi and S. oedipus. She also shows a photograph of a

Rufous-naped Tamarin allegedly performing "Katzbuckel-Drohen," a term which she applies to some of

the Arch performances of other species. But the photograph appears to represent an initial or terminal phase

of the stand-up with General Ruffle. And Epple's

actual description of the behavior in another passage

devoted to S. geoffroyi alone is not incompatible with

the one presented here. Presumably the confusion in

Epple's account is largely a matter of phrasing, due to

the fact that she recognized that geoffroyi has a homologue of the Arch without having the Arch itself.)

The last pattern in this group of Rufous-naped
NUMBER 2 8 41

Tamarin performances is Head-flicking. It occurs more

frequently than any of the others, with the possible exception of Swaying. In its typical form, a single Headflick consists of two or three very rapid but extreme

and conspicuous, and obviously ritualized, lateral

movements. The head and face are turned first to one

side and then back; or first left and then right (or vice

versa) and then back. Sometimes the main movements

are followed by very rapid but slight lateral "vibrations" of the head.

Head-flicking may be silent or accompanied by vocalizations. By far the most common vocalizations are

Loud Sharp Notes. Usually there is one note per single

Head-flick. The only other vocalizations ever heard to

be uttered by adults during Head-flicking were a very

few Soft Sharp Notes, (possibly) a few Sneezing Sharp

Notes, a few single Short Whines, and (twice) Trills.

(In this respect, adult geoffroyi are rather different

from young individuals of the same species, which may

combine Head-flicks with a greater variety of vocalizations. See page 66.)

Adults perform Head-flicking during both interspecific and intraspecific encounters. Wild individuals

perform it as a reaction to potential predators. Captive

individuals may perform it when a human being enters

their cage, especially when attempts are made to catch

them or they have been conditioned to expect to be

caught. In both sets of circumstances, the Head-flicking is frequently, perhaps usually, accompanied by

Tail-ruffling. Possibly, it is accompanied by Crownsmoothing equally frequently. Sometimes, as noted

above, it is combined with Swaying. It usually is followed by overt retreat or escape movements. Apparently identical Head-flicking is frequently performed

by captive individuals when they are released into cages

already occupied by other individuals of the same

species, especially when the newcomers and the

"owners" of the cages are unfamiliar with one another.

This Head-flicking also may be associated with Tailruffling, Crown-smoothing, and/or overt unritualized

hostile movements. The latter may include some overt

attack patterns, but attack after Head-flicking always

is much less common than overt escape.

All this would suggest that Head-flicking is purely

hostile. It should be mentioned, however, that captive

individuals also perform Head-flicks in close association with a variety of other displays during Sexual

Sniffing (see below). Males may even do so during

the Sexual Sniffing which accompanies some copulations (see page 14). But all the situations in which such

behavior occurs probably are very highly ambivalent

and may contain appreciable hostile components. Even

during copulation, a male may be frightened, and possibly even irritated, by the close proximity or behavior

of his companion (or as an after-effect of the maneuvering which may have been necessary to permit

mounting). Thus, there is no reason to believe that the

Head-flicking movements in such circumstances are

not also (and only) expressions of hostile tendencies

which are included in the complex motivation of the

performing animals.

When Head-flicks are performed during reactions to

potential predators, they are most frequent during the

first stages of the reactions, when the performing animals seem to be most excited. Similarly, when they are

performed during obviously hostile disputes among individuals of the same species, they usually are most

frequent during the periods in which the general excitement seems to be greatest.

It seems very probable, therefore, that Head-flicking

is still another high-intensity pattern in which the

escape tendency is greatly preponderant. Possibly, Loud

Sharp Notes with Head-flicks are higher intensity, on

the average, than similar notes without Head-flicking.

Swaying with Head-flicks may be higher intensity

and/or contain a stronger escape component than

Swaying alone.

I can say very little about the signal effects of Headflicking movements, simply because they are impossible

to distinguish from those of the accompanying acoustic

and other visual displays. Possibly, all or most Headflicks function as additional alarm or warning signals

during interspecific encounters and as another form of

appeasement during intraspecific encounters.

Perhaps their principal claim to interest also is comparative. Many New World monkeys give a brief lateral

shake of the head when they sneeze. It has already been

mentioned that Rufous-naped Tamarins perform "ordinary" sneezes in addition to uttering Sneezing Sharp

Notes. These ordinary sneezes sound like soft versions

of the corresponding human pattern. They seem to be

cleaning or "comfort" patterns, a means of clearing

the nasal passages. They are not associated particularly

closely with any special type(s) of social behavior,

and they appear to be quite unritualized, without any

special signal function. Many, but probably not all, of

the ordinary sneezes of Rufous-naped Tamarins are

accompanied by head shakes of the usual platyrrhine

type. These are comparatively very slight and inconspicuous, much less extreme than the typical Head-
42 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

flicks described above. (Possibly, some of the Sneezing

Sharp Notes are accompanied by the same movements

as ordinary sneezes. But, even in these circumstances,

the movements are impossible to confuse with real

Head-flicks.) Nevertheless, it seems quite possible that

the ritualized Head-flicks were derived from the head

shakes accompanying unritualized sneezes, in the

course of evolution, by a process of exaggeration.

If so, the fact that Head-flicks are characteristically

associated with Loud Sharp Notes in S. geoffroyi means

that the species has two more or less stereotyped combinations of sneeze and Sharp Note patterns in its signal

repertory.

This complicates comparisons with other species. For

this reason, and also because brief references to more

or less definitely related patterns of other species are

rather scattered in the preceding pages, it may be useful to insert a partial recapitulation here, to summarize

the sneeze-like and Sharp-Note-like patterns of

Saguinus geoffroyi, Aotus trivirgatus, and Callicebus

moloch, in the hope of clarifying the various resemblances and differences among them.

Saguinus geoffroyi adults have:

1. Ordinary sneezes. Non-ritualized. Without signal

function.

2. Head-flicks. Probably ritualized derivatives of

sneezing movements. So exaggerated in form that they

must have signal function(s).

3. Loud Sharp Notes. Frequently but not invariably

associated with Head-flicks. Primarily alarm or warning signals.

4. Soft Sharp Notes. Very closely related to Loud

Sharp Notes, but not usually associated with any sneezing pattern or derivative thereof. Alarm and/or contact

notes.

5. Sneezing Sharp Notes. Essentially stereotyped

combinations of Soft Sharp Notes and the audible part

of sneezing. Not usually associated with Head-flicking,

the ritualized (visible) derivative of sneezing movements. Alarm and/or contact notes.

Aotus trivirgatus adults have:

1. Ordinary sneezes. Non-ritualized. Without signal

function.

2. Sneeze-grunts. These sound like ritualized combinations of the audible part of ordinary sneezes and

the "Gruff Grunt" vocalizations of the species. Gruff

Grunts by (or in) themselves do not sound like anythink in the repertory of S. geoffroyi. But the Sneezegrunts are relatively loud, sharp, and brief. They also

are associated with Moans and Low Trills, in series, in

much the same way that Loud Sharp Notes are associated with Twitters (which seem to be homologous

with Low Trills). Thus, it is possible that the Sneezegrunts include a component which is homologous with

the Loud Sharp Notes. (This component probably is

quite distinct, in origin, from the Gruff Grunt component. But it is just barely possible, in view of the fact

that some homologues of high-pitched patterns of S.

geoffroyi are low pitched in A. trivirgatus [see page 24]

that the Gruff Grunts themselves are phylogenetically

related, in whole or in part, to the Loud Sharp Notes.)

The loudness, sharpness, and brevity of the Sneezegrunts, all qualities which are reminiscent not only

of Loud Sharp Notes but also some alarm patterns of

many other Platyrrhini such as Cebus and Saimiri,

would suggest that they may have originated as warning signals. But they apparently do not function as such

now. At the present time, they seem to be contact notes.

4. Gulps. Not including any recognizable sneeze or

sneeze-derived component, but rather brief and abrupt;

functioning as contact notes at the present time; possibly related to Gruff Grunts; and, therefore, possibly

having had a similar evolutionary history.

Callicebus moloch adults have:

1. Ordinary sneezes. Non-ritualized. Without signal

function.

2. Hostile sneezes. Identical with ordinary sneezes

in form, but apparently produced by hostile motivation

(with the escape tendency preponderant). Tend to

precede Moans in the same way as the Sneeze-grunts of

Aotus. Signal function(s), if any, obscure.

3. Chuck Notes. Sound quite like Loud Sharp Notes.

Possibly strictly homologous. Probably originated as

warning signals; but functions apparently various at

the present time, differing in different circumstances.

4. Chirrups. Sound like stereotyped intermediates

between Chuck Notes and Moans (i.e., probably composed of all or most of the same elements as the Loud

Sharp Note - Twitter, Sneeze-grunt - Low Trill, and

Sneeze-grunt - Moan series of other species, but with

the various elements "telescoped" together to such an

extent that they have become simultaneous). Signal

functions differing in different circumstances.

5. Callicebus moloch also has several other vocalizations which seem to be related to the Gruff Grunts of

Aotus, but which are even more distinct from any

pattern of S. geoffroyi.

• Apparently Irrelevant Acts.—These are patterns

which appear to be performed "out of context," the
NUMBER 2 8 43

sort of behavior which has been called "displacement"

in the ethological literature.

The number and/or importance of such patterns

would seem to vary considerably from species to species

within the Platyirrhini. Aotus probably has no patterns of this type. All or most of the other species observed would seem to have at least one. This usually

takes the form of movements or postures. (Among

the few possible or probable exceptions to this general

rule may be the hostile sneezes of C. moloch cited above.

These would appear to be "displacement" in the conventional sense of the term.) In most species, the most

common movements are self-grooming, and especially

scratching. Apparently irrelevant scratching certainly

occurs in Saimiri (Ploog, Blitz, and Ploog, 1963), Cebus

spp., Ateles ssp., Alouatta "palliata," and Callicebus

moloch. In all these forms, it is performed in a more

or less wide range of complex or "difficult" social situations, by individuals which are "frustrated" or

thwarted for one reason or another. Ateles and

Alouatta perform apparently irrelevant scratching

comparatively very frequently, and usually in a stereotyped and ritualized form (different in the two genera).

C. moloch performs such patterns much less frequently,

but probably in an equally stereotyped way (although,

again, the form is distinctive).

Saguinus geoffroyi may be partly intermediate between Aotus and some of the larger Platyrrhini with

respect to the development of apparently irrelevant

acts. Most individuals of this species certainly do not

perform "unexpected" comfort movements in most situations of social stress. But this probably is not true of

all individuals in all circumstances.

I saw one captive adult female repeatedly rub her

back, and/or the side of her head and face, against the

walls of her cage immediately after males failed to

respond to her soliciting patterns, "invitations" to

copulate. These movements appeared to be very similar to, or even identical with, "normal" comfort or

cleaning patterns in physical form. They were remarkable only because the female did not have dirt on

her back or face at the times.

Another captive adult female performed more conspicuous, distinctive, and perhaps even more problematic patterns. She was kept alone in a large outdoors

cage. After several months of such isolation, first one

male (a nearly full-grown juvenile) and then another

(completely adult) were released into her cage and

allowed to remain there. These introductions provoked

a great many hostile reactions among all three individuals, plus a variety of friendly or partly friendly, or

even partly sexual, performances; but no immediate

copulation attempts. During the first few days after

the introduction of the males, the female repeatedly

performed a remarkable complex of patterns which

may be called "slow head-scratching." She always did

this when neither male was particularly close. Sitting

silently in a more or less hunched posture, probably a

type of (or related to) the head-down (and similarly

revealing the full extent of the rufous nape patch),

and with her tail Looped up between her legs (see

page 45), she would scratch her head very, very slowly

in an extremely "cautious" looking manner. These

movements were quite different from the usual scratching movements of the species, and the same female in

other circumstances, which are brisk and vigorous. The

female usually began by scratching her white chin.

Then she usually scratched her white crown. This is

illustrated in Figure 166. Occasionally, she omitted

the chin-scratching. Also occasionally, she scratched

her (white) forearm in addition to her chin and crown.

Once, the chin-scratching was preceded by scratching

of the belly or lower breast. But, to my knowledge, the

slow scratching was never extended to any other part

of the body or head. (This is another feature in which

it differed from ordinary self-scratching in other

circumstances.)

The fact that this peculiar behavior was closely

associated with a great variety of both hostile and nonhostile reactions would suggest that it was an expression

of highly ambivalent motivation, the result of a strong

conflict between incompatible tendencies (a particular

type of frustration).

Other males were introduced to other previously

isolated females in a variety of cages of different sizes

and shapes, at the same and at different times of the

year, without ever inducing any similar performance.

This would suggest that the slow scratching of the

one female was a real individual peculiarity. There is

other evidence that points to the same conclusion. Unlike the equally spectacular Lie-back pattern cited

above, the slow scratching was not obviously directed

toward other individuals. Nor did it provoke any obvious, overt reaction by other individuals. This would

indicate that it was not a species-specific display, not

even a high-intensity display which might be expected

to appear only rarely.

If so, the fact that an individual of the species can

develop such an unique pattern is an interesting resemblance to Cebus capucinus (and probably other
44 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

FIGURE 16.—Special postures and movements of adult Rufous-naped Tamarins: a (top), mates

sitting close together, with the female having her tail Looped over the male's leg; b (bottom),

posture assumed by a female during slow head-scratching, with Looped tail and (probably), a

head-down component.
NUMBER 2 8 45

species of Cebus). Some capucinus individuals tend to

develop special "nervous mannerisms" or "quirks" in

captivity (M. Bernstein, personal communication).

These are movements and postures which are not

species-specific (or population-specific). Different individuals may develop different mannerisms, often involving different parts of the body. Many mannerisms

seem to have been derived from ordinary grooming or

scratching movements, but even these are modified in

different ways by different individuals. (C. capucinus

apparently does not have a common stereotyped form

of "displacement" like Ateles and Alouatta. Conversely,

it also seems likely, although it has not been definitely

established yet, that Ateles and Alouatta do not tend

to develop individual quirks in addition to their stereotyped performances.) As a group, the special mannerisms of capucinus individuals appear to be responses

to a fairly wide variety of "conflict" or frustration

situations. But each individual usually is quite consistent in using its own mannerism(s), in more or less the

same form, in the same particular situation (s).

The performance of such mannerisms should reveal a

great deal about the situation and motivation of a

performing animal—to any other individual "prepared" to receive such information in such form. If

quirks really were used in communication, and especially if individuals tended to learn them from one

another, then they would be strictly comparable to the

"artificial" learned sounds used in human languages.

Unfortunately, it is still a dubious question whether or

not C. capucinus individuals pay any signficant attention to the quirks of their companions. But, in any

case, whatever the function(s) of such patterns may

be, the ability to perform a few quirks in exceptional

circumstances, as shown by Rufous-naped Tamarins,

probably represents an early stage in the evolution of

the ability to perform a great many quirks in a wider

range of circumstances, as shown by C. capucinus.

This type of similarity between S. geoffroyi and C.

capucinus is rather surprising in view of the fact that

the two species differ in ecology, and usually are organized in rather different social groups. (C. capucinus

also seems to be much more "intelligent," in the ordinary sense of the term, than S. geoffroyi—and certainly

has a much more "highly developed" brain, of more

obviously complex structure.) It is at least conceivable,

therefore, that the resemblance between the two species

is an indication of special phylogenetic relationship.

But Saguinus can hardly be as closely related to Cebus

as it is to some other genera. See also comments on

page 75.

• Tail Patterns.—The tail probably is the most

"expressive" organ of S. geoffroyi. It can be held and

moved in many different ways, to convey different

messages.

When running or leaping, a Rufous-naped Tamarin

usually lets its tail "stream out" behind the body. The

tail may be nearly straight, more or less horizontal and

continuing the line of the back, or (more frequently)

curved in a modified S-shape, horizontal or slanting

downward at the base, then rising, and then curving

downward at the tip. Figure 1 illustrates a very simple

curve, with moderately extreme Tail-ruffling.

A standing or sitting individual sometimes lets the

tail hang straight, vertically, downward. This is done

when the individual is not alarmed, but is not prepared

to relax. It is not usually combined with vocalizations,

but is frequently followed by walking or running. It can

hardly (by itself) be described as a movement, but it

is potentially capable of transmitting the same message

as the locomotory intention movements of many other

species, and it may subserve the same function (s).

(The usual locomotory intention movement of Callicebus moloch is a raising [upward and backward] of

the basal part of the tail. Rufous-naped Tamarins may

perform similar-looking movements, but apparently

only during some defecation, urination, and ritualized

Rubbing performances. Such movements probably do

not function as [separate] social signals in geoffroyi.)

When a sitting Rufous-naped Tamarin is prepared

to rest or sleep, it brings its tail forward and upward.

Usually, the tail is brought up between the legs. Occasionally, it is brought up alongside the body. Sometimes

the tail is brought up very far, and the distal half left

largely uncurled, so that it stretches up and across the

Whole front of the animal's body and head. This is a

common occurrence in Saimiri, but is not usual in

Saguinus. In most cases, a relaxed Rufous-naped Tamarin, having brought the tail up between the legs,

allows the distal half to "settle" in a loose, often irregular or asymmetrical, loop. The extent to which the tail

is visible, to an observer looking from the front or side,

is quite variable, partly because the "bends" in the

tail may occur in different places between tip and base.

Despite this considerable variability, the pattern as a

whole is exaggerated enough to suggest that it is at

least partly ritualized. The Tail-looping of the slowscratching female illustrated in Figure \6b may be as

"typical" as any, in physical form, in itself. But most

356-597 O - 70 - 4
46

Looping is not combined with either special quirks or

other signal patterns. In particular, it is seldom or

never accompanied by any raising of the hairs of the

tail.

When mates are sitting side by side, one individual

may Loop its tail over part of the body of the other.

An example of this is illustrated in Figure 16a.

Presumably, Tail-looping always functions as a

signal insofar as it indicates that an individual is undisturbed and is not planning to move. When one

individual Loops its tail over the body of its mate, the

performance also may provide some tactile stimulation.

It seldom or never provokes any overt response by the

mate, but the mere contact may help to strengthen

pair bonds. In many circumstances, however, Taillooping may be even more important in quite another

way. The tail often is surprisingly conspicuous in the

field when it is allowed to hang downward. There

often is little or nothing else in the immediate environment which is of comparable length, nearly straight

and vertical, and equally dark. (Most lianas and small

branches are lighter, oblique or horizontal, and/or

twisted or more irregular in shape.) Thus, the tail often

is the first part of the body noticed by a human observer. Other potential predators probably react similarly. Of course, the conspicuousness of the tail is

greatly reduced when it is raised and curved and partly

hidden between the legs. It seems very probable, therefore, that Tail-looping also is a protective device. It

may be a signal to other individuals of the same species,

but it also seems to be a means of concealing a potentially dangerous sign stimulus from individuals of

other species.

The remaining tail patterns may be more highly

ritualized, as they are more stereotyped in some ways.

They are not invariable in form, but the variations are

somewhat more predictable.

The simplest is the Tail-forward. It can be performed by an individual while sitting, standing, or

walking. The tail hangs downward, but is inclined

forward and more or less curved at the tip. The actual

angle of inclination and degree of curving differ in

different circumstances. Two examples are shown in

Figures 17a and 17b.

This obviously is another indication of alarm. It is a

very common reaction of wild individuals to the appearance of a human observer, and it frequently is

followed by overt retreat or escape movements. Probably, it is produced by a rather wide range of hostile

motivation. Sometimes it is performed by individuals

SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

which are absolutely silent and which retreat only

short distances. At other times, it is performed by individuals which utter Loud Sharp Notes and/or Twitters. In such cases, it may be accompanied by Swaying

and followed by rapid and prolonged escape. When

Twitters are uttered, the Tail-forward may also be accompanied by a slight amount of Tail-ruffling, but

otherwise the two patterns seem to be largely or completely mutually exclusive. Very excited individuals

which utter many vocalizations tend to bring the tail

farther forward under the body than do less excited

individuals. Individuals which utter comparatively

many Loud Sharp Notes tend to bring the tail farther

forward than individuals which utter mostly Twitters.

Individuals which have the tail far forward tend to retreat earlier, farther, and /or faster than individuals

which have the tail only slightly forward. These facts

would suggest that the more extreme Tail-forward

patterns are expressions of stronger hostile motivation

(as a whole), and/or relatively greater preponderance

of the escape tendencies, than the less extreme versions of the same pattern.

All forms of the pattern probably function as additional warning signals to other individuals of the same

species. Insofar as they modify the conspicuous verticality of a downward hanging tail, they may also be

protective or concealing in much the same way as

Tail-looping, although to a much lesser extent.

Another pattern may be called "Tip-coiling." This

often looks like an exaggeration of part of one type of

Tail-forward. The distal part of the tail (usually anything from one-fourth to one-half of the total length)

is not only curved, but actually coiled. Sometimes all

the coils are in one plane. In which case, the coiling

usually is tight, and all the coils are touching. At other

times, they may "sprawl" or fall sideways, to produce

a "corkscrew" effect. (This is difficult to describe in

words, but the two forms are illustrated in Figures 17c

and 17c?.) Tip-coiling probably is performed most

frequently by individuals which are sitting or standing

at the time. In these circumstances, the performing

individuals usually let the uncoiled part of the tail

hang straight downward. At least occasionally, however, what seems to be essentially the same pattern may

be performed by an individual which is leaping or

running. Then the longer part of the tail is allowed

to stream out behind, in the usual way, but the tip is

"tied up" in a tight little "knot."

The individuals which perform Tip-coiling often are

unmistakably alarmed. This is another resemblance
FIGURE 17.—Special postures of the tail indicating alarm.

From top to bottom: a, extreme Tail-forward; b, slight Tailforward; c, one form of Tip-coiling; d, another form of Tipcoiling.
48 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

between Tip-coiling and the Tail-forward. But Tipcoiling seems to be relatively rare in the wild, under

natural conditions, and relatively more common in captivity, especially when individuals are rather crowded

together. In captivity, it usually is associated with many

other signal patterns which contain appreciable escape

components (e.g., Loud Sharp Notes, Twitters, Trills,

Crown-smoothing), as well as overt escape and retreat movements; but most of the observed associations were not particularly helpful in revealing how the

motivation and function(s) of the Tip-coiling might

differ from those of the other signals. There is only

a little evidence which may be more useful. The individual seen to perform (usually loose) Tip-coiling most

frequently was a subadult kept in a small cage with

two other individuals of approximately the same age,

to whom it appeared to be slightly subordinate. This

individual also tended to utter Infantile Squeaks and

Infantile Raps relatively frequently, sometimes immediately before or during Tip-coiling. It may also be

significant that the actual coiling part of the pattern is

somewhat similar, in form, to the more extreme Upward Tail-coiling display, which is largely or purely

sexual (see below). These facts might be interpreted

to mean that Tip-coiling is produced by some combination of hostile (primarily escape) and non-hostile motivation, functions as a warning and/or appeasement

or "deception" (see Moynihan, 1955b) display, and

may have originated as a ritualized intermediate between the ordinary Tail-forward and Upward Tailcoiling.

The Upward Tail-coiling itself is the most elaborate

of the special tail patterns. It always is performed, or

at least begun, by an animal who is standing or sitting

at the time. In its typical forms, it always involves the

coiling of the whole of the tail. More often than not, an

animal who performs the pattern has had its tail hanging downward beforehand. In which case, the Coiling

may take either one of two forms. In the simpler of the

two, the actual coiling movements begin at the tip of

the tail, the rest of which continues to hang downward

for the moment, and then continue upward toward the

base, usually in more or less the same plane. The tail

simply "rolls up" into a large coil immediately below

and slightly behind the rear of the body and legs. In

the more complex of the two forms, the whole tail

is lifted upward, to stretch more or less horizontally

backward behind the body, just before or just as the

coiling movements begin. Again, the coiling movements proceed from tip to base. But the process might

be more correctly described as "rolling forward" than

as "rolling up." Sometimes the "rolling forward" is not

all in the same plane. The tail may begin to coil laterally (the broad plane parallel to the ground) and then

continue vertically. The actual coiling itself always is

very rapid, in all circumstances. Thus, the up - lateral -

vertical sequence gives the impression of a sideways

"flick" or "swish." This can be very noticeable; it is

just the sort of movement which tends to attract the

attention of even an inattentive observer. If an individual who performs Upward Tail-coiling has had its tail

draped over or along a branch (rather than hanging

down) beforehand, then the coiling movements will be

more or less upward or forward depending upon the

relative positions of the branch and the body of the

performing individual. In any case, as soon as the coiling is complete, the animal usually slips the coiled tail

forward between its legs, so that the main body of the

coil rests on the substrate beneath the breast or belly.

If the animal was sitting down beforehand, it has to

raise its hind quarters in order to pass the tail forward.

But it almost always sits down again immediately afterwards. Even if it was standing beforehand, it usually sits

down within a few seconds after passing the tail forward. The sitting postures do not seem to be ritualized

as such, apart from the position of the tail. The tail

itself is seldom Ruffled at any stage during the performance. The coiling also usually is and remains very

tight. As a result, the tail becomes very inconspicuous

indeed as soon as it is passed underneath the body, even

less conspicuous than when it is Looped. Not infrequently, it is quite invisible from the side. Having assumed a sitting posture with the tail coiled, an individual may remain in it for several minutes.

All this behavior usually is silent.

As a whole, at least in its typical forms, Upward

Tail-coiling is "essentially" feminine. Females perform it very, very much more frequently than do males.

And, as mentioned above (page 14), Upward Tailcoiling by females apparently is the "normal" precopulatory display of the species.

It certainly seems to be an expression of copulatory

motivation. Females which perform the pattern almost

always are prepared to allow males to mount immediately. (I observed only a very few exceptions to this

general rule, and they all occurred during obviously

ambivalent encounters between males and females who

were not well adjusted to one another. In all these
NUMBER 2 8 49

cases, the development of sexual behavior was interrupted by the outbreak of overt hostilities.)

Upward Tail-coiling was seen to be performed (or

recognized as such) only among individuals kept in

captivity. The fact that it is a "normal" part of the

repertory of the species is indicated by several lines of

evidence. It is quite common in captivity, in some situations. It also is more stereotyped, performed by more

individuals in the same way, than would be expected

of a learned quirk. Presumably, it was not seen or

recognized in the wild simply because copulations

were not observed in the wild.

A complete Upward Tail-coiling performance by a

female usually is very attractive to a male. It frequently

induces the male to approach the female, irrespective

of whether or not he mounts her after the approach.

At the very least, such behavior by a female must

indicate that she is receptive. Conceivably, it may also

be used more "actively," as a soliciting pattern. Some

or all of the components of the performance may

actually stimulate, i.e., increase the actual strength of,

the sexual tendencies of a male. The orientation of the

pattern is somewhat variable. Females which are only

weakly motivated (as shown by the fact that they allow only a few copulations afterwards) tend to perform Upward Tail-coiling wherever they happen to

be when the spirit moves them, without attempting

to orient the pattern in any special way vis a vis

a male. But more highly motivated females definitely

try to "present" their backs (and therefore also reveal

and emphasize the tail movements) to the males. A

female may even approach a male in order to do so.

She may pass right in front of him and perform Upward Tail-coiling only a few centimeters in front

of his face. (This may also provide olfactory information and stimulation.) A female performing Upward

Tail-coiling with her back to a male sometimes looks

over her shoulder, apparently to see what effect her

behavior is producing. (This does not seem to be "discouraging" or intimidating in the same way as the

similar movement during copulation itself, see page

14.)

(It will be noted that the behavior sometimes used

to solicit copulation, apart from the accompanying

tail movements, is not very different from the behavior

sometimes used to solicit Allogrooming.)

Many or most females of long established pairs tend

to perform the actual coiling parts of Upward Tailcoiling with a minimum of "fuss" or "ostentation," i.e.,

they usually do the simplest type of "rolling up." But

females of more recently established pairs, and especially females confronted with quite unfamiliar males,

often perform particularly conspicuous lateral

"swishes."

It seems possible, therefore, that Upward Tail-coiling is partly a double signal. The ultimate result of

the performance, sitting with the tail coiled underneath

the body, may indicate receptivity and nothing else.

Perhaps the actively stimulating effect is produced only

by the approaches and the "preliminary" coiling or

rolling movements.

The form of Upward Tail-coiling is rather surprising in a sexual soliciting pattern. Offhand, one might

have supposed that the position of the tail between

the legs would block access to the female's genitalia.

Obviously this is not the case, but the position of the

tail can hardly facilitate the mechanics of the copulatory act. (It probably is significant, in this connection,

that both Aotus and Callicebus females do not perform

Upward Tail-coiling. If they do anything at all, they

raise the base of the tail or move it to one side immediately before or during copulations. And it has

already been mentioned that a female Rufous-naped

Tamarin which has performed Upward Tail-coiling

before copulation usually "relaxes" and lets the tail become partly uncoiled as the copulation reaches a

climax. See page 14 and also Figure 19.) Thus, it is

evident that Upward Tail-coiling has not been selected

simply because the performance, in itself and apart

from its signal functions, is particularly convenient.

Here again, it seems likely that the concealment (from

the eyes of a potential predator) of the otherwise alltoo-visible tail has been a crucial consideration.

Copulating tamarins probably are particularly vulnerable to predators (they cannot be very "wary" while

their attention is engaged elsewhere). Thus, any protective or concealing device probably is particularly

advantageous at such times. This may explain why S.

geoffroyi has evolved Upward Tail-coiling, rather than

something else, as a precopulatory display. The conspicuous part of the performance, the actual coiling, is

very rapid and brief. And the remainder is as little

conspicuous as anything could reasonably be expected

to be in the circumstances.

Epple (1967) says that a female "saturates" her

tail with urine during Upward Tail-coiling. But the

females observed on Barro Colorado Island certainly

did not urinate visibly at any stage of their

performances.
50

Some other aspects of the timing and occurrence

of the display may deserve to be noted in passing.

No matter how highly motivated she may be, an

unmated female confronted with an unfamiliar male

does not usually perform Upward Tail-coiling until

she is certain that the male is sexually interested in

her. Thus, the first copulation between previously unacquainted individuals may not be preceded by any

special display. The male may take the female by

surprise, and mount her without preliminaries. Such

copulations sometimes appear to be completely successful. But all the subsequent copulations between the

same individuals usually are preceded by Upward

Tail-coiling of the usual types, irrespective of whether

the first attempt has been successful or not.

Females which perform Upward Tail-coiling obviously are sexually "unsatisfied." They could be described as "frustrated." But it should be stressed that

this frustration usually or always is due to the absence

of consummatory stimuli, or the inability to perform the

consummatory act in the absence of a suitable and

willing partner, and not to any motivational conflict.

A female usually stops Upward Tail-coiling immediately, or performs it in a highly modified form (see

below), as soon as any hostile motivation is activated.

Granted that female Upward Tail-coiling is an expression of unsatisfied copulatory motivation, one might

expect that it would cease, at least temporarily, even

in the absence of any hostile behavior, immediately

after a successful copulation has been performed. But

this does not always seem to be the case. I have seen

females perform the pattern immediately after prolonged copulation attempts in which the males made

many pelvic thrusts in a well-oriented and apparently

perfectly normal manner. Even when a female has

partly uncoiled her tail at the climax of a copulation

attempt, she may "re-coil" it again as soon as the male

dismounts. This would seem to suggest two alternative

possibilities. Either females frequently need several

copulations in order to be satisfied (which seems unlikely in view of the usual rarity of copulations among

well-adjusted pairs—see page 14). Or the satisfactions

which they may derive from copulations are not provided, directly, by the movements of the males, but

by some later (presumably physiological) changes

within themselves.

Males were seen to perform, rather than respond to,

Upward Tail-coiling on only two occasions.

Once, it was performed by an adult male shortly

after he was released into the cage of an unfamiliar

SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

adult female. Both individuals had been isolated for

some weeks previously. They showed considerable

overt hostility toward one another when first brought

together. But the male also made intention movements

of approaching the female in a manner which did not

seem to be purely hostile. After some minutes, he

pulled his tail up into a complete but loose spiral (i.e.,

with the coils not touching one another), and held it

behind his body, without making any attempt to bring

it forward between his legs (see Figure 18a). Then he

walked slowly backward toward the female, still maintaining his tail in the same position. Finally, he actually bumped into her. Whereupon she turned her

head and stared at him. And he ran away immediately,

uncoiling his tail as he went.

The other occasion was similar in some respects. An

adult male was released into the cage of an adult female. But these individuals were not the same as those

involved in the incident cited above, and they had had

some previous acquaintance with one another. The

male copulated repeatedly, and apparently successfully,

with the female within a few minutes after being released. Then the female apparently became satiated.

She stopped accepting the male. At which point, he

began to perform a variety of Tail-coiling movements

in rapid succession. They always began while his tail

was hanging downward. Sometimes the Coiling was

slight, hardly more than exaggerated Tip-coiling, and

affecting only part of the tail. At other times, the whole

of the tail was coiled, and even brought up between the

legs; but the male never actually sat down after Coiling in the characteristic manner of females. The coils

of his tail always were quite tight, usually touching one

another throughout. Rather surprisingly, both the extreme and slight forms of Coiling often were accompanied by, or combined with, an appreciable amount

of Tail-ruffling. Even more surprisingly, none of the

performances provoked a direct, unmistakable, response by the female (although she did perform Rubbing from time to time).

The behavior of both these males would seem to be

of the type which has been called "pseudo-female."

The probable or possible significance of such behavior

has been discussed by Morris (1955). Like the corresponding patterns of some other animals (birds and

fish) cited by Morris, the Upward Tail-coiling of the

male Rufous-naped Tamarins appeared to be produced by "arousal and subsequent thwarting of the

sex (i.e., copulatory) drive." Insofar as such behavior is

"unexpected," it might be considered "displacement."
NUMBER 2 8 51

FIGURE 18.—Extreme but "loose" Upward Tail-coiling of adult Rufous-naped Tamarins: a (top),

by male approaching a female; b (bottom), by a female, apparently soliciting or expecting

copulation.
52 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

But it may also have special signal function (s). Although the performances described above did not appear to be effective, it is conceivable that similar behavior by males in other circumstances might stimulate

the sexual tendencies of their partners (i.e., function

in some or all of the same ways as the equivalent behavior of females).

More or less exaggerated and stereotyped forms of

loose Tail-coiling also were seen to be performed only

twice. Once by the male cited above, and once by the

female of a well-established pair. This female and her

mate had been kept together for a long time. They were

seen to copulate once or twice a day for several days in

a row. Then the male seemed to lose interest. On the

following day, the female was seen to go to a branch

on which copulations had occurred previously, pull up

her tail in a complete loose spiral, put it between her

legs, and then sit down with the coils protruding in

front. This is shown in Figure 18b. It appeared to be

as attractive as more conventional performances. The

male ran to the female as soon as she sat down, and

placed one hand upon her back. But then again his

energy failed.

As the illustrations indicate, loose Upward Tailcoiling is remarkably conspicuous when viewed close

up. It is not, however, at all conspicuous when viewed

from a distance, when the concentric coils seem to

disappear, like the stripes of a zebra.

• Pilo-erection and "Smoothing" Patterns.—Adult

Rufous-naped Tamarins seem to have six or seven

more or less distinct patterns of raising or depressing

hair.

One is a General Ruffle, raising all or almost all the

hair of the head, body, limbs, and tail. As noted above,

this may be superimposed upon the stand-up posture

of a very aggressive male (illustrated in Figure 20).

It may also be combined with a variety of other patterns. It is sometimes performed, or assumed, by individuals engaged in violent and obviously aggressive

chases and fights. In these circumstances, it usually is

maintained throughout the whole of an encounter;

i.e., combined with all the vocalizations, locomotory

and fighting postures and movements which may be

performed by the aggressive individuals, irrespective

of whether or not stand-up postures are included

among them. I also have seen General Ruffles assumed

by a captive male and female performing Tongueprotrusion with Head-flicks, and uttering Soft Sharp

Notes and/or Infantile Squeaks, immediately after being introduced to one another and just before beginning to chase and fight; and by another captive male

and female during silent sniffing and Tongue-protrusion immediately after a violent dispute.

All these facts would suggest that General Ruffles are

produced when the tendency to attack is very strong.

Probably when other tendencies also are strong, but

somewhat less so than attack.

Possibly General Ruffles usually or always function

as threat. They must, at least, increase the apparent

size, and therefore "impressiveness," of the performing

individuals.

A pattern which may be called Crown-raising is

much less spectacular. In its typical form, it entails

raising the white hairs of the "blaze" on the forehead

and forepart of the crown to the maximum extent

possible, while raising the rufous hairs of the nape only

moderately (perhaps not at all in some cases) and

leaving the hairs of the body and limbs unruffled. When

an adult performs the pattern, the white hairs of the

"blaze" look very much like those of the young animal

illustrated in Figure 21. (The young itself may or may

not be displaying. See below, page 61.)

During at least some Crown-raising performances

by adults, the hairs of the white stripes across the

cheeks also are raised (brought forward), but this is

noticeable only when viewed very close up.

All the Crown-raising, in fact, is so inconspicuous

from a distance that I cannot be sure that I did not

overlook it quite frequently (see also page 60.) I did

see it performed by wild adults, as a reaction to potential predators, in combination with Loud Sharp Notes,

Swaying, and Tail-ruffling. I also saw it performed

by many captive adults, usually rather aggressive individuals engaged in disputes in less vigorous and/or

less prolonged hostile encounters than those in which

General Ruffles occurred.

This would indicate that adult Crown-raising is

purely hostile. Possibly it is produced by much the same

type of motivation as the General Ruffle, when all the

tendencies involved are weaker on the average. The

individuals which perform it in captivity often seem to

be slightly intimidating to their companions. Perhaps

the pattern itself functions as threat, a rather less

frightening or impressive threat than the General

Ruffle.

Crown-smoothing is the "opposite" of Crown-raising

in form. All the white hairs of the forehead and crown

are smoothed down flat, while the rufous nape hairs
NUMBER 2 8 53

FIGURE 19.—Copulation postures of Rufous-naped

Tamarins. The female has partly uncoiled her tail.
54 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

FIGURE 20.—General Ruffle by an adult male Rufous-naped Tamarin in a stand-up posture.
NUMBER 2 8 55

and the rest of the pelage of body and limbs are maintained in an ordinary unritualized position. This

Crown-smoothing also is difficult to distinguish at a

distance. But it obviously is common and performed in

a considerable variety of circumstances. It is most frequently combined with overt retreat and escape movements and intention movements. Occasionally, it may

be performed by individuals advancing toward others.

Sometimes such advancing individuals show clear signs

of aggressiveness. But they always appear to be simultaneously alarmed to some extent, even though the

alarm is not relatively strong enough to overcome the

tendency to approach. In almost all circumstances,

Crown-smoothing is closely associated or combined

with other signals in which escape is prominent; e.g.,

Trills and other patterns of the Sharp Note complex,

Infantile Squeaks, Tail-ruffling, crouch and headdown postures, and some Rubbing performances. See

Figures 1, 2, 15&, and 15c.

If the Crown-raising which emphasizes the white

areas of the head functions as threat, it seems likely

that the Crown-smoothing which reduces the apparent

size of the white areas functions as appeasement.

Another related pattern which might be considered

"opposed" to Crown-raising is the Rufous Ruffle. In

this pattern, all the rufous hairs of the nape are raised,

while the white hairs of the face and crown are either

smoothed down or maintained in an unritualized position, and the rest of the body and limb pelage (also)

remains "normal." As indicated on page 16, an individual may do this in an apparent attempt to induce

grooming by a companion. It seems to be rare in other

social situations. I noticed only one conspicuous example apart from Allogrooming. This was performed

by a captive male immediately after being introduced

into the cage of an unfamiliar female. She was mildly

aggressive, and the male obviously was both attracted

to and frightened of her. He retreated, apparently reluctantly, whenever she advanced toward him. He

uttered Long Rasps whenever she came particularly

close. He also performed Rufous Ruffles during his

retreats, both when silent and when vocalizing.

Certainly, the Rufous Ruffle cannot be primarily

aggressive. It may be largely due to some combination (s) of a tendency to escape and some friendly and/

or sexual motivation. It may function as another appeasement pattern and/or a releaser of friendly or sexual reactions.

The remaining patterns of this group involve the

hairs of the tail.

Tail-ruffling is one of the most common displays of

the species. In its typical form, it consists of raising all

the hairs of the distal part of the tail (most of the black

part) to a more or less extreme extent. This is illustrated in Figure 1. Typical Tail-ruffling is a very

frequent reaction to the appearance or approach of a

potential predator. In such circumstances, it may

occur by itself alone, or be superimposed upon otherwise unritualized retreat or escape movements, or be

combined with almost any one or several of the other

display patterns expressing some degree of alarm (as

well as other tendencies), including Twitters, Trills,

Sharp Notes, Swaying, and/or Head-flicks. It also may

be combined with either Crown-smoothing or Crownraising, or both in rapid succession. It seems to be

somewhat less characteristic of intraspecific reactions.

But I have seen it combined with, at least, Twitters,

Loud Sharp Notes, Head-flicks, and even sniffing with

Tongue-protrusion, during some encounters between

male and females in captivity.

Tail-ruffling performances certainly are associated

with Twitters much more frequently than with any

other ritualized signal.

All this would suggest that a tendency to escape

usually is predominant during Tail-ruffling, but the

escape must usually or always be accompanied by

some slight activation of friendly and/or sexual

motivation.

Tail-ruffling itself must be low intensity. It is performed more frequently than either Twittering or

Crown-smoothing, and in an even greater variety of

circumstances. All the tendencies involved in the production of Tail-ruffling must be very weak indeed.

It might, in fact, be supposed that Tail-ruffling was

nothing more than "low-intensity Twittering," produced by the same tendencies, in the same proportions, but at a lower level of strength; however, this

probably is not correct. Not only can Tail-ruffling occur

without Twittering, but Twittering can also occur

without Tail-ruffling. It seems likely, therefore, that

there are qualitative as well as quantitative differences

between the causal factors of the two displays. Presumably, there is a slight difference in the relative

strengths of hostile and non-hostile tendencies. Possibly

the Tail-ruffling contains or expresses relatively more

friendly and/or sexual motivation (viz., the captive

male which combined Tail-ruffling with Upward Tailcoiling, described above, page 50).

Rufous-naped Tamarins probably also have distinct

Tail-fluffing and/or Tail-smoothing displays. The tails
56

of at least some individuals certainly appear to be

"thicker," without being obviously Ruffled, at some

times more than at others. The difference, however, is

so slight, and so difficult to distinguish at a distance,

that I could never analyze it properly.

• Facial Expressions.—All tamarins and marmosets

are notoriously "poker faced" (for fairly obvious reasons, see Moynihan, 1967). But S. geoffroyi may have

a slightly greater range of facial expressions and related patterns than some other species.

Perhaps the simplest expression is a slight opening

of the mouth, without making special lip movements

or revealing or emphasizing the teeth in any conspicuous way. This occurs during some vocalizations.

It can also be done silently. When silent, it usually is

maintained for several seconds or even minutes. Presumably as an unritualized intention movement of

vocalizing and/or biting.

Actually, the appearance of the mouth, and the

movements of the lower jaw, are rather different during the utterance of different types of notes and calls.

The mouth is opened more or less widely during Long

Whistles, Long Rasps, Infantile Rasps, and at least

some Infantile Squeaks (see Figures 15b and 21), and

closed after every note of these types, even when they

are uttered in series. It also is opened widely during

Trills and some intermediates between Trills and Twitters. During these performances, the lower jaw vibrates

up and down in rhythm with the notes, but the mouth

is not closed between the successive notes of a single

series. Sometimes the tongue also goes in and out (but

not very far out) in rhythm with the notes. When the

mouth is open, the fleshy pink color of the tongue and

the lining of the mouth may be rather noticeable.

Typical Twitters and Short Whines, on the other hand,

usually or always are uttered with the mouth nearly

or completely closed throughout, without any visible

revelation of pink. Thus, it seems quite possible that

one tamarin could tell what its companions were saying, as long as they were in sight, even if they were

not audible. Such a situation is not very likely to occur

in nature. But the visual information must at least

supplement the acoustic, and may perhaps enhance its

effectiveness.

One captive male was seen to open and close his

mouth repeatedly, without uttering a sound audible

to my ears, much more rapidly and frequently than

usual. Unfortunately, he was not in good health at

the time, and his behavior was difficult to interpret.

Some other Platyrrhini give similar performances as

SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

regular displays, but the behavior of this male may

have been aberrant for his own species. Possibly he

had simply "lost his voice" as a result of illness. Or,

he may have been exhibiting an individual quirk comparable to the others cited above.

Andrew (op. cit.) mentions one facial expression of

S. geoffroyi (which he too calls Oedipomidas spixi);

i.e., a "marked grin." He says that it accompanies

"twitters" and a "rasping screech." (See page 70, for

the probable identity of these sounds according to the

terminology used here.) In another passage of the

same paper, Andrew described the "grin" accompanying "screeches" as "low." Elsewhere, he implies that

the expression accompanying "twitters" is similar. By

his definition, a "low grin" should consist of the drawing back of the corners of the mouth and nothing else.

My own experience would suggest that such drawing

back, although possibly evident in almost all vocalizations given with the mouth open, is almost always very

slight. It certainly is much less well developed in

S. geoffroyi than in some of the larger New World

primates.

There seems to have been only one exception among

the Rufous-naped Tamarins kept in captivity on Barro

Colorado Island. M. H. Robinson (personal communication) says that one individual "showed its fangs"

(drew back the corners of the mouth far enough to

reveal the canines) almost continually for the first few

days after it was brought into the laboratory. The general effect was so unusual that the individual was immediately named "Dracula." By the time that I saw

it a couple of weeks later, the peculiar pattern had

almost disappeared. Presumably it was another individual quirk, and a rather fugitive one.

The most complex of the facial expressions involve,

or are closely associated with, a very conspicuous display which may be called Tongue-protrusion.

It has already been mentioned that the tongue may

be flicked in and out, slightly, during some vocalizations. Apparently identical movements may be performed by both male and females during Allogrooming

(by the groomers), immediately before and/or after

feeding, and even when simply looking at areas or

sites where they are accustomed to feed. In many of

these latter cases, the animals appear to be "tasting,"

or anticipating the taste of, some aspect of the

environment.

But real Tongue-protrusion, as the term is used

here, is much more exaggerated. In its complete and

typical form, the tongue is extended just about as far
NUMBER 2 8 57

as it can go. Usually the tip is curled upward. This is

illustrated in Figure 15a. Sometimes the tongue is held

motionless for several seconds. At other times it may

be vibrated up and down very rapidly. This may be

the highest intensity version of the performance.

Extreme Tongue-protrusion may intergrade with

the simple flicking in and out associated with feeding

and some vocalizations. The tongue can go in and out

more or less rapidly and be protruded to varying

extents.

Both the extreme and intermediate forms of the

display-are almost always silent. But they usually are

accompanied by other ritualized components. The nose

is usually "wrinkled up" and the eyes are half closed.

And an individual performing Tongue-protrusion almost always gives many Head-flicks. When the tongue

goes in and out more or less regularly, there may be

exactly one Flick per protrusion. More frequently, the

synchronization is less perfect. There often are several

Head-flicks while the tongue is maintained in the

extended position. Or the Flicks may occur both during

and between extensions.

As a whole, the real Tongue-protrusion display can

be said to be characteristically masculine. During the

course of the present study, it was seen to be performed by males very much more frequently than by

females.

It was a very common reaction of captive males

when confronted by unfamiliar individuals of their

own species, strangers of either sex and almost any

age. In these circumstances, it often was combined

with sniffing, apparently as a complex form of "investigation" or even "greeting." A male would approach

a stranger and sniff at it, either face to face or nose

to tail, and perform Tongue-protrusion (with accompanying Nose-wrinkling, Eye-closing, and Head-flicks)

throughout the period of sniffing. This often was preceded by Rubbing with Crown-smoothing by the male,

and followed by more of the same and/or overt attacks

and fighting.

Occasionally, a male would perform Tongue-protrusion, with Nose-wrinkling, Eye-closing, and Headflicks, without bothering to approach the stranger.

More than one male was seen to do so when he was

at least 10-15 feet distant from the releasing stimulus.

Perhaps such performances were accompanied by some

sort of "long distance" sniffing.

Typical sniffing with Tongue-protrusion and associated patterns sometimes continued for several minutes, or was frequently repeated, when the stranger

was an adult female. But it usually disappeared

rather rapidly when the stranger was a male and/or

a juvenile.

Similar patterns were performed by males during

copulations, while their faces were pressed down into

the fur of the females' backs.

It is, in fact, this combination of Tongue-protrusion

with Nose-wrinkling, Eye-closing, and Head-flicks

which was subsumed under the heading of "Sexual

Sniffing" in several passages cited above. The whole

combination must be very closely related to the patterns

of many other eutherian mammals which have been

called "Flehmen." See Andrew (op. cit.).

Neither Aotus nor Callicebus has anything strictly

homologous with Tongue-protrusion itself. But, according to Epple (1967), similar patterns are exhibited

by Leontideus rosalia, Callimico goeldii, and species of

Callithrix. This is interesting from a comparative point

of view (see page 74). The Tongue-protrusion of tamarins and marmosets probably also is closely related to

the series of rhythmic tongue movements which are the

usual precopulatory displays of both male and female

Alouatta "palliata" (Carpenter, 1934).

There are several types of variations in the performances of Rufous-naped Tamarins in addition to those

already mentioned.

Real, extreme, Tongue-protrusion is performed by

females occasionally. Thus, for instance, I saw one female perform silent Tongue-protrusion just like the

male with whom she was engaged in mutual nose to

tail sniffing at the time. Another female was seen to

perform more or less similar movements during an

apparently unsuccessful copulation attempt, when she

was resisting the male (M. Bernstein, personal

communication).

(Epple [1967] cites several other possible examples.

But I am not sure that she always distinguished between the ritualized Tongue-protrusion display and the

less extreme, possibly or probably unritualized,

"tasting.")

Several times, wild tamarins were seen to perform

Tongue-protrusion in apparent response to the approach of a human being. I think that these displays

were accompanied by much less well developed Nosewrinkling and Eye-closing than the corresponding patterns of captive animals in partly or wholly sexual

circumstances. Certainly, at least some of the Tongueprotrusion by the wild individuals was not combined

with Head-flicking. One captive adult male also did

Tongue-protrusion directly to me when I entered his
58

cage. This was associated with Head-flicks, but (again)

with little or no Nose-wrinkling and Eye-closing.

The wild individuals uttered Trills and Twitters

before and after their Tongue-protrusion. The captive

male uttered Trills, Short Whines, and Infantile

Squeaks before and after his similar performance. And

the female resisting copulation actually uttered a peculiar muffled, rhythmic noise, possibly a modified version of Broken Rasps, during her Tongue-protrusion.

(It may be added, in this connection, that a captive

juvenile once performed Tongue-protrusion in close

association with Infantile Squeaks, Infantile Rasps,

Long Rasps, and Broken Rasps, when caught and held

in the hand for some minutes. This was done without Eye-closing, Nose-wrinkling, or Head-flicks.)

Obviously the extreme Tongue-protrusion display

with associated patterns is very highly ambivalent, perhaps one of the most highly ambivalent behaviors of

the species. And all or most of the tendencies involved

must be relatively quite strong even in the least highintensity versions.

The activation of hostile motivation is revealed by

the associations with partly or completely hostile calls,

Rubbing and Crown-smoothing, and even overt fighting, as well as the occasional performances toward

potential predators. Copulatory motivation must be

strong in the patterns performed by males during

copulations. This and/or some other sexual tendencies

probably are involved in the "greetings" between

males and females. Sexual and/or friendly tendencies

may be present in the performances directed by males

toward other males or juveniles.

The various patterns probably also are heterogeneous in another sense. As noted above (page 41),

the accompanying Head-flicks may be purely hostile.

The Nose-wrinkling, with the Eye-closing which seems

to be linked to it (see also below), may be almost

purely sexual, or at least more strongly sexual than the

tongue movements themselves.

Three times, I saw captive individuals put their

heads together and partly "interlock" their jaws. This

always was silent. It always occurred in very ambiguous, but at least partly hostile social circumstances.

It appeared to be a very inhibited and/or ritualized

form of mutual biting; but it never produced any visible injuries, and it may have been accompanied by

some sort of mutual "tongue play."

It is mentioned here only because some comments

by J. K. Hampton (personal communication) would

SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

suggest that similar performances may be more common in S. oedipus.

Rufous-naped Tamarins have another pattern which

probably functions as a special signal. The Eye-closing

associated with Tongue-protrusion may entail some

lowering of the "eyebrows," but this is usually or always

slight. Occasionally, individuals of the species may

lower the eyebrows much more vigorously, to produce an extreme Frown, quite similar to the corresponding human pattern in appearance. This may

be purely hostile. I have seen it performed, with Crownraising, by a captive adult male who was making intention movements of attacking me. His Frowning also

was accompanied by a partial closure of the eyes, a

sort of "squinting," but there was little or no trace

of Nose-wrinkling and certainly no Tongue-protrusion.

(Thus, it would seem to be advisable to distinguish

sharply between this squinting and the "real" Eyeclosing as the latter term is used in this paper.)

Exaggerated Frowns, probably with squinting, also may

occur with many or all General Ruffles. Possibly they

are another form of threat.

Epple (1967) cites Frowns by both S. geoffroyi and

S. oedipus. She says that they are accompanied by

protrusion of the lips. I did not notice this myself. The

protrusion of the lips cannot be as conspicuous as in

Ateles, Cebus, or Callicebus moloch.

Rufous-naped Tamarins do not seem to flatten and

erect the ears during hostile reactions in the same

ways as the species of Callithrix described by Epple

(1967). Unlike most species of Callithrix, they do not

have elongated "ear tufts" of black or white hair. But

they may bring their ears forward during some Sexual

Sniffing performances. I do not think that this can

be considered an independent display.

• Significance of Colors.—Most of the more aggressive displays of S. geoffroyi, usually functioning as

threat, are performed facing more or less directly

toward opponents. This must reveal and emphasize

the white on and around the face. And the amount of

visible white is increased by special movements and

postures and/or pilo-erection in such aggressive patterns as the stand-up (with General Ruffle) and

Crown-raising. This would suggest that white may be

intimidating per se. If nothing else, individuals should

learn that a parade of white often precedes attack.

The rufous of the nape, genital region, and base of

the tail, by contrast, is emphasized in a variety of

friendly and/or sexual displays; and also in appeasement. This would suggest that rufous itself may be
NUMBER 2 8 59

"positively non-hostile." At least, an individual performing a pattern emphasizing rufous probably is attempting to indicate that it would prefer to avoid

overt hostilities if possible.

The brindled black and yellow of the back and outer

parts of the limbs may be effectively neutral.

Certain inferences can be drawn from these

assumptions.

The Lie-back posture, with its extensive revelation

of white, should be intimidating.

The ultimate cause of the disappearance of the

Arch display during the evolution of S. geoffroyi probably was that it emphasized the neutrally colored back

instead, or even at the expense, of the white on the

underparts. Arch displays are aggressive, and function

as threat, in all the species in which they are known to

occur at the present time. The Arch of the ancestor

of S. geoffroyi presumably was similar. One can easily

imagine that such a behavior pattern would become

much less effective as soon as white coloration became

intimidating and was concentrated on parts of the

body which the pattern did not emphasize. (And selection probably did not favor the development of white

on the back, because it would render individuals too

nearly continually conspicuous, and therefore vulnerable, to predators, especially flying birds of prey.)

The closely related S. oedipus is quite similar to

geoffroyi in both behavior (see page 66) and many

morphological features, but it has relatively more white

(a very large "top-knot" or mane) and no visible

rufous on its head. Thus, one would expect that individuals of one form would interact with individuals of

the other form rather less easily and efficiently, on the

average, than either would with other individuals of

its own form (see also page 67). If so, then there probably would be selection pressure against hybridization

between the two forms, when and if it should ever

occur in the wild.

GENERAL COMMENT ADULT SIGNAL REPERTORY

Adult Rufous-naped Tamarins certainly have more

types of visual displays, and use them more frequently,

than Callicebus moloch individuals which are approximately equally diurnal and live in rather similarlooking vegetation. To some extent, this seems to be

a real replacement or substitution. Rufous-naped

Tamarins perform visual displays in some circumstances in which C. moloch individuals would be expected to perform acoustic displays. Conversely, C.

moloch individuals perform acoustic displays in some

circumstances in which Rufous-naped Tamarins

would be expected to perform visual displays. This

seems to be another illustration of a general rule among

primates, which has already been summarized as

follows:

. . . vocalization is the principal means of communication in the order as a whole. It probably is actually or potentially the most efficient method of communication between

individuals of all species. It probably has been selected against,

in some species, only because it is equally or more efficient

in communicating information to the 'wrong' individuals

(of the same or other species) as to the 'right' individuals

(Moynihan, 1967).

The wrong individuals are easily identifiable in the

case of the Rufous-naped Tamarin. As has been mentioned repeatedly, individuals of this species seem to

be particularly vulnerable to predation. Certainly

much more so than C. moloch individuals. And vocalizations are much more likely to be noticed by a predator, especially at a distance in forest and scrub, than

are visual displays, especially such patterns as piloerection and positioning of the tail.

In spite of the difference in relative importance of

visual and acoustic displays, it seems likely that the

total number of all specialized signals, mediated by all

senses, is roughly comparable in S. geoffroyi and C.

moloch. Both species have rather extensive repertories

of qualitatively distinct ritualized patterns ("major"

displays in the sense of Moynihan, in press) plus many

other ritualized patterns which can best be described

as only quantitatively distinct. In the case of C. moloch,

most of the latter are intermediate between major displays (usually vocalizations). In adult S. geoffroyi,

most of them are combinations of major displays; for

example, one or more vocalizations combined with one

or more pilo-erection or smoothing patterns, special

positions of the tail, and/or movements of the body or

head. Adult Rufous-naped Tamarins probably have

approximately 32 major displays (give or take a half

dozen). By combining these in various ways, and modifying the forms of particular components of combinations according to circumstances (especially strength of

motivation), they can, and obviously do, produce huge

numbers of recognizably different signals. I could not

always distinguish between the signal valences of some

complex combinations which were only slightly different in form. But such patterns certainly could encode

slightly different '"messages" (in the sense of the term

used by W. J. Smith, 1965). And for logical (meth-
60 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

odological) reasons, the student of behavior must assume that they actually do so.

The display repertory of adult C. moloch seems to

contain a rather large amount of redundancy. Different

displays seem to transmit essentially similar messages

to the same receivers. The approximately equally large

repertory of adult S. geoffroyi also must include some

redundancy, but probably not nearly as much.

Many of the display performances of adult geoffroyi

are less obviously unified or "cohesive" than are those

of moloch. I often found it difficult to grasp what a

single Rufous-naped Tamarin was both saying and

doing, with different parts of its body, at the same

time. Many combinations of displays of the species do

not seem to have any general gestalt as a whole. This

would suggest that different components of the combinations may be designed for, adapted to be perceived

by, different recipients, which also seems reasonable in

many particular instances. Consider, for example, an

individual which utters Loud Sharp Notes and performs Swaying with Tail-ruffling and Crown-smoothing as a reaction to the appearance of a potential predator. The notes and Swaying may be adapted to tell

the predator that it has been discovered. The notes

also may inform other potential prey, individuals of

other species (which might be induced to mob the

predator) as well as other Rufous-naped Tamarins,

that there is danger in the neighborhood. And the

Crown-smoothing and Tail-ruffling may reinforce the

warning for other tamarins of the same social group

as the performer, individuals who are likely to be fairly

close by, at least in sight, more often than not

Thus, one of the reasons why so many Rufous-naped

Tamarins display performances are so complex (compound) may be that they have to work in many

different ways. A single performance probably must

be designed to transmit one or more messages along

different channels, to different distances, and often in

different directions, all simultaneously.

Behavior of Infants and Young Juveniles

Like the female of all or most other species of tamarins

and marmosets, female S. geoffroyi usually conceive

and presumably usually bear two young at a time

(Wislocki, 1939), but both members of a set of twins

are seldom raised successfully in the wild in the

Panamanian region under present conditions. In my

experience, it is very rare to see two infants or juveniles

of the same size, apparently of the same age, in a

group of wild geoffroyi. And all or most of the few

examples seen were in relatively large groups, and may

well have been the offspring of different mothers.

Thus, it would appear that one of a set of twins usually

dies shortly after birth under natural conditions.

(Wislocki also cites several cases of one of a pair of

fetuses being resorbed before birth.) The "extra" individual of every set of twins usually seems to be

nothing more than "reinsurance," a possible replacement for the other member in case of disaster, or an

added but highly speculative "bonus," only to be

cashed (reared) in years when the environment is particularly favorable.

(The limiting factor may be food. Several sets of

twins born in captivity on Barro Colorado Island were

raised successfully by their own parents. Both they

and their mothers were provided with super-abundant

food and a greater choice of things to eat than would

be likely to be encountered in the wild.)

Some aspects of the behavior of young Rufousnaped Tamarins and their parents have already been

described by Epple (1967) and others. The following

account will not attempt to duplicate these descriptions. It will include a little miscellaneous background

information plus analyses of certain infantile signal

patterns.

My own observations of young Rufous-naped

Tamarins were fairly detailed in some respects and

extremely summary or incomplete in others. I saw very

little of the behavior of newly born or very young

infants in the wild, but I did observe large numbers of

older infants and juveniles, one-third to three-quarters

grown, in such areas as Ancon Hill and the Forest

Reserve. Some thirteen young were born alive in captivity on Barro Colorado Island during the course of

this study. Of these, I watched three (one single individual and one set of twins) intensively at irregular

intervals. Many other young which were not born

on Barro Colorado, but some of which were obtained

at very early ages, were hand reared in the laboratory

and studied more nearly continuously.

APPEARANCE

The coloration of newly born young is quite distinctive. The areas of the body which are brindled

in adults appear to be nearly or completely pure black.

The rufous of the nape is already well developed,

and always relatively much more conspicuous than it

usually is in adults. The white crown patch, on the
NUMBER 2 8 61

other hand, is very insignificant. It consists of only

two thin streaks (meeting in front of the rufous to

form a V). It is not very white either, more of a dirty

light gray. Most of the underparts with white or whitish fur in adults are nearly naked in newly born young,

and the bare skin of these areas is an inconspicuous,

medium dark, pinkish gray. Only on the sides of the

neck are there small patches of light gray hair.

This coloration is obviously adaptive. Hostile white

is reduced (and reaches its minimum when an infant

is sleeping or resting quietly, when it usually keeps its

head pressed down into the fur of the adult on which

it is riding). Non-hostile rufous is always at a relative

maximum. Both features should help to avert attack

by adults, either by parents (who might be irritated

or alarmed by their new dependent) or by other

members of the same social group.

By the time that the young are approximately one

month old, they are much more similar to adults in

in appearance, although still easily distinguishable (see

Figure 21). Their peculiar features are concentrated

FIGURE 21.—A young juvenile Rufous-naped Tamarin

uttering Infantile Squeaks.

on the head. The white crown is fully developed. It is,

in fact, even more conspicuous than in adults. It is

relatively larger and often broader, and the hairs of

the crown are usually or always erect or semi-erect.

(This probably means that older infants and young

juveniles do not have distinct Crown-raising and

Crown-smoothing displays, but see page 52.) The

faces of young animals at this stage also are covered

with rather dense coats of light gray hairs. As a result,

they look a great deal "fluffier" than adults. In this

respect, of course, they resemble the young of many

other mammals, species of other orders as well as other

primates.

These features also must be adaptive. The increased

white may help to avert attack, because it is intimidating. Intimidating characters might be expected to be

also irritating in some circumstances. But this is not

usually evident among the threat patterns of Rufousnaped Tamarins. In any case, juveniles may be able

to take more risks than newly born infants, and/or

whatever irritating qualities may be inherent in white

coloration may be contradicted or nullified by

fluffiness.

RELATIONS WITH PARENTS

It is generally supposed (see, for instance, Hill, 1957,

and Sanderson, 1957) that infant and young juvenile

marmosets and tamarins are carried by the male parent most of the time when they are not being suckled

by the mother—at least after the first few days after

birth. This also was true of several infant Night Monkeys and one infant Callicebus moloch born and raised

by their parents in captivity on Barro Colorado Island.

But the division of labor was slightly different in the

case of infant Rufous-naped Tamarins born and raised

in similar circumstances. These infants were carried

by their mothers and fathers with approximately equal

frequency, and they spent considerable time on their

mothers quite apart from feeding. Epple (1967) says

that infants also may be carried by other (presumably

adult) members of the same social group. Possibly

some of this behavior is an artifact of captivity. Possibly

infant Rufous-naped Tamarins are carried longer and/

or more often by their fathers in the wild, where adults

range over wider areas and are in less constant close

proximity to one another.

(As might perhaps have been expected, however, a

single female can rear twins successfully in the conditions of captivity even in the absence of an adult

male.)

An infant being carried by a parent can move about

quite actively on occasion, crawling over different parts

of the parent's body (see below), but these bursts of

activity tend to be brief. Most of the time, the infant remains nearly immobile, apparently asleep or resting.

During the periods of calm, the infant usually rides

high on the parent's back, often in a diagonal transverse position (i.e., arranged in such a way that its

own head is just behind and to one side of the

356-597 O - 70 - 5
62

adult's head). It clutches the adult's fur with both

hands and feet, and keeps its tail firmly pressed against,

or partly coiled around, the adult's body.

My own observations of captive animals suggest that

infants are carried nearly continuously for approximately one month after birth. But they certainly are

capable of moving around independently of adults almost from the very beginning, and they may do so,

very briefly and occasionally, even during the first

week of life. These excursions rapidly become longer

and more frequent during the second month. By the

end of this period, an infant usually is moving independently all the time. (This schedule is smiliar to,

although not exactly identical with, the one reported

byEpple, 1967.)

The process is reversed in only one set of circumstances. As noted above, juveniles may leap onto a

parent's (at least an adult's) back when alarmed.

Even when not disturbed, young juveniles usually

stay within a few inches or feet of their parents during

the first few weeks after beginning to move independently, but older juveniles associate much less

closely. In the wild, parent-young bonds may have become very inconspicuous indeed by the time the young

are half grown.

Adults carrying infants usually pay surprisingly little

obvious attention to their burdens. They tend to move

more cautiously (slowly) when carrying than when not,

but they seldom manipulate or even look directly at

the infants.

An infant usually moves to the breast to suckle by

its own unaided efforts. It does so by moving up and

over the mother's shoulder, and then crawling down to

a nipple. Having reached its goal, it may turn around

and suckle head upward. Then it returns to the

mother's back by the same route. The mother usually

is sitting down during suckling, in a perfectly ordinary

posture with Tail-looping. The infant may be partly

supported by the mother's thighs or knees, but only

rarely does she lift a hand to provide additional support

or guidance.

Presumably infants have to learn which parent gives

milk. I have seen very young infants try to suck on their

fathers' nipples.

Infants usually have to transfer from one parent to

the other on their own. A parent who seems to have

become tired of carrying just sits down. It may do so

where it happens to be at the time, or make a special

effort to join its mate. If it does not go to its mate,

the latter usually comes to it, sooner or later. Then

SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

the two adults sit side by side. Often facing in opposite

directions. At which point, the infant(s) may or may

not crawl from one adult back to the other.

I could not detect any other "commanding" signal,

such as a special call, which initiated or accelerated

transfers.

Obviously, different infants can react differently to

the same external stimulus. When twins are involved,

as in some of the captive animals, one infant may transfer while the other does not.

I never saw a parent lend a helping hand during

a transfer which was proceeding more or less normally.

If an infant should fall, however, a parent usually

will grab it. Once grabbed, the infant clambers back to

the parent's back under its own power.

INFANTILE VOCALIZATIONS

The most common displays of young Rufous-naped

Tamarins are the Squeaks and Infantile Rasps which

have already been mentioned several times above.

Infantile Squeaks are illustrated in Figures 22, 23,

24, and 25. It will be seen that they are quite diverse

in form. All the variants are at least fairly brief, but

some are much shorter than others. On the whole,

they are perhaps most reminiscent of Short Whines.

It is always possible, nevertheless, to distinguish between the two patterns. Infantile Squeaks usually or

always show (on spectrograms) fewer harmonics than

Short Whines. They also are descending in pitch. In

most cases, the descent is much slighter and more

gradual than in Sharp Notes. And even the most

abrupt Infantile Squeaks do not include the initial

rising or horizontal phase which is typical of most

Sharp Notes. When Infantile Squeaks are uttered in

series (see below), the temporal patterning of notes

is never the same as in either Trills or Twitters. All

or most Infantile Squeaks are approximately as loud

as most Twitters; i.e., softer than Loud Sharp Notes

or the majority of Trills. They also have, to human

ears, a very characteristic nasal, "complaining" quality. (They could be described as even more whining

than the Short Whines.)

Infantile Rasps are illustrated in Figures 24 and

25. They do not look very different from Long Rasps

on spectrograms, but they seem to be more even,

"steadier," in pitch. Many of them also are much

shorter than any Long Rasps (without being obviously "fragments" like the "syllables" of Broken

Rasps). They are quite loud and harsh, but they also
NUMBER 2 8 63

have much the same nasal and complaining quality

as the Infantile Squeaks.

Infantile Squeaks sometimes are uttered singly, or

in short homogeneous series which do not include

any other types of notes. This may also be true of Infantile Rasps. But it is much, much more common for

the two patterns to occur together, in rapid succession, in the same series. The two types of notes may

even intergrade during some series. See Figures 22

and 23. Both usually are uttered with the mouth wide

open. This is shown in Figure 21.

Both patterns, when performed by young animals,

seem to be "distress" notes, expressions of "dissatisfaction," and rather generalized as such. They are uttered

by infants and juveniles who are uncomfortable or

unhappy in almost any way—e.g., too hot, too cold,

wet, falling down, in pain, thirsty, hungry, or isolated,

or lost—but perhaps only when the animals cannot

relieve the situation, remove or get away from the

source of the discomfort, by their own unaided efforts.

(Like young Night Monkeys, young Rufous-naped

Tamarins who are just beginning to become dissatisfied

usually start to move, and these initial movements

often are quite silent. Usually, it is only when the first

movements do not procure satisfaction that the animals

begin to vocalize.)

The principal or only casual difference(s) between

Infantile Squeaks and Rasps would seem to be degree

of discomfort and/or strength of frustration. The two

patterns may occur in the same types of situations, but

Squeaks obviously are lower intensity than Rasps. They

are uttered more frequently than Rasps. And a young

animal who is uttering many Rasps usually is unmistakably more unhappy and/or thwarted than an animal which is uttering only Squeaks. This may be

illustrated by the example of an infant which is hungry

but cannot find, or reach, a source of food. After some

preliminary fruitless movements, it utters one or two

brief Squeaks. As it gradually becomes hungrier, it

utters series of notes, including at least one long Squeak

as well as shorter variants, plus one Rasp. When it

becomes hungrier still, it utters longer series including

two or three Rasps. The Rasps themselves also tend to

become longer. During this progression, the infant may

make increasingly vigorous "searching" movements.

And as the series become longer, they also tend to

become more frequent, following one another at ever

shorter intervals.

Young animals raised by their parents, in captivity as

well as in the wild, utter distress calls much less frequently than infants and juveniles raised by human beings in the laboratory. Presumably the young associated with their parents are much less frequently

dissatisfied.

It seems probable, however, that other factors may

also be involved in producing the peculiar behavior of

hand-raised young. Of course, all these young always

suffer from lack of normal companionship. But they

seem to make partial adjustments to this lack quite

easily and rapidly. They usually stop making obvious

escape and continuous searching movements within

a few days after being brought into the laboratory, as

long as they are well provided with such thing as food,

milk, water, suitable ambient temperatures, woolly

towels to grasp, and sleeping boxes. And yet they usually or often utter Squeaks and Infantile Rasps almost

incessantly. Certainly, they tend to vocalize much more

frequently than the young of most other genera of

New World primates in similar circumstances. It is

hard to escape the impression that a good deal of this

vocalization is simply the result of boredom (which

might, after all, be considered another form of distress).

This explanation does not contradict the suggestion

made on page 12. Hand-raised young Rufous-naped

Tamarins utter Squeaks and infantile Rasps relatively

and comparatively frequently at all stages of juvenile

development. Granted that this is partly due to the

fact that human beings are not completely satisfactory

as substitutes for real parents, and that hand-raised

young are often bored, it is still quite possible that the

prolongation of frequent infantile vocalization into the

later stages of the development of such animals is also

partly a consequence of their peculiar relationship with

their human keepers. Human beings may not be very

good parent substitutes, but they remain in loco parentis

much longer than real parents.

It should also be stressed that prolongation of infantile behavior is just as characteristic of all other

New World monkeys raised by humans as of Rufousnaped Tamarins. But this does not affect the fact that

hand-reared Rufous-naped Tamarins utter infantile

vocalizations more frequently at all stages of development than do comparable individuals of most other

species.

The primary function of the distress calls of young

Rufous-naped Tamarins probably is to attract the attention of parents (and possibly other adult members

of a band) and induce them to satisfy the needs of the

young.
64 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

16,000-

\

1 N

\,

0.7

Time (sec.)

FIGURE 22.—Vocalizations of a young Rufous-naped Tamarin. The first note is intermediate

between an Infantile Rasp and an Infantile Squeak. The other three notes are more or less

typical Squeaks.

16,000 -i

*

""¥

0.5

Time (sec.)

1.0

FIGURE 23.—Vocalizations of a young Rufous-naped Tamarin. More Infantile Squeaks and

intermediates between Squeaks and Infantile Rasps.

The precise effects of particular infantile vocalizations are not always easy to detect in the wild under

natural conditions. But certainly parents will catch falling young which are uttering Squeaks and/or Infantile

Rasps. An adult which has left its partly independent

young behind, while moving through trees or scrub,

may stop or even turn back if the young begins to utter

distress calls. This permits the young to rejoin the adult.

And a mother may allow the young to suckle after rejoining in such circumstances.

It probably is significant that there is considerable

individual variation in the arrangement of different

distress notes. All the accompanying illustrations are

derived from recordings of a single young individual

(less than half grown at the time). They indicate that

this individual usually uttered Infantile Rasps before

Squeaks when both types of notes were uttered in a

single series. Other young usually uttered Squeaks before Rasps.

This sort of variation may facilitate individual

recognition.

The situation may be summarized by saying that
NUMBER 2 8

16,000-^

65

*N

,

\

0.5

Time (sec.)

FIGURE 24.—Vocalizations of a young Rufous-naped Tamarin. A brief Infantile Rasp followed

by a prolonged Infantile Squeak.

1.0

16,000**

\

\

0.5

Tim« (sec.)

FIGURE 25.—Vocalizations of a young Rufous-naped Tamarin. A prolonged Infantile Rasp

followed by one (or one and a half) Infantile Squeak(s).

1.0

association between Infantile Squeaks and Infantile

Rasps certainly is stereotyped (ritualized) per se, but

the form of the association is not.

Squeaks and Infantile Rasps can be supplemented

by other vocalizations. It has already been mentioned

(page 11) that young individuals can perform many

typically adult patterns. I have heard captive young

who were one to two months old (still very small)

utter Long Whistles, Twitters, Trills, Loud Sharp

Notes, Soft Sharp Notes (and possibly Sneezing Sharp

Notes), Long Rasps, and probably Broken Rasps, on

a few occasions. Sometimes these patterns were uttered by themselves alone. At other times, they were

incorporated into series of Infantile Squeaks and

Rasps. They all occurred in circumstances which suggested that their motivation was similar to, or identical with, that of the same patterns when performed

by full adults.

There also is some intergradation between typically

adult and typically infantile vocalizations. Infantile

Rasps seem to be particularly likely to intergrade

with Long Whistles and Long Rasps. Squeaks may be
66 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

most likely to intergrade with Twitters (Short Whines)

and Soft Sharp Notes.

(It may have been noticed that I have suggested

that both Long Whistles, and in some circumstances,

distress notes may function as "lost calls." This does

seem to be true. When both types of patterns are

uttered by young, the distress notes seem to be of lower

intensity than Long Whistles. A separated infant or

juvenile usually begins vocalization by uttering distress calls, and then switches to Long Whistles if its

isolation continues.)

The fact that S. geoffroyi has a fairly distinct repertory of infantile vocalization is interesting from a comparative point of view. Young Aotus also have distress

notes which are characteristically infantile. These

probably are related to the infantile vocalizations of

Rufous-naped Tamarins, but they are rather different in some aspects of form. Most conspicuously, they

do not include notes of harsh or rasping quality. As

a whole, the infantile repertory of Aotus seems to be

more similar, in morphology, to the complex of highpitched vocalizations of Callicebus moloch, but the

moloch patterns seem to be almost equally characteristic of both adults and young. Of all the species of

other genera that I have observed at some length, only

Pithecia monacha (very different from tamarins in

some other ways) seems to have both clear and rasping

special infantile distress notes.

OTHER PATTERNS

It is not easy to determine exactly when young Rufousnaped Tamarins first became capable of producing

other display patterns, simply because they seldom

have occasion to do so under normal conditions. Some

patterns certainly appear, or are performed frequently,

earlier than others. I have seen Head-flicking, Tailruffling, Tail-forward, Tip-coiling, and Sit-rubbing

performed by very young individuals in captivity.

Many other signal patterns gradually "drift in" during

the later stages of childhood and adolescence. Even

distinct Crown-raising and Crown-smoothing may appear before full maturity is attained. The only major

hostile or friendly display which I have not seen performed by a subadult individual is the General Ruffle,

and juveniles probably are too weak and/or timid

to engage in the very high-intensity disputes to which

General Ruffles seem to be confined.

Most of these nonvocal patterns are essentially

identical, in form and other respects, with those of

full adults as soon as they appear. The only obvious

exception is provided by the Head-flicks, which may

be combined with a much greater range of calls and

notes (including distress notes, Twitters, Long Rasps,

and Broken Rasps) when performed by (hand-raised)

young than when performed by adults.

Young monkeys of many species are more or less

"playful" (play may be difficult to define theoretically,

but it is usually easy to recognize—see also comments

in Loizos, 1967). The most typical forms of play in

young Rufous-naped Tamarins are chases and

wrestling bouts, with adults as well as other young,

which do not culminate in the vigorous biting and

striking of "real" fights. S. geoffroyi infants and

juveniles perform such patterns approximately as

frequently as young Night Monkeys, less frequently

than young Callicebus moloch.

SIGNALS OF OTHER SPECIES OF SAGU1NUS

A few other forms of the genus have been observed

more or less briefly and casually.

Saguinus oedipus, the closest relative of geoffroyi,

is the best known. Some of its behavior patterns have

been described by Epple (1967 and 1968), Epple and

Lorenz (op. cit.), and Andrew (op. cit.). All the published accounts imply (or state) that many of the

displays of oedipus (at least ritualized movements, postures, and vocalizations) are nearly identical with those

of geoffroyi. They suggest that the behavior of the

two forms may be (even) more similar than their

color patterns. This also is my impression. I kept a

single adult male oedipus in captivity on Barro Colorado Island for almost a year in late 1958 and 1959.

During most of this period, he was kept in an outside pen with three to five geoffroyi individuals (all

adult except one). In these circumstances, he was seen

to perform both nose to nose and nose to tail sniffing

(with the Rufous-naped Tamarins), stand-up postures

(to me), Swaying, Head-flicking, and Tongue-protrusion. He also was heard to utter Twitter-like notes

(and possibly a few Squeaks and/or Soft Sharp Notes),

Trills, Loud Sharp Notes, Long Rasps, and Broken

Rasps. All these patterns were very reminiscent of the

corresponding performances of geoffroyi in form, and

occurred in roughly comparable social situations, although not always with the same frequency (but see

also below). I might add that Epple (1968) describes

another pattern of oedipus which may be strictly homologous with the Long Whistle of geoffroyi; and
NUMBER 2 8 67

Epple and Lorenz (op. cit.) state that oedipus also

performs Rubbing (apparently Pull-rubbing).

It probably is very significant, therefore, that the

male oedipus kept in captivity on Barro Colorado was

the "odd man out" in the group of Rufous-naped

Tamarins with which he was confined. He slept in the

same box with the other animals at night (although

there were alternative sleeping quarters available), and

did not fight with the others any more than they

fought among themselves. But he tended to "keep his

distance" during the day, often remaining oh the edge

or outskirts of the group. He appeared to be followed

and joined by the Rufous-naped Tamarins, and to follow and join them, rather less frequently on the average than they followed and joined one another. (This

partial segregation was particularly remarkable because

some other kinds of specific discrimination seem to

break down in captivity. See page 24).

A third form of the genus is leucopus. This has always been recognized as a good species, but it shares a

number of morphological characters (not including

type of color pattern) with geoffroyi and oedipus, and

may be not very distantly related. (Hershkovitz, 1966,

places all these forms among the "bare-faced" tamarins.) I observed a single leucopus, a male on the

threshold of maturity, in the New York Zoo for several

hours on two successive days in November of 1958.

This animal had been born and raised in captivity,

but was being kept in a small cage by himself (after

an illness) at the time. He was seen to perform many

elaborate Tongue-protrusion displays, apparently as

reactions to my approaches. The Tongue-protrusion

movements themselves were quite like those of

geoffroyi and oedipus in form. To my surprise, however, they usually were accompanied by a peculiar

sound, a sort of "Muffled Chattering" of variable loudness. This was quite different from anything I ever

heard uttered by Rufous-naped Tamarins (but it may,

conceivably, have been related to the sound which M.

Bernstein heard uttered by a female geoffroyi performing Tongue-protrusion during an unsuccessful copulation attempt, see page 57). The leucopus male, also

uttered Short Whines (possibly organized into brief

Twitter series), Soft Sharp Notes, Loud Sharp Notes,

Long Rasps, Broken Rasps (quite distinct from the

Muffled Chatter), Infantile Squeaks, and Infantile

Rasps. All were quite similiar to the corresponding

patterns of geoffroyi in sound, except the Long Rasps

which were much more nasal, i.e., more like Infantile

Rasps in tone.

Another group of species of the genus Saguinus is

even less like geoffroyi in appearance than is leucopus.

It probably includes all the forms which Hershkovitz

(1966) calls "hairy-faced 'white-lipped' tamarins" plus

some others; and it seems to be essentially equivalent

to (although certainly not absolutely identical with)

Hill's (op. cit.) "genus" Tamarinus. Most of the

animals of this group are largely black and rufous, and

have black faces with white muzzles, and sometimes

more or less well-developed white moustaches.

As might be inferred from the preceding passage, the

classification of the forms of this group is still rather

chaotic. To my knowledge, the last published revision

is by Hershkovitz (1966). This is only partial, and unfortunately Hershkovitz does not cite the evidence for

most of his conclusions (viz., page 1). But he does

recognize, and list diagnostic characters for, three species: S. graellsi, S. nigricollis, and S. fuscicollis.

I saw several individuals of this group on various

occasions during the course of the present study. By

sheer chance, they all appeared to have been representatives of the species defined by Hershkovitz.

Six adult individuals (including both males and females) and one juvenile (more than half grown) were

kept in captivity on Barro Colorado Island for almost

two weeks in August 1964. They were obtained from

an animal dealer in Iquitos, Peru. They certainly all

belonged to the same subspecies, apparently a form of

fuscicollis sensu Hershkovitz.

As a precautionary measure, in case there should be

more revisions or changes in the taxonomy of the

group in the future, it may be useful to insert a brief

description of these animals. They had black heads,

ears, and faces, with white muzzles. The white was interrupted only by black on the top of the nose and by

a series of vertical black stripes on the chin just below

the mouth. (The latter were really remarkably conspicious. The alternation of black and white areas on

the chin gave the impression of enormously large teeth,

which can hardly be coincidental. It may be very intimidating.) The white hairs of the muzzle were much

longer ("fuzzier") in the juvenile than in the adults.

There was a not very extensive area of rufous behind

and around the black face and ears. The hands and

feet were black, but the other parts of the limbs were

rufous as were most of the underparts. Most of the

back was brindled black and yellow. Most of the tail

was black. All the individuals were appreciably smaller

than Rufous-naped Tamarins of apparently similar

ages.
68 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

These animals may have arrived on Barro Colorado

Island in a diseased condition. They all died at the end

of two weeks as a result of something which looked

like "fulminating" Leishmaniasis. During the first few

days, however, they were very active and apparently

well adjusted, and they performed many display

patterns.

All the individuals were seen to perform Swaying.

They also uttered many calls. Most of their vocalizations were higher pitched than the corresponding patterns of geoffroyi, possibly in correlation with smaller

body size.

The juvenile uttered many Infantile Squeaks and

Infantile Rasps. Both types of notes seemed to be identical with those of geoffroyi in every respect except

pitch and, possibly, loudness or firmness of tone. They

sounded even "thinner" and slightly "reedy."

Both the juvenile and the adults uttered Short

Whines, Trills, Loud Sharp Notes, and Long Rasps.

These vocalizations also, at least by themselves, were

hardly distinguishable from the corresponding patterns

of Rufous-naped Tamarins except by pitch.

But a few other aspects of the acoustic signal system

were considerably more interesting. The Short Whines

apparently were never organized into stereotyped series

like Twitters. I never heard any Broken Rasps. Their

absence may be correlated with the presence of another

kind of display.

The adults often uttered more or less prolonged

Whistles. At first hearing, these sounded quite like

Long Whistles of geoffroyi, but further analysis revealed appreciable differences. The fuscicollis patterns

were not usually organized in two or three note series.

They were not plaintive in tone. Most of the individual

notes were strongly rising in pitch. Some of them even

"broke off," halfway through, in such a way as to suggest that they had moved up completely into the ultrasonic range. Almost all the fuscicollis Whistles also

occurred in circumstances which were unmistakably

hostile. They frequently intergraded with Long Rasps.

They must, in fact, have been produced by much

the same type of motivation as Long Rasps, but they

appeared to be rather lower intensity on the average.

Thus, for instance, an individual picked up in the

hand usually uttered many Long Rasps and struggled

and fought violently at first. Then it would gradually

relax (start to "give up"1), struggle less violently, and

also switch to Whistles. This would suggest that the

intensity of motivation in the Whistles of fuscicollis

may be much the same as in the Long Rasps of geoffroyi, and that the intensity of motivation in the Long

Rasps of fuscicollis may be much the same as in the

Broken Rasps of geoffroyi.

It has already been mentioned that the Long Rasps

of geoffroyi probably are homologous with the so-called

Screams of many other species of Platyrrhini, including

Aotus and Callicebus moloch. The latter patterns are

basically similar to Long Rasps in almost all respects

except for the fact that they are not (or not very)

harsh. But, simply because they are clearer in tone,

they are even more similar to the Whistles of fuscicollis. This would suggest that the Long Rasps and Whistles of fuscicollis are both descended from the same

ancestral patterns, the Whistles having remained more

primitive in form. If so, then the retention of a hostile Whistle display is a feature in which fuscicollis has

remained more primitive than geoffroyi (and probably more similar to other tamarins such as Leontideus

rosalia and Callimico goeldii).

At this point, it may be useful to pause and recapitulate. There have been so many references to various

Whistles and Rasps, Squeaks and Screams, and related

or associated vocalizations, in the preceding pages that

it may be convenient to provide a partial summary,

an outline of some of the differences and resemblances

among the patterns of the different species cited and

discussed.

1. Aotus trivirgatus has long, clear, high-pitched

scream patterns. These are uttered by both adults and

young. They seem to be purely hostile, and high intensity on the average, when uttered by adults. In the

rather different vocal repertories of infants, however,

they are associated and often intergrade with highpitched Squeaks and High Trills, in what can be called

a Squeak complex. The Squeaks of infants seem to be

generalized distress notes. The Screams of infants,

which are essentially identical with the adult patterns

in form, also seem to be distress notes, higher intensity

than Squeaks, more often than not, at least in the first

stages of infancy. But some of the infantile Screams

may (also) be hostile, and the proportion (although

not necessarily the actual number) of hostile Screams

must increase rapidly as an animal matures.

The Squeak complex Aotus, as a whole, is comparable to the Infantile Squeak - Infantile Rasp complex of Saguinus geoffroyi. Some or all of the patterns

involved probably are partly or wholly homologous.

See also below. And the two complexes further resemble one another in being radically transformed,

largely declining, with age. In the case of Aotus, only
NUMBER 2 8 69

the Squeaks and Screams normally survive into adulthood. And both types of vocalizations are uttered by

adults only in rather restricted circumstances.

Aotus does not have any really harsh rasping

sounds.

But it does have a distinctive Hoot display. Which

usually takes the form of two or three moderately long,

clear, but low-pitched notes. This seems to be entirely

non-hostile, a signal to attract companions (mates or

parents). At least when uttered by adults, the Hoots

do not seem to be particularly closely related to, or

associated with, either Screams or Squeaks.

2. Callicebus moloch also has long, clear, highpitched Screams.

They are part of a complex of high-pitched patterns

which also includes Squeaks, Whistles, and Trills. All

of these patterns seem to be essentially hostile. And

they all seem to be nearly or completely as characteristic of adults as of young.

Callicebus moloch does not, in fact, have any sort of

complex of vocalizations which could be described as

primarily infantile. The species differs from both

Aotus and Saguinus geoffroyi in this respect.

It seems probable, nevertheless, that the Squeaks of

moloch are strictly homologous with those of Night

Monkeys. They are really very similar in form. The

Screams of moloch are slightly more distinctive in

form, but may be equally strictly homologous with the

corresponding patterns of Aotus. Interestingly enough,

the Whistles of moloch look (on sound spectrograms)

even more like the Screams of Aotus. These Whistles

may be homologous with either typical Screams or

intermediates between Screams and Squeaks of Aotus.

This apparent superfluity of homologues is not really

anomalous. The Whistles of moloch often appear to

be low-intensity versions of the Screams, and highintensity versions of the Squeaks. And they certainly

intergrade with both.

The Trills of moloch also may be strictly homologous with the High Trills of Aotus.

Callicebus moloch individuals do not utter harsh

rasping sounds.

Nor do they utter stereotyped series of two or three

non-hostile notes to attract mates, parents, or other

social companions.

3. Saguinus geoffroyi does have Rasping patterns.

They occur in much the same situations, and seem to

subserve the same functions, as the Screams of Aotus

and C. moloch. They may be strictly homologous with

the latter, but they are rather strikingly different in

some, not all, aspects of form.

Other patterns show similar ambiguous relationships. The Infantile Squeaks of Rufous-naped Tamarins may be partly or completely homologous with

the Squeaks of both Aotus and Callicebus moloch, but

again are rather different in form. The Trills of

Rufous-naped Tamarins also have some features in

common with the Trills of C. moloch and the High

Trills of Aotus, but not enough to prove that they

are perfectly homologous in the strictest sense of the

term. Possibly the notes incorporated into the highpitched Trills of all three species have a more or less

remote common origin. But the components of the

Trills of S. geoffroyi are distinctive enough to suggest

that they may have been organized into series

independently.

Saguinus geoffroyi does not have any long, clear,

high-pitched Scream or Whistle pattern which is unmistakably hostile. What it does have is the special

and non-hostile Long Whistle display. This sounds as

if it had been formed by organizing Screams or

Whistles like those of both Aotus and C. moloch into

the temporal arrangement of the Hoots of Aotus.

4. Saguinus fuscicollis has some of the same Rasping

patterns as geoffroyi. Unlike geoffroyi, however, it also

has (presumably retained) long, clear, high-pitched

Whistles which are hostile in motivation.

Saguinus fuscicollis certainly has a special primarily

infantile vocal repertory. This seems to be essentially

identical with that of geoffroyi in form. Presumably

the various components are related to patterns of

Aotus and C. moloch in exactly the same way(s) as

are the corresponding patterns of geoffroyi.

The most enigmatic sounds uttered by the adult

fuscicollis on Barro Colorado Island were Rattles.

These were soft and relatively low pitched (for a tamarin). They were quite common, obviously lower intensity and/or less completely hostile than the Trills.

They may have "taken the place" of the Twitters of

geoffroyi in some sense. But they sounded very much

like Rattles uttered by saki monkeys, Pithecia monacha.

(It will be remembered, in this connection, that P.

monacha individuals are the only other monkeys, apart

from other tamarins of the genus Saguinus, which I

have heard utter both clear and rasping infantile distress notes. The significance of such resemblances can

only be assessed after Pithecia itself has been studied

more intensively.)
70

Two individuals, an adult female and a subadult

male, which were (tentatively) identified as Saguinus

graellsi also were kept on Barro Colorado Island for a

couple of weeks in November 1958. They were observed only very briefly, but a few display patterns

were noted. One or both individuals performed Sitrubbing, and uttered Infantile Squeaks, Short Whines,

Trills, Loud Sharp Notes, and Long Rasps. Four individuals of another form of this group were observed

in the National Zoo in Washington, D.C., at irregular

intervals during both October and November 1958.

They were identified (by the zoo authorities) as Saguinus nigricollis. They were adult or subadult but

I did not check their sexes. They were seen to perform Sit-rubbing, and heard to utter Short Whines,

Trills, Loud Sharp Notes, and brief stereotyped series

of short notes which may, conceivably, have been Twitters. Almost all the observed displays of these presumed

graellsi and nigricollis seemed to be very similar to the

corresponding patterns of both geoffroyi and fuscicollis.

It seems probable, therefore, that the signal system of

geoffroyi is as least fairly typical of the genus Saguinus

as a whole.

FURTHER COMPARISONS

The preceding descriptions and partial summaries may

be completed by a final comparative analysis, paying

special attention to the morphologies of entire repertories and to certain other genera which have not yet

been mentioned very frequently.

Previous Descriptions of S. geoffroyi Vocalizations

Some of the additional genera which must be considered have been observed by other students. As would

be expected, each student has used slightly different

terms. Visual displays usually can be identified in (or

through or behind) any form of description. But the

human language and sensory equipment being what

they are, it is much more difficult to interpret verbal

descriptions of vocalizations. This difficulty may be inescapable. But some of the students of other genera

have also observed S. geoffroyi. Comparisons of their

descriptions of this species with the one given above

may provide a standard by which to assess their accounts of other species. And also, of course, an opportunity to explain certain apparent contradictions or

discrepancies in different accounts of geoffroyi itself.

SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

Some of the defects of the general discussion of tamarin and marmoset behavior in Andrew (op. cit.) have

been mentioned on page 26. In addition to his general

comments, Andrew describes (without illustrating)

two vocalizations of geoffroyi. Some of the details presented would suggest that the patterns which he identified as twitters in this particular species were series of

Infantile Squeaks and that those which he calls "rasping screeches" were Infantile Rasps. The geoffroyi individuals whom he observed probably were infants and/

or older animals which had retained, or reverted to,

infantile behavior in the conditions of captivity.

Epple's (1968) account of the vocalizations of

geoffroyi is much longer and more extensive, but seriously misleading in several respects. The reasons why

her analysis is so poor are not always obvious. One

factor seems to have been that she studied Callithrix

jacchus much more thoroughly than any other marmoset or tamarin, and then "extrapolated" recklessly

from this one species to the others. She recognizes the

same categories of vocalizations, and gives them the

same names, in geoffroyi as in jacchus. Unfortunately,

however, it turns out that the organization of vocal

patterns is quite different in the two species. This will

be discussed below.

The particular patterns of geoffroyi cited by Epple

include:

1. "Te" notes. Epple implies (without actually

stating) that these are the most common and/or characteristic of the vocalizations of infants. She does not

provide any illustration of them, when and as they

are uttered by infants, but all or most of them must be

the same as the notes called Infantile Squeaks in this

paper. Epple seems to have missed the fact that they

usually are uttered in stereotyped series with rasping

notes. She implies that they usually are uttered singly

by young infants. She does say that a young animal

just starting to move independently uttered long series

of "variable, faint, and high-pitched sounds," but she

adds that the notes did not have a distinct rhythm.

This is almost certainly wrong, or at least very atypical

of the species.

She also says that similar notes are uttered by adults.

She calls the adult patterns "monosyllabic calls given

in close visual contact" and "monosyllabic calls in loose

visual contact and when disturbed." She gives two

drawings of sound spectrograms of the latter. They

are very different in appearance. One probably represents a (perhaps slightly aberrant) Twitter. The other

is a perfectly typical series of Infantile Squeaks.
NUMBER 2 8 71

Epple's animals may well have been retarded in the

same way as those studied by Andrew. It is remarkable, nevertheless, that she nowhere recognizes the

real distinction between Twitters (Short Whines) and

Infantile Squeaks, either when uttered by young or

by adults.

2. "Monosyllabic calls given in isolation." This is

illustrated by a drawing of a spectrogram which seems

to represent a three-note Long Whistle performance;

perfectly typical, but rather abbreviated.

3. "Trills given in high excitement." These seem

to be Trills in the sense used here, but Epple's drawing of a sound spectrogram of the pattern is very crude,

omitting part of the relevant detail.

4. "Squeals given in submission." This is illustrated

by an excellent photograph of a spectrogram which

reveals that the pattern is an Infantile Rasp. (I do

not understand how such a harsh note—and the features producing harshness are just as evident in Epple's

spectrogram as in any of mine—could be described as

a Squeal.) As noted above, Epple does not mention

that Infantile Rasps usually are combined with Infantile Squeaks in stereotyped ways. She does, however, state that there is a similar but slightly different

adult pattern, presumably the Long Rasp.

5. "Chatters given when angry." This must be the

Broken Rasp, but it is accompanied by a drawing of

a sound spectrogram which is very crude and incomplete indeed.

6. "Mobbing calls" or "Tsik" notes. The verbal

description of these patterns suggests that they are

Loud Sharp Notes, but the accompanying drawings

of spectrograms are peculiar and puzzling. They show

sounds like the Loud Sharp Notes illustrated in this

paper, but with much longer introductory phases. I am

at a loss to explain this difference. Possibly the patterns illustrated by Epple were ambivalent (some combinations of Long Whistles and Sharp Notes might be

expected to produce the same effect on spectrograms).

It may also be significant that some of the other species

kept by Epple produced similar sounds. Possibly some

of her Rufous-naped Tamarins were learning patterns

from individuals of other species?

7. "Warning calls." As described by Epple, this

category is hardly identifiable. All I can suggest is

that it may represent some type of extreme Sharp

Note.

Signals of Marmosets

Here the most important evidence is provided by

Epple's work on Callithrix jacchus, summarized in her

1967 and 1968 papers (and in a third paper published

under the name of Epple-Hosbacher, also in 1967)

as well as in Epple and Lorenz, op cit. This may be

supplemented, and partly checked, by information

from other sources, including a rather detailed account

of the same species (again ascribed to "Hapale") by

Le Roux (1967), an anecdotal description by Fitzgerald (1935), some brief observations of my own on a

few captive adult jacchus (observed in the London and

Paris zoos in 1959 and 1961), and the results of a

longer but still incomplete study of the related Cebuella pygmaea in captivity on Barro Colorado Island.

Most of the olfactory and visual displays of jacchus

which were seen by Epple have already been cited

above. They include Sit-rubbing, Pull-rubbing, Arch

Postures with a general Ruffle, Frowns, Flattening and

Raising of the Ears and Ear-tufts in threat, an

"Angsthaltung" which consists of a forward movement

of the ears and tufts, and Tongue-protrusion.

I saw slight Swaying performed by both the London

and Paris individuals. Le Roux shows a drawing of

what seems to be more exaggerated Swaying. He also

describes a simple "looking away," like that of Collicebus moloch, and suggests that it may be a very

low-intensity expression of alarm.

The animals in the Paris zoo performed an apparently ritualized Baring of the Teeth pattern. The

lips were separated in front, without being drawn

back at the corners, while the jaws remained almost

or completely closed. The net result was to reveal the

teeth, especially the lower incisors, as a white patch in

the center of the blackish face.

This was essentially identical, at least in form, with

the Baring of the Teeth by Callicebus moloch individuals. It was quite different from both the simple opening of the mouth which is typical of all Saguinus geoffroyi and the "fang showing" of the one aberrant

individual described on page 56 (or any "grins" performed by the individuals observed by Andrew).

Sometimes the Baring of the Teeth by the jacchus

individuals was quite silent. At other times, it was

combined with soft rattling noises.

Some of the latter performances were accompanied

by partial eye-closing. This probably was not the true

Frown of the species. It certainly was different from the

Frown of Saguinus geoffroyi. It was not brought about
72 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

by conspicuous lowering of the eyebrows. Thus, it was

much more reminiscent of the "real" Eye-closing display of geoffroyi. And also a somewhat similar pattern

of Callicebus moloch. As performed by the Callithrix

jacchus individuals in Paris, it was not accompanied

by either Nose-wrinkling or Tongue-protrusion.

Both Le Roux and Fitzgerald show photographs of

Baring of the Teeth and Eye-closing by jacchus. Le

Roux also provides excellent drawings of different intensities of the two patterns.

Cebuella pygmaea seems to have a special facial

expression composed of similar elements. (See Figure

6 in Moynihan, 1967.)

Perhaps the most conspicuous of the ritualized visual (or visual and olfactory) signals of Callithrix jacchus is what Epple calls "Genitalpra'sentieren." Rather

surprisingly, this seems to be purely hostile. A performing animal faces away from its opponent(s), raises its

tail (in the form of a question mark) and reveals its

genito-anal region. A photograph of Epple-Hosbacher

shows that all the hairs of the whole tail may be raised

at the same time, in a sort of extreme Tail-ruffling.

Possibly other parts of the pelage also are raised. This

Genital-presentation may be characteristic of all

marmosets. Epple says that it is performed by Callithrix argentata and C. "leucocephala," and it certainly

occurs in Cebuella pygraea (it was called simply "presentation" in Moynihan, 1967).

Extreme Tail-ruffling also is performed by jacchus

in other situations. Le Roux indicates that it can be

combined with what seems to be an exaggerated Tailforward. The tail is actually pulled up between the legs,

but apparently not Looped or Coiled. This seems to

express high-intensity alarm or fear.

Epple, Le Roux, and Fitzgerald all record Allogrooming by jacchus individuals. The usual version

seems to be identical with that of most other New

World primates in physical form. More significantly, it

seems to be a "general social" or gregarious pattern.

This is another resemblance to Callicebus moloch.

Epple also describes a peculiar display or complex

of displays by jacchus individuals immediately before

copulation attempts. The essential feature is a Licking

of the partner, especially around the face and the foreparts of the body. This may be alternated with "combing" of the partner's pelage, using the incisor teeth.

Both patterns may be preceded by sniffing, Tongueprotrusion, and a possibly distinctive "Lip-smacking."

Le Roux confirms the occurrence of sniffing and

Licking in these circumstances.

It seems overwhelmingly probable that the Licking

and combing, at least, are closely related to, presumably

derived from, more ordinary forms of Allogrooming.

If so, their morphological peculiarities are significant.

To my knowledge, jacchus is the only species of Platyrrhini recorded to have such extremely different

types of Allogrooming, or derivatives thereof, in general social and sexual situations. (The differences between sexual and apparently gregarious Allogrooming

in Saguinus geoffroyi are matters of frequency and

orientation rather than basic form. See page 15.) It

also seems likely that the condition of these patterns

in jacchus is highly specialized.

The vocalizations of jacchus described by Epple may

be summarized (and partly homologized) as follows:

1. "Phee" notes, "monosyllabic calls given in close

visual contact," "monosyllabic calls given in loose

visual contact and in distress," and "monosyllabic calls

given in isolation." These are illustrated by drawings

of sound spectrograms. Both the drawings and the accompanying verbal descriptions would indicate that

they are strictly homologous with patterns of the intergrading Squeak - Whistle complex of Callicebus

moloch (and equivalent to the "trilles et sifflements" of

Le Roux, which are just as reminiscent of the same

moloch sounds). If this interpretation is correct, then

the patterns of this category probably are related to the

Squeaks of Aotus and (perhaps less closely or directly)

to the Infantile Squeaks of Saguinus geoffroyi. But

Epple's account would imply that they are approximately equally characteristic of young and adult jacchus. When uttered by infants, they may be generalized

distress notes. When uttered by adults, they seem to be

purely or largely hostile. This latter point is somewhat

obscured, in the actual account, because some of the

names given to the patterns are deceptive. Epple does

say, however, that even the "monosyllabic calls given in

isolation," when uttered by adults, are given by individuals who can hear others, and "are often accompanied by threat signals such as arch-postures and

genital presenting." This would seem to be conclusive

evidence that the "monosyllabic calls given in isolation"

by jacchus are more like the Whistles of Callicebus

moloch (or Saguinus fusicollis) than like the Long

Whistles of S. geoffroyi. It also, of course, indicates

that the patterns of geoffroyi and jacchus to which

Epple applies this name are not identical or even functionally equivalent (see page 71).

As an example of how confused Epple's descriptions

can become, it may be mentioned that she implies (in
NUMBER 2 8 73

fact actually states) that Arch and Genital-presenting

postures accompany the "monosyllabic calls given in

isolation" (Long Whistles) of S. geoffroyi, although

she also says elsewhere—and this time quite correctly—

that neither posture is assumed by this particular

species!

2. "Twitters." According to Epple, these occur in

three versions in jacchus: infantile, juvenile, and adult.

The juvenile version seems to be perfectly intermediate

between the other two.

All the versions may be partly or wholly homologous

with what I have called Twitters in geoffroyi, but they

are rather different in form(s). Each note of a series

rises much more strongly and steeply in the jacchus

performances than in those of geoffroyi. The rising

phase of each note is followed by a brief descending

phase in the Twitters of infant jacchus. The descending phase seems to be quite absent in the corresponding performance of adults. At least, it is not shown in

the drawing of a sound spectrogram of the pattern

presented by Epple. This would suggest that the adult

performance may also be closely related to the Sharp

Note patterns of S. geoffroyi (and many other species)

and the "Chuck" Notes of Callicebus moloch.

The soft rattling noises which I heard uttered by the

captive individuals in the Paris zoo may have been

some form (s) of Twitters. If so, they confirmed the impression conveyed by Epple's spectrograms. The jacchus patterns sound very different from geoffroyi Twitters to human ears, and presumably also to the ears of

other animals.

3. "Rhythmical calls given in close visual and bodily

contact." Epple does not illustrate this pattern, and

her description is vague (she suggests that the sounds

are "like the faint chirping of birds"). This might

represent something like another (fourth) type of

Twitter.

4. "Squeals given in submission." These are illustrated by a photograph of a sound spectrogram of a

single note which is certainly a Rasp of some sort.

It looks most like the Infantile Rasp of S. geoffroyi,

but Epple (again) implies that the pattern is typical of

individuals of all ages.

This brings up more problems of interpretation.

Epple does not suggest that these Rasps and the

"Phee" Notes are often associated with one another

in stereotyped series. This would seem to indicate that

jacchus does not have a specialized Infantile Squeak -

Infantile Rasp complex like geoffroyi. Possibly Epple's

account of jacchus is correct in this respect, even

though her account of the corresponding behavior of

geoffroyi is not. I never heard any unmistakable Infantile Squeak - Infantile Rasp series uttered by the

jacchus in the London and Paris zoos. And the distress

notes of infant Cebuella pygmaea jeem to be all Squeak

(or other clear sounds) and no Rasp, like those of

Callicebus moloch.

Le Roux, on the other hand, cites a pattern, the

"cri plaintif," which may also be homologous with the

Infantile Rasp of geoffroyi, and he states that it definitely does tend to occur immediately after a "trille"

or a "sifflement." This must produce series like Infantile Squeak - Infantile Rasp sequences, but Le Roux's

account would not suggest that such series are particularly infantile in jacchus.

Thus the whole subject is left up in the air. All one

can say is that some clear sounds of jacchus are quite

similar to some high-pitched notes of Callicebus

moloch, and may or may not be incorporated into

separate infantile and adult complexes.

5. "Tsee tsee tsee . . ." calls "given in aggressive

threat." Epple's description of these notes is accompanied by a drawing of a spectrogram. This looks quite

unlike anything normally uttered by geoffroyi. It

could, conceivably, be related to some Squeak and/or

Sharp Note patterns of other species. In the form described by Epple, however, it seems to be very distinctive, perhaps diagnostic of jacchus (although

further investigation may show that it is shared with

other marmosets).

6. "Chatters given when angry." These are illustrated by a drawing of a spectrogram. If the drawing

is at all adequate, these "chatters" also are distinctive,

but it will be remembered that Epple applied the same

name to the Broken Rasp of geoffroyi, and gave a very

poor drawing of the latter. Possibly the two supposed

"chatters" are related but not identical.

It might be added, in this connection, that Le

Roux's account of the various rapid rhythmic calls of

jacchus cannot always be reconciled, in all details,

with Epple's descriptions. And some of his drawings of

spectrograms also are obscure. But his account confirms the existence of marked differences between

some of the geoffroyi and jacchus patterns of this

general type.

7. "Crackles" and "coughs." These may be very

abbreviated Rasps. They are hostile, used as "mobbing" calls and in aggressive threat.

8. "Tsik" notes. Epple's verbal description would

suggest that these are Loud Sharp Notes, but the ac356-597 O - 70 - 6
74

companying sound spectrogram shows a prolonged

pattern. On the evidence presented, it is impossible

to determine if this is a distortion or not (see also

above, page 71).

9. "Warning calls." Like the patterns of geoffroyi

to which Epple gave the same name, these are essentially unidentifiable.

10. "Screams." These are high-intensity patterns,

produced when the escape tendency is predominant.

Epple does not illustrate them and, again, her verbal

description is somewhat vague. But my own observations of the jacchus individuals in the London and

Paris zoos would indicate that the Screams of this

species are clear in tone, sounding more like the

Screams of Callicebus and Aotus than like the Long

Rasps of Saguinus geoffroyi.

Epple's brief comments on the vocalizations of Callithrix "leucocephala" and C. argentata are not very

useful, except insofar as they suggest that the two species are as similar to jacchus in these respects as in

others. It may be mentioned, however, that the drawing

of what Epple calls a "Trill" of argentata is remarkably reminiscent of the most Trill-like Whistles of Callicebus moloch. This may be of some comparative significance. It also suggest that the supposed "Trills" of

argentata are not strictly homologous with the Trills

of Saguinus geoffroyi (see also page 69).

Final Comments

Some of the implications of the preceding survey are

rather puzzling.

There are many resemblances among many displays

of all New World primates. This is as true of Callithrix and Saguinus as of most other genera. There

also are certain broad features or general aspects of

display behavior which seem to be common to all

marmosets and tamarins. Some of these are cited and

discussed in Moynihan (1967). They include the predominance of high-pitched vocalizations, the restricted

variety of facial expressions, and the (perhaps compensatory) development of diverse sets of pilo-erection

and smoothing patterns.

It is at least conceivable, however, that these features

are nothing more than superficial or immediate adaptations. Like some of the morphological characters shared

by the same animals (e.g., clawlike nails, the loss of

third molars in most genera, and the smoothness of

the cerebral hemispheres), they could be adaptations to

SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

small size and/or some of the consequences or correlates of small size.

Unfortunately, attempts to interpret the real significance of these general features are not helped very

much by more detailed analyses of individual displays.

Point by point comparison of patterns described above

would seem to reveal the following:

1. Some displays are characteristic of either tamarins

or marmosets, but not both. Genital-presenting is a

notable example. But the category may also include

such patterns as Licking and Upward Tail-coiling before copulation.

2. Some displays which are shared by species of both

groups, i.e., Sit-rubbing and the General Ruffle, also

occur in some or all other Platyrrhini.

3. Still other features which are shared, e.g., some

vocal elements, are arranged in different ways in the

two groups.

Of all the more complex and distinctive individual

displays, probably only Tongue-protrusion and Rasps

really suggest that tamarins and marmosets are more

closely related to one another than either is to other

groups of New World primates. Only some tamarins

and marmosets are known to have both patterns, but

this is by no means conclusive. Rasps may take different

forms and/or subserve different functions in different

species. They also seem to be shared with Pithecia.

Tongue-protrusion seems to be shared with Alouatta.

The differences between the signal systems of marmosets and tamarins are perhaps rather surprising.

They are more extensive than might have been expected in view of the fact that all the species conform

to a rather uniform morphological type and (as far as

is known) have similar ecologies and social structures.

Perhaps further studies of other species will reveal

that some have display behavior which is intermediate

between Saguinus geoffroyi and Callithrix jacchus.

My incomplete study of Cebuella pygmaea would suggest, however, that its signal system is even less like

that of geoffroyi than is that of jacchus. Very brief observations of Callimico goeldii would suggest that its

behavior is distinctive rather than intermediate, and

more different from jacchus than from geoffroyi.

(This also is the impression conveyed by Epple's account of the species in her 1968 paper.)

The situation becomes even more complicated when

Callicebus and Aotus are considered. The contrasts

and similarities between these two genera would seem

to be strictly comparable to those between Saguinus

and Callithrix. Aotus and Callicebus resemble one
NUMBER 2 8 75

another in body proportions and some other anatomical features. (So much so that they have been placed

in the same subfamily or tribe by some authors. For

instance, Simpson, 1945.) They also share a number of

more or less general features of display behavior; e.g.,

the inclusion of both high- and low-pitched notes in

the adult vocal repertories. Many of their individual

displays certainly are homologous, but many of these

are shared with many other Platyrrhini. And other displays of the two genera are quite different. Only a

few of their more complex signals; e.g., Tail-twining

and long "Song-like" series of Resonating Notes or

Resonant Grunts, are both distinctive and similar

enough in the two genera to suggest a special

relationship.

In actual fact, as mentioned repeatedly above, there

may be as many or more resemblances between the

signal repertory of Saguinus geoffroyi and that of

Aotus as between the latter and the corresponding

repertory of Callicebus moloch, but the special similarities are quite different in the two cases. The features

common to Aotus and Saguinus geoffroyi include predominantly sexual Allogrooming, Tail-lashing only

during Sit-rubbing, stereotyped series of two or three

long notes to attract mates or companions, comparatively frequent performance of freeze and crouch patterns, and similar forms of Swaying and head-down

postures.

These similarities are all the more remarkable because the two species have rather different social structures, and one is diurnal while the other is nocturnal.

Saguinus geoffroyi seems to show few or no significant special resemblances to Callicebus.

But Callithrix jacchus may. Callithrix and Callicebus seem to share Baring of the Teeth, "general social"

Allogrooming, and some very similar forms of vocalization.

On the other hand, Callithrix jacchus shows few or

no significant special resemblances to Aotus.

Thus, the situation can be outlined as follows:

1. Saguinus resembles both Aotus and Callithrix,

but in different ways. The special features it shares

with Aotus are not the same as those it shares with

Callithrix.

2. Callicebus also resembles both Aotus and Callithrix, again in different ways. The special features it

shares with Aotus are not the same as those it shares

with Callithrix. Nor are the special features which it

shares with Aotus and Callithrix the same as those

which Saguinus shares with the same genera.

3. Callithrix resembles both Saguinus and Callicebus in different ways.

4. Aotus also resembles both Saguinus and Callicebus in different ways. The special features shared by

Aotus, however, are not the same as those shared by

Callithrix.

It may be premature to attempt to draw phylogentic conclusions from data of this type. Obviously, there

must have been considerable parallelism or convergence, of behavioral and/or morphological characters,

during the evolution of some or all of these genera.

Such as they are, the known data might suggest that

marmosets and tamarins are independent derivatives

of a more typically monkey-like stock (animals

of larger size and more completely omnivorous or

even frugivorous diet), or that Callicebus and Aotus

are independent derivatives of some common tamarinmarmoset stock. In the absence of useful information from the paleontological record, these possibilities can be checked only by further studies of other

living forms.

SUMMARY

Saguinus geoffroyi, the Rufous-naped Tamarin, is

fairly widely distributed in parts of Panama and northern Colombia. Individuals of the species have been

observed in the wild, in central Panama, and some

aspects of their behavior have also been studied in the

laboratory.

The species is rather small, for a monkey. It is most

characteristic of dense scrub and not very tall forest,

often second growth, in areas of moderate humidity.

Individuals tend to remain near, but not exactly at,

the edges of such habitats. They are diurnal, almost

completely quadrupedal, and come down to the ground

only occasionally. They eat a variety of foods, including much vegetable matter, but probably prefer insects

when available. They give every indication of being

preyed upon frequently.

Under present conditions in the wild in Panama,

they may occur singly or in groups of two to nine individuals. Each single individual or group seems to have

its own territory. Territories usually are quite large.

The animals move rapidly when active. It probably

is typical for each individual or group to move through

all or most of its territory at least once a day. There

is relatively little trespassing.

The social and ecological relations between Rufousnaped Tamarins and other (non-predatory) animals,
76 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

at least one other mammal and many birds, are complex and probably highly specialized. They may

involve several forms of social mimicry. Competition

between the tamarins and some other species also is reduced by differential timing of activities. The advantages and disadvantages of such arrangements may

help to explain the geographical distribution of the

species and the genus.

The communication system of adult Rufous-naped

Tamarins is composed of a few tactile and olfactory

patterns, a moderate number of different types of vocalizations, and even more kinds of visual signals. Most

of the latter are gross movements of the head and/or

body, pilo-erection and smoothing patterns, and special

ways of holding and moving the tail. The importance,

or preponderance, of visual signals in the adult repertory of the species may be an adaptation to avoid

attracting the attention of predators. Postures and

movements probably are not as conspicuous at long distances, in forest and scrub, as are sounds. The vocalizations include both "clear" and harsh rasping notes,

but all are more or less extremely high pitched. This

may be a similar adaptation. High-pitched sounds do

not carry as far as low-pitched sounds.

Some of the vocalizations of adult Rufous-naped

Tamarins intergrade frequently; others do not. Some

of them usually seem to be quite precise releasers;

others may provide little or nothing more than information for future reference. Different types of signals

are combined in almost endless permutations, probably because it usually is advantageous for a single

performance to transmit one or more messages, along

different channels, to different recipients, all at the

same time.

Among the distinctive features of the species are

individual "quirks." These look like displays. Some of

them may function as signals, but they do not seem

to be species-specific.

Young animals utter well-differentiated distress

notes.

Brief observations of some other species of Saguinus

(oedipus, leucopus, juscicollis, graellsi, and nigricollis)

suggest that many of the displays of geoffroyi are

typical of the genus as a whole.

The phylogenetic implications of the signal system

of Saguinus are perplexing. Saguinus certainly resembles both Aotus (the Night Monkey) and Callithrix

(typical marmosets), but in different ways. It does not

show any special similarities to Callicebus (titi

monkeys). Nor does Callithrix show special similarities to Aotus. Callicebus does resemble both Callithrix

and Aotus, although not in the same ways as Saguinus.

Obviously, there must have been parallelism or convergence, of behavioral and/or morphological characters, during the evolution of some or all of these

genera.

ACKNOWLEDGMENTS

I must thank M. C. M. Hladik, Dr. M. H. Robinson,

and Dr. N. G. Smith for much unpublished information on Rufous-naped Tamarins. Dr. Robinson also

kindly read and criticized the manuscript. I am equally

indebted to Dr. T. H. Reed, Professor F. Bourliere,

and Dr. D. Morris for facilitating observations of captive animals in various zoos.

Dr. and Mrs. W. J. Smith prepared the spectrograms, and provided invaluable assistance in the form

of stimulating discussions of the problems of animal

communication.

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1964. Some Behavior Patterns of Platyrrhine Monkeys.

I. The Night Monkey (Aotus trivigatus). Smithsonian Miscellaneous Collections, 146(5): 1-84.

1966. Communication in the Titi Monkey, Callicebus.

Journal of the Zological Society of London, 150:

77-127.

1967. Comparative Aspects of Communication in New

World Primates. In Primate Ethology, ed. D. Morris. London: Weidenfeld and Nicolson.

1968a. Social Mimicry: Character Convergence versus

Character Displacement. Evolution, 22:315-331.

1968b. The "Coerebini"; a Group of Marginal Areas, Habitats, and Habits. American Naturalist, 102:573-

581.

In press. The Control, Suppression, Decay, Disappearance,

and Replacement of Displays.

Ploog, D. W., J. Blitz, and F. Ploog.

1963. Studies on Social and Sexual Behavior of the Squirrel Monkey (Saimiri sciureus). Folia primatologica,

1:29-66.

Robinson, M. H.

In press. Insect Anti-predator Adaptations and the Behavior of Predatory Primates. Notas del IV Congreso Latinoamericano de Zoologia, Caracas.

Sanderson, I. T.

1957. The Monkey Kingdom: An Introduction to the

Primates. New York: Hanover House.

Simpson, G. G.

1945. The Principles of Classification and a Classification of Mammals. Bulletin of the American Museum of Natural History, 85:1-350.

Smith, W. J.

1965. Message, Meaning, and Context in Ethology.

American Naturalist, 99:405-409.

Wislocki, G. B.

1930. A Study of Scent Glands in the Marmosets, Especially Oedipomidas geofjfroyi. Journal of Mammalogy, 11:478-483.

1936. The External Genitalia of the Simian Primates.

Human Biology 8:309-347.

1939. Observations on Twinning in Marmosets. American Journal of Anatomy, 64:445-483.

V. S. GOVERNMENT PRINTING OFFICE : 1970 O - 359-597



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